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Unintentional parasite conservation success: chewing lice recovered from Crested Ibis, Nipponia nippon, in breeding program facilities in Shaanxi, China

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Abstract

The crested ibis has survived a dramatic population decline during the twentieth century, declining from a range across much of China, Japan, the Korean peninsula and nearby Russia, to a known world population of seven individuals. These formed the basis of a successful breeding program in Shaanxi, China. We examined ibises in this breeding program for ectoparasites, to establish whether any of the three chewing louse species known from this host had survived this severe host population bottleneck. We recovered representatives of three species of lice, identified as the same species as those previously known from the wild populations: Ardeicola nippon, Colpocephalum nipponi, and Ibidoecus meinertzhageni. Of these, the two first species were recovered from almost all examined hosts, whereas I. meinertzhageni was more rare. As these lice are host specific, this implies that all three louse species remarkably survived this bottleneck, and are now thriving in both the reintroduced and captive populations of crested ibis. This constitutes an unintentional success story in the conservation of parasitic species. We provide the first photos of all three species, as well as a preliminary assessment of their conservation status, and discuss the future of chewing louse conservation.

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Data availability

DNA sequences uploaded to GenBank. Voucher specimens deposited in publicly accessible collections (Guangdong Academy of Sciences).

References

  • Ahmad A, Khan V, Badola S, Bansal N, Saxena AK (2010) Population characteristics and the nature of egg shells of two phthirapteran species parasitizing Indian cattle egrets. J Inst Sci 10:163

    Google Scholar 

  • Al-Aredhi HS (2020) Chewing lice parasitic on little egret Egretta garzetta birds collected from Al-Diwaniyah province, Iraq. EurAs J BioSci 14:1915–1918

    Google Scholar 

  • Almberg ES, Cross PC, Dobson AP, Smith DW, Hudson PJ (2012) Parasite invasion following host reintroduction: a case study of Yellowstone’s wolves. Phil Trans R Soc B 367:2840–2851

    Article  PubMed  PubMed Central  Google Scholar 

  • Anaya-Rojas JM, Best RJ, Brunner FS, Eizaguirre C, Leal MC, Melián CJ, Seehausen O, Matthews B (2019) An experimental test of how parasites of predators can influence trophic cascades and ecosystem functioning. Ecology 2019:e02744

    Google Scholar 

  • Archibald GW, Lantis SDH, Munetchika I (1980) Endangered ibises, Threskiornithinae: their future in the wild and in captivity. Int Zool Yearbook 20:6–17

    Article  Google Scholar 

  • Arora GL, Chopra NP (1957) Some observations on the biology of Lipeurus tropicalis Peters (Mallophaga: Ischnocera). Res Bull Panjab Univ 130:485–491

    Google Scholar 

  • Ash JS (1960) A study of the Mallophaga of birds with particular reference to their ecology. Ibis 102:93–110

    Article  Google Scholar 

  • Ash A, Elliot A, Godfrey S, Burmej H, Abdad MY, Northover A, Wayne A, Morris K, Clode P, Lymbery A, Thompson RCA (2017) Morphological and molecular description of Ixodes woyliei n. sp. (Ixodidae) with consideration for co-extinction with its critically endangered marsupial host. Paras Vect 10:70

    Article  Google Scholar 

  • Awad A-HH, Mohammad ZA-A (2015) Chewing lice found on aquatic birds collected from some marshes of Thi-Qar governorate-South of Iraq. J Babylon Univ/pure App Sci 2:694–702

    Google Scholar 

  • Barbosa A, Merino S, de Lope F, Möller AP (2002) Effects of feather lice on flight behaviour of male Barn Swallows (Hirundo rustica). Auk 119:213–216

    Article  Google Scholar 

  • Beg S, Gupta N, Kumar S, Khan V, Bhatnagar S, Saxena AK (2008) Occurrence of Phthiraptera on the House Crow, Corvus splendens (Passeriformes: Corvidae). Entomon 33:75–78

    Google Scholar 

  • BirdLife International (2001) Threatened birds of Asia: the BirdLife International Red Data Book. BirdLife International, Cambridge, UK

  • BirdLife International (2018) Nipponia nippon. The IUCN red list of threatened species 2018: e.T22697548A132069229. https://doi.org/10.2305/IUCN.UK2018-2.RLTST22697548A132069229.en. Accessed 15 Jan 2021.

