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The effect of the ectoparasite Carnus hemapterus on immune defence, condition, and health of nestling European Bee-eaters

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Abstract

One way that parasites influence host survival and fitness is by competing with their hosts for resources that would otherwise be used for growth and immune system development. Thus resource availability, influenced by environmental conditions, may be particularly important during offspring development. This study examined the influence of a haematophagous ectoparasite Carnus hemapterus (Diptera: Milichiidae) in relation to environmental conditions on the growth, immune response, and health of nestling European Bee-eaters (Merops apiaster). The abundance of this bloodsucking ectoparasite per nest was experimentally manipulated to determine its impact on nestling body condition, immune system function in terms of T-cell-mediated and humoral immune response, and two health parameters, sedimentation rate and haematocrit level. Results indicate a significant negative effect of C. hemapterus intensity on nestling body condition and immune response, and on one blood parameter (haematocrit levels). Nestling body condition, γ-globulin levels, wing web swelling, and haematocrit levels increased when parasites were removed. Although a broad spectrum of fitness indicators seems to be affected, no difference in nestling mortality during the experiment was observed between the two treatment groups. Surprisingly, variations in environmental conditions (weather in particular) that likely affected nestling food availability or thermoregulatory demands had no additional effect on the impact of the parasite infestation.

Zusammenfassung

Die Auswirkungen des Ektoparasiten Carnus hemapterus auf die Immunabwehr, Körperkondition und Gesundheit von Nestlingen des Europäischen Bienenfressers Parasiten können das Überleben und die Fitness ihrer Wirte auf unterschiedliche Weise beeinflussen. Unter anderem konkurrieren sie mit ihrem Wirt um Ressourcen die sonst in z.B. Wachstum oder Entwicklung des Immunsystems investiert werden könnten. Ressourcenverfügbarkeit, oft von Umweltbedingungen beeinflusst, spielt daher bei der Embryonal- und Jugendentwicklung eine wichtige Rolle. In dieser Studie werden die Kosten eines hämatophagen Ektoparasiten Carnus hemapterus (Milichiidae, Diptera) unter unterschiedlichen Umweltbedingungen in Bezug auf Wachstum, Immunantwort und Gesundheit nestjunger Europäischer Bienenfresser (Merops apiaster) untersucht. Dazu wurde die Anzahl dieser blutsaugenden Ektoparasiten nestweise manipuliert (erhöht oder reduziert). Bestimmt wurden die Auswirkungen auf Körperkondition; Immunreaktion (T-Zell und humorale Immunantwort) und zwei potentielle Gesundheitsindikatoren im Blut (Sedimentationsrate und Hämatokrit) von Bienenfressernestlingen. Die Ergebnisse zeigen einen signifikant negativen Effekt von C. hemapterus auf Kondition, Immunantwort und Hämatokrit. Werden Parasiten hingegen aus den Nestern entfernt, erhöhen sich Kondition, γ-Globulin, T-Zell Immunantwort und Hämatokrit. Obwohl eine Reihe von Fitnessindikatoren beeinflusst wurde, gab es während des Experimentes keine Unterschiede in der Mortalität der Nestlinge zwischen den beiden Behandlungsgruppen. Überraschenderweise hatten die unterschiedlichen Umweltbedingungen der beiden Untersuchungsjahre keine zusätzlichen Auswirkungen auf die untersuchten Nestlingsparameter.

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References

  • Appleby BM, Anwar MA, Petty SJ (1999) Short-term and long-term effects of food supply on parasite burdens in Tawny Owls, Strix aluco. Funct Ecol 13:315–321. doi:10.1046/j.1365-2435.1999.00319.x

    Article  Google Scholar 

  • Avilés JM, Pérez-Contreras T, Navarro C, Soler JJ (2009) Male spotless starlings adjust feeding effort based on egg spots revealing ectoparasite load. Anim Behav 78:993–999. doi:10.1016/j.anbehav.2009.07.020

    Article  Google Scholar 

  • Baucom RS, De Roode JC (2011) Ecological immunology and tolerance in plants and animals. Funct Ecol 25:18–28. doi:10.1111/j.1365-2435.2010.01742.x

