Skip to main content
Log in

Ectoparasitism as a possible cost of social life: a comparative analysis using Australian passerines (Passeriformes)

  • Original Papers
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The hypothesis that cooperative breeding entails a cost in terms of transmission of ectoparasites was tested by a comparative analysis among sympatric Australian passerines. The general trend found using the allometry method and outgroup analysis indicates that contagious ectoparasites are not more common on cooperatively breeding than on non-cooperatively breeding hosts. Body weight, migratory patterns and relative abundance of hosts are factors far more important than cooperative breeding that affect the levels of ectoparasitism in the host genera studies. Ectoparasitism increases with host body weight and relative adundance, while sedentary host genera tended to show less hippoboscid fly diversity than migratory host genera. There is an interaction between breeding system and migratory pattern when relative density of contagious ectoparasites (i.e. mites, ticks and bird lice) is considered: the number of contagious ectoparasites per host is larger on cooperatively breeding host genera than on non-cooperatively breeding host genera among sedentary passerines, but the trend is reversed for migrant passerines.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alexander RD (1974) The evolution of social behaviour.Annu Rev Ecol Syst 5:325–383

    Google Scholar 

  • Anderson JF, Magnarelli LA (1984) Avian and Mammalian hosts for spirochete-infected ticks and insects in a lymc disease focus in Connecticut. Yale J Biol Med 57:627–641

    Google Scholar 

  • Arendt WJ (1985) Philornis ectoparasitism of Pearly-eyed Thrashers II. Effects on adults and reproduction. Auk 102: 281–292

    Google Scholar 

  • Arlian LG, Vyszenski-Moher DL (1987) Nutritional ecology of parasitic mites and ticks. In: Slansky F, Rodríguez JG (eds) Nutritional ecology of insects, mites, spiders and related invertebrates. Wiley, New York, pp 765–790

    Google Scholar 

  • Barclay RM (1988) Variation in the costs, benefits, and frequency of nest reuse by Barn Swallows (Hirundo rustica). Auk 105:53–60

    Google Scholar 

  • Baron RW, Weintraub J (1987), Immunological responses to parasitic arthropods. Parasitol Today 3:77–82

    Google Scholar 

  • Blakers M, Davies SJJF, Reilly PN (1984) The atlas of Australian birds. Melbourne University Press, Melbourne

    Google Scholar 

  • Bliss CI, Fisher RA (1953) Fitting the negative binomial distribution to biological data. Biometrics 9:176–200

    Google Scholar 

  • Borgia G, Collins K (1989) Female choice for parasite-free male Satin Bowerbirds and the evolution of bright male plumage. Behav Ecol Sociobiol 25:445–454

    Google Scholar 

  • Brooke MdeL (1985) The effect of allopreening on tick burdens of molting eudypid penguins. Auk 102:893–895

    Google Scholar 

  • Brown JL (1987) Helping and communal breeding in birds. Ecology and evolution. Princeton University Press, Princeton

    Google Scholar 

  • Bucher EH (1988) Do birds use biological control against nest parasites? Parasitol Today 4:1–3

    Google Scholar 

  • Büttiker W (1969) Parasiten und nidicolen der Uferschwalbe. Mitt Schweiz Entomol Ges 42:205–220

    Google Scholar 

  • Christidis L, Schodde R (1991) Relationships of Australo-Papuan song birds-protein evidence. Ibis 133:277–285

    Google Scholar 

  • Clark L, Mason JR (1985) Use of nest material as insecticidal and anti-pathogenic agents by the European Starling. Oecologia 67:169–176

    Google Scholar 

  • Clark L, Mason JR (1988) Effect of biologically active plants used as nest material and the derived benefit to starling nestlings. Oecologia 77:174–180

    Google Scholar 

  • Clarke MF, Heathcote CF (1988) Methods for sexing and ageing the Bell Miner Manorina melanophys. Emu 88:118–121

    Google Scholar 

  • Coddington JA (1988) Cladistic tests of adaptational hypotheses. Cladistics 4:3–22

