Skip to main content

Advertisement

Log in

Co-infection with Leucocytozoon and Other Haemosporidian Parasites Increases with Latitude and Altitude in New World Bird Communities

  • Research
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Establishing how environmental gradients and host ecology drive spatial variation in infection rates and diversity of pathogenic organisms is one of the central goals in disease ecology. Here, we identified the predictors of concomitant infection and lineage richness of blood parasites in New Word bird communities. Our multi-level Bayesian models revealed that higher latitudes and elevations played a determinant role in increasing the probability of a bird being co-infected with Leucocytozoon and other haemosporidian parasites. The heterogeneity in both single and co-infection rates was similarly driven by host attributes and temperature, with higher probabilities of infection in heavier migratory host species and at cooler localities. Latitude, elevation, host body mass, migratory behavior, and climate were also predictors of Leucocytozoon lineage richness across the New World avian communities, with decreasing parasite richness at higher elevations, rainy and warmer localities, and in heavier and resident host species. Increased parasite richness was found farther from the equator, confirming a reverse Latitudinal Diversity Gradient pattern for this parasite group. The increased rates of Leucocytozoon co-infection and lineage richness with increased latitude are in opposition with the pervasive assumption that pathogen infection rates and diversity are higher in tropical host communities.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

The bird infection data used in this study are available as Supporting Information Table S1. All parasite sequences are deposited in GenBank, and accession numbers can be found in the Supporting Information Table S1.

Data Accessibility

The raw dataset is available in the Supporting Information. All unpublished DNA sequences will be available in Genbank and MalAvi.

References

  1. Pianka ER (1966) Latitudinal gradients in species diversity: a review of concepts. Am Nat 100:33–46

    Article  Google Scholar 

  2. Hillebrand H (2004) On the generality of the latitudinal diversity gradient. Am Nat 163:192–211. https://doi.org/10.1086/381004

    Article  PubMed  Google Scholar 

  3. Rohde K (1992) Latitudinal gradients in species diversity: the search for the primary cause. Oikos 65:514–527. https://doi.org/10.2307/3545569

    Article  Google Scholar 

  4. Willig MR, Kaufman DM, Stevens RD (2003) Latitudinal gradients in biodiversity: pattern, process, scale, and synthesis. Annu Rev Ecol Evol Syst 34:273–309. https://doi.org/10.1146/annurev.ecolsys.34.012103.144032

    Article  Google Scholar 

  5. Guernier V, Hochberg ME, Guégan J-F (2004) Ecology drives the worldwide distribution of human diseases. PLoS Biol 2:e141. https://doi.org/10.1371/journal.pbio.0020141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993. https://doi.org/10.1038/nature06536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Allen T, Murray KA, Zambrana-Torrelio C, Morse SS, Rondinini C, Di Marco M, Breit N, Olival KJ, Daszak P (2017) Global hotspots and correlates of emerging zoonotic diseases. Nat Commun 8:1124. https://doi.org/10.1038/s41467-017-00923-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Krasnov BR, Shenbroy GI, Khokhlova IS, Degen AA (2004) Flea species richness and parameters of host body, host geography and host ‘milieu.’ J Anim Ecol 73:1121–1128. https://doi.org/10.1111/j.0021-8790.2004.00883.x

    Article  Google Scholar 

  9. Fecchio et al (2020) An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds. J Anim Ecol 89:423–435. https://doi.org/10.1111/1365-2656.13117

    Article  PubMed  Google Scholar 

  10. Matthews KR (2011) Controlling and coordinating development in vector-transmitted parasites. Science 331:1149–1153. https://doi.org/10.1126/science.1198077

    Article  CAS  PubMed  Google Scholar 

  11. Hoarau AOG, Mavingui P, Lebarbenchon C (2020) Coinfections in wildlife: focus on a neglected aspect of infectious disease epidemiology. PLoS Pathog 16(9):e1008790. https://doi.org/10.1371/journal.ppat.1008790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kotepui KU, Masangkay FR, De Jesus Milanez G, Kotepui M (2021) Prevalence and outcomes of malaria as co-infection among patients with human African trypanosomiasis: a systematic review and meta-analysis. Sci Rep 11:23777. https://doi.org/10.1038/s41598-021-03295-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Lafferty KD (2009) The ecology of climate change and infectious diseases. Ecology 90:888–900. https://doi.org/10.1890/08-0079.1

    Article  PubMed  Google Scholar 

  14. Chapa-Vargas L, Matta NE, Merino S (2020) Effects of ecological gradients on tropical avian hemoparasites. In: Santiago-Alarcon D, Marzal A (eds) Avian malaria and related parasites in the tropics, 1st edn. Springer, Cham, pp 349–377

    Chapter  Google Scholar 

  15. Mordecai EA, Ryan SJ, Caldwell JM, Shah MM, LaBeaud AD (2020) Climate change could shift disease burden from malaria to arboviruses in Africa. Lancet Planet Health 4:e416–e423. https://doi.org/10.1016/S2542-5196(20)30178-9

