Sublethal predators and their injured prey: linking aquatic predators and severe limb abnormalities in amphibians

Abstract

While many predators completely consume their prey, others feed only on blood or tissue without killing the prey, sometimes causing ecologically significant levels of injury. We investigated the importance of sublethal predator attacks in driving an emerging issue of conservation importance: missing-limb deformities in amphibians. We combined long-term field data and manipulative experiments to evaluate the role of sublethal predation in causing abnormalities in two regions of central Oregon, U.S.A. Since 1988, western toads (Bufo boreas) in Lake Aspen have exhibited abnormalities dominated by partially missing limbs and digits at annual frequencies from <1% to 35%. On Broken Top volcano, we found comparable types and frequencies of abnormalities in Cascades frogs (Rana cascadae). Field sampling and observational data implicated two aquatic predators in these abnormality phenomena: introduced sticklebacks (Gasterosteus aculeatus) at Lake Aspen and corduliid dragonfly larvae (Somatochlora albicincta) at Broken Top. In experiments, these predators produced limb abnormalities identical to those observed in the respective regions. At Lake Aspen, in situ predator exclosures effectively eliminated abnormalities in toads, while comparisons among years with low and high stickleback abundance and between wetlands with and without sticklebacks reinforced the link between fish and amphibian abnormalities. Neither trematode parasite infection nor pesticide contamination could explain observed abnormalities. Our results suggest that predators are an important explanation for missing-limb abnormalities and highlight the ecological significance of sublethal predation in nature.

Community ecology of invasions: direct and indirect effects of multiple invasive species on aquatic communities

“…The lack of predation on toads is likely due to chemical protection, which often protects bufonid larvae from fish (Kruse and Stone 1984). The sublethal injuries caused by mosquitofish also support the role of predators in contributing to missing-limb abnormalities in amphibians (Bowerman et al 2010). Finally, newts were unaffected by bullfrog larvae, likely because direct competition for food resources and indirect effects were minimal (i.e., bullfrogs did not deplete resources that altered newt prey availability).…”

From a local observation to a European-wide phenomenon: Amphibian deformities at Serra da Estrela Natural Park, Portugal

“…This is not an outlying hypothesis since selective predation by dragonfly nymphs and other aquatic predators has been associated with the most common kinds of limb deformities found in natural populations of anurans (Ballengée Sessions, 2009). Moreover, Odonata nymphs of various species, which have been indicated as predictors of skeletal abnormality frequency (Ballengé Sessions, 2009;Bowerman et al, 2010;Reeves et al, 2010), and diving beetles (Dysticidae), are abundant in Serra da Estrela, particularly in the surveyed sites (Rosa et al, 2012). Interspecific predation on adult L. bo scai by T. m arm o ratus has also been observed at Folgosinho (Baptista et al, 2015), reinforcing the idea of predation as a key stressor in these habitats.…”

Abnormalities in amphibian populations inhabiting agroecosystems in northeastern Buenos Aires Province, Argentina

“…Parasitic infection is probably the most thoroughly studied cause of amphibian malformation thus far, and the trematode Ribeiroia is correlated with high prevalence of abnormal limbs (Johnson et al 2003). Additionally, growing evidence suggests that predators can increase the susceptibility of tadpoles to developmental abnormalities (Bowerman et al 2010, Michel & Burke 2011. This ecological interaction often amplifies the negative effects of environmental conditions, such as pesticide exposure (Relyea 2004(Relyea , 2005.…”