A total of 1,621 wild birds representing 34 species were examined for chewing lice in reed beds in southwestern Slovakia during the pre-breeding migration 2008-2009 and 2016-2019. A total of 377 (23.3%) birds representing 15 species were parasitized by 26 species of chewing lice of 12 genera. Dominant genera were Penenirmus (with dominance 32.6%) and Menacanthus (29.4%), followed by Brueelia (12.6%), Acronirmus (10.8%), Philopterus (7.7%), and Myrsidea (4.2%). We evaluated 33 host-louse associations including both 1) host-generalist, parasitizing more than one host species and host-specific lice, occurring only on a single host species, and 2) lice species with large range geographic distribution, reported across the range of the distribution of their hosts and lice species with only occasional records from a limited area within the range of their hosts. The Bearded Reedling, Panurus biarmicus (Linnaeus, 1758), was parasitized by two species of chewing lice, Menacanthus brelihi Balát, 1981 and Penenirmus visendus (Złotorzycka, 1964), with conspicuously different prevalences (5.6% vs. 58.2%, respectively; n = 251). New material enabled us to redescribe both species of lice: the first one is resurrected from previous synonymy as a valid species. A fragment of the mitochondrial cytochrome oxidase I gene was sequenced from these two species in order to assess their relative phylogenetic position within their genera. Our study demonstrates the importance of an adequate identification of parasites, especially on rarely examined and endangered hosts.

TITLE: Mallophages de la Panure à moustaches (Panurus biarmicus) et diversité des associations mallophages-hôtes des oiseaux dans les roselières en Slovaquie. ABSTRACT: Au total, 1 621 oiseaux sauvages représentant 34 espèces ont été examinés à la recherche de mallophages dans les roselières du sud-ouest de la Slovaquie au cours de la migration de pré-reproduction 2008–2009 et 2016–2019. Parmi ceux-ci, 377 oiseaux (23,3 %), représentant 15 espèces, étaient parasités par 26 espèces de mallophages de 12 genres. Les genres dominants étaient Penenirmus (avec une dominance de 32,6 %) et Menacanthus (29,4 %), suivis de Brueelia (12,6 %), Acronirmus (10,8 %), Philopterus (7,7 %) et Myrsidea (4,2 %). Nous avons évalué 33 associations mallophage-hôte comprenant à la fois 1) des espèces de mallophages généralistes, parasitant plus d’une espèce hôte, et des mallophages spécifiques, présents uniquement sur une seule espèce hôte et 2) des espèces de mallophages ayant une large répartition géographique, signalées à travers l’étendue de la répartition de leurs hôtes, et des espèces de mallophages avec seulement des observations occasionnelles dans une zone limitée à l’intérieur de l’aire de répartition de leurs hôtes. La Panure à moustaches, Panurus biarmicus (Linnaeus, 1758), était parasitée par deux espèces de mallophages, Menacanthus brelihi Balát, 1981 et Penenirmus visendus (Złotorzycka, 1964), avec des prévalences nettement différentes (respectivement 5,6 % et 58,2 %, n = 251). Du nouveau matériel nous a permis de redécrire les deux espèces de mallophages, la première étant ressuscitée de la synonymie précédente en tant qu’espèce valide. Un fragment du gène mitochondrial de la cytochrome oxydase I a été séquencé à partir de ces deux espèces afin d’évaluer leur position phylogénétique relative au sein de leurs genres. Notre étude démontre l’importance d’une identification adéquate des parasites, en particulier sur les hôtes rarement examinés et menacés.

Department of Biology and Wildlife Diseases Faculty of Veterinary Hygiene and Ecology University of Veterinary Sciences Brno Palackeho tr 1946 1 61242 Brno Czechia

Department of Biology University of Trnava Priemyselna 4 918 43 Trnava Slovakia

Department of Parasitology Faculty of Science University of South Bohemia České Budějovice Czechia Institute of Parasitology Biology Centre Czech Academy of Sciences v v i České Budějovice Czechia

Department of Veterinary Sciences Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamycka 129 165 00 Prague 6 Czechia Illinois Natural History Survey Prairie Research Institute University of Illinois Urbana Champaign IL 61820 USA

Institute of Vertebrate Biology Czech Academy of Sciences v v i Kvetna 8 603 65 Brno Czechia

Zobrazit více v PubMed

Adam C. 2007. Data on the chewing louse fauna (Phthiraptera: Amblycera, Ischnocera) from some Romanian autochthonous and exotic birds. Travaux du Muséum National d’Histoire Naturelle “Grigore Antipa”, 50, 145–210.

