Abstract
In group-living animals, the social environment is thought to affect the probability of parasite transmission. Here, I investigate relationships between social behaviour and gastrointestinal parasite product excretion in the carrion crow (Corvus corone). Individuals from a population of non-cooperatively breeding carrion crows excreted less samples containing coccidian oocysts when kept in larger groups (8 or 9 individuals) compared to those individuals kept in smaller groups (2 or 3 individuals). Lower-ranking individuals excreted more samples containing parasite oocysts compared to higher-ranking individuals. The strength of affiliative relationships and number of related individuals in the group did not relate to the proportion of droppings containing coccidian oocysts. The present results confirm an association between social environment and parasite excretion patterns in carrion crows, but the patterns described in the present study differ from previously published data derived from a group of cooperatively breeding crows. This illustrates that differences between the social systems of carrion crows might result in different associations between the social environment and parasite product excretion patterns.
Significance statement
One major cost of group living is increased susceptibility to parasites. Not all individuals are affected by this in the same way. A better understanding of the relationship between social behaviour and parasite burden can help to better understand evolution of group living. I investigate associations between dominance rank, affiliative relationships, group size, and gastrointestinal parasite product excretion in a group of captive carrion crows. Lower-ranking individuals excreted more samples containing parasite oocysts compared to higher-ranking individuals, confirming an association between social relationships and parasite excretion patterns.
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References
Akinyi MY, Jansen D, Habig B, Gesquiere LR, Alberts SC, Archie EA (2019) Costs and drivers of helminth parasite infection in wild female baboons. J Anim Ecol 88:1029–1043. https://doi.org/10.1111/1365-2656.12994
Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Evol Syst 5:325–383
Apanius V (1998) Stress and immune defense. Adv Study Behav 27:133–153
Archie EA, Altmann J, Alberts SC (2012) Social status predicts wound healing in wild baboons. Proc Natl Acad Sci U S A 109:9017–9022. https://doi.org/10.1073/pnas.1206391109
Archie EA, Tung J, Clark M, Altmann J, Alberts SC (2014) Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons. Proc R Soc B 281:20141261. https://doi.org/10.1098/rspb.2014.1261
Azpiroz A, Garmendia L, Fano E, Sanchez-Martin JR (2003) Relations between aggressive behavior, immune activity, and disease susceptibility. Aggress Violent Behav 8:433–453. https://doi.org/10.1016/S1359-1789(02)00066-6
Baglione V, Canestrari D, Marcos JM, Ekman J (2003) Kin selection in cooperative alliances of carrion crows. Science 300:1947–1949. https://doi.org/10.1126/science.1082429
Baglione V, Marcos JM, Canestrari D, Griesser M, Andreotti G, Bardini C, Bogliani G (2005) Does year-round territoriality rather than habitat saturation explain delayed natal dispersal and cooperative breeding in the carrion crow? J Anim Ecol 74:842–851. https://doi.org/10.1111/j.1365-2656.2005.00983.x
Balasubramaniam KN, Beisner BA, Hubbard JA, Vandeleest JJ, Atwill ER, McCowan B (2019) Affiliation and disease risk: social networks mediate gut microbial transmission among rhesus macaques. Anim Behav 151:131–143. https://doi.org/10.1016/j.anbehav.2019.03.009
Barnard CJ, Behnke JM, Gage AR, Brown H, Smithurst PR (1998) The role of parasite–induced immunodepression, rank and social environment in the modulation of behaviour and hormone concentration in male laboratory mice (Mus musculus). Proc R Soc Lond B 265:693–701. https://doi.org/10.1098/rspb.1998.0349
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Beehner JC, Bergman TJ (2017) The next step for stress research in primates: to identify relationships between glucocorticoid secretion and fitness. Horm Behav 91:68–83. https://doi.org/10.1016/j.yhbeh.2017.03.003
Buchholz R (1995) Female choice, parasite load and male ornamentation in wild turkeys. Anim Behav 50:929–943. https://doi.org/10.1016/0003-3472(95)80095-6
