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Morphological and ecological determinants of body temperature of Geukensia demissa, the Atlantic ribbed mussel, and their effects on mussel mortality.

Introduction

Quantitative prediction of the effects of global climate change on species ranges and on patterns of organismal abundance and biodiversity is an important and increasingly pressing issue. Evidence of the impacts of climate change can be seen in a variety of environments, through influences on population abundances, species ranges, and interactions within ecological communities (Walther et al., 2002). Current models suggest that the rate of climate change is accelerating (IPCC, 2001; Stainforth et al., 2005), and changes in air, sea, and surface temperature are likely to have great consequences for the planet's ecosystems, especially in intertidal zones (Ray et al., 1992; Suchanek 1994) where many organisms are thought to live close to their thermal tolerance (Doty, 1946; Connell, 1972; Somero, 2002; Davenport and Davenport, 2005). Body temperature has been shown to control local and latitudinal distributions of many intertidal species (Wethey, 1983; Fields et al, 1993; Bertness et al., 1999), and small changes in global air, surface, and water temperatures are likely to cause shifts in patterns of species distribution over a range of spatial scales (e.g., Southward et al., 1995; Sagarin et al., 1999; Gilman et al., 2006; Helmuth et al., 2006a, b). Therefore, intertidal invertebrate species are potentially very good indicators of the effects of global climate change on species distribution patterns (Barry et al., 1995; Southward et al., 1995; Sagarin et al., 1999; Harley et al., 2006, Helmuth et al., 2006a).

In many cases, however, we do not have sufficient information on the body temperatures of intertidal organisms in the field to gauge how closely intertidal animals are living to their thermal limits (Denny et al., 2006, Helmuth et al., 2006a). Moreover, for many intertidal invertebrates, our knowledge of lethal limits comes from studies conducted in water, despite the fact that recent studies have suggested that both aquatic and aerial temperatures may be important to physiological performance and survival (Stillman, 2003; Tomanek and Sanford, 2003; Somero, 2005; Denny et al., 2006; Fields et al., 2006). During submersion at high tide, organisms are likely to have body temperatures similar to that of the surrounding water (Helmuth, 1998). In contrast, at low tide, the organism must cope with the changing conditions of the terrestrial environment. During aerial exposure, the body temperature of an intertidal invertebrate is driven by multiple climatic factors such as wind speed, solar radiation, cloud cover, and air and surface temperature, and the animal's temperature is often considerably warmer or cooler than the surrounding air (Helmuth, 2002; Denny and Harley, 2006). Significantly, body temperatures experienced during low tide have been shown to cause physiological damage (e.g., Hofmann and Somero, 1995; Stillman, 2003; Somero, 2002, 2005), suggesting that an understanding of geographic patterns in aerial body temperature is crucial for estimating the effects of climate change on intertidal species (Gilman et al., 2006; Helmuth et al., 2006b). Moreover, we often have an incomplete understanding of what aspect of body temperature (maximum, minimum, or time history) most strongly affects survival, growth, and reproduction. Understanding and predicting the effects of climate change on species distribution thus requires that we have not only a detailed understanding of each species' physiological responses to body temperature, but also a concomitantly detailed knowledge of what the patterns of body temperature are in nature, in both aquatic and aerial thermal regimes.

Recent studies have suggested that patterns of intertidal body temperature can be far more complex than previously recognized. Helmuth and Hofmann (2001) showed that body temperatures of rocky intertidal mussels varied by more than 10 [degrees]C owing to the effects of substratum angle, and Denny et al. (2006) found that these variations in substratum angle could account for variability in risk of mortality. Also, since the physical characteristics of an organism (e.g., factors such as shape, color, and mass) affect the likelihood that it will experience extremes in body temperature, patterns in high- and low-temperature stress are likely to vary between species (Denny and Harley, 2006) and with body size (Helmuth, 2002). Thus, two species of organisms, or two organisms of the same species but of varying size, can experience very different body temperatures when exposed to identical physical environments (Helmuth, 2002; Denny and Harley, 2006). While variability in responses to past climate change has been shown to occur with body size (Roy et al., 2001), the underlying biophysical and physiological determinants of this size effect are poorly understood for most intertidal organisms. For rocky intertidal organisms, larger mussels are thought to be more thermally stable than smaller animals because they have greater thermal inertia (Lent, 1968), and small mussels may experience more extreme body temperature during brief exposures to extreme climatic conditions (Helmuth, 1998, Helmuth, 1999). However, over long exposures, large mussels are predicted to reach a more extreme body temperature than small mussels (Helmuth, 1998, Helmuth, 2002).

