Acanthobothrium ulondolozus, Spuy & Smit & Schaeffner, 2022

Spuy, Linda Van Der, Smit, Nico J. & Schaeffner, Bjoern C., 2022, Threatened, host-specific affiliates of a red-listed host: Three new species of Acanthobothrium van Beneden, 1849 (Cestoda: Onchoproteocephalidea) from the endangered white skate, Rostroraja alba (Lac´ep`ede), International Journal for Parasitology: Parasites and Wildlife 17, pp. 114-126 : 121-123

3.4. Acanthobothrium ulondolozus n. sp. ( Figs. 5 and 6)

Description (based on whole mounts of seven mature worms; two mature worms examined with SEM): Worms 9.3–13.5 mm long, greatest width at level of scolex, 32–50 proglottids per worm, euapolytic. Scolex consisting of scolex proper and cephalic peduncle. Scolex proper with four bothridia, 486–599 long by 324–520 wide. Bothridia free posteriorly, 168–190 wide; each bothridium with three loculi and specialised anterior region in form of muscular pad. Muscular pad 128–150 long by 146–162 wide, falciform in shape, with pronounced posterior margin, bearing accessory sucker and one pair of hooks at posterior margin; accessory sucker 27–37 long by 35–48 wide. Anterior loculus (A) 201–212 long; middle loculus (M) 72–120 long; posterior loculus (P) 97–113 long; loculus length ratio (A: M: P) 1.00: 0.53: 0.52; maximum width of scolex at level of middle loculus. Velum absent.

Hooks bi-pronged, hollow, with tubercle on proximal surface of axial prongs; internal channels of axial and abaxial prongs continuous, smooth; axial prongs slightly longer than abaxial prongs; lateral and medial hooks approximately equal in size. Lateral hook measurements: A 60–75, B 154–160, C 131–144, D 212–220. Medial hook measurements: A ′ 62–73, B ′ 144–165, C ′ 121–144, D ’ 203–211. Bases of lateral and medial hooks approximately equal in length; base of medial hook slightly overlapping base of lateral hook along medial axis of bothridium ( Fig. 5D); medial hook base slightly wider than lateral hook base. Tissue covering almost entire length of each prong of hooks. Short cephalic peduncle 1044–1430 long by 76–98 wide.

Cephalic peduncle densely covered with gladiate spinitriches, filitriches not observed ( Fig. 6C). Apical pad and distal bothridial surface covered with papilliform to acicular filitriches and extremely sparsely interspersed gladiate spinitriches ( Fig. 6D). Proximal bothridial surface and bothridial rims covered with gladiate spinitriches, interspersed with acicular filitriches ( Fig. 6E). Anterior region of strobila covered in acicular filitriches ( Fig. 6F). Anterior region of terminal proglottid covered in capilliform filitriches ( Fig. 6G).

Proglottids acraspedote. Immature proglottids 29–48 in number; 2–3 mature proglottids; gravid proglottids absent; terminal proglottid 1063–2134 long by 284–356 wide; terminal proglottid length to width ratio 3.2–6.3: 1.0. Proglottids protandrous; genital pores marginal, irregularly alternating ( Fig. 5A), 48–59% of proglottid length from posterior margin.

Testes conspicuous in mature proglottids, oval in dorsoventral view, 50–61 long by 40–52 wide, arranged in one to two layers in intervascular field ( Fig. 5C), 50–62 in total number, 8–9 in post-poral field; some segments with single testis posterior to ovarian isthmus. Cirrus-sac J-shaped, tilted posteriorly ( Fig. 5C), 171–232 long by 60–73 wide, containing armed cirrus; cirrus greatly expanded at base.

Vagina narrow, relatively thin-walled and straight proximally, extending from ootype along medial line of proglottid to anterior margin of cirrus-sac, then laterally to common genital atrium. Vaginal sphincter prominent ( Fig. 5C). Ovary occupying about half of proglottid length, almost reaching posterior margin of proglottid, H-shaped in dorsoventral view, lobulated ( Fig. 5C), asymmetrical, 107–149 wide at level of ovarian isthmus; poral lobe 431–981 in length; aporal lobe 503–1133 in length; ovarian lobes not reaching cirrus-sac anteriorly; ovarian isthmus located posterior to mid-level of ovary. Mehlis’ gland posterior to ovarian isthmus.

Vitellarium follicular to lobulated; follicles in two lateral bands, 13–21 long by 23–43 wide, length relative to testis length 0.2–0.4: 1.0; each band consisting of two columns, extending from posterior margin of anterior-most testes to near posterior margin of ovary ( Fig. 5C). Vitelline follicle length relative to testis length 0.2–0.4: 1.0. Uterus thin-walled, extending from ovarian isthmus to near anterior margin of proglottid. Eggs not observed.

Type host: White skate, Rostroraja alba (Lac´ep`ede) ( Rajiformes : Rajidae ).

Type locality: Danger Point , Gansbaai, South Africa [34 ◦ 28 ′ 50’’S, 19 ◦ 19 ′ 55’’E] .

Site of infection: Spiral intestine.

Prevalence of infection: 50% (one of two skates examined).

Type material: Holotype deposited at NMB (Accession number: XXX), paratypes in NMB (Accession numbers: XXX-XXX), IPCAS (Accession numbers: XXX-XXX) and MHNG (Accession numbers: XXX-XXX).

