Using biomimetic loggers to measure interspecificand microhabitat variation in body temperaturesof rocky intertidal invertebrates

Justin A LathleanAC David J AyreA Ross A ColemanB

and Todd E MinchintonA

AInstitute for Conservation Biology and Environmental Management amp School of Biological

Sciences University of Wollongong NSW 2522 AustraliaBCentre for Research on Ecological Impacts of Coastal Cities School of Biological Sciences

The University of Sydney NSW 2006 AustraliaCCorresponding author Email jlathleangmailcom

Abstract Until recently marine scientists have relied heavily on satellite sea surface temperatures and terrestrial

weather stations as indicators of theway inwhich the thermal environment and hence the body temperatures of organismsvary 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 1118C on horizontal rocky substrata Across microhabitats daily maximal temperatures of thelimpet Cellana tramoserica were on average 21 and 318C higher than body temperatures of the whelk Dicathais orbita

and the barnacle Tesseropora rosea respectively Among-microhabitat variation in each speciesrsquo 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 248C cooler than those on horizontal rock Likewise dailymaximal body temperatures of whelks were on average 318C 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 speciesrsquo capacity to cope with climate change

Additional keywords Australia barnacle Cellana tramoserica climate change Dicathais orbita habitat temperaturelimpet Tesseropora rosea whelk

Received 1 November 2013 accepted 13 March 2014 published online 26 November 2014

Introduction

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 2009Lima 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 (ie size colour shape and composi-tion) of each species Biomimetic loggers have been used

successfully tomeasure broad-scale body temperatures of single

CSIRO PUBLISHING

Marine and Freshwater Research 2015 66 86ndash94

httpdxdoiorg101071MF13287

Journal compilation CSIRO 2015 wwwpublishcsiroaujournalsmfr

Short Communication

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 1982Chapman 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 conditionsOur 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

Methods

Study location and species

The study was undertaken on an exposed rocky shore at GarieBeach (34810038100S 151803057800E) 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 includingmost notably vertical and horizontal

surfaces rock pools and crevices T rosea and C tramoserica

are 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 15 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

properties of the limpet Tectura persona Therefore the resinlikely acts as an effective surrogate for the internal tissue ofmany marine invertebrates

Since intraspecific variation in body size could lead todifferent heating rates and body temperatures we selectedgastropod shells and barnacle tests of roughly equivalent volumeand filled these with approximately the same amount of resin

Particular care was takenwhen constructing the barnacle loggersto ensure that the operculum remained intact and in the correctposition Once resin had set loggers were calibrated in the

laboratory and deployed into the field usingA-788Z-Spar SplashCompound (Kopperrsquos Co USA) (Fig 1) Calibration involvedplacing all loggers under identical thermal conditions in a

temperature controlled room Differences among all loggersunder these conditions were typical between 01 and 028C

Biomimetic loggers for each species were deployed acrosscommon and abundant microhabitats within the midshore

region at Garie Beach between 5 March and 11 April 2013and body temperatures were recorded every 10min at a resolu-tion of 006258C Four biomimetic loggers for C tramoserica

and four T rosea loggers were attached to either horizontal orsouthward facing vertical emergent rocky substrata (nfrac14 2loggers per microhabitat) while four D orbita loggers were

either submerged in rock pools 01m deep or attached toemergent horizontal rocky substrata (nfrac14 2 loggers per micro-habitat) These microhabitats encompass the most thermally

distinct regions within the mid-intertidal region at Garie Beachfor each species (hereafter referred to either benign or stressfulmicrohabitats) The two microhabitats selected for D orbitawere also intended to reflect the body temperatures of aerially

exposed animals foraging among barnacles and non-foraging

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 87

animals submerged in shallow rock pools Two unmodifiedTidbiT v2 Temp data loggers (Onset Stowaway logger

model UTBI-001 accuracy 028C) with a sampling freq-uency of 10min were also attached to horizontal and southerly

facing vertical rocky substrata (nfrac14 2 loggers per microhabitat)05m to 1m away from biomimetic loggers to compare

temperatures of the lsquomicrohabitatrsquo with that of the three studyspecies Later comparisons between these unmodified Tidbitsand iButton loggers embedded in nearby (1m) rocky substrata

revealed a strong relationship between the two temperaturemeasurements (R2frac14 0883 P 0001 nfrac14 1315) Thereforetemperatures measured by the Tidbit loggers represent an

appropriate estimate of habitat temperatureThe accuracy of biomimetic loggers was assessed by

comparing biomimetic body temperatures with that of three orfour similarly sized live specimens on horizontal rock for three

hours during three non-consecutive low tides Thiswas achievedby inserting a small thermocouple (HANNA HI 935005K-Thermocouple Thermometer resolution 018C) through a

2-mm hole drilled into the shell or test of the live specimensSimilarly to biomimetic loggers the thermocouple was cali-brated in the laboratory before use and produced accuracies

between 01 and 028C Live specimens were located between5 and 10 cm from biomimetic loggers and were all orientated inthe same direction to ensure small-scale thermal heterogeneitydid not affect our comparisons We deliberately undertook our

comparisons during daytime low tides as these conditionsproduce the greatest absolute temperature differences and ther-mal stress as opposed to night time or during high tide when

body temperatures equilibrate with sea temperatures Bodytemperatures of live limpets were highly correlated with biomi-metic temperatures (Fig 2a) with differences being on average

018C (01 se) and no greater than 128C Likewise bodytemperatures of live barnacleswere significantly correlatedwithbiomimetic temperatures (Fig 2b) with differences being on

average 088C (01 se) and no more than 158C Whenmeasuring body temperatures of live whelks in the fieldindividuals would retreat into their shells after being disturbedand would not reattach to the substrata for several hours This

behaviour precluded appropriate comparisons between livewhelks and biomimetic loggers Nevertheless body tempera-tures of live whelks were highly correlated with biomimetic

temperatures (Fig 2c) with differences being on average 208C(03 se) and a maximal difference of 448C Such largediscrepancies between body temperatures of live whelks and

biomimetic loggers were most likely the result of the observedretraction into shell Consequently comparisons of biomimeticdata with in situ body temperatures of live whelks should beviewed with caution

Data analysis

Temperatures recorded by paired biomimetic or TidbiT loggers

within each microhabitat were averaged to produce a singlevalue for each 10min interval Two-factor analysis of variance(ANOVA) was then used to test for statistically significant

differences in body temperatures (mean daily maxima meanand mean daily minima) among species (C tramoserica

T rosea and D orbita) between the different microhabitats

(benign and stressful) One-factor ANOVA was used to test forstatistically significant differences in microhabitat temperatures(mean daily maxima mean and mean daily minima) recordedby TidbiT loggers deployed on horizontal surfaces with

(1) body temperatures of each species and (2) southward-facing

(a)

10 mm

(b)

10 mm

(c)

10 mm

Fig 1 Biomimetic loggers used to record body temperatures of Cellana

tramoserica (a) Tesseropora rosea (b) and Dicathais orbita (c) Note the

external constantan wires used for communicating with computer

88 Marine and Freshwater Research J A Lathlean et al

surfaces Prior to analyses the assumption of homosce-dasticity was checked using ShapirondashWilksrsquo and Cochranrsquostests Where significant differences were found with ANOVAStudentndashNeumanndashKeuls (SNK) tests were used to determine

which species and microhabitats displayed significantly differ-ent body temperatures Due to two malfunctioning T rosea

biomimetic loggers deployed on southward-facing vertical

surfaces analyses were only carried out for measurements takenbetween the 5 and 14 March 2013

Results

Comparisons among microhabitatsand body temperatures

Microhabitat temperatures recorded using unmodified Tidbitloggers were significantly greater than body temperatures

recorded by each of the three different biomimetic loggers inboth thermally stressful and benign microhabitats (Fig 3Table 1) This was most obvious in the stressful microhabitat

(ie horizontal rocky substrata) and for comparisons ofmean daily maximal temperatures and less obvious for dailyminimum temperatures For horizontal rocky substrata tem-peratures reached as high as 4428C which was 88 91 and

1118C higher than the maximal body temperatures ofD orbitaC tramoserica and T rosea respectively On average habitattemperatures were 18 20 and 268C higher than the average

body temperatures of D orbita C tramoserica and T rosea

respectively (Fig 3)

Interspecific comparisons

In both benign and stressful microhabitats body temperaturesrecorded by biomimetic loggers revealed that the limpetC tramoserica experienced consistently higher body tempera-

tures than both the barnacle T rosea and whelkD orbita (Fig 3Table 2) This was most obvious when comparing the dailymean and maxima body temperature of each species (Table 2)

Irrespective of microhabitat the daily maximal body tempera-tures of C tramoserica were on average 21 and 318C warmerthan D orbita and T rosea respectively Interestingly absolutemaximal body temperatures of C tramoserica (3518C) and

D orbita (3548C) within the thermally stressful microhabitathorizontal emergent rock were both several degrees higher thanthe maximal body temperature recorded by T rosea mimics

(3318C) (Fig 3)

Microhabitat comparisons

Habitat and body temperatures recorded by loggers attached tohorizontal emergent rock were consistently higher and dis-played greater daily fluctuations than equivalent measurementstaken on either south-facing vertical surfaces or within shallow

rock pools (Fig 4 Table 2)Measurements taken by unmodifiedloggers revealed that horizontal surfaces experienced signifi-cantly greater daily maximal (F174frac14 1666 P 0001) and

daily mean (F174frac14 2982 P 0001) temperatures than nearbyvertical surfaces with differences as great as 818C (Fig 4a)Likewise daily maximal temperatures of T rosea mimics

placed on southerly facing vertical surfaces were on average248C cooler than those on horizontal emergent rock (Fig 4c)Similarly daily maximal body temperatures of whelks were on

average 318C cooler within shallow rock pools than on hori-zontal emergent rock (Fig 4d ) Among the three study speciesD orbitamimics displayed the greatest microhabitat variabilityin temperatures For example maximal temperatures of

D orbita on horizontal emergent rock were up to 658C higherthan equivalent body temperatures recorded in nearby shallowrock pools (Fig 4d ) By comparison themaximal differences in

body temperatures of C tramoserica and T rosea among thebenign and stressful habitats were 29 and 508C respectivelyInterestingly there was no difference in mean daily maximal

temperatures of C tramoserica mimics placed on either hori-zontal or vertical rocky substrata

Discussion

This study takes advantage of recently developed biomimetic

technology (Lima and Wethey 2009) to estimate the bodytemperatures of three co-occurring species with distinct mor-phological characteristics This is the first time biomimetic

loggers have been used to compare body temperatures of threespecies simultaneously Results highlight that even over a shortperiod of thermal stress morphological differences between

species can alter body temperatures and thus could have con-sequences for interspecific interactions and community-levelprocesses Daily maximal temperatures of limpet mimics wereon average 21 and 318C higher than temperatures of whelk

and barnacle mimics with habitat temperatures up to 1118Chigher than biomimetic measurements These results supportseveral recent studies that show body temperatures of rocky

intertidal ectotherms to be significantly different to ambient

20

25

30

35

20 25 30 35

(R 2 091 P 0001 n 51) (R 2 096 P 0001 n 73) (R 2 096 P 0001 n 18)

20

25

30

35

20 25 30 3520

25

30

35

20 25 30 35

(a) (b) (c)

Biomimetic temperature (C)

Bod

y te

mpe

ratu

re (

C)

Fig 2 Comparisons between biomimetic body temperatures and those recorded for live Cellana tramoserica (a) Tesseropora rosea (b) and

Dicathais orbita (c) 5ndash10 cm away during several daytime low tides

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 89

temperatures (Fitzhenry et al 2004 Szathmary et al 2009)in addition to interspecific variations for animals (Broitmanet al 2009)

We know of only one other study that has simultaneouslymeasured body temperatures of multiple species of rockyintertidal invertebrates using biomimetic technology Broitman

et al (2009) demonstrated that body temperatures of a keystonepredator (the seastar Pisaster ochraceus) were at times in excess

of 108C lower than its prey (the mussel Mytilus californianus)even though both were within the same microhabitat Suchdramatic differences in the body temperatures of P ochraceus

and M californianus are most likely due to differences inmorphology and reflectance (ie P ochraceus is larger thanM californianus does not have a calcareous shell and is usually

brightly coloured) In contrast the three species examined in ourwork all possess an external calcareous shell or test and are all

15

20

25

30

35

40

45Daily maxima

15

20

25

30

35

40

45Habitat Cellana

Tesseropora Dicathaislowast

15

20

25

30Daily mean

15

20

25

30

10

15

20

25Daily minima

10

15

20

25

Mic

roha

bita

tbod

y te

mpe

ratu

re (

C)

Stressful Benign

05-M

ar-1

3

09-M

ar-1

3

13-M

ar-1

3

17-M

ar-1

3

21-M

ar-1

3

25-M

ar-1

3

29-M

ar-1

3

02-A

pr-1

3

06-A

pr-1

3

10-A

pr-1

3

05-M

ar-1

3

09-M

ar-1

3

13-M

ar-1

3

17-M

ar-1

3

21-M

ar-1

3

25-M

ar-1

3

29-M

ar-1

3

02-A

pr-1

3

06-A

pr-1

3

10-A

pr-1

3

Fig 3 Daily maxima mean and minima body temperatures of three different species of rocky intertidal invertebrates compared with habitat

temperature within stressful horizontal (left column) and benign southward facing vertical surfaces (right column) in the mid shore region at

Garie Beach from 5 March to 11 April 2013 Dicathais loggers were placed in shallow rock pools instead of vertical surfaces

90 Marine and Freshwater Research J A Lathlean et al

relatively small (20ndash50mm in length) with no large variationin colour (brown to grey) Regardless we detected significantdifferences in body temperatures of our three species among

multiple microhabitats Such differences in body tempera-ture may have dramatic consequences for interspecific interac-tions and the organisation of rocky intertidal communitieswithin this region

We found that microhabitats were a considerable source oftemperature variability for all three species This supports agrowing body of work that shows small-scale habitat hetero-

geneity is themajor source of body temperature variability amongrocky intertidal invertebrates (Denny et al 2004 Harley 2008Meager et al2011Lathlean et al 2012 2013)Microhabitats that

act as thermal refugia are expected to play an increasinglyimportant role in mitigating the future impacts of climate changeon these benthic communities For example with increasingthermal stress expected to occur on rocky intertidal shores of

south-east Australia we might expect (1) reduced foraging ratesof D orbita as they remain within shallow rock pools for longerperiods of time and (2) migration of C tramoserica away from

horizontal substrata to cooler southerly facing vertical surfacesBoth of these changes would positively affect T rosea byreducing early post-settlement mortality caused by grazing

C tramoserica and the predation of adults by D orbita Conse-quently rocky intertidal communities along the south-east coastof Australia may become increasingly dominated by T rosea

(Underwood et al 1983) Further experimental evidence howev-er is required to determinewhether increasedheat stresswill elicitsuch responses (eg Lathlean and Minchinton 2012)

Predicting the strength of speciesrsquo interactions under futureclimate change scenarios depends largely on understanding theunique physiological responses of individual species in a com-

munity context (Russell et al 2012) Body temperature mea-surements as presented here represent a useful method ofassessing the physiological response of individual organisms

to changing environmental conditions The application of infra-red thermography to rocky intertidal systems has also emergedas an effective means of estimating intra- and inter-specific

variation in body temperatures (Caddy-Retalic et al 2011Chapperon and Seuront 2011a Cox and Smith 2011 Lathleanet al 2012) and could serve as a complementary approach tobiomimetic technology Infrared thermography is particularly

useful for investigating the role of thermoregulatory behaviour(Chapperon and Seuront 2011a 2011b 2012) which wasnot accounted for within the present study More is needed

however because body temperatures alone cannot informresearchers whether an organism is thermally stressed Bodytemperature measurements need to be placed within a physio-

logical context that considers how thermal limits of a speciesvary across broad geographic scales (Tomanek 2008 Dennyand Helmuth 2009 Somero 2010) Unfortunately these funda-mental physiological parameters have yet to be determined for

the majority of rocky intertidal invertebrates of south-eastAustralia To help safeguard these vulnerable benthic commu-nities to climate change (Denny and Harley 2006 Wernberg

et al 2011) we suggest future research should focus on

Table 2 Summary of two-factor ANOVA and SNK for the effect of

species (C tramoserica T rosea D orbita) and microhabitat (benign

stressful) on daily maximal mean and minimum body temperatures

Source df SS F-ratio P-value

Daily Maxima

Species 2 100145 4587 0015

Microhabitat 1 44873 4110 0048

SpeciesMicrohabitat 2 30781 1410 0253

Error 54 589521

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

StressfulBenign

Daily Mean

Species 2 17151 7117 0002

Microhabitat 1 0030 0025 0875

SpeciesMicrohabitat 2 5141 2133 0128

Error 54 65067

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

Stressfulfrac14Benign

Daily Minima

Species 2 11525 4051 0023

Microhabitat 1 6177 4342 0042

SpeciesMicrohabitat 2 4501 1582 0215

Error 54 76818

SNK [species] Cellana

Tesseropora

SNK [microhabitat]

