Learning by embryos and the ghost of predation future

Proceedings of the Royal Society B: Biological Sciences

Volumn 275, Issue 1651, 2008, Pages 2603-2607

  Mathis, Alicia ^a   Ferrari, Maud C O ^b   Windel, Nathan ^a   Messier, François ^b   Chivers, Douglas P ^b  

^a MISSOURI STATE UNIVERSITY   (United States)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Ambystoma annulatum; Embryos; Learning; Predation; Rana sylvatica

Indexed keywords

ADAPTATION; AMPHIBIAN; CHEMICAL CUE; CONDITIONING; EMBRYONIC DEVELOPMENT; LARVA; PREDATION; SHELTER;

ADAPTIVE BEHAVIOR; AMBYSTOMA ANNULATUM; ARTICLE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FROG; HATCHING; NONHUMAN; PREDATION; PRIORITY JOURNAL; RANA SYLVATICA; SALAMANDER; SPECIES HABITAT; STATE DEPENDENT LEARNING;

AMBYSTOMA ANNULATUM; RANA SYLVATICA;

EID: 54249144607     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.0754     Document Type: Article

References (32)

1. Brodman, R. & Jaskula, J. 2002 Activity and microhabitat use during interactions among five species of pond-breeding salamander larvae. Herpetologica 58, 346-354. (doi:10.1655/0018-0831(2002)058[0346: AAMUDI]2.0.CO;2)
2. Brown, G. E. 2003 Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish. 4, 227-234. (doi:10.1046/j.1467-2979.2003.00132.x)
3. Davis, P. D., Glynn, L. M., Schetter, C. D., Hobel, C., Chicz-Demet, A. & Sandman, C. A. 2005 Corticotropin-releasing hormone during pregnancy is associated with infant temperament. Devel. Neurosci. 27, 299-305. (doi:10.1159/000086709)
4. Dugovic, C., Maccari, S., Weibel, L., Turek, F. W. & Van Reeth, O. 1999 High corticosterone levels in prenatally stressed rats predict persistent paradoxical sleep alterations. J. Neurosci. 19, 8656-8664.
5. Gosner, K. L. 1960 A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183-190.
6. Harrison, R. G. 1969 Organization and development of the embryo. New Haven, CT: Yale University Press.
7. Hepper, P. G. 1996 Fetal memory: does it exist? What does it do? Acta Pædiatr. Suppl. 416, 16-20. (doi:10.1111/j.1651-2227.1996. tb14272.x)
8. Hepper, P. G. 1997 Memory in utero? Develop. Med. Child Neurol. 39, 343-346.
9. Hepper, P. G. & Waldman, B. 1992 Embryonic olfactory learning in frogs. Q. J. Exp. Psychol. B 44, 179-197.
10. Holomuzki, J. R. 1985 Life history aspects of the predaceous diving beetle, Dytiscus dauricus (Gebler), in Arizona. Southwest. Nat. 30, 485-490. (doi:10.2307/3671043)
11. Kats, L. B. & Dill, L. M. 1998 The scent of death: chemosensory assessment of predation risk by prey animals. Écoscience 5, 361-394.
12. Kawai, N., Morokuma, S., Tomonaga, M., Horimoto, N. & Tanada, M. 2004 Associative learning and memory in a chimpanzee fetus: learning and long-lasting memory before birth. Dev. Psychobiol. 44, 116-122. (doi:10.1002/dev.10160)
13. Lemaire, V., Koehl, M., Le Moal, M. & Abrous, D. N. 2000 Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl Acad. Sci. USA 97, 11 032-11 037. (doi:10.1073/pnas.97.20.11032)
14. Lima, S. L. & Bednekoff, P. A. 1999 Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am. Nat. 153, 649-659. (doi:10.1086/303202)
15. Mathis, A., Murray, K. L. & Hickman, C. R. 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. (doi:10.1046/j.1439-0310.2003.00849.x)
16. Mirza, R. S. & Chivers, D. P. 2001 Do chemical alarm signals enhance survival in aquatic vertebrates? An analysis of the current research paradigm. In Chemical signals in vertebrates, vol. 9 (eds A. Marchlewska-Koj, J. J. Lepri & D. Müller-Schwarze), pp. 277-284. New York, NY: Plenum.
17. Nyman, S., Wilkinson, R. F. & Hutcherson, J. E. 1993 Cannibalism and size relations in a cohort of larval ringed salamanders (Ambystoma annulatum). J. Herpetol. 27, 78-84. (doi:10.2307/1564909)
18. Orizaola, G. & Braña, F. 2003 Response of predator-naive newt larvae to food and predator presence. Can. J. Zool. 81, 1845-1850. (doi:10.1139/z03-160)
19. Petranka, J. W. 1998 Salamanders of the United States and Canada. Washington, DC: Smithsonian Institution Press.
20. 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. (doi:10.1007/s002650050438)
21. Pinsker, H. M., Hening, W. A., Carew, T. J. & Kandel, E. R. 1973 Long-term sensitization of a defensive withdrawal reflex in Aplysia. Science 182, 1039-1042. (doi:10.1126/science.182.4116.1039)
22. Saglio, P. & Mandrillon, A.-L. 2006 Embryonic experience to predation risk affects tadpoles of the common frog (Rana temporaria). Archiv. Hydrobiol. 166, 505-523. (doi:10.1127/0003-9136/2006/0166-0505)
23. Salm, A. K., Pavelko, M., Krouse, E. M., Webster, W., Kraszpulski, M. & Birkle, D. L. 2004 Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress. Develop. Brain Res. 148, 159-167. (doi:10.1016/j.devbrainres.2003.11.005)
24. Sih, A. & Moore, R. D. 1993 Delayed hatching of salamander eggs in response to enhanced larval predation risk. Am. Nat. 142, 947-960. (doi:10.1086/285583)
25. Skelly, D. K. 1994 Activity level and the susceptibility of anuran larvae to predation. Anim. Behav. 47, 464-468. (doi:10.1006/anbe.1994. 1063)
26. Sneddon, H., Hadden, R. & Hepper, P. G. 1998 Chemosensory learning in the chicken embryo. Physiol. Behav. 64, 133-139. (doi:10.1016/S0031-9384(98)00037-7)
27. Stangel, P. W. 1988 Premetamorphic survival of the salamander Ambystoma maculatum in eastern Massachusetts. J. Herpetol. 22, 345-347. (doi:10.2307/1564160)
28. Uller, T. & Olsson, M. 2006 Direct exposure to corticosterone during embryonic development influences behavior in an ovoviviparous lizard. Ethology 112, 390-397. (doi:10.1111/j.1439-0310.2006.01164.x)
29. Vallée, M., Mayo, W., Dellu, F., Le Moal, M., Simon, H. & Maccari, S. 1997 Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J. Neurosci. 17, 2626-2636.
30. Waldman, B. 1982 Quantitative and developmental analyses of the alarm reaction in the zebra danio Brachydanio rerio. Copeia 1982, 1-9. (doi:10.2307/1444261)
31. Watson, S. & Russell, A. P. 2000 A posthatching developmental staging table for the long-toed salamander, Ambystoma macrodactylum krausei. Amphib.-Reptil. 21, 143-154. (doi:10.1163/156853800507336)
32. Woody, D. R. & Mathis, A. 1998 Acquired recognition of chemical stimuli from an unfamiliar predator: associative learning by adult newts, Notophthalmus viridescens. Copeia 1998, 1027-1031. (doi:10.2307/1447352)