First record of mermithid parasitism in adult biting midges, Culicoides huffi (Diptera: Ceratopogonidae), collected from Southern Thailand, with ultrastructural and molecular characterization | Parasites & Vectors

  • Borkent A, Dominiak P. Catalog of the biting midges of the world (Diptera: Ceratopogonidae). Zootaxa. 2020;4787:1–377.

    Google Scholar 

  • Borkent A, Dominiak P, Daz F. An update and errata for the catalog of the biting midges of the world (Diptera: Ceratopogonidae). Zootaxa. 2022;5120:53–64.

    PubMed 

    Google Scholar 

  • Sick F, Beer M, Kampen H, Wernike K. Culicoides biting midges—underestimated vectors for arboviruses of public health and veterinary importance. Viruses. 2019;11:376.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mullens GR, Murphree CS. Biting midges (Ceratopogonidae). In: Mullen GR, Durden LA, editors. Medical and veterinary entomology. 3rd ed. San Diego: Academic Press; 2019. p. 213–36.

    Google Scholar 

  • Prasad G, Bhatnagar P. Culicoides: biology and transmission of viruses. V National Training Programme. Compendium of Acarines and Insects of Veterinary and Medical Importance. On Centre of Advanced Studies, Department of Parasitology, Veterinary College Bangalore; 2000. p. 34–8.

  • Santiago-Alarcon D, Palinauskas V, Schaefer HM. Diptera vectors of avian haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biol Rev Camb Philos Soc. 2012;87:928–64.

    PubMed 

    Google Scholar 

  • Svobodová M, Dolnik OV, Čepička I, Rádrová J. Biting midges (Ceratopogonidae) as vectors of avian trypanosomes. Parasit Vectors. 2017;10:224.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Bernotienė R, Iezhova TA, Bukauskaitė D, Chagas CRF, Kazak M, Valkiūnas G. Development of Trypanosoma everetti in Culicoides biting midges. Acta Trop. 2020;210:105555.

    PubMed 

    Google Scholar 

  • Pramual P, Khamluea S, Butlun P, Promdungdee A. Molecular detection of filarial nematode from Culicoides biting midges (Diptera: Ceratopogonidae) in northeastern Thailand. Trop Biomed. 2023;40:188–93.

    CAS 
    PubMed 

    Google Scholar 

  • Wirth WW, Hubert AA. The Culicoides of southeast Asia (Diptera Ceratopogonidae). Mem Am Entomol Inst. 1989;44:1–508.

    Google Scholar 

  • Fujisawa Y, Homat T, Thepparat A, Changbunjong T, Sutummaporn K, Kornmatitsuk S, et al. DNA barcode identification and molecular detection of bluetongue virus in Culicoides biting midges (Diptera: Ceratopogonidae) from western Thailand. Acta Trop. 2021;224:106147.

    CAS 
    PubMed 

    Google Scholar 

  • Pramual P, Jomkumsing P, Jumpato W, Bunauea S. Molecular detection of avian haemosporidian parasites in biting midges (Diptera: Ceratopogonidae) from Thailand. Acta Trop. 2021;224:106118.

