© 2002 by The Society for Integrative and Comparative Biology
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Water Temperature, Predation, and the Neglected Role of Physiological Rate Effects in Rocky Intertidal Communities1
1 Hopkins Marine Station, Stanford University, Pacific Grove, California 93950
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Ecologists and physiologists working on rocky shores have emphasized the effects of environmental stress on the distribution of intertidal organisms. Although consumer stress models suggest that physical extremes may often reduce predation and herbivory through negative impacts on the physiological performance of consumers, few field studies have rigorously tested how environmental variation affects feeding rates. I review and analyze field experiments that quantified per capita feeding rates of a keystone predator, the sea star Pisaster ochraceus, in relation to aerial heat stress, wave forces, and water temperature at three rocky intertidal sites on the Oregon coast. Predation rates during 14-day periods were unrelated to aerial temperature, but decreased significantly with decreasing water temperature. There was suggestive but inconclusive evidence that predation rates also declined with increasing wave forces. Data-logger records suggested that thermal stress was rare in the wave-exposed habitats that I studied; sea star body temperatures likely reached warm levels (>24°C) on only 9 dates in 3 yr. In contrast, wind-driven upwelling regularly generated 3 to 5°C fluctuations in water temperature, and field and laboratory results suggest that such changes significantly alter feeding rates of Pisaster. These physiological rate effects, near the center of an organism's thermal range, may not reduce growth or fitness, and thus are distinct from the effects of environmental stress. This study underscores the need to consider organismal responses both under "normal" conditions, as well as under extreme conditions. Examining both kinds of responses is necessary to understand how different components of environmental variation regulate physiological performance and the strength of species interactions in intertidal communities.
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INTRODUCTION |
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Conspicuous patterns of zonation and strong environmental gradients have long attracted ecologists and physiologists to rocky shores (Orton, 1929a
, b; Doty, 1946; Stephenson and Stephenson, 1949; see review by Benson, 2002). Invertebrate and algal species living higher in the rocky intertidal zone must tolerate longer periods of aerial exposure, and thus greater heat and desiccation than low intertidal species. In addition, species inhabiting more wave-exposed areas typically experience greater wave forces and less thermal stress than those in wave-sheltered habitats. These vertical and horizontal gradients in physical factors appear to play a central role in determining the distribution of many intertidal species (Orton, 1929a, b; Doty, 1946; Stephenson and Stephenson, 1949; Connell, 1961; Landenberger, 1969; Dayton, 1971). Recent work has made significant advances in understanding the physiological and molecular mechanisms that adapt intertidal species for life at different tidal heights (Hofmann and Somero, 1995; Stillman and Somero, 1996; Schmidt and Rand, 1999; Tomanek and Somero, 1999; Somero, 2002).
From an ecological perspective, it has become increasingly clear that environmental conditions not only set the distributional limits of many intertidal species, but may also alter the dynamics of these communities. This idea has been developed in environmental stress models that suggest that community dynamics are driven by the influence of stressful physical conditions on the strength of species interactions (Menge and Sutherland, 1976, 1987; Bruno and Bertness, 2001; Menge and Branch, 2001; Menge et al., 2002a). Following the definition of Menge and Sutherland (1987), "stress" in this paper refers to a reduction in the performance or fitness of an organism that arises from exposure to environmental conditions. Stress may be induced by direct mechanical forces acting on the organism ("physical stress"), or by changes in factors like temperature and salinity that affect organisms at the molecular and cellular level ("physiological stress") (Menge and Sutherland, 1987). Exposure to sub-optimal environmental conditions may induce physiological changes in an organism that increase its "cost of living" (Somero, 2002). However, in some cases, these costs may be fully compensated through various regulatory processes. In this paper, physiological changes are not referred to as "stress" unless negative impacts arise at the level of the whole-organism (e.g., as a reduction in growth or fitness).
