Acanthobothrium cairae, Vardo-Zalik, Anne M. & Campbell, Ronald A., 2011

Vardo-Zalik, Anne M. & Campbell, Ronald A., 2011, Five new species of Acanthobothrium van Beneden, 1849 (Cestoda: Tetraphyllidea) in elasmobranchs from the northwest Atlantic and Gulf of Mexico with first records from smooth-hound sharks and guitarfish, Zootaxa 2838, pp. 41-64 : 43-47

Acanthobothrium cairae sp. nov.

( Figs. 1–8 )

Specimens deposited: holotype (USNPC 103801); paratypes (USNPC 103802–103814).

Host: Dasyatis centroura (Mitchill) , Roughtail stingray; Rajiformes : Dasyatidae .

Type locality: Narragansett Bay off Sakonnet Point, Rhode Island, coll. R. A. Campbell.

Site of Infection: spiral intestine.

Prevalence: 3 of 10 individuals examined.

Etymology: The species is named after Dr. Janine Caira, University of Connecticut, for her contributions to the study of cestode systematics and taxonomy.

Description: Based upon measurements of 8 whole mounted specimens, SEM of 2 specimens and serial sections of 8 specimens. Large worms 45–154mm (104, n=8) long, maximum width at gravid segments, 960–1060, composed of 268–491 (401, n=8) segments. Strobila muscular; mature segments acraspedote, apolytic. Scolex proper 1100–1440 long by 1200–1460 wide. Scolex, composed of 4 triloculate bothridia, loculi separated by two thick muscular septa, bothridia free at posterior ends with velum between adjacent bothridia. Bothridia 975–1225 (1063, n=15) long by 550–725 (630, n=10) wide rounded posteriorly, covered with spinitriches over proximal surfaces; apical sucker and pad present, armed with one pair of bifid hooks. Anterior loculus 500–700 (558, n=12) long, middle loculus 175–275 (214, n=12) long, posterior loculus 100–150 (116, n=12) long; ratio of locular lengths (A: M: P) 1: 0.38: 0.21; mean (BL: BW) 1.7: 1. Apical pad rounded 225–400 (347, n=12) long by 450–650 (498, n=12) wide; accessory sucker 125–250 (180, n=10) wide. Hooks symmetrical, stout, prongs markedly unequal, handles about equal in length. Cephalic peduncle 2740–4600 (3179, n=7) long by 520–800 (618, n=7) wide, covered with spinitriches; internal muscle bundles clearly visible, junction of neck most discernible when contracted; (BL: CPL) 1: 1.16 when contracted; (BL: CPL) 1: 1.9 to 2.9 when relaxed. Neck 1600 to 3800 long, transcending into first narrow segments of strobila.

Hook dimensions: Lateral hook (n=5): A= 60 (n=4); B= 125–238 (195) with large pore; C= 113–163 (133) very curved; D= 275–350 (330); E= 250–313 (290); W= 100–125 (113). Medial hook (n=5): A’= 60 (n=4); B’= 188–225 (208) with large pore; C’= 125–138 (128) very curved; D’= 300–375 (338); E’= 250–300 (275); W’= 100–125 (108). (THL: BL) 1: 3.1 to 1: 3.2.

Strobila: Strobila robust with 4 pairs of large longitudinal muscle bundles extending throughout ( Figs. 6–8 ). Immature segments wider than long 259–476 (384, n=8) per worm, gradually elongating with appearance of genital anlagen. Mature segments, number 9–39 (17, n=8) per worm, 1.1 to 1.4 times longer than wide, 700–1725 (949, n=22) long by 550–1200 (756, n=22) wide. Gravid segments trapezoidal, 920–1260 long by 960–1060 wide; length to width ratio 1.11–1.32: 1 (1.21, n=10). Genital pores 36–66% (54%, n=20) of total length from posterior end of segment, irregularly alternating; genital atrium shallow. Cirrus sac near equatorial in immature segments; postequatorial in mature segments, 150–350 (210, n=21) long by 60–225 (105, n=21) wide; pyriform in gravid segments, slightly larger c. 375 by 250. Cirrus armed. Testes 82–166 (118, n=16) in number, slightly subspherical, 50– 100 (63, n=26) long by 60–100 (67, n=26) wide, arranged 2–3 deep in intervascular fields anterior to ovarian isthmus, rarely posterior to isthmus ( Figs. 3 , 7, 8 ); testes atrophied in oldest segments. Testis distribution: 26–65 (41, n=20) preporal, 42–85 (65, n=20) aporal, 12–23 (16, n=20) postporal. Vas deferens extensive forming 10 or more transverse loops filling most of preovarian intervascular region ( Fig. 5 ). Ovary U-shaped, bilobed in cross section, at posterior end of segment, 300–520 (445, n=16) wide in mature segments, poral lobe 200–540 (285, n=19) long, reaching level of cirrus sac and slightly beyond ( Figs. 3, 5 ); aporal lobe 250–620 (363, n=19) long reaching midlevel to near anterior border of cirrus sac; ovary up to 875 wide with lobes up to 450 long in gravid segments. Mehlis’ gland conspicuous, rosette-like mass surrounding ootype, diameter 40–50, at center of ovarian isthmus. Vagina thick-walled, extending in midline from ootype to level of cirrus sac, then continues laterally along anterior margin of cirrus sac as enlarged thick-walled duct to genital atrium; seminal receptacle present; vaginal sphincter absent. Vitellarium follicular in 2 lateral columns c. 200 wide, extending most of segment length; each column 5–6 follicles deep in cross section; follicles ellipsoidal, 32–64 long by 16–24 wide. Vitelline follicles not reaching limits of testicular field anteriorly or full extent of ovary posteriorly; interrupted by cirrus sac and vagina on poral side. Uterus median, broad, columnar, covered with dark staining glandular cells, extends anteriorly from shell gland, ends near anterior extremity, expanded in gravid segments. Uterine pore and eggs not observed. Dorsal and ventral osmoregulatory canals variable in diameter, dorsal canal 20–33 in diameter, ventral canals 20–64 in diameter.

