Oecologia DOI 10.1007/s00442-012-2332-x
POPULATION ECOLOGY - ORIGINAL RESEARCH
Effects of size and size structure on predation and inter-cohort competition in red-eyed treefrog tadpoles Christopher M. Asquith • James R. Vonesh
Received: 25 October 2010 / Accepted: 5 April 2012 Ó Springer-Verlag 2012
Abstract Individual and relative body size are key determinants of ecological performance, shaping the strength and types of interactions within and among species. Size-dependent performance is particularly important for iteroparous species with overlapping cohorts, determining the ability of new cohorts to invade habitats with older, larger conspecifics. We conducted two mesocosm experiments to examine the role of size and size structure in shaping growth and survival in tadpoles of the red-eyed treefrog (Agalychnis callidryas), a tropical species with a prolonged breeding season. First, we used a response surface design to quantify the competitive effect and response of two tadpole size classes across three competitive environments. Large tadpoles were superior per capita effect competitors, increasing the size difference between cohorts through time at high resource availability. Hatchlings were better per biomass response competitors, and maintained the size difference between cohorts when resource availability was low. However, in contrast to previous studies, small tadpoles never closed the size gap with large tadpoles. Second, we examine the relationship between body size, size structure, and predation by dragonfly nymphs (Anax amazili) on tadpole survival and growth. Hatchlings were more vulnerable to predation; predator and large competitor presence interacted to reduce hatchling growth. Again, the size gap between cohorts increased over time, but increased marginally more with predators present.
Communicated by Anssi Laurila. C. M. Asquith J. R. Vonesh (&) Department of Biology, Virginia Commonwealth University, 1000 West Cary Street, P.O. Box 842012, Richmond, VA 23284-2012, USA e-mail:
[email protected]
These findings have implications for understanding how variation in resources and predation over the breeding season will shape population size structure through time and the ability of new cohorts to invade habitats with older conspecifics. Keywords Size structure Age structure Intraspecific competition Predator–prey Non-consumptive predator effect Ontogeny Size scaling
Introduction Body size is a key trait shaping individual performance and the outcome of species interactions (Peters 1983; Brown et al. 2004). For example, the degree to which an individual is able to rapidly deplete resources (i.e., competitive ‘‘effect’’) or grow at depleted resource levels (i.e., competitive ‘‘response’’) is fundamentally linked to body size through the ontogenetic scaling of foraging costs and gains (Sebens 1982; Werner and Gilliam 1984; Werner 1994). Similarly, the degree to which an individual is vulnerable to predation or responds to perceived risk is also linked to body size. Increasing body size generally decreases vulnerability to predation, as growing prey exceed predator capture and handling limitations (Werner and Gilliam 1984). Predation rate can also be a hump-shaped function of body size if, for example, smaller prey are less detectable than intermediate-sized prey (Werner 1988; Persson et al. 1998; Brose 2009; McCoy et al. 2011). Correspondingly, diminishing returns of investing in defensive phenotypes with increasing size due to declining vulnerability and increased metabolic costs may result in predators having smaller nonconsumptive effects on larger prey (Werner and Anholt 1996; Peacor and Werner 2001;
123
Oecologia
Cressler et al. 2010). Thus, individual body size directly impacts both competitive interactions (Wilbur 1984; Werner 1994; Kreutzer and Lampert 1999; Aljetlawi and Leonardsson 2002) and consumptive and nonconsumptive effects of predators (Aljetlawi et al. 2004; Brose 2009; McCoy et al. 2011). Variation in body size within a population (i.e., size structure) is a ubiquitous feature of animal populations that is predicted to influence a suite of ecological processes, including individual life history (Kirkpatrick 1988; Wilbur 1988) and competitive (Ebenman 1988; Smith 1990; Aljetlawi and Leonardsson 2002; Cameron et al. 2007) and predator–prey interactions (Sundell and Norrdahl 2002; Rudolf 2008a, b; Samhouri et al. 2009). In size-structured populations, the outcome of exploitative competition between two size classes depends upon their absolute sizes and the ontogenetic scaling of foraging gains and costs (Werner 1994; Persson and de Roos 2006). As a result, the competitively superior size may depend upon resource availability with declining resources or increased competition favoring smaller, more efficient size classes (Werner 1994). Size structure can also influence vulnerability to predators. When predators have a choice, predation may be size selective, potentially shifting the average phenotype in the population by disproportionately removing certain size classes (Brooks and Dodson 1965; Brodie and Formanowicz 1983). Alternatively, for predators specializing on specific prey size classes, increased size heterogeneity can confuse predators and reduce mortality (Jeschke and Tollrian 2007). Thus, it is important to consider the population size structure context upon which individual sizespecific performance plays out. Individual and relative size are expected to be particularly important for iteroparous species with overlapping cohorts (e.g., fish, Samhouri et al. 2009; amphibians, Werner 1994; trees, Kitajima and Poorter 2011). In these systems, size variation may be strongly multimodal rather than continuous, and new cohorts of small individuals must invade habitats where older, larger cohorts are established. Initial size variation between cohorts may be compounded (i.e., size gap between modes increases) or reduced as a function of environmental conditions and size-dependent scaling of cost and gain curves (Werner 1994; Peacor and Pfsiter 2006; Peacor et al. 2007a). New cohorts may experience a recruitment bottleneck imposed upon them by competition with larger resident cohorts (Schroder et al. 2009), which can slow the rate new cohorts grow through vulnerable sizes, resulting in a strong asymmetry in cohortspecific survival. If predators prefer new cohorts of small prey, larger-size classes may be released from predation (Claessen et al. 2000). Alternatively, input of new cohorts may reduce mortality of predators specializing on specific sizes (Jeschke and Tollrian 2007). Among predaceous taxa,
123
heterogeneous size structure can also result in increased cannibalism (e.g., Anholt 1994; Claessen et al. 2000; Gerber and Echternacht 2000; Cameron et al. 2007; Rudolf 2008a, b; Persson et al. 2003; Balfour et al. 2003) with important consequences for population dynamics. Further, the relationship between size structure and cannibalism in intermediate consumers can depend upon predation risk (Kishida et al. 2011) and plastic responses at lower trophic levels (Kishida et al. 2009, 2011). Thus, understanding the interplay between size and size structure-dependent competition and risk is essential for understanding recruitment in iteroparous species with overlapping cohorts. Despite a long interest in the importance of body size and size structure in shaping species interactions, few studies have quantified both competitive effect and response as a function of animal size or examined whether these relationships depend upon environmental context (but see Goldberg and Fleetwood 1987; Goldberg and Landa 1991; Leisnham and Juliano 2010; Wang et al. 2010). Here, we use the natural size variation observed among tadpoles of the Neotropical leaf breeding treefrog (Agalychnis callidryas) to motivate experiments testing how individual and relative body size affect growth and survivorship. First, we employ a response surface design to quantify competitive response and effect within and between tadpole size classes and to test whether competitive ability depends upon resources. Specifically, we examine the prediction (Werner 1994) that lowering per capita resource availability will favor smaller-size classes and may alter the size class which is competitively superior. In a second experiment, we manipulate tadpole size structure in the presence and absence of a free-roaming lethal predator to examine size-dependent performance and the independent and interactive effects of size structure and predation on tadpole growth and survival. We expect predation and inter-cohort competition to have greater impact on survival and growth of smaller tadpoles. Further, we expect the net effect of predators to shift the size-specific competitive advantage toward larger competitors, causing the size gap between cohorts in mixed treatments to increase when predators are present.
