The understanding of how climate warming may affect the ecological and geographical distributions of intertidal ectotherms requires insight into how their body temperatures vary in relation to environmental temperature (Angilletta, 2009; Helmuth et al., 2010). This issue is particularly relevant in high-shore environments, in which species experience extreme thermal stress regimes during the periods of aerial exposure (McMahon, 1990; Marshall, mcquaid &Williams, 2010a; Marshall, qadirulisyam Bin Mustafa &Williams, 2010b). In fact, high-shore intertidal species are considered more vulnerable to climate warming than low-shore or subtidal species, because they are typically living closer to their thermal tolerance physiological limits in the tropics (see Somero, 2012 for a review). While physiological responses may be relatively limited in mitigating heat stress, behavioural responses may, however, be critical to buffer thermal stress as shown in ectotherms that use a wide range of thermal environments (Kearney, shine & Porter, 2009).

Thermal regulatory behaviours are critical on rocky shores due to the latter's high degree of topographic complexity, hence the related variety of thermal microhabitats (Chapperon & Seuront, 2011a; Lathlean, ayre &Minchinton, 2012) and considerable temporal and spatial fluctuations in environmental temperature (Denny et al., 2011; Gedan et al., 2011; Lathlean, ayre & minchinton, 2014). The behaviours include selection of thermally more benign microhabitats (Chapperon & Seuront, 2011a; Iacarella & Helmuth 2011), formation of aggregations (Chapperon & Seuront, 2012), shell orientation relative to the sun (Muñoz et al., 2005) and shell-posturing behaviour (Marshall et al., 2010a, b).

High shore littorinid snails exhibit shell-posturing behaviour during low tide, i.e. individuals retract their foot into their shell, close their operculum and glue themselves to the substratum with a mucus holdfast that allows them to lift their body off the substratum (McMahon, 1990; Lang, britton &Metz, 1998). This behaviour is considered as an adaptive strategy that minimizes conductive transfer from the substratum to the shell by reducing the amount of the shell in contact with the substratum, while maximizing the shell surface exposed to air currents, hence allowing increased heat transfer from the shell through convective cooling (Miller & Denny, 2011; Marshall & Chua, 2012). More specifically, improved cooling is achieved through shell-standing (Lim, 2008; Miller & Denny, 2011; Marshall & Chua, 2012) and shell-stacking (Marshall et al., 2010b), two related behaviours whereby a snail is respectively attached to the substratum with its aperture facing perpendicularly to the surface (as opposed to downwards) and climbs onto other snails to form a stack or ‘tower’ (Marshall et al., 2010b).

Both shell standing and towering behaviours have previously been shown to be effective strategies to mitigate thermal stress in Echinolittorina malaccana (Marshall et al., 2010b; Marshall & Chua, 2012). These studies were, however, based on the use of biomimetic snail models with thermocouples inserted in them. Such models allow continuous long-term measurements, avoid spurious physiological and behavioural consequences of inserting thermocouples into small organisms and show reasonable correlations between body temperature of model snails and live snails, including for littorinids (Iacarella & Helmuth, 2011; Marshall et al., 2010a; Miller & Denny, 2011). Their generality is, however, intrinsically limited by the number of snails that can be simultaneously studied, e.g. a tower of three E. malaccana shells (Marshall et al., 2010b), and four E. malaccana shells glued on a flat rock surface in standing and non-standing position either under direct sunlight or in the shade (Marshall & Chua, 2012). Further, this approach does not allow simultaneous measurement of snail and substratum temperature at spatial scales compatible with the considerable thermal heterogeneity observed on intertidal rocky shores (Denny et al., 2011; Lathlean et al., 2014). This is not the case, however, with infrared thermography (IRT) that allows—in a relatively limited amount of time and with limited logistics compared with traditional thermal methods—non-invasive simultaneous measurements of both the body temperature of multiple snails and the thermal properties of their substratum at scales compatible with the behavioural biology and ecology of individual organisms (see Lathlean & Seuront, 2014, for a review).

