Ecotoxicology (2009) 18:312318

DOI 10.1007/s10646-008-0285-y

Effects of zinc and cadmium on oxygen consumption and

ammonium excretion in pink shrimp (Farfantepenaeus paulensis,
Perez-Farfante, 1967, Crustacea)
Edison Barbieri

Accepted: 12 November 2008 / Published online: 25 November 2008

Springer Science+Business Media, LLC 2008

Abstract In Brazil, pink shrimp (Farfantepenaeus paulensis) is an important commercially exploited species and is
an ideal animal for studying the impairment caused by the
effects of heavy metals that are often detected in coastal
areas. The main purpose of the present study was to detect
the acute toxicity of cadmium and zinc to F. paulensis and
investigate their effects on oxygen consumption and
ammonium excretion, investigations that have not been
carried out in this species before. First, the acute toxicity of
zinc and cadmium to F. paulensis for 24, 48, 72, and 96 h
medium lethal concentration was examined, which resulted
in the following values: 9.39, 6.00, 4.88, and 3.31 mg/l for
zinc and 2.35, 1.67, 1.26, and 0.83 mg/l for cadmium. Furthermore, we also found that exposure of shrimp to zinc and
cadmium caused an inhibition in oxygen consumption of 25
and 32.4%, respectively, relative to the control. In addition,
after separate exposure to cadmium and zinc, elevations in
ammonium excretion were obtained, which were 42.85 and
51.85% higher than the control, respectively.
Keywords Farfantepenaeus paulensis
Cadmium

Zinc
LC50
Oxygen consumption

Ammonium excretion
Shrimp

Introduction
Heavy metals are the most common pollutants appearing in
many coastal areas worldwide (Joyeux et al. 2004). The
ecological and public health problems caused by the use of
E. Barbieri (&)
Instituto de Pesca-APTA-SAA/SP, Caixa Postal 61, Cananeia,
SP 11990-000, Brazil
e-mail: edisonbarbieri@yahoo.com.br

123

heavy metals has captured the attention of worldwide

environmental organizations. In Brazil, the use of heavy
metals has not yet reached the same proportions that
characterize them as water pollutants in developed countries. Nevertheless, a deep concern is expressed by the
environmental authorities regarding pollution by heavy
metals in certain places and the necessity of preventive
actions with the objective of avoiding future problems.
In Brazil, heavy metals enter the coastal seawater mainly
through the discharge of industrial effluents and the disposal
of wastewater (Barbieri et al. 2004; Damato and Barbieri
2003). High concentrations of heavy metals have been
reported in Brazilian coastal waters (Silva et al. 2006), rivers
and their estuaries (Eysink et al. 1988a, b), and in the tissues
of coastal marine organisms (Carvalho et al. 2000, 2001).
Silva et al. (2006) recorded in the Santos Estuary (Sao Paulo
State, Brazil) 1.6 mg kg-1 of Cd and 466 mg kg-1 of Zn in
the sediment. Cadmium and zinc have been widely recognized as highly toxic when dissolved and in ionic form
(Mance 1987). Zinc and cadmium are very common and
persistent heavy metals in aquatic environments and known
to be highly toxic to marine and estuarine crustaceans
(Papathanassion 1983; Wu and Chen 2004). Zinc is an
essential trace element, in excess of low to medium toxicity.
Cadmium has no essential biological function and is extremely toxic to several organisms. Chronic exposure to
cadmium will cause it to accumulate in the body, particularly in the kidneys and the liver (Williams et al. 1999).
Exposure to heavy metals in aquatic environment produces many physiological changes in crustaceans, including
alterations to their metabolism (Barbieri et al. 2005). These
effects are related to their mechanism of action and,
therefore, are specific for each metal. The metabolic rate of
an organism is a useful and sensitive indication of its daily
consumption of energy. Therefore, in aerobic organisms,