This effect has yet to be explored for intertidal salt marsh organisms. Thus, the failure to consider patterns of aerial temperature and the interactions of morphological factors such as body size on body temperature neglects the potential to detect responses to climate change that may operate on smaller spatial scales, and which may be important determinants of physiological stress. By mechanistically identifying the environmental and morphological determinants of body temperature, we will be better prepared to understand how climate sets local zonation patterns and levels of competitive ability (Wethey, 1983). In addition, the added factor of vertical body position (the proportion of the organism exposed above the substrate) in soft-sediment habitats has not been examined.

Here we quantitatively examine the primary determinants of within-site variability in body temperature of the salt marsh mussel Geukensia demissa. We explicitly examine the effects of body size and small-scale microhabitat (position within the mud surface) on body temperature, and quantify differences in body temperature between sites with and without marsh grass cover. By examining the complex patterns of body temperature and how these temperatures vary with microhabitat, body size, and body position, our goal is to understand where and when the maximum body temperatures are most likely to occur in the field, and to assess how important each of these morphological (size), behavioral (position), and environmental (grass cover) factors are to body temperature. Using these field data to create a laboratory experiment that closely mimics actual field body temperatures, our goal is to determine at what daily maximum body temperature mussel mortality occurs. We are then able to compare laboratory mortality rates to field data to determine whether mortality due to heat stress is likely to be occurring in the field, and if so, where and when it is likely to take place.

Study system

Geukensia demissa (Dillwyn, 1817; formerly Modiolus demissus) is an abundant salt marsh species that plays an ecologically significant role in marsh dynamics by alleviating nutrient deficiencies through deposition of nitrogenous wastes on the sediment surface (Bertness, 1984). In addition, the interaction between Spartina alterniflora and this mussel species prevents marsh disturbance and erosion. Therefore, this species is ideal for an examination of the possible effects of climate change on salt marsh ecosystems in the western Atlantic. G. demissa has a wide geographical range along the eastern coast of North America, from the Gulf of St. Lawrence to Northern Florida (Abbott, 1954), and is found in a range of intertidal microhabitats that can potentially vary greatly in thermal regime.

In salt marsh environments, mussels are buried in the substrate, often up to the level of the siphon, and they have a greatly reduced surface area exposed to air during low tide. However, there can be high variability in mussel body position; some mussels may be completely buried, while others may be almost entirely exposed above the sediment surface. This variation is likely to have a great effect on mussel body temperature. Other sources of microhabitat variation include the amount of standing water in the substrate during low tide (as a function of sediment grain size) and the intensity of solar radiation and wind speed at the level of the sediment surface (as a function of amount of vegetation present). These three variables (body size, body position, and amount of vegetation) thus represent the most likely sources of within-site thermal variability, and we tested their relative importance in modifying the body temperature of G. demissa.

Materials and Methods

Estimating mussel body temperature using physical models

To estimate Geukensia demissa body temperature in the field, we modified Helmuth and Hofmann's (2001) design for a thermally matched (biomimetic) temperature logger. The logger is a physical mimic composed of an empty G. demissa shell, 100% clear silicone caulking, and a small, battery-operated temperature logger (iButton, Maxim Integrated Products, Dallas Semiconductor) that measures estimated mussel body temperature at 20-min intervals in the field. Continuous body temperature data were collected every 20 min from 20 May through 31 August 2004. All data were collected at the Belle W. Baruch Institute in the North Inlet Estuary of South Carolina (33'21.0"N, 79'10.8"W).

