Ecological Archives A/E/M000–000–A1

A. D. Higginson and G. D. Ruxton. 2010. Adaptive changes in size and age at metamorphosis can qualitatively vary with predator type and available defenses. Ecology 20:2756–2768.

Appendix A. Meta-analysis of empirical studies of metamorphic responses to predation risk.

We reviewed the literature cited by Benard (2004) and Relyea (2007) in order to ascertain patterns in the responses to predator presence observed in experiments with amphibious prey (Table A1). The studies included in Table A1 were reviewed by Relyea (2007) and Benard (2004), see Appendix A. Note that the result of one study (Kiesecker et al. 2002) was reported incorrectly by Relyea (2007): metamorphosis actually occurred earlier at a smaller size, rather than earlier at an equal size. Another study (Kurzava and Morin 1998) was reported by Relyea (2007) as caged (nonlethal) predation, but actually involved lethal predation. As a result, effects of predator presence on size and age at metamorphosis are likely to be confounded by changes in food availability (see Introduction, Relyea 2007), so we omitted this study from our analysis. Finally, we also omitted one of the experiments by Vonesh and Warkentin (2006), because the juvenile stage of the prey is rarely attacked by the spider predator. However, we considered different treatments (e.g., food levels, prey density) as separate responses, hence we present responses in 43 experimental conditions from the 41 experiments reviewed by Relyea (2007).

We collated the following data from the articles: (1) Gosner stage: experimenters weighed metamorphs upon the first emergence of a forelimb (stage 42), or on completion of tail resorption (stage 46), and less often at stage 41 and 45. Accordingly, we classified weighing time as either early or late, depending on whether the stage was before or after stage 43. (2) Food level: we recorded the feeding protocol in the experiment as low if food supply was deliberately restricted or at natural levels, and as high if food supply was supplied ad libitum or stated as being high. (3) Location: experiments took place either in a laboratory or in a mesocosm. (4) Predators: those used were insects, fish or amphibians. We classified amphibians and fish together as vertebrates since there were insufficient data for meaningful analysis if they were treated separately. (5) Refuge: we noted whether experimenters reported providing a predator refuge for prey, such as leaves or other suitable substrate for concealment. (6) Active predator: on the basis of published literature we categorised experimental predators as either active searchers or sit-and-wait hunters. Thus dragonfly larvae are sit-and-wait predators (Cooper et al. 1985, Sih et al. 1998), unless they are hungry (Altwegg 2003), and they are able to use mandibles to break up their prey so are unlikely to be gape-limited (Caldwell et al. 1980, Brodie and Formanowicz 1983, Crump 1984, Eklöv and Werner 2000).  Fish, newts, salamander, water bugs and water beetles are active searchers, and of these, the vertebrates usually have to swallow their prey whole and are often gape-limited to the extent that prey above a certain size are invulnerable (Caldwell et al. 1980, Brodie and Formanowicz 1983, Crump 1984, Semlitsch and Whitfield-Gibbons 1988, Sih et al. 1998). In contrast, whilst having less success with larger prey, water beetles and water bugs appear to be not gape-limited (Brodie and Formanowicz 1983). Unfortunately there were insufficient experiments with gape-limited predators for reliable analysis of this factor. All the data are available in Appendix A.

We carried out loglinear frequency analysis tests (Sokal and Rohlf 1995) to determine how these factors were associated with size (smaller, no change, larger in the presence of predators) and age at metamorphosis (younger, no change, older in the presence of predators) in order to assess which factors affected the difference between predator-absent and predator-present treatments (Table A2). We also compiled data on behavioural defenses from the literature by estimating proportion activity (as the proportion of individuals active or the proportion of time individuals spend being active) in predator-present and predator-absent treatments, where they were measured (Table A3).

TABLE A1. Summary of empirical studies of metamorphic responses to predation risk (after Benard 2004, Relyea 2007).

Prey taxa

Prey

Predator species

Gosner
stage

Food

Location

Predator
type

Age

Size

Reference


Amphibian

Agalychnis callidryas

Belostoma sp.

46

Ad lib.

Lab

Bug

Equal

Smaller

Vonesh and Warkentin 2006

Amphibian

Ambystoma macrodactylum

Ambystoma macrodactylum

46

Ad lib.

Lab

Newt

Later

Equal

Wildy et al. 1999

Amphibian

Bombina bombina

Aeshna cyanea

46

Ad lib.

Lab

Dragonfly

Later

Smaller

Vorndran et al. 2002

Amphibian

Bombina variegata

Aeshna cyanea

46

Ad lib.

Lab

Dragonfly

Later

Larger

Vorndran et al. 2002

Amphibian

Bufo americanus

Anax sp.

42

High

Lab

Dragonfly

Equal

Smaller

Skelly and Werner 1990

Amphibian

Bufo americanus

Anax sp.

42

Low

Lab

Dragonfly

Equal

Smaller

Skelly and Werner 1990

Amphibian

Bufo boreas

Notonecta sp.

41

Ad lib.

