Thermally Mediated Body Temperature, Water Content and Aggregation Behaviour in the Intertidal Gastropod Nerita Atramentosa
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Ecol Res DOI 10.1007/s11284-013-1030-4 ORIGINAL ARTICLE Coraline Chapperon • Ce´dric Le Bris • Laurent Seuront Thermally mediated body temperature, water content and aggregation behaviour in the intertidal gastropod Nerita atramentosa Received: 29 March 2012 / Accepted: 20 January 2013 Ó The Ecological Society of Japan 2013 Abstract Intertidal organisms are vulnerable to global reinforces the evidence that mobile intertidal ectotherms warming as they already live at, or near to, the upper could survive locally under warmer conditions if they limit of their thermal tolerance window. The behaviour can locate and move behaviourally in local thermal of ectotherms could, however, dampen their limited refuges. N. atramentosa behaviour, water content and physiological abilities to respond to climate change (e.g. body temperature during emersion seem to be related to drier and warmer environmental conditions) which the thermal stability and local conditions of the habitat could substantially increase their survival rates. The occupied. Aggregation behaviour reduces both desicca- behaviour of ectotherms is still mostly overlooked in tion and heat stresses but only on the boulder field. climate change studies. Here, we investigate the poten- Further investigations are required to identify the dif- tial of aggregation behaviour to compensate for climate ferent behavioural strategies used by ectothermic species change in an intertidal gastropod species (Nerita atra- to adapt to heat and dehydrating conditions at the mentosa) in South Australia. We used thermal imaging habitat level. Ultimately, this information constitutes a to investigate (1) the heterogeneity in individual snail fundamental prerequisite to implement conservation water content and body temperature and surrounding management plans for ectothermic species identified as substratum temperature on two topographically differ- vulnerable in the warming climate. ent habitats (i.e. rock platform and boulders) separated by 250 m at both day- and night-times, (2) the potential Keywords Body temperature Æ Water content Æ relationship between environment temperature (air and Aggregation Æ Snail Æ Thermal imaging Æ Rocky shore Æ substratum) and snail water content and body temper- Ectotherms Æ Desiccation stress Æ Thermal stress Æ ature, and (3) the potential buffering effect of aggrega- Conservation management tion behaviour on snail water content and body temperature. Both substratum and snail temperature were more heterogeneous at small spatial scales (a few Introduction centimetres to a few metres) than between habitats. This Understanding how ectotherms adapt physiologically to & C. Chapperon ( ) Æ heat stress and thermoregulate in response to climate C. Le Bris Æ L. Seuront School of Biological Sciences, Flinders University, GPO Box 2100, warming is essential to determining the limits of their Adelaide, SA 5001, Australia thermal tolerance window (Hofmann and Todgham E-mail: coraline.chapperon@flinders.edu.au 2010). This is critical since temperature has a paramount effect on physiological processes cascading from genes to Present address: C. Le Bris organisms (Somero 2002). This impacts individual per- Laboratoire des Sciences de l’Environnement Marin, Universite´ formance and fitness (Huey and Berrigan 2001), and de Bretagne Occidentale, UMR 6539, Brest, France ultimately sets species biogeographic ranges (Hofmann and Todgham 2010). The physiological thermoregula- L. Seuront Aquatic Sciences, South Australian Research and Development tory abilities of intertidal ectotherms are, however, lim- Institute, West Beach, SA 5022, Australia ited since they already live at, or near to, their upper thermal tolerance limit (Somero 2002). It is thus critical L. Seuront to examine non-physiological means of thermoregula- Centre National de la Recherche Scientifique, Laboratoire tion that could maintain the fitness of intertidal species, d’Oce´anologie et de Ge´osciences, Universite´des Sciences et Technologies de Lille, UMR LOG 8187 Station Marine, hence to some extent the balance of the intertidal eco- 62930 Wimereux, France system, in the changing climate. Ectothermic species can maintain body temperatures within their thermal tolerance window by responding to Materials and methods heat stress over a range of (1) temporal scales spanning from minutes to generations, hence involving processes Study organisms and sampling strategy such as behavioural thermoregulation (Dubois et al. 2009; Munoz et al. 2005), acclimatisation (Sinclair et al. In this study, we investigated the potential links between 2006) and evolutionary adaptation (Somero 2010); and aggregation, heat and desiccation stresses in the