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Prior Exposure Influences the Behavioural Avoidance by An Estuarine, Coastal and Shelf Science 136 (2014) 82e90 Contents lists available at ScienceDirect Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss Prior exposure influences the behavioural avoidance by an intertidal gastropod, Bembicium auratum, of acidified waters Valter Amaral a,b,*, Henrique N. Cabral b, Melanie J. Bishop a a Department of Biological Sciences, Macquarie University, North Ryde, New South Wales 2109, Australia b Centro de Oceanografia, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal article info abstract Article history: Phenotypic plasticity may be critical to the maintenance of viable populations under future environ- Received 22 April 2013 mental change. Here we examined the role of behavioural avoidance of sub-optimal conditions in Accepted 17 November 2013 enabling the intertidal gastropod, Bembicium auratum, to persist in mangrove forests affected by the low Available online 23 November 2013 pH runoff from acid sulphate soils (ASS). Behaviourally, the gastropod may be able to avoid periods of particularly high acidity by using pneumatophores and/or mangrove trunks to vertically migrate above Keywords: the water line or by retreating into its shell. We hypothesised that (1) B. auratum would display greater adaptation and more rapid vertical migration out of acidified than reference estuarine waters, and (2) responses Bembicium auratum fi crawl-out would be more pronounced in gastropods collected from acidi ed than reference sites. Gastropods from fi fi fi invertebrate acidi ed sites showed signi cantly higher activity in and more rapid migration out of acidi ed waters of microhabitat pH 6.2e7.0, than reference waters or waters of pH < 5.0. Gastropods from reference locations showed a pH significantly weaker response to acidified water than those from acidified waters, and which did not significantly differ from their response to reference water. At extremely low pHs, <5.0, a higher pro- portion of both acidified and reference gastropods retreated into their shell than at higher pHs. Both the migration of gastropods out of acidified waters and retraction into their shells serves to reduce exposure time to acidified waters and may reduce the impact of this stressor on their populations. The stronger response to acidification of gastropods from populations previously exposed to this stressor suggests that the response may be learned, inherited or induced over multiple exposures. Our study adds to growing evidence that estuarine organisms may exhibit considerable physiological and behaviour adaptive ca- pacity to acidification. The potential for such adaptive capacity should be incorporated into studies seeking to forecast impacts to marine organisms of environmental change. Ó 2013 Elsevier Ltd. All rights reserved. 1. Introduction organisms to adapt to change may depend on their phenotypic plasticity. Plasticity in life-history, physiology or behaviour may Ecological environments are currently experiencing change at enable populations to persist and maintain viable populations un- unprecedented rates and scales (IPCC, 2007). Where organisms are der a broad range of environmental conditions (Charmantier et al., unable to adapt to this change, restructuring of coastal and estua- 2008; Tuomainen and Candolin, 2011). rine ecosystems (Worm et al., 2006; Richardson and Poloczanska, The acidification of the world’s oceans and estuaries is one 2008), and loss of important ecosystem services (Barbier et al., aspect of environmental change that is presently challenging the 2011) may result. In instances where molecular evolution is con- structure and function of ecosystems. Emissions of CO2 are already strained (Stern and Orgogozo, 2009; Hoffmann et al., 2012), or is producing changes in pH of ecological significance (Fabry et al., insufficiently rapid to keep pace with environmental change (Stern 2008; Hendriks et al., 2010) and are predicted to produce a and Orgogozo, 2009; Lavergne et al., 2013), the capacity of further drop in pH of w0.5 units in the next 100e200 years (Caldeira and Wickett, 2005; IPCC, 2007). Simultaneously, the conversion of wetlands to farmlands is leading to enhanced expo- sure of acid sulphate soils (ASS; Dent and Pons, 1995), the runoff * Corresponding author. Centro de Oceanografia, Faculdade de Ciências da Uni- from which can reduce the pH of adjacent estuaries to as low as 2e6 versidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal. fi E-mail addresses: [email protected] (V. Amaral), [email protected] (H.N. Cabral), (Sammut et al., 1996; NSW DPI, 2006). The acidi cation of seawater [email protected] (M.J. Bishop). can negatively impact marine organisms by impairing their 0272-7714/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ecss.2013.11.019 V. Amaral et al. / Estuarine, Coastal and Shelf Science 136 (2014) 82e90 83 physiological regulation, olfactory discrimination, and predator (2) those sourced from sites recurrently exposed to acidic waters avoidance behaviours and/or causing