Artigo Revisado por pares

Great tits Parus major trade health for reproduction

1996; Royal Society; Volume: 263; Issue: 1376 Linguagem: Inglês

10.1098/rspb.1996.0210

ISSN

1471-2954

Autores

I. Ots, Peeter Hõrak,

Tópico(s)

Bat Biology and Ecology Studies

Resumo

Restricted accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Ots Indrek and Hõrak Peeter 1996Great tits Parus major trade health for reproductionProc. R. Soc. Lond. B.2631443–1447http://doi.org/10.1098/rspb.1996.0210SectionRestricted accessArticleGreat tits Parus major trade health for reproduction Indrek Ots Google Scholar Find this author on PubMed Search for more papers by this author and Peeter Hõrak Google Scholar Find this author on PubMed Search for more papers by this author Indrek Ots Google Scholar Find this author on PubMed and Peeter Hõrak Google Scholar Find this author on PubMed Published:22 November 1996https://doi.org/10.1098/rspb.1996.0210AbstractReproduction and maintenance compete for resources within a single individual. But do individuals invest in reproduction just as much as remains after the requirements of maintenance are covered, or do they sacrifice their health for the sake of still further increase the investment in current reproduction? This question has been found hard to answer because of difficulties of demonstrating that individuals naturally make a reproductive effort of such a magnitude as to inflict health damage. In this paper we present evidence for a trade-off between reproductive effort and health state in great tits, indicated by a positive correlation between total prefledging brood weight and both intensity of Haemoproteus blood parasite infection and heterophile: lymphocyte (H:L) ratio. H:L ratios, which signal stress in birds, were high both among individuals making an intense reproductive effort and among aberrantly behaving individuals, such as females incubating in empty nests and birds which abandoned their broods after blood sampling. Experimental reduction of clutch size resulted in decreased intensity of Haemoproteus parasitemia, providing further evidence that individual great tits accept immunosuppression to increase their reproductive investment.FootnotesThis text was harvested from a scanned image of the original document using optical character recognition (OCR) software. As such, it may contain errors. Please contact the Royal Society if you find an error you would like to see corrected. Mathematical notations produced through Infty OCR. Previous ArticleNext Article VIEW FULL TEXT DOWNLOAD PDF FiguresRelatedReferencesDetailsCited by Rollins R, Mouchet A, Margos G, Chitimia-Dobler L, Fingerle V, Becker N and Dingemanse N (2021) Repeatable differences in exploratory behaviour predict tick infestation probability in wild great tits, Behavioral Ecology and Sociobiology, 10.1007/s00265-021-02972-y, 75:3, Online publication date: 1-Mar-2021. Pigeault R, Cozzarolo C, Glaizot O and Christe P (2019) Effect of age, haemosporidian infection and body condition on pair composition and reproductive success in Great Tits Parus major , Ibis, 10.1111/ibi.12774, 162:3, (613-626), Online publication date: 1-Jul-2020. López‐Pérez J, Meylan P and Goessling J (2020) Sex‐based trade‐offs in the innate and acquired immune systems of Sternotherus minor , Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 10.1002/jez.2424, 333:10, (820-828), Online publication date: 1-Dec-2020. Roast M, Aulsebrook A, Fan M, Hidalgo Aranzamendi N, Teunissen N and Peters A (2019) Short-Term Climate Variation Drives Baseline Innate Immune Function and Stress in a Tropical Bird: A Reactive Scope Perspective, Physiological and Biochemical Zoology, 