To determine mussel mimic accuracy, body temperatures of living mussel were compared to those of mussel mimics at a variety of wind speeds in a wind tunnel in the laboratory. For each trial, 6 living mussels (3 allowed to gape, and 3 rubber-banded shut to prevent gaping) and 2 mussel mimics were arranged in a circle under a halogen heat lamp, and all mussels were buried in a layer of sediment with 3 cm of the animal exposed above the level of substrate. To eliminate potential effects of mussel size, experimental mussels were between 7 and 8 cm in shell length. All mussels were oriented with valves facing into the wind, and all mussels (including mimics) were equidistant from the halogen heat lamp. A ramp was designed using plastic foam (Styrofoam) insulation from the bottom of the wind tunnel to the top of the sediment layer to reduce disturbances in wind flow across the mussels.

We used a metal file to make a small hole in the mussel shell on the posterior end of the shell and inserted copper/constantan thermocouples into the mantle tissue to measure living mussel body temperature every minute. Body temperature data were recorded using a Campbell datalogger (Campbell Scientific, Logan, UT). Estimated mussel body temperatures were measured every minute using iButtons inserted into the mussel mimics. Trials were run under a halogen heat lamp in a wind tunnel for 3 h, with mussels slowly heating under the heat lamp for 90 min and cooling with the lamp off for 90 min. Prior to the experiments, two 1-1 flasks of boiling tapwater were added to the wind tunnel downwind of the mussels to increase the humidity level to at least 80% relative humidity. These humidity levels were maintained throughout the experiments. Three replicate trials were conducted for each of three wind speeds: 0.5, 1, and 1.5 m/s.

Effects of microhabitat, body position, and body size

Three within-site microhabitats were selected on the basis of vegetation (Spartina alterniflora) and sediment type: Microsite 1 (Dry) was not vegetated and had well-drained sediment at low tide; microsite 2 (Wet) had no vegetation and had standing water at low tide; microsite 3 (Grass) had Spartina alterniflora present and had well-drained sediment. All sites were located within 50 m of one another and were at the same tidal height with an average of 67% aerial exposure time per tidal cycle.

Three body sizes were examined: small (4-6 cm in shell length), medium (6-8 cm), and large (8-10 cm). In addition, three body positions of mussels within the sediment (measured in terms of length of shell exposed above the sediment surface) were examined, and all are biologically relevant to field conditions: 0 cm (entirely buried within sediment), 3 cm, and 6 cm (Fig. 1). Mussel models were attached to wooden dowels (3 loggers per dowel, one at each vertical body position; 3 body sizes x 2 replicates = 6 dowels per microsite) using marine epoxy (Evercoat Zspar), and positioned in the sediment to ensure proper positioning.

Temperature analysis

Because of the large number of samples collected by the loggers, body temperatures were summarized on a monthly basis, using average daily maxima (Fitzhenry et al., 2004). For each day of the month, the daily maximum body temperature was calculated for each logger. The daily maxima were then averaged over the entire month. This measurement is useful because it is an indicator of "chronic" high-temperature stress, and it integrates body temperatures experienced during both aerial and aquatic conditions (Helmuth and Hofmann, 2001). Statistical analyses were conducted using an ANOVA and a post hoc Tukey's test (SAS, ver. 8.1). Average daily maximum body temperatures were analyzed separately for each variable: body size, body position, and microhabitat.

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Laboratory study

Thermal regime. Using estimated body temperatures collected in the field, we set up a laboratory experiment to examine the effects of daily maximum temperatures on the survival and growth of G. demissa. Estimated mussel body temperatures collected using mussel thermal mimics during summer 2004 were analyzed to estimate a typical "hot" day in the field for these mussels. Based on past research examining G. demissa heat tolerance (Lent, 1968), days with a body temperature of 45 [degrees]C and higher were considered "hot." We deployed 54 physical loggers in the field during summer 2004 and recorded a total of 141 instances in which the body temperature exceeded 45 [degrees]C. For each of these events, we determined (1) the time of the daily minimum body temperature, (2) the time of the daily maximum body temperature, (3) the rate of heating during the day, and (4) the timing and duration of the high tide. On average, we determined that the mussels experience a nighttime high tide for about 4 h, and that the daily minimum temperature generally occurred around 0600. There was then a period of heating (at an average rate of 2.66 [degrees]C per hour) until 1500 when the maximum body temperature was reached. There was then a cooling period during low tide until the tide came in later in the evening.

