The ability of three species of tadpoles to differentiate among potential fish predators

Ethology

Volumn 114, Issue 7, 2008, Pages 701-710

  Smith, Geoffrey R ^a   Burgett, Amber A ^a   Temple, Kathleen G ^a   Sparks, Kathryn A ^a   Winter, Kristen E ^a  

^a DENISON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIORAL RESPONSE; FROG; PREDATION; PREDATOR;

ANURA; BUFO AMERICANUS; CARASSIUS AURATUS; LEPOMIS MACROCHIRUS; MICROPTERUS; MICROPTERUS SALMOIDES; RANA CATESBEIANA; RANA CLAMITANS;

EID: 44949232339     PISSN: 01791613     EISSN: 14390310     Source Type: Journal    
DOI: 10.1111/j.1439-0310.2008.01505.x     Document Type: Article

References (85)

1. Adams, J. L., Camelio, K. W., Orique, M. J. Blumstein, D. T. 2006 : Does information of predators influence general wariness? Behav. Ecol. Sociobiol. 60, 742 747.
2. Amo, L., López, P. Martín, J. 2004 : Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges. Anim. Behav. 67, 647 653.
3. Anholt, B. R., Skelly, D. K. Werner, E. E. 1996 : Factors modifying antipredator behavior in larval toads. Herpetologica 52, 301 313.
4. Anholt, B. R., Werner, E. Skelly, D. K. 2000 : Effect of food and predators on the activity of four larval ranid frogs. Ecology 81, 3509 3521.
5. Awan, A. R. Smith, G. R. 2007 : The effect of group size on the responses of wood frog tadpoles to fish. Am. Midl. Nat. 158, 79 84.
6. Baumgärtner, D., Jungbluth, A.-D., Koch, U. von Elert, E. 2002 : Effects of infochemicals on microhabitat choice by the freshwater amphipod Gammarus roeseli. Arch. Hydrobiol. 155, 353 367.
7. Bridges, C. M. Gutzke, W. H. N. 1997 : Effects of environmental history, sibship, and age on predator-avoidance responses of tadpoles. Can. J. Zool. 75, 87 93.
8. Brown, R. M. Taylor, D. H. 1995 : Compensatory escape mode trade-offs between swimming performance and maneuvering behavior through larval ontogeny of the wood frog, Rana sylvatica. Copeia 1995, 1 7.
9. Brown, G. E., Bongiorno, T., DiCapua, D. M., Ivan, L. I. Roh, E. 2006 : Effects of group size on the threat-sensitive response to varying concentrations of chemical alarm cues by juvenile convict cichlids. Can. J. Zool. 84, 1 8.
10. Casper, G. S. Hendricks, R. 2005 : Rana catesbeiana Shaw, 1802. American bullfrog. In : Amphibian Declines: The Conservation Status of United States Species (Lannoo, M., ed.). University of California Press, Berkeley, CA, pp. 540 546.
11. Chivers, D. P. Mirza, R. S. 2001 : Importance of predator diet cues in responses of larval wood frogs to fish and invertebrate predators. J. Chem. Ecol. 27, 45 51.
12. Cieri, M. D. Stearns, D. E. 1999 : Reduction of grazing activity of two estuarine copepods in response to the exudates of a visual predator. Mar. Ecol. Prog. Ser. 177, 157 163.
13. Clark, C. W. 1994 : Antipredator behavior and the asset-protection principle. Behav. Ecol. 5, 159 170.
14. Cox, J. G. Lima, S. L. 2006 : Naiveté and an aquatic-terrestrial dichotomy in the effects of introduced predators. Trends Ecol. Evol. 21, 674 680.
15. Eklöv, P. 2000 : Chemical cues from multiple predator-prey interactions induce changes in behavior and growth of anuran larvae. Oecologia 123, 192 199.
16. Eklöv, P. Werner, E. E. 2000 : Multiple predator effects on size-dependent behavior and mortality of two species of anuran larvae. Oikos 88, 250 258.
17. Feminella, J. W. Hawkins, C. P. 1994 : Tailed frog tadpoles differentially alter their feeding behavior in response to non-visual cues from four predators. J. N. Am. Benth. Soc. 13, 310 320.
18. Ferrari, M. C. O., Capitania-Kwok, T. Chivers, D. P. 2006a : The role of learning in the acquisition of threat-senstive responses to predator odours. Behav. Ecol. Sociobiol. 60, 522 527.