StressfulBenign

Table 1 Summary of one-factor ANOVA and SNK tests for the effect

of environmental and species temperature (daily maxima mean and

minima) recorded by TidbiT loggers and the three different biomimetic

loggers attached to horizontal emergent rocky substrata

Source df SS F-ratio P-value

Stressful microhabitat

Daily Maxima 3 472627 9306 0001

Error 36 609445

SNK HabitatAll species

Daily Mean 3 57701 13419 0001

Error 36 51599

SNK HabitatAll species

Daily Minima 3 11786 3929 0034

Error 36 43807

SNK Habitat

Tesseropora only

Benign microhabitat

Daily Maxima 3 245123 7901 0001

Error 36 372295

SNK Habitat and Cellana

Dicathais and Tesseropora

Daily mean 3 28304 9435 0001

Error 36 35118

SNK Habitat and Cellana

Dicathais and Tess

Daily Minima 3 13862 3160 0036

Error 36 52643

SNK Cellana

Dicathais and Tesseropora

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 91

10

15

20

25

30

35

40

45 Habitat

10

15

20

25

30

35

40

45Cellana

10

15

20

25

30

35

40

45Tesseropora

10

15

20

25

30

35

40

45Dicathais

Bod

ym

icro

habi

tat t

empe

ratu

re (

C)

5-Mar 6-Apr9-Mar 10-Apr13-Mar 17-Mar 21-Mar 25-Mar 29-Mar 2-Apr

(a)

(b)

(c)

(d )

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Rockpool

Fig 4 Microhabitat (a) and body temperatures of the limpet Cellana tramoserica (b) the barnacle

Tesseropora rosea (c) and the whelk Dicathais orbita (d ) within thermally stressful (horizontal

substrata) and thermally benign (southerly facing vertical substrata) microhabitats within the midshore

region at Garie Beach from 5 March to 11 April 2013 Body temperatures of T rosea attached to

southerly facing vertical surfaces were only recorded up until the 14 March due to malfunctioning

loggers

92 Marine and Freshwater Research J A Lathlean et al

(i) developing long-term body temperature measurements ofmultiple species using biomimetic loggers and (ii) undertake

physiological experiments aimed at calculating biogeographicvariability in speciesrsquo thermal limits

Acknowledgements

We thank Samuel Wighton and Elizabeth Lathlean for assistance with

biomimetic construction This research was supported by the Institute of

Conservation Biology and Environmental Management at the University

of Wollongong

References

Broitman B R Szathmary P L Mislan K A S Blanchette C A and

Helmuth B (2009) Predator-prey interactions under climate change

the importance of habitat vs body temperature Oikos 118 219ndash224

doi101111J1600-0706200817075X

Caddy-Retalic S Benkendorff K and Fairweather P G (2011) Visual-

izing hotspots Applying thermal imaging to monitor internal tempera-

tures in intertidal gastropods Molluscan Research 31 106ndash113

Chapman M G (1994) Small-scale patterns of distribution and size-

structure of the intertidal littorinid Littorina unifasciata (Gastropoda

Littorinidae) in New South Wales Australian Journal of Marine and

Freshwater Research 45 635ndash652 doi101071MF9940635

Chapperon C and Seuront L (2011a) Space-time variability in environ-

mental thermal properties and snail thermoregulatory behaviour

Functional Ecology 25 1040ndash1050 doi101111J1365-24352011

01859X

Chapperon C and Seuront L (2011b) Behavioral thermoregulation in a

tropical gastropod Links to climate change scenarios Global Change

Biology 17 1740ndash1749 doi101111J1365-2486201002356X

Chapperon C and Seuront L (2012) Keeping warm in the cold On the

thermal benefits of aggregation behaviour in an intertidal ectotherm

Journal of Thermal Biology 37 640ndash647 doi101016JJTHERBIO

201208001

Cox T E and Smith C M (2011) Thermal ecology on an exposed algal

reef infrared imagery a rapid tool to survey temperature at local spatial

scales Coral Reefs 30 1109ndash1120 doi101007S00338-011-0799-2

Creese R G (1982) Distribution and abundance of the Acmaeid Limpet

Patelloida latistrigata and its interaction with barnacles Oecologia 52

85ndash96 doi101007BF00349015

Denley E J and Underwood A J (1979) Experiments on factors

influencing settlement survival and growth of two species of barnacles

in New South Wales Journal of Experimental Marine Biology and

Ecology 36 269ndash293 doi1010160022-0981(79)90122-9

Denny M W and Harley C D G (2006) Hot limpets predicting body

temperature in a conductance-mediated thermal system The Journal of

Experimental Biology 209 2409ndash2419 doi101242JEB02257

Denny M and Helmuth B (2009) Confronting the physiological bottle-

neck A challenge from ecomechanics Integrative and Comparative

Biology 49 197ndash201 doi101093ICBICP070

DennyMW Helmuth B Leonard G H Harley C D G Hunt L J H

and Nelson E K (2004) Quantifying scale in ecology Lessons from

a wave-swept shore Ecological Monographs 74 513ndash532 doi101890

03-4043

DennyMWDowdWWBilir L andMachK J (2011) Spreading the

risk Small-scale body temperature variation among intertidal organisms

and its implications for species persistence Journal of Experimental

Marine Biology and Ecology 400 175ndash190 doi101016JJEMBE

201102006

Fairweather P G (1988a) Correlations of predatory whelks with intertidal

prey at several scales of space and timeMarine Ecology Progress Series

45 237ndash243 doi103354MEPS045237

Fairweather P G (1988b) Movements of intertidal whelks (Morula

marginalba and Thais orbita) in relation to availability of prey and

shelter Marine Biology 100 63ndash68 doi101007BF00392955

Fitzhenry T Halpin P M and Helmuth B (2004) Testing the effects of

wave exposure site and behavior on intertidal mussel body tempera-

tures applications and limits of temperature logger design Marine

Biology 145 339ndash349 doi101007S00227-004-1318-6

Harley C D G (2008) Tidal dynamics topographic orientation and

temperature-mediatedmassmortalities on rocky shoresMarineEcology

Progress Series 371 37ndash46 doi103354MEPS07711

Helmuth B (2002) How do we measure the environment Linking

intertidal thermal physiology and ecology through biophysics Integra-

tive and Comparative Biology 42 837ndash845 doi101093ICB424837

Helmuth B Broitman B R Blanchette C A Gilman S E Halpin PM

Harley C D G OrsquoDonnell M Hoffmann A A Menge B A and

Strickland D (2006a) Mosaic patterns of thermal stress in the rocky

intertidal zone implications for climate change Ecological Monographs

76 461ndash479 doi1018900012-9615(2006)076[0461MPOTSI]20CO2

Helmuth B Mieszkowska N Moore P and Hawkins S J (2006b)

Living on the edge of two changing worlds forecasting the responses of

rocky intertidal ecosystems to climate change Annual Review of

Ecology Evolution and Systematics 37 373ndash404 doi101146

ANNUREVECOLSYS37091305110149

Hidas E Z Russell K G Ayre D J and Minchinton T E (2013)

Abundance of Tesseropora rosea at the margins of its biogeographic

range is closely linked to recruitment but not fecundityMarine Ecology

Progress Series 483 199ndash208 doi103354MEPS10271

Jernakoff P (1983) Factors affecting the recruitment of algae in a midshore

region dominated by barnacles Journal of ExperimentalMarine Biology

and Ecology 67 17ndash31 doi1010160022-0981(83)90132-6

Kordas R L Harley C D G and OrsquoConnor M I (2011) Community

ecology in a warming world The influence of temperature on interspe-

cific interactions in marine systems Journal of Experimental Marine

Biology and Ecology 400 218ndash226 doi101016JJEMBE201102029

Lathlean J A and Minchinton T E (2012) Manipulating thermal stress

on rocky shores to predict patterns of recruitment ofmarine invertebrates

under a changing climate Marine Ecology Progress Series 467

121ndash136 doi103354MEPS09996

Lathlean J A Ayre D J and Minchinton T E (2012) Using infrared

imagery to test for quadrat-level temperature variation and effects on the

early life history of a rocky-shore barnacle Limnology and Oceanogra-

phy 57 1279ndash1291 doi104319LO20125751279

Lathlean J A Ayre D J and Minchinton T E (2013) Temperature

variability at the larval scale affects early survival and growth of an

intertidal barnacle Marine Ecology Progress Series 475 155ndash166

doi103354MEPS10105

Lima F P and Wethey D S (2009) Robolimpets measuring intertidal

body temperatures using biomimetic loggers Limnology and Oceanog-

raphy Methods 7 347ndash353 doi104319LOM20097347

Meager J J Schlacher T A and Green M (2011) Topographic

complexity and landscape temperature patterns create a dynamic habitat

structure on a rocky intertidal shore Marine Ecology Progress Series

428 1ndash12 doi103354MEPS09124

Phillips B F and Campbell N A (1974) Mortality and longevity in the

whelk Dicathais orbita (Gmelin) Australian Journal of Marine and

Freshwater Research 25 25ndash33 doi101071MF9740025

Pincebourde S Sanford E and Helmuth B (2008) Body temperatures

during low tide alters the feeding performance of a top intertidal

predator Limnology and Oceanography 53 1562ndash1573 doi104319

LO20085341562

Russell B D Harley C D G Wernberg T Mieszkowska N Widdi-

combe S Hall-Spencer J M and Connell S D (2012) Predicting

ecosystem shifts requires new approaches that integrate the effects of

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 93

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 1982Chapman 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 conditionsOur 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

Methods

Study location and species

The study was undertaken on an exposed rocky shore at GarieBeach (34810038100S 151803057800E) 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 includingmost notably vertical and horizontal

surfaces rock pools and crevices T rosea and C tramoserica

are 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 15 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

properties of the limpet Tectura persona Therefore the resinlikely acts as an effective surrogate for the internal tissue ofmany marine invertebrates

Since intraspecific variation in body size could lead todifferent heating rates and body temperatures we selectedgastropod shells and barnacle tests of roughly equivalent volumeand filled these with approximately the same amount of resin

Particular care was takenwhen constructing the barnacle loggersto ensure that the operculum remained intact and in the correctposition Once resin had set loggers were calibrated in the

laboratory and deployed into the field usingA-788Z-Spar SplashCompound (Kopperrsquos Co USA) (Fig 1) Calibration involvedplacing all loggers under identical thermal conditions in a

temperature controlled room Differences among all loggersunder these conditions were typical between 01 and 028C

Biomimetic loggers for each species were deployed acrosscommon and abundant microhabitats within the midshore

region at Garie Beach between 5 March and 11 April 2013and body temperatures were recorded every 10min at a resolu-tion of 006258C Four biomimetic loggers for C tramoserica

and four T rosea loggers were attached to either horizontal orsouthward facing vertical emergent rocky substrata (nfrac14 2loggers per microhabitat) while four D orbita loggers were

either submerged in rock pools 01m deep or attached toemergent horizontal rocky substrata (nfrac14 2 loggers per micro-habitat) These microhabitats encompass the most thermally

distinct regions within the mid-intertidal region at Garie Beachfor each species (hereafter referred to either benign or stressfulmicrohabitats) The two microhabitats selected for D orbitawere also intended to reflect the body temperatures of aerially

exposed animals foraging among barnacles and non-foraging

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 87

animals submerged in shallow rock pools Two unmodifiedTidbiT v2 Temp data loggers (Onset Stowaway logger

model UTBI-001 accuracy 028C) with a sampling freq-uency of 10min were also attached to horizontal and southerly

facing vertical rocky substrata (nfrac14 2 loggers per microhabitat)05m to 1m away from biomimetic loggers to compare

temperatures of the lsquomicrohabitatrsquo with that of the three studyspecies Later comparisons between these unmodified Tidbitsand iButton loggers embedded in nearby (1m) rocky substrata

revealed a strong relationship between the two temperaturemeasurements (R2frac14 0883 P 0001 nfrac14 1315) Thereforetemperatures measured by the Tidbit loggers represent an

appropriate estimate of habitat temperatureThe accuracy of biomimetic loggers was assessed by

comparing biomimetic body temperatures with that of three orfour similarly sized live specimens on horizontal rock for three

hours during three non-consecutive low tides Thiswas achievedby inserting a small thermocouple (HANNA HI 935005K-Thermocouple Thermometer resolution 018C) through a

2-mm hole drilled into the shell or test of the live specimensSimilarly to biomimetic loggers the thermocouple was cali-brated in the laboratory before use and produced accuracies

between 01 and 028C Live specimens were located between5 and 10 cm from biomimetic loggers and were all orientated inthe same direction to ensure small-scale thermal heterogeneitydid not affect our comparisons We deliberately undertook our

comparisons during daytime low tides as these conditionsproduce the greatest absolute temperature differences and ther-mal stress as opposed to night time or during high tide when

body temperatures equilibrate with sea temperatures Bodytemperatures of live limpets were highly correlated with biomi-metic temperatures (Fig 2a) with differences being on average

018C (01 se) and no greater than 128C Likewise bodytemperatures of live barnacleswere significantly correlatedwithbiomimetic temperatures (Fig 2b) with differences being on

average 088C (01 se) and no more than 158C Whenmeasuring body temperatures of live whelks in the fieldindividuals would retreat into their shells after being disturbedand would not reattach to the substrata for several hours This

behaviour precluded appropriate comparisons between livewhelks and biomimetic loggers Nevertheless body tempera-tures of live whelks were highly correlated with biomimetic

temperatures (Fig 2c) with differences being on average 208C(03 se) and a maximal difference of 448C Such largediscrepancies between body temperatures of live whelks and

biomimetic loggers were most likely the result of the observedretraction into shell Consequently comparisons of biomimeticdata with in situ body temperatures of live whelks should beviewed with caution

Data analysis

Temperatures recorded by paired biomimetic or TidbiT loggers

within each microhabitat were averaged to produce a singlevalue for each 10min interval Two-factor analysis of variance(ANOVA) was then used to test for statistically significant

differences in body temperatures (mean daily maxima meanand mean daily minima) among species (C tramoserica

T rosea and D orbita) between the different microhabitats

(benign and stressful) One-factor ANOVA was used to test forstatistically significant differences in microhabitat temperatures(mean daily maxima mean and mean daily minima) recordedby TidbiT loggers deployed on horizontal surfaces with

(1) body temperatures of each species and (2) southward-facing

(a)

10 mm

(b)

10 mm

(c)

10 mm

Fig 1 Biomimetic loggers used to record body temperatures of Cellana

tramoserica (a) Tesseropora rosea (b) and Dicathais orbita (c) Note the

external constantan wires used for communicating with computer

88 Marine and Freshwater Research J A Lathlean et al

surfaces Prior to analyses the assumption of homosce-dasticity was checked using ShapirondashWilksrsquo and Cochranrsquostests Where significant differences were found with ANOVAStudentndashNeumanndashKeuls (SNK) tests were used to determine

which species and microhabitats displayed significantly differ-ent body temperatures Due to two malfunctioning T rosea

biomimetic loggers deployed on southward-facing vertical

surfaces analyses were only carried out for measurements takenbetween the 5 and 14 March 2013

Results

Comparisons among microhabitatsand body temperatures

Microhabitat temperatures recorded using unmodified Tidbitloggers were significantly greater than body temperatures

recorded by each of the three different biomimetic loggers inboth thermally stressful and benign microhabitats (Fig 3Table 1) This was most obvious in the stressful microhabitat

(ie horizontal rocky substrata) and for comparisons ofmean daily maximal temperatures and less obvious for dailyminimum temperatures For horizontal rocky substrata tem-peratures reached as high as 4428C which was 88 91 and

1118C higher than the maximal body temperatures ofD orbitaC tramoserica and T rosea respectively On average habitattemperatures were 18 20 and 268C higher than the average

body temperatures of D orbita C tramoserica and T rosea

respectively (Fig 3)

Interspecific comparisons

In both benign and stressful microhabitats body temperaturesrecorded by biomimetic loggers revealed that the limpetC tramoserica experienced consistently higher body tempera-

tures than both the barnacle T rosea and whelkD orbita (Fig 3Table 2) This was most obvious when comparing the dailymean and maxima body temperature of each species (Table 2)

Irrespective of microhabitat the daily maximal body tempera-tures of C tramoserica were on average 21 and 318C warmerthan D orbita and T rosea respectively Interestingly absolutemaximal body temperatures of C tramoserica (3518C) and

D orbita (3548C) within the thermally stressful microhabitathorizontal emergent rock were both several degrees higher thanthe maximal body temperature recorded by T rosea mimics

(3318C) (Fig 3)

Microhabitat comparisons

Habitat and body temperatures recorded by loggers attached tohorizontal emergent rock were consistently higher and dis-played greater daily fluctuations than equivalent measurementstaken on either south-facing vertical surfaces or within shallow

rock pools (Fig 4 Table 2)Measurements taken by unmodifiedloggers revealed that horizontal surfaces experienced signifi-cantly greater daily maximal (F174frac14 1666 P 0001) and

daily mean (F174frac14 2982 P 0001) temperatures than nearbyvertical surfaces with differences as great as 818C (Fig 4a)Likewise daily maximal temperatures of T rosea mimics

placed on southerly facing vertical surfaces were on average248C cooler than those on horizontal emergent rock (Fig 4c)Similarly daily maximal body temperatures of whelks were on

average 318C cooler within shallow rock pools than on hori-zontal emergent rock (Fig 4d ) Among the three study speciesD orbitamimics displayed the greatest microhabitat variabilityin temperatures For example maximal temperatures of

