Title: Partitioning the non-consumptive effects of predators on prey with complex life
histories
Jon M. Davenport1*, Blake R. Hossack2 and Winsor H. Lowe1
1
Division of Biological Sciences, University of Montana, Missoula, MT, USA 59812
2
U.S. Geological Survey, Northern Rocky Mountain Science Center, Aldo Leopold Wilderness
Research Institute, 790 E. Beckwith Ave., Missoula MT, USA 59801
*corresponding author: jon.davenport@mso.umt.edu
1
Appendix A. A table of published references and total number of lines per reference used in the
meta-analysis of prey activity. Predators functional groups are based on published references and
acronyms are as follows: NGL = non-gape-limited, GL = gape-limited, SAP= sit-and-pursue,
ACT = active.
Pelophylax lessonae
# of
lines
6
Altwegg 2002
NGL, SAP
Lithobates sphenocephalus
2
Babbitt 2001
Aeshna palmata
NGL, SAP
Rana aurora
1
Barnett & Richardson 2002
Aeshna palmata
NGL, SAP
Rana pretiosa
1
Barnett & Richardson 2002
Aeshna juncea
NGL, SAP
Rana temporaria
2
Laurila & Kujasalo 1999
Aeshna spp.
NGL, SAP
Rana arvalis
2
Laurila et al. 2006
Triturus vulgaris
GL, ACT
Rana arvalis
2
Laurila et al. 2006
Gasterosteus aculeatus
GL, ACT
Rana arvalis
2
Laurila et al. 2006
Aeshna spp.
NGL, SAP
Rana temporaria
1
Orizaola et al. 2012
Anax spp.
NGL, SAP
Lithobates sylvaticus
8
Relyea 2002
Salmo salar
NGL, ACT
Rana temporaria
2
Nicieza 2000
Belostoma spp.
NGL, SAP
Agalychnis callidryas
2
Vonesh & Warkentin 2006
Anax spp.
NGL, SAP
Anaxyrus americanus
4
Skelly & Werner 1990
Gambusia holbrooki
GL, ACT
Litoria aurea
2
Hamer et al. 2002
Gambusia holbrooki
GL, ACT
Crinea signifera
2
Lane & Mahoney 2002
Gambusia holbrooki
GL, ACT
Limnodynastes tasmaniensis
2
Lane & Mahoney 2002
Ambystoma tigrinum
GL, ACT
Hyla versicolor
2
Skelly 1992
Perca fluviatilis
NGL, ACT
Lestes sponsa
2
Johansson et al. 2001
Salvelinus fontinalis
NGL, ACT
Baetis bicaudatus
4
Peckarsky & McIntosh 1998
Aeshna cyanea
NGL, SAP
Coenagrion puella
8
Mikolajewski et al. 2005
Gobio gobio
NGL, ACT
Lestes depressa
4
Mikolajewski et al. 2007
Predator species
Predator Functional group
Prey Species
Anax imperator
NGL, SAP
Anax junius
2
Source
Literature Cited for Appendix A
Altwegg, R. 2002. Predator-induced life-history plasticity under time constraints in pool frogs.
Ecology 83:2542-2551.
Babbit, K.J. 2001. Behaviour and growth of southern leopard frog (Rana sphenocephala)
tadpoles: Effects of food and predation risk. Canadian Journal of Zoology 79:809-814.
Barnett, H.K., and J.S. Richardson. 2002. Predation risk and competition effects on the lifehistory characteristics of larval Oregon spotted frog and larval red-legged frog. Oecologia
132:436-444.
Hamer, A.J., S.J. Lane, and M.J. Mahony. 2002. The role of introduced mosquitofish (Gambusia
holbrooki) in excluding the native green and golden bell frog (Litoria aurea) from
original habitats in south-eastern Australia. Oecologia 132:445-452.
Johansson, F., R. Stoks, L. Rowe, and M. De Block. 2001. Life history plasticity in a damselfly:
effects of combined time and biotic constraints. Ecology 82:1857-1869.
Lane, S.J., and M.J. Mahony. 2002. Larval anurans with synchronous and asynchronous
developmental periods: contrasting responses to water reduction and predator presence.
Journal of Animal Ecology 71:780-792.
Laurila, A., and J. Kujasalo. 1999. Habitat duration, predation risk and phenotypic plasticity in
common frog (Rana temporaria) tadpoles. Journal of Animal Ecology 68:1123-1132.
Laurila, A., S. Pakkasmaa, and J. Merilä. 2006. Population divergence in growth rate and
antipredator defences in Rana arvalis. Oecologia 147:585-595.
Mikolajewski, D.J., T. Bodin, F. Johansson, and G. Joop. 2005. Phenotypic plasticity in gender
specific life-history: effects of food availability and predation. Oikos 110:91-100.
Mikolajewski, G. Joop, and B. Wohlfahrt. 2007. Coping with predators and food limitation:
testing life history theory for sex-specific larval development. Oikos 116:642-649.
3
Nicieza, A.G. 2000. Interacting effects of predation risk and food availability on larval anuran
behaviour and development. Oecologia 123:497-505.
Orizaola, G., E. Dahl, and A. Laurila. 2012. Reversibility of predator-induced plasticity and its
effects at a life-history switch point. Oikos 121:44-52.
Peckarsky, B.L., and A.R. McIntosh. 1998. Fitness and community consequences of avoiding
multiple predators. Oecologia 113:565-576.