Remarks: Acanthobothrium cairae is the third species of Acanthobothrium reported from the roughtail ray, Dasyatis centroura being preceded by A. paulum and A. woodsholei . Acanthobothrium cairae is very large and muscular with stout hooks and qualifies as a category 3 species (LMMA) according to the system of Ghoshroy& Caira (2001). Both A. paulum and A. woodsholei are smaller category 1 (SFFS) and 2(7) (S(L)FFA) respectively with delicate hooks and strobila unlike A. cairae .

Species of Acanthobothrium comparable to A. cairae in the western Atlantic Ocean and waters of the Gulf of Mexico and Carribean Sea are: A. americanum from Dasyatis americana Hildebrand & Schroeder from Chesapeake Bay, Virginia; A. coronatum from species of skates ( Rajidae ) by Linton (1901, 1924) at Woods Hole, Massachusetts and by Meyers (1959) in the Gulf of St. Lawrence, Canada; and A. tortum from Aetobatus narinari (Euphrasen) in the Gulf of Mexico. Acanthobothrium cairae differs from A. americanum , a category 6 species, in possessing more testes per segment (82–166 vs. 59–78), larger hooks (275–375 vs. max. 180), and asymmetrical hook prongs (188–225 vs. 125–138). Acanthobothrium cairae has longer bothridia (975–1225 vs. 500–660), larger anterior loculi (500–700 vs. 200–350), and fewer postporal testes (12–23 vs. 26–44) than A. tortum . Linton’s (1901, 1924) reports of A. coronatum , a species common to the eastern North Atlantic and Mediterranean Sea ( Williams1969), were considered in error and corrected by Baer (1948) and Baer & Euzet (1962) with the descriptions of A. woodsholei and Acanthobothrium septentrionale Baer & Euzet, 1962 . Acanthobothrium woodsholei is smaller than A. cairae (12 –15 mm vs. 45–154 mm) with fewer testes (50–55 vs. 82–166). Specimens of A. coronatum reported by Meyers (1959) from the skates Dipturus laevis (Mitchill) , Leucoraja ocellata (Mitchill) , and Amblyraja radiata (Donovan) were undescribed and unavailable for comparison; therefore the trans-Atlantic distribution of A. coronatum could not be confirmed.

Two species in the south Atlantic, Acanthobothrium ramiroi Ivanov, 2005 from Argentina and Acanthobothrium terezae Rego & Dias, 1976 from Brasil, in freshwater stingrays ( Rajiformes , Potamotrygonidae ) are similar in size to A. cairae . Both species parasitize Potamotrygon motoro (Müller & Henle) and are distinguished from A. cairae in having dissimilar hooks (hooks similar in A. cairae ), and symmetrical vs. asymmetrical ovarian lobes.

In the North Atlantic, Acanthobothrium icelandicum Manger, 1972 from Raja batis (Linnaeus) is a category 3 species having hooks with prongs of unequal length. Important characters differentiating A. cairae from A. icelandicum are greater size (to 154 mm vs. 67.4 mm), absence of a vaginal sphincter, U-shaped vs. H-shaped ovary, and internal musculature of 8 large muscle bundles (4 dorsal, 4 ventral) in cross-sections of A. cairae vs. 6–10 dorsal and 7–14 ventral in A. icelandicum .

