Ectoparasitism and stress hormones: Strategy of host exploitation, common host-parasite history and energetics matter

Journal of Animal Ecology

Volumn 83, Issue 5, 2014, Pages 1113-1123

  St Juliana, Justin R ^a,b,c   Khokhlova, Irina S ^b   Wielebnowski, Nadja ^d,e   Kotler, Burt P ^b   Krasnov, Boris R ^b  

^a INDIANA STATE UNIVERSITY   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c IVY TECH COMMUNITY COLLEGE   (United States)

^d BROOKFIELD ZOO   (United States)

^e The Oregon Zoo   (United States)

Author keywords

Corticosterone; Faecal glucocorticoid metabolites; Fleas; Parasitism; Principal host; Rodents; Stress

Indexed keywords

ADAPTATION; BODY MASS; ECTOPARASITE; FLY; HORMONE; HOST-PARASITE INTERACTION; METABOLITE; PARASITISM; PHYLOGENETICS; PHYSIOLOGICAL RESPONSE; RODENT;

ACOMYS CAHIRINUS; ACOMYS RUSSATUS; GERBILLUS ANDERSONI; GERBILLUS DASYURUS; GERBILLUS NANUS; GERBILLUS PYRAMIDUM; MAMMALIA; MERIONES CRASSUS; MESOCRICETUS AURATUS; PARAPULEX CHEPHRENIS; RODENTIA; SIPHONAPTERA (FLEAS); SYNOSTERNUS CLEOPATRAE; XENOPSYLLA; XENOPSYLLA CONFORMIS; XENOPSYLLA RAMESIS;

GLUCOCORTICOID;

ANIMAL; BODY WEIGHT; CHEMISTRY; EVOLUTION; FECES; FLEA; HOST PARASITE INTERACTION; HOST RANGE; MURIDAE; PARASITOLOGY; PHYLOGENY; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; BIOLOGICAL EVOLUTION; BODY WEIGHT; FECES; GLUCOCORTICOIDS; HOST SPECIFICITY; HOST-PARASITE INTERACTIONS; MURIDAE; PHYLOGENY; SIPHONAPTERA; STRESS, PHYSIOLOGICAL;

EID: 84906320241     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/1365-2656.12217     Document Type: Article

References (103)

