Capturing migratory birds and examining for ticks (Acari: Ixodida)
Year 2021,
, 1 - 8, 27.01.2021
Adem Keskin
,
Kiraz Erciyas Yavuz
,
Arif Cemal Özsemir
,
Kosta Y. Mumcuoğlu
Abstract
Ticks (Acari: Ixodida) are hematophagous ectoparasites of a wide variety of mammals, birds, reptiles, and amphibians, and are the vectors of many pathogenic agents, such as bacteria, protozoa, and viruses. The seasonal movement and migration of birds is one of the main causes of the dispersal of ticks and tick-borne pathogens. Therefore, identification of ticks associated with migratory birds is a fundamental step to understand the ecology of ticks infesting birds and evaluate their potential as vectors of zoonotic diseases. In this article, we provided a brief review for capturing migrating birds and examining them for ticks.
Thanks
We would like to thank Dr. Christos Barboutis (Hellenic Ornithological Society/BirdLife Greece, Antikythira Bird Observatory, Athens, Greece) for his valuable comments on the manuscript. We also thank to Gökhan Eren (Ondokuz Mayıs University, Faculty of Veterinary Medicine) for providing the photos to Figure 3 and 4, and to Ömral Ünsal Özkoç (Ondokuz Mayıs University, Biology Department) for providing the picture for the Figure 2.
References
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- Apanaskevich, D.A. and Horak, I.G. 2008. The genus Hyalomma Koch, 1844: V. re-evaluation of the taxonomic rank of taxa comprising the H. (Euhyalomma) marginatum Koch complex of species (Acari: Ixodidae) with redescription of all parasitic stages and notes on biology. International Journal of Acarology, 34: 13-42.
doi: 10.1080/01647950808683704
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- Arthur, D.R. 1965. Ticks of the genus Ixodes in Africa. The Athlone Press, University of London, London, UK, 348 pp.
- Baillie, S., Bairlein, F., Clark, J., du Feu, C., Fiedler, W., Fransson, T., Hegelbach, J., Juillard, R., Karcza, Z., Keller, L.F., Kestenholz, M., Schaub, M. and Spina, F. 2007. Bird ringing for science and Conservation. The European Union for Bird Ringing, Abächerli Druck AG, Sarnen, Switzerland, 33 pp.
- Barker, S.C. and Walker, A.R. 2014. Ticks of Australia. The species that infest domestic animals and humans. Zootaxa, 3816: 1-144.
doi: 10.11646/zootaxa.3816.1.1
- Barton, T.R. 1995. A modified technique for extracting live ticks from small soil and litter samples. Experimental and Applied Acarology, 19: 357-360.
doi: 10.1007/BF00052393
- Beer, S.J., Lockwood, G.M., Raijmakers, J.M.H., Scott, W.A., Oschadleus, H.D. and Underhill, L.G. 2001. SAFRING Bird Ringing Manual. Animal Demography Unit, Cape Town, 55 pp.
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doi: 10.1073/pnas.91.21.10034
- Busse, P. 2000. Bird Station Manual. Gdańsk: University of Gdańsk Press, Poland, 264 pp.
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- Clifford, C.M., Anastos, G. and Elbl, A. 1961. The larval Ixodid ticks of the Eastern United States (Acarina-Ixodidae). Miscellaneous Publications of the Entomological Society of America, 2: 213-237.
- Department of Biodiversity-Conservation and Attractions. 2017. Standard Operating Procedure: Mist Net Trapping for Birds. Perth, WA, USA, 19 pp.
- Dietrich, M., Gomez-Diaz, E. and McCoy, K.D. 2011. Worldwide distribution and diversity of seabird ticks: implications for the ecology and epidemiology of tick-borne pathogens. Vector-Borne and Zoonotic Diseases, 11: 453-470.
doi: 10.1089/vbz.2010.0009
- Dubska, L., Literak, I., Kocianova, E., Taragelova, V. and Sychra, O. 2009. Differential role of passerine birds in distribution of Borreliaspirochetes, based on data from ticks collected from birds during the postbreeding mi-gration period in Central Europe. Applied and Envi-ronmental Microbiology, 75: 596-602.
doi: 10.1128/AEM.01674-08
- Dunn, E.H. and Ralph, C.J. 2004. Use of mist nets as a tool for bird population monitoring. Studies in Avian Biol-ogy, 29: 1-6.
