Henry M. Wilbur

Ecological Aspects of Amphibian Metamorphosis: Nonnormal distributions of competitive ability reflect selection for facultative metamorphosis

A synthetic theory of the ecology of amphibian metamorphosis is founded on the observation that the large variation in length of larval period and body size at metamorphosis typical of a particular species of amphibian cannot be directly explained by differences in dates of hatching or egg sizes. It is proposed that as development proceeds, variation in exponential growth coefficients causes a trend from a normal distribution to a skewed distribution of body sizes. The degree of skewing increases and the median of the distribution decreases with increasing initial densities of populations. The relative advantages of the largest members of a cohort may arise from a variety of mechanisms including the production of growth inhibitors, interference competition, and size-selective feeding behavior. These mechanisms result in a nonnormal distribution of competitive ability, a possible source of the density-dependent competition coefficient found in systems with many species (1). In our model the ranges of body sizes and dates of metamorphosis are determined by a minimum body size that must be obtained and a maximum body size that will not be exceeded at metamorphosis. Between these two size thresholds the endocrinological initiation of metamorphosis is expected to be related to the recent growth history of the individual larva. Species that exploit uncertain environments will have a wide range of possible sizes at metamorphosis. Species exploiting relatively certain environments will have a narrower range. The evolution of neoteny and direct development logically follow from the application of these ideas to the ecological context of the evolution of amphibian life histories. Species that live in constant aquatic habitats surrounded by hostile environments (desert ponds, caves, high-altitude lakes) may evolve permanent larvae genetically incapable of metamorphosis. Other populations may evolve a facultative metamorphosis such that populations are a mixture of neotenes and terrestrial adults. Direct development results from selection to escape the competition, predation, and environmental uncertainty characteristic of some aquatic habitats and is usually accompanied by parental care. The relation between our ecological model and the physiological mechanisms that initiate metamorphosis can only be suggested and it remains an open problem for developmental biologists.

REGULATION OF STRUCTURE IN COMPLEX SYSTEMS: EXPERIMENTAL TEMPORARY POND COMMUNITIES'

Interactions among competition, predation, and disturbance in determining the abundances of four species of anurans were studied in a factorial experiment using 36 replicated experimental ponds. Hatchlings of the four species (Rana utricularia, Scaphiopus holbrooki, Bufo americanus, and Hyla chrysoscelis) were introduced at the same relative abundances at a low or a high initial density. Competition determined survival, body size at metamorphosis, and length of larval period in high-density communities, which were food-limited. The predatory salamander Notophthalmus viridescens did not alter either the total number of metamorphs or their combined biomass in the high-density communities, but the relative abundance of metamorphs was shifted as Scaphiopus holbrooki, the com- petitive dominant, was selectively eaten. In low-density communities, predation decreased survival and biomass production of tadpoles, often to zero, in all species. For each of the four combinations of tadpole density and presence or absence of predators, ponds were drained at three rates to simulate different drying regimes. Competition slowed growth and thus increased the risk of desiccation in high-density populations in drying ponds. Predation ameliorated the effects of competition, allowing survivors to grow rapidly enough to meta- morphose before ponds dried. Survival of tadpoles to metamorphosis, body size at metamorphosis, and the timing of metamorphosis were determined in a complex way by interactions among all of the treatment effects and the life history characteristics of the four species studied. Scaphiopus was the species least sensitive to tadpole density and was the competitive dominant in ponds without newts. It has a rapid growth rate and metamorphosed soon enough to escape desiccation. It suffered the greatest risk of predation and was eliminated from even some of the high-density communities. Rana was most successful in low-density communities without predators. No Rana survived in rapidly drying (50-d) ponds because of insufficient time to obtain a minimum size for metamorphosis. Rana were also eliminated from most populations exposed to predation. The effect of competition on Bufo in high-density pop- ulations, few or no survivors, was reversed by predation as newts selectively fed on Sca- phiopus and Rana. This result was most striking in the tanks that dried most rapidly. Hyla did very poorly in all slowly drying (1 OO-d) tanks compared with controls because of intense competition. It had moderate success in high-density communities where newts had re- moved most competitors. These results show that biological and environmental factors interact to determine the structure of anuran communities. Neither competition nor predation is the single unifying force, but rather they interact to determine the different consequences of the date of drying of a pond to the success of each species.