Relyea, R.A. 2002. Local population differences in phenotypic plasticity: Predator-induced
changes in wood frog tadpoles. Ecological Monographs 72:77-93.
Skelly, D.K. 1992. Field evidence for a cost of behavioral antipredator response in a larval
amphibian. Ecology 73:704-708.
Skelly, D.K., and E.E. Werner. 1990. Behavioral and life-historical responses of larval American
toads to an odonate predator. Ecology 71:2313-2322.
Vonesh, J.R., and K.M. Warkentin. 2006. Opposite shifts in size at metamorphosis in response to
larval and metamorph predators. Ecology 87:556-562.
4
Appendix B. A table of published references and total number of lines per reference used in the
meta-analysis of prey larval period. Predators functional groups are based on published
references and acronyms are as follows: NGL = non-gape-limited, GL = gape-limited, SAP= sitand-pursue, ACT = active.
Anax imperator
Anax imperator
Anax imperator
Anax junius
Aeshna palmata
Predator Functional
group
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
Pelophylax lessonae
Pelophylax lessonae
Pelophylax esculentus
Lithobates sphenocephalus
Rana aurora
# of
lines
3
5
5
2
1
Aeshna palmata
NGL, SAP
Rana pretiosa
1
Notonecta spp.
Aeshna brevistyla
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Aeshna juncea
Aeshna juncea
Aeshna juncea
Aeshna juncea
Aeshna spp.
Lissotriton vulgaris
Gasterosteus aculeatus
Aeshna spp.
Anax spp.
NGL, ACT
NGL, SAP
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
GL, ACT
GL, ACT
NGL, SAP
NGL, SAP
Anaxyrus boreas
Limnodynastes peronii
Rana arvalis
Bufo bufo
Rana temporaria
Hyla arborea
Pelobates fuscus
Rana dalmatina
Bufo calamita
Rana temporaria
Rana temporaria
Bufo bufo
Rana temporaria
Rana arvalis
Rana arvalis
Rana arvalis
Rana temporaria
Hyla versicolor
1
1
1
1
1
1
1
1
1
2
2
2
1
2
2
2
1
2
Salmo salar
Salmo trutta
Aeshna cyanea
NGL, ACT
NGL, ACT
NGL, SAP
Rana temporaria
Lissotriton helveticus
Lissotriton spp.
2
1
1
Belostoma spp.
NGL, SAP
Agalychnis callidryas
2
Aeshna cyanea
Aeshna cyanea
Anax spp.
Gambusia holbrooki
Taricha granulosa
Gambusia holbrooki
Gambusia holbrooki
Ambystoma
macrodactylum
Notophthalmus
NGL, SAP
NGL, SAP
NGL, SAP
GL, ACT
GL, ACT
GL, ACT
GL, ACT
GL, ACT
Bufo bombina
Bufo variegata
Anaxyrus americanus
Litoria aurea
Rana aurora
Crinea signifera
Limnodynastes tasmaniensis
Ambystoma macrodactylum
2
2
4
2
1
2
2
2
Altwegg 2002a
Altwegg 2002b
Altwegg 2002b
Babbitt 2001
Barnett & Richardson
2002
Barnett & Richardson
2002
Chivers et al. 1999
Kraft et al. 2005
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Laurila & Kujasalo 1999
Laurila et al. 1998
Laurila et al. 1998
Laurila et al. 2004
Laurila et al. 2006
Laurila et al. 2006
Laurila et al. 2006
Orizaola et al. 2012
Relyea & Hoverman
2003
Nicieza 2000
Orizaola & Bana 2005
Van Buskirk & Schmidt
2000
Vonesh & Warkentin
2006
Vorndran et al. 2002
Vorndran et al. 2002
Skelly & Werner 1990
Hamer et al. 2002
Kiesecker et al. 2002
Lane & Mahoney 2002
Lane & Mahoney 2002
Wildy et al. 1999
GL, ACT
Anaxyrus americanus
2
Raffel et al. 2011
Predator species
Prey Species
5
Source
viridescens
Haemopis sanguisuga
Nepa spp.
Lissotriton vulgaris
Aeshna cyanea
Perca fluviatilis
Perca fluviatilis
Salvelinus fontinalis
NGL, ACT
NGL, SAP
GL, ACT
NGL, SAP
NGL, ACT
NGL, ACT
NGL, ACT
Rana dalmatina
Rana dalmatina
Rana dalmatina
Rana dalmatina
Leucorrhinia dubia
Lestes sponsa
Baetis bicaudatus
1
1
1
1
1
2
4
Salvelinus fontinalis
NGL, ACT
2
Toxorhynchites rutilus
Aeshna cyanea
Perca fluviatilis
Lepomis gibbosus
Anax junius
Anax junius
Anax junius
Australopelopia
prionoptera
Gobio gobio
Salvelinus fontinalis
NGL, SAP
NGL, SAP
NGL, ACT
NGL, ACT
NGL, SAP
NGL, SAP
NGL, SAP
NGL, ACT
Callibaetis ferrugineus
hageni
Aedes triseriatus
Coenagrion puella
Lestes sponsa
Chironomus tentans
Lestes dryas
Lestes forcipatus
Lestes congener
Polypedilum
australotropicus
Lestes depressa
Baetis bicaudatus
NGL, ACT
NGL, ACT
6
16
4
1
7
4
4
3
3
Hettney et al. 2011
Hettney et al. 2011
Hettney et al. 2011
Hettney et al. 2011
Johansson 2002
Johansson et al. 2001
Peckarsky & McIntosh
1998
Caudill & Peckarsky
2003
Hechtel & Juliano 1997
Mikolajewski et al. 2005
Brodin & Johansson 2002
Ball & Baker 1995
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
McKie & Pearson 2006
4
2
Mikolajewski et al. 2007
Peckarsky et al. 2001
Literature Cited for Appendix B
Altwegg, R. 2002a. Predator-induced life-history plasticity under time constraints in pool frogs.