D orbita on horizontal emergent rock were up to 658C higherthan equivalent body temperatures recorded in nearby shallowrock pools (Fig 4d ) By comparison themaximal differences in

body temperatures of C tramoserica and T rosea among thebenign and stressful habitats were 29 and 508C respectivelyInterestingly there was no difference in mean daily maximal

temperatures of C tramoserica mimics placed on either hori-zontal or vertical rocky substrata

Discussion

This study takes advantage of recently developed biomimetic

technology (Lima and Wethey 2009) to estimate the bodytemperatures of three co-occurring species with distinct mor-phological characteristics This is the first time biomimetic

loggers have been used to compare body temperatures of threespecies simultaneously Results highlight that even over a shortperiod of thermal stress morphological differences between

species can alter body temperatures and thus could have con-sequences for interspecific interactions and community-levelprocesses Daily maximal temperatures of limpet mimics wereon average 21 and 318C higher than temperatures of whelk

and barnacle mimics with habitat temperatures up to 1118Chigher than biomimetic measurements These results supportseveral recent studies that show body temperatures of rocky

intertidal ectotherms to be significantly different to ambient

20

25

30

35

20 25 30 35

(R 2 091 P 0001 n 51) (R 2 096 P 0001 n 73) (R 2 096 P 0001 n 18)

20

25

30

35

20 25 30 3520

25

30

35

20 25 30 35

(a) (b) (c)

Biomimetic temperature (C)

Bod

y te

mpe

ratu

re (

C)

Fig 2 Comparisons between biomimetic body temperatures and those recorded for live Cellana tramoserica (a) Tesseropora rosea (b) and

Dicathais orbita (c) 5ndash10 cm away during several daytime low tides

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 89

temperatures (Fitzhenry et al 2004 Szathmary et al 2009)in addition to interspecific variations for animals (Broitmanet al 2009)

We know of only one other study that has simultaneouslymeasured body temperatures of multiple species of rockyintertidal invertebrates using biomimetic technology Broitman

et al (2009) demonstrated that body temperatures of a keystonepredator (the seastar Pisaster ochraceus) were at times in excess

of 108C lower than its prey (the mussel Mytilus californianus)even though both were within the same microhabitat Suchdramatic differences in the body temperatures of P ochraceus

and M californianus are most likely due to differences inmorphology and reflectance (ie P ochraceus is larger thanM californianus does not have a calcareous shell and is usually

brightly coloured) In contrast the three species examined in ourwork all possess an external calcareous shell or test and are all

15

20

25

30

35

40

45Daily maxima

15

20

25

30

35

40

45Habitat Cellana

Tesseropora Dicathaislowast

15

20

25

30Daily mean

15

20

25

30

10

15

20

25Daily minima

10

15

20

25

Mic

roha

bita

tbod

y te

mpe

ratu

re (

C)

Stressful Benign

05-M

ar-1

3

09-M

ar-1

3

13-M

ar-1

3

17-M

ar-1

3

21-M

ar-1

3

25-M

ar-1

3

29-M

ar-1

3

02-A

pr-1

3

06-A

pr-1

3

10-A

pr-1

3

05-M

ar-1

3

09-M

ar-1

3

13-M

ar-1

3

17-M

ar-1

3

21-M

ar-1

3

25-M

ar-1

3

29-M

ar-1

3

02-A

pr-1

3

06-A

pr-1

3

10-A

pr-1

3

Fig 3 Daily maxima mean and minima body temperatures of three different species of rocky intertidal invertebrates compared with habitat

temperature within stressful horizontal (left column) and benign southward facing vertical surfaces (right column) in the mid shore region at

Garie Beach from 5 March to 11 April 2013 Dicathais loggers were placed in shallow rock pools instead of vertical surfaces

90 Marine and Freshwater Research J A Lathlean et al

relatively small (20ndash50mm in length) with no large variationin colour (brown to grey) Regardless we detected significantdifferences in body temperatures of our three species among

multiple microhabitats Such differences in body tempera-ture may have dramatic consequences for interspecific interac-tions and the organisation of rocky intertidal communitieswithin this region

We found that microhabitats were a considerable source oftemperature variability for all three species This supports agrowing body of work that shows small-scale habitat hetero-

geneity is themajor source of body temperature variability amongrocky intertidal invertebrates (Denny et al 2004 Harley 2008Meager et al2011Lathlean et al 2012 2013)Microhabitats that

act as thermal refugia are expected to play an increasinglyimportant role in mitigating the future impacts of climate changeon these benthic communities For example with increasingthermal stress expected to occur on rocky intertidal shores of

south-east Australia we might expect (1) reduced foraging ratesof D orbita as they remain within shallow rock pools for longerperiods of time and (2) migration of C tramoserica away from

horizontal substrata to cooler southerly facing vertical surfacesBoth of these changes would positively affect T rosea byreducing early post-settlement mortality caused by grazing

C tramoserica and the predation of adults by D orbita Conse-quently rocky intertidal communities along the south-east coastof Australia may become increasingly dominated by T rosea

(Underwood et al 1983) Further experimental evidence howev-er is required to determinewhether increasedheat stresswill elicitsuch responses (eg Lathlean and Minchinton 2012)

Predicting the strength of speciesrsquo interactions under futureclimate change scenarios depends largely on understanding theunique physiological responses of individual species in a com-

munity context (Russell et al 2012) Body temperature mea-surements as presented here represent a useful method ofassessing the physiological response of individual organisms

to changing environmental conditions The application of infra-red thermography to rocky intertidal systems has also emergedas an effective means of estimating intra- and inter-specific

variation in body temperatures (Caddy-Retalic et al 2011Chapperon and Seuront 2011a Cox and Smith 2011 Lathleanet al 2012) and could serve as a complementary approach tobiomimetic technology Infrared thermography is particularly

useful for investigating the role of thermoregulatory behaviour(Chapperon and Seuront 2011a 2011b 2012) which wasnot accounted for within the present study More is needed

however because body temperatures alone cannot informresearchers whether an organism is thermally stressed Bodytemperature measurements need to be placed within a physio-

logical context that considers how thermal limits of a speciesvary across broad geographic scales (Tomanek 2008 Dennyand Helmuth 2009 Somero 2010) Unfortunately these funda-mental physiological parameters have yet to be determined for

the majority of rocky intertidal invertebrates of south-eastAustralia To help safeguard these vulnerable benthic commu-nities to climate change (Denny and Harley 2006 Wernberg

et al 2011) we suggest future research should focus on

Table 2 Summary of two-factor ANOVA and SNK for the effect of

species (C tramoserica T rosea D orbita) and microhabitat (benign

stressful) on daily maximal mean and minimum body temperatures

Source df SS F-ratio P-value

Daily Maxima

Species 2 100145 4587 0015

Microhabitat 1 44873 4110 0048

SpeciesMicrohabitat 2 30781 1410 0253

Error 54 589521

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

StressfulBenign

Daily Mean

Species 2 17151 7117 0002

Microhabitat 1 0030 0025 0875

SpeciesMicrohabitat 2 5141 2133 0128

Error 54 65067

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

Stressfulfrac14Benign

Daily Minima

Species 2 11525 4051 0023

Microhabitat 1 6177 4342 0042

SpeciesMicrohabitat 2 4501 1582 0215

Error 54 76818

SNK [species] Cellana

Tesseropora

SNK [microhabitat]

StressfulBenign

Table 1 Summary of one-factor ANOVA and SNK tests for the effect

of environmental and species temperature (daily maxima mean and

minima) recorded by TidbiT loggers and the three different biomimetic

loggers attached to horizontal emergent rocky substrata

Source df SS F-ratio P-value

Stressful microhabitat

Daily Maxima 3 472627 9306 0001

Error 36 609445

SNK HabitatAll species

Daily Mean 3 57701 13419 0001

Error 36 51599

SNK HabitatAll species

Daily Minima 3 11786 3929 0034

Error 36 43807

SNK Habitat

Tesseropora only

Benign microhabitat

Daily Maxima 3 245123 7901 0001

Error 36 372295

SNK Habitat and Cellana

Dicathais and Tesseropora

Daily mean 3 28304 9435 0001

Error 36 35118

SNK Habitat and Cellana

Dicathais and Tess

Daily Minima 3 13862 3160 0036

Error 36 52643

SNK Cellana

Dicathais and Tesseropora

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 91

10

15

20

25

30

35

40

45 Habitat

10

15

20

25

30

35

40

45Cellana

10

15

20

25

30

35

40

45Tesseropora

10

15

20

25

30

35

40

45Dicathais

Bod

ym

icro

habi

tat t

empe

ratu

re (

C)

5-Mar 6-Apr9-Mar 10-Apr13-Mar 17-Mar 21-Mar 25-Mar 29-Mar 2-Apr

(a)

(b)

(c)

(d )

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Rockpool

Fig 4 Microhabitat (a) and body temperatures of the limpet Cellana tramoserica (b) the barnacle

Tesseropora rosea (c) and the whelk Dicathais orbita (d ) within thermally stressful (horizontal

substrata) and thermally benign (southerly facing vertical substrata) microhabitats within the midshore

region at Garie Beach from 5 March to 11 April 2013 Body temperatures of T rosea attached to

southerly facing vertical surfaces were only recorded up until the 14 March due to malfunctioning

loggers

92 Marine and Freshwater Research J A Lathlean et al

(i) developing long-term body temperature measurements ofmultiple species using biomimetic loggers and (ii) undertake

physiological experiments aimed at calculating biogeographicvariability in speciesrsquo thermal limits

Acknowledgements

We thank Samuel Wighton and Elizabeth Lathlean for assistance with

biomimetic construction This research was supported by the Institute of

Conservation Biology and Environmental Management at the University

of Wollongong

References

Broitman B R Szathmary P L Mislan K A S Blanchette C A and

Helmuth B (2009) Predator-prey interactions under climate change

the importance of habitat vs body temperature Oikos 118 219ndash224

doi101111J1600-0706200817075X

Caddy-Retalic S Benkendorff K and Fairweather P G (2011) Visual-

izing hotspots Applying thermal imaging to monitor internal tempera-

tures in intertidal gastropods Molluscan Research 31 106ndash113

Chapman M G (1994) Small-scale patterns of distribution and size-

structure of the intertidal littorinid Littorina unifasciata (Gastropoda

Littorinidae) in New South Wales Australian Journal of Marine and

Freshwater Research 45 635ndash652 doi101071MF9940635

Chapperon C and Seuront L (2011a) Space-time variability in environ-

mental thermal properties and snail thermoregulatory behaviour

Functional Ecology 25 1040ndash1050 doi101111J1365-24352011

01859X

Chapperon C and Seuront L (2011b) Behavioral thermoregulation in a

tropical gastropod Links to climate change scenarios Global Change

Biology 17 1740ndash1749 doi101111J1365-2486201002356X

Chapperon C and Seuront L (2012) Keeping warm in the cold On the

thermal benefits of aggregation behaviour in an intertidal ectotherm

Journal of Thermal Biology 37 640ndash647 doi101016JJTHERBIO

201208001

Cox T E and Smith C M (2011) Thermal ecology on an exposed algal

reef infrared imagery a rapid tool to survey temperature at local spatial

scales Coral Reefs 30 1109ndash1120 doi101007S00338-011-0799-2

Creese R G (1982) Distribution and abundance of the Acmaeid Limpet

Patelloida latistrigata and its interaction with barnacles Oecologia 52

85ndash96 doi101007BF00349015

Denley E J and Underwood A J (1979) Experiments on factors

influencing settlement survival and growth of two species of barnacles

in New South Wales Journal of Experimental Marine Biology and

Ecology 36 269ndash293 doi1010160022-0981(79)90122-9

Denny M W and Harley C D G (2006) Hot limpets predicting body

temperature in a conductance-mediated thermal system The Journal of

Experimental Biology 209 2409ndash2419 doi101242JEB02257

Denny M and Helmuth B (2009) Confronting the physiological bottle-

neck A challenge from ecomechanics Integrative and Comparative

Biology 49 197ndash201 doi101093ICBICP070

DennyMW Helmuth B Leonard G H Harley C D G Hunt L J H

and Nelson E K (2004) Quantifying scale in ecology Lessons from

a wave-swept shore Ecological Monographs 74 513ndash532 doi101890

03-4043

DennyMWDowdWWBilir L andMachK J (2011) Spreading the

risk Small-scale body temperature variation among intertidal organisms

and its implications for species persistence Journal of Experimental

Marine Biology and Ecology 400 175ndash190 doi101016JJEMBE

201102006

Fairweather P G (1988a) Correlations of predatory whelks with intertidal

prey at several scales of space and timeMarine Ecology Progress Series

45 237ndash243 doi103354MEPS045237

Fairweather P G (1988b) Movements of intertidal whelks (Morula

marginalba and Thais orbita) in relation to availability of prey and

shelter Marine Biology 100 63ndash68 doi101007BF00392955

Fitzhenry T Halpin P M and Helmuth B (2004) Testing the effects of

wave exposure site and behavior on intertidal mussel body tempera-

tures applications and limits of temperature logger design Marine

Biology 145 339ndash349 doi101007S00227-004-1318-6

Harley C D G (2008) Tidal dynamics topographic orientation and

temperature-mediatedmassmortalities on rocky shoresMarineEcology

Progress Series 371 37ndash46 doi103354MEPS07711

Helmuth B (2002) How do we measure the environment Linking

intertidal thermal physiology and ecology through biophysics Integra-

tive and Comparative Biology 42 837ndash845 doi101093ICB424837

Helmuth B Broitman B R Blanchette C A Gilman S E Halpin PM

Harley C D G OrsquoDonnell M Hoffmann A A Menge B A and

Strickland D (2006a) Mosaic patterns of thermal stress in the rocky

intertidal zone implications for climate change Ecological Monographs

76 461ndash479 doi1018900012-9615(2006)076[0461MPOTSI]20CO2

Helmuth B Mieszkowska N Moore P and Hawkins S J (2006b)

Living on the edge of two changing worlds forecasting the responses of

rocky intertidal ecosystems to climate change Annual Review of

Ecology Evolution and Systematics 37 373ndash404 doi101146

ANNUREVECOLSYS37091305110149

Hidas E Z Russell K G Ayre D J and Minchinton T E (2013)

Abundance of Tesseropora rosea at the margins of its biogeographic

range is closely linked to recruitment but not fecundityMarine Ecology

Progress Series 483 199ndash208 doi103354MEPS10271

Jernakoff P (1983) Factors affecting the recruitment of algae in a midshore

region dominated by barnacles Journal of ExperimentalMarine Biology

and Ecology 67 17ndash31 doi1010160022-0981(83)90132-6

Kordas R L Harley C D G and OrsquoConnor M I (2011) Community

ecology in a warming world The influence of temperature on interspe-

cific interactions in marine systems Journal of Experimental Marine

Biology and Ecology 400 218ndash226 doi101016JJEMBE201102029

Lathlean J A and Minchinton T E (2012) Manipulating thermal stress

on rocky shores to predict patterns of recruitment ofmarine invertebrates

under a changing climate Marine Ecology Progress Series 467

121ndash136 doi103354MEPS09996

Lathlean J A Ayre D J and Minchinton T E (2012) Using infrared

imagery to test for quadrat-level temperature variation and effects on the

early life history of a rocky-shore barnacle Limnology and Oceanogra-

phy 57 1279ndash1291 doi104319LO20125751279

Lathlean J A Ayre D J and Minchinton T E (2013) Temperature

variability at the larval scale affects early survival and growth of an

intertidal barnacle Marine Ecology Progress Series 475 155ndash166

doi103354MEPS10105

Lima F P and Wethey D S (2009) Robolimpets measuring intertidal

body temperatures using biomimetic loggers Limnology and Oceanog-

raphy Methods 7 347ndash353 doi104319LOM20097347

Meager J J Schlacher T A and Green M (2011) Topographic

complexity and landscape temperature patterns create a dynamic habitat

structure on a rocky intertidal shore Marine Ecology Progress Series

428 1ndash12 doi103354MEPS09124

Phillips B F and Campbell N A (1974) Mortality and longevity in the

whelk Dicathais orbita (Gmelin) Australian Journal of Marine and

Freshwater Research 25 25ndash33 doi101071MF9740025

Pincebourde S Sanford E and Helmuth B (2008) Body temperatures

during low tide alters the feeding performance of a top intertidal

predator Limnology and Oceanography 53 1562ndash1573 doi104319

LO20085341562

Russell B D Harley C D G Wernberg T Mieszkowska N Widdi-

combe S Hall-Spencer J M and Connell S D (2012) Predicting

ecosystem shifts requires new approaches that integrate the effects of

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 93

animals submerged in shallow rock pools Two unmodifiedTidbiT v2 Temp data loggers (Onset Stowaway logger

model UTBI-001 accuracy 028C) with a sampling freq-uency of 10min were also attached to horizontal and southerly

facing vertical rocky substrata (nfrac14 2 loggers per microhabitat)05m to 1m away from biomimetic loggers to compare

temperatures of the lsquomicrohabitatrsquo with that of the three studyspecies Later comparisons between these unmodified Tidbitsand iButton loggers embedded in nearby (1m) rocky substrata

revealed a strong relationship between the two temperaturemeasurements (R2frac14 0883 P 0001 nfrac14 1315) Thereforetemperatures measured by the Tidbit loggers represent an

appropriate estimate of habitat temperatureThe accuracy of biomimetic loggers was assessed by

comparing biomimetic body temperatures with that of three orfour similarly sized live specimens on horizontal rock for three

hours during three non-consecutive low tides Thiswas achievedby inserting a small thermocouple (HANNA HI 935005K-Thermocouple Thermometer resolution 018C) through a

