Acanthobothrium umbungus, 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 : 116-118

3.1. Acanthobothrium umbungus n. sp. ( Figs. 1 and 2)

Description (based on whole mounts of 12 mature and five immature worms; two mature worms examined with SEM): Worms 2.4–8.9 mm long, greatest width at level of scolex, 15–32 proglottids per worm, euapolytic. Scolex consisting of scolex proper and cephalic peduncle. Scolex proper with four bothridia, 415–524 long by 225–385 wide. Bothridia free posteriorly, 118–154 wide; each bothridium with three loculi and specialised anterior region in form of muscular pad. Muscular pad 70–96 long by 93–116 wide, falciform in shape, with pronounced posterior margin, bearing accessory sucker and one pair of hooks at posterior margin; accessory sucker 20–30 long by 31–45 wide. Anterior loculus (A) 125–172 long; middle loculus (M) 65–110 long; posterior loculus (P) 60–105 long; loculus length ratio (A: M: P) 1.00: 0.56: 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 49–69, B 127–158, C 102–125, D 183–208. Medial hook measurements: A ′ 48–71, B ′ 131–162, C ′ 101–121, D ’ 180–216. Bases of lateral and medial hooks approximately equal in length; base of lateral hook slightly overlapping base of medial hook along medial axis of bothridium ( Fig. 1D); lateral hook base slightly wider than medial hook base. Tissue covering almost entire length of each prong of hooks. Short cephalic peduncle 291–834 long by 62–97 wide.

Cephalic peduncle densely covered with gladiate spinitriches, filitriches not observed ( Fig. 2C). Apical pad and distal bothridial surface covered with acicular filitriches and sparsely interspersed gladiate spinitriches ( Fig. 2D). Proximal bothridial surface and bothridial rims covered with gladiate spinitriches, interspersed with acicular filitriches ( Fig. 2E). Entire strobila covered in acicular filitriches ( Fig. 2F and G).

Proglottids acraspedote. Immature proglottids 16–30 in number; 1–2 mature proglottids; gravid proglottids absent; terminal proglottid 426–1460 long by 165–345 wide; terminal proglottid length to width ratio 2.3–5.4: 1.0. Proglottids protandrous; genital pores marginal, irregularly alternating ( Fig. 1A), 49–65% of proglottid length from posterior margin.

Testes conspicuous in mature proglottids, oval in dorsoventral view, 28–59 long by 27–40 wide, arranged in two to three irregular columns anterior to ovarian isthmus ( Fig. 1C), one layer deep, 29–36 in total number, 5–6 in post-poral field. Cirrus-sac pyriform ( Fig. 1C), 107–164 long by 35–71 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 at anterior margin of cirrus-sac to common genital atrium. Vaginal sphincter prominent ( Fig. 1C). Ovary occupying half of proglottid, almost reaching posterior margin of proglottid, Hshaped in dorsoventral view, lobulated ( Fig. 1C), asymmetrical, 60–124 wide at level of ovarian isthmus; poral lobe 139–594 in length; aporal lobe 198–667 in length; ovarian lobes not reaching level of genital opening anteriorly; ovarian isthmus located posterior to mid-level of ovary. Mehlis’ gland posterior to ovarian isthmus.

Vitellarium follicular; follicles in two lateral bands, 6–16 long by 10–32 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. 1C). Uterus thin-walled, extending from ovarian isthmus to near anterior margin of proglottid ( Fig. 1C). 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 “ umbungus ” is derived from “umbungu” [Xhosa; an indigenous language to the Eastern and Western Cape of South Africa] meaning “worm”, referring to the species of tapeworm.

Remarks

Following the description of four new species of Acanthobothrium by Van Der Spuy et al. (2020), a total of 207 valid species of Acanthobothrium are currently recognised worldwide. Ghoshroy and Caira (2001) developed a category classification system that facilitates the differentiation between congeners. Acanthobothrium umbungus n. sp. is a

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category 2 species (sensu Ghoshroy and Caira, 2001), with a relatively small body (<15 mm), few segments (<50 in number), few testes (<80 in number) and asymmetrical ovarian lobes. It was therefore compared to 51 congeners with the same category assignation. The most distinguishable feature of A. umbungus n. sp. is its hooks, as the hooks of most congeners within this category are much smaller in size (lateral hooks: B <117 μm vs 127–158 μm, C <102 μm vs 102–125 μm, D <170 μm vs 183–208 μm; medial hooks: B ’ <125 μm vs 131–162 μm, C ’ <101 μm vs 101–121 μm, D ’ <159 μm vs 180–216 μm, respectively). Based on the hook measurements, A. umbungus n. sp. already differs from all but nine species, namely A. annapienkensis Carvajal et Goldstein (1971) , A. brayi Campbell et Beveridge (2002) , A. domingae Franzese et Ivanov, 2020 , A. gloveri Campbell et Beveridge (2002) , A. guanghaiense Yang, Sun, Zhi, Iwaki, Reyda et Yang (2016) , A. popi Fyler, Caira et Jensen (2009) , A. ppdeleoni Zaragoza-Tapia, Pulido-Flores et Monks, 2020 , A. tasajerasi Brooks (1977) , and A. thomasae Campbell et Beveridge, 2002 . The hooks of both A. annapienkensis and A. domingae exceed that of A. umbungus n. sp. (lateral hooks: B> 180 μm vs 127–158 μm, C> 125 μm vs 102–125 μm, D> 240 μm vs 183–208 μm, respectively). Besides the differences in hook measurements, A. brevissime Linton (1908) , A. campbelli Marques, Brooks et Monks, 1995 , A. edwardsi Williams (1969) , A. lasti Campbell et Beveridge, 2002 , A. minus Tazerouti et al., 2009 , A. mooreae Campbell et