    Google Scholar 

  • Conover WJ (1980) Practical nonparametric statistics, 2nd edn. Wiley, New York

    Google Scholar 

  • Davies CR, Dye CM (1991) Malaria infection rate of Amazonian monkeys increases with sleeping group size. Bull Br Ecol Soc 22:39–44

    Google Scholar 

  • Davies CR, Ayres JM, Dye C, Deane LM (1991) Malaria infection rate of Amazonian primates increases with body weight and group size. Funct Ecol 5:655–662

    Google Scholar 

  • Davies NB (1985) Cooperation and conflict among dunnocks, Prunella modularis in a variable mating system. Anim Behav 33:628–648

    Google Scholar 

  • Duffy DC (1983) The ecology of tick-parasitism on densely nesting peruvian seabirds. Ecology 64:110–119

    Google Scholar 

  • Emlen JT (1986) Responses of breeding Cliff Swallows to nidicolous parasite infestations. Condor 88:110–111

    Google Scholar 

  • Emlen ST, Wrege PH (1986) Forced copulations and intra-specific parasitism: two costs of social living in the White-fronted Beeeater. Ethology 71:2–29

    Google Scholar 

  • Emlen ST, Wrege PH (1989) A test of alternate hypotheses for helping behavior in White-fronted Bee-eaters of Kenya. Behav Ecol Sociobiol 25:303–319

    Google Scholar 

  • Fowler JA, Cohen S (1983) A method for quantitative collection of ectoparasites from birds. Ring Mig 4:185–189

    Google Scholar 

  • Fowler JA, Williams LR (1985) Population dynamics of Mallophaga and Acari on Reed Buntings occupying a communal winter roost. Ecol Entomol 10:377–383

    Google Scholar 

  • Freeland WJ (1976) Pathogens and the evolution of primate sociality. Biotropica 8:12–24

    Google Scholar 

  • Freeland WJ (1977) Blood-sucking flies and primate polyspecific associations. Nature 269:801–802

    Google Scholar 

  • Gaston AJ (1978) The evolution of group territorial behaviour and cooperative breeding. Am Nat 112:1091–1100

    Google Scholar 

  • Gehlbach FR, Baldridge RS (1987) Live blind snakes (Leptotyphlops dulcis) in eastern screech owl (Otus asio) nests: a novel commensalism. Oecologia 71:560–563

    Google Scholar 

  • Godfrey RDJr, Fedynich AM, Pence DB (1987) Quantification of hematozoa in blood smears. J Wildl Dis 23:558–565

    Google Scholar 

  • Gregory RD, Keymer AE, Harvey PH (1991) Life-history, ecology and parasite community structure in Soviet birds. Biol J Linn Soc 43:249–262

    Google Scholar 

  • Hamilton WD (1987) Kinship, recognition, disease, and intelligence: constraints of social evolution. In: Itô Y, Brown JL, Kikkawa J (eds) Animal societies: theories and facts. Japan Sci Soc Press, Tokyo, pp 81–102

    Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387

    Google Scholar 

  • Harvey PH, Mace GM (1982) Comparisons between taxa and adaptive trends: problems of methodology. In: King's College Sociobiology Group (ed) Current problems in sociobiology. Cambridge University Press, Cambridge, pp 343–361

    Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press. Oxford

    Google Scholar 

  • Hastwell K (1991) Use: of mud during preening by currawongs Strepera spp. Aust Bird Watch 14:73

    Google Scholar 

  • Heinsohn RG, Cockburn A, Mulder RA (1990) Avian cooperative breeding: old hypotheses and new directions. Trends Ecol Evol 5:403–407

    Google Scholar 

  • Hemmings AD (1989) Communally breeding skuas: breeding success of pairs, trios and groups of Catharacta lonnbergi on the Chatham Islands, New Zealand. J Zool London 218:393–405

    Google Scholar 

  • Hoogland JL (1979) Aggression, ectoparasitism, and other possible costs of prairie dog (Sciuridae, Cynomys spp.) coloniality. Behaviour 69:1–35

    Google Scholar 

  • Hoogland JL (1981) Nepotism and cooperative breeding in the Black-tailed Prairie Dog (Sciuridae: Cynomys ludovicianus). In: Alexander RD, Tinkle DW (eds) Natural selection and social behaviour. Recent research and new theory. Chiron Press, New York, pp 283–310

