Larval Wood Frogs Research Articles

Importance of predator diet cues in responses of larval wood frogs to fish and invertebrate predators.

We examined the effects of predator diet on the antipredator responses of larval woodfrogs (Rana sylvatica). We found that tadpoles showed stronger responses to fish (Perca flavescens) that were fed tadpoles than those fed invertebrates. Similarly, we found that tadpoles responded more strongly to larval dragonflies (Anax spp.) fed tadpoles than to dragonflies fed invertebrates. The overall intensity of response of tadpoles to fish was much stronger than that to dragonflies. Predator diet effects are not ubiquitous in predator-prey systems. We discuss possible reasons why predator diet effects are seen in some, but not all, predator-prey systems.

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 resource 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.

Trait-Mediated Indirect Effects in Larval Anurans: Reversing Competition with the Threat of Predation

Ecologists recently have been focusing on the role that trait-mediated indirect effects can have on community structure and composition. To date, this work has primarily focused on the effects of predator-induced behavioral plasticity on communities. However, predator-induced morphological plasticity, which has been documented in many taxa, might also lead to trait-mediated indirect effects. Here, I examined how predators altered the behavior and morphology of larval wood frogs (Rana sylvatica) and leopard frogs (R. pipiens) and how these phenotypic changes altered the outcome of competition between the two species. Competition in the absence of caged predators was asymmetric; when reared separately, leopard frogs grew more than wood frogs, but when competing (without predators), wood frogs grew faster than leopard frogs. The presence of caged predators reversed the outcome of competition between the two anuran prey. In the presence of larval dragonflies (Anax spp.) or caged mudminnows (Umbra limi), leopard frogs grew faster than wood frogs while total tadpole biomass production remained unchanged. Thus, there was a predator-mediated indirect effect. Because predators alter both the behavior and morphology of larval anurans and both of these traits are known to affect resource consumption and growth, both are potential mechanisms to explain the change in competitive outcome. Changes in behavior were not related to changes in growth, but changes in morphology (specifically mouth width and tail length) were related to changes in growth. When competitors were added (without predators), wood frogs increased their mouth width by 10% and their tail length by 3%, while leopard frogs increased their mouth width by 5% and did not change their tail length. The greater increase in mouth width for wood frogs should increase their forage intake, since tadpoles feed by scraping periphyton; the importance of a 3% longer tail in competitive ability is unknown. The presence of the predator threat (via chemical cues from the caged predators) reduced both the mouth width and tail length in the two prey species to pre-competition levels. This response corresponded with the reduced competitive ability of the wood frogs. This work demonstrates that both competitors and predators can alter prey morphology and suggests that changes in morphology can cause trait-mediated indirect effects.

TRAIT-MEDIATED INDIRECT EFFECTS IN LARVAL ANURANS: REVERSING COMPETITION WITH THE THREAT OF PREDATION

Ecologists recently have been focusing on the role that trait-mediated indirect effects can have on community structure and composition. To date, this work has primarily focused on the effects of predator-induced behavioral plasticity on communities. However, predator-induced morphological plasticity, which has been documented in many taxa, might also lead to trait-mediated indirect effects. Here, I examined how predators altered the behavior and morphology of larval wood frogs (Rana sylvatica) and leopard frogs (R. pipiens) and how these phenotypic changes altered the outcome of competition between the two species. Competition in the absence of caged predators was asymmetric; when reared separately, leopard frogs grew more than wood frogs, but when competing (without predators), wood frogs grew faster than leopard frogs. The presence of caged predators reversed the outcome of competition between the two anuran prey. In the presence of larval dragonflies (Anax spp.) or caged mudminnows (Umbra limi), leopard frogs grew faster than wood frogs while total tadpole biomass production remained unchanged. Thus, there was a predator-mediated indirect effect. Because predators alter both the behavior and morphology of larval anurans and both of these traits are known to affect resource consumption and growth, both are potential mechanisms to explain the change in competitive outcome. Changes in behavior were not related to changes in growth, but changes in morphology (specifically mouth width and tail length) were related to changes in growth. When competitors were added (without predators), wood frogs increased their mouth width by 10% and their tail length by 3%, while leopard frogs increased their mouth width by 5% and did not change their tail length. The greater increase in mouth width for wood frogs should increase their forage intake, since tadpoles feed by scraping periphyton; the importance of a 3% longer tail in competitive ability is unknown. The presence of the predator threat (via chemical cues from the caged predators) reduced both the mouth width and tail length in the two prey species to pre-competition levels. This response corresponded with the reduced competitive ability of the wood frogs. This work demonstrates that both competitors and predators can alter prey morphology and suggests that changes in morphology can cause trait-mediated indirect effects.