Materials and methods Study system This research was conducted during the wet season at the Smithsonian Tropical Research Institute field station in Gamboa, Panama (9°70 14.0400 N, 79°420 16.6700 W). The redeyed treefrog (A. callidryas) is a leaf-breeding hylid that is widespread throughout lowland tropical rainforests in Central America (Duellman 2001). These anurans breed on
Oecologia
rainy nights throughout the wet season (typically midMay–December) placing clutches of 35 ± 16.7 eggs (Hite 2009) on vegetation overhanging rainforest ponds. At Ocelot Pond, Gamboa, Panama, in 2008, reproductive activity peaked in July (4.05 ± 1.2 clutches m-1 pond edge) and was lowest in November (0.15 ± 0.03 clutches m-1; Hite 2009). Upon hatching, tadpoles drop into the pond where their larval period can last from 35 to 202 days depending on resource availability and predation pressure (Touchon et al., in review). Thus, new hatchlings may compete for resources with each other as well as with varying numbers of tadpoles that arrived earlier in the season. Size structure can also arise among hatchlings from a single oviposition event via predator-induced hatching plasticity (Warkentin 1995, 2011; Willink et al., in review). From hatching to metamorphosis, red-eyed treefrog tadpoles grow considerably, increasing in mass one to two orders of magnitude (from 0.01 to 0.2–1.0 g; McCoy et al. 2011). Red-eyed treefrog tadpoles are typically considered mid-water filter feeders (Wassersug and Rosenberg 1979), although recent studies have shown that they are also effective periphyton grazers (Hite 2009; Costa 2011). Larvae of the Amazon darner dragonfly (Anax amazili: Odonata: Aeshnidae) are common tadpole predators in these ponds. Aeshnid larvae can consume fairly large tadpoles (Van Buskirk 2001), but have shown preference for smaller tadpoles in feeding trials (Brodie and Formanowicz 1983). In addition, aeshnid larvae can have strong, size-dependent non-consumptive effects on tadpole growth and morphology (McCollum 1993; McCollum and Van Buskirk 1996), in some cases shifting the balance of competitive interactions (Werner 1994; Werner and Anholt 1996). Experiment 1: size and size structure effects on intraspecific competition We used a factorial response surface design (Inouye 2001) to measure the per capita and per biomass strength of intraand inter-cohort competition between hatchling and large tadpoles over a 9-day interval. Three densities of hatchling tadpoles (2, 5, and 10 individuals) were crossed with three densities of large tadpoles (2, 5, and 10 individuals) in 40-L plastic containers filled with mixed rain and aged tap water. These nine treatments resulted in six total densities ranging between 4 and 20 tadpoles per mesocosm (0.1–0.5 tadpoles L-1) and seven different proportional combinations of the two cohorts (hatchling: large = 0.2, 0.4, 0.5, 1, 2, 2.5, 5). Treatments were randomized within five replicated spatial blocks in a partially shaded field adjacent to forest (n = 45). Experimental densities overlap the natural range of this species in breeding ponds in Gamboa (Vonesh and Touchon, unpublished data). All replicates received a
common resource ration, generating fivefold variation in per capita resource availability across tadpole densities. Tadpoles were fed 0.1 g (0.003 g L-1) Sera MicronÒ fish fry food (http://www.sera-usa.com) per container initially and after 4 days. Sera MicronÒ is designed to stay in suspension, thus tadpoles likely compete primarily via exploitative mechanisms as they filter resources from the water column. Food quantities were not sufficient to satiate all tadpoles in higher density treatments (McCoy et al., unpublished data). Each container was also provided with five dried leaves (each *250 cm2) for benthic substrate and covered with a fine nylon mesh to prevent colonization of non-experimental organisms. This design enabled us to simultaneously estimate the response of target size classes to manipulated competitor class (e.g., did small versus large tadpoles respond differently to manipulating large tadpoles), as well as the effect of different size classes on a given target class (e.g., were large tadpoles affected differently by manipulating large tadpoles versus small; e.g., Goldberg and Fleetwood 1987; Werner 1994; Werner and Anholt 1996). Further, we examined how per capita resource availability affected competition between cohorts by adding individuals of the manipulated class across three background densities of the unmanipulated size class. This enabled us to empirically examine the prediction arising from Werner’s (1994) conceptual model for the ontogenetic scaling of competitive interactions that a progressive decline in resources will favor smaller-size classes (e.g., see Werner 1994: Fig. 8). As a result, declining resource availability should enhance the ability of the small cohort to close the size gap with the larger cohort and may even shift the competitively superior size class (i.e., larger class grows faster under higher resources but slower under low resources). To obtain large tadpoles, we collected 25 clutches from experimental pond on June 9–13, reared them in the laboratory, and then added hatchlings to 400-L mesocosms on June 18. These tadpoles were fed Spirulina and Sera MicronÒ ad libitum until the start of the experiment *22 days post-hatching. To obtain hatchlings, we collected 12 new clutches on July 2, reared them in the laboratory, and induced them to hatch at 6 days postoviposition, the natural peak of hatching for A. callidryas in Gamboa (Warkentin 2005), by submerging and lightly prodding embryos. At the beginning of the experiment, hatchlings and older tadpoles averaged 11.13 ± 0.86 and 37.16 ± 3.61 mm total length (TL), respectively (mean ± SD, here and throughout). On July 8, tadpoles were digitally photographed with a scale reference and randomly assigned to treatments. Tadpole length was measured from photographs using ImageJ image analysis software (Abramoff et al. 2004). We used a mass to total length regression curve from field and experimental data
