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Colonial waterbirds

as bioindicators
in China and Pakistan
Contact Bulletin of the Partners
EU-INCO-DC Contract IC18-CT98-0294

No. 6 1 May 2001

DRAFT OF THE

Final Scientific Report

Environmental Contamination,
and breeding and foraging ecology,
of selected colonial waterbirds
in China and Pakistan

This report summarizes the results obtained for the EU-INCO-DC project “Colonial waterbirds as
bioindicators in China and Pakistan”. It is still in a draft stage, to be completed before the conclusion of
the project.
This report aims to circulate information among the participants to the research Project, and to provide a
basis for the dissemination of the results to any concerned audience. This material can be:
• freely used by any Partner for results dissemination to any audience, e.g. managers, press, general
public (take care, however, to make clear that these results are partial, do not present them as
conclusive)
• used for scientific publications (in journals, at meetings), but before submitting any publication you
should re-analyze the original data, obtain the approval of all the persons involved in the particular
part of the research you wish to publish, and obtain the approval of the Project coordinator
In any case, when you refer to these data, you must cite the Project name, the contract number, and the
funding by the European Union.

I
Index and Summaries

Introduction page 1
The INCO-DC project “Colonial waterbirds as bioindicators of contamination in selected wetlands
of China and Pakistan” was funded by the European Union (Contract IC18-CT98-0294), and was
accomplished from September 1998 to September 2001 by six partners:
• Dipartimento Biologia Animale, Università di Pavia, Italy
• Departament. de Biologia Animal, Universidad, Barcelona, Spain
• Pakistan Agriculture Research Council, Islamabad, Pakistan
• WWF-Pakistan, Karachi, Pakistan
• Biological Resources Institute, Jiangxi Academy of Sciences, Nanchang, , P.R. China
• Department of Soil Ecology and Environmental Science, Chinese Academy of Sciences,
Nanjing, P.R. China
with collaborations by:
• Dipartimento Chmica Farmaeutica, Università, Viale Taramelli, I-27100 Pavia, Italy
• Dipartimento Chmica generale, Università, Viale Taramelli, I-27100 Pavia, Italy
• Department Biology, Lanzhou University, Lanzohu 730000, PR China

1. Environmental contamination, and human health page 2


A dramatic increase in public concern about the state of the environment has occurred in recent
decades, in relation to a growing evidence that pollution has caused severe environmental
degradation. Nowadays, about 1000 new chemical compounds are being synthesized each year, and
between 60.000 and 95.000 are in use. A solution to the problems posed by contamination must
start from the monitoring of these substances in the environment. In order to monitor pollutants,
their environmental consequences and to assess ecosystem health, we need to use effective
bioindicators, i.e organisms that accumulate contaminants that are present only at trace levels, so as
to allow pollutant detection earlier than would be possible from abiotic samples.
As coastal and inland wetlands in Pakistan and China are subject to increasing pollution from
industrial, urban and agricultural sources, there is a growing urgency to monitor contaminant
levels, to assess the effects of pollutants, and to evaluate the resilience of these wetlands to
pollution. The approach of our study focused on the use of colonial waterbirds as bioindicators of
environmental contamination and other ecosystem changes. While a pletora of studies about
contamination exists for America and Europe, very few studies exist for Asia. This research project
aimed to ascertain the levels of the most widespread contaminants with long term persistence in
some environments of China and of Pakistan.
The general objective was to assess pollutant levels and effects, using egrets and herons (colonial
waterbirds of the Family Ardeidae) as bioindicators. We considered the most widespread
contaminants with long term persistence:
• inorganic elements, particularly heavy metals and other elements of environmental concern
(Cd, Cr, Hg, Pb, Cu, Fe, Mn, As, Ag, Br, Co, Ce, La, Ni, Sc, Se, Zn)
• DDT and derivates
• other organochlorines (HCH+HCB, -HCH, -HCH, - HCH, heptachlor-epoxide -endosulfan)
• polychlorinated biphenyls (PCBs)

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Since biomonitoring programs are most effective when they use a combination of indicators, at
different levels of organization, our research program included the study of:
• eggs: contamination by organic compounds, as indicator of environmental contamination
• feathers: contamination by trace elements, as indicator of environmental contamination
• eggshell thickness and haemathological variables, as indicators of contaminants effects
• breeding success, as indicator of the present impact of contaminants
• breeding population size, as indicator of the long-term impact of contaminants
• contamination in prey of the egrets, as indicator of the contamination of particular habitats
• contamination of the sediments, as indicator of long-term contamination.
The results may indicate the level of pollution in the populations and ecosystems studied, highlight
potential threats to human health, and provide valuable baseline data for comparison with future
conditions in these ecosystems and elsewhere in Asia. The outputs will be useful for management
of these important wetlands, for national policy formulation for pollution control and wetland
conservation, and for the strengthening of pollution control regulations.
Specific objectives were:
• to infer exposure of Little Egrets to pollutants and the general bioavailability of pollutants
• to identify whether concentrations of contaminants found, and any other ecosystem changes
observed, are at levels associated with adverse effects on reproduction
• to disseminate the results among environmental toxicologists and other scientists, ecosystem
managers, environmental policy formulators and legislators.
We summarize here the results of the ecological studies, sample collection and chemical analysis.
The ecological data, besides their own biological interest, provide a background information for the
interpretation of the contamination levels. Contamination data show that concentration levels are
generally lower than the threshold known to harm wildlife, both for metals and other elements, and
for organic compounds, with some exceptions. These results are mostly welcomed, in that they
testify a reduced environmental contamination.

2. Study areas page 10


For each country, we selected one wetland exposed to industrial-urban pollution, one to agricultural
pollution, and one thought to be relatively unpolluted , on the basis of the presence of breeding
colonies of egrets and herons, of their national and global importance, and of their various exposure
to contamination
1) Poyang Lake, Jiangxi, China. The largest freshwater lake in China, and the most important
site for waterfowl; a NEPA nature reserve; expected to be free of pollution.
2) Tai Lake, Jiangsu Province, China. One of the largest lakes, in a highly productive area,
expected to be subject to serious pollution from agriculture and industry.
3) Pearl River Delta and Coastal Area, Guangdong, China, a wide area, expected to be subject
to urban-industrial pollution
4) Haleji Lake, Sindh Province, Pakistan, a freshwater lake, with associated marshes and
adjacent brackish seepage lagoons, expected to be relatively unpolluted
5) Taunsa Barrage, Punjab Province, Pakistan, a storage reservoir behind a barrage on the
River Indus, expected to be subject to pollution from agriculture
6) Karachi Harbour, Pakistan, tidal creeks, mangrove swamps and intertidal mudflats,
expected to be subject to considerable urban and industrial pollution

3. Methods for sample collection and for ecological studies page 14


Our main study species was the Little Egret Egretta garzetta, as monitor of contamination. For the
ecological data however, we decided to consider all the other herons and egrets breeding in the
same colonies, or foraging in the same wetlands, because this could be done with very little
additional effort, but on the other hand it would greatly increase the completeness of the study.

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The collection and analysis of contamination samples remained restricted to the Little Egret, owing
to the high cost of the chemical analyses. In some cases however, Little Egrets were too scarce to
provide sufficient samples, and we were forced to shift to the most similar species (the
Intermediate Egret, or theCattle Egret) as sample species.
During May and June 1999, teams of Asian plus European researchers worked jointly in the Haleji
and in the Poyang study areas. This joint work was also intended as training, so as to ensure that all
the researchers adopt exactly the same techniques. During May and June 2000, joint Asian-
European teams worked in the remaining 4 study areas.
We standardized the field methods (collection of ecological records and of samples for chemical
analysis), in order to ease the comparison of the different study areas. A booklet “Workplan and
methods for Ecological Fieldwork & Sample Collection” was distributed to each participant.
However, complete ecological records were obtained only in a part of the study areas, because of
local constraints.
The ecological records included:
• Locate and census all waterbird colonies within each study area of 200-500 km 2 P P

• Breeding uccess, recorded for a sample of nests in one focal colony of each study area
Prey of the chicks at the focal colony
• Foraging habitats used by the adults within a 10 km radius circle around the focal colony
Prey biomass in rice paddies
• Feeding success and prey type of the foraging adults
We collected the following materials for chemical analysis:
• Eggs from different clutches.
Feathers.of chicks from the same nests from which the eggs had been sampled.
• Prey of the chicks
• Sediments in the different foraging habitats used by the egrets
In addition, eggshell thickness was measured, and blood slides were obtained from the chicks.
Eggshell thickness and haematological variables can be related to contamination.

4. Breeding and foraging ecology of egrets and herons at the Poyang Lake
study area,China page 19
Population. Eight colonies were located and censused, within a study area of approximately 120
by 50 km Census of the nests. The impression is that the density and size of the colonies within the
Poyang lake area is representative of the situation in the whole region. The breeding population is
therefore very large, due to the wide surfaces of aquatic habitats, particularly rice paddies, that
herons can exploit for foraging.
Breeding success. The breeding success of each species can be considered normal, and even
higher, compared to the literature data. This high success preliminarily suggests that no adverse
agent (e.g. contaminants) is affecting reproduction in this study area.
Prey. The main prey type was fish for every bird species. Shrimps, frogs and tadpoles appear in
the diet in decreasing importance
Foraging habitats. The distribution of the foraging herons shows that Little, Intermediate, and
Cattle egrets, and Chinese Pond Herons, forage mostly (for >80% ) on rice paddies. On the other
hand, Great White Egrets forages with almost equal frequency in lakes, ponds, and rice paddies,
while Night Herons forage mostly in lakes and rivers. Since most Little Egret foraged in rice
fields, most sediment samples were collected there.

5. Ecology of egrets and herons at the Tai Lake study area, China page 26
Taihu region is one of the most productive areas for agriculture, and one of the most economically
developed of China. Rice fields account for 90% of total farmland, and the water surface takes 45%

IV
of land. With the rapid economic growth since late ‘70s, water and soil pollution from industry,
agriculture and urban waste has been increasing significantly. Therefore, there is a growing
urgency to monitor contaminant levels in water and soil, and to assess the effects of pollutants to
human and ecosystem health.
Population. Five heronries were found in the area. The Wuxi colony was selected as main study
area, because of its dense population, species, accessibility, and highly exposed to soil and water
pollution from agriculture and industries. The Wuxi colony was very large, with 9700 nests
estimated in 1999, and 36400 nests in 2000.
Breeding Success. The breeding success of Night Heron and Little Egret could be considered
normal, and even slightly higher for Little Egret, compared to the literature data (see Table 3.1).
This suggests that no adverse agent (e.g. contaminants) was severely affecting bird reproduction in
this study area.
Prey. The main prey type was fish, that accounted for 100% of the diet of Little Egret chicks, and
for 95% of the diet of Night Heron chicks, that also received small amounts of frogs, crustaceans
and mammals.
Foraging Habitats. The distribution of the foraging herons and egrets among the available habitats
showed that most Little Egrets, Night Herons, and Chinese Pond Herons, foraged on fish ponds and
on lake shores. The Night herons exploited the open waters of the lake as well. The scarce use of
the rice fields is due to their relatively small surface within the study area. On the other hand, fish
ponds were intensely used, presumably because they are abundant around the colony, and contain
abundant food resources.

6. Breeding and foraging ecology of egrets and herons at the Guandong study area, China page 31

TO BE DONE BY DAI AND RUIZ

7. Breeding and foraging ecology of egrets and herons at Haleji study area, Pakistan page 32
Foraging habitats. We identifyed a total of 15 feeding areas within the Haleji lake, that is
surrounded by arid dry lands, where no suitable place for herons feeding activity is available. The
dominant species was by far the Intermediate egret, the other species being more than one order of
magnitude below it.
Foraging ecology. The Intermediate and the Little egret used areas where water depth covered
between 15 to 45 % of the leg length. Little Egrets tended to change feeding area more frequently
than Intermediate Egrets. The foraging behavior of the two egrets was similar.
Diet. The diet of Intermediate Egret chicks was analysed through the chick regurgitates The most
important prey in number were Caridean shrimps, followed by fish, the other prey being consumed
only in small amounts. In biomass, fish was the most important prey followed by Caridean
shrimps.

8. Breeding and foraging ecology of egrets and herons at Taunsa study area, Pakistan page 41
Population. Two heron colonies were present in 2000: the smaller colony was chosen as the focal
ones for study, because of its accessibility. A second, large but inaccessible colony was located in a
large reed bed.

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Breeding Success. The breeding success of the Little Egret was relatively low, i.e. toward the
lower end of the range of values found in literature, and this may be due either to unfavorable
environmental conditions, e.g. food scarcity, or to the effect of contaminants.
Foraging habitats. A variety of habitats was used for foraging by all the species of egrets and
herons. Cattle Egrets used dry lands more than all the others, as it is usual for this species. The
limited use of the rice paddies is due to the fact that they were flooded only during the last part of
the survey.

9. Breeding and foraging ecology of egrets and herons at Karachi study area, Pakistan page 46
Population. Only one egret colony, with 145 nests, was present within this study area, and for a
radius of at least 20 km.
Breeding Success. Breeding success, studied in all the nests that could be found in the colony, all
belonging to the dark morph of the Little Egret, was low, i.e. toward the lower end of the range of
values found in literature for different locations and years. This relatively low breeding success
may be due either to unfavorable environmental conditions, e.g. food scarcity, or to the effect of
contaminants.
Foraging habitats. The egrets foraged mostly on the surfaces of mud exposed at low tide, and with
lesser frequency on the banks of large canals that connected the lagoon to the sea. The
Intermediate egrets and the Indian Pond Heron foraged mostly on the same habitats.
Prey. All the prey items, collected throughout the study period, were small fish (Liza abu,
Perciformes).

10. Heavy metal contamination in the samples from China page 49


Analytical Methods. Two analytical techniques were used for all the sample materials, that were
split in two parts of similar amounts, whenever possible: Atomic Adsorption Spectrophotometry
(AAS) for cadmium, mercury and lead, and Neutronic Activation Analysis (NAA) for the
remaining elements. The results summarised below, are complete for NNA, but include only about
one half of the results of AAS analysis, that are still in progress.
Contamination level in the samples. In eggs, here were significant differences in mercury,
arsenic, bromine, cobalt, cesium, scandium, selenium and zinc concentration between locations.
The highest levels of mercury, cobalt, cesium, scandium and zinc occurred at Poyang Lake, while
the highest levels of selenium, arsenic and bromine occurred at the Pearl River Delta. The
differences, however, were small, except for zinc, and in general the values were relatively low.
In feathers, there were significant differences in silver, cobalt, cesium, scandium concentration
between locations. The highest levels of cobalt e scandium occurred at the Pearl River Delta, the
highest levels of cesium occurred at Poyang Lake and those of silver occurred at Tai Lake. Again,
these differences were not small, except for cobalt, and the values relatively low.
In prey, there were significant differences in cobalt, cesium, scandium and zinc concentration
between locations. The highest levels of cobalt, cesium, scandium occurred in the prey from
Poyang Lake, while the highest levels of zinc occurred at Tai Lake, and again the differences were
not great and the values very low.
In sediments, there were significant differences in chromium, cesium, selenium and zinc
concentration between locations. The lowest levels of chromium occurred in Pearl River Delta
samples, and the values for Poyang Lake and Tai Lake were much higher and very similar. The
lowest values of cesium and zinc occurred in the Poyang Lake samples and the values for Pearl
River Delta and Tai Lake were much higher and very similar. The lowest values of selenium
occurred in Tai Lake and the concentration for Pearl River Delta and Poyang Lake were much
higher and very similar.

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Evaluation of environmental contamination levels. We discuss the concentration levels,
in relation to the thresholds that may be harmful to the birds, and that may indicate
alarming environmental pollution, and we evaluate the concentration levels in China in
relation to the levels found in other regions. However, the samples analyzed so far, owing
to incomplete analysis by AAS, in some cases are still too few to be meaningful.
Cadmium. Concentrations previously found in healthy populations of egrets and of herons in other
regions were similar to those found in China.
Lead. The levels found in eggs are lower than those previously found in egrets and herons
elsewhere. Much higher levels were found in egret feathers near Hong Kong in the early nineties.
Mercury. The concentrations found in fish are lower or similar to those found elsewhere, and are
gnerraly below the threshold for toxic effects.
Arsenic. Arsenic has been rarely determined in aquatic animals, and comparative data are few. The
concentrations found in tadpoles were rather high.
Copper, manganese, and iron. These elements are essential for life, and only become toxic at high
doses. No data have been published about these metals in eggs or feathers of wild bird populations.
Selenium. The concentrations found in eggs are rather high, but still lower than the threshold affecting bird
reproduction.
Zinc. Althought there were significant differences among the colony sites, the values we found in
eggs and feathers can be considered normal.

11. Heavy metal contamination in the samples from Pakistan page 64


The analytical techniques were the same as described about heavy metal contamination in China.
The results include only a half of the results of AAS analysis, that are still in progress.
Contamination level in the samples. In eggs, there were significant differences in the
concentration of zinc, cadmium, and lead between locations, with the highest levels of zinc and
cadmium in the samples from Haleji. However, the differences were limited, and the values were
very low.
In feathers, t here were significant differences in bromine, cobalt, cesium and copper concentration
between locations. The highest levels of bromine and cesium occurred at Karachi, the highest
levels of cobalt at Taunsa, and those of copper at Haleji. High concentrations of iron were found in
the samples from Karachi and Taunsa.
In prey, there were significant differences in chromium, mercury and lead concentration between
the three location, and the highest levels occurred in the samples from Karachi.
In sediments, there were significant differences in bromine, cesium, lanthanium cadmium and
mercury between the three study areas. The highest levels of bromine, cesium, cadmium and
mercury occurred at Karachi and those of lanthanium at Taunsa.
Evaluation of environmental contamination levels. As for China, we discuss the
concentration levels, in relation to the thresholds that may harm the birds, and that may
indicate alarming pollution, and we evaluate the concentration levels in Pakistan in relation
to those found in other regions. However, the samples analyzed so far, owing to
incomplete analysis by AAS, in some cases are still too few to be meaningful.
Cadmium. Concentrations previously found in healthy populations of egrets and herons in other
regions, were higher to those we found in Pakistan.
Lead. The levels found in eggs from Pakistan were lower than those previously found in egrets and
herons elsewhere.
Mercury. The values found in fish from Karachi were below the concentration associated with sub-
lethal or lethal toxic effects.

VII
Arsenic. It is a toxic, non-essential element, that has been rarely determined in aquatic animals. The
concentrations found in prey samples may be considered rather high.
Selenium. The concentrations found in eggs are rather high, but still lower than threshold that may
affect bird reproduction.
Zinc. The values we found in eggs and feathers can be considered normal.

12. Contamination by organic compounds in the samples from China page 77


Analytical methods. Chemical analyses were low. In prey, higher levels were found in fish and
tadpoles. The highest levels were found in the sediments from Poyang Lake.
PCBs levels were higher in the eggs of egrets from Tai Lake, followed by egrets from Pear River
delta and Poyang Lake. No PCBs were detected either in prey or in sediments at Poyang Lake.
Only vertebrate samples from Tai Lake had significant levels of PCBs. These pollutants were
detected in sediments from both Tai Lake and Pearl River Delta.
Pesticide pollutants were detected in all the eggs, both at Poyang Lake and at the Pearl River Delta.
Only one egg from Tai Lake had levels of pollutants below the limit of detection. The most
abundant pesticides were in all the cases DDTs, and in the Poyang and Pearl River Delta these were
present exclusively as the pp’-DDE congener. The proportion of PCBs was highest at Tai Lake and
Pearl River Delta than in Poyang Lake.
Comparison among study areas. To compare pollutant levels among different areas, only eggs of
Little Egrets have been considered. Significant differences were found for HCB, HCH, and PCB
levels, and for the ratios DDE/DDT, DDT/ TOTAL PESTICIDES, and DDTs/PCBs.
Evaluation of environmental contamination levels. HCB levels in the eggs from the three
areas were significantly different, those collected at the Poyang Lake had much lower
concentrations than those collected either at Tai Lake or at the Pearl River Delta, which in turn had
similar values. The levels found in prey, are surprising at a first, since HCB is present in all prey
from Poyang, but only in a few from Tai Lake. Furthermore, the levels at Poyang were higher than
at Tai Lake. Sediments at Poyang presented detectable levels of HCB, and below the detection
limit at the other two study areas, thus suggesting that HCB pollution is higher in the whole aquatic
compartment (sediment and aquatic biota) at Poyang Lake, while it is higher for terrestrial
secondary consumers at Tai Lake. Such a situation can only be explained by differences in recent
inputs of this pollutant into the aquatic compartment, i.e., at Poyang Lake HCB should have been
introduced more recently than at Tai Lake, where almost all the compound has been already
transferred to the upper levels of the food chain.
For HCH, both the percentages of detection and the concentrations, were similar in eggs from
Pearl River Delta and Tai Lake, and were significantly lower in eggs from the Poyang Lake,
following a trend very similar to that obtained for HCB. For prey items, concentrations were quite
similar between Poyang and Tai Lakes, but the percentages of detection were much higher at Tai
Lake, indicating a more recent pollutant input. Therefore, the results obtained for eggs also agree
with this scenario, since birds at Poyang presented lower levels, probably because they have had
more time to metabolize and excrete these compounds since the last input in that ecosystem.
Cyclodienes levels were very low in eggs and sediments at the Poyang Lake, and weer absent from
prey. This indicates a recent and localized source of pollution. Conversely, the levels at Tai Lake
and Pearl River Delta are higher and much more widespread in eggs, indicating more generalized
and ancient inputs.
DDT and derived compounds, which are the main indicators of pollution deriving from agriculture
treatments, were widely distributed, and were detected in most samples of eggs, prey, and
sediments. Levels in eggs from the three study areas did not differ. Therefore, the pollution by
such compounds is old, intense, generalized and persistent. One sediment sample from Poyang
Lake had extremely high levels of DDT, indicating a recent input of that pesticide in the ecosystem,

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despite that it was officially banned in China in 1982. Levels at Pearl River Delta were higher than
at Tai Lake.
PCBs are the indicators of organochlorine pollution deriving from industrial were done using high
resolution chromatography.
The compounds that were analysed include the following organochlorine that persist in the
environment:
• Hexachlorobenzene (HCB), a fungicide for seed grains and an industrial waste product.
• Hexachlorocyclohexanes (HCHs), used on seed and livestock
• Cyclodienes: Heptachlor and heptachlor epoxide, an insecticide primarily used to control soil
pests
• Endosulfan:an herbicied that however does not accumulate in warm-blooded animals.
• Dichloro-Diphenil-Trichloroethanes (DDTs), with insecticidal properties, which came into
wide agricultural use in the late 1940s, and that caused catastrophic population declines in certain
bird species. It was used extensively in agriculture, but their use has been restricted in most
countries, included Pakistan.
• Polychlorinated Biphenils (PCBs), a group of synthetic chlorinated aromatic hydrocarbons,
used since 1930 in commercial products including heat transfer agents, lubricants, dielectric agents,
flame retardants, plasticizers, and waterproofing materials. Environmental contamination has
resulted from several sources including.
Contamination level in the samples. HCB has been detected in most egg samples, higher levels
being found atTai Lake. HCB was present in all prey samples from Poyang Lake, but in a low
number of prey samples from Tai Lake. For sediments, only those from the Poyang Lake had
detectable quantities of HCB.
HCHs were detected in a high proportion of egg samples from Tai Lake and the Pearl River Delta,
and in few eggs from the Poyang Lake. HCH concentrations in eggs form Tai Lake and Pearl River
Delta were similar.
Cyclodienes. The eggs from Tai Lake and Pearl River Delta presented similar levels, and
cyclodienes were detected in most samples, whereas they were found only in one egg from Poyang
Lake and at a lower concentration. No cyclodienes were detected in prey at Poyang, but these
compounds were present in almost all the prey collected at Tai Lake. For sediments, higher levels
were found at Tai Lake, followed by those at Poyang Lake and at the Pearl River Delta.
DDTs and its metabolites. Total DDT levels were similar in the egret eggs from the three areas,
being detected in almost all the samples. DDTs were detected also in a high percentage of preys,
higher levels being attained by vertebrates, fish and tadpoles. Except for one sample taken in a
pond at Poyang Lake that exceeded 48 mg/kg, concentrations in the sediments sources. Significant
differences were found in the levels of PCBs and in their occurrence among study areas. Their
levels were very low in the eggs from Poyang, while atTaihu Lake the eggs had mean levels about
20 times higher than at Poyang and about double than at the Pearl River Delta. The same trends
were observed for sediments and for prey.. Therefore, Tai Lake is confirmed as the area most
affected by “industrial” pollution in China, among our three study areas.
The ratio DDT / PCB was similar for Tai Lake and the Pearl River Delta, whereas this ratio was
much higher for Poyang Lake, thus indicating a clear predominance of agricultural vs. industrial
pollutants in this last study area.
Comparison with Pakistan and with other regions.This comparison is based exclusively on
pollution in eggs, since heterogeneity of prey and foraging areas precluded the use of other types of
samples.
HCB were only detected in China and not in Pakistan. Levels in Little Egrets from the Danube
Delta were much higher.

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HCH levels in eggs ranged from 10 ppb at Poyang, to 50 ppb at Haleji Lake, and in ascending
order from low to high pollution were: Poyang - Taunsa – Pearl River Delta and Tai Lake – Haleji.
Therefore, for such compounds the Poyang lake fits better the condition of low pollution area, than
its corresponding area in Pakistan (Haleji Lake). In general, the levels were very low, and well
below the dangerous exposure to the toxicant. This is also the case for all the other species of egrets
analyzed in the other study areas, Karachi, Haleji, and Taunsa.
Cyclodienes. Since there are only data from our samples, comparison with other areas is precluded.
The lower levels were found in the most natural areas in China (Poyang) and in Pakistan (Haleji).
Intermediate levels were found at the two agriculture and industry polluted areas in China (Pearl
River Delta and Tai Lake), and higher levels at the two study areas with intense agricultural
(Taunsa) and industrial develoment (Karachi) in Pakistan. However, these levels are much lower
than those reported to have effects in birds.
DDTs. Little Egrets from the three areas in China had similar levels of these pollutants, but they
reach the highest levels in eggs from the supposed pristine area (Poyang Lake), which had levels
about fivefold those of its counterpart in Pakistan (Haleji). Only the most DDT-polluted of our six
study areas (Taunsa), showed higher average levels of DDTs than Poyang Lake. These levels are,
however, below those reported from Europe and America. However, the levels reported for Little
Egrets in Italy wer much lower. In any case, the levels in China and in Pakistan seem to be well
below those having adverse effects on bird reproduction.
PCBs. Except from some samples at Karachi, the levels we found were low compared to literature
data. Poyang and Haleji fitted well to their condition of pollution-free areas for these compounds,
followed in order of increasing contamination, by Taunsa, Pearl River Delta, and Tai Lake. Levels
in Tai Lake are similar to those found in Italy and in other parts of Europe and of America. The
levels are much lower than those affecting embryo development or survival in different bird
species.
Concluding remarks. In China, the Poyang Lake area is characterized by lower impact of HCBs,
HCHs, Cyclodienes and PCBs, but had the highest average levels of DDT. Another characteristic
of Poyang Lake samples was their heterogeneity, since the percentage of samples containing
different organochlorine contaminants was very variable. This indicates that, even though Poyang
Lake ecosystems had low levels of organochlorines, there are important local sources of pollution,
some of them responsible of recent inputs.
At Tai Lake, the pollution was highest for PCBs, indicating that this area, and not the Pearl river
Delta, is the one most affected by industrial pollution. Conversely, the levels of DDTs were
somewhat higher at the Pearl River Delta. At both localities, the input of pollutants seem to be
older, much more homogeneous (i.e. generalized) than at Poyang lake, as indicated by the
percentage of samples having detectable levels of the different organochlorine contaminants. PCB
and DDT excepted, these two areas showed homogeneous levels of pollutants.
In general, the levels found in the different areas included in this study are lower than those
reported for Europe and north America, and below the observed ranges having adverse effects on
bird reproduction or survival.

13. Contamination by organic compounds in samples from Pakistan page 96


The analytical techniques, and the compounds, were the same as described for China.
Contamination level in the samples. HCB levels in the eggs were relatively low, and
were similar for Haleji and for Karachi, while levels from Taunsa were much lower. In
both prey and sediments, HCB was only detected in samples from Haleji Lake.
HCHs were detected in most eggs, but they were almost undetectable in both prey and sediments.
The highest value were found at Haleji.
Cyclodienes were almost absent from Haleji. Nevertheless, although at low levels, they were
detected in egg samples from Taunsa and Karachi. Concentration in Little Egrets from the two

X
latter areas were similar, but Cattle Egret from Taunsa had lower levels. Fish samples from Karachi
had remarkably high concentrations. At Haleji the most abundant cyclodiene was α-endosulfan. In
Taunsa, heptachlor epoxide reached higher concentrations than the other cyclodienes, whereas in
Karachi the most abundant was β-endosulfan.
DDT compounds were found in all the egg samples. Mean levels were higher at Taunsa, followed
by Karachi. Nevertheless, maximum values were found in Intermediate Egrets from Haleji. In prey,
these compounds were not detected in all the samples, highest values being found in fish.
Remarkably, no DDTs were detected in sediment samples from Taunsa.
PCB’s highest values were detected in the eggs from Karachi. Egret eggs from Taunsa had much
lower concentrations, but above those from Haleji. Prey samples from different localities had
similar PCB concentrations. In sediments, the higher values were recorded at Karachi. No PCBs
were found in sediments from Haleji Lake.
Comparison among the three study areas. To compare different areas, only samples form Little
Egrets were considered. Significant differences were found in the levels of HCB, DDTs, PCBs, and
also in the ratio ppDDE/ TOTAL DDTs, and in the ratio DDTs/PCBs.
Evaluation of environmental contamination levels. There is no information about the levels or the
impact of persistent organic pollutants in wetlands of Pakistan. Presently, pesticides in Pakistan
are applied mostly to cotton fields, that are concentrated mainly in Punjab, Sindh, and to a lesser
extent in Baluschistan. The pesticides in use are mostly insecticides. Pesticides are also applied to
other crops, such as vegetables and fruit. Estimated consumption of pesticides in Pakistan ranged
from 13,030 metric tons in 1990-91, to 30,471 metric tons in 1995-96. The results presented here
constitute a first evaluation of the impact of several organochlorine pollutants.
At Haleji Lake, DDTs have been found been found in all the egg samples, and they are the
pollutants which attain the highest concentration in eggs. Concentrations however, were lower or
similar to those reported elsewhere for heron, and in most cases they lower than the levels reported
to be detrimental to these birds. Nevertheless, the concentration in three eggs of Intermediate
Egrets were above these levels, and therefore some birds are exposed to high DDTs levels,
probably while feeding in agricultural areas or paddy fields. Eggshell of these eggs was thinner
than in eggs with less DDT. The high DDE/DDTs ratio in the eggs suggests that exposure to DDT
is recent. Other organochlorines in the eggs, HCHs, HCB and PCBs, are less abundant than DDTs,
and appear in low concentration. Available data on HCH usage indicates a lower consumption of
these pesticides in Pakistan compared to neighbouring countries like India or China. The fact that
no HCH was detected in fish or sediments is in agreement with the findings of several authors, who
reported a low accumulation of HCH in aquatic organisms and sediments in the tropics. The low
levels of PCBs in the eggs at Haleji, and its absence from fish and from sediments, indicate a low
industrial activity.
At Taunsa, the highest organochlorine levels in eggs corresponded to DDTs, mainly DDE
that was found in all the samples, thus indicating a wide distribution. DDE is present in
aquatic prey, fish and frogs, but not in insects sampled. The differences observed between
Little and Cattle egrets at Taunsa are relatable to their feeding habits, since Little Egrets
feed markedly on fish, while Cattle Egrets depend on terrestrial preys, such as including
insects. Cyclodiene compounds were the second organochlorine pollutants in importance in the
eggs, followed by PCBs and HCHs. The level of PCBs are generally low compared to literature
data, and do not pose a threat to the birds.
At Karachi, the samples from the egrets showed high levels of several organochlorine
pollutants, particularly PCBs and DDTs.. Nevertheless, none of the samples had
concentrations above levels associated to risk. These compounds were detected also in the
fish which constitute its prey. Within the sediments, mud has a much higher concentration
compared to samples collected in the channel. PCBs are the organochlorines reaching the
highest levels at Karachi. Their maximum concentrations are found in the eggs, and in lower
amounts in prey and sediments. These pollutants were detected in all the eggs and prey samples,
thus indicating a wide distribution of PCBs in the Karachi area, probably related to discharging of

XI
untreated sewage waters, both from industrial and domestic origin. The sensibility of birds to PCBs
and their effects on bird reproduction are highly variable between species, but the levels of PCBs in
eggs are lower than those reported to cause detrimental effects in other bird species. The levels of
cyclodiene insecticides were also moderately high. These compounds were found in all the egg and
n all the prey samples.
Concluding remarks. Overall, the results show that the egret eggs reflect well the expected
differences in exposure to the different pollutants among the three study areas. Haleji Lake,
selected as the natural area in Pakistan, showed significantly lower concentrations for cyclodienes,
DDTs and PCBs than the other two areas. Taunsa is characterized by higher concentrations of
cyclodienes and DDTs, with relatively low levels of PCBs. Karachi shows relatively high
concentrations of cyclodienes and DDTs, and very high concentartions of PCBs, and it is the only
area where such industrial organochlorines reach higher levels than the pesticide compounds.
In contrast, HCB levels, albeit very low in general, are significantly higher at Haleji, and smaller at
Taunsa than at Karachi. Only at Haleji sediments and prey presented detectable levels of HCB, and
this indicates a recent input.
The average DDTs levels were higher in the eggs at Taunsa and at Karachi, than at Haleji. It must
be taken into account that Taunsa is a mainly agricultural area, which probably received high
inputs of pesticides and of DDTs among them. On the other hand, Karachi lies at the end flow of
the Indus, and receives water which has been used for municipal, agricultural, and industrial
purposes. Moreover, none of the cities along the Indus River treat the water before discharging,
thus agricultural pesticides may arrive with the water supply. The lack of farming activities around
Haleji would result in lower levels of pesticides reaching these waters, and atmospheric transport
would account for most of the DDT presence in the area.
For HCHs, no difference was found among the three study areas. It was shown that about 99,6% of
HCHs applied to paddy fields in tropical agrosystems are volatilized to the atmosphere, and it was
estimated that only 0,1% of the applied HCH was ultimately drained to the sea by the river. In spite
of the recent use of HCH in some Southeastern Asian countries, the residue levels in fish are low,
because of the rapid volatilisation of HCH at tropical latitudes.

14. Conclusions page 116


Contamination data show that concentration levels are generally lower than the threshold known to
harm wildlife, both for metals and other elements, and for organic compounds, with some
exceptions. These results are mostly welcomed, in that they testify a reduced environmental
contamination.

15. References page 117

Appendix A. List of samples collected in China, and their content of metals page 127

Appendix B. List of samples collected in Pakistan, and their content of metals page 132

Appendix C. List of samples collected in China, and their content of organic contaminants page 136

Appendix D. List of samples collected in Pakistan, and their content of organic contaminants page 140

XII
Introduction

The INCO-DC project “Colonial waterbirds as bioindicators of contamination in selected wetlands of


China and Pakistan” was funded by the European Union (Contract IC18-CT98-0294), and was
accomplished from September 1998 to September 2001 by the six partners:

• Dipartimento Biologia Animale, Università, Piazza Botta 9, I-27100 Pavia, Italy


Mauro Fasola (e-mail fasola@ipv36.unipv.it) , project’s coordinator
TU UT

• Departament. de Biologia Animal, Avgda. Diagonal 645, 08028-Barcelona, Spain


Xavier Ruiz (e-mail xruiz@porthos.bio.ub.es), local coordinator

• Pakistan Agriculture Research Council, P.O. Box 1031, Islamabad 45500, Pakistan
Umar Khan Baloch (e-mail ukbaloch@hotmail.com), local coordinator

th
• WWF-Pakistan, 6 Floor, Block 6, P.E.C.H.S Shahra-e-faisal, Karachi 75400, Pakistan
Rahat Jabeen (e-mail wwfkhi@khi.compol.com, rahat@hotmail.com), local coordinator

• Biological Resources Institute, Jiangxi Academy of Sciences, Nanchang, Jiangxi 330029, P.R.
China
Dai Nianhua (e-mail nhdai@public.nc.jx.cn), local coordinator

• Department of Soil Ecology and Environmental Science, Institute of Soil Science, Chinese
Academy of Sciences, P.O. Box 821, Nanjing 210008, P.R. China
Yuanhua Dong (e-mail yhdong@ns.issas.ac.cn), local coordinator

with collaboration by:

• Dipartimento Chmica Farmaeutica, Università, Viale Taramelli, I-27100 Pavia, Italia


Carlo Gandini (e-mail carga@unipv.it) , chemical analisys
TU UT

• Dipartimento Chmica generale, Università, Viale Taramelli, I-27100 Pavia, Italia


Edoardo Orvini (e-mail orvini@chifis.unipv.it) , chemical analisys

• Department Biology, Lanzhou University, Lanzohu 730000, PR China


Yingmei Zhang (e mail pyk@lzu.edu.cn) , collaborator
TU UT

1
1.

Environmental contamination, and human health

Fasola Mauro
Dipartimento Biologia Animale, Università, Piazza Botta 9, I-27100 Pavia, Italy

A dramatic increase in public awareness and concern about the state of the environment has occurred in
recent decades, in relation to a growing evidence on the extent to which pollution has caused severe
environmental degradation. The introduction of harmful substances into the environment has been shown to
have many adverse effects on human health, agricultural productivity, and natural ecosystems, although it is
surprising how resilient environmental systems are to the pollutant burden so far imposed to them. Pollution
is one aspect of environmental degradation which arouses most interest, because it impacts directly upon
people through effects on their health, food, cultural heritage and the countryside. The costs of these effects
in the depreciation of resources, lost productivity and the need to clean up polluted environments are high,
and are increasingly occupying the attention of governments around the world (Alloway & Ayres 1997).
Although cases of acute and overt pollution shock the public opinion, less appreciated but more important is
the fact that most environments suffer from insidious chronic pollution. The effects of chronic pollution only
become apparent after long exposure, e.g. in the case of people exposed to pollutants that may cause cancer
10 or 20 years later, or in the case of toxic effects in trees that appear after 20 years and are irreversible. For
this reason, environmental monitoring is vitally important in detecting insidious pollution. An example of
human health problem which is causing growing concern, is decline in male fertility in technologically
advanced countries over recent decades. This is tought to be caused at least in part, by exposure to pollutants
which have effects similar to female hormones. But exposure to these oestrogenic chemicals has probably
occurred during the past decades, and the time lag for their effects to appear makes remediation difficult.
Pollution is the accumulation and adverse interaction of contaminants with the environment. A contaminant
is any substance that occurs in the environment at least in part through human action, and that at the levels
found, has deleterious effects on living organisms. Contaminants may result from natural processes, but
presently the main concern is that human activities are increasing the amount of contaminants into the
environment. The contaminants are released into environment, consisting of soil, surface waters, the
atmosphere, and their living inhabitants, where they accumulate or undergo physical and chemical changes.
Taken together, the way in which substances are added to the environment, the rate at which these wastes are
added, and the subsequent changes that occur, determine the impact of the contaminant on the environment.
The modern types of contamination include several xenobiotic substances, compounds that are foreign to
natural systems, and which are usually less subject to biodegradation, i.e. the breakdown of organic
compounds by organisms, up to complete degradation and to mineralization. The problem with contaminants
is exacerbated by the human population growth, and hence by the amount of toxic substances produced and
released into the environment (Pepper et al. 1996). Environmental contamination with these substances may
come from many sources:
• air pollution, that may introduce metals into the environment, with the particulate matter produced by
combustion
• surface water pollution, through waste disposal
• agricultural fertilizers, that contain the 16 elements essential for plant growth; but excess amounts of
these elements may cause pollution

2
• agricultural pesticides, which are essential to sustain productivity; however some of these pesticides,
particularly chlorinated hydrocarbons, are very persistent and subject to bioaccumulation
• waste disposal
• industrial processes, that may as a side effect disseminate an array of chemical elements and compounds,
including metals, and polychlorobiphenils used for various processes.
Nowadays, about 1000 new chemical compounds are being synthesized each year, and between 60.000 and
95.000 chemicals are in current commercial use.
Substances may be toxic or non-toxic, but toxicity may depend on concentration above certain thresholds.
Concerns about toxic substances in food and in the environment arose at the beginning of the twentieth
century. The systematic study of toxic effects in laboratory animals began in the 1920s, but toxicology grew
in importance especially after the 1940s, in relation to the development of industry and of evolved
agriculture. One of the factors which led to a increase in environmental awareness and concern about
pollution was the publication of certain inspiring books during the 1960s, like “Silent spring” by Rachel
Carson in 1962. At the time this book was written, developments in plant breeding and pest control had
boosted optimism in advanced countries, food production was increasing rapidly along with an exponential
rise in the use of pesticides and fertilizers, and little attention was given to the consequences of their
accumulation in the environment. The effects of pollutants on animals and humans include acute alteration of
vital parameters, and subclinical, chronic effects that may impair their vitality and reproduction, like
carcinogenesis, mutagenesis, teratogenesis, damage to the immune system, chromosomal abnormalities,
modifications of enzymes function and of nervous transmission. Studies on birds had the merit of raising
early alarms about the dangers posed by pollutants in the environment. Three main mechanisms of bird
population decline in relation to contamination have emerged (Newton 1998). First, some contaminants
cause directly deaths or breeding failures. Secondly, other contaminants act indirectly by reducing food
supply. Thirdly, other chemicals can alter the physical or chemical structure of habitats, making them less
suitable for certain species.
A solution to the problems posed by contamination must start from the monitoring of these substances in the
environment, through the collection and analysis of samples.
While a pletora of studies about environmental contamination exists for America and Europe (summarized in
books such as Alloway & Ayres 1993, Pepper et al. 1996, Beyer et al. 1996), comparatively very few studies
exist for Asia: on birds of China (Burger & Gochfeld 1993, Jeng & Yang 1995) of Korea (Honda et al. 1986,
Lee et al. 1989), of Russia (Lebedev et al. 1998); on other components of the environment of China (Chui et
al.1991, Connell et al. 1998), of Korea (Jung & Thornton 1997), of Japan (Doi et al. 1984), of Iran
(Sodergren et al. 1978), and of India (Ramesh et al. 1992); on humans of China (among others, Cai et al.
1995, Nordberg et al. 1997, Yang et al. 1994), of Japan (Fujiwara 1975, Ikeda 1992), and of India (Nair &
Pillai 1992).
This research project aimed to ascertain the levels of the most widespread contaminants with long term
persistence, heavy metals, chlorinated hydrocarbons, and polychlorobiphenils, in some environments of
China and of Pakistan.

Birds as bioindicators
Toxicology studies the adverse effects of chemicals on the health of both humans and of all the components
of the natural environment. Non-target organisms absorb contaminants through their food, but also through
their skin and through inalation. If pesticides destroyed only the target pests and then quickly broke down to
harmless by-products, problems for their use would be minimal. But most pesticides are non-specific, and
kill a wide range of organisms. Secondly, while some broke down rapidly, others last for weeks, months or
even years in animal bodies or in the physical environment. Thirdly, some pesticides accumulate in body fat
and readily pass from prey to predator, causing secondary poisoning, or even pass along several steps in a
food-chain, affecting animals far removed in trophic position from the target pest. In addition, by
contaminating air and water, some contaminants can reach areas and affect organisms far removed from
points of application, as shown by the famous examples of DDT present in penguins of the Antarctic.
Several authors have pointed to the use of animals to monitor changes in the aquatic or terrestrial
environments. Although the use of sedentary invertebrates has been stressed, some characteristics of birds

3
make them very useful. They are able to integrate pollutant levels in the whole ecosystem or over a broad
area and thus, less sampling would be necessary. Also, since they are usually placed at high nodes in the
food webs they can reflect pollutant hazards to humans (Furness, 1993). Nevertheless, biomonitoring
programmes have been proven to be more satisfactory when combining biological indicators (at different
levels) along with chemical and/or physical ones.
Throughout the world, birds are affected by environmental contaminants including organochlorine
compounds, organophosphorous insectidicdes, trace elements, and petroleum. Well known cases of
population decline due to accumulation of DDT regard some raptors, the Peregrine falcon Falco peregrinus,
the Sparrowhawk Accipiter nisus and the Osprey Pandion haliaetus in Europe, and various fish-eating and
seed-eating birds. Some of these species have now recovered, 20 years after the ban of DDT use in Europe.
Heavy metals, and organic pesticides, are among the major ecotoxicants for which we need the earliest
possible indications of rising levels, both at local and at global scale. The need to determine the exposure to
these pollutants, and to evaluate their effects, has led to the development of numerous monitoring programs.
As it is not possible to measure all ecosystem functions and properties, bioindicators are increasingly used to
monitor environmental quality and ecosystem-level change. A bioindicator may be defined as an organismic
property so strictly associated with particular environmental conditions, that its presence is indicative of the
existence of these conditions.
In order to monitor the abundance of persistent pollutants, their environmental consequences and to assess
ecosystem health, we need to use effective bioindicators, i.e organisms that accumulate contaminants that
may be present only at trace levels, so as to allow pollutant detection earlier than would be possible from
abiotic samples (Pedersen and Myklebust 1993). Bioaccumulated contaminants integrate and reflect both
chronic and intermittent exposure, which could be missed in periodic sampling of abiotic material (Lovett
Doust et al. 1994). Herons and egrets, are at the top of the food chain as predators of aquatic animals, and
therefore accumulate many persistent environmental contaminants, including organochlorine pesticides,
polychlorinated bipheninyles (PCBs) and metals. Their mobility and their use of agricultural habitats result
in high exposure to contaminants, and their communal roosting and nesting facilitate sampling (Kushlan
1993). They are therefore good indicators of the contamination of aquatic environments (Custer et al. 1991).
Biomagnification allows the early detection, at higher trophic levels, of contaminants with relatively low
concentration in the environment (Vermeer and Castilla 1991). Accumulation depends on the transfer of
heavy metals in the food chain and thus on the composition of the diet at different trophic levels. Body load
increases with the age of the animal, if the intake exceeds metabolic rate and excretion (Vaan Straalen 1988).

