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Estuarine, Coastal and Shelf Science 82 (2009) 566572

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Estuarine, Coastal and Shelf Science


journal homepage: www.elsevier.com/locate/ecss

Articial mouth opening fosters anoxic conditions that kill small estuarine sh
Alistair Becker a, *, Laurie J.B. Laurenson a, Kylie Bishop a, b
a
School of Life and Environmental Science, Deakin University, P.O. Box 423, Warrnambool, Victoria 3280, Australia
b
South Coast Natural Resource Management, P.O. Box 1801, Esperance, Western Australia 6450, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Fish kills are not uncommon within estuaries in many regions of the world. In seasonally open systems,
Received 4 March 2008 which are common in temperate areas, they are often associated with mouth openings. Such a kill
Accepted 17 February 2009 occurred in July 2005 in the Surrey Estuary following a closed mouth period of seven months resulting in
Available online 26 February 2009
the loss of many thousands of sh. At the time the sh community within the estuary was under
investigation which provided comprehensive data of this population prior to the kill. Monthly water
Keywords:
quality monitoring was also being conducted prior to the kill and also carried out on a daily basis
dissolved oxygen
following the mouth opening. The Surrey was stratied during the closed mouth phase, isolated waters
stratication
Australia below the halocline had stagnated and become anoxic. As a result only waters above the halocline
seasonally open estuary contained oxygen concentrations capable of sustaining most sh. It appears that if a mouth opening
happens under low ow conditions, a shearing effect occurs within the water column where surface
waters ow out to sea leaving deeper waters behind. This resulted in only anoxic waters being present
for in excess of six days and was responsible for the sh kill. Fish sampling of the Surrey Estuary was
conducted three and six months following the kill and those data were compared to that collected in the
12 months prior to the event. Three months after the kill few sh were collected within the estuary and
included marine opportunists near the mouth and estuarine resident species in the far upper reaches of
the system. However six months following the kill large numbers of estuarine resident species were
collected throughout the Surrey Estuary. As many species were euryhaline, it is believed that some
individuals migrated into freshwater reaches of the Surrey to escape the anoxic conditions within the
estuary. As conditions improved they recolonised the Surrey Estuary. The high fecundity and rapid
growth of these small, short lived species probably aided in their re-establishing populations within the
estuary. It is clear from this research that articial openings of estuaries should be avoided during low
ow periods when oxygen concentrations are low. It also appears that many of the small estuarine
resident species common in seasonally open estuaries are capable of recolonising estuaries following sh
kills. The effects on larger, longer lived resident species are not known but likely to be more detrimental
due to longer time required for them to reach sexual maturity.
2009 Elsevier Ltd. All rights reserved.

1. Introduction may be inaccurate because they generally rely upon visual surveys
(Steffe et al., 2007).
Fish kills are common in estuaries and have been linked to Although estuarine sh kills occur regularly worldwide, their
changes in salinity, temperature and oxygen (Bennett, 1985; Rus- impact on sh populations is rarely investigated and reported
sell, 1994; Whiteld, 1995; Dawson, 2002; Sloan and Kamer, 2005; within the peer reviewed literature. This may be due to difculties
Hoeksema et al., 2006) as well as toxic dinoagellates (Burkholder in accurately determining the scope and extent of the kill due to
et al., 1992; Burkholder et al., 1995). Estimates on the number of sh a lack of suitable temporal data prior to the event. Collection of such
killed in specic instances range from a few thousand (Russell, data is seldom the case as it is generally not known a kill is going to
1994) to more than one million (Hoeksema et al., 2006), however occur until after the fact (Steffe et al., 2007). As such, a paucity of
information exists on the true extent of estuarine sh kills and how
quickly populations are able to recover or recolonise estuaries.
Many sh kills occur in seasonally or intermittently open estu-
* Corresponding author. Present address: South African Institute for Aquatic
aries where connectivity between marine and estuarine environ-
Biodiversity, Private Bag 1015, Grahamstown 6140, South Africa. ments is blocked for a period of time by a sandbar at the mouth
E-mail address: a.becker@saiab.ac.za (A. Becker). (Roy et al., 2001; Harrison and Whiteld, 2006). These sandbars