123
Oecologia
[Vonesh, unpublished data; mass (g) = 0.00001 (tadpole TL mm)2.87, n = 53, r2 = 0.99] to noninvasively estimate mass for each tadpole. At the start of the experiment, hatchling and large tadpoles were estimated to be 0.010 ± 0.002 and 0.328 ± 0.090 g, respectively, and there was no difference in hatchling (F1,256 = 0.89, P = 0.53) or large (F1,256 = 0.29, P = 0.97) tadpole size across treatments. On July 17, the experiment was ended and tadpoles were removed and re-photographed. Experiment 2: size and size structure effects on predation and growth To examine the role of individual size and size structure in shaping mortality and growth in the presence of a predator, we conducted a 2 9 2 9 2 factorial experiment over 6 days in which we manipulated tadpole size (hatchling vs. large), size structure (mixed vs. single) and predator presence (1 larval dragonfly) at a common tadpole density (0.05 tadpoles L-1; 20 tadpoles 400 L-1 mesocosm total, 10 large tadpoles/10 hatchlings in mixed). These eight treatments were replicated five times (n = 40 total) in 30 mesocosms arranged in five spatial blocks (i.e., tadpoles of both sizes in mixed treatments came from a single mesocosms). Each mesocosm received 50 g of air-dried leaf litter for benthic cover and was covered with a screen. Ridges on tank sides provided perches for predators throughout the water column. Tadpole size classes were obtained as above (large: 22 clutches collected on June 30; hatchlings: 20 clutches collected on July 21). Hatchling tadpoles were maintained for 2 days in 40-L plastic containers prior to the experiment. At the beginning of the experiment, hatchlings and large tadpoles averaged 14.10 ± 1.29 and 38.13 ± 3.27 mm TL, respectively (estimated biomass 0.020 ± 0.003 and 0.345 ± 0.082 g). Within size classes, initial TL was not significantly different among treatments for hatchling (F1,298 = 0.25, P = 0.86) or large tadpoles (F1,298 = 0.08, P = 0.97) in single and mixed cohort treatments. Amazon darner (A. amazili) dragonfly larvae dip-netted from Quarry Pond on July 28 (F-0 and F-1 instars; 31.27 ± 3.61 g TL) were used as aquatic predators. Predators were maintained individually in water-filled cups without food for 24 h prior to the experiment. Dragonfly larvae and tadpoles were randomly assigned to predator treatments, digitally photographed, and added to tanks on July 29. Dragonfly larvae were added 10–15 min after tadpoles. On July 29 and August 3, tadpoles were fed 0.3 g (0.0075 g L-1) Sera MicronÒ in order to reflect per capita food availability comparable to medium density treatments above. Duration of this experiment was shaped by the necessity of having surviving hatchling tadpoles for analysis of growth rates (see ‘‘Results’’).
123
Correspondingly, dragonfly larvae were removed from the tanks on August 3 and surviving tadpoles were removed and re-photographed on August 4. Tadpole measurements were as above. Statistical analyses Statistical analyses were conducted in R 2.10.1 (R Core Development Team 2008). We used linear or generalized linear mixed models as implemented in the nlme (Pinheiro et al. 2012) or lme4 (Bates et al. 2011) packages. For all analyses, we began by fitting the maximal model with all interactions of fixed effects and employed the step AIC function or likelihood ratio tests of nested models for model simplification and selection. Model fits were evaluated using standard regression diagnostic plots. Significance of fixed effects was evaluated using type III sums of squares where appropriate. For comparison between size classes, we modeled tank within block as random effects. For comparison within sizes, we included block as a random effect. Our analyses focused on mean tadpole growth and survival for each replicate. For growth, we focused our analysis on absolute growth rate (mg day-1) to facilitate comparison with previous studies (Werner 1994; Werner and Anholt 1996), but also examine treatment effects on relative growth rate [ln (mass2) - ln (mass1)/(time2 time1)]. Survival was modeled as a binomially distributed variable with logit link. In experiment 1, we tested the independent and interactive effects of size class and hatchling and large tadpole density or biomass on survival and growth, followed by tests of effects of tadpole density or biomass within each size class. In experiment 2, we tested the effects of tadpole size, size structure and predator presence on growth and survival of each tadpole size class, followed by tests of predator and size structure effects within each size class. In both experiments, we examined how the gap between hatchlings and large tadpoles changed over the experiment in treatments with mixed cohorts.