10.1086/702310, 92:2, (140-151), Online publication date: 1-Mar-2019. Skwarska J Variation of Heterophil-to-Lymphocyte Ratio in the Great Tit Parus major — a Review, Acta Ornithologica, 10.3161/00016454AO2018.53.2.001, 53:2, (103) Zollinger S, Dorado-Correa A, Goymann W, Forstmeier W, Knief U, Bastidas­Urrutia A, Brumm H and Cooke S (2019) Traffic noise exposure depresses plasma corticosterone and delays offspring growth in breeding zebra finches, Conservation Physiology, 10.1093/conphys/coz056, 7:1, Online publication date: 1-Jan-2019. Svobodová J, Bauerová P, Eliáš J, Velová H, Vinkler M and Albrecht T (2018) Sperm variation in Great Tit males (Parus major) is linked to a haematological health-related trait, but not ornamentation, Journal of Ornithology, 10.1007/s10336-018-1559-7, 159:3, (815-822), Online publication date: 1-Jul-2018. Joseph P, Emberts Z, Sasson D and Miller C (2017) Males that drop a sexually selected weapon grow larger testes, Evolution, 10.1111/evo.13387, 72:1, (113-122), Online publication date: 1-Jan-2018. MacColl E, Vanesky K, Buck J, Dudek B, Eagles‐Smith C, Heath J, Herring G, Vennum C and Downs C (2017) Correlates of immune defenses in golden eagle nestlings, Journal of Experimental Zoology Part A: Ecological and Integrative Physiology, 10.1002/jez.2081, 327:5, (243-253), Online publication date: 1-Jun-2017. van Dijk J and Matson K (2016) Ecological Immunology through the Lens of Exercise Immunology: New Perspective on the Links between Physical Activity and Immune Function and Disease Susceptibility in Wild Animals, Integrative and Comparative Biology, 10.1093/icb/icw045, 56:2, (290-303), Online publication date: 1-Aug-2016. Calero-Riestra M and García J (2016) Sex-dependent differences in avian malaria prevalence and consequences of infections on nestling growth and adult condition in the Tawny pipit, Anthus campestris, Malaria Journal, 10.1186/s12936-016-1220-y, 15:1, Online publication date: 1-Dec-2016. Escallón C, Weinstein N, Tallant J, Wojtenek W, Rodríguez‐Saltos C, Bonaccorso E and Moore I (2016) Testosterone and Haemosporidian Parasites Along a Tropical Elevational Gradient in Rufous‐Collared Sparrows ( Zonotrichia capensis ) , Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 10.1002/jez.2034, 325:8, (501-510), Online publication date: 1-Oct-2016. Biard C, Monceau K, Motreuil S, Moreau J and Metcalf J (2015) Interpreting immunological indices: The importance of taking parasite community into account. An example in blackbirds Turdus merula , Methods in Ecology and Evolution, 10.1111/2041-210X.12371, 6:8, (960-972), Online publication date: 1-Aug-2015. Clark P (2014) Observed variation in the heterophil to lymphocyte ratio values of birds undergoing investigation of health status, Comparative Clinical Pathology, 10.1007/s00580-014-2052-1, 24:5, (1151-1157), Online publication date: 1-Sep-2015. Kulaszewicz I, Wojczulanis-Jakubas K and Jakubas D (2015) Variation of the Savi's Warbler ( Locustella luscinioides ) Leucocyte Profiles and Body Condition in Relation to Age, Sex and Moult , Annales Zoologici Fennici, 10.5735/086.052.0507, 52:5-6, (325-338), Online publication date: 1-Dec-2015. Archie E, Altmann J and Alberts S (2014) Costs of reproduction in a long-lived female primate: injury risk and wound healing, Behavioral Ecology and Sociobiology, 10.1007/s00265-014-1729-4, 68:7, (1183-1193), Online publication date: 1-Jul-2014. Lozano G, Lank D and Addison B (2013) Immune and oxidative stress trade-offs in four classes of Ruffs ( Philomachus pugnax ) with different reproductive strategies , Canadian Journal of Zoology, 10.1139/cjz-2012-0324, 91:4, (212-218), Online publication date: 1-Apr-2013. Krama