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Patterns in avian malaria at founder and source populations of an endemic New Zealand passerine

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Abstract

Significant progress in our understanding of disease transmission in the wild can be made by examining variation in host–parasite–vector interactions after founder events of the host. This study is the first to document patterns in avian malaria, Plasmodium spp., infecting an endemic New Zealand passerine, Anthornis melanura, at multiple-host subpopulations simultaneously. We assess the Beaudoin hypothesis of bimodal seasonality and use AIC model selection to determine host factors associated with disease prevalence. We had the rare opportunity to test the enemy release hypothesis (ERH) after a recent colonisation event of the bellbird host. Four Plasmodium species were found to infect bellbirds. Temporal patterns of three exotic parasite lineages, including GRW06 Plasmodium (Huffia) elongatum, SYAT05 Plasmodium (Novyella) vaughani and a Plasmodium (Haemamoeba) relictum, were sporadic with low prevalence year round. The fourth species was an endemic parasite, an unresolved Plasmodium (Novyella) sp. here called ANME01, which exhibited a strong winter peak at the source subpopulations possibly indicating greater immune stressors at the densely populated source site. At the colonies, we observed bimodal seasonality in the prevalence of ANME01 with autumn and spring peaks. These infection peaks were male-biased, and the amplitude of sex bias was more pronounced at the newer colony perhaps due to increased seasonal competition resulting from territory instability. We observed a decrease in parasite species diversity and increase in body condition from source to founder sites, but statistical differences in the direct relationship between body condition and malaria prevalence between source and colony were weak and significant only during winter. Though our data did not strongly support the ERH, we highlight the benefits of ‘conspecific release’ associated with decreased population density and food competition. Our findings contribute to the identification of ecological and environmental drivers of variability in malaria transmission, which is valuable for predicting the consequences of both natural range expansions, as well as host re-introductions resulting from intensive conservation practices.

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References

  • Applegate JE, Beaudoin RL (1970) Mechanism of spring relapse in avian malaria: effect of gonadotropin and corticosterone. J Wildl Dis 6:443–447

    PubMed  CAS  Google Scholar 

  • Atkinson CT, LaPointe DA (2009) Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. J Avian Med Surg 23:53–63

    Article  PubMed  Google Scholar 

  • Atkinson CT, Woods KL, Dusek RJ, Sileo LS, Iko WM (1995) Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitology 111:S59–S69

    Article  PubMed  Google Scholar 

  • Baillie SM, Brunton DH (2011) Diversity, distribution and biogeographical origins of Plasmodium parasites from the New Zealand bellbird (Anthornis melanura). Parasitology 138:1843–1851

    Article  CAS  Google Scholar 

  • Barraclough RK, Cope T, Peirce MA, Brunton DH (2012) First example of a highly prevalent but low-impact malaria in an endemic New Zealand passerine: Plasmodium of Tiritiri Matangi bellbirds (Anthornis melanura). In: Paul E (ed) Emerging avian disease, studies in Avian Biology no. 42. Cooper Ornithological Society. University of California Press, Berkeley and Los Angeles, pp 55–63

    Google Scholar 

  • Bartle JA, Sagar PM (1987) Intraspecific variation in the New Zealand bellbird Anthornis melanura. Notornis 34:253–306

    Google Scholar 

  • Beadell JS, Gering E, Austin J, Dumbacher JP, Peirce MA, Pratt TK, Atkinson CT, Fleischer RC (2004) Prevalence and differential host-specificity of two avian blood parasite genera in the Australo-Papuan region. Mol Ecol 13:3829–3844

    Article  PubMed  Google Scholar 

  • Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, Jhala YV, Peirce MA, Rahmani AR, Fonseca DM, Fleischer RC (2006) Global phylogeographic limits of Hawaii’s avian malaria. Proc Biol Sci 273:2935–2944

    Article  PubMed  Google Scholar 

  • Beaudoin RL, Applegate JE, Davis DE, McLean RG (1971) A model for the ecology of avian malaria. J Wildl Dis 7:5–13

    PubMed  CAS  Google Scholar 

  • Beldomenico PB, Begon M (2010) Disease spread, susceptibility and infection intensity: vicious circles? Trends Ecol Evol 25:21–27

    Article  PubMed  Google Scholar 

  • Brunton DH, Evans BA, Ji WH (2008) Assessing natural dispersal of New Zealand bellbirds using song type and song playbacks. N Z J Ecol 32:147–154

