Research Article |
Corresponding author: Scott Monks ( monks.scott@gmail.com ) Academic editor: Boyko Georgiev
© 2023 Erick Rodríguez-Ibarra, Juan Violante-González, Scott Monks.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Rodríguez-Ibarra E, Violante-González J, Monks S (2023) Two new species of Acanthobothrium Blanchard, 1848 (Cestoda, Onchoproteocephalidea) from Urobatis jamaicensis (Cuvier, 1816) (Elasmobranchii, Batoidea, Myliobatiformes) of the Mexican Caribbean. ZooKeys 1169: 175-201. https://doi.org/10.3897/zookeys.1169.101968
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Eight specimens of Urobatis jamaicensis were collected from four localities of the Yucatan Peninsula, Mexico, of which four specimens were infected with cestodes of two new species of Acanthobothrium. Acanthobothrium garciaprietoi sp. nov. differs from congeners by a combination of characters including the size of the scolex and bothridia, length of the cephalic peduncle, length of the axial and abaxial prongs and total length of the abaxial prongs of the hooks, size of the cirrus sac and testes in mature proglottids, and the total number of proglottids. The most prominent characteristic distinguishing A. pulidofloresae sp. nov. from other species of the Atlantic Ocean/Caribbean Sea/Gulf of Mexico is the form of the scolex, which has the “clover leaf” configuration. In addition, it can be distinguished by the total length of the worm, total number of proglottids, small accessory suckers, the form of the bothridia, length of the axial and abaxial prongs and total abaxial prong length of hooks, and the number of testes. According to the current category scheme, A. garciaprietoi sp. nov. and A. pulidofloresae sp. nov., belong to categories 1 and 5, respectively.
Elasmobranchs, marine fish parasites, Myliobatiformes, new species, tapeworms
The Family Urotrygonidae (round rays) is represented by approximately 20 species in two genera, Urobatis Garman, 1913 and Urotrygon Gill, 1863. Family members are confined to tropical warm water continental shelves of the Western Atlantic and the Eastern Pacific coasts of the Americas, mainly in demersal inshore habitats (
The genus Acanthobothrium Blanchard, 1848 currently is comprised of 211 species, and is the most diverse genus of Onchoproteocephalidea. Its members principally parasitize batoids and sharks (
As part of a continuing study of the helminths of marine fish, eight specimens of U. jamaicensis were collected in the Yucatan Peninsula, Mexico; four of these were found to be infected with two species of Acanthobothrium. These two and ten other recently described species of Acanthobothrium were added to the checklist by
Eight specimens of Urobatis jamaicensis were collected by local fishermen in the Yucatan Peninsula, Mexico, who donated the spiral intestines to the authors. The locations and number of rays from each location are as follows: two from Xcalak, Quintana Roo (18°15'58.37"N, 87°50'9.00"W) (collected in October 1998), one from Río Lagartos, Yucatán (21°35'58.05"N, 88°9'32.44"W) (February 1999), four from Isla Contoy, Quintana Roo (21°31'44.45"N, 86°48'11.53"W) (February 1999), and one from Isla Cozumel, El Paso de los Cedros, Quintana Roo (20°21'57.74"N, 87°1'32.48"W) (February 1999). Cestodes were removed from the spiral valve of the host, killed with hot water, transferred immediately to AFA (alcohol-formalin-acetic acid) for 24–48 hours, and then stored in 70% ethanol. Specimens were stained either with Mayer’s carmalum or Ehrlich’s hematoxylin following
Because the specimens had been mounted on slides in 1997–1998 (but not studied at that time), one specimen was dismounted from its single slide, placed in 100% Xylol for 24 hours, after which the excess Canada balsam was removed as much as possible with a fine brush in order to process it for scanning electron microscopy (SEM). This specimen was dehydrated through a graded series of ethanol, subjected to critical point drying with CO2 and then sputter coated with a gold‐palladium mixture, mounted on metal beads with silver paste; it was examined using a Hitachi Stereoscan Model S-2469 N at 15 kV (Laboratorio Nacional de Biodiversidad (LANABIO), Instituto de Biología, Universidad Nacional Autónoma de Mexico, Mexico City, Mexico. Illustrations were made with the aid of a drawing tube. Measurements are given in micrometers unless specified otherwise. The range is given, followed in parentheses by the mean, standard deviation, the number of measured worms, and the number of measurements taken. Hook measurements follow
