Zootaxa 4766 (1): 139–172
https://www.mapress.com/j/zt/
Copyright © 2020 Magnolia Press
ISSN 1175-5326 (print edition)
Article
ZOOTAXA
ISSN 1175-5334 (online edition)
https://doi.org/10.11646/zootaxa.4766.1.8
http://zoobank.org/urn:lsid:zoobank.org:pub:776D2EC2-583E-4D6E-85D9-2C4E7801A64F
Three new species of Acanthobothrium Blanchard, 1848 (Cestoda:
Onchoproteocephalidea) in Stingrays (Dasyatidae) from the Pacific coast in Mexico
FRANCISCO ZARAGOZA-TAPIA1, GRISELDA PULIDO-FLORES1,2 & SCOTT MONKS1,2
1
Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, Pachuca, Hidalgo, México.
� zaragoza_tf@live.com.mx https://orcid.org/0000-0003-0811-8460
2
Harold W. Manter Laboratory of Parasitology, University of Nebraska-Lincoln, Lincoln, NE 68588-0514.
� gpflores6@hotmail.com https://orcid.org/0000-0002-0454-8466;
� monks.scott@gmail.com https://orcid.org/0000-0002-5041-8582
Abstract
Three new species of Acanthobothrium Blanchard, 1848 (Onchoproteocephalidea: Onchobothriidae) are described from
Pacific coastal waters of Mexico. Based on four criteria for categorization of species of Acanthobothrium, the three new
species belong to Category 2 species, characterized by their total length (< 15 mm), number of proglottids (< 50) and
testes (<80), and with asymmetrical ovary. Acanthobothrium ppdeleoni n. sp. from diamond stingray Hypanus dipterurus
(Jordan & Gilbert) is differentiated from congeners by a combination of characters including total length of the whole
worms, size of the scolex and bothridia, length of the bases of the hooks and abaxial prongs, and the size of the cirrus sacs
in mature proglottids. Acanthobothrium hypanus n. sp. and A. sinaloaensis n. sp. are described from longtail stingray
Hypanus longus (Garman). Acanthobothrium hypanus n. sp. is differentiated by a combination of characters including
size of the scolex and bothridia, diameter of the accessory sucker, length of the abaxial prongs, size of the cirrus sacs
and testes in mature proglottids. Acanthobothrium sinaloaensis n. sp. is differentiated by a combination of characters
including size of the scolex and bothridia, diameter of the accessory sucker, size of the cirrus sacs in mature proglottids,
number of immature proglottids, number of testes, the length of the lobes of the ovary and the absence of velum between
medial margin of bothridia. Thirteen species of Acanthobothrium have been reported previously from elasmobranchs
from the Pacific coast of Mexico. In the present study, the number of species is elevated to 16.
Key words: Elasmobranchii, Helminth parasites, Hypanus, Myliobatiformes, Onchobothriidae, new species
Introduction
The order Onchoproteocephalidea Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014, contains 11 genera,
with Acanthobothrium Blanchard, 1848 being the most species-rich genus within Onchobothriidae Braun, with 198
species distributed worldwide (Caira & Jensen 2017; Franzese & Ivanov 2018; Rodríguez-Ibarra et al. 2018; Maleki
et al. 2018, 2019; Zaragoza-Tapia et al. 2019). Nevertheless, relatively few occurrences of species of Acanthobothrium have been documented in Mexico. To date, the best-studied locality is the Gulf of California with 10 described
species (Appy & Dailey 1973; Caira & Burge 2001; Caira & Zahner 2001; Ghoshroy & Caira 2001; Merlo-Serna &
García-Prieto 2016); the other three species known from the Pacific coast of Mexico were described from the more
southern states of Jalisco and Guerrero (Monks et al. 1996; Zaragoza-Tapia et al. 2019). In the present paper, three
new species (sensu Ghoshroy & Caira 2001) of Acanthobothrium from Hypanus dipterurus (Jordan & Gilbert) (one
species) and Hypanus longus (Garman) (two species) are described and the number of species of Acanthobothrium
is elevated to 16.