Lab

Bug

Equal

Equal

Chivers et al. 1999

Amphibian

Bufo bufo

Aeshna juncea

42

High

Lab

Dragonfly

Earlier

Smaller

Laurila et al. 1998

Amphibian

Bufo bufo

Dytiscus marginalis

45

Natural

Mesocosm

Beetle

Equal

Equal

Lardner 2000

Amphibian

Bufo bufo

Aeshna juncea

42

Low

Lab

Dragonfly

Equal

Equal

Laurila et al. 1998

Amphibian

Bufo calamita

Dytiscus marginalis

45

Natural

Mesocosm

Beetle

Equal

Equal

Lardner 2000

Amphibian

Crinia signifera

Gambusia holbrooki

42

Ad lib.

Lab

Fish

Equal

Equal

Lane and Mahony 2002

Amphibian

Hyla arborea

Dytiscus marginalis

45

Natural

Mesocosm

Beetle

Equal

Equal

Lardner 2000

Amphibian

Hyla chrysoscelis

Enneacanthus obesus

46

Natural

Mesocosm

Fish

Equal

Equal

Resetarits et al. 2004

Amphibian

Hyla versicolor

Anax sp.

46

Natural

Mesocosm

Dragonfly

Equal

Equal

Relyea and Hoverman 2003

Amphibian

Limnodynastes peronii

Aeshna brevistyla

46

Ad lib.

Lab

Dragonfly

Later

Larger

Kraft et al. 2004

Amphibian

Limnodynastes tasmaniensis

Gambusia holbrooki

42

Ad lib.

Lab

Fish

Equal

Equal

Lane and Mahony 2002

Amphibian

Litoria aurea

Gambusia holbrooki

42

Ad lib.

Lab

Fish

Equal

Equal

Hamer et al. 2002

Amphibian

Pelobates fuscus

Dytiscus marginalis

45

Natural

Mesocosm

Beetle

Equal

Equal

Lardner 2000

Amphibian

Rana arvalis

Dytiscus marginalis

45

Natural

Mesocosm

Beetle

Equal

Equal

Lardner 2000

Amphibian

Rana aurora

Aeshna palmata

42

High

Mesocosm

Dragonfly

Later

Larger

Barnett and Richardson 2002

Amphibian

Rana aurora

Aeshna palmata

42

Low

Mesocosm

Dragonfly

Later

Larger

Barnett and Richardson 2002

Amphibian

Rana aurora

Taricha granulosa

41

Ad lib.

Lab

Newt

Earlier

Smaller

Kiesecker et al. 2002

Amphibian

Rana dalmatina

Dytiscus marginalis

45

Natural

Mesocosm

Beetle

Equal

Equal

Lardner 2000

Amphibian

Rana esculenta

Anax imperator

42

Natural

Mesocosm

Dragonfly

Later

Larger

Altwegg 2002b

Amphibian

Rana lessonae

Anax imperator

42

Natural

Mesocosm

Dragonfly

Later

Larger

Altwegg 2002b

Amphibian

Rana lessonae

Anax imperator

46

Natural

Mesocosm

Dragonfly

Later

Equal

Altwegg 2002a

Amphibian

Rana pretiosa

Aeshna palmata

42

High

Mesocosm

Dragonfly

Later

Smaller

Barnett and Richardson 2002

Amphibian

Rana pretiosa

Aeshna palmata

42

Low

Mesocosm

Dragonfly

Equal

Equal

Barnett and Richardson 2002

Amphibian

Rana ridibunda

Aeshna cyanea

42

High

Mesocosm

Dragonfly

Later

Equal

Van Buskirk and Saxer 2001

Amphibian

Rana sphenocephala

Anax junius

42

High

Lab

Dragonfly

Later

Equal

Babbit 2001

Amphibian

Rana sphenocephala

Anax junius

42

Low

Lab

Dragonfly

Later

Larger

Babbit 2001

Amphibian

Rana sylvatica

Anax sp.

45

Natural

Mesocosm

Dragonfly

Later

Equal

Relyea 2002c

Amphibian

Rana temporaria

Dytiscus marginalis

45

Natural

Mesocosm

Beetle

Equal

Smaller

Lardner 2000

Amphibian

Rana temporaria

Aeshna sp.

42

Ad lib.

Lab

Dragonfly

Later

Larger

Laurila et al. 2004

Amphibian

Rana temporaria

Aeshna juncea

42

High

Lab

Dragonfly

Later

Equal

Laurila and Kujasalo 1999

Amphibian

Rana temporaria

Aeshna juncea

42

High

Lab

Dragonfly

Later

Larger

Laurila et al. 1998

Amphibian

Rana temporaria

Aeshna juncea

42

Low

Lab

Dragonfly

Later

Equal

Laurila and Kujasalo 1999

Amphibian

Rana temporaria

Aeshna juncea

42

Low

Lab

Dragonfly

Later

Larger

Laurila et al. 1998

Amphibian

Rana temporaria

Salmon Salmo salar

46

Ad lib.

