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

Sunriver Nature Center, Box 3533, Sunriver, Oregon 97707, USA.
Ecology (Impact Factor: 4.66). 01/2010; 91(1):242-51. DOI: 10.1890/08-1687.1
Source: PubMed


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.

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    • "There are numerous abiotic and biotic factors that may deteriorate the condition of animals and thus may shape the hostparasite interactions. Especially, sub-lethal effects of predators may greatly worsen the condition of the host (Vermeij, 1982; Bowerman et al., 2010). One of the best examples of this phenomenon is autotomy in some lizards species. "
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    ABSTRACT: The success of ectoparasites depends primarily on the site of attachment and body condition of their hosts. Ticks usually tend to aggregate on vertebrate hosts in specific areas, but the distribution pattern may depend on host body size and condition, sex, life stage or skin morphology. Here, we studied the distribution of ticks on lizards and tested the following hypotheses: occurrence or high abundance of ticks is confined with body parts with smaller scales and larger interscalar length because such sites should provide ticks with superior attachment conditions. This study was performed in field conditions in central Poland in 2008-2011. In total, 500 lizards (Lacerta agilis) were caught and 839 ticks (Ixodes ricinus, larvae and nymphs) were collected from them. Using generalized linear mixed models, we found that the ticks were most abundant on forelimbs and their axillae, with 90% of ticks attached there. This part of the lizard body and the region behind the hindlimb were covered by the smallest scales with relatively wide gaps between them. This does not fully support our hypothesis that ticks prefer locations with easy access to skin between scales, because it does not explain why so few ticks were in the hindlimb area. We found that the abundance of ticks was positively correlated with lizard body size index (snout-vent length). Tick abundance was also higher in male and mature lizards than in female and young individuals. Autotomy had no effect on tick abundance. We found no correlation between tick size and lizard morphology, sex, autotomy and body size index. The probability of occurrence of dead ticks was positively linked with the total number of ticks on the lizard but there was no relationship between dead tick presence and lizard size, sex or age. Thus lizard body size and sex are the major factors affecting the abundance of ticks, and these parasites are distributed nearly exclusively on the host's forelimbs and their axillae.
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    • "Several explanations are possible for the morphological anomalies found in the present study. Because the most frequent anomaly was the loss of hindlimbs, it is possible that anomalies were related to predator attack of juveniles and adults (Bowerman et al. 2010; Johnson and Bowerman 2010). Potential predators include birds (egrets, herons, storks, Kestrel, Falco tinnunculus, and Red-footed Falcon, Falco vespertinus), the European Pond Terrapin (Emys orbicularis), predatory fish, and aquatic arthropods (coleopterans, hemipterans, crayfish). "
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    • "However, an underappreciated but ecologically important effect of predators is sublethal predation. Predators often times only damage prey, which can have lasting impacts on morphology and life-history [15]–[17]. Perhaps the most well known examples of sublethal predation are lizards which autotomize their tails to escape predators [18], [19]. Although the lizard may survive the initial attack, the loss of the tail can decrease locomotor performance, reduce reproductive output and growth rate, and compromise foraging ability [19]. "
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