Morphological Plasticity in Four Larval Anurans Distributed along an Environmental Gradient

We investigated morphological plasticity to the presence of predators in the tadpoles of four ranid frog species distributed along a pond hydroperiod gradient in southeast Michigan. We first reared all four species (Wood Frog, Rana sylvatica; Leopard Frog R. pipiens; Green Frog, R. clamitans; and Bullfrog, R. catesbeiana) under identical laboratory conditions in the presence and absence of caged larval dragonflies (Anax spp.). We then reared wood frog and leopard frog in outdoor mesocosms to examine the predator-induced responses during ontogeny. Finally, we reared leopard frog with predators fed either leopard frog or wood frog larvae to determine whether prey responses depended upon predators consuming conspecific prey. All four ranids exhibited some degree of morphological change in the presence of Anax; these differences were species specific and fairly robust to different experimental conditions. The responses over ontogeny indicated that the changes were direct responses to the predator’s presence and not an indirect result of the predator slowing anuran growth or development. Finally, larval leopard frog responded similarly to predators feeding on conspecifics and congenerics. Taken together, these results suggest that morphological responses to predators may be relatively common in larval anurans. Further, because many of the responses are known to be adaptive antipredator strategies, predator-induced morphological plasticity has important evolutionary and ecological implications.

Predictable changes in predation mortality as a consequence of changes in food availability and predation risk

Theory predicts that animals will have lower activity levels when either the risk of predation is high or the availability of resources in the environment is high. If encounter rates with predators are proportional to activity level, then we might expect predation mortality to be affected by resource availability and predator density independent of the number of effective predators. In a factorial experiment, we tested whether predation mortality of larval wood frogs, Rana sylvatica, caused by a single larval dragonfly, Anax junius, was affected by the presence of additional caged predators and elevated resource levels. Observations were consistent with predictions. The survival rate of the tadpoles increased when additional caged predators were present and when additional resources were provided. There was no significant interaction term between predator density and food concentration. Lower predation rates at higher predator density is a form of interference competition. Reduced activity of prey at higher predator density is a potential general mechanism for this widespread phenomenon. Higher predation rates at low food levels provides an indirect mechanism for density-dependent predation. When resources are depressed by elevated consumer densities, then the higher activity levels associated with low resource levels can lead to a positive association between consumer density and consumer mortality due to predation. These linkages between variation in behaviour and density-dependent processes argue that variation in behaviour may contribute to the dynamics of the populations. Because the capture rate of predators depends on the resources available to prey, the results also argue that models of food-web dynamics will have to incorporate adaptive variation in behaviour to make accurate predictions.

Development of arginine vasotocin innervation in two species of anuran amphibian: Rana catesbeiana and Rana sylvatica.

Arginine vasotocin (AVT) is a neurotransmitter in the amphibian central nervous system and is released from the neurohypophysis in the regulation of hydromineral balance and other homeostatic functions. Many amphibians experience drastic changes in habitat with respect to water availability during their transformation from aquatic larvae to terrestrial adults. To examine whether metamorphosis is accompanied by a reorganization of central vasotocinergic neurons, the developmental organization of vasotocin neurons and nerve fibers was studied with immunocytochemistry in the brains of bullfrogs (Rana catesbeiana) and woodfrogs (R. sylvatica). In bullfrogs, early limb-bud-stage tadpoles had AVT-immunoreactive neurons and nerve fibers in the lateral septal nucleus, amygdala, preoptic hypothalamus, suprachiasmatic nucleus, and posterodorsal tegmentum. Woodfrog larvae showed similar patterns of hypothalamic AVT immunoreactivity, although neuronal staining in the amygdala did not appear until metamorphic climax, and never appeared in septal neurons or in the posterodorsal tegmentum. Whereas the highly terrestrial R. sylvatica adults must adapt to an adult habitat with prolonged periods of dehydration, R. catesbeiana adults remain semiaquatic and, as such, need not develop extreme mechanisms for water retention. Nonetheless, vasotocinergic pathways showed developmental similarities in the two species. The early appearance of AVT innervation in both Rana suggests that AVT has neuroregulatory functions well before metamorphosis.

Lack of an association between heterozygosity and growth rate in the wood frog,Rana sylvatica

The effect of both multilocus and single-locus heterozygosity on growth rate was examined in a cohort of larvae of the wood frog, Rana sylvatica, collected from a pond during the later stages of premetamorphic development. Seven electrophoretically detected enzyme loci were used to determine individual heterozygosity, whereas the growth rate was measured as wet mass. In all cases, no significant correlation was found between multilocus heterozygosity and mass among larvae collected at intervals during the developmental period. In addition, multiple regression analyses indicated that no single locus had a demonstrable effect on growth rate. The results of this study, therefore, provide no evidence for a link between enzyme heterozygosity and growth rate during the later stages of premetamorphic development in wood frog larvae.

