Journal of the Royal Society of Western Australia, 94: 25-28, 2011 The status of the black bream Acanthopagrus butcheri (Pisces: Sparidae) population in Lake Clifton, south-western Australia K A Smith & J Norriss Department of Fisheries, P.O. Box 21, North Beach, 6020, Australia. Corresponding author: 13 [email protected] Manuscript received August 2010; accepted December 2010 Abstract Lake Clifton hosts the largest living, non-marine thrombolite (microbialite) reef in the southern hemisphere. The thrombolite reef was recently listed as a critically endangered ecological community. Tire main threat to the ecology of the lake is increasing salinity, but other threats have also been identified, including the impact of the introduced fish Acanthopagrus butcheri (Munro, 1949). Samples opportunistically collected after a fish kill in 2007 indicated that A. butcheri in this lake experienced very low somatic growth and recruitment failure between 1995 and 2007, probably in response to hypersalinity. The evidence suggests that the A. butcheri population in Lake Clifton is effectively extinct. The proposed conservation strategy for Lake Clifton addresses a range of identified threats, including the eradication of A. butcheri. However, management action in response to this particular threat may no longer be required. The abundance of A. butcheri in the lake is probably very low and the population is likely to become extinct if current environmental trends continue. A dramatic reduction in growth rate after 1995 demonstrates the extraordinary growth plasticity of A. butcheri in response to environmental influences. Keywords: salinity, fish kill, growth, Sparidae, thrombolite Introduction 1987). Hence, a shift from permanently hyposaline to permanently hypersaline conditions threatens the Lake Clifton is a small, permanently closed, coastal survival of the key microbial species responsible for lake on the south-west coast of Western Australia, thrombolite formation. approximately 100 km south of Perth (lat/long S32.745°, In addition to increasing salinity, a range of other El 15.655°). The lake is part of the Peel/Yalgorup system, threats to the thrombolite community in Lake Clifton which was recognised as a 'Wetland of International have been identified, including physical damage to the Importance' under the Ramsar Convention in 1990. The thrombolites during feeding by Acanthopagrus butcheri presence of a unique thrombolite (microbialite) (Munro 1949) (Threatened Species Scientific Committee community in Lake Clifton was a key factor contributing 2010a). Predation by A. butcheri has also been suggested to this listing. In December 2009, the thrombolites in Lake as a factor contributing to a decline in the diversity of Clifton were listed as a 'critically endangered ecological community' under the Australian Commonwealth macroinvertebrate fauna within the lake (Threatened Species Scientific Committee 2010a). The "control and Environment Protection and Biodiversity Conservation eradication of black bream", which were stocked into the (EPBC) Act 1999. Rising salinity in the lake, due to the lake, is one of several Priority Actions proposed to aid inflow of increasingly saline groundwater, was identified the conservation of the thrombolite community as the greatest threat to the thrombolite community (Threatened Species Scientific Committee 2010b). This (Threatened Species Scientific Committee 2010a). action was proposed in the absence of any survey to Lake Clifton was hyposaline (salinity range 8-32 gL1) assess the current status of the A. butcheri population. in the 1970s and 1980s but has become progressively Acanthopagrus butcheri is the largest fish species more saline since 1992 and is now frequently hypersaline reported from Lake Clifton. This euryhaline species (Knott et al. 2003; Luu et at. 2004; Smith et al. 2010). Since occurs in estuaries and coastal lakes across southern 2002, annual salinity has typically ranged from a Australia and is highly targeted by recreational fishers minimum of 20-30 gL 1 in winter to a maximum of 70-80 across this range (Kailola et al. 1993). Anecdotal reports gL_l in autumn (John et al. 2009; Smith et al. 2010). Lake indicate that this species was first introduced to the lake Clifton receives low surface flow and so the salinity of by commercial fishers in 1947 and possibly re-stocked on the lake is mainly a function of groundwater inflow and several subsequent occasions (Dortch 2008; Dortch evaporation (Commander 