Experimental tank set-up. The laboratory experiment was set up to mimic mussel body temperatures under field conditions as closely as possible (Fig. 2), with field conditions based on mussel body temperature data estimated using thermal mimics. In a screened laboratory, we set up six temperature treatments (varying in daily maximum temperature: 30, 35, 40, 45, 50, or 55 [degrees]C). For each treatment, halogen heat lamps (on timers) hanging from the ceiling (varying in intensity and distance from the sediment surface) were used to regulate mussel body temperature from 0600 to 1500. The rate of heating for each treatment was set to fall within the range seen in the field. In addition, there was an artificial tidal cycle (created using a solenoid valve on a timer), with a high tide coming in every day at 1800 and lasting for 4 h. The mussels were fed unfiltered seawater pumped directly from the marsh at the Belle W. Baruch Marine Institute in Georgetown, South Carolina. The seawater used in the experiment was identical in both temperature and salinity to the seawater from the marsh field sites so that any changes in these parameters during the experiment mimicked changes that would also have been experienced by mussels in the field.

For each of the six treatments (20 individuals X 6 treatments X 2 replicates = 240 mussels total), we used a small plastic bin to set up artificial marsh conditions. The bins were layered with a screen mesh along the bottom, a 3-cm layer of natural aquarium gravel (no coloring added), another layer of mesh screen, and a 3-cm layer of sediment collected from the same marsh site as the mussels as the top layer. Five small drainage holes (4 cm in diameter) were punched out of the bottom panel and the side panel (above the level of sediment) of each bin. Unfiltered seawater entered into each tub through PVC pipe coming from the main seawater line, and the water was allowed to flow along the bottom of each tub before draining back out to the marsh. Therefore, there was a constant supply of water to the base of each bin to ensure that the sediment stayed moist even during low tide, mimicking the average marsh conditions as closely as possible. During high tide, water would slowly fill each bin from the bottom. The water level would then reach the holes in the side panel and slowly drain out of the bin. Therefore, this system allowed the water to flood the bins at high tide and also maintained sediment moisture during low tide. In addition, this system allowed seawater to be constantly moving through the system, preventing stagnant conditions and giving a constant food supply to the mussels during high tide.

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Specimen collection and experimental exposure. Live mussels (ranging in shell length from 45 to 70 mm) were collected from the high intertidal marsh at the Belle W. Baruch Marine Institute on 20 May 2005. The mussels were rinsed in saltwater to clean the shells of byssus threads and other debris and then transferred to a holding tank with continuously running unfiltered seawater in the screened laboratory. The mussels were held under these conditions for 2 weeks to remove any effects of thermal history in the field prior to collection. On 4 June 2005, mussels were removed from the holding tanks and individually tagged with a number (a strip of paper, glued to the shell with cyanoacrylate adhesive and coated with a layer of clear nail polish to waterproof the paper), and labeled with a dot of colored nail polish corresponding to the temperature treatment. Mussels were oriented in growth position with the posterior end of the organism perpendicular to the sediment surface. Within 24 h, each mussel had attached to the layer of screen mesh at the bottom of the sediment layer with new byssus threads, and a natural mussel body position was maintained actively throughout the experiment.

The heating regime began on 4 June 2005 and ran for 12 weeks. Estimated body temperature of each treatment was measured every 5 min using a mussel mimic (described above) buried to the same level as the living mussels. Once per week, each bin was examined for dead individuals. Dead mussels were removed, and the date and mussel numbers were recorded. In addition, the estimated body temperature was collected from the mimics each week to ensure that the heating regime was accurate. To maintain accuracy, the heat lamps were slightly repositioned on the basis of the temperatures of the previous week.

