Tohru Fukase

Yukari Nakamura

ナカムラ ユカリ

フカセ トオル

中村 有加里

深瀬 徹

Nakamura, Yukari

ナカムラ, ユカリ

Fukase, Tohru

フカセ, トオル

AROUS Academic Repository of Okayama University of Science / 岡山理科大学学術リポジトリ

Naturalistae 27: 15-17 (Feb. 2023) © 2023 by Okayama University of Science, PDF downloadable at http://www1.ous.ac.jp/garden/- 15 -　Short ReportPrevalence of a mesostigmatic mite, Dermanyssus species (Arachnida: Mesostigmata: Dermanyssidae) in Pallas’s squir-rels, Callosciurus erythraeus in Kanagawa Prefecture, JapanYukari NAKAMURA1* & Tohru FUKASE2 Abstract: To elucidate the prevalence of a mesostigmatic mite, Dermanyssus species, in Pallas’s squirrel, Callosciurus erythraeus, a species invasive to Japan, 240 specimens of the squirrels were examined for the mites during April, 2020-March, 2022. After the squirrels had been captured by the administrative agency as part of a capture policy against harmful mammals in Zushi-shi, a munici-pality in a southern area of Kanagawa prefecture, the animals were euthanized using carbon dioxide inhalation. Dermanyssus mites were detected on three of the squirrels. The collected mites were iden-tified, based on their morphology, as Dermanyssus species, probably D. gallinae, which usually use birds as their major hosts and are often associated with the poultry industry. Infestation of the Pallas’s squirrels by this mite species, even if by accidental parasitism, is thought to occur once in a while. Although the infection source of the mites to the squirrels was unknown, the possibility exist that the mites infested the squirrels when they intruded into poultry houses. Some mammals such as Pallas’s squirrels might be connected with Dermanyssus mite migration.1. Department of Veterinary Medicine, Faculty of Veterinary Medicine, Okayama University of Science, 1-3 Ikoi-no-oka, Imabari-shi, Ehime 794-8555, Japan. 岡山理科大学獣医学部獣医学科，〒794-8555 愛媛県今治市いこいの丘1-3．2. Laboratory of Epidemiology, Department of Veterinary Medicine, Faculty of Veterinary Medicine, Okayama University of Science, 1-3 Ikoi-no-oka, Imabari-shi, Ehime 794-8555, Japan. 岡山理科大学獣医学部獣医学科疫学講座，〒794-8555 愛媛県今治市いこいの丘1-3．*Correspondence: Yukari NAKAMURA, E-mail: y-nakamura@ous.ac.jpI. IntroductionThe Pallas’s squirrel, Callosciurus erythraeus, a species of the family Sciuridae, was original-ly distributed in Southeast Asia from Assam, Arunachal Pradesh, Manipur, and Meghalaya in northeastern India to Myanmar, the Malay Peninsula, Thailand, eastern Cambodia, Laos, and Vietnam, in addition to southeastern China, Hainan Island, and Taiwan. This species of squir-rel has invaded some countries of the world as an alien invasive species (Lurz et al. 2013). In Japan, a subspecies of this squirrel, C. e. flavimanus (synonym: C. e. thaiwanensis, a formerly used subspecies name in Japan), which is not native to Japan, has populated some areas such as Kanaga-wa and Shizuoka prefectures (Tamura 2004, Su-zuki & Torii 2016). Pallas’s squirrels cause such problems as peeling of tree bark, trespassing into houses, and mastication of electric wires, as well as adversely influencing native biogeocenosis (Tamura & Miyamoto 2005). Therefore, alien Pallas’s squirrels cause numerous social problems related to human life in Japan. Some municipali-ties are striving to capture all individuals of this squirrel species.We earlier detected four adult Dermanyssus mites, probably D. gallinae, unexpectedly from the body surface of one Pallas’s squirrel speci-men in April, 2019 (Nakamura & Fukase 2022). Usually, individuals of D. gallinae use birds as the major host animal and often occur in associa-tion with the poultry industry, for which they are recognized as a harmful ectoparasite species of chickens. At the time in 2019, the infestation was presumed not to be prevalent because the mites were not detected from the other 26 squirrels which were captured almost simultaneously in the same area. Nevertheless, there might be some value in investigating the prevalence of this mite species in Pallas’s squirrels, even if the infestation occurs accidentally, because a new host-parasite relationship might occur between an alien mam-mal host and an existing ectoparasite mite.This study was conducted to elucidate the prevalence of Dermanyssus mites among the squirrels.Fig. 1. Dermanyssus species (female, adult) collected from a Pallas’s squirrel, Callosciurus erythraeus. Scale bar = 100 µm.