Testing the threat-sensitive predator avoidance hypothesis: Physiological responses and predator pressure in wild rabbits

Oecologia

Volumn 158, Issue 4, 2009, Pages 615-623

  Monclús, Raquel ^a   Palomares, Francisco ^b   Tablado, Zulima ^b   Martínez Fontúrbel, Ana ^b   Palme, Rupert ^c  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^c UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Fecal corticosterone metabolites; Oryctolagus cuniculus; Predator pressure; Threat sensitive predator avoidance hypothesis

Indexed keywords

CORTICOSTERONE;

ANTIPREDATOR DEFENSE; AVOIDANCE REACTION; CARNIVORE; CENSUS; FECES; FITNESS; FOOD AVAILABILITY; HYPOTHESIS TESTING; LAGOMORPH; METABOLITE; NATIONAL PARK; PHYSIOLOGICAL RESPONSE; PREDATION RISK; STEROID; WILD POPULATION;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; ESCAPE BEHAVIOR; FECES; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; POPULATION DENSITY; PREDATION; RABBIT;

ANIMALS; BEHAVIOR, ANIMAL; CORTICOSTERONE; ESCAPE REACTION; FECES; MODELS, BIOLOGICAL; POPULATION DENSITY; PREDATORY BEHAVIOR; RABBITS; STRESS, PHYSIOLOGICAL;

ANDALUCIA; DONANA NATIONAL PARK; EURASIA; EUROPE; SOUTHERN EUROPE; SPAIN;

ANIMALIA; MAMMALIA; ORYCTOLAGUS CUNICULUS;

EID: 57749186050     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-008-1201-0     Document Type: Article

References (73)

