Ecological immunology of bird-ectoparasite systems.

Ecological immunology is a rapidly expanding field of research that attempts to explain variation in immune function across individuals, populations and species. Birds and ectoparasitic arthropods have frequently been used in attempts to measure the cost of immune function in relation to adult condition, nestling growth and other life history challenges. Unfortunately, most studies in ecological immunology have relied on assays of general immunocompetence that are not connected to actual parasites. A summary of potential interactions between the avian immune system and ectoparasites is provided and methods that can be used to test ecological questions in the context of naturally occurring host-parasite interactions are proposed.

[1]  L. Grubhoffer,et al.  Artificial immunization of pigeons against Argas polonicus (Ixodoidea, Argasidae) , 1990, Medical and veterinary entomology.

[2]  L. Keller,et al.  Pleiotropy in the melanocortin system, coloration and behavioural syndromes. , 2008, Trends in ecology & evolution.

[3]  H. Richner,et al.  Host condition and host immunity affect parasite fitness in a bird–ectoparasite system , 2007 .

[4]  J. Ribeiro,et al.  Negative effect of antibodies against maxadilan on the fitness of the sand fly vector of American visceral leishmaniasis. , 2004, The American journal of tropical medicine and hygiene.

[5]  R. Boughton,et al.  AN INTRODUCED GENERALIST PARASITE, THE STICKTIGHT FLEA (ECHIDNOPHAGA GALLINACEA), AND ITS PATHOLOGY IN THE THREATENED FLORIDA SCRUB-JAY (APHELOCOMA COERULESCENS) , 2006, The Journal of parasitology.

[6]  Z. Barta,et al.  Adaptive Host-Abandonment of Ectoparasites Before Fledging? Within-Brood Distribution of Nest Mites in House Sparrow Broods , 2008, The Journal of parasitology.

[7]  M. Wikelski,et al.  Immunological investments reflect parasite abundance in island populations of Darwin's finches , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  P. Fitze,et al.  Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings , 2003 .

[9]  H. Richner,et al.  Induced responses of nestling great tits reduce hen flea reproduction , 2003 .

[10]  M. Delany,et al.  Host inflammatory response governs fitness in an avian ectoparasite, the northern fowl mite (Ornithonyssus sylviarum). , 2009, International journal for parasitology.

[11]  L. Webster,et al.  Physiological Stress Mediates the Honesty of Social Signals , 2009, PloS one.

[12]  A. Møller,et al.  Genetic and environmental components of phenotypic variation in immune response and body size of a colonial bird, Delichon urbica (the house martin) , 2000, Heredity.

[13]  M. Delany,et al.  MHC haplotype involvement in avian resistance to an ectoparasite , 2008, Immunogenetics.

[14]  A. Roulin,et al.  What Makes a Host Profitable? Parasites Balance Host Nutritive Resources against Immunity , 2007, The American Naturalist.

[15]  F. Dusbábek,et al.  Age-dependent immune response of chickens to feeding by Argas persicus larvae. , 1994, Veterinary parasitology.

[16]  S. Wikel The immunology of host-ectoparasitic arthropod relationships , 1996 .

[17]  D. Hasselquist Comparative immunoecology in birds: hypotheses and tests , 2007, Journal of Ornithology.

[18]  Y. Michalakis,et al.  Local adaptation of the ectoparasite Ixodes uriae to its seabird host , 2002 .

[19]  J. Langhorne,et al.  Cytokine responses of CD4+ T cells during a Plasmodium chabaudi chabaudi (ER) blood-stage infection in mice initiated by the natural route of infection , 2007, Malaria Journal.

[20]  M. Roberts,et al.  Testing the immunocompetence handicap hypothesis: a review of the evidence , 2004, Animal Behaviour.

[21]  W. Hamilton,et al.  Heritable true fitness and bright birds: a role for parasites? , 1982, Science.

[22]  D. Hasselquist,et al.  Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia) , 2006, Proceedings of the Royal Society B: Biological Sciences.

[23]  J. Bany,et al.  Comparison of local and systemic responsiveness of lymphocytes in vitro to Bovicola ovis antigen and concanavalin A in B. ovis-infested and naive lambs. , 1995, International journal for parasitology.