    Google Scholar 

  • Hoogland JL, Sherman PW (1976) Advantages and disadvantages of Bank Swallow (Riparia riparia) coloniality. Ecol Monogr 46:33–58

    Google Scholar 

  • Humason GL (1967) Animal tissue techniques, 2nd edn. Freeman, San Francisco

    Google Scholar 

  • Kaspari M, O'Leary H (1988) Nonparental attendants in a Northtemperate migrant. Auk 105:792–793

    Google Scholar 

  • Koenig WD, Mumme RL (1990) Levels of analysis and the functional significance of helping behavior. In: Bekoff M, Jamieson D (eds) Interpretation and explanation in the study of animal behaviour. Vol II. Explanation, evolution, and adaptation. Westview Press, Boulder, pp 268–303

    Google Scholar 

  • Kuris AM, Blaustein AR, Alió JJ (1980) Hosts as islands. Am Nat 116:570–586

    Google Scholar 

  • Ligon DJ, Stacey PB (1989) On the significance of helping behavior in birds. Auk 106:700–705

    Google Scholar 

  • Margolis L, Esch GW, Holmes JC, Kuris AM, Schad GA (1982) The use of ecological terms in parasitology (report of an ad hoc committee of the American Society of Parasitologists). J Parastiol 68:131–133

    Google Scholar 

  • Marshall AG (1987) Nutritional ecology of ectoparasitic insects. In: Slansky FJr, Rodríguez JG (eds) Nutritional ecology of insects, mites, spiders and related invertebrates. Wiley, New York, pp 721–739

    Google Scholar 

  • Maynard-Smith J (1964) Group selection and kin selection. Nature 201:1145–1147

    Google Scholar 

  • Møller AP (1987) Advantages and disadvantages of coloniatily in the Swallow, Hirundo rustica. Anim Behav 35:819–832

    Google Scholar 

  • Møller AP (1990) Effects of parasitism by a haematophagous mite on reproduction in the Barn Swallow. Ecology 71:2345–2357

    Google Scholar 

  • Møller AP (1991a) Ectoparasite loads affect optimal clutch size in swallows. Funct Ecol 5:351–359

    Google Scholar 

  • Møller AP (1991b) The preening activity of swallows, Hirundo rustica in relation to experimentally manipulated loads of haematophagous mites. Anim Behav 42:251–260

    Google Scholar 

  • Moore J, Simberloff D, Freehling M (1988) Relationships between Bobwhite Quail social-group size and intestinal helminth parasitism. Am Nat 131:22–32

    Google Scholar 

  • Oppenheimer JR (1968) Behaviour and ecology of the white-faced monkey Cebus capuchinus, on Barro Colorado island, C.Z. PhD Thesis, University of Illinois, Urbana

  • Pagel MD, Harvey PH (1988) Recent developments in the analysis of comparative data. Q Rev Biol 63:413–440

    Google Scholar 

  • Poiani A (1990) Communal roosting of the Bell Miner Manorina melanophrys, Meliphagidae. Victoria Nat 107:105–106

    Google Scholar 

  • Poiani A (1992) Hormonal, behavioural and ecological aspects of cooperative breeding in the Bell Miner (Manorina melanophrys, Meliphagidae). PhD Thesis, Department of Zoology, La Trobe University. Melbourne, Australia

  • Poiani A, Rogers A, Rogers K, Rogers D (1990) Asymmetrical competition between the Bell Miner (Manorina melanophrys, Meliphagidae) and other honeyeaters: evidence from Southeastern Victoria, Australia. Oecologia 85: 250–256

    Google Scholar 

  • Poulin R (1991a) Group-living and infestation by ectoparasites in passerines. Condor 93:418–423

    Google Scholar 

  • Poulin R (1991b) Group-living and richness of the parasite fauna in Canadian freshwater fishes. Oecologia 86:390–394

    Google Scholar 

  • Powlesland RG (1977) Effects of the haematophagous mite Ornithonyssus bursa on nestling starlings in New Zealand. N Z J Zool 4:85–94

    Google Scholar 

  • Ranta E (1992) Gregariousness versus solitude: another look at parasite faunal richness in Canadian freshwater fishes. Oecologia 89:150–152