Balát F. 1955. Chewing lice from Tatra national park. Folia Zoologica et Entomologica, 4(4), 389–398. (In Czech).

Balát F. 1966. Federlinge tschechoslowakischer Uferschwalben. Angewandte Parasitologie, 7, 244–248.

Balát F. 1981. A contribution to the knowledge of biting lice (Mallophaga) found on passerines (Passeriformes). Folia Parasitologica, 28, 273–282.

Bernal I, Talabante C, Dik B, Sánchez Martínez LJ, Viejo JL. 2022. Low prevalence of chewing lice (Phthiraptera) in wintering populations of the reed bunting Emberiza schoeniclus (Aves: Passeriformes: Emberizidae) in the Iberian Peninsula. Annals of Parasitology, 68(1), 177–181. PubMed

Birds Directive. 2023. Panurus biarmicus – detailed species summary: Population status and trends at the EU and Member State levels under Article 12 web tool for the period 2013–2018. (accessed 2 September 2023). https://nature-art12.eionet.europa.eu/article12/summary?period=3&subject=Panurus+biarmicus&reported_name=.

BirdLife Internatinal 2023. Species factsheet: Panurus biarmicus. (accessed 2 September 2023). http://datazone.birdlife.org/species/factsheet/bearded-reedling-panurus-biarmicus.

Bush SE, Gustafsson DR, Clayton DH. 2018. New records of ectoparasites from passerine birds in the High Tatras of Slovakia. Oecologia Montana, 27, 43–45.

Bush SE, Reed M, Maher S. 2013. Impact of forest size on parasite biodiversity: implications for conservation of hosts and parasites. Biodiversity and Conservation, 22, 1391–1404.

Demko M, Krištín A, Puchala P. 2013. Red list of birds in Slovakia. Tichodroma, 225, 69–78.

Emerson KC. 1972. Checklist of the Mallophaga of North America (north of Mexico). Part I. Suborder Ischnocera. , Dugway, Utah: . Deseret Test Center, Dugway Proving Ground. p. 200.

Fedorenko IA. 1983. Superfamily Menoponoidea, Fauna Ukrainy 22(5). Institut Zoologii Akademii Nauk Ukraini: RSR, Kiev. p. 1–168. (in Russian).

Gill F, Donsker D, Rasmussen P, Editors. 2023. IOC World Bird List (v13.2). (Accessed 2 September 2023). 10.14344/IOC.ML.13.2. DOI

Gustafsson DR, Bush SE. 2017. Morphological revision of the hyperdiverse Brueelia-complex (Insecta: Phthiraptera: Ischnocera: Philopteridae) with new taxa, checklists and generic key. Zootaxa, 4313, 1–443.

Gustafsson DR, Ošlejšková L, Najer T, Sychra O, Zou F. 2019. Redescriptions of thirteen species of chewing lice in the Brueelia-complex (Phthiraptera, Ischnocera, Philopteridae), with one new synonymy and a neotype designation for Nirmus lais Giebel, 1874. Deutsche Entomologische Zeitschrift (neue Folge), 66, 17–39.

Gustafsson DR, Tian C, Yu X, Xu L, Wu S, Zou F. 2021. Unintentional parasite conservation success: chewing lice recovered from crested ibis, Nipponia nippon, in breeding program facilities in Shaanxi, China. Biodiversity and Conservation, 30, 3939–3963.

Janiga M. 2018. Different coevolutionary breeding strategies of Ischnoceran lice on Prunella collaris and P. modularis in high mountains. Polish Journal of Ecology, 66(2), 182–193.

Janiga M. 2019. Adaptive plasticity in insect parasites – Philopterus lice and their accentor passerine hosts. Polish Journal of Ecology, 66(4), 395–406.

Janiga M, Kubašková Ľ. 2000. The biology of the alpine accentor Prunella collaris. III. The coevolution of alpine accentors and lice (Phthiraptera). Oecologia. Montana, 9(1–2), 24–28.

Janiga M, Mičková A. 2004. The biology of the alpine accentor Prunella collaris. V. The sex ratio and transmission of lice Philopterus emiliae. Oecologia Montana, 13, 17–22.