2-mm hole drilled into the shell or test of the live specimensSimilarly to biomimetic loggers the thermocouple was cali-brated in the laboratory before use and produced accuracies

between 01 and 028C Live specimens were located between5 and 10 cm from biomimetic loggers and were all orientated inthe same direction to ensure small-scale thermal heterogeneitydid not affect our comparisons We deliberately undertook our

comparisons during daytime low tides as these conditionsproduce the greatest absolute temperature differences and ther-mal stress as opposed to night time or during high tide when

body temperatures equilibrate with sea temperatures Bodytemperatures of live limpets were highly correlated with biomi-metic temperatures (Fig 2a) with differences being on average

018C (01 se) and no greater than 128C Likewise bodytemperatures of live barnacleswere significantly correlatedwithbiomimetic temperatures (Fig 2b) with differences being on

average 088C (01 se) and no more than 158C Whenmeasuring body temperatures of live whelks in the fieldindividuals would retreat into their shells after being disturbedand would not reattach to the substrata for several hours This

behaviour precluded appropriate comparisons between livewhelks and biomimetic loggers Nevertheless body tempera-tures of live whelks were highly correlated with biomimetic

temperatures (Fig 2c) with differences being on average 208C(03 se) and a maximal difference of 448C Such largediscrepancies between body temperatures of live whelks and

biomimetic loggers were most likely the result of the observedretraction into shell Consequently comparisons of biomimeticdata with in situ body temperatures of live whelks should beviewed with caution

Data analysis

Temperatures recorded by paired biomimetic or TidbiT loggers

within each microhabitat were averaged to produce a singlevalue for each 10min interval Two-factor analysis of variance(ANOVA) was then used to test for statistically significant

differences in body temperatures (mean daily maxima meanand mean daily minima) among species (C tramoserica

T rosea and D orbita) between the different microhabitats

(benign and stressful) One-factor ANOVA was used to test forstatistically significant differences in microhabitat temperatures(mean daily maxima mean and mean daily minima) recordedby TidbiT loggers deployed on horizontal surfaces with

(1) body temperatures of each species and (2) southward-facing

(a)

10 mm

(b)

10 mm

(c)

10 mm

Fig 1 Biomimetic loggers used to record body temperatures of Cellana

tramoserica (a) Tesseropora rosea (b) and Dicathais orbita (c) Note the

external constantan wires used for communicating with computer

88 Marine and Freshwater Research J A Lathlean et al

surfaces Prior to analyses the assumption of homosce-dasticity was checked using ShapirondashWilksrsquo and Cochranrsquostests Where significant differences were found with ANOVAStudentndashNeumanndashKeuls (SNK) tests were used to determine

which species and microhabitats displayed significantly differ-ent body temperatures Due to two malfunctioning T rosea

biomimetic loggers deployed on southward-facing vertical

surfaces analyses were only carried out for measurements takenbetween the 5 and 14 March 2013

Results

Comparisons among microhabitatsand body temperatures

Microhabitat temperatures recorded using unmodified Tidbitloggers were significantly greater than body temperatures

recorded by each of the three different biomimetic loggers inboth thermally stressful and benign microhabitats (Fig 3Table 1) This was most obvious in the stressful microhabitat

(ie horizontal rocky substrata) and for comparisons ofmean daily maximal temperatures and less obvious for dailyminimum temperatures For horizontal rocky substrata tem-peratures reached as high as 4428C which was 88 91 and

1118C higher than the maximal body temperatures ofD orbitaC tramoserica and T rosea respectively On average habitattemperatures were 18 20 and 268C higher than the average

body temperatures of D orbita C tramoserica and T rosea

respectively (Fig 3)

Interspecific comparisons

In both benign and stressful microhabitats body temperaturesrecorded by biomimetic loggers revealed that the limpetC tramoserica experienced consistently higher body tempera-

tures than both the barnacle T rosea and whelkD orbita (Fig 3Table 2) This was most obvious when comparing the dailymean and maxima body temperature of each species (Table 2)

Irrespective of microhabitat the daily maximal body tempera-tures of C tramoserica were on average 21 and 318C warmerthan D orbita and T rosea respectively Interestingly absolutemaximal body temperatures of C tramoserica (3518C) and

D orbita (3548C) within the thermally stressful microhabitathorizontal emergent rock were both several degrees higher thanthe maximal body temperature recorded by T rosea mimics

(3318C) (Fig 3)

Microhabitat comparisons

Habitat and body temperatures recorded by loggers attached tohorizontal emergent rock were consistently higher and dis-played greater daily fluctuations than equivalent measurementstaken on either south-facing vertical surfaces or within shallow

rock pools (Fig 4 Table 2)Measurements taken by unmodifiedloggers revealed that horizontal surfaces experienced signifi-cantly greater daily maximal (F174frac14 1666 P 0001) and

daily mean (F174frac14 2982 P 0001) temperatures than nearbyvertical surfaces with differences as great as 818C (Fig 4a)Likewise daily maximal temperatures of T rosea mimics

placed on southerly facing vertical surfaces were on average248C cooler than those on horizontal emergent rock (Fig 4c)Similarly daily maximal body temperatures of whelks were on

average 318C cooler within shallow rock pools than on hori-zontal emergent rock (Fig 4d ) Among the three study speciesD orbitamimics displayed the greatest microhabitat variabilityin temperatures For example maximal temperatures of

D orbita on horizontal emergent rock were up to 658C higherthan equivalent body temperatures recorded in nearby shallowrock pools (Fig 4d ) By comparison themaximal differences in

body temperatures of C tramoserica and T rosea among thebenign and stressful habitats were 29 and 508C respectivelyInterestingly there was no difference in mean daily maximal

temperatures of C tramoserica mimics placed on either hori-zontal or vertical rocky substrata

Discussion

This study takes advantage of recently developed biomimetic

technology (Lima and Wethey 2009) to estimate the bodytemperatures of three co-occurring species with distinct mor-phological characteristics This is the first time biomimetic

loggers have been used to compare body temperatures of threespecies simultaneously Results highlight that even over a shortperiod of thermal stress morphological differences between

species can alter body temperatures and thus could have con-sequences for interspecific interactions and community-levelprocesses Daily maximal temperatures of limpet mimics wereon average 21 and 318C higher than temperatures of whelk

and barnacle mimics with habitat temperatures up to 1118Chigher than biomimetic measurements These results supportseveral recent studies that show body temperatures of rocky

intertidal ectotherms to be significantly different to ambient

20

25

30

35

20 25 30 35

(R 2 091 P 0001 n 51) (R 2 096 P 0001 n 73) (R 2 096 P 0001 n 18)

20

25

30

35

20 25 30 3520

25

30

35

20 25 30 35

(a) (b) (c)

Biomimetic temperature (C)

Bod

y te

mpe

ratu

re (

C)

Fig 2 Comparisons between biomimetic body temperatures and those recorded for live Cellana tramoserica (a) Tesseropora rosea (b) and

Dicathais orbita (c) 5ndash10 cm away during several daytime low tides

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 89

temperatures (Fitzhenry et al 2004 Szathmary et al 2009)in addition to interspecific variations for animals (Broitmanet al 2009)

We know of only one other study that has simultaneouslymeasured body temperatures of multiple species of rockyintertidal invertebrates using biomimetic technology Broitman

et al (2009) demonstrated that body temperatures of a keystonepredator (the seastar Pisaster ochraceus) were at times in excess

of 108C lower than its prey (the mussel Mytilus californianus)even though both were within the same microhabitat Suchdramatic differences in the body temperatures of P ochraceus

and M californianus are most likely due to differences inmorphology and reflectance (ie P ochraceus is larger thanM californianus does not have a calcareous shell and is usually

brightly coloured) In contrast the three species examined in ourwork all possess an external calcareous shell or test and are all

15

20

25

30

35

40

45Daily maxima

15

20

25

30

35

40

45Habitat Cellana

Tesseropora Dicathaislowast

15

20

25

30Daily mean

15

20

25

30

10

15

20

25Daily minima

10

15

20

25

Mic

roha

bita

tbod

y te

mpe

ratu

re (

C)

Stressful Benign

05-M

ar-1

3

09-M

ar-1

3

13-M

ar-1

3

17-M

ar-1

3

21-M

ar-1

3

25-M

ar-1

3

29-M

ar-1

3

02-A

pr-1

3

06-A

pr-1

3

10-A

pr-1

3

05-M

ar-1

3

09-M

ar-1

3

13-M

ar-1

3

17-M

ar-1

3

21-M

ar-1

3

25-M

ar-1

3

29-M

ar-1

3

02-A

pr-1

3

06-A

pr-1

3

10-A

pr-1

3

Fig 3 Daily maxima mean and minima body temperatures of three different species of rocky intertidal invertebrates compared with habitat

temperature within stressful horizontal (left column) and benign southward facing vertical surfaces (right column) in the mid shore region at

Garie Beach from 5 March to 11 April 2013 Dicathais loggers were placed in shallow rock pools instead of vertical surfaces

90 Marine and Freshwater Research J A Lathlean et al

relatively small (20ndash50mm in length) with no large variationin colour (brown to grey) Regardless we detected significantdifferences in body temperatures of our three species among

multiple microhabitats Such differences in body tempera-ture may have dramatic consequences for interspecific interac-tions and the organisation of rocky intertidal communitieswithin this region

We found that microhabitats were a considerable source oftemperature variability for all three species This supports agrowing body of work that shows small-scale habitat hetero-

geneity is themajor source of body temperature variability amongrocky intertidal invertebrates (Denny et al 2004 Harley 2008Meager et al2011Lathlean et al 2012 2013)Microhabitats that

act as thermal refugia are expected to play an increasinglyimportant role in mitigating the future impacts of climate changeon these benthic communities For example with increasingthermal stress expected to occur on rocky intertidal shores of

south-east Australia we might expect (1) reduced foraging ratesof D orbita as they remain within shallow rock pools for longerperiods of time and (2) migration of C tramoserica away from

horizontal substrata to cooler southerly facing vertical surfacesBoth of these changes would positively affect T rosea byreducing early post-settlement mortality caused by grazing

C tramoserica and the predation of adults by D orbita Conse-quently rocky intertidal communities along the south-east coastof Australia may become increasingly dominated by T rosea

(Underwood et al 1983) Further experimental evidence howev-er is required to determinewhether increasedheat stresswill elicitsuch responses (eg Lathlean and Minchinton 2012)

Predicting the strength of speciesrsquo interactions under futureclimate change scenarios depends largely on understanding theunique physiological responses of individual species in a com-

munity context (Russell et al 2012) Body temperature mea-surements as presented here represent a useful method ofassessing the physiological response of individual organisms

to changing environmental conditions The application of infra-red thermography to rocky intertidal systems has also emergedas an effective means of estimating intra- and inter-specific

variation in body temperatures (Caddy-Retalic et al 2011Chapperon and Seuront 2011a Cox and Smith 2011 Lathleanet al 2012) and could serve as a complementary approach tobiomimetic technology Infrared thermography is particularly

useful for investigating the role of thermoregulatory behaviour(Chapperon and Seuront 2011a 2011b 2012) which wasnot accounted for within the present study More is needed

however because body temperatures alone cannot informresearchers whether an organism is thermally stressed Bodytemperature measurements need to be placed within a physio-

logical context that considers how thermal limits of a speciesvary across broad geographic scales (Tomanek 2008 Dennyand Helmuth 2009 Somero 2010) Unfortunately these funda-mental physiological parameters have yet to be determined for

the majority of rocky intertidal invertebrates of south-eastAustralia To help safeguard these vulnerable benthic commu-nities to climate change (Denny and Harley 2006 Wernberg

et al 2011) we suggest future research should focus on

Table 2 Summary of two-factor ANOVA and SNK for the effect of

species (C tramoserica T rosea D orbita) and microhabitat (benign

stressful) on daily maximal mean and minimum body temperatures

Source df SS F-ratio P-value

Daily Maxima

Species 2 100145 4587 0015

Microhabitat 1 44873 4110 0048

SpeciesMicrohabitat 2 30781 1410 0253

Error 54 589521

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

StressfulBenign

Daily Mean

Species 2 17151 7117 0002

Microhabitat 1 0030 0025 0875

SpeciesMicrohabitat 2 5141 2133 0128

Error 54 65067

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

Stressfulfrac14Benign

Daily Minima

Species 2 11525 4051 0023

Microhabitat 1 6177 4342 0042

SpeciesMicrohabitat 2 4501 1582 0215

Error 54 76818

SNK [species] Cellana

Tesseropora

SNK [microhabitat]

StressfulBenign

Table 1 Summary of one-factor ANOVA and SNK tests for the effect

of environmental and species temperature (daily maxima mean and

minima) recorded by TidbiT loggers and the three different biomimetic

loggers attached to horizontal emergent rocky substrata

Source df SS F-ratio P-value

Stressful microhabitat

Daily Maxima 3 472627 9306 0001

Error 36 609445

SNK HabitatAll species

Daily Mean 3 57701 13419 0001

Error 36 51599

SNK HabitatAll species

Daily Minima 3 11786 3929 0034

Error 36 43807

SNK Habitat

Tesseropora only

Benign microhabitat

Daily Maxima 3 245123 7901 0001

Error 36 372295

SNK Habitat and Cellana

Dicathais and Tesseropora

Daily mean 3 28304 9435 0001

Error 36 35118

SNK Habitat and Cellana

Dicathais and Tess

Daily Minima 3 13862 3160 0036

Error 36 52643

SNK Cellana

Dicathais and Tesseropora

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 91

10

15

20

25

30

35

40

45 Habitat

10

15

20

25

30

35

40

45Cellana

10

15

20

25

30

35

40

45Tesseropora

10

15

20

25

30

35

40

45Dicathais

Bod

ym

icro

habi

tat t

empe

ratu

re (

C)

5-Mar 6-Apr9-Mar 10-Apr13-Mar 17-Mar 21-Mar 25-Mar 29-Mar 2-Apr

(a)

(b)

(c)

(d )

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Rockpool

Fig 4 Microhabitat (a) and body temperatures of the limpet Cellana tramoserica (b) the barnacle

Tesseropora rosea (c) and the whelk Dicathais orbita (d ) within thermally stressful (horizontal

substrata) and thermally benign (southerly facing vertical substrata) microhabitats within the midshore

region at Garie Beach from 5 March to 11 April 2013 Body temperatures of T rosea attached to

southerly facing vertical surfaces were only recorded up until the 14 March due to malfunctioning

loggers

92 Marine and Freshwater Research J A Lathlean et al

(i) developing long-term body temperature measurements ofmultiple species using biomimetic loggers and (ii) undertake

physiological experiments aimed at calculating biogeographicvariability in speciesrsquo thermal limits

Acknowledgements

We thank Samuel Wighton and Elizabeth Lathlean for assistance with

biomimetic construction This research was supported by the Institute of

Conservation Biology and Environmental Management at the University

of Wollongong

References

Broitman B R Szathmary P L Mislan K A S Blanchette C A and

Helmuth B (2009) Predator-prey interactions under climate change

the importance of habitat vs body temperature Oikos 118 219ndash224

doi101111J1600-0706200817075X

Caddy-Retalic S Benkendorff K and Fairweather P G (2011) Visual-

izing hotspots Applying thermal imaging to monitor internal tempera-

tures in intertidal gastropods Molluscan Research 31 106ndash113

Chapman M G (1994) Small-scale patterns of distribution and size-

structure of the intertidal littorinid Littorina unifasciata (Gastropoda

Littorinidae) in New South Wales Australian Journal of Marine and

Freshwater Research 45 635ndash652 doi101071MF9940635

Chapperon C and Seuront L (2011a) Space-time variability in environ-

mental thermal properties and snail thermoregulatory behaviour

Functional Ecology 25 1040ndash1050 doi101111J1365-24352011

01859X

Chapperon C and Seuront L (2011b) Behavioral thermoregulation in a

tropical gastropod Links to climate change scenarios Global Change

Biology 17 1740ndash1749 doi101111J1365-2486201002356X

Chapperon C and Seuront L (2012) Keeping warm in the cold On the

thermal benefits of aggregation behaviour in an intertidal ectotherm

Journal of Thermal Biology 37 640ndash647 doi101016JJTHERBIO

201208001

Cox T E and Smith C M (2011) Thermal ecology on an exposed algal

reef infrared imagery a rapid tool to survey temperature at local spatial

scales Coral Reefs 30 1109ndash1120 doi101007S00338-011-0799-2

Creese R G (1982) Distribution and abundance of the Acmaeid Limpet

Patelloida latistrigata and its interaction with barnacles Oecologia 52

85ndash96 doi101007BF00349015

Denley E J and Underwood A J (1979) Experiments on factors

influencing settlement survival and growth of two species of barnacles

in New South Wales Journal of Experimental Marine Biology and

Ecology 36 269ndash293 doi1010160022-0981(79)90122-9

Denny M W and Harley C D G (2006) Hot limpets predicting body

temperature in a conductance-mediated thermal system The Journal of

Experimental Biology 209 2409ndash2419 doi101242JEB02257

Denny M and Helmuth B (2009) Confronting the physiological bottle-

neck A challenge from ecomechanics Integrative and Comparative

Biology 49 197ndash201 doi101093ICBICP070

DennyMW Helmuth B Leonard G H Harley C D G Hunt L J H

and Nelson E K (2004) Quantifying scale in ecology Lessons from

a wave-swept shore Ecological Monographs 74 513ndash532 doi101890

03-4043

DennyMWDowdWWBilir L andMachK J (2011) Spreading the

risk Small-scale body temperature variation among intertidal organisms

and its implications for species persistence Journal of Experimental

Marine Biology and Ecology 400 175ndash190 doi101016JJEMBE

201102006

Fairweather P G (1988a) Correlations of predatory whelks with intertidal

prey at several scales of space and timeMarine Ecology Progress Series

45 237ndash243 doi103354MEPS045237

Fairweather P G (1988b) Movements of intertidal whelks (Morula

marginalba and Thais orbita) in relation to availability of prey and

shelter Marine Biology 100 63ndash68 doi101007BF00392955

Fitzhenry T Halpin P M and Helmuth B (2004) Testing the effects of

wave exposure site and behavior on intertidal mussel body tempera-

tures applications and limits of temperature logger design Marine

Biology 145 339ndash349 doi101007S00227-004-1318-6

Harley C D G (2008) Tidal dynamics topographic orientation and

temperature-mediatedmassmortalities on rocky shoresMarineEcology

Progress Series 371 37ndash46 doi103354MEPS07711

Helmuth B (2002) How do we measure the environment Linking

intertidal thermal physiology and ecology through biophysics Integra-

tive and Comparative Biology 42 837ndash845 doi101093ICB424837

Helmuth B Broitman B R Blanchette C A Gilman S E Halpin PM

Harley C D G OrsquoDonnell M Hoffmann A A Menge B A and

Strickland D (2006a) Mosaic patterns of thermal stress in the rocky

intertidal zone implications for climate change Ecological Monographs

76 461ndash479 doi1018900012-9615(2006)076[0461MPOTSI]20CO2

Helmuth B Mieszkowska N Moore P and Hawkins S J (2006b)

