On Pseudoglaridacris laruei (Lamont, 1921) (Cestoda: Caryophyllidae) from Wisconsin, USA: A Review and Perspectives

Collections

Seasonal collections of 403 specimens of P. laruei from the white sucker C. commersoni and the lake chubsucker E. sucetta in Silver and Tichigan lakes, SE Wisconsin were made in April, 1976, April and November, 1977 and April, 1984. A total of 376 specimens of P. laruei were collected from 6 of 10 (60%) examined white suckers in Silver Lake (mean 37.6, maximum 263), and 21 specimens from 7 of 105 (7%) examined white suckers in Tichigan Lake (mean 0.2, maximum 8). In E. sucetta, a total of 5 cestodes were collected from 3 of 116 (3%) examined lake chubsuckers (mean 0.04, maximum 3) in Silver Lake and 1 cestode from 1 of 2 (50%) examined chubsuckers (mean 0.5, maximum 1) in Tichigan Lake.

The lakes

Silver Lake is a land-locked eutrophic natural lake (Kenosha County) (42°32′58″N,88°10′9″W). Tichigan Lake is a relatively large eutrophic impoundment on the Fox River which is a tributary of the Mississippi River in Racine County (42°48′20″N,88°13′00″W).

Methods

After capture and transfer to the laboratory in coolers on ice, the fish were dissected within a few hours after capture. Upon recovery, worms were placed at once in warm 70% ethanol then processed and stained with Semichon’s carmine. Worms were then processed in ascending concentrations of ethanol for dehydration reaching 100%. Worms were ultimately cleared in oil of winter green before whole mounting in Canada balsam. Measurements are in mm or micrometers as noted in Table 1; the range is followed by the mean values between parentheses. Width measurements represent maximum width. Microscope images were created using 10X and 40X objective lenses of a BH2 light Olympus microscope (Olympus Optical Co., Osachi- shibamiya, Okaya, Nagano, Japan) attached to an AmScope 1000 video camera (United Scope LLC, DBA AmScope, Irvine, California), linked to an ASUS lab top equipped with HDMI high-definition multimedia interface system (Taiwan- USA, Fremont, California). Images from the microscope were transferred from the labtop to a USB and stored for subsequent processing on a computer. We found microscope images to be considerably more informative than schematic line drawings as they depict the natural appearance of anatomical structures.

Brief Morphological Description of Adult Cestodes from Wisconsin

Body small-medium with distinct neck (Figs. 9,13), widest at gonopore (Figs. 19-24). It is often dorso-ventrally flattened, covered with thin cuticle enclosing prominent cortical parenchyma and inner and weaker outer longitudinal muscles. Measurements and counts in Table 1. Scolex somewhat bothrioloculodiscate, wider than long, widest near base with fairly parallel sides (II-shaped), tapering anteriorly to a frequently absent terminally hexagonal disc cut by 6 often poorly-demarcated loculi separated by frequently indefinite ribs (Figures 9,11-14). Younger specimens with anteriorly cone-shaped proboscis, no terminal disc and undefined loculi (Figures 1 & 6) as well as with incipient testes and vitellaria (Figure 3) and underdeveloped ovary and uterus (Figures 2,4,5). Scolexes of younger adults with poorly defined terminal disc and loculi (Figures 7,8,10). Testes spheroidal, large, in 2 medium parallel rows occasionally appearing with 3 rows where partially crowded. Testes developing first before vitelline glands (Figures 3,15- 18) and mature adults with testicular field occupying less space than vitellaria anteriorly and posteriorly. Cirrus sac small, round, near ventral surface (Figure 19). Vitelline glands smaller than testes, ovoid-elongate, multi-layered in 2 lateral fields (Figures 3,15-18), extending posteriorly to anterior end of ovarian arms. Vitellaria extend dorsally and ventrally about the edge of testicular field (Figure 18). Post-ovarian vitellaria few, often 1-3 (Figures 19- 22,24,26-29) or absent (Figures 23,25,30). Male and female reproductive systems do not open into common atrium. Vas deference detectable about middle of testicular field ventrally passing into muscular ejaculatorius at seminal vesicle then reaching cirrus sac dorsally and anteriorly at about center of medullary parenchyma. Distinctly lobate ovary H-shaped with long slender converging posterior arms appearing to join when tips of posterior ovarian arms link with few post-ovarian vitellaria often confused with ovarian lobules creating appearance of an inverted A-shaped ovary (Figure 19-29). Rarely, however, true inverted A-shaped ovary distinguishable especially with occasional absence of post-ovarian vitellaria (Figure 30). Ovarian commissure fanning at juncture with ovarian arms and tapering towards center (Figures 19,21). Vagina running posteriorly from female cloaca into receptaculum seminis then posteriorly to anterior and dorsal aspects of ovarian commissure. Uterine coils not extending anterior to cirrus sac but posteriorly reaching to posterior tip of posterior ovarian arms [19, 20, 21, 22, 23, 24, 25]. Posterior end usually conical (Figures 21,23,25,27), rarely rounded [20, 24] with slight terminal middle invagination where excretory vesicle and pore open tremino-ventrally. Egg small, ovoid, thin-shelled, non-operculate.