0272-7714/$ see front matter 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2009.02.016
A. Becker et al. / Estuarine, Coastal and Shelf Science 82 (2009) 566572 567

Fig. 1. Map of the Surrey Estuary showing the six water quality sampling stations (S1S7), the location of the D.O. logger, the main channel (dark grey) and oodzones (light grey)

may block and close the mouth for protracted periods of time, often at the mouth of the closed estuary linking it to the ocean. These
resulting in a deterioration of estuarine water quality. Current openings are generally conducted to relieve ooding which
projections of climate change forecast a probable reduction in occurs due to the damming effect created by the closed mouth
rainfall across temperate regions such as southern Australia and which can result in water levels within the estuary being more
Africa (Schulze et al., 2001; Hughes, 2003). These forecasts would than 1.7 m above mean sea level (or 1.7 AHD). In July 2005,
lead to reduced ows into estuaries resulting in seasonally and following an extended period of closure (seven months), the
seasonally closed systems becoming isolated from the marine estuary was articially opened, subsequently resulting in a sh
environment more regularly and potentially increasing water kill. At the time, the small sized sh community within the
quality problems. If these projections are accurate, without careful Surrey Estuary was under investigation as part of an ongoing
management, sh kills may occur on a more regular basis. research project (Becker and Laurenson, 2007, 2008). As such,
The Surrey Estuary is a small, seasonally open, micro-tidal monthly surveys of sh were taken between July 2004 and June
estuary on the south facing coast of Western Victoria (141 2005. These studies provide a comprehensive picture of the
4201000 E, 38 150 3500 S). It has a history of sh kills that appear to composition and relative abundance of the sh community prior
be associated with the articial opening of its mouth (Barton and to the sh kill event of July 2005.
Sherwood, 2004). Articial opening of the mouth generally This study aims to investigate and identify the cause of the July
involves the use of a backhoe to dig a trench through the sandbar 2005 sh kill within the Surrey Estuary from water quality data

Table 1
Fish species recorded within the Surrey Estuary and the numbers collected prior to and following the July 2005 sh kill. * Samples collected during independent surveys. U
Indicates dead specimens of these species were collected during the sh kill.

Jul- Aug- Sep- Oct- Nov- Dec- Jan- Feb- Mar- Apr- May- Jun- Fish kill Sep- Mar- Aug-06 Sep-07
04 04 04 04 04 04 05 05 05 05 05 05 mortalities 05 06 * *
Acanthopagrus butcheri (black bream) 35 0 2 1 2 1 77 22 8 17 5 15 U 0 29 7 8
Afurcagobius tamarensis (Tamar River goby) 0 0 0 0 0 0 0 1 3 2 4 0 0 1 0 0
Aldrichetta forsteri (yellow eye mullet) 18 2 9 0 4 0 0 28 1 1 0 2 U 17 4 6 0
Amoya bifrenatus (bridled goby) 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Anguilla australis (short nned eel) 0 16 27 25 31 1 0 1 0 0 0 0 U 6 0 1 2
Arripis trutta (Australian salmon) 0 0 0 0 0 0 0 0 2 0 0 0 U 0 1 0 2
Atherinosoma microstoma (small mouth 177 36 274 11 72 19 88 699 306 119 333 13 U 0 399 11 76
hardyhead)
Galaxias maculatus (common galaxias) 121 31 61 6 258 348 38 37 23 11 28 1 U 0 8 20 0
Nannoperca australis (southern pigmy 0 0 1 3 0 0 1 0 0 0 0 0 0 0 0 0
perch)
Philypnodon grandiceps (at-head gudgeon) 39 36 60 295 145 197 574 390 391 501 479 114 U 10 379 146 386
Pseudaphritis urvillii (tupong) 0 1 1 1 0 1 27 3 4 3 0 4 U 0 0 0 0
Pseudogobius olorum (blue spot goby) 47 94 327 112 62 73 185 28 46 26 12 29 U 24 162 95 13
Retropinna semoni (southern smelt) 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0

