TY - JOUR
AU1 - Seuront, Laurent
AU2 - Ng, Terence P T
AU3 - Lathlean, Justin A
AB - Abstract In an era of global change, thermal biology and ecology are becoming increasingly popular topics in invertebrate research, including molluscs. However, this area of research is still very limited, essentially due to the intrinsic spatial limitations of traditional single-point temperature measurements (e.g. thermocouples, iButtons and infrared thermometers). This is not the case, however, with infrared thermography, which has the desirable attribute of producing images that allow for simultaneous measurements of multiple molluscan individuals, species and communities. Infrared thermography allows for spatial and temporal monitoring of microclimates at scales relevant to individual organisms and hence may represent a first step to bridge the gap between field-based approaches (typically spanning from centimetres to tens of metres) to climatic scenarios (typically coarse-grained, i.e. 10 × 10 km). This review first provides a brief history of infrared thermography, followed by a description of the fundamental physical properties and quantities that bridge the gap between the physics of heat transfer and the physics of infrared thermography. We then thoroughly review the thermal biology and ecology of molluscs, and the previous biological and ecological applications of infrared thermography—including the very few in molluscan research. We provide detailed recommendations related to the proper use of infrared thermography. Finally, we discuss the potential applications of infrared thermography in molluscan research, based on case studies involving both terrestrial and intertidal molluscs, with emphasis on its use as a tool for monitoring impacts of climate change. THERMAL BIOLOGY AND ECOLOGY IN A CHANGING WORLD As stated by Angilletta (2013: 1) in his seminal book “unlike many other variables that concern biologists, temperature is not just a property of life; it is a property of matter. Nothing escapes its control.” Temperature indeed controls the individual metabolism and performance that ultimately determine fitness of organisms, structure of populations and function of ecosystems (Huey & Berrigan, 2001; Deutsch et al., 2008; Angilletta, 2013). The effect of temperature on temporal patterns of growth, survival and reproduction has been widely demonstrated in almost all phyla (Kingsolver, 2009; Kingsolver, Diamond & Buckley, 2013). Yet temperature does not affect different organisms equally (Somero, 2010) and does not affect the same organism equally at all stages of its life cycle (Pörtner & Farrell, 2008). Furthermore, organisms do not experience the same level of exposure to temperature at niche and ecosystem levels (Helmuth et al., 2010). In an era where ecosystems are increasingly threatened by anthropogenic climate change, through the increase in both mean temperature and its variability (Walther et al., 2002; Parmesan, 2006), Angilletta’s statement becomes increasingly pertinent in research fields associated with thermal biology and ecology. Shifts in phenology and geographic ranges of species, disruptions of ecological interactions, and changes in biodiversity and productivity driven by climate change have now been widely reported in both terrestrial and marine systems (see Beaugrand, 2015, for a recent review on marine ecosystems). However, the mechanistic links between environmental variables and body temperatures of ectotherms that control local (Miller, Harley & Denny, 2009) and global distribution patterns of organisms (Helmuth et al., 2002) seem to be much more complex than previously anticipated (Helmuth et al., 2011, 2014). The body temperatures of both terrestrial and marine ectotherms are determined by heat fluxes from and towards the organisms (Gates, 1980; Harley et al., 2009). These fluxes are controlled by the interactions between climatic factors such as air and water temperatures (Helmuth, 2002; Vidal et al., 2010), nonclimatic heat sources such as solar irradiance and geothermal heating (Marshall, McQuaid & Williams, 2010), and biotic factors such as morphological and behavioural traits (Miller & Denny, 2011). Thermal conditions experienced by ectothermic organisms are thus determined by a multitude of factors, which often vary at fine spatial (metres) and temporal (minutes) scales, resulting in complex patterns in body temperatures (Helmuth et al., 2002; Woods, Dillon & Pincebourde, 2014). In fact, fine-scale thermal variations in body temperatures of ectotherms often exceed those observed between latitudes in both terrestrial (Deutsch et al., 2008; Angilletta, 2013; Potter, Woods & Pincebourde, 2013) and marine systems (Helmuth et al., 2006; Denny et al., 2011; Meager, Schlacher & Green, 2011). In a warming climate, ectothermic organisms, therefore, face the challenge to maintain their body temperatures at preferred ranges within their thermal tolerance windows by responding to heat stress over a range of (1) temporal scales spanning from minutes to generations (Barnes et al., 2006; Bradshaw & Holzapfel, 2006) and (2) spatial scales ranging from small-scale habitats to large-scale geographic distances (Osovitz & Hofmann, 2007; Denny et al., 2011; Stafford et al., 2015). In this context, measuring temperature, a priori an apparently simple task, is in fact particularly challenging as the understanding of the effect of both hydroclimatic variations and climate change on ectothermic organisms de facto requires information on the temperatures of both the environment and the organisms at temporal scales ranging from minutes to decades and spatial scales ranging from centimetres to thousands of kilometres. This complexity is emphasized by recent evidence that latitudinal patterns of both acute and chronic heat stress may be decoupled from average temperatures, which are typically assumed to decline with increasing latitude (Lathlean, Ayre & Minchinton, 2014). Traditionally, environmental and organismal temperatures have been measured using a range of data loggers (e.g. TidBit, iButton; Angilletta & Krochmal, 2003; Davis, Taylor & Denardo, 2008; Janisch, Wondzell & Ehinger, 2012), thermocouples (Iacarella & Helmuth, 2011) and biomimetic loggers (Lima & Wethey, 2009; Lathlean et al., 2014; Helmuth et al., 2016). All these devices, however, share intrinsic limitations that prevent them from providing synoptic information on both environmental and organismal temperatures at the high spatial resolutions needed to capture small and broad-scale patterns of heat stress (Osovitz & Hofmann, 2007; Denny et al., 2011; Lathlean, Ayre & Minchinton, 2014). Data loggers allow single-point measurements that are limited by their battery life and the very high costs that would be associated with any attempt to cover large distances or surfaces at a spatial resolution compatible with the biology and ecology of individual organisms. Both wired thermocouples (contact or tissue-penetrating) and infrared thermocouples are essentially point measurements of body surfaces, and hence only appropriate for organisms with a limited mobility (Etter, 1988; Helmuth, 1999). Biomimetic loggers, even if they have been developed to match the thermal properties of a range of target organisms (Lima & Wethey, 2009; Szathmary, Helmuth & Wethey, 2009; Lima et al., 2011; Seabra et al., 2011; Lathlean et al., 2014), cannot take into account behavioural thermoregulation (Muñoz et al., 2005; Dubois et al., 2009) or behaviourally-driven selection of thermal refuges (Chapperon & Seuront, 2011a, b). Simultaneous high-resolution measurements of both environmental and organismal temperatures are, however, achievable with infrared thermography if appropriate conditions are met (see below). Here, we first provide a brief history of infrared thermography. We next describe the fundamental physical principles behind infrared thermography and provide an overview of its importance to studies of the biology and ecology of molluscs. The general applications of infrared thermography to a range of physiological, biological and ecological questions are briefly considered. We then thoroughly review the thermal biology and ecology of molluscans, and the previous applications of infrared thermography to their study, including the still very limited amount of published information on the use of thermal imaging. We provide detailed recommendations for the proper use of infrared thermography. Finally, we consider promising areas for the future applications of infrared thermography in molluscan research, in particular in the context of climate change. These areas are illustrated using recent published and unpublished data taken from a wide range of environments and latitudes, to ensure a broad perspective. A BRIEF HISTORY OF INFRARED THERMOGRAPHY Even though no temperature-sensing device in a strict sense was available until the so-called Galileo thermometer in c. 1603 (Loyson, 2012), the ancient Egyptians had an intuitive knowledge of heat radiating from the human body. As reported by Herodotus (484–425 BC), they moved their hands across the surface of the body to scan and evaluate changes in temperature (Herodotus, 1954). Temperature changes were either localized to a specific area or detected over the entire body (Nunn, 2002; Allen & Mininberg, 2005). The ancient Egyptian practice was formalized in 400 BC by the Greek physician Hippocrates (460–370 BC), who wrote that “in whatever part of the body excess of heat or cold is felt, the disease is there to be discovered” (Diakides, Bronzino & Peterson, 2012: 132). The ancient Greeks covered the body in wet mud and the area that dried most quickly indicated the warmest region, and was considered the diseased part (Hodge, 1994). Hippocrates is even credited with describing an early version of a two-dimensional skin temperature-measuring device: a moist linen cloth covering an area of skin to produce an impression of surface temperatures by means of the change in cloth colour (Otsuka & Togawa, 1997). Infrared radiation remained scientifically unknown until William Herschel (1738–1822) studied the heating effect of different colours of light. Building on Newton’s discovery that visible light could be refracted into distinct colour bands, Herschel used a prism to produce a spectrum of colours and measured their heating effect with thermometers (Fig. 1A). He discovered that this effect increased on moving from the blue to the red end of the spectrum. He also noticed that the ‘dark light’ just beyond the range of visible red also produced heat, providing the first evidence for an infrared form of light in part of the electromagnetic spectrum invisible to the human eye (Rogalski, 2012). This radiation, called ‘dark heat’ or ‘calorific rays’ (Herschel, 1800), can be reflected, absorbed and transmitted just like visible light (Barr, 1960, 1961), providing the first evidence for a thermal form of electromagnetic radiation (Rogalski, 2012). The visible light spectrum (as detected by the human eye under daylight conditions) is restricted to a narrow range of wavelengths (0.39–0.78 μm). In turn, the spectrum of infrared radiation ranges from 0.78 μm (i.e. just beyond the visible range) up to a wavelength of 1,000 μm (i.e. close to microwaves; Fig. 1B). The wavelength of infrared radiation utilized by infrared cameras ranges from 0.78 to 14 μm (Kastberger & Stachl, 2003) and can be subdivided into near-infrared (NIR; 0.78–1.7 μm), short-wavelength infrared (SWIR; 1–2.5 μm), mid-wavelength infrared (MWIR; 2–5 μm) and long-wavelength infrared radiations (LWIR; 8–14 μm). Of these four wavelength ranges, SWIR and especially NIR should not be considered as thermal bands in a strict sense, since they are close to the visible spectrum and share some of its properties (Vollmer & Möllmann, 2010). Figure 1. Open in new tabDownload slide A. Experiment conducted by William Herschel (1738–1822) to demonstrate that the heating effect of the different colours of the visible spectrum increases from the blue end of the spectrum to the red (modified from Herschel, 1800). B. Schematic representation of the spectrum of electromagnetic radiation. MWIR and LWIR are the most commonly used bands in infrared thermography (Usamentiaga et al., 2014). Infrared cameras operating in the MWIR and LWIR regions of the spectrum are typically used for high and ambient temperature measurements (Usamentiaga et al., 2014). Most thermal infrared cameras used in biological applications operate within the LWIR region, often referred to as the ‘thermal infrared range’ (Kastberger & Stachl, 2003; Lathlean & Seuront, 2014; Tattersall, 2016). LWIR cameras are preferred in biological applications as they are less influenced by the presence of moisture than MWIR cameras (Usamentiaga et al., 2014) and because they are more affordable, portable and rugged (Lathlean & Seuront, 2014). Note, however, that MWIR cameras are less influenced by optical and electronic noise, and hence offer detection performances superior to those of LWIR cameras due to a reduced signal-to-noise ratio; in other words they typically make up for their reduced radiance detection by a much better detection accuracy (Usamentiaga et al., 2014; see Jorge Aldave et al., 2013, for a review of the relative performances of MWIR and LWIR cameras). The signal-to-noise ratio, however, depends also on the sensitivity of the infrared detector, which can either be cooled or uncooled. Cooled infrared cameras are designed to maximize detection performance through the incorporation of a cryogenic cooling system that reduces the internal temperature of the imaging sensor to much below ambient, in order to reduce the thermal noise induced by the camera components and the infrared sensor itself. These devices allow the detection of thermal radiation with an accuracy as fine as 0.025 °C (Usamentiaga et al., 2014). Uncooled cameras, though less accurate, are generally preferred in biological applications (Kastberger & Stachl, 2003) as, without a cryogenic cooler, they are again more affordable, portable and rugged than cooled ones (Lathlean & Seuront, 2014). As an example, a cooled MWIR camera will offer superior performance with respect to an uncooled LWIR detector, even in the 15–55 °C range. The pioneering work of Herschel led ultimately to the development of infrared sensors essentially used as thermal detectors (such as thermocouples and bolometers), which are still used today, and to the more sensitive and faster photon detectors. Thermal detectors were extensively developed in the 20th century, driven by military applications. The first bolometers were used for the remote detection of people (up to 200 m) and aircraft (up to 1,000 m) in 1914, the first infrared image converter in 1934 and infrared display units in 1939. The origin of modern infrared technology was rooted in the research and development effort conducted during World War II, followed by the ever-growing development of high-performance sensors, which have been extensively used for military, industrial and medical applications (see Biberman & Sendall, 2000; Vollmer & Möllmann, 2010; Rogalski, 2012, for reviews). Infrared thermography now allows noninvasive and real-time visualization of fixed or transient changes in the long-wave radiant energy emanating from an object, hence allowing for the estimation of surface temperature of various substrata and organisms. Recent technological advances in thermal-imaging cameras (i.e. smaller size, reduced power requirements, and increased portability, ruggedness, resolution and sensitivity, together with a significant reduction in cost) have facilitated and expanded their use (Zalameda & Winfree, 2005; Lathlean & Seuront, 2014). This technology is particularly appealing in the research fields of thermal biology and ecology, landscape ecology, behavioural ecology and physiology, as it allows noninvasive measurements of surface temperature patterns over a very broad range of scales—ranging from ocean basins and continents (Kerr & Ostrovsky, 2003) to landscapes (Scherrer & Körner, 2010; Faye et al., 2016; Faye, Dangles & Pincebourde, 2016) and individual organisms (Tattersall & Cadena, 2010; Pincebourde, Sanford & Helmuth, 2013; Tattersall, 2016). More detailed reviews of the history of the discovery of the infrared portion of the light spectrum and its major players, and the subsequent evolution of infrared detectors, have been given by Barr (1960, 1961, 1962), Hudson (2006) and Rogalski (2012). FROM THE PHYSICS OF HEAT TRANSFER TO THE PHYSICS OF INFRARED THERMOGRAPHY Heat is transferred by three mechanisms: radiation, conduction and convection. This is critical to understanding the physics of infrared imaging, as well as the thermal biology and ecology of ectotherms in general and molluscs in particular, because rates of both body heating and cooling fundamentally drive organismal energy budgets (Angilletta, 2013). These mechanisms and the fundamental physical laws that drive them are therefore briefly described. Readers interested in reaching a deeper understanding of the physics of thermal radiation and heat transfer are referred to Incropera et al. (2006) and Sundén (2012) for an introduction to these topics, and Ghoshdastidar (2012), Hahn (2012), Bejan (2013), Modest (2013), Balaji (2015), Howell, Mengüç, and Siegel (2015) and Stewart & Johnson (2016) for details of the physics and related computational tools. Radiation Both inanimate and animate objects with a temperature above absolute zero (i.e. –273.15 °C) emit thermal energy as a result of molecular motion. In addition, the main source of heat experienced on Earth comes from the sun’s electromagnetic radiation, which transmits a fraction of its energy flux in the form of infrared radiation to Earth’s atmosphere, water bodies and land masses (Phillips, 1995). All objects emit an energy flux ϕ. This flux of energy is detected by infrared or thermal cameras and converted to images called ‘thermograms’ (Fig. 2). By inducing a gradient of heat across the surface of a thin oil film, William Herschel showed that a visual interference pattern could be revealed by differential rates of evaporation, thereby producing the first visualization of temperature on a surface (Rogalski, 2012). To explain the relatively complex physics behind the use of a thermogram to estimate an object’s temperature at a distance, we provide a short primer of essential concepts such as black-body radiation, Wien’s displacement law of electromagnetic radiation, Kirchhoff’s radiation law, the Stefan-Boltzmann law and emissivity, which need to be understood in order to conduct thermal measurements and interpret the subsequent thermograms reliably. Black body radiation and Planck’s law A ‘black body’ is an ideal object that completely absorbs all the electromagnetic radiation that it receives at every wavelength. Note that the term ‘black’ does not refer to the colour of an object; rather, it describes how a black body behaves similarly with respect to all wavelengths. In fact, no objects in nature are true black bodies, because all objects emit electromagnetic radiation in part of the electromagnetic spectrum, dependent on their temperature. This concept is central to understanding how thermal imaging operates. It is summarized in Planck’s law, which defines the spectral radiance of the electromagnetic radiation I(λ,T) emitted by a black body in thermal equilibrium at a given temperature T as a function of the radiation wavelength λ according to the equation: I(λ,T)=2hc2λ51ehc/λkT−1(1) where h is the Planck constant (h = 6.62607004 × 10–34 m2 kg s–1), k is the Boltzmann constant (k = 1.38064852 × 10–23 m2 kg s–2 K–1) and c is the speed of light in a vacuum (c = 299,792,458 m s–1). Eq. (1) implies that the spectral radiance I(λ,T) peaks at a characteristic wavelength inversely related to black-body temperature (Fig. 3). For instance, the Sun (at T = 5,800 K) emits radiation that peaks in the visible part of the spectrum, at wavelengths of about 0.5 μm. In contrast, a human (T = 310 K) emits radiation peaking at around 10 μm, i.e. in the infrared part of the spectrum. This is formalized in the following law. Figure 3. Open in new tabDownload slide Spectral radiance of the electromagnetic radiation I(λ,T) of an ideal black-body shown as a function of the radiation wavelength λ and temperature T following Planck’s law. The peaks observed in spectral radiance for each black-body temperature lead to an inverse relationship between wavelength and temperature, i.e., known as Wien’s law. Wien’s displacement law. Wien’s displacement law describes how the spectral radiance of a black body peaks at a wavelength λmax that is inversely proportional to the temperature (Fig. 3): λmax=b/T(2) where b is Wien’s displacement constant (b = 2.8977721 × 10–3 K m). Wien’s law implies, for example, that the colour of stars is determined by their temperature. More practically, it implies that since sensors absorb infrared radiation within limited wavelength ranges according to the material of which they are made, the sensitivity of a given sensor needs to be matched to the range of temperatures being examined in order to achieve a maximum signal-to-noise ratio. For instance, for molluscan body temperatures in the range 15–55 °C (Chapperon & Seuront, 2011a, b; Seuront & Ng, 2016), λmax ranges from 8.8 to 10.1 μm, which is within the range of sensor sensitivity used for biological applications (Kastberger & Stachl, 2003; Lathlean & Seuront, 2014; Tattersall, 2016), i.e. LWIR (8–14 μm). Energy conservation law and Kirchhoff’s radiation law The energy conservation law states that, at thermodynamic equilibrium, at a given wavelength, the incident radiant energy flux Fi arriving at an object is either transmitted, absorbed or reflected; hence: Fi=Ftransmitted+Fabsorbed+Freflected(3) Or, equivalently: τ+α+ρ=1(4) where τ, α and ρ are, respectively, the fractions of the incident radiation that are transmitted, absorbed and reflected, i.e. the transmittance, absorbance and reflectance coefficients. Eq. (4) can be simplified to α + ρ = 1 as, in most materials, including biological surfaces, τ = 0 (i.e. no fraction of the incident radiant flux is transmitted through the material), so all the incident radiation is either absorbed or reflected. Kirchhoff’s law states that, because an ideal black body does not reflect any radiation, the conservation of energy implies that all the radiation absorbed by such a body is emitted, hence ε = α, where the emittance coefficient (or emissivity) ε is the fraction of the black body energy that is emitted (Fig. 4). Since α + ρ = 1, then ε + ρ = 1, which more prosaically translates as ‘good absorbers are good emitters’ (i.e. ε = α) and its corollary ‘good reflectors are poor emitters’ (i.e. ε + ρ = 1). A notable consequence of these statements is that no physical object can emit more radiation than a black body, since emissivity is the ratio of the object’s radiant flux (Mr) to that of a black body at the same temperature (Mb), that is ε = Mr/Mb. Emissivity then equals one (ε = 1) for an ideal black body, and ε < 1 otherwise (Fig. 4). Figure 4. Open in new tabDownload slide Schematic illustration of fate of an incident radiative energy flux Fi on a black body (A) and on grey bodies with various emissivities ε (B–D). B.ε = 2/3. C.ε = 1/3. D.