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A New Demodecidae () from the Yellow-Necked flavicollis (Rodentia: )—Description with Data on Parasitism

Article in Journal of Parasitology · June 2012 DOI: 10.1645/GE-3018.1 · Source: PubMed

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A NEW DEMODECIDAE SPECIES (ACARI) FROM THE YELLOW-NECKED MOUSE APODEMUS FLAVICOLLIS (RODENTIA: MURIDAE)—DESCRIPTION WITH DATA ON PARASITISM

Joanna N. Izdebska Department of Invertebrate Zoology and Parasitology, University of Gdansk,´ Wita Stwosza 59, 80-308 Gdansk,´ Poland. e-mail: [email protected]

The Journal of the American Society of Parasitologists

J. Parasitol., 98(6), 2012, pp. 1101–1104 Ó American Society of Parasitologists 2012

A NEW DEMODECIDAE SPECIES (ACARI) FROM THE YELLOW-NECKED MOUSE APODEMUS FLAVICOLLIS (RODENTIA: MURIDAE)—DESCRIPTION WITH DATA ON PARASITISM

Joanna N. Izdebska Department of Invertebrate Zoology and Parasitology, University of Gdansk,´ Wita Stwosza 59, 80-308 Gdansk,´ Poland. e-mail: [email protected]

ABSTRACT: This paper describes morphological characteristics and the occurrence of corniculatus n. sp., which was found on Apodemus flavicollis in Poland. The yellow-necked murid mouse is a common European ; until now, it was parasitized by a single demodectic species, Demodex rosus, which occurs in the oral cavity and esophagus. The new species was found in hair follicles, particularly within hairy regions of the head and genital–anal area. Demodex corniculatus occurred in 33% of the yellow- necked mice examined. The new species is small (adult stages 140 lm in length); characteristic features of these are massive supracoxal spines (ca. 5–6 lm long) on the dorsal side of the gnathosoma and palps with thick-set, bifurcated terminal spines. This paper also contains a checklist of demodecids in European and cosmopolitan murids.

Demodecidae is a family of parasitic mites characterized not coxal spines, ca. 5–6 long (Figs. 1, 2A, 4A); palps with thickset, bifurcated only by host specificity but also by topical specificity. Synhospital terminal spines (Fig. 2A). Opisthosomal organ present in both sexes, species of demodectic mites occur frequently in different slightly arc-shaped. Adult stages characterized by clear sexual dimor- phism. Females larger than males (almost 30%) with more elongated . They live in various microhabitats of the skin including opisthosoma as compared with males. Supracoxal spines, spines of palps hair follicles of common or sensory hairs, miscellaneous glands and claws slightly smaller in females. and their efferent ducts, or outer layers of epidermis (Bukva, Male (holotype): Body length 122.5 (mean 123.7, n ¼ 16, including 1991; Izdebska, 2010). Some are even associated with the anterior holotype), with width of 23.8 (mean 23.4) (Figs. 1A, 3; Table I). sections of the digestive tract (Nutting et al., 1973; Desch, 1991). Gnathosoma rectangular, oblong (longer than base width); dorsal side This specialization induces development of preferences regarding with 2 solid supracoxal spines, ca. 6 long (Figs. 1A, 2A), which extend the location selection. Accordingly, in species of Apodemus, from edges of gnathosoma, nearly contact each other close to center. demodectic mite species were described that were associated with Three-segmented palps with massive, bifurcated terminal spines (ca. 5.5 common hair follicles (Demodex arvicolae apodemi), sensory hair follicles within the nose region (Demodex longior), glands near the eyes (Demodex lacrimalis, Demodex huttereri, Ophthalmodex apodemi), glands in the ears (Demodex agrarii), and in the oral cavity and esophagus (Demodex rosus) (Hirst, 1919; Lukoschus and Jongman, 1974; Mertens et al., 1983; Bukva et al., 1985, 1992; Bukva, 1994; Izdebska and Cydzik, 2010). Altogether, 13 species of demodectic mites have been identified from European murid including 1 species, D. rosus, reported in the common yellow-necked mouse Apodemus flavicollis. The present paper describes a new species of Demodex from A. flavicollis.

MATERIALS AND METHODS Thirty specimens of the yellow-necked mouse Apodemus flavicollis from the Pomerania region of Poland were examined for ectoparasites in 2009. Skin samples 1-cm2 were collected from the mice from several regions of the body including the head (around eyes, ears, sensory hairs of a nose, lips, and chin), nape, belly, dorsum, limbs, and the genital–anal region. The skin samples were examined for the presence of demodectic mites using the standard method for digestion (Izdebska, 2004), i.e., samples were digested in 10% KOH solution, decanted, and examined using a phase-contrast microscope. The mite specimens recovered were measured and placed in Faure’s solution. All measurements are in micrometers unless otherwise noted. In order to define the level of host infestation, the main parasitological parameters were enumerated, i.e., the prevalence (percentage of infested hosts) and the mean intensity (the average number of parasites in infested hosts).