Environmental contamination by organic compounds


Several organic compounds contaminate the environment, with different properties as regards acute toxicity,
persistence, and accumulation in non-target organisms. Biodegradability is the main characteristic that
renders pesticides environmentally friendly.
Organocholorine insecticides:
• DDT and its metabolites (DDE, DDD), with low acute toxicity but very high persistence, and very high
accumulation.
• Lindane, with low toxicity, and moderate persistence and accumulation
• Ciclodienes (aldrin, dieldrin) with low toxicity, and high persistence and accumulation
The insectidcide DDT came into wide use in agriculture in the late 1940s. Catastrophic population declines
in certain species, notably raptors, and related eggshell thinning were well documented after 1946, the period
associated with the widespread use of DDT and other organochlorines. Therefore, strong concern about
wildlife contamination arose in the 1950s and 1960s, in relation to persistence of DDT in the environment
and to the associated mortality of some species of birds, particularly raptors and waterbirds, in Europe and in
America (Beyer et al. 1996). DT was banned in the United States in 1972, and during the 1970’s in Europe,
but remained in use in the developing countries of Africa and of Asia.
The manufacture and the use of organochlorine compounds in developed nations has decreased remarkably
during the last three decades, but in some developing countries they are still used in the treatment of
agricultural pests and as insecticides for vectors of malaria. In tropical ecosystems the environmental fate of

4
these pollutants is affected by high temperatures and heavy rain, which increase the dispersion rate (Iwata et
al. 1994, Kannan et al. 1995). However, few data on organochlorine pollutants in biota from tropical
ecosystems have been published and, to our knowledge, no data are available from wetlands in Pakistan.
Lindane was still widely used in some parts of Asia during the 1990s.
Organochlorine-caused mortality of adult herons and egrets was attributed primarily to dieldrin exposure
(Custer 2000), and the decline of many species in North America after 1945 probably resulted mainly from
lowered reproductive success. Herons and egrets are highly sensitive to DDE-induced eggshell thinning, that
was first documented in grey herons Ardea cinerea (Prestt 1970).
Organophosphorus (e.g. Parathion, Malathion) and carbammate (e.g. Carbaryl) insecticides, with high
toxicity, but low persistence and accumulation. They are the most widely-used pesticide at present. Their low
persistence diminishes the dangers for the environment.
Polychlorinated biphenyls (PCBs). These compounds have low toxicity, but are persistent. They are
composed by mixtures of biphenyls at different chlonrination levels. They are very widespread, because they
have several uses including insulating or cooling agents, and because contamination results from several
sources including industrial discharge, leak, disposal, and incomplete incineration. Production peaked in
1970, but was then prohibited since 1979 in the United States, where their concentrations are generally low
and not associated with impaired survival and reproduction of herons, with few exceptions. Declines in
populations of gulls, otters and dolphins have been attributed3 to PCBs. At normal levels of exposure, PCBs
are not very toxic to humans, although incidents due to food contamination occurred in Japan.
Dioxins. Appear as by-products of herbicides. Are highly toxic and teratogenic contaminants, suspected to
have had adverse effects on embryonic development of bird species at some locations.
Pesticide usage is increasing, in terms of area treated, of number of applications per year, and of variety of
chemicals in use. By 1990, about 300 chemicals were in use worldwide as insecticides, 290 as herbicides,
and 165 as fungicides and other pesticidal compounds, with a grand total of more than 3000 formulations
(Freedman 1995). Between 1945 and 1989 their use increased by 10 times in the United States, a country
that accounts for about one third of the global total. For these reasons, we can expect that the impact of
pesticides is likely to have increased progressively during the past 50 years, and will continue to increase in
the future.
The studies about the impact of organic pesticides upon wildlife, were directed both at the effects on animals
within treated areas, and at the persistence of residues away from treated areas, as summarized by Beyer et
al. (1996). Among the first reports of organochlorine residues in wildlife were those of DDT in tissues of
birds exposed either to laboratory or to orchard treatments in the 1950s. Experimental applications of DDT
caused considerable mortality of nestling songbirds. Several filed and laboratory studies followed during the
1950s and 1970s. However, some kinds of insecticide effects were not observed until 15 years or more after
the introduction of the synthetic organic insecticides. In particular, the effects in areas away from treatments
were discovered after delay. These studies met several difficulties, including: standardizing the analytical
methods; discerning the causal agent of mortality or of decrease among the many contaminants present in
single organism; identifying the source of contaminants. Contamination studies had also to face skepticism,
and sometimes opposition from people with economic interests in pesticides.
Many studies determined the amount of a chemical present in non-target organisms, and compared the value
with those found to produce detrimental effects. the use of different tissues as samples for analysis made
comparisons difficult. The bioaccumulation through the food chain was also investigated. Residues were not
distributed equally in all habits and in all organisms. The exposure of birds and mammals to residues seemed
related primarily to their food habits. Owing to pesticide-induced reproductive impairment, several bird
species, especially raptors and waterbirds, become endangered or suffered strong reductions in their
populations.
The presence and persistence of pesticide residues in the environment has prompted for monitoring
programs, assisted by governmental agencies in Europe and America

5
Environmental contamination by inorganic elements
Metals and metal-containing contaminants are not degradable in the sense that carbon-based molecules are.
Their nondegradability means that it is difficult to eliminate metal atoms from the environment. Therefore,
localized, elevated levels of metal contamination may occur. These metals can accumulate in biological
systems, where their toxicity poses serious threats to human and environmental health (Pepper et al. 1996).
Unlike most organic pollutants, heavy metals and other inorganic elements occur naturally , and so there is a
range of normal background concentrations of these elements in the soil, sediments, waters, and living
organisms. Pollution gives rise to anomalously high concentrations of these elements relative to the normal
levels, therefore only their relative concentration above a certain threshold indicates pollution.
Heavy metals are widely used for several industrial productions, and consequently they tend to reach the
environment from a vast array of anthropogenic sources as well as natural geochemical processes.
Anthropogenic sources include:
• metalliferous mining and metallurgical industries
• agricultural fertilizers (that may include impurities with Cd, Cr, Mo, Pb, U, V, Zn)
• agricultural pesticides (with Cu, As, Hg, Pb, Mn, Zn)
• agricultural desiccants (As for cotton)
• wastes and sewage from animal farms (As, Cd, Cr, Cu, Ni, Pb, Zn)
• fossil fuel combustion (As, Ba, Cd, Cu, Ni, Pb, Sb, Se, Mn, V)
• other sources, manufacture and disposal
Monitoring heavy metal concentration in biota can reveal trends in time and space of the body burden of
organisms (Reid and Hacher 1982). It is also used to explore the nature and extent of the biological impact of
these metals (Ernst 1991). Heavy metal concentration can be compared to background levels, and their
bioavaibility can be determined. Biomonitoring heavy metals can help when supervising and adjusting
government action to correct this pollution (Canters and Snoo 1993).
After absorption, heavy metals accumulate particularly in bone, kidney, liver, and in feathers. Bird feathers
are particularly useful as an indicator tissue for metal exposure, and have been intensively used to this aim
since the 1960 (Burger 1993). Feathers are rich in keratin, and the metals and metalloids bind to their
sulfhydryl groups. Metal concentration in feather reflects the levels present in the body of the bird at the time
of feather growth, when their blood supply is intact (Goede and deBruin 1984). Circulating levels, however,
can come from current ingestion (through food or water) or from mobilization from metal stored in other
tissues. Indeed, one mechanism birds have for the elimination of heavy metals from their bodies is to
sequester them in their feathers (Braune and Gaskin 1987, Becker et al. 1993). Metals can also be eliminated
directly throught excreta, throught the salt gland (Burger and Gochfeld 1985) or can be stored in tissues
(Braune and Gaskin 1987, Burger 1994). For Mercury, 93% of the body burden is in the birds’ plumage
(Braune and Gaskin 1987). Moreover, nestling of birds such as herons and egrets lose the down they are born
with, and grow entirely new plumage while being cared for by their parents. Thus, metal levels in their
feathers come from the local environment, and can be used as a good indicator of local pollution. Further,
collecting feathers is non-invasive, and birds can be released alive; feathers are easily collected, handled, and
stored in the field and don’t require refrigeration and the same birds can be sampled repeatedly. Furness et al.
() suggest that body feathers are the more suitable tissue for analysis than other feathers, such as those from
wings and tail.
Females can also sequester heavy metal in their eggs (Burger and Gochfeld 1993, Dauwe et al. 1999), and
high levels of mercury (Fimreite et al. 1982, Haseltine et al. 1981), of lead, cadmium (Maedgen et al. 1982),
and of other metals (Burger and Gochfeld 1991, 1993, 1995), have been reported for eggs. In general,
mercury accumulates well in both feathers and eggs, while cadmium and lead accumulate better in feathers
than in eggs. So eggs can supplement feathers, providing additional information than either alone (Becker et
al. 1993).
Hazardous heavy metals. The most hazardouse elements of concern to waterbirds include cadmium,
chromium, mercury, lead, and selenium. (Kushlan & Hafner 2000). At high dose, heavy metals produce
lethally toxic. At low doses, they can cause sublethal toxic effects, such as slower reactions to stimuli or

6
weight loss (Honda et al.1990) Toxic effects of heavy metals are also related to their bioavailability
(Graveland 1990), and to the organism’s physiological status (Osborn 1979, Blomqvist et al. 1987,
Krasowski and Doelma 1990). The interactions between metals are very important as well. Lead, for
example, interacts with calcium or phosporus (Graveland 1990) and interactions between cadmium and
copper, zinc or selenium are well known (Voogt et al. 1980, Goede and Voogt 1985).
Cadmium. A highly toxic non-essential metal, that is a known teratogen and carcinogen, and is probable
mutagen. In birds, effects of chronic cadmium exposure typically include growth retardation, anemia, and
testicular damage (Eisler 1988). It may induce intracellular production of metallothionein, a low- molecular-
weight protein rich in sulfur aminoacids to which cadmium can be bound and, hence, rendered less toxic. A
high accumulation of cadmium can, but does not always, lead to food chain amplification, because
metallothionein-bound cadmium has a long biological half life in animals and because concentrations tend to
increase with age. Cadmium concentrations in birds are almost always highest in the kidney, lower in the
liver and very low in muscle and in eggs. It’ s often not clear wether cadmium in feathers is derived from
deposition into growing feathers from circulating cadmium in the blood, or wether it is all from atmospheric
or aqueous deposition onto feather surfaces (Hahn 1991), so feathers provide little or non information on
cadmium accumulation from food.
Chromium. A micronutrient that is essential to animals. Toxic concentrations for fish range from 0.2 to 5
ppm of water.
Mercury. A toxic metal with no known essential function in vertebrate organisms. Mercury is neurotoxic
and teratogenic, and it is resposible for poisoning of human population through the food chain, from waste to
sediments, to fish consumed by hemansFish-eating birds such as herons and egrets are exposed to mercury
(particularly methylmercury, that is the most stable and toxic form of mercury) in the diet. Much ingested
mercury goes into plumage during feather growth, and the body pool of mercury declines as moult
progresses. In growing chicks, mercury concentrations increase in down but not in soft tissues with age.
Feathers from nestlings provide a good indicator of mercury exposure of the adults.
Lead. A nonessential metal, highly toxic heavy metal that affects all body system. The main sources of lead
pollution are petrol, fumes from petrol combustion, constituents of paint and solders, lead shots used for
hunting. ON a comparative basis, lead is neither as toxic as many other heavy metals nor as bioavailable;
however, it is more obiquitous and it is a cumulative toxic. Lead absorption may result in a range of
sublethal effects or in mortality. It acts at the molecular level affecting the haematological, muscular,
behavioral, nervous and reproductive system. Aquatic birds at risk from lead include waterbirds like ducks
and geese, inhabiting areas with frequent hunting activities. These birds ingest lead shots from the bottom
surface, as they ingest small stones in order to facilitate digestion. Avian predators may eat gamebirds
wounded by hunters, and aquatic birds feeding near smelters, refineries and lead battery recycling plants may
be contaminated. Herons and egrets are generally not at risk from lead, because they do not normally ingest
lead shot, and because forms of lead other than shot do not generally cause clinical signs of lead poisoning in
birds. Lead, like cadmium, cannot be entirely removed by washing procedures, and lead concentrations in
feathers can be attributable both to external contamination and to dietary lead uptake during feather
formation. This could happen particularly in areas subject to the heavy vehicle traffic and continued use of
leaded gasoline.
“Essential” elements. Some elements are required by living organisms in small but critical concentrations
for normal health, and are therefore referred to as “essential”, because they are constituents of enzymes and
of other important proteins, but their excess concentrations cause toxicity. Elements that are certainly
essential are Cu, Mn, Fe, and Zn for both plants and animals, cobalt, Cr, selenium and I for animals, B and
Mo for plants. Some other elements have been shown to have some beneficial effect, but are not likely to be
responsible for deficiency under normal conditions. Their absorption is regulated by homeostatic
mechanisms (Friberg et al. 1986).
Copper may cause toxicity problems in animals grazing on polluted soils if the herbage contains >10 ppm of
Copper.
Very little information is available on the effects of manganese, iron, and cobalt.
Selenium is a naturally-occuring trace element that is essential for animal nutrition, but the range between
dietary requirements and toxic levels is relatively narrow (Eisler 1985, Ohlendorf 1989).

7
Zinc is an essential nutrient for higher animals, and toxicity values are generally greater than values for non-
essential metals. It is relatively non-toxic to animals, and several zinc-based enzymes or other proteins have
been identified.
“Non-essential elements”. Other elements with no known essential biochemical function are called “non-
essential elements” and cause toxicity at concentrations exceeding the organism’s tolerance. All these
elements may be responsible for toxicity at high doses.
Arsenic. Arsenic has been rarely determined in aquatic animals. It is a toxic, non-essential element. The
concentrations found in wildlife range from non-detectable to 2.9 ppm ww. Therefore, the values we found
in tadpoles are rather high.
Very little information is available on the effects of silver, Bromine, cesium, lanthanum, nickel, scandium.

The behaviour of pollutants in the soil


Sediments are repositories for physical and biological debris and sinks for a wide variety of chemicals. The
concern associated with the chemicals sorbed to sediments is that many commercial species and food-chain
organisms spend a major portion of their life-cycle living in or on aquatic sediments. This provides a
pathway for these chemicals to be consumed by higher aquatic life and wildlife, including avian species as
well as humans. Direct transfer of chemicals from sediments to organisms is now considered to be a major
route of exposure for many species. These issues are focusing attention on sediment contamination and
highlight the fact that sediments are an important resource (Adams et al. 1992).
Because sediments are both carriers and potential sources of contaminants in aquatic systems, these materials
may also affect groundwater quality and agricultural products when disposed on land. Contaminant are not
necessarily fixed permanently in the sediments but may be remobilized when physico-chemical conditions
change. Bioavailability of toxic chemicals and food-chain transfer may be strongly affected by such
processes and by the type of chemical binding on the sediment particles. When pollutants reach the soil
surface they are either adsorbed with varying strengths on the colloids at the surface of the topsoil, or are
washed down through the surface layer into the soil profile in rainwater or snow melt. Soluble pollutants will
infiltrate into the topsoil in the system of pores where the adsorption of ions occurs. Insoluble compounds
will accumulate on the surface and hydrophobic organic molecules will bind to sites on soil organic matter
at the soil surface. These substances become incorporated into the topsoil and deeper profile during
mechanical soil movement or down dessiccation cracks while being adsorbed on soil particles. Some organic
pollutant molecules on the soil surface will undergo photolytic decomposition as a result of exposure to UV
wavelengths in daylight.
Several different types of adsorption reaction can occur between the surfaces of organic and mineral colloids
and the pollutants. The extent to which the reactions occur is determined by the composition of the soil
(especially the amounts and types of clay minerals, hydrous oxides and organic matter), the soil pH, redox
status, and the nature of the contaminants. The more strongly pollutants are adsorbed, the less likely they are
to be leached down the soil profile or to be available for uptake by plants. Ionic pollutants such as metal,
inorganic anions and certain organic molecules, such as the bipyridyl herbicides (e.g Paraquat), are adsorbed
onto soil colloids. Non ionic organic molecules, which include hydrocarbons, most organic micropollutants
and pesticides, are adsorbed onto humic polymers by both chemical and physical adsorption mechanisms.
However, some organic pollutants, such as solvent, tend to be relatively easily leached in regions where there
is a marked excess of precipitation relative to evapotranspiration. In many cases, adsorption is a necessary
preliminary stage in the decomposition of organic pollutant molecules by bacterial extracellular enzymes.
Heavy metal ions in soils: heavy metal pollution can affect all environments but its effects are most long
lasting in soils because of the relatively strong adsorption of many metals onto the humic and clay colloids
in soils. The duration of contamination may be for hundreds or thousands of years in many cases (e.g. half-
lives: Cd, 15-1100 years; Cu 310-1500 years and Pb 740-5900) years depending on the soil type and their
physicochemical parameters). Unlike organic pollutants, which will ultimately be decomposed, metals will
remain as metal atoms, although their speciation may change with time as the organic molecules binding
them decompose or soil conditions change.
The extent to which metal ions are adsorbed by cation exchange ( non specific adsorption) depends on the
properties of the metal concerned (valency, radius, degree of hydration and coordination with oxygen), pH,

8
redox conditions, the nature of the adsorbent (permanent and pH-dependent charge, complex-forming
ligands), the concentrations and properties of other metals present, and the presence of soluble ligands in the
surrounding fluids. The selectivity of clay mineral and hydrous oxide adsorbents in soils and sediments for
divalent metals generally follows the order Pb > Cu > Zn > Ni > Cd, but some differences occurs between
minerals and with varying p H conditions. The selectivity order for peat has been shown to be Pb > Cu > Cd
= Zn > Ca. However, in general, Pb and Cu tend to be adsorbed most strongly and Zn and Cd are usually
held more weakly, wich implies that these latter metals are likely to be more labile and bioavailable.
In general, nearly all metals (Except Mo) are most soluble and bioavailable at low pHs and, therefore,
toxicity problems are likely to be more severe in acid environments. In the case of pollution by particles of
sulphide ore minerals, the weathering of the sulphide exacerbates the problem by increasing the acidity of the
soil. In agricultural soils this situation can be mitigated to a considerable extent by liming.

Sediment quality assessment


Sediment quality assessment is considerably complex due to the many site-specific parameters as
bioavailability, sorption kinetics, sediment characteristics (buffer capacity and acid-producing capacity),
sediment deposition and erosion (redox potential) and temporal and spatial differences. The methodologies
developed to date do not adequately deal with the complex nature of sediments.
The way in which sediments are sampled and stored for bioassays or spiked for toxicity tests can lead to
unacceptable variability in results. It is probable that some of the variability in toxicity tests could be
eliminated by the use of artificial sediments, although useful tests can be conducted with natural sediments
providing that the range of acceptability for certain parameters such as the particle size spectrum and the
organic carbon content is tightly defined. There is also need to develop statistical methods that can be used
for analysing dose-response relationships in sediment bioassays which usually include the complex mixture
of substances present in contaminated sediments. Tab. 1.1 gives an overview of the various chemical
available to assess sediment quality.
With regard to chemical methods, there is no immediate indication on biological effects. Their major
advantages lie in their easy application and amendment to modelling approaches. The Background approach
compares actual data with sites comprising natural or insignificant pollutant concentration. The total metal
concentrations in sediments are not good estimations of the bioavailable fraction. The dominant role of the
sediment sulphides in controlling metal bioavailability has been demonstrated (Ankley et al. 1991; Carlson,
1991; Di Toro et al. 1992); they are the key factor for controlling the toxicity of cadmium and nickel and
potentially several other heavy metals (Di Toro et al. 1992). No toxicity is observed from these metals when
bounds to sediments and when, on a molar basis, the concentration of AVS is greater than the sum of the
molar concentrations of the sulphide-binding metal. When the ratio of the AVS to metal concentration drops
below 1, toxicity begins to appear.
With regard to prediction of long-term effects of sediment-bound metals, chemical extraction procedures are
of limited value because they usually involve neither reaction-mechanistic nor kinetic considerations. This
lack, can be avoided by an experimental approach, where sediments can be treated in a circulation system
under controlled intensification of significant release parameters such as pH, redox-potential and
temperature. This method (Schoer and Forstner, 1987) includes an ion-exchange system for extracting and
analysing the released metals at an adequate frequency, and compares sequential extraction before and after
treatment of the samples in the circulation apparatus.
The equilibrium partitioning approach has been chosen because it addresses the two principal technical
issues that must be resolved: the varying bioavailability of chemicals in sediments and the choice of the
appropriate biological-effect concentrations. This approach is based on the theory that contaminants sorbed
to sediments achieve thermodynamic equilibrium over appropriate periods of time between sediment and
sediment and sediment pore water concentrations. At equilibrium, the mass of the chemical present in either
phase can be estimates by measuring the mass present in the other phase.
The apparent effects threshold method (AET) uses empirical field and laboratory data to identify
concentrations of chemicals above which biological effects are always expected. A wide variety of
organisms and biological tests can be used to obtain effects data. These may include benthic infaunal field
surveys and bulk sediment bioassays with various organisms and endpoint.

9
The composition of interstitial water is the most sensitive indicator of the types and extent of reactions that
take place between contaminants on the sediment particles and the aqueous phase which contacts them. The
interstitial water approach is a procedure for measuring the toxicity of sediment-bound chemicals to aquatic
organisms by exposing the organisms to pore water extracted from sediments. Pore water toxicity tests can
be performed with a variety of test organisms, both benthic and water column species. This method is based
on the assumption that the pore water is in equilibrium with the surrounding sediment and that the water
phase provides a directc and important route of exposure for organisms that live in sediments.. I t also
assumes that the “soluble” or “free” uncomplexed fraction of any chemical in the pore water is the fraction
most responsible for observed sediment toxicity (Di Toro et al. 1991).
In the spiked sediment toxicity approach, the toxicity of a specific chemical to one or more benthic
organisms is measured by the addition of the chemical to the test sediments in different doses.
The tissue residue approach relies on an ability to establish a maximum concentration of a chemical in
sediment that will result in an acceptable concentration in aquatic organisms or consumers of aquatic biota
like humans, birds or mammals.
Finally, the sediment quality triad method involves a combination of biological laboratory and field data in
comparison with chemical analyses which compensates the limitations of the individual methods. It consists
of three components (Chapman, 1986):
• Identification and quantification of inorganic and organic contaminants in the sediment with the lowest
limits of detection possible
• Measurement and quantification of toxicity based on bulk sediment laboratory toxicity tests.
• Evaluation of in situ biological effects or alteration.
_______________________________________________________________________________________
Tab. 1.1. Methods for assessing sediment quality (from Calmano W et al. 1996)
_______________________________________________________________________________________
Chemical methods Integrated Chemical and biological method Biological method

Back ground approach Equilibrium partitioning Bulk sediment toxicity


Acid volatile sulfide (AVS)
Apparent effects threshold Fresh benthic approach
Substrate composition Interstitial water toxicity
Long term mobility Spiked sediment toxicity
Tissue residue approach
Sediment quality triad
_______________________________________________________________________________________
The most useful sediment toxicity tests and bioassays are those which measure the chronic toxicity resulting
from long-term exposure because some sedimentary contaminants can be persistent. However, partly due to
problems associated with feeding sediment dwellers in a natural way and partly due to our lack of
understanding the optimum living conditions for these organisms, there are very few sediments tests which
are currently able to measure chronic effects.
As with all ecotoxicological data the most difficult problem in sediment toxicity assessment is the reliable
comparison of data obtained under different sediment conditions and the confident extrapolation of
laboratory-derived sediment test results to the field situation. Some progress has been made for neutral
organic compounds by normalising for the organic carbon content of the test sediment. Normalising for acid
volatile sulphide (AVS) may have equivalent utility for certain metals. However there is a need to develop
similar normalising procedures for the many other confounding factors in sediment test to enable all test
results to be reliably compared. Extrapolation to field situations is even more difficult at present because we
have little information about the impact of sedimentary contaminants under natural conditions. Until we have
a much larger data base of information on pollution effects in experimental mesocosm sediments and are
able to relate bioassay responses in a more structured way to known impacts on wild communities of benthic
organisms, we will not be able to derive specific applications or safety factors to be used when extrapolating
sediment toxicity results.

10
Pollutants in contaminated soil

Many states or countries have established lists of critical concentrations (or trigger concentrations) for the
risk assessment of site and environmental survey data. The basis for these different sets of values varies
according to the target groups they are intended to protect from the effect of the pollutants. Examples of
critical concentrations of heavy metals used in different countries are given in Tab. 1.2, 1.3, 1.4.
Tab. 1.2 shows the critical concentrations used in the Netherlands for contaminated soils. The system is
based on ecological function and comprise target values (TV) for soils which represent the final
environmental quality goals for the Netherlands. The critical values for soils given Table 1.3 for the UK by
the Department of the Environment Interdepartmental Committee for the Reclamation of Contaminated Land
(ICRCL). The list of Trigger Concentrations for Contaminants (DOE, 1987) are more pragmatic and based
mainly on the risk to human health. Unlike the Dutch standards, the ICRCL values vary for different
proposed uses of the contaminated land. The lowest values are given for garden soils where vegetables are
likely to be grown, with higher values for parks and open spaces, and the highest values for land to be
developed for industrial uses where the transfer o pollutants from the soil to plants is not likely to be
significant in terms of his impact on human health.
The new Canadian National Classification System from contaminated soils shown in table III is intended for
use in the evaluation of contaminated sites. The values in the tables enable sites to be classified as high,
medium or low risk according to their impact (current or potential) on human health and ecosystems. It is a
screening system and not intended to be a quantitative risk assessment for individual sites. The 1991
Environmental Quality standards for Netherlands give target values for soils which will be very difficult and
expensive to achieve, especially in the case of some of the ubiquitous contaminants such as Pb. The
Threshold value for Pb under the ICRCL scheme used in the UK is 500 mg/g. This implies that
concentrations below this figure should not cause problems. In contrast, the Dutch target value for Pb is 85
mg/g (for a standard soil) and the Canadian background value is even lower at 25 g/g, but the trigger
concentration for remediation of agricultural land is 375 g/g. The Dutch scheme is based on the ecological
effects of contaminants and, therefore, soils meeting the target values would be suitable for any use, such as
food production or nature conservation. However, the UK and Canadian values take into account different
uses of land. The UK value of 500 g/g Pb is the most achievable, because many urban soils in the UK would
come within this range and the more excessively polluted sites would be considered unacceptable.
Of particular relevance is the intended future use of the contaminated land. In some countries, such as
Netherlands, the intention is to ameliorate the site to a specification which allow the land to be used for any
purpose (multifunctionality). The more pragmatic approach in other countries, such as the UK, is to relate the
site quality specification to the intended use. For example, a contaminated site required for development as a
warehouse complex would not need to have such low concentrations of toxic compounds as a site to be used
for housing, where the residents may grow vegetables in their gardens. However, any explosive hazard, such
as methane release, would need to be removed for both new uses o the site. Even though the use of a site
may not require a high degree of clean-up, the remaining contaminants may migrate within the soil to the
ground-water, undergo chemical changes or remain a potential problem fo future uses of the site.

11
________________________________________________________________________________
Tab. 1.2. Guide values and quality standards used in Netherlands for assessing soil contamination by heavy
metals (Netherlands Ministry of Housing, Phisical Planning and Environment, 1991). STV values in µ g/g.
________________________________________________________________________________
Arsenium 29
Bario 200
Cadmium 0.8
Cobalto 10
Chromium 100
Copper 36
Mercury 0.3
Molibdeno 10
Nickel 35
Lead 85
Sn 20
Zinc 140
________________________________________________________________________________

______________________________________________________________________________________
Table 1.3. UK Department of the Environment ICRCL trigger concentrations for environmental metal
contaminants (total concentratione except where indicated) (Department of the Environment, 1987).
______________________________________________________________________________________
Contaminant (µ g/g) Proposed uses Threshold trigger concentration

Contaminants which may pose hazards to homan health


Arsenium Gardes, allotments 10
Parks, playng fields, open space 40
Cadmium Gardes, allotments 3
Parks, playng fields, open space 15
Chromium (hexavalent) Gardes, allotments 25
Parks, playng fields, open space -
Chromium Gardes, allotments 600
Parks, playng fields, open space 1000
Lead Gardes, allotments 500
Parks, playng fields, open space 2000
Mercury Gardes, allotments 1
Parks, playng fields, open space 20
Selenium Gardes, allotments 3
Parks, playng fields, open space 6

Phytotoxic contaminants not normally hazardous to health


B (water soluble) Any uses where plants grown 3
Copper (total) Any uses where plants grown 130
(extractable) 50
Nickel (total) Any uses where plants grown 70
(extractable) 20
Zinc (total) Any uses where plants grown 300
(extractable) 130
______________________________________________________________________________________

12
______________________________________________________________________________________
Table 1.4. Selected values from the Canadian interim environmental quality criteria for soil (Canadian
Council of Minister of the environment, 1993), soil concentrations in µ g/g.
______________________________________________________________________________________
Background Agricultural Residential Industrial

Arsenium 5 20 30 50
Bario 200 750 500 2000
Berillium 4 4 4 8
Cadmium 0.5 3 5 20
Cobalto 2.5 8 8 -
Chromium 10 40 50 300
Copper 30 150 100 500
CN 0.25 0.5 10 100
CN 2.5 5 50 500
Lead 25 375 500 1000
Mercury 0.1 0.8 2 10
Molibdeno 2 5 10 40
Nickel 20 150 100 500
Se 1 2 3 10
Silver 2 20 20 40
Sn 5 5 50 300
Zinc 60 600 500 1500
______________________________________________________________________________________

Aims of this research


As coastal and inland wetlands in Pakistan and China are subject to increasing pollution from industrial,
urban and agricultural sources, there is a growing urgency to monitor contaminant levels, to assess the
effects of pollutants, and to evaluate the resilience of these wetlands to pollution. The approach of our study
focused on the use of colonial waterbirds as bioindicators of environmental contamination and other
ecosystem changes.
The general objectives of this study were to assess pollutant levels and effects in selected coastal and inland
wetlands in Pakistan and China, using egrets and herons (colonial waterbirds of the Order Ciconiiformes,
Family Ardeidae) as bioindicators. We considered the most widespread contaminants with long term
persistence:
• inorganic elements, particularly heavy metals and other elements of environmental concern (Cd, Cr, Hg,
Pb, Cu, Fe, Mn, As, Ag, Br, Co, Ce, La, Ni, Sc, Se, Zn
• DDT and derivates
• other organochlorines (HCH+HCB, - HCH, -HCH, -HCH, heptachlor-epoxide -endosulfan).
• Polychlorinated biphenyls (PCBs)
Because of the heightened interest in wetland conservation throughout the world, herons and egrets have
become a valuable and popular monitoring guide, because of their conservation value, their vulnerability and
their conspicuousness. (Erwin and Custer, 2000). Moreover, their use for monitoring purposes can provide
data on both exposure hazards and effect responses. A number of aspects of the biology and behaviour of
egrets and herons, makes them particularly appropriate as bioindicators: they are top predators and thus
liable to concentrate contaminants, are widespread, use a variety of habitats, and have been intensely studied
so that abundant comparative information is available (Kushlan 1993, Erwin & Custer 2000). The species

13
selected for study was the Little Egret Egretta garzetta, one of the most widespread and common of the
Ardeidae.
Biological properties at various hierarchical levels have been used as indicators of environmental quality,
and of contamination in particular. Since biomonitoring programs are most effective when they use a
combination of indicators, at different levels of organization, our research program included the study of:
• eggs: contamination by organic compounds, as indicator of general environmental contamination
• feathers: contamination by trace elements, as indicator of general environmental contamination
• suborganismic characteristics (eggshell thickness, haemathological variables), as indicators of
contaminants effect on physiological conditions
• breeding success (clutch size, hatching and fledging success, ,growth rate of chicks), as indicator of the
present impact of contaminants
• breeding population size, as indicator of the long-term impact of contaminants
• prey of the egrets: contamination by organic compounds and by trace elements, as indicator of the
present contamination of particular habitats
• sediments collected in the feeding habitats of the egrets: contamination by organic compounds and by
trace elements, as indicator of the long-term contamination of particular habitats
For each country, Pakistan and China, we selected one wetland exposed to industrial-urban pollution, one to
agricultural pollution, and one thought to be relatively unpolluted; all selected wetlands are of recognised
national and/or global importance. The results may indicate the level of pollution in the populations and
ecosystems studied, highlight any potential threats to human health, and provide valuable baseline data for
comparison with future conditions in these populations and ecosystems and elsewhere in Asia. The outputs
will be useful for management of these important wetlands, for national policy formulation for pollution
control and wetland conservation, and for the strengthening of pollution control regulations.
We aimed to assess both residue levels and effects of pollutants. We expected residue levels to differ among
study areas in relation to ecosystem-level pollution, and particular sources of pollution to be indicated by the
types of contaminants and by their patterns of concentrations in the different samples.
Specific objectives were:
• to measure residue levels of organochlorine compounds and PCBs, and of selected heavy metals and
other elements, in feathers and eggs of Little Egret;
• to measure selected population variables (size of breeding population, success of sample nests) of these
Little Egret populations, and record aspects of their behavioral ecology (foraging habitat, foraging
success of sample adults) that may be related to contamination;
• to infer exposure of these Little Egret populations to pollutants and the general bioavailability of
pollutants, and to infer exposure to other ecosystem changes;
• to assess qualitatively and quantitatively ecosystem-level contamination and other ecosystem changes as
indicated by residue levels and by population and behavioural variables in Little Egrets
• to identify whether concentrations of contaminants found, and any other ecosystem changes observed,
are at levels associated with adverse effects on reproduction;
• to further test the usefulness of colonial waterbirds as bioindicators of environmental contamination and
ecosystem change; and
• to disseminate the results among environmental toxicologists and other scientists, ecosystem managers,
environmental policy formulators and legislators.
We summarize here the results of the ecological studies, sample collection and chemical analysis. The
ecological data, besides their own biological interest, provide a background information for the interpretation
of the contamination levels.

14
2.

Study areas

Fasola Mauro
Dipartimento Biologia Animale, Università, Piazza Botta 9, I-27100 Pavia, Italy

The following 6 wetlands were selected for study on the basis of the presence of breeding colonies of egrets
and herons, of their national and global importance, and of their various exposure to contamination (Fig. 2.1,
2.2, 2.3).

1) Poyang Lake, Jiangxi, China (115°49'-116°46'E, 28°24'-29°46'N): a freshwater lake, the


largest in China (328,300 ha) and the most important site for waterfowl in China, established as
a NEPA nature reserve, expected to be free of pollution. Poyang Lake is the largest freshwater
lake in China. It is located in the floodplain of five inflowing rivers, and it also receives
backflow from the Yangtze River at high floods. It is still in a near-natural state, and the
difference between low water levels in winter and high water levels at the height of the summer
flood might be of 11 metres. Since time immemorial, the whole area of the lake (170 kilometres
long by 17 kilometres wide), and its floodplain has been used by humans for fishing, for grazing
of buffaloes and for cutting of vegetation as fuel. Moreover, the lake constitutes a very
important wintering area for waterfowl. For instance, up to 98% of the Siberian Crane (Grus
leucogeranus), a species of great interest from the point of view of conservation, winters at the
Poyanghu. Large colonies exist with breeding Little Egrets, Intermediate Egrets, Great White
Egrets, Cattle Egrets, Chinese Pond Herons, and Night Herons.

2) Tai Lake, Jiangsu Province, China (30°19’ to 32° 00’ N, 119° 21’ to 122° 00’ E). One of the
largest freshwater lakes in China (242,500 ha), situated in a highly productive rice-growing
area, expected to be subject to serious pesticide and heavy metal pollution from both agriculture
and industry. Tai Lake, with an area exceeding 1,200 km 2 , is located near Wuxi, an industrial
P P

city with a population of 1 million. The agriculture in this area is highly productive and it is
mainly devoted (90% of farmed land) to rice fields. Tai Lake has at its northern part Lake
Wulihu, a lagoon of approximately 10 km 2 . Several tributaries connect the two lakes with other
P P

bodies of water such as the Yangtze River. Lake Wulihu receives millions of tons of industrial
waste water and domestic sewage from Wuxi. Tai Lake also receives direct inputs of
agricultural and some industrial pollutants, as well as sewage from small towns on the west side
of the lake. During most of the year, water flows from Tai Lake to lake Wulihu, but reverse
flow in winter/spring, brings water from lake Wulihu to the Taihu (Zou et al. 1996, Dong and
Zhang, unpubl.). Very large colonies of Night Herons, Little Egrets, Chinese Pond Herons, and
Cattle Egrets, are scattered throughout this area.

3) Pearl River Delta and Coastal Area, Guangdong, China (112°15'-114°15'E, 21°31'-23°15'N). A wide
area, of about 38,000 ha, expected to be subject to urban-industrial pollution. The study site was the
“Ecological Paradise”, a recreational area, located close to the municipality of Shunde. Guangdong
Province is one of the important production areas for traditional rice-fish culture and freshwater fish
farming in China. In 1998, its freshwater farming area reached 362,128 ha, and the output was 1,903
million tons, of which 235,936 ha were ponds with a total output of 1,744 million tons; 93,726 ha
were reservoirs with a total output of 774,000 tons; 29,662 ha were paddy fields with a total output of
202,000 tons. There are three major types of freshwater culture: 1) traditional freshwater farming of

15
four major Chinese carps: Grass carp, Carp, Silver carp, Bighead; 2) introduction of foreign breeds:
Large mouth bass, Tilapia, Pacu, Macrobrachium rosenbergii, Silvery Pomfret; 3) Culture of local
wild species: Eel, Mandarin fish, soft-shelled turtle, China soft-shelled turtle. Large colonies with
several species of herons and egrets are scattered throughout this area.

4) Haleji Lake, Sindh Province, Pakistan (25°48’N, 67°47’E). A freshwater lake, surface area 1,704 ha,
with associated marshes and adjacent brackish seepage lagoons, expected to be relatively unpolluted.
The site is located 15 km west-nortwest of Thatta, and 75 km west of Karachi. Haleji Lake is a ‘clean’
freshwater reservoir with associated marshes and adjacent seepage lagoons, located amid a stony
desert, and covering an area of 10.53 km 2 , reaching a maximum depth of 6 m. Since there is no
P P

agriculture nor industrial activity in the surroundings, pollutants may reach the reservoir mainly
through atmospheric deposition. This wetland hosts regularly between 50,000 and 100,000 birds and it
is especially important for breeding Ardeidae. The most abundant breeding herons and egrets are the
Night Heron and the Intermediate Egret, with lower numbers of Indian Pond Herons, Little Egrets, and
Purple Herons.

5) Taunsa Barrage, Punjab Province, Pakistan (30°42’N, 70°50’E). A storage reservoir behind a barrage
on the River Indus, expected to be subject to pollution from agriculture. Taunsa Barrage is located 20
km northwest of Kot Adu, Muzaffargarh District. It is a large water storage reservoir situated behind a
barrage on the Indus River. Agriculture, mainly cotton, sugar cane, wheat and fodder crops, livestock
grazing and forestry occur in adjacent areas, but also the barrage is used for power generation,
therefore some impact of PCBs is to be expected the land that is exposed to low water levels is leased
to local farmers for cultivation during the dry season. A few large colonies with several species of
egrets and herons exist in this area.

6) Karachi Harbour, Pakistan (24°47’N, 67°11’E; 112). Tidal creeks, mangrove swamps and intertidal
mudflats, expected to be subject to considerable urban and industrial pollution. The study site was
Karachi Ghas Bunder, located in the city of Karachi. It is a degraded mangrove area within the
Karachi Harbour, and it is exposed to high industrial pollution. About 45% of Pakistan Industries are
located in Karachi area, and all their effluents plus the domestic sewage from the city (more than 8
million people) find their way, untreated, into the sea (Khan unpublished). Furthermore, Karachi
Harbour is also exposed to ship wastes and oil spills from the port’s oil terminal. Therefore, a high
incidence of PCBs is to be expected in this area. Only one colony of Little Egrets (dark morph) was
found in this area and n the surrounding coastal areas.

16
Tai Hu
Taunsa barrage (agricultural pollution)
(agricult ural pollution)
Poyang Lake
(unpolluted)

Haleji Lake Pearl River Delta


Karachi Harbour (unpolluted) (industrial. pollution)
(industrial pollution)

Fig. 2.1. Location of the 6 study areas in China and in Pakistan

Fig. 2.2. Location of the 3 study areas in Pakistan. 1: Haleji Lake, 2: Taunsa, 3: Karachi.

17
Fig. 2.3 . Location of the Tai Lake and of the Poyang Lake study areas in China.

Fig. 2.4. Location of the Pearl River Delta study area in China.

18
3.

Methods for sample collection and for the ecological studies

Fasola Mauro
Dipartimento Biologia Animale, Università, Piazza Botta 9, I-27100 Pavia, Italy

General approach
Our initial program included only one species, the Little Egret, as monitor of contamination. For the
ecological data however, we decided to consider all the other herons and egrets breeding in the same
colonies, or foraging in the same wetlands, because this could be done with very little additional effort, but
on the other hand it would greatly increase the completeness of the study.
The collection and analysis of contamination samples remained restricted to the Little Egret, owing to the
high cost of the chemical analyses. In some cases however, Little Egrets were too scarce to
provide sufficient samples, and we were forced to shift to the most similar species (the
Intermediate Egret, or theCattle Egret) as sample species.
The following species of herons, egrets, and other waterbirds, were studied:
Little Egret Egretta garzetta. Wery widespread, both in China and in Pakistan, in all kinds of wet
habitatsl, both natural wetlands and flooded cultivations. It was the main study species
for this project, and egg, feathers, and prey samples were collected from Little Egrets
wherever they were sufficiently abundant A dark morph of the Little Egret, present in
the Karachi study area, is sometimes identified as a separate species, the Western Reef
Heron Egretta gularis., This is a polymorphic group that include dark, white, and
intermediate egrets birds almost identical to the Little Egret. Presently, most authors
(Hancock & Kushlan 1984, Kushlan & Hafner 2000) consider all these egrets as
conspecific. Egretta garzetta schistacea is thus considered a subspecies, and simply a dark
colour morph, of the polymorphic species Little Egret, and it will be.thereafter referred to in
this report as “ Little Egret, dark morph ”. The Western Reef heron occurs only along
the coastline from the Arabian Peninsula and spend most of their time foraging in salt
water or the tidal zone, while the Little Egret is almost entirely a freshwater feeding
species. Samples from Little Egret, dark morph, were collected in the Karachi study
area, where it was he only abundant species.
Intermediate Egret Egretta intermedia. Intermediate Egrets occur in Southern China and in Pakistan. It
was the most abundant egret at Haleji Lake, and because of the ease with which its nests can be sampled, it
was the main study species in this area.
Great White Egret Egretta alba. Widespread both in China and in Pakistan, in all kind of wetlands.It was
not abundant in any of the study areas, and few data were collected on its ecology.
Cattle Egret Bubulcus ibis. This species spread in Pakistan with the development of irrigation. It is a
largely sedentary species, well adapted to grassland areas and to cultivated areas. This species is much more
insectivorous than the other egrets, and is the only egret foraging usually on dry land. This species was
sampled exclusively at Taunsa, where Little Egrets were very scarce.
Night Heron Nycticorax nycticorax. Widespread throughout Southern Asia. Some samples were collected
at Tai Lake from Night Herons, in order to provide comparative material for another research on

19
contamination, that was by the Institute of Soil Science, Chinese Academy of Sciences, with
additional funds provided by the Chinese government.
Chinese Pond Heron Ardeola bacchus. Present in small numbers in the study areas of China. Few data
were collected on its ecology.
Indian Pond Heron Ardeola grayii. Present in small numbers in the study areas of Pakistan. Few data were
collected on its ecology.
Gray Heron Ardea cinerea. Observed in the study areas of both China and Pakistan, and few data collected
on its ecology.
Purple Heron Ardea purpurea. Observed in the study areas of both China and Pakistan; few data collected
on its ecology.
Javanese Cormorant Phalacrocorax niger. This species has been in the past considered conspecific with
P. pygmaeus , although both are easily separable in breeding plumage. In Pakistan this cormorant prefers
freshwater areas. On Haleji Lake, the colonies occupied the small rocky islands inside the lake, nesting on
reed-beds. Diet consist predominantly of small fresh water fish species, as well as frogs and tadpoles. Some
samples were collected from this species as well at the Haleji study area, where the target species, the Little
Egret, was scarce.
During May and June 1999, teams of Asian plus European researchers worked jointly in the Haleji and in the
Poyang study areas. This joint work was also intended as training, so as to ensure that all the researchers
adopt exactly the same techniques. During May and June 2000, joint Asian-European teams worked in the
remaining 4 study areas. In each study area, colony census ,was completed, breeding success, foraging
habitat and feeding success were recorded, and samples for chemical analysis were collected.

Ecological records
We standardized as much as possible the collection of ecological records, so that the data for the different
study areas could be compared. Methods in the field were described in detail in a 20-pages booklet “
Workplan and methods for Ecological Fieldwork & Sample Collection” that included standardized data
forms, and that was distributed to each participant before each field season. These methods follow the ones
already tested in previous studies (Fasola 1994, Fasola 1998). But the specifics detailed below were fulfilled
completely only in a few cases, because of local constraints.

Colony census
The goal was to identify and to census all the waterbird colonies within a general study area of few hundred
square kilometers. The recommended census technique was:
1. locate all the colonies within the study area (an area of 100-200 km 2 )
P P

2. visit each colony repeatedly during the egg and the chick stages
3. for the most abundant species with indistinguishable nests (i.e. most medium-size species of herons and
egrets), perform a “sample count”, i.e. evaluate the numeric proportion between the species during 3
or 4 visits, spaced through the breeding period. This proportion must be assessed by counting and by
identifying nests (distinguished on the basis of the breeding adult or of the chicks) and not by
counting the flying adults. In large colonies, the proportion should be assessed for a sample of nests
(50-100 for each visit) well spaced throughout the entire colony, since one species can be clumped in
a particular sector of the colony
4. for scarce species (for which the proportion as above would not work well) perform a “total count” during
each visit
5. at the peak of colony occupation (usually mid-late breeding season) perform a total count of all the nests
However, it was not possible to obtain precise estimate for some colonies, because they were inaccessible,
the nest were not visible, or because they were too large. In these cases, only a gross estimate of the number
of nests was done. For some large colonies, their size was estimated by: counting the nests within 20-25
sample plots, squares of 10x10 m each; measuring the total surface of the colony; extrapolating the average
density of the plots to the total surface area. Colony size is expressed in number of nests.

20
Breeding Success
Breeding success was recorded for a sample of nests in one of the colonies of the study area, the “focal
colony”. The techniques were:
1. Establish a sample of nests and mark them. The species of the nest was identified from the observation of
the adults on the nests.
2. Perform 2 visits/week to each nest, and at each visit, check the content of each nest. The breeding success
was expressed as no. of eggs/nest, no. of chicks hatched/nest, and no. chicks fledged/nests. Since the
chicks are semi-nidifugous, and cannot be spotted after 15 days old because they escape on the
branches surrounding their nests, the no. chicks fledged/nests, actually means “number of chicks
alive at about 15 days”
3. When the chicks were about 15 days old (the maximum age they can be caught) capture them and
measure tarsus length and body mass. Since tarsus length depends mainly on age, while mass is
largely influenced by the amount of food received, the ratio mass/tarsus lenght indicates the
condition of the chick. A condition index was calculated for each chick as ratio between the actual
mass and the predicted mass for its tarsus length. The predicted mass was calculated from a tarsus-
mass regression, based on the data for all the chicks. The condition index equals 1 when the chick
mass is exactly average, while values above or below 1 indicate the proportion by which the mass is
higher or lower than average.
Breeding success in our study areas was then compared with the success recorded for the same species in
other parts of their distributional range (Tab. 3.1).

______________________________________________________________________________
Tab. 3.1. Breeding success of species of herons and egrets, mean value (an d sample size when available),
from literature for various areas and years. No data are available for the Chinese Pond Heron.
______________________________________________________________________________
No. eggs/ No. chicks No. chicks Country Reference
nest hatched/nest fledged /nest

Little Egret 3.9 3.0 Sichuan (Nanchong 1984) Li et al.,1985


3.9 Shandong (Penglai 1996) Zhou et al.,1998
5.2 4.6 Anhui (Chuzhou1981-3) Jiang et al. 1986
3.6 Henan (Dabieshan1988-9) Zhang et al. 1994
4.5 ( 314) 3.8 (253) 3.4 (247) Italy Fasola 1998
4.8 (199) South Spain Hafner et al. in press
4.3-4.6 South Spain Hafner et al. in press
3.5-4.7 2.4-3.6 South France Hafner et al. in press
4.3 (256) 3.0 (214) Greece Hafner et al. in press
1.5-2.7 (79) Australia Maddock & Baxter 1991

Night Heron 3.9 3.6 Sichuan (Nanchong 1984) Li et al.,1985


3.3 Shandong (Penglai 1996) Zhou et al. 1998
3.4 Henan (Dabieshan1988-9) Zhang et al. 1994
3.4 (213) 2.9 (191) 2.5 (167) Italy Fasola 1998
3.6 (104) 2.2-2.5 (508) South France Fasola & Hafner 1997
2.5 (146) Greece Katzanzidis et al. 1997
1.8 (40) Spain Parejo (pers.com.)
2.1 (36) Spain Pulido et al. 1993

Cattle Egret 2.9-3.4 (1980) France Hafner (pers. com.)


2.7-3.1 (273) Spain Prosper & Hafner 1996
2.3-2.8 (543) Australia Maddock & Baxter 1991

Intermediate Egret 2.0-2.4 (196) Australia Maddock & Baxter 1991


______________________________________________________________________________

21
Diet
Waterbird chicks from 10 to 40 days-old, easily regurgitate food when observers approach. During censuses,
and while recording breeding success, we collected all the regurgitated items. We tried to collect all the prey
items regurgitated by the chicks, and not only the big ones, in order not to bias the sample. Each sample (a
pool of all the items collected in the same day, at one colony, and from one species of egret or heron) was
preserved and examined in the laboratory.