inter- (2) spatial scales ranging from small-scale habitats tidal prosobranch gastropod Nerita atramentosa (Reeve (Chapperon and Seuront 2011a; Denny et al. 2011)to 1855). N. atramentosa was specifically chosen since it is large-scale geographic distances (Osovitz and Hofmann typically found in large aggregations (up to several 2007). In particular, the survival of ectothermic species hundreds of individuals) on temperate South Australian in the warming climate is linked strongly to the dispersal rocky shores (C.C. and L.S., personal observation), and abilities of both organisms and populations within and plays a strategic role on intertidal rocky shores across heterogeneous environments in order to select (Underwood 1984). N. atramentosa appears to be par- thermally favourable habitats (Sorte et al. 2011). For ticularly vulnerable to extreme heat, and hence the instance, some intertidal invertebrates thermoregulate warming climate, due to its (1) geographic position, (2) through microhabitat selection (e.g. Garrity 1984) while shell colour and (3) limited thermoregulatory abilities. some terrestrial vertebrates such as reptiles shuttle be- First, South Australia is the driest state in Australia and tween sun and shade in order to take advantage or avoid is predicted to become both drier and warmer with an solar radiation (e.g. Dı´az and Cabezas- Dı´az 2004; increase in the frequency of extreme maximum temper- Dubois et al. 2009). Intertidal invertebrates also display ature (CSIRO 2010). South Australian oceanic waters a range of thermoregulatory behaviours such as shell have also warmed up more rapidly than anticipated and position adjustment (Munoz et al. 2005) or mushroom- poleward range extension and decline of reef organisms ing behaviour (Williams et al. 2005). On intertidal rocky have already been observed (Wernberg et al. 2011). shores, the frequent formation of aggregates that con- Secondly, N. atramentosa has a black-pigmented shell tain up to hundreds of individuals (Chapman and that enhances both the absorption and retention of solar Underwood 1996) has typically been considered to re- radiation during emersion more than the surrounding duce both thermal and desiccation stresses (Garrity substratum (McMahon 1990). Finally, N. atramentosa 1984; Chapman and Underwood 1992; Raffaelli and individuals remain attached to the substratum even Hawkins 1996; Stafford and Davies 2005, 2011, 2012). above temperatures inducing heat coma (i.e. 38.9 °C) Aggregations may indeed maintain moisture and reduce and some specimens exhibit a lack or limited evaporative evaporation rate through the minimisation of the sur- cooling ability (McMahon 1990). N. atramentosa suc- face-to-volume ratio in contact with the atmosphere cessful dominance on South Australian rocky shores (Chase et al. 1980). For instance, aggregated Nodilitto- nevertheless suggests the existence of some behavioural rina peruviana maintain water content and thermoregu- adjustment of its body temperature and water content to late better than solitary individuals (Rojas et al. 2000). cope with South Australian summer conditions, such as Similarly, aggregated mussels exhibit lower body tem- the formation of aggregates. peratures (4–5 °C) than solitary mussels (Helmuth This study was conducted during the austral summer 1998). (February 2010) on a moderately exposed rocky shore The main objective of this study was to examine located in South Australia (Marino Rocks). This site is whether the aggregation behaviour widespread among characterised by an alongshore gradient in substratum intertidal snails provide benefits in terms of body tem- topographic complexity that includes rock platforms, perature and water content in dry and hot environ- rocks and boulders, and abounds with intertidal snails mental conditions and to discuss its potential (e.g. Bembicium sp., Austrocochlea sp.), especially Nerita implication in the warming climate. In this context, this atramentosa (Reeve 1855) found at each tidal height. study assessed (1) the heterogeneity in snail temperature, In order to assess the potential effect of aggregation water content and environment temperature; (2) the behaviour on both snail body temperature and water relationship between snail water content, body temper- content, we considered solitary and aggregated individ- ature and environment temperature; and (3) the poten- uals. An individual was considered aggregated when tial buffering effect of aggregation behaviour on snail there was a direct shell contact with the shell of at least body temperature and water content in different envi- another conspecific (Chapperon and Seuront 2011a, b). ronmental conditions. The mosaic patterns of environ- However, all aggregated individuals were collected ran- mental/animal temperature and the benefits of domly from different aggregations containing at least