Hymenolepis cratogeomyos, Gardner & Dursahinhan & Campbell & Rácz, 2020

Gardner, Scott L., Dursahinhan, Altangerel T., Campbell, Mariel L. & Rácz, S. Elizabeth, 2020, A new genus and two new species of unarmed hymenolepidid cestodes (Cestoda Hymenolepididae) from geomyid rodents in Mexico and Costa Rica, Zootaxa 4766 (2), pp. 358-376 : 367-371

Hymenolepis cratogeomyos n. sp.

( Figs. 7–9 )

LSIDurn:lsid:zoobank.org:act: BB0861E9-71F4-4618-92BB-601F156C12F0

Symbiotype host: (see Frey et al., 1992). Volcán De Toluca Pocket Gopher, Cratogeomys planiceps Merriam 1895 ( Rodentia : Geomyidae ).

Symbiotype catalog number: LSUMZ 36120.

Type locality/collection date. Mexico, 10 km S, 16 km W Toluca, 3,000 m; lat. 19° 11’

52.8”N, long. 99° 48’ 36”W; 17 February 1998.

Collector: Mark S. Hafner.

Site of infection: Small intestine.

Prevalence: 100% of those examined; one infected of one specimen examined.

Specimens deposited: Holotype, HWML139035 .

Specimens examined: Paratypes: HWML 139036, HWML 139037, HWML 139038, HWML 139039.

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Description: All specimens available were studied, including one full and 2 partial). At time of collection, specimens were placed directly into 95% ethanol, and so are extremely contracted, with only a few mature proglottids non-contracted and available to examine. Scolex ( Fig. 7 ) unarmed, length N = 2, 198–203 (200 ± 2.6), maximum width N = 2, 209–227 (218 ± 12.6). Apical organ (AO), N = 1, 21.8–21.8 (21.8 ± 0) long. Osmoregulatory ducts terminate at base of AO, but do not appear to penetrate AO ( Fig. 7 ). Apical organ sac, N = 3, 55–59 (57 ± 2) long by, N = 2, 33–37 (34.8 ± 2.9) wide. Apical organ sac not extending farther than posterior margins of suckers. Suckers, N = 6, 109–117 (112 ± 3) long by, N = 4, 84–89 (87 ± 2) wide. Neck, N = 1, 375–375 (375 ± 0) long by N = 2, 169–172 (170 ± 2.3) in maximum width. Strobila, N = 2, 88.28–128.58 mm (108.42 ± 28.49 mm) long, with 1,257 –1,266 (1,262 ± 6) proglottids; maximum width 2.72–3.41 mm (3.06 ± 0.49 mm) attained in gravid proglottids. Strobila anapolytic. Strobilar margins craspedote with intersegmental divisions plainly visible in mature and gravid proglottids; length: width ratio of mature and gravid proglottids 0.09–0.178 (N = 4) and 0.11–0.177 (N =4), respectively. Genital pores marginal, dextral, and non-alternating crossing osmoregulatory canals dorsally. Opening of genital pore ringed with deeply staining, densely packed cells. Genital atrium depth, N = 12, 20–25 (22 ± 2). Vaginal opening is anterior to cirrus opening in genital atrium. Dorsal osmoregulatory canals, N = 9, 19–24 (22 ± 2) wide. Ventral osmoregulatory canals, N = 9, 87–95 (92 ± 3) wide. Anlagen of genitalia N =1, 119–119 (119 ± 0) long. Cirrus sac piriform, N = 5, 121–145 (138 ± 10) in maximum length by, N = 5, 45–57 (52 ± 4) in maximum width, the antiporal end of cirrus usually overlapping excretory canal. Cirrus clavate, armed with minute spines. Cirrus armature arranged in welldefined rows. Internal seminal vesicle piriform in shape, N = 7, 80–93 (85 ± 4) long by, N = 8, 31–40 (34 ± 3) wide. External seminal vesicle, elongate fusiform, N = 3, 181–197 (191 ± 9) long by, N = 4, 92–97 (95 ± 2) wide. Testes ovoid, N = 15, 141–190 (167 ± 16) long by, N = 19, 95–121 (106 ± 8) wide, with one poral and two antiporal. Seminal receptacle, N = 4, 745–919 (841 ± 72) long by, N = 8, 75–93 (83 ± 7) wide, positioned anterior and dorsal to ovary and ventral to cirrus sac. Ovary, N = 8, 84–93 (90 ± 3) long by, N = 12, 168–203 (183 ± 12) wide. Ovary deeply lobed, fan shaped and compacted between testes. Vitelline gland, N = 8, 62–80 (72 ± 6) wide by, N = 7, 45–53 (50 ± 3) in maximum long, margins smooth. Vitelline gland near midline, anterior to intersegmental boundaries. Uterus developing laterally from origin in center of proglottid ( Fig. 8 ). Gravid uterus saccular, overlapping osmoregulatory canals and completely filling segment and displacing all internal gonadal tissues. Eggs, N = 52, 62–94 (74 ± 6) long by, N = 52, 40–63 (52 ± 4) wide, sub-spherical. Embryophore ( Fig. 9 ), N = 49, 31–46 (37 ± 3) long by, N = 49, 20–30 (26 ± 3) wide, sub-spherical. Embryo hooks as follows: Description of larger hooks of first and third pairs, hook length, N = 60, 16.0–19.9 (18.0 ± 1.0) by, N = 60, 3.4–4.8 (4.1 ± 0.4) wide at guard. Handle, N = 60, 6.8–11.0 (9.3 ± 0.9) long, blade, N = 60, 5.3–8.6 (7.1 ± 0.6) long. Larger hooks of first and third pairs with robust guard, thick handle, and a broad shallowly-curved, falcate, blade. Smaller hooks of first and third pairs, length, N = 41, 14.2–20.0 (17.5 ± 1.2) long b, N = 41, 2.3–3.3 (2.8 ± 0.2) wide at guard; handle, N = 41, 6.9–10.9 (9.1± 0.9) long, blade, N = 41, 5.4–8.6 (7.0 ± 0.7) long. Smaller hooks of first and third pairs narrow with thin guard and sub-falcate blade. Length of middle hooks, N = 21, 15.4–18.9 (17.1± 1.0) by, N = 21 1.6–2.3 (1.9 ± 0.2) wide at guard; handle, N = 21, 7.5–10.0 (9.0 ± 0.77) long; blade, N = 21, 5.6–8.2 (7.1 ± 0.6) long. Guard of middle pairs of hooks reduced relative to large outer hooks, blade deeply curved and falcate ( Fig. 9 ).