Bugnyar T, Kijne M, Kotrschal K (2001) Food calling in ravens: are yells referential signals? Anim Behav 61:949–958. https://doi.org/10.1006/anbe.2000.1668
Carta LK, Carta DG (2000) Nematode specific gravity profiles and applications to flotation extraction and taxonomy. Nematology 2:201–210
Cavigelli SA, Chaudhry HS (2012) Social status, glucocorticoids, immune function, and health: Can animal studies help us understand human socioeconomic-status-related health disparities? Horm Behav 62:295–313. https://doi.org/10.1016/j.yhbeh.2012.07.006
Chester EM, Bonu T, Demas GE (2010) Social defeat differentially affects immune responses in Siberian hamsters (Phodopus sungorus). Physiol Behav 101:53–58. https://doi.org/10.1016/j.physbeh.2010.04.016
Chiarati E, Canestrari D, Vera R, Marcos JM, Baglione V (2010) Linear and stable dominance hierarchies in cooperative carrion crows. Ethology 116:346–356. https://doi.org/10.1111/j.1439-0310.2010.01741.x
Chiarati E, Canestrari D, Vila M, Vera R, Baglione V (2011) Nepotistic access to food resources in cooperatively breeding carrion crows. Behav Ecol Sociobiol 65:1791–1800. https://doi.org/10.1007/s00265-011-1187-1
Clough D, Heistermann M, Kappeler PM (2010) Host intrinsic determinants and potential consequences of parasite infection in free-ranging red-fronted lemurs (Eulemur fulvus rufus). Am J Phys Anthropol 142:441–452. https://doi.org/10.1002/ajpa.21243
Coté IM, Poulin R (1995) Parasitism and group size in social animals: a meta-analysis. Behav Ecol 6:159–165. https://doi.org/10.1093/beheco/6.2.159
Creel S (2001) Social dominance and stress hormones. Trends Ecol Evol 16:491–497. https://doi.org/10.1016/S0169-5347(01)02227-3
Creel S, Creel N, Wildt DE, Monfort SL (1992) Behavioural and endocrine mechanisms of reproductive suppression in Serengeti dwarf mongooses. Anim Behav 43:231–245. https://doi.org/10.1016/s0003-3472(05)80219-2
Daş G, Savaş T, Kaufmann F, Idris A, Abel H, Gauly M (2011) Precision, repeatability and representative ability of faecal egg counts in Heterakis gallinarum infected chickens. Vet Parasitol 183:87–94. https://doi.org/10.1016/j.vetpar.2011.07.005
de Kort SR, Emery NJ, Clayton NS (2003) Food offering in jackdaws (Corvus monedula). Naturwissenschaften 90:238–240. https://doi.org/10.1007/s00114-003-0419-2
Decristophoris PMA, von Hardenberg A, McElligott AG (2007) Testosterone is positively related to the output of nematode eggs in male Alpine ibex (Capra ibex) faeces. Evol Ecol Res 9:1277–1292
Defolie C, Merkling T, Fichtel C (2020) Patterns and variation in the mammal parasite–glucocorticoid relationship. Biol Rev 95:74–93. https://doi.org/10.1111/brv.12555
DeVries AC, Glasper ER, Detillion CE (2003) Social modulation of stress responses. Physiol Behav 79:399–407. https://doi.org/10.1016/S0031-9384(03)00152-5
Dickinson JL, Euaparadorn M, Greenwald K, Mitra C, Shizuka D (2009) Cooperation and competition: nepotistic tolerance and intrasexual aggression in western bluebird winter groups. Anim Behav 7:867–872. https://doi.org/10.1016/j.anbehav.2008.11.026
Drewe JA (2010) Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proc R Soc Lond B 277:633–642. https://doi.org/10.1098/rspb.2009.1775
Duboscq J, Romano V, Sueur C, MacIntosh AJJ (2016) Network centrality and seasonality interact to predict lice load in a social primate. Sci Rep 6:22095. https://doi.org/10.1038/srep22095
Edgar SA (1955) Sporulation of oocysts at specific temperatures and notes on the prepatent period of several species of avian coccidia. J Parasitol 41:214. https://doi.org/10.2307/3273795
Emery NJ, Seed AM, von Bayern AMP, Clayton NS (2007) Cognitive adaptations of social bonding in birds. Philos Trans R Soc B 362:489–505. https://doi.org/10.1098/rstb.2006.1991
Ezenwa VO, Ghai RR, McKay AF, Williams AE (2016) Group living and pathogen infection revisited. Curr Opin Behav Sci 12:66–72. https://doi.org/10.1016/j.cobeha.2016.09.006
Foerster S, Kithome K, Cords M, Monfort SL (2015) Social status and helminth infections in female forest guenons (Cercopithecus mitis): rank and nematode infections in a forest guenon. Am J Phys Anthropol 158:55–66. https://doi.org/10.1002/ajpa.22764
Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage Publications, Thousand Oakes
