First Description of the Immature Stages and Redescription of the Adults of Cosmiomma Hippopotamensis (Acari: Ixodidae) with Notes on Its Bionomics
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MORPHOLOGY,SYSTEMATICS,EVOLUTION First Description of the Immature Stages and Redescription of the Adults of Cosmiomma hippopotamensis (Acari: Ixodidae) With Notes on Its Bionomics DMITRY A. APANASKEVICH,1,2 JANE B. WALKER,3,4 HELOISE HEYNE,3 3,5 6 J. DU¨ RR BEZUIDENHOUT, AND IVAN G. HORAK Downloaded from https://academic.oup.com/jme/article/50/4/709/889256 by guest on 27 September 2021 J. Med. Entomol. 50(4): 709Ð722 (2013); DOI: http://dx.doi.org/10.1603/ME12271 ABSTRACT Cosmiomma hippopotamensis (Denny, 1843) is one of the most unusual, beautiful, and rare tick species known to the world. All stages of this species possess a unique morphology, on the one hand making them easy to identify, while on the other they exhibit similarities to certain species of Amblyomma Koch, 1844, Dermacentor Koch, 1844, and Hyalomma Koch, 1844. Adults of C. hippo- potamensis have been collected on only two occasions from their hosts, namely Hippopotamus amphibius L. and Diceros bicornis (L.), and have been recorded from only a few widely separated localities in East and southern Africa. Here, the larva and nymph are described and illustrated for the Þrst time, while the male and female are illustrated and redescribed. Data on hosts, geographic distribution, and life cycle of C. hippopotamensis are also provided. KEY WORDS Cosmiomma hippopotamensis, male, female, nymph, larva Cosmiomma hippopotamensis (Denny, 1843) is one of Koch, 1844, that is, Amblyomma hippopotami. Neu- the most striking, but rarely collected, species of Af- mann (1899) initially corrected the name to Ambly- rican ixodid ticks. In 1970, however, a locality in northÐ omma hippopotamense but later placed it in the genus west Namibia, at which it was fairly abundant, was Hyalomma Koch, 1844, changing the combination of discovered, and numerous adult specimens were col- names to Hyalomma hippopotamense (Neumann lected from the vegetation (Bezuidenhout and Sch- 1906). After studying the type specimens and a re- neider 1972). After this discovery, the Þrst experi- evaluation of their morphological characters, Schulze ments on the feeding preferences of the adults were (1919) created an independent genus for this species, made, and most importantly, the nymphs and larvae namely Cosmiomma Schulze, 1919, with I. hippopota- were reared. mensis as the type species of the genus. According to Over time, the taxonomic position of this tick has Hoogstraal (1956), Zumpt (1951) sunk Cosmiomma changed on numerous occasions. The male and female under Dermacentor Koch, 1844. As a result Hoogstraal were originally described as separate species of the (1956) placed C. hippopotamensis in the genus Der- genus Ixodes Latreille, 1796; initially the female as macentor and considered Cosmiomma a subgenus of Ixodes bimaculatus Denny, 1843 and thereafter the Dermacentor. However, after an examination of the male as Ixodes hippopotamensis Denny, 1843. A year publication by Zumpt (1951), we were unable to con- later Koch (1844) realized that I. bimaculatus and I. Þrm this nomenclatural change. Most workers now hippopotamensis are sexes of the same species. He, as agree that Cosmiomma is a monotypic genus compris- a Þrst reviser, assigned priority to the name I. hippo- ing the species C. hippopotamensis. Santos Dias potamensis and placed it in the genus Amblyomma (1958)after studying the original descriptions of I. bimaculatus and I. hippopotamensis decided that page priority should be given to the name Cosmiomma bi- The content is solely the responsibility of the authors and does not maculatum, and he therefore considered this name as necessarily represent the ofÞcial views of the National Institute of Allergy and Infectious Diseases or the National Institutes of Health. valid for the species. However, as mentioned above, 1 United States National Tick Collection, Georgia Southern Uni- Koch (1844), as Þrst reviser, had already given the versity, Statesboro, GA 30460-8056. name I. hippopotamensis priority, and consequently, 2 Corresponding author, e-mail: dapanaskevich@georgiasouthern. according to the International Code of Zoological No- edu. 3 Parasites, Vectors and Vector Borne Diseases, ARC-Onderstepoort menclature (1999 and previous editions), this bi- Veterinary Institute, Onderstepoort 0110, South Africa. nomen should be accepted as valid. Based on a study 4 Deceased 3 April 2009. of the external morphology of the adults, Filippova 5 Present address: P.O. Box 555, Yzerfontein, 7351, South Africa. (1997) considered Cosmiomma to be most closely re- 6 Department of Veterinary Tropical Diseases, Faculty of Vet- erinary Science, University of Pretoria, Onderstepoort 0110, South lated to the Rhipicephalus Koch, 1844 lineage. How- Africa. ever, a later analysis, also based on morphological 0022-2585/13/0709Ð0722$04.00/0 ᭧ 2013 Entomological Society of America 710 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 