Abstract
The biting midges (Ceratopogonidae) are one of the most species-rich families of insects on the planet with over 6,200 named species. However, their true diversity is unknown and this paper is the first to address the question. Our systematic study of the family in Costa Rica indicates that 192 species were present in a four hectare area of cloudforest at Zurquí de Moravia, at 1,600 m after a year of intensive sampling. Combined with a collection from a single Malaise trap at Tapantí for one year, about 40 kms away and also at 1,600 m, the total was 245 species with significant differences between the two areas and with the strong majority unnamed. This compares to 430 named species for all of Costa Rica and 1,314 for the entire Neotropical Region. Barcoding of 221,407 specimens from Costa Rica similarly indicates large numbers of unnamed species with 4,023 BINs present. On this basis, we project at least 5,000 species in Costa Rica and using ratios of named species here and elsewhere, we suggest that nearly 73,000 are present worldwide. Details from Malaise traps in the Área de Conservación Guanacaste also indicate various levels of endemism. Samples from Bolivia support an interpretation of high diversity.
The diversification of the family was examined by comparing phyletic lineages, rather than merely comparing numbers of species in various genera, providing insight as to why some lineages are more diverse than others. Zoogeographic patterns of named species suggest stronger southern connections for Costa Rican Ceratopogonidae in both cloudforest habitats as well as the country as a whole, although many are also more broadly distributed north and south of the country. Comparisons between various collecting methods at Zurquí de Moravia indicate the efficacy of Malaise traps but also the importance of light traps and other methods in sampling adults of Ceratopogonidae. Phenological data from the Malaise traps in the Área de Conservación Guanacaste suggest some patterns of emergence of adults in Costa Rica, the first for any tropical country anywhere.
References
- Barrantes, G. (2009) The role of historical and local factors in determining species composition of the highland avifauna of Costa Rica and Western Panamá. Revista de Biología Tropical, 57 (Supplement 1), 333–349.
- Bickel, D.J. & Tasker, E.M. (2004) Tree trunk invertebrates in Australian forests: conserving unknown species and complex processes. In: Lunney, D. (Ed.), The Conservation of Australia’s Forest Fauna. 2nd Edition. Royal Zoological Society of New South Wales, Mosman, New South Wales, pp. 888–898. https://doi.org/10.7882/FS.2004.888
- Borkent, A. (1991) The Ceratopogonidae (Diptera) of the Galápagos Islands, Ecuador with a discussion of their phylogenetic relationships and zoogeographic origins. Entomologica Scandinavica, 22, 97–122. https://doi.org/10.1163/187631291X00336
- Borkent, A. (2000) Biting midges (Ceratopogonidae: Diptera) from Lower Cretaceous Lebanese amber with a discussion of the diversity and patterns found in other ambers. In: Grimaldi, D. (Ed.), Studies on Fossils in Amber, with Particular Reference to the Cretaceous of New Jersey. Backhuys Publishers, Leiden, pp. 355–451.
- Borkent, A. (2014) The pupae of the biting midges of the World (Diptera: Ceratopogonidae), with a generic key and analysis of the phylogenetic relationships between genera. Zootaxa, 387 (1)9, 1–327. https://doi.org/10.11646/zootaxa.3879.1.1
- Borkent, A. (2017) Ceratopogonidae (Biting Midges). 34. In: Kirk-Spriggs, A.H. & Sinclair, B.J. (Eds.), Manual of Afrotropical Diptera. Vol. 2. Nematocerous Diptera and lower Brachycera. Suricata 5. South African National Biodiversity Institute, Pretoria, pp. 733–812.