ε = 0. Incoming radiation is totally absorbed (Fa) by a black body and owing to the conservation of energy all absorbed radiation has to be emitted (Fe), hence Fa = Fe. On a grey body a fraction of the incident flux Fi can be reflected (Fr), absorbed (Fa) or transmitted (Ft). For the sake of simplicity, Ft has been ignored, as it is usually negligible, hence Fi = Fa + Fr (B, C). Under conditions of thermodynamic equilibrium, Kirschoff’s law implies that the amount of radiation emitted (Fe) must be equivalent to radiation absorbed, thus Fe is usually equal to Fa = Fi − Fr, meaning that there is generally an inverse relationship between an object’s emissivity and reflectivity. A grey body with a high emissivity (B) will then emit more energy than a grey body with a low emissivity (C). A perfectly reflective object (D) does not absorb any of the incident radiation, leading to Fi = Fr, hence Fa = Fe = 0. Stefan-Boltzmann law The Stefan-Boltzmann law describes how the total energy radiated per unit surface area of a black body across all wavelength per unit time (i.e. the radiant flux Mb) is directly proportional to the fourth power of the black-body temperature T: Mb=AσT4(5) where σ is the Stefan-Boltzmann constant (σ = 5.66697 × 10–8 W m–2 K–4) and A the surface area. Note that Eq. (5) results from integrating Eq. (1) through all wavelengths λ from zero to infinity. For an object that does not absorb all incident radiation (often referred to as a ‘grey body’), the Stefan-Boltzmann law has to be reformulated, taking account of the emissivity ε of the object (i.e. ε < 1), as: Mr=AσεT4(6) Note that the emissivity of a grey body is constant and independent of the wavelength. Real objects cannot be considered as grey bodies in the strict sense, as their emissivity is neither constant nor independent of the wavelength (Usamentiaga et al., 2014). However, emissivity varies slowly with wavelengths for solid objects (Usamentiaga et al., 2014), which appear to have an approximately constant emissivity in the infrared region of the radiation spectrum. Emissivity is then typically assumed to be constant for narrow wavelength intervals. In practice, this means that real objects are treated as grey bodies by averaging their emissivity over the short intervals in which infrared sensors work. Emissivity According to Kirchhoff’s law of thermal radiation (see above), the amount of energy emitted by an object is driven by its emissivity ε (Siegel & Howell, 2001; Fig. 4). Emissivity is the ability of an object to emit thermal radiation; it ranges between ε = 1 for a black body, a perfect absorber of thermal radiation (Fig. 4A), and ε = 0 for an object that reflects all electromagnetic radiation (Fig. 4D). Most objects selectively radiate electromagnetic radiation, with wavelength-specific emissivities from 0 to <1. In contrast, a grey body has a constant emissivity (ε < 1) across all wavelengths under consideration (see above), a property used in thermal modelling. As mentioned above in relation to the Stefan-Boltzmann law, one fundamental assumption of thermal imaging is that most objects behave like grey bodies with respect to infrared radiation and hence can be described using a single emissivity value (Fig. 4B, C). Emissivity is independent of surface colour. For instance, white marble, limestone and coal share a similar emissivity of c. 0.95 in the infrared wavelength range, which a priori seems counterintuitive, because dark and white surfaces differ in their abilities to absorb visible light. Nevertheless, both dark and white surfaces absorb radiation very well in the infrared spectrum and hence share a comparable high emissivity. In contrast, emissivity does depend on surface texture. Smooth and polished surfaces reflect radiation very well and hence have a low emissivity. In turn, rough and textured surfaces reflect light less efficiently, so have a higher emissivity than smooth ones. These properties are best illustrated by Leslie’s cube, a device used to demonstrate the differences in thermal radiation emitted from surfaces heated to the same temperature, but differing in colour and texture (Fig. 5; see Vollmer & Möllmann, 2010, for more details). Figure 5. Open in new tabDownload slide Digital (A, B) and infrared (C, D) images of Leslie’s cube. This aluminium device shows how the nature (colour and texture) of surfaces of the different faces of the cube in thermal equilibrium (here 55 °C) influences their emission of thermal radiation. The two faces painted in black (A) and white (B) both emit thermal radiation strongly (red colour on thermograms C, D). In contrast, the reflective mirror-like polished (A) and unpolished (B) faces of the cube emit much more weakly (blue in C, D) and the reflected image of the warm hand is clear (C). Note that reflection of the hand on both aluminium faces is green, indicating a high emissivity surface near body temperature (37 °C). Photo credit: Pieter Kuiper, Public Domain, https://commons.wikimedia.org/w/index.php?curid=13303826. Water content is another factor that is likely to affect the emissivity of an object, since water is an excellent emitter of thermal radiation. The relationship between emissivity and both soil moisture and vegetation water content has been a prolific topic for decades (see Petropoulos, 2014; Srivastava, Petropoulos & Kerr, 2016, for reviews). Note, however, that wet surfaces have to be treated with caution, especially in the context of molluscan research where surface temperatures are frequently used as proxies of body temperature (Lathlean & Seuront, 2014; Seuront & Ng, 2016). Though water films have very high emissivity (typically ε ≥ 0.9), wet surfaces reflect more incident radiation than dry ones (especially in full sunlight) and this effect increases when the viewing angle between the camera and the object decreases (Clark, 1976; Faye, Dangles & Pincebourde, 2016). As a consequence, these surfaces appear cooler than dry ones, which may lead to a systematic underestimation of ectotherm (including molluscan) body temperature using infrared thermography. This source of error could be limited by keeping the viewing angle close to 90° (Clark, 1976), by experimenting when conditions are overcast, or even avoided by carrying out measurements at night. Nevertheless, since thermal stress is obviously greatest during the middle of the day when the sun is highest, and it is often the response to these intense periods of heat stress that concern ecologists, none of the aforementioned solutions are recommended. A practical alternative would be to temporarily shade ectotherms while thermal images are being recorded. Note also that wet surfaces can actually be cooler than dry ones when evaporative cooling (i.e. the process by which the energy needed to convert water into vapour leads to heat loss; see below) takes place. Cooling the surface of the shell of a mollusc, however, does not imply a reduction in the core body temperature, as this would require thermal equilibrium—which only occurs after a delay that depends primarily on the size of the organism and the conductive properties of its tissues. The emissivity of an object may also depend on its morphological complexity (Van Alstyne & Olson, 2014) and structural composition (Rubio, Caselles & Badenas, 1997). For instance, the emissivity of intertidal macroalgae with flat surfaces is relatively constant at the scale of a few centimetres, but varies more in algae with papillate surfaces and in species composed of thin stems and branches (Van Alstyne & Olson, 2014). These results may be related to the intrinsic changes in the angle θ between the infrared camera and the topologically complex surface. Note that the angle effect increases with decreasing values of θ. It is essential to understand the properties described above and the implication that the visual appearance of the surface of an object may be a poor indicator of its emissivity. As discussed below, there are fundamental implications for the thermal biology of molluscs and for their abiotic and biotic environments. It must be stressed that, beyond the emissivity of an object and the absolute quantity of incident infrared radiation, both the orientation of its surface relative to the sun and its surface-to-volume ratio determine the amount of heat that is transferred to the object (Gates, 1980). This is particularly relevant for terrestrial and intertidal invertebrates in general, and in particular for molluscs and their substrata, which are heated up by both direct solar radiation (Fig. 6A) and solar radiation reflected by vegetation and topographic features (Fig. 6B) during the day; infrared radiation is also emitted at night, but reflected radiation strongly decreases. Heat radiation is subsequently emitted from both abiotic and biotic objects (Fig. 6C). Note, however, that while a significant amount of solar radiation is reflected by the atmosphere and clouds (c. 25%) and absorbed by the atmosphere (c. 2%), a variable amount of the radiation reaching the surface of the Earth (c. 50%; e.g. Miller & Wheeler, 2012) may be lost depending on the reflective properties of the objects (Fig. 6D). Figure 6. Open in new tabDownload slide Diagram of the heat exchange pathways between a mollusc and its environment; these include radiation, conduction, convection and evaporation. Heat radiations originate directly from the sun (A) after a significant proportion (c. 30%) has been reflected by the atmosphere, clouds and the surfaces of land, lakes and oceans (D), and indirectly through reflected solar radiations, including diffuse scattering of radiation in the atmosphere (B) and from both abiotic and biotic objects (C). Conduction occurs between objects in contact with each other (E); conduction also occurs within a single object, when its core temperature differs from its surface temperature (F). Convective heat transfer occurs between an object and the surrounding moving fluid (i.e. water or air) (G). Evaporative cooling (H) is the process by which an organism’s body temperature decreases through the energy required to convert liquid to gas; in contrast to radiation, conduction and convection, evaporation is not a mechanism of heat transfer but a source of latent heat. Conduction Conduction is the heat transfer between two objects in contact with one another. Heat travels down a thermal gradient, in exactly the same way that molecules move passively down a gradient in concentration; heat is, therefore, conducted from a warmer to a colder object. This property applies to both the heat conduction between an organism and its substratum (Fig. 6E) and the heat conduction between two organisms in contact with each other. Heat conduction also applies to a single object, when its core temperature differs from its surface temperature (Fig. 6F; Oke, 1987). Specifically, the rate of heat conduction from an object (either inanimate or animate) depends on (1) the conductivity (or rate at which it conducts heat), i.e. the amount of heat that flows per unit of time through a unit area with a temperature gradient of one degree per unit distance (Perry & Green, 2008; for living organisms, the higher their conductivity, the more energy they need per unit of body mass to maintain their heat balance); (2) the size (or volume), i.e. the smaller the object, the shorter the distance heat must travel; (3) the thermal inertia, which depends on the object’s mass and heat capacity, and (4) the surface area that is physically in contact with other objects. As a consequence, the surface-to-volume ratio is a critical parameter, because both abiotic and biotic objects gain (or lose) heat via conduction from (or to) surfaces and objects they are in contact with, but also between their core and surface, when these are at different temperatures. In contrast to endotherms which have varying degrees of insulation (e.g. feathers, fur and/or fat deposits) that enable them to retain their internal heat (Fig. 7A, B) and hence to rely less upon external heat sources, ectotherms and their (vegetal or mineral) substrata have no insulation (Fig. 7C–F) and hence have a higher thermal conductivity (i.e. they easily gain or lose heat from/to the objects with which they are in contact). Note that insulation would be detrimental to ectotherms, because it would slow the rate of heat transfer into the body (Speakman, 2004); as an example, mammalian fur has a thermal conductivity that is more than one order of magnitude lower than mammalian tissue (Schmidt-Nielsen, 1997). Figure 7. Open in new tabDownload slide Illustrations of the effects of presence and absence of insulation in the thermal ecology of endothermic (A, B) and ectothermic (C–F) organisms. A. A group of students on a French rocky shore in winter (air temperature 3 °C), showing differences in thermal signatures of insulated (torsos with winter coats; surface temperature in range 4.5-4.9 °C) and noninsulated (legs with trousers; surface temperature in range 12.7-15.5 °C) body parts. B. Close-up of a student showing lower surface temperatures produced by insulation provided by hair and winter clothing, compared to face surface. C, D. Digital and thermal images of group of Patella vulgata on rocky intertidal substratum during overcast midday winter low tide in absence of wind, showing lack of thermal signature of the limpets. E, F. Thermal signature of Cepaea nemoralis resting on tree branches in sun (E) and shade (F), illustrating the direct link between solar radiations and body temperature in molluscs. Convection Convection is the heat transfer between an object and the surrounding fluid, e.g. water or air, when they have different temperatures (Fig. 6G). In contrast to heat transferred via electromagnetic waves (heat radiation), heat convection is driven by the motion of the fluid surrounding an object (Denny, 1993; Cengel, 2003). Note that in the unlikely instance where the fluid surrounding an object is stagnant, heat transfer occurs in the form of conduction as described in the previous section. Heat convection can be subdivided into free convection and forced convection, where the motion of the surrounding fluid is driven, respectively, by the buoyant forces resulting from the changes in fluid density driven by a temperature gradient or by an external force such as advection or turbulence. As stated for heat conduction, the rate of heat transfer is controlled by (1) the magnitude of the temperature gradient between the object and the fluid, (2) the area of contact between the object and its surrounding fluid, and (3) both the thermal and hydrodynamic properties of the fluid. For instance, water conducts heat 23–25 times faster than air, making water the more efficient medium for heat loss. Evaporation Evaporation is the process by which a liquid converts to a gaseous state. In contrast to radiation, conduction and convection, which are the three mechanisms of heat transfer (i.e. transport of thermal energy), evaporation is not a mechanism of heat transfer, but a phase transition between a liquid and a gaseous state that involves energy. As such, evaporation is a source of latent heat. If an object is covered by a film of water that evaporates, the surface of the object cools down, but the mechanism responsible for heat transfer is essentially convection, i.e. the energy from the surface is transported via water molecules into the surrounding air, and this is convection. In the present context, the energy needed to convert water to gas allows an organism to lose heat even if its body temperature is cooler than the environmental temperature (Fig. 4H; Denny, 1993). This process, referred to as evaporative cooling, is often the only mechanism available to organisms during prolonged exposure to solar radiation by which to dump excess heat efficiently, in an effort to maintain a safe body temperature. In its simplest form (e.g. panting or mouth gaping), evaporative cooling is a very effective strategy used by mammals, birds and reptiles to prevent overheating (Spotila, Terpin & Dodson, 1977; Tattersall & Gerlach, 2005). However, if the air is saturated with water (during periods of high relative humidity or in constantly humid environments), evaporation as a thermoregulatory mechanism becomes inefficient, because net evaporation ceases when the air can no longer absorb additional moisture (Speakman, 2004). FROM THE PHYSICS OF HEAT TRANSFER TO THE THERMAL BIOLOGY AND ECOLOGY OF MOLLUSCS This section briefly reviews how the fundamental mechanisms of heat transfer described above apply to molluscs, whether terrestrial or intertidal, that exchange heat with their environment intermittently through their foot during periods of locomotion and constantly through their shell. Note that because infrared thermography is not applicable in water (see Lathlean & Seuront, 2014) subtidal marine species and aquatic freshwater species are not considered hereafter. Heat transfer and microhabitat selection Microhabitat selection (e.g. of shaded topographical features) is common in both terrestrial and intertidal snails, and is generally considered as an adaptive behavioural response to thermal stress associated with heat radiation from the sun and heat conduction from the substratum (e.g. Chang & Emlen, 1993; Jones & Boulding, 1999; Chapperon & Seuront, 2011a; Cartwright & Williams, 2012). The roles of heat radiation, conduction and convection in driving microhabitat choice of molluscs are, however, difficult to disentangle. For instance, the mangrove snail Littoraria scabra selects its substratum based on the surface temperature of the substratum (Chapperon & Seuront, 2011a). The selected cooler substrata are, however, consistently located on the underside of Rhizophora roots and, hence, in the shade (Chapperon & Seuront, 2011a). The relative contribution of these three processes of heat transfer is also likely to be time-dependent (e.g. day vs night) and context-dependent (e.g. windy vs still). Sheltered microhabitats (e.g. crevices, vertical rock faces, gullies and logs) may reduce the effectiveness of convective cooling of individuals by air currents. For example, crevices have traditionally been considered to be thermal refuges for intertidal molluscs (Garrity, 1984). Recent studies have shown, however, that they may often be as thermally stressful as exposed surfaces—if not more so (Fig. 8A)—although they are selected by numerous molluscan species during summer (Chapperon & Seuront, 2011b; Chapperon, Le Bris & Seuront, 2013). These observations suggest that, under both thermal and desiccation stresses, some microhabitats may primarily act as refuges against desiccation related to convective cooling, especially when compared to a nearby flat substratum, so that microhabitat choice can be driven by humidity rather than temperature. This hypothesis is consistent with observations conducted on two sympatric xerophilic snails from southeastern Spain (Iberus gualtieranus and Sphincterochila candidissima) and two other sympatric snails (Theba pisana and Otala lactea) from a humid Mediterranean zone. Under similar conditions of heat stress, temperature was found to regulate microhabitat selection in the humid environment, while in the arid environment humidity also plays a critical role in habitat selection, even though differences exist between the sympatric species (Moreno-Rueda et al., 2009). Note, however, that crevices may also offer a thermal refuge with higher temperature in winter, and hence be selected by gastropods (Fig. 8B, C). Figure 8. Open in new tabDownload slide Digital and thermal images of crevices on (A) a horizontal rock platform in summer (Jorgensfontein, South Africa) and (B, C) a vertical rock platform in winter (Cape d’Aguilar, Hong Kong). Scale bars: C = 15 cm; D = 4 cm. Heat transfer and shell characteristics Polymorphism in shell colour or pattern is a common phenomenon in a range of molluscs, including terrestrial snails and intertidal bivalves and snails, and has been suggested to have an adaptive significance related to both predation (e.g. Johannesson & Ekendahl, 2002; Surmacki, Ozarowska & Rosin, 2013) and differential heat absorption. This has generated considerable research interests in climatic and microclimatic selection, and hence in the distribution of colour morphs at different spatial scales (e.g. Mitton, 1977; Johnson, 1980, 1981; Heller, 1981; Cowie & Jones, 1985; Etter, 1988). In polymorphic terrestrial species, such as T. pisana and Cepaea nemoralis, shell colour and banding are strongly associated with habitat. Pale and unbanded T. pisana morphs are more common in open, exposed habitats, with higher frequencies of darker, banded snails in shrubby, shady habitats (Johnson, 1980; Heller, 1981). Yellow and banded C. nemoralis are more common in open than in shaded habitats (e.g. woodlands) where darker (pink or brown) and effectively unbanded morphs dominate (Cain & Sheppard, 1954; Parkin, 1971, 1972). These differences have been related to visual selection by avian predators (Surmacki et al., 2013), but also to climatic and microclimatic selection. Climatic selection on both body and shell colour is supported by the large-scale latitudinal variation reported in C. nemoralis in Europe, where paler colours are favoured in areas of higher temperature because of their greater reflectivity of incident solar radiation, and darker colours in cooler areas because of their greater abilities to absorb radiation (Jones, 1973; Heath, 1975; Jones, Leith & Rawlings, 1977; Cowie & Jones, 1985; Chang, 1991). Such observations are also consistent with early field and laboratory measurements showing that fully banded/darker snails heat up more rapidly and reach higher temperatures than unbanded/lighter snails when exposed to radiant heat (Johnson, 1981; Cowie & Jones, 1985; Hazel & Johnson, 1990; Staikou, 1999; Di Lellis et al., 2012). These observations have recently been ratified by the results of a 43-year survey showing that, despite changes in habitat towards greater shadiness (hence the expectation of visual selection for darker snails), the 1.5–2.0 °C temperature increase observed over the study period resulted in shells becoming lighter (Ozgo & Schilthuizen, 2012). Note that shell colour shows stronger and more consistent variation with habitat than do banding patterns, yellow shells being at higher frequencies in open habitats than in woods. There is, however, marked geographical variation in this relationship, which is stronger in southern England and northern France than elsewhere (Cameron & Cook, 2012). Further evidence for microclimatic selection comes from a 34-year survey of T. pisana colour polymorphism across an ecotone, which showed a consistent association of shell banding with habitat and a higher proportion of unbanded snails associated with hotter, sunnier summers (Johnson, 2011). Temporal variation thus supports the hypothesis of microclimatic selection, consistent with the spatial association with habitat. Direct quantitative and simultaneous measurements of air temperature, snail shell and body temperatures, and substratum temperature are, however, still missing, hampering the generalization of these results and prompting the need for further investigations into the thermal biology and ecology of land snails. To our knowledge only a few studies have investigated potential differences in response to sunlight in molluscs of different colour morphs. Hamilton (1973) showed that the black Tegula funebralis heated up faster than the brown T. brunnea when placed in sunlight. This result should, however, be taken with caution given that T. brunnea and T. funebralis are subtidal and intertidal species, respectively. The observed differences may, however, be more related to the fact that T. brunnea and T. funebralis are not conspecific morphs (i.e. their shells do not differ in pigmentation alone) and have been exposed to different selection regimes in different habitats, rather than the result of actual pigmentation-related differences in the absorption of solar radiation by mollusc shells. Mytilus edulis with a higher degree of pale striping on their shells exhibited a lower body temperature than darker morphs under solar radiation (Mitton, 1977). Using empty (seawater-filled and sealed) Nucella lapillus shells exposed to natural sunlight, Etter (1988) showed that brown morphs heated up faster and attained higher temperatures than white morphs. This observation was consistent with experiments conducted on live snails, which showed that brown snails desiccated more rapidly and suffered greater mortality than white morphs (Etter, 1988). It is still unclear, however, whether the differences in shell size, shape, colour and surface patterning observed in molluscs (e.g. Reid, 1989) do significantly affect their ability to absorb thermal radiation. For example, Miller & Denny (2011) showed that body temperature