David K. Skelly

Behavioral and Life‐Historical Responses of Larval American Toads to an Odonate Predator

This study examines the responses of larval American toads (Bufo ameri- canus) to the non-lethal presence of an odonate predator (Anax junius). We performed a laboratory experiment where toad larvae were raised at four food rations crossed with the non-lethal presence (i.e., constrained Anax) and absence of the predator. Tadpoles facul- tatively responded by metamorphosing at smaller sizes in the presence of the predator and at lower food rations. Tadpoles also responded behaviorally to the presence of predators by reducing activity and altering spatial distribution. These latter reactions appeared to contribute to reduced growth rates in the presence of the predator at a given food level. We attempted to separate the effect of the predator on size at metamorphosis into com- ponents due to the effect on growth and to more direct effects of the predator, by comparing size at metamorphosis for individuals growing at the same rate in the presence and absence of the predator (i.e., at different food levels). Our data suggest that the metamorphic response may be mediated primarily through the behavioral effects on growth, which then affect size at metamorphosis. These results are consistent with theories of amphibian metamor- phosis that predict that size at metamorphosis should depend on the relation between growth opportunities and risk of mortality in the larval and adult habitats. We discuss the importance of non-lethal effects of predators on prey performance, species interactions, and the evolution of prey defenses.

Long-term distributional dynamics of a Michigan amphibian assemblage

From 1988 to 1992 we surveyed the distribution of 14 amphibian species in a set of 37 ponds in southeastern Michigan, USA. Thirty-two of these ponds had been surveyed previously between 1967 and 1974. We found that the distributions of amphibian populations (1988-1992) were strongly related to two habitat characteristics: pond hydroperiod and forest canopy cover. Most species exhibited nonrandom distributions with respect to these pond characteristics. Between surveys, the distribution of each species changed, and most species experienced multiple population colonizations and extinctions. Turnover in the distribution of populations among ponds (estimated via Jaccards similarity coefficient) averaged nearly 50% among species. The substantial number of species colonizations (40 cases) and extinc- tions (34 cases) between surveys resulted in little net change in number of breeding popu- lations for most species; just four species experienced net changes of more than two popu- lations. Historical information indicated that, for many ponds, hydroperiod and canopy cover changed between surveys. In several cases habitat changes associated with forest succession apparently had negative impacts on amphibian populations. In ponds that now dry each summer and are under closed canopies, two-thirds of the breeding populations present during 1967-1974 were extinct during the recent survey. No population colonizations occurred in these ponds between surveys, in marked contrast to other ponds, in most of which amphibian species richness either was maintained or increased. In addition, tendencies for ponds to experience population colonizations and extinctions also were associated with pond isolation. Our results highlight the volatile nature of amphibian distributions and point to forest suc- cession, via its effects on canopy and hydroperiod, as a potential force shaping the dynamics of amphibian populations.

FOREST CANOPY AND THE PERFORMANCE OF LARVAL AMPHIBIANS

Freshwater ponds inhabited by larval amphibians can become encroached by forest vegetation. Surveys reveal that gradients formed by canopy cover can act as a selective sieve for the distribution of amphibian larvae among ponds. In eastern North America, many species, including spring peepers (Pseudacris crucifer), are usually absent from ponds where forest canopies have closed over the pond basin. Relatively fewer species, including wood frogs (Rana sylvatica), are commonly present in both closed and open canopy ponds. Long-term observations reveal that canopy development is associated with extinction of spring peeper populations and persistence of wood frog populations. We evaluated performance of spring peeper and wood frog larvae in a set of experiments designed to assess three predictions: (1) that conditions in closed canopy ponds (e.g., lower temperature) are associated with depressed growth rates, (2) that the impact of canopy cover will be more severe on an open canopy specialist vs. a canopy generalist species, and (3) that abiotic differences between closed and open canopy ponds may provide a sufficient explanation for performance patterns. In support of the first prediction, a field transplant experiment showed that both species grew slower in closed vs. open canopy ponds. We found some support for the second prediction during two separate experiments. During the field experiment, the impact of canopy on spring peeper growth was similar to the effect on wood frogs. However, in a common garden experiment (in which physical conditions tended to coverge), spring peepers raised on substrates and water from closed canopy ponds grew substantially slower than conspecifics in the presence of water and substrate from open canopy ponds. By contrast, wood frogs grew faster in the closed canopy treatment. Finally, while recognizing that abiotic variation appears to play an important role in performance across the canopy gradient, we rejected the third hypothesis. We found that a biotic manipulation (food addition) partially mitigated depressed growth rates in closed canopy ponds. This result suggests that biotic factors (e.g., variation in abundance and composition of periphyton) also contribute to performance differences across the canopy gradient.