T, Suraka V, Hukkanen M, Rytkönen S, Orell M, Cīrule D, Rantala M and Krams I (2013) Physiological condition and blood parasites of breeding Great Tits: a comparison of core and northernmost populations, Journal of Ornithology, 10.1007/s10336-013-0969-9, 154:4, (1019-1028), Online publication date: 1-Oct-2013. Jakubas D, Wojczulanis-Jakubas K and Kulaszewicz I (2013) Factors Affecting Haematological Variables and Body Mass of Reed Warblers ( Acrocephalus scirpaceus ) and Sedge Warblers ( A. schoenobaenus ) , Annales Zoologici Fennici, 10.5735/086.050.0302, 50:3, (146-157), Online publication date: 1-Jun-2013. Christe P, Glaizot O, Strepparava N, Devevey G and Fumagalli L (2011) Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress, Proceedings of the Royal Society B: Biological Sciences, 279:1731, (1142-1149), Online publication date: 22-Mar-2012. Roff D and Fairbairn D (2012) THE EVOLUTION OF TRADE-OFFS UNDER DIRECTIONAL AND CORRELATIONAL SELECTION, Evolution, 10.1111/j.1558-5646.2012.01634.x, 66:8, (2461-2474), Online publication date: 1-Aug-2012. Versteegh M, Schwabl I, Jaquier S and Tieleman B (2012) Do immunological, endocrine and metabolic traits fall on a single Pace-of-Life axis? Covariation and constraints among physiological systems, Journal of Evolutionary Biology, 10.1111/j.1420-9101.2012.02574.x, 25:9, (1864-1876), Online publication date: 1-Sep-2012. Jakubas D, Głuchowska M, Wojczulanis-Jakubas K, Karnovsky N, Keslinka L, Kidawa D, Walkusz W, Boehnke R, Cisek M, Kwasniewski S and Stempniewicz L (2011) Foraging effort does not influence body condition and stress level in little auks, Marine Ecology Progress Series, 10.3354/meps09082, 432, (277-290), Online publication date: 27-Jun-2011. Steiger S, Gershman S, Pettinger A, Eggert A and Sakaluk S (2011) Sex differences in immunity and rapid upregulation of immune defence during parental care in the burying beetle, Nicrophorus orbicollis, Functional Ecology, 10.1111/j.1365-2435.2011.01895.x, 25:6, (1368-1378), Online publication date: 1-Dec-2011. Dehnhard N, Poisbleau M, Demongin L and Quillfeldt P (2011) Do leucocyte profiles reflect temporal and sexual variation in body condition over the breeding cycle in Southern Rockhopper Penguins?, Journal of Ornithology, 10.1007/s10336-011-0658-5, 152:3, (759-768), Online publication date: 1-Jul-2011. Jakubas D, Wojczulanis-Jakubas K and Glac W (2011) Variation of the Reed Bunting ( Emberiza schoeniclus ) Body Condition and Haematological Parameters in Relation to Sex, Age and Season , Annales Zoologici Fennici, 10.5735/086.048.0405, 48:4, (243-250), Online publication date: 1-Aug-2011. EDLER R, GOYMANN W, SCHWABL I and FRIEDL T (2010) Experimentally elevated testosterone levels enhance courtship behaviour and territoriality but depress acquired immune response in Red Bishops Euplectes orix, Ibis, 10.1111/j.1474-919X.2010.01075.x, 153:1, (46-58), Online publication date: 1-Jan-2011. Schöpper H, Palme R, Ruf T and Huber S (2011) Chronic stress in pregnant guinea pigs (Cavia aperea f. porcellus) attenuates long-term stress hormone levels and body weight gain, but not reproductive output, Journal of Comparative Physiology B, 10.1007/s00360-011-0591-1, 181:8, (1089-1100), Online publication date: 1-Dec-2011. Dehnhard N, Poisbleau M, Demongin L, Chastel O, van Noordwijk H and Quillfeldt P (2010) Leucocyte profiles and corticosterone in chicks of southern rockhopper penguins, Journal of Comparative Physiology B, 10.1007/s00360-010-0508-4, 181:1, (83-90), Online publication date: 1-Jan-2011. EDLER A and FRIEDL T (2010) Individual quality and carotenoid-based plumage ornaments in male red bishops (Euplectes orix): plumage is not all that