variability related to shell structure and colour in littorinids was negligible (light shells were on average less than 0.5 °C cooler than dark ones) and Cox & Smith (2011) found nonsignificant differences in the emissivity of nine species of intertidal molluscs that varied in shape, size and colour. It is even unclear how differences in gastropod shell colour affect their ability to absorb and reflect thermal radiation. Darker shells are implicitly assumed to absorb more short-wave radiation, and hence to heat up more than lighter morphs under similar conditions, but different colour morphs also absorb and reflect other wavelengths (e.g. dark snail shells provide more protection against UV radiations than pale ones; Williams, 2016), which may impact the capacity to heat up and cool down and explain the lack of significant thermal difference between morphs (Scheil, Gärtner & Köhler, 2012). Heat transfer and shell orientation The orientation of even a stationary shell relative to the sun changes during the course of the day and hence its absorption of thermal radiation changes. Shell orientation has been reported as a behavioural adaptation to limit heat stress in some land species (e.g. T. pisana; McQuaid, Branch & Frost, 1979; Cowie, 1985). Shell orientation was, nevertheless, found to be random in the xerophilic Mediterranean land snail Xeropicta derbentina and unrelated to both shell surface and body temperature (Di Lellis et al., 2012). In intertidal environments, Nerita plicata changes the direction of its shell to face the sun during emersion (Warburton, 1973) and the high-shore Echinolittorina peruviana adjusts its shell orientation to reduce the surface area perpendicular to the sun in order to maintain a lower body temperature during thermally stressful low tides in the summer (Muñoz et al., 2005). Similar observations are lacking, however, in other species under similar conditions of heat stress (e.g. McQuaid & Schermann, 1988; Lang, Britton & Metz, 1998; Miller, 2008). The available results suggest that the role of shell orientation in thermal regulation may be both species-specific and context-specific. The interplay between heat stress and shell orientation may, however, be more complex than appears at first glance. Shell orientation is constrained by its shape (Cook & Jaffar, 1984; Garrity, 1984; Goodfriend, 1986; Okajima & Chiba, 2013) and may therefore be driven by functions that have nothing to do with the thermal nature of the environment, such as stability on the substrate (Bingham, 1972), wave action (Garrity, 1984) and mating (Marshall & Ng, 2013). High-shore snails may favour other behavioural strategies to minimize heat stress, as described in the next section. Heat transfer, aestivation, foot withdrawal and postural behaviour Both terrestrial and intertidal snails face the challenge of survival on substrata that may reach extreme temperatures, in arid and exposed habitats for the former and during daytime low tides for the latter. The amount of heat transfer through conduction from the substratum is, therefore, an important determinant of body temperatures of these animals (Helmuth, 1998; Staikou, 1999; Marshall, McQuaid & Williams, 2010). The problem is especially critical for terrestrial snails, which are very sensitive to desiccation due to their highly water-permeable skin (e.g. they can lose up to 40% of their body mass through evaporation in 2 h; Prior, 1989) and to overheating (Staikou, 1999). Note, however, that land snails are more sensitive to desiccation than intertidal snails because they have thinner shells, often lack an operculum, have large apertures, and do not benefit from the periodic occurrence of hide tides once or twice per day. As a consequence, terrestrial snails restrict their daytime activities to periods of favourable temperature and humidity (Staikou, 1999), are often active at night, climb on vegetation to escape the heat conducted from the substratum (Pomeroy, 1966, 1968; Yom-Tov, 1971) and use aestivation. Aestivation refers to a summer state of inactivity and reduced metabolism (5–30% of the normal rate) that can last for months (Guppy & Withers, 1999; Bishop & Brand, 2000) and is adopted during unfavourable conditions in order to save both water and energy (Pomeroy, 1968; Yom-Tov, 1971; McQuaid et al., 1979; Herreid, 1977; Barnhart & McMahon, 1987; Withers, Pedler & Guppy, 1997). High-shore intertidal snails, in particular rocky-shore littorinids, have also been reported to aestivate for days to weeks (Miller & Denny, 2011; Marshall, Baharuddin & McQuaid, 2013). In addition, they exhibit a suite of behaviours to reduce heat conduction from their substratum, as well as to reduce water loss through evaporation and/or increase convective cooling by air currents, and these behaviours are all coupled with foot withdrawal. Under dry conditions when exposed at low tide, snails may retract the foot into the shell, close the operculum and glue themselves to the rock with a mucus holdfast that allows them to detach their soft body from the substratum (Vermeij, 1971a; Bingham, 1972; Denny, 1984; Garrity, 1984; McMahon & Britton, 1985; Britton & McMahon, 1986; McMahon, 1990; Lang et al., 1998). This simple behaviour provides enough support for littorinids to remain attached on rocks with minimal effort (Denny, 1984) and minimizes water loss from evaporation (Vermeij, 1971a; McMahon, 1990; Britton, 1992; Rojas et al., 2013). It also minimizes conductive transfer from the substratum by reducing the amount of soft tissue and shell in contact with it, while maximizing the shell surface exposed to air currents, thus allowing increased heat transfer from the shell through convective cooling (Miller & Denny, 2011; Marshall & Chua, 2012). Individuals with the foot withdrawn have been found to be 3–5 °C cooler than those with the foot attached to the substratum and this effect was more pronounced in smaller species (Miller & Denny, 2011). Under conditions of extreme heat stress, improved convective cooling is achieved through shell-lifting (Garrity, 1984; Britton, 1995; Lang et al., 1998; Wada & Ito, 2000; Miller & Denny, 2011), shell-standing (Lim, 2008; Miller & Denny, 2011; Marshall & Chua, 2012) and shell-stacking (Marshall, Mustafa & Williams, 2010), also referred to as towering (Seuront & Ng, 2016). Shell-lifting snails have their shell slightly lifted off the substratum with its aperture parallel to the substratum surface. Shell-standing refers to when snails attach to the substratum with their aperture facing perpendicularly to the rock surface (Marshall & Chua, 2012). Towering behaviour occurs when at least two snails (up to five have been observed; Seuront & Ng, 2016), glue vertically on top of each other to form a stack or tower, and all individuals involved in the tower may or may not adopt the former two postures (Lim, 2008; Marshall et al., 2010; Marshall & Chua, 2012; Seuront & Ng, 2016). These various postural behaviours have all been shown to reduce snail body temperature, e.g. up to c. 10 °C in Echinolittorina malaccana and E. radiata (Seuront & Ng, 2016; Fig. 9A, B) and up to 5 °C in Austrolittorina unifasciata (Seuront, unpublished data; Fig. 9C). Note that towers can be either monospecific (Fig. 9A–C) or heterospecific (Fig. 9D), and there is a consistent decrease in snail size observed from the bottom to the top of a tower (i.e. in 96.2% and 97.6% of the towers observed in E. malaccana and E. radiata, respectively, and in 100% of the heterospecific towers; Seuront & Ng, 2016; Fig. 9). This seems to be consistent with an adaptation to heat stress, since heat transfer is inversely proportional to size in both stagnant and moving air, hence smaller individuals would theoretically benefit from a higher position in a tower (Seuront & Ng, 2016). Figure 9. Open in new tabDownload slide Digital and thermal images of shell-towering behaviour in Echinolittorina radiata (A), E. malaccana (B) and Austrolittorina unifasciata (C). This postural behaviour can lead to both monospecific (A-C) and heterospecific (here E. radiata and E. malaccana; D) towers, and consistently results in a decrease in both snail size and temperature from the bottom to the top of a tower. Heat transfer, aggregation and gaping Aggregations have commonly been observed in terrestrial snails and slugs (e.g. Mason, 1970; Chase, Croll & Zeichner, 1980; Giokas, Pafilis & Valakos, 2005; Mysak et al., 2013; Chukwuka et al., 2014; Korabek, Cejka & Jurickova, 2016), intertidal snails (Chelazzi, Innocenti & Della Santina, 1983; Chelazzi, Della Santina & Vannini, 1985; Tong, 1988; Mohammed, 1999), limpets (Keough, Quinn & Bathgate, 1997; Coleman et al., 1999; Coleman & Hawkins, 2000) and chitons (Grayson & Chapman, 2004). Aggregations may help to retain moisture and reduce evaporation rates through the minimization of the surface area in contact with the atmosphere (Chase et al., 1980). For instance, aggregated individuals of E. peruviana maintain water content and thermoregulate better than solitary ones (Rojas et al., 2000) and aggregated individuals of Nerita atramentosa have higher water content than solitary snails. Note, however, that aggregation behaviour of N. atramentosa reduces both desiccation and heat stresses on boulder fields, but not on adjacent rock platforms, which indicates that the role of aggregation behaviour may be habitat-specific (Chapperon et al., 2013). However, when individuals in an aggregation dry up after prolonged periods of heat stress, the beneficial cooling properties of such aggregations begin to break down (e.g. Chapman & Underwood, 1996; Stafford & Davies, 2004; Chapperon & Seuront, 2011a). Under hot and dry conditions, individuals within aggregations may even experience higher body temperatures than solitary snails (Chapman & Underwood, 1996); this effect may be due to reduced convective cooling when air currents are blocked by other individuals. Keeping warm through aggregation can, however, be beneficial during cold periods, as demonstrated in N. atramentosa (Chapperon & Seuront, 2012), although such thermal benefits of ‘huddling up’ have not been found in other rocky-shore species (Echinolittorina malaccana and E. radiata; Seuront & Ng, 2016). Mussels are also characterized by the formation of dense and complex clusters (e.g. van de Koppel et al., 2008; Erlandson, McQuaid & Sköld, 2011). Again, aggregated mussels often exhibit lower body temperatures than solitary ones (Helmuth, 1998). This observation is highlighted in the case of two species of intertidal mussel, the indigenous Perna perna and the invasive Mytilus galloprovincialis, that coexist in large aggregations on the south coast of South Africa. During emersion, P. perna exhibits periodic closure and opening of the shell (i.e. gaping); this behaviour allows the maintenance of aerobic respiration, but increases levels of water loss and the risk of desiccation, due to both evaporation and expulsion of water during valve closure. In contrast, M. galloprovincialis keeps its valves closed when exposed to air. This behaviour reduces the risk of desiccation, but decreases the efficiency of anaerobic respiration (Nicastro et al., 2010). These different responses to aerial exposure, along with different byssal attachment strengths, are thought to determine the different vertical distributions of the two species (Branch & Steffani, 2004; Bownes & McQuaid, 2006; Zardi et al., 2006; Hanekom, 2008). Recent laboratory experiments showed that the gaping behaviour of P. perna was ineffective in reducing the body temperatures of solitary mussels, but that when individuals were surrounded by conspecifics, evaporative cooling effects emerge for the entire cluster (Nicastro et al., 2012). Consequently, increasing densities of M. galloprovincialis within P. perna beds may reduce the ability of individual P. perna to thermoregulate, while allowing M. galloprovincialis to ‘steal’ beneficial thermal properties from P. perna (Lathlean et al., 2016a)—a seldom-studied process referred to as kleptothermy (see Brischoux, Bonnet & Shine, 2009; Corkery, Bell & Nelson, 2014). This hypothesis is consistent with observations that, during periods of severe heat stress, mortality rates of P. perna surrounded by nongaping M. galloprovincialis in the field were higher than those of P. perna surrounded by conspecifics (Nicastro et al., 2012). Heat transfer and evaporative cooling There is a well known trade-off between drought resistance and thermoregulation in terrestrial snails (Rankevich, 1997). Thermoregulation requires water for evaporative cooling. Evaporative cooling is more effective for smaller snails because a smaller body size increases the surface-area-to-volume ratio, which in turn increases both absorption and radiation of heat (Rankevich, 1997; Schmidt-Nielsen, 1997). This is consistent with reports of higher water loss from small compared with large snails, which may lead to a more effective evaporative cooling and, therefore, also provide a possible explanation for the higher heat tolerance of small snails in a range of Mediterranean species such as Xeropicta derbentina, Cernuella virgata and T. pisana (Cowie, 1985; Dittbrenner et al., 2009). In intertidal snails, effective evaporative cooling is achieved by dripping mantle water over the body in low-shore species that are frequently immersed, but not in high-shore species (Garrity, 1984; McMahon, 1990; Britton, 1992). This process has been documented in a variety of neritids (Lewis, 1960, 1963; Vermeij, 1971b). Nerita species store water in the space between the shell and the body wall, and this water is released over the dorsal surface of the foot where evaporative cooling occurs (Vermeij, 1971b). For instance, N. scabricosta aggregates in multilayered clumps of up to 1,000 animals, where snails remained foot-attached to the rock or to conspecifics and trickle water from their shells (Garrity, 1984). Similarly, when N. atramentosa aggregated under a boulder are unexpectedly exposed to direct solar radiation, they became active nearly instantly, crawling onto each other and dripping their mantle water on each other’s shells (Seuront, personal observations). Evaporative cooling hence allows intertidal species to remain active during periods of emersion, even under thermally stressful conditions. For example, evaporative cooling enables Austrocochlea concamerata and N. atramentosa to remain active for 2–3 h at 40 °C (McMahon, 1990). These results seem, however, to be species-dependent because, for example, in the mangrove whelk Telescopium telescopium the problem of water conservation outweighs the benefits obtained in regulating temperature via evaporative cooling (Lasiak & Dye, 1986). Some individuals of N. atramentosa appear to exhibit a lack of or limited evaporative cooling abilities (McMahon, 1990). APPLICATIONS OF INFRARED THERMOGRAPHY IN NON-MOLLUSCS: A BRIEF REVIEW The rationale behind the use of infrared thermography differs fundamentally between endotherms (mostly birds and mammals) and ectotherms (invertebrates, amphibians, reptiles and most fish). Endotherms produce their own heat and hence must have mechanisms to conserve and release this heat as necessary. In contrast, ectotherms derive their body heat from their environment and use behavioural mechanisms to utilize the range of physical processes driving heat exchange. One of the most common applications of infrared thermography in endothermic animals (see Tattersall, 2016, for a review) relates to temperature measurements of the body areas responsible for heat exchange; this exchange is achieved by modifying and controlling blood flow (via vasoconstriction and vasodilatation) into these areas, which experience a much greater range of cutaneous blood flow than elsewhere (Johnson et al., 1986). Such areas (hereafter referred to as ‘thermal windows’) include the ears, feet and nose of mammals, and the bills, feet and facial skin of birds (Tattersall & Cadena, 2010; Tattersall, 2016). Infrared thermography has now been applied extensively to assess endotherm body temperature of these thermal windows, e.g. in ostrich, emu and cassowary (Phillips & Sanborn, 1994), mole-rats (Sumbera et al., 2007), seals (Mauck et al., 2003), bats (Reichard et al., 2010) and elephants (Weissenböck et al., 2010). It has also been applied in the study of conservation of body heat radiation in birds in relation to feather colour (Dove et al., 2007) and of various aspects of human thermoregulation (Bouzida, Bendada & Maldague, 2009; Fournet et al., 2013; Adamczyk et al., 2016). The infrared thermal signature of endotherms has also been used remotely (1) to assess the health of both captive and wild animals (Lavers et al., 2005; Mellish et al., 2013) and (2) to identify and enumerate a range of terrestrial and marine mammals (Cronin et al., 2007). Infrared thermography enables study of the abundance and behaviour of small nocturnal mammals such as bats (Sabol & Hudson, 1995; Hristov, Betke & Kunz, 2008), which are difficult to visualize when emerging from their caves at night. Infrared thermography also found many applications in both vertebrate and invertebrate ectotherms (see McCafferty, 2007; Tattersall & Cadena, 2010; Lathlean & Seuront, 2014; Tattersall, 2016, for reviews). Briefly, infrared thermography has been used to assess various aspects of reptile biology and ecology such as respiratory cooling (Tattersall & Gerlach, 2005; Tattersall, Cadena & Skinner, 2006), habitat choice (Krochmal & Bakken, 2003; Croak et al., 2008; Lelièvre et al., 2010) and the potential links between skin colour and body temperature (Tattersall, Eterovick & De Andrade, 2006). Thermal-imaging technology provides a reasonable approximation to internal body temperature for small vertebrate ectotherms (i.e. <20–50 g) with relatively low thermal inertia (Jones & Avery, 1989; Tattersall, Eterovick & De Andrade, 2006). Its use is more problematic with large ectotherms because (1) regional heating by solar radiation can lead to major differences in the surface temperature throughout the body, without necessarily a similar change in core body temperature, and (2) many of these ectotherms may regulate head or brain temperature rather than body temperature (Tattersall & Cadena, 2010). Finally, infrared thermography is also increasingly used to estimate body temperature in small invertebrates such as insects and spiders (e.g. Rehnberg, 2002; Hunt et al., 2011; Pike, Webb & Shine, 2012) and to assess the thermal heterogeneity of their habitats (Pincebourde & Woods, 2012; Caillon et al., 2014). There are a few studies in which infrared imagery has been used to assess various aspects of non-molluscan intertidal ectotherms, such as the sea star Pisaster ochraceus (Helmuth, 2002; Pincebourde, Sanford & Helmuth, 2008, 2013) and barnacles (Lathlean & Minchinton, 2012; Lathlean, Ayre & Minchinton, 2012, 2013). INFRARED THERMOGRAPHY IN MOLLUSCAN RESEARCH: WHERE WE ARE SO FAR The use of infrared thermography in molluscan research is currently limited to intertidal species. Infrared thermography was first used to measure temperature variability in Mytilus californianus (Helmuth, 2002), while more recent work has investigated the effect of parasitism on M. galloprovincialis and Perna perna (Zardi et al., 2016). The thermal relationship between M. galloprovincialis and P. perna has further been explored through investigations of the effects of (1) varying densities of the two species on the thermal properties of both natural and artificial mussel beds during periods of aerial heat stress of various intensities (Lathlean et al., 2016a) and (2) bed size and the size structure of individuals within beds on small-scale variability in body temperatures (Lathlean et al., 2016b). Intertidal gastropods have also been investigated through the lens of infrared thermography, initially from a purely methodological perspective to compare invasive and noninvasive measures of body temperature in Nerita atramentosa (Caddy-Retalic, Benkendorff & Fairweather, 2011). Subsequent studies have assessed (1) aggregation behaviour associated with heat stress in N. atramentosa (Chapperon & Seuront, 2012; Chapperon et al., 2013) and Echinolittorina peruviana (Rojas et al., 2013); (2) thermoregulation through thermal refuge selection in the mangrove snail Littoraria scabra (Chapperon & Seuront, 2011a) and the rocky-shore N. atramentosa (Chapperon & Seuront, 2011b); (3) heat stress associated with free space in the limpet Patelloida latistrigata (Lathlean, 2014); (4) shell-posture behaviours associated with thermoregulation in E. malaccana and E. radiata (Seuront & Ng, 2016) and patterns of orientation in relation to thermal stress in the limpet Cellana tramoserica (Fraser et al., 2016). Noticeably, and despite the long-lasting interest in assessing various aspects of thermoregulatory behaviour in a range of terrestrial and freshwater snails, e.g. Theba pisana (McQuaid et al., 1979), Lymnaea auricularia (Cabanac & Rossetti, 1987), Biomphalaria glabrata (Lefcort & Bayne, 1991), Lymnaea sp. (Żbikowska, 2001) and Planorbarius corneus (Żbikowska et al., 2013), we are not aware of any attempt to investigate the thermal ecology of terrestrial molluscs through infrared thermography. Despite the potential that infrared thermography is offering, and the need for it in the field of molluscan research, there are several limitations that need to be carefully examined to ensure the robustness of thermal images and subsequent temperature measurements and interpretations. INFRARED THERMOGRAPHY IN MOLLUSCAN RESEARCH: CAUTIONS AND LIMITATIONS Emissivity As stressed earlier, the emissivity of an object (i.e. its ability to emit thermal radiation) fundamentally influences how that object interacts with and emits radiation. Emissivity consequently plays a critical role in the algorithms used to convert the amount of infrared energy to temperatures in most infrared cameras. For biological tissues, the convention has been to use a value of ε between 0.95 and 0.98 (Hammel, 1956; Best & Fowler, 1981; Rubio et al., 1997; Tattersall, 2016), even though the exact value of ε is unlikely to produce much error, since slight variations in the chosen emissivity value lead to minimal variations in the resulting temperatures for high-emissivity objects (Usamentiaga et al., 2014). This is not necessarily the case in molluscan research, as (1) the shells of most molluscs vary in shape, colour and ornamentation, and (2) their biotic or abiotic substrata drastically vary in shape, structure and colour (see Fig. 2A–D, I–L). For example, the emissivity of intertidal macroalgae with flat surfaces is relatively constant at the scale of a few centimetres, but varies more significantly in algae with papillate surfaces and species composed of thin axes and branches (Van Alstyne & Olson, 2014). The use of infrared thermography to measure surface temperatures of molluscs and their substrata in terrestrial and intertidal environments is then potentially limited because (1) different taxa/substrata within a single infrared image may display different emissivity values due to their difference in shape, colour, surface aspect and ornamentation, and (2) these emissivity values may change when organisms or substrata are wet (Lathlean & Seuront, 2014). While the latter limitation may be more difficult to tackle given the temporary nature of the wetted state of a surface, two distinct, though conceptually similar, remedial procedures are described here as a first step to ensure that the temperature measurements provided by infrared thermography are representative of the actual temperature of an object. Figure 2. Open in new tabDownload slide Digital images of various landscapes and organisms shown with the corresponding infrared images, i.e. thermograms, obtained with thermal cameras Testo 875-1iSR (A, B) and Fluke Ti25 (C–N). A, B. The Swire Institute of Marine Science, Hong Kong, with surrounding vegetation and rocky intertidal shore. C, D. One of the authors, J. Lathlean, at work on an intertidal rocky reef in Jorgensfontein, South Africa (note clear