We report for the first time the presence of the snake mite, Ophionyssus natricis (Gervais) (Mesostigmata: Macronyssidae) on captive snakes kept at Panama City, Panama. This occurrence adds a new record to the geographical distribution of O. natricis as well as confirms its high prevalence on captive reptiles. Several Boidae species, Boa constrictor, Epicrates maurus, Corallus ruschenbergerii, Corallus caninus and a Pythonidae, Python regius were found infested with intensities varying from 10 to 2200 mites each. These findings represent the second record of O. natricis for Central America

Bermúdez, Sergio E.

Cleghorn, John E.

Miranda, Roberto J.

Perotti, Maria A.

Acarologia

Miranda, R.J., Cleghorn, J.E., Bermúdez, S.E., Perotti, M.A. (2017): Occurrence of the mite Ophionyssus natricis (Acari: Macronyssidae) on captive snakes from Panama. Acarologia 57 (2): 365-368, DOI: 10.1051/acarologia/20164161, URL: http://dx.doi.org/10.1051/acarologia/2016416

Miranda, R.J.

Cleghorn, J.E.

Bermúdez, S.E.

Perotti, M.A.

ZENODO

Occurrence of the mite Ophionyssus natricis (Acari: Macronyssidae) on captive snakes from Panama

R.J. Miranda

J.E. Cleghorn

S.E. Bermúdez

M.A. Perotti

Crossref

International audienceWe report for the first time the presence of the snake mite, Ophionyssus natricis (Gervais) (Mesostigmata: Macronyssidae) on captive snakes kept in Panama City, Panama. This occurrence adds a new record to the geographical distribution of O. natricis as well as confirming its high prevalence on captive reptiles. Several Boidae species, Boa constrictor, Epicrates maurus, Corallus ruschenbergerii, Corallus caninus and a Pythonidae, Python regius were found infested with intensities varying from 10 to 2200 mites each. These findings represent the second record of O. natricis for Central America

