The view defended in this book is that the "null model" that most ecologists tend to use is inappropriate because it assumes that the amount of prey consumed by each predator is insensitive to the number of conspecifics. The authors argue that the amount of prey available per predator, rather than the absolute abundance of prey, is the basic determinant of the dynamics of predation.
This so-called ratio dependence is shown to be a much more reasonable "null model. Food Chain Equilibria. His theoretical and experimental work is focused to basic questions of predation dynamics and applied work addresses agroecological problems. Lev R. Each mesocosm began with 10 tadpoles per species and therefore mesocosms with A.
This additive design provides a direct test for interspecific competition Underwood, ; Gomez-Mestre and Tejedo, Figure 1. Configuration of the experimental setup used to examine the relative effects of competition and predation on a tropical anuran guild. We also tested the effect of two types of predators dragonfly larvae and water bug on amphibian larvae.
We presented the predators either free uncaged; marked in blue or caged marked in red to test for consumptive and non-consumptive effects of these predators. The experiment lasted 4 weeks and at the end we recorded survival and growth of amphibians, time to and size at metamorphosis, and took tissue samples for isotopic analysis.
All tadpole photos by JT. Our experimental mesocosms were arranged in an open field next to secondary forest and consisted of L round plastic tanks 0. One month before the start of the experiment we added an even mixture of loosely packed dry soil and leaf litter ca. All amphibian and predator species are known to occur in this pond.
We covered the tanks with window screen to prevent colonization by unwanted organisms and allowed rainwater to fill the tanks at the beginning of the experiment. This process allowed a natural food base for the aquatic community to develop, thereby mimicking the conditions of many ponds in the area. To provide spatial complexity, we added three plastic pots containing plants transplanted from Bridge Pond.
Each pot contained four individual plants. The plants were completely submerged beneath the surface of the water but grew and were alive throughout the entire experiment. Since our tanks contained a mixture of vegetation and soil and had been allowed to fill naturally, they contained a substantial amount of visible periphyton at the start of the experiment.
No supplementary food was added to mesocosms during the experiment and tadpoles consumed only what had developed naturally. Each tank contained one predator cage made of a fine mesh that was suspended at the top of the water column on a side of each tank. All cages contained a stick for predators to perch on. Identical empty cages were included in tanks lacking a caged predator treatment. Dragonfly larvae and adult water bugs were collected from ponds in the area and haphazardly assigned to either free or caged predator treatment.
We introduced one predator in each predator cage or left them empty according to the assigned treatment. The average body length of dragonflies was Caged predators were fed every other day with two tadpoles of any one of the five amphibian species included in the experiment, selected on a rotating basis, to ensure consistent alarm cues Peacor, We replaced predators that died as necessary. To ensure that all eggs would hatch at approximately the same time, we collected clutches of A. This allowed all tadpoles to be essentially the same age post-hatching 2 days at the start of the experiment.
All tadpoles and predators were dorsally photographed just before introducing them into the mesocosms. From the first day of the experiment we checked the tanks daily and from the day we found the first metamorph we checked the tanks for metamorphs twice a day. The experiment lasted for 4 weeks and we removed the remaining tadpoles and predators with dip nets between 10 and 13 July.
Immediately upon removal, we individually photographed tadpoles and recorded body mass. All photographs included a ruler for scaling the image and to obtain measurements of predators' body length and tadpoles' body length and total length TL, body plus tail. For individuals that had already metamorphosed, we recorded snout-vent length SVL. Photographs were measured using the program ImageJ 1. Initial total length was At the end of the experiment, all individuals not used for stable isotope analyses were released at the site of collection.
We performed analyses of stable isotopes on one individual per species per tank when available, from 6 of the experimental blocks. We obtained isotopic data from a total of tadpoles A. The isotopic signature does not differ between tadpoles and newly metamorphosed juveniles, because amphibians do not feed during metamorphosis Arribas et al. We also sampled possible food sources i. Weighed samples 0. We conducted all statistical analysis using R 2. We used generalized linear mixed models glmer function in package lme4 to analyze effects of the different treatments on 1 survival, 2 size total length, TL , and 3 diet of amphibians.
We first performed an overall model including the three-way interaction among competition with A. Experimental block was included as a random factor for survival and diet analyses. Block and tank within block were included as random factors for size analyses. In all models described below, we used likelihood ratio tests to evaluate the significance of each predictor.
We analyzed tadpole survival with generalized linear mixed models fitting a binomial error distribution using a logit link function, and analyzed tadpole size and diet stable isotope data fitting a Gaussian error distribution. We assessed model fits using qq-plots and ensured that models were not overdispersed.