- Borkent, A. (2024) The Phylogeny of the genera of biting midges (Diptera: Ceratopogonidae) of the World. Zootaxa, 5438 (1), 1–274. [monograph] https://doi.org/10.11646/zootaxa.5438.1.1
- Borkent, A. & Brown, B.V. (2015) How to inventory tropical flies (Diptera)—one of the megadiverse orders of insects. Zootaxa, 3949 (3), 301–322. https://doi.org/10.11646/zootaxa.3949.3.1
- Borkent, A., Brown, B.V., Borkent, A., Adler, P.H., Amorim, D.S. de, Barber, K., Bickel, D., Boucher, S., Brooks, S.E., Burger, J., Burington, Z.L., Capellari, R.S., Costa, D.N.R., Cumming, J.M., Curler, G., Dick, C.W., Epler, J.H., Fisher, E., Gaimari, S.D., Gelhaus, J., Grimaldi, D.A., Hash, J., Hauser, M., Hippa, H., Ibáñez-Bernal, S., Jaschhof, M., Kameneva, E.P., Kerr, P.H., Korneyev, V., Korytkowski, C.A., Kung, G.A., Kvifte, G.M., Lonsdale, O., Marshall, S.A., Mathis, W., Michelsen, V., Naglis, S., Norrbom, A.L., Paiero, S., Pape, T., Pereira-Colavite, A., Pollet, M., Rochefort, S., Rung, A., Runyon, J.B., Savage, J., Silva, V.C., Sinclair, B.J., Skevington, J.H., Stireman, J.O. III, Swann, J., Vilkamaa, P., Wheeler, T., Whitworth, T., Wong, M., Wood, D.M., Woodley, N., Yau, T., Zavortink, T.J. & Zumbado, M.A. (2018) Remarkable fly (Diptera) diversity in a patch of Costa Rican cloud forest: Why inventory is a vital science. Zootaxa, 4402 (1), 53–90. https://doi.org/10.11646/zootaxa.4402.1.3
- Borkent, A. & Dominiak, P. (2020) Catalog of the biting midges of the World (Diptera: Ceratopogonidae). Zootaxa, 4787 (1), 1–377. https://doi.org/10.11646/zootaxa.4787.1.1
- Borkent, A., Dominiak, P. & Díaz, F. (2022) An update and errata for the catalog of the biting midges of the World (Diptera: Ceratopogonidae). Zootaxa, 5120, 53–64. https://doi.org/10.11646/zootaxa.5120.1.3
- Borkent, A. & Grogan, W.L. (1995) A revision of the genus Ceratopogon Meigen with a discussion of phylogenetic relationships, zoogeography and bionomic divergence (Diptera: Ceratopogonidae). Memoirs of the Entomological Society of Washington, 15, 1–198.
- Borkent, A. & Spinelli, G.R (2007) Neotropical Ceratopogonidae (Diptera: Insecta). In: Adis, J., Arias, J.R, Rueda-Delgado, G. & Wantzen, K.M (Eds.), Aquatic Biodiversity in Latin America (ABLA). Vol. 4. Pensoft, Sofia-Moscow, 198 pp.
- Brown, B.V. 2005. Malaise trap catches and the crisis in Neotropical Dipterology. American Entomologist, 51, 180–183. https://doi.org/10.1093/ae/51.3.180
- Brown, B.V., Borkent, A., Adler, P.H., Amorim, D.S. de, Barber, K., Bickel, D., Boucher, S., Brooks, S.E., Burger, J., Burington, Z.L., Capellari, R.S., Costa, D.N.R., Cumming, J.M., Curler, G., Dick, C.W., Epler, J.H., Fisher, E., Gaimari, S.D., Gelhaus, J., Grimaldi, D.A., Hash, J., Hauser, M., Hippa, H., Ibáñez-Bernal, S., Jaschhof, M., Kameneva, E.P., Kerr, P.H., Korneyev, V., Korytkowski, C.A., Kung, G.A., Kvifte, G.M., Lonsdale, O., Marshall, S.A., Mathis, W., Michelsen, V., Naglis, S., Norrbom, A.L., Paiero, S., Pape, T., Pereira-Colavite, A., Pollet, M., Rochefort, S., Rung, A., Runyon, J.B., Savage, J., Silva, V.C., Sinclair, B.J., Skevington, J.H., Stireman, J.O. III, Swann, J., Thompson, F.C., Vilkamaa, P., Wheeler, T., Whitworth, T., Wong, M., Wood, D.M., Woodley, N., Yau, T., Zavortink, T.J. & Zumbado, M.A. (2018) Comprehensive inventory of true flies (Diptera) at a tropical site. Communications Biology, 1 (21), 1–8. https://doi.org/10.1038/s42003-018-0022-x
- Campos, R.E., Spinelli, G.R. & Mogi, M. (2011) Culicidae and Ceratopogonidae inhabiting phytotelmata in Iguazú National Park, Misiones province, subtropical Argentina. Revista de la Sociedad Entomológica Argentina, 70, 111–118.