Ecology 83:2542-2551.
Altwegg, R. 2002b. Trait-mediated indirect effects and complex life-cycles in two European
frogs. Evolutionary Ecology Research 4:519-536.
Babbit, K.J. 2001. Behaviour and growth of southern leopard frog (Rana sphenocephala)
tadpoles: Effects of food and predation risk. Canadian Journal of Zoology 79:809-814.
Ball, S.L., and R.L. Baker. 1995. The non-lethal effects of predators and the influence of food
availability on life history of adult Chironomus tentans (Diptera: Chironomidae).
Freshwater Biology 34:1-12.
Barnett, H.K., and J.S. Richardson. 2002. Predation risk and competition effects on the lifehistory characteristics of larval Oregon spotted frog and larval red-legged frog. Oecologia
132:436-444.
Brodin, T., and F. Johansson. 2002. Effects of predator-induced thinning and activity changes on
life history in a damselfly. Oecologia 132:316-322.
Caudill, C.C., and B.L. Peckarsky. 2003. Lack of appropriate behavioral or developmental
responses by mayfly larvae to trout predators. Ecology 84:2133-2144.
Chivers, D.P., J.M. Kiesecker, A. Marco, E.L. Wildy, and A.R. Blaustein. 1999. Shifts in life
history as a response to predation in western toads (Bufo boreas). Journal of Chemical
Ecology 25:2455-2463.
De Block, M., M.A. McPeek, and R. Stoks. 2008. Life history plasticity to combined time and
biotic constraints in Lestes damselflies from vernal and temporary ponds. Oikos 117:908916.
7
Hamer, A.J., S.J. Lane, and M.J. Mahony. 2002. The role of introduced mosquitofish (Gambusia
holbrooki) in excluding the native green and golden bell frog (Litoria aurea) from
original habitats in south-eastern Australia. Oecologia 132:445-452.
Hechtel, L.J., and S.A. Juliano. 1997. Effects of a predator on prey metamorphosis: plastic
responses by prey or selective mortality? Ecology 78:838-851.
Hettyey, A., K. Vincze, S. Zsarnóczai, H. Hoi, and A. Laurila. 2011. Costs and benefits of
defences induced by predators differing in dangerousness. Journal of Evolutionary
Biology 24:1007-1019.
Johansson, F. 2002. Reaction norms and production costs of predator-induced morphological
defences in a larval dragonfly (Leucorrhinia dubia: Odonata). Canadian Journal of
Zoology 80:944-950.
Johansson, F., R. Stoks, L. Rowe, and M. De Block. 2001. Life history plasticity in a damselfly:
effects of combined time and biotic constraints. Ecology 82:1857-1869.
Kiesecker, J.M., D.P. Chivers, M. Anderson, and A.R. Blaustein. 2002. Effect of predator diet on
life history shifts of red-legged frogs, Rana aurora. Journal of Chemical Ecology
28:1007-1015.
Kraft, P.G., R.S. Wilson, and C.E. Franklin. 2005. Predator-mediated phenotypic plasticity in
tadpoles of the striped marsh frog, Limnodynastes peronii. Austral Ecology 30:558-663.
Lane, S.J., and M.J. Mahony. 2002. Larval anurans with synchronous and asynchronous
developmental periods: contrasting responses to water reduction and predator presence.
Journal of Animal Ecology 71:780-792.
Lardner, B. 2000. Morphological and life history responses to predators in larvae of seven
anurans. Oikos 88:169-180.
8
Laurila, A., and J. Kujasalo. 1999. Habitat duration, predation risk and phenotypic plasticity in
common frog (Rana temporaria) tadpoles. Journal of Animal Ecology 68:1123-1132.
Laurila, A., J. Kujasalo, and E. Ranta. 1998. Predator-induced changes in life-history in two
anuran tadpoles: Effects of predator diet. Oikos 83:307-317.
Laurila, A., M. Järvi-Laturi, S. Pakkasmaa, and J. Merila. 2004. Temporal variation in predation
risk: Stage dependency, graded responses and fitness costs in tadpole antipredator
defense. Oikos 90-99.
Laurila, A., S. Pakkasmaa, and J. Merilä. 2006. Population divergence in growth rate and
antipredator defences in Rana arvalis. Oecologia 147:585-595.
McKie, B.G., and R.G. Pearson. 2006. Environmental variation and the predator-specific
responses of tropical stream insects: effects of temperature and predation on survival and
development of Australian Chironomidae (Diptera). Oecologia 149:328-339.
Mikolajewski, D.J., T. Bodin, F. Johansson, and G. Joop. 2005. Phenotypic plasticity in gender
specific life-history: effects of food availability and predation. Oikos 110:91-100.
Mikolajewski, G. Joop, and B. Wohlfahrt. 2007. Coping with predators and food limitation:
testing life history theory for sex-specific larval development. Oikos 116:642-649.