  • Bolaños-García R, Rodríguez-Estrella R, Guzmán-Cornejo C (2018) Ectoparasites associated with a great horned owl nesting (Aves: Strigidae) population in fragmented landscape of Baja California peninsula, Mexico. Act Zool Mex (NS) 34:1–15

    Article  Google Scholar 

  • Booth DT, Clayton DH, Block BA (2012) Experimental demonstration of the energetic cost of parasitism in free-ranging hosts. Proc R Soc Lond B 253:125–129

    Google Scholar 

  • Brown NS (1972) The effect of host beak condition on the size of Menacanthus stramineus populations of Domestic Chicken. Poultry Sci 51:162–164

    Article  CAS  Google Scholar 

  • Brown CR, Bomberger Brown M, Rannala B (1995) Ectoparasites reduce long-term survival of their avian hosts. Proc R Soc Lond B 262:313–319

    Article  Google Scholar 

  • Buckley TR, Palma RL, Johns PM, Gleeson DM, Heath ACG, Hitchmough RA, Stringer IAN (2012) The conservation status of small of less well known groups of New Zealand terrestrial vertebrates. N Zeal Entomol 35:137–143

    Article  Google Scholar 

  • Bulgarella M, Palma RL (2017) Coextinction dilemma in the Galápagos Islands: can Darwin’s finches and their native ectoparasites survive the control of the introduced fly Philornis downsi? Ins Cons Div 10:193–199

    Article  Google Scholar 

  • Bush SE, Clayton DH (2006) The role of body size in host specificity: reciprocal transfer experiments with feather lice. Evolution 60:2158–2167

    PubMed  Google Scholar 

  • Bush SE, Harbison CW, Slager DL, Peterson AT, Price RD, Clayton DH (2009) Geographic variation in the community structure of lice on western scrub-jays. J Parasitol 95:10–13

    Article  PubMed  Google Scholar 

  • Bush SE, Villa SM, Boves TJ, Brewer D, Belthoff JR (2012) Influence of bill and foot morphology on the ectoparasites of barn owls. J Parasitol 98:256–261

    Article  PubMed  Google Scholar 

  • Bush SE, Weckstein JD, Gustafsson DR, Allen J, DiBlasi E, Shreve SM, Boldt R, Skeen HR, Johnson KP (2016) Unlocking the black box of feather louse diversity: a molecular phylogeny of the hyper-diverse genus Brueelia. Mol Phyl Evol 94:737–751

    Article  Google Scholar 

  • Carlson CJ, Hopkins S, Bell KC, Doña J, Godfrey SS, Kwak ML, Lafferty KD, Moir ML, Speer KA, Strona G, Torchin M, Wood CL (2020) A global parasite conservation plan. Biol Conserv 250:108596

    Article  Google Scholar 

  • Catanach TA, Valim MP, Weckstein JD, Johnson KP (2018) Cophylogenetic analysis of lice in the Colpocephalum complex (Phthiraptera: Amblycera). Zool Scr 47:72–83

    Article  Google Scholar 

  • Chen BL, Haith KL, Mullens BA (2011) Beak condition drives abundance and grooming-mediated competitive asymmetry in a poultry ectoparasite community. Parasitology 138:748–757

    Article  PubMed  Google Scholar 

  • Chen S, Hao H, Liu Q, Wang R, Zhang P, Wang X, Du E, Yang Z (2013) Phylogenetic and pathogenic analyses of two virulent Newcastle disease viruses isolated from crested ibis (Nipponia nippon) in China. Virus Genes 46:447–453

    Article  PubMed  CAS  Google Scholar 

  • Clay T (1976) The species of Ibidoecus (Phthiraptera) on Threskiornis (Aves). Syst Entomol 1:1–7

    Article  Google Scholar 

  • Clayton DH (1991) Coevolution of avian grooming and ectoparasite avoidance. In: Loye JE, Zuk M (eds) Bird-parasite interactions: ecology, evolution and behavior. Oxford University Press, Oxford

    Google Scholar 

  • Clayton DH, Cotgreave P (1994) Relationship of bill morphology to grooming behaviour in birds. Anim Behav 47:195–201

    Article  Google Scholar 

  • Clayton DH, Walther BA (2001) Influence of host ecology and morphology on the diversity of Neotropical bird lice. Oikos 94:455–467

    Article  Google Scholar 

  • Clayton DH, Lee PLM, Tompkins DM, Brodie ED III (1999) Reciprocal natural selection on host-parasite phenotypes. Am Nat 154:261–270

    Article  PubMed  Google Scholar 

  • Clayton DH, Moyer BM, Bush SE, Jones TG, Gardiner DW, Rhodes BB, Goller F (2005) Adaptive significance of avian beak morphology for ectoparasite control. Proc R Soc Lond B 272:811–817

    Google Scholar 

  • Cohen S, Greenwood MT, Fowler JA (1991) The louse Trinoton anserinum (Amblycera: Phthiraptera), an intermediate host of Sarconema eurycerca (Filarioidea: Nematoda), a heartworm of swans. Med Vet Entomol 5:101–110

    Article  PubMed  CAS  Google Scholar 

  • Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evolution 53:1259–1267

    PubMed  Google Scholar 

  • de Oliveira PA, Ruas JL, Santos LS, Martins NS, de Motta SP, dos Santos CC, Pappen FG, Farias NADR (2019) Chewing lice (Phthiraptera) from crested caracara (Caracara plancus, Falconidae) in Southern Brazil. Sci Anim Health 7:172–179

    Article  Google Scholar 

  • Dik B (2006) Erosive stomatitis in a White Pelican (Pelecanus onocrotalus) caused by Piagetiella titan (Mallophaga: Menoponidae). J Vet Med B 53:153–154

    Article  CAS  Google Scholar 

  • Ding C (2004) Crested ibis research. Shanghai Science and Technology Education Press, Shanghai, China in Chinese

