New Perspectives on Isoglaridacris multivitellaria Amin, 1986 from the Lake Chubsucker Erimyzon sucetta (Lacépède) in Silver Lake, Wisconsin

Introduction

Amin [1, 2, 3, 4] recognized 15 species in 8 families of caryophyllid cestodes mostly from suckers (Catostomidae) in lake and river systems in Arizona and Wisconsin. In Wisconsin, 13 species in 8 genera and 2 families (order Caryophyllidea Van Beneden, in Carus, 1863) were recovered from 3 catostomid and 1 cyprinid fish species in 2 southeastern Wisconsin lakes. The diversity of cestode species was considerably greater (11 species) in Tichigan Lake, connected to the larger Fox River, a tributary of the Mississippi River (the prevalence was, however, lower) than in the smaller land-locked Silver Lake (4 species including Isoglaridacris multivitellaria Amin, 1986). Conditions in Silver Lake appeared to “enhance denser populations of some species including Glaridacris catostomi Cooper, 1920, and Pseudoglaridacris laruei (Lamont, 1921) Oros, Uhrovič, Scholz, 2018 and the acceleration of sexual development and /or early elimination of gravid specimens of others, e.g., G. catostomi and Isoglaridacris agminis Williams and Rogers, 1972 [4]”. Isoglaridacris multivitellaria appears to have a high host specificity in E. sucetta and a highly specific distribution in Silver Lake, and its geographical distribution appears to be of limited and disjunct nature.

Results

Amin [4] gave the only morphological description of I. multivitellaria from the one known population of four specimens collected from one lake chubsuckers E. sucetta captured in Silver Lake, SE Wisconsin in November, 1978. This species has not been reported from E. sucetta or any other host since. He [4] included 9 suitable line drawings of whole or parts of worms (Figs. 5-13). We have restudied two specimens in our personal collection as well as the holotype and the allotype deposited in the Helminthological collection at the Department of Invertebrate Zoology of the National Museum of Natural history, Smithsonian Institution. We have complemented the original description with additional observations and provided microscope images of greater demonstrative value of more features. Table 1 summarizes all currently available measurements and ratios, old and new, and provides a descriptive account of internal anatomical structures. An outline of the updated description is provided below.

Revised Description of I. multivitellaria from E. sucetta in Silver Lake, Wisconsin

Based on 4 specimens. See Table 1 for measurements, ratios, and Figures 1-21 for microscope images. With characters of the genus Isoglaridacris. Worms of medium length, dorsoventrally flattened, widest at gonopore. Scolex fan-shaped with 3 pairs of very shallow loculi (Figs. 1,2). Neck of moderate size, with slight constriction (Fig. 3). Outer longitudinal muscles barely visible (Fig. 1). Testes medullary, usually spheroid but sometimes slightly longer than wide (Figs. 4-9), extending anteriorly about 23-28% of worm length from anterior tip and to near cirrus sac posteriorly. External seminal vesicle obvoid, dorsal, overlapping cirrus sac. Pre-ovarian vitellaria round-ovoid-laterally elongate, smaller than testes, in 2 primary lateral multilayered rows (Fig. 10) that irregularly extend and often merge medially (Figs. 5-9), beginning well anterior to testes anteriorly (Figs. 4, 6) with a distance of 12-21% of worm length. Posteriorly, they terminate medially at site of cirrus sac but decrease in number as they extend more posteriorly in an inverted V-pattern up to a short distance from anterior margin of ovarian arms (Figs. 11, 12). Cirrus sac distant anteriorly, far from ovary, at pit of inverted V-shaped posterior fork of pre- ovarian vitellaria, unarmed, round, large with clear external pattern of concentric rings (Figs. 11, 12). Ovary follicular with anterior arms occasionally unequal, much longer than posterior arms, with thick, commissure scarcely follicular (Figs. 13-17). Vagina straight (Fig. 12), curving just posterior to commissure, without seminal receptacle. Uterine coils between cirrus sac and posterior ovarian arms; indiscernible posterior to commissure. Utero-vaginal canal joins cirrus opening up on the surface as a single gonopore at a distance from posterior end of about 24-32% of worm length. Area between posterior ovarian arms and anterior margin of post-ovarian vitellaria (Figs. 18, 19) not visibly occupied by distinguishable structures except for possible posterior uterine coils. Post-ovarian vitellaria (Figs. 19-21) extensive, numbering 67-100, not continuous with pre-ovarian vitellaria, but usually close to posterior margin of posterior ovarian arms, covering an area of 1.05-1.50 X 0.47-0.70 mm. Eggs ovoid, smooth-shelled, with yolk cells.

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Figure 1-6: The anterior section of specimens of Isoglaridacris multivitellaria from Erimyzon sucetta in Silver Lake, SE Wisconsin. 1, 2. The scolexes of 2 individuals. 3, 4. Scolex, neck and anterior pre-ovarian vitellaria of the allotype specimen. Note the anterior-most testis in Fig. 4 (arrow) well posterior to first vitellaria. 5. Higher magnification of anterior-most testis of allotype specimen. Note the beginning of the medullary merging of lateral vitellaria. 6. High magnification of the allotype section just posterior to that shown in Fig. 5 showing more crowded vitellaria in the middle of the testicular field.