    Article  Google Scholar 

  • Bize P, Roulin A, Bersier L-F, Pfluger D, Richner H (2003) Parasitism and developmental plasticity in Alpine swift nestlings. J Anim Ecol 72:633–639. doi:10.1046/j.1365-2656.2003.00734.x

    Article  Google Scholar 

  • Bize P, Jeanneret C, Klopfenstein A, Roulin A (2008) What makes a host profitable? Parasites balance host nutritive resources against immunity. Am Natur 171:107–118. doi:10.1086/523943

    Article  PubMed  Google Scholar 

  • Blanco G, Tella JL, Potti J, Baz A (2001) Feather mites on birds: costs of parasitism or conditional outcomes? J Avian Biol 32:271–274. doi:10.1111/j.0908-8857.2001.320310.x

    Article  Google Scholar 

  • Brommer JE, Pitala N, Siitari H, Kluen E, Gustafsson L (2011) Body size and immune defense of nestling blue tits (Cyanistes caeruleus) in response to manipulation of ectoparasites and food supply. Auk 128:556–563. doi:10.1525/auk.2011.10284

    Article  Google Scholar 

  • Brzek P, Konarzewski M (2007) Relationship between avian growth rate and immune response depends on food availability. J Exp Biol 210:2361–2367. doi:10.1242/jeb.003517

    Article  PubMed  Google Scholar 

  • Cam E, Monnat JY, Hines JE (2003) Long-term fitness consequences of early conditions in the Kittiwake. J Anim Ecol 72:411–424. doi:10.1046/j.1365-2656.2003.00708.x

    Article  Google Scholar 

  • Cannings RJ (1986) Infestation of Carnus hemapterus Nietzsch (Diptera: Carnidae) in northern saw-whet owl nest. Murrelet 67:83–84

    Article  Google Scholar 

  • Carpenter FL (1975) Bird haematocrits: effects of high altitude and strength of flight. Comp Biochem Physiol 50A:415–417

    Article  Google Scholar 

  • Christe P, Møller AP, De Lope F (1998) Immunocompetence and nestling survival in the House Martin: the tasty chick hypothesis. Oikos 83:175–179. doi:10.2307/3546559

    Article  CAS  Google Scholar 

  • Christe P, Møller AP, Saino N, De Lope F (2000) Genetic and environmental components of phenotypic variation in immune response and body size of a colonial bird, Delichon urbica (the house martin). Heredity 85:75–83. doi:10.1046/j.1365-2540.2000.00732.x

    Article  PubMed  Google Scholar 

  • Cramp S, Simmons KEL (eds) (1985) Handbook of the birds of Europe, the Middle East and North Africa, IV: terns to woodpeckers. Oxford University Press, Oxford

    Google Scholar 

  • Dawson RD, Bortolotti GR (1997) Variation in hematocrit and total plasma proteins of nestling American kestrels (Falco sparverius) in the wild. Comp Biochem Physiol A 117:383–390. doi:10.1016/S0300-9629(96)00364-7

    Article  Google Scholar 

  • De Lope F, Møller AP, de la Cruz C (1998) Parasitism, immune response and reproductive success in the house martin Delichon urbica. Oecologia 114:188–193. doi:10.1007/s004420000527

    Article  PubMed  Google Scholar 

  • De Neve L, Soler JJ, Ruiz-Rodríguez M, Martín-Gálvez D, Pérez-Contreras T, Soler M (2007) Habitat-specific effects of a food supplementation experiment on immunocompetence in Eurasian Magpie Pica pica nestlings. Ibis 149:763–773. doi:10.1111/j.1474-919X.2007.00708.x

    Article  Google Scholar 

  • Eeva T, Klemola T (2013) Variation in prevalence and intensity of two avian ectoparasites in a polluted area. Parasitology 140:1384–1393. doi:10.1017/S0031182013000796

    Article  PubMed  Google Scholar 

  • Fair J, Whitaker S, Pearson B (2007) Sources of variation in haematocrit in birds. Ibis 149:535–552. doi:10.1111/j.1474-919X.2007.00680.x

