Behavioural adaptation to heat stress: shell lifting of the hermit crab Diogenes deflectomanus

Highlights

• Tropical sandy shore habitats reach thermally stressful temperatures for species.

• During emersion sandy-shore hermit crabs exhibit “shell lifting” behaviour.

• This behaviour may reduce conductive and radiative heat gain.

• Shell-lifting reduced body temperatures 10 °C lower than crabs' physiological limits.

• This behaviour buffers against extreme thermal conditions on tropical shores.

Abstract

Behavioural responses to heat and desiccation stress in ectotherms are crucial for their survival in habitats where environmental temperatures are close to or even exceed their upper thermal limits. During low tide periods when pools in intertidal sediments heat up, a novel shell lifting behaviour (when hermit crabs crawl out of pools and lift up their shells) was observed in the hermit crab, Diogenes deflectomanus, on tropical sandy shores. On-shore measurements revealed that the hermit crabs left pools and lifted their shells predominantly when pool water exceeded 35.4 °C. Standing on emersed substrates above the pool water, the hermit crabs maintained their body temperatures at 26 – 29 °C, ∼ 10 °C lower than temperatures at which their physiological performances (as measured using heart rate) reached the maximum. This mismatch between preferred body temperatures and temperatures at maximal physiological performance was also observed under a laboratory controlled thermal gradient, where hermit crabs spent more time at 22 – 26 °C as compared to > 30 °C. These behaviours suggest a thermoregulatory function of the shell lifting behaviour, where the hermit crabs can avoid further increase in body temperatures when pools heat up during low tide periods. Such a behavioural decision allows the hermit crabs to be less prone to the strong temporal fluctuation in temperatures experienced during emersion periods on thermally dynamic tropical sandy shores.

Introduction

The physiological performance of ectotherms is dependent on their body temperatures which are closely linked to environmental conditions (Angilletta, 2009). Since experienced thermal conditions can vary over short spatial and temporal scales in highly dynamic environments, many ectotherms demonstrate morphological, physiological and/or behavioural strategies to maintain their body temperatures and avoid lethal thermal extremes (Angilletta, 2009; Clusella-Trullas et al., 2011; Huey and Kingsolver, 1989; Huey and Stevenson, 1979). In intertidal habitats, with strong variations and extremes in environmental temperature due to the tidal cycle, the evolution of adaptive, thermoregulatory behavioural responses is crucial for ectotherms to ensure normal metabolic functioning, body muscle coordination and ultimately survival (Bertness, 1981b; Crickenberger et al., 2020; Garrity, 1984; Hui et al., 2019; Williams et al., 2005).

Sandy shores are highly dynamic environments with constant changes in physical conditions such as tide, wind and wave action (Brown and McLachlan, 2002). In terms of thermal environment, sandy shores in the tropics are one of the most challenging habitats for the survival of intertidal ectotherms since the sediment surface can heat up rapidly when the tide recedes and can reach temperatures exceeding species’ thermal limits (Hui et al., 2019; Macintosh, 1978). Hermit crabs, which are common detritivores foraging on sediment surfaces and in tide pools during low tides (Bertness, 1981a; Scarratt and Godin, 1992), have both morphological and behavioural adaptations to survive the highly variable physical conditions, particularly during tidal emersion (Reese, 1969; Taylor, 1981). Although some hermit crabs are able to maintain water in their shells to remain hydrated and buffer temperature increase when they are directly exposed to sunlight during emersion (Becchi et al., 2015), behavioural responses in terms of posture or changing microhabitat are often more effective as that would allow individuals to modify their experienced thermal conditions (Becchi et al., 2015; Sunday et al., 2014). Examples of behavioural responses of hermit crabs include withdrawing bodies into their shells, burrowing into the sediments and aggregating underneath boulders or vegetation (Burggren and McMahon, 1981; Rebach, 1974; Reese, 1969; Taylor, 1981; Turra and Denadai, 2002). Whilst hiding in shade underneath boulders or vegetation already enables the hermit crabs to experience cooler and more humid environments, aggregation may further buffer body temperature changes as observed in other intertidal ectotherms (such as littorinids, trochids etc.; Chapman and Underwood, 1996; Snyder‐Conn, 1981; Turra and Leite, 2000; Warburg and Shuchman, 1984). A tight “tide-following” behaviour is also evident in some hermit crabs where foraging individuals move with the tide as it recedes (Gherardi et al., 1990; Rittschof et al., 1995), allowing the crabs to stay moist and minimize the time spent feeding/moving on dry, high shore sediments during low tide periods (Burggren and McMahon, 1981; Turra and Denadai, 2002). This suite of multiple behaviours has been proposed to be critical for hermit crabs to respond rapidly to short-term environmental changes and survive the highly variable, and potentially lethal, thermal environments on sandy shores (Reese, 1969; Taylor, 1981).

A novel behaviour, “shell lifting”, has been observed in the hermit crab, Diogenes deflectomanus Wang & Tung 1980, in Hong Kong. During low tide periods, D. deflectomanus stands on small objects such as oyster shells, cobbles, or rock pieces to elevate itself from moist/waterlogged sediments, typically shallow tide pools. In this position the hermit crab can lift its body to orientate its shell towards the sky and, by holding onto small objects, remain stationary during low tide (Fig. 1). On-shore observations suggest that the hermit crabs are more likely to practice this shell lifting behaviour during hot as compared to cloudy/overcast days, and similar standing behaviour in rocky shore littorinids has been suggested to be thermoregulatory by enhancing convection and reducing conduction from the hot substrate (Lim, 2008; Seuront and Ng, 2016). Accordingly, we hypothesized that this novel shell lifting behaviour could serve a thermoregulatory function to buffer body temperature changes under the variable thermal environment during low tide periods. To test this hypothesis, we quantified the relationship between shell lifting behaviour and body temperature of D. deflectomanus, and how body temperatures attained during shell lifting/non-shell lifting affected the physiological performances of the hermit crabs. We further measured thermal preference of the hermit crabs to evaluate the relevance of shell lifting behaviour in terms of maintaining preferred body temperatures. By combining these physiological and behavioural measurements we evaluated whether shell lifting behaviour can effectively contribute to thermoregulation in D. deflectomanus, and thus provides a novel means for hermit crabs to survive thermal stress during low tide periods on tropical sandy shores.