1. Abiadh, A., Chetoui, M., Lamine-Cheniti, T., Capanna, E. & Colangelo, P. (2010) Molecular phylogenetics of the genus Gerbillus (Rodentia, Gerbillinae): implications for systematics, taxonomy and chromosomal evolution. Molecular Phylogenetics and Evolution, 56, 513-518.
2. Aguirre-Macedo, M.L., Vidal-Martínez, V.M., González-Solís, D. & Caballero, P.I. (2007) Helminth communities of four commercially important fish species from Chetumal Bay, Mexico. Journal of Helminthology, 81, 19-31.
3. Arbiv, A., Khokhlova, I.S., Ovadia, O., Novoplansky, A. & Krasnov, B.R. (2012) Use it or lose it: reproductive implications of experimental host shifting in a haematophagous ectoparasite. Journal of Evolutionary Biology, 25, 1140-1147.
4. Barnard, C.J., Behnke, J.M., Bajer, A., Bray, D., Race, T., Frake, K. et al. (2002) Local variation in endoparasite intensities of bank voles (Clethrionomys glareolus) from ecologically similar sites: morphometric and endocrine correlates. Journal of Helminthology, 76, 103-113.
5. Barnard, C.J., Kulis, K., Behnke, J.M., Bajer, A., Gromadzka-Ostrowska, J., Stachon, M. et al. (2003) Local variation in helminth burdens of bank voles (Clethrionomys glareolus) from ecologically similar sites: temporal stability and relationships with hormone concentrations and social behaviour. Journal of Helminthology, 77, 185-195.
6. Barnes, P.J. (1998) Anti-inflammatory actions of glucocorticoids: molecular mechanisms. Clinical Science, 94, 557-572.
7. Barton, K. (2013) MuMIn: Multi-Model Inference. R Package Version 1.9.5. http://CRAN.R-project.org/package=MuMIn
8. Baucom, R.S. & de Roode, J.C. (2011) Ecological immunology and tolerance in plants and animals. Functional Ecology, 25, 18-28.
9. Beaty, B.J. & Marquardt, W.C. (1996) The Biology of Disease Vectors. University Press of Colorado, Niwot, Colorado.
10. Bininda-Emonds, O.R., Cardillo, M., Jones, K.E., MacPhee, R.D., Beck, R.M., Grenyer, R. et al. (2007) The delayed rise of present-day mammals. Nature, 446, 507-512.
11. Bohus, B., Benus, R.F., Fokkema, D.S., Koolhaas, J.M., Nyakas, C., van Oortmerssen, G.A. et al. (1987) Neuroendocrine states and behavioral and physiological stress responses. Progress in Brain Research (eds V.M.W.E.R. de Kloet & D.D. Wied ), pp. 57-70. Elsevier, Amsterdam.
12. Boonstra, R. (2013) Reality as the leading cause of stress: rethinking the impact of chronic stress in nature. Functional Ecology, 27, 11-23.
13. Boughton, R.K., Atwell, J.W. & Schoech, S.J. (2006) An introduced generalist parasite, the sticktight flea (Echidnophaga gallinacea), and its pathology in the threatened Florida scrub-jay (Aphelocoma coerulescens). Journal of Parasitology, 92, 941-948.
14. Brown, T.T. & Fuller, C.A. (2006) Stress and parasitism of white-footed mice (Peromyscus leucopus) in dry and floodplain environments. Canadian Journal of Zoology, 84, 1833-1839.
15. Carr, J.A. & Summers, C.H. (2002) Is stress more than a disease? A comparative look at the adaptativeness of stress. Integrative and Comparative Biology, 42, 505-507.
16. Cavigelli, S.A. & McClintock, M.K. (2003) Fear of novelty in infant rats predicts adult corticosterone dynamics and an early death. Proceedings of the National Academy of Sciences of the United States of America, 100, 16131-16136.
17. Charbonnel, N., Chaval, Y., Berthier, K., Deter, J., Morand, S., Palme, R. et al. (2008) Stress and demographic decline: a potential effect mediated by impairment of reproduction and immune function in cyclic vole populations. Physiological and Biochemical Zoology: PBZ, 81, 63-73.
18. Chevret, P. & Dobigny, G. (2005) Systematics and evolution of the subfamily Gerbillinae (Mammalia, Rodentia, Muridae). Molecular Phylogenetics and Evolution, 35, 674-688.
