James R. Vonesh

Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines

Abstract. In the last decade there has been increasing evidence of amphibian declines from relatively pristine areas. Some declines are hypothesized to be the result of egg mortality caused by factors such as elevated solar UV-B irradiation, chemical pollutants, pathogenic fungi, and climate change. However, the population-level consequences of egg mortality have not been examined explicitly, and may be complicated by density dependence in intervening life-history stages. Here we develop a demographic model for two amphibians with contrasting life-history strategies, Bufo boreas and Ambystoma macrodactylum. We then use the complementary approaches of elasticity and limitation to examine the relationships among stage-specific survival rates, larval-stage density dependence and amphibian population dynamics. Elasticity analyses showed that for a range of density dependence scenarios both species were more sensitive to changes in post-embryonic survival parameters, particularly juvenile survival, than to egg survival, suggesting that mortality of later stages may play an important role in driving declines. Limitation analyses revealed that larval density dependence can dramatically alter the consequences of early mortality, reducing or even reversing the expected population-level effects of egg mortality. Thus, greater focus on later life stages and density dependence is called for to accurately assess how stressors are likely to affect amphibian populations of conservation concern.

IMPACTS OF ROAD DEICING SALT ON THE DEMOGRAPHY OF VERNAL POOL-BREEDING AMPHIBIANS

Deicing agents, primarily road salt, are applied to roads in 26 states in the United States and in a number of European countries, yet the scale of impacts of road salt on aquatic organisms remains largely under-studied. The issue is germane to amphibian conservation because both adult and larval amphibians are known to be particularly sensitive to changes in their osmolar environments. In this study, we combined survey, experimental, and demographic modeling approaches to evaluate the possible effects of road salt on two common vernal-pond-breeding amphibian species, the spotted salamander (Ambystoma maculatum) and the wood frog (Rana sylvatica). We found that in the Adirondack Mountain Region of New York (USA), road salt traveled up to 172 m from the highway into wetlands. Surveys showed that egg mass densities of spotted salamanders (A. maculatum) and wood frogs (R. sylvatica) were two times higher in forest pools than roadside pools, but this pattern was better explained by road proximity than by increased salinity. Experiments demonstrated that embryonic and larval survival were reduced at moderate (500 muS) and high conductivities (3000 muS) in A. maculatum and at high conductivities in R. sylvatica. Demographic models suggest that such egg and larval stage effects of salt may have important impacts on populations near roads, particularly in the case of A. maculatum, for which salt exposure may lead to local extinction. For both species, the effect of road salt was dependent upon the strength of larval density dependence and declined rapidly with distance from the roadside, with the greatest negative effects being limited to within 50 m. Based on this evidence, we argue that efforts to protect local populations of A. maculatum and R. sylvatica in roadside wetlands should, in part, be aimed at reducing application of road salt near wetlands with high conductivity levels.

The influence of intraguild predation on prey suppression and prey release: a meta-analysis

Intraguild predation (IGP) occurs when one predator species consumes another predator species with whom it also competes for shared prey. One question of interest to ecologists is whether multiple predator species suppress prey populations more than a single predator species, and whether this result varies with the presence of IGP. We conducted a meta-analysis to examine this question, and others, regarding the effects of IGP on prey suppression. When predators can potentially consume one another (mutual IGP), prey suppression is greater in the presence of one predator species than in the presence of multiple predator species; however, this result was not found for assemblages with unidirectional or no IGP. With unidirectional IGP, intermediate predators were generally more effective than the top predator at suppressing the shared prey, in agreement with IGP theory. Adding a top predator to an assemblage generally caused prey to be released from predation, while adding an intermediate predator caused prey populations to be suppressed. However, the effects of adding a top or intermediate predator depended on the effectiveness of these predators when they were alone. Effects of IGP varied across different ecosystems (e.g., lentic, lotic, marine, terrestrial invertebrate, and terrestrial vertebrate), with the strongest patterns being driven by terrestrial invertebrates. Finally, although IGP theory is based on equilibrium conditions, data from short-term experiments can inform us about systems that are dominated by transient dynamics. Moreover, short-term experiments may be connected in some way to equilibrium models if the predator and prey densities used in experiments approximate the equilibrium densities in nature.

