Increased predation risk on mothers affects survival of parasites feeding on the offspring

Animal Behaviour

Volumn 81, Issue 5, 2011, Pages 1071-1075

  Coslovsky, Michael ^a   Richner, Heinz ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Great tit; Maternal effect; Multiple trophic levels; Parasite; Parus major; Predation; Prenatal stress

Indexed keywords

COEVOLUTION; DEFENSE MECHANISM; ECTOPARASITE; EGG; EXPERIMENTAL STUDY; FEEDING BEHAVIOR; FLEA; HABITAT TYPE; HOST-PARASITE INTERACTION; LABORATORY METHOD; MATERNAL EFFECT; NESTLING; PARENTAL INVESTMENT; PASSERINE; POPULATION DYNAMICS; PREDATION RISK; PREDATOR-PREY INTERACTION; RESOLUTION; RESOURCE ALLOCATION; STANDARDIZATION; SURVIVAL; TRADE-OFF;

AVES; CERATOPHYLLUS GALLINAE; PARUS MAJOR; RAPTORES; SIPHONAPTERA (FLEAS); TURDUS PHILOMELOS;

EID: 79953306858     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2011.02.023     Document Type: Article

References (52)

1. Allen D.E., Little T.J. Identifying energy constraints to parasite resistance. Journal of Evolutionary Biology 2011, 24:224-229.
2. Apanius V. Stress and immune defense. Stress and Behavior 1998, 133-153. Academic Press, San Diego. A.P. Møller, M. Milinski, P.J.B. Slater (Eds.).
3. Bakker J.M., van Rees E.P. Prenatal stress and immunocompetence in later life. Developmental Brain Dysfunction 1997, 10:445-461.
4. Boulinier T., Staszewski V. Maternal transfer of antibodies: raising immuno-ecology issues. Trends in Ecology & Evolution 2008, 23:282-288.
5. Chin E.H., Love O.P., Verspoor J.J., Williams T.D., Rowley K., Burness G. Juveniles exposed to embryonic corticosterone have enhanced flight performance. Proceedings of the Royal Society B 2009, 276:499-505.
6. Cockrem J.F., Silverin B. Sight of a predator can stimulate a corticosterone response in the great tit (Parus major). General and Comparative Endocrinology 2002, 125:248-255.
7. Coe C.L., Lubach G.R. Prenatal origins of individual variation in behavior and immunity. Neuroscience and Biobehavioral Reviews 2005, 29:39-49.
8. Coslovsky, M. & Richner, H. In press. Predation risk affects offspring growth via maternal effects. Functional Ecology, doi:10.1111/j.1365-2435.2011.01834.x.
9. Cresswell W. Non-lethal effects of predation in birds. Ibis 2008, 150:3-17.
10. Criscuolo F., Monaghan P., Nasir L., Metcalfe N.B. Early nutrition and phenotypic development: 'catch-up' growth leads to elevated metabolic rate in adulthood. Proceedings of the Royal Society B 2008, 275:1565-1570.
11. Daan S., Dijkstra C., Tinbergen J.M. Family planning in the kestrel (Falco tinnunculus): the ultimate control of covariation of laying date and clutch size. Behaviour 1990, 114:83-116.
12. Devevey G., Bize P., Fournier S., Person E., Christe P. Testing the predictive adaptive response in a host-parasite system. Functional Ecology 2010, 24:178-185.
13. Friman V.-P., Lindstedt C., Hiltunen T., Laakso J., Mappes J. Predation on multiple trophic levels shapes the evolution of pathogen virulence. PLoS ONE 2009, 4:e6761.
14. Gallizzi K., Alloitteau O., Harrang E., Richner H. Fleas, parental care, and transgenerational effects on tick load in the great tit. Behavioral Ecology 2008, 19:1225-1234.
15. Gentle L.K., Gosler A.G. Fat reserves and perceived predation risk in the great tit, Parus major. Proceedings of the Royal Society B 2001, 268:487-491.
16. Gosler A. The Great Tit 1993, Hamlyn, London.
17. Gosler A.G., Greenwood J.J.D., Perrins C. Predation risk and the cost of being fat. Nature 1995, 377:621-623.
18. Götz A.A., Stefanski V. Psychosocial maternal stress during pregnancy affects serum corticosterone, blood immune parameters and anxiety behaviour in adult male rat offspring. Physiology and Behavior 2007, 90:108-115.
19. Groothuis T.G.G., Müller W., von Engelhardt N., Carere C., Eising C. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuroscience and Biobehavioral Reviews 2005, 29:329-352.
20. Hall S.R., Duffy M.A., Caceres C.E. Selective predation and productivity jointly drive complex behavior in host-parasite systems. American Naturalist 2005, 165:70-81.
21. Hatcher M.J., Dick J.T.A., Dunn A.M. How parasites affect interactions between competitors and predators. Ecology Letters 2006, 9:1253-1271.
22. Holt Robert, D., Roy M. Predation can increase the prevalence of infectious disease. American Naturalist 2007, 169:690-699.
23. Krasnov B.R., Khokhlova I.S., Arakelyan M.S., Degen A.A. Is a starving host tastier? Reproduction in fleas parasitizing food-limited rodents. Functional Ecology 2005, 19:625-631.
