Abstract
Hyperparasitism of ectoparasitic water mite larvae on mosquitoes is still a neglected relationship and was investigated only in a few studies. We analysed 2313 female mosquitoes from six different sampling localities with regard to their degree of parasitism with water mite larvae. In total, we found 38 mosquito individuals parasitized by 93 water mite larvae, ranging from 1 to 12 larvae per mosquito. Water mite larvae detected are members of the two species Parathyas cf. barbigera (n = 92) and Arrenurus cf. globator (n = 1). Out of the analysed mosquitoes, individuals out of the species Aedes vexans, Anopheles claviger, Ochlerotatus communis, the Ochlerotatus cantans/annulipes group, Ochlerotatus cataphylla and Ochlerotatus sticticus were tested to be parasitized by water mite larvae. The highest prevalence was found within the species Oc. cataphylla (28.6 %) and Oc. cantans/annulipes (21.7 %). No water mite larvae were found, e.g. on individuals of Aedes cinereus, Coquillettidia richiardii, the Culex pipiens/torrentium group, Ochlerotatus caspius, Ochlerotatus dorsalis or Ochlerotatus punctor. All of the attachment sites were located between the neck and abdomen with the ventral thorax site being the most frequent one.
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References
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search program. Nucleic Acids Res 25:3389–3402
Avšič-Županc T (2013) Mosquito-borne diseases—a new threat to Europe? Clin Microbiol Infect 19:683–684. doi:10.1111/1469-0691.12215
Becker N, Petrić D, Zgomba M, Boase C, Dahl C, Lane J, Kaiser A (2010) Mosquitoes and their control. Kluwer Academic / Plenum Publishers, New York
Becker N, Krüger A, Kuhn C, Plenge-Bönig A, Thomas SM, Schmidt-Chanasit J, Tannich E (2014) Stechmücken als Überträger exotischer Krankheitserreger in Deutschland. Bundesgesundheitsblatt 57:531–540
Böttger K (1962) Zur Biologie und Ethologie der einheimischen Wassermilben Arrenurus (Megaluracarus) globator (Muell.), 1776, Piona nodata nodata (Muell.), 1776 und Eylais infundibulifera meridionalis (Thon), 1899 (Hydrachnellae, Acari). Zool Jb Syst 89:501–584
Böttger K, Martin P (2003) On the morphology and parasitism of Arrenurus globator (O. F. Müller, 1776) (Hydrachnidia, Acari) a water mite with an unusually extensive host spectrum. Acarologia 43:49–57
Davids C, Di Sabatino A, Gerecke R, Gledhill T, Smit H, van der Hammen H (2007) 7. Acari: Hydrachnidia. In: Gerecke R (ed) Chelicerata: Araneae, Acari I; Süßwasserfauna von Mitteleuropa 7/2-1, 1st edn. Elsevier Spektrum Akademischer Verlag, München, pp 262–280
DeGeer C (1778) Mémoires pour server à l’histoire des Insectes. Vol 7, Grefing & Hesselberg, Stockholm
Di Sabatino A, Martin P, Gerecke R, Cicolani B (2002) Hydrachnidia (water mites). In: Rundle SD, Robertson AL, Schmid-Araya JM (eds) Freshwater Meiofauna: Biology and Ecology. Backhuys Publishers, Leiden, The Netherlands, pp 105–133
Di Sabatino A, Gerecke R, Gledhill T, Smit H (2010) Süßwasserfauna von Mitteleuropa Bd.7/2-2 Chelicerata: Acari II, 234 pp
Esteva L, Rivas G, Yang HM (2006) Modelling parasitism and predation of mosquitoes by water mites. J Math Biol 53:540–555
Gerecke R (1994) Ein Bestimmungsschlüssel für die aus der Westpalaearktis bekannten Gattungen der Hydrachnellae mit einer einführenden Übersicht über die im Wasser vorkommenden Milben. Lauterbornia 18:1–84
Gerecke R, Lehmann EO (2005) Towards a long-term monitoring of Central European water mite faunas (Acari: Hydrachnidia and Halacaridae)—considerations on the background of data from 1900 to 2000. Limnologica 35:45–51
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hochberg ME, Ives AR (2000) Parasitoid population biology. Princeton University Press, New Jersey
Ivanova NV, Dewaard JR, Hebert PND (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes. doi:10.1111/j.1471-8286.2006.01428.x
Jalil M, Mitchell R (1972) Parasitism of mosquitoes by water mites. J Med Entomol 9:305–311