- 16 -NAKAMURA & FUKASEII. Materials and MethodsA research survey was conducted during April, 2020-March, 2022 for 240 Pallas’s squirrel spec-imens that were provided from the administrative agency of Zushi-shi, a municipality located in a southern area of Kanagawa prefecture, Japan. The animals had been captured as part of a capture policy against harmful mammals in Zushi-shi, and then had been euthanized by the agency using carbon dioxide inhalation. For the present study, 10 specimens were selected each month randomly in the order of capture during the research peri-od. The body surface of each squirrel specimen was observed in great detail under a magnifying glass to detect Dermanyssus mites. In addition, the hairs of the squirrels were combed vigorously with a flea comb and a slicker brush on a piece of white-colored paper to search for dropped mites.When the mites were collected, they were fixed and preserved using 70% (V/V) ethanol aqueous solution. Subsequently, the preserved mites were dehydrated and then permeated with xylene to be observed morphologically under a light microscope.III. ResultsMites were detected from three of the squirrels, which had been captured respectively in June, September, and October, 2020. These three squir-rels, all adults, were one female and two males. The numbers of the mites obtained from the three squirrels were one from one squirrel and two each from the other two squirrels (Table 1). Skin lesions were not observed in the three squirrels.The detected mites were all adult females (Fig. 1). Their external morphology indicated 0.8 - 1.0 mm idiosoma length, 0.5 - 0.7 mm idiosoma width, a rounded posterior part of the idiosoma, and elongated and stylet-like chelicerae. One pair of stigmata was observed around the coxae of legs II and III. Setae on the idiosoma formed rows. The dorsal plate on the dorsal side was an elongated pentagon, the forward edge of which was angular. Its rear edge was narrow and almost linear. On the ventral side, the sternal plate was broad and bearing two pairs of sternal setae. The genitoventral plate was ligulate. The anal plate was broad and nearly triangular with forward and rear edges that were, respectively, linear and semicircular. The anus opened at the posterior part of anal shield. One of the five detected mites was observed to have sucked blood. From these morphological findings, the mites were identified as belonging to the genus Dermanyssus. They are particularly regarded as having morphological features corresponding to those of the poultry red mite D. gallinae.IV. DiscussionMany Dermanyssus mite species have been described (Roy & Chauve 2009). Of the mites of this genus, D. gallinae has been found mostly with various species of birds and mammals such as rodents, in addition to occurrence at chicken ranches (Pritchard et al. 2015). Nevertheless, no report had described Dermanyssus mites detected from Pallas’s squirrels. Some examples for the ab-sence of Dermanyssus mites in Pallas’s squirrels were obtained through investigations conducted in Japan (Shinozaki et al. 2004) or in Argentina (Gozzi et al. 2013). Whereas, we earlier reported the collection of Dermanyssus mites from a Pal-las’s squirrel in 2019 (Nakamura & Fukase 2022). The findings of the present research reinforce the inference that Pallas’s squirrels can be a host to Dermanyssus mites, even if the prevalence of the mite species is very low in the squirrel population.A strange phenomenon arises with respect to the cathemerality of the mite species and its host squirrel species. Dermanyssus mites are noctur-nal. Therefore, they parasitize their hosts to suck blood during times of darkness. They lurk in cracks and crevices behind objects during other times (Knežević et al. 2017, Gay et al. 2020). Pallas’s squirrels, by contrast, are diurnal (Lurz et al. 2013). It might seem strange that the noctur-nal mites were detected from the diurnal Pallas’s squirrel because the squirrel probably had few opportunities to be infested by the nocturnal mites when the animals were active. Stated differently, when the mites appear from their hiding places to suck the blood of host animals, the squirrels are sleeping at a separated place from the mites’ habitats. A possibility for infestation is that the mites had already inhabited the nests of the squir-rels. Even if that were so, however, the intrusion route of the mites to the nests remains unclear.Although providing a sufficient explanation for infestation of the Pallas’s squirrels by the mites Sex Head and bodylength (cm)Tail length (cm)Body weight (g)Time when miteswere detectedNo. of mitescollectedFemale 20 18 321 Jun. 2020 2Male 21 20 335 Sep. 2020 1Male 22 20 347 Oct. 2020 2Table 1. Summary of the Pallas’s squirrels from which Dermanyssus mites were collected.