Foraging habitats
Foraging habitat was recorded for the adults foraging around the same focal colony at which breeding
success was being studied and at which samples were being collected. The area over which to record
foraging habitats was a 10 km radius circle around the focal colony. Foraging habitat was recorded over the
peak period during which most nests have chicks.
On detailed maps of the study area (1:10.000 scale maps if available), we delimited the surfaces of the
various types of aquatic habitats used by the egrets and herons, within 10 km from the colony. Each “patch”
(i.e. portion of contiguous habitat of the same type) was given a code. These habitats were periodically
suveyed, usually 2 times per week, and the number of egrets and herons present in each patch was recorded.
All the birds present in the foraging areas were recorded, irrespective of their activity.

Prey biomass in rice paddies


In order to assess the value of rice paddies (the main foraging habitat) to egrets and herons, we collected
standard samples of the available prey. A standard sample was obtained with a technique already used
elsewhere (Fasola et al. 1996), by 10 sweeps of a long-handled net every 10 m. Each sample was obtained
from a different field. Each sweep sampled about 0.5 m 2 of area, including the entire water column. The net
P P

was effective in sampling all prey, except frogs that could escape faster than the other prey. Frog number
was estimated by counting the number moving within a 100 by 1-m strip along the sampling itinerary. The
dry mass of a convenient number of prey items was measured in the laboratory. Prey mass was calculated as
g dry weight / 100 m 2 .
P P

Feeding success and prey type


Feeding success and prey type were recorded during focal-animal observations, accomplished during the
surveys for recording foraging habitat:
1. when an actively feeding bird was encountered in a suitable position (i.e. that is neither so far as to be
difficult to observe, nor so close to be scared by the observer), a focal-animal observation of its
feeding activity was performed for a fixed time of 10 min.
2. the bird was observed for 10 min (through a telescope mounted on tripod), and we recorded: feeding
technique; number of pecks and on captures; the type and size of prey. Prey size was estimated in
relation to the bill of the bird.

Collection of samples for chemical analysis


In order to use colonial waterbirds as bioindicators, and in order to select samples that are homogeneous and
comparable for all the study sites, we collected the following materials for chemical analysis.
Eggs. Since pollution levels tend to be more similar within eggs of the same clutch than between eggs from
different clutches, to take an egg per nest may not be a good sampling strategy. A strong intra-clutch effect
can also be found between the first and last egg in a clutch, this effect will depend on clutch-size, and this
source of variability must be taken into account. Since it is not practicable to analyze all the eggs in a clutch ,
because of cost constraints, during 1999 we tried a sampling procedure intended to assess the relevance of
intra-clutch effects, and we collected both single egg taken at random from a nest, and a few entire clutches.
Feathers. Contour feathers were collected from one chick, at the same nests from which the eggs had been
sampled.

22
Prey. The 3 main prey of Little Egrets, from nestling regurgitates, were collected. Whenever possible, 10
items of a prey type collected in a particular day constituted one sample. While collecting the prey of the
chicks for diet analysis, we separated from these prey, 1 “sample for analysis” per week (each consisting of
10 items each, the most fresh ones) for each of the 3 main prey types (by main we mean in relation to mass).
Therefore, 3 samples were collected each week, for the 3 main prey types of that week, whenever possible.
Sediments. Sediments were collected in the different foraging habitats used by the egrets, because
differences in placement, water circulation, biological activity above the sediment, can originate variability
in contamination. In order to obtain a sample large enough to obtain an adequate picture of the pollutants, we
collected several core replicas of sediment in the places where egrets foraged, then we collapsed the replicas
into composite samples to be analysed. The restricted amount of resources available for sediment analyses
forced us to define a sampling scheme that is clearly suboptimal, but probably enough to reach our
objectives, i.e. to estimate the average contamination of the sediment in the wetlands. The samples were
collected at the end of the study period, when we already had knowledge (through the foraging habitat
records) about the habitats used by the egrets.
Sediments were collected using a core sampler (a plastic tube with 5 cm diameter and 2 cm height) pushed
into the mud
Sediment samples were collect by: defining main and secondary habitats; defining how many points
(=number of cores obtained) to sample in each habitat; mixing at random from 4 to 12 cores, to obtain
composite samples.
Due the logistic problems, the only solution for conservation and transport of the samples was to
homogenyse and dry all the wet material (eggs, prey, sediments). Eggs, prey, and sediments, were kept cool,
homogenysed, dried in oven (24-48 h at max 50 °C, to constant weight), and stored in poliethylene vials.
Feathers were simply stored into polytene envelopes. The samples were split in three parts of similar
amounts, one for pesticides and PCB analysis in Spain, one for NAA analysis in Italy, and one for AAS
analysis in Italy.
From each egg, a piece of eggshell, centered at the egg equator, was cut and stored for thickness
measurement. Polytene vials were used for all the material to be analysed, because they are clean from
metals etc. Care was taken that other containers would not contaminate the samples.

Blood slides
Haematological variables can be of great interest in relation to contamination, but adequate blood
conservation for detailed analyses requires freezing, and this would have been difficult. Ee included into our
sampling scheme only blood slides, that were easy to obtain from the chicks we handled, and easy to
conserve. They were obtained from the chicks handled for sampling feathers, and also from any other chick
that were handled for recording breeding success. Slides were dried and stained with Giemsa.

23
4.
Breeding and foraging ecology of egrets
and herons at the Poyang Lake study area, China
Dai Nianhua, Liu Wei
Biological Resources Institute, Jiangxi Acedemy of Sciences, Nanchang, Jiangxi, P.R. China

Fasola Mauro, Giuseppe Gaudenzi


Dipartimento Biologia Animale, Università, Piazza Botta 9, I-27100 Pavia, Italy

This chapter summarizes the eco-ethological data collected during 1999 (5 May- 19 June) at the Poyang
Lake study area (near Nanchng, Jiangxi, 115°49'-116°46'E, 28°24'-29°46'N), the study area of China that
was supposed to be relatively free of pollution. Poyang Lake, the largest freshwater body in China (328,300
ha), is also the most important site for waterfowl in China, and has been established as a NEPA nature
reserve.

Colony census
Eight colonies were located within the study area shown in Fig. 4.1 (an area of approximately 120 by 50
km). We presume that no other, undetected colony existed within this area.
A census of the nests (Tab. 4.1) could be accomplished with reasonable accuracy in 4 of these colonies. The
small size of the Silver Triangle Bridge colony is probably due to limitation of the colony site, a small and
disturbed wood. The other colonies are of medium or large size.
Other colonies were occasionally located during trips outside this area. These colonies seem to be spaced
throughout the region at inter-colony distances of about 30 km, and they are of a size comparable to those of
the ones we censused. The impression is that the density and size of the colonies within the Poyang lake area
is representative of the situation in the whole region. The breeding population is therefore large size, due to
the wide surfaces of aquatic habitats, particularly rice paddies, that herons can exploit for foraging.
The Gongquing colony was chosen as the focal study colony, because it was the only one with nests easy to
visit, and with large populations of several species. All the following data refer to this colony only.

Colony B

Fig. 4.1. Poyang lake area, with location and the


conventional names of the heronries.
Gongqing City

Xingizhou
Xiangshan
Forestry Park

Xihu Garden
Colony B

Silver Traingle
24 Bridge
______________________________________________________________________________
Tab. 4.1. Description of the five colonies censused in the Poyang lake area.
______________________________________________________________________________
Colony Xihu Gongqing Xiangshan Silver Triangle Xingizhou Wanli Colony Colony
Garden City Forestry Park Bridge A B

Coordinates 28°39.412’N 29°13.518’N about 28°50’N about 28°20’N 28°56.310’N


115°57.049’E 115°49.258’E about 116°10’E about 115°58’E 115°48.820’E

Habitat Small woodPart of largePart of a verySmall wood Part of a


in a private mixed large juniperus near roads medium-size
bonsai garden woodland and conifer and buildings juniper
(mainly (broadleaf, woodland, (broadleaf) plantation
false acacias) bamboo, 3 nuclei at 1 km
Nests conifers) each other, Nests
2-10 m high Nests Nests 5-15 m high 5-10 m high
2-10 m high 5-15 m high

No. nests
Total 1,400 2,000 3,000~4,000 170 350 ? ? ?
Little Egret 170 580 ++ 20 25 + +
Intermediate Egret 165 + 20
Great White Egret 50 +
Cattle Egret 420 ++
Chinese Pond Heron 100 70 + 10 315 + +
Night Heron 1130 715 + 120 10 + +
______________________________________________________________________________

Breeding Success
Breeding success was studied in a sample of nests. Priority was given to the Little Egret, whose sample was
therefore the largest, while the sample for the Chinese Pond Heron was very small.
The breeding success of each species (Tab. 4.2) can be considered normal, and even higher, compared to the
literature data. A comparison with the success of Little Egrets and Night Herons in various parts of their
range (Tab. 3.1), shows that at the Gongquing colony the success of these species was at the top end of the
range of values recorded elsewhere. This high success preliminarily suggests that no adverse agent (e.g.
contaminants) is affecting reproduction in this study area.

______________________________________________________________________________
Tab. 4.2. Breeding success in sample nests at the Gongquing colony, mean value (minimum -maximum).
______________________________________________________________________________
No. nests No. eggs/ No. chicks No. chicks
recorded nest hatched/nest fledged /nest

Little Egret 67 4.7 (2-6) 4.1 (2-5) 3.7 (1-5)


Intermediate Egret 21 3.8 (2-5) 3.4 (2-5) 3.0 (2-5)
Cattle Egret 10 3.9 (3-5) 3.4 (2-5) 3.3 (2-5)
Chinese Pond Heron 2 5.0 (4-6) 3.5 (3-4) 3.5 (3-4)
Night Heron 18 3.4 (3-5) 3.2 (3-4) 3.0 (2-4)
______________________________________________________________________________

25
The frequency of clutches of differing size, and their respective success, are shown in Tab. 4.3. Splitting
success among clutch sizes may help discover critical factors., e.g. in case of food limitations, larger clutches
may have a lower success. No such effect appears in the data of Tab. 4.4. The success remains high even for
the larger clutches. Chick condition was estimated only for Little Egrets (Tab. 4.4), and this index as well
remained high for the largest clutches. These results again indicate good breeding conditions, and no adverse
effect on reproduction.

______________________________________________________________________________
Tab. 4.3. Frequency of nests, and breeding success (mean values), in relation to clutch size.
______________________________________________________________________________
Initial clutch size Tot. No.
2 3 4 5 6 study nests
______________________________

Little Egret
Frequency (%) 2 6 29 52 11 63
No. chicks hatched/nest 2.0 2.5 3.7 4.4 4.7
No. chicks fledged/nests 1.0 2.5 3.5 4.1 4.0

Intermediate Egret
Frequency (%) 5 37 32 26 0 19
No. chicks hatched/nest 2.0 2.7 3.7 4.3
No. chicks fledged/nests 2.0 2.7 3.0 4.0

Cattle Egret
Frequency (%) 0 40 30 30 0 10
No. chicks hatched/nest 2.3 3.7 4.3
No. chicks fledged/nests 2.0 3.5 3.7

Chinese Pond Heron


Frequency (%) 50 50 2

Night Heron
Frequency (%) 0 64 29 7 0 14
No. chicks hatched/nest 3.0 3.5 4.0
No. chicks fledged/nests 2.9 3.0 4.0
______________________________________________________________________________

______________________________________________________________________________
Tab. 4.4. Chick condition index in relation to clutch size, for the Little Egret at the Gongquing colony. Index
values >1 indicate larger than average chicks.
______________________________________________________________________________
Initial clutch size
3 4 5 6
______________________________________________
No. chicks measured 8 18 66 13
Mean condition index 0.95 1.01 1.01 0.96
S.D. 0.05 0.06 0.08 0.11

26
Prey

Prey were collected from chicks repeatedly from 15 May to 15 June, at the Gongqing City and at
the Xihu Garden colonies. The pooled results are shown in Fig. 4.2. The main prey type was fish for
every bird species. Shrimps, frogs and tadpoles appear in the diet in decreasing importance. Prey
size is shown in Fig. 4.3.

100 fish

90 frog
80
Diet of chicks (% dry mass)

Tadpole
70

60 snake

50
lizard
40
shrimp
30

20 insect

10
Others
0
Cattle Egret Graet White Little Egret Intermediate Night Heron
Egret Egret

Fig. 4.2. Composition of the diet of the chicks.


mass of prey item (g dry mass)

3 Mean prey mass, all prey


2,5

1,5

0,5

0
Buib Egga Nyny

Fig. 4.3. Mean prey size.

Foraging habitats
The use of foraging habitat by the egrets and herons was studied by surveying the foraging areas shown in
Tab. 4.5, and in Fig. 4.4, during 14 surveys, from 24 May to 19 June.
The distribution of the foraging herons (Tab. 4.6, and same data depicted in Fig. 4.5) shows that Little,
Intermediate, and Cattle egrets, and Chinese Pond Herons, forage mostly (for >80% ) on rice paddies. On the
other hand, Great White Egrets forages with almost equal frequency in lakes, ponds, and rice paddies, while
Night Herons forage mostly in lakes and rivers.
Since most Little Egret foraged in rice fields, most sediment samples were collected there.

_________________________________

27
Tab. 4.5. Habitat types surveyed for foraging
herons.
_________________________________
Habitat types Surface (ha)
Lake 282.37
Ponds 74.95
Rice paddies 503.36
River 106.25
Other 0.80
Total 967.73
_________________________________

Fig. 4.4. Habitat types surveyed, within 7.3 km from the Gongquing colony.

______________________________________________________________________________

28
Tab. 4.6. Distribution of the adult heron and egrets foraging around the Gongquing colony
______________________________________________________________________________
Percentage of birds in each habitat Total no.
Lake Pond Rice paddies River Other birds observed
_____________________________________
Little Egret 7 5 88 0 0 214
Intermediate Egret 6 7 86 0 0 111
Great White Egret 36 29 36 0 0 14
Cattle Egret 5 4 89 0 2 261
Chinese Pond Heron 14 1 83 1 0 78
Night Heron 81 0 0 19 0 43
_____________________________________________________________________________

1,00

RIVER

0,80
RICEFIELDS
Frequency (%)

0,60
POND

0,40
LAKE

0,20
OTHER

0,00
Little Egret Intermediate Great White Cattle Egret Chinese Night Heron
Egret Egret Pond Heron

Fig. 4. 5. Distribution of the adult heron and egrets foraging around the Gongquing colony.

Prey biomass in rice paddies


We assessed the biomass available to egrets and herons in the rice paddies, using a standard sampling
technique, at 82 sites, each in a different rice field through the rice areas depicted in Fig. 4.4.
The most abundant prey types, both as number and mass, were tadpoles and fish. Fish were small, from 3 to
6 cm in standard length. Also abundant were the larvae of different insect groups (Tab. 4.7). The total
biomass in the Nanchnag rice paddies averaged 14.0 g dry weight (Tab. 4.8), an intermediate value in the
range of prey biomass values found in the rice fields of several European regions.

______________________________________________________________________________
Tab. 4.7. Composition of the prey available to egrets and herons in the rice paddies.
______________________________________________________________________________
Fish Frogs Tadpole Shrimp Crab Coleoptera Hemiptera Odonata Snake
larvae larvae larvae
No. items (%) 21.7 3.4 40.3 0.5 0.2 5.4 21.5 7.1 0.1
Biomass (%) 14.4 3.1 58.0 0.5 0.1 1.2 18.0 4.3 0.4

Mean mass of item 0.42 0.56 0.89 0.53 0.53 0.14 0.52 0.38 2.00
______________________________________________________________________________
______________________________________________________________________________

29
Tab. 4.8. Prey biomass (mean g dry weight/100 m2) available to egrets and herons in the rice padddies at the
Gongquing colony, Poyang lake study area. Data for European regions from Fasola et al. (1996).
______________________________________________________________________________
Poyang lake NW NE Rhone Delta Axios Delta Ebro Delta
China Italy Italy France Greece Spain

Total biomass 14.0 131.4 26.2 6.2 10.7 13.1


No. of samples 82 51 13 31 27 12
______________________________________________________________________________

Feeding success and prey type


The feeding success was recorded during 10 min focal animal observations for 41 Little Egrets, 31
Intermediate Egrets, 23 Cattle Egrets, 3 Great White Egrets, and for 3 Chinese Pond Herons, all of which
were feeding in rice fields.
We calculated the feeding success (example in Fig. 4.6) and the feeding technique (example in Fig. 4.7).
However, the most interesting measure, prey mass intake per unit time, could not be evaluated, because only
insufficient data on mean individual prey mass were available, due to the scarcity of data from chick’s prey.
mean no. prey captured / min

0
Chinese Cattle Egret Great White Little Egret Intermediate
Pond Heron Egret Egret

Fig. 4.6. Food intake by adult birds foraging in rice fields.

60
mean no. steps / min

40

20

0
Chinese Pond Cattle Egret Great White Little Egret Intermediate
Heron Egret Egret

Fig. 4.7. One aspect of the feeding technique, number of wading paces / min., of the adult birds foraging in
rice fields.

30
5.
Ecology of egrets and herons
at the Tai Lake study area, China

Dong Yuanhua
Institute of Soil Science, CAS, Nanjing 210008, P.R. China

Zhang Yingmei
Department Biology, Lanzhou University, Lanzohu 730000, PR China

Fasola Mauro
Dipartimento Biologia Animale, Università di Pavia, Pz. Botta 9, 27100 Pavia, Italy

Taihu region is one of the most productive areas for agriculture, and one of the most economically developed
parts of China. Rice fields account for 90% of total farmed land, and the water surface takes 45% of total
land. With the rapid economic growth since late ‘70s, water and soil pollution from industry, agriculture and
urban waste has been increasing significantly. Therefore, there is a growing urgency to monitor contaminant
levels in water and soil, to assess the effects of pollutants to human health and ecosystem health. As it is not
possible to measure all pollution parameters because of time-consume and cost, bioindicators are
increasingly used to monitor environmental quality and ecosystem-level change. As a first step towards
using egrets and herons as bioindicator of pollution at Taihu, we made preliminary survey to find heronries,
and then we selected the most suitable one for censusing the breeding population, recording breeding
success, investigating prey, and collecting samples, from April to July in 1999 and 2000 respectively. This
chapter summarises the results of this research.

Colony census
Five heronries were located in the Taihu area, along the expressway Shanghai-Nanjing (Fig. 5.1, Tab. 5.1).
Other colonies were occasionally found during trips in the surrounding region. These heron colonies
therefore seem to be spaced throughout the region, at distances of about 30 km to 40 km from each other.
The Wuxi colony was the largest, the other colonies were of medium or large size. These five colonies were
found at the same sites both in 1999 and in 2000.
Among these colonies, the one located near Wuxi, in the Yuantouzhu Park, was the most suitable one for
detailed studies, because of its dense population, species, accessibility. The surrounding wetlands, used by
the herons for foraging, are presumably exposed to high pollution from agricultural and industrial activities.
All the following data refer to this colony only.
In 1999, the Wuxi colony was located on the slopes of a hill, over a surface of about 27,219 m 2, and in a
P P

wood with Cinnamamum camphora and Pinus massoniana. Four species of heron breed: mainly the Night
Heron, second in abundance the Little Egret, and a few Chinese Pond Herons and Cattle Egrets. The nests
were very dense, and a total count was impossible. In order to estimate the total nest number, five sample-
areas were established at random, each of 25x25m, the nests were counted accurately in these sample areas,
and the total number in the whole colony was estimated at 9711 nests by extrapolation. The average nest
density is about 0.36m -2, and 1.06 per tree. According to the fr33equency ratio recorded for the four species,
P P

the number of nest were: 9250 of Night Herons, 291 of Little Egrets, 170 of Chinese Pond Herons plus
Cattle Egrets.
In 2000, the Wuxi colony was split in two subcolonies, at a distance of about 1 km. One subcolony was on
the slopes of a hill, approximately 500 m from the 1999 colony site. The second subcolony occupied the top
and the slopes of another hill. Both were in woods with dominant Cinnamamum camphora and Pinus
massoniana. Four species of herons bred, Night Herons and Little Egrets were dominant, with few Chinese
Pond Herons and Cattle Egrets; these two latter species increased after June. The very large size of the
colony made it difficult to estimate the total number of nest. To this aim, 20 sample areas were established at

31
random from top to bottom of the hills, each 10m×10m and square in shape. The surface area of the colony
was measured on a map drawn from data recorded using a GPS with 3-6 m approximation. The surface was
also checked on a 1:10,000 scale map. The nests for the whole and each species were estimated by
extrapolation of the average density of the sample areas, to the whole surface. The nests for Night Herons,
Little Egrets, Chinese Pond Herons and Cattle Egrets were 30100, 4200, 1000, and 1100 respectively.
Therefore the breeding population was much larger than in 1999.

Fig. 5.1. Heronry distribution in the Taihu region

____________________________________________________________________________________
Tab. 5.1. Description of heron colonies in the Taihu study area during 2000
____________________________________________________________________________________
Location Number of nests Vegetation Access
Night Little Chinese Cattle
Heron Egret Pond Heron Egret
Xianren 400 200 100 50 Pine, Chinese Fir easy
Zhengjiang 500 50 500 50 Chinese Fir hard
Changzhou 700 200 2000 100 Chinese Fir hard
Wuxi 30100 4200 1000 1100 Pine, shrub, Camphor very easy
Suzhou 14000 5000 200 1000 Pine, Bamboo, Camphor hard
_____________________________________________________________________________________

32
Breeding Success
Breeding success was investigated at the Wuxi colony, for Night Herons (111 nests studied in 1999, and 214
in 2000), for Little Egret (69 and 85, respectively), of Chinese Pond Heron (6 in 2000). The results are listed
in Tab. 5.2.

____________________________________________________________________________________
Table 5.2. Breeding success in a sample of nests at the Wuxi colony in the two study years, mean value
(minimum -maximum).
____________________________________________________________________________________
Night Heron Little Egret Chinese Pond Heron
_________________ __________________ ___________________
1999 2000 1999 2000 1999 2000
No.eggs/nest 3.6 (2-6) 3.4 (2-7) 4.9 (3-7) 5.1 (2-8) - 4.8 (4-6)
No.chicks/nest 2.7 (1-5) 2.8 (1-5) 4.0 (2-7) 4.3 (2-7) - 4.3 (3-5)
____________________________________________________________________________________

The breeding success of Night Heron and Little Egret could be considered normal, and even slightly higher
for Little Egret, compared to the literature data (see Table 3.1). This suggests that no adverse agent (e.g.
contaminants) was severely affecting bird reproduction in this study area.

Prey
Prey were collected from chicks repeatedly from 8 May to 5 June in 1999 and 2000. The main prey type was
fish, mainly Carassius auratus, Parabramis pekinensis, that accounted for 100% of the diet of Little Egret
chicks, and for 95% of the diet of Night Heron chicks, that also received small amounts of frogs, crustaceans
and mammals (Fig. 5.2). Tadpoles, although not representyed in our samples, were sometimes observed
among the prey regurgitated by the chicks. The size of the food items of the Little Egret was smaller than for
Night Herons (Fig. 5.3), and was mainly small fish and shrimp with body size shorter than 5 cm, including
Carassius auratus, Fluta alba, and Misgurnus anguillicaudatus. The size of the food items of Night Herons
was larger, the largest ones being 20 to 30 cm in length, including Crassius auratus, Parabramis pekinesis,
Misgurnus anguillicaudatus, Fluta alba, Crustacea, Insecta, Rana, and Rodentia.

100 Fish
90

80 Frogs
Diet of chicks (% dry mass)

70

60 Crustacean

50

40 Mammals

30

20

10

0
Little Egret Night Heron

Fig. 5.2. Frequency of different prey types in the diet of Little Egret and Night Heron chicks, at the Wuxi
colony.

33
140 Mean prey length, fish prey

120

mean length, mm
100

80
60

40

20
0
Little Egret Night Heron

Fig. 5.3. Mean prey length in the diet of Little Egret and Night Heron chicks, at the Wuxi colony.

Foraging habitats
A sample of water bodies were surveyed 2-5 times, from 3 to 18 June 2000 (Fig. 5.4). These sample habitats
were scattered within 13 km from the Wuxi colony, and they represented all the habitat types available to the
egrets and herons for foraging. The surface area of the habitats surveyed totalled 881 ha (Tab. 5.3).
The distribution of the foraging herons and egrets among these habitats (Tab. 5.4 and Fig. 5.5) shows that
most Little Egrets, Night Herons, and Chinese Pond Herons, foraged on fish ponds and on lake shores. The
Night herons exploited the open waters of the lake as well. No data are available for Cattle Egrets, that were
never recorded at the sample areas; they probably forage on dry lands. The scarce use of the rice fields is due
to their relatively small surface within the study area. On the other hand, fish ponds were intensely used,
presumably because they are abundant around the colony, and contain abundant food resources.

Fig. 5.4. Sample foraging habitats, that were surv33eyed around the Wuxi colony.
___________________________________________________
Table 5.3. Types of foraging habitats
___________________________________________________
Surface(ha)

34
Fish pond 162.4
Lake shores 189.4
Lake open waters 452.2
Pond 1.7
Rice fields 12.6
River 65.4
Total 880.7
___________________________________________________

____________________________________________________________________________________
Table 5.4. Distribution of the adult heron and egrets foraging around the Wuxi colony
____________________________________________________________________________________
Percentage of birds in each habitat
________________________________________________
Fish Lake Lake Pond Rice River Tot.no.birds
pond shores open waters fields observed

Little Egret 46 53 0 0 0 1 153


Night Heron 46 24 24 0 0 5 66
Cattle Egret 0 0 0 0 0 0 0
Chinese Pond Heron 65 12 0 18 6 0 17
____________________________________________________________________________________

River
100%
Rice fields
80%
Pond
Frequency (%)

60%
Lake open
waters
40% Lake shores

20% Fish pond

0%
Little Egret Night Heron Cattle Egret Chinese Pond
Heron

Fig. 5.5. Distribution of the adult heron and egrets foraging around the Wuxi colony.

35
6.
Breeding and foraging ecology of egrets
and herons at the Guandong study area, China

Dai Nianhua
Biological Resources Institute, Jiangxi Acedemy of Sciences, Nanchang, Jiangxi, P.R. China

Xavier Ruiz
Dipartamento Biologia Animal, Avgda. Diagonal 645, 08028-Barcelona , Spain

DAI AND XAVIER PLEASE WRITE SOMETHING HERE


AT LEAST ABOUT THE DISTRIBUTION OF THE COLONIES WHERE YOU SAMPLED

for the chapter:


7.
Breeding and foraging ecology of egrets and herons
at Haleji study area, Pakistan

Please Xavier:

1. complete the captions to the tabs and figs., as we usually do when we submit a paper to a journal

2. make your additions/crrections to my version (this file), not your old one, in order to maintain the
formatting

36
7.
Breeding and foraging ecology of egrets and herons
at Haleji study area, Pakistan

Xavier Ruiz, Gustavo Llorente, Carolina Sanpera


P P P

Departament. de Biologia Animal, Avgda. Diagonal 645, 08028-Barcelona , Spain

Lluis Jover
Dept. De Salut Pública (Bioestadistica). Universitat de Barcelona

Rahat Jabeen P

th
WWF-Pakistan, 6 Floor, Block 6,, P.E.C.H.S Shahra-e-faisal, Karachi 75400, Pakistan

Foraging habitat
The Haleji lake is surrounded by arid dry lands where no suitable place for herons feeding activity is
available in about 10 km around the colonies, the only exceptions being the Chateji lake which hosts their
own heronries, and the paddy fields around the town of Tatta which are 9 km away from the colonies in the
Haleji. However, these paddy fields were flooded only from the start of June, i.e. when the breeding season
of Little and Intermediate egrets at the Haleji is near the end. Therefore, the only available foraging habitats
for the egrets during the breeding season at the Haleji were the lake itself and their surrounding seepage
lagoons. Once realized this fact, we undertake regular surveys around the lake to count birds and to
identify the feeding areas used by them. Censuses were performed counting birds along the 18 km of
perimetral road around the lake shores. This road is elevated 2-3 meters enabling the observation of both, the
lake surface and the surrounding seepage lagoons. We performed 10 complete census, five in the early
morning and five in the evening. Every census lasted 45 min. in average.
We identifyed a total of 15 feeding areas (Fig. 7.1). The results of the censuses showed that the dominant
species during the day was by far the Intermediate egret (Fig 7.2), the other species being more than one
order of magnitude below it.

Foraging ecology
To analyze the foraging ecology we performed 15 controls distributed among 7 feeding areas (Fig. 7.3). In
every control we observed one to five birds. In each observation we followed a bird during a maximum of 10
minutes or until the bird leaves the feeding area. We defined a patch as the feeding ground used by an egret
between two flight activities within an observation. Therefore, every bird observed has used a minimum of
one patch and an undetermined maximum. However, not all the patches have been defined as above, since
the first patch is defined by the start of the observation and the last one by the end of the observation. To
record the feeding activity during an observation we used a standard data sheet which enabled us to register
the number of steps, stops, prey captures, prey sizes, and any other foraging activities. The birds were
observed using a 20 to 60X spotting scope.
A total of 42 observations were obtained from 7 feeding areas. Most of the observations belonged to
Intermediate Egrets (N=35) irrespective of the feeding area controlled. This was because of the great
dominance of that species in the diurnal heron community of the lake. In fact, it was the only species present
in most of the controls or overly dominant when other species were present. Even though we were not able to
obtain large number of observations of Little Egret (no.=7), we have performed a descriptive analysis
comparing Intermediate Egret and Little Egret.

37
In order to characterize the depth of the feeding grounds used by both egret species, at the start of every
observation we estimated the proportion of the leg that was submerged. The results show that both species
used areas where water depth covered between 15 to 45 % of the leg length. No significant differences
between species were found (Man Whitney test U=67, p=0.53). Since these results refer to a relative measure
of water depth and the leg is longer in the intermediate than in the little egret, this suggests that intermediate
egrets can use a wider range of water depths, i.e. that they have larger relative availability of feeding areas.
According to the duration of the observations, designed to be at maximum of 10 min., we can note that little
egrets tend to change of feeding area more frequently than intermediate egrets. When comparing the
distribution of the duration of observations in each species this trend is very clear and the differences are
significant (Mann-Whitney U=46.5, p=0.008)
When assessing the number of patches used by both species during an observation, it seems that Little egrets
use less patches in average than intermediate egrets and the same effect appears when comparing the number
of unsuccessful patches, i.e., in which no prey were captured. However, when the comparison is done
according to the number of unsuccessful patches relative to the total number of patches used by each species,
the differences between species were not significant (Mann-Whitney U=82, p=0.21), indicating that the
proportion of successful patches was similar for both species. Also, we can compare the number of prey
obtained during an observation, either at a global level or according to prey size (small, medium and large).
In no case there were significant differences between species.
As noted above, the permanence of Little Egrets in a feeding area is significantly lower than for Intermediate
egrets. Such difference can influence some of the apparent differences found later (e.g. the total number of
patches used seems to be smaller in Little Egrets). In order to control for this influence we transformed the
number of patches and the number of prey obtained, in their respective rates per min -1 . Once relativized by
P P

this transformation differences between species were not significant.


During observations the number of steps and stops were also recorded. The number of steps is quite similar
between both species, but the number of stops seems smaller for Little than for Intermediate egrets. When
transforming these values in rates to remove the effects of duration of observations, the apparent differences
disappear (steps per min. -1 Mann-Whitney U=91, p=0.35; stops per min -1 Mann-Whitney U=92, p=0.37)
P P P P

suggesting that foraging patterns were similar.


Using only the observations performed on Intermediate Egrets, because there is no enough sample size for
Little Egret, we have analysed the possible differences between the feeding areas where the controls were
performed. To do this we used two indicative parameters: the number of patches per min. and the number of
prey catched per min., in every observation. When comparing those feeding areas which had a large enough
sample size (i.e. excluding F0 and F5) we found significant differences between feeding areas. Post hoc
comparisons showed that differences are due to lower trophic yield of F4 (Tab. 7.1).
When using patches as the information unit, we can compare both species, because the sample size is then
greatly increased, but we cannot use rates, since we have not recorded the amount of time invested per patch.
This descriptive analysis suggests very similar performances for both species. In fact, differences were not
significant either for number of prey (Mann-Whitney U=3852, p=0.83), nor for number of steps (Mann-
Whitney U=3823, p=0.79), nor for number of stops (Mann-Whitney U=3543.5, p=0.34).
The comparison of the proportion of successful patches (i.e. those in which an egret was able to catch at least
one prey) also gave very similar values for the two species (Tab. 7.2, Likelihood ratio test=0.005, p=0.94).
Very similar values are also found for the two species when analysing the patches according to the maximum
size of the prey catched in them (Likelihood ratio test=1.31, d.f.=3, p=0.73).
In the case of Intermediate Egret for which we have a large enough number of patches, and using the sum of
steps and stops as a proxy of the time invested per patch, we can analyse the relationship of time invested
with the trophic yield of the patch. The association between both variables is shown in Fig 7.4. If we
compare the sum of steps and stops among the patches, grouped in four categories according to the number
of prey catched in them (none, 1, 2, 3 or more), we detect significant differences, which are indicative of the
positive association between the time invested foraging in patch (for which the sum of steps+stops is a
proxy) and the number of prey catched in it (Tab. 7.3). A result in total agreement with the postulates of the
foraging ecology theory.

38
Even though we have not a lot of observations on Little Egret, Fig 7.5 shows that the association between
number of catched prey and effort invested in a patch is similar to that obtained for the Intermediate Egret

_____________________________________________________________________________________
Tab. 7.1.
_____________________________________________________________________________________
Preys/min. Patches/min.
AREA CODE n Mean rank n Mean rank
F1 5 20.50 5 15.60
F2 7 19.43 7 19.86
F3 14 17.75 14 16.57
F4 6 6.83 6 13.17
Total 32 32
Kruskall-Wallis test 8.255 1.714
d.f.= 3 3
P= 0.04 0.63
_____________________________________________________________________________________

_____________________________________________________________________________________
Tab. 7.2.
_____________________________________________________________________________________
success no prey total
Little Egret count 17 14 31
row% 54.8% 45.2%
column% 10.8% 11.0%
Intermediate Egret count 141 113 254
row% 55.5% 44.5%
column% 89.2% 89.0%
total 158 127 285
_____________________________________________________________________________________

_____________________________________________________________________________________
Tab. 7.3.
_____________________________________________________________________________________
Sum of steps+stops
Number of preys n Mean rank
none 141 88.9
1 51 139.8
2 25 190.8
3 or more 37 214.9
Total 254
Kruskall-Wallis test 112.38
d.f.= 3
P= <0.001
_____________________________________________________________________________________

Diet
The diet of Intermediate Egret chicks at Haleji lake was analysed through the regurgitates obtained during
the sampling of blood and feathers. The regurgitates were collected in plastic bags and transported to the
laboratory, where we determined its prey content. All the undigested prey items were individually weighed
with a portable balance (0.01 g) and measured using a caliper (0.01 mm). The rest of the regurgitate was also
inspected to count the distinguishable prey items and then weighed as a whole. A total of 9 Little Egret
chicks with body masses from 105 to 345 g were examined for prey contents, as well as 40 E.i nestlings with
body masses between 125 and 420 g. From these we succeeded in obtaining regurgitates for 3 little and 35
Intermediate Egret chicks.

39
The diet composition was only analysed for Intermediate Egrets (Tab. 7.4, 7.5) because of insufficient
sample size in the case of Little Egrets.
In order to assess the importance of the different prey items we used the following descriptors : Frequency of
occurrence by number and by biomass transformed respectively in percentages, and an index which takes
into account the frequency, the abondance and the homogeneity of consumption for the different prey items
(Use Index). From these analyses it stands out that the most important prey in number are Caridean shrimps
followed by fish (Oreochromis > Colisa = Barbus), the rest being consumed only in small quantities (Fig
7.6). However in biomass the index of use indicates that Oreochromis is the most important prey followed
by Caridean shrimps > Colisa > Glossogobius > Barbus > Rana, all the remaining prey being only
occasionally represented in the diet (Fig 7.7).
Finally we have analysed the distribution of sizes of the main prey consumed by the Intermediate Egret
chicks at the Haleji (Fig 7.8). From these analysis we conclude that most prey are in the range of 2 to 4 cm in
length. In the case of Colisa and Caridean shrimps this range corresponds to the sizes found in the lake, but
for Oreochromis and Barbus, there were larger specimens at the lake and it was probably operating a prey
size selection. This can derive either from the facility of catching smaller exemplars, from active selection by
the egrets to feed their chicks or from the place where the prey were taken (the lake surface) which probably
only hosts juvenile exemplars of these species.

_____________________________________________________________________________________
Tab. 7.4
_____________________________________________________________________________________
Pisces
Cichlidae
Oreochromis niloticus
Anabantidae
Colisa lalia
Cyprinidae
Barbus phuturio (=Puntius phuturio)
Gobiidae
Glossogobius giuris
Amphibia
Ranidae
Rana tigrina (adult and juvenile)
Arthropoda
Crustacea
Caridean shrimps
Insecta
Odonata (adults and larvae)
Hemiptera (Nepidae)
Orthoptera
Coleoptera (adults and larvae)
Lepidoptera (larvae)
_____________________________________________________________________________________

_____________________________________________________________________________________
Tab. 7.4
_____________________________________________________________________________________
Caridean shrimp Colisa Oreochromis Barbus (Puntius) Glossogobius
N Length/N Weight 39/42 21/23 54/57 31/31 7/8
Mean length (mm) 34.21 33.81 30.52 26.78 74.74
(Std. Dev/Min-Max.) (5.56/22.75-47.41) (3.67/26.79- 38.44) (8.98/20-74.95) (5.7/19.34-46.79) (20.95/33.83-96.94)
Mean Weight (g) 0.34 1.28 1.06 0.53 7
(Std. Dev/Min-Max.) (0.13/0.12-0.65) (0.48/0.49-2.12) (1.69/0.15-12.59) (0.57/0.18-3.41) (1.92/0.44-15.14)
_____________________________________________________________________________________

40
Fig. 7.1

41
600
500
Eg
400 Ei
300 Ag
200 Ap
Ac
100
0
e n

0
2

1
ay
F0
F3
F1
F4
F5
F6
F7
F8
F9

F2
Th oo

F1
F1

F1
W
ag
lL
ee
St

Fig 7.2.

2
Number of controls

0
F0 F1 F2 F3 F4 F5 F13

AREA CODE

Fig 7.3.

42
40

30

20
Number of stops

# of preys

3 or more
10
2

0 0
0 25 50 75 100 125 150 175 200

Number of steps

Fig 7.4.

20

15

10
Number of preys

E.intermedia

0 E.garzetta
0 25 50 75 100 125 150 175 200

Sum of steps+stops

Fig 7.5.

43
D i e t o f E g r e t t a i n t e r m e d i ac h i c k s f r o m H a l e j i L a k e ( P a k i s t a n )
U n d e t e r m in e d
C o lis a
B a rb u s

R ana O r e o c h r o m is

O d o n a t a ( la r v a e ) C a r id e a n s h r i m p
Use Index

C o le o p t e r a
0 10 20 30 40 50 60

C o le o p t e r a ( l a r v a e ) H e m ip t e r a

G lo s s o b iu s L e p id o p t e r a ( la r v a e )

O d o n a ta
V e g e ta l
O r th o p te r a

Fig. 7.6.

D i e t o f E g r e t t a i n t e r m e d i ac h i c k s f r o m H a l e j i L a k e ( P a k i s t a n )
B io m a s s
U n d e t e r m in e d
C o lis a
B a rb u s

Rana O r e o c h r o m is

O d o n a ta (la r v a e ) C a r id e a n s h r im p
Use Index

C o le o p te ra
0 10 20 30 40 50

C o le o p t e r a ( la r v a e ) H e m ip t e r a

G lo s s o g o b iu s L e p id o p te ra ( la r v a e )

O d o n a ta
V e g e ta l
O r th o p te r a

Fig. 7.7.

44
Frequency

10
10

0
2
4
6
8
0
2
4
6
8
0 0

8-10 8-10

18-20 18-20

28-30 28-30

C o lis a
38-40 38-40

B a r b u s (P u n tiu s )
48-50 48-50

58-60 58-60

45
> 70 > 70

Fig 7.8.
0 0

8-10 8-10

P re y L e n g th (m m )
18-20 18-20

28-30 28-30

38-40 38-40
O r e o c h r o m is

C a r id e a n s h r im p

48-50 48-50

58-60 58-60

> 70 > 70
8.
Breeding and foraging ecology of egrets and herons
at Taunsa study area, Pakistan
Muhammad Ashiq
Pakistan Agriculture Research Council, P.O. Box 1031, Islamabad 45500, Pakistan

Fasola Mauro, Boncompagni Eleonora, Giuseppe Gaudenzi


Dipartimento Biologia Animale, Università, Piazza Botta 9, I-27100 Pavia, Italy

This chapter summarizes the ecological data collected during 2000 (1 May-18 June) at the Taunsa Barrage
study area (Pakistan, 30°42’N, 70°50’E). This area includes an artificial barrage on the River Indus, the
storage reservoir behind the barrage, the riverside wetlands, and the surrounding area with irrigated crops.
This study area was expected to be subject to pollution from agriculture.

Colony census
Within a radius of 20 km from Taunsa Barrage we found two heron colonies (Tab. 8.1). We presume that no
other, undetected colony existed within several tents of kilometers in the surrounding areas, that are very dry
except for the shores of the River Indus.
One smaller colony we called “canal” (shown in Fig. 8.1 as “colony 2000” ) was located along a large canal;
this colony was chosen as the focal ones for study, because it was the only accessible one.
A second colony was located in a large reed bed, at the left-bottom corner of Fig. 8.1 (but not shown in the
figure). This colony was inaccessible, and only a rough estimate of its size was possible. During the
preliminary survey conducted in 1999, only one big colony had been found, approximately 2 km East of the
Colony 2000.
______________________________________________________________________________
Tab. 8. 1. Description of the two colonies censused in the Taunsa study area in 2000.
_____________________________________________________________________________________
Colony Canal Reed bed
Census accuracy 95% 70%

Coordinates 30°30.213’N 30°30.136’N


70°48.639’E 70°47.236’E

Habitat 10 Acacia trees along an irrigation canaltall reeds, colony about 150x400m
Nests 2-15 m high Nests 3-4 m high

No. nests
Total 368 2700

Little Egret 26 50
Intermediate Egret 22 70
Cattle Egret 305 2000
Indian Pond Heron 60
Purple Heron 10
Night Heron 15 10
Javanese Cormorant 500
______________________________________________________________________________

46
Fig. 8.1. Taunsa study area, colony location, and foraging habitats surveyed within 12.5 km from
the colony. The area in the map is about 15 by 10 km. The inset shows the location of the study
area within Pakistan (small gray square).

Breeding Success
Breeding success was studied in all the accessible nests (Tab. 8.2). The breeding success of the Little Egret
was relatively low, i.e. toward the lower end of the range of values found in literature for different locations
and years (see Tab. 3.1). For Night Herons as well the breeding success was low, but only one nest was
studied. No comparative data are available in the literature for the other species. This relatively low breeding
success may be due either to unfavorable environmental conditions, e.g. food scarcity, or to the effect of
contaminants.
______________________________________________________________________________
Tab. 8.2. Breeding success in sample nests at the Taunsa colony, mean value (minimum -maximum)
______________________________________________________________________________
No. nests No. eggs/ No. chicks No. chicks
recorded nest hatched/nest fledged /nest

Little Egret 6 3.8 (3-5) 3.5 (2-5) 2.5 (2-3)


Intermediate Egret 7 3.0 (2-4) 2.3 (1-3) 2.0 (1-3)
Cattle Egret 64 3.6 (2-6) 2.9 (1-4) 2.7 (1-4)
Night Heron 1 3.0
______________________________________________________________________________

47
The frequency of clutches of differing size, and their respective success, are shown in Tab. IV. Splitting
success among clutch sizes may help discover critical factors. E.g in case of food limitations, larger clutches
may have a lower success. No such effect appears in the data of Tab. 8.3. The success remains high even for
the larger clutches. These results again indicate good breeding conditions.

_____________________________________________________________________________________
Tab. 8.3. Frequency of nests, breeding success (mean values), and chick condition index (mean values), in
relation to clutch size.
______________________________________________________________________________
Initial clutch size Tot. No.
2 3 4 5 6 study nests
______________________________

Cattle Egret
Frequency (%) 2 47 41 9 2 64
No. chicks hatched/nest 1 2.6 3.0 3.2 4.0
No. chicks fledged/nests 1 2.6 2.8 2.8 4.0
______________________________________________________________________________

Foraging habitats
The use of foraging habitat by the egrets and herons was studied by surveying the foraging areas shown in in
Fig. 8.1, and in Tab. 8.4, during 10 surveys, from 18 May to 13 June.
The distribution of the foraging herons (Tab. 8.5, and same data depicted in Fig. 8.2) shows that a variety of
habitats was used for foraging by all the species of egrets and herons. Cattle Egrets used dry lands more than
all the others, as it is usual for this species. The data for Purple Herons are biased by the very small number
of observed birds, only 2. T limited use of the rice paddies is due to the fact that they were flooded only
during the last 10 days of our survey, and later their importance would likely have been greater.
Sediment samples were collected in the ponds, and in the rice paddies, two of the habitats most used by the
foraging egrets, and in the canals, that can be considered representative of all the other water bodies since
they exchanged the water among all of them
_________________________________
Tab. 8.4. Habitat types surveyed for foraging
herons.
_________________________________
Habitat types Surface (ha)

Lake 177.90
Canals 218.73
Ponds 540.12
Wetlands 1383.58
Rice paddies 170.80
Flooded fields 693.91
Dry Fields 385.57

Total 3570.61
___________________________________

48
_____________________________________________________________________________
Tab. 8.5. Distribution of the adult heron and egrets foraging around the Taunsa colony
_____________________________________________________________________________
Percentage of birds in each habitat Total no.
Lake Channels Ponds Wetlands Rice Flooded Dry birds
paddies fields fields observed
_________________________________________________

Little Egret 9 2 24 21 4 29 10 303


Intermediate Egret 8 2 41 29 0 17 4 132
Great White Egret 11 11 27 16 9 15 11 55
Cattle Egret 2 2 5 55 1 17 17 837
Indian Pond Heron 13 0 22 2 8 53 3 64
Purple Heron 50 0 0 50 0 0 0 2
_____________________________________________________________________________

1,00 Lake

Channel
0,80

Pond
Frequency (%)

0,60
Wetland

0,40 Ricefield

Flooded
0,20 field
Dry field

0,00
Little Egret Intermediate Geat White Cattle Egret Indian Pond Purple Heron
Egret Egret Heron

Fig. 8.2. Distribution of the adult heron and egrets foraging around the Taunsa colony

Feeding success and prey type


The feeding success was recorded during 10 min focal animal observations for 24 Cattle Egrets, 58 Little
Egrets, 17 Intermediate Egrets, and 3 Great White Egrets, that were feeding in a variety of habitats.
Their feeding success and some aspects of the feeding technique are shown in Fig. 8.3 and 8.4, respectively.

49
1,6
1,4
1,2
1,0
0,8
0,6
0,4
0,2
0,0
Cattle Egret Little Egret Intermediate Geat White
Egret Egret

Fig. 8.3. Food intake by adult birds.

30

25

20

15

10

0
Cattle Egret Little Egret Intermediate Geat White Egret
Egret

Fig. 8.4. One aspect of the feeding technique, number of wading paces / min., of the adult bird.

50
9.
Breeding and foraging ecology of egrets and herons
at Karachi study area, Pakistan
Jabeen Rahat
th
WWF-Pakistan, 6 Floor, Block 6,, P.E.C.H.S Shahra-e-faisal, Karachi 75400, Pakistan

Gaudenzi Giuseppe
Dipartimento Biologia Animale, Università, Piazza Botta 9, I-27100 Pavia, Italy

This chapter summarizes the ecological data collected during 2000 (1-30 May) at the Karachi study area,
Pakistan (24°47’N, 67°11’E; 112). This areas includes the harbour of Karachi, and the
neighbour tidal creeks, mangrove swamps and intertidal mudflats. This aream was expected to
be subject to considerable urban and industrial pollution. T he most abundant egret was
Egretta grzetta schistacea, a dark colour morph of the polymorphic species Little
Egret.

