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A behavioral trade-off and its consequences for the distribution of Pseudacris treefrog larvae.

INTRODUCTION

One of the primary goals of community ecology is understanding the causes for changes along geographic or environmental gradients. Although experiments have often been used to identify the processes maintaining structure at particular locales, manipulations have been used less often to determine patterns of distribution along gradients (notable exceptions include Connell 1961, Paine 1966, Simberloff and Wilson 1969, Lubchenco 1978, Sousa 1979, Tilman et al. 1981). Among larval anurans, distributions have been found to covary strongly with permanence of aquatic habitats (Collins and Wilbur 1979, Dale et al. 1985). In this study I focus on two species, chorus frogs (Pseudacris triseriata) and spring peepers (P. crucifer), which are quite similar in most aspects of their life histories but show striking differences in their distributions across the pond permanence gradient (see Methods: System).

There have been numerous experiments on competition and predation in communities of larval anurans and their predators (reviewed by Wilbur 1980, 1984, Gurevitch et al. 1992). These studies suggest that the interaction between the intensities of competition and predation contributes to the sorting of amphibian species along the pond permanence gradient. This is because (1) more permanent ponds tend to have more predators (Smith 1983, Woodward 1983, Skelly 1992b), (2) predation tends to reduce the impact of interspecific competition (Morin 1983, Wilbur 1987), and (3) there appears to be an inverse relationship between competitive ability and susceptibility to predators among larval anuran species (Woodward 1982, Morin 1983, Wilbur 1987). However, relatively few anuran studies have been conducted in natural ponds, and of those, almost none have been conducted across a gradient of pond types (for exceptions see Smith 1983, Smith and Van Buskirk, in press). Consequently, the relevance of ideas developed from artificial pond studies to natural communities remains an open question (Jaeger and Walls 1989, Morin 1989, Wilbur 1989). For this reason I conducted a field manipulation to evaluate the roles of competition and predation in determining larval performance of spring peepers and chorus frogs across a set of natural ponds that varied in permanence.

A second novel component of my research concerns an exploration of a behavioral trade-off that potentially underlies patterns of tadpole performance and distribution. Foraging animals can be faced with a conflict between procuring resources and surviving; this trade-off has been found for a diversity of organisms because behavior associated with acquisition of resources often engenders higher rates of mortality from predators (reviewed by Lima and Dill 1990). For anuran larvae this conflict may be mediated through activity (proportion of time spent moving) since there is evidence that activity of larval anurans is related to both growth rate (e.g., Skelly and Werner 1990) and predation risk (e.g., Woodward 1983). If this is true, then interspecific differences in activity may have important ramifications for patterns of larval performance and distribution of species among ponds that vary in permanence and composition of predators.

The aim of this research is to evaluate the possibility that mechanisms operating at the level of the individual explain differences in the impacts of competition, pre-dation, and abiotic factors (e.g., pond drying) on the success of different anurans and, ultimately, explain distribution patterns.

METHODS

System

In southeastern Michigan, chorus frogs and spring peepers are the only spring breeding treefrogs. In many important respects the two species are quite similar. Breeding typically commences in late March and development of the aquatic larvae lasts 2-3 mo (Collins 1975). After metamorphosis into a terrestrial form, individuals reach maturity within 1-2 yr and the species are comparable in adult body size, egg size, and clutch size (Collins 1975).

Chorus frogs and spring peepers typically breed in ponds that range from those that dry in early summer each year, to those that are permanent on the order of decades (Collins and Wilbur 1979). Across this gradient of pond permanence the density of tadpole predators can triple (Skelly 1992b). Composition of the predator fauna also changes, with ephemeral ponds containing primarily small invertebrate predators, and more permanent ponds containing larger predators and even fish (Skelly 1992b; D. K. Skelly, unpublished data). Although larvae of the two Pseudacris species co-occur in many ponds, the overall distributions of the species show strong differences. In samples from southeastern Michigan collected in 22 ponds for up to 4 yr (Skelly 1992b; D. K. Skelly, unpublished data), larval chorus frogs were more abundant than spring peepers in ponds that dried each year and completely absent from permanent ponds where spring peepers were usually present and often abundant. The tendency for spring peeper larvae to be distributed in more permanent and/or more predator rich environments than chorus frogs has also been reported in North Carolina (Alexander 1965), Indiana (Whitaker 1971), and northern Michigan (Smith 1983).

Field experiment

I conducted a field enclosure experiment to examine the roles of interspecific competition and predators in determining larval performance of spring peepers and chorus frogs in a set of ponds that varied in their degree of permanence. Each species was raised alone and in the presence of an equal density of the other species. The three stocking combinations (chorus frog, spring peeper, both species) result in a species treatment (chorus frog or spring peeper), and an interspecific competition treatment (each species alone versus each species with an equal density of the other species). These stocking combinations were crossed with the presence or absence of major local tadpole predators. Each treatment was replicated twice within a pond for a total of 12 enclosures per pond and the design was repeated in 6 different ponds (72 enclosures overall).