    CAS 
    PubMed 

    Google Scholar 

  • Sunantaraporn S, Thepparat A, Phumee A, Sor-Suwan S, Boonserm R, Bellis G, et al. Culicoides Latreille (Diptera: Ceratopogonidae) as potential vectors for Leishmania martiniquensis and Trypanosoma sp. in northern Thailand. PLoS Negl Trop Dis. 2021;15:e0010014.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Ampol R, Somwang P, Khositharattanakool P, Promrangsee C, Pataradool T, Tepboonreung P, et al. Nanopore-based surveillance of Leishmania parasites in Culicoides Latrielle (Diptera: Ceratopogonidae) caught from the affected community and Tham Phra cave in Chiang Rai Province, the endemic area of leishmaniasis in Northern Thailand. Insects. 2024;15:327.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Promrangsee C, Sriswasdi S, Sunantaraporn S, Savigamin C, Pataradool T, Sricharoensuk C, et al. Seasonal dynamics, Leishmania diversity, and nanopore-based metabarcoding of blood meal origins in Culicoides spp. in the newly emerging focus of leishmaniasis in Northern Thailand. Parasit Vectors. 2024;17:400.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Songumpai N, Promrangsee C, Noopetch P, Siriyasatien P, Preativatanyou K. First evidence of co-circulation of emerging Leishmania martiniquensis, Leishmania orientalis, and Crithidia sp. in Culicoides biting midges (Diptera: Ceratopogonidae), the putative vectors for autochthonous transmission in Southern Thailand. Trop Med Infect Dis. 2022;7:379.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kaewmee S, Mano C, Phanitchakun T, Ampol R, Yasanga T, Pattanawong U, et al. Natural infection with Leishmania (Mundinia) martiniquensis supports Culicoides peregrinus (Diptera: Ceratopogonidae) as a potential vector of leishmaniasis and characterization of a Crithidia sp. isolated from the midges. Front Microbiol. 2023;14:1235254.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Seblova V, Sadlova J, Vojtkova B, Votypka J, Carpenter S, Bates PA, et al. The biting midge Culicoides sonorensis (Diptera: Ceratopogonidae) is capable of developing late stage infections of Leishmania enriettii. PLoS Negl Trop Dis. 2015;9:e0004060.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Chanmol W, Jariyapan N, Somboon P, Bates MD, Bates PA. Development of Leishmania orientalis in the sand fly Lutzomyia longipalpis (Diptera: Psychodidae) and the biting midge Culicoides soronensis (Diptera: Ceratopogonidae). Acta Trop. 2019;199:105157.

    PubMed 

    Google Scholar 

  • Becvar T, Vojtkova B, Siriyasatien P, Votypka J, Modry D, Jahn P, et al. Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae). PLoS Pathog. 2021;17:e1009654.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mullens BA, Sarto I Monteys V, Przhiboro AA. Mermithid parasitism in Ceratopogonidae: a literature review and critical assessment of host impact and potential for biological control of Culicoides. Russ Entomol J. 2008;17:87–113.

    Google Scholar 

  • Platzer EG. Biological control of mosquitoes with mermithids. J Nematol. 1981;13:257–62.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Molloy DP. Mermithid parasitism of black flies (Diptera: Simuliidae). J Nematol. 1981;13:250–6.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Huang F, Srisuka W, Aupalee K, Streit A, Fukuda M, Pitasawat B, et al. Diversity of nematodes infecting the human-biting black fly species, Simulium nigrogilvum (Diptera: Simuliidae) in central Thailand. Acta Trop. 2021;224:106140.

    PubMed 

    Google Scholar 

  • Babu SR, Phani V, Meena PK, Chauhan K, Khan MR, Somvanshi VS. Report of a mermithid nematode infection Amyna axis, Chrysodeixis spp. and Spodoptera spp. from India. J Biol Control. 2019;33:217–21.

    CAS 

    Google Scholar 

  • Attard LM, Carreno RA, Paré JA, Peregrine AS, Dutton CJ, Mason TR. Mermithid nematode infection in a colony of blue-winged grasshoppers (Tropidacris collaris). J Zoo Wildl Med. 2008;39:488–92.

    PubMed 

    Google Scholar 

  • Lückmann J, Poinar GO Jr. First record of a Mermithidae (Nematoda) from the meloid beetle Meloe violaceus Marsham, 1802 (Coleoptera: Meloidae). Parasitol Res. 2003;90:82–3.

    PubMed 

    Google Scholar 

  • Tarla G, Poinar G, Tarla S. Hexamermis eurygasteri n. sp. (Nematoda: Mermithidae) parasitising the sunn pest Eurygaster integriceps Puton (Hemiptera: Scutelleridae) in Turkey. Syst Parasitol. 2011;79:195–200.

