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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Available from: Tracy Bowerman, Oct 04, 2015
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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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    ABSTRACT: Many animals respond to predation risk by altering their morphology, behavior, or life-history. We know a great deal about the cues prey respond to and the changes to prey that can be induced by predation risk, but less is known about how plastic responses to predators may be affected by separate plastic responses occurring earlier in life, particularly during the embryonic period. Embryos of a broad array of taxa can respond to egg- or larval-stage risks by altering hatching timing, which may alter the way organisms respond to future predators. Using the red-eyed treefrog (Agalychnis callidryas), a model for understanding the effects of plasticity across life-stages, we assessed how the combined effects of induced variation in the timing of embryo hatching and variation in the larval predator community impacted tadpole morphology, pigmentation and swimming performance. We found that A. callidryas tadpoles developed deeper tail muscles and fins and darker pigmentation in response to fish predators, either when alone or in diverse community with other predators. Tadpoles altered morphology much less so to dragonfly naiads or water bugs. Interestingly, morphological responses to predators were also affected by induced differences in hatching age, with early and late-hatched tadpoles exhibiting different allometric relationships between tail height and body length in different predator environments. Beyond induced morphological changes, fish predators often damaged tadpoles' tails without killing them (i.e., sublethal predation), but these tadpoles swam equally quickly to those with fully intact tails. This was due to the fact that tadpoles with more damaged tails increased tail beats to achieve equal swimming speed. This study demonstrates that plastic phenotypic responses to predation risk can be influenced by a complex combination of responses to both the embryo and larval environments, but also that prey performance can be highly resilient to sublethal predation.
    PLoS ONE 06/2014; 9(6):e100623. DOI:10.1371/journal.pone.0100623 · 3.23 Impact Factor
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    • "Abnormalities observed in nature have been attributed to multiple factors, including toxicants, climate change, UVB, and pathogens (reviewed by Reeves et al. 2013). The majority of these factors are thought to cause abnormalities by disrupting limb development; however, there is growing evidence that limb abnormalities may be traced, at least in part, to how bite injuries disrupt limb regeneration (Sessions & Ruth 1990; Ballengée & Sessions 2009; Bowerman et al. 2010). "
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    ABSTRACT: Multiple factors are thought to cause limb abnormalities in amphibian populations by altering processes of limb development and regeneration. We examined adult and juvenile axolotls (Ambystoma mexicanum) in the Ambystoma Genetic Stock Center (AGSC) for limb and digit abnormalities to investigate the probability of normal regeneration after bite injury. We observed that 80% of larval salamanders show evidence of bite injury at the time of transition from group housing to solitary housing. Among 717 adult axolotls that were surveyed, which included solitary-housed males and group-housed females, approximately half presented abnormalities, including examples of extra or missing digits and limbs, fused digits, and digits growing from atypical anatomical positions. Bite injury likely explains these limb defects, and not abnormal development, because limbs with normal anatomy regenerated after performing rostral amputations. We infer that only 43% of AGSC larvae will present four anatomically normal looking adult limbs after incurring a bite injury. Our results show regeneration of normal limb anatomy to be less than perfect after bite injury.This article is protected by copyright. All rights reserved.
    06/2014; 1(3). DOI:10.1002/reg2.17
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    • "Minnesota 1 More than 5,100 403 7.9 Eaton et al., 2004 1995–1999/ 2000–2002 Alberta, Saskatchewan 1 21,050 150 0.71 Hoppe, 2005 1996–1999 Minnesota 7 796 19 a 2.4 Hoppe, 2005 1996–1999 Minnesota 1 2,828 756 26.7 Taylor et al., 2005 2002 Vermont 6 5,264 83 1.6 Skelly et al., 2007 2002–2003 Vermont 7 3,420 117 3.4 Reeves et al., 2008 2000–2006 Alaska 1 9,268 576 6.2 Bowerman et al., 2009 1988–2008 "
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