Abstract
Bio-invasions are a major threat to biodiversity and ecosystems globally and may contribute to the proliferation of emerging infectious diseases. We examined the prevalence and phylogenetic diversity of avian haemosporidian parasites infecting the non-native house sparrows (Passer domesticus) and the native southern grey-headed sparrows (Passer diffusus). Blood samples from 104 sparrows (74 house sparrows and 30 southern grey-headed sparrows) mist-netted inside and around the Kruger National Park were used. Genomic DNA was extracted from each blood sample and subjected to nested PCR analyses, Sanger sequencing and phylogenetic analyses. Overall, 35.57% (37/104) of the birds sampled were infected with at least one haemosporidian parasites. Southern grey-headed sparrows had a higher parasite prevalence (60%) than house sparrows (24.3%). A total of 16 parasite lineages were identified, of which eight were novel lineages. Whereas Haemoproteus spp. showed the highest lineage diversity, Leucocytozoon spp. were the most prevalent parasites, albeit with significant differences between sparrow species. A single Plasmodium sp. infection was recorded in a southern grey-headed sparrow. In support of the enemy release hypothesis, we found that prevalence on non-native house sparrows was lower than prevalence recorded in their region of origin and also that they were infected only by indigenous parasites lineages.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data for this study is freely available from the South African Foundational Biodiversity Information Programme (FBIP) repository.
References
Angelier F, Brischoux F (2019) Are house sparrow populations limited by the lack of cavities in urbanized landscapes? an experimental test. J Avian Biol 50:e02009. https://doi.org/10.1111/jav.02009
Antonini Y, Lobato DNC, Norte AC, Ramos JA, Moreira PDA, Braga EM (2019) Patterns of avian malaria in tropical and temperate environments: testing the “the enemy release hypothesis”. Biota Neotrop 19(4):e20180716. https://doi.org/10.1590/1676-0611-bn-2018-0716
Atkinson CT, Samuel CT (2010) Avian malaria Plasmodium relictum in native Hawaiian forest birds: epizootiology and demographic impacts on apapane Himatione sanguinea. J Avian Biol 41:357–366. https://doi.org/10.1111/j.1600-048X.2009.04915.x
Beadell JS, Covas R, Gebhard C, Ishtiaq F, Melo M, Schmidt BK, Perkins SL, Graves GR, Fleischer RC (2009) Host associations and evolutionary relationships of avian blood parasites from West Africa. Int J Parasitol 39:257–266. https://doi.org/10.1016/j.ijpara.2008.06.005
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
Bichet C, Brischoux F, Ribout C, Parenteau C, Meillère A, Angelier F (2020) Physiological and morphological correlates of blood parasite infection in urban and non-urban house sparrow populations. PLoS ONE 15:e0237170. https://doi.org/10.1371/journal.pone.0237170
Cadena-Ortiz H, Mantilla JS, de Aguilar JR, Flores D, Bahamonde D, Matta NE, Bonaccorso E (2019) Avian haemosporidian infections in rufous-collared sparrows in an Andean dry forest: diversity and factors related to prevalence and parasitaemia. Parasitology 146:765–773. https://doi.org/10.1017/S0031182018002081
Ciloglu A, Ellis VA, Bernotienė R, Valkiūnas G, Bensch S (2019) A new one-step multiplex PCR assay for simultaneous detection and identification of avian haemosporidian parasites. Parasitol Res 118:191–201. https://doi.org/10.1007/s00436-018-6153-7
Ciloglu A, Ergen AG, Inci A, Dik B, Duzlu O, Onder Z, Yetismis G, Bensch S, Valkiūnas G, Yildirim A (2020) Prevalence and genetic diversity of avian haemosporidian parasites at an intersection point of bird migration routes: Sultan Marshes National Park. Turkey Acta Tropica 210:105465. https://doi.org/10.1016/j.actatropica.2020.105465
