Brian Helmuth

Microhabitats, Thermal Heterogeneity, and Patterns of Physiological Stress in the Rocky Intertidal Zone

Thermal stress has been considered to be among the most important determinants of organismal distribution in the rocky intertidal zone. Yet our understanding of how body temperatures experienced under field conditions vary in space and time, and of how these temperatures translate into physiological performance, is still rudimentary. We continuously monitored temperatures at a site in central California for a period of two years, using loggers designed to mimic the thermal characteristics of mussels, Mytilus californianus. Model mussel temperatures were recorded on both a horizontal and a vertical, north-facing microsite, and in an adjacent tidepool. We periodically measured levels of heat shock proteins (Hsp70), a measure of thermal stress, from mussels at each microsite. Mussel temperatures were consistently higher on the horizontal surface than on the vertical surface, and differences in body temperature between these sites were reflected in the amount of Hsp70. Seasonal peaks in extreme high temperatures (“acute” high temperatures) did not always coincide with peaks in average daily maxima (“chronic” high temperatures), suggesting that the time history of body temperature may be an important factor in determining levels of thermal stress. Temporal patterns in body temperature during low tide were decoupled from patterns in water temperature, suggesting that water temperature is an ineffective metric of thermal stress for intertidal organisms. This study demonstrates that spatial and temporal variability in thermal stress can be highly complex, and “snapshot” sampling of temperature and biochemical indices may not always be a reliable method for defining thermal stress at a site.

INTERTIDAL MUSSEL MICROCLIMATES: PREDICTING THE BODY TEMPERATURE OF A SESSILE INVERTEBRATE

To elucidate the determinants of intertidal invertebrate body temperatures during aerial exposure, I developed deterministic models using the environmental inputs of solar radiation, air temperature, ground temperature, and wind speed to predict the body temperatures of intertidal mussels (Mytilus spp.). Combined with field studies, these models were used to determine the effects of body size on body temperature, and to compare the heat budgets of mussels living as solitary individuals vs. those living in aggregations (beds). On average, the model accurately predicted the body temperatures of solitary mussels in the field to within ∼1°C. Steady-state simulations (using constant environmental conditions) predicted that, under conditions where evaporative water loss is limited, smaller (5 cm) mussels experience lower body temperatures than larger (10 cm) mussels exposed to identical environmental parameters. When evaporative cooling is limited only by intolerance to desiccation, the trend in body size rever...

Modelling the ecological niche from functional traits

The niche concept is central to ecology but is often depicted descriptively through observing associations between organisms and habitats. Here, we argue for the importance of mechanistically modelling niches based on functional traits of organisms and explore the possibilities for achieving this through the integration of three theoretical frameworks: biophysical ecology (BE), the geometric framework for nutrition (GF) and dynamic energy budget (DEB) models. These three frameworks are fundamentally based on the conservation laws of thermodynamics, describing energy and mass balance at the level of the individual and capturing the prodigious predictive power of the concepts of ‘homeostasis’ and ‘evolutionary fitness’. BE and the GF provide mechanistic multi-dimensional depictions of climatic and nutritional niches, respectively, providing a foundation for linking organismal traits (morphology, physiology, behaviour) with habitat characteristics. In turn, they provide driving inputs and cost functions for mass/energy allocation within the individual as determined by DEB models. We show how integration of the three frameworks permits calculation of activity constraints, vital rates (survival, development, growth, reproduction) and ultimately population growth rates and species distributions. When integrated with contemporary niche theory, functional trait niche models hold great promise for tackling major questions in ecology and evolutionary biology.

Long-distance dispersal of a subantarctic brooding bivalve (Gaimardia trapesina) by kelp-rafting

The probability of successful dispersal by sessile benthic invertebrates is thought to strongly influence their geographic distribution and population genetics. Generally, species with long-lived planktonic larvae are expected to exhibit wider distribution patterns than those species which brood their young, due to their presumably greater potential for dispersal. In some cases, however, brooding species exhibit broad distributions and show evidence of genetic exchange with geographically distant populations. One potential factor that has been invoked as an expianation is dispersal by floating and rafting of adults and egg masses. Several studies have shown that it is possible for sessile adults to disperse on the order of several to many thousand kilometers by rafting on debris in ocean currents. With very few exceptions, however, direct evidence of rafting in the open ocean has been lacking. We present evidence of long-distance (1300 to 2000 km) dispersal of a brooding pelecypod,Gaimardia trapesina (Lamarck, 1819), in the Southern Ocean in the vicinity of Cape Horn, the Falkland Islands, and the antarctic island South Georgia (54°S; 37°W). Data on survival and fecundity rates ofG. trapesina and the prevalence of kelp rafts collected during the austral winter of 1993 indicate that dispersal by rafting can occur over ecologically relevant time scales and could potentially serve as a significant means of genetic exchange between populations.