Toxicity of Zn and Cd on Farfantepenaeus paulensis

the quantification of the rate of oxygen consumption will be

directly associated with the amount of energy released from
the oxidation of food substratum. Based on the amount of
oxygen consumed by an animal for a certain period of time,
it is possible to evaluate the energy spent during the same
period to maintain its vital processes (Barbieri 2007).
Evaluation of oxygen consumption and ammonium
excretion was used, for example, to study toxic effects
caused by aromatic compounds (Lemaire et al. 1996),
heavy metals (Barbieri et al. 2005; Wu and Chen 2004),
detergents (Barbieri et al. 1998, 2000, 2002; Christiansen
et al. 1998), and a variety of toxicants (Boudou and Ribeyre 1989).
Pink shrimp (Farfantepenaeus paulensis), found in the
eastern shores of the South America (DIncao 1991) is an
important economic resource. It is also cultivated in Brazilian coastal areas. However, coastal seawater is often
contaminated by heavy metal and others pollutants. Hence,
the impacts of heavy metal should be considered, not only
on cultured shrimp but also the shrimp culture industries
and human health (Wu and Chen 2004).
Heavy metal effects on the respiratory rate of marine
and estuarine organisms have not been extensively studied
(St-Amand et al. 1999; Barbieri 2007). The objective of the
present study was, therefore, to investigate the effect of the
acute toxicity of cadmium and zinc on the oxygen consumption and ammonium excretion of F. paulensis, a
euryhalinic and eurythermal shrimp and an important
commercially exploited species in Brazil, at 20C and 36%
salinity.

Material and methods

The acute toxicity of cadmium and zinc to post-larvae of
shrimp (F. paulensis) cultivated in the laboratory of Instituto de Pesca exposed to different concentrations of these
chemicals for a period of up to 96 h was evaluated, taking
into consideration the economic and ecological importance
of this species and the problems related to pollution in
estuarine regions. A total of 360 larvae of cultivated
shrimp, with 1.8 0.4 g median wet weight and
2.4 0.5 cm total length were used. Groups of 15 individuals were put in 50-l tanks containing seawater at 36%
salinity. The seawater was reconstituted using sea-salt of
Cabo Frio, Rio de Janeiro (Brazil). Three replicates of
groups of 15 individuals were exposed to each one of the
following concentrations of zinc and cadmium: 0.00, 0.10,
1.00, 2.50, 5.00, 10.00, 20.00 and 40.00 mg/l. Dead shrimp
were removed from the tanks and counted at 24, 48, 72,
and 96 h of exposure. The lethal concentration (LC50 with
95% confidence limits) was calculated by Probit analysis
(Zagatto and Bertoletti 2006).

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One hundred and fifty shrimp (F. paulensis), of 2.27

(0.5) g and 1.82 (0.36) cm average, were used for the
routine metabolism measurements using sealed respirometers. The respirometer was made in our laboratory, with
tube of acrylic and covers of PVC. Ten shrimp were subjected individually to oxygen consumption measurements
in one of the concentrations of cadmium (0.0, 0.1, 0.5, 1.0,
and 2.0 mg/l) and zinc (0.0, 0.5, 1.0, 2.0, and 3.0 mg/l).
The pH and oxygen concentration of the test solution at the
different concentrations of ZnSO4 and CdCl2 (0.0, 1.0, 2.5,
and 10 mg/l) were determined; the range of pH values was
7.908.22. The range of oxygen values was 6.206.25 ml
oxygen/l.
Before beginning the experiments, the animals were
maintained in the respirometer with continuous water circulation for at least 90 min to attenuate the handling stress.
Then, the water supply was suspended and the respirometer
closed, so that the shrimp could consume the present
oxygen in the known water volume for a period of 3 h. The
respirometers were protected by a barrier to isolate the
animals from possible movement in the laboratory. The
difference between the oxygen concentrations determined
at the beginning and end of the confinement was used to
calculate the consumption during the period. To minimize
the effect of low oxygen concentration and metabolite
accumulation on the metabolism, the experiment duration
was regulated, so that the oxygen concentration by the end
of experiments was above 70% of its initial concentration.
The dissolved oxygen was determined through the Winkler
Method (Winkler 1888).
To obtain the desired concentration of Zn and Cd, the
necessary volume of the main (mother) substance (1 mg/
Zn/ml or 1 mg/Cd/ml) was calculated for each volume of
respirometer and set with a (micropipet) help at the end of
the acclimation. As soon as substance was added, the entry
orifice was immediately sealed. Additionally, the seawater
in the bottle was sampled at the beginning and end of the
oxygen consumption analysis. Determination of ammonium-nitrogen in the seawater was based on the
phenolhypochlorite method (Solarzano 1969). The average
oxygen-specific consumption and ammonium excretion by
the shrimp was assessed using analysis of variance. All
data were analyzed using the Tukeys multiple comparisons test (P \ 0.05).