    Google Scholar 

  • Ding C (2010) Crested Ibis Chinese Birds 1(2):156–162

    Article  Google Scholar 

  • Doña J, Proctor H, Serran D, Johnson KP, Oddy-van Oploo A, Huguet-Tapia JC, Ascunce MS, Jovani R (2018) Feather mites play a role in cleaning host feathers: new insights from DNA metabarcoding and microscopy. Mol Ecol 28:203–218

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dougherty ER, Carlson CJ, Bueno VM, Burgio KR, Cizauskas CA, Clements CF, Seidel DP, Harris NC (2015) Paradigms for parasite conservation. Conserv Biol 30:724–733

    Article  PubMed  Google Scholar 

  • Durden LA, Keirans JE (1996) Host-parasite coextinction and the plight of tick conservation. Am Entomol 42:87–91

    Article  Google Scholar 

  • Dyer WG, Williams EH Jr, Mignucci-Giannoni AA, Jimené-Merrero NM, Bunkley-Williams L, Moore DP, Pence DB (2002) Helminth and arthropod parasites of the Brown Pelican, Pelecanus occidentalis, in Puerto Rico, with a compilation of all metazoan parasites reported from this host in the Western Hemisphere. Avian Pathol 31:441–448

    Article  PubMed  Google Scholar 

  • Escalante GC, Sweet AD, McCracken KG, Gustafsson DR, Wilson RE, Johnson KP (2016) Patterns of cryptic host specificity in duck lice based on molecular data. Med Vet Entomol 30:200–208

    Article  PubMed  CAS  Google Scholar 

  • Ewen JG, Armstrong DP, Empson R, Jack S, Makan T, McInnes K, Parker KA, Richardson K, Alley M (2012) Parasite management in translocations: lessons from a threatened New Zealand bird. Oryx 46:446–456

    Article  Google Scholar 

  • Fabiyi JP (1980) Survey of lice infesting domestic fowl on the Jos Plateau, Northern Nigeria. Bull Anim Health Prod Afr 29:215–219

    Google Scholar 

  • Fan G, Zhou H, Xi Y, Cao Y, Fu W, Lu B, Nakaya Y, Fujihara N (2000) Pathological characteristics of a dead domestic crested ibis in China. Jpn J Zool Wild Med 5:93–97

    Article  Google Scholar 

  • Fan G, Yang Z, Gao G, Bin J, Qiao H, Huang Z, Hou Y (2004) The histopathologial observations of young crested ibis infected with Escherichia coli. Chin J Zool 39:44–46 (in Chinese)

    Google Scholar 

  • Galloway TD, Lamb RJ (2014) Abundance and stability are species traits for four chewing lice (Phthiraptera: Menoponidae, Philopteridae) on feral pigeons, Columba livia (Aves: Columbiformes: Columbidae). Can Entomol 146:444–456

    Article  Google Scholar 

  • Gerlach J (2014) Haematopinus oliveri. The IUCN red list of threatened species 2014: e.T9621A2142551. https://doi.org/10.2305/IUCN.UK2014-1.RLTST9621A2142551.en. Accessed on 22 Mar. 2021.

  • Girisgin AO, Di B, Girisgin O (2013) Chewing lice (Phthiraptera) species of wild birds in northwestern Turkey with a new host record. Int J Parasit 2:217–221

    Google Scholar 

  • González-Acuña D, Lohse E, Cicchino A, Mironov S, Figueroa RA, Ardiles K, Kinsella M (2011) Parasites of the American kestrel (Falco sparverius) in south-central Chile. J Rapt Res 45:188–193

    Article  Google Scholar 

  • Grandón-Ojeda A, Cortés P, Moreno L, Kinsella JM, Cicchino A, Barrientos C, González-Acuña D, (2019) Gastrointestinal and external parasites of the variable hawk Geranoaetus polyosoma (Accipitriformes: Accipitridae) in Chile. Braz J Vet Parasit 28:376–382

    Article  Google Scholar 

  • Grossi AA, Sharanowski BJ, Galloway TD (2014) Anatoecus species (Phthiraptera: Philopteridae) from Anseriformes in North America and taxonomic status of Anatoecus dentatus and Anatoecus icterodes. Can Entomol 146:598–608

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gustafsson DR, Olsson U (2012) Flyway homogenization or differentiation? Insights from the phylogeny of the sandpiper (Charadriiformes: Scolopacidae: Calidrinae) wing louse genus Lunaceps (Phthiraptera: Ischnocera). Int J Parasitol 42:93–102

    Article  PubMed  Google Scholar 

  • Gustafsson DR, Olsson U (2017) Unexpected distribution patterns of Carduiceps feather lice (Phthiraptera: Ischnocera: Philopteridae) on sandpipers (Aves: Charadriiformes: Scolopacidae). Syst Entomol 42:509–522

    Article  Google Scholar 

  • Gustafsson DR, Tsurumi M, Bush SE (2015) The chewing lice (Insecta: Phthiraptera: Ischnocera, Amblycera) of Japanese pigeons and doves (Columbiformes), with descriptions of three new species. J Parasit 101:304–313