- Durden, L.A. and Keirans, J.E. 1996. Nymphs of the genus Ixodes (Acari: Ixodidae) of the United States: taxonomy, identification key, distribution, hosts, and medi-cal/veterinary importance. Entomological Society of America, Lanham, Maryland, USA, 95 pp.
- Elfving, K., Olsen, B., Bergström, S., Waldenström, J., Lundkvist, A., Sjöstedt, A., Mejlon, H. and Nilsson, K. 2010. Dissemination of spotted fever Rickettsia agents in Europe by migrating birds. PLoS One, 5: e8572.
doi: 10.1371/journal.pone.0008572
- Estrada-Peña, A., Mihalca, A.D. and Petney, T.N. 2017. Ticks of Europe and North Africa: a guide to species identification. Springer, Cham, Switzerland, 404 pp.
- Filippova, N.A. 1997. Fauna of Russia and neighbouring countries. Ixodid ticks of subfamily Amblyomminae. 4 (5). Nauka Publishing House, St. Petersburg, Russia, 436 pp.
- Filippova, N.A. 1977. Ixodid ticks (Ixodinae). Fauna USSR New Ser. 4 (4). Nauka, Moscow, Leningrad, Russia, 316 pp.
- Gosler, A. 2004. Birds in the hand. In: Bird ecology and conservation: a handbook of techniques. Sutherland, W.J., Newton, I. and Green, R. (Eds). Oxford University Press, New York, NY, USA, 85-118.
- Hoogstraal, H., Kaiser, M.N., Traylor, M.A., Gaber, S. and Guindy, E. 1961. Ticks (Ixodoidea) on birds migrating from Africa to Europe and Asia. Bulletin of the World Health Organization, 24: 197-212.
- Horak, I.G., Heyne, H., Williams, R., Gallivan, G.J., Spickett, A.M., Bezuidenhout, J.D. and Estrada-Peña, A. 2018. The ixodid ticks (Acari: Ixodidae) of Southern Africa. Springer, Cham, Switzerland, 676 pp.
- Karger, A., Kampen, H., Bettin, B., Dautel, H., Ziller, M., Hoffmann, B., Süss, J. and Klaus, C. 2012. Species determination and characterization of developmental stages of ticks by whole-animal matrix-assisted laser desorption/ionization mass spectrometry. Ticks and Tick-borne Diseases, 3: 78-89.
doi: 10.1016/j.ttbdis.2011.11.002
- Keskin, A., and Erciyas-Yavuz, K. 2019. Ticks (Acari: Ixodidae) parasitizing passerine birds in turkey with new records and new tick–host associations. Journal of Medical Entomology, 56: 156-161.
doi: 10.1093/jme/tjy151
- Keskin, A., Koprulu, T.K., Bursali, A., Ozsemir, A.C., Erciyas-Yavuz, K. and Tekin, S. 2014. First record of Ixodes ar-boricola (Ixodida: Ixodidae) from Turkey with presence of Candidatus Rickettsia vini (Rickettsiales: Rickettsiaceae). Journal of Medical Entomology, 51: 864-867.
doi: 10.1603/ME13169
- Kim, H.-C., Park, J.-G., Kwon, Y.-S., Kim, M., Park, C.-U., Yun, S.-M., Chon, S.-T., Kim, M.-S.T., Klein, A. and Robbins, R.G. 2018. Ticks collected from soil/nest litter and live and dead nestlings of migratory seabirds during their breeding season at six uninhabited Islands, Republic of Korea during 2009 and 2014-2017. Systematic and Applied Acarology, 23: 1519-1530.
doi: 10.11158/saa.23.8.3
- Leblebicioglu, H., Eroglu, C., Erciyas-Yavuz, K., Hokelek, M., Acici, M. and Yilmaz, H. 2014. Role of migratory birds in spreading Crimean-Congo hemorrhagic fever, Turkey. Emerging Infectious Diseases, 20: 1331-1334.