Total 438 216 762 454 574 641 990 1209 784 680 861 178 57 983 286 487

Prior to Fish Kill After Fish Kill


568 A. Becker et al. / Estuarine, Coastal and Shelf Science 82 (2009) 566572

D.O. (mg/l)
5 July 2005 11 July 2005
0 2 4 6 8 10 0 2 4 6 8 10
0 0

-1 -1

Site1
-2 Site2 -2
Site3 Mouth Opened
-3 Site4 -3
Site5
-4 Site6 -4
Site7
-5 -5

12 July 2005 13 July 2005


0 2 4 6 8 10 0 2 4 6 8 10
0 0

-1 -1
Depth (m)

-2 -2

-3 -3

-4 -4

-5 -5

15 July 2005 29 September 2005


0 2 4 6 8 10 0 5 10 15 20
0 0

-1 -1

-2 -2

-3 -3

-4 -4

-5 -5

Fig. 2. Dissolved oxygen concentrations (mg/L) throughout the water column along the length of the estuary between 5th July and 29th September 2005 within the Surrey estuary.

collected before and after the kill. Additionally, comparisons will be 2.2. Post sh kill sampling
made between the relative size of the sh population in the 12
months prior to the kill with sampling trips conducted following the Fish sampling after the kill followed identical methods to those
event to gauge how the community responded to such a large prior to the kill during 20042005 (Becker and Laurenson, 2008).
disturbance. Fish were collected from six sites along the length of the estuary
using a single wing mini fyke net. Sampling was conducted during
September 2005 and March 2006. At sites 26 a net was set in the
main channel and, if ooded, a second net was set in the adjacent
2. Methods oodzone. Site 1 consisted of only a main channel as little ooding
occurred near the mouth. All nets were set at sunrise, retrieved
2.1. Water quality data collection within an hour of sunset and then reset overnight and hauled the
following sunrise. Fyke nets were constructed from 3 mm honey-
Water quality proles were collected by Deakin University comb mesh with a single wing measuring 3.5 m in length and 70 cm
Water Quality Laboratory. Dissolved oxygen (mg/L and % satura- in height. Additional independent sh data was sourced from the
tion), temperature ( C) and salinity were recorded at half metre Glenelg-Hopkins Catchment Management Authority from surveys
intervals at seven sites along the estuary prior to and following the undertaking during August 2006 and May 2007. Methods for these
sh kill as well as during September 2005 (Fig. 1). Before the arti- surveys were similar to those employed by Becker and Laurenson
cial opening a dissolved oxygen logger was installed halfway (2007), however some site locations differed and additional gear
along the estuary. The logger was suspended half a metre below (a number of box sh traps) were also utilised. As such, the data
a oat and recorded mean hourly oxygen concentrations (mg/L). from these surveys was not included within any statistical analysis
A. Becker et al. / Estuarine, Coastal and Shelf Science 82 (2009) 566572 569

5
D.O. (mg/L)
4

0
00:00 July 7

12:00 July 8

00:00 July 10

12:00 July 11

00:00 July 13

12:00 July 14

00:00 July 16

12:00 July 17

00:00 July 19

12:00 July 20
Fig. 3. Mean hourly dissolved oxygen concentrations recorded by the installed logger within the Surrey Estuary between 7/7/2005 and 20/7/2005. Arrow indicates time at which
the estuary is believed to have been articially opened.