Nicieza, A.G. 2000. Interacting effects of predation risk and food availability on larval anuran
behaviour and development. Oecologia 123:497-505.
Peckarsky, B.L., B.W. Taylor, A.R. McIntosh, M.A. McPeek, and D.A. Lytle. 2001. Variation in
mayfly size at metamorphosis as a developmental response to risk of predation. Ecology
82:740-757.
Orizaola, G., and F. Braña. 2005. Plasticity in newt metamorphosis: The effect of predation at
embryonic and larval stages. Freshwater Biology 50:438-446.
9
Orizaola, G., E. Dahl, and A. Laurila. 2012. Reversibility of predator-induced plasticity and its
effects at a life-history switch point. Oikos 121:44-52.
Raffel, T.R., J.T. Hoverman, N.T. Halstead, P.J. Michel, and J.R. Rohr. 2010. Parasitism in a
community context: trait-mediated interactions with competition and predation. Ecology
91:1900-1907.
Relyea, R.A., and J.T. Hoverman. 2003. The impact of larval predators and competitors on the
morphology and fitness of juvenile tree frogs. Oecologia 134:596-604.
Skelly, D.K., and E.E. Werner. 1990. Behavioral and life-historical responses of larval American
toads to an odonate predator. Ecology 71:2313-2322.
Van Buskirk, J., and B.R. Schmidt. 2000. Predator-induced phenotypic plasticity in larval newts:
Trade-offs, selection, and variation in nature. Ecology 81:3009-3028.
Vonesh, J.R., and K.M. Warkentin. 2006. Opposite shifts in size at metamorphosis in response to
larval and metamorph predators. Ecology 87:556-562.
Vorndran, I.C., E. Reichwaldt, and B. Nürnberger. 2002. Does differential susceptibility to
predation in tadpoles stabilize the Bombina hybrid zone? Ecology 83:1648-1659.
Wildy, E.L., D.P. Chivers, and A.R. Blaustein. 1999. Shifts in life-history traits as a response to
cannibalism in larval long-toed salamanders (Ambystoma macrodactylum). Journal of
Chemical Ecology 25:2337-2346.
10
Appendix C. A table of published references and total number of lines per reference used in the
meta-analysis of prey size at metamorphosis. Predators functional groups are based on published
references and acronyms are as follows: NGL = non-gape-limited, GL = gape-limited, SAP= sitand-pursue, ACT = active.
Anax imperator
Anax imperator
Anax imperator
Anax junius
Aeshna palmata
Predator Functional
group
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
Pelophylax lessonae
Pelophylax lessonae
Pelophylax esculentus
Lithobates sphenocephalus
Rana aurora
# of
lines
6
5
5
2
1
Aeshna palmata
NGL, SAP
Rana pretiosa
1
Notonecta spp.
Aeshna brevistyla
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Aeshna juncea
NGL, ACT
NGL, SAP
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, SAP
Anaxyrus boreas
Limnodynastes peronii
Rana arvalis
Bufo bufo
Rana temporaria
Hyla arborea
Pelobates fuscus
Rana dalmatina
Bufo calamita
Rana temporaria
1
1
1
1
1
1
1
1
1
2
Aeshna juncea
Aeshna juncea
Aeshna spp.
Lissotriton vulgaris
Gasterosteus aculeatus
Aeshna spp.
Anax spp.
Anax spp.
Salmo salar
Salmo trutta
Aeshna cyanea
NGL, SAP
NGL, SAP
NGL, SAP
GL, ACT
GL, ACT
NGL, SAP
NGL, SAP
NGL, SAP
NGL, ACT
NGL, ACT
NGL, SAP
Rana temporaria
Bufo bufo
Rana arvalis
Rana arvalis
Rana arvalis
Rana temporaria
Lithobates sylvaticus
Lithobates sylvaticus
Rana temporaria
Lissotriton helveticus
Lissotriton spp.
2
2
2
2
2
1
1
8
2
1
1
Belostoma spp.
NGL, SAP
Agalychnis callidryas
2
Aeshna cyanea
Aeshna cyanea
Anax spp.
Gambusia holbrooki
Taricha granulosa
NGL, SAP
NGL, SAP
NGL, SAP
GL, ACT
GL, ACT
Bufo bombina
Bufo variegata
Anaxyrus americanus
Litoria aurea
Rana aurora
2
2
4
2
1
Predator species
Prey Species
11
Reference
Altwegg 2002a
Altwegg 2002b
Altwegg 2002b
Babbitt 2001
Barnett & Richardson
2002
Barnett & Richardson
2002
Chivers et al. 1999
Kraft et al. 2005
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Laurila & Kujasalo
1999
Laurila et al. 1998
Laurila et al. 1998
Laurila et al. 2006
Laurila et al. 2006
Laurila et al. 2006
Orizaola et al. 2012
Relyea 2001
Relyea 2002
Nicieza 2000
Orizaola & Bana 2005
Van Buskirk &
Schmidt 2000
Vonesh & Warkentin
2006
Vorndran et al. 2002
Vorndran et al. 2002
Skelly & Werner 1990
Hamer et al. 2002
Kiesecker et al. 2002
Gambusia holbrooki
GL, ACT
Crinea signifera
2
Gambusia holbrooki
GL, ACT
2
Enneacanthus obesus
Ambystoma
macrodactylum
Ambystoma tigrinum
Lepomis macrochirus
GL, ACT
GL, ACT
Limnodynastes
tasmaniensis
Hyla chrysoscelis
Ambystoma macrodactylum
GL, ACT
GL, ACT
Hyla versicolor
Ambystoma talpoiduem
1
2
Notophthalmus
viridescens
Haemopis sanguisuga
Nepa spp.
