Advertisement

Biologia

, Volume 73, Issue 11, pp 1123–1130 | Cite as

Determinants of avian malaria prevalence in mountainous Transcaucasia

  • Hripsime A. Atoyan
  • Mariam Sargsyan
  • Hasmik Gevorgyan
  • Marko Raković
  • Igor Fadeev
  • Vahagn Muradyan
  • Ahmad Daryani
  • Mehdi Sharif
  • Sargis A. AghayanEmail author
Original Article
  • 117 Downloads

Abstract

Deforestation, urban development, and global climate change can lead to dramatic changes of ecological communities and increase prevalence of infectious diseases at higher latitudes and altitudes. Identification of factors responsible for the prevalence of parasites is of crucial importance to understand the dynamics of parasite distribution in a changing environment. Mountain areas are especially suitable for studies of factors governing parasite distribution and prevalence due to heterogeneity of landscapes, climatic regimes, and other biotic and abiotic conditions. We examined 903 avian blood smears collected in mountains of Transcaucasia for prevalence of Haemoproteus and Plasmodium. We found that the haemoparasites prevalence differed among bird species and localities, highlighting the environmental components affecting disease distribution. The prevalence of both Haemoproteus and Plasmodium was significantly higher in males, adults, and migratory species than in females, juveniles, and resident species. Geographic Information System (GIS) and linear regression analyses revealed that elevation and monthly average precipitation were strongly correlated with proportion of infected birds with Plasmodium, indicating that the prevalence increased with increase of monthly average temperature and elevation. Birds from forested and high grassed areas were also more infected with avian haemosporidia. Our study provides baseline data for modelling of parasites distribution under global climate change scenarios, which is of great importance for monitoring and management of communities and environment for conservation and human health.

Keywords

Avian malaria Haemoproteus Plasmodium Prevalence determinants Biotic and abiotic factors 

Notes

Acknowledgments

This work was made possible by a research grant from the Armenian National Science and Education Fund (ANSEF) based in New York, USA (grant number: zoo- 2983). We would like to thank Sergei V. Drovetski from Laboratories for Analytical Biology, National Museum of Natural History, Smithsonian Institution, Washington DC, USA for valuable contribution during field work and manuscript preparation. Fieldwork in Armenia for Marko Raković was supported by Natural History Museum of Belgrade grant “Ptice zapadnog palearktika”.

Compliance with ethical standards

Ethical statement

All biomaterials (birds blood smears collected in 2013 and 2014) used in the study were collected under the permission from the Ministry of Nature Protection of Republic of Armenia given to the Scientific Center of Zoology and Hydroecology, Yerevan, Armenia.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11756_2018_128_MOESM1_ESM.xlsx (72 kb)
ESM 1 (XLSX 72 kb)