    Google Scholar 

  • Buck CL, O’Reilly KA, Kildaw SD (2007) Interannual variability of Black-legged Kittiwake productivity is reflected in baseline plasma corticosterone. Gen Comp Endocrinol 150:430–436. doi:10.1016/j.ygcen.2006.10.011

    Article  PubMed  CAS  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Evol 2:436–443

    Article  Google Scholar 

  • Castro I, Howe L, Tompkins DM, Barraclough RK, Slaney D (2011) Presence and seasonal prevalence of Plasmodium spp. In a rare endemic New Zealand passerine (tieke or saddleback, Philesturnus carunculatus). J Wildl Dis 47:860–867

    PubMed  Google Scholar 

  • Cometti R (1986) Little Barrier Island: New Zealand’s foremost wildlife sanctuary. Hodder and Stoughton, Aukland

    Google Scholar 

  • Cosgrove CL, Wood MJ, Day KP, Sheldon BC (2008) Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. J Anim Ecol 77:540–548

    Article  PubMed  Google Scholar 

  • Craig JL, Douglas ME (1986) Resource distribution, aggressive asymmetries and variable access to resources in the nectar feeding bellbird. Behav Ecol Sociobiol 18:231–240

    Article  Google Scholar 

  • Craig JL, Stewart AM, Brown JL (1982) Subordinates must wait. J Comp Ethol/Z Tierpsychol 60:275–280

    Article  Google Scholar 

  • Davidar P, Morton ES (2006) Are multiple infections more severe for purple martins (Progne subis) than single infections? Auk 123:141–147

    Article  Google Scholar 

  • Dawson RD, Bortolotti GR (2001) Sex-specific associations between reproductive output and hematozoan parasites of American kestrels. Oecologia 126:193–200. doi:10.1007/s004420000506

    Article  Google Scholar 

  • Derraik JGB (2004) Exotic mosquitoes in New Zealand: a review of species intercepted, their pathways and ports of entry. Aust N Z J Public Health 28:433–444

    PubMed  Google Scholar 

  • Deviche P, Sharp PJ (2001) Reproductive endocrinology of a free-living, opportunistically breeding passerine (white-winged crossbill, Loxia leucoptera). Gen Comp Endocrinol 123:268–279

    Article  PubMed  CAS  Google Scholar 

  • Deviche P, Breuner C, Orchinik M (2001) Testosterone, corticosterone, and photoperiod interact to regulate plasma levels of binding globulin and free steroid hormone in dark-eyed juncos, Junco hyemalis. Gen Comp Endocrinol 122:67–77

    Article  PubMed  CAS  Google Scholar 

  • Duncan RP, Blackburn TM (2004) Extinction and endemism in the New Zealand avifauna. Glob Ecol Biogeogr 13:509–517

    Article  Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London

    Google Scholar 

  • Fallon SM, Ricklefs RE, Latta SC, Bermingham E (2004) Temporal stability of insular avian malarial parasite communities. Proc Biol Sci 271:493–500. doi:10.1098/rspb.2003.2621

    Article  PubMed  CAS  Google Scholar 

  • Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • Frank SA (1996) Models of parasite virulence. Q Rev Biol 71:37–78

    Article  PubMed  CAS  Google Scholar 

  • Freeman S, Jackson WM (1990) Univariate metrics are not adequate to measure avian body size. Auk 107:69–74

    Google Scholar 

  • Garamszegi LZ (2011) Climate change increases the risk of malaria in birds. Glob Chang Biol 17:1751–1759. doi:10.1111/j.1365-2486.2010.02346.x

    Article  Google Scholar 

  • Garvin MC, Schoech SJ (2006) Hormone levels and infection of Haemoproteus danilewskyi in free-ranging blue jays (Cyanocitta cristata). J Parasitol 3:659–662

    Article  Google Scholar 

  • Girardet SAB, Veitch CR, Craig JL (2001) Bird and rat numbers on Little Barrier Island, New Zealand, over the period of cat eradication 1976–80. N Z J Zool 28:13–29

    Article  Google Scholar 

  • Goymann W, Landys MM (2011) Testosterone and year-round territoriality in tropical and non-tropical songbirds. J Avian Biol 42:485–489

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Harding KC, Begon M, Eriksson A, Wennberg B (2012) Increased migration in host–pathogen metapopulations can cause host extinction. J Theor Biol 298:1–7