Living on the edge of two changing worlds forecasting the responses of

rocky intertidal ecosystems to climate change Annual Review of

Ecology Evolution and Systematics 37 373ndash404 doi101146

ANNUREVECOLSYS37091305110149

Hidas E Z Russell K G Ayre D J and Minchinton T E (2013)

Abundance of Tesseropora rosea at the margins of its biogeographic

range is closely linked to recruitment but not fecundityMarine Ecology

Progress Series 483 199ndash208 doi103354MEPS10271

Jernakoff P (1983) Factors affecting the recruitment of algae in a midshore

region dominated by barnacles Journal of ExperimentalMarine Biology

and Ecology 67 17ndash31 doi1010160022-0981(83)90132-6

Kordas R L Harley C D G and OrsquoConnor M I (2011) Community

ecology in a warming world The influence of temperature on interspe-

cific interactions in marine systems Journal of Experimental Marine

Biology and Ecology 400 218ndash226 doi101016JJEMBE201102029

Lathlean J A and Minchinton T E (2012) Manipulating thermal stress

on rocky shores to predict patterns of recruitment ofmarine invertebrates

under a changing climate Marine Ecology Progress Series 467

121ndash136 doi103354MEPS09996

Lathlean J A Ayre D J and Minchinton T E (2012) Using infrared

imagery to test for quadrat-level temperature variation and effects on the

early life history of a rocky-shore barnacle Limnology and Oceanogra-

phy 57 1279ndash1291 doi104319LO20125751279

Lathlean J A Ayre D J and Minchinton T E (2013) Temperature

variability at the larval scale affects early survival and growth of an

intertidal barnacle Marine Ecology Progress Series 475 155ndash166

doi103354MEPS10105

Lima F P and Wethey D S (2009) Robolimpets measuring intertidal

body temperatures using biomimetic loggers Limnology and Oceanog-

raphy Methods 7 347ndash353 doi104319LOM20097347

Meager J J Schlacher T A and Green M (2011) Topographic

complexity and landscape temperature patterns create a dynamic habitat

structure on a rocky intertidal shore Marine Ecology Progress Series

428 1ndash12 doi103354MEPS09124

Phillips B F and Campbell N A (1974) Mortality and longevity in the

whelk Dicathais orbita (Gmelin) Australian Journal of Marine and

Freshwater Research 25 25ndash33 doi101071MF9740025

Pincebourde S Sanford E and Helmuth B (2008) Body temperatures

during low tide alters the feeding performance of a top intertidal

predator Limnology and Oceanography 53 1562ndash1573 doi104319

LO20085341562

Russell B D Harley C D G Wernberg T Mieszkowska N Widdi-

combe S Hall-Spencer J M and Connell S D (2012) Predicting

ecosystem shifts requires new approaches that integrate the effects of

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 93

surfaces Prior to analyses the assumption of homosce-dasticity was checked using ShapirondashWilksrsquo and Cochranrsquostests Where significant differences were found with ANOVAStudentndashNeumanndashKeuls (SNK) tests were used to determine

which species and microhabitats displayed significantly differ-ent body temperatures Due to two malfunctioning T rosea

biomimetic loggers deployed on southward-facing vertical

surfaces analyses were only carried out for measurements takenbetween the 5 and 14 March 2013

Results

Comparisons among microhabitatsand body temperatures

Microhabitat temperatures recorded using unmodified Tidbitloggers were significantly greater than body temperatures

recorded by each of the three different biomimetic loggers inboth thermally stressful and benign microhabitats (Fig 3Table 1) This was most obvious in the stressful microhabitat

(ie horizontal rocky substrata) and for comparisons ofmean daily maximal temperatures and less obvious for dailyminimum temperatures For horizontal rocky substrata tem-peratures reached as high as 4428C which was 88 91 and

1118C higher than the maximal body temperatures ofD orbitaC tramoserica and T rosea respectively On average habitattemperatures were 18 20 and 268C higher than the average

body temperatures of D orbita C tramoserica and T rosea

respectively (Fig 3)

Interspecific comparisons

In both benign and stressful microhabitats body temperaturesrecorded by biomimetic loggers revealed that the limpetC tramoserica experienced consistently higher body tempera-

tures than both the barnacle T rosea and whelkD orbita (Fig 3Table 2) This was most obvious when comparing the dailymean and maxima body temperature of each species (Table 2)

Irrespective of microhabitat the daily maximal body tempera-tures of C tramoserica were on average 21 and 318C warmerthan D orbita and T rosea respectively Interestingly absolutemaximal body temperatures of C tramoserica (3518C) and

D orbita (3548C) within the thermally stressful microhabitathorizontal emergent rock were both several degrees higher thanthe maximal body temperature recorded by T rosea mimics

(3318C) (Fig 3)

Microhabitat comparisons

Habitat and body temperatures recorded by loggers attached tohorizontal emergent rock were consistently higher and dis-played greater daily fluctuations than equivalent measurementstaken on either south-facing vertical surfaces or within shallow

rock pools (Fig 4 Table 2)Measurements taken by unmodifiedloggers revealed that horizontal surfaces experienced signifi-cantly greater daily maximal (F174frac14 1666 P 0001) and

daily mean (F174frac14 2982 P 0001) temperatures than nearbyvertical surfaces with differences as great as 818C (Fig 4a)Likewise daily maximal temperatures of T rosea mimics

placed on southerly facing vertical surfaces were on average248C cooler than those on horizontal emergent rock (Fig 4c)Similarly daily maximal body temperatures of whelks were on

average 318C cooler within shallow rock pools than on hori-zontal emergent rock (Fig 4d ) Among the three study speciesD orbitamimics displayed the greatest microhabitat variabilityin temperatures For example maximal temperatures of

D orbita on horizontal emergent rock were up to 658C higherthan equivalent body temperatures recorded in nearby shallowrock pools (Fig 4d ) By comparison themaximal differences in

body temperatures of C tramoserica and T rosea among thebenign and stressful habitats were 29 and 508C respectivelyInterestingly there was no difference in mean daily maximal

temperatures of C tramoserica mimics placed on either hori-zontal or vertical rocky substrata

Discussion

This study takes advantage of recently developed biomimetic

technology (Lima and Wethey 2009) to estimate the bodytemperatures of three co-occurring species with distinct mor-phological characteristics This is the first time biomimetic

loggers have been used to compare body temperatures of threespecies simultaneously Results highlight that even over a shortperiod of thermal stress morphological differences between

species can alter body temperatures and thus could have con-sequences for interspecific interactions and community-levelprocesses Daily maximal temperatures of limpet mimics wereon average 21 and 318C higher than temperatures of whelk

and barnacle mimics with habitat temperatures up to 1118Chigher than biomimetic measurements These results supportseveral recent studies that show body temperatures of rocky

intertidal ectotherms to be significantly different to ambient

20

25

30

35

20 25 30 35

(R 2 091 P 0001 n 51) (R 2 096 P 0001 n 73) (R 2 096 P 0001 n 18)

20

25

30

35

20 25 30 3520

25

30

35

20 25 30 35

(a) (b) (c)

Biomimetic temperature (C)

Bod

y te

mpe

ratu

re (

C)

Fig 2 Comparisons between biomimetic body temperatures and those recorded for live Cellana tramoserica (a) Tesseropora rosea (b) and

Dicathais orbita (c) 5ndash10 cm away during several daytime low tides

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 89

temperatures (Fitzhenry et al 2004 Szathmary et al 2009)in addition to interspecific variations for animals (Broitmanet al 2009)

We know of only one other study that has simultaneouslymeasured body temperatures of multiple species of rockyintertidal invertebrates using biomimetic technology Broitman

et al (2009) demonstrated that body temperatures of a keystonepredator (the seastar Pisaster ochraceus) were at times in excess

of 108C lower than its prey (the mussel Mytilus californianus)even though both were within the same microhabitat Suchdramatic differences in the body temperatures of P ochraceus

and M californianus are most likely due to differences inmorphology and reflectance (ie P ochraceus is larger thanM californianus does not have a calcareous shell and is usually

brightly coloured) In contrast the three species examined in ourwork all possess an external calcareous shell or test and are all

15

20

25

30

35

40

45Daily maxima

15

20

25

30

35

40

45Habitat Cellana

Tesseropora Dicathaislowast

15

20

25

30Daily mean

15

20

25

30

10

15

20

25Daily minima

10

15

20

25

Mic

roha

bita

tbod

y te

mpe

ratu

re (

C)

Stressful Benign

05-M

ar-1

3

09-M

ar-1

3

13-M

ar-1

3

17-M

ar-1

3

21-M

ar-1

3

25-M

ar-1

3

29-M

ar-1

3

02-A

pr-1

3

06-A

pr-1

3

10-A

pr-1

3

05-M

ar-1

3

09-M

ar-1

3

13-M

ar-1

3

17-M

ar-1

3

21-M

ar-1

3

25-M

ar-1

3

29-M

ar-1

3

02-A

pr-1

3

06-A

pr-1

3

10-A

pr-1

3

Fig 3 Daily maxima mean and minima body temperatures of three different species of rocky intertidal invertebrates compared with habitat

temperature within stressful horizontal (left column) and benign southward facing vertical surfaces (right column) in the mid shore region at

Garie Beach from 5 March to 11 April 2013 Dicathais loggers were placed in shallow rock pools instead of vertical surfaces

90 Marine and Freshwater Research J A Lathlean et al

relatively small (20ndash50mm in length) with no large variationin colour (brown to grey) Regardless we detected significantdifferences in body temperatures of our three species among

multiple microhabitats Such differences in body tempera-ture may have dramatic consequences for interspecific interac-tions and the organisation of rocky intertidal communitieswithin this region

We found that microhabitats were a considerable source oftemperature variability for all three species This supports agrowing body of work that shows small-scale habitat hetero-

geneity is themajor source of body temperature variability amongrocky intertidal invertebrates (Denny et al 2004 Harley 2008Meager et al2011Lathlean et al 2012 2013)Microhabitats that

act as thermal refugia are expected to play an increasinglyimportant role in mitigating the future impacts of climate changeon these benthic communities For example with increasingthermal stress expected to occur on rocky intertidal shores of

south-east Australia we might expect (1) reduced foraging ratesof D orbita as they remain within shallow rock pools for longerperiods of time and (2) migration of C tramoserica away from

horizontal substrata to cooler southerly facing vertical surfacesBoth of these changes would positively affect T rosea byreducing early post-settlement mortality caused by grazing

C tramoserica and the predation of adults by D orbita Conse-quently rocky intertidal communities along the south-east coastof Australia may become increasingly dominated by T rosea

(Underwood et al 1983) Further experimental evidence howev-er is required to determinewhether increasedheat stresswill elicitsuch responses (eg Lathlean and Minchinton 2012)

Predicting the strength of speciesrsquo interactions under futureclimate change scenarios depends largely on understanding theunique physiological responses of individual species in a com-

munity context (Russell et al 2012) Body temperature mea-surements as presented here represent a useful method ofassessing the physiological response of individual organisms

to changing environmental conditions The application of infra-red thermography to rocky intertidal systems has also emergedas an effective means of estimating intra- and inter-specific

variation in body temperatures (Caddy-Retalic et al 2011Chapperon and Seuront 2011a Cox and Smith 2011 Lathleanet al 2012) and could serve as a complementary approach tobiomimetic technology Infrared thermography is particularly

useful for investigating the role of thermoregulatory behaviour(Chapperon and Seuront 2011a 2011b 2012) which wasnot accounted for within the present study More is needed

however because body temperatures alone cannot informresearchers whether an organism is thermally stressed Bodytemperature measurements need to be placed within a physio-

logical context that considers how thermal limits of a speciesvary across broad geographic scales (Tomanek 2008 Dennyand Helmuth 2009 Somero 2010) Unfortunately these funda-mental physiological parameters have yet to be determined for

the majority of rocky intertidal invertebrates of south-eastAustralia To help safeguard these vulnerable benthic commu-nities to climate change (Denny and Harley 2006 Wernberg

et al 2011) we suggest future research should focus on

Table 2 Summary of two-factor ANOVA and SNK for the effect of

species (C tramoserica T rosea D orbita) and microhabitat (benign

stressful) on daily maximal mean and minimum body temperatures

Source df SS F-ratio P-value

Daily Maxima

Species 2 100145 4587 0015

Microhabitat 1 44873 4110 0048

SpeciesMicrohabitat 2 30781 1410 0253

Error 54 589521

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

StressfulBenign

Daily Mean

Species 2 17151 7117 0002

Microhabitat 1 0030 0025 0875

SpeciesMicrohabitat 2 5141 2133 0128

Error 54 65067

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

Stressfulfrac14Benign

Daily Minima

Species 2 11525 4051 0023

Microhabitat 1 6177 4342 0042

SpeciesMicrohabitat 2 4501 1582 0215

Error 54 76818

SNK [species] Cellana

Tesseropora

SNK [microhabitat]

StressfulBenign

Table 1 Summary of one-factor ANOVA and SNK tests for the effect

of environmental and species temperature (daily maxima mean and

minima) recorded by TidbiT loggers and the three different biomimetic

loggers attached to horizontal emergent rocky substrata

Source df SS F-ratio P-value

Stressful microhabitat

Daily Maxima 3 472627 9306 0001

Error 36 609445

SNK HabitatAll species

Daily Mean 3 57701 13419 0001

Error 36 51599

SNK HabitatAll species

Daily Minima 3 11786 3929 0034

Error 36 43807

SNK Habitat

Tesseropora only

Benign microhabitat

Daily Maxima 3 245123 7901 0001

Error 36 372295

SNK Habitat and Cellana

Dicathais and Tesseropora

Daily mean 3 28304 9435 0001

Error 36 35118

SNK Habitat and Cellana

Dicathais and Tess

Daily Minima 3 13862 3160 0036

Error 36 52643

SNK Cellana

Dicathais and Tesseropora

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 91

10

15

20

25

30

35

40

45 Habitat

10

15

20

25

30

35

40

45Cellana

10

15

20

25

30

35

40

45Tesseropora

10

15

20

25

30

35

40

45Dicathais

Bod

ym

icro

habi

tat t

empe

ratu

re (

C)

5-Mar 6-Apr9-Mar 10-Apr13-Mar 17-Mar 21-Mar 25-Mar 29-Mar 2-Apr

(a)

(b)

(c)

(d )

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Rockpool

Fig 4 Microhabitat (a) and body temperatures of the limpet Cellana tramoserica (b) the barnacle

Tesseropora rosea (c) and the whelk Dicathais orbita (d ) within thermally stressful (horizontal

substrata) and thermally benign (southerly facing vertical substrata) microhabitats within the midshore

region at Garie Beach from 5 March to 11 April 2013 Body temperatures of T rosea attached to

southerly facing vertical surfaces were only recorded up until the 14 March due to malfunctioning

loggers

92 Marine and Freshwater Research J A Lathlean et al

(i) developing long-term body temperature measurements ofmultiple species using biomimetic loggers and (ii) undertake

physiological experiments aimed at calculating biogeographicvariability in speciesrsquo thermal limits