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   Acarologia is proudly non-profit,with no page charges and free open accessPlease help us maintain this system byencouraging your institutes to subscribe to the print version of the journaland by sending us your high quality research on the Acari.Subscriptions: Year 2017 (Volume 57): 380 €http://www1.montpellier.inra.fr/CBGP/acarologia/subscribe.phpPrevious volumes (2010-2015): 250 € / year (4 issues)Acarologia, CBGP, CS 30016, 34988 MONTFERRIER-sur-LEZ Cedex, FranceACAROLOGIAA quarterly journal of acarology, since 1959Publishing on all aspects of the AcariAll information:   http://www1.montpellier.inra.fr/CBGP/acarologia/acarologia@supagro.inra.frAcarologia is under free license and distributed under the terms of the Creative Commons-BY-NC-ND which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.The digitalization of Acarologia papers prior to 2000 was supported by Agropolis Fondation under the reference ID 1500-024 through the « Investissements d’avenir » programme(Labex Agro: ANR-10-LABX-0001-01)Acarologia 57(2): 365–368 (2017)DOI: 10.1051/acarologia/20164161Occurrence of the mite Ophionyssus natricis (Acari: Macronyssidae) oncaptive snakes from PanamaRoberto J. MIRANDA1,3, John E. CLEGHORN2,3, Sergio E. BERMÚDEZ1,3, María A. PEROTTI4(Received 02 September 2016; accepted 03 October 2016; published online 20 April 2017; edited by Michel BERTRAND)1 Departamento de Investigación en Entomología Médica, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panamá.mirandarjc@gmail.com; bermudezsec@gmail.com2 Escuela de Biología, Universidad de Panamá. jecc008@gmail.com.3 Grupo de Estudios con Ectoparásitos.4 Evolutionary Biology and Ecology Section, School of Biological Sciences, University of Reading, United Kingdom. m.a.perotti@reading.ac.uk.ABSTRACT — We report for the first time the presence of the snake mite, Ophionyssus natricis (Gervais) (Mesostigmata:Macronyssidae) on captive snakes kept in Panama City, Panama. This occurrence adds a new record to the geograph-ical distribution of O. natricis as well as confirming its high prevalence on captive reptiles. Several Boidae species, Boaconstrictor, Epicrates maurus, Corallus ruschenbergerii, Corallus caninus and a Pythonidae, Python regius were found infestedwith intensities varying from 10 to 2200 mites each. These findings represent the second record of O. natricis for CentralAmerica.KEYWORDS — parasitic mites; reptile pets; Boidae; Pythonidae; PanamaThe exotic pet trade has reached worldwide pro-portions and involves a variety of wild animalsfrom invertebrates to vertebrates. The movementof these exotic pets incorporates the translocation ofmany zoonotic diseases and vectors, most of whichare still poorly studied and understood. Inverte-brates, either pets or vectors are perhaps the mostunderstudied. Chelicerates are a good example,with a huge body of literature lecturing on ticks(Ixodida) but very little on small parasitic mites ofexotic pets (Masan et al., 2012). Ophionyssus natri-cis (Gervais, 1844) is the most widespread mite-pestof captive reptiles, particularly snakes (Squamata).This preference for reptiles seems to be characteris-tic of the genus Ophionyssus. Of the 16 species of thisgenus, 15 have been reported as parasites of rep-tiles, with only one species described from a mam-mal (Moraza et al., 2009).Bites of O. natricis cause damages on the skinof captive reptiles, and if the level of infestation ishigh enough or out of control, it will consequentlylead to irritation, anemia and even death (Beck andPantchev, 2006, Hoppman and Wilson, 2007, Ratajet al., 2011). In addition, this mite is able to trans-mit pathogens as hemogregarines, Aeromonas spp.,being the mechanical vector of hemorrhagic sep-ticemia, caused by the motile anaerobic bacillusAeromonas hydrophila, and responsible of or asso-ciated with the still under investigation "InclusionBody Disease" (Camin, 1948; Yunker, 1956; Changand Jacobson, 2010; Mariana et al., 2011). O. natricisis of great concern to zoos, pet shops and privatehttp://www1.montpellier.inra.fr/CBGP/acarologia/ISSN 0044-586-X (print). ISSN 2107-7207 (electronic)365Miranda R.J. et al.TABLE 1: Instars of Ophionyssus natricis observed in subsamples collected from Boa constrictor and its terrarium. [MM: males; FF: females;x˙: average; σ: standard deviation].# females # males1 9 7 0,44 367 3832 7 6 0,46 398 4113 37 11 0,23 437 485Total 53 24 0,31 1202 1279ẋ 18 8 0,31 401 426σ 17 3 35 53% 4,2 1,9 93,9 100SubsamplesAdults Sex ratio (MM/FF+MM)Immature instars Totalcollections of reptiles, especially due to its abilityto spread fast from a single parasitized animal toothers in the same enclosure or nearby (Rodríguezand Lazcano, 1992). Despite being pests of specificreptile hosts, O. natricis can opportunistically moveto other hosts, like other blood sucking mites do,particularly in the domestic environment, e.g. likethose in the families Macronyssidae, Dermanyssi-dae and Laelapidae (O’Donel Alexander, 1984), andwhenever there is a shortage of food or the infes-tation is too severe, implying high competition forresources, the mites are able to affect humans, suchas pet owners, keepers and handlers of infestedsnakes (Hoppman and Wilson, 2007; Rataj et al.,2011; Amanatfard et al., 2014).Ophionyssus natricis was first described from na-tive European snakes and later became associatedwith captive reptiles of different biogeographical re-gions (Fain, 1962; Domrow, 1985; Fain and Bannert,2000; Paredes-León et al., 2008), with just a hand-ful of papers mentioning