Colony census
Only one egret colony were present within this study area (Fig. 9. 1), and for a radius of at least 20 km. Nest
counts (Tab. 9.1) could be accomplished with reasonable accuracy.

Code Type

1 open channel

2 mud

3 channel

4 mud

5 creek

6 mangroves

7 mangroves

51
Fig. 9.1. Karachi study area, with the location of the colony, and with the habitat types surveyed, within 2
km from the colony.
________________________________________________________
Tab. 9.1. Description of the colony in the Karachi study area, 2000.
________________________________________________________
Colony Ghay Bunder
Coordinates 24°51.431’N, 66°56.053’E
Habitat Mangroves on an island,
nests 2-5 m high
No. of nests
Total 145

Little Egret, dark morph 100


Little Egret, white morph 15
Intermediate Egret 20
Indian Pond Heron 10
________________________________________________________

Breeding Success
Breeding success was studied in all the nests that could be found in the colony, all belonging to the dark
morph of the Little Egret. The breeding success (Tab. 9.2). The breeding success of the Little Egret was low,
i.e. toward the lower end of the range of values found in literature for different locations and years (see Tab.
3.1). This relatively low breeding success may be due either to unfavorable environmental conditions, e.g.
food scarcity, or to the effect of contaminants.

______________________________________________________________________________
Tab. 9.2. Breeding success in sample nests at the Karachi colony, mean value (minimum -maximum)
______________________________________________________________________________
No. nests No. eggs/ No. chicks No. chicks
recorded nest hatched/nest fledged /nest

Reef Egret 34 3.6 (2-5) 2.9 (1-5) 2.9 (1-5)


______________________________________________________________________________

The frequency of clutches of differing size, and their respective success, are shown in Tab. 9.3. Splitting
success among clutch sizes may help discover critical factors. E.g in case of food limitations, larger clutches
may have a lower success. No such effect appears in the data of Tab. IV. The success remains high even for
the larger clutches, and this indicates good breeding conditions as regards food availability.

______________________________________________________________________________
Tab. 9.3. Frequency of nests, and breeding success (mean values), in relation to clutch size.
______________________________________________________________________________
Initial clutch size Tot. No.
2 3 4 5 study nests
_________________________
Reef Egret
Frequency (%) 9 30 52 9 33
No. chicks hatched/nest 1.7 2.6 3.3 5.0

52
No. chicks fledged/nests 1.7 2.3 3.5 5.0
______________________________________________________________________________

Foraging habitats
The use of foraging habitat by the egrets and herons was studied by surveying the foraging areas shown in
Fig. 9.1 and in tab. 9.4, during 4 surveys, from 8 to 23 May. The extension of each habitat is expressed as
shore length, and not as surface area, since the egrets exploited all these habitats only along the shores.
The distribution of the foraging herons (Tab. 9.5, and same data depicted in Fig. 9.2) shows that Little Egrets
foraged mostly on the surfaces of mud exposed at low tide, and with lesser frequency on the banks of large
canals that connected the lagoon to the sea. The Intermediate egrets and the Indian Pond Heron foraged
mostly on the same habitats. Therefore, the sediment samples were collected at the two most used habitats,
mud and channels.
________________________________________
Tab. 9.4. Habitat types surveyed for foraging herons.
________________________________________
Length border of (m)

Channels 1890
Muddy shores 740
Mangroves 630
Total 3260
________________________________________

_____________________________________________________________________________
Tab. 9.5.Distribution of the adult heron and egrets foraging around the Karachi colony.
_____________________________________________________________________________
Percentage of birds in each habitat Total no.
Channel Mangroves Mud birds observed
_____________________________________

Little Egret 37 1 62 216


Intermediate Egret 60 10 30 10
Indian Pond Heron 60 10 30 10
_____________________________________________________________________________

1,00

0,90
0,80

0,70
Frequancy (%)

0,60
mud
0,50 mangrooves
channel
0,40

0,30

0,20

0,10

0,00
Little Egret Intermediate Egret Indian Pond Heron

53
Fig. 9.2. Distribution of the adult heron and egrets foraging around the Karachi colony

Feeding success and prey type

All the 89 prey items, collected over 3 weeks throughout the study period, were small fish (Liza abu,
Perciformes). The wet weight of these fish prey averaged 13.8 g, the dry weight 3.7 g, and their length
ranged from 78 to 23 mm
The feeding success was recorded during 10 min focal animal observations for 8 Little Egrets and 4
Intermediate Egrets, from 8 to 23 May.
We calculated the feeding success (example in Fig. 9.6) and the feeding technique (example in Fig. 9.7).

2,0
1,8
1,6
1,4
1,2
1,0
0,8
0,6
0,4
0,2
0,0
Little Egret Intermediate Egret

Fig. 9.3. Food intake by adult birds around the Karachi colony.

70
60

50

40

30
20

10
0
Little Egret Intermediate Egret

Fig. 9.4. One aspect of the feeding technique, number of wading paces / min., of the adult birds foraging
around the Karachi colony.

54
10.
Heavy metal contamination
in the samples from China

Boncompagni Eleonora, Fasola Mauro,


Dipartimento Biologia Animale, Università, Piazza Botta 9, I-27100 Pavia, Italy
Gandini Carlo
Dipartimento Chmica Farmaceutica, Università, Viale Taramelli, I-27100 Pavia, Italy
Orvini Edoardo
Dipartimento Chmica Generale, Università, Viale Taramelli, I-27100 Pavia, Italy

The samples for chemical analysis of contaminants were collected from three study areas:
1) Pearl River Delta, Guangdong, studied in 2000, and expected to be subject to urban-industrial
pollution.
2) Tai Lake, studied in 2000, and expected to be subject to serious pesticide and heavy metal pollution
from both agriculture and industry. The samples were collected at the one colony located in the
Yuantouzhu Park near Wuxi, and surrounded by wetlands presumably exposed to high pollution from
agricultural and industrial activities.
3) Poyang Lake, Jiangxi, studied in 1999, and expected to be free of pollution. The samples were
collected at the colony close to the city of Gongquing, north of Nanchang. Despite being close to Lake
Poyang, the largest freshwater body and the most important site for waterfowl in China, and a NEPA
nature reserve, the area surrounding the Gonquing colony was intensively cultivated, therefore the
samples may reflect some exposure to agricultural pollution.
The egret ecology in these study areas are described in the preceding chapters. This chapter summarizes and
discusses the main results about the levels of heavy metals and of some other inorganic substance of
environmental concern. The rough data are listed in App. A. Further analyses of these results are being
devoted to the publications already issued, in press, or in preparation.

Materials
In order to use colonial waterbirds as bioindicators, and in order to select samples that are homogeneous and
comparable for all the study sites, we collected the following materials for chemical analysis.
Eggs. Since pollution levels tend to be more similar within eggs of the same clutch than between eggs from
different clutches, to take an egg per nest may not be a good sampling strategy. A strong intra-clutch effect
can also be found between the first and last egg in a clutch, this effect will depend on clutch-size, and this
source of variability must be taken into account. Since it is not practicable to analyze all the eggs in a clutch,
because of cost constraints, during 1999 we tried a sampling procedure intended to assess the relevance of
intra-clutch effects, and we collected both single egg taken at random from a nest, and a few entire clutches.
Feathers. Contour feathers were collected from one chick, at the same nests from which the eggs had been
sampled.
Prey. The 3 main prey of the egrets, from nestling regurgitates, were collected. Whenever possible, 10 items
of a prey type collected in a particular day constituted one sample. While collecting the prey of the chicks for
diet analysis, we separated from these prey, 1 “sample for analysis” per week (each consisting of 10 items
each, the most fresh ones) for each of the 3 main prey types (by main we mean in relation to mass).
Therefore, 3 samples were collected each week, for the 3 main prey types of that week, whenever possible.
Sediments. Sediments were collected in the different foraging habitats used by the egrets, because
differences in placement, water circulation, biological activity above the sediment, can originate variability

55
in contamination. In order to obtain a sample large enough to obtain an adequate picture of the pollutants, we
collected several core replicas of sediment in the places where egrets foraged, then we collapsed the replicas
into composite samples to be analysed. The restricted amount of resources available for sediment analyses
forced us to define a sampling scheme that is clearly suboptimal, but probably enough to reach our
objectives, i.e. to estimate the average contamination of the sediment in the wetlands. The samples were
collected at the end of the study period, when we already had knowledge (through the foraging habitat
records) about the habitats used by the egrets.
Sediments were collected using a core sampler (a plastic tube with 5 cm diameter and 2 cm height) pushed
into the mud on the bottom of the sample wetland.
Sediment samples were collect by: defining main and secondary habitats; defining how many points (=
number of cores obtained) to sample in each habitat; mixing at random from 4 to 12 cores, to obtain
composite samples.
Due the logistic problems, the only solution for conservation and transport of the samples was to
homogenyse and dry all the wet material (eggs, prey, sediments). Eggs, prey, and sediments, were kept cool,
homogenysed, dried in oven (24-48 h at max 50 °C, to constant weight), and stored in poliethylene vials.
Feathers were simply stored into polytene envelopes
From each egg, a piece of eggshell, centered at the egg equator, was cut and stored for thickness
measurement. Polytene vials were used for all the material to be analysed, because they are clean from
metals etc. Care was taken that other containers would not contaminate the samples.

Analytical Methods
Two analytical techniques were used for all the sample material, whenever possible: Atomic Adsorption
Spectrophotometry (AAS) for cadmium, mercury and lead, and Neutronic Activation Analysis (NAA) for the
remaining elements.
The samples were split in two parts of similar amounts, one for NAA analysis, and one for AAS analysis.
Unfortunately, some of the feather samples were too small in mass (< 1 mg), could not be further split, and
we decided to devote this limited material only to NAA analysis. The analysis so far are complete for NNA,
but only about one half of the samples have been processed by AAS, therefore the results summarized here
for cadmium, mercury and lead are only partial.
Cadmium and lead were analysed by the Perkin Elmer Aanaliyst 600 atomic adsorption spectrophotometer,
equipped with THGA (Transversely Heated Graphite Furnace), longitudinal AC Zeeman-effect background
correction and autosampler AS-800.
Mercury was analysed by the Perkin Elmer FIAS-100 equipement for cold vapours generation and the
analysis carried out with the Perkin Elmer 3110 Atomic Adsorpion Spectrophotometer.
The control of the instruments and data calculations were performed on PC using the AA WinLab software.
For sample preparation, eggs, preys and sediments must be submitted to a preliminary mineralization
treatment before analysis, in order to eliminate organic matter. Mineralization was performed in a CEM-
MDS 81D microwave oven, operating in teflon bombs with Newtec Valves, by dissolving samples in 30%
nitric acid as described in a previously work (Fasola et al. 1998). The mineralization technique was tested,
for recovery of metals, on the biological reference material using as matrix whole egg powder (8415
Reference Material) certified by NIST (National Institute of Standards & Tecnology). All the samples tested
for Cd,Cr,Hg and Pb gave recoveres ranging from 98 % and 101%.
Preliminary tests were carried out using standard solutions of pure single element dissolved in nitric
acid/water 30% v/v at three different levels. The calibratin curves were found linear for the following ranges
respectively, as absolute concentrations: for Cd ( 2-4-6 ppb), for Cr (5-10-20 ppb), for Hg (2-4-8 ppb) and
for Pb (3-6-12 ppb) corresponding to a detection limit, on the biological sample, of 0.020 ppm, 0.030 ppm
0.010 ppm and 0.030, for Cd, Cr, Hg and Pb respectively. Estimates were made according to standard
addition method (M.Bader,J.Chem.Edu. 57,703 1980) supported by the PC software.
NAA was adopted for analysis of all the others elements (chromim, arsenic, silver, bromium, cobalt,
caesium,lantanium, nickel, scandium, selenium, and zinc) in all the samplematerial. For some materials and

56
for the elements that were measured by AAS as well, the NAA results were only confirmatory, while for
feathers and for many elements, they were the NAA results were the only ones available.Irradiation of the
samples was performed at the irradiation position of the Triga Mark II Nuclear Reactor of the Pavia
University, at a flux of 1x1013n cm-2sec-2. Condition and irradiation time, counting and delay, were chosen
according to the nuclear characteristics of the element to be investigated. Gamma ray spectrometry was
performed using a high resolution intrinsic Ge detector. Data were processed using a computer program from
ORTEC.
All concentrations are expressed in parts per million (μg/g, or ppm) on a dry weight basis.

Data analysis

Sample size in the following tables corresponds to the number of independently sampled nests. For some
clutches, more than one egg was collected, and in these cases we computed a mean value for each clutch and
we used this value as one sample for the statistics.
Contaminant levels were tested for differences among study areas, and whenever possible among prey types
and among sediment origin within each study area, using the Kruskal-Wallis non-parametric variance test,
because the value distribution was non-normal. The geometric mean was used throughout as a parameter of
central tendency, because the frequency distribution of the concentrations was strongly skewed towards low
values. In order to calculate mean concentrations, and in order to perform statistical comparisons, the
samples in which a certain element was not found, were attributed a value corresponding to 1/100 of the
minimum measured concentration for that element.

Contamination levels in the environment


Eggs. The contamination levels in the eggs of Little Egrets are shown in Tab. I and II.
Scandium and selenium were detected in all samples of the three colonies, arsenic and bromine in all
samples from Pearl River Delta and Tai Lake, the only available, cesium and zinc in more than 70% and
nickel and silver in less than 20%. of the samples.
There were significant differences in mercury, arsenic, bromine, cobalt, cesium, scandium, selenium and zinc
concentration between locations. The highest levels of mercury, cobalt, cesium, scandium and zinc occurred
in Little Egret eggs from Poyang Lake, while the highest levels of selenium, arsenic and bromine occurred in
samples from Pearl River Delta. Althought there were significant differences among the colony sites for
mercury, cesium, scandium, selenium and zinc, the differences were not great, except for zinc, and in general
the values were relatively low.

Feathers. The contamination levels in the feathers of Little Egret chicks are shown in Tab. IV; NAA results
are the only ones available, pending the conclusion of the analyses. Cobalt was detected in all samples of the
three colonies, arsenic and bromine in al samples of those from Pearl River Delta, the only avalaible;
cesium,scandium and selenium were found in more than 70% of the samples.
There were significant differences in silver, cobalt, cesium, scandium concentration between locations.
The highest levels of cobalt e scandium occurred in samples from Pearl River Delta, the highest levels of
cesium occurred in samples from Poyang Lake and those of silver occurred in Little Egret from Tai Lake.
Althought there were significant differences among the colony sites for these metals, the differences were
not great, except for cobalt, and the values were again relatively low.

Prey. Contamination levels in the prey collected from the food of Little Egret chicks are shown in Tab. V
and VI. There were significant differences in cobalt, cesium, scandium and zinc concentration between
locations. The highest levels of cobalt, cesium, scandium occurred in the prey of Little Egrets from Poyang
Lake, while the highest levels of zinc occurred in samples from Tai Lake. Althought there were significant

57
differences among the colony sites for these metals, for prey as well the differences were not great and the
values very low.

Sediments. Contamination levels in the sediments collected in wetlands used by Little Egrets as foraging
areas around the colony are shown in Tab. VII and VIII. There were significant differences in chromium,
cesium, selenium and zinc concentration between locations. The lowest levels of chromium occurred in Pearl
River Delta samples and the values for Poyang lake and Tai Lake were much higher and very similar. The
lowest values of cesium and zinc occurred in the Poyang lake samples and the values for Pearl River Delta
and Tai Lake were much higher and very similar. The lowest values of selenium occurred in Tai Lake and
the concentration for Pearl River Delta and Poyang lake were much higher and very similar.

_______________________________________________________________________________________

Tab. 10.1. Concentration of the most hazardous heavy metals in the eggs of Little Egrets. The values are: no.
of samples, (percentage frequency of samples with concentrations above the detection limits, only for
samples with no.>5), geometric mean, maximum and minimum values, ppm on dry weight). Nd = no
detected. Ns = non-significant.
_______________________________________________________________________________________
cadmium chromium mercury lead

Pearl River Delta no. P 2 P


2 2 2
mean Nd 0.053 0.315 0.047
min-max 0.05-0.57 0.28-0.35 0.04-0.05

Poyang Lake noP P


23 (21.7%) 19 (100%) 19 (100%) 23 (78.3%)
mean 0,000001 0.127 0.576 0.221
min-max Nd-0.19 0.001-0.46 0.001-2.13 0.08-2.33

Tai Lake no. 2 2 2 2


mean Nd 0.122 0.240 0.103
min-max 0.10-0.15 0.14-0.41 0.06-0.17

Difference among study areas (P=) N.s N.s 0.02 N.s


_______________________________________________________________________________________

_______________________________________________________________________________________
Tab. 10.2. Concentration of elements that may be responsible for toxicity at high doses, in the eggs of Little
Egrets. Values as in Tab. I.
_______________________________________________________________________________________
copper iron manganese
Pearl River Delta no. P 13 (8%)
P
16 (100%)
P P

mean 0.106 114.082


min-max Nd-1400.00 53.30-312.00

Poyang Lake noP 11 (100%)


P
P 35 (100%)
P
19 (100%)
mean 13.147 118.572 2.795
min-max 4.80-31.60 80.0-217.8 1.30-11.80

Tai Lake no. 7 (14%) P 22 (100%)


P

mean 0.267 177.530


min-max Nd-7810.00 104.0-348.8

Difference among study areas (P=) 0.000


_______________________________________________________________________________________

58
59
______________________________________________________________________________________________________________________________________________
Tab. 10.3. Concentration of other elements of environmental concern, in the eggs of Little Egrets. Values as in Tab. I.
______________________________________________________________________________________________________________________________________________
arsenic silver bromine cobalt cesium lanthanum nickel scandium selenium zinc
Pearl River Delta no. P 17 (100%) 10 (20%)
P
17 (100%) 17 (59%) 17 (100%) 17 (53%) 16 (0%) 17 (100%) 17 (100%) 17 (71%)
mean 0.142 0.00003 40.049 0.004 0.033 0.012 Nd 0.002 3.550 1.07
min- max 0.02-0.83 Nd-0.85 9.66-95.67 Nd-0.60 0.004-0.17 Nd-0.36 0.0003-0.06 2.0-5.95 Nd-556

Poyang Lake no.P P


38 (100%) 17 (100%) 23 (100%) 38 (100%) 38 (100%)
mean 0.118 0.036 0.027 2.919 59.58
min-max 0.06-0.30 0.02-0.35 0.009-0.05 1.97-4.90 43-163

Tai Lake no.P 8 (100%)


P
18 (0%) 8 (100%) 22 (91%) 22 (91%) 8 (37%) 22 (14%) 22 (100%) 22 (100%) 22 (77%)
mean 0.025 Nd 102.957 0.071 0.007 0.012 0.036 0.004 2.689 2.26
min-max 0.02-0.60 63.0-182.0 Nd-1.64 Nd-0.06 Nd-46.0 Nd-7.02 0.001-0.16 1.90-3.98 Nd-82

Difference among study areas (P=) 0.024 Ns 0.001 0.004 0.000 Ns Ns 0.000 0.013 0.000
______________________________________________________________________________________________________________________________________________

60
_______________________________________________________________________________________
Tab. 10.4. Concentration of elements that may be responsible for toxicity at high doses, in the eggs of Little
Egrets. Values as in Tab. I.
_______________________________________________________________________________________
copper iron manganese
Pearl River Delta no. P 13 (8%) P 16 (100%)
P P

mean 0.106 114.082


min-max Nd-1400.00 53.30-312.00

Poyang Lake no P 11 (100%)


P P 35 (100%)
P 19 (100%)
mean 13.147 118.572 2.795
min-max 4.80-31.60 80.0-217.8 1.30-11.80

Tai Lake no. 7 (14%) P 22 (100%)


P

mean 0.267 177.530


min-max Nd-7810.00 104.0-348.8

Difference among study areas (P=) 0.000


_______________________________________________________________________________________

_______________________________________________________________________________________
Tab. 10.5. Concentration of elements that may be responsible for toxicity at high doses, in the feather of
Little Egrets. Values as in Tab. I.
_______________________________________________________________________________________
iron manganese copper
Pearl River Delta N o P 19 (100%)
P 19 (0%)
Mean 490.153 Nd
Min-Max 37.10-4200.00

Poyang Lake NoP 6 (100%)


P
6 (100%) 6 (100%)
Mean 140.617 5.994 38.271
Min-Max 77.00-410.00 3.800-10.240 28.00-49.00

Tai Lake NoP 14 (100%)


P

Mean 192.309
Min-Max 109.840-2100.00

Difference among study areas (P=) 0.000


_______________________________________________________________________________________

61
______________________________________________________________________________________________________________________________________________
Tab. 10.6. Concentration of various elements in the feathers of Little Egrets. Values as in Tab. I.
______________________________________________________________________________________________________________________________________________
arsenic silver bromine cobalt cesium lanthanum nickel scandium selenium zinc
Pearl River Delta no. P 19 (100%) 14 (21%)
P
19 (100%) 19 (100%) 19 (100%) 19 (53%) 19 (21%) 19 (84%) 19 (74%) 19 (68%)
mean 0.243 0.0001 74.377 5.160 0.177 0.028 0.090 0.017 0.612 1.8
min-max 0.02-4.52 Nd-9.11 42.7-138.0 0.33-15.0 0.045-0.42 Nd-2.70 Nd-74.30 Nd-0.50 Nd-41.10 Nd-103

Poyang Lake no.P P


6 (100%) 6 (100%) 6 (100%) 6 (100%) 6 (100%)
mean 0.369 0.027 0.013 1.823 206.1
min-max 0.17-0.83 0.01-0.05 0.008-0.03 1.5-2.2 175-236

Tai Lake no. 14 (92%) 14 (100%) 14 (93%) 14 (21%) 14 (93%) 14 (93%) 14 (93%)
mean 0.001 0.189 0.020 0.070 0.011 1.338 79.6
min-max Nd-0.007 0.10-0.68 Nd-0.07 Nd-19.20 Nd-0.04 Nd-40.43 Nd-320

Difference among study areas (P=) 0.016 0.000 0.000 Ns 0.003 Ns Ns


______________________________________________________________________________________________________________________________________________

62
_______________________________________________________________________________________
Tab. 10.7 Concentration of cadmium, chromium, mercury, and lead in different prey types of Little Egrets.
Values as in Tab. I.
_______________________________________________________________________________________

cadmium chromium mercury lead

Poyang Lake Fish no. 4 4 4 4


mean 0.295 1.339 0.148 1.404
min-max 0.16-0.72 0.83-1.93 0.12-0.23 1.01-2.31

Insect larvae no.P 4 P


4 4 4
mean 0.002 0.018 0.0001 0.019
min-max 0.00003-0.17 0.0002-1.59 Nd-0.49 0.0002-1.44

Shrimp no.P 4 P
4 4 4
mean 0.028 0.208 0.004 0.115
min-max 0.00003-0.39 0.0004-3.83 Nd-0.15 0.0002-2.61

Tadpole,frog no.P 3 P 3 3 3
mean 0.002 0.265 0.001 0.295
min-max Nd-0.18 0.0001-12.64 Nd-0.11 0.0002-12.33

Tai Lake Fish, shrimp no. 3 2 2 2


mean 0.003 0.293 0.072 0.108
min-max Nd-9.00 0.19-0.44 0.05-0.11 0.11-0.11

Difference among study areas (P=) N.s N.s N.s N.s


_______________________________________________________________________________________

_______________________________________________________________________________________
Tab 10.8. Concentration of elements that may be responsible for toxicity at high doses, in different prey
types of Little Egrets. Values as in Tab. I.
_______________________________________________________________________________________
Iron Manganese Copper

Poyang Lake Fish no.


P 3 P 2 1
Mean 673.862 71.120 27.500
Min-max471.50-877.00 56.200-90.00

Shrimp no.
P 3 P 3 1
Mean 945.477 212.035 62.0
Min-max736.80-1317.00139.60-321.20

Tadpole and frog no. P 1 P


1
Mean 5290.0 104.3
Min-max

Tai Lake Fish and shrimp no.


P 5 (100%)
P

Mean 433.596
Min-max141.0-1500.0

Difference among study areas (P=)


_______________________________________________________________________________________

63
______________________________________________________________________________________________________________________________________________
Tab. 10.9. Concentration of other elements in prey of Little Egrets. Values as in Tab. I.
______________________________________________________________________________________________________________________________________________
arsenic silver bromine cobalt cesium lanthanum nickel scandium selenium zinc

Poyang Lake Fish no.


P P
2 3 2 3 3 3 3
mean 1.929 0.697 0.158 1.013 0.298 1.395 155.8
min-max 1.20-3.10 0.57-0.82 0.10-0.25 0.83-1.16 0.21-0.37 1.20-1.56 153-158

Shrimp no.
P 1
P
3 3 3 3 3 3
mean 0.660 0.869 0.161 1.485 0.338 1.077 83.7
min-max 0.82-0.94 0.13-0.20 1.40-1.59 0.30-0.36 0.87-1.27 81-88

Tadpole, frog no.P 1


P 1 1 1 1 1 1
mean 6.900 4.040 1.450 13.000 3.200 2.480 79.9

Tai Lake Fish, shrimp no.


P P 5 (20%) 5 (100%) 5 (100%) 3 5 (100%) 5 (100%) 5 (100%)
mean 0.00001 0.215 0.019 Nd 0.015 1.319 189.7
min-max Nd-0.002 0.10-0.45 0.01-0.04 0.007-0.03 0.47-2.25 163-238

Difference among study areas (P=) 0.004 0.006 N.s 0.004 N.s 0.004
______________________________________________________________________________________________________________________________________________

64
_______________________________________________________________________________________
Tab. 10.10. Concentration of cadmium, chromium, mercury, and lead in sediments. Values as in Tab. I.
_______________________________________________________________________________________
cadmium chromium mercury lead
Pearl River Delta Fish pond no. P 3 P 3 3 3
mean 0.537 11.798 0.155 25.779
min-max 0.40-0.63 10.47-13.20 0.14-0.18 23.2-28.2
Foraging area no. P 6 (100%)
P
6 (100%) 6 (100%) 6 (100%)
mean 0.355 8.524 0.131 20.311
min-max 0.07-0.58 7.14-11.70 0.10-0.28 15.19-26.88
Park no. P 2 P
2 2 2
mean 0.231 8.501 0.136 23.078
min-max 0.13-0.41 8.43-8.57 0.11-0.17 22.24-23.94
Poyang Lake Ricefields no. P 2 P 3 2 2
mean 0.251 32.425 0.096 24.753
min-max 0.21-0.30 31.99-32.73 0.09-0.11 24.10-25.43
Tai Lake Lake no. 2 2 2 2
mean 0.346 54.774 0.117 34.334
min-max 0.34-0.36 50.97-58.87 0.11-0.12 30.8-38.18
Difference among study areas (P=) N.s 0.007 N.s N.s
_______________________________________________________________________________________
_______________________________________________________________________________________
Tab. 10.11. Concentration of elements that may be responsible for toxicity at high doses, in sediments of
Little Egrets. Values as in Tab. I.
_______________________________________________________________________________________
Iron Manganese Copper
Pearl River Delta Fish pond NoP 2 P
1
Mean 45221.68 Nd
Min-max 40900-50000
Foraging area N o P 2 P
2
Mean 37580.05 11.53
Min-max 24100-58600 Nd-2770.0
Park NoP 1P 1
geo. Mean 31500.00 Nd
Min-max
Poyang Lake Ponds NoP P
1 1 1
geo. Mean 3.04 715.77 48.95
Min-,ax
Ricefields NoP 9 (100%)
P
9 (100%) 6 (100%)
geo. Mean 2.91 321.89 106.98
Min-max 2.50-3.46 222.3-362.3 52.34-217.7
Tai Lake Fish ponds NoP 6 (100%)
P

geo. Mean 40442.19


Min-max 34900-49830
Lake NoP 4 (100%)
P

geo. Mean 35301.08


Min-max 31500-39925
Difference among study areas (P=) 0.182

65
______________________________________________________________________________________________________________________________________________
Tab. 10.12. Concentration of other elements in sediments. Values as in Tab. I.
______________________________________________________________________________________________________________________________________________
arsenic silver bromine cobalt cesium lanthanum nickel scandium selenium zinc

Pearl River Delta Fish pond no. P P


2 2 2 2 2 2 2 2 2
mean 16.176 3.983 19.984 10.425 49.115 138.802 16.328 4.274 109.5
min-max13.70-19.10 3.16-5.02 19.2-20.8 10.4-10.45 48.15-50.10 114.0-169.0 15.5-17.2 3.74-4.89 79-151

Foraging area no. P P


2 2 2 2 2 2 2 2 2 2
mean 15.158 0.001 2.005 8.485 7.289 31.786 1.193 11.784 3.343 61.9
min-max 11.1-20.7 Nd-0.34 1.57-2.56 3.2-22.5 4.25-12.5 19.85-50.90 Nd-79.90 7.63-18.20 2.86-3.91 30-124

Park no. P P1 1 1 1 1 1 1 1 1 1
mean 25.4 Nd 1.810 3.720 4.430 1.955 61.800 8.620 2.397 106.0

Poyang Lake Ponds No


P P1 1 1 1 1 1 1 1
mean 17.100 11.533 1.560 45.633 10.267 5.023 49.3
Ricefields no. P 8 (100%)
P
7 (100%) 9 (100%) 9 (100%) 9 (100%) 9 (100%) 9 (100%)
mean 12.88 11.212 2.249 40.045 11.481 3.820 55.3
min-max 10.37-15.0 8.41-22.13 1.55-5.91 29.2-51.1 9.87-13.60 2.13-4.70 36-71

Tai Lake Ponds no. 6 (100%) 6 (100%) 6 (100%) 6 (100%) 6 (100%) 6 (100%) 6 (100%)
mean 0.00003 14.939 7.868 44.891 13.579 2.545 67.2
min-max Nd-0.0038 12.9-18.03 7.07-8.99 37.76-51.02 12.25-14.46 2.04-2.80 58-92

Lake no. 4 4 4 4 4 4 4
mean 0.001 15.197 7.478 63.451 12.835 3.1 131.4
min-max Nd-0.006 14.1-16.82 7.12-8.30 55.7-81.10 11.9-14.17 2.85-3.38 100-162

Difference among study areas (P=) N.s N.s N.s 0.000 N.s N.s N.s 0.007 0.021
______________________________________________________________________________________________________________________________________________

66
Evaluation of contamination levels by heavy metals and other inorganic elements
The number of samples analyzed so far, due to incomplete analysis by AAS, in several cases is still too
small for a meaningful test of statistical significance. We will discuss the concentration levels in relation
to the thresholds that may be harmful to the birds, and that may indicate alarming environmental pollution.
We will also try to evaluate the concentration levels found in China, in relation to the levels found in other
regions, and to the thresholds above which damage from contamination is suffered.
Cadmium. Birds naturally exposed to high levels of cadmium may have evolved greater tolerance to this
element than other bird species, thus it would be difficult to define critical levels of cadmium in tissues
that are applicable to all birds. Cadmium concentration in healthy wild birds vary widely among species
and among populations within species, with mean levels from 0,1 to 32 ppm wet weight in the liver, and
0,3 to 137 ppm ww in kidney. Cadmium concentrations of < 3 ppm dw in the liver and 8 ppm dw in
kidney are considered background concentrations for herons (Scheuhammer 1987), but there are no data
about thresholds levels in feathers or eggs and apparently birds do not transfer cadmium into eggs. Herons
generally do not accumulate cadmium. Grey herons in the Netherlands (Hontelez et al. 1992), Great bleu
herons in Washington and Idaho, (Blus et al. 1985) and Lake Erie, USA (Custer and Mulhern 1983), Little
Egrets from Camargue, France (Cosson et al. 1988), Cattle Egret from India (Husain and Kaphalia 1990),
Eastern Great White Egrets from central Korea (Honda et al. 1985), and Cattle Egrets from Baja
California, Mexico (Mora and Anderson 1995)were all within background concentration for liver and
kidney.
Concentrations previously found in healthy populations of Little Egret and of Night Heron in Italy (Tab.
VII) were similar to those we found in China, although our data for China refer to eggs, while the data
from Italy refer to feathers.
Lead. “Threshold” concentrations for lead poisoning can be defined according to the tissue concentration
at which measurable effects occur. Lead absorption may result in a range of sub-lethal effects or in
mortality. There are difficulties associated with relating tissue lead concentrations to effect. Different
threshold concentrations have been proposed by different authors and have often been chosen to reflect
slightly different things, with no standard definitions. However, tissue lead concentration in waterfowl,
corresponding to sublethal effect, are at least 2 ppm wet weight for liver, 10 ppm dry weight for bone, and
20 µ g/dl for blood. There are no data about thresholds levels in feathers or eggs.
Lead is mainly stored in calcareous tissues (Scheuhammer 1987, Cosson 1989). Methallothionein, a
metal-binding protein of liver and kidney, preferentially binds zinc and cadmium, and possibly other
heavy metals (Nordberg 1972, Osbornet al. 1979, Aaseth and Norseth 1986).
Lead concentrations within this background level were reported in liver of Grey herons in Netherlands
(Hontelez et al. 1992), Great blue herons in Washington and Idaho, USA (Blus et al.1985), Black-crowned
Night Herons along the Atlantic coast, USA (Custer and Mulhern 1983, Little Egrets from Camargue,
France (Cosson et al. 1988), Cattle Egret from India (Husain and Kaphalia 1990), Eatern Great Whit
Egrets from Central Korea (Honda et al. 1985) Great Blue Herons, Snowy Egrets and Cattle Egrets from
South Florida (Rodgers 1997).
The levels of lead we found in eggs from China are lower than those previously found in Little Egrets and
Night Herons in Italy (Tab. VII). Note that our data for China and for Pakistan refer to eggs, while the data
from Italy refer to feathers. We could not analyze feathers, because as mentioned before the amount of
feathers per sample was too small. Much higher lead levels were found in egret feathers near Hong Kong
by Burger and Gochfeld (1993).
Mercury. The concentration of mercury associated with reproductive failure varies by species (Ohlendorf
et al. 1978) and a critical mercury level in eggs has not been measured for any heron species. Mercury
concentration have been reported in heron eggs (for example by Faber and Hickey 1973, Blus et al. 1985,
Hothem et al. 1995, Custer et al. 1997), but are difficult to interpret. The levels of mercury we found in
eggs from China are relatively low, and well below concentration that appear detrimental to reproduction
(at least 2.5 ppm dw). Levels of mercury higher than ours were found in feathers of herons and egrets in
Italy (Tab. 8), in herons and egrets in Hong Kong (Burger and Gochfeld 1993), in adult Great Egrets from

67
Korea (Honda et al. 1986) and in young Cattle Egrets from New-York (Burger et al. 1992). These first two
studies sampled heronries near industrial areas. Concentrations similar to ours were found in eggs of Great
Blue Herons from two colonies in Washington and Idaho (Blus et al. 1982). One of the colony (Ft.Lewis)
was located in the vicinity of areas with severe heavy metals pollution, the other was selcted as the
“control” (Tab. 9).
The concentrations associated with sub-lethal or lethal toxic effects in fishes is in range of 5-10 ppm ww.
The values we found in fish (prey) from China are below this concentration (colony means = 0.072-0.148
ppm dw).
Arsenic. Arsenic has been rarely determined in aquatic animals. It is a toxic, non-essential element. The
concentrations found in wildlife range from non-detectable to 2.9 ppm ww. Therefore, the values we
found in tadpoles are rather high.
Copper, manganese, and iron. These elements are essential for life, and only become toxic at high doses.
Their absorption is regulated by homeostatic mechanisms (Friberg et al. 1986) Lead and cadmium have
unknown physiological roles. At high dose, heavy metals produce lethally toxic. At low doses, they can
cause sublethal toxic effects, such as slower reactions to stimuli or weight loss (Honda et al.1990) Toxic
effects of heavy metals are also related to their bioavailability (Graveland 1990), and to the organism’s
physiological status (Osborn 1979, Blomqvist et al. 1987, Krasowski and Doelma 1990). The interactions
between metals are very important as well. Lead, for example, interacts with calcium or phosporus
(Graveland 1990) and interactions between cadmium and copper, zinc or selenium are well known (Voogt
et al. 1980, Goede and Voogt 1985).
No data have been published about these metals in eggs or feathers of wild bird populations. The
concentrations of Copper associated with lethal toxic effects in a littoral decapod, Palaemon elegans, is
about 700 ppm (White and Rainbow, 1982). The levels of Copper we found in preys (shrimps) are below
these concentrations, but it’s difficult to define absolutely a body concentration range reflecting normal
conditions and to make comparisons because of interspecific variability. Variability in metal accumulation
strategies among organisms, and in the relative importance of the different metals in organisms sharing the
same metal accumulation strategy, makes it difficult the interspecific comparison of metal concentrations
even between closely related species (Moore and Rainbow, 1987; Phillips and Rainbow, 1988).
Selenium. Although selenium occurs in many different forms, most of the laboratory data used to derive
toxic threshold concentrations, were based on one highly toxic form, selenomethionine (oxidation state =
-2). Data were also used from the field, where selenomethionine is believed to be a major, but probably
not the sole, chemical form in the foods of birds. High selenium concentrations have not been documented
in herons. Background selenium concentration in livers of several species of birds from freshwater
averaged 4-10 ppm on d.w and normal egg concentrations were 1-3 ppm on d.w. Selenium concentrations
within this background level were reported in eggs and livers of Great Blue Herons from Lake Erie, USA
(Nims 1987) and in eggs of Black-crowened Night Herons and Great Egrets from California (Ohlendorf
and Marois 1990). Somewhat elevated selenium concentrations were found in Great Blue Heron eggs
from the Upper Missispi River, USA (mean = 3.1 ppm dw, Custer et al. 1997) and Indiana, USA (mean =
4.0 ppm dw, Custer et al. 1998), Grey heron (mean = 3.5 ppm dw) and Black-crowned Night Heron eggs
(mean = 5.9 ppm dw) from the Delta of the Danube (Fossi et al. 1984), Black-crowned Night Heron eggs
(colony means = 2.9-5.7 ppm dw) and Snowy Egret (colony means = 3.0-5.3 ppm dw eggs from San
Francisco Bay, California (Hothem et al. 1995).
The level we found in the feather are similar to values found for colonies in New-York, Delaware, Puerto
Rico and Egypt.
Threshold for tissue concentrations that seems to affect the health and reproductive success of freshwater
fishes is 4 ppm dw. The values we found in fish (prey) from China are below this concentration (colony
means = 1.319-1.395 ppm dw)
The concentrations of selenium we found in eggs are rather high, but still lower than the threshold that
may affect bird reproduction (about 3 ppm, but on wet weigth).
Zinc. Few data have been published about this metal in eggs of wild bird populations. The concentration
of zinc in the egg content of some Mediterranean species is in the range of 37.3-64.2 ppm on d.w.

68
Althought there were significant differences among the colony sites, the values we found in eggs and
feathers can be considered normal.
Death of the crustacean Palaemon elegans occurs when the zinc body content is about 200 ppm (White
and Raimbow, 1982), indicating that much of the extra accumulated zinc is still in metabolically available
form. This lethal accumulated body concentration contrasts markedly with the accumulated zinc
concentrations in barnacles that typically exceed 10,000 ppm, but are known to be in a detoxified form
and therefore not metabolically available (Rainbow, 1987). The levels of Zinc we found in preys (shrimps)
are below these concentrations.

_______________________________________________________________

Table 10.13. Concentrations of mercury, cadmium, and lead in


feathers of Little Egret and of Night Heron chicks, collected in Italy
in 1994. Figures are: geometric mean (ppm on dry weight), and range
in parentheses. From Fasola et al. 1998.
_______________________________________________________________
Mercury Cadmium Lead

Little Egret 2.587 0.635 4.522


(11 samples) (1.296-9.076) (0.360-1.505) (0.803-12.162)

Night Heron 1.982 0.553 3.361


(4 samples) (1.244-2.640) (0.400-0.862) (1.343-6.092)
_______________________________________________________________

_______________________________________________________________
Tab. 10.14. Concentrations of heavy metals in eggs of Great Blue Herons (ppm
on wet weight). Figures are: geometric mean (number of positive samples), and
range. Nd= no detected; Na= not analyzed. From Blus et al. 1982
_______________________________________________________________
_
Colony Year N copper zinc mercury arsenic

Handford 1981 4 1.18 (4) 5.78 (4) 0.17 (4) Na


0.65-2.71 5.30-6.37 0.11-0.37

1982 9 0.56 (9) 4.06 (9) 0.02 (6) Nd


0.45-0.76 3.59-5.68 Nd-0.10

Ft.Lewis 1982 30.46 (3) 3.87 (3) 0.06 (3) Nd


0.29-0.59 3.08-4.66 0.04-0.12
_______________________________________________________________

Sediments. The concentrations of arsenic, zinc, cadmium, mercury, lead, copper (samples from Pearl
river delta), cobalt (from foraging area and park of Pearl river delta), nickel (samples from foraging area
of Pearl river delta) and chromium we found in sediments are lower than critical levels used in the
Netherlands for contaminated soil. Copper, cobalt and nickel levels in the remaining part of the sediments
samples are below the critical level. Using as reference the more pragmatic Canadian method, the arsenic,
cobalt, nickel, silver, zinc lead, cadmium, copper and mercury levels we found both in Pearl river delta
sediment and in Tai lake sediment are lower than the trigger concentrations. Chromium concentration
from Tay lake samples and arsenic, cobalt, copper and chromium level we found in Poyang lake samples
are higher than the critical values. Finally cadmium, lead, mercury and zinc concentrations in sediments
from Poyang Lake were lower than the critical values.

69
11.
Heavy metal contamination
in the samples from Pakistan

Fasola Mauro, Boncompagni Eleonora


Dipartimento Biologia Animale, Università, Piazza Botta 9, I-27100 Pavia, Italy

Gandini Carlo
Dipartimento Chmica Farmaeutica, Università, Viale Taramelli, I-27100 Pavia, Italy

Orvini Edoardo
Dipartimento Chmica Generale, Università, Viale Taramelli, I-27100 Pavia, Italy

Ashiq Muhammad, Umar K. Baloch


Pakistan Agriculture Research Council, P.O. Box 1031, Islamabad 45500, Pakistan

The samples for chemical analysis of contaminants were collected from three study areas:
1. Karachi Harbour, studied in 2000, and expected to be subject to considerable urban and industrial
pollution.
2. Taunsa Barrage, studied in 2000, expected to be subject to pollution from agriculture.
3. Haleji Lake, studied in 1999, expected to be relatively unpolluted.
The egret ecology in these study areas are described in the preceding chapters. This chapter summarizes
and discusses the main results about the levels of heavy metals and of some other inorganic substance of
environmental concern. The rough data are listed in App. B. Further analyses of these results are being
devoted to publications in preparation.

Materials, analytical Methods and Data analysis


The types of materials, the analytical techniques, and the methods used for data analysis, were the same as
described in the chapter “Heavy metal contamination in samples from China”.

Contamination levels in the environment


The number of samples analyzed so far, due to incomplete analysis by AAS, in several cases is still too
small for a meaningful test of statistical significance. We will therefore simply discuss the concentration
levels in relation to the thresholds that may be harmful to the birds, and that may indicate alarming
environmental pollution.
Eggs. The contamination levels in the eggs are shown in Tab. I, II and III.
Selenium and iron were detected in all samples from the three study areas, arsenic and bromine in all
samples from Karachi and Taunsa, the only ones available, scandium in more than 70% and nichel in less
than 20 % of the samples.
There were significant differences in zinc, cadmium, and lead concentration between locations. The
highest levels of zinc occurred in Intermediate Egrets from Haleji and those of cadmium and zinc in Little
Egrets from Haleji. Althought there were significant differences among the study areas for these metals,
the differences were not great, except for zinc , and the values were very low.

70
Feathers. The contamination levels in the feathers of Little Egret chicks are shown in Tab. IV and V;
NAA results are the only ones available, pending the conclusion of the analyses.
There were significant differences in bromine, cobalt, cesium and copper concentration between locations.
The highest levels of bromine and cesium occurred in Little Egrets from Karachi, the highest levels of
cobalt in Little Egrets from Taunsa, and those of copper in Intermediate Egrets from Haleji. High
concentrations of iron were found in the samples from Karachi and Taunsa.

Prey. Contamination levels in the prey collected from the food of Cattle Egret chicks are shown in Tab.
VI, VII, VIII. Again, high concentrations of iron were found.
There were significant differences in chromium, mercury and lead concentration between the three
locations. The highest levels occurred in samples from Karachi.

Sediments. Contamination levels in the sediments collected in wetlands used by Little Egrets,
Intermediate Egrets and Cattle Egret as foraging areas around the colony are shown in Tab.
IX, X, XI
There were significant differences in bromine, cesium, lanthanium cadmium and mercury concentration
between the three locations. The highest levels of bromine, cesium, cadmium and mercury occurred in
samples of Karachi and those of lanthanium in samples from Taunsa.