References

  1. Abella-Medrano CA, Ibáñez-Bernal S, Carbó-Ramírez P, Santiago-Alarcon D (2018) Blood-meal preferences and avian malaria detection in mosquitoes (Diptera : Culicidae) captured at different land use types within a neotropical montane cloud forest matrix. Parasitol Int 67:313–320.  https://doi.org/10.1016/j.parint.2018.01.006 CrossRefGoogle Scholar
  2. Aghayan SA (2012) Migratory birds as a tool to colonize new territories for avian haemosporidians. J Nat Sci 1:20–24Google Scholar
  3. Aghayan SA, Hovhannisyan TS, Ghasabyan MG, Drovetski SV (2013) Preliminary report on avian malaria infection in breeding colony of lesser kestrel in Armenia. Raptors Conserv 26:96–99Google Scholar
  4. Altizer S, Ostfeld RS, Johnson PTJ, Kutz S, Harvell CD (2013) Climate change and infectious diseases: from evidence to a predictive framework. Science 341:514–519.  https://doi.org/10.1126/science.1239401 CrossRefPubMedGoogle Scholar
  5. Álvarez-Ruiz L, Megía-Palma R, Reguera S, Ruiz S, Zamora-Camacho FJ, Figuerola J, Moreno-Rueda G (2018) Opposed elevational variation in prevalence and intensity of endoparasites and their vectors in a lizard. Curr Zool 64:197–204.  https://doi.org/10.1093/cz/zoy002 CrossRefGoogle Scholar
  6. Annetti KL, Rivera NA, Andrews JE, Mateus-Pinilla N (2017) Survey of Haemosporidian parasites in resident and migrant game birds of Illinois. J Fish Wildl Manag 8:661–668.  https://doi.org/10.3996/082016-JFWM-059 CrossRefGoogle Scholar
  7. Asghar M, Hasselquist D, Hansson B, Zehtindjiev P, Westerdahl H, Bensch S (2015) Hidden costs of infection: chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347:436–438.  https://doi.org/10.1126/science.1261121 CrossRefPubMedGoogle Scholar
  8. Atkinson CT, Dusek RJ, Woods KL, Iko WM (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii amakihi. J Wildl Dis 36:197–201.  https://doi.org/10.7589/0090-3558-36.2.197 CrossRefPubMedGoogle Scholar
  9. Atkinson CT, Utzurrum RB, Lapointe DA, Camp RJ, Crampton LH, Foster JT, Giambelluca TW (2014) Changing climate and the altitudinal range of avian malaria in the Hawaiian islands - an ongoing conservation crisis on the island of Kaua’i. Glob Chang Biol 20:2426–2436.  https://doi.org/10.1111/gcb.12535 CrossRefPubMedGoogle Scholar
  10. Baker JR (1975) Epizootiology of some haematozoic protozoa of English birds. J Nat Hist 9:601–609.  https://doi.org/10.1080/00222937500770491 CrossRefGoogle Scholar
  11. Bennett GF, Witt H, White EM (1980) Blood parasites in some Jamaican birds. J Wildl Dis 16:29–38.  https://doi.org/10.7589/0090-3558-16.1.29 CrossRefPubMedGoogle Scholar
  12. Benning TL, LaPointe D, Atkinson CT, Vitousek PM (2002) Interactions of climate change with biological invasions and land use in the Hawaiian islands: modeling the fate of endemic birds using a geographic information system. Proc Natl Acad Sci 99:14246–14249.  https://doi.org/10.1073/pnas.162372399 CrossRefPubMedGoogle Scholar
  13. Bensch S, Waldenström J, Jonzen N, Westerdahl H, Hansson B, Sejberg D, Hasselquist D (2007) Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol 76:112–122.  https://doi.org/10.1111/j.1365-2656.2006.01176.x CrossRefPubMedGoogle Scholar
  14. Calero-Riestra M, García JT (2016) Sex-dependent differences in avian malaria prevalence and consequences of infections on nestling growth and adult condition in the tawny pipit, Anthus campestris. Malar J 15:178.  https://doi.org/10.1186/s12936-016-1220-y
