Synergistic effects of predators and trematode parasites on larval green frog (Rana clamitans) survival

Parasites and predators can have complex, nonadditive effects on a shared group of victims, which can have important consequences for population dynamics. In particular, parasites can alter host traits that influence predation risk, and predators can have nonconsumptive effects on prey traits which...

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Veröffentlicht in:Ecology (Durham) 2013-12, Vol.94 (12), p.2697-2708
Hauptverfasser: Marino, John A., Werner, Earl E.
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description Parasites and predators can have complex, nonadditive effects on a shared group of victims, which can have important consequences for population dynamics. In particular, parasites can alter host traits that influence predation risk, and predators can have nonconsumptive effects on prey traits which influence susceptibility (i.e., infection intensity and tolerance) to parasites. Here, we examined the combined effects of trematode parasites (Digenea: Echinostomatidae) and odonate ( Anax ) predators on the survival of larval green frogs ( Rana clamitans ). First, in a large-scale mesocosm experiment, we manipulated the presence or absence of parasites in combination with the presence of no predator, caged predators, or free predators, and measured survival, traits, and infection. Parasites, caged predators, and free predators decreased survival, and we found a strong negative synergistic effect of parasites in combination with free predators on survival. Importantly, we then examined the potential mechanisms that explain the observed synergistic effect of parasites and predators in a series of follow-up experiments. Results of the follow-up experiments suggest that increased predation susceptibility due to elevated activity levels in the presence of free-swimming parasite infective stages (i.e., an avoidance response) is the most likely mechanism responsible for the observed synergism. These results suggest a potential trade-off in susceptibility to parasites and predators, which can drive nonadditive effects that may have important consequences for natural enemy interactions in natural populations and amphibian conservation.
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In particular, parasites can alter host traits that influence predation risk, and predators can have nonconsumptive effects on prey traits which influence susceptibility (i.e., infection intensity and tolerance) to parasites. Here, we examined the combined effects of trematode parasites (Digenea: Echinostomatidae) and odonate ( Anax ) predators on the survival of larval green frogs ( Rana clamitans ). First, in a large-scale mesocosm experiment, we manipulated the presence or absence of parasites in combination with the presence of no predator, caged predators, or free predators, and measured survival, traits, and infection. Parasites, caged predators, and free predators decreased survival, and we found a strong negative synergistic effect of parasites in combination with free predators on survival. Importantly, we then examined the potential mechanisms that explain the observed synergistic effect of parasites and predators in a series of follow-up experiments. Results of the follow-up experiments suggest that increased predation susceptibility due to elevated activity levels in the presence of free-swimming parasite infective stages (i.e., an avoidance response) is the most likely mechanism responsible for the observed synergism. These results suggest a potential trade-off in susceptibility to parasites and predators, which can drive nonadditive effects that may have important consequences for natural enemy interactions in natural populations and amphibian conservation.</description><identifier>ISSN: 0012-9658</identifier><identifier>EISSN: 1939-9170</identifier><identifier>DOI: 10.1890/13-0396.1</identifier><identifier>PMID: 24597217</identifier><identifier>CODEN: ECGYAQ</identifier><language>eng</language><publisher>Washington, DC: Ecological Society of America</publisher><subject>Amphibia. Reptilia ; Anax ; Anax spp ; Animal and plant ecology ; Animal populations ; Animal, plant and microbial ecology ; Animals ; Biological and medical sciences ; Cercariae ; Conservation ; Digenea ; Echinostomatidae ; Ecological competition ; Frogs ; Fundamental and applied biological sciences. Psychology ; General aspects ; green frog ; Infections ; Insecta ; Insecta - physiology ; Invertebrates ; Larva - parasitology ; Larva - physiology ; Larvae ; larval survival ; Longevity ; Marine ; mesocosms experiment ; natural enemies ; Nemathelminthia. 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In particular, parasites can alter host traits that influence predation risk, and predators can have nonconsumptive effects on prey traits which influence susceptibility (i.e., infection intensity and tolerance) to parasites. Here, we examined the combined effects of trematode parasites (Digenea: Echinostomatidae) and odonate ( Anax ) predators on the survival of larval green frogs ( Rana clamitans ). First, in a large-scale mesocosm experiment, we manipulated the presence or absence of parasites in combination with the presence of no predator, caged predators, or free predators, and measured survival, traits, and infection. Parasites, caged predators, and free predators decreased survival, and we found a strong negative synergistic effect of parasites in combination with free predators on survival. Importantly, we then examined the potential mechanisms that explain the observed synergistic effect of parasites and predators in a series of follow-up experiments. Results of the follow-up experiments suggest that increased predation susceptibility due to elevated activity levels in the presence of free-swimming parasite infective stages (i.e., an avoidance response) is the most likely mechanism responsible for the observed synergism. These results suggest a potential trade-off in susceptibility to parasites and predators, which can drive nonadditive effects that may have important consequences for natural enemy interactions in natural populations and amphibian conservation.