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Urban forests as hubs for novel zoonosis: blood meal analysis, seasonal variation in Culicoides (Diptera: Ceratopogonidae) vectors, and avian haemosporidians

Published online by Cambridge University Press:  28 August 2013

DIEGO SANTIAGO-ALARCON ,
PETER HAVELKA ,
EDUARDO PINEDA ,
GERNOT SEGELBACHER  and
H. MARTIN SCHAEFER
DIEGO SANTIAGO-ALARCON*
Affiliation:
Department of Ecology and Evolutionary Biology, University of Freiburg, Hauptstr. 1, 79104 Freiburg, Baden-Württemberg, Germany Biología y Conservación de Vertebrados, Instituto de Ecología A.C. Carretera Antigua a Coatepec 351, El Haya, C.P. 91070 Xalapa, Veracruz, México
PETER HAVELKA
Affiliation:
Department of Zoology, Staatliches Museum für Naturkunde, Erbprinzenstraße 13, 76133 Karlsruhe, Baden-Württemberg, Germany
EDUARDO PINEDA
Affiliation:
Biología y Conservación de Vertebrados, Instituto de Ecología A.C. Carretera Antigua a Coatepec 351, El Haya, C.P. 91070 Xalapa, Veracruz, México
GERNOT SEGELBACHER
Affiliation:
Department of Wildlife Ecology and Management, University of Freiburg, Tennenbacher Straße 4, 79106 Freiburg, Baden-Württemberg, Germany
H. MARTIN SCHAEFER
Affiliation:
Department of Ecology and Evolutionary Biology, University of Freiburg, Hauptstr. 1, 79104 Freiburg, Baden-Württemberg, Germany
*
*Corresponding author: Biología y Conservación de Vertebrados, Instituto de Ecología A.C. Carretera Antigua a Coatepec 351, El Haya, C.P. 91070 Xalapa, Veracruz, México. E-mail: diego.santiago@inecol.edu.mx
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Summary

Culicoides vectors can transmit a diverse array of parasites and are globally distributed. We studied feeding preferences and seasonal variation of Culicoides (Diptera: Ceratopogonidae) vectors in an urban forest of Germany to determine whether humans living nearby are readily exposed to vector-borne parasites from wild animals. We used a fragment of the mtDNA COI gene to identify hosts from blood meals. We amplified a fragment of the mtDNA cyt b to detect haemosporidian infections in Culicoides abdomens and thoraxes. We detected a total of 22 Culicoides species. Fifty-eight blood meals (84%) were from humans, 10 from birds, and one from livestock. We found Culicoides kibunensis (considered ornithophilic) with 29 human blood meals. Host generalist Culicoides festivipennis and Culicoides obsoletus had 14 human blood meals. Culicoides clastrieri and Culicoides semimaculatus fed on birds; previously humans were their only known host. Six thoraxes and three abdomens were infected with either Haemoproteus pallidulus or Haemoproteus parabelopolskyi. There were changes in Culicoides community structure across months. Culicoides pictipennis was the dominant species during spring, C. kibunensis and C. clastrieri were dominant during summer, and C. obsoletus was dominant by early autumn. All dominant species were generalists feeding on birds, livestock and humans. Our results indicate that humans can serve as a blood source for dominant Culicoides species instead of the normal wild animal hosts in urban areas.