When appropriate, assumptions of normality and homoscedascity of errors were assessed by means of Shapiro-Wilks and Bartlett tests respectively. Since we found significant two- and three-way interactions in the overall model see section Results , we conducted several subsequent analyses to tease apart the effects of competition from predation. First, we evaluated the competitive effect of A. Second, in tanks containing A. Third, in the event of a significant interaction between predator treatment and amphibian species, we performed contrast analyses to examine differences between types of predators dragonfly vs.
Given that these multiple comparisons were at times not orthogonal, we corrected the P -values to minimize the false discovery rate FDR; Benjamini and Hochberg, The FDR is a simple and powerful method for controlling type I error when multiple comparisons are carried out Verhoeven et al. We tested if the initial length of tadpoles explained differential survival among species, using tank means of initial total length for each species.
We analyzed each species size using measurements of tadpoles' total length final TL, in mm , from the photographs taken at the end of the experiment, and including initial body length mean per tank and per species as a covariate in the model to control for initial differences in body size. In testing for differences in isotopic signatures, we first tested for an association between tadpole size TL and isotopic values for each species using linear regressions.
Lastly, we performed the above analyses on each species separately to test the effect of competition from A. We occasionally found undesired dragonflies in our mesocosms at the end of the experiment, presumably introduced with the sediment or leaf litter. Based on external morphology of the nymphs, these dragonflies were from the family Gomphidae and are not reported to feed on tadpoles known diets include midge larvae and oligochaete worms; Mahato and Johnson, ; Alzmann et al. Gomphidae dragonfly nymphs are bottom dwellers with relatively poor eyesight compared with more active predatory species like Anax Corbet, Gomphid nymphs were relatively evenly distributed throughout the experiment, occurring in 17 of our 80 mesocosms, and never in more than three mesocosms from any given treatment.
When they did occur, they were generally sparse mean number of individuals per mesocosm: 3.
Prey: predator ratio dependence in the functional response of a freshwater amphipod
Statistical results for the effects of competition and either caged or uncaged predators on amphibian survival, size and stable isotopes are shown in Table 1. Magnitude and effect sizes for effects of competition and predation on survival, size, and stable isotopes are shown in Table 2. Table 1. Community responses for survival, final total length and stable isotopes to competition and predation.
Table 2. Magnitude and effect size of competition and predation on survival, size, and stable isotopic values of the amphibian community.
In the absence of predators, competition from A. Both free water bugs and free dragonfly larvae, however, greatly reduced tadpole survival. Dragonfly predation varied greatly among amphibian species: E. Water bugs also negatively impacted tadpole survival, although their effect was less marked than that of dragonflies; the most affected species was E. Figure 2. Treatments with water bugs WB are represented with squares and dragonflies D are represented with triangles.
Open white symbols and dashed lines represent caged predators and red filled symbols represent free predators. Caged predators did not significantly affect amphibian survival.
Although species survival varied overall Figure 2 , survival was unaffected by the presence of caged dragonflies or water bugs Table 1 and Appendices 1, 2 in Supplementary Material. We excluded E. In the absence of predation, the largest tadpoles at the end of the experiment were A. Mean size of each species after four weeks is given in Appendix 1 Table A1 in Supplementary Material.
In this predator-free scenario, the presence of A. Only D. The effect of predation on growth was nevertheless stronger than the effect of competition, as indicated by their effect sizes Table 2.
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Figure 3. In general, the two predators exerted opposing effects, with free dragonflies increasing size of all species, whereas free water bugs reduced size of all species. For example, D. When analyzing each species separately Appendix 2 in Supplementary Material we observed that the effect of uncaged dragonflies was highly significant on the size of S.
Lastly, predator effects were not uniform across amphibian species, as E. When looking at species individually Appendix 2 in Supplementary Material , we observed that caged dragonflies had a significant effect on the size of D. Figure 4. For example, in the absence of predators A. In general, the sole effect of competition on the isotopic signature of tadpoles was negligible except for D.
Table 3. Total body length TL of all species except E. In particular, D. Figure 5. Competition and predation are two key factors influencing the structure and dynamics of ecological communities Paine, ; Vellend, ; Arribas et al. These two factors often occur at the same time and the mere presence of predators or competitors, in addition to their density-dependent effects on prey, may force organisms with phenotypic plasticity to shift aspects of their phenotype e.
The relative importance of competition and predation is largely dependent upon factors such as biogeography, the type of predators and competitors, whether the habitat is permanent or ephemeral, or the degree of niche segregation Azevedo-Ramos et al. In our experiment, we quantified the effects of predation and competition on the trophic ecology of a Neotropical larval amphibian guild and found that predators generally had much stronger effects on growth, survival and feeding ecology than competitors. Predators can differentially affect prey survival and alter their growth trajectories by non-randomly consuming individuals of different size classes Claessen et al.