Lissotriton vulgaris
Aeshna cyanea
Perca fluviatilis
Perca fluviatilis
Salvelinus fontinalis
GL, ACT
Anaxyrus americanus
2
NGL, ACT
NGL, SAP
GL, ACT
NGL, SAP
NGL, ACT
NGL, ACT
NGL, ACT
1
1
1
1
1
2
2
Toxorhynchites rutilus
NGL, SAP
Rana dalmatina
Rana dalmatina
Rana dalmatina
Rana dalmatina
Leucorrhinia dubia
Lestes sponsa
Callibaetis ferrugineus
hageni
Aedes triseriatus
16
Lepomis gibbosus
Aeshna cyanea
NGL, ACT
NGL, SAP
Chironomus tentans
Coenagrion puella
4
4
Perca fluviatilis
NGL, ACT
Lestes sponsa
1
Lepomis gibbosus
Anax junius
Anax junius
Anax junius
Perca fluviatilis
NGL, ACT
NGL, SAP
NGL, SAP
NGL, SAP
NGL, ACT
Chironomus tentans
Lestes dryas
Lestes forcipatus
Lestes congener
Coenagrion puella
7
3
4
3
2
Australopelopia
prionoptera
Gobio gobio
NGL, ACT
2
NGL, ACT
Polypedilum
australotropicus
Lestes depressa
Salvelinus fontinalis
Salvelinus fontinalis
NGL, ACT
NGL, ACT
Baetis bicaudatus
Baetis bicaudatus
2
4
12
2
2
4
Lane & Mahoney
2002
Lane & Mahoney
2002
Resetarits et al. 2004
Wildy et al. 1999
Skelly 1992
Jackson & Semlitsch
1993
Raffel et al. 2011
Hettney et al. 2011
Hettney et al. 2011
Hettney et al. 2011
Hettney et al. 2011
Johansson 2002
Johansson et al. 2001
Caudill & Peckarsky
2003
Hechtel & Juliano
1997
Ball & Baker 1996
Mikolajewski et al.
2005
Brodin & Johansson
2002
Ball & Baker 1995
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
Mikolajewski et al.
2008
McKie & Pearson
2006
Mikolajewski et al.
2007
Peckarsky et al. 2002
Peckarsky et al. 2001
Literature Cited for Appendix C
Altwegg, R. 2002a. Predator-induced life-history plasticity under time constraints in pool frogs.
Ecology 83:2542-2551.
Altwegg, R. 2002b. Trait-mediated indirect effects and complex life-cycles in two European
frogs. Evolutionary Ecology Research 4:519-536.
Babbit, K.J. 2001. Behaviour and growth of southern leopard frog (Rana sphenocephala)
tadpoles: Effects of food and predation risk. Canadian Journal of Zoology 79:809-814.
Ball, S.L., and R.L. Baker. 1995. The non-lethal effects of predators and the influence of food
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Freshwater Biology 34:1-12.
Ball, S.L., and R.L. Baker. 1996. Predator-induced life history changes: antipredator behavior
costs or facultative life history shifts? Ecology 77:1116-1124.
Barnett, H.K., and J.S. Richardson. 2002. Predation risk and competition effects on the lifehistory characteristics of larval Oregon spotted frog and larval red-legged frog. Oecologia
132:436-444.
Brodin, T., and F. Johansson. 2002. Effects of predator-induced thinning and activity changes on
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Caudill, C.C., and B.L. Peckarsky. 2003. Lack of appropriate behavioral or developmental
responses by mayfly larvae to trout predators. Ecology 84:2133-2144.
Chivers, D.P., J.M. Kiesecker, A. Marco, E.L. Wildy, and A.R. Blaustein. 1999. Shifts in life
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De Block, M., M.A. McPeek, and R. Stoks. 2008. Life history plasticity to combined time and
13
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Hamer, A.J., S.J. Lane, and M.J. Mahony. 2002. The role of introduced mosquitofish (Gambusia
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original habitats in south-eastern Australia. Oecologia 132:445-452.
Hechtel, L.J., and S.A. Juliano. 1997. Effects of a predator on prey metamorphosis: plastic
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Hettyey, A., K. Vincze, S. Zsarnóczai, H. Hoi, and A. Laurila. 2011. Costs and benefits of
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Jackson, M.E., and R.D. Semlitsch. 1993. Paedomorphosis in the salamander Ambystoma
talpoiduem: effects of a fish predator. Ecology 74:342-350.
Johansson, F. 2002. Reaction norms and production costs of predator-induced morphological
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14
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15
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16
Vorndran, I.C., E. Reichwaldt, and B. Nürnberger. 2002. Does differential susceptibility to
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17
Appendix D. A summary of the studies that examined the non-consumptive effects of predators on metamorphosis of larval
amphibians and invertebrate used in the meta-analyses.
Predator species
Prey species
Reference
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax imperator
Anax junius
Anax junius
Aeshna palmata
Aeshna palmata
Notonecta spp.
Gambusia holbrooki
Gambusia holbrooki
Haemopis sanguisuga
Nepa spp.