Given the important role that predators and herbivores play in structuring many intertidal communities (Paine, 1966; Dayton, 1971; Menge, 1976; Lubchenco, 1978; see review by Paine, 1994), several models have attempted to link environmental variation to community dynamics by considering how stressful conditions may impact the physiological performance of consumers (Menge and Sutherland, 1987; Bertness and Callaway, 1994). An important prediction of consumer stress models (Menge and Olson, 1990) is that environmental stress will limit the effectiveness of consumers in stressful habitats. Near the limits of a consumer's physiological tolerance, stress prevents consumers from occupying certain habitats, providing prey with spatial and/or temporal refuges. For example, environmental stress may restrict mobile consumers to lower tidal heights, to sheltered microhabitats, or to time periods when stresses are reduced (Orton, 1929a, b; Paine, 1974; Menge, 1978a, b; Garrity and Levings, 1981; Levings and Garrity, 1983; Fairweather, 1988; Leonard et al., 1998; Witman and Grange, 1998; Burnaford, 2001; Bruno and Bertness, 2001).
Understanding community dynamics requires identifying not only the stresses that define the spatial and temporal bounds of a consumer's foraging range, but also how environmental variation affects performance and feeding rates within this space normally inhabited by the consumer (Huey and Stevenson, 1979; Kingsolver, 1989). Consumer stress models predict that increasingly stressful conditions should have sub-lethal effects on predators and herbivores that reduce rates of consumption (Menge and Sutherland, 1987; Menge and Olson, 1990). Sub-lethal effects on consumers have been documented largely through correlative field studies (e.g., documenting declines in feeding with intertidal elevation, or with exposure to more extreme wave forces; Menge, 1978a, b; Menge and Olson, 1990).
Only recently have coordinated field and laboratory studies begun to explicitly test the links among environmental variation, physiological performance, rates of consumption, and intertidal community dynamics (Sanford, 1999a, 2002b; Burnaford, 2001; Dahlhoff et al., 2001). To date, these efforts have focused primarily on the potential effects of aerial heat stress on consumers. Over short time scales (hours to weeks), intertidal organisms rarely experience changes in water temperature greater than 3 to 5°C, whereas temperature fluctuations of 10 to 20°C are common during tidal shifts from immersion to emersion (Helmuth, 1999; Helmuth and Hofmann, 2001; E. Sanford, unpublished data). Moreover, extreme temperatures (both maxima and minima) experienced by intertidal organisms also tend to occur during periods of low tide exposure. As a result, ecologists and physiologists working in intertidal systems have typically viewed short-term variation in water temperature as being unimportant relative to conditions experienced during aerial exposure (e.g., Dahlhoff et al., 2001).
In this paper I suggest that an emphasis on environmental stress has caused researchers working in intertidal systems to focus on physical extremes, while overlooking the more subtle environmental variation that may often regulate predation and herbivory on a day-to-day basis. As such, we have largely ignored the importance of physiological rate effects, considered here as changes in the rates of biological processes near the center of an organism's thermal range (Cossins and Bowler, 1987; Hochachka and Somero, 2002). Within an organism's normal thermal range, changes in temperature have well-documented effects on the rates of many physiological processes, due to thermal effects at the molecular and cellular level (Hochachka and Somero, 2002). Given that Q10's commonly lie between 2 and 3 on the rising side of thermal performance curves (Cossins and Bowler, 1987; Hochachka and Somero, 2002), an increase in temperature of 4°C is expected to increase rates of biological processes by 30–55%. Such Q10 effects are ubiquitous in laboratory studies documenting the effects of water temperature on feeding rates in a variety of intertidal consumers (Hanks, 1957; Largen, 1967; Mackenzie, 1969; Newell et al., 1971; Garton and Stickle, 1980; Stickle et al., 1985; Sanchez-Salazar et al., 1987; Stickle and Bayne, 1987). Despite this extensive literature of laboratory studies, field ecologists and physiologists working in intertidal systems have seldom considered possible rate effects generated by short-term fluctuations in near-shore water temperature.