    Article  Google Scholar 

  • Fargallo JA, Blanco G, Potti J, Viñuela J (2001) Nestbox provisioning in a rural population of Eurasian Kestrels: breeding performance, nest predation and parasitism. Bird Study 48:236–244. doi:10.1080/00063650109461223

    Article  Google Scholar 

  • Fitze PS, Richner H (2002) Differential effects of a parasite on ornamental structures based on melanins and carotenoids. Behav Ecol 13:401–407. doi:10.1093/beheco/13.3.401

    Article  Google Scholar 

  • Gessaman JA, Johnstone JA, Hoffmann SW (1986) Haematocrit and erythrocyte numbers for Cooper’s and shar-shinned hawks. Condor 98:95–96

    Article  Google Scholar 

  • Glutz von Blotzheim UN, Bauer KM (1980) Handbuch der Vögel Mitteleuropas. Columbiformes - Piciformes, vol 9. Aula-Verlag, Wiesbaden

    Google Scholar 

  • Graham AL, Shuker DM, Pollitt LC, Auld SKLR, Wilson AJ, Little TJ (2011) Fitness consequences of immune responses: strengthening the empirical framework for ecoimmunology. Funct Ecol 25:5–17. doi:10.1111/j.1365-2435.2010.01777

    Article  Google Scholar 

  • Grimaldi D (1997) The bird flies, genus Carnus: species revision, generic relationships, and a fossil Meoneura in amber (Diptera: Carnidae). Am Mus Nov 3190:1–30

    Google Scholar 

  • Guiguen C, Launay H, Beaucournu J (1983) Ectoparasites des oiseaux en Bretagne. 1. Répartition et écologie d´un diptére hematophage nouveau pour la France: Carnus hemapterus Nitzsch (Cyclorapha, Carnidae). Rev Fr Entomol 5:54–62

    Google Scholar 

  • Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvarnström A (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Philos Trans R Soc B 346:323–331. doi:10.1098/rstb.1994.0149

    Article  CAS  Google Scholar 

  • Hanssen SA, Bustnes JB, Schnug L et al (2013) Antiparasite treatments reduce humoral immunity and impact oxidative status in raptor nestlings. Ecol Evol 3:5157–5166. doi:10.1002/ece3.891

    Article  PubMed  PubMed Central  Google Scholar 

  • Harper DGC (1999) Feather mites, pectoral muscle condition, wing length and plumage coloration of passerines. Anim Behav 58:553–562. doi:10.1006/anbe.1999.1154

    Article  CAS  PubMed  Google Scholar 

  • Harrison GJ, Harrison LR (1986) Clinical avian medicine and surgery. WB Saunders, Philadelphia

    Google Scholar 

  • Heddergott M (2003) Parasitierung nestjunger Turmfalken Falco t. tinnunculus durch die Gefiederfliege Carnus hemapterus (Insecta: Milichiidae, Diptera). Vogelwelt 124:201–205

    Google Scholar 

  • Heylen DJA, Matthysen E (2008) Effect of tick parasitism on the health status of a passerine bird. Funct Ecol 22:1099–1107. doi:10.1111/j.1365-2435.2008.01463.x

    Article  Google Scholar 

  • Hoi H, Hoi C, Krištofík J, Darolová A (2002) Reproductive success decreases with colony size in the European bee-eater. Ethol Ecol Evol 14:99–110. doi:10.1080/08927014.2002.9522749

    Article  Google Scholar 

  • Hoi H, Krištofík J, Darolová A, Hoi C (2010) Are parasite intensity and related costs of the milichiid fly Carnus hemapterus related to host sociality? J Ornithol 151:907–913. doi:10.1007/s10336-010-0529-5

    Article  Google Scholar 

  • Hoi H, Krištofík J, Darolová A, Hoi C (2012) Experimental evidence for costs due to chewing lice in the European bee-eater (Merops apiaster). Parasitology 139:53–59. doi:10.1017/S0031182011001727