Triturus vulgaris
Aeshna cyanea
Lepomis macrochirus
Predator functional
group
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, ACT
GL, ACT
GL, ACT
NGL, ACT
NGL, SAP
GL, ACT
NGL, SAP
GL, ACT
Altwegg 2002a
Altwegg 2002a
Altwegg 2002a
Altwegg 2002a
Altwegg 2002a
Altwegg 2002a
Altwegg 2002b
Altwegg 2002b
Altwegg 2002b
Altwegg 2002b
Altwegg 2002b
Altwegg 2002b
Altwegg 2002b
Altwegg 2002b
Altwegg 2002b
Altwegg 2002b
Babbitt 2001
Babbitt 2001
Barnett & Richardson 2002
Barnett & Richardson 2002
Chivers et al. 1999
Hamer et al. 2002
Hamer et al. 2002
Hettney et al. 2011
Hettney et al. 2011
Hettney et al. 2011
Hettney et al. 2011
Jackson & Semlitsch 1993
Larval
Period
Later
Later
Later
Later
Later
Later
Later
Later
Later
Earlier
Later
Later
Later
Later
Later
Later
Later
Earlier
Earlier
Equal
Equal
Equal
Equal
Later
-
Size at
metamorphosis
Larger
Larger
Larger
Smaller
Smaller
Smaller
Larger
Larger
Larger
Larger
Larger
Larger
Larger
Larger
Larger
Larger
Larger
Smaller
Larger
Smaller
Smaller
Smaller
Larger
Larger
Larger
Larger
Larger
Smaller
Pelophylax lessonae
Pelophylax lessonae
Pelophylax lessonae
Pelophylax lessonae
Pelophylax lessonae
Pelophylax lessonae
Pelophylax lessonae
Pelophylax lessonae
Pelophylax lessonae
Pelophylax lessonae
Pelophylax lessonae
Pelophylax esculentus
Pelophylax esculentus
Pelophylax esculentus
Pelophylax esculentus
Pelophylax esculentus
Lithobates sphenocephalus
Lithobates sphenocephalus
Rana aurora
Rana pretiosa
Anaxyrus boreas
Litoria aurea
Litoria aurea
Rana dalmatina
Rana dalmatina
Rana dalmatina
Rana dalmatina
Ambystoma talpoiduem
Lepomis macrochirus
GL, ACT
Ambystoma talpoiduem
Jackson & Semlitsch 1993
-
Smaller
Taricha granulosa
Aeshna brevistyla
Gambusia holbrooki
Gambusia holbrooki
Gambusia holbrooki
GL, ACT
NGL, SAP
GL, ACT
GL, ACT
GL, ACT
Rana aurora
Limnodynastes peronii
Crinea signifera
Crinea signifera
Limnodynastes
tasmaniensis
Kiesecker et al. 2002
Kraft et al. 2005
Lane & Mahoney 2002
Lane & Mahoney 2002
Lane & Mahoney 2002
Earlier
Later
Later
Earlier
Equal
Smaller
Larger
Larger
Equal
Larger
18
Treatment
Seasonality Exp't; Early
Seasonality Exp't; Delayed
Seasonality Exp't; Late
Pond drying Exp't; Constant
Pond drying Exp't; Slow
Pond drying Exp't; Fast
Competition Treatment 1
Competition Treatment 2
Competition Treatment 3
Competition Treatment 4
Competition Treatment 5
Competition Treatment 1
Competition Treatment 2
Competition Treatment 3
Competition Treatment 4
Competition Treatment 5
Low food, Active
High food, Active
alone treatment, low density
alone treatment, low density
Controls are non-predator cues
Constant water
Declining water
Leech
Water scorpion
newt
dragonfly
early intro only; low fish density;
metamorphs
early intro only; high fish density;
metamorphs
control=blank, treatment=tadpole diet
Constant water
Declining water
Constant water
Gambusia holbrooki
GL, ACT
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Dytiscus marginalis
Aeshna juncea
Aeshna juncea
Aeshna juncea
Aeshna juncea
Aeshna juncea
Aeshna juncea
Aeshna juncea
Aeshna spp.
Triturus vulgaris
Gasterosteus aculeatus
Aeshna spp.
Triturus vulgaris
Gasterosteus aculeatus
Salmo salar
Salmo salar
Salmo trutta
Aeshna spp.
Notophthalmus viridescens
Notophthalmus viridescens
Anax spp.
Anax spp.
Anax spp.
Anax spp.
Anax spp.
Anax spp.
Anax spp.
Anax spp.
Anax spp.
Anax spp.
Anax spp.
Ambystoma tigrinum
Anax spp.
Anax spp.
Anax spp.
Anax spp.