- Caruso, V., Hartop, E., Chimeno, C., Noori, S., Srivathsan, A., Haas, M., Lee, L., Meier, R. & Whitmore, D. (2024) An integrative framework for dark taxa biodiversity assessment at scale: A case study using Megaselia (Diptera, Phoridae). Insect Conservation and Diversity, 2024, 1–20. https://doi.org/10.1111/icad.12762
- Chandler, P.J. (2023) An update of the 1998 Checklist of Diptera of the British Isles. Updated 31 October 2023. Dipterists Forum. Available from: https://www.dipterists.org.uk (accessed 9 October 2024)
- Chatterjee, S., Brahma, S. & Hazra, N. (2018) Seasonal abundance of Culicoides Latreille and Dasyhelea Kieffer (Diptera: Ceratopogonidae) in an agricultural farm, West Bengal, India. Environment and Ecology, 37, 149–155. [2019]
- Coope, G.R. (2010) Coleopteran faunas as indicators of interglacial climates in central and southern England. Quaternary Science Reviews, 29, 1507–1514. https://doi.org/10.1016/j.quascirev.2009.12.017
- Diarra, M., Fall, M., Lancelot, R., Diop, A., Fall, A.G., Dicko, A., Seck, M.T., Garros, C., Allene, X., Rakotoarivony, I. & Bakhoum, M.T. (2015) Modelling the abundances of two major Culicoides (Diptera: Ceratopogonidae) species in the Niayes area of Senegal. PLoS One, 10 (6), e0131021. https://doi.org/10.1371/journal.pone.0131021
- Dipleou, O.O. (1976) Studies of Culicoides species of Nigeria. II. Species collected around wild animals at Ibadan. Veterinary Parasitology, 1, 257–263. https://doi.org/10.1016/0304-4017(76)90098-4
- Elbers, A.R.W. & Meiswinkel, R. (2014) Culicoides (Diptera: Ceratopogonidae) host preferences and biting rates in the Netherlands: Comparing cattle, sheep and the black-light suction trap. Veterinary Parasitology, 205, 330–337. https://doi.org/10.1016/j.vetpar.2014.06.004
- Elias, S.A. (1994) Quaternary insects and their environments. Smithsonian Institution Press, Washington and London, xiii + 284 pp.