19. Christe, P., Richner, H. & Oppliger, A. (1996) Begging, food provisioning, and nestling competition in great tit broods infested with ectoparasites. Behavioral Ecology, 7, 127-131.
20. Combes, C. (2001) Parasitism. The Ecology and Evolution of Intimate Interactions. University of Chicago Press, Chicago, Illinois.
21. De Lope, F., Møller, A.P. & De la Cruz, C. (1998) Parasitism, immune response and reproductive success in the house martin Delichon urbica. Oecologia, 114, 188-193.
22. Degen, A.A. (2006) Effect of macroparasites on the energy budget of small mammals. Micromammals and Macroparasites: From Evolutionary Ecology to Management (eds S. Morand, B.R. Krasnov & R. Poulin ), pp. 371-399. Springer-Verlag, Tokyo, Berlin, Heidelberg, New York.
23. Desantis, L.M., Delehanty, B., Weir, J.T. & Boonstra, R. (2013) Mediating free glucocorticoid levels in the blood of vertebrates: are corticosteroid-binding proteins always necessary? Functional Ecology, 27, 107-119.
24. Dhabhar, F.S. (1998) Stress-induced enhancement of cell-mediated immunity. Annals of the New York Academy of Sciences, 840, 359-372.
25. Dhabhar, F.S. & McEwen, B.S. (1997) Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain, Behavior, and Immunity, 11, 286-306.
26. Dhabhar, F.S. & McEwen, B.S. (1999) Enhancing versus suppressive effects of stress hormones on skin immune function. Proceedings of the National Academy of Sciences of the United States of America, 96, 1059-1064.
27. Dhabhar, F.S. & McEwen, B.S. (2001) Bidirectional effects of stress and glucocorticoid hormones on immune function: possible explanations for paradoxical observations. Psychoneuroimmunology, 3rd edn (eds. R. Ader, D.L. Felten & N. Cohen ), pp. 301-338. Academic Press, San Diego, California.
28. Dlugosz, E.M., Harris, B.N., Saltzman, W. & Chappell, M.A. (2012) Glucocorticoids, aerobic physiology, and locomotor behavior in California mice. Physiological and Biochemical Zoology, 85, 671-683.
29. Dogiel, V.A., Petrushevski, G.K. & Polyanski, Y.I. (1961) Parasitology of Fishes. Oliver & Boyd, Edinburgh, London.
30. Ebert, D. (2005) Ecology, Epidemiology, and Evolution of Parasitism in Daphnia. National Center for Biotechnology Information (US), Bethesda, Maryland.
31. Giorgi, M.S., Arlettaz, R., Christe, P. & Vogel, P. (2001) The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). Proceedings of the Royal Societyof London. Series B, Biological Sciences, 268, 2071-2075.
32. Gooderham, K. & Schulte-Hostedde, A. (2011) Macroparasitism influences reproductive success in red squirrels (Tamiasciurus hudsonicus). Behavioral Ecology, 22, 1195-1200.
33. Goüy de Bellocq, J., Charbonnel, N. & Morand, S. (2008) Coevolutionary relationship between helminth diversity and MHC class II polymorphism in rodents. Journal of Evolutionary Biology, 21, 1144-1150.
34. Harper, J.M. & Austad, S.N. (2000) Fecal glucocorticoids: a non-invasive method of measuring adrenal activity in wild and captive rodents. Physiological and Biochemical Zoology, 73, 12-22.
35. Harris, B.N., Saltzman, W., de Jong, T.R. & Milnes, M. (2012) Hypothalamic-pituitary-adrenal (HPA) axis function in the California mouse (Peromyscus californicus): changes in baseline activity, reactivity, and fecal excretion of glucocorticoids across the diurnal cycle. General and Comparative Endocrinology, 179, 436-450.
36. Hart, B.L. (1990) Behavioral adaptations to pathogens and parasites: five strategies. Neuroscience and Biobehavioral Reviews, 14, 273-294.
37. Harvey, P.H. & Pagel, M.D. (1991) The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.
38. Hawlena, H., Abramsky, Z. & Krasnov, B.R. (2005) Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia, 146, 200-208.
39. Hawlena, H., Krasnov, B.R., Abramsky, Z., Khokhlova, I.S., Saltz, D., Kam, M. et al. (2006) Flea infestation and energy requirements of rodent hosts: are there general rules? Functional Ecology, 20, 1028-1036.