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
GL, ACT
GL, ACT
NGL, SAP
GL, ACT
GL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, SAP
GL, ACT
GL, ACT
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
GL, ACT
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
Limnodynastes
tasmaniensis
Rana arvalis
Bufo bufo
Rana temporaria
Hyla arborea
Pelobates fuscus
Rana dalmatina
Bufo calamita
Rana temporaria
Rana temporaria
Rana temporaria
Rana temporaria
Bufo bufo
Bufo bufo
Rana temporaria
Rana arvalis
Rana arvalis
Rana arvalis
Rana arvalis
Rana arvalis
Rana arvalis
Rana temporaria
Rana temporaria
Triturus helveticus
Rana temporaria
Bufo americanus
Bufo americanus
Hyla versicolor
Hyla versicolor
Lithobates sylvaticus
Lithobates sylvaticus
Lithobates sylvaticus
Lithobates sylvaticus
Lithobates sylvaticus
Lithobates sylvaticus
Lithobates sylvaticus
Lithobates sylvaticus
Lithobates sylvaticus
Hyla versicolor
Anaxyrus americanus
Anaxyrus americanus
Anaxyrus americanus
Anaxyrus americanus
Lane & Mahoney 2002
Earlier
Larger
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Lardner 2000
Laurila & Kujasalo 1999
Laurila & Kujasalo 1999
Laurila et al. 1998
Laurila et al. 1998
Laurila et al. 1998
Laurila et al. 1998
Laurila et al. 2004
Laurila et al. 2006
Laurila et al. 2006
Laurila et al. 2006
Laurila et al. 2006
Laurila et al. 2006
Laurila et al. 2006
Nicieza 2000
Nicieza 2000
Orizaola & Bana 2005
Orizaola et al. 2012
Raffel et al. 2011
Raffel et al. 2011
Relyea & Hoverman 2003
Relyea & Hoverman 2003
Relyea 2001
Relyea 2002
Relyea 2002
Relyea 2002
Relyea 2002
Relyea 2002
Relyea 2002
Relyea 2002
Relyea 2002
Skelly 1992
Skelly & Werner 1990
Skelly & Werner 1990
Skelly & Werner 1990
Skelly & Werner 1990
Later
Earlier
Later
Earlier
Later
Later
Earlier
Later
Later
Later
Later
Earlier
Earlier
Later
Equal
Later
Later
Later
Later
Later
Later
Later
Earlier
Equal
Earlier
Earlier
Later
Earlier
Earlier
Equal
Earlier
Later
Smaller
Smaller
Smaller
Smaller
Larger
Smaller
Larger
Larger
Larger
Larger
Larger
Smaller
Smaller
Larger
Larger
Larger
Larger
Larger
Larger
Larger
Smaller
Smaller
Larger
Smaller
Smaller
Larger
Smaller
Smaller
Smaller
Larger
Larger
Larger
Larger
Smaller
Smaller
Smaller
Smaller
Smaller
Smaller
19
Declining water
Low food; Constant volume
High food; Constant volume
Low food; Frog fed
High food; Frog fed
Low food; Toad fed
High food; Toad fed
Continuous Risk
Gotland populations
Gotland populations
Gotland populations
Uppland populations
Uppland populations
Uppland populations
Food at night
No food at night
No predation in embryonic stage
NP>NP and P>P
low density; no trematode
High density; no trematode
Low competition
High competition
BZM pond, open
CAT pond, open
GPP pond, open
PTP pond, open
DHP pond, closed
SLT pond, closed
SWW pond, closed
WWB pond, closed
food level 1, means from 3 blocks
food level 2, means from 3 blocks
food level 3, means from 3 blocks
food level 4, means from 3 blocks
Aeshna cyanea
NGL, SAP
Triturus spp.
Later
Larger
Agalychnis callidryas
Agalychnis callidryas
Bufo bombina
Bufo bombina
Bufo variegata
Bufo variegata
Ambystoma macrodactylum
Van Buskirk & Schmidt
2000
Vonesh & Warkentin 2006
Vonesh & Warkentin 2006
Vorndran et al. 2002
Vorndran et al. 2002
Vorndran et al. 2002
Vorndran et al. 2002
Wildy et al. 1999
Belostoma spp.
Belostoma spp.
Aeshna cyanea
Aeshna cyanea
Aeshna cyanea
Aeshna cyanea
Ambystoma
macrodactylum
Ambystoma
macrodactylum
Enneacanthus obesus
Enneacanthus obesus
Perca fluviatilis
Perca fluviatilis
Perca fluviatilis
Salvelinus fontinalis
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
GL, ACT
Equal
Later
Later
Later
Later
Later
Later
Smaller
Larger
Smaller
Smaller
Larger
Larger
Smaller
GL, ACT
Ambystoma macrodactylum
Wildy et al. 1999
Later
Smaller
GL, ACT
GL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
Hyla chrysoscelis
Hyla chrysoscelis
Leucorrhinia dubia
Lestes sponsa
Lestes sponsa
Callibaetis ferrugineus
hageni
Callibaetis ferrugineus
hageni
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Aedes triseriatus
Chironomus tentans
Chironomus tentans
Chironomus tentans
Chironomus tentans
Coenagrion puella
Coenagrion puella
Coenagrion puella
Coenagrion puella
Resetarits et al. 2004
Resetarits et al. 2004
Johansson 2002
Johansson et al. 2001
Johansson et al. 2001
Caudill & Peckarsky 2003
Later
Earlier
Earlier
Later
Later
Equal
Smaller
Larger
Larger
Smaller
Smaller
Equal
Salvelinus fontinalis
NGL, ACT
Caudill & Peckarsky 2003
Earlier
Smaller
females
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Toxorhynchites rutilus
Lepomis gibbosus
Lepomis gibbosus
Lepomis gibbosus
Lepomis gibbosus
Aeshna cyanea
Aeshna cyanea
Aeshna cyanea
Aeshna cyanea
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Hechtel & Juliano 1997