_____________________________________________________________________________________
Tab. 11. 1. Concentration of the most hazardous heavy metals in the eggs. The values are: no. of samples.
(percentage frequency of samples with concentrations above the detection limits. only for samples with no.>5).
Geometric mean. maximum and minimum values. ppm on dry weight). Nd = no detected. Ns = non-significant.
_____________________________________________________________________________________
Cadmium Chromium Mercury Lead
Haleji lake Little Egret no. 8 (100%) 8 (100%)
Mean 0.167 0.45
Min-Max 0.06-0.43
0.29- 0.57

Intermediate Egret no. P P 8 (0%) 8 (100%) 8 (100%) 8 (25%)


Mean Nd 0.077 0.27 0.00003
Min-Max 0.06-0.10 0.14-0.53 0.000002-0.15

Karachi Little Egret no.P P 4 (0%) 4 (100%) 4 (100%) 4 (75%)


Mean Nd 0.17 0.16 0.004
Min-Max 0.04-0.66 0.14-0.17 0.000002-0.05

Taunsa Little Egret no.P 1P 1 1 1


Mean Nd
0.077 0.1993 0.18

Cattle Egret no.P 1


P 1 1 1
Mean Nd 0.06 0.03 0.11
Difference among study areas (P=) 0.022 Ns Ns 0.022
_____________________________________________________________________________________

71
_____________________________________________________________________________________
Tab 11.2. Concentration in eggs of elements that may be responsible for toxicity at high doses.
Values as in Tab. I.
_____________________________________________________________________________________
Iron Manganese Copper
Haleji lake Intermediate Egret no.
P 20 (100%)
P 14 (100%) 9 (100%)
Mean 95.92 1.702 11.133
Min-max 57.8-170.3 0.9-5.2 5.69-15.40

Little Egret no.P 8 (100%)


P

Mean 113.16
Min-max 87.9-172.0

Karachi Little Egret no.P 16 (100%)


P 17 (12%)
Mean 179.26 0.169
Min-max 76.4-741.0 Nd-3.30

Taunsa Cattle Egret no.P 10 (100%)


P 8 (0%)
Mean 119.45 Nd
Min-max 83.5-155.0

Little Egret no.P 4 (100%)


P
4 (0%)
Mean 151.90 Nd
Min-max 105.3-221.0
Difference among study area (P=) Ns Ns
_____________________________________________________________________________________

72
73
______________________________________________________________________________________________________________________________________________
Tab 11.3. Concentration of other elements of environmental concern in eggs . Values as in Tab. I.
______________________________________________________________________________________________________________________________________________

Arsenic Silver Bromine Cobalt Cesium Lanthanum Nickel Scandium Selenium Zinc

Haleji lake Little Egret no. 8 (100%) 1 8 (100%) 8 (100%)


Mean 0.043 0.0160 2.275 45.90
Min-max 0.02-0.10 1.7-3.4 25.9-65.9

Intermediate Egret no. 17 (100%) 14 (100%) 20 (100%) 20 (100%)


Mean 0.063 0.029 2.170 47.58
Min-max 0.03-0.16 0.02-0.04 1.00-3.46 29.8-90.8

Karachi Little Egret no. 18 (100%) 12 (8%) 18 (100%) 16 (44%) 16 (81%) 18 (28%) 16 (13%) 16 (94%) 16 (100%) 16 (63%)
Mean 0.035 0.000006 44.58 0.001 0.009 0.002 0.041 0.003 3.226 0.36
Min-max Nd-1.32 Nd-0.63 29.1-98.0 Nd-0.68 Nd-0.135 Nd-0.48 Nd-22.90 Nd-0.036 1.69-8.37 Nd-329.0

Taunsa Little Egret no. 4 (100%) 2 4 (100%) 4 (100%) 4 (50%) 4 (50%) 4 (0%) 4 (100%) 4 (100%) 4 (100%)
Mean 0.006 Nd 44.45 0.035 0.019 0.009 Nd 0.013 2.908 6.36
Min-max Nd-0.34 18.5-76.3 0.02-0.05 0.01-0.03 Nd-0.20 0.006-0.03 1.19-4.14 1.10-28.10

Cattle Egret no. 10 (100%) 7 (14%) 10 (100%) 10 (60%) 10 (100%) 10 (30%) 10 (0%) 10 (100%) 10 (100%) 10 (90%)
Mean 0.003 0.000014 10.24 0.002 0.013 0.003 Nd 0.007 2.580984 8.72
Min-max Nd-0.22 Nd-0.88 4.89-72.60 Nd-0.19 0.005-0.02 Nd-0.25 0.001-0.04 2.00-3.76 Nd-63.0

Difference among study areas (P=) Ns Ns Ns Ns Ns Ns Ns Ns Ns 0026


______________________________________________________________________________________________________________________________________________

74
_______________________________________________________________________________________
Tab 11.4. Concentration in feathers of elements that may be responsible for toxicity at high doses.
Values as in Tab I.
_______________________________________________________________________________________
Iron Manganese Copper

Haleji lake Intermediate Egret no. P 3


P 3 3
Mean 45.3 2.17 39.15
Min-max 41-54 1.1-5.3 10.23-88.76

Little Egret no.P 3


P 3 3
Mean 72.87 2.71 11.08
Min-max 43-120 1.6-4.9 6.15-16.52

Karachi Little Egret no.P P 11 (100%) 11 (9%)


Mean 541.7 0.16
Min-max 96-2130 Nd-36100

Taunsa Cattle Egret no.P P 13 (100%) 10 (10%)


Mean 636.8 0.15
Min-max 110-2070 Nd-5550

Little Egret no.P 3


P 2
Mean 233.33 Nd
Min-max 70-695

Difference among study area (P=) 0.014


_______________________________________________________________________________________

75
_______________________________________________________________________________________________________________________________________________
Tab. 11.5. Concentration of various elements in feathers. Values as in Tab. I.
_______________________________________________________________________________________________________________________________________________
Arsenic Silver Bromine Cobalt Cesium Lanthanum Nickel Scandium Selenium Zinc

Haleji lake Little Egret no. 3 3 3 3


Mean 0.13 0.011 1.711 154
Min-max 0.05-0.23 0.007-0.02 1.37-2.30 123-184

Intermediate Egret no. 3 3 3 3


Mean 0.05 0.005 1.154 214
Min-max 0.03-0.07 0.004-0.005 0.87-1.36 186-264

Karachi Little Egret no. 12 (100%) 12 (8%) 12 (100%) 12 (100%) 12 (83%) 12 (17%) 12 (0%) 12 (75%) 12 (83%) 12 (67%)
Mean 0.042 0.00001 65.89 7.25 0.07 0.002 Nd 0.004 1.438 3
Min-max Nd-2.62 Nd-1.36 40.2-96.4 2.59-15.9 Nd-0.57 Nd-1.80 Nd-0.39 Nd-23.2 Nd-1710

Taunsa Little Egret no. 3 1 3 3 3 3 3 3 3 3


Mean 0.014 Nd 22.22 9.10 0.0005 0.115 Nd 0.019 9.017 0.029
Min-max Nd-1.12 14.8-39.0 4.09-19.3 Nd-0.09 Nd-2.98 0.009-0.03 3.35-27.7 Nd-113

Cattle Egret no. 13 (100%) 9 (11%) 13 (100%) 13 (100%) 13 (85%) 13 (39%) 13 (8%) 13 (77%) 13 (100%) 13 (46%)
Mean 0.003 0.00001 21.95 8.47 0.05 0.008 0.035 0.006 7.46 0.17
Min-max Nd-1.23 Nd-5.05 10.5-37.0 5.98-15.5 Nd-0.40 Nd-1.46 Nd-113.0 Nd-0.498 3.18-21.7 Nd-428

Difference among study area2s (P=) Ns Ns 0.009 0.025 0.041 Ns Ns Ns Ns Ns


_______________________________________________________________________________________________________________________________________________

76
_______________________________________________________________________________________
Tab 11.6. Concentration of cadmium. chromium. mercury. and lead in different prey types. Values as in
Tab. I.
_______________________________________________________________________________________
Cadmium Chromium Mercury Lead

Haleji lake Shrimp Intermediate Egret no. P 3 P


3 3 3
Mean 0.05 0.26 0.12 0.30
Min-Max 0.04-0.07 0.24-0.27 0.10-0.14 0.19-0.63

Karachi Fish Little Egret no.P 3 P


3 3 3
Mean 0.10 16.54 0.57 4.62
Min-Max 0.07-0.13 10.55-24.91 0.53-0.64 3.59-6.37

Taunsa Insect Cattle Egret no.P 2 P


2 2 2
Mean 0.06 2.23 0.02 0.89
Min-Max 0.03-0.12 1.48-3.35 0.02-0.03 0.87-0.90

Difference among study area (P=) Ns 0.044 0.044 0.044


_______________________________________________________________________________________

_______________________________________________________________________________________
Tab 11.7. Concentration of elements that may be responsible for toxicity at high doses, in preys of Cattle
Egret. Values as in Tab I.
_______________________________________________________________________________________
Iron Manganese Copper

Taunsa Insect no.P 2P


2
Mean 1929.5 7.72
Min-max 1700-2190 Nd-1240.0

Fish no.P P1 1
Mean 1046.3 Nd
Min-max

Frog no.P P1 1
Mean 701.0 Nd
Min-max

Mice no. P 1 P
1
Mean 1620.0 Nd
Min-max
_______________________________________________________________________________________

77
______________________________________________________________________________________________________________________________________________
Tab. 11.8. Concentration of other elements in prey of Cattle Egrets. Values as in Tab. I.
______________________________________________________________________________________________________________________________________________
Arsenic Silver Bromine Cobalt Cesium Lanthanum Nickel Scandium Selenium Zinc

Taunsa Insect no. 2 2 2 2 2 2 2 2 2 2


Mean 0.03 Nd 29.04 1.45 0.37 1.90 Nd 0.68 1.98 71.50
Min-max Nd 25.10 1.38 0.35 1.63 0.58 1.13 28.40
0.71 33.60 1.53 0.39 2.21 0.79 3.49 180.00

Fish no. 1 1 1 1 1 1 1 1 1 1
Mean 1.35 Nd 15.30 0.97 0.23 0.45 Nd 0.16 2.76 78.00

Frog no. 1 1 1 1 1 1 1 1 1 1
Mean 0.40 Nd 12.60 0.67 0.28 0.62 Nd 0.26 2.09 77.90

Mice no. 1 1 1 1 1 1 1 1 1 1
Mean 0.54 Nd 10.90 1.51 0.35 1.15 17.10 0.51 2.92 51.50
______________________________________________________________________________________________________________________________________________

78
_______________________________________________________________________________________
Tab 11.9. Concentration of cadmium, chromium, mercury, and lead in sediments. Values as in Tab. I.
_______________________________________________________________________________________
Cadmium Chromium Mercury Lead

Karachi Ghas Bunder mud no. P 3 P 3 3 3


Mean 0.205 32.86 1.53 18.96
Min-Max 0.12-0.32 18.77-45.09 0.78-2.67 6.24-47.72

Taunsa Channel no. P 3 P 3 3 3


Mean 0.068 16.992 0.00001 4.18
Min-Max 0.06-0.09 15.77-19.15 Nd-0.020 3.84-4.61

Difference among study area (P=) 0.05 Ns 0.05 Ns

_______________________________________________________________________________________

_______________________________________________________________________________________
Tab 11.10. Concentration in sediments of elements that may be responsible for toxicity at high doses.
Values as in Tab I.
_______________________________________________________________________________________
Iron Manganese Copper

Karachi Channel no.P 2 P


2
Mean 40987 7.90
Min-max 37500-44800 0.0-1300.0

Mud no.P P
1 1
Mean 15900 Nd
Min-max
Max
Taunsa Channel no.P P
1 1
Mean 39100 2160.0
Min-max

Ponds no.P P1 1
Mean 36100 3760.0
Min-max
9
Ricefield no.P P1 1
Mean 38900 Nd
Min-max

Difference among study area (P=) Ns Ns


_______________________________________________________________________________________

79
______________________________________________________________________________________________________________________________________________
Tab 11.11. Concentration of other elements in sediments. Values as in Tab. I.
______________________________________________________________________________________________________________________________________________
Arsenic Silver Bromine Cobalt Cesium Lanthanum Nickel Scandium Selenium Zinc

Karachi Channel no. 2 2 2 2 2 2 2 2 2 2


Mean 11.94 0.001 15.91 20.34 9.80 27.53 54.25 13.27 3.16 102.74
Min-max 7.46-19.1 Nd-0.28 7.67-33.0 18.8-22.0 9.79-9.8 22.1-34.3 47.4-62.1 11.5-15.3 2.91-3.43 88.7-119.0

Mud no. 1 1 1 1 1 1 1 1 1 1
Mean 4.51 Nd 23.10 6.46 2.19 33.60 38.80 6.30 2.98 7.23

Taunsa Channel no. 1 1 1 1 1 1 1 1 1 1


Mean 4.12 Nd 4.51 12.30 4.05 94.40 Nd 15.80 8.47 54.80

Ponds no. 1 1 1 1 1 1 1 1 1
Mean 4.37 2.55 13.10 4.86 49.25 89.60 14.00 4.16 12.10

Ricefield no. 1 1 1 1 1 1 1 1 1 1
Mean 6.30 0.84 2.84 15.60 7.40 53.50 49.00 15.10 3.24 48.50

Difference among study areas (P=) Ns Ns 0.050 Ns 0.050 0.050 Ns Ns Ns Ns

______________________________________________________________________________________________________________________________________________

80
Evaluation of contamination levels by heavy metals and other inorganic elements
We try to evaluate the concentration levels found in Pakistan, in relation to the levels found in other
regions, and to the thresholds above which damage from contamination is suffered.

Cadmium. Birds naturally exposed to high levels of cadmium may have evolved greater tolerance to this
element than other bird species, thus it would be difficult to define critical levels of cadmium in tissues
that are applicable to all birds. Cadmium concentration in healthy wild birds vary widely among species
and among populations within species, with mean levels from 0,1 to 32 ppm wet weight in the liver, and
0,3 to 137 ppm ww in kidney. Cadmium concentrations of < 3 ppm dw in the liver and 8 ppm dw in the
Kidney are considered background concentrations for herons (Scheuhammer 1987), but there are no data
99about thresholds levels in feathers or eggs and apparently birds do not transfer cadmium into eggs.
Herons generally do not accumulate cadmium. Grey herons in the Netherlands (Hontelez et al. 1992),
Great bleu herons in Washington and Idaho, (Blus et al. 1985) and Lake Erie, USA (Custer and Mulhern
1983), Little Egrets from Camargue, France (Cosson et al. 1988), Cattle Egret from India (Husain and
Kaphalia 1990), Eastern Great White Egrets from central Korea (Honda et al. 1985), and Cattle Egrets
from Baja California, Mexico (Mora and Anderson 1995)were all within background concentration for
liver and kidney.
Concentrations previously found in healthy populations of Little Egret and of Night Heron in Italy (Tab.
VII) were higher to those we found in Pakistan.

Lead. “Threshold” concentrations for lead poisoning can be defined according to the tissue concentration
at which measurable effects occur. Lead absorption may result in a range of sublethal effects or in
mortality. There are difficulties associated with relating tissue lead concentrations to effect. Different
threshold concentrations have been proposed by different authors and have often been chosen to reflect
slightly different things, with no standard definitions. However, tissue lead concentration in waterfowl,
corresponding to sublethal effect, are at least 2 ppm wet weight for liver, 10 ppm dry weight for bone, and
20 µ g/dl for blood. There are no data about thresholds levels in feathers or eggs.
Lead is mainly stored in calcareous tissues (Scheuhammer 1987, Cosson 1989). Methallothionein, a
metal-binding protein of liver and kidney, preferentially binds zinc and cadmium, and possibly other
heavy metals (Nordberg 1972, Osbornet al. 1979, Aaseth and Norseth 1986).
Lead concentrations within this background level were reported in liver of Grey herons in Netherlands
(Hontelez et al. 1992), Great blue herons in Washington and Idaho, USA (Blus et al.1985), Black-crowned
Night Herons along the Atlantic coast, USA (Custer and Mulhern 1983), Little Egrets from Camargue,
France (Cosson et al. 1988), Cattle Egret from India (Husain and Kaphalia 1990), Eatern Great Whit
Egrets from Central Korea (Honda et al. 1985) Great Blue Herons, Snowy Egrets and Cattle Egrets from
South Florida (Rodgers 1997).
The levels of lead we found in eggs from Pakistan are lower than those previously found in Little Egrets
and Night Herons in Italy (Tab. VII). Note that our data for China and for Pakistan refer to eggs, while the
data from Italy refer to feathers. We could not analyze feathers, because as mentioned before. the amount
of feathers per sample was too small. Much higher lead levels were found in egret feathers near Hong
Kong by Burger and Gochfeld (1993).

Mercury. The concentration of mercury associated with reproductive failure varies by species (Ohlendorf
et al. 1978) and a critical mercury level in eggs has not been measured for any heron species. Mercury
concentration have been reported in heron eggs (for example by Faber and Hickey 1973, Blus et al. 1985,
Hothem et al. 1995, Custer et al. 1997), but are difficult to interpret. The levels of mercury we found in
eggs from Pakistan are relatively low, and well below concentration that appear detriment reproduction (at
least 2.5 ppm dw). Levels of mercury higher than ours were found in feathers of herons and egrets in Italy
(Tab. 8), in herons and egrets in Hong Kong (Burger and Gochfeld 1993), in adult Great Egrets from
Korea (Honda et al. 1986) and in young Cattle Egrets from New-York (Burger et al. 1992). These first two
studies sampled heronries near industrial areas. Concentrations similar to ours were found in eggs of Great

81
Blue Herons from two colonies in Washington and Idaho (Blus et al. 1982). One of the colony (Ft.Lewis)
was located in the vicinity of areas with severe heavy metals pollution, the other was selcted as the
“control” (Tab. 9).
The concentrations associated with sub-lethal or lethal toxic effects in fishes is in range of 5-10 ppm ww.
The values we found in fish (prey) from Pakistan (Karachi) are below this concentration ( 0.572 ppm dw).

Arsenic. Arsenic has been rarely determined in aquatic animals. It is a toxic, non-essential element. The
concentrations found in wildlife range from non-detectable to 1.35 ppm ww, and the maximum values
may be considered rather high.

Copper, manganese, and iron are essential elements that become toxic at high doses. Their absorption is
regulated by homeostatic mechanisms (Friberg et al. 1986) Lead and cadmium have unknown
physiological roles. At high dose, heavy metals produce lethally toxic. At low doses, they can cause
sublethal toxic effects, such as slower reactions to stimuli or weight loss (Honda et al.1990) Toxic effects
of heavy metals are also related to their bioavailability (Graveland 1990), and to the organism’s
physiological status (Osborn 1979, Blomqvist et al. 1987, Krasowski and Doelma 1990). The interactions
between metals are very important as well. Lead, for example, interacts with calcium or phosporus
(Graveland 1990) and interactions between cadmium and copper, zinc or selenium are well known (Voogt
et al. 1980, Goede and Voogt 1985).

Selenium. Although selenium occurs in many differnt forms, most of the laboratory data used to derive
toxic threshold concentrations, were based on one highly toxic form, selenomethionine (oxidation state =
-2). Data were also used from the field, where selenomethionine is believed to be a major, but probably
not the sole, chemical form in the foods of birds. High selenium concentrations have not been documented
in herons. Background selenium concentration in livers of several species of birds from freshwater
averaged 4-10 ppm on d.w and normal egg concentrations were 1-3 ppm on d.w. Selenium concentrations
within this background level were reported in eggs and livers of Great Blue Herons from Lake Erie, USA
(Nims 1987) and in eggs of Black-crowened Night Herons and Great Egrets from California (Ohlendorf
and Marois 1990). Somewhat elevated selenium concentrations were found in Great Blue Heron eggs
from the Upper Missispi River, USA (mean = 3.1 ppm dw, Custer et al. 1997) and Indiana, USA (mean =
4.0 ppm dw, Custer et al. 1998), Grey heron (mean = 3.5 ppm dw) and Black-crowned Night Heron eggs
(mean = 5.9 ppm dw) from the Delta of the Danube (Fossi et al. 1984), Black-crowned Night Heron eggs
(colony means = 2.9-5.7 ppm dw) and Snowy Egret (colony means = 3.0-5.3 ppm dw eggs from San
Francisco Bay, California (Hothem et al. 1995).
The concentrations of selenium we found in eggs are rather high, but still lower than threshold that may
affect bird reproduction (about 3 ppm, but on wet weigth). The level we found in the feather are similar to
values found for colonies in New-York, Delaware, Puerto Rico and Egypt.
Threshold for tissue concentrations that seems to affect the health and reproductive success of freshwater
fishes is 4 ppm dw. The values we found in fish (prey) from Pakistan (Taunsa) are below this
concentration (2.760 ppm dw)

Zinc. Few data have been published this metal in eggs of wild bird populations. The concentration of zinc
in the egg content of some Mediterranean species is in the range of 37.3-64.2 ppm on d.w. Althought there
8were significant differences among the colony sites, the values we found in eggs and feathers can be
considered normal.

Sediments. The concentrations of arsenic, zinc, cadmium, chromium and lead we found in sediments are
lower than critical levels used in the Netherlands for contaminated soil, while cobalt, nickel,
mercury and copper levels are higher. Using as reference the more pragmatic Canadian method, the
arsenic, cobalt, nickel, silver, zinc, cadmium, mercury and lead levels at both Karachi and Taunsa
were lower than the trigger concentrations. Only copper concentration in Taunsa sediment is above
the critical level.

82
12.
Contamination by organic compounds
in the samples from China

Ruiz Xavier, Sanpera Carolina , Jover Lluis, Llorente Gustavo


Departament. de Biologia Animal, Avgda. Diagonal 645, 08028-Barcelona , Spain

An Quiong
Institute of Soil Science, CAS, Nanjing 210008, P.R. China

The samples for chemical analysis of contaminants were collected from three study areas:
1. Pearl River Delta, Guangdong, studied in 2000, and expected to be subject to urban-industrial
pollution.
2. Tai Lake, studied in 2000, and expected to be subject to serious pesticide and heavy metal pollution
from both agriculture and industry. The samples were collected at the one colony located in the
Yuantouzhu Park near Wuxi, and surrounded by wetlands presumably exposed to high pollution from
agricultural and industrial activities.
3. Poyang Lake, Jiangxi, studied in 1999, and expected to be free of pollution. The samples were
collected at the colony close to the city of Gongquing, north of Nanchang. Despite being close to Lake
Poyang, the largest freshwater body and the most important site for waterfowl in China, and a NEPA
nature reserve, the area surrounding the Gonquing colony was intensively cultivated, therefore the
samples may reflect some exposure to agricultural pollution.
The egret ecology in these study areas are described in the preceding chapters. This chapter summarizes
and discusses the main results about the levels of organic contaminants. The rough data are listed in App.
C. Further analyses of these results are being devoted to the publications in preparation.
Sampling effort was mainly directed to collect eggs of the Little Egret, the most widespread egrets in the
region, from different areas. In addition, some Night Heron samples were collected in the Tai Lake study
area. The results on Egret’s diet (see chapters 4 and 5) indicate that Little Egrets feed mainly small fish
and shrimps (body size <5 cm), including Carassius auratus, Fluta alba, and Misgurnus anguillicaudatus.
The prey of the Night Heron is larger (up to 20-30 cm), and include C. auratus, Parabramis pekinensis,
Misgurnus anguillicaudatus, Fluta alba, Rana, Insecta, Crustacea and Rodentia.
The organochlorine compounds that were analysed include:
• Hexachlorobenzene (HCB). HCB is a fungicide used for seed grains and is an industrial waste
product from the manufacture of several chlorinated pesticides. It is also used in the manufacture for
tires, and it is present in the herbicide Dacthal and the fungicide pentachloronitrobenzene, and it is
persistent in the environment. (Wiemeyer, 1996).
• Hexachlorocyclohexanes (HCHs). This pesticide is also known as benzene hexachloride, and occurs
as three different isomers, α-, β-,and γ-. The γ- isomer, also known as lindane, is the most active
insecticide. Their major uses are on seed and livestock. Lindane is readily metabolised and excreted in
birds, minimally accumulated in the tissues, and without implication as a problem in the field
(Wiemeyer, 1996).
• Cyclodienes.
Heptachlor, heptachlor epoxide: Hepatchlor is an insecticide primarily used to control soil pests. This
pollutant is ready metabolised to heptachlor epoxide in vertebrates.

83
Endosulfan: Although is a member of the cyclodiene group, differs in properties and effects. The
technical grade consists of two isomers, α- and β-. Endosulfan is rapidly eliminated and does not
appear to accumulate in warm-blooded animals.
• Dichloro-Diphenil-Trichloroethanes (DDTs): pp’-DDT, pp’-DDE, pp’-DDD
DDT is an organochlorine with insecticidal properties, which came into wide agricultural use in the
late 1940s. Catastrophic population declines in certain bird species, notably raptors, and related
eggshell thinning were well documented after 1946. It was used extensively in agriculture, but their
use has been restricted in most countries, included Pakistan. Nevertheless, DDTs still can be found in
the formulation of other insecticides as Dicofol. Technical DDT, the insecticidal formulation applied
to the field, consists of several compounds that may be changed or broken down by a number of
physical or biological factors in the environment. Of these compounds, only pp’-DDT, pp’-DDD and
pp’-DDE have been related to adverse environmental problems. Birds of the Order Ciconiiformes
have been reported as very sensitive to DDE-induced eggshell thinning (Custer, 2000).
• Polychlorinated Biphenils (PCBs). These are a group of synthetic chlorinated aromatic
hydrocarbons. Since, 1930 PCBs have been in general use, having appeared in commercial products
including heat transfer agents, lubricants, dielectric agents, flame retardants, plasticizers, and
waterproofing materials. Their predominant use has been as insulating and cooling agents in closed
electrical transformers and capacitors because their low flammability. Environmental contamination
has resulted from several sources including industrial discharge, leaks from closed systems, disposal
from sewage treatment plants, and incomplete incineration of PCBs. There are 209 possible congeners
of PCBs and some of them could act as a catalyst for many mutagens and carcinogens (Custer, 2000).

Sample preparation and analytical methods


Tab. 12.1 details the samples collected in each of the study areas. In some cases prey samples analysed
corresponded to pooled composites.

_____________________________________________________________________________________
Tab. 12.1. Number of samples obtained in China for each study area during 1999 and 2000. In
parenthesis: no. of items in the composite samples.
_____________________________________________________________________________________
Tai Lake Poyang Lake Pearl River Delta

Eggs (Nest) Little Egret 24 (36) 19 (38) 10 (20)


Night Heron 3

Prey Fish 14 4 (8-12)


Shrimps 1 2 (5,8)
Fish and shrimp 1
Frogs 1 1 (3)
Tadpoles 2 (8,11)
Odonata 4 (2-11)

Sediments Pond 1
Rice field 9
Lake 4 2
Fishpond 6 3
Foraging area 6
_____________________________________________________________________________________

84
Once collected, whole eggs were frozen for later analysis. When more than one egg was collected from
the same nest, a mean value was computed for the nest, and was used for the statistics.
Samples of sediments were taken from different foraging areas used by the egrets, using a 30 cm depth
core. Tab. 12.1 indicates places where sediments were collected. Sediments were air-dried under field
conditions or, if available, in an oven (50º C) before being taken to the lab for analysis.
Prey samples corresponded to chick regurgitates. When possible prey samples were dried in an oven
(50ºC) before transport. When drying was not possible, prey samples were measured, weighed and
preserved in alcohol (60°) in the field. In the laboratory, prey items were classified and individuals of the
same species were pooled to obtain a composite sample. Chemical analysis was usually performed for
each prey type separately, but when this was not the case, the results are grouped in Tab. 12. 1.
Chemical analyses of organochlorines were done at the Laboratory of Toxicology (School of Veterinary
Science, Universitat Autònoma de Barcelona) following Mateo et al. (1998, 1999).
For the analysis, fish and egg samples were homogenised with anhydrous sodium sulphate, followed by
extraction with n-hexane and clean-up with sulphuric acid. The same procedure was used for sediment
samples, but without anhydrous sodium sulphate. PCBs#1 and #209 were used as internal standards. High
resolution chromatographic analyses and quantification of OC residues followed the corrected
Ballschmiter and Zell nomenclature system for PCBs (Guitart et al., 1993). Arochlor 1254 was used to
quantify PCBs reported. Recovery of selected pesticides and PCBs were calculated and considered
satisfactory (70%-100%), but no corrections were made based on recoveries. Blanks were processed
between samples to check the absence of external contamination.
In some eggs, eggshell thickness was measured using a DIGIMATIC counter (Mitutoyo). Accuracy of
measure was to the nearest 0.01 mm. In each eggshell, thickness was measured five times at the equator,
and the arithmetic mean was obtained.
For descriptive statistics, we computed geometric mean and ranges because of the skewed distributions
and those samples in which the compound was not detected were not included. The relationship between
organochlorines was assessed by non-parametric Spearman rho statistic; in this analysis non-detected data
were replaced by a value equal to half the detection limit. To compare mean eggshell thickness between
egg groups we used the non-parametric Mann-Whitney U-test.

Results
In Tab. 12.2 to 12.7, descriptive statisitics are provided for the concentrations of the contaminants in the
samples. Concentrations in the Little Egret eggs are expressed both on wet and on dry weight basis, in
order to allow a comparison with Night Heron eggs, for which only dry weight is reported. The small
sample size and the lack of the wet weight data for the Night Heron precluded further comparisons, and
thus, results and discussion sections are mainly devoted to the Little Egret.
Hexachlorobenzene (HCB). Levels of this pollutant in biota and sediments are shown in Tab. 12.2. HCB
has been detected in most egg samples, higher levels being found in Little Egret eggs from Tai Lake. All
the preys collected at the Poyang had HCB, but a low number of preys in Tai Lake presented this
pollutant. With regard to sediments, only those from the Poyang Lake had detectable quantities of HCB.
Hexachlorocyclohexanes (HCHs). HCH compounds were detected in a high proportion of egg samples
from Tai Lake and Pearl River Delta, whereas few eggs from the Poyang had levels above detection
limits. HCH concentration in eggs form Tai Lake and Pearl River Delta were quite similar.
These pollutants were detected in 26% of preys in Poyang samples and in a 58% in preys from Tai Lake.
The concentration in the sediments has shown to be highly variable (Tab. 12.3).
Cyclodienes. Tab. 12.4 lists the concentration of cyclodienes in biota and sediment. The eggs from Tai
Lake and Pearl River Delta presented similar levels and cyclodienes were detected in most of the samples,
whereas cyclodienes were found only in one egg from Poyang Lake, at a lower concentration. No
cyclodienes were detected in prey consumed by the Egrets in the Poyang, but these compounds were

85
present in almost all the prey collected at Tai Lake. With regard to sediments, higher levels were found in
samples from Tai Lake, followed by those of Poyang Lake and Pearl River Delta.
DDTs and its metabolites. Total DDT levels were similar in the egret eggs from the three areas, being
detected in almost all the samples analysed. DDTs were detected also in a high percentage of preys, higher
levels being attained by vertebrates, fish and tadpoles. Except for one sample taken in a pond at Poyang
Lake that exceeded 48 mg/kg, concentrations in the sediments were low.
As is shown in Tab. 12.6, most of DDT in the eggs corresponded to pp’-DDE, levels of this metabolite
being similar in all the egg samples. In the prey, higher pp’-DDE levels were found in fish and tadpoles.
The highest DDE levels were found in the sediments from Poyang Lake.
PCBs. PCB levels were higher in the eggs of egrets from Tai Lake, followed by egrets from Pear River
delta and Poyang Lake. No PCBs were detected either, in samples of prey or sediments collected at
Poyang Lake. Only vertebrate samples from Tai Lake had significant levels of PCBs. These pollutants
were detected in sediments from both Tai Lake and Pearl River Delta.

Pollutant ratios
In Tab. 12.8, descriptive statistics for groups of pesticide pollutants different from DDT, the sum of
pesticides, sum of organochlorines, and various ratios between pollutants by species and area are
provided.
Pesticide pollutants were detected in all the eggs analysed both, from the Poyang Lake and from Pearl
River Delta. Only one egg from Tai Lake had levels of pollutants below the limit of detection. The most
abundant pesticides were in all the cases DDTs, and in the Poyang and Pearl River Delta these were
present exclusively as the pp’-DDE congener. The proportion of PCBs was highest in Tai Lake and Pearl
River Delta than in Poyang Lake.

Comparison among the species


In egg samples form Tai Lake, a comparison has been carried out between Little Egrets and Night Heron.
The results from the Mann-Whitney test show that DDT levels are significantly higher in the Night Heron
(U= 4.00, p=0.008). The DDTs/PCBs ratio was higher also in this species (U= 7.00, p= 0.021).

Comparison among study areas


To compare pollutant levels among different areas, only eggs of Little Egrets have been considered. In
Fig. 12.1 to 12.6 are depicted the boxplots of egg concentrations (median, interquartile range, range
values and outliers) for different organochlorine compounds in the Little Egrets from the three areas.
Significant differences were found for HCB (X 2: 7.095, p=0.029) and HCH levels (X 2 : 6.856, p=0.032),
P P
P P

PCBs (X 2 : 21.281, p<0.001) and the ratios DDE/DDTs (X 2 : 19.026, p<0.001), DDTs/ΣPEST (X 2 : 35,974,
P P
P P
P P

p<0.001) and DDTs/PCBs (X 2 : 23.840, p<0.001).


P P

86
_____________________________________________________________________________________
Tab. 12.2. Concentrations of hexachlorobenzene HCB (ng/g) in the samples. The values are: number of
samples, percentage of samples with contaminants above detection limit, geometric mean concentration of
the contaminants, minimum an maximum values. All values are expressed as ppb, or ng/g on a dry weight
basis, but for eggs the values are expressed on a wet weight basis (w.w.) as well.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs
Poyang Lake Little Egret 19 74 18.0 (ww= 3.3) 1.0-6.5

Tai Lake Little Egret 24 96 30.6 (ww= 6.3 2.2-37.5


Night Heron* 3 100 36.2 17.0-93.0

Pearl River Delta Little Egret 10 100 31.1 (ww= 6.0) 3.0-10.3

Prey
Poyang Lake Fish 4 100 11.4 4.0-19.0
Shrimps 4 100 15.0 12.0-18.0
Tadpoles 2 100 18.5 18.0-19.0
Frogs 1 100 17.0 17.0-17.0
Odonata 4 100 28.7 14.0-61.0

Tai Lake Fish 14 29 6.7 3.2-16.9


Shrimps 1 0
Fish and shrimp 1 0
Frogs 1 100 7.7 7.7-7.7

Sediments
Poyang Lake Pond 1 100 1.3 1.3-1.3
Ricefield 9 89 1.6 1.3-2.0

Tai Lake Lake 4 0


Fishpond 6 0

Pearl River Delta Lake 2 0


Fishpond 3 0
Foraging area 6 0
_____________________________________________________________________________________

87
____________________________________________________________________________
Tab. 12..3. Concentrations (ng/g) of hexachlorocyclohexane compounds (HCHs), in the samples. Values
as in Tab. 12.2.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs
Poyang Lake Little Egret 19 ( 7) 37 51.9 (ww= 9.6) 4.6-18.3

Tai Lake Little Egret 24 (23) 96 92.0 (ww= 19.2) 3.2-91.8


Night Heron* 3 ( 2) 67 411.4 145.0-1167.0

Pearl River Delta Little Egret 10 (10) 100 97.3 (ww= 18.8) 10.3-38.4

Prey
Poyang Lake Fish 4 ( 1) 25 11.0 11.0-11.0
Shrimps 4 ( 1) 25 9.0 9.0-9.0
Tadpoles 2 ( 1) 50 10.0 10.0-10.0
Frogs 1 ( 0) 0
Odonata 4 ( 1) 25 14.0 14.0-14.0

Tai Lake Fish 14 ( 8) 57 8.7 2.1-37.2


Shrimps 1 ( 1) 100 6.7 6.7-6.7
Fish and shrimp 1 ( 0) 0
Frogs 1 ( 1) 100 5.9 5.9-5.9

Sediments
Poyang Lake Pond 1 ( 0) 0
Ricefield 9 ( 1) 11 0.9 0.9-0.9

Tai Lake Lake 4 ( 0) 0


Fishpond 6 ( 1) 17 26.2 26.2-26.2

Pearl River Delta


Lake 2 ( 0) 0
Fishpond 3 ( 1) 33 1.4 1.4-1.4
Foraging area 6 ( 1) 17 0.8 0.8-0.8
_____________________________________________________________________________________

88
_____________________________________________________________________________________
Tab. 12.4. Concentrations of cyclodiene insecticides in the samples. Values as in Tab. 12.2.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs
Poyang Lake Little Egret 19 ( 1) 5 1.8 (ww= 0.33) 0.3-0.3

Tai Lake Little Egret 24 (23) 96 77.0 (ww= 15.23) 2.9-56.7


Night Heron* 3 ( 1) 33 10.00 10.0-10.0

Pearl River Delta Little Egret 10 (10) 100 85.5 (ww= 16.55) 6.2-76.7

Prey
Poyang Lake Fish 4 ( 0) 0
Shrimps 4 ( 0) 0
Tadpoles 2 ( 0) 0
Frogs 1 ( 0) 0
Odonata 4 ( 0) 0

Tai Lake Fish 14 ( 1) 7 5.7 5.7-5.7


Shrimps 1 ( 1) 100 94.7 94.7-94.7
Fish and shrimp 1 ( 1) 100 19.5 19.5-19.5
Frogs 1 ( 1) 100 12.5 12.5-12.5

Sediments
Poyang Lake Pond 1 ( 1) 100 160.4 160.4-160.4
Ricefield 9 ( 0) 0

Tai Lake Lake 4 ( 1) 25 396.8 396.8-396.8


Fishpond 6 ( 5) 83 55.2 4.0-564.3

Pearl River Delta Lake 2 ( 0) 0


Fishpond 3 ( 1) 33 8.0 8.0-8.0
Foraging area 6 ( 1) 17 3.0 3.0-3.0
_____________________________________________________________________________________

89
_____________________________________________________________________________________
Tab. 12. 5. Concentrations of DDTs (sum) (ng/g) in the samples. Values as in Tab. 12.2.
_____________________________________________________________________________________
no.samples%contaminated mean min-max

Eggs
Poyang Lake Little Egret 19 (19) 100 3016.5 (ww= 547.8) 268.7-1443.6

Tai Lake Little Egret 24 (23) 96 2094.6 (ww= 426.1) 77.2-1081.7


Night Heron* 3 ( 3) 100 4497.4 3203.0-6801.0

Pearl River Delta Little Egret 10 (10) 100 2460.46 (ww= 475.09) 151.24-980.46

Pre
Poyang Lake Fish 4 ( 4) 100 66.9 38.0-111.00
Shrimps 4 ( 3) 75 10.3 9.0-11.0
Tadpoles 2 ( 1) 50 248.0 248.0-248.0
Frogs 1 ( 1) 100 8.0 8.0-8.0
Odonata 4 ( 1) 25 8.0 8.0-8.0

Tai Lake Fish 14 (13) 93 66.6 8.3-211.7


Shrimps 1 ( 1) 100 4.7 4.7-4.7
Fish and shrimp 1 ( 1) 100 18.2 18.2-18.2
Frogs 1 ( 1) 100 10.8 10.8-10.8

Sediments
Poyang Lake Pond 1 ( 1) 100 48632.0 48632-48632
Ricefield 9 ( 8) 89 3.5 1.5-9.7

Tai Lake Lake 4 ( 4) 100 2.4 0.8-6.0


Fishpond 6 ( 1) 17 0.7 0.7-0.7

Pearl River Delta Lake 2 ( 1) 50.0 1.4 1.4-1.4


Fishpond 3 ( 0) 0
Foraging area 6 ( 1) 16.7 2.7 2.7-2.7
_____________________________________________________________________________________

90
_____________________________________________________________________________________
Tab. 12.6. Concentrations of DDE (ng/g) in the samples. Values as in Tab. 12.2.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs
Poyang Lake Little Egret 19 19) 100 3002.5 (ww= 545.3) 263.1-1439.1

Tai Lake Little Egret 24 (23) 96 2011.2 (ww= 408.4 77.22-1077.8


Night Heron 3 ( 3) 100 4402.6 3178.0-6688.0

Pearl River Delta Little Egret 10 (10) 100 2321.9 (ww= 448.4 137.4-945.7

Prey
Poyang Lake Fish 4 ( 4) 100 62.8 38.0-94.0
Shrimps 4 ( 3) 75 10.3 9.0-11.0
Tadpoles 2 ( 1) 50 158.0 158.0-158.0
Frogs 1 ( 1) 100 8.0 8.0-8.0
Odonata 4 ( 1) 25 8.0 8.0-8.0

Tai Lake Fish 14 (13) 93 60.8 8.3-184.8


Shrimps 1 ( 1) 100 4.7 4.7-4.7
Fish and shrimp 1 ( 1) 100 18.2 18.2-18.2
Frogs 1 ( 1) 100 10.8 10.8-10.8

Sediments
Poyang Lake Pond 1 ( 1) 100 3165.0 3165.0-3165.
Ricefield 9 ( 8) 89 3.3 1.5-7.

Tai Lake Lake 4 ( 4) 100 2.1 0.8-4.8


Fishpond 6 ( 1) 17 0.7 0.7-0.7

Pearl River Delta Lake 2 ( 1) 50 1.4 1.4-1.4


Fishpond 3 ( 0) 0
Foraging area 6 ( 1) 17 1.0 0.9-0.9
_____________________________________________________________________________________

91
_____________________________________________________________________________________
Tab. 12.7. Concentrations of PCBs (sum) (ng/g) in different samples. Values as in Tab. 12.2.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs
Poyang Lake Little Egret 19 ( 9) 47 20.3 (ww=3.7) 1.0-35.7

Tai Lake Little Egret 24 (23) 96 393.0(ww= 79.0) 18.9-331.7


Night Heron 3 ( 3) 100 96.2 8.0-505.0

Pearl River Delta Little Egret 10 (10) 100 240.72 (ww= 46.5) 19.1-107.3

Prey
Poyang Lake Fish 4 ( 0) 0
Shrimps 4 ( 0) 0
Tadpoles 2 ( 0) 0
Frogs 1 ( 0) 0
Odonata 4 ( 0) 0

Tai Lake Fish 14 (11) 79 15.6 4.3-76.5


Shrimps 1 ( 0) 0
Fish and shrimp 1 ( 0) 0
Frogs 1 ( 1) 100 10.0 10.0-10.0

Sediments
Poyang Lake Pond 1 ( 0) 0
Ricefield 9 ( 0) 0

Tai Lake Lake 4 ( 4) 100 3.2 1.0-15.7


Fishpond 6 ( 2) 33 0.7 0.4-1.2

Pearl River Delta Lake 2 ( 2) 100 0.5 0.5-.5


Fishpond 3 ( 1) 33 0.8 0.8-.8
Foraging area 6 ( 6) 100 0.7 0.5-.9
_____________________________________________________________________________________

92
_____________________________________________________________________________________

Tab. 12.8 . Mean concentration (ng/g w.w.) of different organochlorines and ratios among different
pollutants in the eggs.
_____________________________________________________________________________________

Poyang Lake Tai Lake Pearl River Delta


____________ _________________________________________
Little Egret Little Egret Night Heron Little Egret

N (detec) 19 (19) 24 (23) 3 ( 3) 10 (10)


% detected 100 96 100 100

Mean ΣPEST (noDDTs) 4.7 45.8 155.8 45.6


Min 0.9 23.5 17.0 27.7
Max 24.8 160.5 1270.0 97.2

Mean ΣPEST 553.9 478.3 4853.3 531.3


Min 276.7 105.3 3378.0 214.7
Max 1445.8 1188.6 8071.0 1031.9

Mean ΣOCs 556.8 576.3 5090.2 580.3


min 284.4 192.33386.0 233.9
max 1445.8 1472.5 8291.0 1103.6

Mean ppDDE/DDTs 1.0 1.0 1.0 1.0


min 1.0 0.8 1.0 0.8
max 1.0 1.0 1.0 1.0

Mean DDTs/ΣPEST 1.0 0.9 1.0 0.9


min 1.0 0.7 0.8 0.7
max 1.0 1.0 1.0 1.0

Mean DDTs/PCBs 260.6 7.1 146.5 10.8


min 25.5 0.9 8.3 4.8
max 759.3 26.5 400.4 17.2
_____________________________________________________________________________________

93
40

30
HCB (ng/g)

20

10

0
N= 14 23 10

L.Poyang Lake TaiHu Shunde EP

Fig. 12.1. Boxplot of HCB (ng/g) in Little Egrets from the three areas under study.

100

80
SUM HCHs (ng/g)

60

40

20

0
N= 7 23 10

L. Poyang L.TaiHu Shunde EP

Fig. 12.2. Boxplot of HCHs (ng/g) in Little Egrets from the three areas under study.

94
80

SUM CYCLODIENES (ng/g)


60

40

20

0
N= 1 23 10

L.Poyang L.TaiHu Shunde EP

Fig. 12.3. Boxplot of ΣCyclodiene insecticides (ng/g) in Little Egrets from the three areas under study.

1600

1400

1200

1000
DDTs (ng/g)

800

600

400

200

0
N= 19 23 10

L. Poyang L. TaiHu Shunde EP

Fig. 12.4. Boxplot of ΣDDTs (ng/g) in Little Egrets from the three areas under study.

95
400

300
SUM PCBs (ng/g)

200

100

0
N= 9 23 10

L. Poyang L. TaiHu Shunde EP

Fig. 12.5. Boxplot of PCBs (ng/g) in Little Egrets from the three areas under study.

500

400

300
DDTs/PCBs

200

100

-100
N= 9 23 10

L. Poyang L.TaiHu Shunde EP

Fig. 12.6. Boxplot of the ratio DDTs/PCBs (ng/g) in Little Egrets from the three areas under study.

96
1600

1400

1200

1000

800

600
SUM PEST

400 (no DDTs) (ng/g)

SUM PEST
200
(ng/g)

0
SUM OCs

-200 (ng/g)
N= 19 19 19 23 23 23 10 10 10

L. Poyang L. TaiHu Shunde EP

Fig. 12.7. Boxplot of several pesticides (ΣPEST excluding DDTs, ΣPEST including DDTs and ΣOCs) in
Little Egrets from the three areas under study,

1,1

1,0

,9

,8

,7

ppDDE/DDTs

,6 DDTs/SUM PEST
N= 19 19 23 23 10 10

L. Poyang L. TaiHu Shunde EP

Fig. 12.8. Boxplot of several ratios (ppDDE/DDTs and DDTs/ ΣPEST) in Little Egrets from the three
areas under study

97
Female effect
In some nests of Little Egrets from different localities, more than one egg was taken to examine the female
effect. In the Poyang, five entire clutches were taken (4 clutches of 5 eggs and 1 clutch of 4 eggs). In Tai
Lake six nests were sampled taking three eggs per nest. In Pearl River Delta, two eggs were taken in each
of the ten nests sampled (see Tab. 12.1). The effect of the laying female on pollutant load in the eggs have
been analysed independently for each of the localities. The results of the analysis ANOVA are shown in
Tab. 12.9.
Only egrets from the Poyang have shown a significant effect of this factor, intraclutch variability being
lower than variability inter-clutches. No such effect was found in any of the other areas.
_____________________________________________________________________________________
Tab. 12.9. Results of the ANOVA analyses for the female effect on pollutant concentrations.
_____________________________________________________________________________________
F Sig.

Poyang Lake ΣDDTs 38.5 .000


ΣPCBs 10.6 .001
ΣPESTICIDES 38.1 .000
ΣOCS 36.4 .000

Tai Lake ΣDDT .31 .897


ΣPCB 2.5 .092
ΣPES .26 .929
ΣOCS 0.6 .715

Pearl River Delta ΣDDT 2.4 .098


ΣPCB 1.2 .403
ΣPES 1.6 .238
ΣOCS 1.6 .241
_____________________________________________________________________________________

Discussion
Hexachlorobenzene. The HCB is a fungicide used for seed treatment and also it is present as a
contaminant in other pesticides. It is not easily bio-degradated and tends to accumulate in sediments and
biota owing to its low octanol-water coefficient and low vapour pressure.
HCB levels in the eggs of Little Egrets from the three areas are significantly different (K-W test,
P=0.029), those collected at the Poyang Lake showing much lower concentrations than those collected
either at Tai Lake or Pearl River Delta, which in turn present quite similar values between them.
The levels in prey, seem to be quite surprising at a first glance, since HCB is present in all preys from
Poyang, but only in a few from Tai Lake. Furthermore, the levels accumulated in prey from Poyang were
higher than those in prey from Tai Lake.
The fact that sediments of Poyang presented detectable levels of this compound, while it is below the
detection limit at the other two sites indicates that sediments of Poyang accumulated higher quantities of
this organochlorine, suggesting that HCB pollution is higher in the whole aquatic compartment (sediment
and aquatic biota) at Poyang Lake, while it is higher for terrestrial secondary consumers at Tai Lake. Such
a situation can only be explained through differences in recent inputs of this pollutant to the aquatic
compartment, i.e., at the Poyang Lake the entering of HCB should have been more recent than at Tai
Lake, where almost all the compound has been already transfered to the upper levels of the food chain.

98
Hexachlorocyclohexanes. The hexachlorocyclohexanes are among the organochlorines showing
relatively higher solubilities and vapour pressures. They are readily metabolized and excreted in birds and
tend to be minimally accumulated in tissues (Blus et al. 1984). Both, percentages of detection and levels
of HCHs were similar in eggs of Little Egrets from Pearl River Delta and Tai Lake, and were significantly
lower in egret eggs from the Poyang Lake, following a trend very similar to that obtained for HCB (see
above). Levels in eggs of Night Herons from Tai Lake were 4 times higher than those of Little Egrets from
the same area. For prey items, concentrations were quite similar between Poyang and Tai Lake, but the
percentages of detection were much higher at Tai Lake, indicating a more recent pollutant input, as it is
also indicated by one of the sediment samples taken in a fish pond which presented levels much above the
others. Therefore, the results obtained for eggs also agree with this scenario, since birds at Poyang
presented lower levels probably because they have had more time to metabolize and excrete these
compounds since the last input in that ecosystem.

Cyclodienes. These compounds are amongst the most dangerous and persistent pesticides. Their levels are
very low at the Poyang Lake and only detected in one egg and in one sediment sample. None of these
compounds were detectable in preys from Poyang Lake. This indicates both, that the levels are low but
probably recent owing to a very localized source of pollution. Conversely, the levels at Tai Lake and Pearl
River Delta are higher and much more widespread for eggs, indicating more generalized and ancient
inputs of such pesticides at these areas. However, the fact that sediments of Tai Lake presented detectable
levels in 60% of the samples, while it was detectable in less than 20% of sediments from Pearl River Delta
indicates that at this area the input of cyclodienes was more ancient than at Tai Lake, where some
sediment samples still showed relatively high levels, which have not been yet transferred to the uppermost
level of the food chain, but are being incorporated by some of the intermediate levels (e.g. shrimps).

