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Environmental temperature influences a variety of organismal processes in ectotherms, including growth, reproduction and survival (Hochachka & Somero 2002). Because body temperature is often a strong correlate of fitness (Huey & Berrigan 2001), organisms have evolved a variety of strategies for regulating their body temperatures. In ectotherms, these strategies fall into three broad categories: behavioural regulation, physiological regulation and morphological regulation. Behavioural options such as movement (active microhabitat selection) and body reorientation are effective means of avoiding potentially damaging body temperatures, and these strategies are commonly used by a variety of ectotherms (Heath 1970). To achieve physiological regulation, animals can alter metabolic rate, heart rate and the flow of blood towards or away from heat sources or sinks (Seebacher & Franklin 2005). Morphological regulation refers to non-behavioural changes in an organism's overall appearance (broadly defined to include both shape and colour), which can influence rates of heat gain and heat loss (e.g., Vermeij 1973; Etter 1988).
Although behavioural and physiological mechanisms of body temperature control are better studied than morphological mechanisms, many of the sessile and slow-moving invertebrate ectotherms that predominate on intertidal shores may be unable to effectively utilize them. For these species, behavioural strategies such as microhabitat selection often cannot be employed over relevant time scales (e.g. over the course of a 6-h low tide). Even behavioural control of evaporative cooling [e.g., gaping in barnacles and bivalves, raising of the shell (mushrooming) in limpets] may be of little consequence in typically small-bodied intertidal animals with limited reservoirs of water (Denny & Harley 2006). The small size of most intertidal animals may also preclude meaningful thermal control via reductions in metabolic rate and shifting patterns of blood flow. Thus, many intertidal species may emphasize morphological strategies to influence their body temperatures.
Adaptation to thermal stress is particularly important on rocky intertidal shores, where substratum temperatures can increase from 10 °C (sea water temperature) to over 40 °C during a single low tide on temperate shores (Harley & Helmuth 2003) and exceed 50 °C on tropical shores (Williams & Morritt 1995). Thermal stress can result in dramatic mortality events via direct impacts on individual organisms (Frank 1965; Sutherland 1970; Tsuchiya 1983). Thermal stress may also lead to mortality indirectly via increased susceptibility to predators (e.g., Frank 1965) and disease (Harvell et al. 2002). Finally, sublethal thermal stress can reduce fitness by incurring physiological costs associated with protection and repair of cellular components (Somero 2002). Given the limitations of behavioural and physiological stress avoidance mechanisms, there may be important temperature-related selection on organismal morphology on rocky shores.
Intertidal limpets are an excellent model system for addressing the role of morphology in moderating thermal stress. All limpet shells are variations on a simple geometric shape – the cone. However, within this conical theme, there is broad variation in shell size, the shape of the aperture, the height : length ratio, and architectural features on the shell's surface. Some aspects of shell morphology appear to correspond to the limpet's thermal environment. For example, Patella vulgata and P. aspera living high on the shore tend to be higher spired than conspecifics living lower on the shore (Orton 1933; Ebling et al. 1962). Shell morphology is plastic in this genus, and P. vulgata transplanted from warmer microhabitats to a cooler microhabitat exhibited a change in their pattern of shell growth from high-spired to low-spired (Moore 1934). Among-species patterns of shell morphology are also apparent; generally speaking, high-shore and tropical limpet species tend to have higher spires and more shell architecture (ridges, etc.) than low-shore and temperate species (Vermeij 1973).
Vermeij (1973) hypothesized that these morphological characteristics were adaptations to thermally stressful conditions. For a limpet of a given volume, an individual with a taller shell will have a smaller area in contact with the substratum, thus reducing conduction when the limpet is sitting on a hot surface. Relatively tall shells may also project up into faster wind velocities, facilitating convective cooling. The addition of bumps, ridges, or other features on the shell will increase convective surface area and increase the rate at which excess heat is lost via convection (Johnson II 1975). Although these hypotheses are intuitive, the actual thermal significance of morphological variation in limpets has not been rigorously tested.
In this study, we investigate the relationship between limpet shell morphology and body temperature during aerial exposure at low tide. We compare three species that differ in both thermal niche and in morphological characteristics: Lottia gigantea, P. vulgata, and Siphonaria gigas. L. gigantea is very low-spired and lacks architectural features on the shell (Fig. 1). Patella vulgata and S. gigas are both high-spired, but they differ in shell architecture. Whereas P. vulgata possesses small and in many cases very faint radial ridges, S. gigas may possess dramatic raised ridges that run from the apex down the length of the shell (Fig. 1). The use of these three species allowed us to explicitly analyze the effectiveness of two morphological strategies: increased spire height, and architectural features that increase shell surface area. We used the morphological characteristics of these three species to parameterize a recently developed heat budget model (Denny & Harley 2006) and thereby to determine the importance of various morphological attributes in controlling predicted body temperature.
Figure 1. Photograph of representative shell morphologies for Lottia gigantea (left), Patella vulgata (centre), and Siphonaria gigas (right). The upper panel is the dorsal view, and the lower panel is the posterior view. Scale bar = 2 cm.
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