    PubMed 

    Google Scholar 

  • Tripodi AD, Strange JP. Rarely reported, widely distributed, and unexpectedly diverse: molecular characterization of mermithid nematodes (Nematoda: Mermithidae) infecting bumble bees (Hymenoptera: Apidae: Bombus) in the USA. Parasitology. 2018;145:1558–63.

    PubMed 

    Google Scholar 

  • Petersen JJ. Nematodes as biological control agents: part I. Mermithidae. Adv Parasitol. 1985;24:307–44.

    CAS 
    PubMed 

    Google Scholar 

  • Abagli AZ, Alavo TBC, Perez-Pacheco R, Platzer EG. Efficacy of the mermithid nematode, Romanomermis iyengari, for the biocontrol of Anopheles gambiae, the major malaria vector in sub-Saharan Africa. Parasit Vectors. 2019;12:253.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Abagli AZ, Alavo TBC. Biocontrol of Culex quinquefasciatus using the insect parasitic nematode, Romanomermis iyengari (Nematoda: Mermithidae). Trop Biomed. 2019;36:1003–13.

    CAS 
    PubMed 

    Google Scholar 

  • Muñoz-Muñoz F, Ramoneda J, Pagès N, Pujol N, Talavera S. Is the morphology of Culicoides intersexes parasitized by mermithid nematodes a parasite adaptation? A morphometric approach to Culicoides circumscriptus (Diptera: Ceratopogonidae). J Invertebr Pathol. 2016;135:1–9.

    PubMed 

    Google Scholar 

  • McKeever S, Brickle DS, Hagan DV. Mouthparts, antennae and genitalia of intersex Culicoides stellifer parasitized by mermithid nematodes. Med Vet Entomol. 1997;11:217–22.

    CAS 
    PubMed 

    Google Scholar 

  • Allahverdipour HH, Talaei-Hassanloui R, Karimi J, Wang Y, Rochlin I, Gaugler R. Behavior manipulation of mosquitoes by a mermithid nematode. J Invertebr Pathol. 2019;168:107273.

    CAS 
    PubMed 

    Google Scholar 

  • de Valdez MR. Parasitoid-induced behavioral alterations of Aedes aegypti mosquito larvae infected with mermithid nematodes (Nematoda: Mermithidae). J Vector Ecol. 2006;31:344–54.

    PubMed 

    Google Scholar 

  • Pramual P, Jomkumsing P, Piraonapicha K, Jumpato W. Integrative taxonomy uncovers a new Culicoides (Diptera: Ceratopogonidae) biting midge species from Thailand. Acta Trop. 2021;220:105941.

    CAS 
    PubMed 

    Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671–5.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Casiraghi M, Anderson TJ, Bandi C, Bazzocchi C, Genchi C. A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology. 2001;122:93–103.

    CAS 
    PubMed 

    Google Scholar 

  • Zhou S, Fu X, Pei P, Kucka M, Liu J, Tang L, et al. Characterization of a non-sexual population of Strongyloides stercoralis with hybrid 18S rDNA haplotypes in Guangxi, Southern China. PLoS Negl Trop Dis. 2019;13:e0007396.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kobylinski KC, Sylla M, Black W, Foy BD. Mermithid nematodes found in adult Anopheles from southeastern Senegal. Parasit Vectors. 2012;5:131.

    PubMed 
    PubMed Central 

    Google Scholar 

  • De Coster W, Rademakers R. NanoPack 2: population-scale evaluation of long-read sequencing data. Bioinformatics. 2023;39:5.

    Google Scholar 

  • Vierstraete AR, Braeckman BP. Amplicon_sorter: a tool for reference-free amplicon sorting based on sequence similarity and for building consensus sequences. Ecol Evol. 2022;12:e8603.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL. NCBI BLAST: a better web interface. Nucleic Acids Res. 2008;36:W5-9.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95–8.