differences in body temperature signatures of exposed and nonexposed body parts. E, F. Patella vulgata on an intertidal rocky reef at Noirda Point, Audresselles, France (note hot thermal signatures of both limpet and crevices on a background of cooler rock). G, H. Native Perna perna and invasive Mytilus galloprovincialis in a mixed bed on an intertidal rocky reef, Jorgensfontein, South Africa. I–L. Rock assemblages of various sizes, the typical habitat of the pulmonate snails Candidula unifasciata, Cernuella virgata and Cochlicella acuta; Wierre-Effroy, France. Note thermal heterogeneity of rocks seemingly similar in shape, colour and size in both assemblages (J, L) and cool thermal signature of the vegetation (L). M, N.Cornu aspersum in its typical environment; Wasquehal, France. Scale bars = 5 cm. First, emissivity can be empirically estimated by simultaneously taking infrared images (TIR) and the in situ temperature of the same object with a calibrated thermocouple (TObject), and subsequently adjusting ε on the infrared camera until TIR = TObject. This approach has been used in a range of studies that used infrared thermography to measure the temperature of intertidal organisms and their substrata, and they have consistently yielded emissivity values in the range 0.95–1.00 (Helmuth, 1998; Denny & Harley, 2006; Miller, Harley & Denny, 2009; Cox & Smith, 2011). Second, emissivity can be estimated by comparing surface temperature estimates to those of substances of known ε. As recommended by most thermal-imaging companies, this can be achieved in practice by sticking a piece of black electrical tape (e.g. Scotch® Black Paper Tape; ε = 0.95) onto the surface of interest, which is then heated up to a temperature of c. 40 °C above ambient temperature (Tattersall, 2016). The surface temperature of the tape is then measured with an infrared device, the surface temperature of the object is measured without the tape, and the emissivity ε is re-set until the two temperatures match one another (Lathlean & Seuront, 2014). Alternatively, the surface of an object can be coated with a matt black paint (e.g. 3-M Black from Minnesota Mining Company or Senotherm from Weilburger Lackfabrik2, which both have an emissivity of c. 0.95) and the above procedure repeated for coated and noncoated surfaces. The estimated emissivity is subsequently used for all temperature measurements of this specific material, either the surface of a (abiotic or biotic) substratum or an organism. In molluscan research, this solution is problematic for shell-less species, either marine or terrestrial, since it involves destructive sampling of the surface, and is impossible to perform on the skin of living animals due to convective and conductive heat exchange from the circulating blood beneath. Since biological tissues are composed primarily of water and organic compounds, emissivity values >0.95 are often assumed, with 0.98 being widely reported as appropriate for human skin (Tattersall, 2016). For shelled molluscs, however, this procedure can be relatively easy to apply under controlled conditions. Note that in instances where surfaces with different emissivity values are considered, one should consider the emissivity of each surface in any subsequent analysis to get reliable temperature measurements. This is easily achieved since many infrared cameras have built-in on-screen emissivity correction capacity and/or come with software that can be used to set a posteriori different emissivity values to specific areas of a thermal image, hence actual temperatures of surfaces with distinct emissivity can be estimated through an appropriate post-processing procedure (Faye et al., 2016). Note, however, that for biological tissue the exact emissivity value is unlikely to produce much error, since most biological surfaces consist of similar substances (Tattersall, 2016). Distance matters The distance d between the camera and a target object is another potential source of bias in temperature estimates using infrared thermography. A recent study inferring the effect of distance on infrared-thermography estimates of the thermal properties of vegetation and landscape mosaics showed that images taken from long distances (typically >20 m) consistently underestimated surface temperatures by up to 3 °C (Faye, Dangles & Pincebourde, 2016). Interestingly, the structural complexity of the surface itself had negligible effect on the surface temperature bias (Faye, Dangles & Pincebourde, 2016). The authors explained the aforementioned bias in terms of atmospheric composition and the pixel-size effect. Specifically, a larger distance implies more air between the object and the camera, leading to more attenuation, mostly due to water vapour in the atmosphere. Therefore, the distance should be a user-set parameter in any camera software in order to account for the air path, and the user must always measure relative humidity (especially for outdoor observations) as an additional input parameter. The so-called ‘pixel-size effect’ (Faye, Dangles & Pincebourde, 2016), or ‘minimum spot-size detection’ (Tattersall, 2016), refers to the change in pixel size with distance, which modifies the temperature measured by an infrared camera. One of the most fundamental consequences of this effect occurs at the physical boundary between an object and its surroundings, because both elements may be included in the same pixel, depending on the shooting distance. In this case, the pixel integrates the infrared information originating from both elements, as a combination of the different temperatures at the sub-pixel scale (Murphy et al., 2014). This sub-pixel temperature combination at the physical borders of the studied surface can be avoided by removing the surface boundary edge, i.e. the boundary pixels, in the infrared image. More precisely, the pixel size effect can be related to d by the function: SR = d × θIFOV, where SR is the spatial resolution of the infrared camera (the size of one pixel) and θIFOV the instantaneous field of view in radians (the angle over which the detector senses radiation). For example, infrared images of a mollusc 1 cm long being visualized with a Fluke Ti25 camera (θIFOV = 0.0015 rad) should be taken at the maximum distance at which the organism could reliably be resolved, at d = 6 m. Since SR is the size of one pixel, additional resolving capacity may be required in this example, e.g. 50 or 100 pixels, requiring the image to be obtained at 13.3 or 6.7 cm, respectively. In a real study of the thermal ecology of the intertidal snail Littorina saxatilis in the size range 5 to 8 mm conducted with a Fluke Ti25 camera, the infrared images were taken at less than 30 cm from the snails to ensure a minimum pixel resolution of 0.5 mm (L. Seuront, unpublished data). In this context, the choice of a thermal camera (and implicitly the objective lens attached to it) should be driven by the requirement that the resolution of the camera is compatible with the targeted organisms and the related empirical constraints that are predicted either in situ or ex situ. In practice, the objects of interest should occupy a number of pixels that allows a spatial resolution of c. one tenth of the object size in the final thermal image, and the potential distance effects mentioned above should be empirically assessed, or at least explored mathematically. Atmospheric effects Natural objects do not behave like black bodies, because their emissivity ε is typically lower than 1. As such, a portion (i.e. 1 – ε) of the radiation arriving to the infrared-imaging device originates from the background environment. This background-reflectance temperature can simply be equated to air temperature in indoors applications of infrared thermography (FLIR, 2007). In outdoor applications, the average sky temperature should be considered as the background-reflectance temperature, noting that this temperature will vary with the time of day and cloud cover. Fortunately, in contrast to smooth and polished anthropogenic surfaces that reflect infrared radiation very well (and hence have a low ε), the emissivities of abiotic and biotic objects that are relevant to molluscan research are high. Consequently, the error caused by background reflectance in the estimated temperature is low, producing a maximum error in absolute temperature that is proportional to the reflectivity of the object (1 – ε), which is typically about 5% (Tattersall, 2016). Variations in solar radiation are also known to affect infrared measurements (Faye et al., 2016), in particular because under full-sun conditions significant short-wave reflection is likely to occur (Tattersall, 2016). These facts imply that measurements of short-wave reflectance as well as solar radiant flux have to be performed to ensure that they are stable during the capture of infrared images in full sunlight. A range of atmospheric gases, especially carbon dioxide, ozone and water vapour, influence the radiant energy detected by infrared sensors (Vollmer & Möllmann, 2010). Water vapour is, however, by far the most important absorber of radiation over the range of wavelengths detected by infrared cameras (Vollmer & Möllmann, 2011). The degree to which air absorbs infrared radiation depends on the wavelength. In the MWIR and LWIR bands, this absorption is low, allowing more radiation to reach the sensor of the camera (Usamentiaga et al., 2014). Atmospheric attenuation of infrared radiations is also dependent on the distance between a thermal camera and a target object, and typically increases with distance, e.g. infrared radiations are attenuated by up to 10% over a path length of 100 m and by more than 90% over 10 km. Though Faye, Dangles & Pincebourde (2016) recommended reducing the shooting distance to the lowest possible in order to yield more accurate surface temperatures, this is not always possible. This is where atmospheric radiative-transfer models could be used to correct the surface temperatures according to atmospheric composition. For example, MODTRAN 6 (MODerate resolution atmospheric TRANsmission) includes the effects of molecular and particulate absorption/emission of the atmosphere present between the thermal sensor and the studied object in its solution of the radiative-transfer equation (Berk et al., 2014). For most ecological and biological applications, and in particular in molluscan research, measurements are likely to be conducted at distances between a few centimetres and a few metres, rather than at the scale of kilometres. Humidity nevertheless influences infrared measurements and should ideally be measured, or at least estimated. Most thermal-imaging software incorporates empirical atmospheric-transmission curves for estimating and correcting the loss of signal resulting from the water vapour pressure and distance (Holst, 2000). Note, however, that for the applications of infrared thermography at distances ranging from a few centimetres to a few metres, the effect of atmosphere is negligible and can therefore simply be neglected. On the reliability of shell temperature vs body temperature A fundamental assumption behind the use of infrared imaging in molluscan research is that there is a relationship between the surface (i.e. tissue or shell) temperature and the actual body temperature. Knowledge of this relationship is absolutely necessary to ensure the reliability of noninvasive surface-temperature measurements as a proxy for internal body temperature. In an early infrared-imaging study of the intertidal Nerita atramentosa, Caddy-Retalic et al. (2011) reported highly significant linear relationships between mantle temperature Tm and the maximum temperature of shell thermal images TSmax when thermal images were taken from ventral and dorsal views of the shell in the range 15–55 °C. In order to avoid handling the snails, they recommended use of the dorsal thermal maximum to predict internal mantle temperature, according to the relationship: Tm=1.121TSmax−2.884 ⁠. Infrared imaging of shell surface temperatures have subsequently been used as a proxy for mantle temperatures in other intertidal snails, e.g. N. atramentosa (Chapperon & Seuront, 2011b, 2012; Chapperon et al., 2013), L. scabra (Chapperon & Seuront, 2011a), Echinolittorina peruviana (Rojas et al., 2013), E. malaccana and E. radiata (Seuront & Ng, 2016), in the limpets Patelloida latistrigata (Lathlean, 2014) and Cellana tramoserica (Fraser, 2014; Fraser et al., 2016) and in the littoral bivalves Perna perna and Mytilus galloprovincialis (Lathlean et al., 2016a, b; Zardi et al., 2016). With the exception of two studies (Caddy-Retalic et al., 2011; Lathlean et al., 2016a) that explicitly demonstrated the linear relationship between body temperature and shell temperature, most of the above-mentioned studies did not directly test this on their model systems, instead making the implicit assumption that surface temperature was an accurate proxy of mantle temperature. Also note that in an earlier work, Helmuth (2002) illustrated the potential use of infrared thermography through images of large beds of Mytilus californianus without further quantification of mussel body temperature. In this context, we quantify hereafter the relationship between internal body temperature (measured invasively using a thermocouple inserted through a hole carefully drilled into the shell to avoid damaging underlying tissue) and surface temperature (estimated with infrared thermography) based on a range of terrestrial (Candidula unifasciata, Cepaea nemoralis, Cernuella virgata, Cochlicella acuta and Cornu aspersum) and intertidal molluscs representative of various climates (Afrolittorina africana, A. knysnaensis, Austrolittorina unifasciata, Nodilittorina pyramidalis, Echinolittorina malaccana, E. radiata, E. hawaiiensis (= Littorina picta; smooth and ornamented morphs), Littorina littorea, L. saxatilis (black, white, yellow and striped morphs), Melarhaphe nerotoides, Littoraria pintado, Mytilus edulis, M. galloprovincialis, N. atramentosa, Nucella lapillus (black, white, brown and striped black/white morphs) and P. perna). Note that in contrast to Caddy-Retalic et al. (2011), who estimated Tm from the maximum temperature of the dorsal surface of N. atramentosa, we recommend considering instead the average surface temperature of the whole shell (TS) as recorded through infrared thermography. This measure represents a better metric of the thermal conditions experienced by a mollusc than TSmax ⁠, which may be strongly biased by e.g. the shape of the shell and its orientation towards the sun (L. Seuront, unpublished data). In addition, the equation used by Caddy-Retalic et al. (2011), i.e. Tm=1.121TSmax−2.884 ⁠, suggests that TSmax typically underestimates and Tm overestimates respectively for low and high temperatures, which is not the case when TS is considered (Fig. 10). The Tm of all the above mentioned species and morphs was highly significantly correlated with their surface temperature in the range 20–55 °C (P < 0.001). More specifically, the slope α in the relationship Tm = αTs + β never differs significantly from the theoretical expectation α = 1 (P > 0.05). This indicates that Tm and Ts covary at the same rate in the temperature range 20–55 °C, and hence that mollusc surface temperature can be considered a reliable proxy of internal temperature. Note that this conclusion holds for each of the aforementioned species, irrespective of the size of the individuals. The thermal inertia is, however, species-dependent and size-dependent (L. Seuront, unpublished data). Figure 10. Open in new tabDownload slide Thermocouple laboratory measurements of mantle temperature (Tm) of Nerita atramentosa as a function of the average shell surface temperature assessed using infrared imaging (TIRT), showing that TIRT is a reliable proxy of mantle temperature. The dashed line is the first bisectrix Tm = TIRT. More generally, though shell temperature and body temperature are consistently significantly correlated in a range of molluscan species, some of these relationships have been derived from laboratory experiments conducted under standardized conditions of heat stress, i.e. in the presence of a single source of heat and in the absence of air movement. These conditions differ from those in the field where molluscs are exposed to multiple heat sources and heat-transfer processes (Fig. 6) and may (Fig. 11B, C), or may not (Fig. 11A), control their body temperature through postural behaviour. In addition, when investigated in situ, molluscs may potentially have been exposed to fluctuating thermal radiation before being scrutinized through the lens of infrared thermography. Further information about the potential links between the size and colour of various mollusc species and the rate of heat transfer is therefore still needed, to ensure that shell temperature is indeed a reliable proxy of body temperature. In particular, assessing the thermal inertia of different species, sizes and morphs, under different conditions of radiation and/or when radiation changes, will provide valuable information on how thermal inertia may help molluscs tolerate short periods at or above lethal temperatures. Figure 11. Open in new tabDownload slide Field measurements of mantle temperature (TIRT) of Nerita atramentosa (A), Echinolittorina malaccana (B) and E. radiata (C) as a function of their substratum temperature in winter (open circles) and summer (grey circles). The dashed lines are the first bisectrix TIRT = TSubstratum. (B and C modified from Seuront & Ng, 2016: fig. 1.) Demystifying the link between colour and heat As defined in the sections describing the physics of heat transfer and of infrared thermography, surfaces of different colours may have a similar emissivity and hence share a similar ability to absorb and emit infrared radiation. This understanding must inform the interpretation of surface temperature measured by infrared thermography and the proper set-up of an infrared camera. On the other hand, the colour of an object does have critical implications for its temperature, as colour defines the way it absorbs and reflects visible light, and hence the quantity of light energy being transferred to that object and subsequently converted to heat. This issue is very simple when comparing black and white objects. Because these objects have a similar emissivity, they both absorb light very well in the infrared spectrum. However, a black object absorbs most of the light in the visual spectrum, which is why it appears black. In turn, a white object reflects most of the light in the visual spectrum. Black objects hence overall absorb more heat than white ones, and thus exhibit higher temperature, when exposed to light (Fig. 12A–C). This is not the case, however, when black and white objects are sheltered from solar radiations (Fig. 12D, E), which illustrates the fundamental difference between direct and indirect radiative heat transfer. Figure 12. Open in new tabDownload slide Illustration of the effect of the colour of a surface on its thermal properties. Surface temperature of a chequerboard made of black, grey and white tiles (A) was measured using infrared thermography under direct sunlight at 28 °C (air temperature) in absence of wind (B,C), and in shade where air temperature was 33 °C (D, E). Under direct sunlight, surface temperature of tiles was very heterogeneous both locally along horizontal transects (B) and globally (C), and colour-dependent with TW < TG < TB (where TW, TG and TB are, respectively, surface temperatures of white, grey and black tiles). In contrast, under shaded conditions, surface temperatures were nearly uniform (D, E), with TW = TG = TB. This is shown by shape of temperature transects traced across the board (black lines in C and E); temperature varied as a step-function dependent on tile colour in the sun (B), but was independent of tile colour in shade (D). Note that sharp decrease in temperature observed in (D) between the temperature plateaux is an artefact related to the temperature of the substratum beneath the tiles, which were not tightly jointed. INFRARED THERMOGRAPHY IN MOLLUSCAN RESEARCH: CURRENT APPLICATIONS AND FUTURE PROSPECTS For the sake of generality, the case studies discussed below are based on thermal images taken in a range of environments under different climatic regimes ranging from temperate to tropical latitudes (France, Spain, South Africa, Australia and Hong Kong) using four different thermal-imaging cameras. The images are analysed with the corresponding firmware and software, to provide the reader unfamiliar with thermal imaging with a range of examples of the capabilities offered by this emerging technology. The thermal cameras used were (1) Fluke Ti20 (Fluke Corporation, Everett, WA), (2) Fluke Ti25, (3) Testo 875-1iSR (Testo AG, Germany) and (4) FLIR ThermaCAM S65 (OR), and the resulting thermal images were analysed using, respectively, InsideIR 4.0 v. 2006, SmartView v. 3.2.639.0, IRSoft v. 3.1 and ThermaCAM Researcher Professional v. 2.10 software packages. The thermal performances of the cameras are very similar, with sensitivities ≤ 0.2 °C (Fluke Ti20), ≤ 0.09 °C (Fluke Ti25), < 0.05 °C (Testo) and 0.08 °C (FLIR) and accuracy is 2% or 2 °C, whichever is greater (Fluke and Testo) and fixed at ±0.2 °C (FLIR) by recalibrating the camera every 2 min. The emissivity (ε) was consistently set at 0.95 (Chapperon & Seuront, 2011a, b; Seuront & Ng, 2016). We discuss both recently published and unpublished data taken from a wide range of environments and latitudes, using various terrestrial and intertidal species of molluscs. We highlight, based on studies conducted both in situ and ex situ, the many applications of infrared thermography to molluscan research ranging from individual thermoregulatory behaviour to landscape and community ecology, hence covering spatial scales ranging from millimetres to hundreds of metres. Mapping mollusc habitat thermal heterogeneity One of the major advantages of using infrared thermography rather than traditional single-point temperature measurement devices (e.g. thermocouples, iButtons and infrared thermometers) is that the images they produce allow for simultaneous measurements of multiple individuals, species and communities. Thermal imaging is particularly useful to assess the thermal properties of contrasting adjacent microhabitats (e.g. horizontal and vertical flat rocks and crevices; Fig. 8). The thermal contrast between flat surfaces and crevices discussed above (Fig. 8) is but one case of the influence of overall topographic complexity. As another example (Fig. 13), anthropogenic south-facing intertidal seawalls characterized by distinct topographic complexity were investigated within 1 h under similar conditions of air temperature and solar radiation and were distinguished by their respective thermal heterogeneity, which increased with topographic complexity. The thermal properties of even flat surfaces are affected by their orientation, colour and biogenic cover, which can result in considerable temperature changes over only a few centimetres, as illustrated by a sea wall (Fig. 14A, B). A vertical cement-coated outside wall of a house exhibits a finer-scale variation in its surface temperature in the range 0.5–1 °C (Fig. 14C, D), which is likely to be related to topographic complexity at the sub-centimetre scale and to the even finer-scale heterogeneity of its internal components. These examples illustrate that even slight differences in topography, colour, biogenic cover and internal structure can affect the thermal signature of a substratum, creating thermally complex landscapes. Figure 13. Open in new tabDownload slide Three anthropogenic surfaces (A, B, south-facing intertidal seawalls located in Dover harbour, England; C, Le Portel, France) of increasing topographic complexity (from A to C), shown together with corresponding infrared images (D–F). The spatial patterns of surface temperatures observed along transect drawn across thermal images (black lines in D–F) show that while no significant differences exist in the mean temperature (D, G: T = 25.4 ± 0.8 °C; E, H: T = 25.2 ± 1.2 °C; F, I: T = 25.4 ± 2.3 °C) the thermal heterogeneity markedly increases with topographic complexity. Note different temperature scales in D–F and G–I, and lower temperature observed in crevices (F). Figure 14. Open in new tabDownload slide Digital (A, C) and thermal (B, D) images of high-shore seawall in Dover harbour, England in spring 2015 (A, B) and of Cernuella virgata glued with a mucus holdfast to outside wall of a house in Wierre-Effroy, France, during a hot summer in August 2016 (B, D). Slight changes in verticality, colour and biogenic cover of the seawall lead to clear differences in surface temperature (A, B). In contrast, the structurally uniform wall is thermally homogenous, making thermal signature of C. virgata highly conspicuous (C, D). Scale bars: A = 30 cm; C = 2 cm. Thermal imaging is also advantageous when the presence or absence of one species or individual influences the thermal properties of another. For example, shading by trees typically lowers the temperatures experienced by understorey plants and invertebrates (Fig. 15A, B). Similarly, the distribution of the barnacle Tesseropora rosea on Australian rocky shores was shown to affect the small-scale patterns of substratum temperature, and hence the abundance and distribution of the small limpet Patelloida latistrigata (Lathlean, 2014; Fig. 15C, D). Other ecosystem engineers such as mussels generate thermally favourable free space, protecting associated invertebrate communities and individuals from heat and desiccation stress (Lathlean et al., 2016a; Fig. 15E, F). Figure 15. Open in new tabDownload slide Digital and infrared images illustrating the thermal buffering properties of biogenic structures such as mangrove vegetation (A, B), ecosystem engineers such as the barnacle Tesseropora rosea (C, D) and the mussels Perna perna and Mytilus galloprovincialis (E, F). The detection of all the above-mentioned small-scale thermal properties of the habitat, though essential to understanding of the physiology, biology and ecology of individual molluscs, could not have been captured by traditional single-point temperature measurements and was only possible through the use of infrared thermography. Mollusc size and shape matters when feeling the heat Body size is an important parameter to consider in thermal ecology, because heat conduction depends on the distance heat has to travel and on the surface-to-volume ratio (see account of physics of heat transfer, above). To illustrate the potential effect of size on heating rate and maximal body temperature, we generated heating curves using biomimetic models (Helmuth, 1998; Denny & Harley, 2006; Denny et al., 2011; Miller & Denny, 2011) of the high-shore gastropod Austrolittorina unifasciata. Biomimetic snails of different sizes (5 mm: n = 3; 10 mm: n = 7; 15 mm: n = 5) were created using hollowed out A. unifasciata shells filled with 3 M Scotchcast 2130 Flame Retardant Compound (Lima & Wethey, 2009). Biomimetic snails were fitted with fine K-type thermocouples and maintained at 20 °C in a cooler until they were fixed with cyanoacrylate glue (Loctite Superglue) onto flat limestone with the aperture orientated towards the substratum (Tsubstratum = 40 ± 1 °C) either (1) in direct sunlight or (2) in shade. Shading was achieved following Marshall & Chua (2012) by using 7, 12 and 17-mm diameter discs supported directly above the shells by fine wires leading from the surface; this ensured only the shells and not the surrounding surfaces were shaded. The difference in the temperature dynamics between the sunned and shaded biomimetic shells demonstrated the direct and indirect effects of heat transfer towards A. unifasciata. The former were heated by direct solar radiation, convection and conduction from the substratum, while the latter were affected only by convection and conduction (Marshall & Chua, 2012). Simultaneous recordings of the snail models were made every 30 s between 11 am and 1 pm on a rocky platform in Lincoln National Park (Australia) on 12 March 2013, when air and limestone surface temperatures were 28 ± 1 °C and 40 ± 1 °C, respectively. The temporal dynamics of the temperature Ti of A. unifasciata models of size i were consistently highly significantly (P < 0.01) fitted by equations of the form, Ti(t)=T0+(Tmaxt/(tm+t))/ki ⁠, where T0 and Tmax are, respectively, the initial and maximal temperatures of the models (T0 = 20 °C), t the time, tm the time at which Ti(t) = Tmax/2, and ki an empirical constant. No significant differences were found in the maximal temperature Tmax (43.9 °C ± 0.5 SD) reached by biomimetic snails of different sizes when exposed to solar radiation (Kruskal-Wallis test, P > 0.05; Zar, 1999). In contrast, tm differed significantly with size (Kruskal-Wallis test, P < 0.05)—the smaller the snails the shorter tm (3, 7 and 13 min for snails 5, 10 and 15 mm in length, respectively). The difference in Tmax estimated for sunned and shaded models also differed significantly with size (P < 0.05) (ΔT = 2.1, 1.6 and 1.4 °C for models 5, 10 and 15 mm in length, respectively). These results are consistent with previous work (Marshall & Chua, 2012) and indicate that (1) the smaller the snail, the faster it warms up, (2) snails of different sizes eventually attain similar maximal temperatures (in less than 2 h under the conditions considered here), and (3) the effect of direct solar radiation is minor, representing between 3.9% and 6.1% of the overall heating. A similar approach was used to assess the effect of shell shape on the heating rates of four species of co-occurring gastropods, Gibbula cineraria, G. umbilicalis, Phorcus (=Osilinus) lineatus and Littorina littorea. The shell surface-to-volume ratio was approximated by the shell aspect ratio (Sar) calculated as Sar = shell height/shell width. Heating rates were estimated for each species for standardized snail sizes in the range 10.7–12.0 mm using the biomimetic approach described above. The biomimetic snails were maintained at room temperature (15 °C) on granite tiles and subsequently placed under infrared lamps (Phillips PAR38) until they reached a stable temperature. Significant differences were found between Sar (Kruskal-Wallis test, and subsequent multiple comparison procedure, P < 0.05; Zar, 1999) with Sar(G. umbilicalis) < Sar(G. cineraria) = Sar(P. lineatus) < Sar(L. littorea). No significant differences were found in Tmax (44.9 °C ± 0.5 SD) reached by biomimetic snails of the four species (Kruskal-Wallis test, P > 0.05). In contrast, tm differed significantly with size (Kruskal-Wallis test, P < 0.05) and tm was longer for a smaller Sar (14 min for L. littorea, Sar = 0.73 ± 0.05; 18 and 19 min for G. cineraria, Sar = 0.58 ± 0.04, and P. lineatus, Sar = 0.56 ± 0.03; 23 min for G. umbilicalis, Sar = 0.53 ± 0.02). Species with a higher surface-to-volume ratio, i.e. higher Sar, heat up significantly more quickly than flatter species. Lastly, using artificially constructed mussel beds composed of Perna perna, Lathlean et al. (2016b) investigated how the size, position and structure of the beds affected the body temperatures of individual mussels within each bed (Fig. 16). Results revealed that small individuals reached higher body temperatures than large individuals, irrespective of mussel-bed size. However, contrary to expectations, average body temperatures and heating rates of individuals within large mussel beds were generally greater than for individuals within small mussel beds. This was thought to be due to differences in convective cooling of large and small mussel beds, since individuals on the leeward side of all beds displayed body temperatures 3–5 °C greater than those on the windward side (Fig. 16A, B). Figure 16. Open in new tabDownload slide Thermograms of artificial Perna perna beds (20 cm in diameter; inset) observed on a flat rocky reef at Jorgensfontein, South Africa, in absence (A) and presence (B) of wind (direction indicated by arrow in B). Individuals on windward side of beds displayed body temperatures 3–5 °C lower than those on leeward side, explained by convective cooling. Thermal heterogeneity within a community A major advantage of using infrared thermography as a tool for measuring in situ thermal variability is that it can simultaneously record fine-scale differences in the body temperatures of numerous individuals within a community. This is particularly relevant in community ecology as all species may not deal similarly with thermal stress, even if they live in the same microhabitat. In this context, inter-individual thermal variability may shed new light on our understanding of key ecological concepts such as keystone species and the stability of community structure (Paine, 1969, 1995). More generally, this is important in an era when increased temperatures associated with climate change are expected to impact different species within ecological communities in different ways. In recent years, much attention has been given to identifying which species within communities are most vulnerable to further increases in temperature, in order to predict how changes in their relative abundance may impact the direction and strength of species interactions (Kordas, Harley & O’Connor, 2011). Infrared thermography can reveal how multiple species within a community respond to contemporary and future levels of heat stress, thus providing a glimpse of how such communities may respond and adapt to climate change. One recent case study that explores this process using infrared thermography was undertaken on rocky intertidal communities along the south coast of South Africa (Lathlean et al., 2016a). Here, the invasive mussel Mytilus galloprovinicialis is found interspersed among mid-intertidal aggregations of the indigenous mussel Perna perna. While belonging to the same family, these two species display different behavioural responses to heat stress during aerial exposure. During emersion, P. perna exhibits periodic closure and opening of the shell (gaping); this behaviour allows the maintenance of aerobic respiration, but increases levels of water loss and the risk of desiccation due to both evaporation and expulsion of water during valve closure. In contrast, M. galloprovincialis keeps its valves closed when exposed to air. This behaviour reduces the risk of desiccation, but decreases the efficiency of anaerobic respiration (Nicastro et al., 2010). These differences in thermoregulatory behaviour result in dramatically different body temperatures, even though individuals are found within the same microhabitat. Through the use of infrared thermography, Lathlean et al. (2016a) were able not only to show that P. perna, when aggregated, maintained lower body temperatures than M. galloprovincialis during exposure to identical levels of heat stress, but also that when interspersed among aggregations of P. perna the invasive M. galloprovincialis benefitted from the evaporative cooling behaviour of the former. Without the use of infrared thermography this interaction could have only been discovered had the researchers simultaneously (though unrealistically) taken thousands of intrusive thermocouple measurements of both species in the field. The use of biomimetic loggers to measure body temperatures of the two species would also have been inappropriate, since such devices cannot model differences in thermoregulatory behaviour of living animals. Intertidal mussels may play an important role as ecosystem engineers, their sometimes extensive aggregations serving to buffer associated epifaunal communities from unfavourable conditions such as heat stress and wave exposure. The effectiveness of mussel beds in providing thermal refugia for other intertidal molluscs may vary depending upon geographic location as well as on the size and structure of the mussel beds themselves. Recent research has used infrared thermography show that both the size of mussel beds and the size of individual mussels within the bed, influence the amount of heat stress experienced by both mussels and their epifaunal communities (Lathlean et al., 2016a). Infrared images have also been used to demonstrate high inter-individual variability in body temperatures of mussels within beds. Thermal gradients of 4–5 °C were found to exist across mussel beds as small as 20 cm2 during extreme heat events with mussels on the windward side displaying cooler temperatures than those on the leeward side of the mussel bed (Lathlean et al., 2016b; Fig. 16A, B). Noticeably, the observed inter-individual variability in body temperatures was three to four times greater than interspecific variability. Observations using infrared thermography have also shown that body temperatures of adjoining mussels orientated perpendicular to the sun can differ by up to 2–3 °C (J.A. Lathlean, unpublished data). Such inter-individual variability within mussel beds may have significant implications for predicting how these ecosystem engineers, and by extension their associated invertebrate communities, may respond and adapt to the increasing frequency and intensity of extreme heat events associated with climate change. Thus, infrared cameras are an important tool for marine conservationists and environmental managers interested in monitoring and predicting responses of molluscan populations to climate change. Thermoregulatory behaviour Despite the widely acknowledged role of a suite of postural behaviours in both marine and terrestrial molluscs to reduce heat conduction from their substrata, as well as reduce water lost through evaporation and/or increase convective cooling by air currents (as reviewed above), little is yet known about the mechanisms driving these behaviours. Marshall & Chua (2012) showed that shell-standing behaviour was triggered by the presence of a temperature gradient in the boundary-layer air close to (<4 mm) the solar-heated rock surface and was not observed when snails were heated in the absence of this gradient. Seuront & Ng (2016) showed that postural behaviours (including shell-lifting, shell-standing and towering) occurred in summer, but not in winter, in the high-shore Echinolittorina malaccana and E. radiata. While these results suggest that postural behaviour may be driven by the temperature of the substratum, Seuront & Ng (2016) did not find any significant relationship between the type of postural behaviour and substratum temperature. Recent fieldwork conducted on Austrolittorina unifasciata in Australia and Littorina saxatilis in Spain nevertheless indicated that postural behaviour only occurred when substratum temperature reached a critical temperature (L. Seuront, unpublished data; Fig. 17). Thus L. saxatilis started exhibiting shell-lifting and shell-standing behaviour at substratum temperatures above 36 °C (Fig. 17A). In A. unifasciata, shell-lifting and shell-standing occurred above 38.8 °C, and shell-towering above 41 °C (Fig. 17B). Figure 17. Open in new tabDownload slide Body temperature (TBody) of the high-shore Littorina saxatilis (A) and Austrolittorina unifasciata (B), shown as a function of their substratum temperature (TSubstrate). Dotted line is first bisextrix, TBody = TSubstrate; vertical dashed line is critical temperature above which snails exhibit postural behaviour. In A the black, grey, orange and white points represent four L. saxatilis morphotypes, respectively black, black-and-white striped, orange, and white; circles and the triangles represent, respectively, individuals lying flat on substratum and shell standing. In B the white, black, red and blue points represent, respectively, A. unifasciata exhibiting no postural behaviour, shell-lifting/shell-standing, and individuals at top and bottom of towers. Though further work is needed to decipher the relationship between the temperatures of molluscs, that of their substrata and their postural behaviour, infrared thermography presents the unique and desirable advantage of allowing multiple measurements of body and substratum temperatures, which is not achievable using traditional single-point temperature measurement devices such as thermocouples, iButtons or infrared thermometers. Mollusc colour polymorphism and thermal properties The potential role of shell colour in regulating body temperature of molluscs is still poorly investigated, despite shell colour polymorphism being a common feature of the populations of many marine and terrestrial molluscs (e.g. Mitton, 1977; Clarke et al., 1978; Clarke, 1979; Johnson, 1980, 1981; Heller, 1981; Raffaelli, 1982; Cain, 1983, 1988; Cowie & Jones, 1985; Etter, 1988; Rehfeld, 1997). The relevance of this aspect of mollusc thermal ecology is illustrated by two examples: the effect of shell colour modification by parasites on body temperatures of mussels and the effect of shell colour on the body temperature of the highly polymorphic Littorina saxatilis. The shells of many molluscs, including mussels and oysters, are often infested with endolithic parasites, which bore into and discolour the exterior surface (Kaehler, 1999; Zardi et al., 2016). In some cases infestations can be so severe that the shell is weakened and must be strengthened by internal shell deposition, resulting in depletion of energy resources (Kaehler & McQuaid, 1999; Zardi et al., 2009). Contrary to this negative relationship between parasite and host, Zardi et al. (2016) used infrared thermography to reveal that phototrophic shell-boring cyanobacteria have a positive, cooling effect on mussel body temperatures during extreme heat events (Fig. 18A). This beneficial effect was due to the white discolouration of the shell and the increased rugosity of the shell surface caused by the excavation activity of the cyanobacteria. Such results have implications for our understanding of mutualistic and parasitic relationships and how these relationships might be expected to change under different climates. This study also demonstrates a potential use of infrared thermography to identify and manage parasitic outbreaks among natural and cultivated populations of mussels and oysters, which are commonly infested with endolithic cyanobacteria. Figure 18. Open in new tabDownload slide Illustration of effect of different shell colours on mollusc body temperature. A. Infrared images of South African Perna perna, showing decrease in body temperature of individuals completely covered by endolithic parasites that cause discolouration (inset, P), when compared with individuals free of parasites (inset, NP; modified from Lathlean et al., 2017: fig. 7). B. The ratio RT (a standardized measure of difference between body temperature Tb and substratum temperature Ts) of the highly polymorphic high-shore Littorina saxatilis did not differ significantly between colour morphotypes (insets) and did not differ significantly from RT = 1, indicating (1) absence of an effect of shell colour on L. saxatilis body temperature and (2) thermal homogeneity between L. saxatilis and its substratum. The polymorphic intertidal snail L. saxatilis is a particularly relevant species for thermal study as it has an unusually wide latitudinal distribution (ranging from South Africa to Svalbard; Reid, 1996; Branch et al., 2010), it occurs in diverse habitats (from sheltered estuaries to highly exposed rocky shores; Clarke, Mill & Grahame, 2000), it is found at most intertidal levels (Sokolova et al., 2000), and can withstand temperatures of up to 35 °C for at least several hours during summer low tides and up to 47 °C during short-term acute heating events (Sokolova et al., 2000). Despite the extreme variability in shell coloration in L. saxatilis (Reid, 1996) and the amount of work conducted on the selective forces controlling colour polymorphism (Ekendahl & Johannesson, 1997; Johannesson, 2003, 2016), there is still a paucity of information on the potential links between shell colour and body temperature of L. saxatilis. Selection processes related to colour include visual selection for cryptic coloration by predators (Johannesson & Ekendahl, 2002; Surmacki et al., 2013) and physiological selection arising from the genetic correlation between shell colour and the physiological response to salinity (Sokolova & Berger, 2000) and to direct thermal selection (Berger, Bogdanov & Sergievsky, 1995). The potential differences in heating rate and maximal body temperature of colour morphs have been investigated by generating heating curves using biomimetic snails of the four colour morphs (black, white, yellow, and black-and-white striped; Fig. 18B) of a high-shore Galician L. saxatilis population (L. Seuront, unpublished data). Biomimetic snails (prepared following Lima & Wethey, 2009) were fixed with cyanoacrylate glue onto flat granite rocks with aperture towards the substratum under direct sunlight or in shade (created following Marshall & Chua, 2012, as described above). For each colour morph, shells (6–7 mm in diameter) were fitted with fine K-type thermocouples (glued inside the shell) and their temperatures simultaneously recorded every 30 s until they reached stable maxima. All measurements were conducted over 2-h periods around solar midday under sunny conditions (solar irradiance 975–1035 W m–2) in the absence of wind with air temperature ranging between 34.2 and 35.6 °C and substratum temperature in the range 42–45 °C. Using a protocol similar to that described above (see example of A. unifasciata of different sizes), it was shown that the temperature of the four biomimetic colour morphs converged towards Tmax within 60 min. No significant differences were found in Tmax between morphs (P > 0.05; Tmax = 41.3 ± 1.4 °C), though the temperature of the black morph increased significantly faster than in other morphs (P < 0.05). The heating rate (estimated as tm, the time needed to reach a temperature Tmax/2) was significantly faster (on average twice as fast) in the biomimetic snails exposed directly to the sun (P < 0.05). This result indicates that direct and indirect heat transfers have comparable contribution to L. saxatilis body temperature. The absence of differences in Tmax between morphs is consistent with field observations of Tb and Ts of the four colour morphs of L. saxatilis considered here; in which the body-to-substratum temperature ratio (BST = Tb/Ts; introduced by Chapperon & Seuront, 2011a, as a standardized measure of the difference between substratum and snail body temperatures) did not significantly differ between morphs (P > 0.05; Fig. 18B). These observations are congruent with both evidence of dark morphs heating up faster than light ones (Etter, 1988) and of the absence of temperature differences in intertidal molluscs varying in structure, shape, size and colour (Miller & Denny, 2011; Cox & Smith, 2011). They nevertheless suggest a decoupling between the heating rate and the maximal temperature reached by molluscs of different colours. Infrared thermography: a tool for monitoring the impacts of climate change on molluscs? A major difficulty for climate-change biologists is the spatial mismatch between the size of organisms and the resolution at which global climate data are collected and modelled: the grid sizes of climate models are on average four orders of magnitude larger than the animals they study (Potter et al., 2013; Torossian, Kordas & Helmuth, 2016). This is particularly critical for minute organisms, because microclimatic conditions often deviate substantially from those generated by the available models (Faye et al., 2014; Hannah et al., 2014; Scheffers et al., 2014a), hindering opportunities to study biotic responses to global warming (Storlie et al., 2014; Scheffers et al., 2014b; Pincebourde & Casas, 2015). There is an urgent need for microclimatic modelling at spatial scales appropriate to organisms, so that mechanistic models at individual levels can be incorporated into models of species distribution and vulnerability to climate change (Potter et al., 2013). Monitoring microclimates at scales relevant to individual organisms is, however, a daunting task owing to the diverse spatial and temporal patterns of microclimatic variation, while climate change