Fraser ON, Bugnyar T (2010) The quality of social relationships in ravens. Anim Behav 79:927–933. https://doi.org/10.1016/j.anbehav.2010.01.008
Fraser ON, Bugnyar T (2012) Reciprocity of agonistic support in ravens. Anim Behav 83:171–177. https://doi.org/10.1016/j.anbehav.2011.10.023
French RA, Zachary JF (1994) Parasitology and pathogenesis of Geopetitia aspiculata (Nematoda: Spirurida) in zebra finches (Taeniopygia guttata): experimental infection and new host records. J Zoo Wildl Med 25:403–422
Frigerio D, Weiss B, Dittami J, Kotrschal K (2003) Social allies modulate corticosterone excretion and increase success in agonistic interactions in juvenile hand-raised graylag geese (Anser anser). Can J Zool 81:1746–1754. https://doi.org/10.1139/Z03-149
Fugazzola MC, Stancampiano L (2012) Host social rank and parasites: plains zebra (Equus quagga) and intestinal helminths in Uganda. Vet Parasitol 188:115–119. https://doi.org/10.1016/j.vetpar.2012.03.019
Glutz von Blotzheim UN (1985) Handbuch der Vögel Mitteleuropas. Aula-Verlag, Wiesbaden
Goymann W, Wingfield JC (2004) Allostatic load, social status and stress hormones: the costs of social status matter. Anim Behav 67:591–602. https://doi.org/10.1016/j.anbehav.2003.08.007
Granthon C, Williams DA (2017) Avian malaria, body condition, and blood parameters in four species of songbirds. Wilson J Ornithol 129:492–508. https://doi.org/10.1676/16-060.1
Habig B, Archie EA (2015) Social status, immune response and parasitism in males: a meta-analysis. Philos Trans R Soc B 370:20140109. https://doi.org/10.1098/rstb.2014.0109
Habig B, Doellman MM, Woods K, Olansen J, Archie EA (2018) Social status and parasitism in male and female vertebrates: a meta-analysis. Sci Rep 8:3629. https://doi.org/10.1038/s41598-018-21994-7
Habig B, Jansen DAWAM, Akinyi MY, Gesquiere LR, Alberts SC, Archie EA (2019) Multi-scale predictors of parasite risk in wild male savanna baboons (Papio cynocephalus). Behav Ecol Sociobiol 73:134. https://doi.org/10.1007/s00265-019-2748-y
Hanley KA, Stamps JA (2002) Does corticosterone mediate bidirectional interactions between social behaviour and blood parasites in the juvenile black iguana, Ctenosaura similis? Anim Behav 63:311–322. https://doi.org/10.1006/anbe.2001.1874
Hau M, Gill SA, Goymann W (2008) Tropical field endocrinology: ecology and evolution of testosterone concentrations in male birds. Gen Comp Endocrinol 157:241–248. https://doi.org/10.1016/j.ygcen.2008.05.008
Hawley DM, Lindström K, Wikelski M (2006) Experimentally increased social competition compromises humoral immune responses in house finches. Horm Behav 49:417–424. https://doi.org/10.1016/j.yhbeh.2005.09.003
Heinrich B (2011) Conflict, cooperation, and cognition in the common raven. Adv Study Behav 43:189–237. https://doi.org/10.1016/B978-0-12-380896-7.00004-6
Hillegass MA, Waterman JM, Roth JD (2008) The influence of sex and sociality on parasite loads in an African ground squirrel. Behav Ecol 19:1006–1011. https://doi.org/10.1093/beheco/arn070
Hillegass MA, Waterman JM, Roth JD (2010) Parasite removal increases reproductive success in a social African ground squirrel. Behav Ecol 21:696–700. https://doi.org/10.1093/beheco/arq041
Hopkins SR, Fleming-Davies AE, Belden LK, Wojdak JM (2020) Systematic review of modelling assumptions and empirical evidence: does parasite transmission increase nonlinearly with host density? Methods Ecol Evol 11:476–486. https://doi.org/10.1111/2041-210X.13361
Hudman SP, Ketterson ED, Nolan V (2000) Effects of time of sampling on oocyst detection and effects of age and experimentally elevated testosterone on prevalence of coccidia in male dark-eyed juncos. Auk 117:1048–1051
Izawa E-I, Watanabe S (2008) Formation of linear dominance relationship in captive jungle crows (Corvus macrorhynchos): implications for individual recognition. Behav Process 78:44–52. https://doi.org/10.1016/j.beproc.2007.12.010
Klein SL (2003) Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiol Behav 79:441–449. https://doi.org/10.1016/S0031-9384(03)00163-X
Klein SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26:247–264. https://doi.org/10.1111/j.0141-9838.2004.00710.x
Levy EJ, Gesquiere LR, McLean E et al (2020) Higher dominance rank is associated with lower glucocorticoids in wild female baboons: a rank metric comparison. Horm Behav 125:104826. https://doi.org/10.1016/j.yhbeh.2020.104826