    Article  CAS  PubMed  Google Scholar 

  • Hornsby MAW, Evan RF, Barber AC (2013) Male European starlings do not use egg spots as a cue to adjust investment in nestlings. Wilson J Ornithol 125:109–115. doi:10.1676/11-167.1

    Article  Google Scholar 

  • Hund AK, Aberle MA, Safran RJ (2015) Parents respond in sex-specific and dynamic ways to nestling ectoparasites. Anim Behav 110:187–196. doi:10.1016/j.anbehav.2015.09.028

    Article  Google Scholar 

  • Johnstone CP, Lill A, Reina RD (2015) Use of erythrocyte indicators of health and condition in vertebrate ecophysiology: a review and appraisal. Biol Rev. doi:10.1111/brv.12219/pdf

    PubMed  Google Scholar 

  • Jones CS, Lessells CM, Krebs JR (1991) Helpers-at-nest in European bee-eaters (Merops apiaster): a genetic analysis. In: Burke T, Dolf G, Jeffreys J, Wolff R (eds) DNA fingerprinting: approaches and applications. Birkhauser, Basel, pp 169–192

    Chapter  Google Scholar 

  • King MO, Owen JP, Schwabl H (2011) Injecting the mite into ecological immunology: measuring the antibody response of house sparrows (Passer domesticus) challenged with hematophagous mites. Auk 128:340–345. doi:10.1525/auk.2011.10253

    Article  Google Scholar 

  • Lacina D (1999) Ectoparasite Carnus hemapterus influences the mass growth rate of nestlings of European kestrel (Falco tinnunculus). Buteo Suppl 1999:29

    Google Scholar 

  • Lehmann T (1993) Ectoparasites: direct impact on host fitness. Parasitol Today 9:8–13

    Article  CAS  PubMed  Google Scholar 

  • Lesko MJ, Smallwood JA (2012) Ectoparasites of American kestrels in northwestern New Jersey and their relationship to nestling growth and survival. J Raptor Res 46:304–313. doi:10.3356/JRR-11-56.1

    Article  Google Scholar 

  • Lessells CM, Avery MI (1989) Hatching asynchrony in European bee-eaters Merops apiaster. J Anim Ecol 58:815–835. doi:10.2307/5126

    Article  Google Scholar 

  • Liker A, Márkus M, Vozár A, Zemankovics E, Rózsa L (2001) Distribution of Carnus hemapterus in a starling colony. Can J Zool 79:574–580. doi:10.1139/cjz-79-4-574

    Article  Google Scholar 

  • Lindström KM, Foufopoulos J, Pärn H, Wikelski M (2004) Immunological investments reflect parasite abundance in island populations of Darwin’s finches. Proc R Soc B 271(1547):1513–1519. doi:10.1098/rspb.2004.2752

    Article  PubMed  PubMed Central  Google Scholar 

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98. doi:10.1034/j.1600-0706.2000.880110.x

    Article  Google Scholar 

  • Lochmiller RI, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503–510. doi:10.2307/4088414

    Article  Google Scholar 

  • Loye JE, Zuk M (eds) (1991) Bird-parasite interactions: ecology, evolution and behaviour. Oxford University Press, Oxford

    Google Scholar 

  • Marshall AG (1981) The ecology of ectoparasite insects. Academic Press, London

    Google Scholar 

  • Martin LB, Han P, Lewittes J, Kuhlman JR, Klasing KC, Wikelski M (2006) Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunological technique. Funct Ecol 20:290–299. doi:10.1111/j.1365-2435.2006.01094.x

    Article  Google Scholar 

  • Martín-Vivaldi M, Ruiz-Rodríguez M, Méndez MJ, Soler J (2006) Relative importance of factors affecting nestling immune response differs between junior and senior nestlings within broods of hoopoes Upupa epops. J Avian Biol 37:467–476. doi:10.1111/j.0908-8857.2006.03660.x

    Article  Google Scholar 

  • Merino S, Møller AP, De Lope F (2000) Seasonal changes in cell-mediated immunocompetence and mass gain in nestling barn swallows: a parasite-mediated effect? Oikos 90:327–332. doi:10.1034/j.1600-0706.2000.900213.x