Keywords

CulicoidesHaemoproteusSylvia atricapillablood meal analysisemergent diseaseconservation medicinehost–parasite interaction

Information

Type
Research Article
Information
Parasitology , Volume 140 , Issue 14 , December 2013 , pp. 1799 - 1810
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Alcaide, M., Rico, C., Ruíz, S., Soriguer, R., Muñoz, J. and Figuerola, J. (2009). Disentangling vector-borne transmission networks: a universal DNA barcoding method to identify vertebrate hosts from arthropod blood meals. PLoS ONE 4, e7092.CrossRefGoogle Scholar
Arinaminpathy, N. and McLean, A. R. (2009). Evolution and emergence of novel human infections. Proceedings of the Royal Society of London, B 276, 3937–3943.Google ScholarPubMed
Atkinson, C. T. (1988). Epizootiology of Haemoproteus meleagridis (Protozoa: Haemosporina) in Florida: potential vectors and prevalence in naturally infected Culicoides (Diptera: Ceratopogonidae). Journal of Medical Entomology 25, 39–44.CrossRefGoogle ScholarPubMed
Atkinson, C. T., Forrester, D. J. and Greiner, E. C. (1988). Epizootiology of Haemoproteus meleagridis (Protozoa: Haemosporina) in Florida: seasonal transmission and vector abundance. Journal of Medical Entomology 25, 45–51.CrossRefGoogle ScholarPubMed
Bartsch, S., Bauer, B., Wiemann, A., Clausen, P.-H. and Steuber, S. (2009). Feeding patterns of biting midges of the Culicoides obsoletus and Culicoides pulicaris groups on selected farms in Brandenburg, Germany. Parasitology Research 105, 373–380.CrossRefGoogle ScholarPubMed
Bearhop, S., Fiedler, W., Furness, R. W., Votier, S. C., Waldron, S., Newton, J., Bowen, G. J., Berthold, P. and Farnsworth, K. (2005). Assortative mating as a mechanism for rapid evolution of a migratory divide. Science 310, 502–504.CrossRefGoogle ScholarPubMed
Bennett, G. F. (1960). On some ornithophilic blood-sucking diptera in the Algonquin Park, Ontario, Canada. Canadian Journal of Zoology 38, 377–389.CrossRefGoogle Scholar
Bennett, G. F. and Cameron, M. (1974). Seasonal prevalence of avian hematozoa in passeriform birds of Atlantic Canada. Canadian Journal of Zoology 52, 1259–1264.CrossRefGoogle ScholarPubMed
Bensch, S. and Åkesson, S. (2003). Temporal and spatial variation of hematozoans in Scandinavian Willow warblers. Journal of Parasitology 89, 388–391.CrossRefGoogle ScholarPubMed
Borkent, A. (2005). The biting midges, the Ceratopogonidae (Diptera). In Biology of Disease Vectors, 2nd Edn (ed. Marquardt, C.), pp. 113–126. Elsevier Academic Press, San Diego, USA.Google Scholar
Bradley, C. A. and Altizer, S. (2007). Urbanization and the ecology of wildlife diseases. Trends in Ecology and Evolution 22, 95–102.CrossRefGoogle ScholarPubMed
Braverman, Y., Boreham, P. F. L., Galun, R. and Ziv, M. (1977). The origin of blood meals of biting midges (Diptera: Ceratopogonidae) and mosquitoes (Diptera: Culicidae) trapped in turkey runs in Israel. Rhodesian Journal of Agricultural Research 15, 101–104.Google Scholar
Burýlova, A. M. (1975). On bloodsucking midges attacking the birds in the forests of Prikamje. Parazitologiya 9, 197–200.Google Scholar
Butenko, O. M. (1967). Some data on the feeding of blood-sucking insects (gnats) on birds. Bjulleten Moskovskogo obsiestva spytatelej prirody, otdel biologiceskij 72, 132–136.Google Scholar
Calisher, C. H. (1994). Medically important arboviruses of the United States and Canada. Clinical Microbiology Reviews 7, 89–116.CrossRefGoogle ScholarPubMed
