Skip to main content

Socially facilitated antipredator behavior by ringed salamanders (Ambystoma annulatum)

Behavioral Ecology and Sociobiology volume 66, pages 811–817 (2012)Cite this article

Abstract

Many aspects of animal behavior can be socially facilitated, including foraging behavior, exploration behavior, and antipredator behavior. Although larvae of the ringed salamander (Ambystoma annulatum) are not gregarious, they can live in high densities and face intense predation pressure during a short period following hatching. In a predator-recognition experiment, we found that these salamanders responded to chemical cues from dragonfly nymphs (Family: Libellulidae) with appropriate antipredator behavior (decreased activity), and this response was absent when salamanders were exposed to chemical cues from nonpredatory mayfly nymphs (Family: Heptageniidae). In a second experiment, we tested whether antipredator behavior in response to chemical cues of dragonflies could be socially facilitated by larval ringed salamanders. We placed an “observer” salamander into a central arena with four “demonstrator” salamanders behind clear barriers around an arena. The barriers ensured that chemical cues would not be detected by the observer. When demonstrators were exposed to chemical cues from dragonflies, the data were consistent with the hypothesis that both demonstrators and observers decreased activity relative to a blank control. Our results provide evidence that social facilitation can occur in larval ringed salamanders, a nonsocial species.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (Canada)

Fig. 1
Fig. 2
Fig. 3

References

  • Altig RA, Christensen MT (1981) Behavioral characteristics of the tadpoles of Rana heckscheri. J Herpetol 15:151–154

    Article  Google Scholar 

  • Angermier WH, Schaul LT, James WT (1959) Conditioning in rats. J Comp Physiol Psychol 52:370–372

    Article  Google Scholar 

  • Azevedo-Ramos C, van Sluys M, Hero J-M, Magnusson I (1992) Influence of tadpole movement on predation by odonate naiads. J Herpetol 26:335–338

    Article  Google Scholar 

  • Birke LA (1974) Social facilitation in the Bengalese finch. Behaviour 48:111–122

    Article  Google Scholar 

  • Blaustein AR, Walls SC (1995) Aggregation and kin recognition. In: Heatwole H, Sullivan BK (eds) Ambphibian biology, vol 2, Social behavior. Surrey Beatty & Sons, Chipping Norton, New South Wales, pp 568–602

    Google Scholar 

  • Boice R, Quanty CB, Williams RC (1974) Competition and possible dominance in turtles, toads and frogs. J Comp Physiol Psychol 86:1116–1131

    Article  PubMed  CAS  Google Scholar 

  • Boland CRJ (2003) An experimental test of predator detection rates using groups of free-living emus. Ethology 109:209–222

    Article  Google Scholar 

  • Brown C, Laland KN (2002) Social learning of a novel avoidance task in the guppy: conformity and social release. Anim Behav 64:41–47

    Article  Google Scholar 

  • Brown C, Markula A, Laland K (2003) Social learning of prey location in hatchery-reared Atlantic salmon. J Fish Biol 63:738–745

    Article  Google Scholar 

  • Brunkow PE, Collins JP (1998) Group size structure affects patterns of aggression in larval salamanders. Behav Ecol 9:508–514

    Article  Google Scholar 

  • Buskirk JV, Arioli M (2002) Dosage response of an induced defense: how sensitive are tadpoles to predation risk? Ecology 83:1580–1585

    Article  Google Scholar 

  • Caldwell JP (1989) Structure and behavior of Hyla geographica tadpole schools with comments on classification of group behavior in tadpoles. Copeia 1989:928–948

    Google Scholar 

  • Caldwell JP, Thorp JH, Jervey TO (1980) Predator–prey relationships among larval dragonflies, salamanders, and frogs. Oecologica 46:285–289

    Google Scholar 

  • Clayton DA (1978) Socially facilitated behavior. Q Rev Biol 53:373–392

    Article  Google Scholar 

  • Coolen I, Dangles O, Casas J (2005) Social learning in noncolonial insects? Curr Biol 15:1931–1935