Size correction: comparing morphological traits among populations and environments

Morphological relationships change with overall body size and body size often varies among populations. Therefore, quantitative analyses of individual traits from organisms in different populations or environments (e.g., in studies of phenotypic plasticity) often adjust for differences in body size to isolate changes in allometry. Most studies of among population variation in morphology either (1) use analysis of covariance (ANCOVA) with a univariate measure of body size as the covariate, or (2) compare residuals from ordinary least squares regression of each trait against body size or the first principal component of the pooled data (shearing). However, both approaches are problematic. ANCOVA depends on assumptions (small variance in the covariate) that are frequently violated in this context. Residuals analysis assumes that scaling relationships within groups are equal, but this assumption is rarely tested. Furthermore, scaling relationships obtained from pooled data typically mischaracterize within-group scaling relationships. We discuss potential biases imposed by the application of ANCOVA and residuals analysis for quantifying morphological differences, and elaborate and demonstrate a more effective alternative: common principal components analysis combined with Burnaby’s back-projection method.

FROM INDIVIDUALS TO ECOSYSTEM FUNCTION: TOWARD AN INTEGRATION OF EVOLUTIONARY AND ECOSYSTEM ECOLOGY

An important goal in ecology is developing general theory on how the species composition of ecosystems is related to ecosystem properties and functions. Progress on this front is limited partly because of the need to identify mechanisms controlling functions that are common to a wide range of ecosystem types. We propose that one general mechanism, rooted in the evolutionary ecology of all species, is adaptive foraging behavior in response to predation risk. To support our claim, we present two kinds of empirical evidence from plant-based and detritus-based food chains of terrestrial and aquatic ecosystems. The first kind comes from experiments that explicitly trace how adaptive foraging influences ecosystem properties and functions. The second kind comes from a synthesis of studies that individually examine complementary components of particular ecosystems that together provide an integrated perspective on the link between adaptive foraging and ecosystem function. We show that the indirect effects of predators on plant diversity, plant productivity, nutrient cycling, trophic transfer efficiencies, and energy flux caused by consumer foraging shifts in response to risk are qualitatively different from effects caused by reductions in prey density due to direct predation. We argue that a perspective of ecosystem function that considers effects of consumer behavior in response to predation risk will broaden our capacity to explain the range of outcomes and contingencies in trophic control of ecosystems. This perspective also provides an operational way to integrate evolutionary and ecosystem ecology, which is an important challenge in ecology.

Compensatory larval responses shift trade-offs associated with predator-induced hatching plasticity

Many species with complex life histories can respond to risk by adaptively altering the timing of key life history switch points, including hatching. It is generally thought that such hatching plasticity involves a trade-off between embryonic and hatchling predation risk, e.g., hatching early to escape egg predation comes at the cost of increased vulnerability to hatchling predators. However, most empirical work has focused on simply detecting predator-induced hatching responses or on the short-term consequences of hatch- ing plasticity. Short-term studies may not allow sufficient time for hatchlings to exhibit compensatory responses, which may extend to subsequent life stages and could alter the nature of the trade-offs associated with hatching plasticity. In this study, we examine the consequences of predator-induced hatching plasticity through the larval stage to metamor- phosis in the East African reed frog, Hyperolius spinigularis. To do this we conducted an experiment in which we manipulated initial larval size and density (mimicking the effects of egg predators) and the presence of aquatic predators. We expected that predator-induced hatchlings (because they are less developed and smaller) would experience higher per capita predation rates and a longer larval period and thus would exhibit lower survival to meta- morphosis in the presence of aquatic predators than larger, more developed, later hatched larvae. Surprisingly, we found that predator-induced hatchlings survived better, not worse, than hatchlings from undisturbed clutches. These results motivated us to develop a model parameterized from additional experiments to explore whether a combination of mecha- nisms, compensatory growth, and density- and size-specific predation, could give rise to this pattern. Predicted survival probabilities from the model with compensatory growth were consistent with those from the field experiment: early hatched larvae grew more rapidly through vulnerable size classes than later hatched larvae, resulting in higher survival at metamorphosis. Thus, in this system, there does not appear to be a trade-off in vulnerability between egg and larval predators. Instead, our results suggest that the cost that balances the survival benefit of hatching early to evade egg predators arises later in the life history, as a result of smaller size at metamorphosis.

Opposite shifts in size at metamorphosis in response to larval and metamorph predators.

Predation risk can cause organisms to alter the timing of life history switch points. Theory suggests that increased risk in an early life stage should select for switching earlier and smaller, while increased risk in the subsequent stage should select for switching later and larger. This framework has frequently been applied to metamorphosis in amphibians, with mixed results. Few studies examining the effect of larval predation risk on metamorphosis have observed the predicted pattern, and no studies, to our knowledge, have examined the effect of increased risk during and after metamorphosis on the timing of this switch point. Here we examine the effect of larval and post-metamorphic predation risk on metamorphosis in the red-eyed treefrog, Agalychnis callidryas. We raised tadpoles in the presence or absence of cues from caged water bugs fed larvae and cues from spiders fed emerging metamorphs. Water bugs are effective larval predators, while spiders are poor larval predators but prey on metamorphs. Furthermore, since spiders forage on the water surface it is possible that tadpoles could assess future risk from this predator. Predators induced opposite shifts in life history. Tadpoles emerged smaller and less developed in response to water bugs, but later and larger in response to spiders. Interestingly, predator effects on larval duration were not independent; tadpoles delayed emerging in response to spiders, but only in the absence of water bugs.