Clark NJ, Olsson-Pons S, Ishtiaq F, Clegg SM (2015) Specialist enemies, generalist weapons and the potential spread of exotic pathogens: malaria parasites in a highly invasive bird. Int J Parasitol 45:891–899. https://doi.org/10.1016/j.ijpara.2015.08.008
Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733. https://doi.org/10.1111/j.1461-0248.2004.00616.x
Dadam D, Robinson RA, Clements A, Peach WJ, Bennett M, Rowcliffe JM, Cunningham AA (2019) Avian malaria-mediated population decline of a widespread iconic bird species. R Soc Open Sci 6:182–197. https://doi.org/10.1098/rsos.182197
Garcia-Longoria L, Marzal A, de Lope F, Garamszegi L (2019) Host-parasite interaction explains variation in the prevalence of avian haemosporidians at the community level. PLoS ONE 14(3):e0205624–e0205624. https://doi.org/10.1371/journal.pone.0205624
Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075. https://doi.org/10.1046/j.1365-294x.1998.00389.x
Grilo ML, Vanstreels RET, Wallace R, García-Párraga D, Braga ÉM, Chitty J, Catão-Dias JL, Madeira de Carvalho LM (2016) Malaria in penguins – current perceptions. Avian Pathol 45:393–407. https://doi.org/10.1080/03079457.2016.1149145
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuc Acids Symp Ser 41:95–98. https://doi.org/10.14601/Phytopathol_Mediterr-14998u1.29
Hanson HE, Mathews NS, Hauber ME, Martin LB (2020) The house sparrow in the service of basic and applied biology. Elife 9:e52803. https://doi.org/10.7554/eLife.52803
Hellgren O, Waldenstrom 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
Hellgren O, Križanauskiene A, Valkiūnas G, Bensch S (2007) Diversity and phylogeny of mitochondrial cytochrome b lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoproteidae). J Parasitol 93:889–896. https://doi.org/10.1645/ge-1051r1.1
Hernandez-Lara C, Gonzalez-Garcia F, Santiago-Alarcon D (2017) Spatial and seasonal variation of avian malaria infections in five different land use types within a Neotropical montane forest matrix. Landsc Urban Plan 157:151–160. https://doi.org/10.1016/j.landurbplan.2016.05.025
Herrera-Dueñas A, Pineda-Pampliega J, Antonio-García MT, Aguirre JI (2017) The influence of urban environments on oxidative stress balance: a case study on the house sparrow in the Iberian Peninsula. Front Ecol Evol 5:1–10. https://doi.org/10.3389/fevo.2017.00106
Hockey P, Dean W, Ryan P (2005) Roberts Birds of Southern Africa, 7th edn. Trustees of the John Voelcker Bird Book Fund, Cape Town
Ishtiaq F, Beadell JS, Warren BH, Fleischer RC (2012) Diversity and distribution of avian haematozoan parasites in the western Indian Ocean region: a molecular survey. Parasitology 139:221–231. https://doi.org/10.1017/S0031182011001831
Ivanova K, Zehtindjiev P, Mariaux J, Dimitrov D, Georgiev BB (2018) Avian haemosporidians from rain forests in Madagascar: molecular and morphological data of the genera Plasmodium, Haemoproteus and Leucocytozoon. Infect Genet Evol 58:115–124. https://doi.org/10.1016/j.meegid.2017.12.017
Jeschke JM, Bacher S, Blackburn TM, Dick JTA, Essl F, Evans T, Gaertner M, Hulme PE, Kühn I, Mrugała A, Pergl J, Pyšek P, Rabitsch W, Ricciardi A, Richardson DM, Sendek A, Vilà M, Winter M, Kumschick S (2014) Defining the impact of non-native species. Conserv Biol 28:1188–1194. https://doi.org/10.1111/cobi.12299
Jia T, Huang X, Valkiūnas G, Yang M, Zheng C, Pu T, Zhang Y, Dong L, Suo X, Zhang C (2018) Malaria parasites and related haemosporidians cause mortality in cranes: a study on the parasites diversity, prevalence and distribution in Beijing Zoo. Malar J 17:234. https://doi.org/10.1186/s12936-018-2385-3