    Article  PubMed  Google Scholar 

  • Hajela KP, Tandan BK (1968) Two new Mallophaga species of the genus Ardeicola Clay, 1935 (Ischnocera: Philopteridae). Ann Entomol S Am 61:146–151

    Article  Google Scholar 

  • Harnos A, Lang Z, Petrás D, Bush SE, Szabó K, Rózsa L (2017) Size matters for lice on birds: coevolutionary allometry of host and parasite body size. Evolution 71:421–431

    Article  PubMed  Google Scholar 

  • Harrison L (1915) Mallophaga from Apteryx, and their significance; with a note on the genus Rallicola. Parasitology 8:88–100

    Article  Google Scholar 

  • Hopkins DE, Chamberlain WF (1972) Sheep biting louse: notes on the biology of lice reared off the host. Ann Entomol S Am 65:1182–1184

    Article  Google Scholar 

  • Humphreys PN (1975) Wet-feather associated with Holomenopon leucoxanthum in a duck. Vet Rec 97:96–97

    Article  PubMed  CAS  Google Scholar 

  • IUCN (2021) The IUCN Red List of threatened species. Version 2020–3. (https://www.iucnredlist.org) [Accessed 2021–03–17].

  • Johnson KP, Bush SE, Clayton DH (2005a) Correlated evolution of host and parasite body size: tests of Harrison’s rule using birds and lice. Evolution 59:1744–1753

    PubMed  Google Scholar 

  • Johnson KP, Cruickshank RH, Adams RJ, Smith VS, Page RDM, Clayton DH (2005b) Dramatically elevated rate of mitochondrial substitution in lice (Insecta: Phthiraptera). Mol Phyl Evol 26:231–242

    Article  Google Scholar 

  • Jørgensen D (2015) Conservation implications of parasite co-reintroduction. Conserv Biol 29:602–604

    Article  PubMed  Google Scholar 

  • Kalamarz E (1963) Studies on the biology of Mallophaga. I The use of Fe59 izotop in studies on food composition of Mallophaga existing on hens (Gallus domesticus L). Zes N Wyz Szkol Rol Olsz 15:257–251

    Google Scholar 

  • Kock RA, Woodford MH, Rossiter PB (2010) Disease risk associated with translocation of wildlife. Rev Sci Technol 29:329–350

    Article  CAS  Google Scholar 

  • Kose M, Möller AP (1999) Sexual selection, feather breakage and parasites: the importance of white spots in the tail of the Barn Swallow (Hirundo rustica). Behav Ecol Sociobiol 45:430–436

    Article  Google Scholar 

  • Kose M, Mänd R, Möller AP (1999) Sexual selection for white tail spots in the Barn Swallow in relation to habitat choice by feather lice. Anim Behav 58:1201–1205

    Article  PubMed  CAS  Google Scholar 

  • Kuiken T, Leighton FA, Wobeser G, Wagner B (1999) Causes of morbidity and mortality and their effect on reproductive success in Double-crested Cormorants in Saskatchewan. J Wildl Dis 35:331–346

    Article  PubMed  CAS  Google Scholar 

  • Kumar P (1965) A new species of Ibidoecus Cummings 1916 (Mallophaga: Ischnocera). Ann Mag Nat Hist 8:391–398

    Article  Google Scholar 

  • Kumar P, Tandan BK (1966) Two new species of Ibidoecus Cummings, 1916 (Mallophaga: Ischnocera). Ann Mag Nat Hist (ser 13) 9:571–580

    Google Scholar 

  • Kwak ML (2018) Australia’s vanishing fleas (Insecta: Siphonaptera): a case study in methods for the assessment and conservation of threatened flea species. J Insect Conserv 22:545–550

    Article  Google Scholar 

  • Kwak ML, Heath ACG, Palma RL (2019) Saving the Manx shearwater flea Ceratophyllus (Emmareus) fionnus (Insecta: Siphonaptera): the road to developing a recovery plan for a threatened ectoparasite. Act Parasit 64:903–910

    Article  Google Scholar 

  • Larkin JL, Alex KJ, Bolin DC, Maehr DS, Cox JJ, Wichrowski MW, Seward NW (2003) Meningeal worm in a reintroduced elk population in Kentucky. J Wildl Dis 39:588–592

    Article  PubMed  Google Scholar 

  • Lavallée CD, Galloway TD, Rochon K (2019) Infestation parameters of chewing lice (Phthiraptera: Amblycera and Ischnocera) on bald eagles, Haliaeetus leucocephalus (Accipitriformes: Accipitridae), in Manitoba, Canada. Can Entomol 152:89–97

    Article  Google Scholar 

  • Ledger JA (1970) Ectoparasite load in a Laughing Dove with a deformed mandible. Ostrich 41:191–194

    Article  Google Scholar 

  • Leonardi MS, Palma RL (2013) Review of the systematics, biology and ecology of lice from pinnipeds and river otters (Insecta: Phthiraptera: Anoplura: Echinophthiriidae). Zootaxa 3630:445–460

    Article  Google Scholar 

  • Li X, Tian H, Li D (2009) Why the crested ibis declined in the middle of the twentieth century. Biodiv Conserv 18:2165–2172