[24]  E. Ketterson,et al.  Steroid Hormones and Immune Function: Experimental Studies in Wild and Captive Dark‐Eyed Juncos (Junco hyemalis) , 2001, The American Naturalist.

[25]  F. Valera,et al.  Ectoparasite load is linked to ontogeny and cell‐mediated immunity in an avian host system with pronounced hatching asynchrony , 2008 .

[26]  S. Edwards,et al.  A cDNA macroarray approach to parasite‐induced gene expression changes in a songbird host: genetic response of house finches to experimental infection by Mycoplasma gallisepticum , 2005, Molecular ecology.

[27]  A. Møller,et al.  Parasitism, immune response and reproductive success in the house martin Delichonurbica , 1998, Oecologia.

[28]  S. Merino,et al.  A meta‐analysis of parasite virulence in nestling birds , 2009, Biological reviews of the Cambridge Philosophical Society.

[29]  G. Hill,et al.  Carotenoid-based plumage coloration predicts resistance to a novel parasite in the house finch , 2004, Naturwissenschaften.

[30]  J. Ribeiro,et al.  The Anopheles gambiae salivary protein gSG6: an anopheline-specific protein with a blood-feeding role. , 2009, Insect biochemistry and molecular biology.

[31]  P. Fitze,et al.  Parasite-induced maternal response in a natural bird population , 2002 .

[32]  N. Saino,et al.  Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rus , 1995 .

[33]  K. Norris,et al.  Ecological immunology: life history trade-offs and immune defense in birds , 2000 .

[34]  J. Bos,et al.  Skin immune system. , 1990, Cancer treatment and research.

[35]  H. Schwabl,et al.  Are Maternal Antibodies Really That Important? Patterns in the Immunologic Development of Altricial Passerine House Sparrows (Passer domesticus) , 2010, PloS one.

[36]  H. Richner,et al.  Parasites shape the optimal investment in immunity , 2006, Proceedings of the Royal Society B: Biological Sciences.

[37]  P. Parker,et al.  Disease ecology in the Galápagos Hawk (Buteo galapagoensis): host genetic diversity, parasite load and natural antibodies , 2006, Proceedings of the Royal Society B: Biological Sciences.

[38]  T. Schnieder,et al.  Monitoring of basophil sensitization to antigens of the cat flea (Ctenocephalides felis felis): a new tool for the diagnosis of feline flea bite hypersensitivity? , 2008, Parasitology Research.

[39]  A. Roulin,et al.  Which chick is tasty to parasites? The importance of host immunology vs. parasite life history , 2003 .

[40]  A. Møller,et al.  Fitness consequences of variation in natural antibodies and complement in the Barn Swallow Hirundo rustica , 2007 .

[41]  A. Møller,et al.  Immunocompetence and nestling survival in the house martin : the tasty chick hypothesis , 1998 .

[42]  A. A. Souza,et al.  Changes in Amounts of Total Salivary Gland Proteins of Lutzomyia longipalpis (Diptera: Psychodidae) According to Age and Diet , 2008, Journal of medical entomology.

[43]  R. Poulin,et al.  Epigenetic effects of infection on the phenotype of host offspring: parasites reaching across host generations , 2008 .

[44]  E. Adkins-Regan Hormones and the development of sex differences in behavior , 2007, Journal of Ornithology.

[45]  Y. Belkaid,et al.  Delayed-type hypersensitivity to Phlebotomus papatasi sand fly bite: An adaptive response induced by the fly? , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[46]  B. Grant,et al.  Ecoimmunity in Darwin's Finches: Invasive Parasites Trigger Acquired Immunity in the Medium Ground Finch (Geospiza fortis) , 2010, PloS one.

[47]  J. Carroll,et al.  Antibody development against northern fowl mites (Acari: Macronyssidae) in chickens. , 1993, Journal of medical entomology.

[48]  K. Wakamatsu,et al.  Strength and cost of an induced immune response are associated with a heritable melanin-based colour trait in female tawny owls. , 2009, The Journal of animal ecology.

[49]  S. Klein,et al.  Hormonal and immunological mechanisms mediating sex differences in parasite infection , 2004, Parasite immunology.