- Epler, J.H. (2017) An annotated preliminary list of the Chironomidae (Diptera) of Zurquí, Costa Rica. CHIRONOMUS Journal of Chironomidae Research, 30, 4–18. https://doi.org/10.5324/cjcr.v0i30.2240
- Fasbender, A. (2023) Revision of the New World Ceratoculicoides Wirth & Ratanaworabhan (Diptera, Ceratopogonidae, Ceratopogonini). European Journal of Taxonomy, 875, 159–202. https://doi.org/10.5852/ejt.2023.875.2147
- Forattini, O.P., Rabello, E.X. & Pattoli, D. (1958) Culicoides da Região Neotropical (Diptera, Ceratopogonidae). II - Observações sôbre biologia em condições naturais. Arquivos da Faculdade de Higiene e Saúde Pública da Universidade de São Paulo, 12 (1), 1–52. https://doi.org/10.11606/issn.2358-792X.v12i1p1-52
- Grimaldi, D.A. & Richenbacher, C. (2023) Exceptional species diversity of Drosophilidae (Diptera) in a Neotropical forest. American Museum Novitates, 3997, 1–28. https://doi.org/10.1206/3997.1
- Halffter, G. (1987) Biogeography of the montane entomofauna of Mexico and Central America. Annual Review of Entomology, 32, 95–114. https://doi.org/10.1146/annurev.en.32.010187.000523
- Harsha, R., Mazumdar, S.M. & Mazumdar, A. (2020) Abundance, diversity and temporal activity of adult Culicoides spp. associated with cattle in West Bengal, India. Medical and Veterinary Entomology, 34, 327–343. https://doi.org/10.1111/mve.12446
- Hartop, E., Srivathsan, A., Ronquist, F. & Meier, R. (2022) Towards large-scale integrative taxonomy (LIT): resolving the data conundrum for dark taxa. Systematic Biology, 71, 1404–1422. https://doi.org/10.1093/sysbio/syac033
- Hartop, E., Lee, L., Srivathsan, A., Jones, M., Peña-Aguilera, P., Ovaskainen, O. & Meier, R. (2024) Resolving biology’s dark matter: species richness, spatiotemporal distribution, and community composition of a dark taxon. BioRxiv, 2024-05. [published online]
- https://doi.org/10.1101/2024.05.07.592951
- Havelka, P. (1976) Ceratopogoniden-Emergenz am Breitenbach und am Rohrwiesenbach (1971–1972). Archiv für Hydrobiologie, Supplment 50, 54–95.
- Havelka, P. & Caspers, N. (1981) Die Gnitzen (Diptera, Nematocera, Ceratopogonidae) eines kleinen Waldbaches bei Bonn. Decheniana Beihefte, 25, 1–100.
- Hebert, P.D.N., Ratnasingham, S., Zakharov, E.V., Telfer, A.C., Levesque-Beaudin, V., Milton, M.A., Pedersen, S., Jannetta, P. & de Waard, J.R. (2016) Counting animal species with DNA barcodes: Canadian insects. Philosophical Transactions of the Royal Society B, 371 (1702), 20150333. https://doi.org/10.1098/rstb.2015.0333
- Hebert, P.D., Braukmann, T.W., Prosser, S.W., Ratnasingham, S., DeWaard, J.R., Ivanova, N.V., Janzen, D.H., Hallwachs, W., Naik, S., Sones, J.E. & Zakharov, E.V. (2018) A Sequel to Sanger: amplicon sequencing that scales. BMC genomics, 19, 1–14. https://doi.org/10.1186/s12864-018-4611-3
- Heller, K., Köhler, A., Menzel, F., Olsen, K.M. & Gammelmo, Ø. (2016) Two formerly unrecognized species of Sciaridae (Diptera) revealed by DNA barcoding. Norwegian Journal of Entomology, 63, 96–115.
- Hsieh, T., Ma, K. & Chaom A. (2024) iNEXT: Interpolation and Extrapolation for Species Diversity. R package Version 3.0.1. Available from: http://chao.stat.nthu.edu.tw/wordpress/software_download/ (accessed 18 July 2024)
- Huerta, H. & Borkent, A. (2005) A new species and first record of Ceratoculicoides Wirth and Ratanaworabhan from the Neotropical Region and new species and records of Brachypogon Kieffer from Mexico (Diptera: Ceratopogonidae). Folia Entomologica Mexicana, 44 (Supplement 1), 111–119.