Results Experiment 1: size and size structure effects on intraspecific competition Survivorship was high (mean % ± 1SD; 99 ± 0.07) and not affected by tadpole size class (t = -1.89, df = 40, P = 0.1), hatchling (t = -1.66, df = 40, P = 0.11) or large tadpole density (t = -1.3, df = 40, P = 0.2) or any of their interactions (all P [ 0.05). Absolute and relative growth rate depended upon the interaction between size class and large density/biomass (Table 1). Large tadpoles had higher absolute growth rates on average (mean g day-1
Oecologia Table 1 Tests for red-eyed treefrog (A. callidryas) tadpole size class and density or biomass effects on tadpole growth rate (mg day-1) in experiment 1 Fixed effect
df
F
P
Size class
1,8
37.3
\0.001
Hatchling Large
1,75 1,75
95.8 7.97
\0.001 0.006
Size class 9 large
1,8
44.06
0.002
Size class
1,7
72.3
Hatchling
1,75
0.79
0.37
Large
1,75
8.63
0.004
Size class 9 large
1,7
2.19
0.003
Size class 9 hatchling
1,7
Model for per capita
Model for per g \0.001
45.3
0.18
Results for relative growth rate mirror absolute growth and are not shown Results show fixed effects retained in final model with associated degrees of freedom, F-statistic, and P values Tank was modeled as a random effect
Table 2 Matrix of regression coefficients (±1SE) of growth rate of the target size class as a function of the density or biomass of the manipulated size class in experiment 1 Target class
Hatchling Large
Manipulated class Hatchling (ind-1)
Large (ind-1)
-0.004 ± 0.001c
-0.007 ± 0.001d
a
-0.019 ± 0.002d
-0.004 ± 0.002 Hatchling (g-1)
Hatchling Large
Large (g-1)
-0.149 ± 0.060b
-0.013 ± 0.002d
b
-0.055 ± 0.006d
-0.435 ± 0.210
Comparing across rows shows competitive ‘‘effect’’ of different classes on a given target class Comparing down columns shows the ‘‘response’’ of a target class to a manipulated competitor class Superscripts indicate statistical significance of each parameter estimate (n = 45, P \ a0.1; b0.05; c0.01; d0.001)
± 1SD; hatchlings 0.004 ± 0.002; large 0.011 ± 0.01; F1,86 = 19.8, P \ 0.001). Hatchlings had higher relative growth rates, increasing mass 61 % over the experiment while large tadpoles increased 11 % on average (F1,86 = 239.3, P \ 0.001). On a per capita basis, large tadpoles were better effect competitors (Table 2, across rows). Hatchling growth declined with increasing hatchling (Fig. 1a) and large tadpole density (Fig. 1b). Regression slope estimates indicate that increasing large tadpole density reduced hatchling growth 1.75 times faster than increasing hatchling density. Large tadpole growth declined with increasing
large tadpole density (Fig. 1d) and, marginally, hatchling density (P = 0.08; Fig. 1c). Slope estimates indicate that increasing large density reduced large tadpole growth 4.75 times faster than increasing hatchling density. Hatchlings were better per capita response competitors (Table 2, down columns), i.e., they were generally less affected by additions of either size classes. Increasing large tadpole density reduced hatchling growth less than it reduced large growth (at only 37 %, the rate it reduced large tadpole growth). Addition of hatchlings affected both sizes similarly. On a per biomass basis, small tadpoles were better effect and response competitors. Both hatchling and large tadpole growth was reduced by increasing the biomass of either size class. However, slope estimates indicate that increasing hatchling biomass reduced hatchling growth 11.5 times and large growth nine times faster than increasing large biomass (Table 2). Hatchlings were less affected by increasing the biomass of either size class. Increasing large or hatchling tadpole biomass reduced hatchling growth at only 24 or 34 % the rate it reduced large tadpole growth (Table 2). Across treatments, the size difference between hatchlings and large tadpoles increased over the course of the experiment (mean difference ± 1SD; initial 316 ± 50 mg, final 379 ± 86 mg, t = -7.79, P \ 0.001). However, the gap declined as a function of large tadpole density or biomass (density F1,40 = 43.05, P \ 0.001; biomass F1,40 = 41.5, P \ 0.001). At low densities of large tadpoles, the gap widened by 51 % over the experiment, whereas at high densities, the difference was unchanged (Fig. 2a). This pattern was driven by the result above; hatchlings were less affected by additional large individuals (or biomass) than large tadpoles (size class 9 large density/biomass interaction; Table 1). As a result, the size gap narrowed at a rate of 15.5 ± 4.0 mg per additional large tadpole. This pattern suggests that as the density of large tadpoles increased and per capita resource availability decreased, the outcome of competitive interactions shifted and removed the large tadpole advantage (Fig. 2b), a pattern consistent with predictions arising from the conceptual model of Werner (1994). Size and size structure effects on competition and predation Tadpole predation was size specific but not size selective. Hatchlings were more vulnerable than large tadpoles. Dragonflies reduced hatchling (z = -9.35, P \ 0.001; Fig. 3a) and large tadpole (z = -3.59, P \ 0.001; Fig. 3b) survival by 81 and 25 %, respectively. Size structure (i.e., single vs. mixed cohorts) had no effect on survival (Table 3). The observed total number of tadpoles killed in the mixed treatments (10.0 ± 4.35SD) was similar to the
123
Oecologia Fig. 1 Growth of the red-eyed treefrog A. callidryas: a, b hatchling tadpoles and c, d large tadpoles as a function of (a, c) hatchling density and (b, d) large tadpole density in experiment 1 (mean ± SE, n = 5 for each symbol). Treatments were 2, 5 or 10 individuals of each size added to each 40-L container
expected predation (11.29 ± 3.54) based on single size treatments (hatchlings 16.4 ± 5.9, large 6.2 ± 3.9) assuming a type I functional response (McCoy et al. 2011), indicating that predators did not show a strong size preference. Growth depended upon the interaction between tadpole size class and size structure, with hatchlings experiencing higher growth in unstructured populations but not large tadpoles (Table 3; Fig. 3c, d). Looking within each size class, hatchling growth depended upon the interaction between predator presence and tadpole size structure. Both predator (F1,9 = 235.4, P \ 0.001) and large tadpole (F1,9 = 235.4, P \ 0.001) presence reduced growth (Fig. 3c); however, their combined negative effects were less than predicted from their independent effects (predator 9 size structure interaction F1,9 = 15.4, P = 0.004). There were no significant predictors of large tadpole growth, although the best fitting model retained a marginally significant size structure by predator interaction term (predator F1,8 = 0.001, P = 0.99; size structure F1,8 = 2.28, P = 0.17; interaction F1,8 = 3.79, P = 0.08). In mixed treatments with both size classes, we examined how the presence of a lethal predator altered the size difference between cohorts over the course of the experiment.
