Ornithodoros (Alectorobius) puertoricensis

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E, Surinam; F, Jamaica; G, Haiti; H, Dominican Republic; I, Puerto Rico; J, St. Croix; K, U.S. Virgin Islands; ... resa Haslett for a critical reading of this manuscript.
Ornithodoros (Alectorobius) puertoricensis (Acari: Argasidae): Redescription by Scanning Electron Microscopy R. G. ENDRIS,1 J. E. KEIRANS,2 R. G. ROBBINS,2 AND W. R. HESS1

J. Med. Entomol. 26(3): 146-154 (1989) ABSTRACT The female, male, nymphal instars, and larva of Ornithodoros puertoricensis Fox are redescribed from specimens collected in Haiti. Data on host species and geographic distribution are also presented. KEY WORDS

Arachnida, Acari, Ornithodoros puertoricensis, redescription

IN 1947, Fox described all active stages of Ornithodoros puertoricensis from reared specimens collected as larvae on domestic rats, Rattus norvegicus and R. rattus, in San Juan, Puerto Rico. At that time, medical acarologists were interested in the ability of argasid ticks to harbor and transmit the spirochetes of human relapsing fever, Borrelia spp. Davis (1955) conducted studies on the biology and vector potential of O. puertoricensis, including unsuccessful attempts to transmit spirochetes that had been isolated from O. dugesi Mazzotti and O. turicata (Duges). Investigations of murine typhus (Fox 1951, Fox & Garcia-Moll 1961, Fox et al. 1964) revealed the seasonal dynamics of O. puertoricensis on rats in San Juan, but to date this species is not known to transmit any human or animal disease. The recent introduction of African swine fever virus to the Caribbean Basin (Hess 1981, Rivera 1983, Buisch 1986, Hess et al. 1987) signals the need for a thorough reexamination of O. puertoricensis. Materials and Methods In February 1983, J. F. Butler, A. F. Beck, and R. G. E. used vacuum sampling machines (Butler & Gibbs 1982, Butler et al. 1985) to collect living nymphs and adults of this species in Haiti. Ticks were extracted from rat burrows, burrowing owl nests, mongoose burrows, and burrows of unknown origin along the northern coast road of the southern peninsula from Miragoane to Mariani and Port-auPrince. North of Port-au-Prince, ticks were taken in the area between Saint-Marc and Gonaives. In the laboratory, several generations were reared from this material by the method of Endris et al. (1986). 1 Plum Island Animal Disease Center, USDA-ARS, P.O. Box 848, Greenport, Long Island, N.Y. 11944. 2 Department of Health and Human Services, Public Health Service, National Institutes of Health, National Institute of Allergy and Infectious Diseases, Department of Entomology, Museum Support Center, Smithsonian Institution, Washington, D.C. 20560.

Representatives of each stage were prepared for scanning electron microscopy (SEM) by the method of Corwin et al. (1979). In the following account, all measurements are in millimeters. Measurements were made with a Filar micrometer, MMS-235 (Wild-Heerbrugg Ltd, Heerbrugg, Switzerland) attached to a stereomicroscope (E. Leitz Inc., Rockleigh, N.J.). Ranges are given and followed by the means of 10 measurements in parentheses. Chaetotaxic terminology is that of Kohls et al. (1965). The holotype (female) and allotype (male) of Ornithodoros puertoricensis (RML 119148) were collected as larvae on Rattus norvegicus at San Juan, Santurce, Puerto Rico, 24 May 1946, by Irving Fox and reared to maturity. This material, including the hypostome and legs I and IV of the holotype mounted on a slide, one paratype (firstinstar nymph, RML 119149, data as above except 7 June 1946), and one slide-mounted paratype (larva, RML 119150, data as above except April 1946), have been deposited in the National Tick Collection, Department of Entomology, Museum Support Center, Smithsonian Institution through the courtesy of Dr. Fox. Specimens described in this study have also been deposited in the National Tick Collection (RML 117905). Ornithodoros (Alectorobius) puertoricensis Fox, 1947 Redescription Female (Fig. 1-8). Body small, 3.40-4.10 (3.73) long, 2.00-2.63 (2.24) broad, broadly rounded posteriorly, subparallel laterally, anteriorly converging rather abruptly to a sharply angular apex; apex broader in engorged specimens; medial dorsal area depressed between raised lateral margins. Color (preserved) light to dark brown. Dorsum (Fig. 1, 3, and 4). Mammillae numerous marginally around circumference of dorsum, much fewer centrally; closely and regularly spaced; size and shape mostly subequal; most of them distinctly separated, some