How do we Measure the Environment? Linking Intertidal Thermal Physiology and Ecology Through Biophysics

Abstract Recent advances in quantifying biochemical and cellular-level responses to thermal stress have facilitated a new exploration of the role of climate and climate change in driving intertidal community and population ecology. To fruitfully connect these disciplines, we first need to understand what the body temperatures of intertidal organisms are under field conditions, and how they change in space and time. Newly available data logger technology makes such an exploration possible, but several potential pitfalls must be avoided. Body temperature during aerial exposure is driven by multiple, interacting climatic factors, and extremes during low tide far exceed those during submersion. Moreover, because of effects of body size and morphology, two organisms exposed to identical climatic conditions can display very different body temperatures, which can also be substantially different from the temperature of the surrounding air. These same factors drive the temperature recorded by data loggers, and one logger type is unlikely to serve as an effective proxy for all organisms at a site. Here I describe the difficulties involved in quantifying patterns of body temperature in intertidal organisms, and explore the implications of this complexity for intertidal physiological ecology. I do so using data from temperature loggers designed to mimic the thermal characteristics of the mussel Mytilus californianus, and deployed at multiple sites along the West Coast of the United States. Results indicate a highly intricate pattern of thermal stress, where the interaction of climate with the dynamics of the tidal cycle determines the timing and magnitude of temperature extremes, creating a unique “thermal signal” at each site.

Physiological Ecology of Rocky Intertidal Organisms: A Synergy of Concepts

Abstract The rocky intertidal zone is among the most physically harsh environments on earth. Marine invertebrates and algae living in this habitat are alternatively pounded by waves and exposed to thermal extremes during low tide periods (Denny and Wethey, 2001). Additionally, they must deal with strong selective pressures related to predation and competition for space (Connell, 1961). As a result, the steep physical gradient and spatially condensed community has made the rocky intertidal zone an ideal “natural laboratory” to study the coupled role of physical and biological factors in determining the abundance and distribution of organisms in nature (Connell, 1961; Paine, 1966, 1994).

Effects of water flow and branch spacing on particle capture by the reef coral Madracis mirabilis (Duchassaing and Michelotti)

Abstract The scleractinian coral Madracis mirabilis forms colonies composed of many narrow branches whose spacing varies across habitats; this is especially evident along a depth gradient. Environmental factors such as irradiance and water movement co-vary along this gradient and both factors could have effects on branch spacing. We examined the effects of water flow on particle capture by Madracis mirabilis in a laboratory flume at Discovery Bay, Jamaica, using hydrated Artemia cysts as experimental particles. Isolated branches of Madracis showed highest particle capture rates in the 10–15 cm s −1 range of flow speeds, although capture was still occurring at about one fourth the maximum rate even at 40–50 cm s −1 . The ability to capture particles at these higher flow speeds results from polyps on downstream sides of branches capturing particles from turbulent eddies in the wake of the branch. At high flows, these polyps are not deformed (flattened) as are the upstream polyps. Two aggregation densities were tested at three flow speeds and both flow and particle capture were measured at each branch. Low density aggregations, comparable to those in low flow and deep reef habitats, captured particles best at the lowest flow speeds tested and capture was relatively uniform through the aggregation. High density aggregations captured particles best at high flow speeds, especially near the downstream end of the aggregation. At low flow speeds, the highest capture rates occurred at the upstream end of the aggregation. Flow speed decreased downstream within aggregations at both low and high densities, especially at higher flow speeds. Turbulence intensity also changed within aggregations, increasing behind the first row of branches at all flow speeds and in both aggregation densities. Total capture rate per polyp was highest at intermediate flow speeds (10–15 cm s −1 ) for single branches and for aggregations due to high encounter rates, while capture efficiency (flux adjusted capture rate) was greatest at low flow speeds. Patterns of flow and particle capture within aggregations suggest that high density aggregations function better in high flow environments. Low density aggregations were able to capture only one fourth as many particles as high density aggregations at the higher speeds used in these experiments. Conversely, high density aggregations captured only about half as many particles at the low flow speed, compared to low density aggregations. Factors other than flow, especially light interception, are likely to affect branch spacing as well. Shallow reef habitats, with high irradiance and high flow conditions, may thus favor tight branch spacing as a response to both environmental variables.