24. Lochmiller R.L., Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity?. Oikos 2000, 88:87-98.
25. Marshall D.J., Uller T. When is a maternal effect adaptive?. Oikos 2007, 116:1957-1963.
26. Martin L.B., Gilliam J., Han P., Lee K., Wikelski M. Corticosterone suppresses cutaneous immune function in temperate but not tropical house sparrows, Passer domesticus. General and Comparative Endocrinology 2005, 140:126-135.
27. Mathot K.J., van den Hout P.J., Piersma T. Differential responses of red knots, Calidris canutus, to perching and flying sparrowhawk, Accipiter nisus, models. Animal Behaviour 2009, 77:1179-1185.
28. Merlot E., Couret D., Otten W. Prenatal stress, fetal imprinting and immunity. Brain, Behavior, and Immunity 2008, 22:42-51.
29. Metcalfe N.B., Monaghan P. Compensation for a bad start: grow now, pay later?. Trends in Ecology & Evolution 2001, 16:254-260.
30. Møller A.P. Interactions between interactions. Annals of the New York Academy of Sciences 2008, 1133:180-186.
31. Mousseau T.A., Fox C.W. The adaptive significance of maternal effects. Trends in Ecology & Evolution 1998, 13:403-407.
32. Mousseau T.A., Fox C.W. Maternal Effects as Adaptations 1998, Oxford University Press, Oxford.
33. Navarro C., de Lope F., Marzal A., Møller A.P. Predation risk, host immune response, and parasitism. Behavioral Ecology 2004, 15:629-635.
34. Oppliger A., Clobert J., Lecomte J., Lorenzon P., Boudjemadi K., John-Alder H.B. Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara. Ecology Letters 1998, 1:129-138.
35. Owen J.P., Delany M.E., Cardona C.J., Bickford A.A., Mullens B.A. Host inflammatory response governs fitness in an avian ectoparasite, the northern fowl mite (Ornithonyssus sylviarum). International Journal for Parasitology 2009, 39:789-799.
36. Packer C., Holt R.D., Hudson P.J., Lafferty K.D., Dobson A.P. Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecology Letters 2003, 6:797-802.
37. Ponton F., Lebarbenchon C., Lefevre T., Biron D.G., Duneau D., Hughes D.P., Thomas F. Parasitology: parasite survives predation on its host. Nature 2006, 440:p. 756.
38. Poulin R. Evolutionary Ecology of Parasites 1997, Chapman & Hall, London.
39. Råberg L., Graham A.L., Read A.F. Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B 2009, 364:37-49.
40. Rigby M.C., Jokela J. Predator avoidance and immune defence: costs and trade-offs in snails. Proceedings of the Royal Society B 2000, 267:171-176.
41. Romero L.M. Physiological stress in ecology: lessons from biomedical research. Trends in Ecology & Evolution 2004, 19:249-255.
42. Saino N., Bertacche V., Ferrari R.P., Martinelli R., Møller A.P., Stradi R. Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection and paternal ornamentation. Proceedings of the Royal Society B 2002, 269:1729-1733.
43. Saino N., Romano M., Ferrari R.P., Martinelli R., Møller A.P. Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. Journal of Experimental Zoology 2005, 303A:998-1006.
44. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 2000, 21:55-89.
45. Scheuerlein A., Van't Hof T.J., Gwinner E. Predators as stressors? Physiological and reproductive consequences of predation risk in tropical stonechats (Saxicola torquata axillaris). Proceedings of the Royal Society B 2001, 268:1575-1582.
46. Sheldon B.C., Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution 1996, 11:317-321.
47. Storm J.J., Lima S.L. Mothers forewarn offspring about predators: a transgenerational maternal effect on behavior. American Naturalist 2010, 175:382-390.
48. Thomson R.L., Tomás G., Forsman J.T., Broggi J., Mönkkönen M. Predator proximity as a stressor in breeding flycatchers: mass loss, stress protein induction, and elevated provisioning. Ecology 2010, 91:1832-1840.
49. Tschirren B., Bischoff L.L., Saladin V., Richner H. Host condition and host immunity affect parasite fitness in a bird-ectoparasite system. Functional Ecology 2007, 21:372-378.
50. Tschirren B., Siitari H., Saladin V., Richner H. Transgenerational immunity in a bird-ectoparasite system: do maternally transferred antibodies affect parasite fecundity or the offspring's susceptibility to fleas?. Ibis 2009, 151:160-170.
51. Verhulst S., Nilsson J.-Å. The timing of birds' breeding seasons: a review of experiments that manipulated timing of breeding. Philosophical Transactions of the Royal Society B 2008, 363:399-410.
52. Ward H.E., Johnson E.A., Salm A.K., Birkle D.L. Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain. Physiology and Behavior 2000, 70:359-366.