counts, Biological Journal of the Linnean Society, 10.1111/j.1095-8312.2009.01354.x, 99:2, (384-397) DEVICHE P, FOKIDIS H, LERBOUR B and GREINER E (2009) Blood parasitaemia in a high latitude flexible breeder, the white-winged crossbill, Loxia leucoptera : contribution of seasonal relapse versus new inoculations , Parasitology, 10.1017/S003118200999134X, 137:2, (261-273), Online publication date: 1-Feb-2010. Shutler D, Lowe A and Robinson S (2010) Relationships between circulating leucocytes and Leucocytozoon simondi in mallard, Anas platyrhynchos, ducklings, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 10.1016/j.cbpa.2009.12.015, 156:1, (46-49), Online publication date: 1-May-2010. Tilgar V, Saag P, Külavee R and Mänd R (2010) Behavioral and physiological responses of nestling pied flycatchers to acoustic stress, Hormones and Behavior, 10.1016/j.yhbeh.2010.02.006, 57:4-5, (481-487), Online publication date: 1-Apr-2010. Bisson I, Butler L, Hayden T, Romero L and Wikelski M (2008) No energetic cost of anthropogenic disturbance in a songbird, Proceedings of the Royal Society B: Biological Sciences, 276:1658, (961-969), Online publication date: 7-Mar-2009. Knowles S, Nakagawa S and Sheldon B (2009) Elevated reproductive effort increases blood parasitaemia and decreases immune function in birds: a meta-regression approach, Functional Ecology, 10.1111/j.1365-2435.2008.01507.x, 23:2, (405-415), Online publication date: 1-Apr-2009. Norte A, Ramos J, Sousa J and Sheldon B (2009) Variation of adult Great Tit Parus major body condition and blood parameters in relation to sex, age, year and season, Journal of Ornithology, 10.1007/s10336-009-0387-1, 150:3, Online publication date: 1-Jul-2009. NORTE A, ARAÚJO P, SAMPAIO H, SOUSA J and RAMOS J (2009) Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health, Ibis, 10.1111/j.1474-919X.2009.00960.x, 151:4, (677-688) Hanley D and Doucet S (2009) Egg coloration in ring-billed gulls (Larus delawarensis): a test of the sexual signaling hypothesis, Behavioral Ecology and Sociobiology, 10.1007/s00265-008-0705-2, 63:5, (719-729), Online publication date: 1-Mar-2009. Fallon S and Ricklefs R (2008) Parasitemia in PCR-detected Plasmodium and Haemoproteus infections in birds , Journal of Avian Biology, 10.1111/j.0908-8857.2008.04308.x, 39:5, (514-522), Online publication date: 1-Sep-2008. APANIUS V, WESTBROCK M and ANDERSON D (2008) REPRODUCTION AND IMMUNE HOMEOSTASIS IN A LONG-LIVED SEABIRD, THE NAZCA BOOBY ( Sula granti ) , Ornithological Monographs, 10.1525/om.2008.65.1.1, 65:1, (1-46), Online publication date: 1-Jan-2008. Ochs C and Dawson R (2008) Patterns of variation in leucocyte counts of female tree swallows, Tachycineta bicolor: Repeatability over time and relationships with condition and costs of reproduction, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 10.1016/j.cbpa.2008.04.003, 150:3, (326-331), Online publication date: 1-Jul-2008. Petes L, Menge B and Harris A (2008) INTERTIDAL MUSSELS EXHIBIT ENERGETIC TRADE-OFFS BETWEEN REPRODUCTION AND STRESS RESISTANCE, Ecological Monographs, 10.1890/07-0605.1, 78:3, (387-402), Online publication date: 1-Aug-2008. French S and Moore M (2008) Immune function varies with reproductive stage and context in female and male tree lizards, Urosaurus ornatus, General and Comparative Endocrinology, 10.1016/j.ygcen.2007.04.007, 155:1, (148-156), Online publication date: 1-Jan-2008. Owen J and Moore F (2008) Swainson's thrushes in migratory disposition exhibit reduced immune function, Journal of Ethology, 10.1007/s10164-008-0092-1, 26:3, (383-388), Online publication date: 1-Sep-2008. Quillfeldt P, Ruiz G, Rivera M and Masello J (2008) Variability in leucocyte