Experimental ecology of food webs : Complex systems in temporary ponds

A food web graphically represents the paths of nutrients and energy through the living components of an ecosystem and the context in which individuals exploit their prey and avoid their enemies. Temporary ponds are excellent arenas for the study of food webs because they are discrete communities that can be mimicked in containers that approach the realism of natural habitats. Artificial ponds permit repeatable initial conditions and sufficient replication of independent experimental units in complex experiments to test hypotheses about the control of structure and function in natural communities. I used a combination of observations of natural ponds, “experimental natural history” of artificial ponds in my study area, and controlled experiments in an array of 144 replicate ponds to develop, then test, hypotheses about how the structures of food webs are regulated. Understanding food webs begins with population biology. Amphibians use the aquatic larval stage of their biphasic life cycle to exploit ephemer...

Competition, Predation, and the Structure of the Ambystoma‐Rana Sylvatica Community

Populations of six species of amphibians were manipulated in field enclosures to study the biological tractability of current concepts of the organization of natural communities. Experimental communities with a known composition of mature eggs were introduced into screen enclosures in a pond to assay the importance of competition and predation to the ecology of amphibian larvae in temporary ponds. The competitive ability of each population was measured by its survivorship, mean length of its larval period, and mean weight at metamorphosis. Three simultaneous experiments (requiring 70 enclosures and 137 populations) were replicated in a randomized complete—block design for variance analysis. The assumptions of the classical Lotka—Volterra model of competition were tested by raising Ambystoma laterale, Ambystoma tremblayi, and Ambystoma maculatum in all combinations of three initial densities (0, 32, and 64). All three measures of competitive ability were affected by competition with other species. Higher—o...

CHOICE OF OVIPOSITION SITE BY HYLA CHRYSOSCELIS: ROLE OF PREDATORS AND COMPETITORS'

The role of predators and competitors in the choice of oviposition site by the treefrog Hyla chrysoscelis was examined in a randomized complete block experiment using 90 replicated experimental ponds. Control ponds containing neither predators nor competitors were contrasted with treatment ponds into which one of four species of predators (Ambystoma maculatum larvae, Enneacanthus chaetodon adults, Notophthalmus viridescens adults, Tramea carolina larvae) or one of two species of competitors (Rana catesbeiana, Hyla chrysoscelis) was added. Treatments had significant effects on the mean number of eggs deposited in ponds. Fewer eggs were laid in ponds with Ambystoma, Enneacanthus, or Hyla, as a result of fewer females laying eggs and fewer eggs laid per visit, compared with control ponds. Notophthalmus, Rana, and Tramea had no effect on the number of eggs laid. Ovipositing Hyla discriminated among potential oviposition sites based on the species present. Choice of oviposition site can determine the success of a females reproductive investment, and it can be a mechanism affecting the structure of ecological communities as well. Our results emphasize the importance of oviposition site choice in the evolution of reproductive patterns and implicate species avoidance by ovipositing females as a mechanism important in generating variability in ecological communities.

Environmental Certainty, Trophic Level, and Resource Availability in Life History Evolution

Evolutionary theory has not yet determined the necessary and sufficient environmental factors that can be used to explain the observed diversity of life history patterns in plants and animals. Although recent theoretical treatments of the evolution of life history rely heavily on the concepts of r- and K-selection, we find this framework inadequate to explain life histories of many well-known organisms. Instead, using well-studied examples from the literature, we attempt to identify causal mechanisms in the evolution of their life histories. The density of the population in relation to resources, the trophic and successional position of the population, and predictability of mortality patterns all appear to be important determinants of adaptive strategies. Therefore, consideration of many environmental dimensions seems essential to provide complete understanding of the evolution of life histories.

Experimental Aquatic Food Webs: Interactions between Two Predators and Two Prey

We performed four replicates of all 16 combinations of the presence and absence of two predators (larvae of the dragonfly Anax junius and adult salamanders Notophthalmus viridescens) and two anuran prey (Bufo americanus and Rana palustris larvae) in an array of artificial temporary ponds. The two species of anurans were introduced at densities high enough to cause density-dependent reductions in survival and body size at metamorphosis and to increase larval period. The two species were in competition when raised together. Notophthalmus reduced the density of Bufo and caused the survivors to metamorphose early and at a small size. Anax caused an even greater reduction in survival but not as strong an acceleration of metamorphosis. Newts also reduced the density of Rana, but survivors benefited by growing rapidly. The effects of Anax were even stronger; the only Rana tadpoles that were able to metamorphose in the 2 mo of the experiment were from ponds in which Anax reduced densities enough to permit rapid growth of the surviving tadpoles.