Six ponds, located on or near the E. S. George Reserve in southeastern Michigan (see Collins and Wilbur 1979 for description), were selected to represent the gradient of habitat types used by one or both frog species. There were three pond categories: (1) temporary ponds, which dry each year, typically in June or July (Harper's Pond, Grassy Dam Pond); (2) intermediate ponds, which retain water during some years but dry in July or August in other years (Ilex Pond, Crescent Pond); and (3) permanent ponds, which have not dried completely for [greater than or equal to]20 yr (George Pond, West Marsh Dam Pond; Collins and Wilbur 1979, Skelly 1992b).

These ponds also vary in other potentially important characteristics. Table 1 shows that the ponds span a range of sizes. Ponds also vary in both temperature, and productivity (see Results: Field experiment). In addition, predator density and composition, measured [TABULAR DATA FOR TABLE 1 OMITTED] immediately prior to the initiation of the field experiment, varied among the six ponds (Table 2). In the field experiment, the predator treatment reflected this variation by manipulating the presence of tadpole predators within enclosures to match locally occurring densities.

Predators included in the design (Table 2) were chosen because of their suspected importance and because they could be effectively manipulated. In particular, predators were included if they were known from laboratory trials (D. K. Skelly, unpublished data) to be effective at preying on Pseudacris tadpoles. Since several predator taxa were able to invade enclosures, the "absence" treatment was not absolute and the experiment is best interpreted as a manipulation of predator densities.

Enclosures were placed in [approximately equal to]40 cm deep water in each pond and oriented perpendicular to the shore; treatments were assigned randomly within 2 spatial blocks (1 replicate per block) in each pond. Enclosures measured 1.1 x 1.5 x 0.8 m and were constructed of wood frames covered with aluminum window screening on the bottom and mosquito netting on the sides. Enclosures also had tops of mosquito netting to prevent colonization by aerial insects and breeding frogs. Forty litres of vegetation and litter raked from the pond bottom (allowed to air dry for [greater than or equal to]24 h) was placed in each enclosure. In ponds that dried during the experiment, enclosures were periodically slid along the bottom to deeper points in the basin so that the drying date of the pond and within the enclosures coincided.

Tadpoles for the experiment were obtained from natural populations on the E. S. George Reserve by collecting chorus frog egg masses from ponds where they had been naturally deposited, and by allowing spring peeper breeding adults to mate in covered 35 x 25 x 14 cm plastic boxes containing water and vegetation (spring peepers deposit their eggs singly making collection of eggs in the field impractical). This latter technique was most successful when pairs were collected already in amplexus and when breeding boxes were floated in a pond near chorusing conspecific males. For both species several clutches from several habitats were mixed to stock enclosures. Larvae were raised in the laboratory for about 2 wk after hatching and provided ad libitum with a 3:1 mixture of Purina Rabbit Chow and TetraMin Fish Flakes. This waiting period was necessary in order to allow stocked tadpoles to grow large enough so that they could not pass through the mesh of the enclosures. At the start of the experiment snout vent length (SVL) of chorus frog larvae measured 3.4 [+ or -] 0.1 mm (mean [+ or -] 1 SE, n = 18 larvae) and spring peeper larvae measured 3.2 [+ or -] 0.1 mm (n = 32 larvae); tadpoles were at Gosner Stages 25 or 26 (Gosner 1960).

Stocking densities in the field experiment were chosen to reflect naturally occurring densities of Pseudacris larvae and predators (Tables 2 and 3). Natural densities were estimated through a modified form of drop box sampling (Wilbur 1984) using a 30 cm diameter steel pipe in lieu of a drop box (Skelly 1992b; D. K. Skelly, unpublished data). Between 9 and 70 samples [TABULAR DATA FOR TABLE 2 OMITTED] [TABULAR DATA FOR TABLE 3 OMITTED] were taken within each pond during each year (n = 16 pond-years, mean [+ or -] 1 SE = 23 [+ or -] 4 samples per pond). Sampling occurred immediately after the cessation of breeding activity, typically during the first half of May. Temporary and intermediate ponds were relatively shallow ([less than] 0.8 m deep) and Pseudacris larvae and predators were found throughout pond basins (D. K. Skelly, personal observations). Accordingly, pipe samples were spread throughout the entire basin within these ponds. In permanent ponds, Pseudacris larvae were concentrated in the littoral zone, while predators were found in the entire pond basin. In these ponds densities of tadpoles were estimated using pipe samples taken within 2 m of the shoreline. Predator densities were calculated using estimates from these pipe samples and from [greater than or equal to]2 hauls with a 7.5 x 2.0 m seine in the deeper pelagic regions based on the average, weighted by area sampled, of pipe sample and seine haul estimates.