50, no. 4 Table 1. C. hippopotamensis, material studied No. of ticksa Host Locality Date Collector Acc. no.b (&NL Kenya, Eastern Province 1 2 Vegetation Makindu, Chale area 2 Jan. 1968 G.C. Backhurst RML 50613 1 Vegetation Makindu, Chale area 10 Nov. 1967 G.C. Backhurst RML 51750 1 Vegetation Makindu, Chale area 10 Nov. 1967 G.C. Backhurst RML 51749 Kenya, Coast Province 1 Vegetation Mazinga Hill, nr. Voi 6 Nov. 1956 D.L.W. Sheldrick JBWC 1 Vegetation Upper Tsavo 30 Oct. 1946 JBWC Namibia, Kunene Region (Kaokoland) 8 8 Vegetation Otjipembe Mar. 1971 J.D. Bezuidenhout RML 62898 3 3 Opowu, Otjijanjasemo 6 Jan. 1960 State veterinarian OP 2703 i Downloaded from https://academic.oup.com/jme/article/50/4/709/889256 by guest on 27 September 2021 811 Mar. 1971 J.D. Bezuidenhout HHC 4 4 10 20 Reared in laboratory RML 65717 1 1 Reared in laboratory RML 122176 27 89 5 Reared in laboratory HHC 10 15 50 300 Reared in laboratory JBWCOP No data 11 ZMB 67 136 65 320 Total a L, larvae; N, nymphs. b RML, US National Tick Collection; JBWC, Jane B. Walker East African Collection; OP, Onderstepoort Veterinary Institute Collection; HHC, Heloise Heyne Collection; JBWCOP, Jane B. Walker Collection at the Onderstepoort Veterinary Institute; ZMB, Museum of Natural History (Berlin). characters, indicated that Cosmiomma was more Cosmiomma hippopotamensis (Denny, 1843) (Figs. closely related to the Dermacentor lineage (Klompen 1–8) et al. 1997). No molecular data have ever been ob- ( (redescription) (Figs. 1A, 2A, and 3). Conscutum tained for this species. (Fig. 1A): broadly oval, widest at mid-length; distance After discovering reared specimens of nymphs and from scapular apices to posterior margin of conscutum larvae in the J. B. Walker and United States National ϭ Tick Collections (USNTC), we decided to describe 5.22Ð6.93 (6.04; n 13), maximum width 4.27Ð5.60 (4.91; n ϭ 13), ratio length to width 1.16Ð1.27 (1.23; these stages and more exactly redescribe the adult ϭ stages to facilitate a better understanding of the phy- n 13). Coloration: ornate with light ivory or pale logenetic position of C. hippopotamensis. yellow enamelled patches grouped in six pairs mar- ginally on a dark brown background, a single central patch anteriorly and a pair of medial patches; some patches may be connected with neighboring patches Materials and Methods as illustrated; small enamelled patches on third and The material examined is summarized in Table 1. fourth festoons. Cervical grooves distinct, moderately Both Þeld-collected and laboratory-reared ticks were deep; a pair of central depressions, and a second pos- studied. The specimens that were examined are de- terior pair that correspond to paramedian grooves; posited in the USNTC (Georgia Southern University, seven distinct festoons. Large punctations sparse, Þne Statesboro), the Gertrud Theiler Tick Museum at the punctations dense, evenly distributed over scutum. ARC-Onderstepoort Veterinary Institute (ARC-OVI) Eyes (Fig. 1A): round, convex, at anterior one-seventh (Onderstepoort, South Africa), Natural History Mu- of scutal length. Setae sparse and short. Venter (Fig. seum of Berlin (NHMB) (Berlin, Germany), and the 2A): as illustrated; setae numerous, short, somewhat personal East African tick collection of the late J. B. longer along posterior margin of venter. Apron of Walker (South Africa). genital aperture (Fig. 2A): at level of coxae II. Adanal The immature stages and the more delicate struc- plates (Figs. 2A and 3A): long and broad, subtriangu- tures of the adults were mounted on glass slides and lar, posterior margin crenulate, length 1.51Ð1.92 (1.69; examined under a light microscope and also by means n ϭ 13), width 0.91Ð1.27 (1.09; n ϭ 13), ratio length to of a scanning electron microscope, and the macro- width 1.41Ð1.72 (1.56; n ϭ 13); setae relatively dense, structures of males and females under a stereoscopic especially on posterior margin of plates. Genital microscope. Measurements for the male and female groove (Fig. 2A): well-developed. Anal groove (Figs. are given in millimeters and those for the various 2A and 3A): indistinct short arch posterior to anus. features of the immature stages in micrometers. The Spiracular plates (Figs. 2A and 3B): positioned on measurements are arranged as follows: minimumÐ ventral surface in unengorged specimens, subtriangu- maximum (mean, n ϭ number of specimens mea- lar with mildly concave anterior margin, greatest di- sured). All illustrations have been drawn by D. A. ameter in anteroposterior plane, length 0.89Ð1.30 Apanaskevich. (1.11; n ϭ 13), width 0.77Ð1.10 (0.95; n ϭ 13), ratio July 2013 APANASKEVICH ET AL.: Cosmiomma hippopotamensis 711 Downloaded from https://academic.oup.com/jme/article/50/4/709/889256 by guest on 27 September 2021 Fig. 1. C. hippopotamensis, dorsally (Namibia). (A) Male. (B) Female. Scale bar ϭ 3 mm. 712 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 50, no. 4 Downloaded from https://academic.oup.com/jme/article/50/4/709/889256 by guest on 27 September 2021 Fig. 2. C. hippopotamensis, ventrally (Namibia). (A) Male.