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Figures 1-6: Microscope images of developing Pseudoglaridacris laruei from Catostomus commersoni in Tichigan Lake, Wisconsin. 1, 2. The anterior and posterior portions of one small 3.1 mm long juvenile with underdeveloped scolex and reproductive system but with testes. 3, 4. The mid-section and posterior portion of one young maturing 5.6 mm long specimen showing underdeveloped vitellaria and posterior displacement of more developed testes (Figure 3) and incipient female reproductive system with barely developing ovarian arm and uterus (Fig. 4). 5. The posterior portion of another specimen with barely developing ovary comparable to that in Fig. 4. 6. A developing scolex of an older juvenile showing undefined loculi and no terminal disc.

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Figures 7-12: Microscope images of the scolexes of adult Pseudoglaridacris laruei from Erimyzon sucetta (Figure 7) and Catostomus commersoni (Figures 8-12) in Tichigan Lake, Wisconsin. Figures show variations in the demarcation of the scolex from anterior trunk (Figure 9) and the expression of loculi (Figures 9,11,12). The terminal disc is marginally developing only in Figures 9,11 and possibly Figure12. Magnification is to the same scale in all figures.

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Figures 13-18: Microscope images of the anterior portion (Figures 13 & 14) and the mid-section (Figures 15-18) of adult Pseudoglaridacris laruei from Catostomus commersoni in Tichigan Lake, Wisconsin. 13, 14. The anterior portions of 2 younger adults showing some delineation of scolex loculi with a suggestion of developing terminal disc. Note the anterior extension of vitellaria compared to testes especially in Figures 14. 15. A normal mid-section of a young adult specimen showing the relative size and shape of the vitellaria compared to the testes in 10X magnification. 16-18. Mid-sections of 3 fully developed adult worms similar to that in Figure15 all at the same magnification at 40X. Note the variation in size of testes and the extreme large size and detail of testes in Figure 18.

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Figures 19-24: Microscope images of the posterior portion of adult Pseudoglaridacris laruei from Catostomus commersoni in Tichigan Lake, Wisconsin. Variations in the shape and organization of the H-shaped ovary in 6 different adult specimens. Note that the long posterior ovarian arms of P. laruei converge to produce what appears to be an inverted A-shaped ovary when posteriorly conjoined with a few post-ovarian vitelline glands resembling ovarian lobules (Figures 19,20,24).

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Figures 25-30: Microscope images of the posterior portion of adult Pseudoglaridacris laruei from Catostomus commersoni in Tichigan Lake, Wisconsin. More variations in the shape and organization of the H-shaped (Figures 25-29) and inverted A-shaped (Figure 30) ovaries in adult specimens. Note the curving inward of the long posterior limb of ovarian arms and the position of the very few post-ovarian vitellaria creating the impression of an inverted A-shaped ovary (Figures 26-28).