Here, I suggest that these rate effects may be at least as important to the dynamics of intertidal communities as the impacts of stressful extremes. I develop this idea by reviewing and analyzing field experiments that have quantified rates of predation by the intertidal sea star Pisaster ochraceus in relation to variation in aerial heat stress, wave forces, and water temperature (Sanford, 1999a, 2002b). My results suggest that Pisaster predation in wave-swept habitats along the Oregon coast is regulated not by thermal stress during aerial exposure, but by changes in water temperature on the order of 3°C.
This paper also briefly reviews laboratory studies testing the effect of water temperature on the feeding and growth of Pisaster and a second predator, the low-intertidal whelk Nucella canaliculata. For both species, differences in water temperature of 3°C significantly affected feeding rates, but not growth rates, suggesting that reduced consumption at colder temperatures was balanced by lower metabolic costs. These physiological rate effects are thus conceptually and mechanistically distinct from the influence of environmental stress; declines in water temperature significantly reduce feeding rates (and thus impacts on prey populations), but do not negatively impact the performance and fitness of the consumer. Overall, these results underscore the need for a broader examination of how different components of environmental variation (e.g., thermal extremes, ranges, and means) affect physiological performance and the strength of species interactions in intertidal communities.
Study system
Experimental work on rocky shores suggests that the structure of many intertidal communities is determined by a subset of key species interactions (Paine, 1966, 1969, 1992; Menge, 1976; Power et al., 1996). In particular, classic studies by R.T. Paine on the Washington coast demonstrated the importance of the interaction between the predatory sea star Pisaster ochraceus and the California mussel Mytilus californianus (Paine, 1966, 1969, 1974). In the presence of Pisaster, a diverse assemblage of invertebrate and algal species occupied the low intertidal zone. When sea stars were experimentally removed, mussels moved down the shore, overgrowing all other species on primary rock surfaces. Paine coined the term "keystone species" to describe a single species (like Pisaster) whose impact on community structure is very large, and disproportionately large relative to its abundance (Paine, 1969; Power et al., 1996).
If key species interactions are sensitive to physical factors, they may function as leverage points in natural systems through which small environmental changes can generate large changes at the community level (Sanford, 1999a, 2002a). Some previous work has considered how environmental factors affect the strength of predation by Pisaster. Although not explicitly tested, thermal stress is thought to set the upper vertical foraging limit of Pisaster (Feder, 1956), and thus provides mussels higher on the shore a spatial refuge from sea star predation (Paine, 1974). There is surprisingly little information on Pisaster's tolerance to heat stress. Feder (1956) found that many Pisaster could recover from 25–55 hr of aerial exposure at 
16–24°C, but the effects of aerial exposure on Pisaster predation are unknown. Wave stress is an additional factor that may mediate the strength of intertidal predation (Menge, 1976; Menge and Sutherland, 1987). The intensity of per capita Pisaster predation appears to decline with increasing wave forces (Menge et al., 1996), and observations suggest that Pisaster ceases foraging altogether during storm events (Robles et al., 1995). Finally, preliminary observations on the Oregon coast suggested that the strength of Pisaster predation was reduced during cold-water upwelling events (Sanford, 1999a, b). Wind-driven upwelling events lasting several days to three or more weeks are common on the Oregon coast from May to September and during these events water temperatures typically drop 3–5°C (Menge et al., 1997).