Acknowledgements

We thank Samuel Wighton and Elizabeth Lathlean for assistance with

biomimetic construction This research was supported by the Institute of

Conservation Biology and Environmental Management at the University

of Wollongong

References

Broitman B R Szathmary P L Mislan K A S Blanchette C A and

Helmuth B (2009) Predator-prey interactions under climate change

the importance of habitat vs body temperature Oikos 118 219ndash224

doi101111J1600-0706200817075X

Caddy-Retalic S Benkendorff K and Fairweather P G (2011) Visual-

izing hotspots Applying thermal imaging to monitor internal tempera-

tures in intertidal gastropods Molluscan Research 31 106ndash113

Chapman M G (1994) Small-scale patterns of distribution and size-

structure of the intertidal littorinid Littorina unifasciata (Gastropoda

Littorinidae) in New South Wales Australian Journal of Marine and

Freshwater Research 45 635ndash652 doi101071MF9940635

Chapperon C and Seuront L (2011a) Space-time variability in environ-

mental thermal properties and snail thermoregulatory behaviour

Functional Ecology 25 1040ndash1050 doi101111J1365-24352011

01859X

Chapperon C and Seuront L (2011b) Behavioral thermoregulation in a

tropical gastropod Links to climate change scenarios Global Change

Biology 17 1740ndash1749 doi101111J1365-2486201002356X

Chapperon C and Seuront L (2012) Keeping warm in the cold On the

thermal benefits of aggregation behaviour in an intertidal ectotherm

Journal of Thermal Biology 37 640ndash647 doi101016JJTHERBIO

201208001

Cox T E and Smith C M (2011) Thermal ecology on an exposed algal

reef infrared imagery a rapid tool to survey temperature at local spatial

scales Coral Reefs 30 1109ndash1120 doi101007S00338-011-0799-2

Creese R G (1982) Distribution and abundance of the Acmaeid Limpet

Patelloida latistrigata and its interaction with barnacles Oecologia 52

85ndash96 doi101007BF00349015

Denley E J and Underwood A J (1979) Experiments on factors

influencing settlement survival and growth of two species of barnacles

in New South Wales Journal of Experimental Marine Biology and

Ecology 36 269ndash293 doi1010160022-0981(79)90122-9

Denny M W and Harley C D G (2006) Hot limpets predicting body

temperature in a conductance-mediated thermal system The Journal of

Experimental Biology 209 2409ndash2419 doi101242JEB02257

Denny M and Helmuth B (2009) Confronting the physiological bottle-

neck A challenge from ecomechanics Integrative and Comparative

Biology 49 197ndash201 doi101093ICBICP070

DennyMW Helmuth B Leonard G H Harley C D G Hunt L J H

and Nelson E K (2004) Quantifying scale in ecology Lessons from

a wave-swept shore Ecological Monographs 74 513ndash532 doi101890

03-4043

DennyMWDowdWWBilir L andMachK J (2011) Spreading the

risk Small-scale body temperature variation among intertidal organisms

and its implications for species persistence Journal of Experimental

Marine Biology and Ecology 400 175ndash190 doi101016JJEMBE

201102006

Fairweather P G (1988a) Correlations of predatory whelks with intertidal

prey at several scales of space and timeMarine Ecology Progress Series

45 237ndash243 doi103354MEPS045237

Fairweather P G (1988b) Movements of intertidal whelks (Morula

marginalba and Thais orbita) in relation to availability of prey and

shelter Marine Biology 100 63ndash68 doi101007BF00392955

Fitzhenry T Halpin P M and Helmuth B (2004) Testing the effects of

wave exposure site and behavior on intertidal mussel body tempera-

tures applications and limits of temperature logger design Marine

Biology 145 339ndash349 doi101007S00227-004-1318-6

Harley C D G (2008) Tidal dynamics topographic orientation and

temperature-mediatedmassmortalities on rocky shoresMarineEcology

Progress Series 371 37ndash46 doi103354MEPS07711

Helmuth B (2002) How do we measure the environment Linking

intertidal thermal physiology and ecology through biophysics Integra-

tive and Comparative Biology 42 837ndash845 doi101093ICB424837

Helmuth B Broitman B R Blanchette C A Gilman S E Halpin PM

Harley C D G OrsquoDonnell M Hoffmann A A Menge B A and

Strickland D (2006a) Mosaic patterns of thermal stress in the rocky

intertidal zone implications for climate change Ecological Monographs

76 461ndash479 doi1018900012-9615(2006)076[0461MPOTSI]20CO2

Helmuth B Mieszkowska N Moore P and Hawkins S J (2006b)

Living on the edge of two changing worlds forecasting the responses of

rocky intertidal ecosystems to climate change Annual Review of

Ecology Evolution and Systematics 37 373ndash404 doi101146

ANNUREVECOLSYS37091305110149

Hidas E Z Russell K G Ayre D J and Minchinton T E (2013)

Abundance of Tesseropora rosea at the margins of its biogeographic

range is closely linked to recruitment but not fecundityMarine Ecology

Progress Series 483 199ndash208 doi103354MEPS10271

Jernakoff P (1983) Factors affecting the recruitment of algae in a midshore

region dominated by barnacles Journal of ExperimentalMarine Biology

and Ecology 67 17ndash31 doi1010160022-0981(83)90132-6

Kordas R L Harley C D G and OrsquoConnor M I (2011) Community

ecology in a warming world The influence of temperature on interspe-

cific interactions in marine systems Journal of Experimental Marine

Biology and Ecology 400 218ndash226 doi101016JJEMBE201102029

Lathlean J A and Minchinton T E (2012) Manipulating thermal stress

on rocky shores to predict patterns of recruitment ofmarine invertebrates

under a changing climate Marine Ecology Progress Series 467

121ndash136 doi103354MEPS09996

Lathlean J A Ayre D J and Minchinton T E (2012) Using infrared

imagery to test for quadrat-level temperature variation and effects on the

early life history of a rocky-shore barnacle Limnology and Oceanogra-

phy 57 1279ndash1291 doi104319LO20125751279

Lathlean J A Ayre D J and Minchinton T E (2013) Temperature

variability at the larval scale affects early survival and growth of an

intertidal barnacle Marine Ecology Progress Series 475 155ndash166

doi103354MEPS10105

Lima F P and Wethey D S (2009) Robolimpets measuring intertidal

body temperatures using biomimetic loggers Limnology and Oceanog-

raphy Methods 7 347ndash353 doi104319LOM20097347

Meager J J Schlacher T A and Green M (2011) Topographic

complexity and landscape temperature patterns create a dynamic habitat

structure on a rocky intertidal shore Marine Ecology Progress Series

428 1ndash12 doi103354MEPS09124

Phillips B F and Campbell N A (1974) Mortality and longevity in the

whelk Dicathais orbita (Gmelin) Australian Journal of Marine and

Freshwater Research 25 25ndash33 doi101071MF9740025

Pincebourde S Sanford E and Helmuth B (2008) Body temperatures

during low tide alters the feeding performance of a top intertidal

predator Limnology and Oceanography 53 1562ndash1573 doi104319

LO20085341562

Russell B D Harley C D G Wernberg T Mieszkowska N Widdi-

combe S Hall-Spencer J M and Connell S D (2012) Predicting

ecosystem shifts requires new approaches that integrate the effects of

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 93

temperatures (Fitzhenry et al 2004 Szathmary et al 2009)in addition to interspecific variations for animals (Broitmanet al 2009)

We know of only one other study that has simultaneouslymeasured body temperatures of multiple species of rockyintertidal invertebrates using biomimetic technology Broitman

et al (2009) demonstrated that body temperatures of a keystonepredator (the seastar Pisaster ochraceus) were at times in excess

of 108C lower than its prey (the mussel Mytilus californianus)even though both were within the same microhabitat Suchdramatic differences in the body temperatures of P ochraceus

and M californianus are most likely due to differences inmorphology and reflectance (ie P ochraceus is larger thanM californianus does not have a calcareous shell and is usually

brightly coloured) In contrast the three species examined in ourwork all possess an external calcareous shell or test and are all

15

20

25

30

35

40

45Daily maxima

15

20

25

30

35

40

45Habitat Cellana

Tesseropora Dicathaislowast

15

20

25

30Daily mean

15

20

25

30

10

15

20

25Daily minima

10

15

20

25

Mic

roha

bita

tbod

y te

mpe

ratu

re (

C)

Stressful Benign

05-M

ar-1

3

09-M

ar-1

3

13-M

ar-1

3

17-M

ar-1

3

21-M

ar-1

3

25-M

ar-1

3

29-M

ar-1

3

02-A

pr-1

3

06-A

pr-1

3

10-A

pr-1

3

05-M

ar-1

3

09-M

ar-1

3

13-M

ar-1

3

17-M

ar-1

3

21-M

ar-1

3

25-M

ar-1

3

29-M

ar-1

3

02-A

pr-1

3

06-A

pr-1

3

10-A

pr-1

3

Fig 3 Daily maxima mean and minima body temperatures of three different species of rocky intertidal invertebrates compared with habitat

temperature within stressful horizontal (left column) and benign southward facing vertical surfaces (right column) in the mid shore region at

Garie Beach from 5 March to 11 April 2013 Dicathais loggers were placed in shallow rock pools instead of vertical surfaces

90 Marine and Freshwater Research J A Lathlean et al

relatively small (20ndash50mm in length) with no large variationin colour (brown to grey) Regardless we detected significantdifferences in body temperatures of our three species among

multiple microhabitats Such differences in body tempera-ture may have dramatic consequences for interspecific interac-tions and the organisation of rocky intertidal communitieswithin this region

We found that microhabitats were a considerable source oftemperature variability for all three species This supports agrowing body of work that shows small-scale habitat hetero-

geneity is themajor source of body temperature variability amongrocky intertidal invertebrates (Denny et al 2004 Harley 2008Meager et al2011Lathlean et al 2012 2013)Microhabitats that

act as thermal refugia are expected to play an increasinglyimportant role in mitigating the future impacts of climate changeon these benthic communities For example with increasingthermal stress expected to occur on rocky intertidal shores of

south-east Australia we might expect (1) reduced foraging ratesof D orbita as they remain within shallow rock pools for longerperiods of time and (2) migration of C tramoserica away from

horizontal substrata to cooler southerly facing vertical surfacesBoth of these changes would positively affect T rosea byreducing early post-settlement mortality caused by grazing

C tramoserica and the predation of adults by D orbita Conse-quently rocky intertidal communities along the south-east coastof Australia may become increasingly dominated by T rosea

(Underwood et al 1983) Further experimental evidence howev-er is required to determinewhether increasedheat stresswill elicitsuch responses (eg Lathlean and Minchinton 2012)

Predicting the strength of speciesrsquo interactions under futureclimate change scenarios depends largely on understanding theunique physiological responses of individual species in a com-

munity context (Russell et al 2012) Body temperature mea-surements as presented here represent a useful method ofassessing the physiological response of individual organisms

to changing environmental conditions The application of infra-red thermography to rocky intertidal systems has also emergedas an effective means of estimating intra- and inter-specific

variation in body temperatures (Caddy-Retalic et al 2011Chapperon and Seuront 2011a Cox and Smith 2011 Lathleanet al 2012) and could serve as a complementary approach tobiomimetic technology Infrared thermography is particularly

useful for investigating the role of thermoregulatory behaviour(Chapperon and Seuront 2011a 2011b 2012) which wasnot accounted for within the present study More is needed

however because body temperatures alone cannot informresearchers whether an organism is thermally stressed Bodytemperature measurements need to be placed within a physio-

logical context that considers how thermal limits of a speciesvary across broad geographic scales (Tomanek 2008 Dennyand Helmuth 2009 Somero 2010) Unfortunately these funda-mental physiological parameters have yet to be determined for

the majority of rocky intertidal invertebrates of south-eastAustralia To help safeguard these vulnerable benthic commu-nities to climate change (Denny and Harley 2006 Wernberg

et al 2011) we suggest future research should focus on

Table 2 Summary of two-factor ANOVA and SNK for the effect of

species (C tramoserica T rosea D orbita) and microhabitat (benign

stressful) on daily maximal mean and minimum body temperatures

Source df SS F-ratio P-value

Daily Maxima

Species 2 100145 4587 0015

Microhabitat 1 44873 4110 0048

SpeciesMicrohabitat 2 30781 1410 0253

Error 54 589521

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

StressfulBenign

Daily Mean

Species 2 17151 7117 0002

Microhabitat 1 0030 0025 0875

SpeciesMicrohabitat 2 5141 2133 0128

Error 54 65067

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

Stressfulfrac14Benign

Daily Minima

Species 2 11525 4051 0023

Microhabitat 1 6177 4342 0042

SpeciesMicrohabitat 2 4501 1582 0215

Error 54 76818

SNK [species] Cellana

Tesseropora

SNK [microhabitat]

StressfulBenign

Table 1 Summary of one-factor ANOVA and SNK tests for the effect

of environmental and species temperature (daily maxima mean and

minima) recorded by TidbiT loggers and the three different biomimetic

loggers attached to horizontal emergent rocky substrata

Source df SS F-ratio P-value

Stressful microhabitat

Daily Maxima 3 472627 9306 0001

Error 36 609445

SNK HabitatAll species

Daily Mean 3 57701 13419 0001

Error 36 51599

SNK HabitatAll species

Daily Minima 3 11786 3929 0034

Error 36 43807

SNK Habitat

Tesseropora only

Benign microhabitat

Daily Maxima 3 245123 7901 0001

Error 36 372295

SNK Habitat and Cellana

Dicathais and Tesseropora

Daily mean 3 28304 9435 0001

Error 36 35118

SNK Habitat and Cellana

Dicathais and Tess

Daily Minima 3 13862 3160 0036

Error 36 52643

SNK Cellana

Dicathais and Tesseropora

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 91

10

15

20

25

30

35

40

45 Habitat

10

15

20

25

30

35

40

45Cellana

10

15

20

25

30

35

40

45Tesseropora

10

15

20

25

30

35

40

45Dicathais

Bod

ym

icro

habi

tat t

empe

ratu

re (

C)

5-Mar 6-Apr9-Mar 10-Apr13-Mar 17-Mar 21-Mar 25-Mar 29-Mar 2-Apr

(a)

(b)

(c)

(d )

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Rockpool

Fig 4 Microhabitat (a) and body temperatures of the limpet Cellana tramoserica (b) the barnacle

Tesseropora rosea (c) and the whelk Dicathais orbita (d ) within thermally stressful (horizontal

substrata) and thermally benign (southerly facing vertical substrata) microhabitats within the midshore

region at Garie Beach from 5 March to 11 April 2013 Body temperatures of T rosea attached to

southerly facing vertical surfaces were only recorded up until the 14 March due to malfunctioning

loggers

92 Marine and Freshwater Research J A Lathlean et al

(i) developing long-term body temperature measurements ofmultiple species using biomimetic loggers and (ii) undertake

physiological experiments aimed at calculating biogeographicvariability in speciesrsquo thermal limits

Acknowledgements

We thank Samuel Wighton and Elizabeth Lathlean for assistance with

biomimetic construction This research was supported by the Institute of

Conservation Biology and Environmental Management at the University

of Wollongong

References

Broitman B R Szathmary P L Mislan K A S Blanchette C A and

Helmuth B (2009) Predator-prey interactions under climate change

the importance of habitat vs body temperature Oikos 118 219ndash224

doi101111J1600-0706200817075X

Caddy-Retalic S Benkendorff K and Fairweather P G (2011) Visual-

izing hotspots Applying thermal imaging to monitor internal tempera-

tures in intertidal gastropods Molluscan Research 31 106ndash113

Chapman M G (1994) Small-scale patterns of distribution and size-

structure of the intertidal littorinid Littorina unifasciata (Gastropoda

Littorinidae) in New South Wales Australian Journal of Marine and

Freshwater Research 45 635ndash652 doi101071MF9940635

Chapperon C and Seuront L (2011a) Space-time variability in environ-

mental thermal properties and snail thermoregulatory behaviour

Functional Ecology 25 1040ndash1050 doi101111J1365-24352011

01859X

Chapperon C and Seuront L (2011b) Behavioral thermoregulation in a

tropical gastropod Links to climate change scenarios Global Change

Biology 17 1740ndash1749 doi101111J1365-2486201002356X

Chapperon C and Seuront L (2012) Keeping warm in the cold On the

thermal benefits of aggregation behaviour in an intertidal ectotherm

Journal of Thermal Biology 37 640ndash647 doi101016JJTHERBIO

201208001

Cox T E and Smith C M (2011) Thermal ecology on an exposed algal

reef infrared imagery a rapid tool to survey temperature at local spatial

scales Coral Reefs 30 1109ndash1120 doi101007S00338-011-0799-2

Creese R G (1982) Distribution and abundance of the Acmaeid Limpet

Patelloida latistrigata and its interaction with barnacles Oecologia 52

85ndash96 doi101007BF00349015

Denley E J and Underwood A J (1979) Experiments on factors

influencing settlement survival and growth of two species of barnacles

in New South Wales Journal of Experimental Marine Biology and

Ecology 36 269ndash293 doi1010160022-0981(79)90122-9

Denny M W and Harley C D G (2006) Hot limpets predicting body

temperature in a conductance-mediated thermal system The Journal of

Experimental Biology 209 2409ndash2419 doi101242JEB02257

Denny M and Helmuth B (2009) Confronting the physiological bottle-

neck A challenge from ecomechanics Integrative and Comparative

Biology 49 197ndash201 doi101093ICBICP070

DennyMW Helmuth B Leonard G H Harley C D G Hunt L J H

and Nelson E K (2004) Quantifying scale in ecology Lessons from

a wave-swept shore Ecological Monographs 74 513ndash532 doi101890

03-4043

DennyMWDowdWWBilir L andMachK J (2011) Spreading the

risk Small-scale body temperature variation among intertidal organisms

and its implications for species persistence Journal of Experimental

Marine Biology and Ecology 400 175ndash190 doi101016JJEMBE

201102006

Fairweather P G (1988a) Correlations of predatory whelks with intertidal

prey at several scales of space and timeMarine Ecology Progress Series

45 237ndash243 doi103354MEPS045237

Fairweather P G (1988b) Movements of intertidal whelks (Morula

marginalba and Thais orbita) in relation to availability of prey and

shelter Marine Biology 100 63ndash68 doi101007BF00392955

Fitzhenry T Halpin P M and Helmuth B (2004) Testing the effects of

wave exposure site and behavior on intertidal mussel body tempera-

tures applications and limits of temperature logger design Marine

Biology 145 339ndash349 doi101007S00227-004-1318-6

Harley C D G (2008) Tidal dynamics topographic orientation and

temperature-mediatedmassmortalities on rocky shoresMarineEcology

Progress Series 371 37ndash46 doi103354MEPS07711

Helmuth B (2002) How do we measure the environment Linking

intertidal thermal physiology and ecology through biophysics Integra-

tive and Comparative Biology 42 837ndash845 doi101093ICB424837

Helmuth B Broitman B R Blanchette C A Gilman S E Halpin PM

Harley C D G OrsquoDonnell M Hoffmann A A Menge B A and

Strickland D (2006a) Mosaic patterns of thermal stress in the rocky

intertidal zone implications for climate change Ecological Monographs

76 461ndash479 doi1018900012-9615(2006)076[0461MPOTSI]20CO2

Helmuth B Mieszkowska N Moore P and Hawkins S J (2006b)