We used IRT to investigate and compare the potential consequences of standing and towering behaviours on the body temperature of two tropical rocky-shore snails, Echinolittorina malaccana (Philippi, 1847) and E. radiata (Souleyet, 1852) (Caenogastropoda: Littorinidae). These two species were chosen as they co-occur in the high-shore zone of Hong Kong where they experience extreme heating, with rock temperature often exceeding 50 °C in summer (Williams, 1994). Field observations were conducted during both Hong Kong's cold, dry winter (4 December 2014) and its hot, wet summer (5–6 August 2014; Kaehler & Williams, 1997) during daytime low tides (i.e. below 1.4 m above CD) when snails were consistently dry and inactive on a semiexposed shore (Lobster Bay, Cape D'Aguilar, Hong Kong). The section of the shore we investigated was a flat rocky platform characterized by a paucity of topographic features such as rock pools, cracks and crevices. The abundance and behaviour of E. malaccana and E. radiata were assessed from 15 haphazardly placed 25 × 25 cm quadrats. All quadrats were placed in the high-intertidal zone, on dry rocks directly exposed to sun, and thermal measurements conducted between 10.00 and 14.00. This procedure ensured the absence of any behavioural difference driven by rock humidity and time of day (see Muñoz et al., 2005). Further, no significant differences were observed in the thermal properties of the quadrats (Kruskal-Wallis test, P > 0.05), with substratum temperatures consistently ranging between 40.5 and 55 °C. The observed postural behaviours included ‘non-standing’ (shell glued to the substratum with its aperture facing the substratum horizontally), ‘standing’ (shell glued to the surface with its aperture facing perpendicularly to the surface, and the major shell axis laying vertically) and ‘towering’ (a snail was attached to the substratum with its aperture facing the substratum either horizontally or vertically and up to three other snails were glued vertically on top of each other to form a stack). ‘Aggregation’ describes an individual in direct shell contact with the shell of at least one other conspecific (Chapperon & Seuront, 2011a, b). Substratum and snail body temperatures (Ts and Tb, respectively) were measured with thermal imaging cameras, a Testo 875-1iSR (Testo AG, Germany) in winter and a Fluke Ti25 (Fluke Corporation, USA) in summer. The thermal performances of cameras are very similar (sensitivities at 30 °C are <0.05 °C (Testo) and ≤0.09 °C (Fluke) and do not vary significantly with temperature (L. Seuront, unpublished data), and accuracy for both is 2% or 2 °C, whichever is greater). Preliminary measurements of various surface temperatures did not exhibit any significant differences in the temperature returned by both cameras. Shell temperature (assessed through IRT) was used as a proxy for snail body temperature (assessed with type K thermocouples inserted into the mantle) as preliminary laboratory trials found no significant differences (P > 0.05) in E. malaccana and E. radiata between shell temperature and mantle temperature, respectively, in the range 25–45 °C. Thermal images were subsequently analysed using IRSoft v. 3.1 (Testo AG, Germany) and SmartView v. 3.2.639.0 (Fluke Corporation, USA). This is consistent with previous work conducted on Littoraria scabra (Chapperon & Seuront, 2011a) and Nerita atramentosa (Caddy-Retalic, Benkendorff & Fairweather, 2011; Chapperon & Seuront, 2011b). The difference, ΔT, between Tb and Ts quantified the difference in temperature between the snail body and its substratum. The ratio RT = Tb/Ts was used as a standardized measure of the difference between substratum and snail body temperatures. Because the variables Tb, Ts, ΔT and RT were non-normally distributed (Kolmogorov-Smirnov test, P < 0.05), nonparametric statistics were used throughout. All pairwise comparisons between species, site and season were conducted using the Wilcoxon-Mann-Whitney U-test. Multiple comparisons between postural behaviours were conducted using the Kruskal-Wallis test, and a subsequent multiple comparison procedure based on the Tukey test was used to identify distinct groups of measurements (Zar, 1999). No significant differences in size were found between species, sites and season (P > 0.05); E. malaccana ranged between 4.2 and 11.9 mm in shell length (N = 232) and E. radiata between 4.5 and 11.8 mm (N = 226).