0022-2585/89/0146-0154$02.00/0 © 1989 Entomological Society of America

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Fig. 1-4. Ornithodoros (A.) puertoricensis (RML 117905), female. (1) Dorsal view, 42x. (2) Ventral view, 42 x. (3) Posterolateral quadrant, 95 x. (4) Disk and adjacent mammillae, 424 x.

with lateral buttresses interlocking; dorsally smooth, often with 2 or 3 minute setae arising marginally; uneven lateral buttresses extending from dorsal surface to intermammillary integument. Disks very numerous, depressed below level of mammillae; size, shape, and arrangement as illustrated (Fig. 1, 3, and 4), disk surface depressed within a peripheral ridge divided into several compartments, compartmental surface pebbled. Posteromedian row elongate, extending about xh of body length. Setae minute, inconspicuous. Lateral suture absent. Venter (Fig. 2). Mammillae posteriorly approximately as on dorsum; disks present only in grooves and 2 lateral depressions. Genital area (Fig. 5) as illustrated; anterior and posterior labia subequal,

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surface arranged in partially subparallel ridges or diffuse, rough, nonaligned network in different specimens; anterior labial pore absent. Capitulum (Fig. 6) situated in a camerostome anterior to coxae 1 and hood. Cheeks elongate, narrow; in some specimens enfolding palps and hypostome (not illustrated), in others splayed back, not covering palps and mouth parts (illustrated). Hood small, ventroflexed. Basis capituli micromammillated, 0.22-0.32 (0.27) long, 0.33-0.38 (0.35) broad, about 3 minute pairs posterolateral setae; posthypostomal setae long, arising from a truncated median extension of the basis and extending % the hypostomal length; postpalpal setal pair small. Palpi globose; surface of segment 1 micromammillated, medial flange

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Fig. 5-8. Ornithodoros (A.) puertoricensis (RML 117905), female. (5) Genital area, 318x. (6) Capitulum, ventral view, 212 x. (7) Hypostome and palpi, 424 x. (8) Haller's organ, 848 x.

smooth, partially or sometimes entirely enfolding nondentate portion of hypostome; segments 2-4 smooth, breadth successively decreasing from segments 1-4. Hypostome (Fig. 7) 0.12-0.19 (0.15) long, deeply indented apically, subparallel laterally, corona of several irregular hooklet files (inconspicuous except under SEM); dental formula 2/2 in files of about 3 angular denticles. Legs long, narrow. Coxae I and II separated, II-IV contiguous. Tarsi narrow, lacking humps and protuberances. Tarsus I abruptly tapering distally, 0.39-0.48 (0.43) long, 0.11-0.15 (0.12) broad. Claws large. Haller's organ as in Fig. 8. Tarsus IV gradually tapering distally, 0.47-0.56 (0.51) long, 0.10-0.12 (0.11) broad.

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Male (Fig. 9-12). Similar to female except for sexual characters and smaller size. Body (Fig. 9 and 10) 2.74-3.33 (3.04) long, 1.68-1.93 (1.79) broad. Capitulum (Fig. 11) similar to that of female, 0.21-0.26 (0.24) long, 0.28-0.32 (0.31) broad. Hypostome (Fig. 11) 0.12-0.17 (0.15) long, denticles small, in two irregular rows. Genital area (Fig. 12) as illustrated, with scalelike crenulations in posterior portion of genital flap. Tarsus I 0.330.42 (0.36) long, 0.10-0.12 (0.11) broad; tarsus IV 0.37-0.47 (0.42) long, 0.09-0.11 (0.10) broad. First Nymphal Instar (Fig. 13-16). 1.53-1.78 (1.65) long, 1.03-1.19 (1.10) broad; all specimens engorged. Dorsum (Fig. 13 and 14) with mammillae numerous but widely separated peripher-

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Fig. 9-12. Ornithodoros (A.) puertoricensis (RML 117905), male. (9) Dorsal view, 53x. (10) Posterolateral quadrant, 212 x. (11) Capitulum, ventral view, 212 x. (12) genital area, 318 x.