Loehle C (1995) Social barriers to pathogen transmission in wild animal populations. Ecology 76:326–335
Lopes PC, Block P, König B (2016) Infection-induced behavioural changes reduce connectivity and the potential for disease spread in wild mice contact networks. Sci Rep 6:31790. https://doi.org/10.1038/srep31790
Ludwig SC, Kapetanopoulos K, Kotrschal K, Wascher CAF (2017) Effects of mate separation in female and social isolation in male free-living Greylag geese on behavioural and physiological measures. Behav Process 138:134–141. https://doi.org/10.1016/j.beproc.2017.03.002
Marzal A, de Lope F, Navarro C, Møller AP (2005) Malarial parasites decrease reproductive success: an experimental study in a passerine bird. Oecologia 142:541–545. https://doi.org/10.1007/s00442-004-1757-2
McEwen BS, Biron CA, Brunson KW et al (1997) The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions. Brain Res Rev 23:79–133
Meide M (1984) Raben- und Nebelkrähe. Westarp Wissenschaften, Magdeburg
Muehlenbein MP, Watts DP (2010) The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. BioPsychoSocial Med 4:21. https://doi.org/10.1186/1751-0759-4-21
Müller-Klein N, Heistermann M, Strube C, Franz M, Schülke O, Ostner J (2019) Exposure and susceptibility drive reinfection with gastrointestinal parasites in a social primate. Funct Ecol 33:1088–1098. https://doi.org/10.1111/1365-2435.13313
Neumann C, Duboscq J, Dubuc C, Ginting A, Irwan AM, Agil M, Widdig A, Engelhardt A (2011) Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating. Anim Behav 82:911–921. https://doi.org/10.1016/j.anbehav.2011.07.016
Patterson JEH, Ruckstuhl KE (2013) Parasite infection and host group size: a meta-analytical review. Parasitology 140:803–813. https://doi.org/10.1017/S0031182012002259
Puehringer-Sturmayr V, Wascher CAF, Loretto M-C, Palme R, Stoewe M, Kotrschal K, Frigerio D (2018) Seasonal differences of corticosterone metabolite concentrations and parasite burden in northern bald ibis (Geronticus eremita): the role of affiliative interactions. PLoS ONE 13:e0191441. https://doi.org/10.1371/journal.pone.0191441
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.r723project.org/
Rafalinirina AH, Randrianasy J, Wright PC, Ratsimbazafy J (2019) Effect of socio-ecological factors and parasite infection on body condition of Brown Mouse Lemur Microcebus rufus (Mammalia: Primates: Cheirogaleidae). J Threat Taxa 11:13632–13643. https://doi.org/10.11609/jott.4799.11.6.13632-13643
Rau ME (1983) Establishment and maintenance of behavioural dominance in male mice infected with Trichinella spiralis. Parasitology 86:319–322. https://doi.org/10.1017/S0031182000050484
Rifkin JL, Nunn CL, Garamszegi LZ (2012) Do animals living in larger groups experience greater parasitism? A meta-analysis. Am Nat 180:70–82. https://doi.org/10.1086/666081
Rimbach R, Bisanzio D, Galvis N, Link A, Di Fiore A, Gillespie TR (2015) Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics. Philos Trans R Soc B 370:20140110. https://doi.org/10.1098/rstb.2014.0110
Romano V, Duboscq J, Sarabian C, Thomas E, Sueur C, MacIntosh AJJ (2016) Modeling infection transmission in primate networks to predict centrality-based risk: Individual Centrality and Infection Flow. Am J Primatol 78:767–779. https://doi.org/10.1002/ajp.22542
Romeo C, Wauters LA, Santicchia F, Dantzer B, Palme R, Martinoli A, Ferrari N (2020) Complex relationships between physiological stress and endoparasite infections in natural populations. Curr Zool 66:449–457. https://doi.org/10.1093/cz/zoaa029
Rousset F, Thomas F, De Meeûs T, Renaud F (1996) Inference of parasite-induced host mortality from distributions of parasite loads. Ecology 77:2203–2211
Sachser N, Dürschlag M, Hirzel D (1998) Social relationships and the management of stress. Psychoneuroendocrino 23:891–904
Sánchez-Tójar A, Schroeder J, Farine DR (2018) A practical guide for inferring reliable dominance hierarchies and estimating their uncertainty. J Anim Ecol 87:594–608. https://doi.org/10.1111/1365-2656.12776
Schnieder T, Boch J, Supperer R (2006) Veterinärmedizinische Parasitologie, 6th edn. Parey, Berlin