doi: 10.3201/eid2008.131547
- Luz, H.R., H. Faccini, J.L., Landulfo, G.A., Berto, B.P. and Ferreira, I. 2012. Bird ticks in an area of the Cerrado of Minas Gerais State, southeast Brazil. Experimental and Applied Acarology, 58: 89-99.
doi: 10.1007/s10493-012-9572-7
- Martins, T.F., Onofrio, V.C., Barros-Battesti, D.M. and Labruna, M.B. 2010. Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: Descriptions, redescriptions, and identification key. Ticks and Tick-borne Diseases, 1: 75-99.
doi: 10.1016/j.ttbdis.2010.03.002
- Medlock, J., Balenghien, T., Alten, B., Versteirt, V. and Schaffner, F. 2018. Field sampling methods for mosquitoes, sandflies, biting midges and ticks - VectorNet project 2014-2018. European Centre for Disease Prevention and Control & European Food Safety Authority.
doi: 10.2903/sp.efsa.2018.EN-1435
- Mumcuoglu, K.Y., Banet-Noach, C., Malkinson, M., Shalom, U. and Galun, R. 2005. Argasid ticks as possible vectors of West Nile Virus in Israel. Vector-Borne and Zoonotic Diseases, 5: 65-71.
doi: 10.1089/vbz.2005.5.65
- Nava, S., Venzal, J.M., Acuña, D.G., Martins, T.F. and Gug-lielmone, A.A. 2017. Ticks of the southern cone of America: diagnosis, distribution, and hosts with tax-onomy, ecology and sanitary importance. Academic Press, London, UK, 348 pp.
- Ogrzewalska, M., Pacheco, R.C., Uezu, A., Richtzenhain, L.J., Ferreira, F. and Labruna, M.B. 2009. Ticks (Acari: Ixodidae) infesting birds in an Atlantic rain forest region of Brazil. Journal of Medical Entomology, 46: 1225-1229.
doi: 10.1603/033.046.0534
- Ralph, C. J., Dunn, E.H., Peach, W.J. and Handel, C.M. 2004. Recommendations for the use of mist nets for inventory and monitoring of bird populations. Studies in Avian Biology, 29: 187-196.
- Roberts, F.H.S. 1970. Australian ticks. CSIRO, Melbourne, Australia, 267 pp.
- Robinson, R.A., Morrison, C.A., and Baillie, S.R. 2014. Integrating demographic data: towards a framework for monitoring wildlife populations at large spatial scales. Methods in Ecology and Evolution, 5: 1361-1372.
doi: 10.1111/2041-210X.12204
- Roselli, M.A., Cady, S.M., Lao, S., Noden, B.H. and Loss, S.R. 2020. Variation in tick load among bird body parts: implications for studying the role of birds in the ecology and epidemiology of tick-borne diseases. Journal of Medical Entomology, 57: 845-851.
doi: 10.1093/jme/tjz228
- Schneider, S.C., Parker, C.M., Miller, J.R., Page-Fredericks, L. and Allan, B.F. 2015. Assessing the contribution of songbirds to the movement of ticks and Borrelia burgdorferi in the Midwestern United States during fall migration. Ecohealth, 12: 164-173.
doi: 10.1007/s10393-014-0982-3
- Walker, J.B., Keirans, J.E. and Horak, I.G. 2000. The genus Rhipicephalus (Acari: Ixodidae): a guide to the brown ticks of the world. Cambridge University Press, Cambridge, UK, 643 pp.
- Wallménius, K., Barboutis, C., Fransson, T., Jaenson, T.G., Lindgren, P.-E., Nyström, F., Olsen, B., Salaneck, E. and Nilsson, K. 2014. Spotted fever Rickettsia species in Hyalomma and Ixodes ticks infesting migratory birds in the European Mediterranean area. Parasites and Vectors, 7: 318.
doi: 10.1186/1756-3305-7-318
- Wilkinson, D.A., Dietrich, M., Lebarbenchon, C., Jaeger, A., Le Rouzic, C., Bastien, M., Lagadec, E., McCoy, K.D., Pas-calis, H., Le Corre, M., Dellagi, K. and Tortosa, P. 2014. Massive infection of seabird ticks with bacterial species related to Coxiella burnetii. Applied and Environmental Microbiology, 80: 3327-3333.
doi: 10.1128/AEM.00477-14
Year 2021,
, 1 - 8, 27.01.2021
Adem Keskin
,
Kiraz Erciyas Yavuz
,
Arif Cemal Özsemir
,
Kosta Y. Mumcuoğlu
References
- Allan, S.A. 2013. Tick rearing and in vitro feeding.In: Biology of Ticks. Sonenshine, D.E. and Roe, R.M. (Eds), Oxford University Press, New York, NY, USA, 445-473.