but the results are presented in Table 1 to provide comparable they began to rise again. By 29 September 2005, a sharp halocline
descriptive information on the sh population during these times. had re-established although salinities near the mouth were
generally higher than in upstream sections of the estuary.
2.3. Statistical analysis A drop exceeding 1.2 m in water level was observed following
the articial mouth opening (Table 2). As the water level dropped it
Differences in total catch (CPUE dened as number sh/ drained the ooded margins and exposed normally submerged
net h1) between September 2006 and March 2007 (post sh kill) mud banks in the lower estuary.
to the data collected in the 12 months prior to the sh kill were
tested using a one way ANOVA. Only data collected from the main
channel sites was included in the analysis due to some oodzone 3.2. Effect of the mouth opening on the small sized sh community
sites only being sampled sporadically prior to the kill and never within the Surrey Estuary
following the sh kill (due to the decrease in water level following
the opening). As a preliminary ANOVA did not reveal any differ- The articial mouth opening led to signicant losses of sh.
ences between diel periods (day/night samples) this data was Many sh were caught up in vegetation surrounding the estuary or
subsequently pooled. Data was fourth root transformed to meet the covered in mud, making accurate counts impossible, although it
assumptions of ANOVA. Homogeneity of variance was checked by was apparent many thousands of sh died.
observing plots of residuals and normality assessed with p-plots Nine species were identied as suffering mortalities during the
(Quinn and Keough, 2002). Unplanned pairwise comparisons of the sh kill (Table 1). Monthly mean total catches for the 12 months
monthly CPUE were performed with Tukeys post hoc test. prior to the sh kill were consistent, the exception being June 2005
(three weeks prior to the sh kill) when a lower catch was observed
3. Results (Fig. 5). The September 2005 survey (three months following the
kill) had a low total catch of 57 individuals. Most of these sh were
3.1. Hydrodynamic changes within the Surrey Estuary following the either marineestuarine opportunists (Aldrichetta forsteri) caught
July 2005 mouth opening near the mouth, or estuarine residents (Pseudogobius olorum)
collected in the far upper reaches of the estuary (Table 1). The
Prior to the articial mouth opening, oxygenated water occurred March 2006 survey (six months following the kill) saw the total
only in the upper layers of the water column in the lower half of the catch rise signicantly to levels equal to or higher than those
estuary (Fig. 2). Within upper sections of the estuary (sites 57) recorded prior to the sh kill. The catch was relatively diverse with
anoxic conditions existed from the bottom to the surface. By 12 July, eight species identied, including a number of estuarine resident
one day following the articial opening, virtually all water within species. When the total catch from all months was compared
the estuary was anoxic. These conditions persisted until 15 July a signicant difference was found (F 2.946; d.f. 13; p < 0.01).
when oxygen levels in the deeper layers near the mouth began to Pairwise comparisons identied signicant differences between
rise (Fig. 2). The dissolved oxygen logger recorded a large drop in the total catch in September 2005 (three months following the kill)
oxygen levels within the mid-reaches of the estuary following the with six of the months prior to the kill (including September 2004)
articial opening of the mouth (Fig. 3). It was not until 18 July that and the collection taken in March 2006.
dissolved oxygen levels began to rise in this section of the estuary. The independent surveys carried out in August 2006 and May
Immediately following the breaching, the halocline broke down, 2007 similarly contained mostly estuarine resident species.
particularly near the mouth, but also, to a lesser extent, in the Although numbers cannot be directly compared they were still
upstream sections of the estuary (Fig. 4). Salinity concentrations considerably higher and more diverse than those recorded in the
remained relatively low at the downstream sites until 15 July when months immediately following the kill.
570 A. Becker et al. / Estuarine, Coastal and Shelf Science 82 (2009) 566572

Salinity (PSU)
5 July 2005 11 July 2005
0 10 20 30 40 0 10 20 30 40
0 0

-1 -1

Site 1
-2 -2
Site 2
Site 3
-3 -3
Site 4
Site 5 Mouth Opened
-4 -4
Site 6
Site 7
-5 -5

12 July 2005 13 July 2005


0 10 20 30 40 0 10 20 30 40
0 0

-1 -1
Depth (m)

-2 -2

-3
-3

-4
-4
-5
-5

15 July 2005 29 September 2005


0 10 20 30 40 0 10 20 30 40
0 0

-1 -1

-2 -2

-3 -3

-4 -4

-5 -5

Fig. 4. Salinity throughout the water column along the length of the estuary between 5th July and 29th September 2005 within the Surrey Estuary.