    Article  PubMed  CAS  Google Scholar 

  • Hasselquist D, Ostman O, Waldenström J, Bensch S (2007) Temporal patterns of occurrence and transmission of the blood parasite Haemoproteus payevskyi in the great reed warbler Acrocephalus arundinaceus. J Ornithol 148:401–409

    Article  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  PubMed  CAS  Google Scholar 

  • Hellgren O, Waldenström J, Perez-Tris J, Szollosi E, Hasselquist D, Križanauskienė A, Ottosson U, Bensch S (2007) Detecting shifts of transmission areas in avian blood parasites—a phylogenetic approach. Mol Ecol 16:1281–1290

    Article  PubMed  Google Scholar 

  • Howe L, Castro I, Schoener ER, Hunter S, Barraclough RK, Alley MR (2012) Malaria parasites (Plasmodium spp.) infecting introduced, native and endemic New Zealand birds. Parasitol Res. doi:10.1007/s00436-01102577-z

  • Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (2002) Ecology of wildlife diseases. Oxford University Press, Oxford

    Google Scholar 

  • Illera JC, Emerson BC, Richardson DS (2008) Genetic characterization, distribution and prevalence of avian pox and avian malaria in the Berthelot’s pipit (Anthus berthelotii) in Macaronesia. Parasitol Res 103:1435–1443. doi:10.1007/s00436-008-1153-7

    Article  PubMed  Google Scholar 

  • Jarvi SI, Schultz JJ, Atkinson CT (2002) PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. J Parasitol 88:153–158

    PubMed  Google Scholar 

  • Jarvi SI, Farias MEM, Baker H, Freifeld HB, Baker PE, Van Gelder E, Massey JG, Atkinson CT (2003) Detection of avian malaria (Plasmodium spp.) in native land birds of American Samoa. Conserv Genet 4:29–637

    Article  Google Scholar 

  • Jennelle CS, Cooch EG, Conroy MJ, Senar JC (2007) State-specific detection probabilities and disease prevalence. Ecol Appl 17:154–167

    Article  PubMed  Google Scholar 

  • Keymer AE, Anderson RM (1979) Dynamics of infection of Tribolium confusum by Hymenolepis diminuta—influence of infective-stage density and spatial-distribution. J Parasitol 79:195–207

    Article  CAS  Google Scholar 

  • Kilpatrick AM (2006) Facilitating the evolution of resistance to avian malaria in Hawaiian birds. Biol Conserv 128:475–485

    Article  Google Scholar 

  • Knowles SCL, Wood MJ, Alves R, Wilkin TA, Bensch S, Sheldon BC (2011) Molecular epidemiology of malaria prevalence and parasitaemia in a wild bird population. Mol Ecol 20:1062–1076

    Article  PubMed  Google Scholar 

  • Lachish S, Knowles SCL, Alves R, Wood MJ, Sheldon BC (2011) Infection dynamics of endemic malaria in a wild bird population: parasite species-dependent drivers of spatial and temporal variation in transmission rates. J Anim Ecol 80:1207–1216. doi:10.1111/j.1365-2656.2011.01893.x

    Article  PubMed  Google Scholar 

  • LaPointe DA, Lee GM, Atkinson CT (2010) Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawai’i. J Parasitol 96:318–324

    Article  PubMed  Google Scholar 

  • Lively CM (2006) The ecology of virulence. Ecol Lett 9:1089–1095. doi:10.1111/j.1461-0248.2006.00969.x

    Article  PubMed  Google Scholar 

  • Lymbery AJ, Thompson RCA (2012) The molecular epidemiology of parasite infections: tools and applications. Mol Biochem Parasitol 181:102–116. doi:10.1016/j.molbiopara.2011.10.006

    Article  PubMed  CAS  Google Scholar 

  • Lynn SE, Breuner CW, Wingfield JC (2001) Short-term fasting in a songbird leads to elevated free corticosterone levels due to decreased corticosterone binding globulin. Am Zool 41:1511–1512

    Google Scholar 

  • MacArthur RH, Wilson EO (1963) An equilibrium theory of island biogeography. Evolution 17:373–387

    Article  Google Scholar 

  • Martinsen ES, Perkins SL, Schall JJ (2008) A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Mol Phylogenet Evol 47:261–273

    Article  PubMed  CAS  Google Scholar 

  • Marzal A, Bensch S, Reviriego M, Balbontin J, De Lope F (2008) Effects of malaria double infection in birds: one plus one is not two. J Evol Biol 21:979–987