Results

Logger accuracy

Comparison of mussel mimic body temperatures and living mussel body temperatures showed that mimics provide a close estimate of living tissue temperatures and that mimic accuracy increases with increasing wind speed (Table 1). Mimics tended to warm more quickly and cool more quickly than living mussels, but the general patterns of body temperature remained the same (Fig. 3). Additionally, due to the potential effects of cooling through evaporation on mussel body temperature, some mussels were banded shut to prevent gaping. If cooling was occurring via evaporation, we expected banded mussels to have higher body temperatures. However, results showed that the body temperature of banded mussels closely resembled that of mussels allowed to gape, and at times it tended to be cooler (Fig. 3).

Temperature analysis

On several occasions, loggers were lost or damaged. In these situations, temperature data have been omitted, causing a few gaps in the summer temperature data. Body temperatures were similar for all three body sizes, regardless of body position, microhabitat, or month (Fig. 4). There was no significant effect of body size and no significant interactions between body size and either body position or microhabitat (Table 2). Therefore, the analysis was conducted a second time, eliminating the variable of body size from the ANOVA. The results of the two-way ANOV As by month (Table 3) showed a significant effect of body position on mussel body temperature across all summer months. In general, the 0-cm body position was warmer at night than the others and cooler in the day, suggesting a less extreme environment (Fig. 4). Mussels in the 6-cm body position experienced both the hottest and coldest temperature (in most cases) throughout the summer (Fig. 4). At one point, a mussel in the 6-cm position was up to 25 [degrees]C hotter than mussels in the 0-cm position (compared within one body size and one microhabitat), the largest difference seen among all of the variables examined.

Body temperature differences based on microhabitat were more difficult to interpret (Fig. 4). When microhabitat differences within one body size and body position were compared there was a very large effect of marsh location in some cases (Fig. 4). In each of these cases, Grass was the hottest site, Dry was intermediate, and Wet was the coolest. There was a significant effect of microhabitat in every month except August, suggesting that there was a differential rate of heating in early and late summer months between sites, but that sites were consistently hot in August, with no statistical difference in mussel body temperature between sites (Table 3). Mussels at the 0-cm body position were not significantly distinct across microhabitats. However, at the 6-cm body position, microhabitat had a significant effect, with Grass being warmer than Dry, which was warmer than Wet. When comparing average daily maximum mussel body temperature by month, May was the hottest summer month for all sites and body positions (Fig. 5). In addition, there was a significant interaction between microsite and vertical position during June (Table 3). At the Dry and Wet microsites, mussels at the 3-cm body position more closely resembled those at the 0-cm body position early in summer, but more closely resembled those at the 6-cm body position in August (Fig. 5). On the other hand, at the Grass microsite, the 0-cm and 3-cm positions were more closely matched, while the 6-cm one was distinctly warmer (Fig. 5).

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Mussel survival

Owing to daily fluctuations in air temperature in the screened seawater laboratory, the distinct body temperature treatments were not maintained as expected. Therefore, laboratory data are presented as a linear regression based on actual average daily maxima experienced by the mussels. The mussel survival rate decreased sharply at average daily maximum body temperatures above 45 [degrees]C, and mortality was 100% above 50 [degrees]C (Fig. 6). In addition, an increase in the total time spent above 45 [degrees]C (measured in degree minutes) resulted in an increase in mortality rates (Fig. 7). Using the laboratory data, we determined the number of days in summer 2004 in which field conditions corresponded to a potential mortality event for G. demissa (Table 4A). The highest potential mortality risk occured in the vegetated microhabitat and for mussels exposed at the 6-cm vertical body position. We also determined the number of days in summer 2004 that would have resulted in a potential mortality event based on an increase of either 2 [degrees]C (Table 4B) or 3 [degrees]C (Table 4C) in mussel body temperature. If body temperatures increase even a few degrees, the potential for mortality will be greater in all microhabitats and depths; with an increase of 3 [degrees]C in body temperature, there is a potential for mortality to occur across the entire population, regardless of microhabitat or vertical body position.