19. Ferrari, M. C. O., Messier, F. Chivers, D. P. 2006b : The nose knows: minnows determine predator proximity and density through detection of predator odours. Anim. Behav. 72, 927 932.
20. Formanowicz, D. R. Jr. 1986 : Anuran tadpole/aquatic insect predator-prey interactions: tadpole size and predator capture success. Herpetologica 42, 367 373.
21. Glandt, D. 1985 : Preying on tadpoles by the goldfish Carassius auratus auratus and the rudd Scardinius erythrophthalmus. Salamandra 21, 180 185.
22. Golden, D. R., Smith, G. R. Rettig, J. E. 2000 : Effects of age and group size on habitat selection and activity level in Xenopus laevis tadpoles. Trans. Nebraska Acad. Sci. 26, 23 27.
23. Golden, D. R., Smith, G. R. Rettig, J. E. 2001 : Effects of age and group size on habitat selection and activity level in Rana pipiens tadpoles. Herpetol. J. 11, 69 73.
24. Golub, J. L. Brown, G. E. 2003 : Are all signals the same? Ontogenetic change in the response to conspecific and heterospecific chemical alarm signals by juvenile green sunfish (Lepomis cyanellus). Behav. Ecol. Sociobiol. 54, 113 118.
25. Gosner, K. L. 1960 : A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183 190.
26. Green, D. M. 2005 : Bufo americanus Holbrook, 1836. American toad. In : Amphibian Declines: The Conservation Status of United States Species (Lannoo, M., ed.). University of California Press, Berkeley, CA, pp. 386 390.
27. Greene, E. Meagher, T. 1998 : Red squirrels, Tamiasciurus hudsonicus, produce predator-class specific alarm calls. Anim. Behav. 55, 511 518.
28. Helfman, G. S. 1989 : Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav. Ecol. Sociobiol. 24, 47 58.
29. Helfman, G. S. Winkelman, D. L. 1997 : Threat sensitivity in bicolor damselfish: effects of sociality and body size. Ethology 103, 369 383.
30. Hirvonen, H., Ranta, E., Piironen, J., Laurila, A. Peuhkuri, N. 2000 : Behavioural responses of naïve Arctic charr young to chemical cues from salmonid and non-salmonid fish. Oikos 88, 191 199.
31. Hölker, F. Stief, P. 2005 : Adaptive behaviour of chironomid larvae (Chironomus riparius) in response to chemical stimuli from predators and resource density. Behav. Ecol. Sociobiol. 58, 256 263.
32. Holomuzki, J. R. Short, T. M. 1990 : Ontogenetic shifts in habitat use and activity in a stream-dwelling isopod. Hol. Ecol. 13, 300 307.
33. Kats, L. B., Petranka, J. W. Sih, A. 1988 : Antipredator defenses and the persistence of amphibian larvae with fishes. Ecology 69, 1865 1870.
34. Koperski, P. 1998 : Predator-prey interactions between larval damselflies and mining larvae of Glyptotendipes gripekoveni (Chironomidae): reduction in feeding activity as an induced defence. Freshw. Biol. 39, 317 324.
35. Kotler, B. P., Brown, J. S. Bouskila, A. 2004 : Apprehension and time allocation in gerbils: the effects of predatory risk and energetic state. Ecology 85, 917 922.
36. Kusch, R. C., Mirza, R. S. Chivers, D. P. 2004 : Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows. Behav. Ecol. Sociobiol. 55, 551 555.
37. Laurila, A., Järvi-Latui, M., Pakkasmaa, S. Merilä, J. 2004 : Temporal variation in predation risk: stage-dependency, graded responses and fitness costs in tadpole anti-predator defences. Oikos 107, 90 99.
38. Laurila, A., Pakkasmaa, S. Merilä, J. 2006 : Population divergence in growth rate and antipredator defenses in Rana arvalis. Oecologia 147, 585 595.
39. Lawler, S. P. 1989 : Behavioural responses to predators and predation risk in four species of larval anurans. Anim. Behav. 38, 1039 1047.
40. Lefcort, H. 1996 : Adaptive, chemically mediated fright response in tadpoles of the southern leopard frog, Rana utricularia. Copeia 1996, 455 459.