40. Hawlena, H., Krasnov, B.R., Abramsky, Z., Khokhlova, I.S., Goüy de Bellocq, J. & Pinshow, B. (2008) Effects of food abundance, age, and flea infestation on the body condition and immunological variables of a rodent host, and their consequences for flea survival. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 150, 66-74.
41. Helios De Rosario-Martinez, H. (2013) phia: Post-Hoc Interaction Analysis. R Package Version 0.1-5. http://CRAN.R-project.org/package=phia.
42. Ioff, I.G. (1941) Ecology of Fleas in Relevance to their Medical Importance. Pyatygorsk Publishers, Pyatygorsk, USSR. (In Russian).
43. Jansa, S.A. & Weksler, M. (2004) Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Molecular Phylogenetics and Evolution, 31, 256-276.
44. Kam, M., Degen, A.A., Khokhlova, I.S., Krasnov, B.R. & Geffen, E. (2010) Do fleas affect energy expenditure of their free-living hosts? PLoS ONE, 5, e13686.
45. Kedra, A.H., Kruszewicz, A.G., Mazgajski, T.D. & Modlińska, E. (1996) The effects of the presence of fleas in nest boxes on fledglings of pied flycatchers and great tits. Acta Parasitologica, 41, 211-213.
46. Khokhlova, I.S., Krasnov, B.R., Kam, M., Burdelova, N.I. & Degen, A.A. (2002) Energy cost of ectoparasitism: the flea Xenopsylla ramesis on the desert gerbil Gerbillus dasyurus. Journal of Zoology, 258, 349-354.
47. Khokhlova, I.S., Spinu, M., Krasnov, B.R. & Degen, A.A. (2004a) Immune response to fleas in a wild desert rodent: effect of parasite species, parasite burden, sex of host and host parasitological experience. Journal of Experimental Biology, 207, 2725-2733.
48. Khokhlova, I.S., Spinu, M., Krasnov, B.R. & Degen, A.A. (2004b) Immune responses to fleas in two rodent species differing in natural prevalence of infestation and diversity of flea assemblages. Parasitology Research, 94, 304-311.
49. Khokhlova, I.S., Ghazaryan, L., Krasnov, B.R. & Degen, A.A. (2008) Effects of parasite specificity and previous infestation of hosts on the feeding and reproductive success of rodent-infesting fleas. Functional Ecology, 22, 530-536.
50. Koren, L., Mokady, O., Karaskov, T., Klein, J., Koren, G. & Geffen, E. (2002) A novel method using hair for determining hormonal levels in wildlife. Animal Behaviour, 63, 403-406.
51. Krasnov, B.R. (2008) Functional and Evolutionary Ecology of Fleas: A Model for Ecological Parasitology. Cambridge University Press, Cambridge, England.
52. Krasnov, B.R., Khokhlova, I.S. & Shenbrot, G.I. (2004a) Sampling fleas: the reliability of host infestation data. Medical and Veterinary Entomology, 18, 232-240.
53. Krasnov, B.R., Shenbrot, G.I., Medvedev, S.G., Vatschenok, V.S. & Khokhlova, I.S. (1997) Host-habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev desert. Parasitology, 114, 159-173.
54. Krasnov, B.R., Hastriter, M.W., Medvedev, S.G., Shenbrot, G.I., Khokhlova, I.S. & Vashchenok, V.S. (1999) Additional records of fleas (Siphonaptera) on wild rodents in the southern part of Israel. Israel Journal of Zoology, 45, 333-340.
55. Krasnov, B.R., Khokhlova, I.S., Oguzoglu, I. & Burdelova, N.V. (2002) Host discrimination by two desert fleas using an odour cue. Animal Behaviour, 64, 33-40.
56. Krasnov, B.R., Shenbrot, G.I., Khokhlova, I.S. & Poulin, R. (2004b) Relationships between parasite abundance and the taxonomic distance among a parasite's host species: an example with fleas parasitic on small mammals. International Journal for Parasitology, 34, 1289-1297.
57. Lochmiller, R.L. & Deerenberg, C. (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88, 87-98.
58. Malisch, J.L., Saltzman, W., Gomes, F.R., Rezende, E.L., Jeske, D.R. & Garland, T. Jr (2007) Baseline and stress-induced plasma corticosterone concentrations of mice selectively bred for high voluntary wheel running. Physiological and Biochemical Zoology, 80, 146-156.