- 16 -NAKAMURA & FUKASEII. Materials and MethodsA research survey was conducted during April, 2020-March, 2022 for 240 Pallas’s squirrel spec-imens that were provided from the administrative agency of Zushi-shi, a municipality located in a southern area of Kanagawa prefecture, Japan. The animals had been captured as part of a capture policy against harmful mammals in Zushi-shi, and then had been euthanized by the agency using carbon dioxide inhalation. For the present study, 10 specimens were selected each month randomly in the order of capture during the research peri-od. The body surface of each squirrel specimen was observed in great detail under a magnifying glass to detect Dermanyssus mites. In addition, the hairs of the squirrels were combed vigorously with a flea comb and a slicker brush on a piece of white-colored paper to search for dropped mites.When the mites were collected, they were fixed and preserved using 70% (V/V) ethanol aqueous solution. Subsequently, the preserved mites were dehydrated and then permeated with xylene to be observed morphologically under a light microscope.III. ResultsMites were detected from three of the squirrels, which had been captured respectively in June, September, and October, 2020. These three squir-rels, all adults, were one female and two males. The numbers of the mites obtained from the three squirrels were one from one squirrel and two each from the other two squirrels (Table 1). Skin lesions were not observed in the three squirrels.The detected mites were all adult females (Fig. 1). Their external morphology indicated 0.8 - 1.0 mm idiosoma length, 0.5 - 0.7 mm idiosoma width, a rounded posterior part of the idiosoma, and elongated and stylet-like chelicerae. One pair of stigmata was observed around the coxae of legs II and III. Setae on the idiosoma formed rows. The dorsal plate on the dorsal side was an elongated pentagon, the forward edge of which was angular. Its rear edge was narrow and almost linear. On the ventral side, the sternal plate was broad and bearing two pairs of sternal setae. The genitoventral plate was ligulate. The anal plate was broad and nearly triangular with forward and rear edges that were, respectively, linear and semicircular. The anus opened at the posterior part of anal shield. One of the five detected mites was observed to have sucked blood. From these morphological findings, the mites were identified as belonging to the genus Dermanyssus. They are particularly regarded as having morphological features corresponding to those of the poultry red mite D. gallinae.IV. DiscussionMany Dermanyssus mite species have been described (Roy & Chauve 2009). Of the mites of this genus, D. gallinae has been found mostly with various species of birds and mammals such as rodents, in addition to occurrence at chicken ranches (Pritchard et al. 2015). Nevertheless, no report had described Dermanyssus mites detected from Pallas’s squirrels. Some examples for the ab-sence of Dermanyssus mites in Pallas’s squirrels were obtained through investigations conducted in Japan (Shinozaki et al. 2004) or in Argentina (Gozzi et al. 2013). Whereas, we earlier reported the collection of Dermanyssus mites from a Pal-las’s squirrel in 2019 (Nakamura & Fukase 2022). The findings of the present research reinforce the inference that Pallas’s squirrels can be a host to Dermanyssus mites, even if the prevalence of the mite species is very low in the squirrel population.A strange phenomenon arises with respect to the cathemerality of the mite species and its host squirrel species. Dermanyssus mites are noctur-nal. Therefore, they parasitize their hosts to suck blood during times of darkness. They lurk in cracks and crevices behind objects during other times (Knežević et al. 2017, Gay et al. 2020). Pallas’s squirrels, by contrast, are diurnal (Lurz et al. 2013). It might seem strange that the noctur-nal mites were detected from the diurnal Pallas’s squirrel because the squirrel probably had few opportunities to be infested by the nocturnal mites when the animals were active. Stated differently, when the mites appear from their hiding places to suck the blood of host animals, the squirrels are sleeping at a separated place from the mites’ habitats. A possibility for infestation is that the mites had already inhabited the nests of the squir-rels. Even if that were so, however, the intrusion route of the mites to the nests remains unclear.Although providing a sufficient explanation for infestation of the Pallas’s squirrels by the mites Sex Head and bodylength (cm)Tail length (cm)Body weight (g)Time when miteswere detectedNo. of mitescollectedFemale 20 18 321 Jun. 2020 2Male 21 20 335 Sep. 2020 1Male 22 20 347 Oct. 2020 2Table 1. Summary of the Pallas’s squirrels from which Dermanyssus mites were collected.