    Article  PubMed  CAS  Google Scholar 

  • Marzal A, Ricklefs RE, Valkiūnas G et al (2011) Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS One 6:e21905. doi:10.1371/journal.pone.0021905

    Article  PubMed  CAS  Google Scholar 

  • McCurdy DG, Shutler D, Mullie A, Forbes MR (1998) Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 82:303–312

    Article  CAS  Google Scholar 

  • Merila J, Andersson M (1999) Reproductive effort and success are related to haematozoan infections in blue tits. Ecoscience 6:421–428

    Google Scholar 

  • Michel C, Duclos M, Cabanac M, Richard D (2005) Chronic stress reduces body fat content in both obesity-prone and obesity-resistant strains of mice. Horm Behav 48:172–179. doi:10.1016/j.yhbeh.2005.02.004

    Article  PubMed  CAS  Google Scholar 

  • Miller HC, Lambert DM (2004) Genetic drift outweighs balancing selection in shaping post-bottleneck major histocompatibility complex variation in New Zealand robins (Petroicidae). Mol Ecol 13:3709–3721

    Article  PubMed  CAS  Google Scholar 

  • Norris K, Anwar M, Read AF (1994) Reproductive effort influences the prevalence of haematozoan parasites in great tits. J Anim Ecol 63:601–610

    Article  Google Scholar 

  • Nunn CL, Lindenfors P, Pursall ER, Rolff J (2009) On sexual dimorphism in immune function. Proc Biol Sci 364:61–69

    Google Scholar 

  • Palinauskas V, Valkiūnas G, Bolshakov CV, Bensch S (2008) Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Exp Parasitol 120:372–380

    Article  PubMed  Google Scholar 

  • Perez-Tris J, Hellgren O, Križanauskienė A, Waldenström J, Secondi J, Bonneaud C, Fjeldsa J, Hasselquist D, Bensch S (2007) Within-host speciation of malaria parasites. PLoS One 2:e235. doi:10.1371/journal.pone.0000235

    Article  PubMed  Google Scholar 

  • Phillips BL, Kelehear C, Pizzatto L, Brown GP, Barton D, Shine R (2010) Parasites and pathogens lag behind their host during periods of host range advance. Ecology 91:872–881

    Article  PubMed  Google Scholar 

  • Porter WP, Vakharia N, Klousie WD, Duffy D (2006) Po’ouli landscape bioinformatics models predict energetics, behavior, diets, and distribution on Maui. Integr Comp Biol 46:1143–1158

    Article  PubMed  CAS  Google Scholar 

  • Poulin R (1996) Sexual inequalities in helminth infections: a cost of being a male? Am Nat 147:287–295

    Article  Google Scholar 

  • Reiter P (2001) Climate change and mosquito-borne disease. Environ Health Perspect 109:141–161

    PubMed  Google Scholar 

  • Restif O, Amos W (2010) The evolution of sex-specific immune defences. Proc Biol Sci 277:2247–2255

    Article  PubMed  Google Scholar 

  • Rimmer A (2004) Tiritiri Matangi Island: a model of conservation. Tandem, Auckland

    Google Scholar 

  • Rolff J (2002) Bateman’s principle and immunity. Proc Biol Sci 269:867–872

    Article  PubMed  Google Scholar 

  • Schalk G, Forbes MR (1997) Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78:67–74

    Article  Google Scholar 

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90

    Article  CAS  Google Scholar 

  • Sommer S (2003) Effects of habitat fragmentation and changes of dispersal behavior after a recent population decline on the genetic variability of noncoding and coding DNA of a monogamous Malagasy rodent. Mol Ecol 12:2845–2851

    Article  PubMed  CAS  Google Scholar 

  • Spottiswoode C, Moller AP (2004) Extrapair paternity, migration, and breeding synchrony in birds. Behav Ecol 15:41–57

    Article  Google Scholar 

  • Steadman DW, Greiner EC, Wood CS (1990) Absence of blood parasites in indigenous and introduced birds from the Cook Islands, South-Pacific. Conserv Biol 4:398–404

    Article  Google Scholar 

  • Stjernman M, Raberg L, Nilsson JA (2004) Survival costs of reproduction in the blue tit (Parus caeruleus): a role for blood parasites? Proc Biol Sci 271:2387–2394

    Article  PubMed  Google Scholar 

  • Tompkins DM, Gleeson DM (2006) Relationship between avian malaria distribution and an exotic invasive mosquito in New Zealand. J R Soc N Z 36:51–62