59. Mazgajski, T.D., Kedra, A.H., Modlińska, E. & Samborski, J. (1997) Fleas Siphonaptera influence the condition of Starling Sturnus vulgaris nestlings. Acta Ornithologica, 32, 185-190.
60. Millspaugh, J.J. & Washburn, B.E. (2004) Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. General and Comparative Endocrinology, 138, 189-199.
61. Møller, A.P. & Rózsa, L. (2005) Parasite biodiversity and host defenses: chewing lice and immune response of their avian hosts. Oecologia, 142, 169-176.
62. Monello, R.J., Millspaugh, J.J., Woods, R.J. & Gompper, M.E. (2010) The influence of parasites on faecal glucocorticoid metabolite levels in raccoons: an experimental assessment in a natural setting. Journal of Zoology, 282, 100-108.
63. Mooring, M.S., Blumstein, D.T. & Stoner, C.J. (2004) The evolution of parasite-defence grooming in ungulates. Biological Journal of the Linnean Society, 81, 17-37.
64. Mooring, M.S., Benjamin, J.E., Harte, C.R. & Herzog, N.B. (2000) Testing the interspecific body size principle in ungulates: the smaller they come, the harder they groom. Animal Behaviour, 60, 35-45.
65. Mooring, M.S., Reisig, D.D., Niemeyer, J.M. & Osborne, E.R. (2002) Sexually and developmentally dimorphic grooming: a comparative survey of the ungulata. Ethology, 108, 911-934.
66. Morand, S. & Poulin, R. (2000) Nematode parasite species richness and the evolution of spleen size in birds. Canadian Journal of Zoology, 78, 1356-1360.
67. Möstl, E. & Palme, R. (2002) Hormones as indicators of stress. Domestic Animal Endocrinology, 23, 67-74.
68. Munck, A., Guyre, P.M. & Holbrook, N.J. (1984) Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocrine Reviews, 5, 25-44.
69. Nikitina, N.A. & Nikolaeva, G.A. (1981) A study of the ability of rodents to clean themselves of specific and nonspecific fleas. Zoologicheskiǐ Zhurnal, 60, 165-167.
70. Palme, R. (2005) Measuring fecal steroids: guidelines for practical application. Annals of the New York Academy of Sciences, 1046, 75-80.
71. Paradis, E., Claude, J. & Strimmer, K. (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289-290.
72. Peckett, A.J., Wright, D.C. & Riddell, M.C. (2011) The effects of glucocorticoids on adipose tissue lipid metabolism. Metabolism, 60, 1500-1510.
73. Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D. & the R Development Core Team. (2013) nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3.1-108.
74. Poulin, R. (2005) Relative infection levels and taxonomic distances among the host species used by a parasite: insights into parasite specialization. Parasitology, 130, 109-115.
75. Poulin, R. (2007) Evolutionary Ecology of Parasites: From Individuals to Communities, 2nd edn. Princeton University Press, Princeton, New Jersey.
76. R Development Core Team. (2012) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.
77. Råberg, L., Graham, A.L. & Read, A.F. (2009) Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society of London, 364, 37-49.
78. Raveh, A., Kotler, B.P., Abramsky, Z. & Krasnov, B.R. (2011) Driven to distraction: detecting the hidden costs of flea parasitism through foraging behaviour in gerbils. Ecology Letters, 14, 47-51.
79. Ribeiro, J.M. (1987) Role of saliva in blood-feeding by arthropods. Annual Review of Entomology, 32, 463-478.
80. Ribeiro, J.M. (1989) Role of saliva in tick/host interactions. Experimental and Applied Acarology, 7, 15-20.
81. Richner, H., Oppliger, A. & Christe, P. (1993) Effect of an ectoparasite on reproduction in great tits. Journal of Animal Ecology, 62, 703-710.
82. Ritter, R.C. & Epstein, A.N. (1974) Saliva lost by grooming: a major item in the rat's water economy. Behavioral Biology, 11, 581-585.