Each enclosure was checked for metamorphs at least every other day during the metamorphic period. Frogs were not collected from enclosures until at least one forelimb had emerged (Gosner Stage 42), with many being collected after they had passed this state (Gosner Stages 43-46). All metamorphs were staged and measured (SVL) on the day of capture. SVL was used as the measure of metamorphic size because it remained relatively constant across the developmental stages during metamorphic climax compared to mass, which can drop by [greater than]50% between Gosner Stages 42 and 46 (Adolph 1931).

Pond productivity (Table 1) in the six ponds was assessed by incubating four glass microscope slides (2.5 x 7.5 cm) vertically in a floating rack that held them [approximately equal to] 1 cm apart from each other and 1 cm below the surface of the water. Large grazers of periphyton were excluded from the slides by suspending mosquito netting from the floating frame. Racks were floated in open water near the pens for a period of 10 d (3-13 June 1991). Immediately upon collection slides were preserved in 6% formalin. Dry periphyton biomass was assayed on each slide by drying the slide to constant mass at 80 [degrees] C, weighing the slide, then scraping the one side of the slide completely and then reweighing.

Temperature within the six ponds was measured between 1300 and 1400 on 3 June 1991, in order to determine relative differences in thermal environment among ponds. Two readings of water temperature were taken in each pond. All readings were taken on a clear day without cloud cover and each reading was taken within a 1/2 cm of the water surface where it was not shaded by vegetation or other obstructions. One reading was taken within 1 m of shore, and the other reading was taken between 1 and 2 m from shore.

Survivorship values were adjusted to account for invasion of Pseudacris larvae from outside of enclosures. Although stocked larvae were too large to pass out of enclosures through the mesh, late breeding in some habitats enabled small larvae to enter enclosures from the pond. Each pond had four enclosures that contained only chorus frog larvae and four enclosures that contained only spring peeper larvae. Since these enclosures initially contained only one species they could be used to calculate an average invasion rate for the other species (number of individuals of species x invaded per enclosure). For each species, this number of expected invaders was subtracted from the observed number of survivors prior to an arcsine transformation. In most ponds the invasion rate was low (mean = 2.0 individuals per enclosure), but in George Pond invasion by spring peeper larvae was excessive (mean = 25.5 individuals per enclosure). For this reason, George Pond was excluded from statistical analyses.

One of the temporary ponds, Harper's Pond, dried before any metamorphs emerged. Therefore, survivorship was zero across all treatments and no metamorphic size or larval period estimates were possible for this pond. The remaining four ponds, composed of one temporary pond (Grassy Dam Pond), two intermediate ponds (Crescent Pond, Ilex Pond), and one permanent pond (West Marsh Dam Pond), were included in the statistical analysis of the field experiment.

Metamorphic size (SVL) and larval period measures from these four ponds were untransformed prior to analysis. For measurement of larval period, 15 April 1991 was designated as day 0 for the field experiment.

Laboratory behavior experiments

I conducted three laboratory experiments to evaluate the role of behavior in mediating a trade-off between foraging gain and predation risk in tadpoles. Tadpoles for all experiments were obtained from natural populations on the E. S. George Reserve either by collecting larvae directly from the field (1989) or by collecting eggs and hatching larvae in the laboratory (1990, 1991). All experiments were conducted in a laboratory by stocking five conspecific larvae (either spring peepers or chorus frogs) into each of a set of 3.0-L (16 x 31 x 9 cm) plastic containers on a shelf in the laboratory. These containers were filled with aged well water and exposed to a 14:10 light: dark cycle from fluorescent lights. Tadpoles were fed a ground 3:1 mixture of Purina Rabbit Chow and TetraMin Fish Flakes (Alford and Harris 1988).

In each experiment I assessed tadpole activity in each container up to three times per day by counting the number of tadpoles active (out of five) at the instant of observation. Behavioral measurements were made by slowly approaching containers and recording the disposition of tadpoles from [approximately equal to]0.5 m away. There was no indication that tadpoles altered behavior upon the approach of an observer and subsequent behavior measurements on a number of species using video cameras (E. E. Werner, B. R. Anholt, and D. K. Skelly, unpublished data) have yielded results comparable to those obtained from direct observation. For the purposes of these experiments "activity" was recorded as any behavior involving movement. For both spring peeper and chorus frogs, rasping at surfaces and swimming (sensu Lawler 1989) comprised the majority of activity observations. Activity indices were generated for each container by calculating the average number of tadpoles active across all observations. Growth responses (mass gained per individual per day) were calculated using total initial and final masses of the five individuals in each container. Particulars of the design for each of the three experiments are described below.

