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Seasonal migration distance varies with natal dispersal and predicts parasitic infection in song sparrows

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Abstract

Seasonal migration and natal dispersal represent the major large-scale movements in the lives of animals. Individuals that are relatively prone to movement and exploration might thus be more likely to disperse and also to migrate farther. Such movement might be either negatively associated with parasitic infection (if infection prevents hosts from successful long-distance migration) or positively associated (e.g. if longer-distance migrants encounter more abundant or more diverse parasites). We examined whether natal dispersal tendency predicts seasonal migration distance in song sparrows (Melospiza melodia) and whether migration distance predicts infection with bloodborne parasites upon arrival at the breeding grounds. Migration distance, inferred from stable hydrogen isotope analysis (δ2H) of winter-grown tissue, was repeatable (repeatability = 0.41) over years. Birds that were more likely to have immigrated from outside the breeding grounds, as inferred from genetic assignment tests, also overwintered farther south, as inferred from stable isotope analysis. The finding that individuals more prone to movement in the context of natal dispersal also tended to travel farther, on average, in the context of seasonal migration suggests consistent individual variation in large-scale movements across these two contexts. Although statistically significant, this effect was modest in scope and subtle relative to sex differences in inferred migration distance. Among after-second-year individuals, but not yearlings, longer-distance migrants were more likely, on average, to be infected with bloodborne parasites. Individual variation in propensity to long-distance movement may interact with age-related variation in exposure or susceptibility to parasites, to shape the role of animal migration in transporting infectious disease.

Significance statement

In many animal species, individuals vary consistently in activity and movement over small geographic scales. Large-scale movements such as seasonal migration are of particular interest because they can influence disease risk, but until recently, such movements have been difficult to track. We used stable isotope analysis to estimate overwintering latitude of song sparrows returning to their breeding grounds. Individuals overwintering farther south were also more likely to have immigrated from outside the breeding site, indicating that movement is correlated across the contexts of migration and dispersal. Rates of infection with bloodborne parasites increased with migration distance in older birds, but not in yearlings. Our findings suggest that individual variation in movement may interact with age-related variation in infection risk, to shape the role of animal migration in transporting parasites.

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References

  • Altizer SA, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science 331:296–302

    Article  CAS  PubMed  Google Scholar 

  • Arcese P (1989) Intrasexual competition, mating system and natal dispersal in song sparrows. Anim Behav 38:958–979

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) lme4: linear mixed-effects models using Eigen and S4. R package version 1:1–9 https://CRAN.R-project.org/package=lme4

    Google Scholar 

  • Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradley C, Altizer S (2005) Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts. Ecol Lett 8:290–300

    Article  Google Scholar 

  • Buehler DM, Tieleman BI, Piersma T (2010) Indices of immune function are lower in red knots (Calidris canutus) recovering protein than in those storing fat during stopover in Delaware Bay. Auk 127:394–401

    Article  Google Scholar 

  • Davis A, Arcese P (1999) An examination of migration in song sparrows using banding recovery data. N Am Bird Bander 24:122–128

    Google Scholar 

  • Dingemanse NJ, Both C, van Noordwijk AJ, Rutten AL, Drent PJ (2003) Natal dispersal and personalities in great tits (Parus major). Proc R Soc Lond B 270:741–747

    Article  Google Scholar 

  • Figuerola J, Green AJ (2000) Haematozoan parasites and migratory behaviour in waterfowl. Evol Ecol 14:143–153

    Article  Google Scholar 

  • Fraser D, Gilliam J, Daley M, Le A, Skalski G (2001) Explaining leptokurtic movement distributions: intrapopulation variation in boldness and exploration. Am Nat 158:124–135

    Article  CAS  PubMed  Google Scholar 

  • Garamszegi LZ (2010) The sensitivity of microscopy and PCR-based detection methods affecting estimates of infection prevalence of blood parasites in birds. J Parasitol 96:1197–1203

    Article  PubMed  Google Scholar 

  • Gauthreaux SA Jr (1978) The ecological significance of behavioral dominance. In: Bateson PPG, Klopfer PH (eds) Perspectives in ecology. Springer Verlag, New York, pp. 17–54