    Article  PubMed  CAS  Google Scholar 

  • Crane AL, Mathis A (2011a) Landmark learning by the Ozark zigzag salamander (Plethodon angusticlavius). Curr Zool 57:485–490

    Google Scholar 

  • Crane AL, Mathis A (2011b) Predator-recognition training: a conservation strategy to increase postrelease survival of hellbenders in head-starting programs. Zoo Biol 30:611–622

    Google Scholar 

  • Curio E (1988) Cultural transmission of enemy recognition by birds. In: Zentall TR, Galef BG (eds) Social learning, psychological and biological perspectives. Lawrence-Erlbaum, Hillsdale, NJ, pp 3–28

    Google Scholar 

  • da Silva J, Terhune JM (1988) Harbour seal grouping as an anti-predator strategy. Anim Behav 36:1309–1316

    Article  Google Scholar 

  • Deni R, Jorgensen BW (1976) Inhibition of fixed interval bar-pressing in rats during exposure to a trained companion. Psychol Rep 39:243–246

    Article  Google Scholar 

  • Ferrari MCO, Messier F, Chivers DP (2007) First documentation of cultural transmission of predator recognition by larval amphibians. Ethology 113:621–627

    Article  Google Scholar 

  • Fiorito GB Jr, Scotto P (1992) Observational learning in Octopus vulgaris. Science 256:545–547

    Article  PubMed  CAS  Google Scholar 

  • Fronzuto JA, Verrell PA (2007) In the eye of the tiger: predator avoidance tactics differ among life-history stages of an ambystomatid salamander. Ethol Ecol Evol 19:101–112

    Article  Google Scholar 

  • Galef BG Jr (1988) Imitation in animals: history, definition, and interpretation of data from the psychological laboratory. In: Zentall TR, Galef BG (eds) Social learning, psychological and biological perspectives. Lawrence Erlbaum, Hillsdale, NJ, pp 3–28

    Google Scholar 

  • Gall BG, Mathis A (2010) Innate predator recognition and the problem of introduced trout. Ethology 116:47–58

    Article  Google Scholar 

  • Harris RN, Vess TJ, Hammond JI, Lindermuth CJ (2003) Context-dependent kin discrimination in larval four-toed salamanders Hemidactylium scutatum (Caudata: Plethodontidae). Herpetologica 59:164–177

    Article  Google Scholar 

  • Harrison RG (1969) Organization and development of the embryo. Yale Univ, Press, New Haven, CT

    Google Scholar 

  • Hetherington TE, Lombard RE (1983) Mechanisms of underwater hearing in larval and adult tiger salamanders Ambystoma tigrinum. Comp Biochem Phys A 74:555–559

    Article  CAS  Google Scholar 

  • Higgins JJ, Tashtoush S (1994) An aligned rank transform test for interaction. Nonlinear World 1:201–211

    Google Scholar 

  • Hokit DG, Walls SC, Blaustein AR (1996) Context-dependent kin discrimination in larvae of the marbled salamander, Ambystoma opacum. Anim Behav 52:17–31

    Article  Google Scholar 

  • Hughes RN (1969) Social facilitation of locomotion and exploration in rats. Br J Psychol 60:385–388

    Article  PubMed  CAS  Google Scholar 

  • Kats LB (1988) The detection of certain predators via olfaction by small-mouthed salamander larvae (Ambystoma texanum). Behav Neural Biol 50:126–131

    Article  PubMed  CAS  Google Scholar 

  • Keeling LJ, Hurnik JF (1993) Chickens show socially facilitated feeding behaviour in response to a video image of a conspecific. Appl Anim Behav Sci 36:223–231

    Article  Google Scholar 

  • Laland K, Kendall JR (2003) What the models say about social learning. In: Perry S, Fragaszy D (eds) The biology of traditions: models and evidence. Cambridge Univ Press, Cambridge, pp 33–55