1988; Davies & Lane 1996). unpubl. data). Anecdotal reports and genetic evidence Thrombolites in Lake Clifton have historically formed as indicate the most likely sources of introduced fish are the a result of the growth of cyanobacteria Scytonema sp., adjacent estuaries of Pcel-Harvey and Leschenault Inlet which are dependant on a constant discharge of fresh to (Chaplin et al. 1998; Dortch 2008). brackish groundwater directly into their habitat (Moore The population of A. butcheri in Lake Clifton was 'rediscovered' in 1996 by recreational anglers who were © Royal Society of Western Australia 2011 fishing from a boardwalk recently constructed as a 25 Journal of the Royal Society of Western Australia, 94(1), March 2011 viewing platform for thrombolites. After a 2-week period Oxygen and salinity are infrequently monitored in Lake of intense recreational fishing, the Department of Clifton and levels immediately prior to the fish kill were Fisheries implemented a permanent ban on fishing in the not available. However, salinity measured shortly after lake. The ban was intended to protect the fish (initially the kill, in February 2007, was 79 gL 1 (John et al. 2009). thought to be an endemic population) and to prevent This is approaching the upper salinity tolerance for A. accidental damage to the thrombolites. butcheri and likely to result in osmotic stress (Partridge & Jenkins, 2002; Hoeksema et al. 2006). However, high Prior to this study, information about the status of the salinity does not appear to have been the primary cause A. butcheri population in Lake Clifton was derived from a of death in 2007. A period of increasing salinity, sample of 100 individuals collected in November 2006 eventually reaching a lethal level, would be expected to (Sarre & Potter 2000). In February 2007 a fish kill result in an extended period of stress and probably also a resulting in the deaths of hundreds of individual A. protracted period of mortality. The fins and skin of dead butcheri created an unexpected opportunity to collect fish were intact and did not show signs of external additional samples and reassess this population. lesions, disease or injuries that are often seen on fish that have been subjected to a long period of extreme osmotic Methods stress (Hoeksema et al. 2006). The external condition of the fish suggested that death occurred relatively rapidly. The fish kill was first reported by members of the Also, all fish were at a similar stage of decomposition, public on 13 February 2007. Dead fish were observed suggesting that they had died at approximately the same floating in shallow water around the thrombolites along time. the north eastern shore. Dead fish had apparently The fish kill coincided with the sudden, widespread accumulated in this region as a result of a prevailing dislodgement of large benthic microbial mats in the lake south-westerly wind. The total number of dead fish in (John et al. 2009). Dead fish and pieces of microbial mats, this area were estimated to be 600-800 (A. Kidd (DEC), up to 50 cm in diameter, were observed floating together pers. comm.). among the thrombolites. The decomposition of these On 15 February 2007 a random sample of 163 partly mats may have created hypoxic zones and led to the decomposed fish was collected from a 100 m length of sudden asphyxiation of fish. Hence, asphyxia was likely shoreline adjacent to the thrombolite viewing platform to be the primary cause of death in Lake Clifton in along the north eastern shore. The total length (TL) of February 2007. each fish was measured to the nearest millimetre. Other The total lengths of dead A. butcheri collected from biological data such as weight or sex was unobtainable Lake Clifton in February 2007 ranged from 235 to 328 from each fish due to the advanced state of mm, with an average length of 271 + 14 (+ s.d.) mm. All decomposition. fish were estimated to be 11 years old and therefore Sagittal otoliths were extracted from 100 fish. A spawned in late 1995. transverse section of 300 pm thickness was taken through The mean length-at-age of fish collected in 2007 was the core of one otolith from each fish. Sections were substantially lower than that predicted by von viewed with reflected light against a black background. Bertalanffy growth parameters derived from fish Age was determined by enumeration of opaque and collected from Lake Clifton in 1996 (429 mm TL at 11 translucent zones, which are deposited annually in A. years of age) (Sarre & Potter 