123
We found marginal support for our prediction the size gap between hatchlings and large tadpoles would increase in the presence of predators [change in size difference (g ± 1SD) no predator (n = 5) - 0.045 ± 0.014, predator (n = 4) - 0.13 ± 0.11, one-tailed t test t = -1.73, df = 7, P = 0.06].
Discussion In many natural systems, new cohorts of small individuals must invade habitats where older, larger conspecifics are already established, resulting in competitive interactions between size classes. In systems characterized by direct interference competition, large individuals are often favored. However, when competition is primarily exploitative in nature, it is not possible to specify competitive ability based simply on body size (Werner 1994). Rather, we expect that competitive effect and response will be determined by the scaling of energetic gain and cost relationships as a function of body size (Werner and Gilliam 1984). Werner (1994) developed a conceptual model based on environmentally determined scaling constants, general power functions describing scaling of metabolic costs in
Oecologia
Fig. 2 a Change in absolute difference in tadpole mass between hatchling and large-size classes over the course of experiment 1 as a function of large tadpole density (mean ± 95 % CI, n = 15 for each symbol). Positive values indicate that size variance (size gap) increased and negative values that size variance decreased. b Effect of resource environment on competition between size classes following Werner (1994, Fig. 8). Net gain curves represent the difference between power functions describing gain (k1(mass)0.56) and cost (k1(mass)0.83) curves. Declining availability of per capita resources as large tadpole density increases from low to high is represented by an arbitrary decrease in the proportionality constant, k1. The dashed vertical lines indicate initial hatchling (Hi) and large tadpole (Li) mass and their intersection with the net gain curves indicate the growth of size classes at different densities of the largesize class (i.e., additions of 2, 5, and 10 large tadpoles per mesocosms). Hatchlings grow slower than large tadpoles at low and medium densities of large tadpoles, but growth for hatchlings and large tadpoles is similar at high densities of large tadpoles
anurans (Sebens 1982), and the allometric scaling of buccal pumping in filter feeding tadpoles (Wassersug and Rosenberg 1979). Within this framework, competitive effect is determined by the per capita impact of an individual on resources and is determined by the gain curve, whereas competitive response is related to the ability to tolerate a given resource level and is determined by the net gain curve (Fig. 2b), the difference between cost and gain curves. Because gain increases monotonically with size, large-size classes are expected to be better effect
competitors. Werner (1994) and Werner and Anholt (1996) found this to be the case, as did we. Both hatchlings and large tadpoles were more affected by increasing large tadpole density than by increasing hatchling density (Table 2, across rows). We also found that, on a per biomass basis, large tadpoles responded more strongly than hatchlings to increased biomass of both size classes and that hatchlings had much larger effects on both size classes. Thus, on a per mass basis, hatchlings were superior competitors (Werner 1994; Werner and Anholt 1996). Where our results differed with those of Werner (1994) and Werner and Anholt (1996) is that small tadpoles in both these previous studies had higher absolute growth rates than larger tadpoles and ‘‘caught up’’ with the largersize class, closing the size gap over the course of the study. Werner (1994) found that small tadpoles that were initially 32 % of large tadpole mass increased to 77 % of large mass over the course of that experiment. In contrast, in our study, hatchlings had lower absolute growth and lost ground with the large tadpoles (Fig. 2a). Across treatments, the size difference between hatchlings and large tadpoles increased by 23 % by the end of our experiment. This important difference between studies can potentially be explained within Werner’s (1994) framework for the ontogenetic scaling of competitive relationships. While competitive effect is determined by size, indeterminacy in size-dependent interactions arises due to the response component of competition. Because response is determined by the difference between cost and gain functions, the relative responses of two competing size classes depends on their absolute sizes (Werner 1994). If both sizes are to the left of the peak of the net gain curve (e.g., Fig. 2b, low), growth of the large class is greater, and the resulting positive feedback to the large class allows even greater net gains as the large class ‘‘climbs the net gain curve faster’’ as the superior competitor (Werner 1994). If this is the case, we would expect the variance in size to increase over time as large tadpoles ‘‘pull away’’ from the small tadpoles. This pattern is consistent with our findings. Indeed, Werner (1994) argues that many competitive interactions among tadpoles may be restricted to this case as tadpoles metamorphose before or shortly after they cross the gain/cost break-even point. We think this scenario is likely for anurans found in seasonal aquatic habitats where there is a premium on reaching metamorphosis before habitats dry down. In contrast, Werner (1994) interprets the fact that small tadpoles gain ground in his studies as evidence that small tadpoles are on the ascending portion of the net gain curve while large tadpoles are on the descending portion. As a result, increased growth yields increasingly diminished returns to large tadpoles, while smaller tadpoles ‘‘accelerate’’ growth as they climb the gain curve, closing the size gap and reducing size variance (Werner 1994).