ally, fewer centrally. All mammillae without the lateral buttresses characteristically seen in adults and other nymphal stages; most mammillae with a minute white seta. Disks (Fig. 14) few, represented by a semiorganized, circular arrangement of integumental pores and surface structures. Capitulum (Fig. 15 and 16) elongate in engorged specimens. Posthypostomal setal pair long, postpalpal setal pair short, a single, minute, posterolateral setal pair. Hypostome apically indented, dentition 2/2 in files of 6 or 7 irregular denticles. Second, Third, and Fourth Nymphal Instars. Similar to adults in all morphological characteristics except smaller in size and lacking genital areas. Second instar 1.56-1.83 (1.71) long, 1.04-1.22 (1.12)

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broad; third instar 1.93-2.37 (2.10) long, 1.21-1.48 (1.32) broad; fourth instar 2.03-2.59 (2.38) long, 1.24-1.59 (1.45) broad. Larva (Fig. 17-20). Body. Unengorged 0.4630.504 (0.490) long (including capitulum), 0.3950.425 (0.404) broad. Dorsal plate (Fig. 17) large, pyriform, broadest posteriorly, 0.219-0.259 (0.241) long, 0.162-0.191 (0.174) broad. Dorsum with 16 or 17 pairs of setae, typically with 14 dorsolateral pairs and 3 central pairs; DAL average 0.077, DPL average 0.082. Venter (Fig. 18) with 8 pairs of setae including 1 pair on anal valves, plus PMS present posterior to anus. Capitulum (Fig. 19) 0.092-0.119 (0.099) long, 0.114-0.141 (0.130) broad. Two pairs posthypostomal setae; PH, 0.009-0.016

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r

16 Fig. 13-16. Ornithodoros (A.) puertoricensis (RML 117905), first nymphal instar. (13) Posterolateral quadrant, 212 x. (14) Disk and adjacent mammillae, 530 x. (15) capitulum, ventral view, 424 x. (16) Hypostome and palpi, 742 x.

(0.012) long, PH2 0.013-0.022 (0.017) long. Dis- PC, 1 PM, 1 pair B, 1 pair AV, 1 pair MV, 1 pair tance between setae of PH, average 0.021, between BV, and 1 pair PL. setae of PH2 average 0.067. Palpi 0.192-0.228 (0.208) long; average length of palpal articles 1-4: 0.034, 0.083, 0.061, 0.030, respectively. HypoDiscussion stome (Fig. 19 and 20) very long, arising from a slightly elevated median extension of the basis caHost records for O. puertoricensis are entirely pituli; 0.200-0.237 (0.219) long, 0.028-0.037 (0.033) based on larvae, which have been collected from broad. Dentition 3/3 in anterior lk, 2/2 for about at least 21 species of mammals, two reptiles, and 7 rows, without teeth in basal V*. File 1 with 21-one bird (Table 1). The variety of known hosts 23 denticles, 2 with 18-20, 3 with 12-13. Legs. underscores the need for further collecting, parTarsus I 0.123-0.145 (0.136) long, 0.043-0.053 ticularly of reptiles and birds. As yet, postlarval (0.049) broad. Setal formula: 1 pair A, 1 DM, 5 stages have not been recorded from any animal,

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Fig. 17-20. Ornithodoros (A.) puertoricensis (RML 117905), larva. (17) Dorsal view, 170x. (18) Ventral view, 212 x. (19) Capitulum, ventral view, 318 x. (20) Hypostome, 636 x. but it is assumed that they secrete themselves in the nests and burrows of their hosts (Jones et al. 1972). The northern and southern limits of the range of O. puertoricensis are not clearly defined. Numerous specimen records exist for the West Indies, southern Central America, and northern South America (Fig. 21). However, the U.S. National Museum of Natural History contains a single collection of larvae (RML 33406) from the legs of a burrowing owl, Speotyto cunicularia, taken on Isla Clarion (18'22°N, 114°44"W)) Islas de Revillagigedo, Mexico. In southern South America, the distributional picture is confused. Maldonado Capriles & Medina

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Gaud (1977) listed O. puertoricensis from Argentina, Bolivia, Brazil, and Paraguay but provided no collection data. We have not seen specimens from these countries, and in the absence of further information, such records are suspect. Laboratory studies by Fox (1947) and Davis (1955) on the biology and life history of O. puertoricensis are summarized in Table 2. Although both studies were conducted at room temperature, the duration of each immature stage reported by Davis was generally twice as long as that by Fox; Davis attributed this discrepancy to "different conditions" between the two laboratories. However, Fox used white rats as laboratory hosts, and Davis