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Levin II, Parker PG (2012) Haemosporidian parasites: impacts on avian hosts. In: Miller RE, Fowler M (eds) Fowler’s zoo and wild animal medicine, 1st edn. Saunders, Saint Louis, pp 356–363
Loiseau C, Iezhova T, Valkiūnas G, Chasar A, Hutchinson A, Buermann W, Smith TB, Sehgal RNM (2010) Spatial variation of haemosporidian parasite infection in African rainforest bird species. J Parasitol 96:21–29. https://doi.org/10.1645/GE-2123.1
Lutz HL, Hochachka WM, Engel JI, Bell JA, Tkach VV, Bates JM, Hackett SJ, Weckstein JD (2015) Parasite prevalence corresponds to host life history in a diverse assemblage of Afrotropical birds and haemosporidian parasites. PLoS ONE 10:e0121254. https://doi.org/10.1371/journal.pone.0121254
Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL (2014) Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol-Par 3:171–177. https://doi.org/10.1016/j.ijppaw.2014.04.002
MacLeod CJ, Paterson AM, Tompkins DM, Duncan RP (2010) Parasites lost – do invaders miss the boat or drown on arrival? Ecol Lett 13:516–527. https://doi.org/10.1111/j.1461-0248.2010.01446.x
Magudu K, Downs CT (2015) The relative abundance of invasive house sparrows (Passer domesticus) in an urban environment in South Africa is determined by land use. Afr J Wildl Res 45:354–359. https://doi.org/10.3957/056.045.0354
Marzal A, Møller AP, Espinoza K, Morales S, Luján-Vega C, Cárdenas-Callirgos JM, Mendo L, Álvarez-Barrientos A, González-Blázquez M, García-Longoria L, de Lope F, Mendoza C, Iannacone J, Magallanes S (2018) Variation in malaria infection and immune defence in invasive and endemic House Sparrows. Anim Conserv 21:505–514. https://doi.org/10.1111/acv.12423
Marzal A, Ricklefs R, Valkiunas G, Albayrak T, Arriero E, Bonneaud C, Czirjak G, Ewen J, Hellgren O, Horakova D, Iezhova T, Jensen H, Krizanauskiene A, Lima M, de Lope F, Magnussen E, Martin L, Moller A, Palinauskas V, Pap P, Perez-Tris J, Sehgal R, Soler M, Szollosi E, Westerdahl H, Zetindjiev P, Bensch S (2011) Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE 6:e21905. https://doi.org/10.1371/journal.pone.0021905
Musa S, Mackenstedt U, Woog F, Dinkel A (2019) Avian malaria on Madagascar: prevalence, biodiversity and specialization of haemosporidian parasites. Int J Parasitol 49(3):199–210. https://doi.org/10.1016/j.ijpara.2018.11.001
Ndlovu M (2018) Birdcall lures improve passerine mist-net captures at a sub-tropical African savanna. PLoS ONE 13:e0199595. https://doi.org/10.1371/journal.pone.0199595
Niebuhr CN, Blasco-Costa I (2016) Improving detection of avian malaria from host blood: a step towards a standardised protocol for diagnostics. Parasitol Res 115(10):3905–3911. https://doi.org/10.1007/s00436-016-5157-4
Niebuhr CN, Poulin R, Tompkins DM (2016) Is avian malaria playing a role in native bird declines in New Zealand? Testing hypotheses along an elevational gradient. PLoS ONE 11:e0165918. https://doi.org/10.1371/journal.pone.0165918
Okanga S, Cumming GS, Hockey PAR, Nupen L, Peters JL (2014) Host specificity and co-speciation in avian haemosporidia in the Western Cape, South Africa. Plos ONE 9:e86382. https://doi.org/10.1371/journal.pone.0086382
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: community ecology package. R package version 2.5–6. https://CRAN.R-project.org/package=vegan. Accessed 7 Oct 2020
Outlaw DC, Harvey JA, Drovetski SV, Voelker G (2016) Diversity and distribution of avian haemosporidians in sub-Saharan Africa: an inter-regional biogeographic overview. Parasitology 144(4):1–9. https://doi.org/10.1017/S0031182016001979
Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390. https://doi.org/10.1016/j.tree.2004.05.002
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/. Accessed 7 Oct 2020
Rojo MÁ, Campos F, Santamaría T, Hernández MÁ (2014) Haemosporidians in Iberian Bluethroats Lusciniasvecica. Ardeola 61:135–143. https://doi.org/10.13157/arla.61.1.2014.135
Santiago-Alarcon D, Carbó-Ramírez P, Macgregor-Fors I, Chávez-Zichinelli CA, Yeh PJ (2020) The prevalence of avian haemosporidian parasites in an invasive bird is lower in urban than in non-urban environments. Ibis 162:201–214. https://doi.org/10.1111/ibi.12699
Schirmel J, Bundschuh M, Entling MH, Kowarik I, Buchholz S (2016) Impacts of invasive plants on resident animals across ecosystems, taxa, and feeding types: a global assessment. Glob Chang Biol 22:594–603. https://doi.org/10.1111/gcb.13093
Sheldon EL, Griffith SC (2017) A high incidence of non-cavity nesting in an introduced population of House Sparrows suggests that the species should not be constrained by cavity-nest site availability. Avian Res 8:29. https://doi.org/10.1186/s40657-017-0087-0
Shochat E, Lerman SB, Anderies JM, Warren PS, Faeth SH, Nilon CH (2010) Invasion, competition, and biodiversity loss in urban ecosystems. Bioscience 60:199–208. https://doi.org/10.1525/bio.2010.60.3.6
Sijbranda DC, Campbell J, Gartrell BD, Howe L (2016) Avian malaria in introduced, native and endemic New Zealand bird species in a mixed ecosystem. New Zeal J Ecol 40:72–79. https://doi.org/10.20417/nzjecol.40.8
Valkiūnas G (2004) Avian malaria parasites and other haemosporidia. CRC Press, Boca Raton
Van Hemert C, Meixell BW, Smith MM, Handel CM (2019) Prevalence and diversity of avian blood parasites in a resident northern passerine. Parasites Vector 12:292. https://doi.org/10.1186/s13071-019-3545-1
van Wilgen NJ, Goodall V, Holness S, Chown SL, McGeoch MA (2016) Rising temperatures and changing rainfall patterns in South Africa’s national parks. Int J Climatol 36:706–721. https://doi.org/10.1002/joc.4377
Videvall E (2019) Genomic advances in avian malaria research. Trends Parasitol 35(3):254–266. https://doi.org/10.1016/j.pt.2018.12.005
Acknowledgements
We are grateful to several students from the Organisation of Tropical Studies (OTS) who assisted in bird captures in the field.
Funding
Funding for this study came from the National Research Foundation (NRF), the Foundational Biodiversity Information Programme (FBIP) and the University of the Free State.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
The study was approved by the South African National Park (Research Permit No. NDLM1262) and the University of the Witwatersrand Animal Ethics Screening Committee (Clearance Certificate No. 2015/02/B). Other ethical clearances were delivered by the University of the Free State to M Ndlovu (UFS-AED2017/0004) and MB Wardjomto (UFS-AED2018/0012). Permission to conduct research in terms of Sect. 20 of the Animal Disease Act 1984 (Act No 35 Of 1984) was obtained from the Department of Agriculture, Forestry and Fisheries of South Africa (Ref number 12/11/1/4). The Bushbuckridge Municipality in Mpumalanga province granted access to sampling sites outside the Park.
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Berit Bangoura.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wardjomto, M.B., Ndlovu, M., Pérez-Rodríguez, A. et al. Avian haemosporidia in native and invasive sparrows at an Afrotropical region. Parasitol Res 120, 2631–2640 (2021). https://doi.org/10.1007/s00436-021-07214-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07214-8