[50]  P. Schmid-Hempel,et al.  Principles of ecological immunology , 2008, Evolutionary applications.

[51]  A. Pernthaner,et al.  Cutaneous cytokine gene expression and cellular responses in lambs infested with the louse, Bovicola ovis, and following intradermal injection of crude louse antigen. , 2009, Veterinary immunology and immunopathology.

[52]  A. Møller,et al.  Effects of a Dipteran Ectoparasite on Immune Response and Growth Trade-Offs in Barn Swallow, Hirundo rustica, Nestlings , 1998 .

[53]  N. Metcalfe,et al.  Carotenoid Modulation of Immune Function and Sexual Attractiveness in Zebra Finches , 2003, Science.

[54]  Transgenerational immunity in a bird-ectoparasite system: do maternally transferred antibodies affect parasite fecundity or the offspring's susceptibility to fleas? , 2009 .

[55]  D. Hasselquist,et al.  Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[56]  M. Polák,et al.  Host inbreeding increases susceptibility to ectoparasitism , 2007, Journal of evolutionary biology.

[57]  P. Fitze,et al.  Carotenoid‐Based Plumage Colors and Immune Function: Is There a Trade‐Off for Rare Carotenoids? , 2007, The American Naturalist.

[58]  K. Salvante TECHNIQUES FOR STUDYING INTEGRATED IMMUNE FUNCTION IN BIRDS , 2006 .

[59]  R. Dawson,et al.  Parasite-mediated growth patterns and nutritional constraints in a cavity-nesting bird. , 2008, The Journal of animal ecology.

[60]  Gregory F Ball,et al.  Individual variation and the endocrine regulation of behaviour and physiology in birds: a cellular/molecular perspective , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[61]  J. Ewen,et al.  Maternally invested carotenoids compensate costly ectoparasitism in the hihi , 2009, Proceedings of the National Academy of Sciences.

[62]  F. Mougeot Ornamental comb colour predicts T-cell-mediated immunity in male red grouse Lagopus lagopus scoticus , 2008, Naturwissenschaften.

[63]  L. Garamszegi,et al.  Bird song and parasites , 2005, Behavioral Ecology and Sociobiology.

[64]  B. Faivre,et al.  Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird (Turdus merula) , 2008, Proceedings of the Royal Society B: Biological Sciences.

[65]  D. Gourichon,et al.  Microsatellite mapping of QTLs affecting resistance to coccidiosis (Eimeria tenella) in a Fayoumi × White Leghorn cross , 2009, BMC Genomics.

[66]  T. Boulinier,et al.  Maternal transfer of antibodies: raising immuno-ecology issues. , 2008, Trends in ecology & evolution.

[67]  K. Gallizzi,et al.  A parasite-induced maternal effect can reduce survival times of fleas feeding on great tit nestlings , 2008 .

[68]  R. Ricklefs,et al.  No simple answers for ecological immunology: relationships among immune indices at the individual level break down at the species level in waterfowl , 2006, Proceedings of the Royal Society B: Biological Sciences.

[69]  H. Richner,et al.  Immunocompetence of nestling great tits in relation to rearing environment and parentage , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[70]  A. Møller,et al.  Cost of parasitism and host immune defence in the sand martin Riparia riparia: a role for parent-offspring conflict? , 1999, Oecologia.

[71]  L. Saks,et al.  Do standard measures of immunocompetence reflect parasite resistance? The case of Greenfinch coccidiosis , 2006 .

[72]  A. Ducrest,et al.  Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba) , 2001 .

[73]  J. Bos Skin Immune System : Cutaneous Immunology and Clinical Immunodermatology, Third Edition , 2004 .

[74]  D. Hasselquist,et al.  Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity , 2006, Proceedings of the Royal Society B: Biological Sciences.

[75]  E. Riley,et al.  Optimal immune responses: immunocompetence revisited. , 2005, Trends in ecology & evolution.

[76]  D. Clayton,et al.  How Birds Combat Ectoparasites , 2010 .

[77]  D. Clayton,et al.  Where are the parasites in the PHA response? , 2007, Trends in ecology & evolution.

[78]  C. Atkinson,et al.  Parasitic diseases of wild birds , 2008 .