123
Oecologia Fig. 3 Effect of predator presence and tadpole size structure (i.e., mixed or single cohorts) on a hatchling, b large tadpole survival, c hatchling, and d large tadpole growth (mean ± SE, n = 5 for each symbol)
Table 3 Tests for tadpole size class, predator presence and tadpole size structure (mixed vs. single) on overall survival and growth rate (mg day-1) in experiment 2 Fixed effect
df
t
P
Model for survival Size class
1,8
-0.84
0.43
Predator Size class 9 predator
1,25 1,8
-5.59 2.65
\0.001 0.029
df
F
P
Model for growth Size class
1,6
7.62
0.03
Predator
1,22
0.05
0.82
Size structure
1,22
0.83
0.37
Size class 9 predator
1,6
3.66
0.10
Size class 9 size structure
1,22
5.17
0.03
Results for relative growth rate mirror absolute growth and are not shown Results show fixed effects retained in final model with associated degrees of freedom, F-statistic, and P values Tank was modeled as a random effect
123
This scenario may be more characteristic of amphibians found in permanent habitats where multiple growing seasons are possible. Werner (1994) also predicted that a progressive decrease in resources, e.g., due to an increase in the density of a manipulated class, should shift the relative responses of two competing size classes. Specifically, a larger class should grow faster when resources are high, but grow slower when resources are limiting. Because we employ a full response surface design, we are in a position to test this prediction (Werner 1994; Werner and Anholt 1996 used smaller additive designs). We find that when the density of large tadpoles is low and, since all treatments received the same resource supplement, resource availability (per capita or per biomass) is high, large tadpoles grow faster and the gap widens by 52 %. This pattern could result from both size classes being to the left of the peak of the net gain curve (Fig. 2b, low density). However, at high density and low resource availability, the difference in size between classes remains unchanged over the experiment (Fig. 2a). We would expect this result if at the lower resource
Oecologia
availability the net gain curve shifts lower, resulting in the large-size class having lower growth—similar to that of the small class (Fig. 2b, high density). New cohorts of small individuals must invade habitats where predators as well as larger conspecifics have established. Differences in size-specific consumptive and nonconsumptive predator effects or size-selective predation may also influence their success. Predator effects were strongly dependent on size and, for hatchling tadpoles, size structure. Hatchlings were 2.6 times more vulnerable to predation by A. amazili compared to large tadpoles and declining vulnerability over this tadpole size range appears to be general to a number of predators in this system (McCoy et al. 2011). Thus, new hatchling cohorts must also run a gauntlet of initial vulnerability in order to reach larger-size classes and the rate at which they grow through this window of vulnerability will determine mortality due to predation (Vonesh and Bolker 2005). In addition, predators dramatically reduced the final size of hatchlings but not large tadpoles. This reduction in hatchling growth is likely due to trade-offs associated with reduced foraging (Van Buskirk et al. 1997a, b) or elevated physiological costs associated with predator stressors (Steiner 2007). Selective predation could have played a role in shaping hatchling size, if for example predators preferentially consumed larger hatchlings. However, the final size distribution of the hatchlings from predator and predator-free treatments showed little overlap (hatchlings no predator: 19.4–27.3 mm; predator: 13.9–23.0 mm), indicating that the size distribution of hatchlings in the presence of Anax is not simply a truncation of the predatorfree pools. The magnitude of growth reduction seen here in response to a free-roaming lethal A. amazili (64 %) is very similar to our studies with caged A. amazili in the same venue (*60 %; McCoy et al., in review) and larger than observed in some previous studies with caged aeshnid predators and tadpoles (e.g., Werner and Anholt 1996). These results suggest that, despite an increase in per capita resource availability due to prey thinning by predators, trait-mediated effects dominate the net predator effects on hatchling growth. While both predators and large competitors reduced hatchling growth, their combined effects on growth were less than predicted from their independent effects. Predators reduced growth less dramatically when large competitors were present. This finding may reflect resourcedependent expression of plastic defensive phenotypes by hatchlings. Hatchlings already reducing growth in response to competition may have been unable to reduce growth much further in response to predators. However, while the combined effects of predator and large tadpoles on hatchling growth may have been less than predicted from their independent effects, overall, the net effect of predators
favored larger-size classes and the size gap between cohorts tended to increase more when predators were present. This finding is consistent with Peacor et al. (2007b), which shows that that size-dependent nonconsumptive effects of predators on growth can result in increased size variation. This asymmetry in size class vulnerability and dependence of intra-cohort competitive interactions on resources or density has implications for tadpole growth and size structure over the wet season. Early in the season, when densities are low and resources are high, large tadpoles in our system have strong per capita effects on entering hatchlings that limit their ability to gain on larger individuals. However, as more effective competitors on a per biomass basis, small tadpoles can persist in the system growing slowly until released from competition by metamorphosis of larger classes. Size structure early in the season may be strongly bimodal, with slow-growing smaller classes ‘‘waiting’’ for rapidly growing large tadpoles to metamorphose. As a result, new cohorts stalled in a vulnerable size class may experience relatively high mortality while larger, older cohorts accelerate up the net gain curve toward the size refuge and metamorphosis. As tadpole densities increase and pond resources are depleted over the course of the season, we might expect conditions to increasingly favor hatchlings and size variation within the pond to decrease. These conditions could result in fairly even growth among size classes, less size variation in metamorphs, and a more even distribution of predation across sizes. If resources were further depleted such that the intersection between the net gain curve and minimum size for metamorphosis is below the break-even point, small tadpoles may even be able to grow, converge and accumulate on a larger-size class that is unable to attain metamorphosis. Similar scenarios have been observed in some fish populations in which strong competition between year classes results in juvenile bottlenecks. In these systems, regulation by competition at bottlenecks can weaken when some individuals become large enough to become piscivorous and/or cannibalistic (Persson and Greenberg 1990; Olson et al. 1995). This may occur in size-structured populations of aquatic insects and amphibians in which cannibalism is common (e.g., Hopper et al. 1996; Rudolf 2008a, b; Kishida et al. 2009, 2011), including the tadpoles of some tropical hylids (Crump 1990; Hawley 2009). However, cannibalism is unlikely to be important in our system. Roberts (1994) reports egg cannibalism by A. callidryas, but this could only hold for eggs which become flooded, and experiments designed to elicit cannibalism (i.e., high density, large size variation) have failed to reveal any evidence of intraguild predation (Vonesh, unpublished data).