83. Robar, N., Murray, D.L. & Burness, G. (2011) Effects of parasites on host energy expenditure: the resting metabolic rate stalemate. Canadian Journal of Zoology, 89, 1146-1155.
84. Sapolsky, R.M., Romero, L.M. & Munck, A.U. (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21, 55-89.
85. Schmid-Hempel, P. & Ebert, D. (2003) On the evolutionary ecology of specific immune defence. Trends in Ecology & Evolution, 18, 27-32.
86. Scott, M.E. & Lewis, J.W. (1987) Population dynamics of helminth parasites in wild and laboratory rodents. Mammal Review, 17, 95-103.
87. Sheriff, M.J., Dantzer, B., Delehanty, B., Palme, R. & Boonstra, R. (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia, 166, 869-887.
88. Šimková, A., Ottová, E. & Morand, S. (2006) MHC variability, life traits and parasite diversity of European cyprinid fish. Evolutionary Ecology, 20, 465-477.
89. Šimková, A., Lafond, T., Ondračková, M., Jurajda, P., Ottová, E. & Morand, S. (2008) Parasitism, life history traits and immune defence in cyprinid fish from Central Europe. BMC Evolutionary Biology, 8, 29.
90. Słomczyńskii, R., Kaliński, A., Wawrzyniak, J., Bańbura, M., Skwarska, J., Zieliński, P. et al. (2006) Effects of experimental reduction in nest microparasite and macroparasite loads on nestling hemoglobin level in blue tits Parus caeruleus. Acta Oecologica, 30, 223-227.
91. Solomon, M.B., Sakai, R.R., Woods, S.C. & Foster, M.T. (2011) Differential effects of glucocorticoids on energy homeostasis in Syrian hamsters. American Journal of Physiology. Endocrinology and Metabolism, 301, E307-E316.
92. Touma, C. & Palme, R. (2005) Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Annals of the New York Academy of Sciences, 1046, 54-74.
93. Tracey, K.J. (2002) The inflammatory reflex. Nature, 420, 853-859.
94. Traub, R. (1972) Relationship between spines, combs and other skeletal features of fleas (Siphonaptera) and vestiture, affinities and habits of their hosts. Journal of Medical Entomology, 9, 601.
95. Tripet, F., Glaser, M. & Richner, H. (2002) Behavioural responses to ectoparasites: time-budget adjustments and what matters to Blue Tits Parus caeruleus infested by fleas. IBIS, 144, 461-469.
96. Wasser, S.K., Hunt, K.E., Brown, J.L., Cooper, K., Crockett, C.M., Bechert, U. et al. (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. General and Comparative Endocrinology, 120, 260-275.
97. Wedekind, C. (1992) Detailed information about parasites revealed by sexual ornamentation. Proceedings of the Royal Society of London. Series B, Biological Sciences, 247, 169-174.
98. Wegner, K.M., Kalbe, M., Kurtz, J., Reusch, T.B. & Milinski, M. (2003) Parasite selection for immunogenetic optimality. Science, 301, 1343.
99. Weil, Z.M., Martin, L.B. & Nelson, R.J. (2006) Interactions among immune, endocrine, and behavioural response to infection. Micromammals and Macroparasites: From Evolutionary Ecology to Management (eds S. Morand, B.R. Krasnov & R. Poulin ), pp. 443-473. Springer-Verlag, Tokyo.
100. Wielebnowski, N. (2003) Stress and distress: evaluating their impact for the well-being of zoo animals. Journal of the American Veterinary Medical Association, 223, 973-977.
101. Wielebnowski, N. & Watters, J. (2007) Applying fecal endocrine monitoring to conservation and behavior studies of wild mammals: important considerations and preliminary tests. Israel Journal of Ecology & Evolution, 53, 439-460.
102. Wingfield, J.C. & Kitaysky, A.S. (2002) Endocrine responses to unpredictable environmental events: stress or anti-stress hormones? Integrative and Comparative Biology, 42, 600-609.
103. Wingfield, J.C., Maney, D.L., Breuner, C.W., Jacobs, J.D., Lynn, S., Ramenofsky, M. et al. (1998) Ecological bases of hormone-behavior interactions: the "emergency life history stage". American Zoologist, 38, 191-206.