Bothriocephalus kupermani, Choudhury & Scholz & Beuchel, 2022

Choudhury, Anindo, Scholz, Tomáš & Beuchel, Joseph S., 2022, A New Species Of Bothriocephalus (Cestoda: Bothriocephalidae) From Lepomis Spp. (Actinopterygii: Centrarchidae) In North America, Journal of Parasitology 108 (4), pp. 343-352 : 344-348

publication ID	https://doi.org/ 10.1645/21-70
publication LSID	lsid:zoobank.org:pub:2F4250A3-6CA6-48DE-8232-5E9333C7DFF9
DOI	https://doi.org/10.5281/zenodo.7756204
persistent identifier	https://treatment.plazi.org/id/701C450F-6CE8-4CF8-ADB6-164F49BBAF39
taxon LSID	lsid:zoobank.org:act:701C450F-6CE8-4CF8-ADB6-164F49BBAF39
treatment provided by	Felipe
scientific name	Bothriocephalus kupermani
status	sp. nov.

Treatment

Bothriocephalus kupermani View in CoL n. sp.

( Figs. 1–4 View Figure 1 View Figure 2 View Figure 3 View Figure 4 )

Informal synonyms: ‘ Bothriocephalus sp. ’ (PBI-487) of Brabec et al. (2015); ‘Pumpkinseed morph’ of Choudhury and Scholz (2020).

Material studied: The description is based on whole, unstained, and unmounted specimens, specimens processed for SEM, and 18 specimens prepared as stained whole mounts. Measurements are from stained whole mounts as follows (number of worms in parentheses): 8 gravid specimens and 1 mature non-gravid specimen from pumpkinseed from Paul Lake, 5 November 2001 (2), Peter Lake, 13 July 2003 (4). Bolger Bog, 12 August 2003 (2) and Caribou Lake (1), and 1 gravid specimen from green sunfish from Duck Creek on 12 July 2009. In addition, 8 stained immature worms from pumpkinseed from Paul Lake, Peter Lake, and Shawano Lake were also studied but not used for measurements.

Description: Bothriocephalidea , Bothriocephalidae . Body 21– 43 mm (35 mm) long, maximum width 973–1,595 (1,078) in posterior third. Strobila gradually widening posteriorly, comprising craspedote proglottids (primary and secondary), trapezoidal especially in anterior half, posterior proglottids with rounded edges, often losing craspedote appearance ( Figs. 1 View Figure 1 , 2 View Figure 2 ); proglottids covered with coniform spinitriches ( Fig. 4F, G View Figure 4 ). Except for first few proglottids, immature proglottids including those without obvious anlagen of gonads numerous, wider than long, mature proglottids (with sperm in external sperm duct) very few (1–2), 175–507 (495) long by 781–1,232 (894) wide, length:width ratio 0.11–0.55 (0.55). Gravid proglottids much wider than long ( Fig. 1D, E View Figure 1 ), first gravid proglottid 183–512 long by 750–1530 wide, length:width ratio 0.15–0.55, proglottids often narrower at end of strobila, posterior-most proglottid 252–750 (750) long by 751– 1,208 (751) wide, length:width 0.2–1.0 (1.0).

Longitudinal musculature well-developed, formed by numerous muscle fibers. Osmoregulatory canals usually in several (usually 2–3) pairs ( Fig. 1E View Figure 1 ). Ventral osmoregulatory canals wide, sinuous to almost straight ( Fig. 1E View Figure 1 ). Dorsal osmoregulatory canals narrow, thin-walled, slightly sinuous, median to ventral osmoregulatory canals ( Fig. 1E View Figure 1 ).