In order to provide an update to the information in the table published by
Species of Acanthobothrium different categories that were compared with A. garciaprietoi sp. nov. and A. pulidofloresae sp. nov. Note: * = Species with characters used are mostly assigned to category 5; ** = species with characters used are mostly assigned to another category, but some of them allow them to be in category 5; † = species considerate as species inquirenda by
Species | Type host | Type locality | Source |
---|---|---|---|
Category 1 | |||
A. fogeli Goldstein, 1964 | Gymnura lessae (Yokota & Carvalho, 2017) (as Gymnura micrura (Bloch & Schneider, 1801)) | Northeastern Gulf of Mexico, Florida | Goldstein (1964) |
A. himanturi Brooks, 1977 | Styracura schmardae (Werner, 1904) (as Himantura schmardae) | Caribbean Sea, La Cienaga, Magdalena, Colombia | Brooks (1977) |
A. lentiginosum Vardo-Zalik & Campbell, 2011 | Pseudobatos lentiginosus (Garman, 1880) (as Rhinobatos lentiginosus) | Gulf of Mexico | Vardo-Zalik and Campbell (2011) |
A. lineatum Campbell, 1969 | Hypanus americanus (Hildebrand & Schroeder, 1928) (as Dasyatis americana) | Chesapeake Bay, Virginia, USA | Campbell (1969) |
A. marplatensis Ivanov & Campbell, 1998 | Atlantoraja castelnaui (Miranda Ribeiro, 1907) (as Rioraja castelnaui) | Mar del Plata, Buenos Aires, Argentina | Ivanov and Campbell (1998) |
A. schalli Vardo-Zalik & Campbell, 2011 | Mustelus canis (Mitchill, 1815) | Gulf of Mexico | Vardo-Zalik and Campbell (2011) |
A. stefaniae Franzese & Ivanov, 2018 | Discopyge tschudii Heckel, 1846 | Coastal waters off Mar Chiquita City, Buenos Aires Province |
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A. ulmeri Vardo-Zalik & Campbell, 2011 | Rostroraja texana Chandler, 1921 (as Raja texana) | Gulf of Mexico | Vardo-Zalik and Campbell (2011) |
A. westi Vardo-Zalik & Campbell, 2011 | R. texana | Gulf of Mexico | Vardo-Zalik and Campbell (2011) |
Category 2 | |||
A. tasajerasi Brooks, 1977 | S. schmardae | Caribbean Sea, La Cienaga, Magdalena, Colombia | Brooks (1977) |
A. cartagenensis Brooks & Mayes, 1980 | Urobatis jamaicensis (Cuvier, 1816) | Cartagena, Colombia | Brooks and Mayes (1980) |
A. urotrygoni Brooks & Mayes, 1980 | Urotrygon venezuelae (Schultz, 1949) | Cartagena, Colombia | Brooks and Mayes (1980) |
Category 1 and 2 | |||
A. carolinae Franzese & Ivanov, 2020 | Bathyraja magellanica (Philippi, 1902) | Coastal waters off Puerto San Julián, Santa Cruz Province |
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A. domingae Franzese & Ivanov, 2020 | Dipturus brevicaudatus (Marini, 1933) | Coastal waters off Santa Teresita, Buenos Aires Province |
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Category 3 | |||
A. majumdari Pramanik & Manna, 2010† | Carcharias walbeehmii (Bleeker, 1856) | Digha coast, India |
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A. robertsoni Campbell & Beveridge, 2002 | Trygonorrhina fasciata Müller & Henle, 1841 | Middleton, South Australia |
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A. zugeinensis Yang & Lin, 1994† | T. zugei (as Dasyatis zugei) | Xiamen, South Fujian, China |
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Category 4 | |||
A. adlardi Campbell & Beveridge, 2002 | Pristiophorus cirratus (Latham, 1794) | Port Stanvac, South Australia |
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A. dasybati Yamaguti, 1934 (Yamaguti, 1952) | Hemitrygon akajei (Müller & Henle, 1841) (as Dasyatis akajei) | Tarumi, Kobe, Japan | Yamaguti (1934) |
A. cestraciontis (Yamaguti, 1934) | Heterodontus japonicus (Miklouho-Maclay & Macleay, 1884) (as Cestracion japonicus) | Pacific Ocean, Japan | Yamaguti (1934) |
A. cribbi Campbell & Beveridge, 2002 | Gymnura australis (Ramsay & Ogilby, 1886) | Gulf of Carpentaria, Northern Territory, Australia |
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A. micracantha Yamaguti, 1952 | H. akajei | Nagasaki, East China Sea, Japan | Yamaguti (1952) |
A. grandiceps Yamaguti, 1952 | Telatrygon zugei (Müller & Henle, 1841) (as Trygon zugei) | East China Sea, Japan | Yamaguti (1952) |
A. ijimai Yoshida, 1917 | H. akajei | Tokyo, Japan |
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A. karachiense Bilqees, 1980 | Mustelus manazo Bleeker, 1855 (as Cynias manazo) | Karachi Coast, Pakistan | Bilqees (1980) |