Discussion

Temperature patterns

The results of this study suggest that patterns of mussel body temperature in soft-sediment habitats, and specifically the effects of body size on body temperature, can be drastically different from those seen in the rocky intertidal zone (Denny and Harley, 2006). For example, the lower thermal inertia of small rocky intertidal mussels allows them to heat more quickly than large mussels, leading to differences in body temperature across a range of body sizes in this environment (Helmuth, 1998). Conversely, no pattern was seen across body size and body temperature in the salt marsh habitat. It is likely that this difference is due in part to the mussels' large contact area with the substrate. The mud acts as one large heat sink, heating slowly and retaining heat once warm. With an increase in contact between the organism and the substrate, the organism body temperature is more closely related to the substrate temperature, as has been observed for rocky intertidal barnacles (Wethey, 2002). This mechanism works well to describe the lack of difference in body size for mussels held at the 0-cm body position. However, mussels at the 6-cm body position have very little contact with the soft-sediment substrate, and still body size does not play a significant role in determining body temperature. The reasons why body size does not appear to affect body temperature in salt marsh mussels therefore remains enigmatic.

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We found that the effect of microhabitat is similar to that seen in other habitats, including the rocky intertidal zone. The mussels are likely to experience body temperature differences over very small scales (1-10 m) within the same salt marsh, due to presence or absence of vegetation. However, past studies have suggested that the presence of Spartina alterniflora in the habitat would act as a cooling agent by providing shade to the substrate and the mussels (Kuenzler, 1961). Our results suggest that the presence of Spartina may have quite the opposite effect for G. demissa, as the vegetated site was the hottest of three microhabitats. One possible explanation for this trend is a decrease in convection due to the cordgrass. With an increase in vegetation close to the sediment surface, wind speed decreases, reducing cooling through evaporation and convection. In general, evaporative cooling is already low in this species due to the high humidity levels (80%-90% relative humidity) close to the sediment substrate. Additionally, comparison of banded and gaping mussels in this study suggested that evaporative cooling does not play a role in the body temperature of this species. However, the reduced wind speed is likely to greatly decrease convective cooling. In most cases, the sediment heats to a higher temperature than the air above the substrate. With reduced air flow, the ability of the substrate and the organisms embedded in it to lose heat to the environment decreases. Also, although the vegetation is likely to increase shading to the substrate in some situations, we have found that mussels are most likely to experience maximum body temperatures early in the afternoon, when the sun is directly overhead, reducing any effect shading would have on body temperature.

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Although we found that microhabitat plays a role in determining body temperature, the main factor that appears to affect body temperature is vertical body position. A vertical difference of 6 cm results in up to a 25 [degrees]C difference in body temperature. These results suggest that small-scale differences in vertical position (cm) are more important in determining potential heat stress than are meters of horizontal position (microhabitat) or several hundred kilometers in latitude (climate).

We suggest that mussels in the 6-cm body position are at a strong thermal disadvantage to those at more buried body positions. The question remaining is, can mussels actively regulate their vertical position in the sediment? As larvae mussels settle out of the water column onto the substrate, there is a preferential settlement on or near the shells of conspecifics (Bertness and Grosholz, 1985; Nielson and Franz, 1995). As a result of this behavior, mussels are often found in large clumps, which may result in crowding that causes them to be pushed farther above the sediment surface as surrounding mussels grow in size. However, it is not rare to find a solitary mussel in the salt marsh habitat, especially at the higher tidal heights where density is lower. If exposed body positions are negative, one would expect solitary mussels to be completely buried, which is not always the case.

Often solitary mussels are found at vertical body positions of 3-6 cm above the sediment surface, suggesting either an advantage to this position or the inability to regulate body position above a certain body size. It is possible that an increase in flow rate during high tide allows for better food consumption as the individual moves away from the substrate. In addition, a mussel may have to use less energy to remove sediment from the water column during feeding events when it is farther from the mud surface. Another possible explanation for the large numbers of mussels found at the 3-6-cm position in the field may be that increased body temperatures are beneficial to a point. For example, it is possible that at these positions, mussels experience increased rates of metabolism, digestion, and growth, while experiencing hot, but sublethal, temperatures most of the summer. Even if these mussels run some risk of being exposed to lethal body temperatures throughout the summer months, thermal benefits at the 3- and 6-cm body positions may outweigh these risks.