Moreover, these effects of predators often have cascading consequences for community structure Post et al. We observed interspecific competition in our system, although it was rather asymmetrical across species. Agalychnis callidryas tadpoles were the largest in our experiment, and we expected all other species to experience detrimental effects from competition with them. However, only D. Counterintuitively, the size of D. This indicates that A. Nevertheless, we found that predation played a more important role than competition in shaping the structure of our tropical tadpole guild, including effects on prey growth, survival and feeding niche.
Freely roaming predators greatly reduced survival of all amphibian species. Dragonfly nymphs had a very strong impact, reducing survival of three species E. Water bugs were less effective predators than dragonflies, preferentially consuming E. Most individuals of E. This seems particularly likely since water bugs generally forage at the top of the water column while E. It is not uncommon for two predators in the same environment to have substantially different effects on prey species Atwood et al.
Given the strong predation effects previously documented on A. For example, dragonflies rapidly decimated D. In view of these results, it is clear that realistic estimates of predation rates need to take into account other biotic elements of the natural community. Direct consumption is not the only way that predators can affect community structure Hammill et al.
Predators can have many non-lethal, indirect effects on morphology, behavior, or life history which also have important consequences for community dynamics Lima, ; Agrawal, The non-lethal presence of caged dragonflies reduced tadpole growth in most species, as the perceived risk of predation through chemical cues typically causes reduced activity and lower metabolism Van Buskirk and Yurewicz, ; Werner and Peacor, We did not detect indirect effects of water bugs, although phenotypic responses to these predators have been seen in other studies McIntyre et al.
We used stable isotope analyses to assess the realized feeding niche of each member of our tadpole community. Stable isotopes constitute a valuable tool to evaluate the trophic status of individuals, and represent the combination of food sources an organism has accumulated over time Kilham et al.
Stable isotopes helped us identify that tadpoles altered their trophic status in response to the presence of predators and competitors, although different species responded in different ways. For example, both types of free roaming predators caused D. In a freshwater food web similar to ours, a shift to a higher trophic level was seemingly due to an increased proportion of zooplankton in the diet Costa and Vonesh, a. However, in species such as D. Predator effects on A. Similarly, competition with A.
Thus, the same predator or competitor can have very different, even opposing, effects on different species. These effects may stem from adaptive shifts of the different tadpole species, but are more likely the direct result of changes in foraging behavior resulting from the presence of predators or competitors. However, more studies will be needed to assess this hypothesis.
Not only did competition and predation have species-specific effects, but the interaction between competition and predation differed across prey taxa as well. These effects were primarily seen for nitrogen, but one species S. An example of the interplay between predation and competition can be seen when looking at the effects of A. In the absence of predators, A. However, free water bugs removed the effect of competition and caged dragonfly nymphs reversed it.
Similarly, A. Our results demonstrate that competition and predation interact to affect feeding ecology in complex ways. Certainly thinning of dominant species drives some of these patterns, but thinning alone does not appear to fully explain our results. Clearly there are inherent interspecific differences in trophic level and feeding. For example, the two most closely related species the two Dendropsophus species fed at very different trophic levels, with D. Focused assays of feeding behavior and experimental diets to estimate discriminant factors will be needed in order to be able to relate the shift in isotopic values with changes in diet composition Caut et al.
Such a pattern likely results from changes in the relative composition of otherwise diverse diets, rather than marked shifts from one food type to another Arribas et al. In summary, we demonstrate that predation and, to a lesser extent, competition, have strong top-down effects structuring a guild of Neotropical amphibian larvae and their trophic status.
Predation and competition differentially altered growth, survival and the trophic niches of multiple amphibian species, with potential downstream ramifications for resource assimilation and energy flow between aquatic and terrestrial habitats. Longer-term studies of trophic alterations and structure in aquatic communities are needed to clarify the ecological consequences and cascading effects of amphibian losses in food webs across the world, given that they are the most endangered group of vertebrates Stuart et al.
JT and IG-M conceived the study and designed the experiment. RA and JT setup the mesocosms and collected the animals. RA conducted the experiment and collected the data. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We also thank the unconditional help in the field and experimental work from H. Lee, G. Toral, K. Warkentin, T. Hammer, P. Marting, U. Somjee, I.
Hoffmann, and any others who passed by and gave a hand. The mesocosm array was made possible by an NSF grant to K. Warkentin and J. Ackerly, D. Community assembly, niche conservatism, and adaptive evolution in changing environments. Plant Sci. Agrawal, A. Phenotypic plasticity in the interactions and evolution of species.
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