A. macrocephalum Wang & Yang, 2001 | H. akajei | Xiamen, Fujiari, China | Wang and Yang (2001) |
A. pingtanensis Wang, 1984 | Neotrygon kuhlii (Müller & Henle, 1841) (as Dasyatis kuhlii) | Fujian Province, China | Wang (1984) |
Category 5 | |||
A. amazonensis Mayes, Brooks & Thorson, 1978 | Potamotrygon circularis (German, 1913) | Itacuari River, Brazil | Mayes et al. (1978) |
A. angelae Campbell & Beveridge, 2002 | Hypnos monopterygius (Shaw, 1795) | Yarraville Shoals, South Australia |
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A. confusum Baer & Euzet, 1962 | N. kuhlii | Indian Ocean, Sri Lanka | Baer and Euzet (1962) |
A. edmondsi Campbell & Beveridge, 2002 | Parascyllium ferrugineum (McCulloch, 1911) | Port Stanvac, South Australia |
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A. franus Marques, Centritto & Stewart, 1997* | Narcine entemedor (Jordan & Starks, 1895) | Cuajiniquil Beach, Gulf of Santa Helena, Guanacaste, Costa Rica | Marques et al. (1997b) |
A. giganticum Sanaka, Lakshmi & Hanumantharao, 1993 | G. micrura | Waltair coast, India | Sanaka et al. (1993) |
A. goldsteini Appy & Dailey, 1973* | Platyrhinoidis triseriata (Jordan & Gilbert, 1880) | Seal Beach, California, USA | Appy and Dailey (1973) |
A. hispidum Riser, 1955 | Tetronarce californica (Ayres, 1855) | Monterey Bay, California, USA | Riser (1955) |
A. inbiorium Marques, Centritto & Stewart, 1997 | N. entemedor | Cuajiniquil Beach, Gulf of Santa Helena, Guanacaste, Costa Rica | Marques et al. (1997b) |
A. indicum (Subhapradha, 1955) | Narcine brasiliensis (Olfers, 1831) (as Narcine braunii) | Madras Coast, India | Subhapradha (1955) |
A. katherineae Gallagher & Caira, 2020 | Squaliolus aliae (Teng, 1959) | Taiwan Strait, landed at Donggang, Pingtung Province, Taiwan |
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A. lintoni Goldstein, Henson & Schlicht, 1968** | N. brasiliensis | Gulf of Mexico, Texas, USA | Goldstein et al. (1969) |
A. manteri Hassan, 1983 | Pastinachus sephen (Forsskål, 1775) (as Dasyatis sephen) | Mediterranean Sea, Egypt | Hassan (1983) |
A. maryanskii Caira & Burge, 2001 | Diplobatis ommata (Jordan & Gilbert, 1890) | Loreto, Gulf of California, Mexico |
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A. paulum Linton, 1890** | Bathytoshia centroura (Mitchill, 1815) (as Trygon centrura [sic]) | Woods Hole, Massachusetts, USA | Linton (1890), Vardo- Zalik and Campbell (2011) |
A. psammobati Carvajal & Goldstein, 1969 | Psammobatis scobina (Philippi, 1857) | South Pacific Ocean, between Papudo and Talcahuano, Chile | Carvajal-G. and Goldstein (1969) |
A. quinonesi Mayes, Brooks & Thorson, 1978 | Potamotrygon magdalenae (Duméril, 1865) | Magdalena River, Cienaga Jobo, vicinity of San Cristobal, Bolivar, Colombia | Mayes et al. (1978) |
A. rajaebatis (Rudolphi, 1810) Euzet, 1959 | Dipturus oxyrinchus (Linnaeus, 1758) (as Raja bati) | Mediterranean Sea | Rudolphi (1810) |
A. regoi Brooks, Mayes & Thorson, 1981 | Potamotrygon hystrix (Müller & Henle, 1841) | Orinoco River Delta, Orinoco River near Los Castillos, Venezuela | Brooks et al. (1981) |
A. rhinobati Alexander, 1953** | Pseudobatos productus (Ayres, 1854) (as Rhinobatos productus) | Santa Monica Harbor, California, USA | Alexander (1953) |
Species of Acanthobothrium reported from the different species of elasmobranchs of the world (update of Zaragoza-Tapia, 2020a). Abbreviations: Gd = Geographical distribution; Ht = Holotype; Nt = Neotype; Pt = Paratype; Va = Voucher; Loc = Locality; Sou = Source; Cat = Category designation (modified from Zaragoza-Tapia 2020a).
Species | Ht | Nt, Pt or Va | Host | Gd | Loc | Sou | Cat |
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A. carolinae Franzese & Ivanov, 2020 | MACN-Pa 716 | MACN-Pa 717/1-4, 718/1-3, 719/1-2; IPCAS C-838; LRP 10179-10184 | Bathyraja magellanica (Philippi, 1902) | WSA, ESP | Coastal waters off Puerto San Julián, Santa Cruz Province, Argentina |
|
1 and 2 |
A. carolinae | NR | NR | Bathyraja magellanica | WSA, ESP | Coastal waters off Río Grande, Tierra del Fuego Province, off Banco Burdwood, Argentina |
|
– |
A. domingae Franzese & Ivanov, 2020 | MACN-Pa 720 | MACN-Pa 721/1-3, 722/1-9, 723; IPCAS C-839; LRP 10185-10195 | Dipturus brevicaudatus (Marini, 1933) | WSA | Coastal waters off Santa Teresita, Buenos Aires Province, Argentina |
|
1 and 2 |
A. domingae | NR | NR | Dipturus brevicaudatus | WSA | Coastal waters off Río Grande, Tierra del Fuego Province, off Banco Burdwood, Argentina |
|
– |
