Biol Invasions (2010) 12:715–719 DOI 10.1007/s10530-009-9478-4
INVASION NOTE
The apparent demise of the Asian date mussel Musculista senhousia in Western Australia: or using acts of god as an eradication tool Justin I. McDonald Æ Fred E. Wells
Received: 5 January 2009 / Accepted: 6 May 2009 / Published online: 26 May 2009 Ó Springer Science+Business Media B.V. 2009
Abstract Musculista senhousia (Benson in Cantor, 1842) is a small thin-shelled mytilid inhabiting intertidal and shallow subtidal sediments. Prior to 2000, M. senhousia was widespread in the Swan River estuary, Perth, Western Australia. In 2000 the Perth region experienced its largest recorded summer rainfall event, with over 270 GL entering the estuary. The rainfall formed a freshwater lens over much of the river and a subsequent toxic algal bloom of the cyanobacterium Microcystis aeruginosa. M. aeruginosa produces a toxin microcystin, known to have adverse effects upon molluscs. Surveys to assess the status of M. senhousia in the estuary in 2007 failed to find any individuals. We suggest the apparent death of M. senhousia from the estuary may be attributable to a combination of high seasonal variability in the J. I. McDonald (&) Ministry of Agriculture and Forestry, P.O. Box 2526, Wellington, New Zealand e-mail:
[email protected] F. E. Wells Field Museum of Natural History, Chicago, IL, USA Present Address: F. E. Wells Enzer Marine Environmental Consulting, P.O. Box 4176, Wembley, WA 6014, Australia J. I. McDonald F. E. Wells Western Australian Fisheries and Marine Research Laboratories, P.O. Box 20, North Beach, WA 6920, Australia
mussel’s populations, high summer rainfall reducing salinity, and a toxic algal bloom that eliminated any remaining M. senhousia individuals. Keywords Biological invasion Eradication Introduced species Non-indigenous Pest Salinity
Introduction Bivalves are often successful invaders of marine and freshwater environments (Creese et al. 1997). The Asian date mussel Musculista senhousia is an invasive species with a record of causing both ecological and social impacts around the globe. M. senhousia can dominate benthic communities and potentially exclude native species (Crooks 1996). M. senhousia (Benson in Cantor, 1842) was recorded in the Swan and Canning Rivers, Western Australia in 1987 (Slack-Smith and Brearley 1987). M. senhousia populations in the Swan River region reached densities of up to 2,600 m2 (Summers 1994), great enough to form extensive smothering mats. These populations were found from intertidal to subtidal habitats (to a depth of 4 m), although in other regions it has been recorded to depths of 20 m and on soft or hard substrata. The presence of these mats elsewhere has been shown to dramatically alter the natural benthic habitat, changing both the local physical
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environment and the resident macro-invertebrate assemblage (Allen and Williams 2003). Prior to 2000, there were documented widespread populations of M. senhousia in the Swan River region. In 2007, our survey of the Swan River region (incorporating Swan-Canning River system and adjacent Cockburn Sound) failed to locate a single M. senhousia individual. This paper explores the possible natural mechanisms that could have caused the apparent demise of this introduced species from the Swan River region.
M. senhousia (Wildsmith 2007) at Guildford, Maylands and Garrett Road Bridge. In October 2007, a detailed search of 43 sites was undertaken in the Swan River region to document the distribution of M. senhousia. The search covered a range of sites where M. senhousia was documented to occur (major long term documented populations and new recordings) and any areas that might be considered suitable habitat.
Methods
No evidence of M. senhousia was recorded at any of the 43 sites examined. Subsequent discussions with local researchers and examination of grey literature revealed no reports of this species since late 1999 (R. Black and A. Brearley, personal communication, 2008). To try and explain this demise we investigated the occurrence of large-scale natural and anthropogenic disturbance events in years following the last known recording of the mussel in 1999. In January 2000, the Perth metropolitan region received its highest recorded summer rainfall ever, with 139 mm, compared to a 30-year mean of only 17.6 mm (Bureau of Meteorology 2008). A short time later Cyclone Steve crossed the Western Australian coastline, with associated rainfall further soaking the catchment. The result was that 270 GL entering Swan estuary (Swan River Trust 2000), significantly altering the normal summer pattern of Swan River system. The normal spring/summer pattern of this system consists of seawater (35 ppt) from the open-ocean and lower estuary migrating into the upper estuary in a saltwater wedge, beneath the freshwater upper layer. Mixing then occurs so that lower regions of the Swan are effectively seawater (35 ppt) and upper regions as high as 25 ppt.