    Article  Google Scholar 

  • Li Y, Ye X, Wang M, Li W, Dong R, Huo Z, Yu X (2018) Survival rates of a reintroduced population of the crested ibis Nipponia nippon in Ningshan County (Shaanxi, China). Bird Conserv Int 28:145–156

    Article  Google Scholar 

  • Liu YZ (1981) The re-discovery of the crested ibis in Qinling Mountain. Act Zoo Sin 27:273

    Google Scholar 

  • Liu Y, Chen S (eds) (2021) The CNG Field Guide to the Birds of China. Hunan Science and Technology Press, Changsha, China (in Chinese)

    Google Scholar 

  • Malenke JR, Newbold N, Clayton DH (2011) Condition-specific competition governs the geographic distribution and diversity of ectoparasites. Am Nat 177:522–534

    Article  PubMed  CAS  Google Scholar 

  • Martin Mateo MP (1994) Phthiraptera from Platalea leucorodia L (Aves: Ciconiiformes: Threskiornithidae) in Spain. Res Rev Parasit 54:109–115

    Google Scholar 

  • Me E (2013) Ein Phänomen besonders bei Vögeln: Trinken von Tränenflüssigkeit (Lachrymophagie) durch Tierläuse (Insecta, Phthiraptera). Vogelwarte 51:15–23

    Google Scholar 

  • Mey E (2005) Psittacobrosus bechsteini: ein neuer ausgestorbener Federling (Insecta, Phthiraptera, Amblycera) vom Dreifarbenara Ara tricolor (Psittaciiformes), nebst einer annotierten Übersicht über fossile und resent ausgestorbene Tierluause. Anz Ver Thür Ornith 5:201–217

    Google Scholar 

  • Mey E (2017) Neue Gattungen und Arten aus dem Brueelia-Komplex (Insecta, Phthiraptera, Ischnocera, Philopteridae s. l.). Rudolst Naturhist Schr 22:85–215

    Google Scholar 

  • Mey E, Cicchino A, González-Acuña D (2016) Consumo de secreción ocular de aves por piojos Amblycera en Chila y Argentina. Bol Chil Ornit 12:30–35

    Google Scholar 

  • Milotic M, Lymbery A, Thompson A, Doherty J-F, Godfrey S (2020) Parasites are endangered by the conservation of their hosts: meta-analysis of the effect of host captivity on the odds of parasite infection. Biol Conserv 248:108702

    Article  Google Scholar 

  • Mironov SV, Efeykin BD, Ibanez JC, Sumaya AM, Tolstenkov OO (2018) Captive individuals of endangered Philippine raptors maintain native feather mites (Acariformes: Pterolichoidea) species. Int J Parasit 7:116–133

    Google Scholar 

  • Mitchell RM, Dick JA (1977) Ectoparasites from Nepal birds. J Bombay Nat Hist Soc 74:264–274

    Google Scholar 

  • Moreno Mañas E, Gonzálvez JM, del Rocío Ruiz YCM, Gilbert T, Ortiz J, Espeso G, Benzal J, Ibáñez B, Valera Hernández F (2019) Survey of husbandry practices for Bovidae in zoos: the importance of parasite management for reintroduction programmes. Vet Rec 184:282–287

    Article  PubMed  Google Scholar 

  • Moyer BR, Peterson AT, Clayton DH (2002) Influence of bill shape on ectoparasite load in Western Scrub-jays. Condor 104:675–678

    Article  Google Scholar 

  • Mus S, Afroz SDA, Khanum H (2011) Occurrence of ecto- and endoparasites in pigeon (Columba livia Linn.). Univ J Rajshahi Univ 20:73–75

    Google Scholar 

  • Nagata H, Yamagishi S (2013) Re-introduction of crested ibis on Sado Island, Japan. In: Soorae, PS (ed.) Global re-introduction perspectives: 2013. Further case-studies from around the globe. IUCN/SSC Re-introduction Specialist Group and Environment Agency-Abu Dhabi. Gland, Switzerland and Abu Dhabi, United Arab Emirates.

  • Naz S, Rizvi SA, Sychra O (2010) The high rate of infestation of chewing lice (Phthiraptera) in Rock Pigeons (Columba livia Gmelin 1789) in Pakistan. Trop Zool 23:21–28

    Google Scholar 

  • Nelson BC (1971) Successful rearing of Colpocephalum turbinatum (Phthiraptera). Nature 232:255

    CAS  Google Scholar 

  • Northover AS, Lymbery AJ, Wayne AF, Godfrey SS, Thompson RCA (2018) The hidden consequences of altering host-parasite relationships during fauna translocations. Biol Conserv 220:140–148

    Article  Google Scholar 

  • Obanda V, Kagira JM, Chege S, Okita-Ouma B, Gakuya F (2011) Trypanosomosis and other co-infections in translocated black (Diceros bicornis michaeli) and white (Ceratotherium simum simum) rhinoceroses in Kenya. Sci Parasit 12:103–107