- 17 -Dermanyssus mites on alien squirrels, Callosciurus erythraeusis difficult, one hypothesis is that the squirrels of the present cases had acted exceptionally during nighttime. During the night, the squirrels might have been infested by the mites and captured by traps soon after: before the mites returned to their hiding places. Alternatively, a mite that infested a squirrel during nighttime might not return to its hiding place because of the squirrel’s movement from place to place.In addition, the existence of poultry red mites on squirrels during the daytime cannot be denied because a certain population of them are reported as invariably found on chicken body surfaces differing from the general behavior of the mite species (Nakamae et al. 1997a, 1997b).However, lack of detection of the mites in any of the other 237 Pallas’s squirrels indicates that the mite infestation is not rife among the animals living in that area. Accordingly, infestation found in the present case of the squirrel was not inferred as representing a prevalent condition.The place at which the three mite-positive squirrels had been infested by the mites was un-certain. The possibility exists that the infestation occurred at a nearby chicken ranch if the squirrels had invaded such a structure. Another possibility is that animals such as the Pallas’s squirrel might facilitate the transfer of Dermanyssus mites among chicken ranches, even though the preva-lence of the mites is very low among the squirrels.AcknowledgmentsWe thank Mr. Akihito Nishida of Sanei Sho-doku Corporation for providing the squirrel specimens.ReferencesGay, M., Lempereur, L., Francis, F. & Megido, R. C. (2020) Control of Dermanyssus gallinae (De Geer 1778) and other mites with volatile organic compounds, a review. Parasitology 147: 731-739.Gozzi, A. C., Guichón, M. L., Benitez, V. V. & Lareschi, M. (2013) Arthropod parasites of the red-bellied squirrel Callosciurus erythraeus introduced into Argentina. Medical and Veterinary Entomology 27: 203-208.Knežević, S., Pajić, M., Petrović, A., Vidaković, S., Babić, J., Živkov-Baloš, M., Pušic, I., Savić, S. & Stojanov, I. (2017) Dermanyssus gallinae - overview: life cy-cle, morphology, prevalence and control measures in poultry farms. Arhiv Veterinarske Medicine 10: 53-62.Lurz, P. W. W., Hayssen, V., Geissler, K. & Bertolino, S. (2013) Callosciurus erythraeus (Rodentia: Sciuridae). Mammalian Species 45: 60-74.Nakamae, H., Fujisaki, K., Kishi, S., Yashiro, M., Oshiro, S. & Furuta, K. (1997a) The new parasitic ecology of chicken mites Dermanyssus gallinae, parasitizing and propagating on chickens even in the day time. Japanese Poultry Science 34: 110-116.Nakamae, H., Kishi, S., Fujisaki, K., Oshiro, S. & Furuta, K. (1997b) Incidence of the parasitism of chicken mite Dermanyssus gallinae parasitizing and propagating on chicken even in the day time and their life cycle. Japanese Poultry Science 34: 240-247.Nakamura, Y. & Fukase, T. (2022) A mesostigmatic mite, Dermanyssus species collected from a Pallas’s squir-rel, Callosciurus erythraeus. Naturalistae 26: 43-45.Pritchard, J., Kuster, T., Sparagano, O. & Tomley, F. (2015) Understanding the biology and control of the poultry red mite Dermanyssus gallinae: a review. Avian Pa-thology 44: 143-153.Roy, L. & Chauve, C. (2009) The genus Dermanyssus (Mesostigmata: Dermanyssidae): history and species characterization. In: Sabelis, M. W. & Bruin, J. (eds.), Trends in Acarology: Proceedings of the 12th Inter-national Congress, pp. 49-55, Springer Netherlands.Shinozaki, Y., Shiibashi, T., Yoshizawa, K., Murata, K., Kimura, J., Maruyama, S., Hayama, Y., Yoshida, H. & Nogami, S. (2004) Ectoparasites of the Pallas squirrel, Callosciurus erythraeus, introduced to Japan. Medical and Veterinary Entomology 18: 61-63.Suzuki, K. & Torii, H. (2016) Range expansion of invasive Callosciurus squirrels in Hamamatsu City, Shizuoka Prefecture. Mammalian Science 56: 199-205.Tamura, N. (2004) Population dynamics and expansion of introduced Formosan squirrels in Kanagawa Prefec-ture, Japan. Japanese Journal of Conservation Ecology 9: 37-44.Tamura, N. & Miyamoto, A. (2005) Countermeasures against expansion of the alien Formosan squirrel in Kanagawa. Natural History Report of Kanagawa 26: 57-60.中村有加里・深瀬徹：神奈川県で捕獲されたクリハラリスCallosciurus erythraeus におけるDermanyssus属ダニの寄生状況要約われわれは2019年４月に神奈川県において捕獲されたクリハラリス１匹の体表から偶発的にDermanyssus属ダニを検出したが，これにもとづいて2020年４月から2022年３月の２年間に同地域で捕獲されたクリハラリスにおけるこのダニの寄生割合を検索した．毎月10匹のクリハラリスを検査した結果，2020年６月と９月，10月に各１匹から１-２個体のDermanyssus属ダニの雌成ダニが検出され，これらはワクモ（D. gallinae）である可能性が高いと考えた．ワクモは養鶏場に多発する鶏の外部寄生虫として知られており，クリハラリスが養鶏場に侵入した際に，その寄生を受けたことを考察した．また，偶発的にしてもワクモの寄生を受けたクリハラリスは，このダニの蔓延に関与する可能性がある．(Accepted 6 December 2022) 

