using biomimetic loggers to measure interspecific and microhabitat variation in body temperatures of...
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Using biomimetic loggers to measure interspecificand microhabitat variation in body temperaturesof rocky intertidal invertebrates
Justin A. LathleanA,C, David J. AyreA, Ross A. ColemanB
and Todd E. MinchintonA
AInstitute for Conservation Biology and Environmental Management & School of Biological
Sciences, University of Wollongong, NSW 2522, Australia.BCentre for Research on Ecological Impacts of Coastal Cities, School of Biological Sciences,
The University of Sydney, NSW 2006, Australia.CCorresponding author. Email: firstname.lastname@example.org
Abstract. Until recently, marine scientists have relied heavily on satellite sea surface temperatures and terrestrialweather stations as indicators of theway inwhich the thermal environment, and hence the body temperatures of organisms,vary over spatial and temporal scales. We designed biomimetic temperature loggers for three species of rocky intertidalinvertebrates to determine whether mimic body temperatures differ from the external environment and among species and
microhabitats. For all three species, microhabitat temperatures were considerably higher than the body temperatures, withdifferences as great as 11.18C on horizontal rocky substrata. Across microhabitats, daily maximal temperatures of thelimpet Cellana tramoserica were on average 2.1 and 3.18C higher than body temperatures of the whelk Dicathais orbitaand the barnacle Tesseropora rosea respectively. Among-microhabitat variation in each species temperature was equallyas variable as differences among species within microhabitats. Daily maximal body temperatures of barnacles placed onsoutherly facing vertical rock surfaces were on average 2.48C cooler than those on horizontal rock. Likewise, dailymaximal body temperatures of whelks were on average 3.18C cooler within shallow rock pools than on horizontal rock.Our results provide new evidence that unique thermal properties and microhabitat preferences may be importantdeterminants of species capacity to cope with climate change.
Additional keywords: Australia, barnacle, Cellana tramoserica, climate change, Dicathais orbita, habitat temperature,limpet, Tesseropora rosea, whelk.
Received 1 November 2013, accepted 13 March 2014, published online 26 November 2014
In a warming world, interspecific differences in body tem-peratures and thermal tolerances will produce a variety ofresponses among key species within a community. Rockyintertidal shores and their associated biological communities
have emerged as excellent study systems to investigate howclimate change will affect marine organisms (Helmuth et al.2006b). As for many other biological communities, the persis-
tence of rocky intertidal organisms will be dependent on theirability to adapt to the changing conditions, either physiologi-cally or behaviourally (by seeking out more benign micro-
habitats) (Helmuth et al. 2006a; Tomanek 2008; Somero 2010).Because many intertidal organisms live at or close to theirthermal limits (Denny and Harley 2006; Somero 2010), suchphysiological responses may be limited. Rocky intertidal shores
are characterised by high degrees of topographic complexityproducing a variety of microhabitats, including those that mayfunction as thermal refugia for organisms sheltering from
extreme heat stress (Denny et al. 2011; Lathlean et al. 2012).
Our ability to assess how these microhabitats mitigate the neg-
ative effects of global warming for rocky intertidal communitiesis primarily dependent on characterising interspecific variationin body temperatures within and outside thermal refugia.
Due to the dynamic nature of the marine environment,
measuring body temperatures of marine organisms has provensomewhat difficult, and ambient temperature measurementstaken by simple waterproof sensors may not reflect the actual
body temperatures of an organism (Fitzhenry et al. 2004).Technological advances within the past decade, however, haveallowed marine ecologists to use biomimetic loggers to record
the temperatures experienced by target organisms over extendedperiods of time (Pincebourde et al. 2008; Broitman et al. 2009;Lima and Wethey 2009; Szathmary et al. 2009). These biomi-metic loggers are capable of estimating interspecific variation in
body temperatures because they incorporate the unique mor-phological characteristics (i.e. size, colour, shape and composi-tion) of each species. Biomimetic loggers have been used
successfully tomeasure broad-scale body temperatures of single
Marine and Freshwater Research, 2015, 66, 8694
Journal compilation CSIRO 2015 www.publish.csiro.au/journals/mfr
species (Helmuth 2002; Helmuth et al. 2006a; Seabra et al.2011) but we know of only one study that has made interspecific
comparisons using biomimetic technology (Broitman et al.2009) and one other that uses infrared thermography (Cox andSmith 2011). These studies revealed that body temperatures
of different species occupying the samemicrohabitat could varyat times by 5 to 108C, demonstrating the need for additionalinterspecific comparisons in order to predict how spatial het-
erogeneity of the thermal environment will impact on intertidalcommunities. Therefore, by developing biomimetic loggers forseveral co-occurring species, ecologists can investigate the roletemperature plays in regulating interspecific interactions.
