Foraging Trade-Offs Along a Predator–permanence Gradient in Subalpine Wetlands

Abstract

We conducted a series of field and laboratory experiments to determine the direct and indirect effects of a top predator, the tiger salamander (Ambystoma tigrinum nebulosum), on larvae of two species of limnephilid caddisflies (Limnephilus externus and Asynarchus nigriculus) in subalpine wetlands in central Colorado. Asynarchus larvae predominate in temporary wetlands and are aggressive intraguild predators on Limnephilus larvae, which only predominate in permanent basins with salamanders. We first conducted a field experiment in mesocosms (cattle tanks) to quantify the predatory effects of different life stages of salamanders on the two caddisfly species. Two life stages of the salamanders (larvae and paedomorphs) preferentially preyed on Asynarchus relative to Limnephilus. Subsequent laboratory experiments revealed that high Asynarchus activity rates and relatively ineffective antipredatory behaviors led to higher salamander detection and attack rates compared to Limnephilus. In a second field experiment (full factorial for presence and absence of each of the three species), we found that salamander predation on Asynarchus had an indirect positive effect on Limnephilus: survival was higher in the presence of salamanders ϩ Asynarchus than with just Asynarchus. In the laboratory we compared the predatory effects of salamanders with and without their mouths sewn shut and found the observed indirect positive effect on Limnephilus survival to be mainly the result of reduced numbers of Asynarchus rather than salamander-induced changes in Asynarchus behavior. We argue that indirect effects of predator-predator interactions on shared prey will be mainly density-mediated and not trait-mediated when one of the predators (in this case, Asynarchus) is under strong selection for rapid growth and therefore does not modify foraging behaviors in response to the other predator. The reciprocal dominance of Limnephilus and Asynarchus in habitats with and without salamanders probably reflects a tradeoff between competitive superiority and vulnerability to predation. The high activity levels and aggressiveness that enable Asynarchus to complete development in temporary habitats result in strong asymmetric competition (via intraguild predation) with Limnephilus. In permanent habitats these same behaviors increase Asynarchus vulnerability to salamander predation, which indirectly benefits Limnephilus. This and previous work implicate salamanders as keystone predators that exert a major influence on the composition of benthic and planktonic assemblages in subalpine wetlands.

Consumptive effects of fish reduce wetland crayfish recruitment and drive species turnover

“…This interpretation was supported by the signiWcant eVect of sunWsh on P. fallax density and biomass in the second experiment (2010) when only P. fallax juveniles were stocked in the experimental wetlands. Wissinger et al (1999b) demonstrated that the caddisXy Asynarchus nigriculus inhabiting temporary subalpine wetlands excludes slower growing caddisXies by intraguild predation; and we note it is also possible that P. alleni may prey upon P. fallax, but that interaction remains to be studied. EVects of predators on prey populations and communities are manifested via both consumptive and non-consumptive mechanisms (Preisser et al 2005).…”

“…In contrast, invertebrate communities inhabiting longer-hydroperiod habitats, where Wsh or salamanders are the top predators, tend to lack the largest predatory invertebrates, and are dominated by species with relatively lower activity levels (with lower growth rates) and potentially smaller sizes that make them less vulnerable to fast-moving visual vertebrate predators (Wellborn et al 1996;McCauley 2008). A byproduct of these correlations is the observation that predatory interactions between vertebrate predators and invertebrate species with which they do not coexist tend to be stronger than interactions between those predators and coexisting species (Wellborn et al 1996;Wissinger et al 1999b; Garcia and Mittelbach 2008). Recent studies suggest that the presence of large-bodied Wshes may be more important than Wsh presence (i.e., small or large-bodied Wsh) for determining the life histories of co-existing invertebrates (Dorn 2008;McCauley 2008;McCauley et al 2008).…”

A growth/mortality trade-off in larval salamanders and the coexistence of intraguild predators and prey

“…Two recent studies of invertebrates (Wissinger et al 1999;Suhling 2001) have also demonstrated that intraguild predators are more active and experience higher top predator-imposed mortality than their intraguild prey. The potential for top predators to influence coexistence in many systems with IGP through density-mediated effects deserves further investigation in a variety of taxa to assess whether this may be a general pattern.…”

“…A recent study by Wissinger et al (1999) makes a compelling case for the importance of top predators in influencing coexistence between intraguild predators and prey. In this study, a caddisfly intraguild predator (Asynarchus) was more active and aggressive than its intraguild prey (the caddisfly Limnephilus), giving it a competitive advantage.…”

“…By preferentially consuming Asynarchus, the salamander predator facilitated the persistence of Limnephilus with its competitive superior. Understanding the effects of a top predator on intraguild predators and prey enabled the investigators to explain shifts in the relative abundance of the two caddisfly species across the range of wetlands where they were observed (Wissinger et al 1999). The key to their study, and to future studies on IGP, lies in focusing on the traits of intraguild predators and prey and their consequences to interactions with other species to elucidate the mechanisms underlying their performance in different contexts.…”