DESCRIPTION Demodex corniculatus n. sp. (Figs. 1–3, Table I)

Diagnosis: Small follicle mite (adult stages 140 in length) in hairy skin of yellow-necked mouse. On dorsal side of gnathosoma, 2 massive supra-

Received 21 October 2011; revised 8 June 2012; accepted 13 June 2012. FIGURE 1. Demodex corniculatus n. sp. (A) Male, dorsal view; (B) DOI: 10.1645/GE-3018.1 female, ventral view.

1101 1102 THE JOURNAL OF PARASITOLOGY, VOL. 98, NO. 6, DECEMBER 2012

Taxonomic summary Host and locality: The yellow-necked mouse, Apodemus flavicollis (Melchior, 1834), hosts were trapped in Pomerania (548190N, 188120E; 548150N, 188140E), Poland, in March 2009. Holotype (No 41/09) was collected from A. flavicollis. Deposition of materials: Preparations with the specimens were stored in the collection of the Department of Invertebrate Zoology and Parasitol- ogy at the University of Gdansk´ (Holotype male, RAfDc01, 27 paratypes RAfDc02–RAfDc28). Etymology: The specific epithet corniculatus (horned, crescent-shaped) refers to the massive supracoxal spines and the shape of the spines on the palps (Figs. 1A, 2A, 3, 4A). Distribution and intensity of infection: Demodex corniculatus exhibited a prevalence of 33.3% in yellow-necked mice, with the mean intensity of 2.8 specimens per host. Fragments of skin possessed exclusively adult specimens (16 males, 12 females) and some oval eggs. Because the level at infestation was very low, no lesions were observed. All specimens were found in the hairy skin of the head (eyelids, cheeks, ears, and chin) and in the skin of the genital–anal area. Male mice were more frequently infested (7 of 15 males, 3 of 15 females).

DISCUSSION

The yellow-necked mouse is a common rodent living through- out most of Europe and some parts of Asia. Its parasitofauna is relatively well explored, but to date only 1 species of Demodex mite has been reported for this mouse species; it is associated with the oral cavity and anterior sections of the digestive tract (Bukva et al., 1985). From 2 to 4 species of Demodex mites have been recorded from other murid rodents in Europe (Table II). FIGURE 2. Demodex corniculatus n. sp., male. (A) Gnathosoma, With respect to morphological features and site of infection, the ventral view; (B) aedeagus; (C) opisthosomal organ. new species seems most similar to D. arvicolae, which has been reported from among the European murids and voles. Highly long). On ventral side of gnathosoma, oval pharyngeal bulb with distinct specialized demodecid species are usually associated with just 1 subgnathosomal setae on both sides (Fig. 2A). Four pairs of 6- host species. However, D. arvicolae has been observed in house segmented legs on podosoma which project beyond its edges; 2 solid claws on each tarsal segment. Epimeral plates narrow, rectangular (pair mice, striped field and wood mice, short-tailed and common voles, II and III) or trapezoidal (pair I and IV) (Fig. 3). Opisthosoma and the bank vole (Hirst, 1919). Four D. arvicolae subspecies have constitutes ca. 55% of body length (Table I), straight, somewhat been identified, although they are also often recognized as distinct narrower than podosoma, slightly tapered toward end, clearly striated. species in different hosts. Moreover, subspecies from different Opisthosomal organ present, slightly arc-shaped (Fig. 2C). An aedeagus (mean 21.9 long) on dorsal side, situated between third and first pair of hosts are characterized by great morphological heterogeneity. legs (Figs. 1A, 2B). Therefore, it seems that D. arvicolae is a species that requires Female: Females more slender and longer than males; body length taxonomic revision (Izdebska, 2000). 155.9, width 25.9 (Table I). Shape and morphological details of A common trait of D. arvicolae is the presence of massive gnathosoma similar to male. Spines on palpi slightly smaller (ca. 5 long), supracoxal spines on the dorsal side of the gnathosoma, more less massive; also, supracoxal spines somewhat smaller (ca. 4.5 long) and finer (Fig. 1B). Podosoma more elongated as compared with male; legs prominent compared with other demodecids. In addition, the smaller, also with double claws. Epimeres narrow, pairs II, III, and IV spines differ to some extent, among different forms from rectangular, pair I trapezoidal (Fig. 1B). Opisthosoma 60% of body length particular host species, in their size, shape, and location. In this (Table I), clearly striated, elongated, in widest place slightly wider than respect, D. corniculatus is most similar to the D. arvicolae widest place of podosoma; gradually tapered toward end. Opisthosomal organ present, similar as in male, but less curved. Vulva (11.7 long) on apodemi; its spines, however, are bigger, more massive, and of a abdominal side, located below incision of pair IV of epimeral plates (Fig. different shape (Fig. 4). It also differs from D. arvicolae in the 1B). shape of spines on the palpi (large, massive, bifurcated). Sexual

FIGURE 3. Demodex corniculatus n. sp., male. IZDEBSKA—DEMODEX CORNICULATUS N. SP. 1103

TABLE I. Body size [lm] of Demodex corniculatus n. sp.

