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Spreading the Risk: Small-Scale Body Temperature Variation Among Intertidal Organisms and Its Implications for Species Persistence

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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 (2011) 175–190 Contents lists available at ScienceDirect Journal of Experimental Marine Biology and Ecology journal homepage: www.elsevier.com/locate/jembe Spreading the risk: Small-scale body temperature variation among intertidal organisms and its implications for species persistence Mark W. Denny ⁎, W. Wesley Dowd, Lisa Bilir, Katharine J. Mach Hopkins Marine Station of Stanford University, Pacific Grove, CA 93950, USA article info abstract Keywords: The intertidal zone of wave-swept rocky shores is a potentially useful system in which to monitor, Thermal stress experimentally manipulate, and possibly forecast the ecological consequences of impending changes in Climate change environmental temperature. However, the spatial and temporal complexity of the shoreline's thermal Ecological physiology environment challenges ecologists' ability to progress from site-specific measurements to general predictions. Risk In this study, we conducted intensive field experiments to quantify inter-individual variation in body Intertidal ecology Variation temperature among organisms and surrogate organisms at a typical intertidal site, and we used these Thermal limits measurements to characterize micro-scale variation in potential thermal stress. Within the 336-m extent of our site, local variation was substantial in several metrics of extreme and cumulative thermal exposure. The within-site variation in extreme temperatures rivaled (and in some cases greatly exceeded) variation among sites along 14° of latitude (1660 km of Pacific shoreline). Application of our within-site data to a simple theory of risk suggests that small-scale spatial variation in temperature can reduce the chance of local extirpation that otherwise would accompany an increase in average habitat temperature or an increase in the frequency of extreme thermal events. The magnitude of this “buffering” effect also depends heavily on inter-individual variation in thermal tolerance, a factor that has received relatively little attention from physiologists. We hope that by highlighting the important role of within-site variability (both of temperature and tolerance) in the persistence of intertidal populations, this study will foster further research into the biophysical, physiological, behavioral, and genetic interactions underlying ecological dynamics on wave-washed shores. © 2011 Elsevier B.V. All rights reserved. 1. Introduction very near their lethal thermal limits, and the most warm-adapted of these species tend to have the least physiological reserve to cope with Rising concentrations of atmospheric carbon dioxide and other warming (e.g., Stillman and Somero, 1996, 2000; Stillman, 2002). greenhouse gases are currently causing a worrisome increase in Indeed, Harley (2008) has documented recent mass mortalities of globally averaged air temperature (IPCC, 2007), and the scientific mussels and limpets on wave-swept shores. Shifts in geographical community has mobilized to predict the ecological effects of range and fluctuations in abundance have already been observed in consequent climate change. Wave-washed rocky shores provide a response to recent warming, particularly in Europe where long-term potentially important system in which to develop and test these and broad scale baselines exist (e.g. Lima et al., 2006, 2007; predictive abilities, in large part because the rich history of Mieszkowska et al., 2007; Hawkins et al., 2008, 2009). The general experimentation on intertidal communities provides a wealth of interpretation of these findings is that relatively small changes in baseline information on distribution and the roles of competition, imposed body temperatures, due to direct or indirect effects of global predation, facilitation, dispersal, recruitment, disturbance, environ- change, could elicit profound population and ecological shifts, making mental stress, and patch dynamics (e.g., Bertness et al., 2001; Helmuth intertidal communities a bellwether for the consequences of climate and Tomanek, 2002; Helmuth et al., 2006a). In addition, intertidal change (Southward et al., 1995; Helmuth et al., 2006a). animals and seaweeds may be particularly sensitive to both direct and However, as Pincebourde et al. (2008) note, rocky intertidal shores indirect effects of environmental temperature change (Sanford, 2002; are “among the most thermally complex” on Earth. Variegated Helmuth et al., 2006a, 2011-this issue; Somero, 2002, 2010; Lockwood topography and the ever-changing pattern of the tides can cause and Somero, 2011-this isue). For example, a variety of intertidal organisms in close proximity to experience dramatically different organisms already periodically experience habitat temperatures at or thermal environments (e.g., Harley and Helmuth, 2003; Denny et al., 2006; Harley, 2008; Miller et al., 2009). Furthermore, different species respond differently to thermal stress (e.g., Somero, 2010; Marshall ⁎ Corresponding author at: Hopkins Marine Station, 