41. Marcus, J. P. Brown, G. E. 2003 : Response of pumpkinseed sunfish to conspecific chemical alarm cues: an interaction between ontogeny and stimulus concentration. Can. J. Zool. 81, 1671 1677.
42. Marquis, O., Saglio, P. Neveu, A. 2004 : Effects of predators and conspecific chemical cues on the swimming activity of Rana temporaria and Bufo bufo tadpoles. Arch. Hydrobiol. 160, 153 170.
43. Mathis, A. Vincent, F. 2000 : Differential use of visual and chemical cues in predator recognition and threat-sensitive predator-avoidance responses by larval newts (Notophthalmus viridescens). Can. J. Zool. 78, 1646 1652.
44. McIntosh, A. R. Peckarsky, B. L. 2004 : Are mayfly anti-predator responses to fish odour proportional to risk? Arch. Hydrobiol. 160, 145 151.
45. McIntosh, A. R., Peckarsky, B. L. Taylor, B. W. 1999 : Rapid size-specific changes in the drift of Baetis bicaudatus (Ephemeroptera) caused by alterations in fish odour concentration. Oecologia 118, 256 264.
46. Meyer, A. H., Schmidt, B. R. Grossenbacher, K. 1998 : Analysis of three amphibian populations with quarter-century long time-series. Proc. R. Soc. Lond. 265B, 523 528.
47. Mittelbach, G. G. 1981 : Foraging efficiency and body size: a study of optimal diet and habitat useby bluegills. Ecology 62, 1370 1386.
48. Nicieza, A. G. 1999 : Context-dependent aggregation in common frog Rana temporaria tadpoles: influence of developmental stage, predation risk and social environment. Funct. Ecol. 13, 852 858.
49. Orizaola, G. Braña, F. 2003 : Response of predator-naïve newt larvae to food and predator presence. Can. J. Zool. 81, 1845 1850.
50. Pauley, T. K. Lannoo, M. J. 2005 : Rana clamitans Latreille, 1801. Green frog. In : Amphibian Declines: The Conservation Status of United States Species (Lannoo, M., ed.). University of California Press, Berkeley, CA, pp. 549 552.
51. Peacor, S. D. Werner, E. E. 2000 : Predator effects of an assemblage of consumers through induced changes in consumer foraging behavior. Ecology 81, 1998 2010.
52. Pearl, C. A., Adams, M. J., Schuytema, G. S. Nebeker, A. V. 2003 : Behavioral responses of anuran larvae to chemical cues of active and introduced predators in the Pacific Northwestern United States. J. Herpetol. 37, 572 576.
53. Peckarsky, B. L. 1980 : Predator-prey interactions between stoneflies and mayflies: behavioral observations. Ecology 61, 932 943.
54. Persons, M. H. Rypstra, A. L. 2001 : Wolf spiders show graded antipredator behavior in the presence of chemical cues from different sized predators. J. Chem. Ecol. 27, 2493 2504.
55. Pettersson, L. B., Nilsson, P. A. Brönmark, C. 2000 : Predator recognition and defence strategies in crucian carp, Carassius carassius. Oikos 88, 200 212.
56. Porej, D. Hetherington, T. E. 2005 : Designing wetlands for amphibians: the importance of predatory fish and shallow littoral zones in structuring of amphibian communities. Wetlands Ecol. Manage. 13, 445 455.
57. Puttlitz, M. H., Chivers, D. P., Kiesecker, J. M. Blaustein, A. R. 1999 : Threat-sensitive predator avoidance by larval Pacific treefrogs (Amphibia, Hylidae). Ethology 105, 449 456.
58. Reinhardt, U. G. 2002 : Asset protection in juvenile salmon: how adding biological realism changes a dynamic foraging model. Behav. Ecol. 13, 94 100.
59. Reinhardt, U. G. Healey, M. C. 1999 : Season- and size-dependent risk taking in juvenile coho salmon: experimental evaluation of asset protection. Anim. Behav. 57, 923 933.
60. Relyea, R. A. 2001a : Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82, 523 540.
61. Relyea, R. A. 2001b : The relationship between predation risk and antipredator responses in larval anurans. Ecology 82, 541 554.
62. Relyea, R. A. 2003 : How prey respond to combined predators: a review and an empirical test. Ecology 84, 1827 1839.