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Table 1. Host records for larvae of O. (A.) puertoricensis Genus and species

Order: family

Collection site

Rattus rattus Ratttis norvegicus Felis catus Sylvilagus brasiliensis Proechimys sp. Nectomys sp. Herpestes javanicus auropunctatus Proechimys guyannensis Proechimys semispinosus Dasyprocta fuliginosa Sigmodon alstoni Zygodontomys brevicauda Sylvilagus floridanus Tamandua tetradactyla Conepatus semistriatus Monodelphis brevicaudata Marmosa robinsoni Artibeus lituratus Iguana sp. Lizard (unidentified) Speotyto cunicularia Proechimys trinitatus Homo sapiens Dasyprocta punctata Didelphis marsupialis Nectomys squamipes

Rodentia: Muridae Rodentia: Muridae Carnivora: Felidae Lagomorpha: Leporidae Rodentia: Echimyidae Rodentia: Cricetidae Carnivora: Herpestidae Rodentia: Echimyidae Rodentia: Echimyidae Rodentia: Dasyproctidae Rodentia: Cricetidae Rodentia: Cricetidae Lagomorpha: Leporidae Edentata: Myrmecophagidae Carnivora: Mustelidae Marsupialia: Didelphidae Marsupialia: Didelphidae Chiroptera: Phyllostomidae Sauria: Iguanidae Sauria Strigiformes: Strigidae Rodentia: Echimyidae Primates: Hominidae Rodentia: Dasyproctidae Marsupialia: Didelphidae Rodentia: Cricetidae

Puerto Rico Puerto Rico Puerto Rico Panama Jamaica Jamaica Jamaica Venezuela Venezuela Venezuela Venezuela Venezuela Venezuela Venezuela Venezuela Venezuela Venezuela Venezuela Venezuela Venezuela Mexico Trinidad Panama Nicaragua Nicaragua Trinidad

used guinea pigs; differences in the quality of host blood could well have affected engorgement time. Based on data from both authors, an estimate of the time required to complete a single egg-to-egg

Source Fox (1947) Fox (1947) Fox (1977) Fairchild et al. (1966) Fairchild et al. (1966) Fairchild et al. (1966) Webb (1980), Thompson (1950) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) Jones et al. (1972) RML 33406 Kohls et al. (1965) Kohls et al. (1965) RML 54795 RML 45587, 45588 RML 34498

generation is 91.2 d. This estimate does not include the period between molting and feeding for nymphs and adults. Therefore, the generation time probably exceeds 100 d.

Table 2. Summary of laboratory biology of O. (A.) puertoricensis (1955)

based on the work of Fox (1947) and Davis Author

n"

Fox (1947)

na

Davis (1955)

Mean duration larval feeding (d)





887

5.3 ± 0.9b

Mean time (d) from feeding to molt Larvae Nymph

65

52

6.4 ± 0.9

45 26 22 9

16-31C 17-206 20-48c 23-55 c

12 1 0 9 4 8 5 2 9d

92.3

1 2 3 4

% Third-instar nymph molted to 6 % Third-instar nymph molted to 9 % Fourth-instar nymph molted to S % Fourth-instar nymph molted to 9 Mean duration of copulation (min) Mean time (d) from feeding to oviposition Mean no. eggs per 9, gonotrophic cycle 1 Mean no. eggs per 9, gonotrophic cycle 2 Mean egg incubation time, d

66 45 18 6

3.1 ± 0.5 6.8 10.4 12.5 14.3

± ± ± ±

9 4 1 4 — — — —

69.2 30.7 20.0 80.0





" n, number of specimens. " Larvae fed on three guinea pigs. f No specific data given. ll n, number of egg batches.

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— — — —

1.3 2.5 1.5 1.0

7.7

100.0 8.6 ± 0.8 12.6 ± 6.1 182 ± 40 389 ± 52 16.2 ± 3.1

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Distribution of Ornithodoros puertoricensis

Fig. 21. Geographic distribution of O. (A.) puertoricensis. A, Nicaragua; B, Panama; C, Colombia; D, Venezuela; E, Surinam; F, Jamaica; G, Haiti; H, Dominican Republic; I, Puerto Rico; J, St. Croix; K, U.S. Virgin Islands; L, Guadeloupe; M, Trinidad. Not shown: Mexico.

