Ecologists have long called for using individual ecologies to understand population dynamics (Schoener 1986; Kingsolver 1989; Koehl 1989; Lawton 1991). Linking individual ecologies to population dynamics requires addressing three primary questions (sensu Kingsolver 1989): (i) how do the organismal phenotypes interact with environmental conditions to determine the physiological experience of organisms? (ii) how do these physiological experiences constrain individual ecologies including behaviour and rates of energy use and acquisition? and (iii) how do these behavioural and energetic implications determine population dynamics? The Metabolic Theory of Ecology (hereafter MTE, Brown et al. 2004) has renewed interest within the last decade in using energetics to scale across levels of ecological organization. The MTE defines metabolism to encompass the acquisition and processing of energy from the environment and the allocation of this energy to survival, growth and reproduction (Brown et al. 2004). Studies of clinal variation have reveal biogeographical and evolutionary consequences of individual energetics (Angilletta, Sears & Steury 2004; Karl & Fischer 2008; Ellers & Driessen 2011).
We illustrate this integration from individual energetics to abundance and distribution using a case study: grasshopper communities along a 2000 m elevation gradient near Boulder, CO. The grasshopper communities were initially surveyed by Gordon Alexander between the 1930s and the 1960s. Recent resurveys have found that the extent and even direction of phenological shifts in response to recent climate change have varied between species and along the gradient (Nufio et al. 2010). Why have some populations and species exhibited more pronounced responses to recent climate change than others? Can contrasting metabolic constraints resulting from phenotypic differences account for differential responses to recent climate change between species and along the gradient?
Idiosyncratic responses, particularly species shifting their distributions to different extents and in different directions, have frequently been observed in response to past climate change across a variety of taxa (Williams & Jackson 2007). Yet, we are largely unable to account for or accurately predict these individualistic responses. Efforts to use species traits to predict responses to recent climate change generally predict only a small, but significant, amount of variation (Buckley & Kingsolver 2013). One potential explanation is that the interaction between a species' phenotype and environmental conditions has distinct energetic and demographic implications. Here, we investigate this explanation by documenting clinal variation in grasshopper traits and climates and exploring the ecological implications of this variation. By combining data on phenotypic clines with weather and climate data along an elevation gradient, we develop biophysical and energetic models to explore population and species differences in body temperature, activity and energy balance. We also review approaches for characterizing organism–environment interactions and their impacts on individual ecologies (challenges 1 and 2 introduced above) and illustrate these approaches with our grasshopper case study. We conclude by discussing techniques for translating this information into population dynamics (challenge 3).
Clinal Variation and Its Energetic Implications
Studying phenotypic variation across elevation and other environmental gradients can identify traits that may determine energetics and fitness in a given environment (Chown, Gaston & Robinson 2004; Helmuth, Kingsolver & Carrington 2005; Gaston et al. 2009; Kingsolver 2009). Clinal variation linked to thermal environments has been widely observed across taxa (Angilletta, Niewiarowski & Navas 2002; Blanckenhorn & Demont 2004; Gotthard 2004). Significant clinal variation along elevation gradients has been particularly well documented for insects. Gradients in colour influence solar absorbance and body temperatures and thermal tolerances tend to match environmental temperatures. A well-documented form of insect clinal variation is the temperature-size rule, wherein cold temperatures delay development and result in larger body sizes (Whitman 2008). High-elevation insects typically respond to the reduced and variable temperatures and short growing seasons by reducing the number of developmental stages, generations or developmental thresholds (Hodkinson 2005).
Phenotypic traits including size and shape, coloration, behavioural posture and microhabitat selection determine how environmental conditions translate into body temperatures. Environmental factors such as radiation intensities and wind speeds influence body temperatures in addition to air and surface temperatures. Biophysical models enable the integration of environmental conditions and species traits to predict body temperatures. Biophysical models are heat budgets that balance energy input from solar radiation against the sum of thermal radiation, convection and conduction (Porter & Gates 1969; Gates 1980; Campbell & Norman 2000). The translation between environmental and body temperatures is complicated by behavioural thermoregulation, which can effectively buffer changes in environmental temperature (Kearney, Shine & Porter 2009).
Energy acquisition by ectothermic animals is constrained by their ability to locomote in order to gather resources and their ability to process the gathered resources via handling and assimilation. These processes are highly dependent on body temperatures. Rates of locomotion, feeding, assimilation and other aspects of performance form a humped-shaped function of temperature (i.e. a thermal performance curve) (Huey & Kingsolver 1989). These curves underlie many strategies to address the energetic implications of phenotypes. Activity time, which can be estimated by comparing thermal limits for locomotion to body temperatures, has frequently been used to quantify metabolic constraints (Kearney & Porter 2004; Buckley 2008; Sinervo et al. 2010).