In winter, E. malaccana and E. radiata were both found on substrata ranging from 17 to 19 °C (Fig. 1). Both species were observed occurring higher on the shore as compared with summer during low tide and aggregating in crevices (Table 1) at densities ranging between 0 and 260 m−2. No postural behaviour was ever observed in either E. malaccana or E. radiata. Body temperatures Tb were significantly positively correlated (Pearson's r, P < 0.01) with substratum temperature Ts in both species. Tb were not significantly different (P > 0.05) from Ts for both species. This resulted in ΔT and RT that were, respectively, not significantly different from 0 and 1 for both E. malaccana and E. radiata (P > 0.05). These results differ from previous winter observations conducted on Nerita atramentosa on South Australian rocky shores (Chapperon & Seuront, 2012). First, N. atramentosa was consistently significantly warmer than its substratum for both solitary (1.21 ± 0.01 °C) and aggregated (1.41 ± 0.02 °C) individuals. This suggests that in contrast to N. atramentosa, E. malaccana and E. radiata may not benefit from direct solar heating in winter, as suggested for E. malaccana with biomimetic models (Marshall & Chua, 2012). Second, our results show that aggregated E. malaccana and E. radiata exhibit similar thermal properties whether they were solitary or aggregated. This suggests that aggregation does not provide any thermal benefit to E. malaccana and E. radiata in winter. This contrasts with previous observations showing that aggregated individuals of N. atramentosa were significantly warmer than their surrounding substratum, with the thermal difference ΔT being c. 2 °C greater for aggregated than solitary individuals (Chapperon & Seuront, 2012).

Table 1.

Absolute and relative frequency of occurrence of different behaviours (solitary, towering and aggregated) and postures (non-standing vs standing) in Echinolittorina malaccana and E. radiata in winter and summer, and the corresponding substratum temperature Ts (°C).

 Season Solitary
 
Towering
 
Aggregated
 
Non-standing Standing T2 T3 T4 T5 Non-standing Standing 
E. malaccana 
N (%) Winter 10 (22.2%) – – – – – 35 (77.8%) – 
 Summer 33 (29.5%) 27 (24.1%) 40 (35.7%) 4 (3.6%) 5 (4.5%) 3 (2.7%) – 
Ts Winter 18.0 ± 1.1a – – – – – 18.0 ± 0.5a – 
 Summer 45.5 ± 1.2a 44.35 ± 0.9a 45.3 ± 1.1a 48.5 ± 1.1b 49.2 ± 1.0c 52.7 ± 1.3d   
E. radiata 
N (%) Winter 9 (17.3%) – – – – – 43 (82.7%) – 
 Summer 22 (20.4%) 34 (31.5%) 26 (24.1%) 7 (6.5%) 6 (5.6%) 2 (1.9%) 7 (6.5%) 4 (3.7%) 
Ts Winter 17.9 ± 0.5a – – – – – 17.3 ± 0.6a – 
 Summer 43.8 ± 1.5a 43.9 ± 1.2a 44.3 ± 0.9a 44.5 ± 1.1a 44.1 ± 1.0a 47.0 ± 0.7b 44.2 ± 0.7a 43.5 ± 0.8a 
 Season Solitary
 
Towering
 
Aggregated
 
Non-standing Standing T2 T3 T4 T5 Non-standing Standing 
E. malaccana 
N (%) Winter 10 (22.2%) – – – – – 35 (77.8%) – 
 Summer 33 (29.5%) 27 (24.1%) 40 (35.7%) 4 (3.6%) 5 (4.5%) 3 (2.7%) – 
Ts Winter 18.0 ± 1.1a – – – – – 18.0 ± 0.5a – 
 Summer 45.5 ± 1.2a 44.35 ± 0.9a 45.3 ± 1.1a 48.5 ± 1.1b 49.2 ± 1.0c 52.7 ± 1.3d   
E. radiata 
N (%) Winter 9 (17.3%) – – – – – 43 (82.7%) – 
 Summer 22 (20.4%) 34 (31.5%) 26 (24.1%) 7 (6.5%) 6 (5.6%) 2 (1.9%) 7 (6.5%) 4 (3.7%) 
Ts Winter 17.9 ± 0.5a – – – – – 17.3 ± 0.6a – 
 Summer 43.8 ± 1.5a 43.9 ± 1.2a 44.3 ± 0.9a 44.5 ± 1.1a 44.1 ± 1.0a 47.0 ± 0.7b 44.2 ± 0.7a 43.5 ± 0.8a 