Acknowledgment We thank Michael Monahan for technical assistance in rearing the specimens, Joseph Beaton and Anthony Dobek for their artistic and photographic assistance, Irving Fox for depositing type specimens of Ornithodoros puertoricensis in the National Tick Collection, and Theresa Haslett for a critical reading of this manuscript.

References Cited Buisch, W. W. 1986. African swine fever in this continent, pp. 17-21. In Proceedings, Livestock Conservation Institute, April 8-10, 1986, Omaha, Nebr. Livestock Conservation Institute, South St. Paul, Minn. Butler, J. F. & E. Cibbs. 1982. Sampling techniques for burrow-dwelling ticks and other arthropods. Food and Agricultural Organization/African Swine Fever Newsletter 20.

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Butler, J. F., D. D. Wilson, G. I. Garris, H. G. Koch, J. M. Crum & V. E. Castellanos. 1985. Survey for potential soft tick (Acari: Argasidae) vectors of African swine fever on the island of Hispaniola. Exp. Appl. Acarol. 1: 63-72. Corwin, D., C. M. Clifford & J. E. Keirans. 1979. An improved method for cleaning and preparing ticks for examination with the scanning electron microscope. J. Med. Entomol. 16: 352-353. Davis, G. E. 1955. Observations on the biology of the argasid tick Ornithodoros puertoricensis Fox. J. Parasitol. 41(1): 76-79. Endris, R. G., T. M. Haslett, M. J. Monahan, W. R. Hess & L. C. Rutledge. 1986. Techniques for mass rearing soft ticks (Acari: Argasidae). J. Med. Entomol. 23: 225-229. Fairchild, G. B., G. M. Kohls & V. J. Tipton. 1966. The ticks of Panama (Acarina: Ixodoidea), pp. 167219. In R. L. Wenzel & V. J. Tipton [eds.], Ectopar-

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asites of Panama. Field Museum of Natural History, Chicago. Fox, I. 1947. Ornithodoros puertoricensis, a new tick from rats in Puerto Rico. J. Parasitol. 33(3): 253-259. 1951. Relative and seasonal abundance of the common rat ectoparasites of San Juan, Puerto Rico. J. Parasitol. 37(1): 85-95. 1977. The domestic cat, Felis catus L., a new host record for the tick, Ornithodoros puertoricensis. J. Agric. Univ. Puerto Rico 61(4): 509. Fox, I. & I. Carcia-Moll. 1961. Rat ectoparasite surveys in relation to murine typhus fever in Puerto Rico. Am. J. Trop. Med. Hyg. 10: 566-573. Fox, I., I. G. Bayana & G. A. Rivera.

1964.

Rat

ectoparasite surveys in Puerto Rico with toxicological studies on Xenopsylla cheopis. Am. J. Trop. Med. Hyg. 13(6): 887-896. Hess, W. R. 1981. African swine fever: a reassessment. Adv. Vet. Sci. Comp. Med. 25: 39-69. Hess, W. R., R. G. Endris, T. M. Haslett, M. J. Monahan

& J. P. McCoy. 1987. Potential arthropod vectors of African swine fever virus in North America and the Caribbean Basin. Vet. Parasitol. 26(1-2): 145-155.

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the Western Hemisphere. Brigham Young University Science Bulletin 17. Provo, Utah. Kohls, G. M., D. E. Sonenshine & C. M. Clifford.

1965.

The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). II. Identification of the larvae of the Western Hemisphere and descriptions of three new species. Ann. Entomol. Soc. Am. 58(3): 331-364. Maldonaldo Capriles, J. & S. Medina Gaud. 1977. The ticks of Puerto Rico (Arachnida: Acarina) J. Agric. Univ. Puerto Rico 61: 402-404. Rivera, E. M. 1983. African swine fever in the Dominican Republic, pp. 17-24. In P. J. Wilkinson [ed.], African swine fever. Proceedings of a Commission of the European Communities/Food and Agricultural Organization Seminar, Sassari, Sardinia, 23-25 Sept. 1981. Thompson, G. B. 1950. Ticks of Jamaica, B.W.I. Records and notes (including a summary of the distribution of the West Indian species). Ann. Mag. Nat. Hist. 12(3): 220-229. Webb, J. W. 1980. Parasites of small Indian mongoose on St. Croix, Virgin Islands. J. Parasitol. 66(1): 176178.

Jones, E. K., C. M. Clifford, J. E. Keirans & G. M.

Kohls. 1972. The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in

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Received for publication 26 May 1988; accepted 30 August 1988.