123
Oecologia
There has been a long history of research regarding the role of body size and size structure in population and community ecology (e.g., Brooks and Dodson 1965; Peters 1983; Ebenman and Persson 1988) and it continues to be a topic of considerable interest (e.g., Crumrine 2010; Kishida et al. 2011; McCoy et al. 2011). Size structure can have important consequences for life history (Claessen et al. 2000) and can alter invasion success (Schroder et al. 2009) and population and community structure and dynamics (De Roos et al. 2003; Persson et al. 2003). Here, we build upon earlier studies (e.g., Werner 1994; Werner and Anholt 1996) and show that, in this system, predation depends upon prey size but not prey size structure, while individual size and size structure within populations coupled with predator presence determine competitive interactions. Further, in contrast to previous studies, we find that smallsize classes were unable to close the size gap with larger individuals, but that this competitive asymmetry weakened as resource availability declined, as predicted by theory. This may be the more typical condition for anuran with aquatic larvae and prolonged breeding and has implications for how size-structured interactions between tadpoles and their predators may shift over the season. Acknowledgments We thank the Autoridad Nacional del Ambiente de Panama´ for permission to conduct this research in Panama (Permiso No. SE/A-41-08) and the Smithsonian Tropical Research Institute for use of its facilities and logistical support. This research was conducted under Boston University IACUC protocol # 08-011 and STRI’s IACUC protocol 2008-04-06-24-08. We would like to thank S. Gonzalez, I. Smith, H. McLeod, A. Lebron, and the rest of the 2009 Vonesh-Warkentin ‘‘Fear, death and life history switch points’’ Gamboa, Panama research group for their assistance in the field. We also thank D. Young, S. McIninch, L. Bulluck, J. Touchon, M. McCoy, J. Kraus, A. Laurila and three anonymous reviewers for comments that improved the manuscript. This work was funded by the National Science Foundation (DEB-0717200 to J.R.V.) and the Sigma Xi Grants-in-Aid of Research (CMA) and was conducted in partial fulfillment of a MS degree in Biology at V.C.U. by CMA.
References Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with image. J Biophotonics Intl 11:36–42 Aljetlawi AA, Leonardsson K (2002) Size-dependent competitive ability in a deposit-feeding amphipod, Monoporeia affinis. Oikos 97:31–44 Aljetlawi AA, Sparrevik E, Leonardsson K (2004) Prey-predator sizedependent functional response: derivation and rescaling to the real world. J Anim Ecol 73:239–252 Anholt BR (1994) Cannibalism and early instar survival in a larval damselfly. Oecologia 99:60–65 Balfour RA, Buddle CM, Rypstra AL, Walker SE, Marshall SD (2003) Ontogenetic shifts in competitive interactions and intraguild predation between two wolf spider species. Ecol Entomol 28:25–30 Bates D, Maechler M, Bolker B. (2011) Linear mixed-effects models using S4 classes. R package version 0.999375-42
123
Brodie DB, Formanowicz DR (1983) Prey size preference of predators: differential vulnerability in larval anurans. Herpetologica 39:67–75 Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150:28–35 Brose U (2009) Body-mass constraints on foraging behavior determine population and food web dynamics. Funct Ecol 24:28–34 Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789 Cameron TC, Wearing HJ, Rohani P, Sait SM (2007) Two-species asymmetric competition: effects of age structure on intra- and interspecific interactions. J Anim Ecol 76:83–93 Claessen D, Van Oss C, De Roos AM, Persson L (2000) The impact of size-dependent predation on population dynamics and individual life history. Ecology 83:1660–1675 Costa Z (2011) Species level differences in the ecology of two Neotropical tadpoles: responses to nonlethal predators and the roles of competition and resource use. Master’s thesis, Virginia Commonwealth University, Richmond Cressler CE, King AA, Werner EE (2010) Interactions between behavioral and life-history trade-offs in the evolution of integrated predator-defense plasticity. Am Nat 176:276–288 Crump ML (1990) Possible enhancement of growth in tadpoles through cannibalism. Copeia 1990:560–564 Crumrine PW (2010) Size-structured cannibalism between top predators promotes the survival of intermediate predators in an intraguild predation system. J N Am Benth Soc 29(2):636–646 De Roos AM, Persson L, McCauley E (2003) The influence of size dependent life-history traits on the structure and dynamics of populations and communities. Ecol Lett 6:473–487 Duellman WE (2001) The hylid frogs of Middle America. Society for the Study of Amphibians and Reptiles, St. Louis Ebenman B (1988) Competition between age classes and population dynamics. J Theor Biol 131:389–400 Ebenman B, Persson L (1988) Size-structured populations: ecology and evolution. Springer, Berlin Gerber GP, Echternacht AC (2000) Evidence for asymmetrical intraguild predation between native and introduced Anolis lizards. Oecologia 124:599–607 Goldberg DE, Fleetwood L (1987) Comparison of competitive effects and responses among annual plants. J Ecol 75:1131–1144 Goldberg DE, Landa K (1991) Competitive effect and response— hierarchies and correlated traits in the early stages of competition. J Ecol 79(4):1013–1030 Hawley TJ (2009) The ecological significance and incidence of intraguild predation and cannibalism among anurans in ephemeral tropical pools. Copeia 2009:748–757 Hite JL (2009) Predator and abiotic effects on hatching phenotype and survival of arboreal frog eggs with implications for phytoplankton. Master’s thesis, Virginia Commonwealth University, Richmond Hopper KR, Crowley PH, Kielman D (1996) Density dependence, hatching synchrony, and within-cohort cannibalism in young dragonfly larvae. Ecology 77:191–200 Inouye BD (2001) Response surface experimental designs for investigating interspecific competition. Ecology 82:2696–2706 Jeschke JM, Tollrian R (2007) Prey swarming: which predators become confused and why? Anim Behav 74:387–393 Kirkpatrick M (1988) The evolution of size in size-structured populations. In: Ebenman B, Persson L (eds) Size-structured populations: ecology and evolution. Springer, New York, pp 13–28 Kishida O, Trussell GC, Nishimura K, Ohgushi T (2009) Inducible defenses in prey intensify predator cannibalism. Ecology 90: 3150–3158 Kishida O, Trussell GC, Ohno A, Kuwano S, Ikawa T, Nishimura K (2011) Predation risk suppresses the positive feedback between size structure and cannibalism. J Anim Ecol 80:1278–1287