Beveridge, 2002, A. quadripartitum Williams (1968) , A. sphaera Maleki, Malek et Palm, 2013 , A. stevensi Campbell et Beveridge, 2002 , A. thomasae , A. tripartitum Williams (1968) , and A. zapterycum Ostrowski de Nunez, 1971 , can also be differentiated from A. umbungus n. sp. in the following features: a shorter body (<2.4 mm vs 2.4–8.9 mm, respectively), fewer proglottids (<13 vs 15–32, respectively), and fewer testes (<25 vs 29–59, respectively). By comparing the scolex length, A. brevissime , A. campbelli , A. chisholmae Campbell et Beveridge, 2002 , A. dujardini van Beneden (1850) , A. edwardsi , A. hypanus Zaragoza-Tapia, Pulido-Flores et Monks, 2020 , A. lasti , A. lilium Baer et Euzet, 1962 , A. mashnihae Fyler et Caira, 2006 , A. microhabentes Van Der Spuy, Smit et Schaeffner (2020) , A. microtenuis Van Der Spuy, Smit et Schaeffner, 2020 , A. minus , A. mooreae , A. ppdeleoni , A. puntarenesense Marques, Brooks et Monks, 1995 , A. sinaloansis Zaragoza-Tapia, Pulido-Flores et Monks, 2020 , A. sphaera , A. tasajerasi , A. thomasae , A. urotrygoni Brooks et Mayes, 1980 , A. vargasi Marques, Brooks et Monks, 1995 , A. walkeri Campbell et Beveridge, 2002 , and A. zapterycum , all have a shorter scolex compared to A. umbungus n. sp. (<400 μm vs 415–542 μm, respectively). Furthermore, A. lasti , A. microhabentes , A. mooreae , A. puntarenasense , A. rajivi Ghoshroy et Caira, 2001 , A. sinaloansis , A. sphaera , and A. urotrygoni also differ from A. umbungus n. sp. in the following features: bothridium width (<112 μm

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vs 118–154 μm, respectively), middle loculus length (<62 μm vs 65–110 μm, respectively) and posterior loculus length (<56 μm vs 60–105 μm, respectively). Acanthobothrium umbungus n. sp. can further be distinguished from A. minus , A. mooreae , A. sphaera , A. tasajerasi , and A. thomasae as they all have a shorter cephalic peduncle (<274 μm vs 291–834 μm, respectively), whereas A. chisholmae , A. cimari Marques, Brooks et Monks, 1995 , A. crassus Van Der Spuy, Smit et Schaeffner, 2020 , A. dolichocollum Van Der Spuy, Smit et Schaeffner, 2020 , and A. dujardini all have a longer cephalic peduncle (> 1000 μm vs 291–834 μm, respectively). Furthermore, A. carolinae Franzese et Ivanov, 2020 , A. costarricense Marques, Brooks et Monks, 1995 , A. guanghaiense and A. puntarenesense all have a wider cephalic peduncle than that of A. umbungus n. sp. (> 103 μm vs 62–97 μm, respectively). Regarding the cirrus-sac and ovary, the length of the cirrus-sac of A. campbelli , A. chisholmae , A. mashnihae , A. microhabentes , A. minus , A. soniae Zaragoza-Tapia, Pulido-Flores, Violante-Gonzalez et Monks, 2019 , A. tetabuanense Reyda et Caira, 2006 , and A. tripartitum is <100 μm while that of A. umbungus n. sp. measures 107–164 μm; the width of the cirrus-sac of A. brachyacanthum Riser (1955) , A. costarricense and A. olseni Dailey et Mudry, 1968 is> 84 μm versus that of A. umbungus n. sp. with 35–71 μm; and the ovary width of A. campbelli , A. costaricense , A. gloveri , A. semnovesiculum Verma (1928) , and A. thomasae are all <53 μm while that of A. umbungus n. sp. ranges between 60 and 124 μm. Acanthobothrium umbungus n. sp. can also be distinguished from A. bobconniorum Fyler et Caira, 2010 , A. crassus , A. dolichocollum , A. microhabentes , A. microtenuis , and A. popi by its lack in testes posterior to the ovarian isthmus. Only A. urotrygoni and A. woodsholei Baer (1948) have a larger body size than A. umbungus n. sp. with> 12 mm versus 2.4–8.9 mm (respectively). Additionally, A. annapienkensis , A. brayi , A. bullardi Ghoshroy et Caira, 2001 , A. domingae and A. woodsholei differ from A. umbungus n. sp. in the following features: scolex length (> 560

μm vs 415–542 μm, respectively), bothridium width (> 176 μm vs 118–154 μm, respectively) and cirrus-sac width (> 85 μm vs 35–71 μm, respectively). More species containing a wider bothridium than A. umbungus n. sp. are A. carolinae , A. chisholmae , and A. costarricense (> 161 μm vs 118–154 μm, respectively). Acanthobothrium bobconniorum , A. cimari , A. costarricense , A. crassus , A. dujardini , A. hypanus , A. popi , A. puntarenesense and A. semnovesiculum all have more testes than

A. umbungus n. sp. (> 36 vs 29–36, respectively).

Acanthobothrium umbungus n. sp. represents the third species of Acanthobothrium and the seventh cestode record from this host. In southern Africa, only four species of Acanthobothrium are currently known ( Van Der Spuy et al., 2020). Including A. umbungus n. sp., it not only increases the number of species of this genus in the Eastern South Atlantic Ocean but also marks southern Africa as an understudied biogeographical region with the potential of an immense hidden parasite diversity.