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Field predation rates
I quantified rates of Pisaster predation to test: (1) whether predation was reduced during upwelling events, and (2) whether per capita feeding rates varied with aerial heat stress, waves forces, and/or water temperature. Experiments were conducted at three wave-exposed sites (Strawberry Hill, Pigeon Reef, and Bob Creek Wayside) separated by several hundred meters within Neptune State Park (44°15'N, 124°07'W) on the central Oregon coast. Experiments were replicated at this spatial scale because water temperatures varied little (generally <0.2°C) over these distances, yet the sites were far enough apart that foraging sea stars were unlikely to move among them. At each site, I identified two rocky outcrops or benches (mean area ± SEM = 132.5 ± 49.7 m2) that were in close proximity to one another, yet isolated by surge channels and sand. All sea stars were routinely removed from one bench in each pair and allowed to remain at natural densities on the other.
In April and May 1997, I transplanted 20 clumps of 50 mussels to +0.7 m above Mean Low Low Water (MLLW) on each of these benches. This tidal height corresponded to the vertical height where Pisaster were most abundant at these sites (Sanford, 1999b). Mytilus californianus (shell length, 4.5 to 5.5 cm) were placed in overlapping rows under VexarTM mesh cages that were screwed into the rock. Cages held mussels in place, allowed them to reattach firmly to the rock with byssal threads, and protected them from being eaten by sea stars until cages were removed (Paine, 1976; Menge et al., 1994).
Beginning in mid June, I conducted five consecutive experiments to measure the intensity of sea star predation during periods lasting 14 days each. Starting dates were set a priori as the first day of each spring tide series, so that each experiment consisted of a similar 14-day tidal cycle. At the start of each experiment, I randomly selected four mussel transplants on each bench and removed their cages, thereby exposing these mussels to sources of mortality. I then recorded mussel survivorship in each transplant after 14 days, and local sea star density (defined as the number of sea stars in a 1 m radius around each clump) on 6–8 days during each period.
Per capita predation rates were calculated for each site by subtracting the mortality of mussels after 14 days on benches without Pisaster (i.e., background mortality due to other predators or physical factors) from the mortality of mussels after 14 days on benches with Pisaster, divided by the mean local density of sea stars around that transplant. Thus there were four measures of per capita predation rate (mussels consumed * sea star–1* day–1) for each site x time period combination.
Quantification of environmental conditions
I tested whether variation in predation intensity on transplanted mussels was associated with changes in water temperature, aerial temperatures, and wave forces. A data-logger (Optic StowAwayTM, Onset Computer Corp., Pocasset, MA) was installed in the low intertidal zone (+0.7 m above MLLW) at each site to record water temperature (during high tide) or air temperature (during low tide) every 30 min. Data-loggers were positioned on horizontal surfaces that were exposed to full sunlight during daylight periods of aerial exposure. From these records, I calculated high tide water temperatures at each site, defined as the mean of all readings during a period from two hours before to two hours after each high tide. I also extracted the maximum temperature recorded during each period of aerial exposure, from 90 min before low tide until re-submergence. The time of low and high tides was estimated using NOAA tide charts. In addition to data collected during the predation experiments, temperatures were recorded at these same positions over a longer study period (May 1996–May 1999).
I tested whether temperatures recorded by data-loggers during periods of aerial exposure could be used to predict sea star body temperatures (and thus potential heat stress) during low tide. On 20 dates during these experiments, I laid a 30 m transect parallel to the water (at roughly +0.7 m above MLLW), near the data-logger at Strawberry Hill. I randomly selected 10 sea stars along the transect and used a digital thermometer and hypodermic probe (Thermometer Model HH-21; Probe Model HYP-1, Omega Engineering, Inc, Stamford, CT) to measure their body temperatures 20–30 min before they were re-submerged by the incoming tide. Sea star body temperatures generally peaked just prior to being re-submerged (E. Sanford, unpublished data). I compared these body temperatures to the maximum temperature recorded by the data-logger during that low tide.
Since consumer efficiency may be reduced during periods of increased wave stress (see references in Menge and Olson, 1990), five wave force dynamometers (Bell and Denny, 1994) were deployed in the low zone at each site to record variation in maximum wave forces. Dynamometers were read and reset every 24 hr for the first 5–7 days of each period.
