Body size is a key trait of individuals and is known to influence the type and strength of species interactions (De Roos, Persson & McCauley 2003a; Yang & Rudolf 2010). In natural communities, the size distribution of predators commonly differs between communities and within a season. However, the consequences of variation in the size distribution of predator communities on predator–prey dynamics are not well understood. Here, I show the per-capita strength of prey suppression is altered by seasonal changes in mean predator (cannibal) size but also through changes in the size distribution within a predator population. This suggests that seasonal variation within a single trait, body size, can influence predator–prey dynamics in natural communities.
Average Predator Size and Prey Mortality
The relative difference in body size between a predator and its prey is known to be a key factor in determining per-capita predation rates (e.g. Thompson 1975; Wahlstrom et al. 2000; Aljetlawi, Sparrevik & Leonardsson 2004; Brose et al. 2008; Rudolf 2008a). This would suggest that changes in mean body size of predators are also likely to alter the strength of top-down control imposed by predators on their prey. Although laboratory experiments clearly indicated that per-capita predation rates increased with predator size and significantly differed between predator size classes (Fig. 2), prey mortality did not consistently increase with average predator size in the field and was similar among treatments with the two largest size classes (Fig. 3a). While predation rates are expected to be lower in the field compared to laboratory experiments (e.g. owing to more complex habitat structure and alternative food in the field), the question is why the relative differences between size classes disappeared.
Although it is possible that the increased variation in mortality reduced statistical power to detect a difference, effect size (i.e. mean difference) between the two largest predator size classes was very small. In addition, when considering both single and mixed sized predator treatments, mortality did not consistently increase with the average size of the predator within treatments either (Fig. 3a) but instead peaked when all three predatory size classes were present. It is possible that the interference among similar sized individuals in the field reduced per-capita predation rates. Recent experiments suggest that interference among similar sized predators may increase with absolute size (V. H. W. Rudolf, unpublished data), which would reduce the differences in prey mortality between treatments with different size classes in the field. However, it is unlikely to explain why mortality rates were highest when all three size classes were present and not when only large predators were present. This suggests that changes in the distribution of predator body sizes were also an important component determining the effect of predators on prey survival. The study was designed to mimic natural seasonal changes in body size distribution within a predator population and not to explicitly compare the relative effects of changing the mean and distribution of sizes of predators or how both variables interact. This will require future studies that manipulate both statistics independently. Nonetheless, the results clearly indicate that given a fixed predator density, changing the size structure within a predator population can alter prey suppression through changes in the mean size and size distribution of predators.
Seasonal Changes in Variation of Predator Body Sizes
Mortality rates of the prey were significantly altered by changes in the predator size distribution, clearly indicating the importance of seasonal shifts in predator body size composition. However, the pattern did not simply follow a general increase in average size of predators (Fig. 3a). Instead, contrary to the expectations, mortality rates peaked when all three predator size classes were present. In addition, mortality rates in this treatment were significantly higher than expected based on the individual effects of each size class, indicating that size classes were not substitutable. This indicates an increase in prey suppression with higher body size diversity. The finding seems to be contradictory to results from other studies and my laboratory experiment. In previous studies on odonates, predatory crabs and salamanders, pairing two different size classes always resulted in lower prey mortality rates than expected based on individual effects, irrespective of whether the small size class consisted of conspecifics or heterospecifics (Crumrine 2005, 2010; Griffen & Byers 2006; Rudolf 2006). In all four studies, the authors argue that risk of predation (or cannibalism) increases within the predators when two different size classes are present, resulting in concurrent behavioural changes (i.e. anti-predator behaviour) in the smaller size class that led to the lower-than-expected prey mortality. Consistent with these studies, my laboratory experiment indicated strong behavioural effects; the presence of a large size class dramatically reduced predation rates of smaller predators. In addition, the probability of cannibalism is known to increase with increasing size differences between individuals in the study species (see Results) (Wissinger 1988, V. H. W. Rudolf, unpublished data). Cannibalism among large cannibalistic size classes was also present in the field experiment, although cannibalism rates did not differ between treatments. Why then were prey mortality rates higher than expected when all three size classes were present?
Increasing the size range within predators can have at least three key effects besides altering mean size (Fig. 1): (i) it could alter behavioural interference among predators altering the per-capita predation rate of individuals (i.e. non-consumptive indirect effects), (ii) it could alter the rate of predation within the predator community (i.e. large predators cannibalizing small predators), leading to indirect ‘consumptive effects’ (consumptive mediated indirect effects), and (iii) it could increase top-down control if different sized predators have different feeding niches. In the field experiment, interference between predators was present (i.e. cannibalism occurred), and the laboratory experiment indicated that smaller predators alter their behaviour and consumption rates in the presence of large predators. Yet, the higher-than-expected prey mortality at the highest body size diversity suggests that both factors did not substantially reduce prey mortality. It is however possible that behavioural interactions between different size classes increased prey mortality. For example, previous studies (Ferris & Rudolf 2007; Rudolf 2008b) indicated that small predators alter their behaviour in the presence of larger conspecifics. If large predators caused changes in the spatial dispersion of small predators and prey or cause both to use the same refuge/microhabitat, this would increase encounter rates among small predators and prey.