DDTs. DDTs, which are the main indicators of pollution deriving from agriculture treatments, were
widely distributed, being detected in most of the samples of either eggs, preys or sediments. Levels in
Egret eggs from the three areas did not show statistical differences and most of DDT corresponded to
DDE. These two facts are clear indicators of old, intense, generalized and persistent pollution by such
compounds. However, it is worth mentioning one sediment sample collected at Poyang lake which showed
extremely high levels of DDTs, most of them as p.p.’ DDT, i.e. the non-metabolized original molecule,
therefore indicating the recent input of that pesticide in the ecosystem, despite that it was officially banned
in China in 1982.
Their distribution among the different compartments follows well a biomagnification process model in
which the last pollutant input is relatively old, with most of the compound transferred to the uppermost
levels of the food chain. The only exception to this, belongs to Poyang Lake where some tadpoles might
accumulate high levels of DDTs. This can be explained because tadpoles feed on suspended sediments
bio-turbated by themselves, thus increasing greatly the bioavailability of the pesticide already trapped in
the sediment. The fact that most of the pollution accumulated by tadpoles is in the form of p.p.’ DDD, a
metabolite of DDT formed by bacteria living in anoxic environments (Matsumura 1992), confirms this
hypothesis. Also is to be noted that only 50% of tadpoles presented detectable levels, indicating that DDT
accumulation in sediments of Poyang Lake is far from being homogeneous, owing to recent inputs of such
pesticides at some places of the lake (see above).
At the other two localities it is important to note that, in average, levels at Pearl River Delta are higher
than at Tai Lake.

PCBs. These compopunds are the indicators of organochlorine pollution deriving from industrial sources.
Significant differences were found in the levels of PCBs and their detectability according to localities.
They reached very low levels in the eggs from Poyang, where only a 50% of the samples presented
detectable levels. In LakeTaihu eggs, the mean levels were about 20 times higher than at Poyang and ca.
double than at Pearl River Delta. At these two localities, moreover, PCBs were detected in almost all the
samples. The same trends were observed in sediment and prey samples, PCBs being undetectable at
Poyang. Therefore, the area most affected by “industrial” pollution in China according to our results (Tai

99
Lake) does not correspond to the area previously selected and supposed to be the most polluted by
industrial activity, i.e. the Pearl River Delta (Pearl River Delta).
When considering the ratio between DDTs and PCBs, it is worth note that values are quite similar for Tai
Lake and Pearl River Delta, whereas the ratio showed much more elevated values at Poyang, because of
dominance of DDTs over PCBs at this area, indicating a clear predominance of agricultural vs. industrial
pollutants.

Comparison with Pakistan and with other regions


This comparison will be based exclusively on egg pollution burdens, since heterogeneity of prey and
foraging areas precluded the use of other types of samples.
HCB. These compounds were only detected in samples from China and not in Pakistan. Levels in Little
Egret eggs from Chinese areas were quite similar (ca. 3-6 ppb) and very low, as it happened for the other
species analyzed, which showed narrow ranges (2-30 ppb). Levels in Little Egrets from the Danube delta
were much higher (487 ppb, Aurigi et al. 2000).

HCHs. Only our data and a single value for A. purpurea in Doñana (Alberto and Peña 1981) are available
for comparison. In all our areas the Little egret was the species attaining the higher levels of pollution by
such compounds. Levels in eggs of that species ranged from 10 ppb at Poyang to 50 ppb at Haleji Lake. In
ascending order (from low to high pollution) the areas were: Poyang -> Taunsa –> Pearl River Delta and
Tai Lake –> Haleji. Therefore, for such compounds the Poyang lake fits better the condition of low
pollution area than their corresponding area in Pakistan (i.e. Haleji lake). The fact that the levels in Little
Egret eggs, which feeds mainly in the seepage lagoons around Haleji (Ruiz et al. midterm report), are
higher than those found in eggs of E. intermedia from the same locality, which forages mainly inside the
lake, agrees well with the fact that only in one sediment sample from Haleji seepage lagoons, the HCHs
were also detected. In any case, the levels are very low in general and well below the dangerous exposure
to the toxicant (4000 to 37000 ppb ww). This is also the case for all the other species analyzed in the
different areas, e.g. E. gularis from Karachi, E. intermedia from Haleji, Bubulcus from Taunsa and
Phalacrocorax from Haleji.

Cyclodienes. Since there are only data from our samples, comparison with other areas is precluded.
The lower levels corresponded to the “pristine” areas in both countries, i.e. to the Poyang and Haleji (ND
to 1 ppb), intermediate levels in Little Egrets from agriculture and industry polluted areas in China: Pearl
River Delta and Tai Lake (ca. 15 ppb), and higher levels in egrets from areas devoted to agriculture
(Taunsa) and industrial activities (E.gularis from Karachi) in Pakistan (ca. 30 ppb). However, these levels
are far from those reported to have effects in birds, which are in the range of more than 1500 ppb, e.g. for
the eggs of the American Kestrel (Falco sparverius) (Henny et al. 1983)

DDTs. Little Egrets from the three areas in China present quite similar levels of these pollutants, but they
reach the highest levels in eggs from the supposed pristine area, that is, the Poyang lake, which in this case
exhibits levels about fivefold those of their counterpart in Pakistan (Lake Haleji). In fact, only the most
DDT polluted area among all those analyzed (Taunsa), showed higher average levels than the Poyang
lake. These levels are, however, below those reported for Little Egrets from the Ebro (Ruiz et al. 1991) or
the Danube (Aurigi et al. 2000) deltas. Also the levels are higher in the USA, according to data obtained
for eggs of E. thula from Texas (Mora 1996) or from San Francisco Bay. However, the levels reported for
Little Egrets in Italy by Fasola et al. (1998) are much lower. In any case, the levels reported in this study
seem to be well below the ranges showing adverse effects in bird reproduction (Blus 1996), despite that
significant eggshell thinning has been detected in one case for E. intermedia of Haleji lake (Sanpera et al.
in press).

100
PCBs. Excepting E. gularis from Karachi the levels we have found in the different areas and species are
low when compared to literature data (see Tab.). Poyang and Haleji fitted well to their condition of
pollution-free areas for these compounds (ca. 1-3 ppb), followed by Taunsa (20 ppb), Pearl River Delta
(46) and Tai Lake (78). Levels in Tai Lake are similar to Little Egrets from N Italy (Fasola 1998), E. thula
and E. tricolor from Texas (Mora 1996) and Night Heron from the Danube (Aurigi et al. 2000).
E. gularis from Karachi showed similar levels to those reported for Little Egrets and E. alba from the
Danube (Aurigi et al. 2000), but much lower than in Little Egrets from the Ebro Delta (Ruiz et al. 1991).
The levels reported in this study are much lower than those affecting embryo development or survival and
egg hatchability in different bird species, which used to be 5000 ppb ww or higher (Hoffman et al. 1996).

Concluding remarks
In China the Poyang lake area is characterized by lower impact of HCBs, HCHs, Cyclodienes and PCBs.
However, the egret eggs of that ecosystem showed the highest average levels of DDTs. Another
characteristic of Poyang Lake samples is their heterogeneity, since the percentage of samples containing
detectable levels for the different organochlorine families is very variable. This indicates that, even though
the ecosystem presented low levels of organochlorines, there are important local sources of pollution,
some of them responsible of recent inputs. Such heterogeneity is also responsible for the female effect
detected for organochlorine levels in eggs of Poyang, since the different individuals foraging at different
places can be exposed to very different levels of pollution, then each female layed eggs containing very
different burdens of organochlorines in relation to females using other feeding grounds.
At the Tai Lake area, the pollution is the highest for PCBs, indicating that this area, and not the Pearl river
Delta, is the one most affected by industrial pollution. Conversely, the levels of DDTs are somewhat
higher in Pearl River Delta. At both localities, the pollutants input seem to be older, much more
homogeneous (i.e. generalized) than at Poyang lake, as indicated by the percentage of samples having
detectable levels of the different organochlorine families. PCBs and DDTs excepted, these two areas
showed rather homogeneous levels of pollutants.
In general the levels found in the different areas included in this study are lower than those reported for
other areas of the world (Europe, USA) and below the observed ranges having adverse effects on bird
reproduction or survival.

101
13.
Contamination by organic compounds
in samples from Pakistan

Sanpera Carolina, Ruiz Xavier, Llorente Gustavo, Jover Lluis


Departament. de Biologia Animal, Avgda. Diagonal 645, 08028-Barcelona , Spain

Ashiq Muhammad, Umar K. Baloch


Pakistan Agriculture Research Council, P.O. Box 1031, Islamabad 45500, Pakistan

The samples for chemical analysis of contaminants were collected from three study areas:
1. Karachi Harbour, studied in 2000, and expected to be subject to considerable urban and industrial
pollution.
2. Taunsa Barrage, studied in 2000, expected to be subject to pollution from agriculture.
3. Haleji Lake, studied in 1999, expected to be relatively unpolluted.
The egret ecology in these study areas are described in the preceding chapters. This chapter summarizes
and discusses the main results about the levels of organochlorine compounds of environmental concern.
The rough data are listed in App. D. Further analyses of these results are being devoted to publications in
preparation.
The manufacture and the use of organochlorine compounds in developed nations has decreased
remarkably during the last three decades, but in some developing countries they are still used in the
treatment of agricultural pests and as insecticides for vectors of malaria. In tropical ecosystems the
environmental fate of these pollutants is affected by high temperatures and heavy rain, which increase the
dispersion rate (Iwata et al. 1994, Kannan et al. 1995). However, few data on organochlorine pollutants in
biota from tropical ecosystems have been published and, to our knowledge, no data are available from
wetlands in Pakistan.
Although initially sampling in different areas was thought to be directed mainly to the Little Egret , the
difficulties found for sampling nests of this species at some localities made that the sampling effort had to
be allocated on other ardeidae species. Thus, species analysed included Intermediate Egrets (Egretta
intermedia)., the dark morph of the Little Egret (designed by some authors as Western Reef Heron Egretta
gularis) , the Cattle Egret (Bubulcus ibis, and the Javanese Cormorant (Phalacrocorax niger)
The organochlorine compounds that were analysed are the same as for China (see the preceding
chapter).

Sample preparation and analytical methods


In Tab. 13.1 the samples collected for organochlorine analyses in each of the three areas of study, are
indicated. Note that prey sample analysed correspond to composites resulting from the pooling of several
prey items, as indicated. Fish prey collected in Haleji Lake correspond to four species, Oreochromis
niloticus (21 fish pooled in 2 samples), Puntius phuturio (38 fish pooled in 2 samples), Colisa lalia (10
fish pooled in 3 samples), Glossogobius giuris (n = 6) , and one indeterminate species of crustacean, a
caridean shrimp (29 shrimps pooled in 3 samples). Fish collected in the Karachi area corresponded to the
species Liza abu.
The sampling procedures, the chemical analytical techniques, and the data treatment were the same as
described for China (see the preceding chapter).

102
_____________________________________________________________________________________
Tab. 13. 1. Samples obtained for each area in Pakistan during the fieldwork campaigns of 1999 and 2000.
In parenthesis: no. of items in the composite samples.
_____________________________________________________________________________________
Haleji Lake Taunsa Karachi

Eggs (Nest) Little Egret 8 4


Intermediate Egret 22 (20)
Little Egret (dark morph) 28 (14)
Cattle Egret 10 (9)
Javanese Cormorant 4 (1)

Preys Fishes 16 1 (9) 3 (15)


Shrimps 2
Frogs 1 (10)
Mice 1 (5)
Coleoptera 1 (ind.)
Crickets 1 (20)

Sediments Pond 3
Rice field 3
Channel 3 6
Mud 3
Seepage lagoon 10
_____________________________________________________________________________________

Results
Descritive statistics for different pollutants are given in Tab. 13.2 to13.7. Concentrations are expressed in
ng/g. Concentration in the eggs is reported on a wet weight basis to allow comparison with other literature
data. Prey and sediment levels are given on a dry weight basis.

Hexachlorobenzene (HCB). Levels of this pollutant in the eggs were relatively low (Tab. 13.2), and
were similar in the egrets from Haleji and those from Karachi colony of the Little Egret (dark morph).
Levels in egrets form Taunsa were much lower. In both, prey and sediments, HCB was only detected in
samples from Haleji Lake (Tab. 13.2).

Hexachlorocyclohexanes (HCHs). Levels of HCHs in different samples are provided in Tab. 13.3. HCHs
were detected in most of the eggs (Tab. 13.3), but they were almost undetectable in both prey and
sediments (Tab. 13.3). The highest mean value for these pollutants was found in the Little Egret from
Haleji , although Intermediate Egrets from this area reached the maximum values. In the species from
Haleji, β-HCH was the most abundant isomer, whereas in Taunsa and Karachi it was the lindane (γ-HCH).

Cyclodienes. Cyclodiene values for different samples are given in Tab. 13.4. In the samples from Haleji,
these compounds were almost absent. Nevertheless, although at low levels they were detected in egg
samples from Taunsa and Karachi. Concentration in Egrets from both areas were quite similar, but Cattle
Egret from Taunsa had lower levels. Fish samples from Karachi present remarkably high concentrations
(Tab. 13.4).

103
In Intermediate Egrets from Haleji the most abundant cyclodiene was α-endosulfan. In Taunsa, heptachlor
epoxide levels were above the other cyclodienes, whereas in Karachi the most abundant was β-endosulfan.

DDTs. DDT compounds, mainly as pp’DDE, were found in all the egg samples analysed (Tab. 13.5 and
13.6). Mean levels were higher in Little Egrets from Taunsa, followed by the Western Reef Heron from
Karachi. Nevertheless, maximum values were found in Intermediate Egrets from Haleji. In prey, these
compounds were not detected in all the samples, highest values being found in fish (Tab. 13.5 and 13.6) .
Remarkably, no DDTs were detected in sediment samples from Taunsa (Tab. 13.5 and 13.6).

PCBs. With regard to PCBs, the highest values were detected in the eggs from Western Reef Heron from
Karachi colony (Tab. 13.7). Egret eggs from Taunsa present concentrations much lower, but above those
from Haleji. Prey samples from different localities present PCB concentrations which are quite similar
(Tab. 13.7). In sediments, the higher values were recorded in the Karachi area. No PCBs were found in
sediments from Haleji Lake (Tab. 13.7).

In Tab. 13.8, descriptive statistics for the different groups of pollutants (non-DDT pesticides, sum of
pesticides, sum of organochlorines and different pollutant ratios by area and species, are given.

Comparison between species from the same area. Statistical comparisons between species from the
same areas have been carried out for Little and Intermediate Egrets from Haleji Lake (Fig. 13.1) and the
only significant difference detected was in the HCHs levels, for which the Little Egret showed higher
concentrations (Mann-Whitney U=13, p= 0.013).
In Taunsa, significant differences between Little and Cattle Egret were found in both, DDTs (U= 3, p=
0,01) and PCBs (U= 5, p= 0,0365), no significant differences were found for the other pollutants (Fig.
13.2).

Comparison between the three areas. To compare different areas, only Egretta species were considered.
In Fig. 13.3 to13.7, boxplots (plotting the median, interquartile range and range excluding outliers) of
different pollutants in eggs from the study areas are depicted. Significant differences were found for HCB
levels (Kruskall-Wallis: Χ2= 17.062, p< 0.001), DDTs (Kruskall-Wallis: Χ2= 13,580, p=0.001), PCBs
(Kruskall-Wallis: Χ2= 27,450, p< 0.001), and also in the ratio ppDDE/Sum of DDTs (Kruskall-Wallis:
Χ2= 20,716, p< 0.001) and in the ratio DDTs/PCBs (Kruskall-Wallis: Χ2= 25,248, p< 0.001) (Figs. 13.8
and 13.9).

Female effect. In the colony of Western Reef Heron from Karachi, in which two eggs were sampled in
each nest the result of the ANOVA showed that there is a female effect on PCBs concentration in
the eggs (F= 3.813, p= 0.009) as well as on the final levels of organochlorine pollutants (F= 3.037,
p= 0.024).

104
_____________________________________________________________________________________
Tab. 13.2. Concentrations of hexachlorobenzene HCB (ng/g) in the samples. The values are: number of
samples, percentage of samples with contaminants above detection limit, geometric mean concentration of
the contaminants, minimum an maximum values. All values are expressed as ppb, or ng/g on a dry weight
basis, but for eggs the values are expressed on a wet weight basis (w.w.) as well.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs
Haleji Lake Little Egret 8 ( 6) 75 3.4 2.4-4.8
Iintermediate Egret 20 (16) 80 3.7 2.2-4.6
Javanese Cormorant 1 (1) 100 2.9 2.7-3.1

Taunsa Little Egret 4 ( 2) 50 0.5 0.4-.6


Cattle Egret 9 ( 4) 44 0.6 0.4-0.9

Karachi Little Egret (dark morph)14 (13) 93 2.1 1.1-6.8

Prey
Haleji Lake Fishes 16 (14) 88 11.5 1.8-59.7
Shrimps 2 ( 2) 100 5.7 5.6-5.7

Taunsa Fishes 1 ( 0) 0
Frogs 1 ( 0) 0
Mice 1 ( 0) 0
Coleoptera 1 ( 0) 0
Crickets 1 ( 0) 0

Karachi Fishes 3 ( 0) 0

Sediment
Haleji Lake Seepage lagoon 10 ( 6) 60 1.1 0.4-1.7

Taunsa Pond 3 ( 0) 0
Rice field 3 ( 0) 0
Channel 3 ( 0) 0

Karachi Channel 6 ( 0) 0
Mud 3 ( 0) 0
_____________________________________________________________________________________

105
_____________________________________________________________________________________
Tab. 13.3. Concentrations (ng/g) of hexachlorocyclohexane compounds (HCHs) in the samples. Values as
in Tab. 13.2.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs

Haleji Lake Little Egret 8 ( 6) 75 49.9 16.2-147.9


Intermediate Egret 20 (16) 80 7.7 0.2-1377.4
Javanese Cormorant 1 (1) 100 2.0 1.6-2.2

Taunsa Little Egret 4 ( 4) 100 17.6 4.4-39.9


Cattle Egret 9 ( 8) 89 4.8 2.1-37.6

Karachi Little Egret (dark morph) 14 (14) 100 9.1 3.3-91.5

Prey
Haleji Lake Fishes 16 ( 0) 0
Shrimps 2 ( 0) 0

Taunsa Fishes 1 ( 0) 0
Frogs 1 ( 0) 0
Mice 1 ( 0) 0 2
Coleoptera 1 ( 0) 0
Crickets 1 ( 1) 100 2.8 2.8-2.8

Karachi Fishes 3 ( 0) 0

Sediments
Haleji Lake Seepage lagoon 10 ( 1) 10.0 1.0 1.0- 1.0

Taunsa Pond 3 ( 0) 0
Ricefield 3 ( 0) 0
Channel 3 ( 0) 0

Karachi Channel 6 ( 0) 0
Mud 3 ( 0) 0
_____________________________________________________________________________________

106
_____________________________________________________________________________________
Tab. 13.4. Concentrations of cyclodiene insecticides (ng/g) in the samples. . Values as in Tab. 13.2.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs
Haleji Lake Little Egret 8 ( 0) 0
Intermediate Egret 20 ( 2) 10.0 1.6 0.7-3.6
Javanese cormorant 1 ( 0) 0

Taunsa Little Egret 4 ( 4) 100 26.7 7.8-151.0


Cattle Egret 9 ( 8) 89 9.5 1.4-49.4

Karachi Little Egret (dark morph) 14 (14) 100 33.0 12.1-98.1

Prey
Haleji Lake Fishes 16 ( 3) 19 3.9 0.7-10.5
Shrimps 2 ( 0) 0

Taunsa Fishes 1 ( 0) 0
Frogs 1 ( 1) 100 61.9 61.9-61.9
Mice 1 ( 0) 0
Coleoptera 1 ( 1) 100 10.6 10.6-10.6
Crickets 1 ( 1) 100 12.6 12.6-12.6

Karachi Fishes 3 ( 3) 100 227.7 146.2-349.5

Sediments
Haleji Lake Seepage lagoon 10 ( 0) 0

Taunsa Pond 3 ( 3) 100 7.0 0.7-67.7


Ricefield 3 ( 2) 67 7.8 5.9-10.3
Channel 3 ( 1) 33 1.3 1.3-1.3

Karachi Channel 6 ( 1) 17 1.4 1.4-1.4


Mud 3 ( 2) 67 1.2 1.1-1.3
_____________________________________________________________________________________

107
_____________________________________________________________________________________
Tab. 13.5. Concentrations of DDTs (sum) (ng/g) in the samples. Values as in Tab. 13.2.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs
Haleji Lake Little Egret 8 ( 8) 100 134.6 39.1-1884.7
Intermediate Egret 20 (20) 100 173.3 33.5-20982.9
Javanese Cormorant 1 (1) 100 31.7 20.9-38.9

Taunsa Little Egret 4 ( 4) 100 607.0 164.3-4202.5


Cattle Egret 9 ( 9) 100 68.7 25.4-2957.5

Karachi Little Egret (dark morph) 14 (14) 100 541.6 361.4-1064.6

Prey
Haleji Lake Fishes 16 ( 9) 56 23.6 7.6-149.3
Shrimps 2 ( 1) 50 16.6 16.6-16.6

Taunsa Fishes 1 ( 1) 100 78.4 78.4-78.4


Frogs 1 ( 1) 100 8.4 8.4-8.4
Mice 1 ( 0) 0
Coleoptera 1 ( 0) 0
Crickets 1 ( 0) 0

Karachi Fishes 3 ( 3) 100 32.1 29.6-34.4

Sediments
Haleji Lake Seepage lagoon 10 ( 3) 30 7.0 1.4-22.2

Taunsa Pond 3 ( 0) 0
Ricefield 3 ( 0) 0
Channel 3 ( 0) 0

Karachi Channel 6 ( 3) 50 2.3 0.4-7.5


Mud 3 ( 3) 100 26.8 5.7-127.4
_____________________________________________________________________________________

108
_____________________________________________________________________________________
Tab. 13.6. Concentrations of DDE (ng/g) in the samples. Values as in Tab. 13.2.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs
Haleji Lake Little Egret 8 ( 8) 100 133.9 39.1-1884.7
Intermediate Egret 20 (20) 100 166.5 29.6-20846.6
Javanese Cormorant 1 (1) 100 30.8 20.9-37.3

Taunsa Little Egret 4 ( 4) 100 526.4 161.0-3169.3


Cattle Egret 9 ( 9) 100 66.9 25.4-2329.7

Karachi Little Egret (dark morph) 14 (14) 100 477.7 319.2-983.7

Prey
Haleji Lake Fishes 16 ( 9) 56 13.8 2.0-149.3
Shrimps 2 ( 0) 0

Taunsa Fishes 1 ( 1) 100 69.3 69.3-69.3


Frogs 1 ( 1) 100 8.4 8.4-8.4
Mice 1 ( 0) 0
Coleoptera 1 ( 0) 0
Crickets 1 ( 0) 0

Karachi Fishes 3 ( 3) 100 10.1 9.3-11.1

Sediments
Haleji Lake Seepage lagoon 10 ( 3) 30 5.1 1.4-10.3

Taunsa Pond 3 ( 0) 0
Ricefield 3 ( 0) 0
Channel 3 ( 0) 0

Karachi Channel 6 ( 3) 50 0.9 0.4-2.0


Mud 3 ( 3) 100 5.8 1.3-22.7
_____________________________________________________________________________________

109
_____________________________________________________________________________________
Tab. 13.7. Concentrations of PCBs (sum) (ng/g) in the samples. Values as in Tab. 13.2.
_____________________________________________________________________________________
no.samples %contaminated mean min-max

Eggs
Haleji Lake Little Egret 8 ( 3) 38 1.6 0.9-4.6
Intermediate Egret 20 (15) 75 2.5 1.0-54.6
Javanese Cormorant 1 (1) 100 2.6 1.9-3.5

Taunsa Little Egret 4 ( 4) 100 20.7 7.3-131.9


Cattle Egret 9 ( 8) 89 5.3 1.2-258.0

Karachi Little Egret (dark morph) 14 (14) 100 853.8 492.1-1677.1

Prey
Haleji Lake Fishes 16 ( 2) 13 2.9 1.5-5.7
Shrimps 2 ( 1) 50 10.6 10.6-10.6

Taunsa Fishes 1 ( 1) 100 7.4 7.4-7.4


Frogs 1 ( 1) 100 6.5 6.5-6.5
Mice 1 ( 1) 100 6.0 6.0-6.0
Coleoptera 1 ( 1) 100 9.0 9.0-9.0
Crickets 1 ( 1) 100 6.8 6.8-6.8

Karachi Fishes 3 ( 3) 100 5.8 4.5-6.6

Sediments
Haleji Lake Seepage lagoon 10 ( 0) 0

Taunsa Pond 3 ( 3) 100 0.6 0.5-.0.9


Ricefield 3 ( 1) 33 0.5 0.5-.0.5
Channel 3 ( 3) 100 0.6 0.3-0.8

Karachi Channel 6 ( 4) 67 0.8 0.5-1.9


Mud 3 ( 2) 67 16.6 4.3-63.4
_____________________________________________________________________________________

110
_____________________________________________________________________________________
Tab. 13.8 . Mean concentration (ng/g w.w.) of different organochlorines and ratios among different
pollutants in the eggs.
_____________________________________________________________________________________

Haleji Lake Taunsa Karachi


_____________________________ ______________ __________
Little Intermediate Javanese Little Cattle Little Egret
Egret Egret Cormorant Egret Egret (dark morph)

N (detec) 8( 7) 20(19) 1(1) 4( 4) 9( 8) 14(14)


% detected 88 95 100 100 89 100
Mean ΣPEST (noDDTs) 37.5 11.7 4.9 48.9 16.5 47.7
Min 4.55 .22 4.66 12.22 6.94 21.34
Max 152.02 1377.43 5.10 174.81 87.83 183.24

N (detec) 8( 8) 20(20) 1(1) 4( 4) 9( 9) 14(14)


% detected 100 100 100 100 100 100
Mean ΣPEST 202.1 187.9 34.8 670.5 85.2 597.3
Min 43.66 33.50 20.87 206.94 27.80 386.25
Max 1934.55 22360.30 43.98 4377.25 3045.31 1119.26

N (detec) 8( 8) 20(20) 1(1) 4( 4) 9( 9) 14(14)


% detected 100 100 100 100 100 100
Mean ΣOCs 205.1 195.4 35.9 693.8 90.1 1462.3
min 48.21 38.54 20.87 220.58 27.80 950.02
max 1934.55 22360.30 43.98 4509.12 3303.33 2788.46

N (detec) 8( 8) 20(20) 1(1) 4( 4) 9( 9) 14(14)


% detected 100 100 100 100 100 100
Mean ppDDE/DDTs .99 .96 .97 .87 .98 .88
min .957 .827 .932 .754 .788 .763
max 1.000 1.000 1.000 .980 1.000 .959

N (detec) 8( 8) 20(20) 1(1) 4( 4) 9( 9) 14(14)


% detected 100 100 100 100 100 100
Mean DDTs/ΣPEST .72 .92 .91 .91 .81 .91
min .277 .659 .877 .794 .668 .802
max 1.000 1.000 1.000 .960 1.000 .951

N (detec) 8( 3) 20(15) 1(1) 4( 4) 9( 8) 14(14)


% detected 38 75 100 100 89 100
Mean DDTs/PCBs 40.5 117.5 14.4 33.3 16.9 .65
min 8.591 3.069 10.045 12.042 5.317 .350
max 67.600 519.300 18.818 53.045 30.013 .909
_____________________________________________________________________________________

111
3000

2000

SUMPEST (no DDTs)


(ng/g)
1000
SUMPEST
(ng/g)

SUMOCs
0 (ng/g)
N= 7 8 8 18 19 19
Egretta garzetta Egretta intermedia

Fig. 13.1. Boxplot of pesticides and organochlorines in Little Egret and Intermediate Egrets from Haleji
Lake.

5000

4000

3000

SUMPEST (no DDTs)


2000
(ng/g)

SUMPEST
1000 (ng/g)

SUMOCs

0 (ng/g)
N= 4 4 4 8 9 9

Egretta garzetta Bubulcus ibis

Fig. 13.2. Boxplot of pesticides and organochlorines in Little Egret and Cattle Egrets from Taunsa.

112
8

2
HCB (ng/g)

0
N= 22 2 13

Haleji Lake Taunsa Barrage Karachi Ghas Bunder

Fig. 13.3. Boxplot of HCB (ng/g) in egrets from the three areas under study.

200

150

100
sum HCHs (ng/g)

50

0
N= 22 4 14

Haleji Lake Taunsa Barrage Karachi Ghas Bunder

Fig. 13.4. Boxplot of HCHs (ng/g) in egrets from the three areas under study.

113
200

150
sum Cyclodiene pest. (ng/g)

100

50

0
N= 2 4 14

Haleji Lake Taunsa Barrage Karachi Ghas Bunder

Fig. 13.5. Boxplot of ΣCyclodiene Insecticides (ng/g) in egrets from the three areas under study.

5000

4000

3000

2000
sum DDTs (ng/g)

1000

0
N= 28 4 14

Haleji Lake Taunsa Barrage Karachi Ghas Bunder

Fig. 13.6. Boxplot of ΣDDTs (ng/g) in egrets from the three areas under study.

114
2000

1500

1000
sum PCBs (ng/g)

500

0
N= 18 4 14

Haleji Lake Taunsa Barrage Karachi Ghas Bunder

Fig. 13.7. Boxplot of PCBs (ng/g) in egrets from the three areas under study.

140

120

100

80

60

40
sum DDTs/PCBs

20

-20
N= 18 4 14

Haleji Lake Taunsa Barrage Karachi Ghas Bunder

Fig. 13.8. Boxplot of the ratio DDTs/PCBs in egrets from the three areas under study.

115
5000

4000

3000

2000 SUM PEST

(no DDTs) (ng/g)

SUM PEST
1000
(ng/g)

SUM OCs

0 (ng/g)
N= 25 27 27 4 4 4 14 14 14

Haleji Lake Taunsa Barrage Karachi Ghas Bunder

Fig. 13.9. Boxplot of several pesticides (ΣPEST excluding DDTs, ΣPEST, ΣOCs) in egrets from the three
areas under study.

1,2

1,0

,8

,6

,4

ppDDE/DDTs

,2 DDTs/SUM PEST
N= 27 27 4 4 14 14

Haleji Lake Taunsa Barrage Karachi Ghas Bunder

Fig. 13.10. Boxplot of several ratios (ppDDE/DDTs and DDTs/ΣPEST) in egrets from the three areas
under study.

116
Discussion
There is no information about the levels or the impact of persistent organic pollutants in the biota from
different wetlands in Pakistan, because, as far as we know, no previous works evaluating pollution in
organisms have been published. The present use of pesticides in Pakistan is concentrated on cotton fields,
which production is concentrated mainly in the Punjab and in the Sindh provinces, and to a lesser extent
in the Baluschistan. The pesticides applied are mostly insecticides against a number of pest species, e.g.
white fly, jassid, aphid and bollworms. Pesticides are also being used in other crops, such as vegetables
and fruit . Estimated figures on consumption of pesticides in Pakistan ranged from: 13,030 metric tons
estimated for 1990-91 to 30,471 metric tons in 1995-96 (source: STAT-USA on the internet, US
Department of Commerce). The results presented here constitute a first approximation to evaluate impact
of several organochlorine pollutants using wading birds as indicators.
In order to compare data gathered in the present work, organochlorine concentrations on the same or
related species from other areas have been used. In Tab. 13.9 information on organochlorines in eggs from
Ardeidae species from several localities have been compiled.

Haleji Lake. The two egret species sampled at Haleji Lake, the Little and the Intermediate egrets, present
few differences between them with regard to the levels of different pollutants (Tab. 13.10).
In both species, DDTs are the pollutants which attain the higher concentrations in eggs. The distribution of
these compounds in the area is thought to be wide, since they had been found in all the egg samples, thus
pointing to the ubiquity of DDTs in the Lake and in the egret’s foraging areas. Among DDTs, pp’-DDE
was the main isomer corresponding to the 99% of total DDTs in Little Egrets and 96% in Intermediate
Egrets. DDE concentrations in Egrets from Haleji were lower than reported elsewhere for eggs of large
herons, such as Great Blue Heron (Fitzner et al. 1988, Custer et al. 1997, 1998) , its values being the same
order of magnitude to those reported for other medium sized herons from the Mediterranean basin (Ruiz et
al. 1991, Fasola et al. 1998) and the United States (Mora, 1996, Rodgers 1997). Mean DDE levels found
in the eggs are much lower than levels reported by Blus et al. (1980) as having biological effects on birds
(< 2 mg/Kg ww) or by Custer et al. (1997) to impair avian reproduction in herons (10 mg/kg ww).
Nevertheless, the concentration in three eggs of Intermediate Egret were above these levels (2.27, 11.93
and 29.76 μg/g ww) and thus, some birds are exposed to high DDTs levels, probably while feeding in
agricultural areas or paddy fields. The two eggs with the higher levels belong to the same nest and reflect
an outstanding effect of the breeding female on the egg pollutant burdens, as has been described
previously by Pastor et al. (1995). We have also measured the eggshell thickness in these eggs and we
found them to be thinner than the other eggshells collected (Mann-Whitney U= 3.00, p= 0.013). Eggshell
thinning has been recognized as one of the main causes of reproductive failure in bird populations (Blus et
al. 1980, Furness 1993, Blus 1996).
DDE was also the main metabolite present in sediment samples. The high DDE/DDTs ratio in the eggs
suggest that exposure to DDTs has not been recent, indicating that DDT has been metabolised by the bird
or that DDT is mainly consumed as DDE.
Other organochlorines analysed in the eggs, as HCHs, HCB and PCBs follow in abundance to DDTs, but
their concentrations are low. Available data on HCH usage indicates a lower consumption of these
pesticides in Pakistan compared to neighbouring countries like India or China ( Kannan et al. 1992, Iwata
et al. 1994, Li et al. 1998), although long-range atmospheric transport could occur. The fact that no HCH
was detected in fish or sediment samples is in agreement with the findings of several authors (Iwata et al.
1994, Kannan et al, 1995) who reported a low accumulation of HCHs in aquatic organisms and sediments
pointing to the high temperatures of the tropics, and its higher solubility as the cause for the low levels of
semi-volatile contaminants in these compartments. Pastor et al. (1996), when studied transfer of organic
pollutants between different egg compartments in the Audouin’s gull (Larus audouinii ) found that HCHs
transfer from yolk sacs to embryos was lower than for other organic pollutants because of its higher
polarity.

117
The low levels of PCBs in the eggs of egrets from Haleji and the absence of these compounds in the fish
or sediment samples are indicators of the low industrial activity around the area, also suggesting that most
of the egrets are sedentary.
Sampling for the Javanese Cormorant was conducted on an opportunistic basis, and four eggs
corresponding to one whole nest were taken. All the pollutants analysed showed low concentrations, under
levels reported for other Phalacrocorax species from elsewhere (Custer et al. 1997, Custer et al. 1999,
Aurigi et al. 2000). In relation to Egrets from Haleji, the levels in cormorants are also remarkably low.
This might be due to the fact that cormorants forage on the lake bottom. Since Haleji is surrounded by a
stony desert, the main source of pollutants should be the atmospheric deposition. Therefore, most of them
should be retained by the huge amount of aquatic plants present on the lake surface, thus never reaching
the bottom of the lake and making bioavailavility of these compounds lower for benthonic animals on
which cormorants prey. Anyway, this hypothesis will remain untested until specific work addressed to
elucidate it is undertaken.

Taunsa. In the eggs of the two species sampled in this area (Little and Cattle Egrets) the higher
organochlorine levels corresponded to DDTs mainly DDE (87% in Little Egret and 98% in Cattle Egret).
These compounds were found in all the egg samples, thus indicating a wide distribution pattern. The two
species present differences, as the levels in the eggs of Little Egrets were eight times higher than in the
Cattle Egrets.
The DDE concentrations reported for eggs of Little Egrets from other localities show great variation,
probably related to local conditions, although Custer (2000) states that they are usually low?. Fasola et al.
(1998) found low DDE levels in egrets from N Italy, but Aurigi et al. (2000) found very high DDTs levels
in the same species inhabiting the Danube Delta. The results obtained by Ruiz et al. (1991) in the Ebro
Delta (Spain) for the same two species considered here show the opposite trend to what we have observed,
since levels in the Cattle Egret were ten times higher than those of the Little Egret. Possible reasons to
explain this difference remain unclear. Nevertheless, DDT levels in both egrets are in agreement with
observations made in their prey items. In fact, DDE is present in aquatic preys both, in fish and frogs
collected in Taunsa, but not in the insects sampled in the terrestrial media. Thus, observed differences
between both species should be related to their feeding habits since, while Little Egrets feed markedly on
fish, the Cattle Egrets show a feeding behaviour more dependent on terrestrial preys, including insects
(Cramp and Simmons 1977).
Among other factors which could contribute to the observed results, it should be considered the possibility
that in the terrestrial media DDTs remain immobilized in the soil during the drought period and thus, they
are unavailable to the insects during this period. Contrarily, in the aquatic environment dynamics of the
contaminant would be subjected to partition equilibrium dynamics between sediment and water, which
could explain in part their presence in the aquatic biota. Alternatively it should be considered that Egrets at
Taunsa can move to other places to forage, or that the egrets are partially migratory birds at this locality.
A similar problem was encountered with the other pollutants analysed. In the eggs cyclodiene compounds
were the second organochlorine pollutants in importance, followed by PCBs and HCHs. In all the cases a
marked difference exists between the two species, Little Egrets reaching always the higher concentrations.
It must be stressed that the results in prey and sediments deserve further study, as there is not a clear
agreement between pollutant levels in these samples and those in the eggs. The levels of PCBs in the eggs
are generally low compared to data reported in the literature (see Tab. 13.9) and doesn’t represent a risk
for the bird populations inhabiting this area.

Karachi. The Western Reef Heron sampled in the Karachi area, presents high levels of several
organochlorine pollutants, particularly PCBs and DDTs.
The concentration of DDT compounds in the eggs was high (GM= 542 ng/g ww), 88% of them
corresponding to DDE. Nevertheless, it must be pointed out that variability is relatively small (min: 361,
max: 1064) and thus, none of the samples present concentrations above levels associated to risk (>2 μg/g
ww, Blus et al. 1980). These compounds were detected also in the fish which constitute its prey, but DDE
percentage is then much lower, about one third, the rest corresponds mainly to pp’-DDD. Within the

118
sediments, mud has a much higher concentration compared to samples collected in the channel and in that,
only a fraction about 20- 40% was pp’-DDE, most of the compound being present as pp’-DDD. This
metabolite is formed in the soil owing to anaerobic bacteria (Matsumura 1975).
The PCBs are the organochlorines reaching the highest levels in this area. Their maximum concentrations
are found in the eggs (GM= 854 ng/g ww), and in lower quantities, they have been detected also in prey
and sediments. Egg concentrations are similar to those reported by Aurigi (2000) for Little Egrets from the
Danube Delta. These pollutants were detected in all the eggs and prey samples, pointing to a wide
distribution of PCBs in the Karachi area, probably related to discharging of untreated sewage waters, both
from industrial and domestic origin. The sensibility of birds to PCBs and their effects on bird reproduction
are highly variable between species, levels as low as 100 ng/g ww in the eggs from chickens have been
reported to decrease gluconeogenic enzyme activity in experimental conditions (Srebocan et al. 1977,
reported by Hoffman et al. 1996). Nevertheless, the levels of PCBs in Western Reef Heron eggs are lower
than the levels reported by Hoffman et al. (1996) to cause effects in other bird species in the field.
Both pollutants, DDTs and PCBs, as well as the sum of organochlorines, present a marked effect of the
female, that is, variability between eggs from the same nest (within component) is significantly lower than
between eggs from different nests (between component), indicating that just one egg per nest is enough to
evaluate the pollution level by these compounds.
The levels of cyclodiene insecticides are also moderately high, β-endosulfan being the main compound
involved in the egg’s pollution burden. These compounds have been identified in every egg and in all the
prey samples, but nothing could be said about, as their effects in birds and eggs remain largely unknown
(Wiemeyer, 1996).
Comparison between areas. Overall, the results show that Egret eggs reflect well the differences in
expected exposure to the different pollutants according to which the areas were choosen. Thus, Haleji
Lake, elected as the “pristine” area in Pakistan, showed significantly lower concentrations in average for
Cyclodienes, DDTs and PCBs than the other two areas, while Taunsa is characterized by a combination
of larger concentrations of Cyclodienes and DDTs with relatively low levels of PCBs, and the Karachi
harbour by relatively large concentrations of Cyclodienes, DDTs and very high concentartions of PCBs,
being the only area where such industrial organochlorines reach higher levels than the pesticide
compounds.
In contrast, the HCB levels, being very low in general, are significantly larger at Haleji and smaller at
Taunsa than at Karachi Harbour. The fact that only at Haleji, the sediments and prey presented detectable
levels of that compound, reveals that more or less recent inputs of such compound have taken place at this
site. HCB is used for fungicidal seed treatments, therefore, perhaps local population living around the lake
has used this compound to preserve seeds or foodstuff.
The average DDTs levels were higher in the eggs from Little Egrets collected at Taunsa and in Western
Reef Heron from Karachi colony, than in the Intermediate Egrets from Haleji. It must be taken into
account that Taunsa is an area mainly devoted to agriculture which probably received in the past high
inputs of pesticides and among them, DDTs. On the other hand, Karachi is at the tail-end of the surface
water supplies from the Indus. The city receives water which has been used for municipal, agricultural,
and industrial purposes, often several times. Moreover, none of the cities along the Indus River treat the
water before discharging it in the river (Rahman et al. 1997), thus agricultural pesticides are expected to
arrive through water supply and subsequent domestic sewage. The lack of farming activities around Haleji
would result in lower levels of pesticides reaching these waters, so, atmospheric transport would account
for most of the DDT presence in the area. Also, it must be pointed out that practically all DDT residues in
Haleji corresponded to pp’-DDE,
With regard to HCHs, no differences were found between different areas, and even higher concentrations
were attained by egret eggs from Haleji Lake. Carey et al. (1998, and references herein) stated that about
99,6% of HCHs applied to paddy fields in tropical agrosystems are volatilized to the atmosphere and
estimated than only 0,1% of the applied HCH was ultimately drained to the sea by the river. Kannan et al.
(1995) report that in spite of the recent use of HCH in some southeast Asian countries, as India, the
residue levels in fish are low, because of the rapid volatilisation of HCH isomers in tropical latitudes.

119
___________________________________________________________________________________________
Tab. 13.9. Levels of DDTs and PCBs in herons and egrets from different regions (literature data)
___________________________________________________________________________________________
N PP-DDE PP-DDD DDTs PCBs Source

Ardea alba Everglades. FL 6 80 40 <0.05 Rodgers1997


Ardea alba Lake Kissimee. FL 5 <0.05 <0.05 Rodgers 1997
Ardea cinerea Danube Delta 2 1285.2 283 Aurigi et al. 2000
Ardea herodias LLMadre.TX 10 735 396 Mora 1996
Ardea herodias British Colum.CAN 47 85 - 549 418 - 1220 Elliott et al. 1989
Ardea herodias Wa. USA 30 35 - 2220 139 - 15580 Speich et al. 1992
Ardea herodias Columbia.USA 38 3120 - 4710 nd - 490 1560 - 2240 Fitzner et al. 1988
Ardea herodias Marshes. USA 19 440 - 3610 nd - 1000 360 - 3340 Fitzner et al. 1988
Ardea herodias Puget. USA 3 1470 nd 3350 Fitzner et al. 1988
Ardea herodias Mississipi. USA 50 1310 14.9 3040 Custer et al. 1997
Ardea herodias Indiana. USA 10 1580 30 4900 Custer et al. 1998
Ardea herodias Oak Ridge 100 -240 Halbrook et al.1999
Ardea purpurea Ebro. Spain ? 1300 1400 3200 Ruiz et al. 1991
Ardea purpurea Doñana. Spain 3 2372 1704 Alberto & Peña 1981
Ardeola ralloides Ebro. Spain ? 200 200 500 Ruiz et al. 1991
Ardeola ralloides Macedonia. GR 20 3.8 nd Albanis et al. 1996
Cattle Egret Ebro D. Spain ? 2600 2800 3300 Ruiz et al. 1991
Cattle Egret Taunsa 10 66.9 68.7 5.3 Present study
Egretta alba Danube Delta 1 4764.5 785.8 Aurigi et al. 2000
Egretta caerulea Everglades. FL 6 340 <0.05 <0.05 Rodgers 1997
Egretta caerulea Lake Kissimee. FL 4 <0.05 <0.05 <0.05 Rodgers1997
Little Egret Italy 22 30 39 77 Fasola et al. 1998
Little Egret Ebro. Spain ? 600 800 2700 Ruiz et al. 1991
Little Egret Haleji 8 133.9 134.6 1.6 Present study
Little Egret Taunsa 4 526.4 607.0 20.7 Present study
Little Egret PoyangHu, China 38 545.28 547.83 3.71 Present study
Little Egret TaiHu, China 36 408.41 426.06 78.97 Present study
Little Egret Shunde EP, China 20 448.38 475.09 46.48 Present study
Little Egret Danube Delta 3 16939.7 764.59 Aurigi et al. 2000
Little Egret (dark) Karachi 28 477.7 541.6 853.77 Present study
Intermediate Egret Haleji 22 166.5 173.3 2.53 Present study
Egretta thula LLMadre.TX 4 249 78 Mora 1996
Egretta thula SFrancisco 50 824-3010 nd-246 185 - 5380 Hothem et al. 1995
Egretta tricolor LLMadre.TX 4 56 67 Mora 1996
Night Heron TaiHu, China 3 4402.63 4497.42 96.15 Present study
Night Heron Italy 7 14 41 4 Fasola et al. 1998
Night Heron Italy 20 82 90 Fasola et al. 1987
Night Heron Sfrancisco Bay 1591 466 - 5970 nd -25 603-4130 Hothem et al. 1995
Night Heron Green B. Wi 1? 2200 30 11000 Custer&Custer 1995
Night Heron Or/Wa. USA 14 400-4600 nd - 50 r: nd - 610 Blus et al. 1997
Night Heron Danube Delta 1 850.6 93.1 Aurigi et al. 20009
Phalacrocorax auritus Green B. Wi 3900 13600 Custer et al. 1999
Phalacrocorax auritus Green B. Wi 2220 13000 Custer et al. 1997
Phalacrocorax carbo Danube Delta 10 4340.01 527.6 Aurigi et al.2000
Javanese Cormorant Haleji 4 30.8 31.7 2.6 Present study
Phalacrocorax pygmaeus Danube Delta 4 3645.99 897.85 Aurigi et al. 2000
___________________________________________________________________________________________

120
_______________________________________________
Tab. 13.10 (ng/g)
_______________________________________________
Little Egret Intermediate Egret

DDE 134 166


DDTs 135 173
HCHs 50 8
HCB 3.44 3.66
Cyclodienes nd 1.6
PCBs 1.62 2.53
_______________________________________________

121
14.
Conclusions

TO BE EXPANDED

Contamination data show that concentration levels are generally lower than the threshold known to harm
wildlife, both for metals and other elements, and for organic compounds, with some exceptions. These
results are mostly welcomed, in that they testify a reduced environmental contamination.