Density‐Dependent Aspects of Growth and Metamorphosis in Bufo Americanus

Larvae of Bufo americanus (Anura: Bufonidae) were reared at controlled densities and food levels in laboratory populations and at controlled densities in enclosures in a farm pond in one— and two—species populations. Survival during the larval period was independent of population density however, the proportion of the population that successfully metamorphosed was a negative, exponential function of density. This outcome is interpreted as the result of the effect of density on the growth rate of larvae. In high density populations, a few individuals grow at the expense of smaller members of the cohort, which then have a lowered probability of metamorphosis. In spite of the strong effect of environmental heterogeneity in field experiments, the mean size at metamorphosis was significantly decreased as the initial density of either Bufo (—0.00031 g—body wt per unit increase in density) or Rana palustris (—0.00020 g—body wt per unit increase) was increased. Rana palustris frequently breeds at the same time an...

Priority Effects in Experimental Pond Communities: Competition between Bufo and Rana

The effect of order to hatching on the outcome of larval competition between two species of frogs breeding in 27 artificial ponds was studied. There were nine different treatments, each replicated three times: all combinations of various introductions of Bufo americanus hatchlings (none added, 500 added on day 0, or 500 added on day 6) and various introductions of Rana sphenocephala hatchlings (none added, 100 added on day 0, or 100 added on day 6). Response variables were the body size at metamorphosis, the length of the larval period of each individual, and the number of survivors of each species in each experimental pond. Bufo individuals and populations did best when alone. Also, they did better when introduced on day 6 rather than day 0. This may have been because the standing crop of food was greater in the communities that were 6 d older. When present with Rana, Bufo did better if added before Rana and worse if added after Rana, as compared to when both species were added at the same time. These results are consistent with a mechanism of size—specific competition. Rana also did best when alone and when introduced late rather than early. Rana did better when added after Bufo and worse when added before Bufo as compared to when both species were introduced at the same time. These results are not consistent with simple size—specific competition. When the species were together, both species did best when Bufo was added early and Rana was added late. These results suggest that optimal oviposition behavior is problematical for female frogs: the time that will be best depends on whether or not another species will be present at the time of hatching.

Propagule Size, Number, and Dispersion Pattern in Ambystoma and Asclepias

The empirical study of life history patterns has revealed a complex of interrelated adaptations that cannot easily be explained by reference to the models of demographers. Parental investment can be expended in many ways by manipulating propagule size, propagule number, and the pattern of propagule dispersal in time and space. Each aspect of reproduction entails a balance between the benefits and cost of current reproduction versus future reproduction. Natural selection results in the pattern of reproduction that maximizes the lifetime contribution of an individual to future generations. The compromise between propagule size and propagule number is modeled by the effects of competitive challenges during the early juvenile period, dispersal mechanisms, and mechanisms of predator defense. The position of the balance is modeled by the interaction of the level of investment per clutch and the functional dependence of early juvenile survival on propagule size. The spatial pattern of egg deposition is modeled by the energetic cost of nest construction and the mortality risk to the female and the foraging efficiency of nest predators. The advantage of multiple nests is related to the variance of the number of survivors rather than the mean number of survivors. The timing and size of successive clutches is modeled in relation to the length of the growing season, the extent of parental care, female mortality patterns, and the rate at which eggs can be produced. Successive clutches may be smaller and more widely spaced in time if the rate at which females can produce eggs or female survival decreases as the season progresses. In a group of four sympatric salamanders of the genus Ambystoma the pattern of egg production can be interpreted as a suite of adaptations to the annual uncertainty of the environment in which the larvae live. The salamanders differ in egg size, egg number, egg dispersion, size at metamorphosis, length of juvenile period, size at maturity, parental investment, and adult survival rate. They all reproduce during a few weeks after the ponds have thawed, have aquatic, carnivorous larvae, and are secretive during the terrestrial adult stage. In a group of six milkweeds of the genus Asclepias seed production can be interpreted as a suite of adaptations to the risk of herbivore damage, adult survival, colony size, and the spatial and temporal pattern of opportunities for seedling establishment. The species have different growth forms, habitat distributions, flower number and arrangements, number of follicles per plant, number of seeds per follicle, and individual seed weights. All species have similar mechanisms of seed dispersal, pollinator relationships, and herbivore defense mechanisms. These examples demonstrate some fundamental differences between angiosperms and vertebrates. The sedentary habit of plants often results in extreme phenotypic plasticity. The frequent occurrence of multiple shoot units per plant permits a diversity of breeding systems that may yield genetic diversity among half-sibs produced at the same time as well as a high level of spatial (different fruits) and temporal heterogeneity in seed production. Seeds may be dispersed long distances and may lie dormant for years until conditions are promising for seedling success. Vertebrates are constrained by their bilateral body form and single reproductive system. Clutches are usually discrete and probably are generally composed of full sibs that are born at nearly the same time. A wide range of developmental diversity is possible, from a prolonged larval stage to direct development. Mobility permits a high level of habitat selection, parental control over the microhabitat of the hatchlings, and the evolution of complex behavioral systems of parental care.