at a global scale generates even more complexity (Woods, Dillon & Pincebourde, 2015). As emphasized in the present work, one of the essential features of infrared thermography, especially when compared with traditional single-point temperature measurements, is that thermal images allow for simultaneous measurements of multiple individuals, species and communities. Combining infrared thermography with new three-dimensional photographic techniques, spectrometers and lightweight unmanned aerial vehicles (i.e. drones) may be a first step in producing fine-scale thermal maps of entire ecosystems at scales pertinent to individual organisms (Lathlean & Seuront, 2014; Faye et al., 2016). In this context, we suggest that infrared thermography could play a major role in developing and improving environmental management and conservation plans for systems vulnerable to future climate change in general, and for both terrestrial and intertidal molluscs in particular. Such thermal maps would increase the computational power of ecological models designed to predict how and when specific organisms will respond to future climate change. This approach could be used to identify areas or microhabitats that (1) will act as thermal refugia for intertidal organisms during future extreme heat events, (2) qualify for increased conservation status because they exhibit reduced thermal heterogeneity, and (3) present increased likelihood of restoration success if a target species is transplanted to the area. These issues are pertinent for molluscs that live in particularly heterogeneous habitats, since a recent study showed theoretically that ectotherms thermoregulate more accurately when thermal resources are spatially dispersed than when clumped (Sears et al., 2016). This prediction was supported by observations of thermoregulatory behaviours of lizards in outdoor arenas with known temperature distributions. In practice, the thermal quality of a given habitat could be quantified through a generalization of BST. For instance, knowing the thermal tolerance limit of a species (i.e. heat coma and lethal temperatures) and the thermal property of a given habitat recorded in space and time through infrared thermography, it is possible to produce an indicator of the suitability of a habitat to an organism (or species) i as: BSTi = Tb(i)/Ts, where Tb(i) is the organismal coma or lethal temperature of i. Areas where BSTi < 1 and BSTi > 1 will then be considered as viable or not for the species. More generally, a critical BSTi could be defined as: BSTc = Tsc/Ts, where Tsc is a critical surface temperature (either minimal or maximal) returned by climatic scenarios and Ts the substratum temperature actually measured using infrared thermography at scales pertinent to individual organisms (Lathlean, Seuront & Ng, 2017). This approach is notable because (1) it explicitly takes into account small-scale heterogeneity of habitat (e.g. crevices, pits, boulders and flat rocks) that defines a species’ thermal landscape, and hence its realized ecological niche, and (2) it represents a first step to bridge the gap between field-based approaches that typically span from centimetres to tens of metres to climate scenarios that are generally coarse-grained (i.e. 10 × 10 km). Torossian et al. (2016) have discussed the mismatch between scales of climatic observations and the much-needed biological details. In an era where much attention has been given to predicting which species are going to be ‘winners’ or ‘losers’ under future climate-change scenarios (Somero, 2010), as well as how changes in the relative abundance of different species may impact the direction and strength of species’ interactions (Kordas et al., 2011) and demographic responses (Kordas & Harley, 2016), the use of infrared thermography as a tool for monitoring and predicting changes in community structure is appealing. This is important for both natural and harvested mollusc populations that are under increasing threat of both ocean warming and acidification (Barton et al., 2012). As recently stressed (Lathlean et al., 2017), infrared thermography not only offers a glimpse of how multiple species within a community may respond to contemporary and future levels of heat stress, but can also reveal which individuals within a population are most susceptible to elevated heat stress (e.g. Lathlean et al., 2016b). If genetically determined, it is this inter-individual variability among populations that will largely determine whether a population will be capable of adapting to the rapidly changing climate. CONCLUSIONS: MOLLUSCAN RESEARCH MAY WELL FEEL THE HEAT Both the reviews and the case studies presented here demonstrate that infrared thermography is an effective tool for investigating a range of ecological patterns and processes from a unique perspective. In particular, it has the desirable advantage over traditional single-point temperature measurements (e.g. thermocouples, iButtons and infrared thermometers) in that the images it produces allow for simultaneous measurements of multiple molluscan individuals, species and communities. However, even though the number and diversity of ecological applications of infrared thermography has steadily risen over the last two decades, due to increasingly portable and affordable infrared-imaging technology, its use in molluscan research is still in its infancy. This is especially true in terrestrial ecosystems, where only a very few of the many mollusc habitat types and taxa have been sampled (e.g. Lathlean & Seuront, 2014; Lathlean et al., 2017). Uniquely, infrared thermography has the potential to bridge the long-acknowledged gap between scales of actual observations and the much-needed biological details (Potter et al., 2013; Torossian et al., 2016). This is achievable through a better quantification of microclimates across appropriate spatial and temporal scales, so that mechanistic models at the individual levels can ultimately be better incorporated into models of species distribution and vulnerability to climate change. In this context, we suggest that infrared thermography should play a key role in understanding and managing how molluscan species, populations and communities and their environments will be affected by increasing temperatures associated with climate change. It is apparent from both the inherent complexity of patterns and processes involved in molluscan thermal biology, and from the wide range of applications of infrared thermography in molluscan research, that our journey towards understand the ecology of molluscs from a bottom-up approach—through the lens of infrared thermography—is still in an early stage. ACKNOWLEDGEMENTS Editor David Reid is warmly acknowledged for his interest in our work, for inviting us to write this review, and for his insightful comments and suggestions on the accepted version of this work. Sylvain Pincebourde is acknowledged for his thorough review of a previous version of this manuscript. Four anonymous reviewers are thanked for their constructive criticisms and suggestions, which greatly improved this work, especially with regards to the physics of heat transfer. K. Nicastro, G. Zardi and C. McQuaid are acknowledged for numerous stimulating discussions on infrared imaging and the thermal ecology of molluscs. Special thanks to Associate Editor Mark Davies for all his advice and suggestions, as well as for thoroughly editing two previous versions of this work; his efforts considerably improved its quality. 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. 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 the Australian Research Council’s Discovery Projects funding scheme (projects DP0664681 and DP0988554), a Bonus Qualité Recherche (BQR) International (Axe 3a) from the University of Lille 1—Sciences and Technologies. This work is a contribution to the CPER research project CLIMIBIO. The authors thank the French Ministère de l’Enseignement Supérieur et de la Recherche, the Hauts de France Region and the European Funds for Regional Economical Development for their financial support for this project. REFERENCES Adamczyk , J.G. , Krasowska , I., Boguszewski , D. & Reaburn , P. 2016 . The use of thermal imaging to assess the effectiveness of ice massage and cold-water immersion as methods for supporting post-exercise recovery . Journal of Thermal Biology , 60 : 20 – 25 . Google Scholar Crossref Search ADS PubMed WorldCat Allen , J.P. & Mininberg , D.T. 2005 . The art of medicine in ancient Egypt . Metropolitan Museum of Art , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Angilletta , M.J. 2013 . Thermal adaptation: a theoretical and empirical synthesis . Oxford University Press , Oxford . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Angilletta , M.J. & Krochmal , A.R. 2003 . The thermochron: a truly miniature and inexpensive temperature logger . Herpetological Review , 34 : 31 – 32 . Google Scholar OpenURL Placeholder Text WorldCat Balaji , C. 2015 . Essentials of radiation heat transfer . John Wiley , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Barnes , D.K.A. , Hodgson , D.A., Convey , P., Allen , C.S. & Clarke , A. 2006 . Incursion and excursion of Antarctic biota: past, present and future . Global Ecology and Biogeography , 15 : 121 – 142 . Google Scholar Crossref Search ADS WorldCat Barnhart , M.C. & McMahon , B.R. 1987 . Discontinuous CO2 release and metabolic depression in dormant land snails . Journal of Experimental Biology , 128 : 123 – 138 . Google Scholar OpenURL Placeholder Text WorldCat Barr , E.S. 1960 . Historical survey of the early development of the infrared spectral region . American Journal of Physics , 28 : 42 – 54 . Google Scholar Crossref Search ADS WorldCat Barr , E.S. 1961 . The infrared pioneers—I. Sir William Herschel . Infrared Physics , 1 : 1 – 4 . Google Scholar Crossref Search ADS WorldCat Barr , E.S. 1962 . The infrared pioneers—II. Macedonio Melloni . Infrared Physics , 2 : 67 – 73 . Google Scholar Crossref Search ADS WorldCat Barton , A. , Hales , B., Waldbusser , G.G., Langdon , C. & Feely , R.A. 2012 . The Pacific oyster, Crassostrea gigas, shows negative correlation to naturally elevated carbon dioxide levels: implications for near-term ocean acidification effects . Limnology and Oceanography , 57 : 698 – 710 . Google Scholar Crossref Search ADS WorldCat Beaugrand , G. 2015 . Marine biodiversity, climate variability and global change. In: Routledge . Taylor & Francis , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Bejan , A. 2013 . Convection heat transfer . Wiley , New York . Google Scholar Crossref Search ADS Google Preview WorldCat COPAC Berger , V. , Bogdanov , D. & Sergievsky , S. 1995 . The role of shell colour polymorphism in temperature adaptations of the gastropod Littorina saxatilis (Olivi) . Proceedings of the Zoological Institute of the Russian Academy of Science , 264 : 46 – 60 . Google Scholar OpenURL Placeholder Text WorldCat Berk , A. , Conforti , P., Kennett , R., Perkins , T., Hawes , F. & van den Bosch , J. 2014. MODTRAN6: a major upgrade of the MODTRAN radiative transfer code . Proceedings of SPIE 90880, Algorithms and technologies for multispectral, hyperspectral, and ultraspectral imagery XX (International Society for Optics and Photonics), 90880H. Best , R.G. & Fowler , R. 1981 . Infrared emissivity and radiant surface temperatures of Canada and snow geese . Journal of Wildlife Management , 45 : 1026 – 1029 . Google Scholar Crossref Search ADS WorldCat Biberman , L.M. & Sendall , R.L. 2000 . A brief history of imaging devices for night vision. In: Electro-optical imaging: system performance and modelling ( L.M. Biberman, ed.), pp. 1 – 26 . SPIE Press , Bellingham, WA . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Bingham , F.O. 1972 . The influence of environmental stimuli on the direction of movement of the supralittoral gastropod Littorina irrorata . Bulletin of Marine Science , 22 : 309 – 335 . Google Scholar OpenURL Placeholder Text WorldCat Bishop , T. & Brand , M.D. 2000 . Processes contributing to metabolic depression in hepatopancreas cells from the snail Helix aspersa . Journal of Experimental Biology , 203 : 3603 – 3612 . Google Scholar PubMed OpenURL Placeholder Text WorldCat Bouzida , N. , Bendada , A. & Maldague , X.P. 2009 . Visualization of body thermoregulation by infrared imaging . Journal of Thermal Biology , 34 : 120 – 126 . Google Scholar Crossref Search ADS WorldCat Bownes , S.J. & McQuaid , C.D. 2006 . Will the invasive mussel Mytilus galloprovincialis Lamarck replace the indigenous Perna perna L. on the south coast of South Africa? Journal of Experimental Marine Biology and Ecology , 338 : 140 – 151 . Google Scholar Crossref Search ADS WorldCat Bradshaw , W.E. & Holzapfel , C.M. 2006 . Evolutionary response to rapid climate change . Science , 312 : 1477 – 1478 . Google Scholar Crossref Search ADS PubMed WorldCat Branch , G.M. , Griffiths , C.L., Branch , M.L. & Beckley , L.E. 2010 . Two oceans. A guide of the marine life of southern Africa . Struik Nature , Cape Town . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Branch , G.M. & Steffani , C.N. 2004 . Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck) . Journal of Experimental Marine Biology and Ecology , 300 : 189 – 215 . Google Scholar Crossref Search ADS WorldCat Brischoux , F. , Bonnet , X. & Shine , R. 2009 . Kleptothermy: an additional category of thermoregulation, and a possible example in sea kraits (Laticauda laticaudata, Serpentes) . Biology Letters , 5 : 729 – 731 . Google Scholar Crossref Search ADS PubMed WorldCat Britton , J.C. 1992 . Evaporative water loss, behaviour during emersion, and upper thermal tolerance limits in seven species of eulittoral-fringe Littorinidae (Mollusca: Gastropoda) from Jamaica. In: Proceedings of the Third International Symposium on Littorinid Biology ( J. Grahame, P.J. Mill & D.G. Reid, eds), pp. 69 – 83 . Malacological Society of London , London . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Britton , J.C. 1995 . The relationship between position on shore and shell ornamentation in two size-dependent morphotypes of Littorina striata, with an estimate of evaporative water loss in these morphotypes and in Melarhaphe neritoides . Hydrobiologia , 309 : 129 – 142 . Google Scholar Crossref Search ADS WorldCat Britton , J.C. & McMahon , R.F. 1986 . The relationship between vertical distribution evaporative water loss rate behavior and some morphometric parameters in four species of rocky intertidal gastropods from Hong Kong. In: Proceedings of the Second International Marine Biological Workshop: the marine flora and fauna of Hong Kong and southern China ( B. Morton, ed.), pp. 1153 – 1171 . Hong Kong University Press , Hong Kong . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Cabanac , M. & Rossetti , Y. 1987 . Fever in snails, reflection on a negative result . Comparative Biochemistry and Physiology A , 87 : 1017 – 1020 . Google Scholar Crossref Search ADS WorldCat Caddy-Retalic , S. , Benkendorff , K. & Fairweather , P.G. 2011 . Visualizing hotspots: applying thermal imaging to monitor internal temperatures in intertidal gastropods . Molluscan Research , 31 : 106 – 113 . Google Scholar OpenURL Placeholder Text WorldCat Caillon , R. , Suppo , C., Casas , J., Woods , H. & Pincebourde , S. 2014 . Warming decreases thermal heterogeneity of leaf surfaces: implications for behavioural thermo- regulation by arthropods . Functional Ecology , 28 : 1449 – 1458 . Google Scholar Crossref Search ADS WorldCat Cain , A.J. 1983 . Ecology and ecogenetics of terrestrial molluscan populations. In: The mollusca , Vol. 6 ( W.D. Russell-Hunter, ed.) Russell-Hunter W.D., pp. 597 – 647 . Academic Press , New York . Ecology. Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Cain , A.J. 1988 . The colours of marine bivalve shells with special reference to Macoma balthica . Malacologia , 28 : 289 – 318 . Google Scholar OpenURL Placeholder Text WorldCat Cain , A.J. & Sheppard , P.M. 1954 . Natural selection in Cepaea . Genetics , 39 : 89 – 116 . Google Scholar PubMed OpenURL Placeholder Text WorldCat Cameron , R.A.D. & Cook , L.M. 2012 . Habitat and the shell polymorphism of Cepaea nemoralis (L.): interrogating the Evolution Megalab database . Journal of Molluscan Studies , 78 : 179 – 184 . Google Scholar Crossref Search ADS WorldCat Cartwright , S.R. & Williams , G.A. 2012 . Seasonal variation in utilization of biogenic microhabitats by littorinid snails on tropical rocky shores . Marine Biology , 159 : 2323 . Google Scholar Crossref Search ADS PubMed WorldCat Cengel , Y.A. 2003 . Heat transfer. A practical approach . McGraw-Hill , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Chang , H.W. 1991 . Activity and weight loss in relation to solar radiation in the polymorphic land snail Cepaea nemoralis . Journal of Zoology , 225 : 213 – 225 . Google Scholar Crossref Search ADS WorldCat Chang , H.W. & Emlen , J.M. 1993 . Seasonal variation of microhabitat distribution of the polymorphic land snail Cepaea nemoralis . Oecologia , 93 : 501 – 507 . Google Scholar Crossref Search ADS PubMed WorldCat Chapman , M.G. & Underwood , A.J. 1996 . Influences of tidal conditions, temperature and desiccation on patterns of aggregation of the high-shore periwinkle, Littorina unifasciata, in New South Wales, Australia . Journal of Experimantal Marine Biology and Ecology , 196 : 213 – 237 . Google Scholar Crossref Search ADS WorldCat Chapperon , C. , Le Bris , C. & Seuront , L. 2013 . Thermally-mediated body temperature, water content and aggregation behaviour in the intertidal gastropod Nerita atramentosa . Ecological Research . doi10.1007/s11284-013-1030-4 . Google Scholar OpenURL Placeholder Text WorldCat Chapperon , C. & Seuront , L. 2011 a. Space-time variability in environmental thermal properties and snail thermoregulatory behaviour . Functional Ecology , 25 : 1040 – 1050 . Google Scholar Crossref Search ADS WorldCat Chapperon , C. & Seuront , L. 2011 b. Behavioral thermoregulation in a tropical gastropod: links to climate change scenarios . Global Change Biology , 17 : 1740 – 1749 . Google Scholar Crossref Search ADS WorldCat Chapperon , C. & Seuront , L. 2012 . Keeping warm in the cold: on the thermal benefits of aggregation behaviour in an intertidal ectotherm . Journal of Thermal Biology , 37 : 640 – 647 . Google Scholar Crossref Search ADS WorldCat Chase , R. , Croll , R.P. & Zeichner , L.L. 1980 . Aggregation in snails, Achatina fulica . Behavioural and Neural Biology , 30 : 218 – 230 . Google Scholar Crossref Search ADS WorldCat Chelazzi , G. , Della Santina , P. & Vannini , M. 1985 . Long-lasting substrate marking in the collective homing of the gastropod Nerita textilis . Biological Bulletin , 168 : 214 – 221 . Google Scholar Crossref Search ADS WorldCat Chelazzi , G. , Innocenti , R. & Della Santina , P. 1983 . Zonal migration and trail following of an intertidal gastropod analysed by LED tracking in the field . Marine Behaviour and Physiology , 10 : 121 – 136 . Google Scholar Crossref Search ADS WorldCat Chukwuka , C.O. , Ejere , V.C., Asogwa , C.N., Nnamonu , E.I., Okeke , O.C., Odii , E.I., Ugwu , G.C., Okanya , L.C. & Levi , C.A. 2014 . Eco-physiological adaptation of the land snail Achatina achatina (Gastropoda: Pulmonata) in tropical agro-ecosystem . Journal of Basic and Applied Zoology , 67 : 48 – 57 . Google Scholar Crossref Search ADS WorldCat Clark , J.A. 1976 . Effects of surface emissivity and viewing angle on errors in thermography . Acta Thermographica , 1 : 138 – 141 . Google Scholar OpenURL Placeholder Text WorldCat Clarke , B.C. 1979 . The evolution of genetic diversity . Proceedings of the Royal Society B , 205 : 453 – 474 . Google Scholar Crossref Search ADS WorldCat Clarke , B.C. , Arthur , W., Horsley , D.T. & Parkin , D.T. 1978 . Genetic variation and natural selection in pulmonate snails. In: The pulmonates , Vol. 2A ( V. Fretter & J.F. Peake, eds), pp. 220 – 270 . Academic Press , New York . Systematics, evolution and ecology. Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Clarke , A.P. , Mill , P.J. & Grahame , J. 2000 . Biodiversity in Littorina species (Mollusca: Gastropoda): a physiological approach using heat-coma . Marine Biology , 137 : 559 – 565 . Google Scholar Crossref Search ADS WorldCat Coleman , R.A. , Goss-Custard , J.D., Durell , S.E.A. & Hawkins , S.J. 1999 . Limpet Patella spp. consumption by oystercatchers Haematopus ostralegus: a preference for solitary prey items . Marine Ecology Progress Series , 183 : 253 – 261 . Google Scholar Crossref Search ADS WorldCat Coleman , R.A. & Hawkins , S.J. 2000 . Limpet relocation from home-scars in relation to position in group . Journal of the Marine Biological Association of the United Kingdom , 80 : 1133 – 1134 . Google Scholar Crossref Search ADS WorldCat Cook , L.M. & Jaffar , W.N. 1984 . Spire index and preferred surface orientation in some land snails . Biological Journal of the Linnean Society , 21 : 307 – 313 . Google Scholar Crossref Search ADS WorldCat Corkery , I. , Bell , B.D. & Nelson , N.J. 2014 . Behavioral thermoregulation of the tuatara, Sphenodon punctatus, under hydric and digestive constraints . Herpetological Conservation and Biology , 9 : 29 – 37 . Google Scholar OpenURL Placeholder Text WorldCat Cowie , R.H. 1985 . Microhabitat choice and high temperature tolerance in the land snail Theba pisana (Mollusca: Gastropoda) . Journal of Zoology , 207 : 201 – 211 . Google Scholar Crossref Search ADS WorldCat Cowie , R.H. & Jones , J.S. 1985 . Climatic selection on body colour in Cepaea . Heredity , 55 : 261 – 267 . Google Scholar Crossref Search ADS WorldCat Cox , T.E. & 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 : 1109 – 1120 . Google Scholar Crossref Search ADS WorldCat Croak , B.M. , Pike , D.A., Webb , J.K. & Shine , R. 2008 . Three-dimensional crevice structure affects retreat site selection by reptiles . Animal Behaviour , 76 : 1875 – 1884 . Google Scholar Crossref Search ADS WorldCat Cronin , M. , Duck , C., Cadhla , O.O., Nairn , R., Strong , D. & O’keeffe , C. 2007 . An assessment of population size and distribution of harbour seals in the Republic of Ireland during the moult season in August 2003 . Journal of Zoology , 273 : 131 – 139 . Google Scholar Crossref Search ADS WorldCat Davis , J.R. , Taylor , E.N. & Denardo , D. 2008 . An automated temperature-based option for estimating surface activity and refuge use patterns in free-ranging animals . Journal of Arid Environments , 72 : 1414 – 1422 . Google Scholar Crossref Search ADS WorldCat Denny , M.W. 1984 . Mechanical properties of pedal mucus and their consequences for gastropod structure and performance . American Zoologist , 24 : 23 – 36 . Google Scholar Crossref Search ADS WorldCat Denny , M.W. 1993 . Air and water: the biology and physics of Life’s media . Princeton University Press , Princeton, NJ . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Denny , M.W. , Dowd , W., Bilir , L. & Mach , K.