    Google Scholar 

  • Oniki Y, Butler JF (1989) The presence of mites and insects in the gut of two species of chewing lice (Myrsidea sp. and Philopterus sp., Mallophaga): accident or predation? Rev Bras Biol 49:1013–1016

    Google Scholar 

  • Órdenes JS-M, Ibánez CB, Contreras LR, Schmäschke R, Daugshies A, González-Acuna D (2005) Ectoparasitismo en tiquque común Milvago chimango chimango (Vieillot, 1816) (Aves, Falconidae) en la zona de Nuble, Chile. Lundiana 6:49–55

    Google Scholar 

  • Parker KA, Brunton DH, Jakob-Hoff R (2006) Avian translocations and disease; implications for New Zealand conservation. Pac Conserv Biol 12:155–162

    Article  Google Scholar 

  • Pérez JM, Palma RL (2001) A new species of Felicola (Phthiraptera: Trichodectidae) from the endangered Iberian lynx: another reason to ensure its survival. Biodiv Conserv 10:929–937

    Article  Google Scholar 

  • Pérez JM, Ruiz-Martínez I, Cooper JE (1996) Occurrence of chewing lice on Spanish raptors. Ardeola 43:129–138

    Google Scholar 

  • Pérez JM, Sánchez I, Palma RL (2013) The dilemma of conserving parasites: the case of Felicola (Lorisicola) isidoroi (Phthiraptera: Trichodectidae) and its host, the endangered Iberian lynx (Lynx pardinus). Ins Cons Div 6:680–686

    Article  Google Scholar 

  • Piross IS, Fehérvári P, Vas Z, Solt S, Horváth É, Palatitz P, Giosele C, Gustin M, Pedrelli M, Kumar RS, Williams NP, Pretorius R, Bernitz Z, Bernitz H, Harnos A (2015) Louse (Insecta: Phthiraptera) infestations of the Amur falcon (Falco amurensis) and the red-footed falcon. Orn Hung 23:58–65

    Article  Google Scholar 

  • Piross IS, Saliga R, Solt S, Horváth É, Kotymán L, Harnos A, Rózsa L, Palatitz P, Fehérvári P (2018) A tolltetű-fertőzöttség és a fészekaljméret kapcsolata a vörös vércsénél (Falco tinnunculus). Magy Allat Lap 140:745–753

    Google Scholar 

  • Piross IS, Solt S, Horváth É, Kotymán L, Palatitz P, Bertók P, Szabo K, Vili N, Rózsa L, Hamos A, Fehérvári P (2020) Sex-dependent changes in the louse abundance of red-footed falcons (Falco vespertinus). Parasit Res 119:1327–1335

    Article  Google Scholar 

  • Price RD, Beer JR (1965) The Colpocephalum (Mallophaga: Menoponidae) of the Ciconiiformes. Ann Entomol Soc Am 58:111–131

    Article  Google Scholar 

  • Price RD, Hellenthal RA, Palma RL 2003. World checklist of chewing lice with host associations and keys to families and genera. In: Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (eds) The Chewing lice: world checklist and biological overview. Illinois Natural History Survey Special Publication, Champaign

  • Qing B, Zhai T, Ding H, Yan L (2009) A case of diagnosis and treatment of zinc deficiency disease of the crested ibis. Chin J Wildl 30:147–148

    Google Scholar 

  • Rékási J, Rózsa L, Kiss BJ (1997) Patterns in the distribution of avian lice (Phthiraptera: Amblycera, Ischnocera). J Adv Biol 28:150–156

    Google Scholar 

  • Rivera-Parra JL, Levin II, Parker PG (2014) Comparative ectoparasite loads of five seabird species in the Galapagos Islands. J Parasit 100:569–577

    Article  PubMed  Google Scholar 

  • Robinson AT, Hines PP, Sorensen JA, Bryan SD (1998) Parasites and fish health in a desert stream, and management implications for two endangered fishes. N Am J Fish Man 18:599–608

    Article  Google Scholar 

  • Rózsa L, Vas Z (2015) Co-extinct and critically co-endangered species of parasitic lice, and conservation-induced extinction: should lice be reintroduced to their hosts? Oryx 49:107–110

    Article  Google Scholar 

  • Rózsa L, Rékási J, Reiczigel J (1996) Relationship of host coloniality to the population ecology of avian lice. J Anim Ecol 65:242–248

    Article  Google Scholar 

  • Saxena AK (2017) Population characteristics of black kite lice. J Parasit Dis 41:684–686

    Article  PubMed  CAS  Google Scholar 

  • Saxena AK, Agarwal GP (1982) Effect of different temperatures and humidities on the development of the eggs of poultry louse, Lipeurus lawrensis tropicalis. (Phthiraptera: Ischnocera). Ang Parasit 23:227–230

    CAS  Google Scholar 

  • Saxena AK, Agarwal GP (1983) In vitro rearing of Mallophaga. Ang Parasit 24:178–183

    CAS  Google Scholar 

  • Seegar WS, Schiller EL, Sladen WJL, Trpis M (1976) A Mallophaga, Trinoton anserinum, as a cyclodevelopmental vector for a heartworm parasite of waterfowl. Science 194:739–741