The cane toad's (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model

Invasive species threaten biological diversity throughout the world. Understanding the dynamics of their spread is critical to mitigating this threat. In Australia, efforts are underway to control the invasive cane toad (Chaunus [Bufo] marinus). Range models based on their native bioclimatic envelope suggest that the cane toad is nearing the end of its invasion phase. However, such models assume a conserved niche between native and invaded regions and the absence of evolution to novel habitats. Here, we develop a dynamically updated statistical model to predict the growing extent of cane toad range based on their current distribution in Australia. Results demonstrate that Australian cane toads may already have the ability to spread across an area that almost doubles their current range and that triples projections based on their native distribution. Most of the expansion in suitable habitat area has occurred in the last decade and in regions characterized by high temperatures. Increasing use of extreme habitats may indicate that novel ecological conditions have facilitated a broader realized niche or that toad populations at the invasion front have evolved greater tolerance to extreme abiotic conditions. Rapid evolution to novel habitats combined with ecological release from native enemies may explain why some species become highly successful global invaders. Predicting species ranges following invasion or climate change may often require dynamically updated range models that incorporate a broader realization of niches in the absence of natural enemies and evolution in response to novel habitats.

Microgeographic adaptation and the spatial scale of evolution

Local adaptation has been a major focus of evolutionary ecologists working across diverse systems for decades. However, little of this research has explored variation at microgeographic scales because it has often been assumed that high rates of gene flow will prevent adaptive divergence at fine spatial scales. Here, we establish a quantitative definition of microgeographic adaptation based on Wrights dispersal neighborhood that standardizes dispersal abilities, enabling this measure to be compared across species. We use this definition to evaluate growing evidence of evolutionary divergence at fine spatial scales. We identify the main mechanisms known to facilitate this adaptation and highlight illustrative examples of microgeographic evolution in nature. Collectively, this evidence requires that we revisit our understanding of the spatial scale of adaptation and consider how microgeographic adaptation and its driving mechanisms can fundamentally alter ecological and evolutionary dynamics in nature.

EFFECT OF FOOD AND PREDATORS ON THE ACTIVITY OF FOUR LARVAL RANID FROGS

When animals are more active they encounter both more food and more predators. Thus, activity rates mediate a trade-off between growth rates and predation risk. Models of the trade-off generally, but not exclusively, predict reduced activity when re- source availability increases or when predation risk increases. In a laboratory setting, we videotaped larvae of four species of ranid frogs (bullfrog, Rana catesbeiana; green frog, R. clamitans; leopard frog, R. pipiens; and wood frog, R. sylvatica). Changes in activity level in response to changes in food and predator density were measured. Overall, species reduced both the proportion of time active and swimming speed with increases in resource level and predator density. These effects were additive. Regardless of food level, additional predators reduced activity levels similar amounts in all four species. Larger animals, which are less vulnerable to predation, were more active than smaller animals. Leopard frog and wood frog larvae, which are characteristic of more temporary waters, responded more strongly to variation in food levels than did bullfrog and green frog larvae.