Temperature also affects rates of energy use. In ectotherms, body temperature exerts an exponential effect on metabolic rates, with individuals with warmer body temperatures requiring disproportionately more energy per unit time (Gillooly et al. 2001). The metabolic impacts of recent climate warming on ectotherms are estimated to be equivalent in tropical and temperate regions despite the greater magnitude of warming in temperate regions. The equivalency is due to the exponential temperature dependency of metabolic rate occurring at higher temperatures in the tropics (Dillon, Wang & Huey 2010). Rates of energy acquisition and use can be compared to estimate the amount of discretionary energy available to organisms for growth and reproduction.
Case Study: Grasshoppers along an Alpine Elevation Gradient
Our focal taxa, grasshoppers, exemplify how phenotypes vary along elevation gradients and influence energetics and demography. Grasshoppers tend to reverse the temperature-size rule, perhaps due to other constraints on size such as food availability (Whitman 2008). Their thermal conditions have been found to affect digestive efficiency (Harrison & Fewell 1995) and life-history traits such as clutch and egg sizes (Dearn 1977; Hassall et al. 2006). In one of our focal species (Melanoplus sanguinipes), both metabolic rates (Rourke 2000) and thermoregulatory behaviours (Samietz, Salser & Dingle 2005) vary among populations along an elevation gradient in California. High-elevation populations of M. sanguinipes, which experience an abbreviated growing season, exhibit accelerated juvenile development and a reduced number of days to first reproduction (Dingle, Mousseau & Scott 1990). There is a higher incidence of diapause, and diapause occurs at a later developmental stage in these populations. Clinal variation in diapause may indicate adaptation to environmental uncertainty, whereas variation in development rates may indicate adaptation to season length (Dingle, Mousseau & Scott 1990.
Many grasshopper species, especially at higher elevations, have evolved shorter wings, leading to a reduction in flight capacity and dispersal distances. Short-winged and flightless species in mountain regions show greater genetic differentiation among geographical populations and a greater potential for local adaptation (Knowles 2000; Knowles & Otte 2000). We examine four focal species that are expected to differ in their exposure to climate change and their potential for local adaptation. Melanoplus dodgei and Aeropedellus clavatus are short-winged species with limited dispersal among sites along the elevational gradient, increasing their potential for local adaptation. Camnula pellucida and M. sanguinipes are long-winged species that are occasionally collected as accidentals at sites along the gradient where juveniles are not collected. These latter species thus have a higher dispersal capacity and a greater potential for gene flow across populations. All four of these species occur from the upper foothills to the subalpine, while M. dodgei, A. clavatus and occasionally M. sanguinipes occur in the alpine.
Abundance changes over the past 50 years have varied among species and along the elevation gradient (Fig. S1, Supporting information). The fastest developing species (A. clavatus and M. dodgei) have advanced their phenology (Fig. S1, Supporting information). The slowest developing species (C. pellucida) has advanced phenology at high elevation but delayed phenology at lower elevation. The species with intermediate phenology (M. sanguinipes) has delayed phenology.
The three grasshopper genera are phylogenetically distinct and likely established in North America following a complex history of dispersal events (Contreras & Chapco 2006). Melanoplus sanguinipes is broadly distributed, while the clade containing M. dodgei diversified in the Rocky Mountains following multiple dispersal events [with the split between melanopline genera occuring ~106 ya (Knowles & Otte 2000)]. Given these phylogenetic distinctions and our small number of focal species, we do not account for evolutionary history in our analyses.
In this study, we examine phenotypic variation among populations and species across four sites along the 40th N parallel in Boulder County, CO: Eldorado (1740 m), Bettaso Preserve (1980 m), A1 (2185 m), B1 (2591 m), C1 (3048) and D1 (3749 m). The habitats at these sites are grassy clearings associated with upper prairie, foothill, montane, subalpine and alpine life zones, respectively. First, we document clinal variation in body size, thermal tolerance and metabolic rate for the four focal grasshopper species. Second, we develop a simple biophysical model that can be used to integrate phenotypic and weather data in order to predict patterns of body temperatures for each species along the elevational gradient. Finally, we examine the implications of the clinal variation for rates of energy use and the potential duration of activity along the elevation gradient.