The symbols Ti indicate the number of snail layers found in a tower, where i = 2 to 5. Note that in the vast majority of observed cases (93.2%) only one snail was found per layer; in 4.7% and 2.1% of the observed towers, we found two and three snails on the second layer (i.e. T2). The ±errors are 95% confidence intervals. The letters a–d identify statistically distinct groups of measurements.

Figure 1.

Body temperature Tb of Echinolittorina malaccana (red) and E. radiata (blue) as a function of their substratum surface temperature Ts in winter (diamonds) and summer (circles). The dashed line is the first bissectrix, Tb = Ts. The insets show a digital image (A) and the corresponding thermal image (B) of a monospecific tower of E. malaccana (left) and a heterospecific tower made of two E. malaccana and one E. radiata at the top (right).

Figure 1.

Body temperature Tb of Echinolittorina malaccana (red) and E. radiata (blue) as a function of their substratum surface temperature Ts in winter (diamonds) and summer (circles). The dashed line is the first bissectrix, Tb = Ts. The insets show a digital image (A) and the corresponding thermal image (B) of a monospecific tower of E. malaccana (left) and a heterospecific tower made of two E. malaccana and one E. radiata at the top (right).

In summer, both E. malaccana and E. radiata were found on surfaces with temperatures, respectively, in the range 40.5 to 54.5 °C, and 42.3 to 52.0 °C (Fig. 1; Table 1) and at densities ranging between 0 and 320 m−2 for E. malaccana and 0 and 224 m−2 for E. radiata. Echinolittorina malaccana was not observed in aggregation and this rarely occurred in E. radiata (Table 1). Note that dense aggregations of both species were, however, not uncommon during low tide in summer (Stafford, davies & williams, 2007), which suggests temporal variations in the behaviour. The observed behavioural properties were not equally likely (χ2 tests, P < 0.01). Specifically, non-standing, standing and towering snails represented 29.5, 24.1 and 46.4% of postural behaviours in E. malaccana, and 20.4, 31.5 and 38.1% in E. radiata (Table 1). No significant correlation was found between snail density and any of the observed behavioural properties for both species (P > 0.05). This suggests that tower formation is not related to any density-dependent effect.

The observed towers included two to five layers of snails. In the vast majority of cases (93.2%), only one snail was found per layer. Layers made of two or three snails also occurred however, in 4.7% and 2.1% of observed towers, respectively. These snails were consistently found on the second layer of towers. Towers were either monospecific or heterospecific. Heterospecific towers (Fig. 1) occurred occasionally, representing 3.4% of the observed towers. The size of snails consistently decreased from the bottom to the top of a tower in 96.2 and 97.6% of the towers observed in E. malaccana and E. radiata, respectively, and in 100% of the heterospecific towers. Towers of two snails were by far the most abundant (Table 1).

Substratum temperatures Ts significantly differ between E. malaccana behavioural groups (P < 0.05; Table 1). Specifically, in E. malaccana non-standing, standing snails and snail towers including less than three snails were found on surfaces with not significantly different temperatures Ts (P > 0.05). These substrata were significantly cooler (P < 0.05) than substrata holding towers of three to five individuals. These towers were found on significantly increasingly hot surfaces (P < 0.05). Noticeably, Ts did not significantly differ between solitary (either non-standing or standing) E. radiata, and E. radiata in towers of up to four individuals (Table 1). In turn, towers of five snails and both non-standing and standing snails in aggregates were found on significantly warmer surfaces (P < 0.05). As observed in winter, Tb were significantly positively correlated (P < 0.01) with Ts for both species. However, Tb were significantly cooler than Ts for both species (P < 0.05), with the difference ΔT ranging on average between 2.6 and 10.3 °C for E. malaccana, and between 2.7 and 7.8 °C for E. radiata, depending on snail postural behaviour (Table 2). Similarly, RT was between 0.94 and 0.80 in E. malaccana and 0.94 and 0.83 in E. radiata (Table 2). The temperature difference ΔT and temperature ratio RT, respectively, significantly decreased and increased from non-standing to standing snails, and with the elevation of a snail in a tower (Table 2). No correlation was found between snail size and any of the thermal properties investigated here, irrespective of the elevation of a snail in a tower (P > 0.05). These observations show that the behaviourally-induced cooling effect consistently increases with the vertical distance to the substratum, irrespective of snail size. The reported changes in postural behaviour are hence likely to reduce convective heat gain from the substratum, while improving convective cooling, and stress the thermal advantages of both standing and towering behaviours (Marshall et al., 2010b; Marshall & Chua, 2012).