1. Allier C, González Bernáldez F, Díaz Ramírez L (1974) Mapa ecológico de la reserva biológica de Doñana. CSIC, Estación Biológica de Doñana, Sevilla
2. R Apfelbach CD Blanchard RJ Blanchard RA Hayes IS McGregor 2005 The effects of predator odors in mammalian prey species: a review of field and laboratory studies Neurosci Biobehav Rev 29 1123 1144
3. R Boonstra D Hik GR Singleton A Tinnikov 1998 The impact of predator-induced stress on the snowshoe hare cycle Ecol Monogr 79 371 394
4. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach. Springer-Verlag, New York
5. SG Carobrez OC Gasparotto B Buwalda B Bohus 2002 Long-term consequences of social stress on corticosterone and IL-1ß levels in endotoxin-challenged rats Phys Behav 76 99 105
6. M Clinchy L Zanette R Boonstra JC Wingfield JNM Smith 2004 Balancing food and predator pressure induces chronic stress in songbirds Proc R Soc B 271 2473 2479
7. JF Cockrem B Silverin 2002 Sight of a predator can stimulate a corticosterone response in the great tit (Parus major) Gen Comp Endocrinol 125 248 255
8. Cook CJ, Mellor DJ, Harris PJ, Ingram JR, Matthews LR (2001) Hands-on and hands-off measurement of stress. In: Moberg GP, Mench JA (eds) The biology of animal stress. Basic principles and implications for animal welfare. CABI Publishing, Oxon, pp 123-146
9. P Deviche JC Wingfield PJ Sharp 2000 Year-class differences in the reproductive system, plasma prolactin and corticosterone concentrations, and onset of prebasic molt in male dark-eyed juncos (Junco hyemalis) during the breeding period Gen Comp Endocrinol 118 425 435
10. AM Dufty J Clobert AP Møller 2002 Hormones, developmental plasticity and adaptation Trends Ecol Evol 17 190 196
11. MCO Ferrari DP Chivers 2006 Learning threat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information? Anim Behav 71 19 26
12. P Ferreras JF Beltrán JJ Aldama M Delibes 1997 Spatial organization and land tenure system of the endangered Iberian lynx (Lynx pardinus) J Zool 243 163 189
13. PE Foam MC Harvey RS Mirza GE Brown 2005 Heads up: Juvenile convict cichlids switch to threat-sensitive foraging tactics based on chemosensory information Anim Behav 70 601 607
14. W Goymann JC Wingfield 2004 Allostatic load, social status and stress hormones: the costs of social status matter Anim Behav 67 591 602
15. W Goymann ML East B Wachter OP Höner E Möstl TJ Van't Hof H Hofer 2001 Social, state-dependent and environmental modulation of faecal glucocorticoid levels in free ranging female spotted hyenas Proc R Soc B 268 2453 2459
16. TJ Greives JM Casto ED Ketterson 2007 Relative abundance of males to females affects behavior, condition and immune function in a captive population of dark-eyed juncos Junco hyemalis J Avian Biol 38 255 260
17. LA Hawkins AE Magurran JD Armstrong 2007 Innate abilities to distinguish between predator species and cue concentration in Atlantic salmon Anim Behav 73 1051 1057
18. GS Helfman 1989 Threat-sensitive predator avoidance in damselfish-trumpetfish interactions Behav Ecol Sociobiol 24 47 58
19. P Horat RD Semlitsch 1994 Effects of predation risk and hunger on the behaviour of two species of tadpoles Behav Ecol Sociobiol 34 393 401
20. S Huber R Palme W Arnold 2003 Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus) Gen Comp Endocrinol 130 48 54
21. LB Kats LM Dill 1998 The scent of death: chemosensory assessment of predation risk by prey animal Écoscience 5 361 394
22. B Kesavaraju K Damal SA Juliano 2007 Threat-sensitive behavioral responses to concentrations of water-borne cues from predation Ethology 113 199 206
23. AS Kitaysky JC Wingfield JF Piatt 1999 Dynamics of food availability, body condition and physiological stress response in breeding black-legged kittiwakes Funct Ecol 13 577 584
24. K Kotrschal K Hirschenhauser E Möstl 1998 The relationship between social stress and dominance is seasonal in greylag geese Anim Behav 55 171 176
25. C Kraus HG Rödel 2004 Where have all the cavies gone? Causes and consequences of predation by the minor grison on a wild cavy population Oikos 105 489 500
26. RC Kusch RS Mirza DP Chivers 2004 Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows Behav Ecol Sociobiol 55 551 555
27. RB Lanctot SA Hatch VA Gill M Eens 2003 Are corticosterone levels a good indicator of food availability and reproductive performance in a kittiwake colony? Horm Behav 43 489 502
28. MM Landys M Ramenofsky JC Wingfield 2006 Actions of glucocorticoids at a seasonal baseline as compared to stress-related levels in the regulation of periodic life processes Gen Comp Endocrinol 148 132 149
29. SL Lima LM Dill 1990 Behavioral decisions made under the risk of predation: a review and prospectus Can J Zool 68 619 640
30. L Lombardi N Fernández S Moreno 2007 Habitat use and spatial behaviour in the European rabbit in three Mediterranean environments Basic Appl Ecol 8 453 463
31. CJ Loose P Dawidowicz 1994 Trade-offs in diel vertical migration by zooplankton: the costs of predator avoidance Ecology 75 2255 2263
32. S Mañosa PJ Cordero 1992 Seasonal and sexual variation in the diet of the common buzzard in Northeastern Spain J Raptor Res 26 235 238
33. Matteri RL, Carroll JA, Dyer CJ (2001) Neuroendocrine responses to stress. In: Moberg GP, Mench JA (eds) The biology of animal stress. Basic principles and implications for animal welfare. CABI Publishing, Oxon, pp 43-76
34. McCullagh P, Nelder JA (1996) Generalized linear models. Monographs on statistics and applied probability 37. Chapman and Hall, London
35. RS Mirza A Mathis DP Chivers 2006 Does temporal variation in predation risk influence the intensity of antipredator responses? A test of the risk allocation hypothesis Ethology 112 44 51
36. R Monclús HG Rödel D von Holst J de Miguel 2005 Behavioural and physiological responses of naive European rabbits to predator odour Anim Behav 70 753 761