    Google Scholar 

  • Reyer H-U, Dittami JP, Hall MR (1986) Avian helpers at the nest: are they psychologically castrated? Ethology 71:216–228

    Google Scholar 

  • Ridley M (1983) The explanation of organic diversity. Clarendon Press, Oxford

    Google Scholar 

  • Ridley M (1989) Why not to use species in comparative tests. J Theor Biol 136:361–364

    Google Scholar 

  • Rogers K, Rogers A, Rogers D (1986) Bander's aid: a guide to ageing and sexing bush birds. A. Rogers, St. Andrews

    Google Scholar 

  • Rubenstein DI, Hohmann ME (1989) Parasites and social behavior of island feral horses. Oikos 55:312–320

    Google Scholar 

  • Russell EM (1989) Co-operative breeding—a Gondwanan perspective. Emu 89:61–62

    Google Scholar 

  • Shearer PR (1973) Missing data in quantitative designs. J Stat Soc Ser C Appl Stat 22:135–140

    Google Scholar 

  • Sherman PW, Seeley TD, Reeve HK (1988) Parasites, pathogens, and polyandry in social hymenoptera. Am Nat 131:602–610

    Google Scholar 

  • Shields WM, Crook JR (1987) Barn Swallow coloniality: a net cost for group breeding in the Adirondacks? Ecology 68:1373–1386

    Google Scholar 

  • Shykoff JA, Schmid-Hempel P (1991) Genetic relatedness and eusociality: parasite-mediated selection on the genetic composition of groups. Behav Ecol Sociobiol 28:371–376

    Google Scholar 

  • Sibley CG, Ahlquist JE (1985) The phylogeny and classification of the Australo-papuan passerine birds. Emu 85: 1–14

    Google Scholar 

  • Simmons KEL (1966) Anting and the problem of self-stimulation. J Zool 149:145–162

    Google Scholar 

  • Skutch AF (1961) Helpers among birds. Condor 63:198–226

    Google Scholar 

  • Smith RJ (1984) Determination of relative size: the “criterion of subtraction” problem in allometry. J Theor Biol 108:131–142

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. 2nd edn. Freeman New York

    Google Scholar 

  • Trail PW, Strahl SD, Brown JL (1981) Intanticide in relation to individual and flock histories in a communally breeding bird, the Mexican Jay (Aphelocoma ultramarina). Am Nat 118:72–82

    Google Scholar 

  • Vehrencamp SL (1979) The roles of individual, kin and group selection in the evolution of sociality. In: Marler P, Vandenbergh JG (eds) Handbook of behavioral neurobiology. Vol. 3 Social behavior and communication. Plenum Press, New York, pp 351–394

    Google Scholar 

  • Wallace BM, Pence DB (1986) Population dynamics of the helminth community from migrating Blue-winged Teal: loss of helminyhs without replacement on the wintering grounds. Can J Zool 64:1765–1773

    Google Scholar 

  • Wheeler TA, Threlfall W (1986) Observations on the ectoparasites of some Newfoundland passerines (Aves: Passeriformes). Can J Zool 64:630–636

    Google Scholar 

  • Wikel SK (1982) Immune responses to arthropods and their products. Annu Rev Entomol 27:21–48

    Google Scholar 

  • Wimberger PH (1984) The use of green plant material in bird nests to avoid ectoparasites. Auk 101:615–618

    Google Scholar 

  • Yamagishi S, Fujioka M (1986) Heavy brood parasitism by the Common Cuckoo Cuculus canorus on the Azure-winged Magpie Cyanopica cyana. Tori 34:91–96

    Google Scholar 

  • Zahavi A (1974) Co-operative breeding in Eurasian birds. In: Frith HJ, Calaby JH (eds) Proceedings of the 16th International Ornithological Congress. Australian Academy of Science, Canberra, pp 685–693

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, New Jersey

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Poiani, A. Ectoparasitism as a possible cost of social life: a comparative analysis using Australian passerines (Passeriformes). Oecologia 92, 429–441 (1992). https://doi.org/10.1007/BF00317470

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00317470

Key words

Navigation