Results
Mortality
The percent mortality of F. paulensis exposed to zinc and
cadmium at each 24-h interval is shown in Tables 1 and 2.
No deaths of control animals were observed. The higher the

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E. Barbieri

concentration of metal the shrimp were exposed to, the

higher the mortality observed. After being exposed to
cadmium, death was first observed at a concentration of
1.0 mg Cd/l in the first 24 h. Mortality rates of 100% were
observed after a 24-h exposure at concentrations of
10.0 mg Cd/l and were also 100% after 96 h at a concentration of 5.0 mg Cd/l. Only 22.22% average mortality was
observed during the first 24 h at 5.0 mg Zn/l, while 100%
mortality rates during the first 24 h were recorded at
40.0 mg Zn/l.
Medium lethal concentration
The acute toxicity of zinc to shrimp larvae exposed to
different concentrations of this metal for periods of up to
96 h, expressed as the medium lethal concentration (LC50),
was 9.39, 6.00, 4.88, and 3.31 mg/l for the 24-, 48-, 72-,
and 96-h exposure, respectively (Table 1). The LC50 values
for cadmium were 2.35, 1.67, 1.26 and 0.83 mg/l for 24,
48, 72, and 96 h, respectively (Table 2).
Oxygen consumption and ammonium excretion
For shrimp acclimated to a temperature of 20C, the specific oxygen consumption decreased with an increase in
zinc concentration. The average of specific oxygen consumption of shrimp exposed to 2.5, 5.0 and 10 mg Zn/l was
0.00463, 0.00404, and 0.00372 ml oxygen/g/min, respectively (Fig. 1). These values represent a metabolic level
decrease of 6.65, 18.54, and 25.00%, relative to the control.
After exposure for 3 h, the average levels of ammonium

Fig. 1 Variation of shrimp specific oxygen consumption at different

zinc concentrations. The bars are the respective standard deviations
(n = 5)

excreted by F. paulensis exposed to 5.0 and 10 mg Zn/l

were 25.00 and 42.85% higher compared with the average
amount of the control animals (Fig. 2).
Using Tukeys statistical test (P \ 0.05) it was verified
that the average oxygen consumption and ammonium
excretion at zinc concentrations of 5.0 and 10 mg/l was
significantly different from the control (0.0 mg/l). At 1.0
and 2.5 mg Zn/l, there was no significant difference.
The results shown in Fig. 3 clearly reveal inhibitory
effects on oxygen consumption caused by 1.0 mg Cd/l,
which is close to their 3-h LC50 values. The F. paulensis
consumed different quantities of oxygen at different

Table 1 Percent mortality (%) of F. paulensis exposed to various zinc concentrations for 96 h and its medium lethal concentration (LC50 with
95% confidence limits) calculated by Probit analysis
Exposure time (h)

LC50 (mg Zn/l)

Zinc concentration (mg Zn/l)

0

0.1

24

0.0

0.0

48

0.0

0.0

72

0.0

0.0

96

0.0

0.0

1.0

2.5

5.0

10

20

0.0

11.11

22.22

44.44

11.11

11.11

22.22

88.88

11.11

22.22

33.33

11.11

22.22

44.44

40
100

9.39 (6.0614.54)

100

77.77

100

6.00 (3.749.63)

100

100

100

4.88 (2.938.13)

100

100

100

3.31 (1.567.13)

Table 2 Percent mortality (%) of F. paulensis exposed to various cadmium concentrations for 96 h and its medium lethal concentration (LC50
with 95% confidence limits) calculated by Probit analysis
Exposure time (h)

LC50 (mg Cd/l)

Cadmium concentration (mg Cd/l)

0

0.1

1.0

2.5

5.0

10

20

40

24

0.0

0.0

22.22

44.44

55.55

100

100

100

2.35 (1.334.15)

48

0.0

0.0

33.33

55.55

66.66

100

100

100

1.67 (0.903.07)

72

0. 0

11.11

33.33

66.66

88.88

100

100

100

1.26 (0.572.78)

96

0.0

22.22

44.44

77.77

100

100

100

0.83 (0.272.60)

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100

Toxicity of Zn and Cd on Farfantepenaeus paulensis

Fig. 2 Variation of shrimp ammonium excreted at different zinc

concentrations. The bars are the respective standard deviations
(n = 5)

315

Fig. 4 Variation of shrimp ammonium excretion at different cadmium concentrations. The bars are the respective standard deviations
(n = 5)

averages at concentrations of 0.5, 1.0, and 2.0 mg/l of

cadmium are significantly different from the control
(0.0 mg/l). At 0.1 mg Cd/l, there was no significant
difference.