Johnson KP, Moyle RG, Witt CC, Faucett RC, Weckstein JD. 2001. Phylogenetic relationships in the louse genus Penenirmus based on nuclear (EF-1alpha) and mitochondrial (COI) DNA sequences. Systematic Entomology, 26(4), 491–497.

Johnson KP, Adams RJ, Clayton DH. 2002. The phylogeny of the louse genus Brueelia does not reflect host Phylogeny. Biological Journal of the Linnean Society London, 77(22), 233–247.

Johnson KP, Weckstein JD, Witt CC, Faucett RC, Moyle RG. 2002. The perils of using host relationships in parasite taxonomy: phylogeny of the Degeeriella complex. Molecular Phylogenetics and Evolution, 23(2), 150–157. PubMed

Johnson KP, Cruickshank RH, Adams RJ, Smith VS, Page RD, Clayton DH. 2003. Dramatically elevated rate of mitochondrial substitution in lice (Insecta: Phthiraptera). Molecular Phylogenetics and Evolution, 26(2), 231–242. PubMed

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. 2012. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. PubMed PMC

Keller V, Herrando S, Voříšek P, Franch M, Kipson M, Milanesi P, Martí D, Anton M, Klvaňová A, Kalyakin MV, Bauer HG, Foppen RPB. 2020. European Breeding Bird Atlas 2: Distribution. Barcelona: Abundance and Change. European Bird Census Council & Lynx Edicions.

Kettle PR. 1983. The seasonal incidence of parasitism by Phthiraptera on starlings (Sturnus vulgaris) in England. New Zealand Entomologist, 7(4), 403–408.

Kloubec B, Capek M. 2005. Seasonal and diel budgets of song: a study of Savi’s warbler (Locustella luscinioides). Journal of Ornithology, 146, 206–2014.

Krištofík J. 2000. Synonymical notes to the Menacanthus species (Phthiraptera, Menoponidae) living on Passeriformes (Aves). Acta Parasitologica, 45(1), 57–58.

Kumar S, Stecher G, Tamura K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Phylogenetics and Evolution, 33, 1870–1874. PubMed PMC

Light JE, Nessner CE, Gustafsson DR, Wise SR, Voelker G. 2016. Remarkable levels of avian louse (Insecta: Phthiraptera) diversity in the Congo Basin. Zoologica Scripta, 45, 538–551.

Martinů J, Sychra O, Literák I, Capek M, Gustafsson DR, Štefka J. 2015. Host generalists and specialists emerging side by side: an analysis of evolutionary patterns in the cosmopolitan chewing louse genus Menacanthus . International Journal for Parasitology, 45, 63–73. PubMed

Mey E. 2023. Phthiraptera, in de Jong Y, Editor. Fauna European Consortium. Checklist dataset. (accessed 23 August 2023).. 10.15468/ymk1bx. DOI

Najer T, Sychra O, Kounek F, Papoušek I, Nguyen MH. 2014. Chewing lice (Phthiraptera: Amblycera, Ischnocera) from wild birds in southern Vietnam, with descriptions of three new species. Zootaxa, 3755(5), 419–433. PubMed

Najer T, Papoušek I, Adam C, Trnka A, Quach VT, Nguyen CN, Figura R, Literák I, Sychra O. 2020. New records of Philopterus (Ischnocera: Philopteridae) from Acrocephalidae and Locustellidae, with description of one new species from Regulidae. European Journal of Taxonomy, 632, 1–37.

Ošlejšková L, Krištofík J, Trnka A, Sychra O. 2021. An annotated checklist of chewing lice (Phthiraptera: Amblycera, Ischnocera) from Slovakia. Zootaxa, 5069, 1–80. PubMed

Palma RL, Price RD. 2006. Lice of the genus Philopterus Nitzsch (Phthiraptera: Ischnocera: Philopteridae) parasitic on host of the genus Emberiza (Passeriformes: Emberizidae). New Zealand Journal of Zoology, 33, 1–6.

Paterson A, Palma RL, Gray RD. 1999. How frequently do avian lice miss the boat? Implications for coevolutionary studies Systematic Biology, 48, 214–223.