A Toad More Traveled: The Heterogeneous Invasion Dynamics of Cane Toads in Australia

To predict the spread of invasive species, we need to understand the mechanisms that underlie their range expansion. Assuming random diffusion through homogeneous environments, invasions are expected to progress at a constant rate. However, environmental heterogeneity is expected to alter diffusion rates, especially by slowing invasions as populations encounter suboptimal environmental conditions. Here, we examine how environmental and landscape factors affect the local invasion speeds of cane toads (Chaunus [Bufo] marinus) in Australia. Using high‐resolution cane toad data, we demonstrate heterogeneous regional invasion dynamics that include both decelerating and accelerating range expansions. Toad invasion speed increased in regions characterized by high temperatures, heterogeneous topography, low elevations, dense road networks, and high patch connectivity. Regional increases in the toad invasion rate might be caused by environmental conditions that facilitate toad reproduction and movement, by the evolution of long‐distance dispersal ability, or by some combination of these factors. In any case, theoretical predictions that neglect environmental influences on dispersal at multiple spatial scales may prove to be inaccurate. Early predictions of cane toad range expansion rates that assumed constant diffusion across homogeneous landscapes already have been proved wrong. Future attempts to predict range dynamics for invasive species should consider heterogeneity in (1) the environmental factors that determine dispersal rates and (2) the mobility of invasive populations because dispersal‐relevant traits can evolve in exotic habitats. As an invasive species spreads, it is likely to encounter conditions that influence dispersal rates via one or both of these mechanisms.

Forest fragmentation predicts local scale heterogeneity of Lyme disease risk

Fragmentation of the landscape has been proposed to play an important role in defining local scale heterogeneity in Lyme disease risk through influence on mammalian host density and species composition. We tested this observed relationship in a suburban region around Lyme, Connecticut, where we collected data on the density of the tick vector, Ixodes scapularis and prevalence of the Lyme bacterium, Borrelia burgdorferi at 30 sites. Analysis of the landscape pattern of forest patches was performed using satellite imagery. The calculated landscape indices, which included patch size and isolation, revealed a positive link between fragmentation and both tick density and infection prevalence in ticks. In spite of higher entomologic risk, human incidence of Lyme disease is lower in fragmented contexts suggesting that entomologic risk is not the critical driver of human infections. These results represent a departure from the prior claims that fragmentation and human Lyme disease risk are positively linked. A complete understanding of the influence of landscape fragmentation will allow for improved risk mapping and potential environmental management of Lyme disease.

EXPERIMENTAL VENUE AND ESTIMATION OF INTERACTION STRENGTH

Ecologists utilize laboratories, mesocosms, and field environments as the settings for their experiments. However, the ways in which these venues influence exper- imental outcomes remain poorly understood. I tested the effect of experimental venue by conducting parallel manipulations in mesocosms and in the field. A target-neighbor ex- periment estimating the impact of larval wood frog (Rana sylvatica) density on the per- formance of spring peeper (Pseudacris crucifer) larvae was carried out in a set of artificial pond mesocosms and within mesh enclosures placed in natural ponds. Larvae of P. crucifer suffered sharp reductions in growth and development in the presence of increasing R. sylvatica densities when reared in mesocosms, but showed no response in field enclosures. A comparative test suggested that mesocosms yielded relatively unrealistic responses. These findings demonstrate that, apart from other considerations such as spatial scale, experimental venue can alter conclusions regarding interactions between species. If venue dependence is widespread, ecologists will need to strategically assess the choice of venue when con- sidering the goals of their experiments.

MICROGEOGRAPHIC COUNTERGRADIENT VARIATION IN THE WOOD FROG, RANA SYLVATICA

Abstract Prior studies have shown that macrogeographic gradients in temperature associated with latitude and altitude can lead to countergradient patterns of variation in a number of taxa: individuals from colder environments are known to grow or develop faster than their conspecifics from warmer environments when placed in a common setting. In this study, I hypothesized that countergradient variation also is important at microgeographic scales. The wood frog, Rana sylvatica, breeds in open‐canopied, temporary wetlands as well as those heavily shaded by vegetation. Shading leads to cooler thermal environments that are associated with embryonic development rates as much as 50% slower than those in unshaded wetlands. Wetlands with contrasting canopy environments are often found within tens or hundreds of meters of each other. In a common garden experiment, embryos from nearby natural wetlands displayed countergradient variation: individuals collected from shaded wetlands developed up to 12% faster than those collected from relatively unshaded wetlands. The results of this study suggest that the concept of countergradient variation may be extended to small scales of space. In addition, the rate and scale of vegetation dynamics (the agent of wetland shading) imply that divergence in development among residents of nearby wetlands may be relatively rapid, on the order of decades.