Discussion

Fig. 3 Variation of shrimp specific oxygen consumption at different

cadmium concentrations. The bars are the respective standard
deviations (n = 5)

cadmium concentrations. After exposure to 0.5 mg Cd/l for

3 h, levels of oxygen consumed by treated F. paulensis
were obviously lower than those of control individuals.
During the 3 h of the experiment, the average levels of
oxygen consumed by F. paulensis exposed to 0.5, and 1.0
and 2.0 mg Cd/l were 10.00, 26.40, and 32.40% lower than
the control, respectively (Fig. 3). Unlike the inhibition of
oxygen consumption, exposure to 2.0 mg Cd/l for 3 h
caused elevations in the levels of ammonium excreted by
F. paulensis. After exposure for 3 h, the average levels of
ammonium excreted by F. paulensis treated with 1.0 and
2.0 mg Cd/l were 37.03 and 51.85% respectively, above
the average amount of the control animals (Fig. 4).
Using Tukeys statistical test (P \ 0.05), it was found
that the oxygen consumption and ammonium excretion

The toxicity of heavy metals for crustaceans has been

studied by several authors (Mance 1987; Vanegas et al.
1997; Wong et al. 1993; Wu and Chen 2004). The results
of this study confirm that the heavy metals zinc and cadmium are toxic to F. paulensis, an ecologically and
economically important shrimp in the coastal waters of
South America. In this study when comparing the zinc and
the cadmium, the most acutely toxic metal was cadmium.
The toxicity of zinc and cadmium to marine crustaceans
is well-documented, but not for F. paulensis. For example,
the 96-h LC50 of cadmium for Litopenaeus vannamei was
1.07 mg/l (Wu and Chen 2004) and for Litopenaeus schimitti was 0.18 mg/l (Barbieri 2007). In addition, 96-h LC50
values of cadmium for larvae of Cancer irroratus and
Paragrapsus quadridentatus are 0.25 and 0.49 mg Cd/l
(Banijts-Claus and Benijts 1975; Martin et al. 1981).
Likewise, the 96-h LC50 of zinc is 1.35 mg/l for larvae of
L. vannamei (Wu and Chen 2004) and 43.87 mg Zn/l for
Penaeus setiferus (Vanegas et al. 1997). In this study,
cadmium exhibited greater toxicity to F. paulensis than
zinc. Barbieri (2007) worked with another prawn species,
L. schmitti, and discussed that the greater toxicity of cadmium might be expected, because zinc is an essential metal
that is regulated by decapod crustaceans, whereas cadmium
has no known biological function.

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Studies on the effect of heavy metals on the respiration of

decapod crustaceans demonstrated that the decrease in
oxygen consumption rates was related to concentration,
exposure time, and larval stage (St-Amand et al. 1999;
Barbieri et al. 2005; Barbieri 2007). When fiddler crab
(Uca pugilator) larvae were exposed to 180 lg/l (180 ppb)
mercury for 6 h, DeCoursey and Vernberg (1972) observed
an oxygen consumption decrease of 28% for the zoeae III
stage and 62% for the zoeae V stage. McMahon (2001), in
a review of the responses of aquatic crustaceans in low
ambient dissolved oxygen, mentioned that many crustaceans possess an excellent regulatory ability in their
oxygen consumption patterns and thus were called oxygen
regulators. The present experiments also demonstrated that
oxygen consumed by F. paulensis showed no linear relationship to ambient oxygen levels, regardless of whether
the shrimp were exposed to a heavy metal. Despite their
regulatory capability, the oxygen consumption rate was
indeed inhibited after F. paulensis was exposed to high
concentrations of cadmium. Similar results were also
observed in different shrimp species (Chinni et al. 2002;
St-Amand et al. 1999; Wu and Chen 2004).
Respiratory impairment in crustaceans resulting from
exposure to heavy metals was also reviewed (Spicer and
Weber 1991), and it was concluded that oxygen consumption generally decreases when crustaceans are
acutely exposed to heavy metals. In addition, after exposure to a sublethal concentration (1.44 mg/l) of lead for
30 days, it was evident that lead inhibits oxygen consumption in Penaeus indicus; similar results have been
obtained with other crustaceans studied (Chinni et al.
2000). Those authors assumed that cytological damage
should be related to the decrease in oxygen consumption,
because the gills are most likely the first target of waterborne heavy metals, including thickening of bronchial
epithelium and deep changes in hemolymph patterns in the
gills, with a concomitant increase in vacuolization and
reduced hemolymph spaces, causing perfusion stagnation.
Cytological and histological damage caused by heavy
metal exposure in Penaeus japonicus was also reported
(Soegianto et al. 1999a, b). For example, when P. japonicus were exposed to different concentrations of heavy
metals, the following could be observed: an increased
number of nephrocytes in gill filaments; a blackened
appearance of the gills; necrosis of gill cells resulting in
narrowed or obstructed hemolymphatic vessels; the
appearance of a space between the cuticle and the epithelial cells, which contain black electron-dense material;
and even fragmentation of nuclei within gill cells. Thus,
the main pathological effect on the respiratory system
caused by cadmium is the interference with the respiratory