  15. Chaves LF, Hamer GL, Walker ED, Brown WM, Ruiz MO, Kitron UD (2011) Climatic variability and landscape heterogeneity impact urban mosquito diversity and vector abundance and infection. Ecosphere 2:art70.  https://doi.org/10.1890/ES11-00088.1 CrossRefGoogle Scholar
  16. Cornuault J, Khimoun A, Harrigan RJ, Bourgeois YXC, Milá B, Thébaud C, Heeb P (2013) The role of ecology in the geographical separation of blood parasites infecting an insular bird. J Biogeogr 40:1313–1323.  https://doi.org/10.1111/jbi.12098 CrossRefGoogle Scholar
  17. da Amaral HLC, Bergmann FB, dos Santos PRS, Silveira T, Krüger RF (2017) How do seasonality and host traits influence the distribution patterns of parasites on juveniles and adults of Columba livia? Acta Trop 176:305–310.  https://doi.org/10.1016/j.actatropica.2017.08.023 CrossRefGoogle Scholar
  18. Dawson RD, Bortolotti GR (1999) Prevalence and intensity of hematozoan infections in a population of American kestrels. Can J Zool 77:162–170.  https://doi.org/10.1139/z98-206 CrossRefGoogle Scholar
  19. DeGroote LW, Rodewald PG (2010) Blood parasites in migrating wood-warblers (Parulidae): effects on refueling, energetic condition, and migration timing. J Avian Biol 41:147–153.  https://doi.org/10.1111/j.1600-048X.2009.04782.x CrossRefGoogle Scholar
  20. Dimitrov D, Palinauskas V, Iezhova TA, Bernotienė R, Ilgūnas M, Bukauskaitė D, Zehtindjiev P, Ilieva M, Shapoval AP, Bolshakov CV, Markovets MY, Bensch S, Valkiūnas G (2015) Plasmodium spp: an experimental study on vertebrate host susceptibility to avian malaria. Exp Parasitol 148:1–16.  https://doi.org/10.1016/J.EXPPARA.2014.11.005 CrossRefGoogle Scholar
  21. Drovetski SV, Aghayan SA, Mata VA, Lopes RJ, Mode NA, Harvey JA, Voelker G (2014) Does the niche breadth or trade-off hypothesis explain the abundance-occupancy relationship in avian Haemosporidia? Mol Ecol 23:3322–3329.  https://doi.org/10.1111/mec.12744 CrossRefPubMedGoogle Scholar
  22. Dunn JC, Cole EF, Quinn JL (2011) Personality and parasites: sex-dependent associations between avian malaria infection and multiple behavioural traits. Behav Ecol Sociobiol 65:1459–1471.  https://doi.org/10.1007/s00265-011-1156-8 CrossRefGoogle Scholar
  23. Ehrmann S, Liira J, Gärtner S, Hansen K, Brunet J, Cousins SAO, Deconchat M, Decocq G, De Frenne P, De Smedt P, Diekmann M, Gallet-Moron E, Kolb A, Lenoir J, Lindgren J, Naaf T, Paal T, Valdés A, Verheyen K, Wulf M, Scherer-Lorenzen M (2017) Environmental drivers of Ixodes ricinus abundance in forest fragments of rural European landscapes. BMC Ecol 17:31.  https://doi.org/10.1186/s12898-017-0141-0
  24. Ellis VA, Medeiros MCI, Collins MD, Sari EHR, Coffey ED, Dickerson RC, Lugarini C, Stratford JA, Henry DR, Merrill L, Matthews AE, Hanson AA, Roberts JR, Joyce M, Kunkel MR, Ricklefs RE (2017) Prevalence of avian haemosporidian parasites is positively related to the abundance of host species at multiple sites within a region. Parasitol Res 116:73–80.  https://doi.org/10.1007/s00436-016-5263-3 CrossRefPubMedGoogle Scholar
  25. Fallon SM, Bermingham E, Ricklefs RE (2005) Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. Am Nat 165:466–480.  https://doi.org/10.1086/428430 CrossRefPubMedGoogle Scholar
  26. Freed L, Cann R (2013) Vector movement underlies avian malaria at upper elevation in Hawaii: implications for transmission of human malaria. Parasitol Res 112:3887–3895.  https://doi.org/10.1007/s00436-013-3578-x CrossRefPubMedGoogle Scholar
  27. Freeman-Gallant CR, Taff CC (2017) Age-specific patterns of infection with haemosporidians and trypanosomes in a warbler: implications for sexual selection. Oecologia 184:813–823.  https://doi.org/10.1007/s00442-017-3919-z CrossRefPubMedGoogle Scholar