Etymology: This tapeworm species was named after the generic name of its type host “ cratogeomyos ” meaning “of Cratogeomys .”

Differential Diagnosis: Hymenolepis cratogeomyos n. sp. exhibits characteristics of Hymenolepis as defined by Yamaguti (1959) and Schmidt (1986) but later refined by Makarikov & Tkach (2013). There is no evidence that geomyid rodents have ever occurred in the Palearctic region ( Kurtén & Anderson, 1980) therefore we restrict comparison of this species with those of the genus Hymenolepis known to occur in mammals from the Nearctic and Neotropical regions, see Gardner (1985) and Gardner & Schmidt (1988). Hymenolepis cratogeomyos n. sp. can be recognized as distinct from all known species of Hymenolepis from the Nearctic region by possessing a greater width of dorsal osmoregulatory canal, longer seminal receptacle, and an apical organ sac with lightly crenulated margins.

Comparisons of H. cratogeomyos with other hymenolepidids from geomyid rodents

Hymenolepis cratogeomyos differs from H. geomydis in having a greater number of proglottids, longer apical organ, shorter and narrower apical organ sac, shorter neck, smaller vitelline gland, wider ventral osmoregulatory canals, longer and wider external seminal vesicle, smaller width of egg and embryo, anlagen of genitalia appearing earlier, wider guard of first and third pairs of large hooks, more compact ovary, and smooth vitelline gland margins.

Hymenolepis cratogeomyos n. sp. can be separated from H. weldensis by the following characters: wider strobila, a greater number of proglottids, longer apical organ, shorter and narrower apical organ sac, shorter neck, shorter cirrus sac, longer testes, longer and wider external seminal vesicle, expanded ovary, deeper genital atrium, narrower embryo, and earlier anlagen of genitalia. Hymenolepis cratogeomyos also differs from H. weldensis in the shape and armature pattern of the cirrus, the cirrus of H. cratogeomyos is partially clavate with well-defined gridded rows of minute hooks. Hymenolepis cratogeomyos differs from H. tualatinensis in being larger in all respects except that H. cratogeomyos has eggs possessing embryophores that are smaller and the anlagen appears earlier in the strobila. In addition, H. cratogeomyos differs from H. tualatinensis in having an ovary that is compact, fan-shaped, and with multiple lobes, genital pores, a cirrus that is clavate and with a different pattern of spines, and eggs with hooks that are much more robust than those in H. tualatinensis .

Hymenolepis cratogeomyos can be readily distinguished from H. irazuensis by the more compact ovary (not extremely bilobed as in H. cratogeomyos ) and the fact that the scolex has no sucker pockets. Hymenolepis cratogeo- myos can be readily distinguished from H. irazuensis in having a longer and wider strobila, greater number of proglottids, shorter and narrower apical organ sac, narrower neck, wider seminal receptacle, shorter and wider ovary, smaller vitelline gland, shorter and wider external seminal vesicle, deeper genital atrium, wider ventral excretory canal, and longer and wider eggs and embryo. The embryo hooks of H. cratogeomyos differ from the hooks of H. irazuensis by the following characters: a longer handle, blade, and total length and a narrower guard of the big and small hooks of the first and third pairs, and greater total length of the middle embryo hooks. Additionally, H. cratogeomyos has an ovary that is multilobed with deep small lobes and not extremely bilobed, cirrus sac that partially overlaps the ventral excretory canal, and a smooth-edged vitelline gland.

Comparisons of H. cratogeomyos with Hymenolepis species from Sciurid, Cricetid, and Murid Rodents in

the Nearcti c.

