Revisiting Hunterella nodulosa Mackiewicz and McCrae, 1962 (Cestoda: Caryophyllidae) from Catostomus commersoni (Lacépède) with a Special Treatment of its Ecological Diversity in Wisconsin Waters

Introduction

Mackiewicz [1] reviewed the morphology, anatomy, development, zoogeography, and systematics of the Caryophyllidea van Beneden, 1893 (Cestoidea) and indicated the existence of 89 species and 37 genera in these monozoic cestodes. Mackiewicz [2] provided perspectives on the evolution, biology, and zoogeography of 128 species in 45 genera of caryophyllids from the Nearctic, Neotropical, Palearctic, Ethiopian, Oriental, and Australian regions. Mackiewicz [3] later recognized about 150 species in 41 genera worldwide (except for the Neotropical Region). Of

these, 14 genera and 90 species belonging to 3 families were described from the Indo-Malayan region from Bagridae, Heteropneustidae, Schilbeidae and Siluridae, Cypriniformes and cobitid fishes [3]. Ash, et al. [4, 5] invalidated a large number of inadequately described species from clariid and catfishes in India and neighboring countries. Most recently, however, Scholz, et al. [6] and Scholz and Kuchta [7] recognized only 117 species and 46 genera in order Caryophyllidea Carus, 1863 parasitizing teleost fish (Cypriniformes, Siluriformes, and some catfish). Chubb JC [8] reviewed the seasonal ecology of the Caryophyllidea in the various climate zones of the world.

Amin OM [9, 10, 11, 12] recognized 15 species in 8 families of caryophyllid cestodes mostly from suckers (Catostomidae) in lake and river systems in Arizona and Wisconsin. These included Hunterella nodulosa Mackiewicz and McCrae, 1962 from Catostomus commersoni (Lacépède) in one lake and two river systems in Wisconsin. Hunterella nodulosa has had a turbulent nomenclature and taxonomic history since its original description as Monobothrium terebrans Linton, 1893 from Catostomus adrens (Jordan and Gilbert) in Wyoming. Nybelin [13] recognized Linton’s species in Monobothrium and Woodland [14] and transferred it to the genus Caryophylleaus Gmelin, 1790 as amended. Hunter [15] provided a detailed description of Linton’s [16] species as Caryophyllaeus terebrans (Linton, 1893) Char. emend, and coined his redescription as a “revised description … based on the original paper of Linton [16] upon some but not all of his original slides and some of the same species collected from Ictiobus bubalus (Rafinesque).” Hunter [15] (p. 30) considered this cestode as “the first cestodarian parasite to be recorded from North America.” Hunter [15] may have not picked up only Linton’s slides of Caryophyllaeus terebrans. In their description of H. nodulosa, Mackiewicz, et al. [17] (p.804) noted that the slides of Linton’s Caryophyllaeus terebrans paratypes included two different genera: H. nodulosa and “another worm corresponding to the “adult specimen” of Linton and Caryophyllaeus terebrans (Linton) as understood by Hunter [15]”. The primary difference between worms in these 2 genera was cited to be in the reproductive structures as depicted in figures 15 and 13. These authors Mackiewicz, et al. [17] ventured that this “other worm” could be Glaridacris catostomi Cooper, 1920 which often appeared in cross infections of C. commersoni with H. nodulosa. At this point in time, one wonders about the justification for creating a new taxon for C. terebrans since the generic diagnosis of Hunterella according to Mackiewicz and McCrae [17] perfectly matches the relevant elements of Linton’s [16] description and the follow-up by Hunter [15] instead of simply and selectively redescribing or revising Linton description based on slide USNM Helminthol. Coll. No.

51074 & 35.51a of the worm species Mackiewicz, et al. [17] considered H. nodulosa, as Hunter [15] did.

One will find the description of Linton [16] based on the above two slides to have embodied every single detail of the diagnosis of H. nodulosa in Mackiewicz and McCrae [17] quoted verbatim following. “Caryophyllaeidae without suckers, loculi, or other organs of attachment on scolex. Cirrus opens separately from female gonopore. Ovary H-shaped. Coils of uterus not extending anteriorly beyond cirrus pouch. Longitudinal muscles diffuse, not forming definite layers except in the posterior regions of the body. Inner longitudinal muscles loosely arranged in a broad band around the medullary region. Vitellaria embedded within this medullary region, generally surrounded on all sides by fibers of the inner longitudinal muscles. Post-ovarian vitellaria and external seminal vesicle present.” Based on the arguments of Mackiewicz and McCrae [17], other authors like Barčák, et al. [18] mistakenly listed the current taxonomic status or valid name of “Caryophyllaeus terebrans (Linton 1893) Woodland, 1923 as Glaridacris terebrans (Linton, 1893) Mackiewicz, 1974 (which was) “originally described in Monobothrium but Woodland [14] synonymized this genus with Caryophyllaeus.” What Barčák, et al. [18] were actually referring to is “the other worm” (slide no. 32.51b) and not slide no. 32.51a which contained Linton’s H. nodulosa as Mackiewicz [19] later on acknowledged. Mackiewicz [19] may have resolved this dilemma by declaring that “there are no authentic records of Caryophyllaeus Gemlin (with typical flabelliform scolex) in the Nearctic.” In Wisconsin, Amin [12, 20] gave an account of H. nodulosa from C. commersoni in the Pike and Root rivers and Tichigan Lake, SE Wisconsin, and made a brief distinction between it and the description of Mackiewicz, et al. [17].