Morphologic features Male (n ¼ 16) Female (n ¼ 12)

Length of gnathosoma 14.7 (10.5–17.5), SD 2.8 16.4 (13.0–17.5), SD 1.7 Width of gnathosoma (at base) 13.3 (10.0–17.3), SD 2.4 14.8 (12.5–17.6), SD 1.8 Length of podosoma 42.7 (36.3–50.1), SD 4.3 47.6 (37.5–53.0), SD 5.2 Width of podosoma 23.4 (20.1–27.5), SD 2.2 21.1 (17.5–23.7), SD 1.7 Length of opisthosoma 69.4 (57.5–92.4), SD 8.8 91.9 (72.5–130.1), SD 21.8 Width of opisthosoma 22.9 (20.0–27.5), SD 2.5 25.9 (20.2–28.8), SD 3.0 Aedeagus 21.9 (18.0–25.0), SD 2.1 — Vulva — 11.7 (9.0–16.3), SD 3.1 Total length of body 123.7 (111.8–157.5), SD 12.1 155.9 (136.3–199.8), SD 23.6 dimorphism in these 2 species is expressed in a different way. widened towards the end), they have similar dimensions. In D. Although in D. arvicolae specimens of both sexes often differ in corniculatus, the female is much larger (almost 30%) than males, proportions, e.g., the ratio of the podosoma width to the slender, elongated, with the opisthosoma tapering posteriorly. In opisthosoma and in shape (opisthosoma of females is sometimes D. a. apodemi, the aedeagus is blaze-shaped and is situated

TABLE II. Occurrence of demodecids in murid rodents.

Host Species of Demodecidae Records

Apodemus agrarius (Pallas, 1771) Demodex agrarii Bukva, 1994 Slovak Republic (Bukva, 1994) Poland (Izdebska and Cydzik, 2010) Demodex apodemi (Hirst, 1918) (¼ Demodex Russia (Bregetova et al., 1955) arvicolae apodemi Hirst, 1918) Poland (Izdebska and Cydzik, 2010) Demodex huttereri Mertens, Lukoschus, and Germany (Mertens et al., 1983) Nutting, 1983 Apodemus flavicollis (Melchior, 1834) Demodex rosus Bukva, Vitovec and Vlcek, 1985 Czech Republic (Bukva et al., 1985) Demodex corniculatus n. sp. Poland (present) Apodemus sylvaticus Linnaeus, 1758 Demodex apodemi (Hirst, 1918) (¼ Demodex England (Hirst, 1919) arvicolae apodemi Hirst, 1918) Russia (Bregetova et al., 1955) Demodex lacrimalis Lukoschus and Jongman, Netherlands, Italy (Lukoschus and Jongman, 1974) 1974 Demodex longior Hirst, 1918 England (Hirst, 1919) Russia (Bregetova et al., 1955) Ophthalmodex apodemi Bukva, Nutting, and Czech Republic, Netherlands (Bukva et al., 1992) Desch, 1992 musculus Linnaeus, 1758 Demodex flagellurus Bukva, 1985 Czech Republic (Bukva 1985, 1990) Poland (Izdebska, 2000; Izdebska and Rolbiecki, 2006) Demodex musculi (Oudemans, 1897) (¼Demodex Europe (Hirst, 1919) arvicolae musculi Oudemans, 1897) Russia (Bregetova et al., 1955) Poland (Izdebska, 2000) Rattus norvegicus (Berkenhout, 1769) Demodex nanus Hirst, 1918 [Redescription, Europe (Hirst, 1919) Desch 1987] Russia (Bregetova et al., 1955) North America (Desch, 1987) Poland (Izdebska, 2004; Izdebska and Rolbiecki, 2004) Demodex norvegicus Bukva, 1995 Czech Republic (Bukva, 1995) Poland (Izdebska, 2004; Izdebska and Rolbiecki, 2004) Demodex ratti Hirst, 1917 (Redescription, Europe (Hirst, 1919) Bukva 1995) Russia (Bregetova et al., 1955) Czech Republic (Bukva, 1995) Poland (Izdebska, 2004; Izdebska and Rolbiecki, 2004) Demodex ratticola Bukva, 1995 Czech Republic (Bukva, 1995) Rattus rattus (Linnaeus, 1758) Demodex nanus Hirst, 1918 Europe (Hirst, 1919) North America (Desch, 1987) Leopoldamys sabanus (Thomas, 1887) Demodex sabani Desch, Lukoschus, and Asia (Desch et al., 1984) Leopoldamys edwardsi (Thomas, 1882) Nadchatram, 1984 Niviventer cremoriventer (Miller, 1900) Niviventer rapit (Bonhote, 1903) Rattus annandalei (Bonhote, 1903) Rattus tiomanicus (Miller, 1900) Sundamys muelleri (Jentink, 1879) 1104 THE JOURNAL OF PARASITOLOGY, VOL. 98, NO. 6, DECEMBER 2012

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