    Article  PubMed  PubMed Central  Google Scholar 

  16. Oakgrove KS, Harrigan RJ, Loiseau C, Guers S, Seppi B, Sehgal RNM (2014) Distribution, diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations. Int J Parasitol 44:717–727. https://doi.org/10.1016/j.ijpara.2014.04.011

    Article  PubMed  Google Scholar 

  17. de Angeli DD, Fecchio A, Braga ÉM, Poulin R (2021) Migratory birds have higher prevalence and richness of avian haemosporidian parasites than residents. Int J Parasitol 51:877–882. https://doi.org/10.1016/j.ijpara.2021.03.001

    Article  Google Scholar 

  18. McNew et al (2021) Contrasting drivers of diversity in hosts and parasites across the tropical Andes. Proc Natl Acad Sci U S A 118:e2010714118. https://doi.org/10.1073/pnas.2010714118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Pigeault R, Chevalier M, Cozzarolo CS, Baur M, Arlettaz M, Cibois A, Keiser A, Guisan A, Christe P, Glaizot O (2022) Determinants of haemosporidian single- and co-infection risks in western palearctic birds. Int J Parasitol 52:617–627. https://doi.org/10.1016/j.ijpara.2022.05.002

    Article  CAS  PubMed  Google Scholar 

  20. Kamiya T, O’Dwyer K, Nakagawa S, Poulin P (2014) What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biol Rev 89:123–134. https://doi.org/10.1111/brv.12046

    Article  PubMed  Google Scholar 

  21. Fecchio et al (2021) Global drivers of avian haemosporidian infections vary across zoogeographical regions. Glob Ecol Biogeogr 30:2393–2406. https://doi.org/10.1111/geb.13390

    Article  Google Scholar 

  22. Galen SC, Borner J, Martinsen ES, Schaer J, Austin CC, West CJ, Perkins SL (2018) The polyphyly of Plasmodium: comprehensive phylogenetic analyses of the malaria parasites (order Haemosporida) reveal widespread taxonomic conflict. R Soc Open Sci 5:171780. https://doi.org/10.1098/rsos.171780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Bell AS, De Roode JC, Sim D, Read AF (2006) Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60:1358–1371. https://doi.org/10.1111/j.0014-3820.2006.tb01215.x

    Article  PubMed  Google Scholar 

  24. Galen SC, Speer KA, Perkins SL (2019) Evolutionary lability of host associations promotes phylogenetic overdispersion of co-infecting blood parasites. J Anim Ecol 88:1936–1949. https://doi.org/10.1111/1365-2656.13089

    Article  PubMed  Google Scholar 

  25. Starkloff N, Galen S (2023) Coinfection rates of avian blood parasites increase with latitude in parapatric host species. Parasitology 150:329–336. https://doi.org/10.1017/S0031182022001792

    Article  PubMed Central  Google Scholar 

  26. Merino et al (2008) Haematozoa in forest birds from southern Chile: latitudinal gradients in prevalence and parasite lineage richness. Austral Ecol 33:329–340. https://doi.org/10.1111/j.1442-9993.2008.01820.x

    Article  Google Scholar 

  27. Ruhs EC, Martin LB, Downs CJ (2020) The impacts of body mass on immune cell concentrations in birds. Proc R Soc B: Biol Sci 287:20200655. https://doi.org/10.1098/rspb.2020.0655

    Article  CAS  Google Scholar 

  28. Minias P (2019) Evolution of heterophil/lymphocyte ratios in response to ecological and life-history traits: a comparative analysis across the avian tree of life. J Anim Ecol 88:554–565. https://doi.org/10.1111/1365-2656.12941

    Article  PubMed  Google Scholar 

  29. Barrow LN, McNew SM, Mitchell N, Galen SC, Lutz HL, Skeen H, Valqui T, Weckstein JD, Witt CC (2019) Deeply conserved susceptibility in a multi-host, multi-parasite system. Ecol Lett 22:987–998. https://doi.org/10.1111/ele.13263

    Article  PubMed  Google Scholar 

  30. Fecchio et al (2019) Avian host composition, local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds. Mol Ecol 28:2681–2693. https://doi.org/10.1111/mec.15094

    Article  PubMed  Google Scholar 

  31. Fecchio et al (2022) Beta diversity, prevalence, and specificity of avian haemosporidian parasites throughout the annual cycle of Chilean Elaenia (Elaenia chilensis), a Neotropical austral migrant. Parasitology 149:1760–1768. https://doi.org/10.1017/S0031182022001317

    Article  PubMed  Google Scholar 

  32. 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. https://doi.org/10.1645/GE-184R1

    Article  CAS  PubMed  Google Scholar 

  33. Bell JA, Weckstein JD, Fecchio A, Tkach VV (2015) A new real-time PCR protocol for detection of avian haemosporidians. Parasit Vectors 8:383. https://doi.org/10.1186/s13071-015-0993-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Harrigan RJ, Sedano R, Chasar JA, Nguyen JT, Whitaker A, Smith TB (2014) New host and lineage diversity of avian haemosporidians in the northern Andes. Evol Appl 7:799–811. https://doi.org/10.1111/eva.12176