Laboratory predation and growth rates
I also examined the effects of water temperature on the feeding and growth of (1) Pisaster ochraceus, and (2) the whelk Nucella canaliculata under controlled conditions at Hatfield Marine Science Center in Newport, Oregon. In separate experiments, sea stars and whelks were maintained in closed tanks under two treatments: constant 9°C or constant 12°C. These treatments simulated water temperatures that organisms would experience on the Oregon coast during summers with either very intense upwelling or no upwelling, respectively. A third treatment (not discussed here) simulated the fluctuating temperatures characteristic of intermittent upwelling (Sanford, 2002b). Each treatment was replicated with four closed tanks (110-liter capacity), each of which held four sea stars (starting wet weight = 118–138 g) or 8 whelks (starting shell length = 15.0 ± 0.2 mm). Water temperatures were regulated to ±0.1°C using temperature control equipment. Sea stars and whelks were fed mussels ad libitum (Mytilus trossulus, shell length range = 32–42 mm or 25–31 mm, respectively). I recorded the number of mussels consumed in each tank every 14 days. Sea star growth was assessed by weighing individuals at the beginning and end of the 18-wk study (June–October 1996). For whelks, the growing lip of each individual was notched at the beginning of the experiment, and growth was defined as new shell added to the body whorl by the end of the 12-wk experiment (June–August 1997). For a complete description of the experimental design and protocol see Sanford (2002b).
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Temperatures recorded by data-loggers during periods of aerial exposure were a good predictor of sea star body temperature (Fig. 1). The maximum data-logger reading during low tide generally estimated sea star body temperatures to within ± 2–3°C. The temperature sensor of this data-logger model was sealed in air within a dark plastic casing that absorbed solar radiation and therefore did not record air temperature per se. These properties of the data-logger may roughly mimic those of a sea star that has large spaces within each arm and an aboral surface that absorbs solar radiation. However, unmodified data-loggers may not accurately predict the body temperature of all intertidal invertebrates (e.g., mussels; Helmuth and Hofmann, 2001
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Per capita predation rates varied considerably during the five experimental periods (Fig. 2A) and were consistent with the a priori hypothesis that Pisaster feeding rates are reduced during upwelling events (ANOVA, contrast the third period with the other four, F1,53 = 5.91, P = 0.018). Predation rates were lowest during a persistent upwelling event (late July) in which mean water temperatures dropped about 3°C (Fig. 2B). Neither maximum low tide temperatures nor wave forces appeared to be greater during this period of reduced predation (Fig. 2C, D).
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To examine these patterns more quantitatively, I tested for associations between predation rates and each of the environmental parameters using multiple linear regression (MLR). The dependent variable was per capita predation rate (n = 3 sites x 5 time periods = 15 measurements), and the independent variables were: (1) water temperature (mean during 28 high tides per period), (2) potential heat stress (defined as the mean of the maximum data-logger temperature from the 5 warmest low tides per period), and (3) wave forces (mean of dynamometer reading on 5–7 days per period). For illustration, simple linear regressions are presented in Figure 3. In the MLR model, predation rate was significantly associated with water temperature (P = 0.006), but not potential heat stress (P = 0.92). After adjusting for variation associated with water temperature, there was suggestive but inconclusive evidence that predation was related to wave forces (P = 0.090). If a data point identified as an outlier was removed from analysis, there was a statistically significant negative relationship between wave forces and predation (P = 0.010). Together, water temperature and wave forces explained 55.5% of the variation in per capita predation rates.
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The association between predation and wave forces appeared to be a spatial pattern rather than a temporal pattern; the site with consistently greater wave forces (Bob Creek) tended to have lower per capita predation rates throughout the study. As a result, if "site" was included as a factor in the MLR model, wave force was no longer significant (P = 0.86). Therefore, these results cannot distinguish the potential effect of wave force on predation from that of some other factor that was also consistently different at Bob Creek.