Predation on Larval and Embryonic Amphibians by Acid-Tolerant Caddisfly Larvae (Ptilostomis postica)

We examined effects of predation by larvae of the caddisfly Ptilostomis postica on survival of embryonic and larval wood frogs (Rana sylvatica) and spotted and Jefferson salamanders (Ambystoma maculatum and A. jeffersonianum). Studies of predation were conducted both in the laboratory and natural ponds. We also estimated the tolerance to low pH of P. postica in laboratory trials. There were significant effects of predation by P. postica on overall hatching success of A. maculatum in one laboratory experiment; there was no difference between embryos from opaque versus clear egg mass morphs. Ptilostomis postica preyed on larvae of R. sylvatica and A. jeffersonianum in the laboratory and showed no preference in choice of prey

Genetic Variation in Tolerance of Amphibians to Low pH

0bservations of within-species variation in acid sensitivity have prompted speculation that genetic variation exists in the response of amphibians to low pH conditions. Study of embryonic acid tolerance in the wood frog, Rana sylvatica, suggests that variation in hatching success at low pH is largely influenced by maternal factors, which may or may not be genetic. There is limited evidence that direct genetic factors influence differences in acid tolerance of embryos. Data from other species are largely consistent with these findings. Among wood frog larvae, there was no evidence of a maternal influence on survival time at low pH, but direct genetic variation was present

Kin recognition by larval wood frogs (Rana sylvatica): effects of diet and prior exposure to conspecifics.

We investigated kin recognition by larval wood frogs (Rana sylvatica) in blind laboratory experiments using spatial affinity as a recognition assay. Tadpoles reared with full-sibs displayed a significant preference for familiar full-sibs over unfamiliar non-kin, but failed to discriminate between unfamiliar full-sibs and unfamiliar paternal half-sibs. Tadpoles reared in social isolation (with or without maternal egg jelly) from the two-celled embryonic stage displayed a significant preference for unfamiliar full-sibs over unfamiliar non-kin. Tadpoles reared on a meat diet with their full-sibs: 1) exhibited a significant preference for unfamiliar full-sibs fed meat over unfamiliar non-kin fed meat, 2) failed to discriminate between unfamiliar full-sibs fed lettuce and unfamiliar non-kin fed meat, 3) exhibited a significant preference for unfamiliar non-kin fed meat over unfamiliar non-lin fed lettuce, 4) failed to discriminate between unfamiliar full-sibs fed meat and unfamiliar full-sibs fed lettuce, and 5) displayed a significant spatial preference for odors associated with meat (a familiar food) over odors associated with lettuce (an unfamiliar food). Our results, together with those of Cornell et al. (1989), indicate that the recognition cue of larval R. sylvatica has both genetic and environmental (dietary) components. Our findings establish that previous exposure to maternal egg jelly, kin, or conspecifics is not necessary for the development of kin recognition ability in larval R. sylvatica. Our results are more consistent with the self-learning of recognition cues (a form of phenotype matching) than with a recognition mechanism that involves a genetically fixed recognition template. Finally, our results indicate that increasing similarity between the recognition template and perceived cue does not necessarily result in increasing spatial affinity for kin.

The effects of food and density on growth and metamorphosis in larval wood frogs (Rana sylvatica) from central Labrador

Two experiments were performed on Rana sylvatica tadpoles from central Labrador to test for effects of food and density on growth and metamorphosis. In an experiment examining for the presence of diffusible growth inhibitors, one group of tadpoles was given water treated by adding a high density of sibling tadpoles, and another group was given filtered lake water. No diffusible growth inhibitors existed in this population, as body weight measured weekly, weight at metamorphosis, and duration of larval stage did not differ between control and treated groups. In a food-density experiment, effects of food and larval density were examined by subjecting tadpoles at four different densities to four food levels, creating a 4 × 4 food–density matrix. Food and density both affected growth rate, weight at metamorphosis, and duration of larval stage. Socially governed negative density-dependent interactions are either nonexistent in northern populations, or were completely masked by slight positive effects of grouping. Results suggest that northern larvae differ in life-history strategy from southern populations, and the possibility of overwintering in immature stages of high-latitude populations is discussed.