100 Ocean View Blvd, Pacific Grove, CA 93950, USA. Tel.: +1 831 655 6207. and McQuaid, 2010), and the response even within a species can vary E-mail address: [email protected] (M.W. Denny). from place to place (e.g., Kuo and Sanford, 2009). This small-scale 0022-0981/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2011.02.006 176 M.W. Denny et al. / Journal of Experimental Marine Biology and Ecology 400 (2011) 175–190 environmental and physiological complexity can confound compar- glued to the substratum (Fig. 1). We attempted to install each device with ison among sites (e.g., Wethey, 2002; Harley and Helmuth, 2003; minimal disturbance to the surrounding organisms. Because of its Harley, 2008), a difficulty that poses a serious challenge for intertidal spherical shape, each ball presented the same area for solar heating ecologists as they attempt to predict large-scale effects of rising regardless of the orientation of its mounting; only the properties of the temperatures (e.g. Poloczanska et al., 2008, barnacle species compo- microhabitat–rather than the instrument–vary from location to location. sition with different future climate scenarios). iButtons have a precision of 0.5 °C, and to improve accuracy, each How can intertidal ecologists best incorporate local thermal instrument was calibrated prior to deployment. Temperatures were variability into their predictions of the effects of climate change? As recorded every 10 min for 12 days. These temperature loggers were not a step toward answering this question, we address two fundamental intended to mimic any particular organism, but rather to provide a issues. First, how variable is body temperature among individuals at a standard measure of temperature that could be compared among single site in the intertidal zone? Previous experiments that included locations without complications due to organisms' variable morphology. measurement of within-site variation generally relied on indirect The “thermal mass” of each logger (the product of its mass [80.65 gm] and measurements (e.g., Elvin and Gonor, 1979; Harley, 2008) or a small specific heat capacity [377 J kg−1 °C−1]) is the same as that of a 7.24 gm number (2–6) of direct measurements (e.g. Helmuth and Hofmann, organism with the specific heat of water (4200 Jkg−1 °C−1), such as a 2001; Helmuth et al., 2006b; Harley, 2008; Petes et al., 2008). In field small mussel. Because the thermal conductivity of the PVC connecting experiments, we have used a more intense deployment of measuring rod is relatively low (0.19 Wm−1°C−1 compared to 2.3 Wm−1 °C−1 for devices (up to 221), and document extreme inter-individual variation granite or 0.6 Wm−1 °C−1 for water), the loggers are not as tightly in body temperatures. We then examine the implications of this coupled to the temperature of the rock as are organisms such as acorn variability for local species persistence. Specifically, we ask, how does barnacles and limpets, which maintain effective conductive contact within-site variability affect the fraction of a population killed by heat with the substratum (Wethey, 2002; Denny and Harley, 2006). stress? We conclude that, if sufficiently large, within-site variability in The distance between adjacent temperature loggers was measured thermal experience can buffer the local effects of either long-term along the shore using large calipers. For the first 98 measurement temperature trends or increased frequency of stochastic, extreme locations, the spacing between them was 0.46 m, for the next 75 events. We suspect that, at least in some cases (e.g., Broitman et al., locations, spacing was 1.72 m, and for the remaining 48 locations, 2009), local variability will play a more important role in population, spacing was 3.44 m. species, and community-level responses to global change than mean A similar set of measurements was conducted at a reduced number regional differences among sites. Our results further highlight the (173) of locations (a total transect length of 235 m) beginning on need for ecophysiological and evolutionary studies examining the September 11, 2002. Temperatures were recorded every 10 min for effects of this fine scale of variability on intertidal populations. 12 days. 2. Materials and methods 2.2. Simulated mussel bed We present the results of six independent intertidal experiments fi that vary in their physical scale (less than 1 m to 100 s of m), duration, As a rst means to estimate the details of small-scale variation in time of year, and level of biological similitude. All data were collected mussel body temperature, 114 mussel shells (Mytilus californianus) at Hopkins Marine Station (HMS) of Stanford University in Pacific were used to construct a small simulated bed approximately 23 cm in Grove, California, USA (36° 37′15″ N, 121° 54′ 15″ W). The granite diameter. Shells were obtained from the bed at HMS, and were typical substratum adjacent to HMS forms a topographically complex of mussels at this site, with lengths varying between 42 and 65 mm. shoreline typical of many intertidal sites, and is classed as “moder- We extracted the resident mussel from each shell and replaced it with ately exposed” to waves (Ricketts et al., 1985).
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