Mussel survival

We showed that mussels can die when exposed to a heating regime similar to that seen regularly during the summer months. Even a few moments of exposure at about 50 [degrees]C is enough to result in 100% mortality. At the same time, we recorded temperatures above 50 [degrees]C in the field during summer 2004. In addition, we found a strong decrease in survival at daily maximum body temperatures about 45 [degrees]C, conditions that are seen in the field fairly regularly.

A previous study has suggested that, thanks to the cooling from evaporation from the surrounding mud. mussels in the salt marsh habitat are not likely to reach their thermal limits (Lent, 1969). Although most previous studies have examined the thermal limits of submerged mussels (e.g., Hilbish, 1987), some references to heating during aerial exposure can be found (Read and Cumming, 1967; Lent, 1968). However, these studies concluded that the upper tolerance limit lies between 36 and 40 [degrees]C. In this study, technological advances allowed us to measure mussel body temperature in the field and discover that mussel temperature often exceeds that of air temperature, contrary to past suggestions (Lent, 1969). In addition, we have shown that mussel body temperature often exceeds both the previously determined limits (36-40 [degrees]C) and the current thermal limits discovered here (!!45 [degrees]C). On the basis of these results, we suggest that mortality occurs in South Carolina estuaries during the summer months at a variety of microhabitats within the salt marsh.

Implications for climate change

The Intergovernmental Panel on Climate Change 2001 Synthesis report (IPCC, 2001) outlines several several scenarios of climate change, in particular with expected increases in air temperature. For two of these scenarios, A2 and B2, air temperature in coastal South Carolina is expected to increase by 2 to 3 [degrees]C, respectively, by the year 2100. Given that mortality due to heat stress should already be occurring in South Carolina salt marshes, it is likely that heat stress will continue and possibly become a greater concern over time. More specifically, the majority of heat-related mortalities in this mussel population are predicted to be currently occurring at the 6-cm position and to a lesser extent at the 3-cm position. While air temperatures may not translate directly into changes in body temperature (see below) they may give some indication of what changes lie ahead. With a 3 [degrees]C increase in mussel body temperature, mortality due to heat stress may be likely to occur at all microhabitats and at all vertical body positions, making the entire mussel population vulnerable to heat mortality.

However, the current climate-change scenarios predict temperature changes in terms of air and water temperatures only. Although these predictions may allow for some rough estimates of future conditions for Geukensia demissa populations in South Carolina, these predictions do not suggest what future trends in mussel body temperature will be. As shown by Gilman et al. (2006), climate-change predictions for a species require the following three items: (1) current and future climate predictions, (2) the relationship between climate and body temperature for that species, and (3) the physiological tolerances of that species. In this study, we have successfully measured animal body temperature in the field and begun exploring the physiological tolerance of G. demissa. However, we still do not understand the exact relationship between air temperature and body temperature, and therefore we cannot accurately predict how mussel body temperature will change with the current climate-change scenarios. It is likely that a 1 [degrees]C increase in air temperature will not result in an equal increase in mussel body temperature (Gilman et al., 2006).

Assuming that an increase in air temperature will result in at least a small increase in mussel body temperature, more and more mussels may become prone to heat stress, and G. demissa populations may suffer. This species has been shown to play a key role in the salt marsh ecosystem, specifically--through its interaction with Spartina alterniflora--in terms of the nitrogen cycle (Jordan and Valiela, 1982) and the prevention of marsh erosion (Bertness, 1984). Therefore, it is possible that a strong decrease in the abundance of G. demissa may lead to a die-off of Spartina alterniflora in some areas. With a loss of vegetation, the salt marshes will be more prone to erosion. Therefore, the ability to monitor the body temperature of this species and the potential effects of this temperature on population may have larger implications if climate change influences the levels of heat stress being experienced by this mussel population.