Geographic Variation in Acid Tolerance of Connecticut Wood Frogs

Acid waters are often toxic to amphibians, but the ability of these animals to survive in acidic conditions varies considerably within and among species. We examined geographic variation in the acid tolerance of wood frog (Rana sylvatica) embryos and larvae from eight ponds in Connecticut, which differed in their levels of acidity. Embryos produced by adult frogs from the different ponds varied significantly in the ability to hatch in acidic solutions. Hatching success of the embryos was not correlated with the acid levels in the ponds. Tadpole survival in low pH solutions also differed among the ponds, and acid tolerance of tadpoles was correlated with pond pH (tadpoles produced by adults from acidic ponds tended to be more acid tolerant). Results of genetic crosses among frogs from different ponds suggested that the geograhic differences in acid tolerances of embryos are not genetically determined, but population differences in the tolerance of tadpoles to acidity appear to have some genetic basis.

Variation in acid tolerance of Connecticut wood frogs: genetic and maternal effects

Acid tolerance in wood frog (Rana sylvatica) embryos and larvae was examined in full- and half-sib families. Among the embryos, no significant difference in acid tolerance at pH 3.75 was observed among the progeny of males. At pH 4 only slight differences in embryo acid tolerance existed among the progeny of males mated to the same female. Thus, there is relatively little direct genetic variation in embryo acid tolerance. However, progeny from different females differed significantly in their acid tolerance at both pH 4 and pH 3.75, indicating that maternal factors are important in embryo acid tolerance. Whether these maternal factors are genetic is not known. Among larvae, maternal factors did not appear to influence acid tolerance, but significant genetic variation was present. Larval survival in an acidic solution was not correlated with embryo acid tolerance.

Acid Tolerance in Connecticut Wood Frogs (Rana sylvatica)

-Acid tolerance limits were measured in wood frog (Rana sylvatica) embryos and larvae from a population located in New London, Connecticut. Among embryos, relative hatching success was high and not significantly different in solutions with pH 7.2-7.6, pH 6.0, pH 5.0 and pH 4.0. However, at pH 3.75 relative hatching success dropped to 50% and less than 1% of embryos survived at pH 3.5 or below. At pH 4.0 the number of developmental abnormalities among surviving embryos increased significantly, and at pH 3.75 35% of surviving embryos appeared abnormal. Larvae were more acid tolerant than embryos, and this tolerance appeared to increase as the larvae developed. Measurements of acidity in the natural breeding habitat indicated that considerable temporal and spatial variation may occur within a single pond, but the levels of acidity measured did not exceed the species' tolerance limits. The effect of hydrogen ion concentration, or pH, on freshwater ecosystems has recently been the focus of intensive study (Drablos and Tollan, 1980; Hutchinson and Havas, 1980). In spite of a growing interest in environmental acidity and its influence on plants and animals, one large group of aquatic vertebrates, the amphibians, has received relatively little attention. Many temperate zone frogs and salamanders exhibit complex life history patterns in which courtship and spawning typically occur in small ephemeral bodies of water, embryos and larvae develop in the aquatic environment, and metamorphosis results in a transition to terrestrial habitats. (There are, however, many variations of this pattern; see Salthe and Mecham, 1964 and Dent, 1968). Aquatic life history stages may be particularly susceptible to acidity, but the importance of this environmental factor in limiting the natural distributions of amphibians is not yet clearly understood. Gosner and Black (1957) first provided evidence that frog species differ in their ability to survive acidic conditions. They measured the acid tolerance limits of 11 species from New Jersey, and found that those frogs breeding in the naturally acidic waters of the Pine Barrens were more acid tolerant than those breeding only in more neutral waters. Two other investigations have also examined embryo survival of several amphibian species in acid bog water, and both detected differences among species in bog water tolerance (Karns, 1983; Saber and Dunson, 1978). Pough and Wilson (1977) tested acid tolerance in two salamander species, and found that embryos of the spotted salamander (Ambystoma maculatum) displayed increased mortality in even slightly acidic pond water. Jefferson's salamander (Ambystoma jeffersonianum) appeared to be more acid tolerant. Furthermore, Pough (1976) correlated pond acidity with embryo survivial in field populations of Ambystoma maculatum and suggested that this animal is in danger of localized extinction as a result of increasing acidity by acid precipitation. However, Cook (1978) found that populations of spotted salamanders from the Connecticut Valley of Massachusetts were considerably more acid tolerant. Thus geographical variation in acid tolerances is implicated for this species. In other studies, Schlichter (1980) investigated acid tolerance in Rana pipiens, Porter and Hakanson (1976) evaluated the impact of acid mine drainage on the distribution of Bufo boThis content downloaded from 157.55.39.128 on Mon, 18 Jul 2016 05:41:09 UTC All use subject to http://about.jstor.org/terms