Jöst H, Bialonski A, Storch V, Günther S, Becker N, Schmidt-Chanasit J (2010) Isolation and phylogenetic analysis of Sindbis viruses from mosquitoes in Germany. J Clin Microbiol 48:1900–1903
Jöst H, Bialonski A, Schmetz C, Günther S, Becker N, Schmidt-Chanasit J (2011a) Isolation and phylogenetic analysis of Batai virus, Germany. Am J Trop Med Hyg 84:241–243
Jöst H, Bialonski A, Maus D, Sambri V, Eiden M, Groschup MH, Günther S, Becker N, Schmidt-Chanasit J (2011b) Isolation of usutu virus in Germany. Am J Trop Med Hyg 85:551–553
Kraus O (1984) Hoyers Gemisch statt Polyvinyl-Lactophenol. Mikrokosmos 73:54–55
Kumar NP, Rajavel AR, Natarajan R, Jambulingam P (2007) DNA barcodes can distinguish species of Indian mosquitoes (Diptera: Culicidae). J Med Entomol 44:1–7
Lanciani CA (1979) Water mite-induced mortality in a natural population of the mosquito Anopheles crucians (Diptera: Culicidae). J Med Entomol 15:529–532
Martin P (2004) Specificity of attachment sites of larval water mites (Hydrachnidia, Acari) on their insect hosts (Chironomidae, Diptera)—evidence from some stream-living species. Exp Appl Acarol 34:95–112
Martin P (2008) Wassermilben (Hydrachnidia, Acari) und Insekten: Ein Überblick über eine selten betrachtete Beziehung. Entomol Heute 20:45–75
Martin P, Stur E (2006) Parasite-host associations and life cycles of spring-living water mites (Hydrachnidia, Acari) from Luxembourg. Hydrobiologia 573:17–37
McBride CS, Baier F, Omondi AB, Spitzer SA, Lutomiah J, Sang R, Ignell R, Vosshall LB (2014) Evolution of mosquito preference for humans linked to an odorant receptor. Nature 515:222–227
McCallister GL, Mullins GR, McCallister ZG (1999) Acarine parasites of mosquitoes in west central Colorado. Proc Annu Meet Utah Mosq Abatement Assoc 52:28–30
Meyer E (1985) Der Entwicklungszyklus von Hydrodroma despicies (O. F. Müller 1776) (Acari: Hydromidae). Arch Hydrobiol Suppl 198:321–453
Milne MA, Townsend VJ Jr, Smelser P, Felgenhauer BE, Moore MK, Smyth FJ (2009) Larval aquatic and terrestrial mites infesting a temperate assemblage of mosquitoes. Exp Appl Acarol 47:19–33
Mohrig W (1969) Die Culiciden Deutschlands. Parasitologische Schriftenreihe 18. Gustav Fischer Verlag, Jena
Mullen GR (1974) Acarine parasites of mosquitoes. II. Illustrated larval key to the families and genera of mites reportedly parasitic on mosquitoes. Mosq News 34:183–195
Mullen GR (1977) Acarine parasites of mosquitoes. IV. Taxonomy, life history and behavior of Thyas barbigera and Thyasides sphagnorum (Hydrachnellae: Thyasidae). J Med Entomol 13:475–485
Münchberg P (1935) Über die bisher bei einigen Nematocerenfamilien (Culicidae, Chironomidae, Tipulidae) beobachteten ektoparasitären Hydracarinenlarven. Z Morphol Ökol Tiere 29:720–749
Münchberg P (1936) Zur Kenntnis des Larvenparasitismus der Thyasinae (Hydracarina), zugleich ein Beitrag über Schmarotzer der Limnobiinae (Diptera). Int Rev Hydrobiol 33:313–326
Münchberg P (1954) Zur Kenntnis der an Culiciden (Diptera) schmarotzenden Arrenurus-Larven (Hydracarina), sowie über die Bedeutung dieser Parasiten für Wirt und Mensch. Parasitol Res 16:298–312
Münchberg P (1956) Über die an Limoniidae und Tipulidae parasitierenden Milbenlarven. Parasitol Res 17:330–338
Nielsen BO (1998) The water mite Thyas barbigera Viets (Hydrachnellae: Thyasidae) parasitizing mosquitoes. Eur Mosq Bull 2:10–12
Poulin R, Morand S (2000) The diversity of parasites. Q Rev Biol 75:277–293
Proctor HC, Smith IM, Cook DR, Smith BP (2015) Chapter 25—Subphylum Chelicerata, Class Arachnida. In: Thorp J, Rogers DS (eds) Thorp and Covich’s Freshwater Invertebrates, 4th edn. Academic, Boston, pp 599–660
Rack G (1976) Milben (Acarina) von europäischen Limoniinen (Diptera, Nematocera). Mitt Hamburg Zool Mus Inst 73:63–85
Rack G (1977) Weitere Untersuchungen über Milben (Acarina) an Nematocera (Diptera). Acarologia 19:20–25