On rocky intertidal shores of south-eastAustralia, interactionsbetween several dominant benthic invertebrates have previouslybeen shown to strongly influence community structure (Denley
and Underwood 1979; Creese 1982; Jernakoff 1983; Underwoodet al. 1983; Fairweather 1988a, 1988b). Key species include thebarnacle Tesseropora rosea, the limpet Cellana tramoserica and
the predatory whelkDicathais orbita. Here, adult T. rosea have anegative effect on C. tramoserica by reducing grazing activitiesand growth rates (Underwood et al. 1983). In turn, grazingactivities ofC. tramoserica reduce the survival of recently settled
T. rosea larvae. Processes affecting the relative abundance ofT. rosea are particularly important since: (1) T. rosea is thepreferred prey of several predatory whelks, including D. orbita
(Fairweather 1988a, 1988b); (2) adult T. rosea provide importantmicrohabitats for several small gastropods (Creese 1982;Chapman 1994); and (3) the presence of T. rosea promotes the
settlement and growth ofmacroalgae and conspecifics (Jernakoff1983; Lathlean et al. 2012, 2013). Understanding how bodytemperatures vary among each of these interacting specieswithin
various microhabitats will improve our ability to predict futurespecies interactions and community-level responses to climatechange (Kordas et al. 2011).
The aim of this study was to compare the body temperatures
of three interacting species of intertidal invertebrates acrossseveral common microhabitats on a single rocky shore. We didthis by designing and deploying biomimetic temperature loggers
that mimic the habitat-forming barnacle T. rosea, the predatorywhelk D. orbita, and the intertidal limpet C. tramoserica. Ourfirst objective was to test whether the unique morphological
characteristics of each species influenced the body temperaturesof individuals exposed to the same environmental conditions.Our second objective was to investigate whether the bodytemperatures of invertebrates are lower when they occupy
certain microhabitats thus allowing those habitats to functionas thermal refugia.
Study location and species
The study was undertaken on an exposed rocky shore at GarieBeach (34810038.100S, 151803057.800E) near Sydney in south-eastern Australia. The rocky platform at Garie Beach is pri-
marily composed of siltstone and is grey in colour. The platformhas an east to south-easterly aspect and an overall slight tomoderate (0 to 208) inclination. The topographic landscape ofthe rocky platform is moderately complex, producing a variety
ofmicrohabitats including,most notably, vertical and horizontal
surfaces, rock pools and crevices. T. rosea and C. tramosericaare typically found on horizontal to vertical emergent rocky
substrata exposed to full sunlight within the mid shore region onexposed rocky shores (Denley and Underwood 1979; Under-wood et al. 1983; Hidas et al. 2013).D. orbita is, however, more
abundant within crevices and shallow rock pools within both themid- and low-shore regions and is typically not found on verticalsurfaces (Phillips and Campbell 1974; Fairweather 1988a,
1988b). Rocky shores within this region experiencemixed semi-diurnal tides with a daily tidal range of 1.5 to 2m.
Biomimetic logger design and deployment
Biomimetic loggers for each of the three species were designedfollowing Lima and Wethey (2009). For each logger, thisinvolved dissecting a DS1922L iButton and removing the
internal circuit board and lithium battery. Two exposed con-stantan wires penetrating the shells of the limpet and whelk, andthe test of the barnacle, were used as contacts for logger pro-
gramming and subsequent data retrieval (Fig. 1). These wereconnected to the logger circuit board by soldering two pieces ofwirewrap wire to either the negative or IO terminal. Once con-nected each logger was coated in a waterproof resin (3M
Scotchcast 2130 Flame Retardant Compound) and placed insidean empty test or shell where extra resin was used to fill anyinterstitial space. Temperatures recorded by these biomimetic
loggers will therefore be strongly influenced by the thermalproperties of this resin. Lima and Wethey (2009) demonstratedthat 3M Scotchcast 2130 effectively mimicks the thermal