37. R Monclús HG Rödel R Palme D von Holst J de Miguel 2006 Non-invasive measurement of the physiological stress response of wild rabbits to the odour of a predator Chemoecology 16 25 29
38. R Monclús HG Rödel D von Holst 2006 Fox odour increases vigilance in European rabbits: a study under semi-natural conditions Ethology 112 1186 1193
39. E Möstl R Palme 2002 Hormones as indicators of stress Domest Anim Endocrinol 23 67 74
40. E Möstl S Meßmann E Bagu C Robia R Palme 1999 Measurement of glucocorticoid metabolite concentrations in faeces of domestic livestock J Vet Med 46 621 632
41. NJD Nagelkerke 1991 A note on a general definition of the coefficient of determination Biometrika 78 691 692
42. BC Nephew LM Romero 2003 Behavioral, physiological, and endocrine responses of starlings to acute increases in density Horm Behav 44 222 232
43. PA Nilsson C Brönmark LB Pettersson 1995 Benefits of a predator-induced morphology in crucian carp Oecologia 104 291 296
44. R Palme 2005 Measuring fecal steroids. Guidelines for practical application Ann NY Acad Sci 1046 1 6
45. F Palomares 2001 Comparison of 3 methods to estimate rabbit abundance in a Mediterranean environment Wildl Soc Bull 29 578 585
46. F Palomares M Delibes 1993 Social organization in the Egyptian mongoose: group size, spatial behaviour and inter-individual contacts in adults Anim Behav 45 917 925
47. F Palomares P Ferreras A Travaini M Delibes 1998 Co-existence between Iberian lynx and Egyptian mongooses: Estimating interaction strength by structural equation modelling and testing by an observational study J Anim Ecol 67 967 978
48. MS Pollock RG Friesen RJ Pollock RC Kusch DP Chivers 2005 The avoidance response of fathead minnows to chemical alarm cues: Understanding the effects of donor gender and breeding condition Chemoecology 15 205 209
49. VV Pravosudov AS Kitaysky JC Wingfield 2001 Long-term unpredictable foraging conditions and physiological stress response in mountain chickadees (Poecile gambeli) Gen Comp Endocrinol 123 324 331
50. EL Preisser DI Bolnick MF Benard 2005 Scared to death? The effects of intimidation in predator-prey interactions Ecology 86 501 509
51. MH Puttlitz DP Chivers JM Kiesecker AR Blaustein 1999 Threat-sensitive predator avoidance by larval pacific treefrogs (Amphibia, Hylidae) Ethology 105 449 456
52. SA Raouf LC Smith M Bomberger Brown JC Wingfield CR Brown 2006 Glucocorticoid hormone levels increase with group size and parasite load in cliff swallows Anim Behav 71 39 48
53. E Revilla F Palomares 2002 Spatial organization, group living and ecological correlates in low-density population of Eurasian badgers, Meles meles J Anim Ecol 71 497 512
54. S Rivas-Martínez M Costa S Castroviejo E Valdes 1980 Vegetación de Doñana (Huelva, España) Lazaroa 2 1 189
55. HG Rödel A Bora J Kaiser P Kaetzke M Khaschei D von Holst 2004 Density dependent reproduction in the European rabbit: a consequence of individual response and age-dependent reproductive performance Oikos 104 529 539
56. HG Rödel A Bora P Kaetzke M Khaschei H Hutzelmeyer D von Holst 2004 Over-winter survival in subadult European rabbits: weather effects, density dependence, and the impact of individual characteristics Oecologia 140 566 576
57. K Rogovin JA Randall I Kolosova M Moshkin 2003 Social correlates of stress in adult males of the great gerbil, Rhombomys opimus, in years of high and low population densities Horm Behav 43 132 139
58. Román J, Palomares F, Revilla E, Rodríguez A, Tablado Z, López-Bao JV, d'Amico M (2006) Seguimiento científico de las actuaciones del proyecto LIFE-naturaleza Recuperación de las poblaciones de lince ibérico en Andalucía. LIFE 02NAT/8609. Final Report submitted to Consejería de Medio Ambiente, Junta de Andalucía, Sevilla, Spain, p 94
59. LM Romero 2002 Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates Gen Comp Endocrinol 128 1 24
60. Sapolsky RM (1992) Neuroendocrinology of the stress-response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioural Endocrinology. MIT Press, Cambridge, pp 287-324
61. C Teplitsky S Plénet P Joly 2005 Costs and limits of dosage response to predation risk: to what extent can tadpoles invest in anti-predator morphology? Oecologia 145 364 370
62. C Touma R Palme 2005 Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of a validation Ann NY Acad Sci 1046 54 74
63. C Touma R Palme N Sachser 2004 Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones Horm Behav 45 10 22
64. C Touma N Sachser E Möstl R Palme 2003 Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice Gen Comp Endocrinol 130 267 278
65. JP Veiga F Hiraldo 1990 Food habits and the survival and growth of nestlings in two sympatric kites (Milvus milvus and Milvus nigrans) Holarctic Ecol 13 62 71
66. Villafuerte R (1994) Riesgo de predación y estrategias defensivas del conejo, Oryctolagus cuniculus, en el parque nacional de Doñana. Ph.D. Thesis. University of Córdoba, Córdoba, Spain
67. E von Borell J Ladewig 1992 Relationship between behavior and adrenocortical response pattern in domestic pigs App Anim Behav Sci 34 195 206
68. D von Holst 1998 The concept of stress and its relevance for animal behavior Adv Stud Behav 27 1 131
69. D von Holst H Hutzelmeyer P Kaetzke M Khaschei R Schönheiter 1999 Social rank, stress, fitness, and life expectancy in wild rabbits Naturwissenschaften 86 388 393
70. JM Wallage-Drees 1989 A field study of seasonal changes in Circardian activity of rabbits Z Säugetierk 54 22 30
71. T Weingrill DA Gray L Barrett SP Henzi 2004 Fecal corticosteroid levels in free-ranging female chacma baboons: Relationships to dominance, reproductive state and environmental factors Horm Behav 45 259 269
72. JC Wingfield 2005 The concept of allostasis: coping with a capricious environment J Mamm 86 248 254
73. SC Zapata A Travaini P Ferreras M Delibes 2007 Analysis of trophic structure of two carnivore assemblages by means of guild identification Eur J Wildl Res 53 276 286