The larva of the ixodid tick Dermacentor parumapertus Neumann, chiefly a parasite of hares and rabbits, is redescribed using scanning electron micrographs of seven specimens derived from two engorged females collected from two black-tailed jackrabbits, Lepus californicus, at the Black Gap Wildlife Management Area, Brewster County, southwestern Texas. The use of chaetotaxy for separating the genera of Ixodidae is discussed, and a morphological key is provided for separating the larvae of D. parumapertus from those of five other Dermacentor species with partly sympatric geographic ranges.
Introduction
The hard tick Dermacentor parumapertus Neumann (Acari: Ixodidae) occurs in the western United States southward at least as far as northern Mexico (Cooley 1938; Guglielmone et al. 2014; Guzmán-Cornejo et al. 2016). Hosts for all parasitic stages include hares and rabbits, particularly the black-tailed jackrabbit, Lepus californicus Gray. Immature stages are also commonly found on many other small mammals, and host records for larval D. parumapertus include >20 other species that exist sympatrically with L. californicus (Bishopp & Trembley 1945; Gastfriend 1955; Johnson 1966; Furman & Loomis 1984) (Table 1). Adults have been collected occasionally from hosts other than lagomorphs, including artiodactyls (Bovidae, Cervidae) and carnivores (Canidae) (Allred & Roscoe 1956; Guglielmone & Robbins 2018). Tick bite records from humans are relatively rare (Roscoe 1956; Johnson 1966; Furman & Loomis 1984). Since the adults are strictly host specific (less so for immatures) (Hoogstraal & Aeschlimann 1982), D. parumapertus is rarely encountered, except by hunters or scientists collecting rabbits for study. Records of D. parumapertus in the scientific literature are relatively scarce, and little information is available concerning this species' taxonomy, biology and ecology beyond the investigations conducted during the first half of the 20th Century (Hooker et al. 1912; McCampbell 1926; Cooley 1938; Fremling & Gastfriend 1955; Allred & Roscoe 1956). The original description of the immature stages of D. parumapertus was published in 1912 (Hooker et al. 1912), and the most recent redescription of the larva appeared almost 40 years ago (Furman & Loomis 1984); however, both descriptions were relatively brief. Using specimens that we obtained in 2015 and subsequently prepared for multiple scanning electron micrographs (SEM), we are now able to provide a more detailed redescription of the larval stage of D. parumapertus.
Methods
Source of ticks. Our collections were part of a broader tick-borne disease survey at the Black Gap Wildlife Management Area, located near Alpine, in Brewster County, southwestern Texas. Specimens were removed from black-tailed jackrabbits shot by experienced hunters and wildlife biologists, and these procedures were reviewed and approved by the Institutional Animal Care and Use Committee at the Centers for Disease Control and Prevention (Paddock et al. 2017). One adult male/female pair from our collections was sent to the last author (RGR) for confirmation. Larvae used in this study were obtained by rearing eggs laid by two engorged female D. parumapertus collected from two separate jackrabbits in July 2015. A week after eclosion, larvae were placed in 70% ethanol and kept in the lab until SEM studies could be conducted in 2022.
Scanning electron microscopy. Seven larval specimens (3 from one rabbit and 4 from the other) were removed from the storage ethanol and transferred to fresh 70% ethanol. Specimens were sonicated for 4–5 seconds to remove any debris, then larvae were further dehydrated in 90% and 100% ethanol. The specimens were subsequently placed in hexamethyldisilazide (HMDS) for 2 hours and then air dried to remove the HMDS. Tick larvae were mounted on aluminum stubs with carbon tape and coated with platinum. Specimens were then examined with a JEOL 6500F Field Emission scanning electron microscope (Tokyo, Japan) at 5 kV, and 38 images were digitally recorded.
Setal nomenclature. Terminology of setae followed that of Clifford & Anastos (1960), largely based on previous work, and was selected for its relative simplicity; an alternate system has been proposed by Klompen et al. (1996) but is not in wide use. Lindquist et al. (2016) compared and discussed these two systems.
Results and Discussion
In North America, larvae of all Dermacentor species possess a unique suite of morphological and setal characters that include: absence of an anal groove (Figure 1); nine festoons present (Figure 1); one pair of posthypostomal setae (Figure 2); all four palpal segments distinctly visible, dorsally and ventrally; four pairs of large wax glands (formerly sensilla sagittiformia) present, one pair dorsally between marginal dorsal setae 3 and 4 (Figure 3), and three pairs ventrally, posterior to coxae I-III (Figure 4); bases of prehalleral setae in tandem, not parallel (Figure 5) (Clifford et al. 1960). Additionally, across the genus Dermacentor, including the former genus Anocentor (=Otocentor), all nine pairs of body setae are identical in number: scutal (Sc), 3 pairs of setae; marginal dorsal (Md), 8 pairs; central dorsal (Cd), 2 pairs; supplementary (S), 0 pairs; sternal (St), 3 pairs; preanal (Pa), 2 pairs; premarginal (Pm), 4 pairs; marginal ventral (Mv), 5 pairs; anal (A), 1 pair.