Scolex 414–805 (458) long, with nearly parallel margins through most of its length, dorsoventrally ( Figs. 1B, C View Figure 1 , 2 A, D View Figure 2 , 3A, B View Figure 3 ) and laterally ( Figs. 1A View Figure 1 , 2C View Figure 2 , 3C View Figure 3 , 4B View Figure 4 ), occasionally slightly wider in middle ( Figs. 1A View Figure 1 , 3C View Figure 3 , 4A View Figure 4 ), maximum lateral width 151–210, maximum dorsoventral width 183–296 (296). Scolex gently narrowing anteriorly before widening to form slightly convex (almost blunt in dorsoventral view), bilobed apical disc with rounded outer corners ( Figs. 1A–C View Figure 1 , 3A–C View Figure 3 , 4A– C View Figure 4 ). Apical disc 151–215 wide laterally, 179–234 (234) wide dorsoventrally. Bothria shallow, wide, opening anteriorly to shallow hollow at base of apical disc ( Figs. 1B, C View Figure 1 , 3A, B View Figure 3 , 4A View Figure 4 ). Lateral surface of scolex may possess medial, shallow groove ( Figs. 4 A, B View Figure 4 ). Neck short, 105–180 (180) wide, almost as wide as scolex and first proglottid ( Figs. 1A–C View Figure 1 , 2A–D View Figure 2 ). Scolex with coniform spinitriches, capilliform filitriches, tumuli ( Fig. 4A, D View Figure 4 ), patch/tuft of capilliform filitriches at center of apical disc ( Fig. 1C, E View Figure 1 ).

Testes oval to subspherical, variable in size, 36–83 long by 26– 57 wide, medullary, 38–62 (49) per proglottid, ovoid to spherical, in 2 lateral fields on each side; most testes in main external (outer) field between ventral osmoregulatory canals, with only few testes in inner, narrow irregular field, median to internal ventral osmoregulatory canal ( Figs. 1E View Figure 1 , 3F View Figure 3 ). Cirrus sac median, anterior to ovary, transversely oval to subspherical in dorsoventral view, 61–74 (74) long by 63–90 (78) wide, leading to common genital pore on mid-dorsal surface of proglottid ( Fig. 1E View Figure 1 ); genital pore postequatorial to almost equatorial, situated at 51–65% of proglottid length; external sperm duct (vas deferens) lateral to cirrus sac ( Fig. 1E View Figure 1 ).

Ovary compact, median, near posterior margin of proglottid, irregular in shape (slightly asymmetrical), weakly bilobed, with narrower mid-region (ovarian isthmus), 62–100 (88) long by 218– 368 (248) wide ( Figs. 1E View Figure 1 , 3E View Figure 3 ), occupying 23–38% of proglottid width. Vagina tubular, narrower in proximal part, sinuous, widened, thick-walled in distal part, opening to common genital pore on dorsal surface ( Fig. 1E View Figure 1 ). Vitelline follicles very variable in shape, from elongate to almost spherical, 25–61 long by 20–46 wide, cortical, extensive, forming wide lateral fields on each side of proglottid from its lateral margins to beyond dorsal osmoregulatory canals medially, also variably and more sparsely present medially, often confluent by narrow field at level of ovary and uterine pore ( Figs. 1D, E View Figure 1 , 3D View Figure 3 ).

Uterus tubular, thick-walled, looped in proximal part (anterodorsal to ovary and dorsal to vagina), then turning anterolaterally, circumventing vaginal canal ventrally, thereafter directed anteriorly, winding ( Fig. 1E View Figure 1 ). In gravid proglottids, terminal (distal) part enlarged to form transversely oval, thick-walled uterine sac filled with numerous eggs; width of uterine sac in last proglottids 44–69% of proglottid width (usually about 50%). Uterine sacs open on ventral surface by almost medially situated, slit-like uterine pore situated at variable distance (at 18–37% of proglottid length) from anterior margin of proglottids ( Figs. 1D, E View Figure 1 ). Eggs ovoid, 46–54 long by 32–34 wide (n ¼ 48), tanned when fully developed, operculate, unembryonated in utero.

Taxonomic Summary

Type host: Lepomis gibbosus (Linnaeus, 1758) (Centrarchiformes: Centrarchidae ).

Additional hosts: Lepomis cyanellus Rafinesque, 1819 (this study and museum material), L. macrochirus Rafinesque, 1819 (museum material), L. megalotis (Rafinesque, 1820) (museum material) (all Centrarchiformes: Centrarchidae ) (see Table I View Table I ).

Site of infection: Intestine.