Taxonomic Summary

• Type Host: White sucker Catostomus commersoni Lacépède
• Other Hosts: Lake chubsucker Erimyzon sucetta Lacépède, northern hogsucker Hypentelium nigricans (Lesueur), shorthead redhorse Moxostoma macrolepidotum (Lesueur) (Table 1)
• Type Locality: Lake Mendota, Wisconsin
• Other Localities: Green, Silver, and Tichigan lakes, Wisconsin; Douglas Lake, Michigan; Red Cedar River, NW Wisconsin (Table 1)
• Deposited specimens: US National Museum Helminthological collections nos. 78655, 78656 & Milwaukee Public Museum coll. no. IZ985-01B.

Remarks

The original description [17] was limited in scope but Lamont’s Figure 2 of a whole worm made up for much lost detail. It (Figure 2) showed a well-developed scolex with a terminal disc and 6 loculi, 74 large almost globular testes receding short of the field occupied by the compact vitelline glands anteriorly and posteriorly, H-shaped ovarian arms converging and connected posteriorly by a few post-ovarian vitellaria, and uterine coils not reaching past the cirrus sac anteriorly but extending to near posterior end of the worm. Lamont [17], however, over simplified her treatment, missed much detail and made a few errors such as stating that “This primitive scolex has four poorly defined suckers with an obscure terminal disk at the anterior end” (p. 2). True, in our specimens the scolex has poorly defined loculi and an obscure terminal disc but, however, it has 6 and not 4 loculi. Hunter [14] emphasized the deficiencies in Lamont’s description and provided novel observations and interpretations of unusual features. For example, he also acknowledged the “irregularly marked loculi … beneath the disc” (p. 70). Hunter [14] further defined the fibers of the outer longitudinal muscles as “infrequently found in the neck just under the basement membrane” (p. 71). Hunter [14] identified 8 pairs of ascending and descending excretory canals and reported 2 rows of testes but occasionally observed 1 or 3. Hunter [14] characterized the II-shaped scolex as belonging to Glaridacris different from that of Isoglaridacris hexacotyle in not being pointed distally and from G. catostomi in not being wedge-shaped. The scolex of both I. hexacotyle and G. catostomi shared 6 loculi with P. laruei but lacked its terminal disc. Hunter GW [14] also noted than P. laruei has the smallest cirrus sac and eggs, and that “the male and female reproductive systems do not open into a common genital atrium” (p. 75).

In our specimens, the scolexes may assume diverse shapes with the terminal disc protruding as Hunter [14]

previously observed. Hunter [14] speculated that in fully contracted scolexes, the terminal disc alone shows and that “the remainder of the scolex appears swollen laterally when the parallel longitudinal muscles within the scolex (are) drawn down inside by the action of the strong inner longitudinal muscles.” Hunter GW [14] also observed that the terminal disc may be absent, as we did, as it can be “pulled in between the bands or due to degeneration of the scolex before fixation” (p. 75). The typical II-shaped scolex characteristic of P. laruei was attributed to the action of the specialized muscles flattening the distal end [14].

Our specimens exhibited the usual variations in the shape of scolex, the number of testes and post-ovarian vitellaria as often observed by Mackiewicz JS [15] and Williams DD [16]. Specimens from C. commersoni, however, had smaller cirrus sac, and ovarian arms, shorter post-gonopore distance, and fewer post-ovarian vitellaria compared to those from E. sucetta. Our specimens from C. commersoni varied from those of Hunter GW [14] and Williams [16] who reported fewer testes and smaller cirrus sac (Table 1). In New York, Mackiewicz JS [15] concluded that P. laruei was the most common species of caryophyllids found in C. commersoni. In the Red Cedar River, Wisconsin, Williams DD [16] reported P. laruei from 2 additional species of suckers, Hypentelium nigricans (Lesueur) and Moxostoma macrolepidotum (Lesueur) and compared its morphometrics (Table 1) with those of Pseudoglaridacris oligorchis (Haderlie, 1953) Oros, Uhrovič, Scholz, 2018. Williams [16] presented 17 informative line drawings of immature, nongravid and gravid specimens from all hosts covering a considerable range of morphological variations.

Non-taxonomic issues from our local Wisconsin material included the persistent localization of worms in posterior intestinal sites, late summer early autumn recruitment and spring maturation, and localization in concurrent infections [12]. Other issues related to host and geographical distribution, misidentifications, size allometry, studies of scolex and neck, scolex glands, histopathology, and calcareous corpuscles were summarized by Hoffman GL [17].