In hosts from European waters and the Mediterranean, Acanthobothrium cairae is similar to A. crassicolle , A. intermedium , A. coronatum , Acanthobothrium rajaebatis ( Rudolphi, 1809) , A. septentrionale and Acanthobothrium zschokkei Baer, 1948 . Williams (1969) considered all of these species to be in need of further study but recognizable by their hosts (none from stingrays) and hook formula. Acanthobothrium septentrionale from Raja sp. in the North Atlantic is a category 3 species that differs from A. cairae in smaller total hook length (123–129 vs. 275– 375) and fewer testes (60–90 vs. 82–166). Goldstein (1967) and Manger (1972) both indicate that there are 3 accessory suckers per bothridium in A. septentrionale though neither Baer & Euzet (1962) nor Williams (1969) make mention of it.

Acanthobothrium cairae is similar to A. crassicolle in size and general morphology but the descriptions of A. crassicolle by both Dollfus (1926) and Baer (1948) conflict in the symmetry of the ovarian lobes, failure of the ovarian lobes to reach the cirrus sac and the more anterior position of the genital pore. Euzet (1959; p. 147–149) recognized two variants of A. crassicolle from stingrays in the Mediterranean Sea, one being a smaller variant from Dasyatis pastinaca (Linnaeus) and A. crassicolle var. magnum Euzet, 1959 from the pelagic stingray Dasyatis violacea (Bonaparte) . The smaller variant of A. crassicolle from D. pastinaca resembles A. cairae in the possession of large longitudinal muscle bundles visible in the cephalic peduncle, hook form and ovarian form, but differs in smaller hooks (200–230 vs. 275–375), larger anterior loculi (500–700 vs. 350–400), longer cephalic peduncle (2.7– 4.6 mm vs. 1–1.5 mm) and segment length to width ratio (1.1–1.4 vs. 2.5 times longer than wide). Goldstein (1967) gave specific status to A. crassicolle var. magnum from D. violacea and recognized A. intermedium as a distinct species. Acanthobothrium cairae differs from A. magnum in being smaller (45–154mm vs. 350–500 mm), and having fewer testes (82–166 vs. 220) and shorter hook handles (60 vs. 145–155).

Euzet (1959) considered A. intermedium to be a variant of A. crassicolle distinguished by its anapolysis and smaller hook measurements. Acanthobothrium cairae is apolytic and possesses larger hooks (250–375 vs. 175). Vouchers (2) and transverse sections catalogued as A. crassicolle and A. intermedium (MHNG 40016: 88/61 and 88/66) from Raja sp. from Banyuls differ from A. cairae in that the cephalic peduncle is smooth instead of covered with spinitriches, the strobila is slender and delicate instead of muscular and robust as in A. cairae , the gravid segments (MHNG 40016: 88/59) are larger (1780–2720 long by 1880–2100 wide vs. 920–1260 by 960–1060 in A. cairae ) and the uterus has numerous lateral branches (lacking in A. cairae ).

Comparison of A. cairae to A. coronatum from the eastern North Atlantic and Mediterranean Sea is based upon the descriptions of Williams (1969) and Euzet (1959; p. 143–145) and examination of museum specimens(MHNG 40003, 88/40; 40009, 88/61) from the type host, Scyliorhinus stellaris (Linnaeus) . Williams (1969) considered A. coronatum a species specific to S. stellaris despite the fact that it has been reported from various species of sharks, skates and rays of several families. Fyler & Caira (2006) correctly listed A. coronatum as a category 4 species whereas A. cairae belongs to category 3. In addition to its asymmetrical ovary, other contrasting differences between A. cairae and A. coronatum include: a robust, muscular strobila; medial and lateral hook prongs of distinctly unequal length (asymmetrical); greater total hook length (250–375 vs. 210–230); larger bothridia (975–1225 vs. 700–900); more preporal testes (26–65 vs. 14–30); absence of a vaginal sphincter (present in A. coronatum ), and extent of the poral ovarian lobes (to cirrus sac vs. posterior to cirrus sac).

Euzet (1959) and Williams (1969) both provided descriptions of A. rajaebatis from skates ( Rajidae ). Baer (1948) and Euzet (1959) described A. zschokkei from Torpedo torpedo Linnaeus in the Mediterranean Sea. Fyler and Caira (2006) consider both to be category 5 species. Acanthobothrium cairae , a category 3 species, differs from A. rajaebatis and from A. zschokkei by its larger hooks (275–375 vs. 180–190, 150–160 respectively), in having more testes (82–166 vs. 58–85, 33–46 respectively) and an asymmetrical vs. symmetrical ovary.