2000) (Fig. 1). In 1996, the A. butcheri otoliths (Morison ef al. 1998). Opaque zones in A. butcheri population in Lake Clifton exhibited a relatively butcheri otoliths are typically deposited during spring fast growth rate, which was significantly higher than (Sarre & Potter 2000). The first complete annual growth measured in three other south-western 'increment' was defined as an opaque core followed by a Australian estuaries (Moore River, Walpole/Nornalup translucent zone plus an opaque zone. Subsequent Inlet, Wellstead Estuary) and slightly higher than growth increments were defined as a translucent zone plus an opaque zone. Each otolith was assigned one of the following margin categories: l=translucent margin, 400 - marginal increment <50% complete; 2=translucent E margin, marginal increment >50% complete; 3=opaque E / / margin. All otoliths were read once by an experienced £ 300 - / reader and once by a second experienced reader. There O) / 2 was 100% agreement between these readings. c / _<D 200 / In south-western Australian estuaries, A. butcheri Is - / typically spawn between October and December (Sarre & o / Potter 1999). Therefore, an average birth date of 1 I- 100 ' - Lake Clifton 1996 O Lake Clifton 2007 November was assigned to all fish collected from Lake Clifton in 2007. 0 (cid:9632)- 0 5 10 15 20 Results and Discussion Age (years) High salinity and low oxygen have been suggested as Figure 1. Length-at-age of Acantlwpagrus butcheri collected from Lake Clifton in 1996 (represented by von Bertalanffy growth factors contributing to the sudden mortality of black curve fitted by Sarre (1999)) and length-at-age (mean + s.d.) of bream in Lake Clifton in February 2007 (John et al. 2009). fish collected from Lake Clifton in 2007. 26 Smith & Norriss: Acanthopsgrus butcheri in Lake Clifton measured in the Swan Estuary (approximately 90 km to natural mortality, imply a high initial abundance of each the north of Lake Clifton) (Sarre & Potter 2000). The age class. This would have required substantial magnitude of the decline in growth in Lake Clifton quantities of fish to be stocked into the lake each year. A between 1996 and 2007 indicated that all of the fish more likely mechanism is natural recruitment. Hence, the collected in 2007 had experienced slow growth over majority of the fish collected in 1996 and in 2007 were numerous years. Overall, these observations suggest that probably spawned in Lake Clifton and were the environmental conditions in Lake Clifton were relatively descendants of a small number of introduced fish. favourable to the growth of A. butcheri prior to 1996 but Reproduction by A. butcheri (as measured by sperm were unfavourable after 1996. motility, egg fertilization, egg survival and larval Previous observations of differences in growth rates development) can occur at salinities of 10-35 gL1 but, among estuaries have provided evidence of the plasticity within this range, is most successful at salinities of 20-35 of growth by A. butcheri (Sarre & Potter 2000). These gL 1 (Haddy & Pankhurst 2000). This optimal range differences are environmentally driven and do not reflect reflects the salinities at which A. butcheri typically genetic differences between populations (Partridge et nl. spawns in the wild (Nicholson et at. 2008). The potential 2004). The decline in growth of A. butcheri in Lake Clifton of A. butcheri to reproduce successfully at salinities above between 1996 and 2007 further demonstrates the seawater has not been examined. However, in the extraordinary growth plasticity of this species in congeneric Acanthopagrus berda, sperm motility occurs response to environmental factors. over a wide salinity range (5-60 gL1) but peaks sharply at approximately 25-35 gL’1 (Molony & Sheaves 2001). In Acanthopagrus butcheri can tolerate a wide range of another euryhaline sparid, Sparus sarba, hatching of salinities, from 0 to at least 60 gL'1. Juveniles and adults viable larvae is limited to salinities of 9-54 gL'1 but typically display signs of osmotic stress, including highest rates occur between 20-36 gL 1 (Mihelakakis & reduced growth, external lesions and mortality at Kitajima 1994). The optimal salinity ranges for these salinities above 60 gL1, although adult fish have been species correspond to the salinities at which they observed in the wild at salinities of up to 114 gL1 typically spawn in the wild. Therefore, it is likely that (Partridge & Jenkins 2002; Hocksema et at. 2006). The reproductive success of