The effect of predator presence on activity and growth rate of small tadpoles. - This experiment was designed to determine whether activity is positively correlated with growth rate of Pseudacris tadpoles by using the nonlethal presence of a predator to elicit a facultative reduction in activity (e.g., Skelly and Werner 1990, Skelly 1992a) and examining its consequence on growth rates. The experiment was conducted in May 1990 and lasted 13 d. Treatments consisted of tadpole species (spring peeper or chorus frog) crossed with the presence or absence of a caged predator, larval Anax junius (Odonata:Aeschnidae), each replicated five times. Anax is commonly found co-occurring with both spring peeper and chorus frog larvae (D. K. Skelly, unpublished data). Five tadpoles of the appropriate species were haphazardly assigned to each of 20 containers (5 replicates per treatment). Each container also held a 7.5 x 2.8 cm cage constructed of aluminum wire, plastic mesh, and fiberglass screen at one end. A single Anax larva recently fed one conspecific tadpole was placed in each of the predator treatment containers. Anax were replaced approximately every 4 d. Food was presented at 6-d intervals at a ration of 10% of body mass per individual tadpole per day. Chorus frog tadpoles (47.9 [+ or -] 5.3 mg, mean [+ or -] 1 SE) started out larger than peeper tadpoles (29.6 [+ or -] 4.7 mg) and therefore rations were scaled to the most recent measurement of mean mass within a species (tadpoles were weighed at the beginning of the experiment and again after 6 d). All individuals were initially at Gosner Stage 25. Over the course of the experiment activity was measured 29 times. Water temperature was 21.3 [+ or -] 1.1 [degrees] C (n = 11) during the experiment. All tadpoles survived the duration of the experiment.

The effect of food availability on activity and growth rate of small tadpoles. - This experiment was designed to determine whether activity and growth rate differed between spring peeper and chorus frog tadpoles, and whether these responses were altered by changes in food availability. The experiment was conducted in June 1989 and lasted 6 d. Treatments included tadpole species (spring peeper or chorus frog) and food level (low: 5% of initial body mass per tadpole per day, or high: 15% of initial body mass per tadpole per day), each replicated three times. Five tadpoles of the appropriate species were haphazardly assigned to each of 12 containers. Location of containers on the shelf was determined randomly. Food was presented in two 3-d rations. Initially all tadpoles were at Gosner Stage 25 and mass was roughly equivalent between species (spring peeper: 36.2 [+ or -] 2.4 mg, chorus frog: 34.4 [+ or -] 3.5 mg [mean [+ or -] 1 SE]). Food ration was calculated based on the common mean initial mass (35.3 mg). Over the course of the experiment activity was measured 17 times. Water temperature was 19.3 [+ or -] 1.7 [degrees] C (n = 10) during the experiment. All tadpoles survived the duration of the experiment.

The effects of predator presence and food availability on activity of large larvae. - This experiment was conducted to determine how activity responses of spring peepers and chorus frogs change ontogenetically (by examining larger, more developmentally advanced larvae than in the previous two experiments) and to determine the interaction between responses to predator presence and food availability by using a factorial design. The experiment was conducted in May and June of 1991 and lasted 6 d. Containers of either spring peeper or chorus frog larvae were subject to treatments consisting of a food manipulation (low food: 5% of body mass per tadpole per day, high food: 15% of body mass per tadpole per day) crossed with absence or non-lethal presence of larval Anax. Each treatment was replicated five times for a total of 40 containers. All containers held a 7.5 x 2.8 cm predator cage. Anax were fed a conspecific tadpole prior to being introduced into containers, and were replaced at 3-d intervals. Food was presented in two 3-d rations based on the initial average mass pooled over both species. Spring peeper (119.2 [+ or -] 14.7 mg) and chorus frog (116.8 [+ or -] 15.0 mg) tadpoles were roughly equivalent in size at the beginning of the experiment, although chorus frogs were somewhat more advanced developmentally (see Results: Predator and food responses of large larvae). Forelimb emergence (Gosner Stage 42) is an unambiguous sign of the onset of metamorphosis in anurans. Individuals with erupted forelimbs were removed from containers. Activity was measured 21 times in each container. For containers with fewer than five individuals (because of metamorphosed individuals) activity scores from each observation were scaled to reflect the number of tadpoles active if five individuals had been present (e.g., if 4 individuals were present and 2 were active, the transformed number active score was 2.5). Each container had at least three individuals at the conclusion of the experiment. Because tadpoles typically lose mass in the latter stages of larval development (e.g., Herreid and Kinney 1967), mass gain is not an effective measure of food intake, and so growth responses of large larvae were not analyzed. Temperature was 23.2 [+ or -] 1.5 [degrees] C (n = 6) over the course of the experiment. No tadpoles died during this experiment; however, 24 of the 100 chorus frog larvae and 2 of the 100 peeper larvae reached forelimb emergence (Gosner Stage 42) prior to its conclusion.

RESULTS

Field experiment revealed effects of drying and predators, but not competition

Performance of Pseudacris varied widely among ponds (Tables 4 and 5, Figs. 1-3) with survivorship to metamorphosis, metamorphic size, and larval period each contributing to variation among ponds. Specifically, in a discriminant function analysis on the multivariate response of tadpoles to different ponds (Table 6), I found that the first and second axes were highly correlated with larval period and size respectively. The third axis showed strong positive correlations with both survivorship and size. Overall, the analysis correctly [TABULAR DATA FOR TABLE 4 OMITTED] [TABULAR DATA FOR TABLE 6 OMITTED] identified ponds based on the multivariate response 69% of the time.