Seivwright LJ, Redpath SM, Mougeot F, Watt L, Hudson PJ (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J Helminthol 78:69–76. https://doi.org/10.1079/JOH2003220
Sheridan JF, Dobbs C, Brown D, Zwilling B (1994) Psychoneuroimmunology: stress effects on pathogenesis and immunity during infection. Clin Microbiol Rev 7:200–212
Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010) Female chacma baboons form strong, equitable, and enduring social bonds. Behav Ecol Sociobiol 64:1733–1747. https://doi.org/10.1007/s00265-010-0986-0
Soma KK (2006) Testosterone and aggression: Berthold, birds and beyond. J Neuroendocrinol 18:543–551. https://doi.org/10.1111/j.1365-2826.2006.01440.x
Spreafico M, Szipl G, Kotrschal K, Wascher CAF (2012) Physiological and behavioural response in carrion crows (Corvus corone corone) after relocation to a new environment. Wien Tierarztl Monat 99(Suppl 1):61 (abstract)
Stöwe M, Bugnyar T, Schloegl C, Heinrich B, Kotrschal K, Möstl E (2008) Corticosterone excretion patterns and affiliative behavior over development in ravens (Corvus corax). Horm Behav 53:208–216. https://doi.org/10.1016/j.yhbeh.2007.09.021
VanderWaal KL, Obanda V, Omondi GP, McCowan B, Wang H, Fushing H, Isbell LA (2016) The “strength of weak ties” and helminth parasitism in giraffe social networks. Behav Ecol 27:1190–1197. https://doi.org/10.1093/beheco/arw035
von Holst D (1998) The concept of stress and its relevance for animal behavior. Adv Study Behav 27:1–131
Wascher CAF, Arnold W, Kotrschal K (2008) Heart rate modulation by social contexts in greylag geese (Anser anser). J Comp Psychol 122:100–107. https://doi.org/10.1037/0735-7036.122.1.100
Wascher CAF, Scheiber IBR, Weiß BM, Kotrschal K (2009) Heart rate responses to agonistic encounters in greylag geese, Anser anser. Anim Behav 77:955–961. https://doi.org/10.1016/j.anbehav.2009.01.013
Wascher CAF, Kulahci IG, Langley EJG, Shaw RC (2018) How does cognition shape social relationships? Philos Trans R Soc B 373:20170293. https://doi.org/10.1098/rstb.2017.0293
Wascher CAF, Canestrari D, Baglione V (2019) Affiliative social relationships and coccidian oocyst excretion in a cooperatively breeding bird species. Anim Behav 158:121–130. https://doi.org/10.1016/j.anbehav.2019.10.009
Wittig RM, Crockford C, Weltring A, Deschner T, Zuberbühler K (2015) Single aggressive interactions increase urinary glucocorticoid levels in wild male chimpanzees. PLoS ONE 10:e0118695. https://doi.org/10.1371/journal.pone.0118695
Young AJ, Carlson AA, Monfort SL, Russell AF, Bennett NC, Clutton-Brock T (2006) Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc Natl Acad Sci USA 103:12005–12010. https://doi.org/10.1073/pnas.0510038103
Young C, Majolo B, Schülke O, Ostner J (2014) Male social bonds and rank predict supporter selection in cooperative aggression in wild Barbary macaques. Anim Behav 95:23–32. https://doi.org/10.1016/j.anbehav.2014.06.007
Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1024
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extension in ecology with R. Springer, New York
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I am very grateful to Gaius de Smidt for detailed feedback on the manuscript. I also thank two anonymous referees for valuable comments on the manuscript.
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This work was supported by the Fonds zur Förderung Wissenschaftlicher Forschung Austria (FWF) project P21489-B17 to Kurt Kotrschal and CAFW, and permanent support was provided by the ‘Verein der Förderer’ and the Herzog von Cumberland Stiftung.
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All procedures were conducted in accordance with the ASAB/ABS guidelines for the treatment of animals in behavioural research. The keeping of these captive birds was authorized under a license issued to the Cumberland Wildlife park Grünau (AT00009917). Data collection was entirely non-invasive, and no further animal experimental license was required.
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Wascher, C.A. Association between social factors and gastrointestinal parasite product excretion in a group of non-cooperatively breeding carrion crows. Behav Ecol Sociobiol 75, 30 (2021). https://doi.org/10.1007/s00265-021-02967-9
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DOI: https://doi.org/10.1007/s00265-021-02967-9