    Article  PubMed  CAS  Google Scholar 

  • Selim MK, El-Kasaby A, El-Refall AH (1968) External parasites of Domestic Pigeon in United Arab Republic. Ang Parasit 9:74–84

    Google Scholar 

  • Shi S, Cao Y (2001) The crested ibis in China. China Forestry Publishing House, Beijing, China

    Google Scholar 

  • Shi D, Yu X, Fan C, Cao Y (1991) Narrating the process of the decline and death of the crested ibis. J Northwest Uni 21:25–30

    Google Scholar 

  • Singer FJ, Willams E, Miller MW, Zeigenfuss LC (2000) Population growth, fecundity, and survivorship in recovering populations of bighorn sheep. Restor Ecol 8:75–84

    Article  Google Scholar 

  • Singh SK, Surman KA, Saxena AK (1998) Population composition of four Phthirapteran ectoparasites infesting Blue Rock Pigeon, Columba livia Gmelin. J Parasit Dis 22:144–147

    Google Scholar 

  • Spencer HG, Zuk M (2016) For the host’s sake: the pluses of parasite conservation. Trends Ecol Evol 31:341–343

    Article  PubMed  Google Scholar 

  • Stockdale HJ, Raun ES (1965) Biology of chicken bodylouse, Menacanthus stramineus. Ann Entomol Soc Am 58:802–805

    Article  Google Scholar 

  • Sychra O, Najer T, Kounek F, Hung NM, Tolstenkov OO (2014) Myrsidea claytoni (Phthiraptera: Menoponidae) from Cymbirhynchus macrorhynchos (Passeriformes: Eurylaimidae): a case of natural host switching. J Parasit 100:280–283

    Article  PubMed  Google Scholar 

  • Tandan BK (1958a) Mallophagan parasites from Indian birds–part V. Species belonging to the genus Ibidoecus Cummings, 1916 (Ischnocera). Trans Roy Ent Soc Lond 110:393–410

    Article  Google Scholar 

  • Tandan BK (1958b) Mallophaga (Insecta). Part II a new species of Ibidoecus Cummings, 1916. Nat Hist Rennell Island 2:151–154

    Google Scholar 

  • Taylor AL (1981) Adventitious molt in red knot possibly caused by Actornithophilus (Mallophaga, Menoponidae). J Field Ornith 52:241

    Google Scholar 

  • Thorne ET, Williams ES (1988) Disease and endangered species: the black-footed ferret as a recent example. Conserv Biol 2:66–74

    Article  PubMed Central  Google Scholar 

  • Touati L, Samraoui B (2013) Diversity and distribution of avian lice on greater flamingo chicks (Phoenicopterus roseus) in Algeria. Av Biol Res 6:261–268

    Article  Google Scholar 

  • Touati L, Figuerola J, Alfarhan AH, Samraoui B (2015) Distribution patterns of ectoparasites of glossy ibis (Plegadis falcinellus) chicks. Zool Ecol 25:46–53

    Google Scholar 

  • van Oosterhout C, Smith AM, Hänfling B, Ramnarine IW, Mohammed RS, Cable J (2007) The guppy as a conservation model: implications of parasitism and inbreeding for reintroduction success. Conserv Biol 21:1573–1583

    PubMed  Google Scholar 

  • Villa SM, Evans MD, Subhani YK, Altuna JC, Bush SE, Clayton DH (2018) Body size and fecundity are correlated in feather lice (Phthiraptera: Ischnocera): implications for Harrison’s rule. Ecol Entomol 43:394–396

    Article  Google Scholar 

  • Villa SM, Altuna JC, Ruff JS, Beach AB, Mulvey LI, Poole EJ, Campbell HE, Johnson KP, Shapiro MD, Bush SE, Clayton DH (2019) Rapid experimental evolution of reproductive isolation from a single natural population. Proc Nat Acad Sci USA 116:13440–13445

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Waki T, Shimano S (2020) A report of infection in the crested ibis Nipponia nippon with feather mites in current Japan. J Acarol Soc Jpn 29:1–8

    Article  Google Scholar 

  • Warnes ML (1981) Insect ectoparasites of the Rook (Corvus frugilegus L). Entomol Month Mag 117:249–252

    Google Scholar 

  • Weckstein JD (2004) Biogeography explains cophylogenetic patterns in toucan chewing lice. Syst Biol 53:154–164

    Article  PubMed  Google Scholar 

  • Whiteman NK, Parker PG (2004a) Body condition and parasite load predict territory ownership in the Galapagos Hawk. Condor 106:915–921

    Article  Google Scholar 

  • Whiteman NK, Parker PG (2004b) Effects of host sociality on ectoparasite population biology. J Parasit 90:939–947

    Article  PubMed  Google Scholar 

  • Whiteman NK, Parker PG (2005) Using parasites to infer host population history: a new rationale for parasite conservation. Anim Conserv 8:175–181

    Article  Google Scholar 

  • Whiteman NK, Matson KD, Bollmer JL, Parker PG (2006) Disease ecology in the Galápagos Hawk (Buteo galapagoensis): host genetic diversity, parasite load and natural antibodies. Proc R Soc B 273:797–804