A. microhabentes Van Der Spuy, Smit & Schaeffner, 2020 | NMB P-604 | NMB P-605-P-606; IPCAS C-848; MHNG PLAT-137324, 137334 | Raja straeleni (Poll, 1951) | ESA, ECA | South-eastern Atlantic Ocean off De Kelders, South Africa |
|
2 |
A. microtenuis Van Der Spuy, Smit & Schaeffner, 2020 | NMB P-607 | NMB P-608-P-609; IPCAS C-849; MHNG PLAT-137335, 137340 | Raja straeleni | ESA, ECA | South-eastern Atlantic Ocean off De Kelders, South Africa |
|
2 |
A. crassus Van Der Spuy, Smit & Schaeffner, 2020 | NMB P-610 | NMB P-611; IPCAS C-850; MHNG PLAT-137341 | Raja straeleni | ESA, ECA | South-eastern Atlantic Ocean off De Kelders, South Africa |
|
2 |
A. dolichocollum Van Der Spuy, Smit & Schaeffner, 2020 | NMB P-612 | NMB P-613; IPCAS C-851; MHNG PLAT-137342, 137343 | Raja straeleni | ESA, ECA | South-eastern Atlantic Ocean off Hermanus, South Africa |
|
2 |
A. umbungus Van Der Spuy, Smit & Schaeffner, 2022 | NR | NR | Rostroraja alba (Lacépède, 1803) | ENA, MED, ECA, ESA, WIO | Danger Point, Gansbaai, South Africa |
|
2 |
A. usengozinius Van Der Spuy, Smit & Schaeffner, 2022 | NR | NR | Rostroraja alba | ENA, MED, ECA, ESA, WIO | Danger Point, Gansbaai, South Africa |
|
2 |
A. ulondolozus Van Der Spuy, Smit & Schaeffner, 2022 | NR | NR | Rostroraja alba | ENA, MED, ECA, ESA, WIO | Danger Point, Gansbaai, South Africa |
|
2 |
A. katherineae Gallagher & Caira, 2020 | NMNS 8249-001 | LRP 10260, 10015, 10016; USNM 1618754, 1618752, 1618753 | Squaliolus aliae (Teng, 1959) | EIO, NIO, WCP, WNP, WSP | Taiwan Strait, landed at Donggang, Pingtung Province, Taiwan |
|
5 |
A. garciaprietoi sp. nov. | CNHE 11881 | CNHE 11882, HWML-216977, CHE-P00146 | Urobatis jamaicensis (Cuvier, 1816) | WCA, WNA | Isla Contoy, Playa Ixmapoit, Quintana Roo, Mexico | This studio | 1 |
A. pulidofloresae sp. nov. | CNHE 11880 | CHE P00145 | Urobatis jamaicensis | WCA, WNA | Isla Cozumel, El Paso de los Cedros, Quintana Roo, Mexico | This studio | 5 |
A. barusi Pramanik & Manna, 2010 | Department of Zoology, University of Calcutta #004 | Department of Zoology, University of Calcutta #003 | Aetobatus narinari | NIO | Digha coast, West Bengal, India |
|
3 (4) |
A. majumdari Pramanik & Manna, 2010 | Department of Zoology, University of Calcutta #0013 | Department of Zoology, University of Calcutta #003 | Carcharias walbeehmi Bleeker, 1856 | NIO | Digha coast, India |
|
3(4) |
A. paramanandai Pramanik & Manna, 2010 | Department of zoology, University of Calcutta #002 | Department of zoology, University of Calcutta #003 | Carcharhinus hemiodon (Valenciennes, 1839) | NIO | Digha coast, West Bengal, India |
|
3(4) |
A. tsingtaoensis Tseng, 1933 | NR | NR | Hemitrygon akajei | WNP | China | Tseng (1933) | – |
A. zugeinensis Yang & Lin, 1994 | NR | NR | Telatrygon zugei | WNP | Xiamen, South Fujian, China |
|
3 |
CNHE Colección Nacional de Helmintos del Instituto de Biología, Universidad Nacional Autónoma de México, México;
CHE Colección de Helmintos, Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, Pachuca, México.
Type material was deposited in CNHE (holotype and paratypes),
Family Onchobothriidae Braun, 1900
Acanthobothrium coronatum (Rudolphi, 1819) Blanchard, 1848
Holotype (CNHE–11880), 1 paratype (CHE-P00145).
Urobatis jamaicensis (Cuvier, 1816) (Elasmobranchii: Myliobatiformes: Urotrygonidae).
Isla Cozumel, El Paso de los Cedros, (20°21'57.74"N, 87°1'32.48"W), Quintana Roo, Mexico.
Spiral valve.
14.28%
The species is named in honor of Dra. Griselda Pulido-Flores (Universidad Autónoma del Estado de Hidalgo, Centro de Investigaciones Biológicas, Hidalgo, Mexico) for her contributions to the academic training of the first author, and to knowledge of helminths, as well as for her friendship.
Acanthobothrium pulidofloresae sp. nov. is a Category 5 species. Body relatively long (41 mm long); scolex in a “clover leaf” configuration; apical suckers small, 12–13 (12.6 ± 2; 1; 3) long by 30–32 (31.33 ± 3; 1; 3) wide; strobila of 152–164 proglottids; short hooks, in claw configuration, 47–60 testes per proglottid; ovary symmetrical.
(Based upon measurements of one complete worm and one partial worm mounted on slides). Entire worm 41 mm long, greatest width at scolex (Figs
Acanthobothrium pulidofloresae sp. nov. A–D, G holotype (CNHE–11880) E, F paratype (CHE-P00145) A scolex B pair of hooks C apical suckers with pads muscular D apical sucker E mature proglottid F terminal mature proglottid G complete tapeworm. Scale bars: 50 μm (B, D); 100 μm (C); 200 μm (A, E, F); 3 mm (G).