ZooBank number for species: XXXXXX.

Etymology: The species name “ ulondolozus ” is derived from “ulondolozo” [Xhosa; an indigenous language to the Eastern and Western Cape of South Africa] meaning “conservation”, referring to the need for having better conservation plans for threatened elasmobranch species, which would also protect a wide variety of host-specific affiliate species facing an increased risk of co-extinction.

Remarks

All of the new species described in the present study seem most distinguishable by their hooks. Just as Acanthobothrium umbungus n. sp. and A. usengozinius n. sp., A. ulondolozus n. sp. is identified as a category 2 species. However, unlike the two new congeners, A. ulondolozus n. sp.

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is the only species in the present study with occasional testes posterior to the ovarian isthmus. This is still regarded as an exceptional feature among species of Acanthobothrium , being present in less than 10% of all species recognised within this genus worldwide. Hence, A. ulondolozus n. sp. can easily be distinguished from all but 16 congeners (across all categories). From the remaining 16 species of Acanthobothrium known to bear this feature, only six are identified as category 2 species, namely A. bobconniorum , A. crassus , A. dolichocollum , A. microhabentes , A. microtenuis , and A. popi . Acanthobothrium microhabentes and A. microtenuis were only recently described from the same biogeographical region by Van Der Spuy et al. (2020). However, both species differ from A. ulondolozus n. sp. in smaller metrical features (i.e. total length, scolex length, scolex width, bothridium width, lateral hooks, medial hooks, cephalic peduncle width, cirrus-sac length, poral and aporal ovarian length, ovarian width; see Van Der Spuy et al., 2020), while A. bobconniorum , A. crassus , A. dolichocollum and A. popi differ from A. ulondolozus n. sp. in the following features: smaller lateral hooks (A <60 μm vs 60–75 μm, B <120 μm vs 154–160 μm, C <100 μm vs 131–144 μm, D <175 μm vs 212–220 μm, respectively), smaller medial hooks (A ’ <60 μm vs 62–73 μm, B ’ <119 μm vs 144–165 μm, C ’ <108 μm vs 121–144 μm, D ’ <175 μm vs 203–211 μm, respectively), a shorter terminal proglottid (<1320 μm vs 1663–2134 μm, respectively), a narrower terminal proglottid (<260 μm vs 284–356 μm, respectively), a shorter cirrus-sac (<152 μm vs 171–232 μm, respectively) and smaller testes (<50 μm vs 50–61 μm, respectively). Furthermore, A. bobconniorum and A. popi differ from A. ulondolozus n. sp. in the following features: total length (<7.1 mm vs 9.3–13.5 mm, respectively), cephalic peduncle length (<650 μm vs 1044–1430 μm, respectively), and testes length (<50 μm vs 50–61 μm, respectively). Both A. crassus and A. dolichocollum have a shorter scolex than A. ulondolozus n. sp. (<450 μm vs 486–599 μm, respectively). Additionally, the width of both the bothridium and cephalic peduncle can also be used to distinguish A. ulondolozus n. sp. form A. dolichocollum , as the latter species has a narrower bothridium (<134 μm vs.168–190 μm, respectively), and a narrower cephalic peduncle (<73 μm vs.76–98 μm, respectively).

Species of Acanthobothrium possessing testes posterior to the ovarian isthmus seem to be restricted to the families Dasyatidae (i.e. Himantura Müller et Henle ), Rhinidae (i.e. Rhynchobatus Müller et Henle ), Rhinobatidae (i.e. Rhinobatos Linck ) and Rajidae (i.e. Raja Linnaeus ), with the latter family including the host observed in the present study. The addition of yet another South African congener, A. ulondolozus n. sp., not only brings the total of species known to possess this remarkable feature to 17 species (across all categories), but also subsequently confirms Van Der Spuy et al.’s (2020) statement that this feature is not limited to the Indo-Pacific Ocean. Moreover, the plausibility regarding the relatedness of A. ulondolozus n. sp. with other congeners only invites further

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research engagement. The fact that A. ulondolozus n. sp. is synhospitalic with two other congeners and sharing a rare morphological feature with only 16 other species of Acanthobothrium worldwide (i.e. four from South Africa), further supports the need for future research into a more comprehensive phylogenetic analysis of these cestodes. Gathering information on the molecular phylogeny could prove if species presenting testes located in this region might in fact comprise their own monophyletic clade ( Fyler and Caira, 2010), along with possible effects caused by regional geographical influences (i.e. the Eastern South Atlantic Ocean vs. the Indo-Pacific Ocean), given that adult species of Acanthobothrium are restricted to the same geographical limits portrayed by their hosts ( Zaragoza-Tapia et al., 2020a).

Acanthobotrium ulondolozus n. sp. is the fifth cestode species known to parasitise the endangered white skate, R. alba , and the first cestode species infecting this host bearing testes posterior to the ovarian isthmus. This adds R. alba to the list of elasmobranch species known to host species of Acanthobothrium with this particularly rare morphological feature. Furthermore, A. ulondolozus n. sp. represents the seventh species known from the southeastern Atlantic Ocean off the coast of southern Africa, and the fifth species from this region with testes posterior to the ovarian isthmus, a feature previously thought to be restricted to the Indo-Pacific Ocean ( Fyler et al., 2009; Fyler and Caira, 2010; Maleki et al., 2015).