    Article  Google Scholar 

  • Møller AP (1997) Parasitism and the evolution of host life history. In: Clayton DH, Moore J (eds) Host parasite evolution: General principles and avian models. Oxford University Press, Oxford, pp 105–127

    Google Scholar 

  • Nordberg S (1936) Biologisch-ökologische Untersuchungen über die Vogelnidikolen. Acta Zool Fenn 21:1–168

    Google Scholar 

  • Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26. doi:10.1093/beheco/11.1.19

    Article  Google Scholar 

  • Owen JP, Nelson AC, Clayton DH (2010) Ecological immunology of bird-ectoparasite systems. Trends Parasitol 26:530–539. doi:10.1016/j.pt.2010.06.005

    Article  PubMed  Google Scholar 

  • Richner H, Oppliger A, Christe P (1993) Effect of an ectoparasite on reproduction in great tits. J Anim Ecol 62:703–710. doi:10.2307/5390

    Article  Google Scholar 

  • Ricklefs RE (1965) Brood reduction in the curve-billed thrasher. Condor 67:505–510. doi:10.2307/1365614

    Article  Google Scholar 

  • Roulin A (1998) Cycle de reproduction et abondance du diptère parasite Carnus hemapterus dans les nichées de chouettes effraies Tyto alba. Alauda 66:265–272

    Google Scholar 

  • Roulin A, Riols C, Dijkstra C, Ducrest AL (2001) Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behav Ecol 12:103–110

    Article  Google Scholar 

  • Roulin A, Brinkhof MWG, Bize P, Richner H, Jungi TW, Bavoux C, Boileau N, Burneleau G (2003) Which chick is tasty to parasites? The importance of host immunology vs. parasite life history. J Anim Ecol 72:75–81. doi:10.1046/j.1365-2656.2003.00677.x

    Article  Google Scholar 

  • Roulin A, Christe P, Dijkstra C, Ducrest AL, Jungi T (2007) Origin-related, environmental, sex, and age determinants of immunocompetence, susceptibility to ectoparasites, and disease symptoms in the barn owl. Biol J Linn Soc 90:703–718. doi:10.1111/j.1095-8312.2007.00759.x

    Article  Google Scholar 

  • Roulin A, Gasparini J, Froissart L (2008) Pre-hatching maternal effects and the tasty chick hypothesis. Evol Ecol Res 10:463–473

    Google Scholar 

  • Rynkiewicz EC, Hawlena H, Durden LA, Hastriter MW, Demas GE, Clay K (2013) Associations between innate immune function and ectoparasites in wild rodent hosts. Parasitol Res 12:1763–1770. doi:10.1007/s00436-013-3335-1

    Article  Google Scholar 

  • Saadeh C (1998) The erythrocyte sedimentation rate: old and new clinical applications. South Med J 61:220–225. doi:10.1097/00007611-199803000-00001

    Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321. doi:10.1016/0169-5347(96)10039-2

    Article  CAS  PubMed  Google Scholar 

  • Simon A, Thomas D, Blondel J, Perret P, Lambrechts MM (2004) Physiological ecology of Mediterranean blue tits (Parus caeruleus L.): effects of ectoparasites (Protocalliphora spp.) and food abundance on metabolic capacity of nestlings. Physiol Bioch Zool 77:492–501. doi:10.1086/383512

    Article  Google Scholar 

  • Slagsvold T (1986) Asynchronous versus synchronous hatching in birds: experiments with the pied flycatcher. J Anim Ecol 55:1115–1134. doi:10.2307/4437

    Article  Google Scholar 

  • Slagsvold T, Sandvik J, Rofstad G, Lorentsen O, Husby M (1984) On the adaptive value of intraclutch egg-size variation in birds. Auk 101:685–697

    Article  Google Scholar 

  • Slagsvold T, Amundsen T, Dale S (1994) Selection by sexual conflict for evenly spaced offspring in blue tits. Nature 370:136–138. doi:10.1038/370136a0