    CAS 

    Google Scholar 

  • Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021;38:3022–7.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Puillandre N, Brouillet S, Achaz G. ASAP: assemble species by automatic partitioning. Mol Ecol Resour. 2021;21:609–20.

    PubMed 

    Google Scholar 

  • Buckley JJC. On Culicoides as a vector of Onchocerca gibsoni (Cleland and Johnston, 1910). J Helminthol. 1938;16:121–58.

    Google Scholar 

  • Villemant C, Zuccon D, Rome Q, Muller F, Poinar GO Jr, Justine JL. Can parasites halt the invader? Mermithid nematodes parasitizing the yellow-legged Asian hornet in France. PeerJ. 2015;3:e947.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Benelli G, Buttazzoni L, Canale A, D’Andrea A, Del Serrone P, Delrio G, et al. Bluetongue outbreaks: looking for effective control strategies against Culicoides vectors. Res Vet Sci. 2017;115:263–70.

    PubMed 

    Google Scholar 

  • Shults P, Cohnstaedt LW, Adelman ZN, Brelsfoard C. Next-generation tools to control biting midge populations and reduce pathogen transmission. Parasit Vectors. 2021;14:31.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Carpenter S, Mellor PS, Torr SJ. Control techniques for Culicoides biting midges and their application in the U.K. and northwestern Palaearctic. Med Vet Entomol. 2008;22:175–87.

    CAS 
    PubMed 

    Google Scholar 

  • Meloni G, Cossu M, Foxi C, Vento L, Circosta S, Burrai E, et al. Combined larvicidal and adulticidal treatments to control Culicoides biting midges (Diptera: Ceratopogonidae): results of a pilot study. Vet Parasitol. 2018;257:28–33.

    CAS 
    PubMed 

    Google Scholar 

  • Lincoln VJ, Page PC, Kopp C, Mathis A, von Niederhäusern R, Burger D, et al. Protection of horses against Culicoides biting midges in different housing systems in Switzerland. Vet Parasitol. 2015;210:206–14.

    CAS 
    PubMed 

    Google Scholar 

  • Narladkar BW, Shivpuje PR, Harke PC. Fungal biological control agents for integrated management of Culicoides spp. (Diptera: Ceratopogonidae) of livestock. Vet World. 2015;8:156–63.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Baylis HA. The larval stages of the nematode Mermis nigrescens. Parasitology. 1947;38:59–65.

    Google Scholar 

  • Batson BS. Ultrastructure of the trophosome, a food-storage organ in Gastromermis boophthorae (Nematoda: Mermithidae). Int J Parasitol. 1979;9:505–14.

    Google Scholar 

  • Poinar GO, Hess R. Fine structure of the trophosome in Romanomermis culicivorax. Tissue Cell. 1977;9:633–42.

    Google Scholar 

  • Mullens BA, Velten RK. Laboratory culture and life history of Heleidomermis magnapapula in its host, Culicoides variipennis (Diptera: Ceratopogonidae). J Nematol. 1994;26:1–10.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Rusconi JM, Di Battista C, Balcazar D, Rosales M, Achinelly MF. Amphimermis enzoni n. sp. (Nematoda: Mermithidae) parasitizing damselflies and dragonflies in Argentina. J Nematol. 2020;52:1–9.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Poinar GO, Mullens BA. Heleidomermis magnapapula n. sp. (Mermithidae: Nematoda) parasitizing Culicoides variipennis (Ceratopogonidae: Diptera) in California. Revue Nematol. 1987;10:387–91.