Hooks with axial and abaxial prongs, hollow, with tubercle on proximal surface of axial prong; internal channels of axial and abaxial prongs continuous, smooth; base and anterior part of each hook embedded in muscular pad; handle short and thin, prongs short with tips turned inwards; abaxial prongs longer than axial prongs. Bases (handles) of medial and lateral hooks articulated to each other; lateral hooks relatively longer than internal hooks. Lateral hook measurements: A 36–42 (39 ± 3; 1; 4), B 48–60 (51 ± 7; 1; 4), C 57–68 (62.4 ± 8; 1; 4), D 76–87 (81 ± 7; 1; 4). Medial hook measurements: A’ 38–42 (40.8 ± 3; 1; 4), B’ 39–57 (36 ± 6; 1; 3), C’ 48–59 (52 ± 6; 1; 4), D’ 73–80 (76 ± 4; 1; 3) (Figs
Cephalic peduncle 14.6 mm long, 220–317 (268 ± 69, n = 2) wide at mid-level; presence and type of microtriches not confirmed. Proglottids craspedote. Immature proglottids 230–500 (369 ± 81; 2; 8) long by 537–866 (708 ± 157; 2; 8) wide; mature proglottids, 537–1000 (753 ± 181; 2; 7) long by 476–769 (627 ± 137; 2; 7) wide; terminal mature proglottids 915–1793 (1196 ± 344; 2; 5) long by 415–633 (525 ± 105; 2; 5) wide. Gravid proglottids not observed. Genital pores lateral, irregularly alternating, 23–37% (29 ± 5; 2; 6) of total length of proglottid from anterior end in mature proglottids; in terminal mature proglottids, 22–43% (29 ± 9; 2; 5); genital atrium shallow. Testes oval in dorsoventral view, arranged irregularly anterior to ovarian lobes, two layers deep, 48–78 (64 ± 8; 2; 24) long by 24–59 (44 ± 8; 1; 24) wide (Figs
For U. jamaicensis, this is the second species of Acanthobothrium that has been described. Acanthobothrium cartagenensis was designated to Category 1, recently reassigned by
Acanthobothrium pulidofloresae sp. nov. is easily distinguished from the other species of Category 5 because none of them has a scolex configuration called “clover leaf” (
Acanthobothrium pulidofloresae sp. nov. differs from A. amazonensis and A. quinonesi because it is relatively longer; however, A. regoi is approximately the same size (41 mm vs. A. amazonensis = 35, A. quinonesi = 25, and A. regoi = 45). These species also differ in the number of proglottids (152–164 vs. 75–100, 55–75, 87–120, respectively). The new species has a smaller accessory sucker (12–13 long by 30–32 wide vs. 85–107, 53–66, 61–102 in diameter, respectively). The hooks are shorter (total abaxial length 78–94 vs. 145–184, 100–142, 122–163, respectively) and the number of testes is less (47–60 vs. 50–72 in A. amazonensis, 43–62 in A. quinonesi, 47–70). The new species differs also from A. manteri because that species is slightly longer (the new species is 41 mm long vs. A. manteri 36–65 mm long. However, it is smaller than A. rajaebatis (41 mm long vs. 50–60 mm); has a smaller accessory sucker (12–13 long by 30–32 wide vs. 198 and 312 in diameter), shorter hooks (total abaxial length 78–94 vs. 175 and 305 and fewer testes per proglottids (47–60 vs. 55–74 and 58–85). Finally, it differs in the number of proglottids but there is some overlap in range (152–164 for A. pulidofloresae sp. nov. vs. 120–170 for A. manteri, and 80–120 for A. rajaebatis).
The new species is different from A. franus (16–40 long, 68–141 proglottids) and A. psammobati (34 long, 90 proglottids) by being longer and having a greater number of proglottids. Acanthobothrium inbiorium (28–82 long, 156–223 number of proglottids) is longer and has a greater number of proglottids than A. pulidofloresae sp. nov. In addition, A. franus, A. psammobati and A. inbiorium differ by presenting accessory sucker larger in diameter (A. pulidofloresae sp. nov. 12–13 vs. 60–159, 50, 20–75, respectively), bothridium longer (A. pulidofloresae sp. nov. 425–470 vs. 627–1408, 605, 480–680, respectively). Acanthobothrium pulidofloresae sp. nov. and A. psammobati have hooks that are relatively equal in length (A. pulidofloresae sp. nov., total abaxial length = 78–94 vs. A. psammobati = 91) and the hooks of the new species are shorter in length than those of A. franus (354–465) and A. inbiorium (95–120). Acanthobothrium pulidofloresae sp. nov. differs in the total number of testes (47–60) from A. franus (24–59), and A. psammobati (77), although there is some overlap with A. ibiorium (44–73).
Finally, A. angelae, A. confusum, A. edmondsi, A. giganticum, A. hispidium, and A. xiamenensis are worms with range in lengths of 50–240 mm vs. the 41 mm length of A. pulidofloresae sp. nov. Acanthobothrium angelae, A. confusum, A. giganticum, A. hispidium, A. maryanskii, A. xiamenensis have 250–500 proglottids, all more than A. pulidofloresae sp. nov. (152–164 proglottids), and A. edmondsi (47–86), A. goldsteini (60), and A. rhinobati (50) have a lesser number of proglottids than the new species. Acanthobothrium indicum has approximately the same number of proglottids as A. pulidofloresae sp. nov. (152–164 proglottids) but it is smaller in overall length (41 mm vs. 25 mm of A. indicum), and the new species has less testes per proglottid than A. indicum (47–60 vs. 70 of A. indicum). Acanthobothrium katherineae is shorter than the new species (21 vs. 41 mm of A. pulidofloresae sp. nov.), the anterior loculus is longer that of A. pulidofloresae (336–417 vs. 160–175, respectively), and it has a greater number of testes (A. katherineae = 55–69 vs. A. pulidofloresae sp. nov. = 47–60). Acanthobothrium angelae, A. confusum, A. edmondsi, A. giganticum, A. goldsteini, A. maryanskii, and A. xiamenensis have an accessory sucker greater in diameter than that of A. pulidofloresae.