While the discriminant function analysis shows how performance varied among ponds, I was also interested in determining the effects of particular manipulations across the set of ponds with respect to the univariate responses (such as the effect of predator addition on survivorship of tadpoles). First, although there was no main effect of predator addition on multivariate performance, the effect of predator addition varied among ponds (Tables 4 and 5). Predator effects on survivorship (as measured from a univariate ANOVA comparable in structure to the MANOVA presented in Table 5) showed that trends in survivorship with the addition of predators ranged from increases or small decreases in survivorship in a temporary pond and both intermediate ponds to strongly negative effects in a permanent pond where fish were manipulated (pond x predator interaction from univariate ANOVA on survivorship to metamorphosis: P [less than] 0.001; Fig. 1). In general, the effects of predator addition on survivorship were more negative in ponds where more and larger predators were manipulated. Addition of predators tended to yield smaller metamorphs with longer larval periods in most ponds (Figs. 2 and 3), although these trends were small and not significant within univariate analyses (in univariate ANOVAs on metamorphic size and larval period, predator effects and predator x pond interactions were not significant: P [greater than] 0.150 in all cases).

Second, I took a similar approach to asking how the addition of an equal density of potential competitors affected performance. In contrast to the effects of predator addition, addition of potential competitors had no overall effect on performance and this response did not differ between species or among ponds (Tables 4 and 5). Univariate analyses failed to detect any main effect of competition treatment on survivorship to metamorphosis, size, or larval period (P [greater than] 0.170 in each case), however there was an indication that competitive effects on survivorship varied among ponds (pond x competition effect in univariate ANOVA on survivorship to metamorphosis: P = 0.017). The addition of potential competitors was associated with a drop in survivorship in a permanent pond (West Marsh Dam Pond). However, this pattern appears to be a result of the invasion of predatory larval dragonflies (Anax junius) into two species enclosures in this pond (Skelly 1992b).

In addition to examining variation among ponds, and between predator and competition treatments, this experimental design allowed the comparison of performance between the two Pseudacris species. Chorus frogs and spring peepers exhibited a strong overall difference in performance (Tables 4 and 5) primarily due to larger size at metamorphosis [ILLUSTRATION FOR FIGURE 2 OMITTED] and longer larval periods [ILLUSTRATION FOR FIGURE 3 OMITTED] of spring peepers compared to chorus frogs (discriminant function analysis: Table 7). The trend for more rapid development of chorus frogs was consistent among ponds, whereas the size advantage of spring peepers was absent within a temporary pond and increased in more permanent ponds (Table 4). Although survivorship did not differ between species overall (species effect in univariate ANOVA on survivorship to metamorphosis: P = 0.895), a strong interaction between species and pond (MANOVA results: Table 5) partially reflects different patterns of survivorship between species across the set of ponds (pond x species interaction in univariate ANOVA on survivorship to metamorphosis: P [less than] 0.001). Although the two species survived about equally well in both intermediate ponds, chorus frogs survived much better than spring peepers in a temporary pond and much worse than spring peepers in a permanent pond [ILLUSTRATION FOR FIGURE 1 OMITTED].

I also measured temperature and productivity in each pond (Table 1). Both water temperature (one-way ANOVA: [F.sub.5,6] = 7.4, P [less than] 0.05) and periphyton biomass (one-way ANOVA: [F.sub.5,16] = 18.0, P [less than] 0.01) varied among ponds. In addition there was a weak positive association between temperature and productivity (product-moment correlation: n = 6 ponds, r = 0.423, P [greater than] 0.20). Harper's Pond dried the day the periphyton assay was removed from ponds. Consequently, unlike any of the other habitats, the assay from this pond incubated in a near-dry habitat where temperature and nutrient concentrations are likely to have greatly increased, potentially leading to large increases in productivity (Wetzel 1983). When data from the other five ponds are analyzed without Harper's Pond, the effect of pond on temperature is still evident (one-way ANOVA: [F.sub.4,5] = 13.5, P [less than] 0.01) as is variation among ponds in periphyton biomass (one-way ANOVA: [F.sub.4,15] = 5.7, P [less than] 0.01). Without Harper's Pond the positive association between temperature and periphyton biomass is strengthened (product-moment correlation: n = 5 ponds, r = 0.885, P [less than] 0.02).

Laboratory experiments supported role of activity-based trade-off between gain and risk

These experiments were conducted to evaluate the contribution of activity in mediating a trade-off between foraging gain and predation risk that has potential implications for patterns of performance and distribution of Pseudacris larvae. The concise version of what is reported below is that when spring peeper and chorus frog tadpoles reduced activity (in the nonlethal presence of a predator), this response was associated with a drop in growth rate. Interspecifically, this correlation held up as well. Chorus frog larvae were both more active and also grew faster than spring peeper larvae.