Larvae of D. parumapertus possess each of the above characters, as do those of five generally recognized Nearctic Dermacentor whose ranges are partly sympatric with this species: D. albipictus (Packard), D. andersoni Stiles, D. hunteri Bishopp, D. occidentalis Marx, and D. variabilis (Say). There are no larval data yet available for the recently described Dermacentor similis (Lado et al. 2021). Together, larvae of these six species are difficult to separate based on morphology alone. For that reason, the following key utilizes morphological characters in combination with species-specific ecological and host information, an adaptation of the approach employed in other keys to the adult Dermacentor of the Western Hemisphere (Yunker et al. 1986).
Key to the larvae of Dermacentor species sympatric with Dermacentor parumapertus
1. Lateral margins of basis capituli not pointed; spurs of coxae II and III indistinct or absent; widespread in North and Central America, principally on Artiodactyla (Bovidae and Cervidae) and Perissodactyla (Equidae) D. albipictus
- Lateral margins of basis capituli moderately or sharply pointed; coxa II with faint or definite external spur 2
2. Internal spur of coxa I pointed and extending beyond posterior coxal margin; coxae II and III about equal in size; widespread in eastern and central North America, including eastern Mexico, principally on multiple families of Rodentia D. variabilis
- Internal spur of coxa I smaller and pointed or blunt; coxa II somewhat larger than coxa III 3
3. Coxa I with pointed internal spur; coxa III lacking spur; Pacific coast from Oregon to northwestern Mexico, principally on Lagomorpha (Leporidae) and multiple families of Rodentia D. occidentalis
- Coxa I with blunt internal spur; coxae II and III with small, broad external spurs 4
4. Lateral margins of basis capituli moderately pointed; coxae II and III with distinct, broad external spurs; scrub and xeric habitats, principally on Lagomorpha (Leporidae) and multiple families of Rodentia D. parumapertus
- Lateral margins of basis capituli sharply pointed; coxae II and III with small or faint external spurs 5
5. Coxa II conspicuously broader than coxa III; coxae II and III with faint external spurs; desert southwest of U.S. and northwestern Mexico, principally on Rodentia (Cricetidae) D. hunteri
- Coxa II slightly larger than coxa III; coxae II and III with faint external spurs, especially coxa III; xeric shrublands and temperate conifer forests, principally on Lagomorpha (Leporidae) and multiple families of Rodentia D. andersoni
TABLE 1.
Host records for larvae of Dermacentor parumapertus. Scientific and common names of hosts are from the Integrative Taxonomic Information System ( www.itis.gov), a consortium of U.S., Canadian, and Mexican organizations and taxonomic specialists, accessed March 2023.
The larva of D. parumapertus may therefore be further described as follows:
Body oval, tapering anteriorly, length from scutal emargination to posterior body margin 0.61–0.63 mm (mean 0.62), width 0.40–0.46 mm (mean 0.44), widest at about level of coxae III. Scutum 0.18–0.22 mm long (mean 0.20), 0.32–0.34 mm wide (mean 0.33), scutal surface reticulate, cervical grooves deep, extending about one-third length of scutum and converging posteriorly, eyes situated at posterolateral corners of scutum and slightly elevated. Capitulum dorsally 0.13–0.16 mm wide (mean 0.15), 0.11–0.12 mm long (mean 0.11) from palpal apices to posterior margin of basis. Lateral margins moderately pointed and flange-like, posterior margin broadly concave; ventrally, hypostome bluntly rounded apically, length of toothed portion 0.038–0.040 mm long (mean 0.039), dentition 2/2, with 6–7 principal denticles per file. Coxa I with blunt internal spur, coxae II–III each with distinct, broad external spur.
More comparative studies of preimaginal North American Dermacentor species are required, including those species that have not been redescribed for decades. For example, the larvae and nymphs of D. halli McIntosh and D. hunteri were last described by Brinton et al. (1965) and Furman & Loomis (1984), respectively; the latter authors were also the last to describe the nymphs of D. occidentalis and D. parumapertus (Guglielmone et al. 2020). It is hoped that the present work will stimulate others, particularly investigators with an interest in tick surveillance, to conduct similar studies. Future taxonomic redescriptions will require an integrative approach that incorporates molecular, geographical, ecological, and proteomic components. There are likely additional cryptic species among those current recognized, as evidenced by recent studies (Beati et al. 2013; Lado et al. 2021).
Acknowledgements
We thank personnel at the Texas Parks & Wildlife's Wildlife Division, Black Gap Wildlife Management Area, for their help in sampling jackrabbits. All material in this paper has been reviewed by the Walter Reed Army Institute of Research. There is no objection to its presentation and/or publication. The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or reflecting the true views of the Centers for Disease Control and Prevention, the U.S. Department of the Army or the Department of Defense.
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