    Article  Google Scholar 

  • Tompkins DM, Dunn AM, Smith MJ, Telfer S (2011) Wildlife diseases: from individuals to ecosystems. J Anim Ecol 80:19–38

    Article  PubMed  Google Scholar 

  • Trivers RL (1972) Mother–offspring conflict. Am Zool 12:648

    Google Scholar 

  • Valkiūnas G (2005) Avian malaria parasites and other Haemosporidia. CRC, Florida

    Google Scholar 

  • Valkiūnas G (2011) Haemosporidian vector research: marriage of molecular and microscopical approaches is essential. Mol Ecol 20:3084–3086

    Article  PubMed  Google Scholar 

  • Valkiūnas G, Zehtindjiev P, Olof H, Ilieva M, Iezhova TA, Bensch S (2007) Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp nov. Parasitol Res 6:1311–1322. doi:10.1007/s00436-006-0409-3

    Article  Google Scholar 

  • Valkiūnas G, Zehtindjiev P, Dimitrov D, Križanauskienė A, Iezhova TA, Bensch S (2008) Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank. Parasitol Res 102:1185–1193

    Article  PubMed  Google Scholar 

  • van Oers K, Richardson DS, Saether SA, Komdeur J (2010) Reduced blood parasite prevalence with age in the Seychelles Warbler: selective mortality or suppression of infection? J Ornithol 151:69–77

    Article  Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The challenge hypothesis—theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846. doi:10.1086/285134

    Article  Google Scholar 

  • Wingfield JC, Bruener C, Jacobs J (1997) Corticosterone and behavioral responses to unpredictable events. In: Harvey S, Etches RJ (eds) Perspectives in avian endocrinology. Society for Endocrinology, Bristol, pp 267–278

    Google Scholar 

  • Wood MJ, Cosgrove CL, Wilkin TA, Knowles SCL, Day KP, Sheldon BC (2007) Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Mol Ecol 16:3263–3273

    Article  PubMed  CAS  Google Scholar 

  • Zehtindjiev P, Križanauskienė A, Scebba S, Dimitrov D, Valkiūnas G, Hegemann A, Tieleman BI, Bensch S (2012) Haemosporidian infections in skylarks (Alauda arvensis): a comparative PCR-based and microscopy study on the parasite diversity and prevalence in southern Italy and the Netherlands. Eur J Wildl Res 58:335–344

    Article  Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1023. doi:10.1016/S0020-7519(96)00086-0

    PubMed  CAS  Google Scholar 

  • Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160:S9–S22. doi:10.1086/342131

    Article  PubMed  Google Scholar 

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Acknowledgements

This study was funded by a Canadian Natural Science and Engineering Research Council (NSERC) PGS scholarship to S.M.B. and the New Zealand Institute of Natural Sciences (INS) Massey University to D.H.B. All blood collection from birds was performed under permit of New Zealand Department of Conservation (DOC), Auckland Regional Council (ARC) and Massey University Animal Ethics Committee (MUAEC). Gracious thanks especially to Jordi Segers, Morag Fordham and Simon Fordham, and also to Barbara Egli, Eva Krause and Birgit Ziesemann who helped capture bellbirds in the Hauraki Gulf. We extend many thanks to Dr. Peter Ritchie (Victoria University of Wellington) for permitting S.M.B. to do the malaria PCR and sequencing in his genetics lab at the School of Biological Sciences, Victoria University of Wellington, Wellington, New Zealand.

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  1. Rosemary K. Barraclough

    Present address: Ecology, Evolution and Behaviour, School of Biological Sciences, University of Auckland, Auckland, New Zealand

  2. Shauna M. Baillie

    Present address: Department of Biology, University of Winnipeg, 515 Portage Avenue, Winnipeg, Manitoba, R3B 2E9, Canada

Authors and Affiliations

  1. Institute of Natural Sciences, Massey University, Private Bag 102-904 North Shore Mail Centre, Auckland, 0745, New Zealand

    Shauna M. Baillie, David Gudex-Cross, Rosemary K. Barraclough & Dianne H. Brunton

  2. Fenner School of Environment and Society, College of Medicine, Biology and Environment, Australia National University, Canberra, ACT, 0200, Australia

    Wade Blanchard

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Baillie, S.M., Gudex-Cross, D., Barraclough, R.K. et al. Patterns in avian malaria at founder and source populations of an endemic New Zealand passerine. Parasitol Res 111, 2077–2089 (2012). https://doi.org/10.1007/s00436-012-3055-y

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