Prevalence of a mesostigmatic mite, Dermanyssus species (Arachnida: Mesostigmata: Dermanyssidae) in Pallas’s squirrels, Callosciurus erythraeus in Kanagawa Prefecture, Japan

https://ous.repo.nii.ac.jp/?action=repository_action_common_download&item_id=3243&item_no=1&attribute_id=18&file_no=1

カナガワケン デ ホカク サレタ クリハラリス Callosciurus erythraeus ニオケル Dermanyssusゾク ダニ ノ キセイ ジョウキョウ

カナガワケンデホカクサレタクリハラリス Callosciurus erythraeus ニオケル Dermanyssusゾクダニノキセイジョウキョウ

Abstract

Similar works

Full text

Available Versions

AROUS Academic Repository of Okayama University of Science / 岡山理科大学学術リポジトリ

カナガワケン デ ホカク サレタ クリハラリス Callosciurus erythraeus ニオケル Dermanyssusゾク ダニ ノ キセイ ジョウキョウ

Abstract

Similar works

Full text

Available Versions

AROUS Academic Repository of Okayama University of Science / 岡山理科大学学術リポジトリ

カナガワケンデホカクサレタクリハラリス Callosciurus erythraeus ニオケル Dermanyssusゾクダニノキセイジョウキョウ