Patterns of Richness and Abundance in a Tropical African Leaf‐litter Herpetofauna1

I compared species richness and habitat correlates of leaf-litter herpetofaunal abundance in undisturbed and selectively logged forests, and an abandoned pine plantation in Kibale National Park, Uganda. I sampled 50 randomly located 25 m2 litter plots in each area during the wet and dry seasons in 1997. Ten anuran, five lizard, and three snake species were captured in plots over the study. Assemblage composition was most similar at logged and unlogged sites. The logged forest herpetofauna had higher species richness and abundance than the unlogged forest, but diversity was greater in the unlogged forest due to greater evenness. In contrast, the pine plantation site had the highest richness, abundance, and evenness of the three study sites, but species composition was distinct from the other areas. Herpetofaunal densities were significantly lower in all three areas during the dry season than in the wet season. During the dry season, soil moisture, litter mass, topography, shrub cover, and number of fallen logs were significant positive predictors of herpetofaunal presence in litter plots, but only soil moisture was significant in the wet season. The interaction of moisture and topography appears to be important in determining seasonal patterns of litter herpetofaunal distribution. Comparison of litter herpetofaunal studies across the tropics have shown that mid-elevation faunas generally support fewer species than lowland faunas. Compared with other tropical mid-elevation litter faunas, Kibale supports an intermediate number of species, but at lower densities than observed at any other mid-elevation site reported in the literature.

Sequential predator effects across three life stages of the African tree frog, Hyperolius spinigularis

While theoretical studies of the timing of key switch points in complex life cycles such as hatching and metamorphosis have stressed the importance of considering multiple stages, most empirical work has focused on a single life stage. However, the relationship between the fitness components of different life stages may be complex. Ontogenetic switch points such as hatching and metamorphosis do not represent new beginnings—carryover effects across stages can arise when environmental effects on the density and/or traits of early ontogenetic stages subsequently alter mortality or growth in later stages. In this study, I examine the effects of egg- and larval-stage predators on larval performance, size at metamorphosis, and post-metamorphic predation in the African tree frog Hyperolius spinigularis. I monitored the density and survival of arboreal H. spinigularis clutches in the field to estimate how much egg-stage predation reduced the input of tadpoles into the pond. I then conducted experiments to determine: (1) how reductions in initial larval density due to egg predators affect larval survival and mass and age at metamorphosis in the presence and absence of aquatic larval predators, dragonfly larvae, and (2) how differences in mass or age at metamorphosis arising from predation in the embryonic and larval environments affect encounters with post-metamorphic predators, fishing spiders. Reduction in larval densities due to egg predation tended to increase per capita larval survival, decrease larval duration and increase mass at metamorphosis. Larval predators decreased larval survival and had density-dependent effects on larval duration and mass at metamorphosis. The combined effects of embryonic and larval-stage predators increased mass at metamorphosis of survivors by 91%. Larger mass at metamorphosis may have immediate fitness benefits, as larger metamorphs had higher survival in encounters with fishing spiders. Thus, the effects of predators early in ontogeny can alter predation risk even two life stages later.

PREDATOR-INDUCED SHIFTS IN MOSQUITO OVIPOSITION SITE SELECTION: A META-ANALYSIS AND IMPLICATIONS FOR VECTOR CONTROL

The global resurgence and emergence of new mosquito-borne diseases and increasing resistance of mosquitoes to chemical pesticides have prompted renewed interest in biocontrol methods that use aquatic predators of mosquito larvae. For disease vectors with complex life cycles, like mosquitoes, in which adults are terrestrial and choose aquatic habitats in which to deposit their offspring, shifts in oviposition site selection may have important consequences for vector population dynamics and epidemiology. While there have been numerous studies of mosquito oviposition site selection, methodology and results vary, making it difficult to evaluate the general importance of predator-induced shifts in oviposition site selection for biocontrol scenarios. Here we use meta-analysis to provide a quantitative framework for examining variation in mosquito oviposition responses to predators. Overall, we find a broad pattern of predator avoidance among mosquito and predator taxa. The primary factor explaining variation in...