- Janzen, D.H., Hallwachs, W. (2019) How a tropical country can DNA barcode itself. iBOL Barcode Bulletin, 2 Octtober 2019, 1–5. https://doi.org/10.21083/ibol.v9i1.5526
- Janzen, D.H., Hallwachs, W., Pereira, G., Blanco, R., Masis, A., Chavarria, M.M., Chavarria, F., Guadamuz, A., Araya, M., Smith, M.A. & Valerio, J. (2020) Using DNA-barcoded Malaise trap samples to measure impact of a geothermal energy project on the biodiversity of a Costa Rican old-growth rain forest. Genome, 63 (9), 407–436. https://doi.org/10.1139/gen-2020-0002
- Kirk-Spriggs, A.H. & Muller, B.S. (2017). 9. Biogeography of Diptera. In: Kirk-Spriggs, A.H. & Sinclair, B.J. (Eds.), Manual of Afrotropical Diptera. Vol. 1. Nematocerous Diptera and lower Brachycera. Suricata 5. South African National Biodiversity Institute, Pretoria, pp. 203–238
- Kitching, R.L., Bickel, D., Creagh, A.C., Hurley. K. & Symonds, C. (2004) The biodiversity of Diptera in Old World rain forest surveys: a comparative faunistic analysis. Journal of Biogeography, 31, 1185–1200. https://doi.org/10.1111/j.1365-2699.2004.01096.x
- Knausenberger, W.I. (1987) Contributions to the autecology and ecosystematics of immature Ceratopogonidae (Diptera), with emphasis on the tribes Heteromyiini and Sphaeromiini in the Middle Atlantic United States. Ph.D. Dissertation, Virginia Polytechnic Institute and State University, Blacksburg, Virginia, xxix + 729 pp.
- Kolbert, E. (2014) The sixth extinction: An unnatural history. Henry Holt and Company, New York, New York, 336 pp.
- Lane, J. (1946) Duas espécies novas de Ceratopogonídeos Brasileiros (Diptera Ceratopogonidae (Heleidae)). Livro de Homenagem a R.F. d’Almeida, 22, 219–225. https://doi.org/10.11606/issn.2358-792X.v1i2p225-240
- Lin, X., Stur, E., Ekrem, T. (2015) Exploring genetic divergence in a species-rich insect genus using 2790 DNA barcodes. PLoS ONE, 10 (9), e0138993. https://doi.org/10.1371/journal.pone.0138993
- Masteller, E.C. & Wagner, R. (1984) The impact of sewage effluent on the occurrence of Psychodidae (Diptera) in a stream. Freshwater Invertebrate Biology, 3 (2), 98–104. https://doi.org/10.2307/1467098
- Meier, R., Blaimer, B. B., Buenaventura, E., Hartop, E., von Rintelen, T., Srivathsan, A. & Yeo, D. (2022) A re-analysis of the data in Sharkey et al.’s (2021) minimalist revision reveals that BINs do not deserve names, but BOLD Systems needs a stronger commitment to open science. Cladistics, 38 (2), 264–275. https://doi.org/10.1111/cla.12489
- Meiswinkel, R., Venter, G.J. & Nevill, E.M. (2004) Vectors: Culicoides spp. In: Coetzer, J.A.W. & Tustin, R. (Eds.), Infectious Diseases of Livestock. 2nd Edition. Oxford University Press, Cape Town, pp. 93–136.
- Paulson, D., Schorr, M., Abbott, J., Bota-Sierra, C., Deliry, C., Dijkstra, K.-D. & Lozano, F. (Coordinators) (2024) World Odonata List. OdonataCentral, University of Alabama. Available from: https://www.odonatacentral.org/app/#/wol/ (accessed 24 June 2024)
- Qian, H., Zhang, J. & Zhao, J. (2022). How many known vascular plant species are there in the world? An integration of multiple global plant databases. Biodiversity Science, 30 (7), 22254. https://doi.org/10.17520/biods.2022254
- Ratnasingham S. & Hebert P.D.N. (2013) A DNA-Based registry for all animal species: the Barcode Index Number (BIN) System. PLoS ONE, 8 (8), e66213.