</description><subject>Amphibia. Reptilia</subject><subject>Anax</subject><subject>Anax spp</subject><subject>Animal and plant ecology</subject><subject>Animal populations</subject><subject>Animal, plant and microbial ecology</subject><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Cercariae</subject><subject>Conservation</subject><subject>Digenea</subject><subject>Echinostomatidae</subject><subject>Ecological competition</subject><subject>Frogs</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>General aspects</subject><subject>green frog</subject><subject>Infections</subject><subject>Insecta</subject><subject>Insecta - physiology</subject><subject>Invertebrates</subject><subject>Larva - parasitology</subject><subject>Larva - physiology</subject><subject>Larvae</subject><subject>larval survival</subject><subject>Longevity</subject><subject>Marine</subject><subject>mesocosms experiment</subject><subject>natural enemies</subject><subject>Nemathelminthia. Plathelmintha</subject><subject>Odonata</subject><subject>odonate predators</subject><subject>Parasite hosts</subject><subject>parasite-host interactions</subject><subject>Parasites</subject><subject>Planorbella trivolvis</subject><subject>population dynamics</subject><subject>Predation</subject><subject>predator-prey interactions</subject><subject>Predators</subject><subject>Predatory Behavior</subject><subject>Rana</subject><subject>Rana clamitan</subject><subject>Rana clamitans</subject><subject>Rana clamitans - parasitology</subject><subject>Rana clamitans - physiology</subject><subject>risk</subject><subject>Snails</subject><subject>spp</subject><subject>synergism</subject><subject>synergistic effects</subject><subject>Tadpoles</subject><subject>Trematode Infections - parasitology</subject><subject>Trematode Infections - veterinary</subject><subject>trematode parasites</subject><subject>Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution</subject><issn>0012-9658</issn><issn>1939-9170</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkl1rFDEUhoMotq5e-APUgAjtxdScfE1yKUv9gIJg7YVX4WwmWWaZnRmT2db992bZtQtSwdwcQp687zl5Q8hLYBdgLHsPomLC6gt4RE7BCltZqNljcsoY8MpqZU7Is5xXrCyQ5ik54VLZmkN9SpbX2z6kZZun1tMQY_BTpkOkYwoNTkPKFPuGTimsy64JdMSEuZ1CgXraYbrFji5TCD2NaVjSs2_YI_UdrtsJ-3xO8ybdtgV6Tp5E7HJ4cagzcvPx8vv8c3X19dOX-YerCpVmddV4LhGkZqZW0fCgpJcWIAjFFVto3xhrOFjJoDaylpKzJgYrvFWLOsS6ETNyttcd0_BzE_Lk1m32oeuwD8MmO1CcCQ3S6v9AmeLSaLND3_6FroZN6ssgrkiBMEpoU6jzPeXTkHMK0Y2pXWPaOmBuF5QD4XZBlTojrw-Km8U6NPfkn2QK8O4AYPbYxYS9b_ORM0wLw0Th9J67a7uw_beju5z_4AyElcC5tjuDV_uLq1xyPgqL0gDAbpo3-_OIg8NlKuY310VBl09kaw3s-Co4bcehdyHjg5M-QN13NTbRTb8m8RulXdD1</recordid><startdate>201312</startdate><enddate>201312</enddate><creator>Marino, John A.</creator><creator>Werner, Earl E.</creator><general>Ecological Society of America</general><general>ECOLOGICAL SOCIETY OF AMERICA</general><scope>FBQ</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope></search><sort><creationdate>201312</creationdate><title>Synergistic effects of predators and trematode parasites on larval green frog (Rana clamitans) survival</title><author>Marino, John A. ; Werner, Earl E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a5607-dc24a1460875f82e54c4911e35250b6cd89821940178474420dfe93c95b7ef7d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Amphibia. Reptilia</topic><topic>Anax</topic><topic>Anax spp</topic><topic>Animal and plant ecology</topic><topic>Animal populations</topic><topic>Animal, plant and microbial ecology</topic><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Cercariae</topic><topic>Conservation</topic><topic>Digenea</topic><topic>Echinostomatidae</topic><topic>Ecological competition</topic><topic>Frogs</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>General aspects</topic><topic>green frog</topic><topic>Infections</topic><topic>Insecta</topic><topic>Insecta - physiology</topic><topic>Invertebrates</topic><topic>Larva - parasitology</topic><topic>Larva - physiology</topic><topic>Larvae</topic><topic>larval survival</topic><topic>Longevity</topic><topic>Marine</topic><topic>mesocosms experiment</topic><topic>natural enemies</topic><topic>Nemathelminthia. 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In particular, parasites can alter host traits that influence predation risk, and predators can have nonconsumptive effects on prey traits which influence susceptibility (i.e., infection intensity and tolerance) to parasites. Here, we examined the combined effects of trematode parasites (Digenea: Echinostomatidae) and odonate ( Anax ) predators on the survival of larval green frogs ( Rana clamitans ). First, in a large-scale mesocosm experiment, we manipulated the presence or absence of parasites in combination with the presence of no predator, caged predators, or free predators, and measured survival, traits, and infection. Parasites, caged predators, and free predators decreased survival, and we found a strong negative synergistic effect of parasites in combination with free predators on survival. Importantly, we then examined the potential mechanisms that explain the observed synergistic effect of parasites and predators in a series of follow-up experiments. 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subjects Amphibia. Reptilia
Anax
Anax spp
Animal and plant ecology
Animal populations
Animal, plant and microbial ecology
Animals
Biological and medical sciences
Cercariae
Conservation
Digenea
Echinostomatidae
Ecological competition
Frogs
Fundamental and applied biological sciences. Psychology
General aspects
green frog
Infections
Insecta
Insecta - physiology
Invertebrates
Larva - parasitology
Larva - physiology
Larvae
larval survival
Longevity
Marine
mesocosms experiment
natural enemies
Nemathelminthia. Plathelmintha
Odonata
odonate predators
Parasite hosts
parasite-host interactions
Parasites
Planorbella trivolvis
population dynamics
Predation
predator-prey interactions
Predators
Predatory Behavior
Rana
Rana clamitan
Rana clamitans
Rana clamitans - parasitology
Rana clamitans - physiology
risk
Snails
spp
synergism
synergistic effects
Tadpoles
Trematode Infections - parasitology
Trematode Infections - veterinary
trematode parasites
Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution
title Synergistic effects of predators and trematode parasites on larval green frog (Rana clamitans) survival
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