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E. Barbieri

system, including cellular respiration (Koizumi et al.

1994; Spicer and Weber 1991).
Depending on nutritional conditions, ammonium is one
of the final products following catabolism, principally of
amino acids that might have an alimentary or muscular
origin (Mayzaud and Conover 1988). In addition to being
used as energy substrates and components of body structures, amino acids can be more important than ions in the
maintenance of osmotic pressure in prawns, such as
P. setiferus (McFarland and Lee 1963; Rosas et al. 1999).
Typically, increases in ammonium excretion reflect an
increase in catabolism of amino acids. However, when
exposed to lethal concentrations of heavy metals, dysfunction of ammonium excretion control follows gill
damage. Chinni et al. (2000, 2002) found that ammonium
excretion was inhibited in P. indicus postlarvae exposed to
sublethal concentrations of lead. Although there is still no
confirmed evidence, it is assumed that the decrease in
ammonia-nitrogen excretion by P. indicus postlarvae in the
presence of toxicants can be attributed to a reduction in the
metabolic rate or to an interaction of lead with pathways
for the production of ammonia-nitrogen. Differences in the
present study may be a result of the metals used and their
concentrations, shrimp species used, and other abiotic
factors, such as salinity and temperature. However, much
effort still needs to be devoted to determining the relationship between heavy metal exposure and ammonium
excretion to verify these questions.
In Metapenaeus ensis, there was a clear decrease in
sensitivity to heavy metals during development from protozoea to postlarvae. Other studies have also confirmed that
tolerance to pollutants increases with age in marine crustaceans. Penaeus monodon showed a progressive increase
in tolerance to ammonia (Chin and Chen 1987) and nitrite
(Chen and Chin 1988) as the larvae developed from nauplii
to postlarvae.
From an ecotoxicological point-of-view, the concentrations used in this study that caused significant effects on the
measured parameters can potentially be found by shrimps
in their natural environment. The zinc and cadmium concentration reported in sediments and suspended material
from the Santos estuary (Santos, Brazil) averages 1.7 and
2600 lg/g in the more polluted areas (Zagatto and Bertoletti 2006). Although F. paulensis lives along the Brazilian
coast (DIncao 1991), the potential risk of cadmium for this
species should be seriously considered, especially taking
into account that F. paulensis is a detritivore, sedimentconsumer species. Cadmium and zinc, like other heavy
metals, present a high absorption to fine sediments, such as
clay, abundant in the bottom and coastal areas of the
mentioned estuary.

Toxicity of Zn and Cd on Farfantepenaeus paulensis

Conclusion
In this study, zinc and cadmium showed elevated toxicity
to F. paulensis. Cadmium and zinc caused an inhibition in
oxygen consumption of 25 and 32.4%, relative to the
control. However, after separate exposure to zinc and
cadmium, elevations in ammonium excretion were
observed that were 42.85 and 51.85% higher than the
control. Results show that F. paulensis is a good test
organism for studying heavy metal pollution and good test
organism for in situ assessment of water pollution as
opposed to bench tests. Our future work will focus on both
the acute effects of these heavy metals on F. paulensis at
other biological levels, such as histological and biochemical levels, and chronic effects on metabolism, molting,
effects of heavy metals in different temperatures, salinity
levels and growth rates which are also very important for
the prawn culture industry.
Acknowledgment I would like to thank the FAPESP (processo
2007/50147-7), for their support during the undertaking of this study.

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