    Article  PubMed  PubMed Central  Google Scholar 

  37. Bensch S, Pérez-Tris J, Waldenström J, Hellgren O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58:1617–1621. https://doi.org/10.1554/04-026

    Article  CAS  PubMed  Google Scholar 

  38. Bensch S, Hellgren O, Pérez-Tris J (2009) MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Resour 9:1353–1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x

    Article  PubMed  Google Scholar 

  39. Fick SE, Hijmans RJ (2017) WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 37:4302–4315. https://doi.org/10.1002/joc.5086

    Article  Google Scholar 

  40. De La Torre GM, Campião KM (2021) Bird habitat preferences drive hemoparasite infection in the Neotropical region. Integr Zool 16:755–768. https://doi.org/10.1111/1749-4877.12515

    Article  CAS  PubMed  Google Scholar 

  41. Tobias et al (2022) AVONET: morphological, ecological and geographical data for all birds. Ecol Lett 25:581–597. https://doi.org/10.1111/ele.13898

    Article  PubMed  Google Scholar 

  42. R Core Team (2017) A language and environment for statistical computing. R Foundation for Statistical Computing

  43. Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO (2012) The global diversity of birds in space and time. Nature 491:444–448. https://doi.org/10.1038/nature11631

    Article  CAS  Google Scholar 

  44. Bürkner PC (2017) brms: an R package for Bayesian multilevel models using Stan. J Stat Softw 80: 27239. https://doi.org/10.18637/jss.v080.i01

  45. Svensson E, RÅberg L, Koch C, Hasselquist D (1998) Energetic stress, immunosuppression and the costs of an antibody response. Funct Ecol 12:912–919. https://doi.org/10.1046/j.1365-2435.1998.00271.x

    Article  Google Scholar 

  46. González AD, Matta NE, Ellis VA, Miller ET, Ricklefs RE, Gutiérrez HR (2014) Mixed species flock, nest height, and elevation partially explain avian haemoparasite prevalence in Colombia. PLoS ONE 9:e100695. https://doi.org/10.1371/journal.pone.0100695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Lotta IA, Pacheco MA, Escalante AA, González AD, Mantilla JS, Moncada LI, Adler PH, Matta NE (2016) Leucocytozoon diversity and possible vectors in the Neotropical highlands of Colombia. Protist 167:185–204. https://doi.org/10.1016/j.protis.2016.02.002

    Article  Google Scholar 

  48. McCreadie JW, Adler PH, Hamada N (2005) Patterns of species richness for blackflies (Diptera: Simuliidae) in the Nearctic and Neotropical regions. Ecol Entomol 30:201–209. https://doi.org/10.1111/j.0307-6946.2005.00681.x

    Article  Google Scholar 

  49. Ramiro RS, Pollitt LC, Mideo N, Reece SE (2016) Facilitation through altered resource availability in a mixed-species rodent malaria infection. Ecol Lett 19:1041–1050. https://doi.org/10.1111/ele.12639

    Article  PubMed  PubMed Central  Google Scholar 

  50. Mcqueen PG, Mckenzie FE (2006) Competition for red blood cells can enhance Plasmodium vivax parasitemia in mixed-species malaria infections. Am J Trop Med Hyg 75:112–125

    Article  PubMed  Google Scholar 

  51. Chakarov N, Veiga J, Ruiz-Arrondo I, Valera F (2021) Atypical behavior of a black fly species connects cavity-nesting birds with generalist blood parasites in an arid area of Spain. Parasit Vectors 14:298. https://doi.org/10.1186/s13071-021-04798-z

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank numerous ornithologists and field assistants for their help with sampling birds. We also thank all collaborators who contributed to previously published data as well as the authors that made their data publicly available. We are in debt to the governmental agencies from Brazil and the USA for issuing all permits necessary for collection of new blood samples. Field collection and reagents for molecular analyses were funded in part by National Science Foundation grants DEB-1503804 to JDW.

Author information

Authors and Affiliations

Authors

Contributions

AF and DAD conceived the idea, designed the research, and wrote the manuscript. DAD ran the analyses. EJW, JDW, and JHD generated new data. JAB curated the data. All authors contributed critically to the manuscript drafts and gave final approval for publication.

Corresponding author

Correspondence to Alan Fecchio.

Ethics declarations

Competing interests

The authors declare no competing interests.

Conflict of Interest

The authors declare no competing interests.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 937 KB)

Supplementary file2 (XLSX 17 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fecchio, A., Bell, J.A., Williams, E.J. et al. Co-infection with Leucocytozoon and Other Haemosporidian Parasites Increases with Latitude and Altitude in New World Bird Communities. Microb Ecol 86, 2838–2846 (2023). https://doi.org/10.1007/s00248-023-02283-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-023-02283-x

Keywords

Navigation