Lab

Fish

Later

Larger

Nicieza 2000

Amphibian

Rana temporaria

Salmo salar

46

Low

Lab

Fish

Equal

Smaller

Nicieza 2000

Amphibian

Triturus alpestrish

Aeshna cyanea

42

High

Mesocosm

Dragonfly

Later

Larger

Van Buskirk and Schmidt 2000

Amphibian

Triturus helveticush

Salmo trutta

46

Ad lib.

Lab

Fish

Equal

Equal

Orizaolo and Braña 2005

                   

Insect

Aedes triseriatus

Toxorhynchites rutilis

 

 

Insect

Equal

Equal

Hechtel and Juliano 1997

Insect

Aedes triseriatus

Toxorhynchites rutilis

 

 

Insect

Later

Equal

Hechtel and Juliano 1997

Insect

Baetis bicaudatus

Salvelinus fontinalis

 

 

Fish

Earlier

Smaller

Peckarsky et al 2002

Insect

Baetis bicaudatus

Salvelinus fontinalis

 

 

Fish

Earlier

Smaller

Peckarsky et al 2001

Insect

Baetis bicaudatus

Salvelinus fontinalis

 

 

Fish

Equal

Smaller

Peckarsky and McIntosh 1998

Insect

Baetis bicaudatus

Megarcys signata

 

 

Insect

Equal

Smaller

Peckarsky and McIntosh 1998

Insect

Baetis bicaudatus

Megarcys signata

 

 

Insect

Later

Smaller

Peckarsky and McIntosh 1998

Insect

Baetis bicaudatus

Megarcys signata

 

 

Insect

Equal

Smaller

Peckarsky et al. 1993

Insect

Baetis tricaudatus

Rhinicthtys. cataractae,

 

Fish

Later

Smaller

Scrimgeour and Culp 1994

Insect

Callibaetis ferrugineus hageni

Salvelinus fontinalis

 

 

Fish

Equal

Equal

Caudill and Peckarsky 2003

Insect

Chironomus tentans

Lepomis gibbosus

 

 

Fish

Equal

Equal

Ball and Baker 1996

Insect

Chironomus tentans

Lepomis gibbosus

 

 

Fish

Later

Equal

Ball and Baker 1996

Insect

Drunella coloradensis

Salvelinus fontinalis

 

 

Fish

Equal

Equal

Dahl and Peckarsky 2002

Insect

Ephemerella invaria

Rhinicthtys cataractae
and Etheostoma flabellare

Fish

Earlier

Smaller

Dahl and Peckarsky 2003

Insect

Ephemerella subvaria

Luxilus cornutus

 

 

Fish

Later

Equal

Tseng 2003

Insect

Lestes sponsa

Perca fluviatilis

 

 

 

Fish

Later

Smaller

Johansson et al. 2001

Insect

Leucorrhinia dubia

Perca fluviatilis

 

 

 

Fish

Equal

Equal

Johansson 2002


 

TABLE A2. Results of log linear analyses on the observed change in size and age at metamorphosis for the amphibian experiments reported in Relyea (2007). See text for explanation of the experimental variables. Initially we assumed that all responses were possible, and in all cases found a strong interaction between size and age (G4 > 19.22, P < 0.001) because three responses were not observed (see Table A3). This had very little effect on the other interactions so we report the results of analyses in which we assumed structural zeros in the cells of those three responses (Sokal and Rohlf 1995), and compared hierarchical models using maximum likelihood in R (Free Software Foundation). No third-order interactions were significant. We also carried out analysis with all the experimental variables in a single contingency table, but no third-order or higher interactions were detected.

 

Experimental variable

Response variable

Deviance

df

P

Gosner stage

Size

0.882

2

0.643

 

Age

3.405

2

0.182

 

Size–Age

0.022

4

0.999

Food level

Size

0.850

2

0.653

 

Age

4.568

2

0.100

 

Size-Age

0.160

4

0.997

Location

Size

1.518

2

0.468

 

Age

1.262

2

0.532

 

Size-Age

0.053

4

0.999

Predator taxa

Size

0.644

2

0.725

 

Age

2.429

2

0.296

 

Size-Age

0.094

4

0.998

Refuge provided

Size

0.235

2

0.888

 

Age

4.712

2

0.095

 

Size-Age

0.001

4

0.999

Active predator

Size

1.12

2

0.572

 

Age

11.66

2

0.003

 

Size-Age

0.535

4

0.969

 

 

 

 


 

TABLE A3. The number of studies on amphibian and insect prey (in bold, respectively) reviewed by Relyea (2007: Appendix 1) and Benard (2004: Table 2) showing each combination of size and age at metamorphosis in response to increased predation risk from caged predators. Also, the mean (± SE) difference in the proportion of prey active between predator present and predator absent treatments in studies that reported behavioral responses. Number of studies in italics.

 

 

Size

 

 

Age

Smaller

Equal

Larger

Earlier

2 / 3
0.010 (0) N = 1

 

 

Same

5 / 3
0.108 (0.005) N = 4

15 / 5
0.008 (0.011) N = 5

 

Later

2 / 3
0.260 (0.092) N = 3

7 / 3
0.096 (0.093) N = 5

12 / 0
0.233 (0.076) N = 4


 

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