A. butcheri declines rapidly as extremely slow growth of A. butcheri collected from salinity increases beyond 35 gL'1 and is limited to Lake Clifton in 2007 suggests that these individuals may salinities well below 60 gL1. have experienced prolonged periods of osmotic stress and spent a substantial part of their life at salinities Despite substantial penalties for unlawful above 60 gL L translocations of fish, introductions of non-endemic A. butcheri into inland lakes is a widespread problem in Other factors could also have potentially affected the south-western Australia, with various potential growth rate of A. butcheri in Lake Clifton. In particular, ecological, social and economic impacts (e.g. Smith et at. increased salinity may have altered the composition of 2009). Most recently, a population of A. butcheri was the invertebrate community in the lake, forcing a change discovered in Lake Thetis, another inland lake containing in the diet of A. butcheri. However, the stomach contents a significant benthic microbial community (Grey et nl. of fish sampled in 1996 were dominated (40% by volume) 1990; N. Casson [DEC] pers. comm.). Acanthopagrus by Capitella capitata (Polychaeta), which was abundant in butcheri in Lake Thetis were discovered during a fish kill Lake Clifton sediments in the late 1990s (Sarre et nl. 2000; in February 2010. The salinity of Lake Thetis is typically Konishi et at. 2001). Capitella capitata is extremely hypersaline and was approximately 57 gL'1 during the euryhaline (Geddes & Butler 1984) and is likely to have fish kill (K. Smith unpubl. data). As with Lake Clifton, remained abundant despite recent hypersalinity. this discovery generated concerns about the potential Therefore, the dominant prey item consumed by A. impacts to microbialites and whether management action butcheri was probably relatively constant from 1996 to should be taken. Improved knowledge of the upper 2007 and a dietary shift is unlikely to have caused the salinity limits for reproduction, growth and survival by decline in growth. A. butcheri would assist in determining the need for In addition to effects on growth, recent environmental management action in such cases. conditions in Lake Clifton appear to have also negatively In summary, the environmental conditions in Lake impacted on the reproductive output of A. butcheri. A Clifton since 1995 appear to have been highly sample of 100 A. butcheri collected from the lake in 1996 unfavourable for both growth and reproduction of A. included ten age classes ranging from 1 to 19 years (Sarre butcheri. High salinity is likely to be the primary factor 1999). 'This suggested that spawning had occurred in at contributing to slow growth and recruitment failure. least 10 of the years from 1977 to 1995. In 2007, the Given that salinity is predicted to remain high, and absence of all year classes except 1995 suggests limited or possibly increase, it appears unlikely that any surviving zero recruitment in 1996 and all subsequent years. A. butcheri in the lake will successfully breed again. It is unlikely that many of the fish captured in 1996 The proposed conservation strategy for Lake Clifton were introduced (i.e. spawned elsewhere and aims to address a range of identified threats to translocated to Lake Clifton). In 1996, anglers removed thrombolites, including the eradication of the introduced many hundreds of large bream from the lake. Also, A. butcheri population (Threatened Species Scientific anecdotal reports from fishers indicate that some fishing Committee 2010b). However, management action in had been occurring for several years prior to 1996. Even response to this particular threat may no longer be after this population depletion, numerous large fish were required. The abundance of A. butcheri in the lake is still available to be captured by Sarre (1999). These high probably very low and the population is likely to become catch rates, occurring after the effects of fishing and extinct if current environmental trends continue. 27 Journal of the Royal Society of Western Australia, 94(1), March 2011 Acknowledgements: This manuscript was much improved by suggestions Moore L S 1987 Water chemistry of the coastal saline lakes of made by B. Molony and 2 anonymous reviewers. the Clifton-Preston Lakeland System, south-western Australia, and its influence on stromatolite formation. Australian Journal of Marine & Freshwater Research 38: 647- References 660. 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