    Google Scholar 

  • Gregory RD (1990) Parasites and host geographic range as illustrated by waterfowl. Funct Ecol 4:645–654

    Article  Google Scholar 

  • Griffith SC, Stewart IRK, Dawson DA, Owens IPF, Burke T (1999) Contrasting levels of extra-pair paternity in mainland and island populations of the house sparrow (Passer domesticus): is there an “island effect”? Biol J Linn Soc 68:303–316

    Google Scholar 

  • Hellgren O, Waldenström J, Bensch S (2004) A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J Parasitol 90:797–802

    Article  CAS  PubMed  Google Scholar 

  • Hill NJ, Takekawa JY, Ackerman JC, Hobson KA, Herring G, Cardona CJ, Runstadler JA, Boyce WM (2012) Migration strategy affects avian influenza dynamics in mallards (Anas platyrynchos). Mol Ecol 21:5986–5999

    Article  PubMed  Google Scholar 

  • Hjernquist MB, Veen T, Font L, Klaassen M (2009) High individual repeatability and population differentiation in stable isotope ratios in winter-grown collared flycatcher Ficedula albicollis feathers. J Avian Biol 40:102–107

    Article  Google Scholar 

  • Hobson KA, Van Wilgenburg SL, Faaborg J, Toms JD, Rengifo C, Llanes Sosa A, Aubry Y, Brito Aguilar R (2014) Connecting breeding and wintering grounds of Neotropical migrant songbirds using stable hydrogen isotopes: a call for an isotopic atlas of migratory connectivity. J Field Ornithol 85:237–257

    Article  Google Scholar 

  • Hoye BJ, Fouchier RAM, Klaassen M (2012) Host behaviour and physiology underpin individual variation in avian influenza virus infection in migratory Bewick’s swans. Proc R Soc Lond B 279:529–534

    Article  CAS  Google Scholar 

  • Jeffrey KJ, Keller LF, Arcese P, Bruford MW (2001) The development of microsatellite loci in the song sparrow, Melospiza melodia (Aves) and genotyping errors associated with good quality DNA. Mol Ecol Notes 1:11–13

    Article  Google Scholar 

  • Jenkins KD, Cristol DA (2002) Evidence of differential migration by sex in white-throated sparrows (Zonotrichia albicollis). Auk 119:539–543

    Article  Google Scholar 

  • Ketterson ED, Nolan V Jr (1976) Geographic variation and its climatic correlates in the sex ratio of eastern-wintering dark-eyed juncos (Junco hyemalis hyemalis). Ecology 57:679–693

    Article  Google Scholar 

  • Lessells CM, Boag PT (1987) Unrepeatable repeatabilities—a common mistake. Auk 104:116–121

    Article  Google Scholar 

  • Martin TE, Møller AP, Merino S, Clobert J (2001) Does clutch size evolve in response to parasites and immunocompetence? P Natl Acad Sci USA 98:2071–2076

    Article  CAS  Google Scholar 

  • Møller AP, Erritzøe J (1998) Host immune defence and migration in birds. Evol Ecol 12:945–953

    Article  Google Scholar 

  • Møller AP, Erritzøe J (2001) Dispersal, vaccination and regression of immune defence organs. Ecol Lett 4:484–490

    Article  Google Scholar 

  • Møller AP, Martin-Vivaldi M, Soler J (2004) Parasitism, host immune defence and dispersal. J Evol Biol 17:603–612

    Article  PubMed  Google Scholar 

  • Møller AP, Szép T (2011) The role of parasites in ecology and evolution of migration and migratory connectivity. J Ornithol 152:141–150

    Article  Google Scholar 

  • Morton ML (1992) Effects of sex and birth date on premigration biology, migration schedules, return rates and natal dispersal in the mountain white-crowned sparrow. Condor 94:117–133

    Article  Google Scholar 

  • Nebel S, Buehler DM, MacMillan A, Guglielmo CG (2013) Flight performance of western sandpipers, Calidris mauri, remains uncompromised when mounting an acute phase immune response. J Exp Biol 216:2752–2759

    Article  PubMed  Google Scholar 

  • Newton I (2008) The migration ecology of birds. Academic Press, London

    Google Scholar 

  • Nieuwenhuis R, te Grotenhuis M, Pelzer B (2012) Influence.ME: tools for detecting influential data in mixed effect models. R Journal 4:38–47