Total predation decreased sharply during upwelling as a result of declines in per capita effects, coupled with declines in the density of foraging sea stars. Per capita predation rates were roughly halved by a decline in water temperature of 4°C (Fig. 3A; Q10 = 4.8 between 9.5°C and 13.5°C). The local density of sea stars (number*m–2) around the mussel transplants also declined significantly with decreasing temperature (P = 0.012, y = 1.8x–9.0). This was apparently the result of more sea stars remaining temporarily inactive in low zone channels or shallow subtidal waters during cold-water upwelling events, rather than sea star mortality or dislodgment by waves (Sanford, 1999b). This combination of physiological and behavioral effects suggests that changes in water temperature may generate non-linear changes in total predation (Sanford, 1999a, 2002a); with a decline of 4°C, there were about half as many foraging sea stars, each eating about half as much, leading to an exponential decline in predation intensity.
Inspection of data-logger records from 1996–1998 revealed that Pisaster body temperatures, as reflected by maximum data-logger temperatures (see Fig. 1), seldom reached warm levels in these wave-exposed habitats (Fig. 4). During this three-year study interval, peak sea star body temperatures likely reached or exceeded 24°C on only 9 dates. During 1996–1998, the average of peak sea star body temperatures during May–August low tides was about 14°C. Thus on most days, low tide emersion caused only a minor, temporary warming of Pisaster body temperatures in this habitat.
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Periodic declines in water temperature of 3 to 5°C were a common feature at these sites during the upwelling season (Fig. 5). In addition, there was considerable inter-annual variation in the frequency and intensity of upwelling, as indicated by the percent of high tides during May through August in which water temperatures were <10°C. Only 13.8% of high tides fell below this temperature in 1997 (an El Niño year), compared to 48.5% and 29.6% in 1996 and 1998, respectively.
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In the laboratory, water temperature had a significant effect on feeding rates of both Pisaster and the whelk Nucella canaliculata over the course of 18-wk and 12-wk experiments, respectively (Fig. 6). The effect was most pronounced during the first six weeks of the experiment when sea stars in constant 12°C tanks consumed
40% more mussels than those in 9°C tanks (Sanford, 2002a). By the end of the experiment, this difference was reduced, apparently because warmer sea stars became satiated earlier on the ad libitum diet (see Sanford, 2002b for a complete discussion of these experiments). For both sea stars and whelks, individuals in the colder tanks did not grow at slower rates despite consuming fewer mussels (Fig. 6). This suggests that metabolic costs were lower at colder temperatures, such that reduced consumption did not lead to reduced growth. Data presented elsewhere (Sanford, 2002b) suggest that fluctuating water temperatures may increase growth rates, presumably because consumers feed intensely during warmer periods, but enjoy reduced energetic costs during intermittent periods of cold water (McLaren, 1963; Brett, 1971).
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DISCUSSION |
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Thermal stress often plays an important role in defining the spatial and temporal niche in which intertidal consumers can forage. There are numerous examples of environmental stress restricting specific mobile consumers to certain zones or microhabitats within the intertidal zone (Orton, 1929a
, b; Feder, 1956; Landenberger, 1969; Paine, 1974; Menge, 1976, 1978a, b; Garrity and Levings, 1981; Levings and Garrity, 1983; Fairweather, 1988; Leonard et al., 1998; Stillman and Somero, 1996; Burnaford, 2001). These studies help explain why a particular consumer is not found in all habitats, but tell us less about how environmental variation affects that consumer in its normal habitat. In particular, in areas where consumers are active and abundant, are rates of predation and herbivory regulated by environmental factors?
