Predicting Indirect Effects of Predator-Prey Interactions.

SYNOPSIS: Predicting the effects of climate change on species and communities remains a pre-eminent challenge for biologists. Critical among this is understanding the indirect effects of climate change, which arise when the direct, physiological effects of climate on one species change the outcome of its interaction with a second species, altering the success of the second species. A diverse array of approaches to predicting indirect effects exists from mechanistic models, which attempt to build-up from physiological changes to ecological consequences, to ecological models that focus solely on the ecological scale. Here I review studies of the indirect effects of temperature on two predator-prey systems in rocky intertidal habitats. Laboratory and field studies have shown that temperature can indirectly affect interactions through both physiological and behavioral changes in predator and prey, but no model yet captures the full range of these effects. The three main categories of changes are metabolic rate effects, stress effects, and behavioral avoidance. Mechanistic models best capture the first two of these three dynamics, while ecological models have focused mainly on the last two. The challenge remains to correctly identify a species' vulnerability to climate change, which differs from its physiological sensitivity. The best approach may be to use detailed physiological-scale studies of indirect effect in a few systems to ground truth simpler models that can be applied more broadly. Model development and testing is also hampered by the small number of field studies of indirect effects in natural systems, particularly studies that examine natural temporal or spatial variation in climate.

Long-term, high frequency in situ measurements of intertidal mussel bed temperatures using biomimetic sensors.

At a proximal level, the physiological impacts of global climate change on ectothermic organisms are manifest as changes in body temperatures. Especially for plants and animals exposed to direct solar radiation, body temperatures can be substantially different from air temperatures. We deployed biomimetic sensors that approximate the thermal characteristics of intertidal mussels at 71 sites worldwide, from 1998-present. Loggers recorded temperatures at 10-30 min intervals nearly continuously at multiple intertidal elevations. Comparisons against direct measurements of mussel tissue temperature indicated errors of ~2.0-2.5 °C, during daily fluctuations that often exceeded 15°-20 °C. Geographic patterns in thermal stress based on biomimetic logger measurements were generally far more complex than anticipated based only on 'habitat-level' measurements of air or sea surface temperature. This unique data set provides an opportunity to link physiological measurements with spatially- and temporally-explicit field observations of body temperature.

Do species' traits predict recent shifts at expanding range edges?

Although some organisms have moved to higher elevations and latitudes in response to recent climate change, there is little consensus regarding the capacity of different species to track rapid climate change via range shifts. Understanding species' abilities to shift ranges has important implications for assessing extinction risk and predicting future community structure. At an expanding front, colonization rates are determined jointly by rates of reproduction and dispersal. In addition, establishment of viable populations requires that individuals find suitable resources in novel habitats. Thus, species with greater dispersal ability, reproductive rate and ecological generalization should be more likely to expand into new regions under climate change. Here, we assess current evidence for the relationship between leading-edge range shifts and species' traits. We found expected relationships for several datasets, including diet breadth in North American Passeriformes and egg-laying habitat in British Odonata. However, models generally had low explanatory power. Thus, even statistically and biologically meaningful relationships are unlikely to be of predictive utility for conservation and management. Trait-based range shift forecasts face several challenges, including quantifying relevant natural history variation across large numbers of species and coupling these data with extrinsic factors such as habitat fragmentation and availability.

Heating up relations between cold fish: competition modifies responses to climate change.

Most predictions about species responses to climate change ignore species interactions. Helland and colleagues (2011) test whether this assumption is valid by evaluating whether ice cover affects competition between brown trout [Salmo trutta (L.)] and Arctic charr [Salvelinus alpines (L.)]. They show that increasing ice cover correlates with lower trout biomass when Arctic charr co-occur, but not in charr's absence. In experiments, charr grew better in the cold, dark environments that typify ice-covered lakes. Decreasing ice cover with warmer winters could mean more trout and fewer charr. More generally, their results provide an excellent example, suggesting that species interactions can strongly modify responses to climate change.