dissolution of the exoskeleton would display stronger responses to this disturbance than those of calcifying organisms (Munday et al., 2009; Ries et al., 2009; from unaffected, reference sites. Melatunan et al., 2013). Among marine organisms, intertidal mol- luscs (e.g. oysters and gastropods) are among the most vulnerable 2. Materials and methods to acidification (Fabry et al., 2008; Guinotte and Fabry, 2008; Hendriks et al., 2010). They rely on a calcium carbonate exoskel- 2.1. Sampling sites, gastropods and test waters eton to protect them from predation and desiccation stress, they have limited ability to regulate their internal pH and, in the case of To test the hypothesis that Bembicium auratum gastropods species with a sessile life-history stage, cannot escape from acidic previously exposed to runoff from ASS would display stronger waters (Bamber, 1987, 1990; Sammut et al., 1995; Ries et al., 2009). avoidance behaviours to acidified waters than naive gastropods, we Although many molluscs display strong negative responses to reciprocally exposed gastropods from acidified and reference sites acidification, some appear to exhibit considerable capacity to adapt of an estuary to water sourced from acidified and reference sites of to this stressor (Bibby et al., 2007; Ries et al., 2009; Hendriks et al., that same estuary. Water and gastropods were collected from two 2010). For example, the effect of runoff from acid sulphate soils on acidified and two reference sites within each of the Hunter (32.915 the shell strength and density of wild populations of Saccostrea S,151.801 E) and Port Stephens (32.708 S, 152.196 E) estuaries, NSW, glomerata oysters and Bembicium auratum was less than predicted Australia. At each site, B. auratum were found attached to the from experiments exposing naive oysters to this stressor (Amaral pneumatophores of the grey mangrove, Avicennia marina and on et al., 2011a, 2012a). Whereas naive individuals rapidly developed the surface of the sediment. Acidified sites were situated within tissue lesions and experienced shell dissolution that ultimately 900 m of major ASS discharge drains, in areas classified by the NSW resulted in mortality (Dove and Sammut, 2007a,b), wild pop- Government as being of high ASS runoff risk (Naylor et al., 1998; ulations were able to persist in a periodically acidifying environ- NSW DECCW, 2012), and with a history of low pH (NSW DPI, ment (Amaral et al., 2011a, 2012a). Wild populations of molluscs 2006, 2008, 2009). Reference sites were situated at least 2400 m that are recurrently exposed to acidified conditions are likely to away from drains in areas of low ASS runoff risk (Naylor et al., 1998; experience intense selective pressure for resistance to acidification NSW DECCW, 2012) and where we had not observed pH values (Trussell, 1996; Jones and Boulding, 1999; Melatunan et al., 2013). lower than 7.6 (Table 1). Sites within each estuary were of similar Additionally, phenotypically plastic physiological and behavioural water temperature, but those adjacent to drains were on average 10 responses to the conditions may confer some resistance to the times more acidic and of slightly lower (w1 unit) salinity than stressor (Ries et al., 2009; Rodolfo-Metalpa et al., 2011). Oysters can reference sites (Table 1). We have previously documented differ- endure pulses of exposure to sub-optimal conditions by closing ences in the abundance, morphology and growth of molluscs be- their valves and relying on their tough shells, built mainly of calcite, tween these acidified and reference sites (Amaral et al., 2011a, to protect them from predators (Stenzel, 1964; Dove and Sammut, 2012a,b). 2007a; Green and Barnes, 2010). Gastropods, on the other hand, Experiments were repeated on four occasions, during late fall build their shells from the more soluble aragonite and are mobile and early winter of 2012. At low tide of each sampling date, we (Taylor and Reid, 1990), so may benefit from moving to microhab- collected test water from surface waters adjacent to each site, and itats in which they escape acidification or reduce the frequency and Bembicium auratum gastropods of 11e14 mm in shell height from duration of their exposure to it (Marshall et al., 2008). the pneumatophore zone (mean low water þ 0.5e0.7 m). This size Gastropods commonly use behavioural avoidance (i.e. move- of gastropod is numerically dominant at our sampling sites (Amaral ment into protected microhabitats or retraction into the shell) to et al., 2011a) and differs in shell strength (by >60 N) between reduce their susceptibility to predators (Richardson and Brown, acidified and reference sites (Amaral et al., 2012a). Only gastropods 1992; Jacobsen and Stabell, 1999). The role of similar strategies in without shell fouling or visible shell damage were used. Test waters enabling them to persist in acidic water has, however, seldom been were continuously aerated with air stones until experimentation, considered (Bibby et al., 2007), and never using wild organisms that within 1.5 h of collection.
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