Chao, A. and Shen, T. J. (2010). Program SPADE (Species Prediction And Diversity Estimation). http://chao.stat.nthu.edu.tw.Google Scholar
Clark, G. W. (1964). Frequency of infection and seasonal variation of Leucocytozoon berestneffi in the yellow-billed magpie, Pica nuttalli. Journal of Protozoology 11, 481–484.CrossRefGoogle ScholarPubMed
Coggeshall, L. T. (1940). The infection of Anopheles quadrimaculatus with a monkey malaria parasite, Plasmodium cynomolgi, and with an avian parasite, Plasmodium lophurae. Journal of Parasitology 26, S44–S45.Google Scholar
Delécolle, J. C. (1985). Nouvelle contribution à l’étude systématique et iconographieque des espèces du genre Culicoides (Diptera: Ceratopogonidae) du Nord – Est de la France. Thèse. Université Louis Pasteur de Strasbourg, pp. 1–238.Google Scholar
Enayati, A. and Hemingway, J. (2010). Malaria management: past, present, and future. Annual Review of Entomology 55, 569–591.CrossRefGoogle ScholarPubMed
Ewald, P. W. (1994). Evolution of Infectious Disease. Oxford University Press, New York, USA.CrossRefGoogle Scholar
Feinsinger, P. (2001). Designing Field Studies for Biodiversity Conservation. The Nature Conservancy, Island Press, Washington, USA.Google Scholar
Fritz, H. G. (1982). Dissertation – Ökologische und systematische Untersuchungen an Diptera/Nematocera (Insecta) in Überschwemmungsgebieten des Nördlichen Oberrheins – Ein Beitrag zur Ökologie großer Flußauen – Fachbereich 10: Biologie der Technischen Hochschule Darmstadt. Dissertation, 296 pp. Information from p. 108.Google Scholar
Garvin, M. C. and Greiner, E. C. (2003). Ecology of Culicoides (Diptera: Ceratopogonidae) in Southcentral Florida and experimental Culicoides vectors of the avian hematozoan Haemoproteus danilewskyi Kruse. Journal of Wildlife Diseases 39, 170–178.CrossRefGoogle ScholarPubMed
Gethmann, J., Hoffmann, B., Probst, C., Beer, M., Conraths, F. J. and Mettenleiter, T. C. (2010). A survey of three years with bluetongue disease serotype 8 in Germany (in German). Tierärztliche Umschau 64, 4–12.Google Scholar
Greiner, E. C. (1975). Prevalence and potential vectors of Haemoproteus in Nebraska mourning doves. Journal of Wildlife Diseases 11, 150–156.CrossRefGoogle Scholar
Havelka, P. (1976). Limnologische und systematische Studien an Ceratopogoniden (Diptera: Nematocera). Beiträge zur Entomologie Berlin 26, 211–305.Google Scholar
Havelka, P. and Aguilar, M. (1999). Ceratopogonidae. In Checkliste der Dipteren Deutschlands: Studia Dipterologica (ed. Schumann, H., Bährmann, R. and Stark, A.), pp. S33–S38. Suppl. 2. Ampyx-Verlag, Halle (Saale), Germany.Google Scholar
Hellgren, O., Waldenström, J. and Bensch, S. (2004). A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90, 797–802.CrossRefGoogle ScholarPubMed
Henderson, P. A. and Seaby, R. M. H. (2002). Species Diversity and Richness v.3.02. PISCES Conservation Ltd., Pennington, UK.Google Scholar
Herman, C. M. (1938). Mosquito transmission of avian malaria parasites (Plasmodium circumflexum and P. cathemerium). American Journal of Hygiene 27, 345–350.Google Scholar
Hörbrand, T. and Geier, M. (2009). Monitoring of Culicoides at nine locations in southern Germany (2007–2008). Parasitology Research 105, 387–392.CrossRefGoogle ScholarPubMed
Institute for Animal Health (IAH), Vector-borne diseases – culicoides.net – UK Culicoides reference laboratory. http://www.bluetonguevirus.org/culicoides.Google Scholar
Janovy, J. Jr. (1966). Epidemiology of Plasmodium hexamerium Huff, 1935, in meadowlarks and starlings of the Cheyenne Bottoms, Barton County, Kansas. Journal of Parasitology 52, 573–578.CrossRefGoogle ScholarPubMed