profiles in thin-billed prions Pachyptila belcheri, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 10.1016/j.cbpa.2008.02.021, 150:1, (26-31), Online publication date: 1-May-2008. Edler R and Friedl T (2008) Within-pair young are more immunocompetent than extrapair young in mixed-paternity broods of the red bishop, Animal Behaviour, 10.1016/j.anbehav.2007.05.004, 75:2, (391-401), Online publication date: 1-Feb-2008. Cláudia Norte A, Sheldon B, Paulo Sousa J and Albino Ramos J (2008) Repeatability and Method-Dependent Variation of Blood Parameters in Wild-Caught Great Tits Parus major , Acta Ornithologica, 10.3161/000164508X345347, 43:1, (65-75), Online publication date: 1-Jun-2008. Ricklefs R, Sheldon K and Johnson K (2007) Malaria Prevalence and White-Blood-Cell Response to Infection in a Tropical and in a Temperate Thrush, The Auk, 10.1093/auk/124.4.1254, 124:4, (1254-1266), Online publication date: 1-Oct-2007. Tarlow E and Blumstein D (2007) Evaluating methods to quantify anthropogenic stressors on wild animals, Applied Animal Behaviour Science, 10.1016/j.applanim.2006.05.040, 102:3-4, (429-451), Online publication date: 1-Feb-2007. ROFF D and FAIRBAIRN D (2007) The evolution of trade-offs: where are we?, Journal of Evolutionary Biology, 10.1111/j.1420-9101.2006.01255.x, 20:2, (433-447), Online publication date: 1-Mar-2007. Tummeleht L, Mägi M, Kilgas P, Mänd R and Hõrak P (2006) Antioxidant protection and plasma carotenoids of incubating great tits (Parus major L.) in relation to health state and breeding conditions, Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 10.1016/j.cbpc.2006.08.004, 144:2, (166-172), Online publication date: 1-Oct-2006. Degen A Effect of macroparasites on the energy budget of small mammals Micromammals and Macroparasites, 10.1007/978-4-431-36025-4_19, (371-399) Garvin M and Schoech S (2006) Hormone Levels and Infection of Haemoproteus danilewskyi in Free-Ranging Blue Jays (Cyanocitta cristata), Journal of Parasitology, 10.1645/GE-759R.1, 92:3, (659-662), Online publication date: 1-Jun-2006. Kilgas P, Mänd R, Mägi M and Tilgar V (2006) Hematological parameters in brood-rearing great tits in relation to habitat, multiple breeding and sex, Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 10.1016/j.cbpa.2006.02.038, 144:2, (224-231), Online publication date: 1-Jun-2006. Owen J and Moore F (2006) Seasonal Differences in Immunological Condition of Three Species of Thrushes, The Condor, 10.1093/condor/108.2.389, 108:2, (389-398), Online publication date: 1-May-2006. Kilgas P, Tilgar V and Mänd R (2006) Hematological Health State Indices Predict Local Survival in a Small Passerine Bird, the Great Tit ( Parus major ) , Physiological and Biochemical Zoology, 10.1086/502817, 79:3, (565-572), Online publication date: 1-May-2006. Tinne S, Rianne P and Marcel E (2005) Experimental removal of the male parent negatively affects growth and immunocompetence in nestling great tits, Oecologia, 10.1007/s00442-005-0088-2, 145:1, (165-173), Online publication date: 1-Aug-2005. Friedl T and Edler R (2005) Stress-dependent trade-off Between Immunological Condition and Reproductive Performance in the Polygynous Red Bishop (Euplectes orix), Evolutionary Ecology, 10.1007/s10682-005-0509-z, 19:3, (221-239), Online publication date: 1-May-2005. Verhulst S, Riedstra B and Wiersma P (2005) Brood size and immunity costs in zebra finches Taeniopygia guttata , Journal of Avian Biology, 10.1111/j.0908-8857.2005.03342.x, 36:1, (22-30), Online publication date: 1-Jan-2005. Hõrak P, Surai P, Ots I and Møller A (2004) Fat soluble antioxidants in brood-rearing great tits Parus major : relations to health and appearance , Journal