It is also possible that interference is stronger within size classes than between size classes. In that case, reducing the density within a size class would result in an increase in the per-capita predation rate of individuals, leading to higher-than-expected prey mortality (Greig & Wissinger 2010). Given the substitutive experimental design in this experiment, which held total density constant, this scenario would also result in an increase in consumption rate in the mixed predator treatment. However, given that large predators strongly reduced foraging rates of small predators in the laboratory experiment, we would expect that this increase in foraging rate would only occur in the largest predator size class.
Alternatively, niche complementarity (i.e. differences in feeding niches) among different sized predators could have been responsible for increased prey mortality. Previous studies suggest that risk enhancement (i.e. higher-than-expected prey mortality) can arise when predators differ in their microhabitat use (Soluk & Collins 1988; Schmitz 2007). Thus, if different sized predators inherently use different microhabitats, this could explain why the observed mortality was higher than expected when multiple predator size classes were present. Unfortunately, it was not feasible to test for differences in microhabitat use as larvae bury in the substrate and are typically impossible to see in the field experimental set-up. However, different sized individuals often vary in habitat use (e.g. Werner & Hall 1988; Persson & Eklov 1995; Biro, Post & Parkinson 2003; Rudolf 2006; Rudolf & Armstrong 2008), so it is plausible that this could have been the case in this study as well.
Finally, differences in feeding niches may arise because predation rates vary with the relative body size of predators and prey. In most species, optimal attack rates and preferences change with relative size differences of predator and prey (e.g. Thompson 1978; Mittelbach 1981; Aljetlawi, Sparrevik & Leonardsson 2004). Thus, given a sufficient size distribution in the prey, increasing the size range of predators is likely to increase prey mortality. In this scenario, one would expect that (i) the mean size and size distribution of the prey differ between treatments with single sized predators and (ii) the skewness of prey sizes should differ between treatments with single or multiple size classes. While results indicated significant treatment effects on prey size structure, only the maximum prey size differed between treatments. As expected, maximum prey size decreased as predator size increased when only one predator size class was present. However, maximum prey size was higher in all treatments with mixed predator size classes than in any single predator size class. There was no difference in minimum prey size, skewness or mean prey size among predator treatments. Thus, there is some limited evidence that different sized predators may favour different prey sizes. Although the signal seems weak, this may partly explain why prey mortality was higher than expected when all predator size classes were present. While there was some size variation in the prey, the size range in the prey had to be constrained to avoid cannibalism within the prey. A larger prey size range may have increased predator niche complementarity and resulted in higher prey mortality in mixed predator treatments. Irrespective of the underlying mechanisms, the results clearly show that increasing the size range within predators can increase prey mortality. This suggests that we cannot simply predict prey mortality based on the average body size of predators. Instead, we also need to account for the size distribution within predators.
While the present study used seasonal variation in size within a cannibalistic population as a model system, it is likely that the results apply to many other systems where body size differs between predator species. Empirical data indicate that the ecological variation among size classes within species is often similar or larger than ecological differences between similar sized species within a predator community (Polis 1984; Munoz & Ojeda 1998; Woodward & Hildrew 2002; Rudolf & Armstrong 2008). Focusing on size variation within a species has the benefit that size is the main factor that varies, while most other traits (e.g. general morphology or feeding mode) remain constant. Using different sized species would introduce additional differences between predators, which would make it more difficult to isolate the single effects of body size. However, species may differ in their anti-predator behaviour [including showing no anti-predator response (Greig & Wissinger 2010)], or individuals may respond differently to intra- vs. interspecific predators (Ferris & Rudolf 2007; Rudolf & Armstrong 2008), which could lead to different indirect interactions and thus consequences of increasing the size variation within a predator community than what I observed in this study. Thus, the next important step will be to test whether the findings of this study hold true across species that differ in other aspects of their biology and whether size variation remains an important predictor despite these differences. Ecologists increasingly recognize that average body size of individuals or species determines dynamics of predator–prey interactions, the stability of complex food webs and dynamics of entire ecosystems (Brose, Williams & Martinez 2006; e.g. De Roos & Persson 2002; De Roos, Persson & Thieme 2003b; De Roos et al. 2008; Otto, Rall & Brose 2007; Rudolf 2007a,b). The current study suggests that variation in body size could also be an important conduit that links the effects of changing biodiversity to the functioning of ecosystems.
Classical unstructured predator–prey models assume that the per-capita interaction strength among species is constant. However, almost all species grow during the course of a season. Previous studies have demonstrated that seasonal changes in body size can alter the strength or even the type of species interactions (reviewed in Yang & Rudolf 2010). This study extends previous research by demonstrating that seasonal variation in the size structure of predators can alter the interaction strength between predators and prey, and the effects often cannot be predicted by averaging among size classes. Thus, seasonal changes may result in nonlinear dynamics that cannot be predicted by the average body size during a season. Given the importance of the strength of species interactions for dynamics and stability of complex communities (McCann, Hastings & Huxel 1998), this suggests that seasonal variation in size structure can have important implications for the dynamics of natural communities.