4. Discussion Estuary, indeed monitoring conducted between 2003 and 2005


regularly recorded low dissolved oxygen in deeper waters, particu-
4.1. Physical processes leading to the sh kill larly during periods of mouth closure (Becker, 2007). This pattern of
deep water anoxia is also common in other seasonally closed
It appears that fatally low levels of dissolved oxygen, associated systems along the western coast of Victoria and is generally associ-
with the articial mouth opening were responsible for the sh kill ated with extend periods of mouth closure (Sherwood, 1985).
within the Surrey Estuary. Before the mouth opening, oxygen levels The water quality data collected prior to and following the
were at critically low levels throughout most of the estuary, partic- mouth opening indicates the water column undergoes a shearing
ularly in the upper reaches where anoxic water extended from the effect if the opening occurs during periods of low ow, where
bottom of the water column, through the halocline to the surface. surface water ows out to sea leaving only deeper waters behind.
Though deeper waters in the downstream half of the estuary were Dissolved oxygen concentration recorded on the day of the kill
also anoxic, waters above the halocline were well oxygenated. Deep supports this theory. This data was collected approximately 4 h
water anoxia is not an uncommon phenomenon within the Surrey following the opening and show sites which previously contained
well oxygenated surface water (sites 13) already had seriously
depleted oxygen concentrations throughout the water column.
Table 2
Water level of the Surrey Estuary AHD (above mean sea level) prior to and following Surface waters had at this time owed out of the estuary leaving
the articial opening of the mouth on the 11th July 2005. only deeper anoxic water behind. The drop in water height further
conrms this, as it shows in the hours following the mouth
10 Jul 2005 11 Jul 2005 12 Jul 2005 13 Jul 2005
opening, there was a net loss of water within the estuary rather
1.64 1.35 0.5 0.4
than a displacement from waters further upstream. In the hours
A. Becker et al. / Estuarine, Coastal and Shelf Science 82 (2009) 566572 571

1.6

1.4

1.2

Mean Total CPUE Fish Kill


1

0.8

0.6

0.4

0.2

0
23-25 Jul 04

19-12 Aug 04

14-16 Sep 04

12-14 Oct 04

16-18 Nov 04

13-15 Dec 04

11-13 Jan 05

17-19 Feb 05
20-22 Mar 05

12-14 Apr 05

10-12 May 05

14-16 Jun 05
Jul 05

Aug 05

15-17 Sep 05

Oct 05
Nov 05

Dec 05

Jan 06
Feb 06
12-14 Mar 06
Fig. 5. Mean monthly total CPUE in the Surrey Estuary between July 2004 and June 2005 with the two additional post kill surveys conducted in September 2005 and March 2006
(s.e.).