Acanthobothrium manteri Hassan, 1983 in Pastinachus (= Dasyatis ) sephen (Müller & Henle) from the Mediterranean Sea is a category 3 species with asymmetrical hook prongs but is distinguished from A. cairae by possession of shorter hooks (150–170 vs. 275–375), fewer testes per segment (55–74 vs. 82–166) and fewer postporal testes (5–7 vs. 12–23).

Four category 3 species have been described from waters of the eastern Pacific Ocean, i.e. Acanthobothrium chilensis Rego, Vicente & Herrera, 1968 from Sarda chiliensis (Cuvier) , Acanthobothrium cleofanum Monks, Brooks & Perez-Ponce de Leon, 1996 from Dasyatis longa ( Garman) , and Acanthobothrium holorhini Alexander, 1953 and Acanthobothrium maculatum Riser, 1955 from Myliobatis californica Gill. Acanthobothrium cairae is a larger worm than A. chilensis and A. holorhini (44–154 mm vs. 40mm, 24mm respectively); it has more segments (268–491 vs. 97–150) and larger anterior loculi (500–700 vs. 127–235) than A. cleofanum . Compared to A. maculatum from M. californica , A. cairae is larger (44–154 mm vs. 35 mm) and possesses more aporal testes (42–85 vs. 30–41).

Acanthobothrium cairae is easily differentiated from Acanthobothrium obuncus Marques, Brooks & Barriga, 1997 from Dasyatis longa in Pacific waters off Ecuador by hook symmetry, total hook length (275–375 vs. 115– 130), and number of testes (82–166 vs.70–77).

Of the eight category 3 species from waters outside the Atlantic and eastern Pacific Oceans, A. cairae most closely resembles five species from which it is differentiated as follows: from Acanthobothrium australe Robinson, 1965 in greater number of segments (268–491 vs. 230) and smaller scolex width (1200–1460 vs. 1800–2600); A. cairae differs from Acanthobothrium blairi Campbell & Beveridge, 2002 in lacking lateral hook spurs, absence of a bar sclerite joining the hook handles and segment shape (elongated vs. narrow); it differs from Acanthobothrium chengi Cornford,1974 by larger hooks (275–375 vs. 200–270), fewer testes (82–166 vs. 120–235) and ovarian shape (wider than long vs. longer than wide); fewer postporal testes (12–23 vs. 37–44), fewer aporal testes (42–85 vs. 88–113), and smaller hook handles (60 vs. 107–130) separates A. cairae from Acanthobothrium gasseri Campbell& Beveridge, 2002 ; it can be distinguished from Acanthobothrium gibsoni Campbell & Beveridge, 2002 in having a shorter posterior loculus (100–150 vs. 240–250), shorter hook handles (60 vs.>150), and greater apical pad diameter (450–650 vs. 410). Acanthobothrium cairae can be differentiated from Acanthobothrium gracile Yamaguti, 1952 by its larger bothridia (975–1225 vs. 350–450), shorter cephalic peduncle and neck (maximum 8.4 mm combined vs. 28–34 mm) and longer hook prongs (118–238 vs. 70–84); its shorter bothridia (975–1225 vs. 1840–2220) and shorter posterior loculus (175–275 vs. 740–800) separates it from Acanthobothrium robertsoni Campbell & Beveridge, 2002 ; and A. cairae differs from Acanthobothrium waltairense Maheswari, Sanaka, Lakshmi & Rao, 1987 in having shorter hook handles (60 vs. 128–144), presence of postporal testes and a wider strobila (0.55–1.2 mm vs. 0.4–0.5 mm).

Figures

FIGURES 1 – 5. Acanthobothrium cairae sp. nov. from Dasyatis centroura. 1. Scolex (holotype). 2. Hooks. 3. Mature segment. Muscle bundles omitted for clarity. 4. Detail of terminal genitalia. 5. Gravid segment. Scale bars: Figs. 1, 3, 5 = 250 µm. Figs. 2, 4 = 100 µm.

FIGURES 6 – 8. Transverse sections of Acanthobothrium cairae sp. nov. 6. Immature segment, anterior to cirrus sac. Note 8 large muscle bundles. 7. Mature segment, anterior to ovary. Note testes, vitellaria, uterus and 8 large muscle bundles. 8. Mature segment. Section at level of ovarian isthmus. Note bilobed ovary and 8 large muscle bundles. Abbreviations: dc, dorsal osmoregulatory canal; m, muscle bundle; o, ovary; t, testis; u, uterus; v, vagina; vc, ventral osmoregulatory canal; vt, vitelline follicles, Scale bars: Figs. 6 – 8 = 200 µm.