The following species of Acanthobothrium are described as having a clover-leaf scolex configuration: Category 3, A. robertsoni; Category 4, A. adlardi, A. cestraciontis, A. dasybati, A. grandiceps, A. karachiense, A. ijimai, A. macrocephalum and A. pingtanensis; A. mujibi has not been assigned to a category because of the lack of data in the description. Acanthobothrium cribbi is illustrated as having a scolex with bothridia that extend almost to have a petaloid scolex; however, the species is not described as having a clover-leaf scolex configuration (
Acanthobothrium pulidofloresae sp. nov. differs from the ten species with a petaloid scolex in the following characteristics: A. robertsoni is longer than the new species (83 mm vs. 41 mm of A. pulidofloresae sp. nov.), has a greater number of proglottids (395 vs. 152–164), the scolex is larger (3000–3250 vs. 288), the accessory suckers are larger (104–152 vs. 12–13 long by 30–32 wide), the bothridia and loculi are longer (1840–2220 vs. 425–470), the hooks are longer in total abaxial length (133–208 vs. 84–90), and the number of testes is greater (116–163 vs. 47–60). Acanthobothrium adlardi has a greater number of proglottids (235 vs. 152–164), the scolex is larger (800–1500 vs. 288), the accessory suckers are reported as being absent, the bothridia (and loculi) are longer (1100–1500 vs. 425–470), the hooks are longer in total abaxial length (148–176 vs. 84–90), and the number of testes is greater (83–103 vs. 47–60). Acanthobothrium cestraciontis differs from the new species by being longer (282 mm vs. 41), the accessory suckers are reported as being absent, the hooks are longer in total abaxial length (270–290 vs. 84–90), and the number of testes is greater (120 vs. 47–60). Acanthobothrium dasybati differs by being longer (52 mm), less proglottids (100), the accessory suckers are reported as being absent, the hooks are longer in total abaxial length (130 vs. 84–90), and the number of testes is greater (90–100 vs. 47–60). Acanthobothrium grandiceps differs from the new species by being shorter (14–20 mm vs. 41 mm), having a greater number of proglottids (950 vs. 152–164), the accessory suckers are larger (200–210 vs. 12–13 long by 30–32 wide), the bothridia (and loculi) are longer (2200–2300 vs. 427–460), the hooks are longer in total abaxial length (165–180 vs. 84–90), and the number of testes is greater (110–130 vs. 47–60). Acanthobothrium karachiense is different from the new species by having a greater number of proglottids (278–293 vs. 152–164, the scolex is larger (1750–1790 vs. 288), the bothridia (and loculi) are longer (1290–1450 vs. 427–460), it has smaller hooks in total abaxial length (62–68 vs. 84–90), and the number of testes is greater (74–98 vs. 47–60). Acanthobothrium ijimai differs from the new species by having larger accessory suckers (100 vs. 12–13 long by 30–32 wide), the bothridia are longer (1600–1700 vs. 425–470), the hooks are longer in total abaxial length (90–110 vs. 84–90), and the number of testes is greater (100–130 vs. 47–60). Acanthobothrium macrocephalum differs from the new species by being longer (82–287 mm vs. 41), having a greater number of proglottids (209–1000 vs. 152–164), the scolex is larger (3000–3250 vs. 288), the accessory suckers are larger (146–308 vs. 12–13 long by 30–32 wide), the bothridia (and loculi) are longer (1230–2471 vs. 425–470), the hooks are longer in the total abaxial length (96–142 vs. 84–90), and the number of testes is greater (92–145 vs. 47–60). Acanthobothrium pingtanensis differs from the new species by being longer (150–160 mm vs. 41 mm), the scolex is larger (3200–3680 vs. 288), the accessory sucker is larger (320–340 in diameter vs. 12–13 long by 30–32 wide), and the total number of testes is greater (92–106 vs. 47–60). Acanthobothrium mujibi differs from the new species by having a larger scolex (750–800 vs. 288 of A. pulidofloresae sp. nov.), bothridia that are longer (930 vs. 427–460), smaller hooks in total abaxial length (58–76 vs. 84–90), and the number of testes is less (36–41 vs. 47–60). Finally, A. cribbi is different from A. pulidofloresae sp. nov. by being somewhat larger (50 mm vs. 41 mm), having a greater number of proglottids (200–300 vs. 152–164), larger accessory suckers (80–152 in diameter vs. 12–13 long by 30–32 wide), and a greater total number of testes (72–96 vs. 47–60).
Three other species cataloged as species inquirendae by
Acanthobothrium pulidofloresae sp. nov. differs from A. zugeinensis by being shorter (41 mm vs. 140–160 mm), having a shorter scolex (288 long by 413 µm wide vs. 2601 by 2506 µm, see
Holotype
(CNHE–11881), 1 paratype (CNHE–11882), 4 paratypes (CHE–P00146), 1 paratype (
Urobatis jamaicensis (Cuvier, 1816) (Elasmobranchii: Myliobatiformes: Urotrygonidae).
Isla Contoy, Playa Ixmapoit (21°31'44.45"N, 86°48'11.53"W) Quintana Roo, Mexico.
Spiral valve.
14.28%
The species is named in honor of M. C. Luis García-Prieto (Universidad Nacional Autónoma de México, Instituto de Biología, México) for his friendship and for his contributions to the knowledge of helminths.
Acanthobothrium garciaprietoi sp. nov. is a Category 1 species. Body small; relatively robust bothridia; large apical suckers; 7–9 proglottids; long hooks; 18–26 testes per proglottid; cirrus sac and the vagina share a common opening within the genital atrium; arms of ovary symmetrical.