122
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_________________________________________________________________________________________________________________________
Appendix A. List of samples collected in China (from Guandong in 2000, Poyang lake 1999, Wuxi 2000), and their content of metals and other
elements (ppm, on dry weight of the sample, nd: not detected, empty cells mean elements not analysed for that sample).
______________________________________________________________________________________________________________________________________________________________________________________________________________________________
Ordi Study Material Type Species Code Cad Mercu Lead Chro Cop Iron Manga Arse Sil Bro Co Ce Lantha Nic Scan Sele Zinc
nal area of mium ry mium per nese nic ver mine balt sium num kel dium nium
no. the
of sample
the
sample

1 Pearl River Egg albumen Little Eg. 02_2


2 Pearl River Egg albumen Little Eg. 03_1
3 Pearl River Egg albumen Little Eg. 320_2
4 Pearl River Egg albumen Little Eg. 322_2
5 Pearl River Egg albumen Little Eg. 97_2
6 Pearl River Egg Little Eg. 6 nd nd 209,300 0,173 55,100 0,352 0,035 nd nd 0,000 4,127 162,000
7 Pearl River Egg Little Eg. 20 nd nd 79,950 nd 54,400 0,076 0,027 nd nd 0,002 4,747 31,800
8 Pearl River Egg Little Eg. 27 nd nd 130,000 0,156 nd 13,500 0,052 0,020 0,059 nd 0,016 3,080 2,660
9 Pearl River Egg Little Eg. 02_1-ct nd nd 73,900 0,163 nd 20,870 nd 0,034 0,226 nd 0,005 1,997 37,400
10 Pearl River Egg Little Eg. 03_1 nd nd 91,450 0,602 28,900 0,010 0,033 0,313 nd 0,001 2,620 nd
11 Pearl River Egg Little Eg. 18_1 nd 0,352 0,049 nd nd 128,130 nd 74,700 0,078 0,027 0,105 nd 0,000 3,073 14,900
12 Pearl River Egg Little Eg. 18_2 nd 0,282 0,044
13 Pearl River Egg Little Eg. 220_1
14 Pearl River Egg Little Eg. 220_2
15 Pearl River Egg Little Eg. 314_1 nd nd 131,500 0,327 51,270 0,154 0,050 0,264 nd 0,001 3,587 91,100
16 Pearl River Egg Little Eg. 314_2
17 Pearl River Egg Little Eg. 318_1 nd nd 312,000 0,452 nd 67,700 0,222 0,086 nd nd 0,063 5,170 0,499
18 Pearl River Egg Little Eg. 318_2
19 Pearl River Egg Little Eg. 320_1 nd 1400,000 119,550 0,814 nd 50,700 nd 0,012 nd nd 0,001 4,197 54,300
20 Pearl River Egg Little Eg. 321_1 nd nd 129,750 0,828 22,400 0,035 0,011 nd nd 0,001 4,690 nd
21 Pearl River Egg Little Eg. 321_2
22 Pearl River Egg Little Eg. 322_1
23 Pearl River Egg Little Eg. 323_1 nd nd 67,900 0,312 0,846 9,660 nd 0,075 nd nd 0,007 4,007 18,500
24 Pearl River Egg Little Eg. 323_2
25 Pearl River Egg Little Eg. 35_1 nd 105,000 nd nd 95,667 nd 0,168 0,171 nd 0,002 5,953 nd
26 Pearl River Egg Little Eg. 35_2
27 Pearl River Egg Little Eg. 53_1 nd 53,300 0,427 nd 47,400 nd 0,033 0,158 0,002 2,083 35,600
28 Pearl River Egg Little Eg. 53_2
29 Pearl River Egg Little Eg. 59_1 nd 232,300 0,361 0,361 40,800 nd 0,066 0,365 nd 0,002 2,487 nd
30 Pearl River Egg Little Eg. 59_2
31 Pearl River Egg Little Eg. 68_1 nd nd 114,300 nd nd 64,000 nd 0,051 0,171 nd 0,000 4,587 20,200
32 Pearl River Egg Little Eg. 68_2
33 Pearl River Egg Little Eg. 97_1 nd nd 68,050 0,345 82,400 0,077 0,030 nd nd 0,001 2,790 nd
34 Pearl River Egg yolk Little Eg. 02_2
35 Pearl River Egg yolk Little Eg. 03_2
36 Pearl River Egg yolk Little Eg. 320_2
37 Pearl River Egg yolk Little Eg. 322_2 nd 274,000 nd nd 25,900 0,598 0,004 nd nd 0,007 4,040 556,000
38 Pearl River Egg yolk Little Eg. 97_2
39 Pearl River Feathers Little Eg. 2
40 Pearl River Feathers Little Eg. 3
41 Pearl River Feathers Little Eg. 4
42 Pearl River Feathers Little Eg. 6

133
43 Pearl River Feathers Little Eg. 7
44 Pearl River Feathers Little Eg. 8
45 Pearl River Feathers Little Eg. 18 nd nd 150,000 nd nd 138,000 7,590 0,424 nd nd nd 41,100 nd
46 Pearl River Feathers Little Eg. 20
47 Pearl River Feathers Little Eg. 27 nd nd 385,000 1,230 nd 85,000 3,930 0,259 nd nd nd 13,500 nd
48 Pearl River Feathers Little Eg. 35 nd nd 38,100 1,260 nd 55,600 2,470 0,045 nd nd nd nd nd
49 Pearl River Feathers Little Eg. 53 nd nd 350,000 0,773 nd 62,200 5,200 0,228 nd nd 0,120 1,580 817,000
50 Pearl River Feathers Little Eg. 59 12,500 nd 1090,000 nd nd 42,700 5,530 0,257 1,440 nd 0,106 4,890 1030,000
51 Pearl River Feathers Little Eg. 68 9,950 nd 575,000 nd 56,000 10,800 0,087 0,873 nd 0,035 2,800 38,200
52 Pearl River Feathers Little Eg. 97 15,700 nd 1553,000 1,290 71,000 6,870 0,061 0,441 53,300 0,019 3,500 983,000
53 Pearl River222 Feathers Little Eg. 220 nd nd 780,000 1,320 2,650 112,000 8,130 0,046 0,642 nd 0,090 1,690 4,390
54 Pearl River Feathers Little Eg. 314 nd nd 752,000 4,520 9,110 102,000 5,960 0,252 nd nd 0,111 nd 28,500
55 Pearl River Feathers Little Eg. 318 nd nd 236,000 1,670 74,500 12,200 0,254 1,800 nd 0,102 nd nd
56 Pearl River Feathers Little Eg. 320 29,400 nd 1120,000 2,820 77,500 7,790 0,135 0,545 74,300 0,105 2,580 131,000
57 Pearl River Feathers Little Eg. 321 14,000 nd 736,000 nd 64,600 6,050 0,274 nd nd 0,049 5,370 nd
58 Pearl River Feathers Little Eg. 322 nd nd 37,100 nd nd 91,700 9,120 0,269 nd nd 0,019 8,100 73,400
59 Pearl River Feathers Little Eg. 323 nd nd 850,000 nd nd 82,800 4,590 0,277 nd nd 0,060 8,750 2,670
60 Pearl River Feathers Little Eg. ***5 nd nd 238,000 2,830 nd 59,900 0,330 0,136 0,671 22,000 0,094 0,790 158,000
61 Pearl River Feathers Little Eg. **1 6,010 nd 1330,000 2,190 6,330 74,300 1,610 0,402 0,885 24,600 0,495 1,760 373,000
62 Pearl River Feathers Little Eg. 0_2 nd nd 675,000 nd nd 58,900 15,000 0,055 2,700 nd 0,265 nd nd
63 Pearl River Feathers Little Eg. 0_3 17,800 nd 4200,000 2,270 nd 46,800 5,520 0,340 nd nd 0,132 nd 119,000
64 Pearl River Feathers Little Eg. 0_6 nd nd 540,000 nd nd 132,000 4,310 0,410 0,646 nd 0,084 22,600 13,000
65 Pearl River Sediment Fish ponds -5 0,400 0,179 26,186 105,000 nd 50000,000 19,100 3,160 20,800 10,450 48,150 169,000 17,200 4,885 79,400
66 Pearl River Sediment Fish ponds -6 0,616 0,144 28,197
67 Pearl River Sediment Fish ponds -1 0,626 0,144 23,202 93,400 40900,000 13,700 5,020 19,200 10,400 50,100 114,000 15,500 3,740 151,000
68 Pearl River Sediment Foraging area -2 0,485 0,114 25,074 95,700 2770,000 58600,000 20,700 nd 2,560 22,500 12,500 50,900 79,900 18,200 3,908 124,000
69 Pearl River Sediment Foraging area -3 0,469 0,124 26,876
70 Pearl River Sediment Foraging area -4 0,537 0,277 22,520
71 Pearl River Sediment Foraging area -9 0,073 0,096 15,982 48,600 nd 24100,000 11,100 0,344 1,570 3,200 4,250 19,850 nd 7,630 2,859 30,900
72 Pearl River Sediment Foraging area -10 0,388 0,125 19,060
73 Pearl River Sediment Foraging area -11 0,575 0,107 15,186
74 Pearl River Sediment Park -7 0,131 0,172 23,944 49,300 nd 31500,000 25,400 nd 1,810 3,720 4,430 1,955 61,800 8,620 2,397 106,000
75 Pearl River Sediment Park -8 0,407 0,108 22,243
76 Poyang Lake Egg Little Eg. Eg1-1 nd 1,460 0,122 0,970 127,600 0,100 2,390 63,000
77 Poyang Lake Egg Little Eg. Eg100-27 nd 1,320 2,149 217,800 0,110 4,860 60,600
78 Poyang Lake Egg Little Eg. Eg103-28 nd 0,797 0,159 0,730 113,900 0,098 2,900 78,000
79 Poyang Lake Egg Little Eg. Eg105-29 nd 0,883 0,156 0,260 109,660 0,070 4,300 57,500
80 Poyang Lake Egg Little Eg. Eg106-30 nd 0,813 0,133 0,990 132,100 0,160 2,500 54,300
81 Poyang Lake Egg Little Eg. Eg109A-31 nd 0,587 90,200 2,700 0,110 0,350 0,027 2,050 55,100
82 Poyang Lake Egg Little Eg. Eg109B-32 104,800 0,090 3,650 121,100
83 Poyang Lake Egg Little Eg. Eg109C-33 106,400 0,060 0,018 3,500 59,050
84 Poyang Lake Egg Little Eg. Eg109D-34 0,550 103,200 0,081 3,100 47,370
85 Poyang Lake Egg Little Eg. Eg109E-35 0,057 0,389 0,523 133,000 0,090 1,970 48,700
86 Poyang Lake Egg Little Eg. Eg10A-15 nd 0,593 0,300 141,600 0,090 2,300 51,700
87 Poyang Lake Egg Little Eg. Eg10B-16 126,000 3,200 0,140 0,030 0,032 3,050 61,000
88 Poyang Lake Egg Little Eg. Eg10C-17 16,900 125,000 2,500 0,160 0,034 0,038 3,420 60,600
89 Poyang Lake Egg Little Eg. Eg10D-18 0,477 7,500 143,000 3,200 0,210 0,045 0,045 3,640 71,400
90 Poyang Lake Egg Little Eg. Eg10E-19 0,090 0,574 0,280 156,000 2,700 0,170 0,034 0,027 3,330 66,000
91 Poyang Lake Egg Little Eg. Eg11-20 nd 1,207 0,083 1,550 96,200 0,096 2,900 58,200
92 Poyang Lake Egg Little Eg. Eg111-36 nd 2,131 0,087 0,930 95,100 0,070 4,900 54,000
93 Poyang Lake Egg Little Eg. Eg115-37 nd 0,892 0,093 0,760 113,400 0,089 2,300 50,600
94 Poyang Lake Egg Little Eg. Eg123-38 nd 0,884 0,077 161,300 0,110 2,250 54,400
95 Poyang Lake Egg Little Eg. Eg13-21 nd 0,621 0,091 111,000 0,110 0,009 2,700 51,000
96 Poyang Lake Egg Little Eg. Eg15A-22 nd 0,001 31,600 120,000 2,100 0,120 0,035 0,034 3,750 49,100
97 Poyang Lake Egg Little Eg. Eg15B-23 15,400 98,000 1,700 0,110 0,029 4,250 52,100
98 Poyang Lake Egg Little Eg. Eg15C-24 105,000 1,300 0,130 0,034 0,026 3,710 48,100
99 Poyang Lake Egg Little Eg. Eg15D-25 0,315 4,800 108,000 1,700 0,150 0,028 0,028 3,690 61,500
100 Poyang Lake Egg Little Eg. Eg18-26 nd 0,532 2,333 1,000 114,500 0,095 2,400 43,400
101 Poyang Lake Egg Little Eg. Eg2A-2 nd 0,479 11,800 0,110 0,020 0,027 2,030 52,800

134
102 Poyang Lake Egg Little Eg. Eg2B-3 17,100 3,500 0,180 0,025 0,027 2,370 54,100
103 Poyang Lake Egg Little Eg. Eg2C-4 14,900 2,400 0,083 0,029 2,260 62,000
104 Poyang Lake Egg Little Eg. Eg2D-5 0,217 18,500 113,000 2,240 0,084 0,027 0,028 2,420 55,200
105 Poyang Lake Egg Little Eg. Eg2E-6 0,093 0,467 0,109 11,400 95,400 2,430 0,097 0,032 0,032 2,430 55,300
106 Poyang Lake Egg Little Eg. Eg3-7 nd 0,898 0,133 0,860 120,200 0,160 2,240 163,200
107 Poyang Lake Egg Little Eg. Eg5A-8 nd 0,522 148,000 2,960 0,250 0,033 0,034 2,960 62,300
108 Poyang Lake Egg Little Eg. Eg5B-9 113,000 3,400 0,170 0,021 0,033 3,590 65,100
109 Poyang Lake Egg Little Eg. Eg5C-10 80,000 3,200 0,120 0,033 0,030 2,970 54,200
110 Poyang Lake Egg Little Eg. Eg5D-11 0,298 11,800 124,000 3,700 0,150 0,046 0,029 4,000 51,900
111 Poyang Lake Egg Little Eg. Eg5E-12 0,185 1,010 0,100 10,800 108,000 3,200 0,150 0,033 0,032 3,290 58,900
112 Poyang Lake Egg Little Eg. Eg8-13 nd 0,909 0,100 0,700 98,600 0,120 0,020 2,300 49,600
113 Poyang Lake Egg Little Eg. Eg9-14 nd 0,532 0,124 0,550 190,000 0,300 0,015 2,000 87,500
114 Poyang Lake Feathers Little Eg. EG100A2
115 Poyang Lake Feathers Little Eg. EG103A
116 Poyang Lake Feathers Little Eg. EG105A 1,310 36,500 170,000 5,590 0,830 0,052 0,018 1,780 224,000
117 Poyang Lake Feathers Little Eg. EG111A
118 Poyang Lake Feathers Little Eg. EG115
119 Poyang Lake Feathers Little Eg. EG11A 37,900 77,000 3,800 0,170 0,018 0,010 2,200 204,000
120 Poyang Lake Feathers Little Eg. EG123A
121 Poyang Lake Feathers Little Eg. EG13A
122 Poyang Lake Feathers Little Eg. EG18A
123 Poyang Lake Feathers Little Eg. EG1B
124 Poyang Lake Feathers Little Eg. EG26A
125 Poyang Lake Feathers Little Eg. EG28A
126 Poyang Lake Feathers Little Eg. EG31A 0,470 35,000 135,000 7,160 0,190 0,013 0,025 1,500 236,000
127 Poyang Lake Feathers Little Eg. EG38B
128 Poyang Lake Feathers Little Eg. EG39C 0,930 49,000 110,000 6,750 0,440 0,046 0,012 1,600 175,000
129 Poyang Lake Feathers Little Eg. EG3A
130 Poyang Lake Feathers Little Eg. EG40B 1,910 28,000 410,000 10,240 0,710 0,022 0,014 1,860 208,000
131 Poyang Lake Feathers Little Eg. EG50A
132 Poyang Lake Feathers Little Eg. EG8A2 1,260 47,300 97,000 4,410 0,300 0,031 0,008 2,100 195,000
133 Poyang Lake Feathers Little Eg. EG9A
134 Poyang Lake Prey Fish Little Eg. EGP14/06/99-4 0,375 0,115 2,308 877,000 3,100 0,815 0,250 1,160 0,370 1,200 156,000
135 Poyang Lake Prey Fish Little Eg. EGP07/06/99-3 0,717 0,121 1,036
136 Poyang Lake Prey Fish Little Eg. EGP24/05/99-6 0,161 0,228 1,610 27,500 740,000 90,000 1,200 0,730 0,100 1,080 0,340 1,450 153,300
137 Poyang Lake Prey Fish Little Eg. EGP31/05/99-8 0,174 0,151 1,010 471,500 56,200 0,570 0,830 0,210 1,560 158,000
138 Poyang Lake Prey Frog Little Eg. EGFR14/06/99-15 0,177 0,113 12,075
139 Poyang Lake Prey Insect larvae Little Eg. EGLL07/06/99-12 0,000 0,000 0,000
140 Poyang Lake Prey Insect larvae Little Eg. EGLL14/06/100-11 0,164 0,494 1,372
141 Poyang Lake Prey Insect larvae Little Eg. EGLL24/05/99-13 0,170 0,050 1,443
142 Poyang Lake Prey Insect larvae Little Eg. EGOL31/05/99-7 0,000 0,000 0,000
143 Poyang Lake Prey Shrimp Little Eg. EGG14/06/99-5 0,256 0,121 0,203 736,800 139,600 0,660 0,850 0,162 1,400 0,300 0,870 81,500
144 Poyang Lake Prey Shrimp Little Eg. EGG7/06/99 1,600 62,000 1317,000 212,600 0,940 0,130 1,470 0,360 1,130 87,500
145 Poyang Lake Prey Shrimp Little Eg. EGG24/05/99-1 0,000 0,000 0,000
146 Poyang Lake Prey Shrimp Little Eg. EGG7/06/99-2 0,184 0,122 2,611
147 Poyang Lake Prey Shrimp Little Eg. EGS31/05/99-9 0,385 0,145 1,887 871,000 321,200 0,820 0,197 1,590 0,359 1,270 82,100
148 Poyang Lake Prey Tadpole Little Eg. EGLR24/05/99-14 0,174 0,112 12,334
149 Poyang Lake Prey Tadpole Little Eg. EGT31/05/99-10 0,000 0,000 0,000 15,300 5290,000 104,300 6,900 4,040 1,450 13,000 3,200 2,480 79,900
150 Poyang Lake Sediment Ponds PONDS -10 85,333 48,950 3,043 715,770 17,100 11,533 1,560 45,633 10,267 5,023 49,267
151 Poyang Lake Sediment Ricefields M.1999.RF1-1 0,210 0,088 25,428 90,667 3,130 222,290 14,900 4,363 45,667 13,600 4,700 65,567
152 Poyang Lake Sediment Ricefields M.1999.RF2-2 0,299 0,105 24,095 94,667 3,460 342,420 12,823 8,413 5,910 43,300 11,800 4,633 65,467
153 Poyang Lake Sediment Ricefields M.1999.RF3-3 73,200 93,570 2,767 341,670 22,133 3,203 51,100 9,867 2,133 48,333
154 Poyang Lake Sediment Ricefields M:1999.RF4-4 88,967 94,450 3,270 312,625 13,000 11,240 1,667 32,633 13,433 3,743 65,000
155 Poyang Lake Sediment Ricefields M.1999.RF5-5 83,500 131,510 2,680 323,290 13,633 12,137 1,547 45,300 10,700 3,680 50,000
156 Poyang Lake Sediment Ricefields M.1999.RF6-6 88,767 2,923 358,550 10,595 8,943 1,633 29,200 12,233 3,837 57,833
157 Poyang Lake Sediment Ricefields M1999RF7-7 80,600 217,730 2,503 362,250 10,367 8,600 1,617 35,167 10,667 4,250 47,233
158 Poyang Lake Sediment Ricefields M.1999RF8-8 84,367 113,190 2,737 337,205 15,000 11,400 1,600 41,200 11,150 4,130 71,600
159 Poyang Lake Sediment Ricefields M.1999.RF9-9 78,367 52,340 2,863 322,225 13,600 1,633 41,900 10,467 4,023 36,500
160 Tai Lake Egg Little Eg. Eg58 (1)-1/5e nd 0,140 0,063

135
161 Tai Lake Egg Little Eg. Eg70 (2)-1/6e nd 0,411 0,169 2,390 nd 299,000 nd 105,030 1,110 0,026 nd nd 0,001 3,960 7,490
162 Tai Lake Egg Little Eg. Eg22 (3)-1/6e
163 Tai Lake Egg Little Eg. Eg93 (4)-1/5e 0,287 225,000 nd 0,039 0,005 1,780 0,002 3,980 0,047
164 Tai Lake Egg Little Eg. Eg3 (5)-5e
165 Tai Lake Egg Little Eg. Eg1 (6)-1/6e 1,010 nd 104,000 nd 100,130 0,458 0,010 nd nd 0,001 1,907 nd
166 Tai Lake Egg Little Eg. Eg2 (7)
167 Tai Lake Egg Little Eg. Eg248 (8) nd nd 322,000 nd nd 125,700 1,640 0,015 0,298 nd 0,007 3,550 nd
168 Tai Lake Egg Little Eg. Eg6 (9)
169 Tai Lake Egg Little Eg. Eg208 (10)
170 Tai Lake Egg Little Eg. Eg4 (11) nd 7810,000 212,000 0,600 182,000 1,110 0,023 nd 7,020 0,004 2,880 nd
171 Tai Lake Egg Little Eg. Eg58 (12) 0,635 140,200 nd 0,051 0,013 nd 0,002 1,900 52,100
172 Tai Lake Egg Little Eg. Ra1a (13)-2/5e 3,640 nd 236,000 nd nd 91,100 0,956 0,059 nd nd 0,157 3,770 nd
173 Tai Lake Egg Little Eg. Rb1b (14)-2/5e nd 109,200 nd 0,027 0,008 nd 0,003 2,106 42,600
174 Tai Lake Egg Little Eg. Ra2a (15)-2/5e nd nd 174,000 nd nd 72,600 0,684 0,033 nd nd 0,031 2,670 3,520
175 Tai Lake Egg Little Eg. Ra2b (16)-2/5e
176 Tai Lake Egg Little Eg. Ra3a (17)-2/6e
177 Tai Lake Egg Little Eg. Ra3b (18)-2/6e
178 Tai Lake Egg Little Eg. Ra4a (19)-2/5e nd 118,240 nd 0,045 0,005 nd 0,002 2,340 52,810
179 Tai Lake Egg Little Eg. Ra4b (20)-2/5e 0,530 108,250 nd 0,086 0,004 nd 0,003 2,730 67,980
180 Tai Lake Egg Little Eg. Ra5a (21)-2/5e nd 127,000 nd 0,032 0,006 3,110 0,002 2,350 50,600
181 Tai Lake Egg Little Eg. Ra5b (22)-2/5e
182 Tai Lake Egg Little Eg. Ra6a (23)-2/5e 0,590 121,140 nd 0,040 0,003 nd 0,003 2,960 54,720
183 Tai Lake Egg Little Eg. Ra6b (24)-2/5e 121,000 nd 0,034 0,007 nd 0,002 2,796 50,670
184 Tai Lake Egg Little Eg. Ra7a (25)-2/6e 1,210 170,000 nd 126,000 0,948 0,022 46,000 nd 0,003 3,480 nd
185 Tai Lake Egg Little Eg. Ra7b (26)-2/6e 0,338 124,500 nd 0,037 0,004 nd 0,003 2,160 54,800
186 Tai Lake Egg Little Eg. Ra8a (27)-2/5e 0,622 336,300 nd nd 0,010 nd 0,003 2,850 57,900
187 Tai Lake Egg Little Eg. Ra8b (28)-2/5e 0,770 348,800 nd nd 0,016 nd 0,006 2,810 82,400
188 Tai Lake Egg Little Eg. Ra9a (29)-2/6e
189 Tai Lake Egg Little Eg. Ra9b (30)-2/6e
190 Tai Lake Egg Little Eg. Eg504 (31)-1/5e 2,860 nd 305,000 nd nd 62,970 0,881 0,041 0,381 nd 0,045 2,460 51,600
191 Tai Lake Egg Little Eg. Eg501 (32)-1/5e 0,620 235,000 nd 0,075 nd nd 0,003 2,320 55,400
192 Tai Lake Egg Little Eg. Ra10a (33)-2/6e 0,690 143,000 nd 0,038 0,011 nd 0,002 2,270 48,500
193 Tai Lake Egg Little Eg. Ra10b (34)-2/6e 0,485 167,400 nd 0,064 nd nd 0,003 2,360 53,700
194 Tai Lake Egg Little Eg. Eg308 (35)-1/6e
195 Tai Lake Egg Little Eg. Eg273 (36)-1/6e
196 Tai Lake Egg Little Eg. Eg244 (37)
197 Tai Lake Egg Night Her. EGG001 0,182 0,438 0,115
198 Tai Lake Egg Night Her. EGG003 0,108 0,224 0,098
199 Tai Lake Egg Night Her. EGG007 0,145 0,506 0,112
200 Tai Lake Feathers Little Eg. 1 4,640 191,000 0,003 0,177 0,026 nd 0,014 1,340 168,000
201 Tai Lake Feathers Little Eg. 2 2,960 2100,000 0,003 0,260 0,031 nd 0,018 40,430 290,000
202 Tai Lake Feathers Little Eg. 3 1,250 109,840 0,001 0,102 0,043 6,980 0,011 1,420 120,650
203 Tai Lake Feathers Little Eg. 4 2,580 144,000 0,000 0,214 0,032 nd 0,015 1,630 117,000
204 Tai Lake Feathers Little Eg. Eg208b 1,230 156,500 0,003 0,128 0,067 nd 0,034 1,540 187,500
205 Tai Lake Feathers Little Eg. Eg22d 2,230 184,300 0,004 0,151 0,038 nd 0,042 1,910 222,500
206 Tai Lake Feathers Little Eg. Eg248c nd 135,300 0,007 0,126 0,054 19,200 0,019 2,560 172,000
207 Tai Lake Feathers Little Eg. Eg273c 1,840 199,800 nd 0,180 0,056 nd 0,028 2,160 265,000
208 Tai Lake Feathers Little Eg. Eg308d 2,580 233,000 0,003 0,570 nd nd 0,015 1,780 294,000
209 Tai Lake Feathers Little Eg. Eg501d 4,450 254,000 0,002 0,680 0,028 nd 0,030 2,400 320,500
210 Tai Lake Feathers Little Eg. Eg504d 1,110 125,000 0,002 0,208 0,026 nd nd nd nd
211 Tai Lake Feathers Little Eg. Eg58d 1,140 136,000 0,002 0,155 0,023 nd 0,016 1,310 217,000
212 Tai Lake Feathers Little Eg. Eg70c 1,460 169,000 0,003 0,114 0,017 8,600 0,017 1,480 184,000
213 Tai Lake Feathers Little Eg. Eg93b 1,860 112,500 0,003 0,118 0,024 nd 0,020 1,660 176,000
214 Tai Lake Prey Fish Little Eg. Fi1 nd 0,047 0,109
215 Tai Lake Prey Fish Little Eg. Fi2 1,020 487,600 nd 0,177 0,016 nd 0,024 1,730 212,000
216 Tai Lake Prey Fish Little Eg. Fi3 (li)
217 Tai Lake Prey Fish Little Eg. Fi4
218 Tai Lake Prey Fish Little Eg. Fi5 0,861 763,600 nd 0,216 0,021 nd 0,012 0,468 163,770
219 Tai Lake Prey Fish Little Eg. Fi6 2,950 141,000 0,002 0,449 0,018 nd 0,007 1,330 238,000

136
220 Tai Lake Prey Fish Little Eg. Fi7 9,000
221 Tai Lake Prey Fish Little Eg. Fi8
222 Tai Lake Prey Fish Little Eg. Fi9 1,760 1500,000 nd 0,278 0,040 0,028 2,250 180,000
223 Tai Lake Prey Fish Little Eg. Fi10
224 Tai Lake Prey Fish Little Eg. Fi11
225 Tai Lake Prey Fish Little Eg. Fi12
226 Tai Lake Prey Fish Little Eg. Fi13
227 Tai Lake Prey Fish Little Eg. Fi14 2,710 194,620 nd 0,096 0,011 0,016 1,650 165,000
228 Tai Lake Prey Fish,Shrimp Little Eg. Fi+S1 0,041 0,109 0,106
229 Tai Lake Prey Frog Little Eg. Fr1
230 Tai Lake Prey Shrimp Little Eg. S1
231 Tai Lake Sediment Fish ponds F.P.1 78,200 39400,000 0,003 14,100 7,066 44,650 13,000 2,720 57,560
232 Tai Lake Sediment Fish ponds F.P.2 91,510 42000,000 nd 18,025 8,990 51,020 14,460 2,600 63,260
233 Tai Lake Sediment Fish ponds F.P.3 91,390 49830,000 0,004 17,660 7,555 45,650 14,270 2,790 67,270
234 Tai Lake Sediment Fish ponds F.P.4 84,900 39800,000 nd 12,900 8,140 37,760 14,120 2,040 91,720
235 Tai Lake Sediment Fish ponds F.P.5 77,130 38200,000 nd 14,270 7,900 42,170 12,250 2,410 62,200
236 Tai Lake Sediment Fish ponds F.P.6 86,160 34900,000 nd 13,455 7,690 49,420 13,510 2,800 65,680
237 Tai Lake Sediment Lake L1 0,335 0,123 30,873 116,650 39925,000 0,006 16,820 8,295 55,700 14,170 3,379 150,500
238 Tai Lake Sediment Lake L2 0,357 0,111 38,183 100,196 34300,000 0,006 15,300 7,165 81,095 12,100 2,900 162,000
239 Tai Lake Sediment Lake L3 88,050 31500,000 0,005 14,700 7,120 58,540 11,900 2,853 121,300
240 Tai Lake Sediment Lake L4 84,800 36000,000 nd 14,100 7,390 61,300 13,300 3,190 100,740
______________________________________________________________________________________________________________________________________________________________________________________________________________________________

137
____________________________________________________________________________________________________________________________________
Appendix B. List of samples collected in Pakistan (from Haleji in 1999, Karachi in 2000, Tounsa in 2000), and their content of metals and other elements (ppm, on
dry weight of the sample, nd: not detected, empty cells mean elements not analysed for that sample).
______________________________________________________________________________________________________________________________________________________________________________________________________________________________
Ordi Study Material Type Species Code Cad Mercu Lead Chro Cop Iron Manga Arse Sil Bro Co Ce Lantha Nic Scan Sele Zinc
nal area of mium ry mium per nese nic ver mine balt sium num kel dium nium
no. the
of sample
the
sample

241 Haleji Lake Egg Little Eg. Eg/N10E3-2 0,090 0,457 0,170 108,800 0,029 1,700 61,400
242 Haleji Lake Egg Little Eg. Eg/N12E2-3 0,232 0,558 0,280 106,400 0,050 0,016 2,100 58,900
243 Haleji Lake Egg Little Eg. Eg/N22E2-4 0,064 0,380 0,430 87,900 0,065 2,100 36,300
244 Haleji Lake Egg Little Eg. Eg/N26E1-5 0,425 0,555 0,400 112,300 0,025 2,900 39,500
245 Haleji Lake Egg Little Eg. Eg/N28E1-6 0,184 0,570 0,100 105,500 0,016 2,450 25,900
246 Haleji Lake Egg Little Eg. Eg/N30E1-7 0,109 0,291 0,380 123,100 0,100 2,200 65,900
247 Haleji Lake Egg Little Eg. Eg/N31E4-8 0,244 0,539 0,820 172,000 0,070 3,400 51,600
248 Haleji Lake Egg Little Eg. Eg/N7E1-1 0,220 0,343 0,150 105,300 0,045 1,800 43,100
249 Haleji Lake Egg Interm. Eg. E/N9E2-6 11,000 82,700 1,300 0,090 0,028 1,550 48,300
250 Haleji Lake Egg Interm. Eg. Ei/ N1 E1-1 0,269 5,690 1,300 1,530
251 Haleji Lake Egg Interm. Eg. Ei/ N20E1-8 nd 0,261 0,151 14,700 97,700 1,800 0,075 0,030 2,380 47,600
252 Haleji Lake Egg Interm. Eg. Ei/N11E1-7 0,269 104,300 5,200 0,160 0,030 2,790 48,300
253 Haleji Lake Egg Interm. Eg. Ei/N2 E3-2 0,560 72,950 2,800 0,089 0,030 2,490 43,350
254 Haleji Lake Egg Interm. Eg. Ei/N21E1-9 0,227 12,600 80,000 1,700 0,050 0,027 2,160 51,500
255 Haleji Lake Egg Interm. Eg. Ei/N24E2-10 nd 0,238 nd 9,000 127,000 1,400 0,097 0,032 2,500 53,500
256 Haleji Lake Egg Interm. Eg. Ei/N25E3-11 nd 0,161 nd 14,000 104,800 1,100 0,062 0,029 1,520 53,500
257 Haleji Lake Egg Interm. Eg. Ei/N27E1-12 nd 0,340 nd 15,400 136,700 1,900 0,099 0,037 3,460 74,300
258 Haleji Lake Egg Interm. Eg. Ei/N32E2-13 nd 0,344 nd 0,890 129,200 2,000 0,035 2,660 55,100
259 Haleji Lake Egg Interm. Eg. Ei/N32E3-14 100,900 1,800 0,110 0,028 2,640 56,200
260 Haleji Lake Egg Interm. Eg. Ei/N34E4-15 0,120 88,300 0,030 1,000 32,900
261 Haleji Lake Egg Interm. Eg. Ei/N35E4-16 0,200 57,800 0,043 3,100 32,700
262 Haleji Lake Egg Interm. Eg. Ei/N4 E3-3 nd 0,289 0,057 0,390 74,600 1,600 0,076 0,029 2,870 48,100
263 Haleji Lake Egg Interm. Eg. Ei/N40E1-17 nd 0,525 nd 0,189 98,000 29,800
264 Haleji Lake Egg Interm. Eg. Ei/N41E1-18 0,180 170,300 0,054 2,800 90,800
265 Haleji Lake Egg Interm. Eg. Ei/N42E2-19 0,120 80,400 0,035 2,550 41,500
266 Haleji Lake Egg Interm. Eg. Ei/N43E1-20 0,220 97,850 0,030 0,016 2,150 40,300
267 Haleji Lake Egg Interm. Eg. Ei/N43E2-21 0,240 83,400 0,030 1,700 40,500
268 Haleji Lake Egg Interm. Eg. Ei/N5E1-4 nd 0,144 nd 9,270 103,900 0,900 0,079 0,037 1,780 62,100
269 Haleji Lake Egg Interm. Eg. Ei/N8E3-5 0,430 12,600 86,000 1,500 0,028 1,660 36,800
270 Haleji Lake Egg Interm. Eg. Ei/N33 E2
271 Haleji Lake Egg Javanese C. C1N2-1
272 Haleji Lake Egg Javanese C. C2N2-2
273 Haleji Lake Egg Javanese C. C3N2-3
274 Haleji Lake Egg Javanese C. C4N2-4
275 Haleji Lake Feathers Little Eg. E.g. 8 0,250 16,520 75,000 2,600 0,210 0,009 2,300 123,000
276 Haleji Lake Feathers Little Eg. E.g.9
277 Haleji Lake Feathers Little Eg. E.g.11
278 Haleji Lake Feathers Little Eg. E.g.12
279 Haleji Lake Feathers Little Eg. E.g. 33 0,310 13,400 43,000 1,580 0,047 0,007 1,370 184,000
280 Haleji Lake Feathers Little Eg. E.g.34
281 Haleji Lake Feathers Little Eg. E.g.41
282 Haleji Lake Feathers Little Eg. E.g.42
283 Haleji Lake Feathers Little Eg. E.g. 43 0,760 6,150 120,000 4,880 0,230 0,022 1,590 163,000
284 Haleji Lake Feathers Interm. Eg. E.i.1
285 Haleji Lake Feathers Interm. Eg. E.i.2
286 Haleji Lake Feathers Interm. Eg. E.i.3
287 Haleji Lake Feathers Interm. Eg. E.i.4

138
288 Haleji Lake Feathers Interm. Eg. E.i.5
289 Haleji Lake Feathers Interm. Eg. E.i.6
290 Haleji Lake Feathers Interm. Eg. E.i. 7 0,280 88,760 42,000 5,340 0,043 0,005 1,300 201,000
291 Haleji Lake Feathers Interm. Eg. E.i.13
292 Haleji Lake Feathers Interm. Eg. E.i.14
293 Haleji Lake Feathers Interm. Eg. E.i.16
294 Haleji Lake Feathers Interm. Eg. E.i.17
295 Haleji Lake Feathers Interm. Eg. E.i.18
296 Haleji Lake Feathers Interm. Eg. E.i.19
297 Haleji Lake Feathers Interm. Eg. E.i.20
298 Haleji Lake Feathers Interm. Eg. E.i.22
299 Haleji Lake Feathers Interm. Eg. E.i.23
300 Haleji Lake Feathers Interm. Eg. E.i.24
301 Haleji Lake Feathers Interm. Eg. E.i.25
302 Haleji Lake Feathers Interm. Eg. E.i.26
303 Haleji Lake Feathers Interm. Eg. E.i.27
304 Haleji Lake Feathers Interm. Eg. E.i.28
305 Haleji Lake Feathers Interm. Eg. E.i.29
306 Haleji Lake Feathers Interm. Eg. E.i. 30 0,150 66,100 53,800 1,700 0,069 0,004 1,360 264,000
307 Haleji Lake Feathers Interm. Eg. E.i.31
308 Haleji Lake Feathers Interm. Eg. E.i.32
309 Haleji Lake Feathers Interm. Eg. E.i.35
310 Haleji Lake Feathers Interm. Eg. E.i.36
311 Haleji Lake Feathers Interm. Eg. E.i.37
312 Haleji Lake Feathers Interm. Eg. E.i.38
313 Haleji Lake Feathers Interm. Eg. E.i.39 0,170 10,230 41,000 1,130 0,034 0,005 0,870 186,000
314 Haleji Lake Feathers Interm. Eg. E.i.40
315 Haleji Lake Feathers Interm. Eg. E.i.44
316 Haleji Lake Feathers Interm. Eg. E.i.45
317 Haleji Lake Feathers Interm. Eg. E.i.46
318 Haleji Lake Feathers Interm. Eg. E.i.47
319 Haleji Lake Feathers Interm. Eg. E.i.48
320 Haleji Lake Prey Fish Interm. Eg. Barbus-7
321 Haleji Lake Prey Fish Interm. Eg. Barbus-19
322 Haleji Lake Prey Fish Interm. Eg. Colisa-16
323 Haleji Lake Prey Fish Interm. Eg. Colisa-17
324 Haleji Lake Prey Fish Interm. Eg. Colisa-18
325 Haleji Lake Prey Fish Interm. Eg. Gloss8
326 Haleji Lake Prey Fish Interm. Eg. Gloss9
327 Haleji Lake Prey Fish Interm. Eg. Glos10
328 Haleji Lake Prey Fish Interm. Eg. Glos11
329 Haleji Lake Prey Fish Interm. Eg. Glos12
330 Haleji Lake Prey Fish Interm. Eg. Glos13
331 Haleji Lake Prey Fish Interm. Eg. Oreoc2
332 Haleji Lake Prey Fish Interm. Eg. Oreoc3
333 Haleji Lake Prey Fish Interm. Eg. Oreoc4
334 Haleji Lake Prey Fish Interm. Eg. Oreoc5
335 Haleji Lake Prey Fish Interm. Eg. Oreoc6
336 Haleji Lake Prey Shrimp Interm. Eg. Carrid1 0,042 0,120 0,233
337 Haleji Lake Prey Shrimp Interm. Eg. Carrid14 0,039 0,098 0,190
338 Haleji Lake Prey Shrimp Interm. Eg. Carrid15 0,070 0,137 0,629
339 Karachi Egg Little Eg. Egu1a nd 0,138 0,047 nd nd 99,000 nd 30,800 nd nd nd nd 0,001 1,690 nd
340 Karachi Egg Little Eg. Egu1b nd 0,153 0,044
341 Karachi Egg Little Eg. Egu2a nd 0,174 nd 0,319 nd 150,000 nd nd 42,500 nd 0,042 nd nd 0,002 2,640 nd
342 Karachi Egg Little Eg. Egu2b nd 0,159 0,045
343 Karachi Egg Little Eg. Egu5a nd nd 110,000 0,324 38,000 0,082 0,018 nd nd 0,003 3,070 32,800
344 Karachi Egg Little Eg. Egu5b
345 Karachi Egg Little Eg. Egu9a 1410,000 nd 51,300 nd
346 Karachi Egg Little Eg. Egu9b

139
347 Karachi Egg Little Eg. Egu21a nd nd 92,100 nd nd 44,800 nd 0,135 0,321 nd 0,005 5,610 2,710
348 Karachi Egg Little Eg. Egu21b
349 Karachi Egg Little Eg. Egu22 1,820 nd 741,000 nd nd 29,100 nd 0,053 nd nd 0,013 2,160 140,000
350 Karachi Egg Little Eg. Egu50a 1,100 nd 360,000 0,231 nd 46,100 nd 0,014 nd 22,900 0,023 2,980 nd
351 Karachi Egg Little Eg. Egu50b
352 Karachi Egg Little Eg. Egu53a nd 183,000 1,320 nd 29,800 0,141 nd 0,366 nd 0,036 2,130 4,440
353 Karachi Egg Little Eg. Egu53b
354 Karachi Egg Little Eg. Egu54a nd nd 156,000 nd nd 50,600 0,110 0,024 nd nd nd 3,350 nd
355 Karachi Egg Little Eg. Egu54b
356 Karachi Egg Little Eg. Egu55 nd 3300,000 76,400 0,448 nd 98,000 0,005 0,098 nd nd 0,007 2,870 nd
357 Karachi Egg Little Eg. Egu56a nd nd 183,000 0,509 nd 44,700 0,678 0,072 nd nd 0,014 3,810 329,000
358 Karachi Egg Little Eg. Egu56b
359 Karachi Egg Little Eg. Egu57a 3,480 nd 99,500 0,239 0,637 51,500 nd 0,045 0,279 nd 0,002 3,160 14,700
360 Karachi Egg Little Eg. Egu57b
361 Karachi Egg Little Eg. Egu58a nd nd 481,000 nd nd 34,300 nd 0,073 0,317 nd 0,008 2,240 222,000
362 Karachi Egg Little Eg. Egu58b
363 Karachi Egg Little Eg. Egu59a nd nd 191,000 0,485 nd 57,900 nd nd nd 9,530 0,010 5,050 nd
364 Karachi Egg Little Eg. Egu59b
365 Karachi Egg Little Eg. Egu60 nd nd 581,000 0,295 nd 43,500 nd 0,037 nd nd 0,005 8,370 0,406
366 Karachi Egg Little Eg. Egu61a nd 0,837 43,300 nd
367 Karachi Egg Little Eg. Egu61b
368 Karachi Egg Little Eg. Egu62a nd nd 114,000 0,272 48,300 0,188 0,022 0,480 nd 0,006 3,140 30,500
369 Karachi Egg Little Eg. Egu62b
370 Karachi Egg Little Eg. Egu63b nd nd 117,200 nd 51,200 0,081 0,008 nd nd 0,001 3,790 11,600
371 Karachi Egg albumen Little Eg. Egu3alb. nd 4800,000 122,700 nd 69,400 nd 0,183 nd nd 0,002 1,460 nd
372 Karachi Egg albumen Little Eg. Egu63a alb. 4,540 nd 23,600 nd nd 80,200 2,050 0,097 0,280 nd nd 11,240 nd
373 Karachi Egg albumen Little Eg. Egu63c alb. nd nd 121,000 nd nd 79,900 0,104 0,094 nd nd 0,029 1,560 nd
374 Karachi Egg yolk Little Eg. Egu3yolk nd nd 295,000 0,175 0,751 24,000 2,170 0,078 nd nd 0,006 7,500 287,000
375 Karachi Egg yolk Little Eg. Egu63a yolk nd nd 240,000 0,389 27,100 0,153 0,009 nd nd 0,002 4,340 79,000
376 Karachi Egg yolk Little Eg. Egu63c yolk nd 120,800 nd 16,000 0,338 0,017 0,622 nd 0,004 1,430 84,800
377 Karachi Feathers Little Eg. Egu 100 15,500 nd 109,000 nd nd 64,300 15,900 0,351 1,420 nd nd 12,000 609,000
378 Karachi Feathers Little Eg. Egu1a (a+b) nd 95,900 nd nd 59,300 4,400 0,191 1,800 nd nd 7,460 nd
379 Karachi Feathers Little Eg. Egu 1b
380 Karachi Feathers Little Eg. Egu200a(a+b) nd nd 938,000 0,654 nd 74,000 5,010 0,540 nd nd 0,072 18,700 242,000
381 Karachi Feathers Little Eg. Egu 200b
382 Karachi Feathers Little Eg. Egu4a(a+b) 7,530 nd 307,000 nd nd 69,500 7,880 0,216 nd nd 0,048 2,160 435,000
383 Karachi Feathers Little Eg. Egu 4b
384 Karachi Feathers Little Eg. Egu 5a nd 36100,000 1400,000 nd nd 57,400 14,000 nd nd nd 0,005 nd 227,000
385 Karachi Feathers Little Eg. Egu66a(a+b) 7,380 nd 328,000 1,550 nd 82,100 5,580 0,196 nd nd 0,020 2,450 152,000
386 Karachi Feathers Little Eg. Egu 66b
387 Karachi Feathers Little Eg. Egu68a(a+b) 6,110 nd 431,000 2,620 1,360 81,300 5,580 0,436 nd nd 0,054 7,020 189,000
388 Karachi Feathers Little Eg. Egu 68b
389 Karachi Feathers Little Eg. Egu69a(a+b) 9,710 nd 1050,000 0,777 nd 71,600 8,920 0,572 nd nd 0,066 1,850 1710,000
390 Karachi Feathers Little Eg. Egu 69b
391 Karachi Feathers Little Eg. Egu 70b nd nd 1,280 nd 75,200 9,480 0,307 nd nd nd 23,200 nd
392 Karachi Feathers Little Eg. Egu 7b 9,380 nd 782,000 0,723 nd 42,700 5,450 nd nd nd 0,009 1,370 nd
393 Karachi Feathers Little Eg. Egu 80a 23,100 nd 2130,000 nd nd 96,400 14,800 0,441 nd nd 0,392 4,850 nd
394 Karachi Feathers Little Eg. Egu8a(a+b) nd nd 1130,000 nd nd 40,200 2,590 0,215 nd nd 0,041 nd 449,000
395 Karachi Feathers Little Eg. Egu 8b
396 Karachi Prey Fish Little Eg. F1 0,072 0,549 3,589
397 Karachi Prey Fish Little Eg. F2 0,103 0,533 4,322
398 Karachi Prey Fish Little Eg. F3 0,131 0,641 6,366
399 Karachi Sediment Channel C.K.1
400 Karachi Sediment Channel C.K.2
401 Karachi Sediment Channel C.K.3 174,000 1300,000 37500,000 7,460 0,278 33,000 18,800 9,790 22,100 47,400 11,500 2,914 88,700
402 Karachi Sediment Mud G.B.1 0,228 1,724 22,904
403 Karachi Sediment Mud G.B.2 0,316 2,675 47,718
404 Karachi Sediment Mud G.B.3 0,120 0,775 6,236 308,000 nd 15900,000 4,510 nd 23,100 6,460 2,190 33,600 38,800 6,300 2,975 7,230
405 Karachi Sediment Channel O.C.1