    Article  PubMed  Google Scholar 

  • Windsor DA (1995) Equal rights for parasites. Conserv Biol 9:1–2

    Article  Google Scholar 

  • Wobeser G, Johnson GR, Acompanado G (1974) Stomatitis in a juvenile White Pelican due to Piagetiella peralis (Mallophaga: Menoponidae). J Wildl Dis 10:135–138

    Article  PubMed  CAS  Google Scholar 

  • Worth CB (1940) A note on the dissemination of Mallophaga. Bird-Band 11:23–24

    Google Scholar 

  • Xi Y, Lu B, Fujihara N (2001) Captive rearing and breeding of the crested ibis, Nipponia nippon. J Poultry Sci 38:213–224

    Article  Google Scholar 

  • Xi Y, Wood C, Lu B, Zhang Y (2007) Prevalence of a septicemia disease in the crested ibis (Nipponia nippon) in China. Av Dis 51:614–617

    Article  Google Scholar 

  • Yamashina Y, Nakanishi G (eds.) Toki, Nipponia nippon: Tasogare ni kieta hishoun shi. Tokyo Kenkyusha, Tokyo, Japan (in Japanese)

  • Yamato Y, Nakanishi G (1983) Crested ibis (Nipponia nippon). Educ J 1983:79 ((in Japanese))

    Google Scholar 

  • Yosef R, Strutzer O, Tabibi R, Rózsa L (2009) Lice infestations of steppe buzzards (Buteo buteo vulpinus) differ from those of common buzzards (Buteo buteo buteo). J Rapt Res 53:102–108

    Article  Google Scholar 

  • Yu X, Liu N, Xi Y, Lu B (2006) Reproductive success of the crested ibis Nipponia nippon. Bird Conserv Int 16:325–343

    Article  Google Scholar 

  • Yu X, Chang X, Li X, Chen W, Shi L (2009) Return of the crested ibis Nipponia nippon: a reintroduction programme in Shaanxi province, China. BirdingASIA 11:80–82

    Google Scholar 

  • Yu X, Li X, Huo Z (2015) Breeding ecology and success of a reintroduced population of the endangered crested ibis Nipponia nippon. Bird Cons Int 25:207–219

    Article  Google Scholar 

  • Zhang X, Qiao JY, Wu XM, Ma QY, Hu H, Wang J, Che LF (2014) Ascaris spp. and Capillaria caudinflata infections in captive-bred crested ibis (Nipponia nippon) in China. Zoo Biol 34:80–84

    Article  PubMed  CAS  Google Scholar 

  • Zhou H, Fan G, Cao Y, Fu W, Lu B, Xi Y (2000) The pathological diagnosis of the death of a domesticated crested ibis. Act Univ Agri Boreali-Occ 28:60–64

    Google Scholar 

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Acknowledgements

We would like to thank the staff at the Shaanxi Provincial Rare Wildlife Rescue and Breeding Research Center, the Hanzhong Crested Ibis National Nature Reserve, and the Crested Ibis Release Base in Ningshan County, who allowed us to survey ibises for lice, and assisted in the catching and handling of ibises. Three anonymous reviewers provided helpful comments to an earlier version of this manuscript, for which we are grateful.

Funding

Work was funded by the National Natural Science Foundation of China [Grant Numbers 31961123003; 31872245; 31572282], the Pearl River Talent Recruitment Program, Guangdong Province [Grant Number 2019QN01N968], and the Introduction of Full-Time High-Level Talent Fund of the Institute of Zoology, Guangdong Academy of Sciences [Grant Numbers GIABR-GJRC201701].

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Authors and Affiliations

  1. Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, 105 Xingang West Road, Haizhu District, Guangzhou, 510260, Guangdong, China

    Daniel R.. Gustafsson, Chunpo Tian & Fasheng Zou

  2. College of Life Sciences, Shaanxi Normal University, 620 West Chang’an Street, Chang’an District, Xi’an, 710061, Shaanxi, China

    Chunpo Tian, Xiaoping Yu, Lulu Xu & Si Wu

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  1. Daniel R.. Gustafsson
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  2. Chunpo Tian
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  3. Xiaoping Yu
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  4. Lulu Xu
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  5. Si Wu
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  6. Fasheng Zou
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Contributions

DRG identified specimens and wrote manuscript; CT collected samples, extracted and sequenced DNA, and produced slide-mounted specimens; XY collected samples and provided access to ibis breeding centres; LX, and SW collected samples; FZ edited manuscript.

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Correspondence to Daniel R.. Gustafsson.

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Ethical approval

The present study was carried out in strict accordance with the Regulation for the Administration of Laboratory Animals (Decree No. 2, State Science and technology Commission of the People’s Republic of China, 14 November 1988).

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Communicated by Louise Amy Ashton.

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Gustafsson, D.R., Tian, C., Yu, X. et al. Unintentional parasite conservation success: chewing lice recovered from Crested Ibis, Nipponia nippon, in breeding program facilities in Shaanxi, China. Biodivers Conserv 30, 3939–3963 (2021). https://doi.org/10.1007/s10531-021-02283-8

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