- https://doi.org/10.1371/journal.pone.0066213
- Ratnasingham, S., Wei, C., Chan, D., Agda, J., Agda, J., Ballesteros-Mejia, L., Boutou, H.A., El Bastami, Z.M., Ma, E., Manjunath, R. & Rea, D. (2024) BOLD v4: A centralized bioinformatics platform for DNA-Based biodiversity data. In: DNA Barcoding: Methods and Protocols. Springer USA, New York, New York, pp. 403–441. https://doi.org/10.1007/978-1-0716-3581-0_26
- Rich, P.V. & Rich, T.H. (1983). The Central American dispersal route: biotic history and paleogeography. In: Costa Rican natural history. University of Chicago Press, Chicago, Illinois, pp. 12–34.
- Ronderos, M.M., Spinelli, G.R & Díaz, F. (2004) Description of larva and redescription of pupa and adult of Palpomyia guarani. Revista de la Sociedad Entomológica Argentina, 63, 45–54.
- Santarém, M.C.A. & Felippe-Bauer, M.L. (2024). Analysis of Brazilian Ceratopogonidae (Diptera: Culicomorpha) species diversity and knowledge assessment. Zoologia, Curitiba, 41, e23066. https://doi.org/10.1590/S1984-4689.v41.e23066
- Santarém, M.C.A., Borkent, A., Spinelli, G.R. & Felippe-Bauer, M.L. (2018) New Neotropical species of Downeshelea Wirth and Grogan and redescription of D. multilineata (Lutz) (Diptera: Ceratopogonidae). Journal of Natural History, 52, 509–540. https://doi.org/10.1080/00222933.2018.1437231
- Santarém, M.C.A., Borkent, A. & Felippe-Bauer, M.L. (2020) Taxonomic revision of Neotropical Downeshelea Wirth and Grogan predaceous midges (Diptera: Ceratopogonidae). Insects, 11, 1–94. https://doi.org/10.3390/insects11010009
- Savage, J.M. (2002) The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. University of Chicago press, Chicago, Illinois, 934 pp.
- Scheffer, E.G., Venter, G.J., Labuschagne, K., Page, P.C., Mullens, B.A., MacLachlan, N.J., Osterrieder, N. & Guthrie, A.J. (2012) Comparison of two trapping methods for Culicoides biting midges and determination of African horse sickness virus prevalence in midge populations at Onderstepoort, South Africa. Veterinary Parasitology, 185 (2–4), 265–273. https://doi.org/10.1016/j.vetpar.2011.09.037
- Semken, H.A., Miller, B.B. & Stevens, J.B. (1964) Late Wisconsin woodland musk oxen in association with pollen and invertebrates from Michigan. Journal of Paleontology, 38, 823–835.
- Sharkey, M.J., Janzen, D.H., Hallwachs, W., Chapman, E.G., Smith, M.A., Dapkey, T., Brown, A., Ratnasingham, S., Naik, S., Manjunath, R. & Perez, K. (2021) Minimalist revision and description of 403 new species in 11 subfamilies of Costa Rican braconid parasitoid wasps, including host records for 219 species. ZooKeys, 1013, 1. https://doi.org/10.3897/zookeys.1013.55600
- Spinelli, G.R. & Borkent, A. (2004) New species of Central American Culicoides Latreille (Diptera: Ceratopogonidae) with a synopsis of species from Costa Rica. Proceedings of the Entomological Society of Washington, 106, 361–395.
- Spinelli, G.R. & Wirth, W.W. (1990) Neotropical predaceous midges of the genus Bezzia (Diptera: Ceratopogonidae) Part III. The gibbera group of species. Insecta Mundi, 4, 11–32.
- Spinelli, G.R. & Wirth, W.W. (1991) The Neotropical predaceous midges of the genus Bezzia (Diptera: Ceratopogonidae) Part IV. The dentifemur and venustula groups. Insecta Mundi, 5, 1–17.