of Avian Biology, 10.1111/j.0908-8857.2004.03167.x, 35:1, (63-70), Online publication date: 1-Jan-2004. Edler R, Klump G and Friedl T (2010) Do blood parasites affect reproductive performance in male red bishops ( Euplectes orix )? A test of the Hamilton-Zuk hypothesis , Ethology Ecology & Evolution, 10.1080/08927014.2004.9522623, 16:4, (315-328), Online publication date: 1-Oct-2004. Shutler D, Mullie A and Clark R (2004) Tree swallow reproductive investment, stress, and parasites, Canadian Journal of Zoology, 10.1139/z04-016, 82:3, (442-448), Online publication date: 1-Mar-2004. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology, Proceedings of the Royal Society of London. Series B: Biological Sciences, 270:1513, (357-366), Online publication date: 22-Feb-2003. Clutton-Brock T and Pemberton J (2009) Soay Sheep Faivre B, Préault M, Salvadori F, Théry M, Gaillard M and Cézilly F (2003) Bill colour and immunocompetence in the European blackbird, Animal Behaviour, 10.1006/anbe.2003.2142, 65:6, (1125-1131), Online publication date: 1-Jun-2003. Mänd R and Tilgar V (2002) Does supplementary calcium reduce the cost of reproduction in the Pied Flycatcher Ficedula hypoleuca?, Ibis, 10.1046/j.1474-919X.2003.00123.x, 145:1, (67-77) Wells J (2003) Parent‐Offspring Conflict Theory, Signaling of Need, and Weight Gain in Early Life, The Quarterly Review of Biology, 10.1086/374952, 78:2, (169-202), Online publication date: 1-Jun-2003. Roff D, Mostowy S and Fairbairn D (2002) THE EVOLUTION OF TRADE-OFFS: TESTING PREDICTIONS ON RESPONSE TO SELECTION AND ENVIRONMENTAL VARIATION, Evolution, 10.1111/j.0014-3820.2002.tb00851.x, 56:1, (84-95), Online publication date: 1-Jan-2002. Roff D, Mostowy S and Fairbairn D (2002) THE EVOLUTION OF TRADE-OFFS: TESTING PREDICTIONS ON RESPONSE TO SELECTION AND ENVIRONMENTAL VARIATION, Evolution, 10.1554/0014-3820(2002)056[0084:TEOTOT]2.0.CO;2, 56:1, (84), . Pap P (2002) Breeding time and sex-specific health status in the barn swallow ( Hirundo rustica ) , Canadian Journal of Zoology, 10.1139/z02-200, 80:12, (2090-2099), Online publication date: 1-Dec-2002. Sanz J, Moreno J, Arriero E and Merino S (2002) Reproductive effort and blood parasites of breeding pied flycatchers: the need to control for interannual variation and initial health state, Oikos, 10.1034/j.1600-0706.2002.960212.x, 96:2, (299-306), Online publication date: 1-Feb-2002. Deviche P, Greiner E and Manteca X (2001) Seasonal and age-related changes in blood parasite prevalence in dark-eyed juncos (Junco hyemalis, Aves, Passeriformes), Journal of Experimental Zoology, 10.1002/jez.1027, 289:7, (456-466), Online publication date: 1-Jun-2001. Hautekèete N, Piquot Y and Van Dijk H (2008) Investment in survival and reproduction along a semelparity-iteroparity gradient in the Beta species complex , Journal of Evolutionary Biology, 10.1046/j.1420-9101.2001.00322.x, 14:5, (795-804), Online publication date: 15-Sep-2001. Sanz J, Arriero E, Moreno J and Merino S (2001) Female Hematozoan Infection Reduces Hatching Success but not Fledging Success in Pied Flycatchers Ficedula hypoleuca, The Auk, 10.1093/auk/118.3.750, 118:3, (750-755), Online publication date: 1-Jul-2001. Cichoń M, Dubiec A and Chadzińska M (2001) The effect of elevated reproductive effort onhumoral immune function in collared flycatcher females, Acta Oecologica, 10.1016/S1146-609X(00)01094-8, 22:1, (71-76), Online publication date: 1-Jan-2001. Dawson R and Bortolotti G (2000) EFFECTS OF HEMATOZOAN PARASITES ON CONDITION AND RETURN RATES OF AMERICAN KESTRELS, The Auk, 10.1642/0004-8038(2000)117[0373:EOHPOC]2.0.CO;2, 117:2, (373), . Shanley D and Kirkwood T (2000) CALORIE RESTRICTION AND AGING: A