Table 2.

Thermal properties of Echinolittorina malaccana and E. radiata in summer for different behaviours (solitary, towering and aggregated) and postures (non-standing vs standing).

 Solitary
 
Towering
 
Aggregated
 
Non-standing Standing Tbns Tbs T1 T2 T3 T4 Non-standing Standing 
E. malaccana 
Tb 41.0 ± 1.7 39.6 ± 1.0 39.7 ± 0.7 40.3 ± 2.1 38.7 ± 1.7 39.4 ± 1.5 37.5 ± 0.6 38.2 ± 0.4 – – 
 DT 2.6 ± 1.2 4.1 ± 1.3 2.81 ± 1.0 4.05 ± 1.3 5.8 ± 1.6 6.9 ± 1.0 7.9 ± 1.7 10.3 ± 1.1 – – 
RT 0.94 ± 0.02 0.91 ± 0.03 0.94 ± 0.02 0.91 ± 0.03 0.87 ± 0.03 0.88 ± 0.02 0.86 ± 0.03 0.80 ± 0.02 – – 
E. radiata 
Tb 42.8 ± 2.5 40.2 ± 1.7 41.3 ± 0.9 41.7 ± 3.1 39.5 ± 2.5 42.6 ± 3.8 42.2 ± 3.1 42.4 ± 3.0 40.3 ± 0.9 39.4 ± 1.1 
 DT 2.7 ± 1.0 4.3 ± 1.3 4.6 ± 0.8 4.2 ± 1.4 5.7 ± 1.4 5.7 ± 1.5 6.5 ± 0.7 7.8 ± 1.2 3.9 ± 0.6 4.1 ± 1.1 
RT 0.94 ± 0.02 0.90 ± 0.03 0.90 ± 0.02 0.91 ± 0.03 0.87 ± 0.03 0.88 ± 0.03 0.85 ± 0.02 0.83 ± 0.02 0.91 ± 0.01 0.91 ± 0.03 
 Solitary
 
Towering
 
Aggregated
 
Non-standing Standing Tbns Tbs T1 T2 T3 T4 Non-standing Standing 
E. malaccana 
Tb 41.0 ± 1.7 39.6 ± 1.0 39.7 ± 0.7 40.3 ± 2.1 38.7 ± 1.7 39.4 ± 1.5 37.5 ± 0.6 38.2 ± 0.4 – – 
 DT 2.6 ± 1.2 4.1 ± 1.3 2.81 ± 1.0 4.05 ± 1.3 5.8 ± 1.6 6.9 ± 1.0 7.9 ± 1.7 10.3 ± 1.1 – – 
RT 0.94 ± 0.02 0.91 ± 0.03 0.94 ± 0.02 0.91 ± 0.03 0.87 ± 0.03 0.88 ± 0.02 0.86 ± 0.03 0.80 ± 0.02 – – 
E. radiata 
Tb 42.8 ± 2.5 40.2 ± 1.7 41.3 ± 0.9 41.7 ± 3.1 39.5 ± 2.5 42.6 ± 3.8 42.2 ± 3.1 42.4 ± 3.0 40.3 ± 0.9 39.4 ± 1.1 
 DT 2.7 ± 1.0 4.3 ± 1.3 4.6 ± 0.8 4.2 ± 1.4 5.7 ± 1.4 5.7 ± 1.5 6.5 ± 0.7 7.8 ± 1.2 3.9 ± 0.6 4.1 ± 1.1 
RT 0.94 ± 0.02 0.90 ± 0.03 0.90 ± 0.02 0.91 ± 0.03 0.87 ± 0.03 0.88 ± 0.03 0.85 ± 0.02 0.83 ± 0.02 0.91 ± 0.01 0.91 ± 0.03 