  28. Fuller T, Bensch S, Müller I, Novembre J, Pérez-Tris J, Ricklefs RE, Smith TB, Waldenström J (2012) The ecology of emerging infectious diseases in migratory birds: an assessment of the role of climate change and priorities for future research. Ecohealth 9:80–88.  https://doi.org/10.1007/s10393-012-0750-1 CrossRefPubMedGoogle Scholar
  29. Garamszegi LZ (2011) Climate change increases the risk of malaria in birds. Glob Chang Biol 17:1751–1759.  https://doi.org/10.1111/j.1365-2486.2010.02346.x CrossRefGoogle Scholar
  30. Garrett KA, Dobson ADM, Kroschel J, Natarajan B, Orlandini S, Tonnang HEZ, Valdivia C (2013) The effects of climate variability and the color of weather time series on agricultural diseases and pests, and on decisions for their management. Agric For Meteorol 170:216–227.  https://doi.org/10.1016/j.agrformet.2012.04.018 CrossRefGoogle Scholar
  31. Gonzalez-Quevedo C, Davies RG, Richardson DS (2014) Predictors of malaria infection in a wild bird population: landscape-level analyses reveal climatic and anthropogenic factors. J Anim Ecol 83:1091–1102.  https://doi.org/10.1111/1365-2656.12214 CrossRefPubMedGoogle Scholar
  32. Granthon C, Williams DA (2017) Avian malaria, body condition, and blood parameters in four species of songbirds. Wilson J Ornithol 129:492–508.  https://doi.org/10.1676/16-060.1 CrossRefGoogle Scholar
  33. Illera JC, López G, García-Padilla L, Moreno Á (2017) Factors governing the prevalence and richness of avian haemosporidian communities within and between temperate mountains. PLoS One 12:e0184587.  https://doi.org/10.1371/journal.pone.0184587 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Isaksson C, Sepil I, Baramidze V, Sheldon BC (2013) Explaining variance of avian malaria infection in the wild: the importance of host density, habitat, individual life-history and oxidative stress. BMC Ecol 13:15.  https://doi.org/10.1186/1472-6785-13-15 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Jarvi SI, Farias MEM, Baker H, Freifeld HB, Baker PE, Van Gelder E, Massey JG & Atkinso CT (2003) Detection of avian malaria (Plasmodium spp) in native land birds of American Samoa. Conserv Genet 4:629–637.  https://doi.org/10.1023/a:1025626529806 CrossRefGoogle Scholar
  36. Jenkins T, Thomas GH, Hellgren O, Owens IPF (2012) Migratory behavior of birds affects their coevolutionary relationship with blood parasites. Evolution 66:740–751.  https://doi.org/10.1111/j.1558-5646.2011.01470.x CrossRefPubMedGoogle Scholar
  37. Karadjian G, Puech M-P, Duval L, Chavatte J-M, Snounou G, Landau I (2013) Haemoproteus syrnii in Strix aluco from France: morphology, stages of sporogony in a hippoboscid fly, molecular characterization and discussion on the identification of Haemoproteus species. Parasite 20:32.  https://doi.org/10.1051/parasite/2013031 CrossRefGoogle Scholar
  38. Kataoka H, Nakano J, Kondo Y, Honda Y, Sakamoto J, Origuchi T, Okita M (2017) The influence of aging on the effectiveness of heat stress in preventing disuse muscle atrophy. Physiol Int 104:316–328.  https://doi.org/10.1556/2060.104.2017.4.1 CrossRefPubMedGoogle Scholar
  39. Kaufman Y, Tanre D (1992) Atmospherically resistant vegetation index (ARVI) for EOS-MODIS. IEEE Trans Geosci Remote Sens 30:261–270.  https://doi.org/10.1109/36.134076 CrossRefGoogle Scholar
  40. Kulma K, Low M, Bensch S, Qvarnström A (2014) Malaria-infected female collared flycatchers (Ficedula albicollis) do not pay the cost of late breeding. PLoS One 9:e85822.  https://doi.org/10.1371/journal.pone.0085822 CrossRefGoogle Scholar