- Apanaskevich, D.A. and Horak, I.G. 2008. The genus Hyalomma Koch, 1844: V. re-evaluation of the taxonomic rank of taxa comprising the H. (Euhyalomma) marginatum Koch complex of species (Acari: Ixodidae) with redescription of all parasitic stages and notes on biology. International Journal of Acarology, 34: 13-42.
doi: 10.1080/01647950808683704
- Apanaskevich, D.A. and Oliver Jr, J.H. 2014. Life cycles and natural history of ticks. In: Biology of ticks. Sonenshine, D.E. and Roe, R.M. (Eds). Oxford University Press, New York, NY, USA, 59-73.
- Arthur, D.R. 1965. Ticks of the genus Ixodes in Africa. The Athlone Press, University of London, London, UK, 348 pp.
- Baillie, S., Bairlein, F., Clark, J., du Feu, C., Fiedler, W., Fransson, T., Hegelbach, J., Juillard, R., Karcza, Z., Keller, L.F., Kestenholz, M., Schaub, M. and Spina, F. 2007. Bird ringing for science and Conservation. The European Union for Bird Ringing, Abächerli Druck AG, Sarnen, Switzerland, 33 pp.
- Barker, S.C. and Walker, A.R. 2014. Ticks of Australia. The species that infest domestic animals and humans. Zootaxa, 3816: 1-144.
doi: 10.11646/zootaxa.3816.1.1
- Barton, T.R. 1995. A modified technique for extracting live ticks from small soil and litter samples. Experimental and Applied Acarology, 19: 357-360.
doi: 10.1007/BF00052393
- Beer, S.J., Lockwood, G.M., Raijmakers, J.M.H., Scott, W.A., Oschadleus, H.D. and Underhill, L.G. 2001. SAFRING Bird Ringing Manual. Animal Demography Unit, Cape Town, 55 pp.
- Black, W.C. and Piesman, J. 1994. Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proceedings of the National Academy of Sciences of the United States of America, 91: 10034-10038.
doi: 10.1073/pnas.91.21.10034
- Busse, P. 2000. Bird Station Manual. Gdańsk: University of Gdańsk Press, Poland, 264 pp.
- Busse, P. and Meissner, W. 2015. Bird ringing station manual. De Gruyter Open, Berlin/Munich/Boston, 211 pp.
- Clifford, C.M., Anastos, G. and Elbl, A. 1961. The larval Ixodid ticks of the Eastern United States (Acarina-Ixodidae). Miscellaneous Publications of the Entomological Society of America, 2: 213-237.
- Department of Biodiversity-Conservation and Attractions. 2017. Standard Operating Procedure: Mist Net Trapping for Birds. Perth, WA, USA, 19 pp.
- Dietrich, M., Gomez-Diaz, E. and McCoy, K.D. 2011. Worldwide distribution and diversity of seabird ticks: implications for the ecology and epidemiology of tick-borne pathogens. Vector-Borne and Zoonotic Diseases, 11: 453-470.
doi: 10.1089/vbz.2010.0009
- Dubska, L., Literak, I., Kocianova, E., Taragelova, V. and Sychra, O. 2009. Differential role of passerine birds in distribution of Borreliaspirochetes, based on data from ticks collected from birds during the postbreeding mi-gration period in Central Europe. Applied and Envi-ronmental Microbiology, 75: 596-602.
doi: 10.1128/AEM.01674-08
- Dunn, E.H. and Ralph, C.J. 2004. Use of mist nets as a tool for bird population monitoring. Studies in Avian Biol-ogy, 29: 1-6.