Living on the edge of two changing worlds forecasting the responses of

rocky intertidal ecosystems to climate change Annual Review of

Ecology Evolution and Systematics 37 373ndash404 doi101146

ANNUREVECOLSYS37091305110149

Hidas E Z Russell K G Ayre D J and Minchinton T E (2013)

Abundance of Tesseropora rosea at the margins of its biogeographic

range is closely linked to recruitment but not fecundityMarine Ecology

Progress Series 483 199ndash208 doi103354MEPS10271

Jernakoff P (1983) Factors affecting the recruitment of algae in a midshore

region dominated by barnacles Journal of ExperimentalMarine Biology

and Ecology 67 17ndash31 doi1010160022-0981(83)90132-6

Kordas R L Harley C D G and OrsquoConnor M I (2011) Community

ecology in a warming world The influence of temperature on interspe-

cific interactions in marine systems Journal of Experimental Marine

Biology and Ecology 400 218ndash226 doi101016JJEMBE201102029

Lathlean J A and Minchinton T E (2012) Manipulating thermal stress

on rocky shores to predict patterns of recruitment ofmarine invertebrates

under a changing climate Marine Ecology Progress Series 467

121ndash136 doi103354MEPS09996

Lathlean J A Ayre D J and Minchinton T E (2012) Using infrared

imagery to test for quadrat-level temperature variation and effects on the

early life history of a rocky-shore barnacle Limnology and Oceanogra-

phy 57 1279ndash1291 doi104319LO20125751279

Lathlean J A Ayre D J and Minchinton T E (2013) Temperature

variability at the larval scale affects early survival and growth of an

intertidal barnacle Marine Ecology Progress Series 475 155ndash166

doi103354MEPS10105

Lima F P and Wethey D S (2009) Robolimpets measuring intertidal

body temperatures using biomimetic loggers Limnology and Oceanog-

raphy Methods 7 347ndash353 doi104319LOM20097347

Meager J J Schlacher T A and Green M (2011) Topographic

complexity and landscape temperature patterns create a dynamic habitat

structure on a rocky intertidal shore Marine Ecology Progress Series

428 1ndash12 doi103354MEPS09124

Phillips B F and Campbell N A (1974) Mortality and longevity in the

whelk Dicathais orbita (Gmelin) Australian Journal of Marine and

Freshwater Research 25 25ndash33 doi101071MF9740025

Pincebourde S Sanford E and Helmuth B (2008) Body temperatures

during low tide alters the feeding performance of a top intertidal

predator Limnology and Oceanography 53 1562ndash1573 doi104319

LO20085341562

Russell B D Harley C D G Wernberg T Mieszkowska N Widdi-

combe S Hall-Spencer J M and Connell S D (2012) Predicting

ecosystem shifts requires new approaches that integrate the effects of

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 93

relatively small (20ndash50mm in length) with no large variationin colour (brown to grey) Regardless we detected significantdifferences in body temperatures of our three species among

multiple microhabitats Such differences in body tempera-ture may have dramatic consequences for interspecific interac-tions and the organisation of rocky intertidal communitieswithin this region

We found that microhabitats were a considerable source oftemperature variability for all three species This supports agrowing body of work that shows small-scale habitat hetero-

geneity is themajor source of body temperature variability amongrocky intertidal invertebrates (Denny et al 2004 Harley 2008Meager et al2011Lathlean et al 2012 2013)Microhabitats that

act as thermal refugia are expected to play an increasinglyimportant role in mitigating the future impacts of climate changeon these benthic communities For example with increasingthermal stress expected to occur on rocky intertidal shores of

south-east Australia we might expect (1) reduced foraging ratesof D orbita as they remain within shallow rock pools for longerperiods of time and (2) migration of C tramoserica away from

horizontal substrata to cooler southerly facing vertical surfacesBoth of these changes would positively affect T rosea byreducing early post-settlement mortality caused by grazing

C tramoserica and the predation of adults by D orbita Conse-quently rocky intertidal communities along the south-east coastof Australia may become increasingly dominated by T rosea

(Underwood et al 1983) Further experimental evidence howev-er is required to determinewhether increasedheat stresswill elicitsuch responses (eg Lathlean and Minchinton 2012)

Predicting the strength of speciesrsquo interactions under futureclimate change scenarios depends largely on understanding theunique physiological responses of individual species in a com-

munity context (Russell et al 2012) Body temperature mea-surements as presented here represent a useful method ofassessing the physiological response of individual organisms

to changing environmental conditions The application of infra-red thermography to rocky intertidal systems has also emergedas an effective means of estimating intra- and inter-specific

variation in body temperatures (Caddy-Retalic et al 2011Chapperon and Seuront 2011a Cox and Smith 2011 Lathleanet al 2012) and could serve as a complementary approach tobiomimetic technology Infrared thermography is particularly

useful for investigating the role of thermoregulatory behaviour(Chapperon and Seuront 2011a 2011b 2012) which wasnot accounted for within the present study More is needed

however because body temperatures alone cannot informresearchers whether an organism is thermally stressed Bodytemperature measurements need to be placed within a physio-

logical context that considers how thermal limits of a speciesvary across broad geographic scales (Tomanek 2008 Dennyand Helmuth 2009 Somero 2010) Unfortunately these funda-mental physiological parameters have yet to be determined for

the majority of rocky intertidal invertebrates of south-eastAustralia To help safeguard these vulnerable benthic commu-nities to climate change (Denny and Harley 2006 Wernberg

et al 2011) we suggest future research should focus on

Table 2 Summary of two-factor ANOVA and SNK for the effect of

species (C tramoserica T rosea D orbita) and microhabitat (benign

stressful) on daily maximal mean and minimum body temperatures

Source df SS F-ratio P-value

Daily Maxima

Species 2 100145 4587 0015

Microhabitat 1 44873 4110 0048

SpeciesMicrohabitat 2 30781 1410 0253

Error 54 589521

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

StressfulBenign

Daily Mean

Species 2 17151 7117 0002

Microhabitat 1 0030 0025 0875

SpeciesMicrohabitat 2 5141 2133 0128

Error 54 65067

SNK [species] Cellana

Dicathais and Tesseropora

SNK [microhabitat]

Stressfulfrac14Benign

Daily Minima

Species 2 11525 4051 0023

Microhabitat 1 6177 4342 0042

SpeciesMicrohabitat 2 4501 1582 0215

Error 54 76818

SNK [species] Cellana

Tesseropora

SNK [microhabitat]

StressfulBenign

Table 1 Summary of one-factor ANOVA and SNK tests for the effect

of environmental and species temperature (daily maxima mean and

minima) recorded by TidbiT loggers and the three different biomimetic

loggers attached to horizontal emergent rocky substrata

Source df SS F-ratio P-value

Stressful microhabitat

Daily Maxima 3 472627 9306 0001

Error 36 609445

SNK HabitatAll species

Daily Mean 3 57701 13419 0001

Error 36 51599

SNK HabitatAll species

Daily Minima 3 11786 3929 0034

Error 36 43807

SNK Habitat

Tesseropora only

Benign microhabitat

Daily Maxima 3 245123 7901 0001

Error 36 372295

SNK Habitat and Cellana

Dicathais and Tesseropora

Daily mean 3 28304 9435 0001

Error 36 35118

SNK Habitat and Cellana

Dicathais and Tess

Daily Minima 3 13862 3160 0036

Error 36 52643

SNK Cellana

Dicathais and Tesseropora

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 91

10

15

20

25

30

35

40

45 Habitat

10

15

20

25

30

35

40

45Cellana

10

15

20

25

30

35

40

45Tesseropora

10

15

20

25

30

35

40

45Dicathais

Bod

ym

icro

habi

tat t

empe

ratu

re (

C)

5-Mar 6-Apr9-Mar 10-Apr13-Mar 17-Mar 21-Mar 25-Mar 29-Mar 2-Apr

(a)

(b)

(c)

(d )

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Rockpool

Fig 4 Microhabitat (a) and body temperatures of the limpet Cellana tramoserica (b) the barnacle

Tesseropora rosea (c) and the whelk Dicathais orbita (d ) within thermally stressful (horizontal

substrata) and thermally benign (southerly facing vertical substrata) microhabitats within the midshore

region at Garie Beach from 5 March to 11 April 2013 Body temperatures of T rosea attached to

southerly facing vertical surfaces were only recorded up until the 14 March due to malfunctioning

loggers

92 Marine and Freshwater Research J A Lathlean et al

(i) developing long-term body temperature measurements ofmultiple species using biomimetic loggers and (ii) undertake

physiological experiments aimed at calculating biogeographicvariability in speciesrsquo thermal limits

Acknowledgements

We thank Samuel Wighton and Elizabeth Lathlean for assistance with

biomimetic construction This research was supported by the Institute of

Conservation Biology and Environmental Management at the University

of Wollongong

References

Broitman B R Szathmary P L Mislan K A S Blanchette C A and

Helmuth B (2009) Predator-prey interactions under climate change

the importance of habitat vs body temperature Oikos 118 219ndash224

doi101111J1600-0706200817075X

Caddy-Retalic S Benkendorff K and Fairweather P G (2011) Visual-

izing hotspots Applying thermal imaging to monitor internal tempera-

tures in intertidal gastropods Molluscan Research 31 106ndash113

Chapman M G (1994) Small-scale patterns of distribution and size-

structure of the intertidal littorinid Littorina unifasciata (Gastropoda

Littorinidae) in New South Wales Australian Journal of Marine and

Freshwater Research 45 635ndash652 doi101071MF9940635

Chapperon C and Seuront L (2011a) Space-time variability in environ-

mental thermal properties and snail thermoregulatory behaviour

Functional Ecology 25 1040ndash1050 doi101111J1365-24352011

01859X

Chapperon C and Seuront L (2011b) Behavioral thermoregulation in a

tropical gastropod Links to climate change scenarios Global Change

Biology 17 1740ndash1749 doi101111J1365-2486201002356X

Chapperon C and Seuront L (2012) Keeping warm in the cold On the

thermal benefits of aggregation behaviour in an intertidal ectotherm

Journal of Thermal Biology 37 640ndash647 doi101016JJTHERBIO

201208001

Cox T E and Smith C M (2011) Thermal ecology on an exposed algal

reef infrared imagery a rapid tool to survey temperature at local spatial

scales Coral Reefs 30 1109ndash1120 doi101007S00338-011-0799-2

Creese R G (1982) Distribution and abundance of the Acmaeid Limpet

Patelloida latistrigata and its interaction with barnacles Oecologia 52

85ndash96 doi101007BF00349015

Denley E J and Underwood A J (1979) Experiments on factors

influencing settlement survival and growth of two species of barnacles

in New South Wales Journal of Experimental Marine Biology and

Ecology 36 269ndash293 doi1010160022-0981(79)90122-9

Denny M W and Harley C D G (2006) Hot limpets predicting body

temperature in a conductance-mediated thermal system The Journal of

Experimental Biology 209 2409ndash2419 doi101242JEB02257

Denny M and Helmuth B (2009) Confronting the physiological bottle-

neck A challenge from ecomechanics Integrative and Comparative

Biology 49 197ndash201 doi101093ICBICP070

DennyMW Helmuth B Leonard G H Harley C D G Hunt L J H

and Nelson E K (2004) Quantifying scale in ecology Lessons from

a wave-swept shore Ecological Monographs 74 513ndash532 doi101890

03-4043

DennyMWDowdWWBilir L andMachK J (2011) Spreading the

risk Small-scale body temperature variation among intertidal organisms

and its implications for species persistence Journal of Experimental

Marine Biology and Ecology 400 175ndash190 doi101016JJEMBE

201102006

Fairweather P G (1988a) Correlations of predatory whelks with intertidal

prey at several scales of space and timeMarine Ecology Progress Series

45 237ndash243 doi103354MEPS045237

Fairweather P G (1988b) Movements of intertidal whelks (Morula

marginalba and Thais orbita) in relation to availability of prey and

shelter Marine Biology 100 63ndash68 doi101007BF00392955

Fitzhenry T Halpin P M and Helmuth B (2004) Testing the effects of

wave exposure site and behavior on intertidal mussel body tempera-

tures applications and limits of temperature logger design Marine

Biology 145 339ndash349 doi101007S00227-004-1318-6

Harley C D G (2008) Tidal dynamics topographic orientation and

temperature-mediatedmassmortalities on rocky shoresMarineEcology

Progress Series 371 37ndash46 doi103354MEPS07711

Helmuth B (2002) How do we measure the environment Linking

intertidal thermal physiology and ecology through biophysics Integra-

tive and Comparative Biology 42 837ndash845 doi101093ICB424837

Helmuth B Broitman B R Blanchette C A Gilman S E Halpin PM

Harley C D G OrsquoDonnell M Hoffmann A A Menge B A and

Strickland D (2006a) Mosaic patterns of thermal stress in the rocky

intertidal zone implications for climate change Ecological Monographs

76 461ndash479 doi1018900012-9615(2006)076[0461MPOTSI]20CO2

Helmuth B Mieszkowska N Moore P and Hawkins S J (2006b)

Living on the edge of two changing worlds forecasting the responses of

rocky intertidal ecosystems to climate change Annual Review of

Ecology Evolution and Systematics 37 373ndash404 doi101146

ANNUREVECOLSYS37091305110149

Hidas E Z Russell K G Ayre D J and Minchinton T E (2013)

Abundance of Tesseropora rosea at the margins of its biogeographic

range is closely linked to recruitment but not fecundityMarine Ecology

Progress Series 483 199ndash208 doi103354MEPS10271

Jernakoff P (1983) Factors affecting the recruitment of algae in a midshore

region dominated by barnacles Journal of ExperimentalMarine Biology

and Ecology 67 17ndash31 doi1010160022-0981(83)90132-6

Kordas R L Harley C D G and OrsquoConnor M I (2011) Community

ecology in a warming world The influence of temperature on interspe-

cific interactions in marine systems Journal of Experimental Marine

Biology and Ecology 400 218ndash226 doi101016JJEMBE201102029

Lathlean J A and Minchinton T E (2012) Manipulating thermal stress

on rocky shores to predict patterns of recruitment ofmarine invertebrates

under a changing climate Marine Ecology Progress Series 467

121ndash136 doi103354MEPS09996

Lathlean J A Ayre D J and Minchinton T E (2012) Using infrared

imagery to test for quadrat-level temperature variation and effects on the

early life history of a rocky-shore barnacle Limnology and Oceanogra-

phy 57 1279ndash1291 doi104319LO20125751279

Lathlean J A Ayre D J and Minchinton T E (2013) Temperature

variability at the larval scale affects early survival and growth of an

intertidal barnacle Marine Ecology Progress Series 475 155ndash166

doi103354MEPS10105

Lima F P and Wethey D S (2009) Robolimpets measuring intertidal

body temperatures using biomimetic loggers Limnology and Oceanog-

raphy Methods 7 347ndash353 doi104319LOM20097347

Meager J J Schlacher T A and Green M (2011) Topographic

complexity and landscape temperature patterns create a dynamic habitat

structure on a rocky intertidal shore Marine Ecology Progress Series

428 1ndash12 doi103354MEPS09124

Phillips B F and Campbell N A (1974) Mortality and longevity in the

whelk Dicathais orbita (Gmelin) Australian Journal of Marine and

Freshwater Research 25 25ndash33 doi101071MF9740025

Pincebourde S Sanford E and Helmuth B (2008) Body temperatures

during low tide alters the feeding performance of a top intertidal

predator Limnology and Oceanography 53 1562ndash1573 doi104319

LO20085341562

Russell B D Harley C D G Wernberg T Mieszkowska N Widdi-

combe S Hall-Spencer J M and Connell S D (2012) Predicting

ecosystem shifts requires new approaches that integrate the effects of

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 93

10

15

20

25

30

35

40

45 Habitat

10

15

20

25

30

35

40

45Cellana

10

15

20

25

30

35

40

45Tesseropora

10

15

20

25

30

35

40

45Dicathais

Bod

ym

icro

habi

tat t

empe

ratu

re (

C)