Ball & Baker 1996
Ball & Baker 1996
Ball & Baker 1996
Ball & Baker 1996
Mikolajewski et al. 2005
Mikolajewski et al. 2005
Mikolajewski et al. 2005
Mikolajewski et al. 2005
Earlier
Earlier
Equal
Later
Earlier
Earlier
Equal
Earlier
Earlier
Earlier
Later
Later
Later
Earlier
Earlier
Later
Earlier
Earlier
Earlier
Later
Smaller
Equal
Smaller
Smaller
Equal
Larger
Equal
Equal
Smaller
Smaller
Equal
Smaller
Larger
Larger
Equal
Equal
Smaller
Smaller
Smaller
Smaller
Larger
Larger
Larger
Equal
females, durham, 1 predator feeding
females, durham, 1 predator not feeding
females, normal, 1 predator feeding
females, normal, 1 predator not feeding
males, durham, 1 predator feeding
males, durham, 1 predator not feeding
males, normal, 1 predator feeding
males, normal, 1 predator not feeding
females, vero beach, 1 predator feeding
females, vero beach, 1 predator not feeding
females, normal, 1 predator feeding
females, normal, 1 predator not feeding
males, vero beach, 1 predator feeding
males, vero beach, 1 predator not feeding
males, normal, 1 predator feeding
males, normal, 1 predator not feeding
high food level, females laying eggs
medium food level, females laying eggs
high food level, females not laying eggs
medium food level, females not laying eggs
female, low food level
male, low food level
female, high food level
male, high food level
20
Water bug
Spider
Cefa populations
Frata populations
Lupsa populations
Baita populations
Typical fed Tubifex vs. Typical fed
conspecific
Typical fed Tubifex vs. Cannibal fed
conspecific
Low density
High density
no time constraint
time constraint
males
Perca fluviatilis
Lepomis gibbosus
Lepomis gibbosus
Lepomis gibbosus
Lepomis gibbosus
Lepomis gibbosus
Lepomis gibbosus
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
Lestes sponsa
Chironomus tentans
Chironomus tentans
Chironomus tentans
Chironomus tentans
Chironomus tentans
Chironomus tentans
Brodin & Johansson 2002
Ball & Baker 1995
Ball & Baker 1995
Ball & Baker 1995
Ball & Baker 1995
Ball & Baker 1995
Ball & Baker 1995
Earlier
Later
Later
Later
Later
Later
Later
Equal
Smaller
Smaller
Smaller
Smaller
Smaller
Smaller
Lepomis gibbosus
Anax junius
Anax junius
Anax junius
Anax junius
Anax junius
Anax junius
Anax junius
Anax junius
Anax junius
Anax junius
Anax junius
Perca fluviatilis
Perca fluviatilis
Australopelopia
prionoptera
Australopelopia
prionoptera
Gobio gobio
Gobio gobio
Gobio gobio
Gobio gobio
Salvelinus fontinalis
Salvelinus fontinalis
Salvelinus fontinalis
Salvelinus fontinalis
Salvelinus fontinalis
Salvelinus fontinalis
NGL, ACT
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, SAP
NGL, ACT
NGL, ACT
NGL, ACT
Chironomus tentans
Lestes dryas
Lestes dryas
Lestes dryas
Lestes dryas
Lestes forcipatus
Lestes forcipatus
Lestes forcipatus
Lestes forcipatus
Lestes congener
Lestes congener
Lestes congener
Coenagrion puella
Coenagrion puella
Polypedilum
australotropicus
Polypedilum
australotropicus
Lestes depressa
Lestes depressa
Lestes depressa
Lestes depressa
Baetis bicaudatus
Baetis bicaudatus
Baetis bicaudatus
Baetis bicaudatus
Baetis bicaudatus
Baetis bicaudatus
Ball & Baker 1995
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
De Block et al. 2008
Mikolajewski et al. 2008
Mikolajewski et al. 2008
McKie & Pearson 2006
Later
Earlier
Later
Later
Later
Later
Later
Earlier
Equal
Later
Later
Later
-
Smaller
Smaller
Equal
Smaller
Smaller
Smaller
Larger
Smaller
Smaller
Smaller
Smaller
Smaller
Smaller
Smaller
Equal
male, low food level
male, medium food level
male, high food level
female that laid eggs, medium food level
female that laid eggs, high food level
female that did not lay eggs, medium food
level
female that did not lay eggs, high food level
early larvae, high food
early larvae, low food
delayed larvae, high food
delayed larvae, low food
early larvae, high food
early larvae, low food
delayed larvae, high food
delayed larvae, low food
early larvae, high food
early larvae, low food
delayed larvae, high food
male, no conspecific predation, with fish
female, no conspecific predation, with fish
male, caged Australopelopia presence
McKie & Pearson 2006
-
Equal
female, caged Australopelopia presence
Mikolajewski et al. 2007
Mikolajewski et al. 2007
Mikolajewski et al. 2007
Mikolajewski et al. 2007
Peckarsky et al. 2002
Peckarsky et al. 2002
Peckarsky et al. 2001
Peckarsky et al. 2001
Peckarsky et al. 2001
Peckarsky et al. 2001
Later
Earlier
Later
Earlier
Earlier
Earlier
Smaller
Smaller
Larger
Larger
Smaller
Smaller
Larger
Larger
Smaller
Smaller
male, high food level
female, high food level
male, low food level
female, low food level
male, summer
female, summer
females, winter
males, winter
females, summer
males, summer
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
NGL, ACT
21