Thermal biology of rocky intertidal mussels : Quantifying body temperatures using climatological data

Despite numerous studies demonstrating the importance of body temperature to the fitness of intertidal invertebrates, surprisingly little is known of what these temperatures are under normal field conditions. Using environmental data collected at semi-exposed rocky intertidal beaches in the northeastern Pacific, I compared predictions of the body temperatures of mussels (Mytilus californianus) based on small-scale (microclimate-level) environmental data averaged over a range of time scales (5 minutes to 1 hour) to those generated using continuous measurements. The error in predicting maximum and mean body temperatures introduced through the use of hourly environmental averages was generally less than 1°–2°C. I then predicted body temperatures of mussels during aerial exposure using historical, hourly weather data from federal meteorological databases. I used environmental data collected over a 30-yr (1961–1990) period on the Olympic Peninsula of Washington State to estimate the body temperatures of mussel aggregations at two tidal heights under conditions of aerial exposure during a “typical” climatological year. Estimated body temperatures commonly fluctuated by 20°C or more during a period of ≤12 h and did not correlate well with air temperatures. The data indicated that mussels were, on average, hotter at this site during spring (April–June) than in summer (July–September) and colder in autumn (October–December) than in winter (January–March), primarily due to the effect of tidal cycles in determining exposure time. Results of simulations where the effects of climate and tidal cycle were decoupled suggested that the timing of aerial exposure, which can vary consistently over relatively small spatial scales (<100 km), can be more important than seasonal (spring vs. summer) differences in climatic conditions in determining body temperatures. Because of the interactive effects of climate and tidal cycle on body temperatures, populations of mussels in this region living at the same tidal height but separated by only tens of kilometers are predicted to experience very different thermal regimes. As a result, the intertidal environment represents a unique habitat for investigating the thermal biology of invertebrates over a range of spatial and temporal scales.

The influence of colony morphology and orientation to flow on particle capture by the scleractinian coral Agaricia agaricites (Linnaeus)

The scleractinian coral Agaricia agaricites (Linnaeus) is a common component of reef systems throughout the Caribbean. The morphology of A. agaricites is extremely variable, including flat unifacial plates, upright bifacial plates, and encrusting forms. Transects conducted on the fore reef of Discovery Bay, Jamaica, indicated that the morphology of colonies growing on horizontal substrata was strongly related to depth. Colonies in shallower water (7–12 m) tended to encrust or form unifacial plates, while deeper colonies (20 m) were primarily upright and bifacial. Furthermore, 90% of all bifacial colonies were oriented directly perpendicular to (feeding surface facing) the dominant direction of flow. Bifacial colonies also tended to have larger corallites, and possessed ridges which angled upward away from the substratum. Measurements of flow conducted at this site indicated that ambient flow speeds generally decrease with increasing depth. A series of feeding trials was conducted in a laboratory flume over a range of flow speeds characteristic of those found on the reef (3–50 cm · s−1) to address the hypothesis that variations in colony morphology and orientation to flow represent mechanisms for maximizing particle capture. Upright bifacial colonies oriented perpendicular to flow fed at significantly higher rates than bifacial colonies oriented parallel to flow. Bifacial colonies were never, however, able to capture more particles per unit surface area than were unifacial plates, at any flow speed. In all colony morphologies tested, capture shifted from upstream to downstream areas with increasing flow speed, suggesting that feeding did not involve the inertial impaction of particles. Particle capture was highest at intermediate flow speeds, although horizontal-plating colonies were able to feed well over the entire range of flow speeds tested. Behavioral observations suggest that particle capture was aided by currents originating within the polyps, and apparently did not involve mucus entrapment, as previously suggested. Measurements of flow at points near the surface of colonies in the field indicated that flow conditions at 20 m roughly match flow conditions in the experimental flume, suggesting that the results of the feeding trials may be extrapolated to feeding in situ. The results thus suggest that colony morphology does not represent a mechanism for maximizing particle capture per unit tissue, but instead may have evolved as the result of other selective pressures such as spatial competition or gas exchange. Thus, by growing away from the substratum, colonies could potentially increase particle capture, and colony biomass, per unit of available substrate. The orientation of colonies into flow, however, does increase food capture, and may have arisen secondarily as a compromise between selective pressures.

Biomechanics meets the ecological niche: the importance of temporal data resolution

SUMMARY The emerging field of mechanistic niche modelling aims to link the functional traits of organisms to their environments to predict survival, reproduction, distribution and abundance. This approach has great potential to increase our understanding of the impacts of environmental change on individuals, populations and communities by providing functional connections between physiological and ecological response to increasingly available spatial environmental data. By their nature, such mechanistic models are more data intensive in comparison with the more widely applied correlative approaches but can potentially provide more spatially and temporally explicit predictions, which are often needed by decision makers. A poorly explored issue in this context is the appropriate level of temporal resolution of input data required for these models, and specifically the error in predictions that can be incurred through the use of temporally averaged data. Here, we review how biomechanical principles from heat-transfer and metabolic theory are currently being used as foundations for mechanistic niche models and consider the consequences of different temporal resolutions of environmental data for modelling the niche of a behaviourally thermoregulating terrestrial lizard. We show that fine-scale temporal resolution (daily) data can be crucial for unbiased inference of climatic impacts on survival, growth and reproduction. This is especially so for species with little capacity for behavioural buffering, because of behavioural or habitat constraints, and for detecting temporal trends. However, coarser-resolution data (long-term monthly averages) can be appropriate for mechanistic studies of climatic constraints on distribution and abundance limits in thermoregulating species at broad spatial scales.