5-Mar 6-Apr9-Mar 10-Apr13-Mar 17-Mar 21-Mar 25-Mar 29-Mar 2-Apr

(a)

(b)

(c)

(d )

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Vertical (South)

Horizontal

Rockpool

Fig 4 Microhabitat (a) and body temperatures of the limpet Cellana tramoserica (b) the barnacle

Tesseropora rosea (c) and the whelk Dicathais orbita (d ) within thermally stressful (horizontal

substrata) and thermally benign (southerly facing vertical substrata) microhabitats within the midshore

region at Garie Beach from 5 March to 11 April 2013 Body temperatures of T rosea attached to

southerly facing vertical surfaces were only recorded up until the 14 March due to malfunctioning

loggers

92 Marine and Freshwater Research J A Lathlean et al

(i) developing long-term body temperature measurements ofmultiple species using biomimetic loggers and (ii) undertake

physiological experiments aimed at calculating biogeographicvariability in speciesrsquo thermal limits

Acknowledgements

We thank Samuel Wighton and Elizabeth Lathlean for assistance with

biomimetic construction This research was supported by the Institute of

Conservation Biology and Environmental Management at the University

of Wollongong

References

Broitman B R Szathmary P L Mislan K A S Blanchette C A and

Helmuth B (2009) Predator-prey interactions under climate change

the importance of habitat vs body temperature Oikos 118 219ndash224

doi101111J1600-0706200817075X

Caddy-Retalic S Benkendorff K and Fairweather P G (2011) Visual-

izing hotspots Applying thermal imaging to monitor internal tempera-

tures in intertidal gastropods Molluscan Research 31 106ndash113

Chapman M G (1994) Small-scale patterns of distribution and size-

structure of the intertidal littorinid Littorina unifasciata (Gastropoda

Littorinidae) in New South Wales Australian Journal of Marine and

Freshwater Research 45 635ndash652 doi101071MF9940635

Chapperon C and Seuront L (2011a) Space-time variability in environ-

mental thermal properties and snail thermoregulatory behaviour

Functional Ecology 25 1040ndash1050 doi101111J1365-24352011

01859X

Chapperon C and Seuront L (2011b) Behavioral thermoregulation in a

tropical gastropod Links to climate change scenarios Global Change

Biology 17 1740ndash1749 doi101111J1365-2486201002356X

Chapperon C and Seuront L (2012) Keeping warm in the cold On the

thermal benefits of aggregation behaviour in an intertidal ectotherm

Journal of Thermal Biology 37 640ndash647 doi101016JJTHERBIO

201208001

Cox T E and Smith C M (2011) Thermal ecology on an exposed algal

reef infrared imagery a rapid tool to survey temperature at local spatial

scales Coral Reefs 30 1109ndash1120 doi101007S00338-011-0799-2

Creese R G (1982) Distribution and abundance of the Acmaeid Limpet

Patelloida latistrigata and its interaction with barnacles Oecologia 52

85ndash96 doi101007BF00349015

Denley E J and Underwood A J (1979) Experiments on factors

influencing settlement survival and growth of two species of barnacles

in New South Wales Journal of Experimental Marine Biology and

Ecology 36 269ndash293 doi1010160022-0981(79)90122-9

Denny M W and Harley C D G (2006) Hot limpets predicting body

temperature in a conductance-mediated thermal system The Journal of

Experimental Biology 209 2409ndash2419 doi101242JEB02257

Denny M and Helmuth B (2009) Confronting the physiological bottle-

neck A challenge from ecomechanics Integrative and Comparative

Biology 49 197ndash201 doi101093ICBICP070

DennyMW Helmuth B Leonard G H Harley C D G Hunt L J H

and Nelson E K (2004) Quantifying scale in ecology Lessons from

a wave-swept shore Ecological Monographs 74 513ndash532 doi101890

03-4043

DennyMWDowdWWBilir L andMachK J (2011) Spreading the

risk Small-scale body temperature variation among intertidal organisms

and its implications for species persistence Journal of Experimental

Marine Biology and Ecology 400 175ndash190 doi101016JJEMBE

201102006

Fairweather P G (1988a) Correlations of predatory whelks with intertidal

prey at several scales of space and timeMarine Ecology Progress Series

45 237ndash243 doi103354MEPS045237

Fairweather P G (1988b) Movements of intertidal whelks (Morula

marginalba and Thais orbita) in relation to availability of prey and

shelter Marine Biology 100 63ndash68 doi101007BF00392955

Fitzhenry T Halpin P M and Helmuth B (2004) Testing the effects of

wave exposure site and behavior on intertidal mussel body tempera-

tures applications and limits of temperature logger design Marine

Biology 145 339ndash349 doi101007S00227-004-1318-6

Harley C D G (2008) Tidal dynamics topographic orientation and

temperature-mediatedmassmortalities on rocky shoresMarineEcology

Progress Series 371 37ndash46 doi103354MEPS07711

Helmuth B (2002) How do we measure the environment Linking

intertidal thermal physiology and ecology through biophysics Integra-

tive and Comparative Biology 42 837ndash845 doi101093ICB424837

Helmuth B Broitman B R Blanchette C A Gilman S E Halpin PM

Harley C D G OrsquoDonnell M Hoffmann A A Menge B A and

Strickland D (2006a) Mosaic patterns of thermal stress in the rocky

intertidal zone implications for climate change Ecological Monographs

76 461ndash479 doi1018900012-9615(2006)076[0461MPOTSI]20CO2

Helmuth B Mieszkowska N Moore P and Hawkins S J (2006b)

Living on the edge of two changing worlds forecasting the responses of

rocky intertidal ecosystems to climate change Annual Review of

Ecology Evolution and Systematics 37 373ndash404 doi101146

ANNUREVECOLSYS37091305110149

Hidas E Z Russell K G Ayre D J and Minchinton T E (2013)

Abundance of Tesseropora rosea at the margins of its biogeographic

range is closely linked to recruitment but not fecundityMarine Ecology

Progress Series 483 199ndash208 doi103354MEPS10271

Jernakoff P (1983) Factors affecting the recruitment of algae in a midshore

region dominated by barnacles Journal of ExperimentalMarine Biology

and Ecology 67 17ndash31 doi1010160022-0981(83)90132-6

Kordas R L Harley C D G and OrsquoConnor M I (2011) Community

ecology in a warming world The influence of temperature on interspe-

cific interactions in marine systems Journal of Experimental Marine

Biology and Ecology 400 218ndash226 doi101016JJEMBE201102029

Lathlean J A and Minchinton T E (2012) Manipulating thermal stress

on rocky shores to predict patterns of recruitment ofmarine invertebrates

under a changing climate Marine Ecology Progress Series 467

121ndash136 doi103354MEPS09996

Lathlean J A Ayre D J and Minchinton T E (2012) Using infrared

imagery to test for quadrat-level temperature variation and effects on the

early life history of a rocky-shore barnacle Limnology and Oceanogra-

phy 57 1279ndash1291 doi104319LO20125751279

Lathlean J A Ayre D J and Minchinton T E (2013) Temperature

variability at the larval scale affects early survival and growth of an

intertidal barnacle Marine Ecology Progress Series 475 155ndash166

doi103354MEPS10105

Lima F P and Wethey D S (2009) Robolimpets measuring intertidal

body temperatures using biomimetic loggers Limnology and Oceanog-

raphy Methods 7 347ndash353 doi104319LOM20097347

Meager J J Schlacher T A and Green M (2011) Topographic

complexity and landscape temperature patterns create a dynamic habitat

structure on a rocky intertidal shore Marine Ecology Progress Series

428 1ndash12 doi103354MEPS09124

Phillips B F and Campbell N A (1974) Mortality and longevity in the

whelk Dicathais orbita (Gmelin) Australian Journal of Marine and

Freshwater Research 25 25ndash33 doi101071MF9740025

Pincebourde S Sanford E and Helmuth B (2008) Body temperatures

during low tide alters the feeding performance of a top intertidal

predator Limnology and Oceanography 53 1562ndash1573 doi104319

LO20085341562

Russell B D Harley C D G Wernberg T Mieszkowska N Widdi-

combe S Hall-Spencer J M and Connell S D (2012) Predicting

ecosystem shifts requires new approaches that integrate the effects of

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 93

(i) developing long-term body temperature measurements ofmultiple species using biomimetic loggers and (ii) undertake

physiological experiments aimed at calculating biogeographicvariability in speciesrsquo thermal limits

Acknowledgements

We thank Samuel Wighton and Elizabeth Lathlean for assistance with

biomimetic construction This research was supported by the Institute of

Conservation Biology and Environmental Management at the University

of Wollongong

References

Broitman B R Szathmary P L Mislan K A S Blanchette C A and

Helmuth B (2009) Predator-prey interactions under climate change

the importance of habitat vs body temperature Oikos 118 219ndash224

doi101111J1600-0706200817075X

Caddy-Retalic S Benkendorff K and Fairweather P G (2011) Visual-

izing hotspots Applying thermal imaging to monitor internal tempera-

tures in intertidal gastropods Molluscan Research 31 106ndash113

Chapman M G (1994) Small-scale patterns of distribution and size-

structure of the intertidal littorinid Littorina unifasciata (Gastropoda

Littorinidae) in New South Wales Australian Journal of Marine and

Freshwater Research 45 635ndash652 doi101071MF9940635

Chapperon C and Seuront L (2011a) Space-time variability in environ-

mental thermal properties and snail thermoregulatory behaviour

Functional Ecology 25 1040ndash1050 doi101111J1365-24352011

01859X

Chapperon C and Seuront L (2011b) Behavioral thermoregulation in a

tropical gastropod Links to climate change scenarios Global Change

Biology 17 1740ndash1749 doi101111J1365-2486201002356X

Chapperon C and Seuront L (2012) Keeping warm in the cold On the

thermal benefits of aggregation behaviour in an intertidal ectotherm

Journal of Thermal Biology 37 640ndash647 doi101016JJTHERBIO

201208001

Cox T E and Smith C M (2011) Thermal ecology on an exposed algal

reef infrared imagery a rapid tool to survey temperature at local spatial

scales Coral Reefs 30 1109ndash1120 doi101007S00338-011-0799-2

Creese R G (1982) Distribution and abundance of the Acmaeid Limpet

Patelloida latistrigata and its interaction with barnacles Oecologia 52

85ndash96 doi101007BF00349015

Denley E J and Underwood A J (1979) Experiments on factors

influencing settlement survival and growth of two species of barnacles

in New South Wales Journal of Experimental Marine Biology and

Ecology 36 269ndash293 doi1010160022-0981(79)90122-9

Denny M W and Harley C D G (2006) Hot limpets predicting body

temperature in a conductance-mediated thermal system The Journal of

Experimental Biology 209 2409ndash2419 doi101242JEB02257

Denny M and Helmuth B (2009) Confronting the physiological bottle-

neck A challenge from ecomechanics Integrative and Comparative

Biology 49 197ndash201 doi101093ICBICP070

DennyMW Helmuth B Leonard G H Harley C D G Hunt L J H

and Nelson E K (2004) Quantifying scale in ecology Lessons from

a wave-swept shore Ecological Monographs 74 513ndash532 doi101890

03-4043

DennyMWDowdWWBilir L andMachK J (2011) Spreading the

risk Small-scale body temperature variation among intertidal organisms

and its implications for species persistence Journal of Experimental

Marine Biology and Ecology 400 175ndash190 doi101016JJEMBE

201102006

Fairweather P G (1988a) Correlations of predatory whelks with intertidal

prey at several scales of space and timeMarine Ecology Progress Series

45 237ndash243 doi103354MEPS045237

Fairweather P G (1988b) Movements of intertidal whelks (Morula

marginalba and Thais orbita) in relation to availability of prey and

shelter Marine Biology 100 63ndash68 doi101007BF00392955

Fitzhenry T Halpin P M and Helmuth B (2004) Testing the effects of

wave exposure site and behavior on intertidal mussel body tempera-

tures applications and limits of temperature logger design Marine

Biology 145 339ndash349 doi101007S00227-004-1318-6

Harley C D G (2008) Tidal dynamics topographic orientation and

temperature-mediatedmassmortalities on rocky shoresMarineEcology

Progress Series 371 37ndash46 doi103354MEPS07711

Helmuth B (2002) How do we measure the environment Linking

intertidal thermal physiology and ecology through biophysics Integra-

tive and Comparative Biology 42 837ndash845 doi101093ICB424837

Helmuth B Broitman B R Blanchette C A Gilman S E Halpin PM

Harley C D G OrsquoDonnell M Hoffmann A A Menge B A and

Strickland D (2006a) Mosaic patterns of thermal stress in the rocky

intertidal zone implications for climate change Ecological Monographs

76 461ndash479 doi1018900012-9615(2006)076[0461MPOTSI]20CO2

Helmuth B Mieszkowska N Moore P and Hawkins S J (2006b)

Living on the edge of two changing worlds forecasting the responses of

rocky intertidal ecosystems to climate change Annual Review of

Ecology Evolution and Systematics 37 373ndash404 doi101146

ANNUREVECOLSYS37091305110149

Hidas E Z Russell K G Ayre D J and Minchinton T E (2013)

Abundance of Tesseropora rosea at the margins of its biogeographic

range is closely linked to recruitment but not fecundityMarine Ecology

Progress Series 483 199ndash208 doi103354MEPS10271

Jernakoff P (1983) Factors affecting the recruitment of algae in a midshore

region dominated by barnacles Journal of ExperimentalMarine Biology

and Ecology 67 17ndash31 doi1010160022-0981(83)90132-6

Kordas R L Harley C D G and OrsquoConnor M I (2011) Community

ecology in a warming world The influence of temperature on interspe-

cific interactions in marine systems Journal of Experimental Marine

Biology and Ecology 400 218ndash226 doi101016JJEMBE201102029

Lathlean J A and Minchinton T E (2012) Manipulating thermal stress

on rocky shores to predict patterns of recruitment ofmarine invertebrates

under a changing climate Marine Ecology Progress Series 467

121ndash136 doi103354MEPS09996

Lathlean J A Ayre D J and Minchinton T E (2012) Using infrared

imagery to test for quadrat-level temperature variation and effects on the

early life history of a rocky-shore barnacle Limnology and Oceanogra-

phy 57 1279ndash1291 doi104319LO20125751279

Lathlean J A Ayre D J and Minchinton T E (2013) Temperature

variability at the larval scale affects early survival and growth of an

intertidal barnacle Marine Ecology Progress Series 475 155ndash166

doi103354MEPS10105

Lima F P and Wethey D S (2009) Robolimpets measuring intertidal

body temperatures using biomimetic loggers Limnology and Oceanog-

raphy Methods 7 347ndash353 doi104319LOM20097347

Meager J J Schlacher T A and Green M (2011) Topographic

complexity and landscape temperature patterns create a dynamic habitat

structure on a rocky intertidal shore Marine Ecology Progress Series

428 1ndash12 doi103354MEPS09124

Phillips B F and Campbell N A (1974) Mortality and longevity in the

whelk Dicathais orbita (Gmelin) Australian Journal of Marine and

Freshwater Research 25 25ndash33 doi101071MF9740025

Pincebourde S Sanford E and Helmuth B (2008) Body temperatures

during low tide alters the feeding performance of a top intertidal

predator Limnology and Oceanography 53 1562ndash1573 doi104319

LO20085341562

Russell B D Harley C D G Wernberg T Mieszkowska N Widdi-

combe S Hall-Spencer J M and Connell S D (2012) Predicting

ecosystem shifts requires new approaches that integrate the effects of

Interspecific and microhabitat variation in body temperature Marine and Freshwater Research 93

climate change across entire systems Biology Letters 8 164ndash166

doi101098RSBL20110779

Seabra R Wethey D S Santos A M and Lima F P (2011) Side

matters Microhabitat influence on intertidal heat stress over a

large geographical scale Journal of Experimental Marine Biology

and Ecology 400 200ndash208

Somero G N (2010) The physiology of climate change how

potentials for acclimatization and genetic adaptation will determine

lsquolsquowinnersrsquorsquo and lsquolsquolosersrsquorsquo The Journal of Experimental Biology 213

912ndash920

Szathmary P L Helmuth B andWethey D S (2009) Climate change in

the rocky intertidal zone predicting andmeasuring the body temperature

of a keystone predator Marine Ecology Progress Series 374 43ndash56

doi103354MEPS07682

Tomanek L (2008) The importance of physiological limits in determining

biogeographical range shifts to global change the heat-shock response

Physiological and Biochemical Zoology 81 709ndash717 doi101086

590163

Underwood A J Denley E J and Moran M J (1983) Experimental

analyses of the structure and dynamics of mid-shore rocky intertidal

communities in NewSouthWalesOecologia 56 202ndash219 doi101007

BF00379692

Wernberg T Russell B D Moore P J Ling S D Smale D A

Campbell A Coleman M A Steinberg P D Kendrick G A and

Connell S D (2011) Impacts of climate change in a global hotspot for

temperate marine biodiversity and ocean warming Journal of Experi-

mental Marine Biology and Ecology 400 7ndash16 doi101016JJEMBE

201102021

wwwpublishcsiroaujournalsmfr

94 Marine and Freshwater Research J A Lathlean et al