    Google Scholar 

  • Pagenkopp KM, Klicka J, Durrant KL, Garvin JC, Fleischer RC (2008) Geographic variation in malarial parasite lineages in the common yellowthroat (Geothlypis trichas). Conserv Genet 9:1577–1588

    Article  Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Potvin DA, Crawford PW, MacDougall-Shackleton SA, MacDougall-Shackleton EA (2015) Song repertoire size, not territory location, predicts reproductive success and territory tenure in a migratory songbird. Can J Zool 93:627–633

    Article  Google Scholar 

  • Price PW, Westoby M, Rice B (1988) Parasite-mediated competition—some predictions and tests. Am Nat 131:544–555

    Article  Google Scholar 

  • Saino N, Romano M, Scandolara C, Rubolini D, Ambrosini R, Caprioli M, Costanzo A, Romano A (2014) Brownish, small and lousy barn swallows have greater natal dispersal propensity. Anim Behav 87:137–146

    Article  Google Scholar 

  • Salkeld DJ, Trivedi M, Schwarzkopf L (2008) Parasite loads are higher in the tropics: temperate to tropical variation in a single host-parasite system. Ecography 31:538–544

    Article  Google Scholar 

  • Sardell RJ, Keller LF, Arcese P, Bucher T, Reid JM (2010) Comprehensive paternity assignment: genotype, spatial location and social status in song sparrows, Melospiza melodia. Mol Ecol 19:4352–4364

    Article  PubMed  Google Scholar 

  • Scott TR (2004) Our current understanding of humoral immunity of poultry. Poultry Sci 83:575–579

    Article  Google Scholar 

  • Smith JNM, Arcese P, Schluter D (1986) Song sparrows grow and shrink with age. Auk 103:210–212

    Google Scholar 

  • Snoejis T, Van de Casteele T, Adriaensen F, Matthysen E, Eens M (2004) A strong association between immune responsiveness and natal dispersal in a songbird. Proc R Soc Lond B 271:S199–S201

    Article  Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton

    Google Scholar 

  • Valkiūnas G, Iezhova TA, Krizanauskiene A, Palinauskas V, Sehgal RN, Bensch S (2008) A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J Parasitol 94:1395–1401

  • Wassenaar LI (2008) An introduction to light stable isotopes for use in terrestrial animal migration studies. In: Hobson KA, Wassenaar LI (eds) Tracking animal migration with stable isotopes. Elsevier, San Diego, pp. 21–44

    Chapter  Google Scholar 

  • Wassenaar LI, Hobson KA (2000) Stable-carbon and hydrogen isotope ratios reveal breeding origins of red-winged blackbirds. Ecol Appl 10:911–916

    Article  Google Scholar 

  • Wassenaar LI, Hobson KA (2003) Comparative equilibrium and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isot Environ Healt S 39:211–217

    Article  CAS  Google Scholar 

  • West BT, Welch KB, Galecki A (2015) Linear mixed models: a practical guide using statistical software, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  • Woodworth BK, Newman AEM, Turbek SP, Dossman BC, Hobson KA, Wassenaar LI, Mitchell GW, Wheelwright NT, Norris DR (2016) Differential migration and the link between winter latitude, timing of migration, and breeding in a songbird. Oecologia 181:413–422

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Queen’s University Biological Station for logistic support and Scott MacDougall-Shackleton plus two anonymous reviewers for helpful comments.

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Correspondence to Elizabeth A. MacDougall-Shackleton.

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This study was funded by the Natural Sciences and Engineering Research Council (NSERC), Canada (grant number 293123-2012RGPIN).

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The authors declare that they have no conflict of interest.

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All applicable international, national and institutional guidelines for the care and use of animals were followed.

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Communicated by W. Wiltschko

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Kelly, T.R., MacGillivray, H.L., Sarquis-Adamson, Y. et al. Seasonal migration distance varies with natal dispersal and predicts parasitic infection in song sparrows. Behav Ecol Sociobiol 70, 1857–1866 (2016). https://doi.org/10.1007/s00265-016-2191-2

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