63. Relyea, R. A. 2004 : Fine-tuned phenotypes: Tadpole plasticity under 16 combinations of predators and competitors. Ecology 85, 172 179.
64. Relyea, R. A. Werner, E. E. 1999 : Quantifying the relation between predator-induced behavior and growth performance in larval anurans. Ecology 80, 2117 2124.
65. Richardson, J. M. L. 2001 : A comparative study of activity levels in larval anurans and responses to the presence of different predators. Behav. Ecol. 12, 51 58.
66. Rochette, R. Himmelman, J. H. 1996 : Does vulnerability influence trade-offs made by whelks between predation risk and feeding opportunities? Anim. Behav. 52, 783 794.
67. Rochette, R., Dill, L. M. Himmelman, J. H. 1997 : A field test of threat sensitivity in a marine gastropod. Anim. Behav. 54, 1053 1062.
68. Salo, P., Korpimäki, E., Banks, P. B., Nordström, M. Dickman, C. R. 2007 : Alien predators are more dangerous than native predators to prey populations. Proc. R. Soc. Lond. 274B, 1237 1243.
69. Schmitz, O. J. 2005 : Behavior of predators and prey and links with population-level processes. In : Ecology of Predator-Prey Interactions (Barbosa, P. Castellanos, I., eds). Oxford University Press, Oxford, pp. 256 278.
70. Schoeppner, N. M. Relyea, R. A. 2008 : Detecting small environmental differences: risk-response curves for predator-induced behavior and morphology. Oecologia 154, 743 754.
71. Semlitsch, R. D. Gibbons, J. W. 1988 : Fish predation in size-structured populations of treefrog tadpoles. Oecologia 75, 321 326.
72. Sih, A. 1986 : Antipredator responses and the perception of danger by mosquito larvae. Ecology 67, 434 441.
73. Smith, G. R., Boyd, A., Dayer, C. B. Winter, K. E. in press : Behavioral responses of American toad and bullfrog tadpoles to the presence of cues from the invasive fish, Gambusia affinis. Biol. Invas. in press.
74. Stankowich, T. Blumstein, D. T. 2005 : Fear in animals: a meta-analysis and review of risk assessment. Proc. R. Soc. Lond. 272B, 2627 2634.
75. Swart, C. C. Taylor, R. C. 2004 : Behavioral interactions between the giant water bug (Belostoma lutarium) and tadpoles of Bufo woodhousii. Southeast. Nat. 3, 13 24.
76. Takahara, T., Kohmatsu, Y., Maruyama, A. Yamaoka, R. 2003 : Effects of fish chemical cues on tadpole survival. Ecol. Res. 18, 793 796.
77. Teplitsky, C., Plénet, S. Joly, P. 2003 : Tadpoles' responses to risk of fish introduction. Oecologia 134, 270 277.
78. Travis, J., Keen, W. H. Julianna, J. 1985 : The role of relative body size in a predator-prey relationship between dragonfly naiads and larval anurans. Oikos 45, 59 65.
79. Turner, A. M., Fetteroff, S. A. Bernot, R. J. 1999 : Predator identity and consumer behavior: differential effects of fish and crayfish on the habitat use of a freshwater snail. Oecologia 118, 242 247.
80. Van Buskirk, J. 2003 : Habitat partitioning in European and North American pond-breeding frogs and toads. Div. Distrib. 9, 399 410.
81. Wahle, R. A. 1992 : Body-size dependent anti-predator mechanisms of the American lobster. Oikos 65, 52 60.
82. Werner, E. E., Hall, D. J., Laughlin, D. R., Wagner, D. J., Wilsmann, L. A. Funk, F. C. 1977 : Habitat partitioning in a freshwater fish community. J. Fish. Res. Board Can. 34, 360 370.
83. Williams, P. J. Brown, J. A. 1991 : Developmental changes in foraging-predator avoidance trade-offs in larval lumpfish Cyclopterus lumpus. Mar. Ecol. Prog. Ser. 76, 53 60.
84. Wohlfahrt, B., Mikolajewski, D. J., Joop, G. Suhling, F. 2006 : Are behavioural traits in prey sensitive to the risk imposed by predatory fish?. Freshw. Biol. 51, 76 84.
85. Zhao, X., Ferrari, M. C. O. Chivers, D. P. 2006 : Threat-sensitive learning of predator odours by a prey fish. Behaviour 143, 1103 1121.