LIFE-HISTORY ANALYSIS, Evolution, 10.1554/0014-3820(2000)054[0740:CRAAAL]2.3.CO;2, 54:3, (740), . Doums C and Schmid-Hempel P (2000) Immunocompetence in workers of a social insect, Bombus terrestris L., in relation to foraging activity and parasitic infection , Canadian Journal of Zoology, 10.1139/z00-035, 78:6, (1060-1066), Online publication date: 1-Jun-2000. Moshkin M, Gerlinskaya L and Evsikov V (2000) The Role of the Immune System in Behavioral Strategies of Reproduction, Journal of Reproduction and Development, 10.1262/jrd.46.341, 46:6, (341-365), . Lochmiller R, Ditchkoff S and Sinclair J (2000) Developmental Plasticity of Postweanling Cotton Rats (Sigmodon hispidus) as an Adaptation to Nutritionally Stochastic Environments, Evolutionary Ecology, 10.1023/A:1011014814256, 14:2, (127-142), Online publication date: 1-Mar-2000. Dawson R and Bortolotti G (2000) Effects of Hematozoan Parasites on Condition and Return Rates of American Kestrels, The Auk, 10.1093/auk/117.2.373, 117:2, (373-380), Online publication date: 1-Apr-2000. Sinclair J and Lochmiller R (2000) The winter immunoenhancement hypothesis: associations among immunity, density, and survival in prairie vole ( Microtus ochrogaster ) populations , Canadian Journal of Zoology, 10.1139/z99-203, 78:2, (254-264), Online publication date: 5-Mar-2000. Shanley D and Kirkwood T (2000) CALORIE RESTRICTION AND AGING: A LIFE-HISTORY ANALYSIS, Evolution, 10.1111/j.0014-3820.2000.tb00076.x, 54:3, (740-750), Online publication date: 1-Jun-2000. Appleby B, Anwar M and Petty S (2002) Short‐term and long‐term effects of food supply on parasite burdens in Tawny Owls, Strix aluco , Functional Ecology, 10.1046/j.1365-2435.1999.00319.x, 13:3, (315-321), Online publication date: 1-Jun-1999. Shutler D, Ankney C and Mullie A (1999) Effects of the blood parasite Leucocytozoon simondi on growth rates of anatid ducklings , Canadian Journal of Zoology, 10.1139/z99-121, 77:10, (1573-1578), Online publication date: 1-Dec-1999. Bergstrom C and Lachmann M (1998) Signaling among relatives. III. Talk is cheap, Proceedings of the National Academy of Sciences, 10.1073/pnas.95.9.5100, 95:9, (5100-5105), Online publication date: 28-Apr-1998. Apanius V (1998) Stress and Immune Defense Stress and Behavior, 10.1016/S0065-3454(08)60363-0, (133-153), . Matson K, Horrocks N, Tieleman B and Haase E (2012) Intense flight and endotoxin injection elicit similar effects on leukocyte distributions but dissimilar effects on plasma-based immunological indices in pigeons, Journal of Experimental Biology, 10.1242/jeb.072264 Madelaire C, Zena L, Dillon D, Silva D, Hunt K, Buck C, Bícego K and Gomes F (2021) Who Rules Over Immunology? Seasonal Variation in Body Temperature, Steroid Hormones, and Immune Variables in a Tegu Lizard, Integrative and Comparative Biology, 10.1093/icb/icab093 Zamora-Camacho F and Comas M (2018) Early swelling response to phytohemagglutinin is lower in older toads, PeerJ, 10.7717/peerj.6104, 6, (e6104) Murdock C, Foufopoulos J, Simon C and Clarke R (2013) A Transmission Model for the Ecology of an Avian Blood Parasite in a Temperate Ecosystem, PLoS ONE, 10.1371/journal.pone.0076126, 8:9, (e76126) This Issue22 November 1996Volume 263Issue 1376 Article InformationDOI:https://doi.org/10.1098/rspb.1996.0210PubMed:8952087Published by:Royal SocietyPrint ISSN:0962-8452Online ISSN:1471-2954History: Manuscript received16/04/1996Manuscript accepted18/06/1996Published online01/01/1997Published in print22/11/1996 License:Scanned images copyright © 2017, Royal Society Citations and impact Large datasets are available through Proceedings B's partnership with Dryad

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