following the mouth opening, dissolved oxygen concentrations at consistent with a survey carried by the Department of Primary
sites 6 and 7 rose at the surface and were probably caused by well Industries in August 2005 (Grixti et al., 2006).
oxygenated water within the inundated adjacent wetlands (Becker, Mean total catch during 20042005 was relatively consistent
2007) owing into the main channel as the surface water sheared with the exception of June 2005 when catch rates dropped, coin-
off. By 12 July the wetlands were completely drained and surface ciding with changes in water quality, notably a marked reduction in
waters at sites 6 and 7 were again anoxic. dissolved oxygen concentrations (Becker, 2007). There was no
Dissolved oxygen levels remained low throughout the water evidence of sh mortalities at this time. Active avoidance of hypoxic
column along the estuary in the days following the mouth opening. conditions within estuaries by nekton has previously been reported
Following the initial shearing process which initiated the kill, the (Pihl et al., 1991). With many of the species being euryhaline
region of anoxic water that was present in upper reaches of the (McDowall, 1996), it is possible that some migrated into the
estuary owed downstream and occupied the entire estuary, exac- freshwater reaches of the Surrey to escape the hypoxic conditions
erbating the sh kill. The low 4 ML/day ow (mean July ow between present in much of the estuary, resulting in the low catch. It is also
1975 and 2004 is 169 ML/day  8 ML/day) into the estuary explains possible that large numbers of sh were congregating in small
why well oxygenated freshwater did not ow into the estuary and pockets of higher oxygen concentration within the estuary or
ush out the anoxic water. Indeed it was not until 15 July when dis- physically stressed and moving little. The passive nature of the gear
solved oxygen concentrations began to rise caused by what appears used requires sh to be mobile and will not collect stationary
to be marine water owing into the lower sections of the Surrey. individuals (Smith and Hindell, 2005).
The last sh kill within the Surrey occurred during winter of The catch three months following the kill (September 2005) saw
1999 which was also the last time annual high winter freshwater a further drop in total catch and was signicantly lower than the
ows failed (mean July 1999 ow was 6 ML/day  0.5 ML/day). catch recorded during six of the months prior to the sh kill and
Over the past ten years there has been no evidence of a sh kill March 2006. At this time water quality had improved and there
occurring from a natural (unassisted) mouth opening which appeared no physiological reason for sh that may have migrated
generally occurs during periods of annual high rainfall and high upstream prior to the sh kill to escape hypoxic conditions, not to
ow into the estuary. The 1999 kill was again the result of an return to the estuary.
articial mouth opening and clearly highlights the requirement of By the end of March 2006 there was evidence of recovery in the
high freshwater inows to minimise the risk of sh kills associated sh population. Species present were mostly juvenile Atherinosoma
with such mouth openings. microstoma and Philypnodon grandiceps with catch rates equal to or
higher than those observed during the consecutive 12 month
4.2. Impact and recovery of the sh population sampling period (Becker and Laurenson, 2008). Surveys during
August 2007 and May 2007 similarly found a number of species in
Articial opening of the mouth resulted in high mortalities of numbers comparable to those recorded by Becker and Laurenson
sh within the estuary. The proportion of individuals affected (2008). This implies that enough individuals survived the sh kill to
varied between species, though the large numbers of dead sh successfully introduce new recruits into the estuary. Given the
observed both within the water and along the banks, suggests opportunistic reproductive strategy of these species (Winemiller,
a signicant percentage of the population died. Low catches during 2005), it is not unexpected that such species were most abundant.
September 2005 appeared to support high mortality levels and is Such reproductive strategies manage best following signicant
572 A. Becker et al. / Estuarine, Coastal and Shelf Science 82 (2009) 566572

disturbances and point to a resilient ecological community (Hol- Becker, A., Laurenson, L.J.B., 2008. Presence of sh on the shallow ooded margins
of a small intermittently open estuary in south eastern Australia under variable
ling, 1973). It is unlikely the high catch during March 2006 was due
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ambush-predator dinoagellate distribution and environmental-conditions.
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system (as a result of the sh kill) the current year class of small Burkholder, J.M., Noga, E.J., Hobbs, C.H., Glasgow, H.B., 1992. New phantom dino-
species could be particularly successful. agellate is the causative agent of major estuarine sh kills. Nature 360, 768.
Dawson, K., 2002. Fish kill events and habitat losses of the Richmond River, NSW
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thopagrus butcheri as this species does not reach sexual maturity death event in the Surrey River, Victoria. Report 10, Queenscliff.
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