In 1987, four years since the initial identification of M. senhousia in the Swan River region, populations of M. senhousia extended from the saline lower reaches of the Swan River to the brackish waters of the upper Swan (Fig. 1). M. senhousia had such spatially consistent populations in this region that the local university (University of Western Australia) used populations for study in their undergraduate degree (R. Black personal communication 2008). Macro-invertebrate sampling in 2005 in the upper reaches of the Swan River by a PhD student at Murdoch University identified a small number of
Results
Discussion
Fig. 1 Distribution of main known populations of Musculista senhousia prior to 2000 (adapted from Slack-Smith and Brearley 1987)
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Simberloff and Gibbons (2004) define a phenomenon known as spontaneous collapse, where a well established non-indigenous species, without management actions, suddenly undergoes spontaneous decline, sometimes to extinction. We propose that a combination of high seasonal variability in populations of M. senhousia, uncharacteristically high summer rainfall reducing salinity, and a toxic algal bloom
The apparent demise of the Asian date mussel Musculista senhousia in Western Australia
combined to cause the apparent demise (spontaneous collapse) of the documented mussel populations in the Swan region. The unusual rainfall in late January early February 2000 lowered the salinity in the Swan to 5–10 ppt, ensuring effectively freshwater in the upper reaches and slightly saline in middle and lower reaches (Swan River Trust 2000). This freshwater lens meant most surface waters (down to 4 m) were freshwater with only slightly more saline water beneath. SlackSmith and Brearley (1987) in their paper documenting M. senhousia in the Swan River estuary, note that M. senhousia populations in the Swan River exhibited high seasonal mortality. They postulate that this could be due to decreasing salinity as with Mytilus edulis planulatus or be post-reproductive as in Musculista glaberrima (Wilson and Hodgkin 1967). The high mortality is further supported by Summers (1994) who states that populations at Chidley Point (also the population used initially to identify this species) declined by as much as 97% over the autumn/winter period, believed to be linked to reduced salinity during this time. The huge freshwater input to the Swan River occurring in 2000 also brought approximately 800 t of nitrogen and 35 t phosphorus from the surrounding land catchment (Swan River Trust 2000). Nitrogen levels entering the system, as high as 7 mg/l, were seven times the limit considered healthy for freshwater entering estuaries. Phosphorus was two to three times the limit considered healthy (0.2–0.3 mg/l). Consequently dissolved inorganic nitrogen was 5–12 times higher than normal. The result was a cyanobacterium bloom of the species Microcystis aeruginosa that covered much of the system (Swan River Trust 2000; Fig. 2). The Microcystis bloom in the Swan region in 2000 was so concentrated that in parts cells reached 130 million per ml (average 5,000–14,000 cells ml; Swan River Trust 2000). M. aeruginosa produces a toxin called microcystin (Oh et al. 2000). Microcystins are hepatotoxic, tumour promoting (Falconer 1991) and induce liver cell apoptosis (Chen et al. 2005), they therefore cause serious, often lethal, health effects on fish, domestic animals and humans (World Health Organisation 2003; Azevedo et al. 2002; Carmichael 2001). The levels of microcystin in the Swan region exceeded the World Health Organisation’s recommended levels of 0.5 lg/l and at one stage reached 8 lg/l (Swan River Trust 2000). In a study by Juhel et al. (2006) microcystins produced by M. aeruginosa,
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Fig. 2 Main concentrations of Microcystis bloom in 2000. Red dots indicate main known populations of M. senhousia prior to this event (adapted from Swan River Trust 2000)
caused zebra mussels (Dreissena polymorpha) to produce large quantities of mucous pseudofaeces, developing a condition known as ‘pseudodiarrhoea’. This response could be considered as analogous to the acute diarrhoeal symptoms of microcystin toxicity in humans (World Health Organisation 2003). The impact of pseudodiarrhoea on zebra mussels exposed to high levels of microcystins for long periods is not known, but at the very least the response is likely to be energetically costly, since molluscan mucus is known to be biologically expensive to produce (Davies and Hawkins 1998). Musculista senhousia, like its invasive counterpart D. polymorpha, is an efficient suspension feeder that occurred in very high densities (up to 2,600 m2) in the Swan region (Summers 1994). The toxic M. aeruginosa bloom that existed in the Swan region may have had a similar adverse effect on populations of M. senhousia stressed by abrupt changes in salinity prompted by the huge freshwater input. This hypothesis is supported by studies that show long term effects of microcystins on zebra mussel larvae (Dionisio Pires et al. 2003) and other zooplankton species (Demott 1999). These
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studies all showed that microcystins had an inhibitory effect, mostly on growth, feeding and generally survival of the animals. Direct causality between the apparent demise of M. senhousia and the ‘natural causes’ stated in this paper cannot be proven. The apparent loss of the documented mussel populations from the Swan River system, however, conveys a spatial and temporal relationship between these ‘natural’ events and the last reports of the mussel species in this system. The exception to this was the small population identified by Wildsmith (2007) in 2005 in the upper reaches of the Swan estuary. The habitat type in this upper region is characterised by small fetches, riverine salinity and muddy substrate and is highly susceptible to high freshwater inundation. Targeted sampling during this study to examine these sites failed to find any specimens. The high post-reproductive mortality associated with M. senhousia seems the most likely cause of this upper Swan populations decline. Even if all animals were not affected there is a threshold where even if a few persist the population may no longer be viable. A comparable demise is noted in populations of the invasive Mayan Cichlid (Cichasoma urophthalmus) by Simberloff and Gibbons (2004). This nonindigenous species once comprised over 40% of the fish trapped in the Everglades. However, populations suddenly crashed to only 3% of the fish trapped, with populations remaining around this level. The crash in population was unexplained but was correlated with changes in minima temperature (Trexler et al. 2000— quoted in Simberloff and Gibbons 2004). At the landscape level while there appears to be an apparent demise of M. senhousia in the Swan River estuary, a small residual population may exist that could lead to a re-establishment of this species. Ongoing monitoring is needed to determine the status of this species. Acknowledgments We thank Dr. Kashane Chalermwat of Burapha University, Thailand, Mike Travers and Emily Gates who assisted in the fieldwork component. Dr. Grey Coupland who reviewed a draft of this paper. This project was funded by a Natural Heritage Trust grant (project no. 053085).
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