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Figure 7-12: The mid-section of specimens of Isoglaridacris multivitellaria from Erimyzon sucetta in Silver Lake, SE Wisconsin. 7-9. Variations of the frequency of irregular extension of lateral vitellaria into the middle testicular field. In Fig. 9, they practically congest the whole middle section. 10. A lateral perspective of extruded cirrus sac across from multi-layered rows of pre-ovarian vitellaria dorsally (top). 11. The position of the cirrus sac (arrow) at the pit of the inverted V-shaped posterior margin of pre-ovarian vitellaria. 12. A high magnification of the cirrus sac showing its characteristic external concentric rings and the straight vagina (arrow).

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Figure 13-18: The ovarian structure of specimens of Isoglaridacris multivitellaria from Erimyzon sucetta in Silver Lake, SE Wisconsin. 13. The anterior unequal ovarian arms of the allotype. 14. The mid-section of the unequal ovarian arms of the allotype showing the robust V-shaped commissure. 15. The unequal anterior ovarian arm of another specimen. 16. Detail of one side of the ovary showing the long anterior arm, commissure (arrow), and the short posterior arm. 17. A clear view of the unequal ovarian arms of the allotype. 18. The space between the posterior margin of the ovary (right) and the anterior margin of the post-ovarian vitellaria (left) with no clear evidence of the presence of post-ovarian uterine coils.

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Figure 19-21: The post-ovarian vitellaria of the allotype of Isoglaridacris multivitellaria from Erimyzon sucetta in Silver Lake, SE Wisconsin. 19. A whole view of the posterior body segment enclosing the post-ovarian vitellaria. 20, 21. Higher magnification of the posterior and anterior post- ovarian vitellaria, respectively.

Discussion

Despite the limitations of the small number of specimens available for this study, we have been able to shed considerably more light on the morphological features characterizing this unusual cestode. We have provided a more comprehensive morphological treatment of I. multivitellaria. Ecological factors add to the distinctiveness of this cestode. Only 4 worms were found in one individual lake chub sucker in one land-locked lake in Wisconsin when 116 lake chubsuckers were examined in the same lake between 1976 and 1984 [4]. It is clearly a rare cestode. This scarce occurrence has been similarly documented in at least two other incidences. The description of I. erraticus Williams, 1975 was based on 7 specimens recovered from one individual of Moxostoma sp. and that of I. etowani Williams, 1975 on 154 specimens from one (of 87) Hypentelium etowanum (Jordan) [8].

The ecological distribution of I. multivitellaria is comparable to that of Isoglaridacris agminis Williams and Rogers, 1972 in Wisconsin. In Wisconsin, both cestode species were collected only from E. sucetta in Silver Lake, SE Wisconsin. Williams, et al. [10] originally described I. agminis from E. sucetta in Alabama and since then it was reported mostly from the same host species in Arkansas, North Carolina, Mississippi, and Florida (Fig. 31 in Amin, et al. [9]). The sporadic distribution of I. agminis in independent waters in these states appear to be related to the disjunct distribution of E. sucetta in North America which was well documented by Mandrak, et al. [11]. See map (Fig. 31 in Amin, et al. [9]). Trautman [12] hypothesized that this “fragmentation was the result of northeastern range expansion during the warm Hypsithermal Period (ca. 7000 to 5000 years before present), and subsequent range contraction and fragmentation during the wane of this Period” (page 5). This fragmentation left residual pockets of suckers in isolated streams along with their parasites including I. multivitellaria. Figure 31 in Amin, et al. [9] shows the extension of E. sucetta into the SE third of Wisconsin including Kenosha County where the land-locked Silver Lake is located in the SE corner of the state. A similar pattern appears to occur in other species of fish parasites. For instance, Amin [13] demonstrated that the present distribution of 3 species of acanthocephalans of the genus Acanthocephalus Koelreuter 1771 in North America, especially Acanthocephauls dirus (Van Cleave, 1931) in the post-glacial streams of SE Wisconsin “formed after the withdrawal of the Lake Michigan lobe of the Wisconsin ice sheet from the area between 15,000 and 12,000 B.P. (page 216).” It is not unlikely that future research may produce new records of I. multivitellaria and of I. agminis, from E. sucetta in states within its range where infections in chubsuckers have not been reported, i.e., Georgia, Louisiana, or Michigan.

Acknowledgments

This project was supported by an Institutional Grant from the Parasitology Center, Inc. (PCI), Scottsdale, Arizona. We recognize the efforts by a number of former independent study students at the University of Wisconsin-Parkside, Kenosha for help with collecting and processing collections of fish parasites in lakes and streams of SE Wisconsin over the years, notably Pat Adams, Leslie Burns, Janet Burrows, Marsha Cowen, and Robert Bauer.

Declarations

Compliance with Ethical Standards

• Conflict of Interest: The authors declare no conflicts of interest or competing interests.
• Ethical Approval: The authors declare that they have observed all applicable ethical standards.
• Availability of Data: All presented and related data are available by contacting the senior author.