Environmental stress models predict that sub-lethal stresses may often reduce rates of consumption (Menge and Sutherland, 1987; Menge and Olson, 1990). Chronic exposure to extreme periods of heat and desiccation may produce cellular damage that reduces feeding, and ultimately reduces growth and fitness. In contrast, the results of this study suggest that predation by the sea star Pisaster ochraceus is regulated primarily by physiological rate effects, generated by relatively small changes in water temperature in the central portion of Pisaster's thermal range. These Q10 effects are distinct from environmental stress, and may have little or no fitness consequences for Pisaster (but see Sanford, 2002b for a discussion of the effects of fluctuating temperatures).
These ideas are illustrated in a conceptual model showing the hypothesized relationships of temperature vs. feeding, metabolism, and growth (Fig. 7). At some high and low critical temperatures, feeding rates drop off sharply to zero. Across the normal range of water temperatures, feeding rates increase linearly with temperature until functional constraints cause them to plateau at some maximal rate. Metabolic rate is roughly an exponential function of temperature, until it drops off at some critical upper temperature (Cossins and Bowler, 1987). In this simple model, growth is the difference between these two functions for food intake and metabolic cost.
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Similar graphical models for net energy gain in ectotherms have been presented previously (Huey, 1982
; Levinton, 1983; see also Sanford, 2002b). In these models, ingestion rate and metabolic rate are drawn as smooth curves, resulting in a single optimal temperature for growth. In contrast, in this model I note that invertebrate feeding and metabolic rates often show a linear increase with temperature, within a species' normal thermal range (e.g., Largen, 1967; Mackenzie, 1969; Ulbricht, 1973; Newell and Branch, 1980). If the linear segments of these functions have similar slopes, growth will remain consistent across the range of normal water temperatures, rather than there being a single optimal temperature. This occurs because the reduction in energetic intake with decreasing temperature is balanced by a reduction in metabolic costs, as suggested by my laboratory results (Fig. 6). If environmental stress is defined as conditions having a negative impact on growth, then stress is absent in the center of this temperature range, although feeding rates drop sharply with temperature (Fig. 7).
Based on this model, characterizing the environmental conditions that consumers experience is clearly important. In particular, how often do thermally stressful conditions occur in wave-exposed habitats, relative to less extreme, rate-altering fluctuations in water temperature? In this study there was no association between variation in potential heat stress and Pisaster predation rates, and sea star temperatures appeared to reach relatively warm levels (>24°C) on only about 9 dates during a three-year period. The majority of low tide exposures appeared to elevate body temperatures only a few degrees above ambient sea temperature. Moreover, in these wave-exposed, low-intertidal habitats (where Pisaster are most abundant), organisms spend >80% of their lives submerged. Most intertidal consumers show little or no movement during aerial exposure (e.g., Newell et al., 1971; Garrity and Levings, 1981), and may cease feeding at low tide even when prey are held in their grasp. Exposure to mild air temperatures may thus merely elevate body temperatures temporarily, whereas changes in water temperature will directly affect foraging activity, and set the thermal conditions under which most cellular and physiological processes occur. Along the coasts of Oregon and California, wind-driven upwelling regularly generates short-term fluctuations in water temperature of 3–5°C, and my field and laboratory results indicate that these changes significantly alter feeding rates. Moreover, inter-annual variation in upwelling patterns (Fig. 5), may generate among-year variation in the strength of impacts on prey populations (Sanford, 1999a).
In addition to this experimental work, other considerations suggest that thermal stress may not be a significant concern for Pisaster, at least in some wave-exposed habitats. Although foraging Pisaster sometimes migrate vertically with the rising and falling tide (Mauzey, 1967; Robles et al., 1995), more commonly sea stars in Oregon suspend vertical migrations and remain hunched over patches of prey for days at a time (Menge et al., 2002b). Because tides along the Pacific coast of North America are mixed semidiurnal tides, total emersion time of intertidal organisms does not increase linearly with vertical position on the shore (Doty, 1946). For example, Pisaster living in the low intertidal zone are generally emersed only once per day, whereas mussels in the mid-intertidal zone are frequently exposed to aerial conditions twice per day. In fact, this non-linear gradient in emersion time is thought to set the vertical foraging limit of Pisaster (Feder, 1956). In regions with true semidiurnal tides, the low-intertidal zone is often exposed to aerial conditions twice per day. Interestingly, in New Zealand (where semidiurnal tides exist), the sea star Stichaster australis generally migrates upshore with the incoming tide, removes prey, and then retreats with the prey to the low zone prior to each low tide (Menge et al., 2002b). Presumably this "drive-thru" foraging strategy minimizes exposure to thermal stress, and the infrequency of this behavior in Oregon may suggest that Pisaster seldom experience thermally stressful conditions in wave-exposed, intertidal habitats.