(Based on 4 complete worms and 9 partial worms mounted on slides.) Entire worms 1.3 mm–2.1 mm (1.8 mm ± 0.4 mm, 4, 4) long; greatest width at scolex, euapolytic; 7–9 (8 ± 1, 4, 4) proglottids per worm (Figs
Acanthobothrium garciaprietoi sp. nov. SEM images. Paratype (not deposited) A scolex B bothridial muscular pad with pair of hooks C central area of scolex proper between the bothridia D gladiate spinitriches located on the proximal bothridial surface, see image C E papilliform filitriches located on the scolex proper, behind the bothridia, see image C F coniforme spinitriches located on the cephalic peduncle. Scale bars: 5 μm (D–F); 30 μm (C); 100 μm (A, B).
Hooks bipronged, hollow, with tubercle on the proximal surface of the axial prong; internal channels of axial and abaxial prongs continuous, smooth, the base and anterior part of each hook embedded in muscular pad; axial prongs much longer than abaxial prongs (Figs
Cephalic peduncle 175–288 (232 ± 35, 13, 7) long by 58–90 (74 ± 11, 13, 7) wide, covered with coniform spinitriches (see
Cirrus sac pyriform, 98–143 (125 ± 12, 9, 13) long, 30–88 (50 ± 15, 9, 13) wide in mature proglottids. Cirrus expanded at base, armed with spinitriches. Vagina thick walled, walls covered with gland cells, extending along medial line of proglottid from oötype, reaching to anterior margin of cirrus sac to common genital atrium; vaginal sphincter absent; seminal receptacle not seen. Vagina canal descends on the aporal side of proglottid relatively to the midline of proglottid, often with loops. Ovary with symmetrical lobes; poral lobe 133–375 (241 ± 79, 8, 3) long in mature proglottids, reaching to cirrus sac; aporal lobe 130–375 (240 ± 78, 8, 3) long, extending to the anterior margin of the cirrus sac. Ovary inverted A-shaped in dorsoventral view, lobulated, ovarian isthmus posterior to mid-point of ovary. Mehlis’ gland posterior to ovarian isthmus (Figs
Vitellarium follicular, consisting of two lateral bands; each band consists of two columns of relatively large, elongate to oval follicles, extending from near anterior margin of proglottid to near posterior margin of proglottid, interrupted by vagina and cirrus sac; follicles 345–425 (391± 23, 3, 9) long, 14–22 (17 ± 3, 3, 9) wide. Uterus thin-walled, sacciform, extends from near anterior part of proglottid to near oӧtype. Excretory ducts lateral. Eggs not seen.
This is the third species of Acanthobothrium described from U. jamaicensis. Acanthobothrium garciaprietoi sp. nov. is a category 1 species (sensu
Currently, in Category 1, there are 57 species (
However, A. garciaprietoi sp. nov. should be compared with the species assigned to Category 2 that inhabit the same geographical region because the species in Categories 1 and 2 are similar; the two categories differ only in relation to the symmetry of the ovarian arms. Of the 55 species that are included in Category 2, only two have been reported from the same host and/or to inhabit the same general region: A. tasajerasi and A. urotrygoni, both from the Caribbean Sea (Table
Of the species of Acanthobothrium in category 1, all except A. stefaniae, have acraspedote strobili; some are euapolytic or apolytic, and some are hyperapolytic. Members of Acanthobothrium known from the Gulf of Mexico are A. fogeli, A. lentiginosum, A. lineatum, A. schalli, A. ulmeri, and A. westi. Acanthobothrium garciaprietoi sp. nov. differ from A. fogeli, A. lineatum, and A. schalli by being shorter, with fewer proglottids, and less testes, except A. lentiginosum, A. ulmeri and A. westi, which overlap in total length, number of proglottids, number of testes and in the diameter of the accessory sucker. Acanthobothrium lentiginosum is similar to the new species. However, it has a scolex that, on the average, is longer (288–474 vs. 225–320), and somewhat longer bothridia (272–474 vs. 245–313) with longer loculi; the hooks have a longer abaxial prong (80–110 vs. 78–83), the cephalic peduncle is longer (288–456 vs. 175–288) and the genital pore is differently positioned (59–69 vs. 26–46, respectively). Acanthobothrium ulmeri differs from the new species by having a larger scolex (357–464 vs. 225–320), longer bothridia (281–432 vs. 245–313) and larger loculi; the hooks are shorter, with the axial prong (61–78 vs. 90–105) long and the abaxial prong (59–72 vs. 78–83) long; prongs that are both shorter in total length (77–103 vs. 115–135), and the cephalic peduncle is shorter (48–176 vs. 175–288). Acanthobothrium westi differs from the new species in having the scolex and smaller loculi (215–277 vs. 225–320, respectively), hooks with shored handles (25–28 vs. 28–38), axial prongs (42–53 vs. 90–105), and the abaxial prongs (38–48 vs. 78–83); the cephalic peduncle is longer (216–480 vs. 175–288), the cirrus sac is shorter (72–84 vs. 98–143), and range in the number of testes is less (20–24 vs. 18–26).
Of the species of Acanthobothrium reported from the South Atlantic, A. marplatensis, is much larger (4.79 mm–8.44 mm vs. 1.3 mm–2.1 mm for the new species), it has a greater number of proglottids (18–30 vs. 7–9, respectively), more testes per proglottid (24–39 vs. 18–26). The hooks of A. marplatensis are shorter, the cirrus sac rises towards the anterior end of the proglottid and the cirrus sac of the new species extends horizontally in mature proglottids (Fig.