- Durden, L.A. and Keirans, J.E. 1996. Nymphs of the genus Ixodes (Acari: Ixodidae) of the United States: taxonomy, identification key, distribution, hosts, and medi-cal/veterinary importance. Entomological Society of America, Lanham, Maryland, USA, 95 pp.
- Elfving, K., Olsen, B., Bergström, S., Waldenström, J., Lundkvist, A., Sjöstedt, A., Mejlon, H. and Nilsson, K. 2010. Dissemination of spotted fever Rickettsia agents in Europe by migrating birds. PLoS One, 5: e8572.
doi: 10.1371/journal.pone.0008572
- Estrada-Peña, A., Mihalca, A.D. and Petney, T.N. 2017. Ticks of Europe and North Africa: a guide to species identification. Springer, Cham, Switzerland, 404 pp.
- Filippova, N.A. 1997. Fauna of Russia and neighbouring countries. Ixodid ticks of subfamily Amblyomminae. 4 (5). Nauka Publishing House, St. Petersburg, Russia, 436 pp.
- Filippova, N.A. 1977. Ixodid ticks (Ixodinae). Fauna USSR New Ser. 4 (4). Nauka, Moscow, Leningrad, Russia, 316 pp.
- Gosler, A. 2004. Birds in the hand. In: Bird ecology and conservation: a handbook of techniques. Sutherland, W.J., Newton, I. and Green, R. (Eds). Oxford University Press, New York, NY, USA, 85-118.
- Hoogstraal, H., Kaiser, M.N., Traylor, M.A., Gaber, S. and Guindy, E. 1961. Ticks (Ixodoidea) on birds migrating from Africa to Europe and Asia. Bulletin of the World Health Organization, 24: 197-212.
- Horak, I.G., Heyne, H., Williams, R., Gallivan, G.J., Spickett, A.M., Bezuidenhout, J.D. and Estrada-Peña, A. 2018. The ixodid ticks (Acari: Ixodidae) of Southern Africa. Springer, Cham, Switzerland, 676 pp.
- Karger, A., Kampen, H., Bettin, B., Dautel, H., Ziller, M., Hoffmann, B., Süss, J. and Klaus, C. 2012. Species determination and characterization of developmental stages of ticks by whole-animal matrix-assisted laser desorption/ionization mass spectrometry. Ticks and Tick-borne Diseases, 3: 78-89.
doi: 10.1016/j.ttbdis.2011.11.002
- Keskin, A., and Erciyas-Yavuz, K. 2019. Ticks (Acari: Ixodidae) parasitizing passerine birds in turkey with new records and new tick–host associations. Journal of Medical Entomology, 56: 156-161.
doi: 10.1093/jme/tjy151
- Keskin, A., Koprulu, T.K., Bursali, A., Ozsemir, A.C., Erciyas-Yavuz, K. and Tekin, S. 2014. First record of Ixodes ar-boricola (Ixodida: Ixodidae) from Turkey with presence of Candidatus Rickettsia vini (Rickettsiales: Rickettsiaceae). Journal of Medical Entomology, 51: 864-867.
doi: 10.1603/ME13169
- Kim, H.-C., Park, J.-G., Kwon, Y.-S., Kim, M., Park, C.-U., Yun, S.-M., Chon, S.-T., Kim, M.-S.T., Klein, A. and Robbins, R.G. 2018. Ticks collected from soil/nest litter and live and dead nestlings of migratory seabirds during their breeding season at six uninhabited Islands, Republic of Korea during 2009 and 2014-2017. Systematic and Applied Acarology, 23: 1519-1530.
doi: 10.11158/saa.23.8.3
- Leblebicioglu, H., Eroglu, C., Erciyas-Yavuz, K., Hokelek, M., Acici, M. and Yilmaz, H. 2014. Role of migratory birds in spreading Crimean-Congo hemorrhagic fever, Turkey. Emerging Infectious Diseases, 20: 1331-1334.
doi: 10.3201/eid2008.131547
- Luz, H.R., H. Faccini, J.L., Landulfo, G.A., Berto, B.P. and Ferreira, I. 2012. Bird ticks in an area of the Cerrado of Minas Gerais State, southeast Brazil. Experimental and Applied Acarology, 58: 89-99.