More specifically, I found that the nonlethal presence of a predator had strong effects on the responses of small Pseudacris larvae (Table 8, [ILLUSTRATION FOR FIGURE 4 OMITTED]). Although responses differed between species, introduction of a predator was associated with overall declines in activity and growth rate. Discriminant function analysis revealed that the effect of predator presence was due more to differences in activity than differences in growth rates (correlations between coefficients of discriminant functions and response variables were 0.723 for activity and 0.133 for growth rate; the function correctly assigned containers to predator treatments in 85% of all cases). However, univariate ANOVAs showed significant main effects of predator presence on activity and growth rate (P [less than or equal to] 0.006 in both cases). In this experiment, the effect of species on response measures (Table 8) potentially reflects an initial body size difference of 18 mg, consequent differences in food rationing (which was based on initial size), and/or an interspecific difference independent of body size and food rationing.

In a separate experiment, initial sizes of chorus frog and spring peeper larvae were matched and tadpoles were raised at one of two food rations (Table 9, [ILLUSTRATION FOR FIGURE 1 OMITTED]). The differences between species observed in this experiment reflected higher activity levels and growth rates among chorus frogs compared to spring peepers (correlations between coefficients of discriminant functions and response variables were roughly equivalent at 0.474 for activity and 0.287 for growth rate; the function correctly assigned containers to species in all cases). In univiariate ANOVAs, species had significant effects on both activity and growth rate (P [less than] 0.005 in both cases).

Food ration also influenced responses in this experiment (Table 9). Increased food availability was associated with decreased activity and increased growth rate. Discriminant function analysis showed that the effect of food ration was more strongly associated with growth rate differences between food rations as opposed to activity differences (correlations between coefficients of discriminant functions and response variables were 0.694 for growth rate and -0.368 for activity; the function correctly identified food level in 92% of all cases). Results from univariate ANOVAs showed that food ration had significant effects on both activity and growth rate (P [less than] 0.020 in both cases). Compared to spring peeper larvae, activity and growth [TABULAR DATA FOR TABLE 6 OMITTED] rate of chorus frog larvae responded more strongly to change in food ration (Table 9, [ILLUSTRATION FOR FIGURE 5 OMITTED]). In fact, spring peeper activity and growth rate differed little between food rations whereas chorus frogs were much less active and grew more rapidly at high food [ILLUSTRATION FOR FIGURE 1 OMITTED].

In a third experiment I examined the activity responses of larger spring peeper and chorus frog larvae to the nonlethal presence of a predator and two different food rations (Table 10, [ILLUSTRATION FOR FIGURE 6 OMITTED]). There was no overall difference in activity between large spring peepers and large chorus frogs. Although activity in low food treatments tended to be higher than activity in corresponding high food treatments in three of four cases [ILLUSTRATION FOR FIGURE 6 OMITTED], the trend was not significant (Table 10, P = 0.296). On average, large larvae were less than half as active when in the presence of Anax. Finally, there was a significant three-way interaction among tadpole species, food, and predator treatments. At low food level, chorus frogs appeared to be less responsive to predator presence than at high food. Spring peepers reduced activity in response to Anax regardless of food treatment.

DISCUSSION

The field manipulation showed that performance of Pseudacris larvae (measured as survivorship to metamorphosis, metamorphic size, and larval period) exhibited striking variation across a set of natural ponds. In addition, chorus frogs and spring peepers differed sharply in their patterns of survivorship and growth among ponds. Relative performance of the two species along the pond permanence gradient matched their natural distributions: compared to spring peepers the performance of chorus frogs was strongest in a temporary pond, comparable within ponds of intermediate permanence, and weakest in a permanent pond.
TABLE 7. Results of discriminant function analysis for differences
in survivorship to metamorphosis, metamorphic size, and larval
period between two Pseudacris species. The discriminant function was
significant in predicting species membership (likelihood ratio test:
P [less than] 0.001). Standardized coefficients are presented along
with correlations between coefficients and measures of performance.


Response        Coefficient   Correlation


Survivorship       0.208         0.015
Size               0.634         0.593
Larval period      1.015         0.757


Contrary to results from most previous experiments on larval anurans, interspecific competition does not appear to have substantial impacts on performance in these populations. Despite the fact that stocking densities in the field experiment were at or well above natural densities, addition of an equal density of potential competitors had little effect on either Pseudacris species. Although stronger competitive effects could come from other species that frequently co-occur with Pseudacris larvae (e.g., Rana sylvatica: Morin and Johnson 1988), preliminary evidence from a field manipulation (examining competitive effects of R. clamitans on spring peepers) similarly suggests that inter-specific competition does not contribute to segregation of larval anuran species in these populations (D. K. Skelly, unpublished data).