Acanthobothrium cartagenensis and A. himanturi have been reported from the Caribbean Sea. Acanthobothrium cartagenensis differs from and A. garciaprietoi sp. nov. by having a greater number of proglottids (13 vs. 7–9, respectively); its scolex is square (300–300), while that of A. garciaprietoi sp. nov. is wider than long (225–320 long 275–323 wide); the loculi of A. cartagenensis are shorter (1:0.3:0.3 vs. 1:0.4:0.4). The apical pads of A. cartagenensis are 67 in diameter, and they are relatively elliptical with no invaginations in the hook region; in contrast, those of A. garciaprietoi sp. nov. are larger (76–83 long by 95–110 wide), with an invagination in the region between the hooks. The cephalic peduncle of A. caragenensis is shorter than that of A. garciaprietoi sp. nov. (180 long by 120 wide vs. 175–288 long by 58–90 wide). The testes of A. cartagenensis are smaller in diameter (30–45 vs. 50–75 long by 30–55 wide of A. garciaprietoi sp. nov.), but the cirrus sac of A. garciaprietoi sp. nov. is larger. The lobes of the ovary of A. cartagenensis are longer than those of A. garciaprietoi sp. nov. (210–390 long by 60–112 wide vs. 133–375 long).
Acanthobothrium himanturi differs from the new species by being longer (3.84–9.3 mm vs. 1.3–2.1 mm, respectively), slightly large scolex (240–350 vs. 225–320), longer bothridia (297–432 vs. 245–313) and longer cephalic peduncle (300–1,000 vs. 175–288). The handles of the hooks of A. himanturi are 43–61 long, the abaxial prong is 73–99 long, and the axial prong is 86–116 long, all being longer (28–38, 78–83, 90–105, respectively) than those of A. garciaprietoi sp. nov. It has a greater number of testes (38–57 vs. 18–26) and the ovarian lobes are longer and narrower (480–600 vs. 133–375) than those of A. garciaprietoi sp. nov.
Compared to the other two species in Categories 1 and 2, A. garciaprietoi sp. nov. differ from A. carolinae by the shorter body (1.3 mm–2.1 mm vs. 1.81mm–3.93, respectively), smaller number of proglottids (7–9 vs. 8–17), and the larger hooks. The new species A. garciaprietoi sp. nov., differs from A. domingae by the body size (1.3 mm –2.1 mm vs. 3.5 mm –5.4 mm, respectively), the number of proglottids (7–9 vs. 14–18, respectively), and the smaller hooks (115–135 vs. 168–238, respectively).
It is good practice to describe a species based on as large number of specimens as possible and, if the material permits, include molecular information on the species. However, sometimes the material is limited and, in name of “the progress of knowledge and science” (
The study of parasites of elasmobranchs in Mexico was initiated by
As can be seen from the cited works, the majority of the species from elasmobranchs that have been described to date from Mexican waters are cestodes. Many of them have been assigned to the genus Acanthobothrium, which currently is represented world-wide by 213 nominal species. Of these, 25 have been recently described: 13 from the Atlantic (
The majority of species of Acanthobothrium have scolex moderately to completely attached to the scolex proper by membranous tissue (velum) that holds the bothridia close to the scolex. In contrast, the species with a “clover-leaf” scolex (
Within Acanthobothrium, 13 species from Australian, the Western Pacific region, and Indian Ocean were described as having a “clover-leaf” scolex: A. adlardi, A. cestraciontis, A. dasybati, A. grandiceps, A. karachiense, A. ijimai, A. macrocephalum, A. mujibi, A. pingtanensis, and A. robertsoni. Three other species (A. majumdari, A. tsingtaoensis, and A. zugeinensis) are not included in the list above because they are not considered valid taxa by
The material for this study was collected during the fieldwork of the Dra. Grisel-da Pulido-Flores as part of her Doctorate in Science studies in Ecology and Sustainable Development at El Colegio de la Frontera Sur during 1999–2001 (CONACyT Scholarship No. 137558). The authors would like to thank the curatorial staff (Scott L. Gardner and Gabor R. Racz,
The authors have declared that no competing interests exist.
No ethical statement was reported.
This work was supported by Consejo Nacional de Ciencia y Tecnología, México. ER-I received a doctoral scholarship (No. 473690) from CONACyT; this study was part of his Doctoral studies in Biodiversity and Conservation, Univer-sidad Autónoma del Estado de Hidalgo and the Postdoctoral Scholarship (2022–2023), Modality 1, by CONACyT (No. CVU 763872).
ER-I, gathered data and wrote first draft of ms.; JV-G, revised ms.; SM, PI and revised final draft of ms.
Erick Rodríguez-Ibarra https://orcid.org/0000-0002-2930-8709
Juan Violante-González https://orcid.org/0000-0001-6291-8763
Scott Monks https://orcid.org/0000-0002-5041-8582
All of the data that support the findings of this study are available in the main text or Supplementary Information.
Update to Zaragoza-Tapia et al. 2020- Host relationships and geographic distribution of species of Acanthobothrium Blanchard, 1848 (Onchoproteocephalidea, Onchobothriidae) in elasmobranchs: a metadata analysis (up to 2020 to 2022)
Data type: Occurrences and distribution
Explanation note: This document is an update of the original data set of the host relationships and biographic distribution of parasites of the genus Acanthobothrium of the elasmobranch definitive host, to include species described from 2020 to 2022.