A framework for community interactions under climate change.

Predicting the impacts of climate change on species is one of the biggest challenges that ecologists face. Predictions routinely focus on the direct effects of climate change on individual species, yet interactions between species can strongly influence how climate change affects organisms at every scale by altering their individual fitness, geographic ranges and the structure and dynamics of their community. Failure to incorporate these interactions limits the ability to predict responses of species to climate change. We propose a framework based on ideas from global-change biology, community ecology, and invasion biology that uses community modules to assess how species interactions shape responses to climate change.

Organismal climatology: analyzing environmental variability at scales relevant to physiological stress.

Predicting when, where and with what magnitude climate change is likely to affect the fitness, abundance and distribution of organisms and the functioning of ecosystems has emerged as a high priority for scientists and resource managers. However, even in cases where we have detailed knowledge of current species' range boundaries, we often do not understand what, if any, aspects of weather and climate act to set these limits. This shortcoming significantly curtails our capacity to predict potential future range shifts in response to climate change, especially since the factors that set range boundaries under those novel conditions may be different from those that set limits today. We quantitatively examine a nine-year time series of temperature records relevant to the body temperatures of intertidal mussels as measured using biomimetic sensors. Specifically, we explore how a 'climatology' of body temperatures, as opposed to long-term records of habitat-level parameters such as air and water temperatures, can be used to extrapolate meaningful spatial and temporal patterns of physiological stress. Using different metrics that correspond to various aspects of physiological stress (seasonal means, cumulative temperature and the return time of extremes) we show that these potential environmental stressors do not always occur in synchrony with one another. Our analysis also shows that patterns of animal temperature are not well correlated with simple, commonly used metrics such as air temperature. Detailed physiological studies can provide guidance to predicting the effects of global climate change on natural ecosystems but only if we concomitantly record, archive and model environmental signals at appropriate scales.

Variation in the sensitivity of organismal body temperature to climate change over local and geographic scales.

Global climate change is expected to have broad ecological consequences for species and communities. Attempts to forecast these consequences usually assume that changes in air or water temperature will translate into equivalent changes in a species' organismal body temperature. This simple change is unlikely because an organism's body temperature is determined by a complex series of interactions between the organism and its environment. Using a biophysical model, validated with 5 years of field observations, we examined the relationship between environmental temperature change and body temperature of the intertidal mussel Mytilus californianus over 1,600 km of its geographic distribution. We found that at all locations examined simulated changes in air or water temperature always produced less than equivalent changes in the daily maximum mussel body temperature. Moreover, the magnitude of body temperature change was highly variable, both within and among locations. A simulated 1 degrees C increase in air or water temperature raised the maximum monthly average of daily body temperature maxima by 0.07-0.92 degrees C, depending on the geographic location, vertical position, and temperature variable. We combined these sensitivities with predicted climate change for 2100 and calculated increases in monthly average maximum body temperature of 0.97-4.12 degrees C, depending on location and climate change scenario. Thus geographic variation in body temperature sensitivity can modulate species' experiences of climate change and must be considered when predicting the biological consequences of climate change.

Life at the edge: an experimental study of a poleward range boundary.

Experimental studies of biogeographic processes are important, but rarely attempted because of the logistical challenges of research at large spatial scales. I used a series of large-scale transplant experiments to investigate the mechanisms controlling species abundance near a poleward range boundary. The intertidal limpet Collisella scabra experiences a 100-fold decline in abundance over the northernmost 300 km of its range. Temperature and food supply both strongly influenced individual survival, growth, and maturation. Regression analysis also revealed significant interactions among these conditions: the effect of one could not be predicted without knowing the level of the other. But these relationships could not explain geographic abundance patterns. Instead, individual limpets were highly successful at sites with relatively low abundance. These results suggest that, even though temperature is important to the success of individual C. scabra populations, the primary effect of warming temperatures under climate change may not be a shift in geographic distribution.