Price RD. 1977. The Menacanthus (Mallophaga: Menoponidae) of the Passeriformes (Aves). Journal of Medical Entomology, 14, 207–220. PubMed

Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH. 2003. The chewing lice: world checklist and biological overview, The chewing lice: world checklist and biological overview. Illinois Natural History Survey Special Publication. p. 24.

Rékási J. 1993. Bird lice (Mallophaga) parasiting the birds of Hungary. Aquila, 100, 71–93.

Rékási J, Kiss JB, Sándor AD. 2017. Chewing lice (Phthiraptera: Amblycera, Ischnocera) recorded from birds in the Danube Delta Biosphere Reserve: a literature review with new data. Aquila, 124, 7–33.

Rheinwald G. 1968. Die Mallophagengattung Ricinus De Geer, 1778. Revision der ausseramerikanischen Arten. Mitteilungen aus dem Hamburg Zoologischen Museum Institut, 65, 181–326.

Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. PubMed

Rózsa L, Rékási J, Reiczigel J. 1996. Relationship of host coloniality to the population ecology of avian lice (Insecta: Phthiraptera). Journal of Animal Ecology, 65, 242–248.

Sychra O, Literák I, Podzemný P, Benedikt V. 2008. Insect ectoparasites from wild passerine birds in the Czech Republic. Parasite, 15, 599–604. PubMed

Sychra O, Sychrová V, Literák I. 2008. Identity of Menacanthus obrteli Balát (Phthiraptera: Menoponidae) from the Savi’s Warbler (Passeriformes: Sylviidae). Biologia (B Zool.), 63(5), 686–688.

Sychra O, Literák I, Podzemný P, Harmat P, Hrabák R. 2011. Insect ectoparasites on wild birds in the Czech Republic during the pre-breeding period. Parasite, 18, 13–19. PubMed PMC

Sychra O, Kounek F, Papoušek I, Capek M, Cárdenas-Callirgos JM, Franco S, Literák I. 2014. Chewing lice (Phthiraptera: Amblycera et Ischnocera) from wrens (Passeriformes: Troglodytidae), with description of a new species of Myrsidea. Acta Entomologica Musei Nationalis Pragae, 54(1), 1–27.

Sychra O, Kolenčík S, Papoušek I, Bilbija B, Literák I. 2021. Myrsidea quadrifasciata (Phthiraptera: Amblycera) – a unique host generalist among highly host-specific chewing lice. Arthropod Systematics & Phylogeny, 79, 379–400.

Sychra O, Ošlejšková L, Skoupá Ž, Najer T, Literák I, Papoušek I, Trnka A, Capek M. 2023. Chewing lice of passerine birds in reed beds in Slovakia, with a special focus on Panurus biarmicus. Medical and Veterinary Entomology, 37, 300–307. PubMed

Takano OM, Voelker G, Gustafsson DR, Light JE. 2018. Molecular phylogeny and novel host associations of avian chewing lice (Insecta: Phthiraptera) from South Africa. Systematic Entomology, 44, 289–304.

Trnka A, Capek M, Kloubec B. 2003. Vtáky národnej prírodnej rezervácie Parížske močiare [Birds of the National Nature Reserve Parížske močiare Marsh, SW Slovakia]. Bratislava: Veda. p. 161. (in Slovak, with an English summary).

Vas Z, Privigyei C, Prohaszka VJ, Csorgo T, Rózsa L. 2012. New species and host association records for the Hungarian avian louse fauna (Insecta: Phthiraptera). Ornis Hungarica, 20(1), 44–49.

Złotorzycka J. 1964. Mallophaga parasitizing Passeriformes and Pici II. Brueeliinae. Acta Parasitologica Polonica, 12(24), 239–282.

Złotorzycka J. 1976. Chewing lice – Mallophaga, part 2 Superfamily Menoponoidea. Warszava: Panstwowe Wydawnictwo Naukowe. p. 190. (in Polish).

Złotorzycka J. 1997. Chewing lice (Mallophaga), systematic part: Goniodidae and Philopteridae. Wroclaw: Wydawnictwo Uniwersyteta Wroclawskiego. p. 308. (in Polish).

Złotorzycka J, Modrzejewska M. 2001. Chewing lice (Mallophaga), systematic part: Rallicolidae and Pseudonirmidae. Wroclaw: Wydawnictwo Uniwersyteta Wroclawskiego. p. 180. (in Polish).