Hymenolepis cratogeomyos can be separated from H. robertrauschi in having a longer and wider strobila, greater number of proglottids, longer apical organ, shorter cirrus sac, longer and wider external seminal vesicle, wider ventral canals, narrower internal seminal vesicle, narrower embryo, and the anlagen of the genitalia appears earlier in the strobila. In addition, H. cratogeomyos differs from H. robertrauschi by the following characters: a piriform cirrus sac, cirrus armature arrangement of well-defined rows, and cirrus sac that crosses osmoregulatory canals to the mid line of the ventral canal, this in contrast to the cirrus sac of H. robertrauschi that does not touch or cross the osmoregulatory canals.

Hymenolepis cratogeomyos differs from H. pitymi by the following characters: longer and wider strobila, greater number of proglottids, shorter apical organ, wider apical organ sac, longer and wider neck, longer and wider cirrus sac, longer and wider external seminal vesicle, longer and wider internal seminal vesicle, wider seminal receptacle, longer and wider ovary, longer vitelline gland, deeper genital atrium, wider ventral excretory canals, longer and wider eggs, wider embryos, and greater total length of middle embryo hooks and a cirrus armature arrangement of well-defined gridded rows.

Hymenolepis cratogeomyos can be recognized as distinct from H. folkertsi in having a wider strobila, greater number of proglottids, shorter apical organ, shorter and narrower apical organ sac, deeper genital atrium, wider seminal receptacle, longer and wider external seminal vesicle, longer and wider testes, and wider ventral canals. Hymenolepis cratogeomyos can be distinguished from H. folkertsi in having the following characters: piriform cirrus sac that usually overlaps the ventral excretory canal, clavate cirrus, and a much more reduced AO relative to that of H. folkertsi .

Hymenolepis cratogeomyos is readily distinguishable from H. diminuta by the following characters: wider strobila, more great number of proglottids, longer apical organ, shorter and narrower apical organ sac, longer neck, shorter cirrus sac, wider external seminal vesicle, shorter internal seminal vesicle, deeper genital atrium, wider ventral excretory canals, narrower embryo, narrower guard of middle embryo hooks, and earlier anlagen of genitalia. Hymenolepis cratogeomyos can be recognized as distinct from H. diminuta by the following characters: non-alternating genital pores, a cirrus sac that usually overlaps the ventral excretory canal, and cirrus spines formed in evenly spaced rows and columns.

Generally, the characters that serve to distinguish H. diminuta from other species also suffice to distinguish H. citelli from other species as the adult characters of H. diminuta and H. citelli appear indistinguishable ( Gardner & Schmidt 1988). Hymenolepis cratogeomyos can be recognized as distinct from H. citelli by the following characters: wider strobila, shorter apical organ, shorter and narrower apical organ sac, longer and wider neck, longer and wider internal seminal vesicle, longer external seminal vesicle, longer testes, wider seminal receptacle, wider ventral excretory canal, wider cirrus sac, piriform cirrus sac, and a genital pore that is non-alternating. Note: It is the opinion of the authors that new specimens from the type locality of H. citelli should be collected to confirm its validity.

Hymenolepis cratogeomyos can be recognized as distinct from H. scalopi Schultz, 1939 described from Scalopus aquaticus Linnaeus, 1758 collected from the vicinity of Stillwater, Oklahoma by the following characters (see Table 2 ): wider strobila, greater number of proglottids, longer apical organ, shorter and narrower apical organ sac, earlier anlagen of genitalia, longer and wider external seminal vesicle, longer testes, wider seminal receptacle, shorter ovary, shorter vitelline gland, wider and shorter neck, deeper genital atrium, and a larger ventral excretory canal. In addition, H. cratogeomyos can be separated from H. scalopi in having a piriform cirrus sac that extends further than the ventral excretory canal, and a larger ovary that is expanded laterally. Note: It is interesting that this species has never been reported after its initial description. At this time we have been unable to locate the voucher specimens of the type host H. scalopi so it remains an enigma as to whether this cestode was actually recovered from a mole collected from near Stillwater, OK.

Prevalence of hymenolepidids in Geomyidae of Costa Rica and México

During the field work by Bonino in Costa Rica (1989–1990), 127 individuals of H. heterodus , were collected and examined for helminths. Hobergia irazuensis n. gen., n. sp. was found in 1.6% of all specimens examined; all infected individual pocket gophers were found at a single collection locality, occurring in 5.3% of those individuals of H. heterodus examined at the locality Potrero Cerrado.

Relative to Hymenolepis cratogeomyos n. sp., one individual of C. planiceps was incidentally found infected with cestodes ( Hafner et al. 2004).

Figures

FIGURE 7. Scolex of Hymenolepis cratogeomyos n. sp. showing relatively large apical organ sac.

FIGURE 8. Line drawing of one of the last mature proglottids (see text for definition) of Hymenolepis cratogeomyos n. sp.

FIGURE 9. Egg of Hymenolepis cratogeomyos n. sp. showing relatively delicate of development of embryo hooks with usual dimorphic hooks of the lateral pairs and the monomorphic hooks of the central pair in the embryophore larva