    Google Scholar 

  • Mullens BA, Luhring KA. Parasite load effects on sex ratio, size, survival and mating fitness of Heleidomermis magnapapula in Culicoides sonorensis. J Nematol. 2023;55:20230052.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Herbison R, Evans S, Doherty JF, Algie M, Kleffmann T, Poulin R. A molecular war: convergent and ontogenetic evidence for adaptive host manipulation in related parasites infecting divergent hosts. Proc Biol Sci. 2019;286:20191827.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sharp AL, Hunter FF. Chiasmate meiosis in male black fly (Diptera:Simuliidae) larvae associated with mermithid infections (Nematoda: Mermithidae). Can J Zool. 2008;86:1198–202.

    Google Scholar 

  • Bhattacharya G, Mazumdar A, Hazra N. Pathological changes in mermithid nematode infected Stictochironomus polystictus (Kieffer) (Diptera, Chironomidae, Chironominae). Proc Zool Soc. 2014;67:153–7.

    Google Scholar 

  • Beck EC. A population study of the Culicoides of Florida (Diptera: Heleidae). Mosq News. 1958;18:6–11.

    Google Scholar 

  • Smith WW. Mermithid-induced intersexuality in Culicoides stellifer (Coquillett). Mosq News. 1966;26:442–3.

    Google Scholar 

  • Smith WW, Perry VG. Intersexes in Culicoides spp. caused by mermithid parasitism in Florida. J Econ Entomol. 1967;60:1026–7.

    Google Scholar 

  • Erram D, Blosser EM, Burkett-Cadena N. Habitat associations of Culicoides species (Diptera: Ceratopogonidae) abundant on a commercial cervid farm in Florida, USA. Parasit Vectors. 2019;12:367.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Callot J. Action d’un Agamomermis sur les caractères sexuels d’un Cératopogonidé. Annales de Parasitologie. 1959;34:439–43.

    CAS 

    Google Scholar 

  • Callot J, Kremer M. Intersexués chez des Culicoides (Diptera: Ceratopogonidae). Annales de Parasitologie. 1963;38:113–20.

    CAS 

    Google Scholar 

  • Poinar G Jr, Monteys I Sarto V. Mermithids (Nematoda: Mermithidae) of biting midges (Diptera: Ceratopogonidae): Heleidomermis cataloniensis n. sp. from Culicoides circumscriptus Kieffer in Spain and a species of Cretacimermis Poinar, 2001 from a ceratopogonid in Burmese amber. Syst Parasitol. 2008;69:13–21.

    PubMed 

    Google Scholar 

  • Muñoz-Muñoz F, Talavera S, Carpenter S, Nielsen SA, Werner D, Pagès N. Phenotypic differentiation and phylogenetic signal of wing shape in western European biting midges, Culicoides spp., of the subgenus Avaritia. Med Vet Entomol. 2014;28:319–29.

    PubMed 

    Google Scholar 

  • Jobling B. The structure of the head and mouthparts in Culicoides pulicaris, L. (Diptera Nematocera). Bull Entom Res. 1928;18:211–36.

    Google Scholar 

  • Pérez-Pacheco R, Platzer EG, Granados-Echegoyen C, Martinez-Tomas SH, Zárate-Nicolás BH, Quiroz-González B, et al. Prevalence of four nematode species (Mermithidae) in adult mosquitoes (Diptera: Culicidae): first comments since infection/parasitism in fourth-instar larvae. Microorganisms. 2024;12:2388.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Petersen JJ, Willis OR, Chapman HC. Release of Romanomermis culicivorax for the control of Anopheles albimanus in El Salvador I. Mass production of the nematode. Am J Trop Med Hyg. 1978;27:1265–7.

    CAS 
    PubMed 

    Google Scholar 

  • Petersen JJ. Mass production of the mosquito parasite Romanomermis culicivorax: effect of density. J Nematol. 1980;12:45–8.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Thepparat A, Kamata N, Siriyasatien P, Prempree W, Dasuntad K, Chittsamart B, et al. Seasonal abundance and diversity of Culicoides biting midges in livestock sheds in Kanchanaburi Province, Thailand. Insects. 2024;15:701.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Continue Reading