Jones, K. E., Pater, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman, J. L. and Daszak, P. (2008). Global trends in emerging infectious diseases. Nature 451, 990–993.CrossRefGoogle ScholarPubMed
Jost, L. (2006). Entropy and diversity. Oikos 113, 363–375.CrossRefGoogle Scholar
Jost, L. (2010). The relation between evenness and diversity. Diversity 2, 207–232.CrossRefGoogle Scholar
Keeling, M. J. and Rohani, P. (2008). Modeling Infectious Diseases in Humans and Animals. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Kiel, E., Liebisch, G., Focke, R. and Liebisch, A. (2009). Monitoring of Culicoides at 20 locations in northwest Germany. Parasitology Research 105, 351–357.CrossRefGoogle ScholarPubMed
Kim, K. S., Tsuda, Y., Sasaki, T., Kobayashi, M. and Hirota, Y. (2009). Mosquito blood-meal analysis for avian malaria study in wild bird communities: laboratory verification and application to Culex sasai (Diptera: Culicidae) collected in Tokyo, Japan. Parasitology Research 105, 1351–1357.CrossRefGoogle ScholarPubMed
Kitaoka, S., Morii, T. and Kosuge, M. (1965). Field experiments on the repellents to chicken biting midges. Japanese Journal of Sanitary Zoology 16, 244–248.Google Scholar
Klei, T. R. and DeGiusti, D. L. (1975). Seasonal occurrence of Haemoproteus columbae Kruse and its vector Pseudolynchia canariensis Bequaert. Journal of Wildlife Diseases 11, 130–135.CrossRefGoogle ScholarPubMed
Kremer, M. (1965). Contribution a l'étude du genre Culicoides Latreille, particulièrement en France. Editions P. Lechevalier Paris. Encyclopédie Entomologique Série, A 39, 3–299.Google Scholar
Križanauskienė, A., Pérez-Tris, J., Palinauskas, V., Hellgren, O., Bensch, S. and Valkiūnas, G. (2010). Molecular phylogenetic and morphological analysis of haemosporidian parasites (Haemosporida) in a naturally infected European songbird, the Blackcap Sylvia atricapilla, with description of Haemoproteus pallidulus sp. nov. Parasitology 137, 217–227.CrossRefGoogle Scholar
Lassen, S. B., Nielsen, S. A., Skovgård, H. and Kristensen, M. (2011). Molecular identification of blood meals from biting midges (Diptera: Ceratopogonidae: Culicoides Latreille) in Denmark. Parasitology Research 108, 823–829.CrossRefGoogle Scholar
Lefèvre, T., Gouagna, L.-C., Dabiré, K. R., Elguero, E., Fontenille, D., Renaud, F., Costantini, C. and Thomas, F. (2009). Beyond nature and nurture: phenotypic plasticity in blood-feeding behavior of Anopheles gambiae s.s. when humans are not readily accessible. American Journal of Tropical Medicine and Hygiene 81, 1023–1029.CrossRefGoogle Scholar
Mayne, B. (1928). An anopheline mosquito as host for the parasites of bird malaria. Indian Journal of Medical Research 16, 557–558.Google Scholar
McGhee, R. B. (1951). The adaptation of the avian malaria parasite Plasmodium lophurae to a continuous existence in infant mice. Journal of Infectious Diseases 88, 86–97.CrossRefGoogle ScholarPubMed
McGhee, R. B. (1957). Comparative susceptibility of various erythrocytes to four species of avian Plasmodia. Journal of Infectious Diseases 100, 92–96.CrossRefGoogle ScholarPubMed
Mehlhorn, H., Walldorf, V., Klimpel, S., Jahn, B., Jaeger, F., Eschweiler, J., Hoffmann, B. and Beer, M. (2007). First occurrence of Culicoides obsoletus-transmitted bluetongue virus epidemic in central Europe. Parasitology Research 101, 219–228.CrossRefGoogle ScholarPubMed