There is evidence, however, that patterns of performance and distribution may be substantially influenced by both pond drying and predation. Pond drying completely eliminated larval cohorts of both Pseudacris species in one temporary pond and resulted in mortality of both species in the other temporary pond (doomed tadpoles were found in the bottoms of dried enclosures). Predator addition had severe negative effects on larval performance particularly within a permanent pond where fish were manipulated. The impacts of these factors at opposite ends of the permanence gradient are expected given the tendency for more and larger predators to be distributed in more permanent [TABULAR DATA FOR TABLE 8 OMITTED] ponds (Table 2; Kenk 1949, Heyer et al. 1975, Smith 1983, Woodward 1983).

Relative abilities of spring peepers and chorus frogs to exploit ponds of different permanence could be related to differences in susceptibility to pond drying and predation. Specifically, better performance of chorus frogs in a temporary pond may be a function of more rapid development by this species [ILLUSTRATION FOR FIGURE 3 OMITTED]. Conversely, poorer performance of chorus frogs relative to spring peepers in a permanent pond may reflect greater susceptibility to predators (see also Van Buskirk 1988). Comparable levels of performance in intermediate ponds are associated with a lack of mortality from pond drying, and relatively small impacts of predation on larval performance. While these results suggest that spring peepers and chorus frogs display inverse relative abilities to cope with pond drying and predators, the results of the field manipulation do not provide a complete explanation for this pattern.
TABLE 9. Results of MANOVA for the effects of tadpole species
(chorus frog or spring peeper) and food level (5% or 15% of body
mass per day) on mean number of tadpoles active per observation and
mean growth rate over the 6-d laboratory experiment. At the
beginning of the experiment tadpoles were at equivalent sizes and
developmental states.


                     Degrees
                        of
                     freedom
                   Nu-     De-
                  mera-   nomi-   Wilks'
Source            ator    nator   lambda     F         P


Tadpole species     2       7     0.133    22.813   0.0009
Food level          2       7     0.215    12.763   0.0046
Species x Food      2       7     0.335     6.954   0.0217


Because I was interested in the mechanisms underlying segregation of Pseudacris species, I also performed experiments to evaluate the role of a behavioral trade-off between foraging gain and predation risk. If a behavioral attribute such as activity is positively related to both foraging gain and predation risk, then interspecific differences in activity could be responsible for differences in performance and distribution across the pond permanence gradient. Under this scenario increased activity allows more rapid rates of growth and development only at the cost of greater predation risk. Because of the way that pond drying and predators influence larval anurans at opposite ends of the permanence gradient, more active species should tend to be found in less permanent ponds (Ludwig and Rowe 1990, Werner and Anholt 1993).

The presence of a gain-risk trade-off seems highly probable given the natural history of anuran larvae. Many anuran larvae, including both Pseudacris species examined here, frequently feed by using keratinized labial teeth to rasp at food-covered surfaces (Wassersug 1980). This form of activity, along with intervening bouts of swimming, were the most frequent types of activity observed in the laboratory experiments providing a proximate basis for a positive relationship between activity and growth rate. There is also good evidence that activity is a major determinant of risk to potential prey within aquatic systems. In a review of foraging behavior of aquatic invertebrate predators, Sih and Moore (1990) report 28 of 33 studies showed that predator diet composition was strongly influenced by relative activity levels of potential prey items. Studies dealing specifically with larval anurans as prey have also found that activity is positively related to predation risk (Woodward 1983, Lawler 1989, Richards and Bull 1990, Skelly 1994).

Results from the laboratory experiments provide support for the existence of an activity-based trade-off, and suggest that interspecific differences in activity contribute to relative performance of the two Pseudacris species. Intraspecifically, increased activity is associated with higher growth rates for both species [ILLUSTRATION FOR FIGURE 4 OMITTED]. Interspecific differences in activity [ILLUSTRATION FOR FIGURE 5 OMITTED] correspond closely to community level patterns. Compared to spring peepers, chorus frogs are more active, grow and develop faster, appear to be less susceptible to pond drying but more susceptible to predators, and tend to be distributed in less permanent ponds. This hierarchy of relationships provides an explanation for patterns of relative distribution based on the behavioral attributes of Pseudacris larvae.

Given the importance of activity to patterns of larval performance and distribution implied by the results of this study, plasticity in activity could provide a means to improve performance and extend the range of potential breeding habitats. Considered in the context of a recent model of activity (Werner and Anholt 1993), variation exhibited by Pseudacris larvae was in the predicted directions. Namely, larvae reduced activity in the presence of predators, increased activity at lower food density, and reduced activity response to predators at lower food density. However, particularly among spring peeper larvae, there was a lack of response to altered conditions in a number of instances. There are many reasons for a lack of plasticity, and resolution among possible alternatives is typically difficult (Sih 1987). However, the lack of an activity response to food by spring peepers is not due to their inability to assess changes in food concentration. Spring peeper larvae along with several other anuran species are known to facultatively modulate buccal pumping rate in response to changes in suspended algal concentrations (Seale and Wassersug 1979, Seale and Beckvar 1980, Scale et al. 1982).
TABLE 10. Three-way analysis of variance on mean number of tadpoles
active per observation of large chorus flog and spring peeper
tadpoles raised at two food levels (5% and 15% of body mass per day)
crossed with the absence or nonlethal presence of a predator (Anax
junius).