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 : 175 – 190 . Google Scholar Crossref Search ADS WorldCat Denny , M.W. & Harley , C.D.G. 2006 . Hot limpets: predicting body temperature in a conductance-mediated thermal system . Journal of Experimental Biology , 209 : 2409 – 2419 . Google Scholar Crossref Search ADS PubMed WorldCat Deutsch , C.A. , Tewksbury , J.J., Huey , R.B., Sheldon , K.S., Ghalambor , C.K., Haak , D.C. & Martin , P.R. 2008 . Impacts of climate warming on terrestrial ectotherms across latitude . Proceedings of the National Academy of Science of the USA , 105 : 6668 – 6672 . Google Scholar Crossref Search ADS WorldCat Di Lellis , M.A. , Seifan , M., Troschinski , S., Mazzia , C., Capowiez , Y., Triebskorn , R. & Köhler , H.R. 2012 . Solar radiation stress in climbing snails: behavioural and intrinsic features define the Hsp70 level in natural populations of Xeropicta derbentina (Pulmonata) . Cell Stress and Chaperones , 17 : 717 – 727 . Google Scholar Crossref Search ADS PubMed WorldCat Diakides , M. , Bronzino , J.D. & Peterson , D.R. 2012 . Medical infrared imaging: principles and practices . CRC Press , Boca Raton, FL . Google Scholar Crossref Search ADS Google Preview WorldCat COPAC Dittbrenner , N. , Lazzara , R., Köhler , H.R., Mazzia , C., Capowiez , Y. & Triebskorn , R. 2009 . Heat tolerance in Mediterranean land snails: histopathology after exposure to different temperature regimes . Journal of Molluscan Studies , 75 : 9 – 18 . Google Scholar Crossref Search ADS WorldCat Dove , C.J. , Rijke , A.M., Wang , X. & Andrews , L.S. 2007 . Infrared analysis of contour feathers. The conservation of body heat radiation in birds . Journal of Thermal Biology , 32 : 42 – 46 . Google Scholar Crossref Search ADS WorldCat Dubois , Y. , Blouin-Demers , G., Shipley , B. & Thomas , D. 2009 . Thermoregulation and habitat selection in wood turtles Glyptemys insculpta: chasing the sun slowly . Journal of Animal Ecology , 78 : 1023 – 1032 . Google Scholar Crossref Search ADS PubMed WorldCat Ekendahl , A. & Johannesson , K. 1997 . Shell colour variation in Littorina saxatilis Olivi (Prosobranchia: Littorinidae): a multi-factor approach . Biological Journal of the Linnean Society , 62 : 401 – 419 . Google Scholar OpenURL Placeholder Text WorldCat Erlandson , J. , McQuaid , C.D. & Sköld , M. 2011 . Patchiness and co-existence of indigenous and invasive mussels at small-spatial scales: the interaction of facilitation and competition . PLoS One , 6 : e26958 . Google Scholar Crossref Search ADS PubMed WorldCat Etter , R.J. 1988 . Physiological stress and colour polymorphism in the intertidal snail Nucella lapillus . Evolution , 42 : 660 – 680 . Google Scholar Crossref Search ADS PubMed WorldCat Faye , E. , Dangles , O. & Pincebourde , S. 2016 . Distance makes the difference in thermography for ecological studies . Journal of Thermal Biology , 56 : 1 – 9 . Google Scholar Crossref Search ADS PubMed WorldCat Faye , E. , Herrera , M., Bellomo , L., Silvain , J.F. & Dangles , O. 2014 . Strong discrepancies between local temperature mapping and interpolated climatic grids in tropical mountainous agricultural landscapes . PLoS One , 9 : e105541 . Google Scholar Crossref Search ADS PubMed WorldCat Faye , E. , Rebaudo , F., Yanez-Cajo , D., Cauvy-Fraunié , S. & Dangles , O. 2016 . A toolbox for studying thermal heterogeneity across spatial scales: from unmanned aerial vehicle imagery to landscape metrics . Methods in Ecology and Evolution , 7 : 437 – 446 . Google Scholar Crossref Search ADS WorldCat FLIR . 2007 . The ultimate infrared handbook for R&D professionals. Available at www.fluke.com. Fournet , D. , Ross , L., Voelcker , T., Redortier , B. & Havenith , G. 2013 . Body mapping of thermoregulatory and perceptual responses of males and females running in the cold . Journal of Thermal Biology , 38 : 339 – 344 . Google Scholar Crossref Search ADS WorldCat Fraser , C.M. 2014 . Orientation of a keystone grazer: behavioural mechanisms, physiological consequences and ecological implications. PhD thesis, University of Sydney. Fraser , C.M. , Seebacher , F., Lathlean , J. & Coleman , R.A. 2016 . Facing the heat: does desiccation and thermal stress explain patterns of orientation in an intertidal invertebrate? PLoS One , 11 : e0150200 . Google Scholar Crossref Search ADS PubMed WorldCat Garrity , S.D. 1984 . Some adaptations of gastropods to physical stress on a tropical rocky shore . Ecology , 65 : 559 – 574 . Google Scholar Crossref Search ADS WorldCat Gates , D.M. 1980 . Biophysical ecology . Dover , New York . Google Scholar Crossref Search ADS Google Preview WorldCat COPAC Ghoshdastidar , P.S. 2012 . Heat transfer . Oxford University Press, Oxford . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Giokas , S. , Pafilis , P. & Valakos , E. 2005 . Ecological and physiological adaptations of the land snail Albinaria caerulea (Pulmonata: Clausiliidae) . Journal of Molluscan Studies , 71 : 15 – 23 . Google Scholar Crossref Search ADS WorldCat Goodfriend , G.A. 1986 . Variation in land-snails shell form and size and its causes: a review . Systematic Zoology , 35 : 204 – 223 . Google Scholar Crossref Search ADS WorldCat Grayson , J.E. & Chapman , M.G. 2004 . Patterns of distribution and abundance of chitons of the genus Ischnochiton in intertidal boulder fields . Austral Ecology , 29 : 363 – 373 . Google Scholar Crossref Search ADS WorldCat Guppy , M. & Withers , P. 1999 . Metabolic depression in animals: physiological perspectives and biochemical generalizations . Biological Reviews of the Cambridge Philosophical Society , 74 : 1 – 40 . Google Scholar Crossref Search ADS PubMed WorldCat Hahn , D.W. 2012 . Heat conduction . Wiley , New York . Google Scholar Crossref Search ADS Google Preview WorldCat COPAC Hamilton , W. 1973 . Life’s color code . McGraw-Hill , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Hammel , H.T. 1956 . Infrared emissivities of some arctic fauna . Journal of Mammalogy , 37 : 375 – 378 . Google Scholar Crossref Search ADS WorldCat Hanekom , N. 2008 . Invasion of an indigenous Perna perna mussel bed on the south coast of South Africa by an alien mussel Mytilus galloprovincialis and its effect on the associated fauna . Biological Invasions , 10 : 233 – 244 . Google Scholar Crossref Search ADS WorldCat Hannah , L. , Flint , L., Syphard , A.D., Moritz , M.A., Buckley , L.B. & Mccullough , I.M. 2014 . Fine-grain modeling of species’ response to climate change: holdouts, stepping-stones, and microrefugia . Trends in Ecology & Evolution , 29 : 390 – 397 . Google Scholar Crossref Search ADS PubMed WorldCat Harley , C.D.G. , Denny , M.W., Mach , K.J. & Miller , L.P. 2009 . Thermal stress and morphological adaptations in limpets . Functional Ecology , 23 : 292 – 301 . Google Scholar Crossref Search ADS WorldCat Hazel , W.N. & Johnson , M.S. 1990 . Microhabitat choice and polymorphism in the land snail Theba pisana (Muller) . Heredity , 65 : 449 – 454 . Google Scholar Crossref Search ADS WorldCat Heath , D.J. 1975 . Colour, sunlight and internal temperatures in the land-snail Cepaea nemoralis (L.) . Oecologia , 19 : 29 – 38 . Google Scholar Crossref Search ADS PubMed WorldCat Heller , J. 1981 . Visual versus climatic selection of shell banding in the landsnail Theba pisana in Israel . Journal of Zoology , 194 : 85 – 101 . Google Scholar Crossref Search ADS WorldCat Helmuth , B. 1998 . Intertidal mussel microclimates: predicting the body temperature of a sessile invertebrate . Ecological Monographs , 68 : 51 – 74 . Google Scholar Crossref Search ADS WorldCat Helmuth , B. 1999 . Thermal biology of rocky intertidal mussels: quantifying body temperatures using climatological data . Ecology , 80 : 15 – 34 . Google Scholar Crossref Search ADS WorldCat Helmuth , B. 2002 . How do we measure the environment? Linking intertidal thermal physiologyand ecology through biophysics . Integrative and Comparative Biology , 42 : 837 – 845 . Google Scholar Crossref Search ADS PubMed WorldCat Helmuth , B.S. , Broitman , B.R., Blanchette , C.A., Gilman , S., Halpin , P., Harley , C.D.G., O’donnell , M.J., Hofmann , G.E., Menge , B. & Strickland , D. 2006 . Mosaic patterns of thermal stress in the rocky intertidal zone: implications for climate change . Ecological Monographs , 76 : 461 – 479 . Google Scholar Crossref Search ADS WorldCat Helmuth , B. , Broitman , B.R., Yamane , L., Gilman , S.E., Mach , K., Mislan , K.A.S. & Denny , M.W. 2010 . Organismal climatology: analyzing environmental variability at scales relevant to physiological stress . Journal of Experimental Biology , 213 : 995 – 1003 . Google Scholar Crossref Search ADS PubMed WorldCat Helmuth , B. , Choi , F., Matzelle , A., Torossian , J.E. et al. 2016 . Long-term, high frequency in situ measurements of intertidal mussel bed temperatures using biomimetic sensors . Nature Scientific Data , 3 : 160087 . Google Scholar Crossref Search ADS WorldCat Helmuth , B. , Harley , C.D.G., Halpin , P.M., O’donnell , M., Hofmann , G.E. & Blanchette , C.A. 2002 . Climate change and latitudinal patterns of intertidal thermal stress . Science , 298 : 1015 – 1017 . Google Scholar Crossref Search ADS PubMed WorldCat Helmuth , B. , Russell , B.D., Connell , S.D., Dong , Y., Harley , C.D.G., Lima , F.P., Sara , G., Williams , G.A. & Mieszkowska , N. 2014 . Beyond long-term averages: making biological sense of a rapidly changing world . Climate Change Responses , 1 : 6 . Google Scholar Crossref Search ADS WorldCat Helmuth , B. , Yamane , L., Lalwani , S., Matzelle , A., Tockstein , A. & Gao , N. 2011 . Hidden signals of climate change in intertidal ecosystems: what (not) to expect when you are expecting . Journal of Experimental Marine Biology and Ecology , 400 : 191 – 199 . Google Scholar Crossref Search ADS WorldCat Herodotus . 1954 . The histories . Penguin , London . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Herreid , C.F. 1977 . Metabolism of land snails (Otala lacteal) during dormancy, arousal and activity . Comparative Biochemistry and Physiology , 56 : 211 – 215 . Google Scholar Crossref Search ADS PubMed WorldCat Herschel , W. 1800 . Experiments on the refrangibility of the invisible rays of the Sun . Philosophical Transactions of the Royal Society of London , 90 : 284 – 292 . Google Scholar Crossref Search ADS WorldCat Hodge , S.D. 1994 . Thermography and personal injury litigation . John Wiley , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Holst , G.C. 2000 . Common sense approach to thermal imaging . SPIE Optical Engineering Press , Bellingham, WA . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Howell , J.R. , Mengüç , M.P. & Siegel , R. 2015 . Thermal radiation heat transfer . CRC Press , Boca Raton, FL . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Hristov , N.I. , Betke , M. & Kunz , T.H. 2008 . Applications of thermal infrared imaging for research in aeroecology . Integrative and Comparative Biology , 48 : 50 – 59 . Google Scholar Crossref Search ADS PubMed WorldCat Hudson , R.D. 2006 . Infrared system engineering . Wiley Interscience , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Huey , R.B. & Berrigan , D. 2001 . Temperature, demography, and ectotherm fitness . American Naturalist , 158 : 204 – 210 . Google Scholar Crossref Search ADS PubMed WorldCat Hunt , V.L. , Lock , G.D., Pickering , S.G. & Charnley , A.K. 2011 . Application of infrared thermography to the study of behavioural fever in the desert locust . Journal of Thermal Biology , 36 : 443 – 451 . Google Scholar Crossref Search ADS WorldCat Iacarella , J.C. & Helmuth , B. 2011 . Experiencing the salt marsh environment through the foot of Littoraria irrorata: behavioral responses to thermal and desiccation stresses . Journal of Experimental Marine Biology and Ecology , 409 : 143 – 153 . Google Scholar Crossref Search ADS WorldCat Incropera , F.P. , Dewitt , D.P., Bergman , T.L. & Lavine , A.S. 2006 . Introduction to heat transfer . Wiley , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Janisch , J.E. , Wondzell , S.M. & Ehinger , W.J. 2012 . Headwater stream temperature: interpreting response after logging, with and without riparian buffers, Washington, USA . Forest Ecology and Management , 270 : 302 – 313 . Google Scholar Crossref Search ADS WorldCat Johannesson , K. 2003 . Evolution in Littorina: ecology matters . Journal of Sea Research , 49 : 107 – 117 . Google Scholar Crossref Search ADS WorldCat Johannesson , K. 2016 . What can be learnt from a snail? Evolutionary Applications , 9 : 153 – 165 . Google Scholar Crossref Search ADS PubMed WorldCat Johannesson , K. & Ekendahl , A. 2002 . Selective predation favouring cryptic individuals of marine snails (Littorina) . Biological Journal of the Linnean Society , 76 : 137 – 144 . Google Scholar Crossref Search ADS WorldCat Johnson , M.S. 1980 . Asociation of shell banding and habitat in a colony of the land snail Theba pisana . Heredity , 45 : 7 – 14 . Google Scholar Crossref Search ADS WorldCat Johnson , M.S. 1981 . Effects of migration and habitat choice on shell banding frequencies in Theba pisana at a habitat boundary . Heredity , 47 : 121 – 133 . Google Scholar Crossref Search ADS WorldCat Johnson , M.S. 2011 . Thirty-four years of climatic selection in the land snail Theba pisana . Heredity , 106 : 741 – 748 . Google Scholar Crossref Search ADS PubMed WorldCat Johnson , J.M. , Brengelmann , G.L., Hales , J.R., Vanhoutte , P.M. & Wenger , C.B. 1986 . Regulation of the cutaneous circulation . Federation Proceedings , 45 : 2841 – 2850 . Google Scholar PubMed OpenURL Placeholder Text WorldCat Jones , J.S. 1973 . Ecological genetics and natural selection in molluscs . Science , 182 : 546 – 552 . Google Scholar Crossref Search ADS PubMed WorldCat Jones , S.M. & Avery , R.A. 1989 . The use of a pyroelectric vidicon infrared camera to monitor the body temperatures of small terrestrial vertebrates . Functional Ecology , 3 : 373 – 377 . Google Scholar Crossref Search ADS WorldCat Jones , K.M. & Boulding , E.G. 1999 . State-dependent habitat selection by an intertidal snail: the costs of selecting a physically stressful microhabitat . Journal of Experimental Marine Biology and Ecology , 242 : 149 – 177 . Google Scholar Crossref Search ADS WorldCat Jones , J.S. , Leith , B.H. & Rawlings , P. 1977 . Polymorphism in Cepaea: a problem with too many solutions? Annual Review of Ecology and Systematics , 8 : 109 – 143 . Google Scholar Crossref Search ADS WorldCat Jorge Aldave , I. , Venegas Bosom , P., Vega González , L., López de Santiago , I., Vollheim , B., Krausz , L. & Georges , M. 2013 . Review of thermal imaging systems in composite defect detection . Infrared Physics & Technology , 61 : 167 – 175 . Google Scholar Crossref Search ADS WorldCat Kaehler , S. 1999 . Incidence and distribution of phototrophic shell-degrading endoliths of the brown mussel Perna perna . Marine Biology , 135 : 505 – 514 . Google Scholar Crossref Search ADS WorldCat Kaehler , S. & McQuaid , C.D. 1999 . Lethal and sub-lethal effects of phototrophic endoliths attacking the shell of the intertidal mussel Perna perna . Marine Biology , 135 : 497 – 503 . Google Scholar Crossref Search ADS WorldCat Kastberger , G. & Stachl , R. 2003 . Infrared imaging technology and biological applications . Behavior Research Methods, Instruments, and Computers , 35 : 429 – 439 . Google Scholar Crossref Search ADS WorldCat Keough , M.J. , Quinn , G.P. & Bathgate , R. 1997 . Geographic variation in interactions between size classes of the limpet Cellana tramoserica . Journal of Experimental Marine Biology and Ecology , 215 : 19 – 34 . Google Scholar Crossref Search ADS WorldCat Kerr , J.T. & Ostrovsky , M. 2003 . From space to species: ecological applications for remote sensing . Trends in Ecology and Evolution , 18 : 299 – 305 . Google Scholar Crossref Search ADS WorldCat Kingsolver , J.G. 2009 . The well-temperatured biologist . American Naturalist , 174 : 755 – 768 . Google Scholar PubMed OpenURL Placeholder Text WorldCat Kingsolver , J.G. , Diamond , S.E. & Buckley , L.B. 2013 . Heat stress and the fitness consequences of climate change for terrestrial ectotherms . Functional Ecology , 27 : 1415 – 1423 . Google Scholar Crossref Search ADS WorldCat Korabek , O. , Cejka , T. & Jurickova , L. 2016 . Tandonia kusceri (Pulmonata: Milacidae), a slug new for Slovakia . Malacologica Bohemoslovaca , 15 : 1 – 8 . Google Scholar OpenURL Placeholder Text WorldCat Kordas , R.L. & Harley , C.D.G. 2016 . Demographic responses of coexisting species to in situ warming . Marine Ecology Progress Series , 546 : 147 – 161 . Google Scholar Crossref Search ADS WorldCat Kordas , R.L. , Harley , C.D.G. & O’Connor , M.L. 2011 . Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems . Journal of Experimental Marine Biology and Ecology , 400 : 218 – 226 . Google Scholar Crossref Search ADS WorldCat Krochmal , A.R. & Bakken , G.S. 2003 . Thermoregulation is the pits: use of thermal radiation for retreat site selection by rattlesnakes . Journal of Experimental Biology , 206 : 2539 – 2545 . Google Scholar Crossref Search ADS PubMed WorldCat Lang , R. , Britton , J. & Metz , T. 1998 . What to do when there is nothing to do: the ecology of Jamaican intertidal littorinidae (Gastropoda: Prosobranchia) in repose . Hydrobiologia , 378 : 161 – 185 . Google Scholar Crossref Search ADS WorldCat Lasiak , T. & Dye , A.H. 1986 . Behavioural adaptations of the mangrove whelk, Telescopium telescopium (L.), to life in a semi-terrestrial environment . Journal of Molluscan Studies , 52 : 174 – 179 . Google Scholar Crossref Search ADS WorldCat Lathlean , J.A. 2014 . Not all space is created equal: distribution of free space and its influence on heat-stress and the limpet Patelloida latistrigata . Journal of Thermal Biology , 46 : 16 – 23 . Google Scholar Crossref Search ADS PubMed WorldCat Lathlean , J.A. , Ayre , D.J., Coleman , R.A. & Minchinton , T.E. 2014 a. Using biomimetic loggers to measure interspecific and microhabitat variation in body temperatures of rocky intertidal invertebrates . Marine and Freshwater Research , 66 : 86 – 94 . Google Scholar Crossref Search ADS WorldCat Lathlean , J.A. , Ayre , D.J. & 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 Oceanography , 57 : 1279 – 1291 . Google Scholar Crossref Search ADS WorldCat Lathlean , J.A. , Ayre , D.J. & Minchinton , T.E. 2013 . Temperature variability at the larval scale affects early survival and growth of an intertidal barnacle . Marine Ecology Progress Series , 475 : 155 – 166 . Google Scholar Crossref Search ADS WorldCat Lathlean , J.A. , Ayre , D.J. & Minchinton , T.E. 2014 . Estimating latitudinal variability in extreme heat stress on rocky intertidal shores . Journal of Biogeography , 41 : 1478 – 1491 . Google Scholar Crossref Search ADS WorldCat Lathlean , J.A. & Minchinton , T.E. 2012 . Manipulating thermal stress on rocky shores to predict patterns of recruitment of marine invertebrates under a changing climate . Marine Ecology Progress Series , 467 : 121 – 136 . Google Scholar Crossref Search ADS WorldCat Lathlean , J.A. & Seuront , L. 2014 . Infrared thermography in marine ecology: methods, previous applications and future challenges . Marine Ecology Progress Series , 514 : 263 – 277 . Google Scholar Crossref Search ADS WorldCat Lathlean , J. , Seuront , L., McQuaid , C.D., Ng , T.P.T., Zardi , G.I. & Nicastro , K.R. 2016 a. Cheating the locals: invasive mussels steal and benefit from the cooling effect of indigenous mussels . PLoS One , 11 : e0152556 . Google Scholar Crossref Search ADS PubMed WorldCat Lathlean , J. , Seuront , L., McQuaid , C.D., Ng , T.P.T., Zardi , G.I. & Nicastro , K.R. 2016 b. Size and position (sometimes) matter: small-scale patterns of heat-stress associated with two co-occurring mussels with different thermoregulatory behaviour . Marine Biology , 163 : 189 . Google Scholar Crossref Search ADS WorldCat Lathlean , J. , Seuront , L. & Ng , T.P.T. 2017 . On the edge: the use of infrared thermography in monitoring responses of intertidal organisms to heat stress . Ecological Indicators , 81 : 567 – 577 . Google Scholar Crossref Search ADS WorldCat Lavers , C. , Franks , K., Floyd , M. & Plowman , A. 2005 . Application of remote thermal imaging and night vision technology to improve endangered wildlife resource management with minimal animal distress and hazard to humans . Journal of Physics: Conference Series—Sensors and their Applications XIII , 15 : 207 – 212 . Google Scholar Crossref Search ADS WorldCat Lefcort , H. & Bayne , C.J. 1991 . Thermal preferences of resistant and susceptible strains of Biomphalaria glabrata (Gastropoda) exposed to Schistosoma mansoni (Trematoda) . Parasitology , 103 : 357 – 362 . Google Scholar Crossref Search ADS PubMed WorldCat Lelièvre , H. , Blouin-Demers , G., Bonnet , X. & Lourdais , O. 2010 . Thermal benefits of artificial shelters in snakes: a radiotelemetric study of two sympatric colubrids . Journal of Thermal Biology , 35 : 324 – 331 . Google Scholar Crossref Search ADS WorldCat Lewis , J.B. 1960 . The fauna of rocky shores of Barbados, West Indies . Canadian Journal of Zoology , 38 : 391 – 435 . Google Scholar Crossref Search ADS WorldCat Lewis , J.B. 1963 . Environmental and tissue temperatures of some tropical intertidal marine animals . Biological Bulletin , 124 : 277 – 284 . Google Scholar Crossref Search ADS WorldCat Lim , S.S. 2008 . Body posturing in Nodilittorina pyramidalis and Austrolittorina unifasciata (Mollusca: Gastropoda: Littorinidae): a behavioural response to reduce heat stress . Memoirs of the Queensland Museum , 54 : 339 – 347 . Google Scholar OpenURL Placeholder Text WorldCat Lima , F.P. , Burnett , N.P., Helmuth , B., Kish , N., Aveni-Deforge , K. & Wethey , D.S. 2011 . Monitoring the intertidal environment with biomimetic devices. In: Biomimetic based applications ( A. George, ed.), pp. 499 – 522 . IntechOpen , London . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Lima , F.P. & Wethey , D.S. 2009 . Robolimpets: measuring intertidal body temperatures using biomimetic loggers . Limnology and Oceanography: Methods , 7 : 347 – 353 . Google Scholar Crossref Search ADS WorldCat Loyson , P. 2012 . Galilean thermometer not so Galilean . Journal of Chemical Education , 89 : 1095 – 1098 . Google Scholar Crossref Search ADS WorldCat Marshall , D.J. , Baharuddin , N. & McQuaid , C.D. 2013 . Behaviour moderates climate warming vulnerability in high-rocky-shore snails: interactions of habitat use, energy consumption and environmental temperature . Marine Biology , 160 : 2525 – 2530 . Google Scholar Crossref Search ADS WorldCat Marshall , D.J. & Chua , T. 2012 . Boundary layer convective heating and thermoregulatory behaviour during aerial exposure in the rocky eulittoral fringe snail Echinolittorina malaccana . Journal of Experimental Marine Biology and Ecology , 430 : 25 – 31 . Google Scholar Crossref Search ADS WorldCat Marshall , D.J. , McQuaid , C.D. & Williams , G.A. 2010 . Non-climatic thermal adaptation: implications for species’ responses to climate warming . Biology Letters , 6 : 669 – 673 . Google Scholar Crossref Search ADS PubMed WorldCat Marshall , D.J. , Mustafa , S.A.D. & Williams , G.A. 2010 . Cooling towers of marine snails: is higher better? Sciencia Bruneiana , 11 : 47 – 52 . Google Scholar OpenURL Placeholder Text WorldCat Marshall , D.J. & Ng , T.P.T. 2013 . Shell standing in littorinid snails: a multifunctional behaviour associated with mating? Journal of Molluscan Studies , 79 : 74 – 75 . Google Scholar Crossref Search ADS WorldCat Mason , C.F. 1970 . Snail populations, beech litter production, and the role of snails in litter decomposition . Oecologia , 5 : 215 – 239 . Google Scholar Crossref Search ADS PubMed WorldCat Mauck , B. , Bilgmann , K., Jones , D.D., Eysel , U. & Dehnhardt , G. 2003 . Thermal windows on the trunk of hauled-out seals: hot spots for thermoregulatory evaporation? Journal of Experimental Biology , 206 : 1727 – 1738 . Google Scholar Crossref Search ADS PubMed WorldCat McCafferty , D.J. 2007 . The value of infrared thermography for research on mammals: previous applications and future directions . Mammal Reviews , 37 : 207 – 223 . Google Scholar Crossref Search ADS WorldCat McMahon , R.F. 1990 . Thermal tolerance, evaporative water loss, air-water oxygen consumption and zonation of intertidal prosobranchs: a new synthesis . Hydrobiologia , 193 : 241 – 260 . Google Scholar Crossref Search ADS WorldCat McMahon , R.F. & Britton , J.C. 1985 . The relationship between vertical distribution, thermal tolerance, evaporative water loss rate, and behaviour on emergence in six species of mangrove gastropods from Hong Kong. In: Proceedings of the Second International Workshop on the Malacofauna of Hong Kong and Southern China ( B. Morton & D. Dudgeon, eds), pp. 563 – 582 . Hong Kong University Press , Hong Kong . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC McQuaid , C.M. , Branch , G.M. & Frost , P.G.H. 1979 . Aestivation behaviour and thermal relations of the pulmonate Theba pisana in a semi-arid environment . Journal of Thermal Biology , 4 : 47 – 55 . Google Scholar Crossref Search ADS WorldCat McQuaid , C.D. & Schermann , P.A. 1988 . Thermal stress in a high shore intertidal environment: morphological and behavioural adaptations of the gastropod Littorina africana. In: Behavioural adaptation to intertidal life ( G. Chelazzi & M. Vannini, eds), pp. 213 – 224 . Plenum Press , New York . Google Scholar Crossref Search ADS Google Preview WorldCat COPAC Meager , J.J. , Schlacher , T.A. & Green , M. 2011 . Topographic complexity and landscape temperature patterns create a dynamic habitat structure on a rocky intertidal shore . Marine Ecology Progress Series , 428 : 1 – 12 . Google Scholar Crossref Search ADS WorldCat Mellish , J. , Nienaber , J., Polasek , L. & Horning , M. 2013 . Beneath the surface: profiling blubber depth in pinnipeds with infrared imaging . Journal of Thermal Biology , 38 : 10 – 13 . Google Scholar Crossref Search ADS PubMed WorldCat Miller , L.P. 2008 . Life on the edge: morphological and behavioural adaptations for survival on wave-swept shores. PhD thesis, Stanford University, CA. Miller , L.P. & Denny , M.W. 2011 . Importance of behaviour and morphological traits for controlling body temperature in littorinid snails . Biological Bulletin , 220 : 209 – 223 . Google Scholar Crossref Search ADS PubMed WorldCat Miller , L.P. , Harley , C.D.G. & Denny , M.W. 2009 . The role of temperature and desiccation stress in limiting the local-scale distribution of the owl limpet Lottia gigantea . Functional Ecology , 23 : 756 – 767 . Google Scholar Crossref Search ADS WorldCat Miller , C.B. & Wheeler , P.A. 2012 . Biological oceanography . Wiley-Blackwell , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Mitton , J.B. 1977 . Shell color and pattern variation in Mytilus edulis and its adaptive significance. Chesapeake . Science , 18 : 387 – 390 . Google Scholar OpenURL Placeholder Text WorldCat Modest , M.F. 2013 . Radiative heat transfer . Academic Press , Cambridge, MA . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Mohammed , S.Z. 1999 . Aspects on clustering and movements of the intertidal gastropod, Planaxis sulcatus (Gastropoda/Planaxidae) in the Suez Canal . Indian Journal of Marine Sciences , 28 : 320 – 324 . Google Scholar OpenURL Placeholder Text WorldCat Moreno-Rueda , G. , Ruiz-Ruiz , A., Collantes-Martin , E. & Arrebola , J.R. 2009 . Relative importance of humidity and temperature on microhabitat use by land snails in arid versus humid environments. In: Arid environments and wind erosion ( A. Fernandez-Bernal & M.A. De La Rosa, eds), pp. 331 – 343 . Nova Science Publishers , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Muñoz , J.L.P. , Finke , G.R., Camus , P.A. & Bozinovic , F. 2005 . Thermoregulatory behavior, heat gain and thermal tolerance in the periwinkle Echilittorina peruviana in central Chile. Comparative and Biochemical . Physiology A , 142 : 92 – 98 . Google Scholar OpenURL Placeholder Text WorldCat Murphy , S.W. , Oppenheimer , C. & de Souza-Filho , C.R. 2014 . Calculating radiant flux from thermally mixed pixels using a spectral library . Remote Sensing of the Environment , 142 : 83 – 94 . Google Scholar Crossref Search ADS WorldCat Mysak , J. , Horsak , M., Svobodova , E. & Cernohorsky , N. 2013 . Small-scale distribution of terrestrial snails: patterns of species richness and abundance related to area . Journal of Molluscan Studies , 79 : 118 – 127 . Google Scholar Crossref Search ADS WorldCat Nicastro , K.R. , Zardi , G.I., McQuaid , C.D., Pearson , G.A. & Serrao , E.A. 2012 . Love thy neighbour: group properties of gaping behaviour in mussel aggregation . PLoS One , 7 : e47382 . Google Scholar Crossref Search ADS PubMed WorldCat Nicastro , K. , Zardi , G., McQuaid , C.D., Stephens , L., Radloff , S. & Blatch , G. 2010 . The role of gaping behaviour in habitat partitioning between coexisting intertidal mussels . BioMedCentral Ecology , 10 : 17 . Google Scholar Crossref Search ADS WorldCat Nunn , J.F. 2002 . Ancient Egyptian medicine . University of Oklahoma Press , Norman, OK . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Okajima , R. & Chiba , S. 2013 . Adaptation from restricted geometries: the shell inclination of terrestrial gastropod . Evolution , 67 : 429 – 437 . Google Scholar Crossref Search ADS PubMed WorldCat Oke , T.R. 1987 . Boundary layer climates . Routledge, Taylor & Francis , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Osovitz , C.J. & Hofmann , G.E. 2007 . Marine macrophysiology: studying physiological variation across large spatial scales in marine systems . Comparative Biochemistry and Physiology A , 147 : 821 – 827 . Google Scholar Crossref Search ADS WorldCat Otsuka , K. & Togawa , T. 1997 . Hippocratic thermography . Physiological Measurements , 18 : 227 – 232 . Google Scholar Crossref Search ADS WorldCat Ozgo , M. & Schilthuizen , M. 2012 . Evolutionary change in Cepaea nemoralis shell colour over 43 years . Global Change Biology , 18 : 74 – 81 . Google Scholar Crossref Search ADS WorldCat Paine , R.T. 1969 . A note on trophic complexity and community stability . American Naturalist , 103 : 91 – 93 . Google Scholar Crossref Search ADS WorldCat Paine , R.T. 1995 . A conversation on refining the concept of keystone species . Conservation Biology , 9 : 962 – 964 . Google Scholar Crossref Search ADS WorldCat Parkin , D.T. 1971 . Visual selection in the land snail Arianta arbustorum . Heredity , 26 : 35 – 47 . Google Scholar Crossref Search ADS WorldCat Parkin , D.T. 1972 . Climatic selection in the land snail Arianta arbustorum in Derbyshire, England . Heredity , 28 : 49 – 56 . Google Scholar Crossref Search ADS WorldCat Parmesan , C. 2006 . Ecological and evolutionary responses to recent climate change . Annual Review of Ecology, Evolution, and Systematics , 37 : 637 – 669 . Google Scholar Crossref Search ADS WorldCat Perry , D.W. & Green , R.H. 2008 . Perry’s chemical engineers’ handbook . McGraw-Hill , New York . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Petropoulos , G.P. 2014 . Remote sensing of energy fluxes and soil moisture content . CRC Press , Boca Raton, FL . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Phillips , K.H. 1995 . A guide to the Sun . Cambridge University Press , Cambridge, UK . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Phillips , P.K. & Sanborn , A.F. 1994 . An infrared, thermographic study of surface-temperature in 3 ratites: ostrich, emu and double wattled cassowary . Journal of Thermal Biology , 19 : 423 – 430 . Google Scholar Crossref Search ADS WorldCat Pike , D.A. , Webb , J.K. & Shine , R. 2012 . Hot mothers, cool eggs: nest-site selection by egg-guarding spiders accommodates conflicting thermal optima . Functional Ecology , 26 : 469 – 475 . Google Scholar Crossref Search ADS WorldCat Pincebourde , S. & Casas , J. 2015 . Warming tolerance across insect ontogeny: influence of joint shifts in microclimates and thermal limits . Ecology , 96 : 986 – 997 . Google Scholar Crossref Search ADS PubMed WorldCat Pincebourde , S. , Sanford , E. & Helmuth , B. 2008 . Body temperature during low tide alters the feeding performance of a top intertidal predator . Limnology and Oceanography , 53 : 1562 – 1573 . Google Scholar Crossref Search ADS WorldCat Pincebourde , S. , Sanford , E. & Helmuth , B. 2013 . Survival and arm abscission are linked to regional heterothermy in an intertidal sea star . Journal of Experimental Biology , 216 : 2183 – 2191 . Google Scholar Crossref Search ADS PubMed WorldCat Pincebourde , S. & Woods , A.H. 2012 . Climate uncertainty on leaf surfaces: the biophysics of leaf microclimate and their consequences for leaf-dwelling organisms . Functional Ecology , 26 : 844 – 853 . Google Scholar Crossref Search ADS WorldCat Pomeroy , D.E. 1966 . The ecology of Helicella virgata and related species of snails in South Australia. PhD thesis, University of Adelaide. Pomeroy , D.E. 1968 . Dormancy in the land snail Helicella virgata (Pulmonata: Helicidae) . Australian Journal of Zoology , 16 : 857 – 869 . Google Scholar Crossref Search ADS WorldCat Potter , K.A. , Woods , H.A. & Pincebourde , S. 2013 . Microclimatic challenges in global change biology . Global Change Biology , 19 : 2932 – 2939 . Google Scholar Crossref Search ADS PubMed WorldCat Prior , D.J. 1989 . Contact-rehydration in slugs: a water regulatory behaviour . Slugs and Snails in World Agriculture , 41 : 217 – 223 . Google Scholar OpenURL Placeholder Text WorldCat Pörtner , H.O. & Farrell , A.P. 2008 . Ecology, physiology and climate change . Science , 322 : 690 – 692 . Google Scholar Crossref Search ADS PubMed WorldCat Raffaelli , D. 1982 . Recent ecological research on some European species of Littorina . Journal of Molluscan Studies , 48 : 342 – 354 . Google Scholar Crossref Search ADS WorldCat Rankevich , D. 1997 . Genetic variation and resistance to dessication in populations of landsnails on the southern and northern slopes of Nahal Oren . Technion , Haifa, Israel . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Rehfeld , K. 1997 . Molluskenscalen . Naturwissenschaftliche Rundschau , 1 : 9 – 17 . Google Scholar OpenURL Placeholder Text WorldCat Rehnberg , B.G. 2002 . Heat retention by webs of the fall webworm Hyphantria cunea (Lepidoptera: Arctiidae): infrared warming and forced convective cooling . Journal of Thermal Biology , 27 : 525 – 530 . Google Scholar Crossref Search ADS WorldCat Reichard , J.D. , Fellows , S.R., Frank , A.J. & Kunz , T.H. 2010 . Thermoregulation during flight: body temperature and sensible heat transfer in free-ranging Brazilian free-tailed bats (Tadarida brasiliensis) . Physiological and Biochemical Zoology , 83 : 885 – 897 . Google Scholar Crossref Search ADS PubMed WorldCat Reid , D.G. 1989 . The comparative morphology, phylogeny and evolution of the gastropod family Littorinidae . Philosophical Transactions of the Royal Society of London B , 324 : 1 – 110 . Google Scholar Crossref Search ADS WorldCat Reid , D.G. 1996 . Systematics and evolution of Littorina . Ray Society , London . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Rogalski , A. 2012 . History of infrared detectors . Opto-electronics Review , 20 : 279 – 308 . Google Scholar Crossref Search ADS WorldCat Rojas , S.M. , Castillo , S.B., Escobar , J.B., Shinen , J.L. & Bozinovic , F. 2013 . Huddling up in a dry environment: the physiological benefits of aggregation in an intertidal gastropod . Marine Biology , 160 : 1119 – 1126 . Google Scholar Crossref Search ADS WorldCat Rojas , S.M. , Farina , J.M., Soto , R.E. & Bozinovic , F. 2000 . Geographic variability in thermal tolerance and water economy of the intertidal gastropod Nodilittorina peruviana (Gastropoda: Littorinidae, Lamarck, 1822) . Revista Chilena de Historia Natural , 73 : 543 – 552 . Google Scholar Crossref Search ADS WorldCat Rubio , E. , Caselles , V. & Badenas , C. 1997 . Emissivity measurements of several soils and vegetation types in the 8–14 mm wave band: analysis of two field methods . Remote Sensing of the Environment , 59 : 490 – 521 . Google Scholar Crossref Search ADS WorldCat Sabol , B.M. & Hudson , M.K. 1995 . Technique using thermal infrared-imaging for estimating populations of gray bats . Journal of Mammalogy , 76 : 1242 – 1248 . Google Scholar Crossref Search ADS WorldCat Scheffers , B.R. , Edwards , D.P., Diesmos , A., Williams , S.E. & Evans , T.A. 2014 b. Microhabitats reduce animal’s exposure to climate extremes . Global Change Biology , 20 : 495 – 503 . Google Scholar Crossref Search ADS PubMed WorldCat Scheffers , B.R. , Evans , T.A., Williams , S.E. & Edwards , D.P. 2014 a. Microhabitats in the tropics buffer temperature in a globally coherent manner . Biology Letters , 10 : 20140819 . Google Scholar Crossref Search ADS PubMed WorldCat Scheil , A.E. , Gärtner , U. & Köhler , H.-R. 2012 . Colour polymorphism and thermal capacities in Theba pisana (O.F. Müller 1774) . Journal of Thermal Biology , 37 : 462 – 467 . Google Scholar Crossref Search ADS WorldCat Scherrer , D. & Körner , C. 2010 . Infrared thermometry of alpine landscapes challenges climatic warming projections . Global Change Biology , 16 : 2602 – 2613 . Google Scholar OpenURL Placeholder Text WorldCat Schmidt-Nielsen , K. 1997 . Animal physiology. Adaptation and environment . Cambridge University Press , Cambridge, UK . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Seabra , R. , Wethey , D.S., Santos , A.M. & 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 : 200 – 208 . Google Scholar Crossref Search ADS WorldCat Sears , M.W. , Angilletta , M.J., Schuler , M.S., Borchert , J., Dilliplane , K.F., Stegman , M., Rusch , T.W. & Mitchell , W.A. 2016 . Configuration of the thermal landscape determines thermoregulatory performance of ectotherms . Proceedings of the National Academy of Sciences of the USA , 113 : 10595 – 10600 . Google Scholar Crossref Search ADS PubMed WorldCat Seuront , L. & Ng , T.P.T. 2016 . Standing in the sun: infrared thermography reveals distinct thermal regulatory behaviours in two tropical high-shore littorinid snails . Journal of Molluscan Studies , 82 : 336 – 340 . Google Scholar Crossref Search ADS WorldCat Siegel , R. & Howell , J. 2001 . Thermal radiation heat transfer . CRC Press , Boca Raton, FL . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Sokolova , I.M. & Berger , V.J. 2000 . Physiological variation related to shell colour polymorphism in White Sea Littorina saxatilis . Journal of Experimental Marine Biology and Ecology , 245 : 1 – 23 . Google Scholar Crossref Search ADS WorldCat Sokolova , I.M. , Granovitch , A.I., Berger , V.J. & Johannesson , K. 2000 . Intraspecific physiological variability of the gastropod Littorina saxatilis related to the vertical shore gradient in the White and North Seas . Marine Biology , 137 : 297 – 308 . Google Scholar Crossref Search ADS WorldCat Somero , G.N. 2010 . The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’ . Journal of Experimental Biology , 213 : 912 – 920 . Google Scholar Crossref Search ADS PubMed WorldCat Speakman , J. 2004 . Thermoregulation. In: Encyclopedia of energy ( C.J. Cleveland, ed.), pp. 125 – 137 . Elsevier Academic Press , New York . Google Scholar Crossref Search ADS Google Preview WorldCat COPAC Spotila , J.R. , Terpin , K.M. & Dodson , P. 1977 . Mouth gaping as an effective thermoregulatory device in alligators . Nature , 265 : 235 – 236 . Google Scholar Crossref Search ADS PubMed WorldCat Srivastava , P.K. , Petropoulos , G.P. & Kerr , Y.H. 2016 . Satellite soil moisture retrieval. In: Techniques and applications . Elsevier , Amsterdam . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Stafford , R. & Davies , M.S. 2004 . Temperature and desiccation do not affect aggregation behaviour in high shore littorinids in north-east England . Journal of Negative Results—Ecology & Evolutionary Biology , 1 : 16 – 20 . Google Scholar OpenURL Placeholder Text WorldCat Stafford , R. , Ng , T.P.T., Williams , G.A. & Davies , M.S. 2015 . A biologically relevant rapid quantification of physical and biological stress profiles on rocky shores . Ecological Informatics , 25 : 43 – 48 . Google Scholar Crossref Search ADS WorldCat Staikou , A.E. 1999 . Shell temperature, activity and resistance to desiccation in the polymorphic land snail Cepaea vindobonensis . Journal of Molluscan Studies , 65 : 171 – 184 . Google Scholar Crossref Search ADS WorldCat Stewart , S.M. & Johnson , R.B. 2016 . Blackbody radiation. A history of thermal radiation computational aids and numerical methods . CRC Press , Boca Raton, FL . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Storlie , C. , Merino-Viteri , A., Phillips , B., Vanderwal , J., Welbergen , J. & Williams , S. 2014 . Stepping inside the niche: microclimate data are critical for accurate assessment of species’ vulnerability to climate change . Biology Letters , 10 : 20140576 . Google Scholar Crossref Search ADS PubMed WorldCat Sumbera , R. , Zelova , J., Kunc , P., Knizkova , I. & Burda , H. 2007 . Patterns of surface temperatures in two mole-rats (Bathyergidae) with different social systems as revealed by IR-thermography . Physiology and Behavior , 92 : 526 – 532 . Google Scholar Crossref Search ADS PubMed WorldCat Sundén , B. 2012 . Introduction to heat transfer . WIT Press , Southampton, UK . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Surmacki , A. , Ozarowska , A. & Rosin , Z.M. 2013 . Color polymorphism in a land snail Cepaea nemoralis (Pulmonata: Helicidae) as viewed by potential avian predators . Naturwissenschaffeten , 100 : 533 – 540 . Google Scholar Crossref Search ADS WorldCat Szathmary , P.L. , Helmuth , B. & Wethey , D.S. 2009 . Climate change in the rocky intertidal zone: predicting and measuring the body temperature of a keystone predator . Marine Ecology Progress Series , 374 : 43 – 56 . Google Scholar Crossref Search ADS WorldCat Tattersall , G.J. 2016 . Infrared thermography: a non-invasive window into thermal physiology . Comparative Biochemistry and Physiology A , 202 : 78 – 98 . Google Scholar Crossref Search ADS WorldCat Tattersall , G.J. & Cadena , V. 2010 . Insights into animal temperature adaptations revealed through thermal imaging . Imaging Science Journal , 58 : 261 – 268 . Google Scholar Crossref Search ADS WorldCat Tattersall , G.J. , Cadena , V. & Skinner , M.C. 2006 . Respiratory cooling and thermoregulatory coupling in reptiles . Respiration, Physiology and Neurobiology , 154 : 302 – 318 . Google Scholar Crossref Search ADS WorldCat Tattersall , G.J. , Eterovick , P.C. & De Andrade , D.V. 2006 . Tribute to R. G. Boutilier: skin colour and body temperature changes in basking Bokermannohyla alvarengai (Bokermann 1956) . Journal of Experimental Biology , 209 : 1185 – 1196 . Google Scholar Crossref Search ADS PubMed WorldCat Tattersall , G.J. & Gerlach , R.M. 2005 . Hypoxia progressively lowers thermal gaping thresholds in bearded dragons, Pogona vitticeps . Journal of Experimental Biology , 208 : 3321 – 3330 . Google Scholar Crossref Search ADS PubMed WorldCat Tong , L.K.Y. 1988 . The reproductive biology of Thais clavigera and Morula musiva (Gastropoda: Muricidae) in Hong Kong . Asian Marine Biology , 5 : 65 – 75 . Google Scholar OpenURL Placeholder Text WorldCat Torossian , J.L. , Kordas , R. & Helmuth , B. 2016 . Cross-scale approaches to forecasting biogeographic responses to climate change. In: (A.J. Dumbrell, R.L. Kordas & G. Woodward, eds), pp. 317 –433. Advances in Ecological Research, Vol. 55, Academic Press, Oxford. Usamentiaga , R. , Venegas , P., Guerediaga , J., Vega , L., Molleda , J. & Bulnes , F.G. 2014 . Infrared thermography for temperature measurement and non-destructive testing . Sensors , 14 : 12305 – 12348 . Google Scholar Crossref Search ADS PubMed WorldCat van Alstyne , K.L. & Olson , T.K. 2014 . Estimating variation in surface emissivities of intertidal macroalgae using an infrared thermometer and the effects on temperature measurements . Marine Biology , 161 : 1409 – 1418 . Google Scholar Crossref Search ADS PubMed WorldCat van de Koppel , J , Gascoigne , J.C., Theraulaz , G., Rietkerk , M., Mooij , W.M. & Herman , P.M.J. 2008 . Experimental evidence for spatial self-organization and its emergent effects in mussel bed ecosystems . Science , 322 : 739 – 742 . Google Scholar Crossref Search ADS PubMed WorldCat Vermeij , G.J. 1971 a. Substratum relationships of some tropical Pacific intertidal gastropods . Marine Biology , 10 : 315 – 320 . Google Scholar Crossref Search ADS WorldCat Vermeij , G.J. 1971 b. Temperature relationships of some tropical Pacific intertidal gastropods . Marine Biology , 10 : 308 – 314 . Google Scholar Crossref Search ADS WorldCat Vidal , M.A. , Habit , E., Victoriano , P., Gonzalez-Gajardo , A. & Ortiz , J.C. 2010 . Thermoregulation and activity pattern of the high-mountain lizard Phymaturus palluma (Tropiduridea) in Chile . Zoologia , 27 : 13 – 18 . Google Scholar Crossref Search ADS WorldCat Vollmer , M. & Möllmann , K.P. 2010 . Infrared thermal imaging: fundamentals, research and applications . Wiley-VCH , Weinheim, Germany . Google Scholar Crossref Search ADS Google Preview WorldCat COPAC Wada , S. & Ito , A. 2000 . Preliminary observation on tip-lip attachment in the periwinkle Nodilittorina radiata . Bulletin of Marine Science and Fisheries Kochi University , 20 : 15 – 24 . Google Scholar OpenURL Placeholder Text WorldCat Walther , G.R. , Post , E., Convey , P., Menzel , A., Parmesan , C., Beebee , T.J.C., Fromentin , J.M., Hoegh-Guldberg , O. & Bairlein , F. 2002 . Ecological responses to recent climate change . Nature , 416 : 389 – 395 . Google Scholar Crossref Search ADS PubMed WorldCat Warburton , K. 1973 . Solar orientation in the snail Nerita plicata (Prosobranchia: Neritacea) on a beach near Watamu, Kenya . Marine Biology , 23 : 93 – 100 . Google Scholar Crossref Search ADS WorldCat Weissenböck , N.M. , Weiss , C.M., Schwammer , H.M. & Kratochvil , H. 2010 . Thermal windows on the body surface of African elephants (Loxodonta africana) studied by infrared thermography . Journal of Thermal Biology , 35 : 182 – 188 . Google Scholar Crossref Search ADS WorldCat Williams , S.T. 2016 . Molluscan shell colour . Biological Reviews , 92 : 1039 – 1058 . Google Scholar Crossref Search ADS PubMed WorldCat Withers , P. , Pedler , S. & Guppy , M. 1997 . Physiological adjustments during aestivation by the Australian land snail Rhagada tescorum (Mollusca: Pulmonata: Camaenidae) . Australian Journal of Zoology , 45 : 599 – 611 . Google Scholar Crossref Search ADS WorldCat Woods , H.A. , Dillon , M.E. & Pincebourde , S. 2015 . The roles of microclimatic diversity and of behavior in mediating the responses of ectotherms to climate change . Journal of Thermal Biology , 54 : 86 – 97 . Google Scholar Crossref Search ADS PubMed WorldCat Yom-Tov , Y. 1971 . Body temperature and light reflectance in two desert snails . Proceedings of the Malacological Society of London , 39 : 319 – 326 . Google Scholar OpenURL Placeholder Text WorldCat Zalameda , J.N. & Winfree , W.P. 2005 . Investigation of uncooled microbolometer focal plane array infrared camera for quantitative thermography . Journal of Nondestructive Evaluation , 24 : 1 – 9 . Google Scholar Crossref Search ADS WorldCat Zar , J.H. 1999 . Biostatistical analysis . Prentice Hall , Upper Saddle River, NJ . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Zardi , G.I. , Nicastro , K.R., McQuaid , C.D. & Gektidis , M. 2009 . Effects of endolithic parasitism on invasive and indigenous mussels in a variable physical environment . PLoS One , 4 : e6560 . Google Scholar Crossref Search ADS PubMed WorldCat Zardi , G.I. , Nicastro , K.R., McQuaid , C.D., Ng , T.P.T., Lathlean , J. & Seuront , L. 2016 . Enemies with benefits: otherwise parasitic endoliths protect mussels against heat stress . Scientific Reports , 6 : 31413 . Google Scholar Crossref Search ADS PubMed WorldCat Zardi , G. , Nicastro , K., McQuaid , C., Ruis , M. & Porri , F. 2006 . Hydrodynamic stress and habitat partitioning between indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels: constraints of an evolutionary strategy . Marine Biology , 150 : 79 – 88 . Google Scholar Crossref Search ADS WorldCat Żbikowska , E. 2001 . Do larvae of Trichobilharzia szidati and Echinostoma revolutum generate behavioral fever in Lymnaea stagnalis individuals? Parasitology Research , 96 : 68 – 72 . Google Scholar OpenURL Placeholder Text WorldCat Żbikowska , E. , Wrotek , S., Cichy , A. & Kozak , W. 2013 . Thermal preferences of wintering snails Planorbarius corneus (L.) exposed to lipopolysaccharide and zymosan . Journal of Invertebrate Pathology , 112 : 57 – 61 . Google Scholar Crossref Search ADS PubMed WorldCat © The Author(s) 2018. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved. For Permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) © The Author(s) 2018. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved. For Permissions, please email: journals.permissions@oup.com
TI - A review of the thermal biology and ecology of molluscs, and of the use of infrared thermography in molluscan research
JF - Journal of Molluscan Studies
DO - 10.1093/mollus/eyy023
DA - 2018-08-01
UR - https://www.deepdyve.com/lp/oxford-university-press/a-review-of-the-thermal-biology-and-ecology-of-molluscs-and-of-the-use-OxvSkeKqcG
SP - 203
EP - 232
VL - 84
IS - 3
DP - DeepDyve
ER -