  41. Laurance SGW, Jones D, Westcott D, Mckeown A, Harrington G, Hilbert DW (2013) Habitat fragmentation and ecological traits influence the prevalence of avian blood parasites in a tropical rainforest landscape. PLoS One 8:e76227.  https://doi.org/10.1371/journal.pone.0076227 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Liao W, Atkinson CT, LaPointe DA, Samuel MD (2017) Mitigating future avian malaria threats to Hawaiian forest birds from climate change. PLoS One 12:e0168880.  https://doi.org/10.1371/journal.pone.0168880 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Mangudo C, Aparicio JP, Rossi GC, Gleiser RM (2017) Tree hole mosquito species composition and relative abundances differ between urban and adjacent forest habitats in northwestern Argentina. Bull Entomol Res 108:203–212.  https://doi.org/10.1017/S0007485317000700 CrossRefPubMedGoogle Scholar
  44. Marzal A, Balbontín J, Reviriego M, García-Longoria L, Relinque C, Hermosell IG, Magallanes S, López-Calderón C, de Lope F, Møller AP (2016) A longitudinal study of age-related changes in Haemoproteus infection in a passerine bird. Oikos 125:1092–1099.  https://doi.org/10.1111/oik.02778 CrossRefGoogle Scholar
  45. Matthews AE, Ellis VA, Hanson AA, Roberts JR, Ricklefs RE, Collins MD (2016) Avian haemosporidian prevalence and its relationship to host life histories in eastern Tennessee. J Ornithol 157:533–548.  https://doi.org/10.1007/s10336-015-1298-y CrossRefGoogle Scholar
  46. Meléndez L, Laiolo P, Mironov S, García M, Magaña O, Jovani R (2014) Climate-driven variation in the intensity of a host-symbiont animal interaction along a broad elevation gradient. PLoS One 9:e101942.  https://doi.org/10.1371/journal.pone.0101942 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Milich L, Weiss E (2000) GAC NDVI interannual coefficient of variation (CoV) images: ground truth sampling of the Sahel along north-south transects. Int J Remote Sens 21:235–260.  https://doi.org/10.1080/014311600210812 CrossRefGoogle Scholar
  48. Morand S, Krasnov B, Poulin R (2006) Micromammals and macroparasites. Springer-Verlag, Tokyo.  https://doi.org/10.1007/978-4-431-36025-4 CrossRefGoogle Scholar
  49. Muradyan VS, Asmaryan SG, Saghatelyan AK (2016) Assessment of space and time changes of NDVI (biomass) in Armenia’s mountain ecosystems using remote sensing data. Curr Probl Remote Sens Earth from Sp 13:49–60.  https://doi.org/10.21046/2070-7401-2016-13-1-49-60 CrossRefGoogle Scholar
  50. Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB (2010) Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci U S A 107:15135–15139.  https://doi.org/10.1073/pnas.1006422107 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Padilla DP, Illera JC, Gonzalez-Quevedo C, Villalba M, Richardson DS (2017) Factors affecting the distribution of haemosporidian parasites within an oceanic island. Int J Parasitol 47:225–235.  https://doi.org/10.1016/j.ijpara.2016.11.008 CrossRefPubMedGoogle Scholar
  52. Pérez-Rodríguez A, Fernández-González S, de la Hera I & Pérez-Tris J (2013) Finding the appropriate variables to model the distribution of vector-borne parasites with different environmental preferences: climate is not enough. Glob Chang Biol 19:3245–3253.  https://doi.org/10.1111/gcb.12226
  53. Podmokła E, Dubiec A, Drobniak SM, Sudyka J, Krupski A, Arct A, Gustafsson L, Cichoń M (2017) Effect of haemosporidian infections on host survival and recapture rate in the blue tit. J Avian Biol 48:796–803.  https://doi.org/10.1111/jav.01108 CrossRefGoogle Scholar