140
406 Karachi Sediment Channel O.C.2 245,000 nd 44800,000 19,100 nd 7,670 22,000 9,800 34,300 62,100 15,300 3,430 119,000
407 Karachi Sediment Channel O.C.3
408 Tounsa Egg Cattle Eg. Bi6 nd 0,034 0,106 nd nd 110,000 nd 0,882 22,000 0,020 0,022 nd nd 0,039 2,000 12,700
409 Tounsa Egg Cattle Eg. Bi14 nd nd 83,500 nd nd 6,150 0,006 0,005 0,191 nd 0,001 3,760 20,100
410 Tounsa Egg Cattle Eg. Bi21 nd nd 123,000 0,218 nd 10,270 nd 0,013 nd nd 0,009 2,190 16,400
411 Tounsa Egg Cattle Eg. Bi23 nd nd 96,300 nd 5,560 0,008 0,009 nd nd 0,004 3,620 nd
412 Tounsa Egg Cattle Eg. Bi25 nd nd 155,000 nd 72,600 0,195 0,021 nd nd 0,004 3,390 63,000
413 Tounsa Egg Cattle Eg. Bi30a nd 136,000 nd nd 5,950 0,058 0,022 0,220 nd 0,023 2,313 22,900
414 Tounsa Egg Cattle Eg. Bi30b nd nd 131,000 nd nd 10,500 nd 0,016 nd nd 0,010 2,210 28,600
415 Tounsa Egg Cattle Eg. Bi31 nd nd 135,000 nd nd 8,180 nd 0,011 nd nd 0,007 2,026 25,100
416 Tounsa Egg Cattle Eg. Bi35 nd nd 135,000 nd nd 9,002 nd 0,016 nd nd 0,003 2,487 43,200
417 Tounsa Egg Cattle Eg. Bi54 nd 108,000 nd 4,896 0,054 0,011 0,245 nd 0,005 2,520 29,000
418 Tounsa Egg Little Eg. Eg2 nd 0,199 0,177 nd nd 105,300 nd 51,100 0,031 0,017 0,096 nd 0,006 3,510 5,820
419 Tounsa Egg Little Eg. Eg17 nd nd 125,000 nd nd 18,500 0,053 0,026 0,201 nd 0,033 1,190 1,101
420 Tounsa Egg Little Eg. Eg18 nd nd 221,000 nd 76,300 0,045 0,010 nd nd 0,006 4,137 28,100
421 Tounsa Egg Little Eg. Eg29 1,080 nd 183,000 0,343 nd 54,100 0,021 0,033 nd nd 0,024 4,140 9,060
422 Tounsa Feathers Cattle Eg. Bi21a 9,930 252,000 nd nd 25,100 5,980 0,342 nd nd nd 5,700 nd
423 Tounsa Feathers Cattle Eg. Bi21b nd 199,000 nd nd 16,300 6,560 0,156 1,460 nd 0,005 4,180 139,000
424 Tounsa Feathers Cattle Eg. Bi22a nd nd 1160,000 nd nd 10,500 9,580 0,369 nd nd 0,406 5,130 nd
425 Tounsa Feathers Cattle Eg. Bi24a nd nd 110,000 nd nd 28,000 8,670 0,401 nd nd 0,035 10,400 12,300
426 Tounsa Feathers Cattle Eg. Bi47 nd 1650,000 nd nd 11,000 9,790 0,370 nd nd 0,498 6,980 nd
427 Tounsa Feathers Cattle Eg. Bi52a nd nd 388,000 nd 21,000 8,700 nd nd nd 0,031 8,380 nd
428 Tounsa Feathers Cattle Eg. Bi53a 7,290 5550,000 1260,000 nd 37,000 8,890 0,051 nd nd 0,042 3,180 nd
429 Tounsa Feathers Cattle Eg. Bi54a 11,300 nd 585,000 nd 34,100 15,500 0,043 0,710 nd 0,056 9,740 nd
430 Tounsa Feathers Cattle Eg. Bi6 17,200 nd 1250,000 nd nd 16,000 7,670 0,256 0,165 nd 0,270 6,400 384,000
431 Tounsa Feathers Cattle Eg. Bi61a 7,300 nd 355,000 nd nd 26,200 8,200 0,131 nd 113,000 nd 11,000 220,000
432 Tounsa Feathers Cattle Eg. Bi68a nd nd 1720,000 nd 5,050 34,900 7,610 0,186 0,604 nd nd 21,700 nd
433 Tounsa Feathers Cattle Eg. Bi77a nd nd 2070,000 nd nd 31,300 6,040 nd 0,545 nd 0,037 12,300 256,000
434 Tounsa Feathers Cattle Eg. Bi85a 10,500 nd 594,000 1,230 17,100 10,400 0,075 nd nd 0,032 5,130 428,000
435 Tounsa Feathers Little Eg. Eg14a nd nd 260,000 nd 19,000 19,300 0,093 nd nd 0,025 7,900 113,000
436 Tounsa Feathers Little Eg. Eg64a nd 70,300 nd nd 14,800 4,090 nd 2,980 nd 0,009 27,700 nd
437 Tounsa Feathers Little Eg. Eg65 12,400 nd 695,000 1,120 39,000 9,540 nd 0,867 nd 0,031 3,350 nd
438 Tounsa Prey Insects Cattle Eg. Tcr 0,119 0,025 0,903 5,930 nd 1700,000 nd nd 25,100 1,530 0,350 1,630 nd 0,581 3,487 180,000
439 Tounsa Prey Fish Cattle Eg. Tfi 2,570 nd 1046,300 1,350 nd 15,300 0,965 0,228 0,453 nd 0,157 2,760 78,000
440 Tounsa Prey Frog Cattle Eg. Tfr 3,100 nd 701,000 0,401 nd 12,600 0,671 0,275 0,621 nd 0,261 2,087 77,900
441 Tounsa Prey Insects Cattle Eg. Tin 0,034 0,018 0,872 8,380 1240,000 2190,000 0,713 nd 33,600 1,380 0,391 2,210 nd 0,788 1,129 28,400
442 Tounsa Prey Mice Cattle Eg. Tmo 4,400 nd 1620,000 0,536 nd 10,900 1,510 0,346 1,150 17,100 0,511 2,924 51,500
443 Tounsa Sediment Channel C1 0,057 nd 3,842 169,000 2160,000 39100,000 4,120 nd 4,510 12,300 4,045 94,400 nd 15,800 8,467 54,800
444 Tounsa Sediment Channel C2 0,061 nd 4,609
445 Tounsa Sediment Channel C3 0,091 0,020 4,121
446 Tounsa Sediment Channel C4
447 Tounsa Sediment Ponds P.1 104,000 3760,000 36100,000 4,370 2,550 13,100 4,860 49,250 89,600 14,000 4,160 12,100
448 Tounsa Sediment Ponds P.2
449 Tounsa Sediment Ponds P.3
450 Tounsa Sediment Ricefields RF.1 107,000 nd 38900,000 6,300 0,843 2,840 15,600 7,400 53,500 49,000 15,100 3,240 48,500
451 Tounsa Sediment Ricefields RF.2
452 Tounsa Sediment Ricefields RF.3
______________________________________________________________________________________________________________________________________________________________________________________________________________________________

141
____________________________________________________________________________________________________________________________________
Appendix C. List of samples collected in China (from Guandong in 2000, Poyang lake 1999, Wuxi 2000), and their content of organic contaminants
(ppb, or ng/g on dry weight basis, empty cells mean not detected at the equipment detection limits). If fresh weight of the analyzed sample was
available it has been included with the corresponding dry weight to make possible the transformation to concentrations on wet weight basis.
YEA Year
NES Nest id.#
EGG Egg id.#
LAB Original label
LOC Locality
11 Haleji Lake
12 Taunsa Barrage
13 Karachi Ghas Bunder
21 Lake Poyang (Nanchang)
22 Lake TaiHu (Wuxi)
23 Ecol. Park (Guandong)
SPE Species
1 Egretta garzetta
2 Egretta intermedia
3 Egretta gularis
4 Bubulcus ibis
5 Nycticorax nycticorax
6 Phalacrocorax niger
21 Fishes
22 Shrimps
23 Fish and shrimp
24 Tadpoles
25 Frogs
26 Mice
27 Coleoptera
28 Odonata
29 Crickets
41 Lake
42 Fishpond
43 Pond
44 Ricefield
45 Channel
46 Mud
47 Foraging area
48 Seepage lagoon
TYP Type
1 Egg content
2 Preys
3 Sediments
D_C Dry weight (g)
F_C Fresh weight (g)
AHC alfa-HCH (ng/g)
GHC gama-HCH (ng/g)
BHC beta-HCH (ng/g)
DHC delta-HCH (ng/g)
HEP Heptachlor (ng/g)
HEX Heptachlor-epoxi (ng/g)
ALDR Aldrin (ng/g)
AES alfa-Endosulfán (ng/g)
BES beta-Endosulfán (ng/g)

142
PPDDE pp-DDE (ng/g)
PPDDD pp-DDD (ng/g)
PPDDT pp-DDT (ng/g)
SHCB HCB (ng/g)
SHCH sum HCHs (ng/g)
SCIC sum Cyclodiene pest. (ng/g)
SDDT sum DDTs (ng/g)
SPCB sum PCBs (ng/g)

______________________________________________________________________________________________________________________________________________________________________________________________________________________________
YEA NES EGG LAB LOC SPE TYP D_C F_C AHC GHC BHC DHC HEP HEX ALD AES BES PPDDE PPDDD PPDDT SHCB SHCH SCIC SDDT SPCB

99 1 9 EgM1 EGG 21 1 1 4,2740 22,2960 1901,4 17,4 1901,4 28,8


99 2 1 EgM2A EGG 21 1 1 4,1330 22,3870 46,4 4,8 3049,9 9,5 51,2 3049,9
99 2 2 EgM2B EGG 21 1 1 4,1540 22,4380 73,8 2335,5 27,6 7,1 73,8 2363,1
99 2 3 EgM2C EGG 21 1 1 4,0490 21,9640 65,7 4356,1 11,2 65,7 4356,1 5,7
99 2 4 EgM2D EGG 21 1 1 4,3870 22,8910 42,4 2860,4 29,7 10,3 42,4 2890,1 7,9
99 2 5 EgM2E EGG 21 1 1 4,4190 22,8630 2504,3 29,1 7,9 2533,4
99 3 9 EgM3 EGG 21 1 1 4,0520 21,1070 2062,4 23,1 2062,4
99 5 1 EgM5A EGG 21 1 1 3,4810 19,5960 43,6 816,9 7,0 43,6 816,9 7,9
99 5 2 EgM5B EGG 21 1 1 3,5980 20,6020 63,8 2146,1 46,4 13,7 63,8 2192,5 74,4
99 5 3 EgM5C EGG 21 1 1 3,2860 19,4430 77,3 1602,9 43,1 17,0 77,3 1646,0 63,8
99 5 4 EgM5D EGG 21 1 1 3,6620 21,2290 21,5 1225,3 11,8 15,1 12,8 21,5 1252,3 40,7
99 5 5 EgM5E EGG 21 1 1 3,3630 18,0750 23,3 1684,9 35,3 15,3 23,3 1720,2 32,3
99 8 9 EgM8 EGG 21 1 1 4,2160 22,7820 35,6 29,5 4042,3 25,1 28,8 65,2 4067,5 5,4
99 9 9 EgM9 EGG 21 1 1 4,2060 22,4680 68,1 29,4 6435,5 34,9 97,5 6435,5
99 10 1 EgM10A EGG 21 1 1 3,7000 20,2370 85,0 5890,1 33,1 18,0 85,0 5923,2 21,4
99 10 2 EgM10B EGG 21 1 1 3,8820 22,0390 19,2 7642,8 36,7 22,2 24,0 19,2 7701,7 9,8
99 10 3 EgM10C EGG 21 1 1 3,9040 21,0820 6199,9 6199,9
99 10 4 EgM10D EGG 21 1 1 3,7680 22,8660 24,6 7990,0 127,8 11,0 24,6 8117,7 36,0
99 10 5 EgM10E EGG 21 1 1 3,8880 21,4220 274,7 8059,5 55,6 23,7 274,7 8115,0 32,2
99 11 9 EgM11 EGG 21 1 1 3,4610 18,6780 2830,0 35,1 2830,0
99 13 9 EgM13 EGG 21 1 1 3,5310 18,3680 2634,0 17,6 21,8 2651,5 18,0
99 15 1 EgM15A EGG 21 1 1 4,0070 22,8740 5005,7 51,0 28,4 5056,7 84,0
99 15 2 EgM15B EGG 21 1 1 3,8680 20,3740 49,3 4575,0 75,6 18,8 49,3 4650,6 226,8
99 15 3 EgM15C EGG 21 1 1 4,0000 21,9190 50,7 5,8 5177,4 113,3 21,8 50,7 5,8 5290,7 316,5
99 15 4 EgM15D EGG 21 1 1 4,1180 21,8910 52,2 4707,5 109,3 30,3 52,2 4816,8 144,0
99 18 9 EgM18 EGG 21 1 1 4,1020 21,4070 1809,9 16,1 27,0 1826,0
99 100 9 EgM100 EGG 21 1 1 3,6540 21,1910 3476,3 14,4 3476,3
99 103 9 EgM103 EGG 21 1 1 4,5800 25,3300 7959,2 24,8 12,0 7983,9
99 105 9 EgM105 EGG 21 1 1 4,2790 23,5450 1855,4 5,2 1855,4
99 106 9 EgM106 EGG 21 1 1 3,7030 18,2710 1657,0 7,6 1657,0
99 109 1 EgM109A EGG 21 1 1 4,1310 21,4990 39,3 3915,5 29,1 72,0 39,3 3944,6 11,9
99 109 2 EgM109B EGG 21 1 1 4,3730 22,0030 3258,9 59,7 3258,9
99 109 3 EgM109C EGG 21 1 1 4,3180 22,0500 32,8 3175,5 8,3 70,1 32,8 3183,8 11,9
99 109 4 EgM109D EGG 21 1 1 4,5630 23,6680 43,1 3496,6 82,1 43,1 3496,6
99 109 5 EgM109E EGG 21 1 1 4,1560 22,6990 3185,9 54,6 3185,9
99 111 9 EgM111 EGG 21 1 1 3,0690 18,4030 3592,3 9,3 3592,3 8,7
99 115 9 EgM115 EGG 21 1 1 3,5910 22,6140 2254,7 27,1 2254,7
99 123 9 EgM123 EGG 21 1 1 3,3620 21,9580 2323,4 19,5 26,7 2342,9
99 EG MP 14-6-99 21 21 2 2,7650 11,5080 11,0 50,0 14,0 11,0 50,0
99 EG MP 7-6-99 21 21 2 ,8070 5,1380 38,0 19,0 38,0
99 EG MP 31-5-99 21 21 2 3,0480 11,9260 87,0 8,0 16,0 95,0
99 EG MP 24-5-99 21 21 2 3,9590 14,8700 94,0 17,0 4,0 111,0
99 EG MG 14-5-99 21 22 2 4,8900 22,3270 9,0 11,0 13,0 9,0 11,0
99 EG MG 7-6-99 21 22 2 6,0730 24,7340 9,0 12,0 9,0
99 EG MS 31-5-99 21 22 2 3,6590 15,6680 11,0 18,0 11,0
99 EG MG 24-5-99 21 22 2 1,5270 6,0230 18,0
99 EG MLR 24-5-99 21 24 2 1,0210 3,3440 10,0 18,0 10,0

143
99 EG MT 31-5-99 21 24 2 3,5770 11,0830 158,0 90,0 19,0 248,0
99 EG MFR 14-5-99 21 25 2 1,5630 6,2320 8,0 17,0 8,0
99 EG MOL 31-5-99 21 28 2 ,5380 2,3140 14,0 8,0 15,0 14,0 8,0
99 EG MLL 14-6-99 21 28 2 ,1370 ,5800 53,0
99 EG MLL 7-6-99 21 28 2 ,4060 1,6180 61,0
99 EG MLL 24-5-99 21 28 2 ,3790 1,6390 14,0
99 POND 21 43 3 3,4 157,0 3165,0 3792,0 41675,0 1,3 160,4 48632,0
99 RF I 21 44 3 3,3 1,8 3,3
99 RF II 21 44 3 6,2 ,9 1,3 7,1
99 RF III 21 44 3 1,6 1,6
99 RF IV 21 44 3 6,1 3,6 1,4 9,7
99 RF V 21 44 3 1,5 1,6 1,5
99 RF VI 21 44 3 ,9 7,4 2,0 ,9 7,4
99 RF VII 21 44 3 4,0 1,6 4,0
99 RF VIII 21 44 3 1,5 1,4 1,5
99 RF IX 21 44 3 1,4
00 1 9 Eg 001 w/00 22 1 1 4,3900 22,6300 8,2 24,1 84,9 8,3 15,0 1834,0 10,0 13,9 32,2 108,2 1844,0 398,7
00 3 9 Eg 003 w/00 22 1 1 3,5400 19,0400 34,7 35,3 64,0 7,7 16,0 1818,0 53,8 33,9 70,0 87,7 1871,8 141,0
00 4 9 Eg 004 w/00 22 1 1 3,4700 19,1900 23,7 38,6 42,4 6,6 1829,8 37,1 21,1 62,3 49,0 1866,9 185,3
00 5 9 Eg 005 w/00 22 1 1 4,0800 21,1500 13,0 61,6 52,8 45,1 1730,6 120,7 124,6 74,7 97,9 1851,2 298,1
00 6 9 Eg 006 w/00 22 1 1 4,1700 21,3800 15,4 73,6 49,9 61,1 1753,1 120,8 192,0 89,0 111,1 1873,9 270,2
00 22 9 Eg22 w/00 22 1 1 4,4600 22,3500 17,4 57,5 68,5 5,8 1763,2 73,3 32,9 74,9 74,3 1836,5 179,2
00 58 9 Eg 58 w/00 22 1 1 3,7800 19,1400 10,7 5,4 69,4 4,4 41,4 390,8 11,3 16,0 115,1 390,8 440,7
00 70 9 Eg 70 w/00 22 1 1 4,1500 21,1500 10,6 62,7 5,4 2,1 7,2 1516,9 79,9 31,7 73,3 14,7 1596,8 211,7
00 93 9 Eg 93 w/00 22 1 1 4,0700 21,9300 49,0 98,2 48,0 28,8 2383,7 57,1 262,0 30,1 147,2 76,7 2702,9 102,0
00 208 9 Eg 208 w/00 22 1 1 4,1300 21,3400 44,7 80,3 110,8 36,7 17,6 1608,9 12,0 55,3 235,8 54,3 1620,8 322,0
00 248 9 Eg 248 w/00 22 1 1 4,5500 22,7600 45,5 79,8 13,2 1858,9 78,9 12,2 45,5 93,0 1937,8 167,1
00 505 9 Eg 20000505 w/00 22 1 1 6,8 35,9 99,4 15,5 19,6 1928,1 11,1 22,0 42,7 134,5 1939,2 487,4
00 10019 Eg-Rb 001 w/00 22 1 1 4,2100 22,7500 24,7 93,3 97,6 57,4 26,5 4187,1 357,7 1073,2 18,2 118,1 181,5 5618,0 1436,1
00 10019 Eg-Ra 001 w/00 22 1 1 3,7500 19,5800 10,2 68,6 54,5 21,8 6,1 1581,2 112,3 36,4 133,3 27,9 1693,5 3017,3
00 10019 Eg-Rc 001 w/00 22 1 1 4,0600 21,8300 19,0 97,6 9,5 2,9 5,6 1701,9 64,1 53,5 116,6 18,0 1766,0 813,8
00 10029 Eg-Rb 002 w/00 22 1 1 4,3000 23,7600 15,3 101,5 101,9 93,3 25,3 11886,2 307,8 1279,6 28,8 116,8 220,4 13473,6 1186,3
00 10029 Eg-Ra 002 w/00 22 1 1 3,7700 19,8800 11,1 58,0 56,3 3,1 5,5 1834,6 119,0 42,3 69,0 64,9 1953,5 3117,5
00 10029 Eg-Rc 002 w/00 22 1 1 4,0800 21,8800 14,9 104,7 81,7 4,8 9,0 1750,9 18,8 44,2 119,6 95,5 1769,6 977,1
00 10039 Eg-Rb 003 w/00 22 1 1 4,2500 21,4800 39,8 80,3 29,4 983,7 11,8 221,5 120,1 29,4 995,6 493,6
00 10039 Eg-Ra 003 w/00 22 1 1 4,3100 21,4600 25,9 65,1 64,7 20,4 1594,6 22,5 13,7 51,7 90,9 85,1 1630,8 360,1
00 10039 Eg-Rc 003 w/00 22 1 1 4,3900 22,5800 9,2 149,7 65,7 42,8 5,7 2481,3 99,5 39,3 224,6 48,4 2580,8 929,7
00 10049 Eg-Rb 004 w/00 22 1 1 4,2300 20,9800 53,7 91,0 29,2 2,7 25,2 1109,6 5,8 199,0 144,8 57,1 1115,4 552,6
00 10049 Eg-Ra 004 w/00 22 1 1 3,9300 20,2200 10,5 54,4 88,7 9,9 2,8 5,2 1560,7 8,2 15,8 153,6 18,0 1568,8 330,0
00 10049 Eg-Rc 004 w/00 22 1 1 4,5200 22,8700 8,9 171,0 115,8 3,5 2721,0 50,3 179,9 119,3 2721,0 1011,7
00 10059 Eg-Rb 005 w/00 22 1 1 4,3200 12,0900 19,1 51,0 85,6 2,2 60,2 4,2 11,5 6019,8 30,4 492,5 152,2 155,7 78,1 6542,7 759,1
00 10059 Eg-Ra 005 w/00 22 1 1 3,6300 17,8200 13,3 112,1 5,1 41,1 1703,9 66,0 20,8 24,2 125,4 46,2 1790,7 107,8
00 10059 Eg-Rc 005 w/00 22 1 1 4,4700 24,0300 10,9 33,6 74,0 5,2 6,5 1030,6 31,2 118,5 11,7 1030,6 298,3
00 10069 Eg-Rb 006 w/00 22 1 1 4,3500 22,5100 11,3 44,3 145,4 8,7 16,8 9,0 6173,4 18,9 434,1 53,7 201,0 34,4 6626,4 648,1
00 10069 Eg-Ra 006 w/00 22 1 1 3,7600 18,5500 22,4 137,0 111,7 74,3 3,7 25,4 1707,1 82,2 20,5 271,1 103,4 1789,3 87,5
00 10069 Eg-Rc 006 w/00 22 1 1 5,0000 23,9600 15,5 31,0 89,1 7,4 948,0 36,1 46,4 96,5 948,0 209,7
00 10079 Eg-Ra 007 w/00 22 1 1 4,0400 21,1800 10,7 35,6 132,9 1,1 67,1 13,1 18,2 2920,1 95,0 13,5 179,3 99,6 3015,1 718,5
00 10089 Eg-Ra 008 w/00 22 1 1 3,8300 19,9900 16,6 38,4 106,3 75,9 4,8 29,6 3002,3 42,3 12,1 161,2 110,3 3044,6 805,5
00 10389 Eg D308 w/00 22 1 1 3,9300 20,4500 6,9 80,4 71,1 31,1 6,7 1875,9 7,9 12,0 158,3 37,7 1883,8 683,5
00 12449 Eg C244 w/00 22 1 1 4,0700 21,9000 6,7 53,9 99,3 3,5 2,9 947,5 14,6 60,6 105,8 947,5 335,6
00 15019 Eg CE 501 w/00 22 1 1 8,9400 20,3800 26,9 182,5 123,7 5,7 2343,7 27,1 209,4 129,3 2343,7 647,4
00 15049 Eg-CE 504 W/00 22 1 1 3,5400 19,4100 4,6 56,5 78,8 5909,7 21,2 14,7 61,1 78,8 5930,9 402,6
99 1 9 YTZHNNEGG001 22 5 1 1167,0 10,0 6688,0 113,0 93,0 1167,0 10,0 6801,0 220,0
99 2 9 YTZHNNEGG003 22 5 1 145,0 3178,0 25,0 30,0 145,0 3203,0 8,0
99 7 9 YTZHNNEGG007 22 5 1 4015,0 161,0 17,0 4176,0 505,0
00 Wuxi col. Fi 1 22 21 2 37,2 53,7 37,2 53,7 8,4
00 Wuxi col. Fi 2 22 21 2 5,1 5,3 184,8 26,9 16,8 10,4 211,7
00 Wuxi col. Fi 3 22 21 2 171,2 10,2 181,4 12,8
00 Wuxi col. Fi 4 22 21 2

144
00 Wuxi col. Fi 5 22 21 2 19,3 8,3 19,3 8,3 76,5
00 Wuxi col. Fi 6 22 21 2 5,7 16,4 5,7 16,4 9,2
00 Wuxi col. Fi 7 22 21 2 141,0 15,2 156,2 8,2
00 Wuxi col. Fi 8 22 21 2 3,3 35,5 3,2 3,3 35,5 8,8
00 Wuxi col. Fi 9 22 21 2 4,2 72,0 8,2 4,2 80,1 8,3
00 Wuxi col. Fi 10 22 21 2 2,1 37,7 19,1 4,6 2,1 56,8 15,5
00 Wuxi col. Fi 11 22 21 2 3,8 2,2 172,6 6,0 172,6 4,3
00 Wuxi col. Fi 12 22 21 2 75,5 32,6 7,8 108,2 56,9
00 Wuxi col. Fi 13 22 21 2 52,7 52,7 74,6
00 Wuxi col. Fi 14 22 21 2 23,6 72,0 23,6 72,0
00 Wuxi col. S1 22 22 2 6,7 94,7 4,7 6,7 94,7 4,7
00 Wuxi col. (Fi+S)1 22 23 2 19,5 18,2 19,5 18,2
00 Wuxi col. Fr 1 22 25 2 5,9 5,0 7,5 10,8 7,7 5,9 12,5 10,8 10,0
00 SED/L1 Wuxi-CH 22 41 3 396,7 8 4,3 1,5 396,7 5,8 ,9
00 SED/L2 Wuxi-CH 22 41 3 4,8 1,1 6,0 1,4
200 SED/L3 Wuxi-CH 22 41 3 1,2 1,2 5,1
00 SED/L4 Wuxi-CH 22 41 3 ,8 ,8 15,6
00 SED/FP1 Wuxi-CH 22 42 3 14,0 14,0
00 SED/FP2 Wuxi-CH 22 42 3 76,9 76,9 ,4
00 SED/FP3 Wuxi-CH 22 42 3 564,2 564,2
00 SED/FP4 Wuxi-CH 22 42 3 ,5 25,7 208,9 26,2 208,9
00 SED/FP5 Wuxi-CH 22 42 3 4,0 4,0
00 SED/FP6 Wuxi-CH 22 42 3 ,7 ,7 1,2
00 18 1 Eg 18-1,GD/00 23 1 1 6,0500 30,4200 36,6 29,7 58,3 2,0 1481,7 25,4 19,0 66,3 60,2 1507,2 175,6
00 18 2 Eg 18-2,GD/00 23 1 1 3,9220 18,8690 37,6 61,4 679,4 2805,6 64,3 16,9 99,0 679,4 2870,0 166,5
00 35 1 Eg 35-1,GD/00 23 1 1 4,1260 20,8560 33,2 81,1 91,1 4,9 2794,6 91,1 16,2 114,2 96,0 2885,8 272,6
00 35 2 Eg 35-2,GD/00 23 1 1 3,7330 19,9840 3,2 55,0 160,2 5,9 2585,3 42,2 14,7 58,3 166,0 2627,5 295,1
00 53 1 Eg 53-1,GD/00 23 1 1 4,1940 21,3930 8,0 80,6 63,6 60,0 2,9 3122,8 92,4 34,1 15,3 152,2 62,9 3249,3 355,3
00 53 2 Eg 53-2,GD/00 23 1 1 3,8510 20,8410 6,1 47,3 31,2 3,8 1728,9 29,0 26,6 53,4 35,0 1757,9 171,0
00 59 1 Eg 59-1,GD/00 23 1 1 6,0500 30,0940 4,2 21,0 51,6 72,3 6,0 2231,3 64,5 20,7 76,8 78,4 2295,7 210,1
00 59 2 Eg 59-2,GD/00 23 1 1 6,0310 29,4410 4,2 19,4 88,8 24,6 2389,3 78,4 23,2 23,7 113,4 2467,7 206,7
00 68 1 Eg 68-1,GD/00 23 1 1 5,1950 26,9030 10,3 21,6 95,2 27,7 2582,9 82,6 42,1 31,9 122,9 2665,5 192,6
00 68 2 Eg 68-2,GD/00 23 1 1 5,8590 29,6400 60,0 130,7 64,5 39,3 7045,4 161,9 107,5 33,2 190,8 103,8 7314,8 537,1
00 220 1 Eg 220-1,GD/00 23 1 1 4,6400 23,3200 8,9 10,0 13,2 8,6 1349,6 88,6 254,2 34,8 19,0 21,8 1692,4 82,9
00 220 2 Eg 220-2,GD/00 23 1 1 4,6500 23,5000 15,0 27,3 67,5 26,3 2,2 20,8 2720,0 228,0 60,7 109,8 49,3 2948,0 502,9
00 314 1 Eg 314-1,GD/00 23 1 1 4,3200 21,7800 5,1 9,5 17,0 3,2 1014,4 77,3 19,5 14,5 20,2 1091,7 159,2
00 314 2 Eg 314-2,GD/00 23 1 1 4,2300 22,9800 16,8 26,3 95,5 34,9 6,5 3,6 2390,6 143,1 473,0 57,2 138,6 45,0 3006,8 152,0
00 318 1 Eg 318-1,GD/00 23 1 1 3,9100 21,4600 11,2 57,8 86,6 43,1 20,8 2441,0 13,0 50,7 155,5 63,9 2454,0 533,5
00 318 2 Eg 318-2,GD/00 23 1 1 3,3300 19,1000 16,0 101,2 160,2 47,4 6,9 22,3 3282,3 12,1 13,8 64,8 277,3 76,6 3308,2 673,4
00 321 1 Eg 321-1,GD/00 23 1 1 4,9000 26,8900 6,8 127,8 72,8 14,7 7,7 16,5 5592,5 124,4 45,1 207,5 38,9 5716,9 409,6
00 321 2 Eg 321-2GD/00 23 1 1 4,5600 23,8100 4,9 47,8 58,3 62,5 6,0 2759,0 15,8 38,4 111,0 68,5 2774,8 86,7
00 323 1 Eg 323-1,GD/00 23 1 1 4,6100 24,0900 7,6 57,6 106,4 110,6 4,3 3,7 786,4 9,7 23,3 41,6 171,6 118,6 819,4 116,2
00 323 2 Eg 323-2,GD/00 23 1 1 4,8000 24,2500 4,9 31,6 240,3 2,7 628,1 8,2 99,8 39,3 36,6 243,0 736,0 80,9
00 SED-7 GD/00 23 41 3 ,4
00 SED-8 GD/00 23 41 3 1,4 1,4 ,5
00 SED-1 GD/00 23 42 3
00 SED-5 GD/00 23 42 3 ,8 ,6 1,4 ,8
00 SED-6 GD/00 23 42 3 8,0 8,0
00 SED-2 GD/00 23 47 3 ,4 ,4 3,0 ,8 3,0 ,9
00 SED-3 GD/00 23 47 3 ,6
00 SED-4 GD/00 23 47 3 ,7
00 SED-9 GD/00 23 47 3 ,9
00 SED-10 GD/00 23 47 3 ,9 1,8 2,7 ,5
00 SED-11 GD/00 23 47 3 ,5
______________________________________________________________________________________________________________________________________________________________________________________________________________________________

145
____________________________________________________________________________________________________________________________________
Appendix D. List of samples collected in Pakistan (from Haleji in 1999, Karachi in 2000, Tounsa in 2000), and their content of organic contaminants
(ppb, or ng/g on dry weight basis). other details as in App. C.
______________________________________________________________________________________________________________________________________________________________________________________________________________________________
YEA NES EGG LAB LOC SPE TYP D_C F_C AHC GHC BHC DHC HEP HEX ALD AES BES PPDDE PPDDD PPDDT SHCB SHCH SCIC SDDT SPCB
99 7 1 Eg/N7 E1 11 1 1 3.6199 18.8827 777.0 777.0
99 10 3 Eg/N10 E3 11 1 1 3.7779 19.7001 737.0 649.0 29.0 25.0 737.0 678.0
99 12 2 Eg/N12 E2 11 1 1 4.0296 19.4736 189.0 22.0 189.0 22.0
99 22 2 Eg/N22 E2 11 1 1 3.8265 21.1493 112.0 3163.0 14.0 112.0 3163.0
99 26 1 Eg/N26 E1 11 1 1 3.2424 18.8120 858.0 338.0 24.0 858.0 338.0 5.0
99 28 1 Eg/N28 E1 11 1 1 3.7240 22.0456 209.0 57.0 274.0 14.0 266.0 274.0
99 30 1 Eg/N30 E1 11 1 1 3.6093 19.1160 264.0 9982.0 264.0 9982.0
99 31 4 Eg/N31 E4 11 1 1 3.3191 18.4169 81.0 9.0 272.0 17.0 90.0 272.0 6.0
99 1 1 Ei/N1 E1 11 2 1 5.3216 26.9168 83.7 33.3 724.7 21.4 23.4 117.0 746.1 9.1
99 2 3 Ei/N2 E3 11 2 1 4.4280 24.1392 4.1 679.7 74.5 18.2 4.1 754.2 245.7
99 4 3 Ei/N4 E3 11 2 1 4.2659 22.3245 49.8 3.7 1726.8 51.5 18.2 21.4 49.8 3.7 1796.5
99 5 1 Ei/N5 E1 11 2 1 3.4586 14.4583 294.4 4.5 3102.8 29.9 182.2 14.6 298.9 3314.9 228.1
99 8 3 Ei/N8 E3 11 2 1 5.2386 27.6142 270.1 11986.8 66.2 270.1 12053.0
99 9 2 Ei/N9 E2 11 2 1 4.7996 24.3784 87.0 2859.8 21.8 87.0 2859.8 5.5
99 11 1 Ei/N11 E1 11 2 1 4.7857 23.1663 257.0 19.0 257.0 6.0
99 20 1 Ei/N20 E1 11 2 1 4.8892 24.9102 229.0 20.0 229.0 5.0
99 21 1 Ei/N21 E1 11 2 1 4.7164 24.0854 8.0 316.0 21.0 8.0 316.0
99 24 2 Ei/N24 E2 11 2 1 4.3514 26.3145 4.0 94.0 3567.0 163.0 43.0 21.0 98.0 3773.0 8.0
99 25 3 Ei/N25 E3 11 2 1 5.5356 25.7937 253.0 20.0 253.0
99 27 1 Ei/N27 E1 11 2 1 4.8618 24.0438 3.0 202.0 21.0 3.0 202.0 6.0
99 32 2 Ei/N32 E2 11 2 1 3.2815 17.8535 3863.0 64906.0 166.0 3863.0 65072.0
99 32 3 Ei/N32 E3 11 2 1 4.1267 18.8874 9359.0 136223.0 1108.0 311.0 9359.0 137331.0
99 33 2 Ei/N33 E2 11 2 1 3.7453 19.7319 4.0 655.0 20.0 4.0 655.0 5.0
99 34 4 Ei/N34 E4 11 2 1 4.3365 23.5425 8.0 251.0 16.0 8.0 251.0 6.0
99 35 4 Ei/N35 E4 11 2 1 4.5074 23.1802 47.0 608.0 15.0 47.0 608.0 12.0
99 40 1 Ei/N40 E1 11 2 1 5.1432 26.5568 153.0 20.0 173.0 26.0
99 41 1 Ei/N41 E1 11 2 1 4.0957 17.0780 37.0 15.0 1035.0 202.0 14.0 16.0 37.0 15.0 1251.0 5.0
99 42 2 Ei/N42 E2 11 2 1 4.0621 22.0430 2.0 183.0 358.0 22.0 12.0 185.0 380.0 6.0
99 43 1 Ei/N43 E1 11 2 1 3.5344 19.8777 2.0 163.0 28.0 14.0 2.0 191.0 45.0
99 43 2 Ei/N43 E2 11 2 1 3.5819 19.4869 234.0 25.0 18.0 259.0 35.0
99 9 C1N2 11 6 1 2.5464 16.1024 132.0 132.0
99 9 C2N2 11 6 1 2.5647 15.2346 13.0 207.0 16.0 13.0 207.0 11.0
99 9 C3N2 11 6 1 2.4217 15.0663 10.0 206.0 15.0 19.0 10.0 221.0 22.0
99 9 C4N2 11 6 1 2.5479 15.9910 14.0 234.0 10.0 18.0 14.0 244.0
99 PREY 2 - Oreochromis 11 21 2 .5791 3.4117 149.3 5.6 149.3
99 PREY 3 - Oreochromis 11 21 2 .4898 3.3518
99 PREY 4 - Oreochromis 11 21 2 1.5325 8.3633 10.5 36.8 10.5
99 PREY 5 - Oreochromis 11 21 2 1.6106 8.6285 21.3 3.8 21.3
99 PREY 6 - Oreochromis 11 21 2 .6305 3.3312 33.5 1.8 33.5
99 PREY 7 - Barbus 11 21 2 1.5373 7.6788 11.6 4.7 11.6
99 PREY 8 - Glossogobiu 11 21 2 1.4202 5.4343 5.4
99 PREY 9 - Glossogobiu 11 21 2 .7732 3.2941 32.9
99 PREY 10 - Glossogobi 11 21 2 2.5968 11.5862 35.2
99 PREY 11 - Glossogobi 11 21 2 1.7272 7.9042
99 PREY 12 - Glossogobi 11 21 2 2.0190 9.3381 8.2 15.7 11.8 31.3 8.2 27.5
99 PREY 13 - Glossogobi 11 21 2 .6147 2.7931 59.7
99 PREY 16 - Colisa 11 21 2 1.0701 4.3766 12.7 12.8 10.0 25.6
99 PREY 17 - Colisa 11 21 2 .8967 3.6083 7.6 5.3 7.6 1.5
99 PREY 18 - Colisa 11 21 2 1.1740 4.6638 4.9 16.9 4.7 21.8 5.7
99 PREY 19 - Barbus 11 21 2 1.5801 6.2967 .7 2.0 13.8 35.2 .7 15.8
99 PREY (1 + 14) - Carr 11 22 2 .3026 5.9460 16.6 5.6 16.6 10.6

146
99 PREY 15 - Carridean 11 22 2 .3805 2.7981 5.7
99 SD 1 11 48 3 10.3 11.9 22.2
99 SD 2 11 48 3 1.0 1.1 1.0
99 SD 3 11 48 3 1.4
99 SD 4 11 48 3
99 SD 5 11 48 3 1.4 1.4
99 SD 6 11 48 3
99 SD 7 11 48 3 1.7
99 SD 8 11 48 3 1.2
99 SD 9 11 48 3 9.4 1.7 .4 11.1
99 SD 10 11 48 3 1.6
00 2 9 Eg 2 TB-Pak 12 1 1 3.5950 17.1640 7.7 13.5 37.2 1151.9 9.4 102.2 21.2 37.2 1263.5 34.8
00 17 9 Eg 17 TB-Pak 12 1 1 3.9440 18.2780 185.0 100.9 5.5 2890.0 35.0 518.4 185.0 106.4 3443.3 64.9
00 18 9 Eg 18 TB-Pak 12 1 1 4.3110 21.7400 4.2 113.9 428.6 332.7 15982.3 4101.9 1108.4 2.1 118.1 761.3 21192.6 665.0
00 29 9 Eg 29 TB-Pak 12 1 1 3.8900 19.2780 9.7 105.3 87.5 5.7 798.1 16.0 3.1 115.1 93.3 814.1 67.6
00 6 9 Bi 6 TB-Pak 12 4 1 4.2030 18.3260 10.4 11.4 35.8 320.8 21.8 35.8 320.8 46.9
00 14 9 Bi 14 TB-Pak 12 4 1 5.4890 24.3060 5.3 17.3 6.1 300.8 2.0 22.6 6.1 300.8 10.0
00 21 9 Bi 21 TB-Pak 12 4 1 4.3060 19.6750 6.1 22.6 58.6 321.1 28.7 58.6 321.1 13.1
00 23 9 Bi 23 TB-Pak 12 4 1 3.5690 18.9370 10.6 .7 96.3 216.3 11.2 96.3 216.3 11.8
00 25 9 Bi 25 TB-Pak 12 4 1 4.1110 21.6270 16.4 181.4 8.0 5.0 246.6 12255.7 3302.9 4.6 197.8 259.6 15558.6 1357.4
00 30 1 Bi 30a TB-Pak 12 4 1 4.8240 22.9730 9.8 .9 4.5 2.8 113.0 10.7 7.3 113.0 5.7
00 30 2 Bi 30b TB-Pak 12 4 1 4.6790 23.2730 6.9 5.0 84.5 3.9 173.2 2.8 11.9 88.4 173.2 6.2
00 31 9 Bi 31 TB-Pak 12 4 1 4.4860 20.8950 5.9 5.1 68.5 181.9 11.0 68.5 181.9 12.1
00 35 9 Bi 35 TB-Pak 12 4 1 3.7390 21.8000 162.1 162.1
00 54 9 Bi 54 TB-Pak 12 4 1 4.0750 21.9030 9.3 12.6 15.1 3.3 136.7 3.6 22.0 18.4 136.7 25.7
00 Prey/TFI TB-Pak 12 21 2 69.3 9.1 78.4 7.4
00 Prey/TFR TB-Pak 12 25 2 61.9 8.4 61.9 8.4 6.5
00 Prey/TMO TB-Pak 12 26 2 6.0
00 Prey/TIN TB-Pak 12 27 2 10.6 10.6 9.0
00 Prey/TCR TB-Pak 12 29 2 2.8 12.6 2.8 12.6 6.8
00 SED/P1 TB-Pak 12 43 3 67.7 67.7 .6
00 SED/P2 TB-Pak 12 43 3 7.4 7.4 .5
00 SED/P3 TB-Pak 12 43 3 .7 .7 .9
00 SED/RF1 TB-Pak 12 44 3 10.3 10.3
00 SED/RF2 TB-Pak 12 44 3 .5
00 SED/RF3 TB-Pak 12 44 3 5.9 5.9
00 SED/C1 TB-Pak 12 45 3 .7
00 SED/C2 TB-Pak 12 45 3 .3
00 SED/C3 TB-Pak 12 45 3 1.3 1.3 .8
00 1 1 Egu 1A KGB-Pak 13 3 1 5.9600 23.9300 19.0 24.2 46.0 36.8 1797.4 199.4 13.3 43.2 82.7 1996.8 2994.3
00 1 2 Egu 1B KGB-Pak 13 3 1 3.9400 21.6900 5.3 14.6 14.5 5.4 1420.2 4.4 19.9 19.9 1420.2 2196.8
00 2 1 Egu 2A KGB-Pak 13 3 1 4.3000 20.2600 11.5 1593.4 64.4 58.9 11.5 1657.8 2636.6
00 2 2 Egu 2B KGB-Pak 13 3 1 3.5000 13.3800 11.6 13.0 121.4 9.4 1755.7 142.4 3.8 24.5 130.7 1898.1 3170.9
00 5 1 Egu 5A KGB-Pak 13 3 1 3.8000 19.7800 16.1 18.2 76.5 71.9 1863.2 373.0 10.1 34.3 148.4 2236.2 2988.2
00 5 2 Egu 5B KGB-Pak 13 3 1 3.2700 18.1700 13.9 21.2 30.4 64.2 1785.4 298.6 12.0 35.1 94.5 2084.0 3484.2
00 9 1 Egu 9A KGB-Pak 13 3 1 5.1000 24.0700 10.2 15.3 71.6 19.7 1929.1 244.1 12.6 25.5 91.3 2173.2 6184.8
00 9 2 Egu 9B KGB-Pak 13 3 1 4.3100 22.4700 12.0 22.1 40.7 31.6 2139.4 417.4 16.6 34.1 72.3 2556.8 7321.5
00 21 1 Egu 21A KGB-Pak 13 3 1 4.8400 24.9700 10.4 47.5 100.5 9.0 63.5 3401.7 431.7 14.4 58.0 173.0 3833.4 6977.4
00 21 2 Egu 21B KGB-Pak 13 3 1 3.9900 21.4300 6.5 29.3 74.2 14.2 11.6 2728.7 328.1 8.1 35.7 99.9 3056.9 4515.1
00 50 1 Egu 50A KGB-Pak 13 3 1 3.6200 19.5500 16.3 35.9 131.8 7.8 52.9 745.5 3780.9 467.0 11.9 52.1 938.0 4247.9 6239.9
00 50 2 Egu 50B KGB-Pak 13 3 1 3.9400 21.6900 10.1 86.0 17.1 20.0 228.2 31.6 101.8 10.1 123.1 361.6 64.5
00 53 1 Egu 53A KGB-Pak 13 3 1 4.9700 25.9100 38.6 37.7 78.6 106.4 3347.0 591.2 76.3 185.0 3938.1 5764.7
00 53 2 Egu 53B KGB-Pak 13 3 1 4.4300 24.5400 10.2 27.8 58.9 18.2 2644.0 495.5 10.2 38.0 77.1 3139.5 4548.5
00 54 1 Egu 54A KGB-Pak 13 3 1 4.1700 20.2500 17.4 20.6 99.6 38.5 2465.9 378.5 21.7 38.0 138.1 2844.5 5646.5
00 54 2 Egu 54B KGB-Pak 13 3 1 4.6000 21.8000 8.4 11.7 19.9 21.2 2078.9 269.1 8.9 20.1 41.0 2348.0 4764.8
00 56 1 Egu 56A KGB-Pak 13 3 1 4.8400 23.9200 53.9 72.3 131.9 35.5 19.6 4695.0 472.0 126.2 187.0 5167.0 8277.0
00 56 2 Egu 56B KGB-Pak 13 3 1 4.8800 24.7600 14.1 59.0 85.6 32.9 13.2 5162.2 336.5 26.6 73.1 131.7 5498.6 8440.8
00 57 1 Egu 57A KGB-Pak 13 3 1 5.0000 26.3900 33.5 23.2 14.3 63.0 1887.9 180.8 56.7 77.3 2068.7 3617.3
00 57 2 Egu 57B KGB-Pak 13 3 1 4.9500 25.9900 14.4 15.9 60.7 18.5 1473.8 263.2 16.8 30.3 79.2 1737.0 2321.7

147
00 58 1 Egu 58A KGB-Pak 13 3 1 4.7300 23.0500 5.8 33.8 105.8 11.1 3072.5 5.3 39.6 116.9 3072.5 4643.7
00 58 2 Egu 58B KGB-Pak 13 3 1 4.2600 21.1100 14.9 28.6 92.8 9.0 438.6 2676.5 245.2 8.8 43.5 540.4 2921.7 3138.4
00 59 1 Egu 59A KGB-Pak 13 3 1 3.6700 17.9700 7.1 830.7 13.0 717.7 3407.2 548.6 6.7 837.8 730.6 3955.8 7331.6
00 59 2 Egu 59B KGB-Pak 13 3 1 4.0300 19.0200 22.3 33.5 101.4 11.3 17.7 4002.6 587.2 23.7 55.8 130.4 4589.8 8763.4
00 61 1 Egu 61A KGB-Pak 13 3 1 3.4200 20.3600 21.6 83.8 3399.7 208.1 21.6 83.8 3607.8 3993.9
00 61 2 Egu 61B KGB-Pak 13 3 1 3.6300 21.0500 20.4 6.9 176.2 18.8 49.8 719.5 3569.4 473.1 12.6 27.4 964.2 4042.5 5613.2
00 62 1 Egu 62A KGB-Pak 13 3 1 4.5900 21.4600 25.7 20.3 57.3 25.5 1009.2 272.5 46.1 82.8 1281.7 1482.8
00 62 2 Egu 62B KGB-Pak 13 3 1 7.5300 23.9000 41.5 36.5 83.0 15.9 316.7 1482.5 487.0 78.0 415.6 1969.5 2117.3
00 Prey/F1 KGB-Pak 13 21 2 231.2 11.1 21.5 231.2 32.6 6.6
00 Prey/F2 KGB-Pak 13 21 2 146.2 9.3 20.3 146.2 29.6 6.4
00 Prey/F3 KGB-Pak 13 21 2 349.5 10.0 24.4 349.5 34.4 4.5
00 SED/OC1 KGB-Pak 13 45 3 1.4 2.0 5.5 1.4 7.5 .6
00 SED/OC2 KGB-Pak 13 45 3 .9 2.7 3.6 .5
00 SED/OC3 KGB-Pak 13 45 3 .8
00 SED/CK1 KGB-Pak 13 45 3 .4 .4 1.9
00 SED/CK2 KGB-Pak 13 45 3
00 SED/CK3 KGB-Pak 13 45 3
00 SED/GB1 KGB-Pak 13 46 3 1.3 6.9 19.3 1.3 26.3 4.3
00 SED/GB2 KGB-Pak 13 46 3 1.1 22.7 85.1 19.7 1.1 127.4 63.4
00 SED/GB3 KGB-Pak 13 46 3 1.3 4.5 5.7
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148