- Srivathsan, A., Ang, Y., Heraty, J.M., Hwang, W.S., Jusoh, W.F., Kutty, S.N., Puniamoorthy, J., Yeo, D., Roslin, T. & Meier, R. (2023) Convergence of dominance and neglect in flying insect diversity. Nature ecology & evolution, 7 (7), 1012–1021. https://doi.org/10.1038/s41559-023-02066-0
- Steyn, D.G., Moisseeva, N., Harari, O. & Welch, W.J. (2016) Temporal and spatial variability of annual rainfall patterns in Guanacaste, Costa Rica. Technical Report, The University of British Columbia, 2016. Available from: https://hdl.handle.net/2429/59971 (accessed 23 July 2024)
- Stork, N.E. (1991) The composition of the arthropod fauna of Bornean lowland rain forest trees. Journal of Tropical Ecology, 7, 161–180. https://doi.org/10.1017/S0266467400005319
- Szadziewski, R., Borkent, A. & Dominiak, P. (2013) Ceratopogonidae. In: de Jong, H. & Pape, T. (Eds.), Fauna Europaea: Diptera: Nematocera. Fauna Europaea. Version 2.6.2. Available from: http://www.faunaeur.org (accessed 22 April 2023)
- Tilki, N. & Dik, B. (2003) Farklı renkteki ışıkların Culicoides (Diptera: Ceratopogonidae) türlerinin yakalanmaları üzerine etkileri. Türkiye Parazitoloji Dergisi, 27 (2), 144–147.
- Venter, G.J., Boikanyo, S.N. & De Beer, C.J. (2018) The efficiency of light‐emitting diode suction traps for the collection of South African livestock‐associated Culicoides species. Medical and Veterinary Entomology, 32 (4), 509–514. https://doi.org/10.1111/mve.12313
- Viennet, E., Garros, C., Lancelot, R., Allène, X., Gardès, L., Rakotoarivony, I., Crochet, D., Delécolle, J.C., Moulia, C., Baldet, T. & Balenghien, T. (2011) Assessment of vector/host contact: comparison of animal-baited traps and UV-light/suction trap for collecting Culicoides biting midges (Diptera: Ceratopogonidae), vectors of Orbiviruses. Parasites & Vectors, 4, 1–12. https://doi.org/10.1186/1756-3305-4-119
- Watson, C.N. Jr. & Heyn, M.W. (1993) A preliminary survey of the Chironomidae (Diptera) of Costa Rica, with emphasis on the lotic fauna. Netherlands Journal of Aquatic Ecology, 26, 257–262. [1992] https://doi.org/10.1007/BF02255249
- Wilkerson, R.C., Linton, Y.-M. & Strickman, D. (2021) Mosquitoes of the World. Vols. 1 & 2. John Hopkins University Press, Baltimore, Maryland, 1308 pp.
- Wirth, W.W. & Blanton, F.S. (1959) Biting midges of the genus Culicoides from Panama (Diptera: Heleidae). Proceedings of the United States National Museum, 109, 237–482. https://doi.org/10.5479/si.00963801.109-3415.237
- Wirth, W.W. & Grogan, W.L. (1983) The Nearctic species of the Bezzia bivittata group (Diptera: Ceratopogonidae). Proceedings of the Biological Society of Washington, 96, 489–523.
- Wirth, W.W. & Hubert, A.A. (1960) Ceratopogonidae (Diptera) reared from cacti, with a review of the copiosus group of Culicoides. Annals of the Entomological Society of America, 53, 639–658. https://doi.org/10.1093/aesa/53.5.639
- Wirth, W.W. & Lee, D.J. (1967) New species of Culicoides from high altitudes in the Colombian Andes (Diptera: Ceratopogonidae). Proceedings of the United States National Museum, 124, 1–22. https://doi.org/10.5479/si.00963801.124-3626.1