    Chapter  Google Scholar 

  • Lamp WO, Britt NW (1981) Resource partitioning by two species of stream mayflies (Ephemeroptera: Heptageniidae). Great Lakes Entomol 14:151–157

    Google Scholar 

  • Laurila A, Kujasalo J, Ranta E (1998) Predator-induced changes in life history in two anuran tadpoles: effects of predator diet. Oikos 83:307–317

    Article  Google Scholar 

  • Leadbetter E, Chittka L (2009) Bumble-bees learn the value of social cues through experience. Biol Lett 5:310–312

    Article  Google Scholar 

  • Lefcort H (1998) Chemically mediated fright response in southern toad (Bufo terrestris) tadpoles. Copeia 1998:445–450

    Article  Google Scholar 

  • Mathis A (2003) Use of chemical cues in detection of conspecific predators and prey by newts, Notophthalmus viridescens. Chemoecology 13:193–197

    Article  Google Scholar 

  • Mathis A, Vincent F (2000) Differential use of visual and chemical cues in predator recognition and treat-sensitive predator-avoidance responses by larval newts (Notophthalmus viridescens). Can J Zool 78:1646–1652

    CAS  Google Scholar 

  • Mathis A, Chivers DP, Smith RJF (1996) Cultural transmission of predator recognition in fishes: intraspecific and interspecific learning. Anim Behav 51:185–201

    Article  Google Scholar 

  • Mathis A, Murray KL, Hickman CR (2003) Do experience and body size play a role in responses of larval ringed salamanders, Ambystoma annulatum, to predator kairomones? Laboratory and field assays. Ethology 109:159–170

    Article  Google Scholar 

  • Mathis A, Ferrari MCO, Windel N, Messier F, Chivers DP (2008) Learning by embryos and the ghost of predation future. P Roy Soc Lond B 275:2603–2607

    Article  Google Scholar 

  • Merritt RW, Cummins KW (1996) An introduction to the aquatic insects of North America. Kendall/Hunt Publishing Company, Dubuque, IA

    Google Scholar 

  • Minshall JN (1967) Life history and ecology of Epeorus pleuralis (Banks) (Epemeroptera: Heptageniidae). Am Midl Nat 78:369–388

    Article  Google Scholar 

  • Mirza RS, Chivers DP (2003) Response of juvenile rainbow trout to varying concentrations of chemical alarm cue: response thresholds and survival during encounters with predators. Can J Zool 81:88–95

    Article  Google Scholar 

  • Mirza RS, Ferrari MCO, Kiesecker JM, Chivers DP (2006) Responses of American toad tadpoles to predation cues: behavioral response thresholds, treat-sensitivity and acquired predator recognition. Behaviour 143:877–889

    Article  Google Scholar 

  • Nyman S, Wilkinson RF, Hutcherson JE (1993) Cannibalism and size relations in a cohort of larval ringed salamanders (Ambystoma annulatum). J Herpetol 27:78–84

    Article  Google Scholar 

  • Peterson CL, Wilkinson RF, Moll D, Holder T (1991) Premetamorphic survival of Ambystoma annulatum. Herpetologica 47:96–100

    Google Scholar 

  • Petranka J, Hayes L (1998) Chemically mediated avoidance of a predatory odonate (Anax junius) by American toad (Bufo americanus) and wood frog (Rana sylvatica) tadpoles. Behav Ecol Sociobiol 42:263–271

    Article  Google Scholar 

  • Pfennig DW, James JP, Ziemba RE (1999) A test of alternative hypothesis for kin recognition in cannibalistic tiger salamanders. Behav Ecol 10:436–443

    Article  Google Scholar 

  • Pulliam HR (1973) On the advantages of flocking. J Theor Biol 38:419–422

    Article  PubMed  CAS  Google Scholar 

  • Sih A, Kats LB (1994) Age, experience, and the response of streamside salamander hatchlings to chemical cues from predatory sunfish. Ethology 96:253–259