Results

Amin [12] gave morphological notes of H. nodulosa from the Wisconsin population collected from the white sucker C. commersoni captured in Tichigan Lake, SE Wisconsin between 1976 and 1984. Amin [12] made initial taxonomic comparisons with specimens from other collections in Colorado and New York [17]. We have restudied specimens in our personal collection from Tichigan Lake as well as many other specimens from the Root and Pike Rivers in SE Wisconsin. Measurements of about 10 specimens were made in 1967-1968 [12] and new measurements and observations of additional specimens from the other collections in the Root and Pike Rivers were recently made and added to the earlier measurements creating combined measurements included in Table 1.

Our Wisconsin specimens were smaller than those from Colorado and New York [17] and had fewer testes and larger cirrus sacs (Table 1). Compared to the Wisconsin populations from Tichigan Lake and the Root River, those from the Pike River assumed frequent odd shapes and were characteristically and distinctly smaller in body size and corresponding sizes of scolex, vitellaria, testes, post- gonopore distance, external seminal vesicle, cirrus sac, ovarian arms, commissure, and eggs (Table 1).

We provide below an elaborate revised description based on our Wisconsin material and give detailed comparative morphometrical data (Table 1) high-lightening extreme variations from the other description by Mackiewicz, et al. [17]. Relevant concepts of Hunter [15] are considered. Our description traces anatomical structures from the scolex anteriorly to the posterior end, not essentially by organ system.

Discussion

While specimens of H. nodulosa from SE Wisconsin were collectively markedly smaller than those studied in New York and Colorado (Table 1), the growth of those from the Pike River appear to have been stunted compared to those from the adjacent Root River even though the smallest Pike River specimens (1.22 mm long) were sexually mature with eggs. We attribute such morphometric differences to physiographic factors related to water quality of the streams. Differences in the levels of non-fecal organic pollutants in these two streams and the higher flow rates in the larger Root River as calculated by the Southeastern Wisconsin Regional Planning Commission [21] may be related. Additionally, the Pike River specimens manifested the widest diversity of body forms exclusively including drop-shaped specimens (Figs. 2, 3).

Hunter’s [15] revision of Caryophyllaeus terebrans based on Linton’s [16] Monobothrium terebrans after Woodland’s [14] synonymization of the two genera was detailed but included elements of 2 species, one of which was later described by Mackiewicz and McCrae [17] as H. nodulosa. Hunter [15] recognized the possibility that he may have been dealing with two species when confronted with the other longer forms later recognized as a species of Glaridacris Cooper, 1920 by stating that “either Linton had representatives of two species or that one matured too early before the male reproductive system had completed its development, the reverse of the normal condition” (p. 33). Hunter [15] then dismissed the first possibility by immediately stating that “The latter explanation has been accepted by the author” (p. 34). Amin [12] have often observed that specimens of H. nodulosa “cohabited with G. catostomi in anterior intestinal locations of C. commersoni” [12] (Figs. 1,2, p. 51, 52).

Some of the elements of Hunter’s [15] treatment of Linton’s [16] account attributable to H. nodulosa as we now recognize it includes being embedded in intestinal wall in pits, reproductive systems opening apart, scolex bluntly cone-shaped with no suckers or loculi, vitellaria being “marginal” and posterior, and H-shaped globular ovary. Some of his [15] elements not attributable to H. nodulosa include adults as long as 30 mm long, distinct neck, inner and outer longitudinal muscles present and equally prominent, and absence of seminal receptacle.

The description of H. nodulosa by Mackiewicz and McCrae [17] was thorough almost leaving no detail uncovered. The description of that new genus was almost identical to that of Linton’s, partim [16] and the distributional records and morphological treatment were meticulous. Few statements, however, produced the following questions. For example, unlike their Fig. 3 (p. 800) of a mature worm correctly showing anterior-most testes to be more anterior than anterior-most vitellaria, Fig. 6 of a “larva” (actually a young adult with an incipient reproductive system with identifiable male and female gonopores, testes, and vitellaria) depicting anterior-most testes well posterior to anterior-most vitellaria [17]. In our specimens developing juveniles have a complete set of testes before vitellaria began to emerge. They [17] described the vitellaria as “arranged circularly around testes” (p. 799). Their cross-section (Fig. 13, p. 802) does depict this arrangement which appears to be true but only at the posterior body as Fig. 3 of a mature worm suggests. However, for most of the length of the body, the pre-ovarian vitellaria appears to be primarily lateral with an only occasional incursion into the testicular medullary field (our figures 7, 8); microscope images don’t lie. Their fixed specimens (Fig. 9) assumed a wide variety of atypical forms [17] the last of which was similar to our drop-shaped fixed specimens from the Pike River (Figs. 2,3). A line drawing of one such specimen was incorrectly placed with others of Biacetabulum biloculoides Mackiewicz and McCrae, 1965 collected from C. commersoni in the Root River [11]. These authors [17] did not explain why the number of testes or the size of eggs were discretely different between specimens from New York and those from Colorado. The disconnected distribution of worms from the same host species in separate waters within Wisconsin and in various states may be related to the disjunct post-glacial distribution of their primary hosts.

Acknowledgments

This project was supported by an Institutional Grant from the Parasitology Center, Inc. (PCI), Scottsdale, Arizona.

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.