Adding Infection to Injury: Synergistic Effects of Predation and Parasitism on Amphibian Malformations

Abstract

We explored the importance of interactions between parasite infection and predation in driving an emerging phenomenon of conservation importance: amphibian limb malformations. We suggest that injury resulting from intraspecific predation in combination with trematode infection contributes to the frequency and severity of malformations in salamanders. By integrating field surveys and experiments, we evaluated the individual and combined effects of conspecific attack and parasite (Ribeiroia ondatrae) infection on limb development of long-toed salamanders (Ambystoma macrodactylum). In the absence of Ribeiroia, abnormalities involved missing digits, feet, or limbs and were similar to those produced by cannibalistic attack in experimental trials. At field sites that supported Ribeiroia, malformations were dominated by extra limbs and digits. Correspondingly, laboratory exposure of larval salamanders to Ribeiroia cercariae over a 30-day period induced high frequencies of malformations, including extra digits, extra limbs, cutaneous fusion, and micromelia. However, salamander limbs exposed to both injury and infection exhibited 3-5 times more abnormalities than those exposed to either factor alone. Infection also caused significant delays in limb regeneration and time-to-metamorphosis. Taken together, these results help to explain malformation patterns observed in natural salamander populations while emphasizing the importance of interactions between parasitism and predation in driving disease.

Individual and combined effects of multiple pathogens on Pacific treefrogs

“…Our finding that Ribeiroia delayed development of P. regilla larvae in experiment 2 is consistent with negative effects on rate of development previously found in frog and salamander larvae (Johnson et al 2006(Johnson et al , 2008Johnson and Hartson 2009). Although the effects of Ribeiroia on developmental rate are more subtle than their effects on survival and deformities, they could lead to substantial effects at the population level because they may ultimately impair survival, growth, and reproduction, as evidenced by the positive correlations found between rapid metamorphosis and adult recruitment and fitness in amphibians (Smith 1987;Semlitsch et al 1988).…”

“…Infected snails shed freeswimming Ribeiroia cercariae, which infect frog and salamander larvae and encyst as metacercariae, resulting in a variety of limb deformities, elevated mortality, delayed metamorphosis, and delayed regeneration following limb injury (Johnson et al 1999(Johnson et al , 2001(Johnson et al , 2006Kiesecker 2002;Blaustein and Johnson 2003;Schotthoefer et al 2003). Ribeiroia-associated limb deformities are widespread in the United States (Johnson et al 2002aKiesecker 2002), and qualitative evidence supports the hypothesis that the prevalence of Ribeiroia-induced limb deformities in amphibians in the western USA has recently increased Johnson and Lunde 2005).…”

It’s a predator–eat–parasite world: how characteristics of predator, parasite and environment affect consumption

“…500 μm) were less frequently consumed by both fish and larval damselflies. However, these results depended strongly on light availability; trials conducted in the dark led to significantly fewer parasites consumed overall, especially those with a size of <1,000 μm, emphasizing the importance of circadian shedding times of parasite free-living stages for or pathology (Johnson et al 2006;Keesing et al 2006;Belden and Wojdak 2011;Duffy et al 2011).…”

Beyond immunity: quantifying the effects of host anti-parasite behavior on parasite transmission

“…In tadpoles, Echinostoma infection can reduce survival, inhibit renal function, and cause edema (Fried et al 1997;Schotthoefer et al 2003;Holland et al 2007). Infection by Ribeiroia ondatrae (hereafter Ribeiroia) reduces survival and induces severe malformations, including missing limbs, skin webbings, and extra limb elements (Sessions and Ruth 1990;Johnson et al 1999Johnson et al , 2001Johnson et al , 2006Kiesecker 2002;Stopper et al 2002;Johnson and Hartson 2009). Because the severity of pathology depends on the number of parasites a host supports ("intensity-dependent pathology"; Johnson et al 1999Johnson et al , 2001Schotthoefer et al 2003;Holland et al 2007), behaviors that reduce infection may be important mechanisms to reduce disease (e.g., Kiesecker and Skelly 2000;Taylor et al 2004;Koprivnikar et al 2006).…”