Mehlhorn, H., Walldorf, V., Klimpel, S., Schmahl, G. (2008). Outbreak of bluetongue disease (BTD) in Germany and the danger for Europe. Parasitology Research 103(Suppl.), S79–S86.CrossRefGoogle ScholarPubMed
Mehlhorn, H., Walldorf, V., Klimpel, S., Schmahl, G., Al-Quraishy, S., Walldorf, U., Mehlhorn, B. and Bätza, H.-J. (2009). Entomological survey on vectors of bluetongue virus in Northrhine-Westfalia (Germany) during 2007 and 2008. Parasitology Research 105, 321–329.CrossRefGoogle ScholarPubMed
Mellor, P. S., Boorman, J. and Baylis, M. (2000). Culicoides biting midges: their role as arbovirus vectors. Annual Review of Entomology 45, 307–340.CrossRefGoogle ScholarPubMed
Minár, J. (1965). Tabanidae, Ceratopogonidae, Simuliidae from the Lipno Water – Reservoir. Československá Parazitologie 12, 197–206.Google Scholar
Nielsen, O. B. (1964). Studies on the Danish biting midges, Culicoides Latreille (Dipt., Ceratopogonidae). Entomlogiske Meddelelser 32, 261–276.Google Scholar
Nielsen, O. B. (1971). Some observations on biting midges (Diptera: Ceratopogonidae) attacking grazing cattle in Denmark. Entomologica Scandinavica 2, 94–98.CrossRefGoogle Scholar
Országh, I. (1976). Die Gattung Culicoides Latr. 1809 (Diptera, Ceratopogonidae) in Slowakei. Acta Facultatis Rerum Naturalium Universitatis Comenianae – Zoologia 21, 1–88.Google Scholar
Paclt, J., Callot, J. and Kremer, M. (1970). Cératopogonidés piqueurs habitant les tourbières et les biotopes non-tourbeux de la partie supérieure d'orava (Diptera Nematocera). Biológia (Bratislava) 25, 751–759.Google Scholar
Pérez-Tris, J. and Bensch, S. (2005 a). Diagnosing genetically diverse avian malarial infections using mixed-sequence analysis and TA-cloning. Parasitology 131, 15–23.CrossRefGoogle ScholarPubMed
Pérez-Tris, J. and Bensch, S. (2005 b). Dispersal increases local transmission of avian malaria parasites. Ecology Letters 8, 838–845.CrossRefGoogle Scholar
Pérez-Tris, J. and Tellería, J. L. (2002). Migratory and sedentary blackcaps in sympatric non-breeding grounds: implications for the evolution of avian migration. Journal of Animal Ecology 71, 211–224.CrossRefGoogle Scholar
Pérez-Tris, J., Bensch, S., Carbonell, R., Helbig, A. J. and Tellería, J. L. (2004). Historical diversification of migration patterns in a passerine bird. Evolution 58, 1819–1832.CrossRefGoogle Scholar
Pérez-Tris, J., Hellgren, O., Križanauskienė, A., Waldenström, J., Secondi, J., Bonneaud, C., Fjeldså, J., Hasselquist, D. and Bensch, S. (2007). Within-host speciation of malaria parasites. PLoS ONE 2, e235.CrossRefGoogle ScholarPubMed
Quan, M., Van Vuuren, M., Howel, P. G., Groenewald, D. and Guthrie, A. J. (2008). Molecular epidemiology of the African horse sickness virus S10 gene. Journal of General Virology 89, 1159–1168.CrossRefGoogle ScholarPubMed
Ratnasingham, S. and Hebert, P. D. N. (2007). BOLD: the barcode of life data system (www.barcodinglife.org). Molecular Ecology Notes 7, 355–364.CrossRefGoogle ScholarPubMed
Reiczigel, J. (2003). Confidence intervals for the binomial parameter: some new considerations. Statistics in Medicine 22, 611–621.CrossRefGoogle ScholarPubMed
Rolshausen, G., Segelbacher, G., Hobson, K. A. and Schaefer, H. M. (2009). Contemporary evolution of reproductive isolation and phenotypic divergence in sympatry along a migratory divide. Current Biology 19, 2097–2101.CrossRefGoogle ScholarPubMed
Rolshausen, G., Hobson, K. A. and Schaefer, H. M. (2010). Spring arrival along a migratory divide of sympatric blackcaps (Sylvia atricapilla). Oecologia 162, 175–183.CrossRefGoogle ScholarPubMed