Although thermal stress does not appear to regulate Pisaster feeding rates, tolerance of aerial temperatures may have played an important evolutionary role in shaping Pisaster's physiology. Clearly if temperatures greater than 24°C were lethal to some Pisaster, then even a single hot day would be a very strong selective force. In addition, environmental stress may have a large impact on community structure by determining where and when Pisaster can actively forage. In the Pacific Northwest, the effects of Pisaster in the intertidal zone are sharply reduced during winter months, when many individuals move into shallow subtidal waters, perhaps due to increased wave stress and/or the threat of freezing air temperatures (Mauzey, 1966; Paine, 1974; Sanford, 1999b). In addition, heat and desiccation stress may set the vertical limit of Pisaster's foraging range (Feder, 1956), and if this limit were to change, it would have profound effects on community structure (Paine, 1974). Thus, environmental stress may determine the temporal and spatial distribution of Pisaster's effects, whereas changes in water temperature appear to play a significant role in determining the strength of those effects.
In summary, environmental variation is assumed to influence the physiological performance of intertidal organisms, which in turn may alter the strength of species interactions, with effects at the community level (Menge and Sutherland, 1987). Although logical, ecologists and physiologists have only recently begun to rigorously test this chain of effects. By linking water temperature and the strength of keystone predation, the experiments reviewed here suggest a pathway through which variation in the frequency and intensity of upwelling may be linked to changes at the community-level (Sanford, 1999a, 2002a). More broadly, this paper demonstrates the importance of: (1) accurately characterizing the environmental variation that key interactors experience, and (2) understanding how components of this variation (e.g., thermal extremes, means, and ranges) impact these organisms' physiology and feeding. The analysis presented here suggests that physiological rate effects, occurring near the middle of consumers' thermal ranges, may make an important and overlooked contribution to the dynamics of rocky intertidal communities.
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ACKNOWLEDGMENTS |
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I thank B. Helmuth and L. Tomanek for inviting me to participate in this productive and stimulating symposium. For their many contributions to this research, I am grateful to my graduate advisors, B. A. Menge and J. Lubchenco, and members of the Lubchenco-Menge and Somero Labs. This paper was significantly improved by constructive comments from B. A. Menge, G. N. Somero, J. H. Stillman, and R. B. Huey. Financial support was provided by a National Science Foundation Predoctoral Fellowship, and the David and Lucile Packard Foundation. This is contribution number 66 of the Partnership for Interdisciplinary Studies of Coastal Oceans (PISCO): A Long-Term Ecological Consortium funded by the David and Lucile Packard Foundation.
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FOOTNOTES |
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1 From the Symposium Physiological Ecology of Rocky Intertidal Organisms: From Molecules to Ecosystems presented at the Annual Meeting of the Society for Comparative and Integrative Biology, 2–7 January 2002, at Anaheim, California.
2 E-mail: Eric_Sanford{at}brown.edu
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References |
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Bell, E. C., and M. W. Denny. 1994. Quantifying "wave exposure": A simple device for recording maximum velocity and results of its use at several field sites. J. Exp. Mar. Biol. Ecol, 181:19-29.
Benson, K. R. 2002. The study of vertical zonation on rocky intertidal shores—a historical perspective. Integ. and Comp. Biol, 42:776-779.
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