  54. Reiter ME, LaPointe DA (2007) Landscape factors influencing the spatial distribution and abundance of mosquito vector Culex quinquefasciatus (Diptera: Culicidae) in a mixed residential-agricultural community in Hawai’i. J Med Entomol 44:861–868.  https://doi.org/10.1093/jmedent/44.5.861 PubMedGoogle Scholar
  55. Ricklefs RE, Fallon SM, Bermingham E (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Syst Biol 53:111–119.  https://doi.org/10.2307/4135399 CrossRefPubMedGoogle Scholar
  56. Rivera J, Barba E, Mestre A, Rueda J, Sasa M, Vera P, Monrós JS (2013) Effects of migratory status and habitat on the prevalence and intensity of infection by haemoparasites in passerines in eastern Spain. Anim Biodivers Conserv 36:113–122Google Scholar
  57. Soares L, Escudero G, Penha VAS, Ricklefs RE (2016) Low prevalence of haemosporidian parasites in shorebirds. Ardea 104:129–141.  https://doi.org/10.5253/arde.v104i2.a8 CrossRefGoogle Scholar
  58. Spurgin LG, Illera JC, Padilla DP, Richardson DS (2012) Biogeographical patterns and co-occurrence of pathogenic infection across island populations of Berthelot’s pipit (Anthus berthelotii). Oecologia 168:691–701.  https://doi.org/10.1007/s00442-011-2149-z CrossRefGoogle Scholar
  59. Svobodová M, Weidinger K, Peške L, Volf P, Votýpka J, Voříšek P (2014) Trypanosomes and haemosporidia in the buzzard (Buteo buteo) and sparrowhawk (Accipiter nisus): factors affecting the prevalence of parasites. Parasitol Res 114:551–560.  https://doi.org/10.1007/s00436-014-4217-x CrossRefGoogle Scholar
  60. Valkiunas G (1997) Bird Haemosporida. Acta Zool Lith 3–5 (Monography)Google Scholar
  61. Valkiūnas G, Iezhova TA, Križanauskienė A, Palinauskas V, Sehgal RNM, Bensch S (2008) A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J Parasitol 94:1395–1401.  https://doi.org/10.1645/GE-1570.1 CrossRefPubMedGoogle Scholar
  62. Videvall E, Cornwallis CK, Palinauskas V, Valkiunas G, Hellgren O (2015) The avian transcriptome response to malaria infection. Mol Biol Evol 32:1255–1267.  https://doi.org/10.1093/molbev/msv016 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Watts DM, Burke DS, Harrison BA, Whitmire RE, Nisalak A (1987) Effect of temperature on the vector efficiency of Aedes aegypti for dengue 2 virus. Am J Trop Med Hyg 36:143–152.  https://doi.org/10.1139/b89-069 CrossRefGoogle Scholar
  64. Zamora-Vilchis I, Williams SE, Johnson CN (2012) Environmental temperature affects prevalence of blood parasites of birds on an elevation gradient: implications for disease in a warming climate. PLoS One 7:e39208.  https://doi.org/10.1371/journal.pone.0039208 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Zhou G, Munga S, Minakawa N, Githeko AK, Yan G (2007) Spatial relationship between adult malaria vector abundance and environmental factors in western Kenya highlands. Am J Trop Med Hyg 77:29–35 Available at: https://earthexplorer.usgs.gov/ CrossRefGoogle Scholar

Copyright information

© Institute of Zoology, Slovak Academy of Sciences 2018

Authors and Affiliations

  1. 1.Faculty of BiologyYerevan State UniversityYerevanArmenia
  2. 2.Scientific Centre of Zoology and Hydroecology, NAS RAYerevanArmenia
  3. 3.Natural History Museum of BelgradeBelgradeSerbia
  4. 4.Department of CollectionsState Darwin MuseumMoscowRussia
  5. 5.Center for Ecological-Noosphere Studies NAS RAYerevanArmenia
  6. 6.Toxoplasmosis Research CenterMazandaran University of Medical SciencesSariIran
  7. 7.School of Medical SciencesIslamic Azad UniversitySariIran

Personalised recommendations