Type locality: Paul Lake (46°15 ′ 04.78 ′′ N, 89°30 ′ 12.94 ′′ W; 516 meters above sea level [m a.s.l.]), University of Notre Dame Environmental Research Center ( UNDERC), Michigan ( Upper Peninsula ) near Land-o-Lakes, Wisconsin. GoogleMaps

Additional localities: Peter Lake (46°15 ′ 10.17 ′′ N, 89°30 ′ 12.94 ′′ W; 518 m a.s.l.); GoogleMaps Bolger Bog (46°13 ′ 47.37 ′′ N, 89°29 ′ 96 ′′ W; 507 m a.s.l.), both UNDERC lakes, Wisconsin; GoogleMaps Shawano Lake , Wisconsin (44°47 ′ 11.88 ′′ N, 88°32 ′ 39.60 ′′ W) GoogleMaps ; Caribou Lake , Minnesota (47°42 ′ 59.04 ′′ N, 90°39 ′ 18.18 ′′ W) GoogleMaps , Duck Creek near Hobart , Wisconsin (44°32 ′ 01.09 ′′ N, 88°07 ′ 44.89 ′′ W) GoogleMaps , Fox River at Voyageur Park, De Pere , Wisconsin (44°27 ′ 03.39 ′′ N, 088°03 ′ 51.83 ′′ W) GoogleMaps .

Geographical distribution: Canada (Ontario) , Mexico (precise locality not known; fish host introduced), United States (Alabama, Michigan, Minnesota, Nebraska, Ohio, Oklahoma, Wisconsin) .

Infection rate: Mean abundance: 20.6 ± 25.3; 0–112 tapeworms/fish; prevalence: 83% of 30 fish examined from the type locality.

Type material (all from L. gibbosus ): Holotype: USNM 1593369 View Materials , Paul Lake , UNDERC , Michigan, 5 November 2001 . Paratypes: USNM 1593370–1593373 View Materials , HWML 216811–216817 View Materials , IPCAS C-914 /1.

Molecular data: The following DNA sequence data are available in GenBank (https://www.ncbi.nlm.nih.gov/genbank/) (the region of the genome is followed by the GenBank accession number: 18S rDNA (ssr DNA): KR780953 View Materials , 18S rDNA (V8 region, partial): MT532462 View Materials – MT532463 View Materials ; ITS-1 (partial): MT532532 View Materials – MT532537 View Materials ; ITS-2 (partial): MT532512 View Materials – MT532513 View Materials ; 28S rDNA (lsr DNA): KR780906 View Materials , 16S rDNA (rrnL): KR780867 View Materials ; cytochrome c oxidase subunit 1 (COI): KR780814 View Materials .

ZooBank registration: urn:lsid:zoobank.org:act:701C450F-6CE8-4CF8-ADB6-164F49BBAF39 .

Etymology: The species is named after the late Boris Kuperman, whose sudden demise in 2002 robbed parasitology of a wise, gifted, and gentle practitioner who continued his new life in the United States with the same lifelong passion he always had for our beloved subject, and whose seminal work on the genus Triaenophorus inspired the senior authors (A.C. and T.S.) many years ago.

Remarks

Bothriocephalus kupermani differs from other species of Bothriocephalus parasitizing freshwater fishes in North America, namely B. claviceps , B. cuspidatus , B. formosus , and B. pearsei , by the following characteristics: (1) the scolex is almost rectangular in dorsoventral and lateral profiles, with nearly parallel margins (vs. arrow-shaped and narrowing towards the apical disc in B. cuspidatus and with maximum width in the anterior third in B. claviceps ), with shallow and wide bothria with almost parallel margins (widest in the posterior or middle part in other taxa); (2) small body size (maximum of 43 mm vs. 133 and 137 mm in B. cuspidatus and B. claviceps , respectively; Scholz, 1997); and (3) extensive vitelline follicles that are also present medially, i.e., in the cortex of the ovarian and uterine region (absent anteriorly and never or seldom confluent posteriorly in other species except B. formosus , which has markedly different scolex and tiny strobila compared to the new species; see Scholz, 1997; Choudhury and Scholz, 2020). Bothriocephalus kupermani is also typified by a relatively high number of immature proglottids without obvious anlagen of gonads and fewer testes (38–62) than B. cuspidatus from Walleye (62–101).

The validity of B. kupermani is also supported by molecular data of Brabec et al. (2015; isolate called ‘ Bothriocephalus sp. n., ‘PBI-487 ′ in their fig. 2) and Choudhury and Scholz (2020). The specimen from green sunfish, L. cyanellus , is similar in its morphology to specimens from the type host, L. gibbosus , and is considered conspecific.