Rózsa, L., Reiczigel, J. and Majoros, G. (2000). Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232.CrossRefGoogle ScholarPubMed
Santiago-Alarcon, D., Bloch, R., Rolshausen, G., Schaefer, H. M. and Segelbacher, G. (2011). Prevalence, diversity, and interaction patterns of avian haemosporidians in a four-year study of blackcaps in a migratory divide. Parasitology 138, 824–835.CrossRefGoogle Scholar
Santiago-Alarcon, D., Palinauskas, V. and Schaefer, H. M. (2012 a). Diptera vectors of avian haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews 87, 928–964.CrossRefGoogle ScholarPubMed
Santiago-Alarcon, D., Havelka, P., Schaefer, H. M. and Segelbacher, G. (2012 b). Blood meal analysis reveals avian Plasmodium infections and broad host preferences of Culicoides (Diptera: Ceratopogonidae) vectors. PLoS ONE 7, e31098.CrossRefGoogle Scholar
Santiago-Alarcon, D., Mettler, R., Segelbacher, G. and Schaefer, H. M. (2013). Haemosporidian parasitism in the blackcap (Sylvia atricapilla) in relation to spring arrival and body condition. Journal of Avian Biology (in press) doi: 10.1111/j.1600-048X.2013.00181.x.CrossRefGoogle Scholar
Shirihai, H., Gargallo, G. and Helbig, A. J. (2001). Sylvia Warblers. Princeton University Press, Princeton, NJ, USA.Google Scholar
Sol, D., Jovani, R. and Torres, J. (2000). Geographical variation in blood parasites in feral pigeons: the role of vectors. Ecography 23, 307–314.CrossRefGoogle Scholar
Solow, A. R. (1993). A simple test for change in community structure. Journal of Animal Ecology 62, 191–193.CrossRefGoogle Scholar
Super, P. E. and van Riper, C. III (1995). A comparison of avian hematozoan epizootiology in two California coastal scrub communities. Journal of Wildlife Diseases 31, 447–461.CrossRefGoogle ScholarPubMed
Szadziewski, R. (1984). On synonymy and morphology of some Culicoides species (Diptera, Ceratopogonidae). Polskie Pismo Entomolgiczne 53, 559–556.Google Scholar
Tellería, J. L. and Pérez-Tris, J. (2003). Seasonal distribution of a migratory bird: effects of local and regional resource tracking. Journal of Biogeography 30, 1583–1591.CrossRefGoogle Scholar
Valkiūnas, G. (2005). Avian Malaria Parasites and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
Valkiūnas, G. and Iezhova, T. A. (2004 a). Detrimental effects of Haemoproteus infections on the survival of biting midge Culicoides impunctatus (Diptera: Ceratopogonidae). Journal of Parasitology 90, 194–196.CrossRefGoogle ScholarPubMed
Valkiūnas, G. and Iezhova, T. A. (2004 b). The transmission of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) of blackcap by Culicoides impunctatus (Diptera: Ceratopogonidae). Journal of Parasitology 90, 196–198.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Liutkevičius, G. and Iezhova, T. A. (2002). Complete development of three species of Haemoproteus (Haemosporida, Haemoproteidae) in the biting midge Culicoides impunctatus (Diptera, Ceratopogonidae). Journal of Parasitology 88, 864–868.CrossRefGoogle ScholarPubMed
Valkiūnas, G., Žičkus, T., Shapoval, A. P. and Iezhova, T. A. (2006). Effect of Haemoproteus belopolskyi (Haemosporida: Haemoproteidae) on body mass of the blackcap Sylvia atricapilla. Journal of Parasitology 92, 1123–1125.CrossRefGoogle ScholarPubMed
Vorsprach, B., Meiser, C. K., Werner, D., Balczun, C. and Schaub, G. A. (2009). Monitoring of Ceratopogonidae in southwest Germany. Parasitology Research 105, 337–344.CrossRefGoogle ScholarPubMed
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