                              Mean
Source                 df     Square      F        P


Tadpole species         1      0.01      0.08    0.779
Predator                1      0.94      7.55    0.010
Food                    1      0.14      1.13    0.296
Spec x Pred             1      0.01      0.02    0.897
Spec x Food             1      0.24      1.94    0.173
Pred x Food             1      0.11      0.90    0.350
Spec x Pred x Food      1      0.57      4.61    0.039
Error                  32      0.12


Why should chorus frog larvae respond to food concentration, while spring peeper larvae did not? One potential explanation involves the difference in the consequences of changes in activity for tadpoles inhabiting temporary as opposed to permanent aquatic habitats. In more permanent ponds the major cost of low activity (low rates of growth and development) will be delayed metamorphosis and, potentially, reduced metamorphic size. In ephemeral ponds the cost of low activity is raised to include an increased likelihood of death when the pond dries. Conversely, in ephemeral ponds the cost of higher activity (more rapid growth and development) is a relatively smaller increase in predation risk compared to the situation in more permanent ponds where predator densities are higher. These relationships may favor higher activity and greater plasticity of activity (at least with respect to food concentration) for species such as chorus frogs that do not typically utilize permanent ponds.

Conclusions

Reductionist approaches to the study of communities are warranted if they allow improved understanding over more phenomenological analyses. In this study, knowledge of behavior, and in particular of a trade-off based on activity, was useful in understanding the pattern of distribution of two species of anuran larvae. Previous studies of larval anurans have suggested that segregation of species among ponds might be related to a competition-predation gradient for two reasons. First, competition should be more prevalent in less permanent ponds, where predators are less abundant and hence less able to mediate competitive release among anuran larvae. Second, there appears to be a positive relationship between competitive ability and susceptibility to predation. As a result superior competitors and species resistant to predators should be differentially arrayed among ponds.

In this study competition between Pseudacris species had little effect on performance, yet the two species are segregated along the pond permanence gradient in southeastern Michigan in a manner consistent with a hypothesis based on the competition-predation gradient. The implications of activity for rates of growth and development and for predation risk, coupled with interspecific differences between larval chorus frogs and spring peepers, provide an explanation for the distribution of these species in the absence of competition. This does not mean that competition will be unimportant in explaining tadpole distributions elsewhere. But even where competition is important, activity could still be a key parameter. Specifically, in the presence of strong competition activity is likely to have implications for abilities to depress food resources and to withstand depressed resources. Preliminary results suggest that this is so (Werner 1991, 1992, 1994) offering a mechanism for the observed correspondence between competitive ability and the use of ephemeral aquatic habitats (Woodward 1982, Morin 1983).

The use of behavioral mechanisms, and of activity in particular, in the study of communities is potentially of broad application. In order to grow and reproduce organisms must procure resources while simultaneously avoiding many potential mortality sources. There are good reasons to expect that activity will often mediate a conflict between these goals. Because resources typically have heterogeneous distributions in space (Naeem 1990) and can become locally depleted through time (Charnov 1976), movement is a fundamental component of foraging for a wide variety of animals (e.g., McPeek 1990, Pough and Taigen 1990).

In moving however, animals will often increase their risk of predation. At the most basic level, encounter rates with predators are likely to increase with increased activity (Abrams 1991, Werner and Anholt 1993). For a diversity of predators, prey movement is actually associated with the process of detecting prey, either visually (e.g., fish: Wright and O'Brien 1982, McPeek 1990) or via mechanosensory receptors (e.g., odonates: Kanou and Shimozawa 1983, Richards and Bull 1990). These relationships suggest that activity-based trade-offs may apply to a wide array of systems. Where the trade-off applies, consideration of activity should provide improved understanding of distribution patterns and community composition.

ACKNOWLEDGMENTS

I thank Tom Slawski, Tim Howard, Rachel Simpson, and Jonathan Stober for invaluable field assistance. Earl Werner, Peter Kareiva, Gary Belovsky, Spencer Cortwright, Bill Fagan, Deborah Goldberg, Martha Groom, Eli Holmes, Ron Nussbaum, Miguel Pascual, Terry Root, Cheryl Schultz, David Smith, Rachel Standish, Josh Van Buskirk, Gary Wellborn, Uno Wennergren, and three anonymous reviewers made valuable comments on previous versions of this manuscript. Ron Nussbaum, Jack Haynes, and the maintenance crew provided access to the George Reserve. This research was supported by funding from the University of Michigan and by a Grant-in-Aid of Research from Sigma Xi. Preparation of this manuscript was supported in part by a fellowship from the Australian Flora and Fauna Research Program, University of Wollongong.

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