Rajendran R, Prasad RS (1992) Influence of mite infestation on the longevity and fecundity of the mosquito Mansonia uniformis (Diptera: Insecta) under laboratory conditions. J Biosci 17:35–40
Reinert JF (2000) New classification for the composite genus Aedes (Diptera: Culicidae: Aedini), elevation of subgenus Ochlerotatus to generic rank, reclassification of the other subgenera, and notes on certain subgenera and species. J Am Mosq Control Assoc 16:175–188
Reinhardt K (1996) Negative effects of Arrenurus water mites on the flight distances of the damselfly Nehalennia speciosa (Odonata: Coenagrionidae). Aquat Insects 18:233–240
Sánchez MI, Coccia C, Valdecasas AG, Boyero L, Green AJ (2005) Parasitism by water mites in native and exotic Corixidae: Are mites limiting the invasion of the water boatman Trichocorixa verticalis (Fieber, 1851)? J Insect Conserv. doi:10.1007/s10841-015-9764-7
Sharma SN, Prasad RN (1992) Water mite (Arrenurus sp.) parasitizing mosquitoes in district Shahjahanpur, U. P. Indian J Malariol 29:255–258
Smith BP (1988) Host-parasite interaction and impact of larval water mites on insects. Annu Rev Entomol 33:487–507
Smith BP, Laughland LA (1990) Stimuli inducing detachment of larval Arrenurus danbyensis (Hydrachnidia: Arrenuridae) from adult Coquillettidia perturbans (Diptera: Culicidae). Exp Appl Acarol 9:51–62
Smith IM, Oliver DR (1986) Review of parasitic associations of larval water mites (Acari: Parasitengona: Hydrachnida) with insect hosts. Can Entomol 118:407–472
Smith IM, Cook DR, Smith BP (2009) Water mites (Hydrachnida) and other arachnids. In: Thorp JH, Covich AP (eds) Ecology and classification of North American freshwater invertebrates, 3rd edn. Academic, San Diego, pp 485–585
Snell AE, Heath ACG (2006) Parasitism of mosquitoes (Diptera: Culicidae) by larvae of Arrenuridae and Microtrombidiidae (Acari: Parasitengona) in the Wellignton region, New Zealand. N Z J Zool 33:9–15
Spurrier MF (1998) Mite parasitism of mosquitoes in Central Wyoming. Great Basin Nat 58:184–187
Stechmann D-H (1978) Eiablage, Parasitismus und postparasitische Entwicklung von Arrenurus-Arten (Hydrachnellae, Acari). Parasitol Res 57:169–188
Stechmann D-H (1980) Zum Wirtskreis syntopischer Arrenurus-Arten (Hydrachnellae, Acari) mit parasitischer Entwicklung an Nematocera (Diptera). Parasitol Res 62:267–283
Ullrich F (1978) Biologisch-ökologische Studien an den Larven rheophiler Wassermilben (Hydrachnellae, Acari), Schlitzer Produktionsbiologische Studien (29). Arch Hydrobiol Suppl 54:189–255
Ventim R, Ramos JA, Osório H, Lopes RJ, Pérez-Tris J, Mendes L (2012) Avian malaria infections in western European mosquitoes. Parasitol Res 111:637–645
Wainstein BA (1980) Opredelitel lichinok vodjanych kleshchei. Inst Biol Vnutrenn Vod, Nauka, 238pp
WHO (2014a) Vector-borne diseases, Malaria. http://www.who.int/mediacentre/factsheets/fs387/en/index1.html. Accessed 10 March 2015
WHO (2014b) Vector-borne diseases, Dengue. http://www.who.int/mediacentre/factsheets/fs387/en/index2.html. Accessed 10 March 2015
Wiliams CR, Proctor HC (2002) Parasitism of mosquitoes (Diptera: Culicidae) by larval mites (Acari: Parasitengona) in Adelaide, South Australia. Aust J Etomol 41:161–163
Acknowledgments
This research was funded by the ERA-Net BiodivERsA, with the national funders German Research Foundation (DFG KL 2087/6-1), Austrian Science Fund (FWF I-1437) and The French National Research Agency (ANR-13-EBID-0007-01), part of the 2013 BiodivERsA call for research proposals, by the research funding programme “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research and the Arts, and by the Senate Competition Committee grant (SAW-2014-SGN-3) of the Leibniz Association.
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Werblow, A., Martin, P., Dörge, D.D. et al. Hyperparasitism of mosquitoes by water mite larvae. Parasitol Res 114, 2757–2765 (2015). https://doi.org/10.1007/s00436-015-4482-3
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DOI: https://doi.org/10.1007/s00436-015-4482-3