    Article  Google Scholar 

  • Skelly DK (1994) Activity level and the susceptibility of anuran larvae to predation. Anim Behav 47:464–468

    Article  Google Scholar 

  • Stauffer H-P, Semlitsch RD (1993) Effects of visual, chemical and tactile cues of fish on the behavioural responses of tadpoles. Anim Behav 46:355–364

    Article  Google Scholar 

  • Stofer A, White C (2004) Phenotypically plastic responses of larval tiger salamanders, Ambystoma tigrinum, to different predators. J Herpetol 38:612–615

    Article  Google Scholar 

  • Sudd JH (1972) The absence of social enhancement of digging in pairs of ants (Formica lemani Bondroit. Anim Behav 20:813–819

    Article  Google Scholar 

  • Sullivan AM, Maerz JC, Madison DM (2002) Anti-predator response of red-backed salamanders (Plethodon cinereus) to chemical cues from garter snakes (Thamnophis sirtalis): laboratory and field experiments. Behav Ecol Sociobiol 51:227–233

    Article  Google Scholar 

  • Uematsu T (1971) Social facilitation in feeding behavior of the guppy. I. Preliminary experiment. Jpn J Ecol 21:48–51

    Google Scholar 

  • Urban MC (2008) Salamander evolution across a latitudinal cline in gape-limited predation risk. Oikos 117:1037–1049

    Article  Google Scholar 

  • Verrell P (2000) Methoxychlor increases susceptibility to predation in the salamander Ambystoma macrodactylum. Bull Environ Contam Toxicol 64:85–92

    Article  PubMed  CAS  Google Scholar 

  • Voshell JR Jr (2002) A guide to common freshwater invertebrates of North America. McDonald and Woodward Publishing Company, Blacksburg, VA

    Google Scholar 

  • Whiten A, Horner V, de Waal FBM (2005) Conformity to cultural norms of tool use in chimpanzees. Nature 437:737–740

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson A, Mandl I, Bugnyar T, Huber L (2010a) Gaze following in the red-footed tortoise (Geochelone carbonaria). Anim Cogn 13:765–769

    Article  PubMed  Google Scholar 

  • Wilkinson A, Kuenstner K, Mueller J, Huber L (2010b) Social learning in a non-social reptile (Geochelone carbonaria). Biol Lett 6:614–616

    Article  PubMed  Google Scholar 

  • Yurewicz KL (2004) A growth/mortality trade-off in larval salamanders and the coexistence of intraguild predators and prey. Oecologia 132:102–111

    Article  Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall, Englewood Cliffs, NJ

    Google Scholar 

  • Zentall TR (2004) Action imitation in birds. Learn Behav 32:15–23

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Missouri State University Biology Department for support. We are especially grateful to the Kirby family for access to their pond, and we thank Janice Greene, director of Bull Shoals Field Station, for access to our other collecting site. We also thank Andrew Hoffman for help collecting egg masses, and we thank Michael Lampe and Valerie Jones for help with observations in Experiment 1.

Ethical standards

This project was approved by Missouri State University’s IACUC (protocol: 2008AA) which follows the current guidelines in the state of Missouri and in the USA for the humane and ethical use of animals in research. Collecting was conducted with permits from the Missouri Department of Conservation (permits: 14363 and 13611).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Missouri State University, Springfield, MO, 65897, USA

    Adam Crane, Alicia Mathis & Carly McGrane

Authors
  1. Adam Crane
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alicia Mathis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carly McGrane
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adam Crane.

Additional information

Communicated by T. Bakker

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Crane, A., Mathis, A. & McGrane, C. Socially facilitated antipredator behavior by ringed salamanders (Ambystoma annulatum). Behav Ecol Sociobiol 66, 811–817 (2012). https://doi.org/10.1007/s00265-012-1329-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-012-1329-0

Keywords

  • Social facilitation
  • Predator recognition
  • Ringed salamander
  • Ambystoma annulatum
  • Dragonfly nymph