Conclusions

Unlike past studies examining patterns in the body temperature of rocky intertidal invertebrates (e.g., Helmuth and Hofmann, 2001), our results, obtained by directly measuring body temperature patterns in the field, show that body size is of little importance in determining body temperature in the soft sediment habitats. Second, in agreement with other studies in the rocky intertidal zone (e.g., Helmuth, 1998), we found that small horizontal scales are important in the soft-sediment habitat. However, the dominant determinant of body temperature is vertical position in the sediment, and a few centimeters can result in temperature differences of more than 20 [degrees]C. Therefore, the ability of mussels to regulate vertical position and the causes for mussel positioning in the field have become of greater interest than initially expected. In the laboratory, we found it is possible to recreate the typical "stressful" day in the intertidal, showing that mussel mortality is occurring at temperatures of 45 [degrees]C and higher. What is of greatest interest in this study is the potential for mussel mortality to be occurring in the field on a regular basis. On the basis of field and laboratory data, we have concluded that mussel mortality due to heat stress should be occurring at a variety of microhabitats within South Carolina estuaries.

Acknowledgments

The authors thank S. Forehand for assistance with laboratory set-up, and the Belle W. Baruch Marine Institute for access to field sites and for use of the running seawater laboratory. In addition, we thank K. A. Smith, L. Szathmary, C. Purvis, L. Burnett, J. Hilbish, D. Wethey, and S. Woodin for help in editing earlier versions of the manuscript. This research was funded by the National Science Foundation (OCE-0323364) and by NOAA NA04NOS4780264.

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JENNIFER JOST* AND BRIAN HELMUTH

Department of Biological Sciences and Belle W. Baruch Institute, University of South Carolina, Columbia, South Carolina 29208

Received 22 September 2006; accepted 9 May 2007.

* To whom correspondence should be addressed. E-mail: jostja@unc.edu
Table 1 Average ([+ or -] standard error) and maximum temperature
differences ([degrees]C) between average mussel mimic estimated body
temperature and living mussel body temperatures for three wind speeds

                  Average difference                  Maximum difference
Wind speed (m/s)  ([degrees]C)        Standard Error  ([degrees]C)

0.5               1.50                0.0605          4.87
1                 1.11                0.0856          4.05
1.5               1.15                0.0798          4.72

Data are averaged over three 3-h replicate trials per wind speed.

Table 2 Fixed effects ANOVA by month for the average daily maximum
mussel body temperature taken from a South Carolina estuary for three
body sizes during the summer of 2004 show no significant effects

Month   DF  Type III SS  Mean Square  F value  P value

June    2    0.3003135   0.1501567    0.24     0.7917
July    2    5.3729286   2.6864643    2.7      0.0865
August  2   11.65681     5.828405     1.34     0.2793

Table 3 Fixed effects ANOVA by month for the average daily maximum
mussel body temperature taken from a South Carolina estuary for three
microsites, three vertical body positions, and possible interactions
during the summer of 2004

                          Type III  Mean    F       P
Month   Source        DF  SS        Square  value   value

June    site          2     9.47      4.74    7.66   0.0015
        depth         2   211.38    105.69  170.88  <0.0001
        site X depth  4    17.47      4.37    7.06   0.0002
July    site          2     7.64      3.82    3.38   0.0435
        depth         2   249.20    124.60  110.14  <0.0001
        site X depth  4     5.35      1.34    1.18   0.3323
August  site          2     2.18      1.09    0.30   0.7438
        depth         2   179.98     89.99   24.66  <0.0001
        site X depth  4    16.09      4.02    1.10   0.3679

Table 4 Number of days in 2004 when mussel body temperatures were above
45 [degrees]C in the South Carolina salt marsh based on microhabitat and
vertical body position for three conditions: (A) summer 2004 estimated
mussel body temperatures, (B) a body temperature increase of
2 [degrees]C, and (C) a body temperature increase of 3 [degrees]C

Condition  Site  0 cm  3 cm  6 cm

A          SC1    1    11    14
           SC2    0     3     5
           SC3    3     2    29
B          SC1    4    17    31
           SC2    0     6    16
           SC3    9     5    44
C          SC1    5    23    35
           SC2    2    10    23
           SC3   10     8    55
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Author:Jost, Jennifer; Helmuth, Brian
Publication:The Biological Bulletin
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Date:Oct 1, 2007
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