doi: 10.1007/s10493-012-9572-7
- Martins, T.F., Onofrio, V.C., Barros-Battesti, D.M. and Labruna, M.B. 2010. Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: Descriptions, redescriptions, and identification key. Ticks and Tick-borne Diseases, 1: 75-99.
doi: 10.1016/j.ttbdis.2010.03.002
- Medlock, J., Balenghien, T., Alten, B., Versteirt, V. and Schaffner, F. 2018. Field sampling methods for mosquitoes, sandflies, biting midges and ticks - VectorNet project 2014-2018. European Centre for Disease Prevention and Control & European Food Safety Authority.
doi: 10.2903/sp.efsa.2018.EN-1435
- Mumcuoglu, K.Y., Banet-Noach, C., Malkinson, M., Shalom, U. and Galun, R. 2005. Argasid ticks as possible vectors of West Nile Virus in Israel. Vector-Borne and Zoonotic Diseases, 5: 65-71.
doi: 10.1089/vbz.2005.5.65
- Nava, S., Venzal, J.M., Acuña, D.G., Martins, T.F. and Gug-lielmone, A.A. 2017. Ticks of the southern cone of America: diagnosis, distribution, and hosts with tax-onomy, ecology and sanitary importance. Academic Press, London, UK, 348 pp.
- Ogrzewalska, M., Pacheco, R.C., Uezu, A., Richtzenhain, L.J., Ferreira, F. and Labruna, M.B. 2009. Ticks (Acari: Ixodidae) infesting birds in an Atlantic rain forest region of Brazil. Journal of Medical Entomology, 46: 1225-1229.
doi: 10.1603/033.046.0534
- Ralph, C. J., Dunn, E.H., Peach, W.J. and Handel, C.M. 2004. Recommendations for the use of mist nets for inventory and monitoring of bird populations. Studies in Avian Biology, 29: 187-196.
- Roberts, F.H.S. 1970. Australian ticks. CSIRO, Melbourne, Australia, 267 pp.
- Robinson, R.A., Morrison, C.A., and Baillie, S.R. 2014. Integrating demographic data: towards a framework for monitoring wildlife populations at large spatial scales. Methods in Ecology and Evolution, 5: 1361-1372.
doi: 10.1111/2041-210X.12204
- Roselli, M.A., Cady, S.M., Lao, S., Noden, B.H. and Loss, S.R. 2020. Variation in tick load among bird body parts: implications for studying the role of birds in the ecology and epidemiology of tick-borne diseases. Journal of Medical Entomology, 57: 845-851.
doi: 10.1093/jme/tjz228
- Schneider, S.C., Parker, C.M., Miller, J.R., Page-Fredericks, L. and Allan, B.F. 2015. Assessing the contribution of songbirds to the movement of ticks and Borrelia burgdorferi in the Midwestern United States during fall migration. Ecohealth, 12: 164-173.
doi: 10.1007/s10393-014-0982-3
- Walker, J.B., Keirans, J.E. and Horak, I.G. 2000. The genus Rhipicephalus (Acari: Ixodidae): a guide to the brown ticks of the world. Cambridge University Press, Cambridge, UK, 643 pp.
- Wallménius, K., Barboutis, C., Fransson, T., Jaenson, T.G., Lindgren, P.-E., Nyström, F., Olsen, B., Salaneck, E. and Nilsson, K. 2014. Spotted fever Rickettsia species in Hyalomma and Ixodes ticks infesting migratory birds in the European Mediterranean area. Parasites and Vectors, 7: 318.
doi: 10.1186/1756-3305-7-318
- Wilkinson, D.A., Dietrich, M., Lebarbenchon, C., Jaeger, A., Le Rouzic, C., Bastien, M., Lagadec, E., McCoy, K.D., Pas-calis, H., Le Corre, M., Dellagi, K. and Tortosa, P. 2014. Massive infection of seabird ticks with bacterial species related to Coxiella burnetii. Applied and Environmental Microbiology, 80: 3327-3333.
doi: 10.1128/AEM.00477-14