Tbns and Tbs: non-standing and standing snails found at the bottom of a tower; T1, T2, T3 and T4: standing snails found on 1st, 2nd, 3rd and 4th levels of a tower, respectively. The ±errors are 95% confidence intervals.

The temperature differences ΔT reported here are much larger than those estimated from aestivating Nodilittorina pyramidalis and Austrolittorina unifasciata (respectively, 0.10 ± 0.61 and 0.71 ± 0.98 °C for non-standing and standing individuals; Lim, 2008); these species do not form towers, however, even at substratum temperatures that are suggested to trigger towering behaviour in E. malaccana and E. radiata (Lim, 2008; L. Seuront, unpublished data). Further, the RT values reported in the present work are consistently smaller than previous estimates obtained under similar conditions of heat stress from Littoraria scabra in a Fijian mangrove (RT in the range 0.99–1.01; Chapperon & Seuront, 2011a) and Nerita atramentosa on South Australian rocky shores (RT in the range 1.00–1.15; Chapperon & Seuront, 2011b; Chapperon, le Bris &Seuront, 2013); these species do not exhibit any postural behaviour, but instead select thermally favourable microhabitats (Chapperon & Seuront, 2011a, b; Chapperon et al., 2013). To our knowledge, the only attempt to link substratum temperature and postural behaviour mechanistically in an intertidal gastropod showed that E. malaccana standing behaviour was triggered by the presence of a temperature gradient in the boundary layer air above the solar-heated rock surface, but was not observed when snails were heated in the absence of this gradient (Marshall & Chua, 2012). While this is at best speculative, the measured very hot substratum temperature and the absence of wind during our observations were compatible with the presence of a thermal gradient in the boundary layer air. Such a gradient would typically favour larger snails (Marshall & Chua, 2010b), though no significant differences in size were found between non-standing and standing solitary snails (P > 0.05). In turn, since heat transfer is inversely proportional to size in both stagnant and moving air (see, e.g. Denny, 1993), small individuals would theoretically benefit from a higher position in a tower. This observation is consistent with the fact that all observed towers were formed of snails of decreasing size from bottom to top. Furthermore, even if towering behaviour has been suggested to be rather incidental (Marshall et al., 2010b) and to result from trail-following at benign temperatures (Marshall & Chua, 2012), the frequency of the observed postural behaviours, their links to substratum temperature and their clear effects on snail body temperature are all in favour of an adaptive behaviour driven by selection.

This work uniquely used infrared thermography—a still relatively novel method in molluscan research (see Lathlean & Seuront, 2014)—to reveal unexpected differences in the behavioural ecology and thermal biology of two species of snails co-occurring in a topographically simple though thermally extreme environment, which may suggest niche differentiation. Our results also show that E. malaccana and E. radiata are very well adapted to heat stress among littorinids in particular, and intertidal gastropod in general. There is a need to identify the spectrum of behavioural strategies available to various species (e.g. posturing, aggregation and habitat selection) to reach a better understanding of how high-shore gastropods may face climate variability in an era of global change.

We thank the Agriculture, Fisheries and Conservation Department of the Hong Kong SAR Government for the permission to work at the Cape D'Aguilar Marine Reserve (Permit No.: (107) in AF GR MPA 01/5/2 Pt.15). The Testo thermal camera was funded by the Small Project Fund (Grant No.: 201309176082) from The University of Hong Kong. L. Seuront was financially supported by a Bonus Qualité Recherche (BQR) International from the University of Lille 1 – Sciences and Technologies (France). Prof. Mark Davies and two anonymous referees are acknowledged for their constructive comments and suggestions on a previous version of this work. Prof. Davies is acknowledged for his contribution in improving the language of the manuscript.

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