Oecologia Kitajima K, Poorter L (2011) Functional basis for resource niche partitioning by tropical trees. In W. Carson and S. Schnitzer (eds) Tropical forest community ecology. Wiley–Wiley-Blackwell, Hoboken Kreutzer C, Lampert W (1999) Exploitative competition in differently sized Daphnia species: a mechanistic explanation. Ecology 80: 2348–2357 Leisnham PT, Juliano SA (2010) Interpopulation differences in competitive effect and response of the mosquito Aedes aegypti and resistance to invasion by a superior competitor. Oecologia 164(1):221–230 McCollum SA (1993) Ecological consequences of predator-inducedpolyphenism in larval hylid frogs. PhD dissertation. Duke University, Durham, NC McCollum SA, Van Buskirk J (1996) Costs and beneÒts of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution 50:583–593 McCoy MW, Bolker BM, Warkentin KM, Vonesh JR (2011) Predicting predation through prey ontogeny using size-dependent functional response models. Am Nat 177:752–766 Olson MH, Mittelbach GG, OSenberg CW (1995) Competition between predator and prey-resource-based mechanisms and implications for stage structured dynamics. Ecology 76:1758– 1771 Peacor SD, Pfsiter CA (2006) Experimental and model analyses of the effects of competition on individual size variation in wood frog (Rana sylvatica) tadpoles. J Anim Ecol 75:990–999 Peacor SD, Werner EE (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proc Natl Acad Sci USA 98(7):3904–3908 Peacor SD, Bence JR, Pfister CA (2007a) The effect of sizedependent growth and environmental factors on animal size variability. Theor Popul Biol 71:80–94 Peacor SD, Schiesari L, Werner EE (2007b) Mechanisms of nonlethal predator effect on cohort size variation: ecological and evolutionary implications. Ecology 88(6):1536–1547 Persson L, de Roos AM (2006) Size-structured interactions and the dynamics of aquatic systems. Pol J Ecol 54:621–632 Persson L, Greenberg LA (1990) Interspecific and intraspecific size class competition affecting resource use and growth of perch, Perca fluviatilis. Okios 40:197–206 Persson L, Leonardsson K, de Roos AM, Gyllenberg M, Christensend B (1998) Ontogenetic scaling of foraging rates and the dynamics of a size-structured consumer-resource. Theor Popul Biol 54(3): 270–293 Persson L, De Roos AM, Claessen D, Bystrom P, Lovgren J, Sjogren S, Svanback R, Wahlstrom E, Westman E (2003) Gigantic cannibals driving a whole-lake trophic cascade. Proc Nat Acad Sci USA 100(7):4035–4039 Peters RH (1983) The ecological implications of body size: Cambridge studies in ecology. Cambridge University Press, New York Pinheiro J, Bates D, DebRoy S, Sarkar D, The R Development Core Team (2012) nlme: linear and nonlinear mixed effects models. R package version 3.1–103 R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0, http://www.R-project.org Roberts WE (1994) Evolution and ecology of arboreal egg-laying frogs. PhD dissertation, University of California, Berkeley Rudolf VHW (2008a) Consequences of size-structure in the prey for predator-prey dynamics: the composite functional response. J Anim Ecol 77:520–528 Rudolf VHW (2008b) Impact of cannibalism on predator-prey dynamics: size-structured interactions and apparent mutualism. Ecology 86:1650–1660
Samhouri JF, Steele MA, Forrester GE (2009) Inter-cohort competition drives density dependence and selective mortality in a marine fish. Ecology 90:1009–1020 Schroder A, Nilsson KA, Persson L, van Kooten T, Reichstein B (2009) Invasion success depends on invader body size in a sizestructured mixed predation-competition community. J Anim Ecol 78:1152–1162 Sebens KP (1982) The limits of indeterminate growth: an optimal size model applied to passive suspension feeders. Ecology 63: 209–222 Smith CK (1990) Effects of variation in body size on intraspecific competition among larval salamanders. Ecology 71:1777–1788 Steiner UK (2007) Linking antipredator behaviour, ingestion, gut evacuation and costs of predator-induced responses in tadpoles. Anim Behav 74:1473–1479 Sundell J, Norrdahl K (2002) Body size-dependent refuges in voles: an alternative explanation of the Chitty effect. Ann Zool Fenn 39:325–333 Van Buskirk J (2001) Specific induced responses to different predator species in anuran larvae. J Evol Biol 14:482–489 Van Buskirk J, McCollum SA, Werner EE (1997a) Natural selection for environmentally induced phenotypes in tadpoles. Evolution 51:1983–1992 Van Buskirk J, McCollum SA, Werner EE (1997b) Natural selection for environmentally induced phenotypes in tadpoles. Evolution 51:1983–1992 Vonesh JR, Bolker BM (2005) Compensatory larval responses shift trade-offs associated with predator-induced hatching plasticity. Ecology 86:1580–1591 Wang P, Stieglitz T, Zhou DW, Cahill JF (2010) Are competitive effect and response two sides of the same coin, or fundamentally different? Funct Ecol 24(1):196–207 Warkentin KW (1995) Adaptive plasticity in hatching age: a response to predation risk trade-offs. Proc Natl Acad Sci USA 92:3507– 3510 Warkentin KW (2005) How do embryos assess risk? Vibrational cues in predator-induced hatching of red-eyed treefrogs. Anim Behav 70:59–71 Warkentin KW (2011) Plasticity of hatching in amphibians: evolution, trade-offs, cues and mechanisms. Integr Comp Biol 51: 111–127 Wassersug RJ, Rosenberg K (1979) Surface anatomy of branchial food traps of tadpoles: a comparative study. J Morphol 159: 393–425 Werner EE (1988) Size, scaling and the evolution of life. In: Ebenman B, Persson L (eds) Size-structured populations: ecology and evolution. Springer, Heidelberg, pp 60–81 Werner EE (1994) Ontogenetic scaling of competitive relations: sizedependent effects and responses in two anuran larvae. Ecology 75:197–213 Werner EE, Anholt BR (1996) Predator-induced behavioral indirect effects: consequences to competitive interactions in anuran larvae. Ecology 77:157–169 Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425 Wilbur HM (1984) Complex life cycles and community organization in amphibians. In: Price PW, Slobodchikoff CW, Gaud WS (eds) A new ecology: novel approaches to interactive systems. Wiley, New York, pp 195–224 Wilbur HM (1988) Interactions between growing predators and growing prey. In: Ebenmann B, Persson L (eds) Size-structured populations: ecology and evolution. Springer, Berlin, pp 157–182
123