    Article  Google Scholar 

  • Soler JJ, Møller AP, Soler M, Martínez JG (1999) Interactions between a brood parasite and its host in relation to parasitism and immune defence. Evol Ecol Res 1:189–210

    Google Scholar 

  • Soler JJ, De Neve L, Pérez-Contreras T, Soler M, Sorci G (2003) Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc B 270(1512):241–248. doi:10.1098/rspb.2002.2217

    Article  PubMed  PubMed Central  Google Scholar 

  • Sumasgutner P, Vasko V, Varjonen R, Korpimäki E (2014) Public information revealed by pellets in nest sites is more important than ecto-parasite avoidance in the settlement decisions of Eurasian kestrels. Behav Ecol Sociobiol 68:2023–2034. doi:10.1007/s00265-014-1808-6

    Article  Google Scholar 

  • Szép T, Møller A (1999) Cost of parasitism and host immune defence in the sand martin Riparia riparia: a role for parent-offspring conflict? Oecologia 119:9–15. doi:10.1007/s004420050755

    Article  PubMed  Google Scholar 

  • Tschirren B, Fitze PS, Richner H (2003) Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. J Anim Ecol 72:839–845. doi:10.1046/j.1365-2656.2003.00755.x

    Article  Google Scholar 

  • Václav R, Calero-Torralbo MA, Valera F (2008) Ectoparasite load is linked to ontogeny and cell-mediated immunity in an avian host system with pronounced hatching asynchrony. Biol J Linn Soc 94:463–473. doi:10.1111/j.1095-8312.2008.00985.x

    Article  Google Scholar 

  • Valera F, Casas-Crivillé A, Hoi H (2003) Interspecific parasite exchange in a mixed colony of birds. J Parasitol 89:245–250. doi:10.1645/0022-3395(2003)089[0245:IPEIAM]2.0.CO;2

  • Valera F, Hoi H, Darolová A, Krištofík J (2004) Size versus health as a cue for host choice: a test of the tasty chick hypothesis. Parasitology 129:59–68. doi:10.1017/S0031182004005232

    Article  CAS  PubMed  Google Scholar 

  • Van de Pol M, Bruinzeel LW, Heg D, Van der Jeugd HP, Verhulst S (2006) A silver spoon for a golden future: long-term effects of natal origin on fitness prospects of oystercatchers (Haematopus ostralegus). J Anim Ecol 5:616–626. doi:10.1111/j.1365-2656.2006.01079.x

    Google Scholar 

  • Walter G, Hudde H (1987) Die Gefiederflkiege Carnus hemapterus (Milichiidae, Diptera), ein Ektoparasit der Nestlinge. J Ornitol 128:251–255

    Article  Google Scholar 

  • Wiebe KL (2009) Nest excavation does not reduce harmful effects of ectoparasitism: an experiment with a woodpecker, the northern flicker Colaptes auratus. J Avian Biol 40:166–172. doi:10.1111/j.1600-048X.2009.04481.x

    Article  Google Scholar 

  • Wingfield JC, Maney DL, Breuner CW, Jacobs JD, Lynn S, Ramenofsky M, Richardson RD (1998) Ecological bases of hormone-behavior interactions: the “emergency life history stage”. Am Zool 38:191–206

    Article  CAS  Google Scholar 

  • Withworth TL (1976) Host and habitat preferences, live history and pathogenicity and population regulation in species of Protocaliphora Hough (Diptera: Caliphoridae). Dissertation, Utah State University

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Acknowledgements

This project was supported by the Scientific Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic and the Slovak Academy of Sciences (VEGA Project Number 2/0137/13). All animal experiments were in accordance with Slovak law and were approved by the Ministry of Environment of the Slovak Republic (permit number 4453/2008-2.1/jam). We thank the two anonymous reviewers whose comments and suggestions helped improve and clarify the manuscript.

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Hoi, H., Darolová, A., Krištofík, J. et al. The effect of the ectoparasite Carnus hemapterus on immune defence, condition, and health of nestling European Bee-eaters. J Ornithol 159, 291–302 (2018). https://doi.org/10.1007/s10336-017-1500-5

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