infestation of wild snakes(Yunker, 1956, Simonov and Zinchenko, 2010).To date, O. natricis have been reported in Africa(Yunker, 1956), Europe (Beck and Pantchev, 2006;Simonov and Zinchenko, 2010), Oceania (Domrow,1985), Asia (Mariana et al., 2011), and America(Schroeder, 1934; Camin, 1948). Specifically for theNeotropical region, O. natricis has been only re-ported from Mexico (Rodríguez and Lazcano, 1992;Paredes-León et al., 2008) and Nicaragua (Rimbaudet al., 2006).This is the first report documenting O. natricis oncaptive snakes from the City of Panama, Panama.Occurrence of mites was recorded between Mayand June 2015, from homes that kept reptiles aspets, captive in small micro-cosmos. The findingsincluded five species of snake-hosts: Boa constrictorLinnaeus, 1758, Epicrates maurus Gray 1849, Corallusruschenbergerii (Cope, 1876), Corallus caninus (Lin-naeus, 1758) and Python regius (Shaw, 1802). Thesnakes had been living in captivity in their respec-tive homes for several months (9-48 months). Inall cases they were maintained in individual terrar-iums constructed with wooden frames, glass walls,and with wood paper as substrate. The owners in-dicated that the snakes were more aggressive thanusual, and any severe skin damage was observedand recorded. After collection of mites from thesnakes, all snakes and terrariums were treated withFipronex® and the success of the control became ev-ident days later.The ectoparasites were removed manually byone of the authors (JEC), and preserved by plac-ing them in vials with 70% ethanol. Once in thelaboratory, a sample of 30 mites (randomly takenfrom the 5 snakes) was treated with 10% NaOH andmounted using Hoyer’s medium. Species identi-fication followed the key of Moraza et al. (2009).The slides were deposited into the "Dr. Eustor-gio Mendez" Zoological Collection of the GorgasMemorial Institute.The number of mites collected on E. maurus, C.ruschenbergerii, C. caninus and P. regius was between10-50 specimens. Remarkable was the infestation366Acarologia 57(2): 365–368 (2017)over Boa constrictor and its terrarium, estimatingthat there were approximately 4000 individuals, es-timation based on three subsamples of 2 ml each(Table 1). Most specimens were immature stagesand adults (females) (Figure 1). Empty puparia ofPhoridae flies and some individuals of Glycycome-tus malaysiensis (Fain and Nadchatram, 1980) (Aero-glyphidae) were also present in this sample.FIGURE 1: Habitus of Ophionyssus natricis female, collected fromBoa constrictor terrarium. Scale bar = 0.35 mm.Previous reports of mites parasitizing pet-reptiles in Panama include a tick species close toAmblyomma flavomaculatum on Varanus exanthemati-cus (Bosc, 1792) (Bermúdez and Miranda, 2011), thepterygosomatid mite Geckobiella stamii Hirst, 1917on Iguana iguana (L. 1758) (Murgas et al., 2013)and the argasid tick Ornithodoros puertoricensis Fox1947 on Varanidae and Pythonidae (Bermúdez et al.,2015).The predominance of females (Table 1, sex ra-tio) and immature stages was noted earlier by Dom-row (1985) and Mariana et al. (2011), and thesetwo works emphasised that a single female couldgenerate a large offspring. In fact, a female biasis the canon for haplodiploid species and O. na-tricis is one of them, this is also a common fea-ture of many Macronyssidae. They reproduce byarrhenotokous parthenogenesis, where females arediploid and males are the result of unfertilized eggs(Oliver, 1966). Its nidicolous behavior correspondswell with acarine haplodiploid clades having adap-tations to live in patchy or ephemeral environments(Perotti and Braig, 2009).This mite species must be considered a risk tohumans, pet owners or keepers, in addition to rep-tiles, due to the stress caused by the implicit bitesand further infection (Schultz, 1975, Rataj et al.,2011, Amanatfard et al., 2014). There is also an extrarisk for humans handling animals, especially if thesnakes are not normally aggressive, because this be-havior increases with high infestations of O. natricis(Amanatfard et al., 2014).Finally, the infestations of captive animals by O.natricis should be considered as a serious risk in thetrade business and maintenance procedures of ex-otic reptiles, and efforts should focus on keepingcaptive animals under periodic health checks andunder treatment. The application of biological con-trol methods including the use of predatory mitessuch as Laelapidae and/or Cheyletus (Schillinger etal., 2013) or the applications of low toxicity aca-ricide compounds (Rodríguez and Lazcano, 1992)have proven to be successful and affordable to keepcaptive pets in good health.ACKNOWLEDGEMENTSWe are grateful to Lionel Schillinger (Cliniquevétérinaire du village d’Auteuil, France) for provid-ing literature. doi:REFERENCESBeck W., Pantchev N. 2006 — Schlangenmilbenbefall(Ophionyssus natricis) beim Grünen Leguan (Iguanaiguana)- Ein Fallbericht — Kleintierpraxis, 51, 3-7.Bermúdez S., Miranda R. 2011 — De mascotas exóticasy turistas: nuevas oportunidades para la introducciónde ectoparásitos en Panamá — Bol. SEA, 48, 491-492.Bermúdez S., Miranda R., Cleghorn J., Venzal J. 2015 —Ornithodoros (Alectorobius) puertoricensis (Ixodida: Ar-367Miranda R.J. et al.gasidae) parasitizing exotic reptiles pets in Panama—Rev. FAVE- Cienc. 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Acarologia is under freelicense. This open-access article is distributed under theterms of the Creative Commons-BY-NC-ND which per-mits unrestricted non-commercial use, distribution, andreproduction in any medium, provided the original au-thor and source are credited.368