Materials and methods
Two specimens of Hypanus dipterurus (Jordan & Gilbert) (Diamond stingray) were purchased from local fisher-
Accepted by N. Dronen: 4 Mar. 2020; published: 17 Apr. 2020
157
men at Bahía de Chamela, Jalisco, Mexico (19°30’N; 105°04’W; February, 1995) and one specimen of H. longus
(Garman) (Longtail stingray) at La Puntilla, Mazatlán, Sinaloa, Mexico (23°11’N; 106°25’W; January, 2004). The
spiral intestine was removed from each ray and opened by longitudinal incision. Cestodes were relaxed with fresh
water for 2–5 minutes, killed with hot tap water, transferred immediately to AFA (alcohol-formalin-acetic acid) for
24–48 hr., and then stored in 70% ethanol until processed. Specimens were stained either with Mayer’s carmalum
or Ehrlich’s hematoxylin and mounted in Canada balsam for examination as whole mounts. Stained specimens
were examined using a Leica DM-LB2 microscope with both light and Normarsky differential interference contrast
(DIC) optics. Figures were drawn with the aid of a drawing tube. Measurements are given in micrometers unless
specified otherwise. The range is given, followed by mean, standard deviation, number of measured worms and
number of measurements taken in parentheses. Hook measurements follow Euzet (1959) as modified by Monks et
al. (1996), and Ghoshroy & Caira (2001). Other hook terminology follows Caira (1985). Designation of proglottid apolysis follows Caira et al. (1999) and Franzese & Ivanov (2018). For comparative purposes, specimens from
some collections were studied: Colección Nacional de Helmintos (CNHE), Instituto de Biología, Universidad Nacional Autónoma de México (IBUNAM), Mexico City, México; the Harold W. Manter Laboratory of Parasitology
(HWML), University of Nebraska-Lincoln, Lincoln, Nebraska, U.S.A.; and the Colección de Helmintos (CHE),
Centro de Investigaciones Biológicas, Universidad Autónoma de Hidalgo, Pachuca, Mexico. Material examined includes: Acanthobothrium bullardi Ghoshroy & Caira, 2001 (CNHE–4046, México); A. campbelli Marques, Brooks
& Monks, 1995 (CNHE–3033, Costa Rica; HWML–38546, Costa Rica); A. costarricense Marques, Brooks &
Monks, 1995 (CNHE–3034, Costa Rica); A. dasi Ghoshroy & Caira, 2001 (CNHE–4044, México; HWML–15549,
15550, 15551, México); A. puntarenasense Marques, Brooks & Monks, 1995 (CNHE–4176, Costa Rica); A. rajivi
Ghoshroy & Caira, 2001 (CNHE–4039, México); A. soniae Zaragoza-Tapia, Pulido-Flores, Violante-Gonzalez, &
Monks, 2019 (CNHE–11136; HWML–139978, México) and A. vargasi Marques, Brooks & Monks, 1995 (HWML
38545, Costa Rica). The holotype and paratypes were deposited in the CNHE and HWML.
In order to facilitate comparisons among species of Acanthobothrium, the categorical method proposed by
Ghoshroy & Caira (2001) and by Fyler & Caira (2006) was used in conjunction with the current literature. Application and validity of scientific names, authorities, and common names of rays are in accord with Last et al. (2016)
and Froese & Pauly (2018).
Results
Order Onchoproteocephalidea Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014
Family Onchobothriidae Braun, 1900
Genus Acanthobothrium Blanchard, 1848
Type species: Acanthobothrium coronatum (Rudolphi, 1810) Blanchard, 1848
Acanthobothrium ppdeleoni n. sp.
(Figs. 1, 4–12)
urn:lsid:zoobank.org:act:F5611609-1B2D-42D9-9B1C-A2328EDD6DAB
Type host: Hypanus dipterurus (Myliobatiformes: Dasyatidae).
Type locality: Bahía de Chamela, Jalisco, Mexico.
Site of infection: Spiral intestine.
Deposited material: Holotype (CNHE–11253), 5 paratypes (CNHE–11254), and 7 paratypes (HWML–
216260).
ZooBank registration: The Life Science Identifier (LSID) urn:lsid:zoobank.org:act:F5611609-1B2D-42D99B1C-A2328EDD6DAB
Etymology: This species is named in honor of Dr. Gerardo Pérez-Ponce de León of the Laboratorio de Helmintología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, México, for his
contributions to knowledge of Platyhelminthes.
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FIGURES 1–3. Light microscope photographs of entire worms of the three new species (Holotypes). 1. Acanthobothrium
ppdeleoni n. sp. (CNHE–11253); 2. Acanthobothrium hypanus n. sp. (CNHE–11255); 3. Acanthobothrium sinaloaensis n. sp.
(CNHE–11257). Scale bars: 1, 2 and 3 = 500 μm.
Description. Based on whole mounts of 9 mature worms and 5 incomplete specimens. Entire worms 2.5–5.95
mm (3.76 ± 1.2; 9; 9) long, greatest width at scolex (Fig. 1), euapolytic; 6–14 (11 ± 3; 9; 9) proglottids per worm
(Fig. 1). Scolex consisting of scolex proper and cephalic peduncle, scolex proper with four bothridia, 225–365 (285
± 44; 11; 11) long by 160–250 (219 ± 27; 10; 10) wide. Maximum width of scolex at level of middle loculus (Figs.
4 and 9); surfaces of scolex covered with microtriches (Fig. 10). Bothridia free posteriorly, 188–263 (224 ± 19; 11;
20) long by 78–125 (104 ± 13; 11; 20) wide; each with 3 loculi separated by two transverse septa, and specialized
anterior region in form of muscular pad (Figs. 4 and 9). Muscular pad 60–70 (66 ± 3; 11; 14) long by 83–100 (91 ±
6; 11; 14) wide, with apical sucker 24–31 (27 ± 3; 11; 22) long by 25–38 (31 ± 4; 11; 22) wide, each with one pair of
bipronged hooks at posterior margin (Figs. 4 and 9). Anterior loculus of bothridia 125–150 (131 ± 8; 10; 20) long;
middle loculus 35–63 (42 ± 7; 10; 20) long; posterior loculus 25–75 (53 ± 13; 10; 20) long (Figs. 4 and 9); loculus
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length ratio (anterior:middle:posterior) 1:0.32:0.40. Velum present between medial margins of bothridia at posterior
margin of middle loculus (Figs. 4 and 9).
Hooks bipronged, hollow, with tubercle on proximal surface of 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
slightly longer than abaxial prongs (Figs. 4–5 and 9). Bases (handles) of medial and lateral hooks articulated each
another; lateral and medial hooks approximately equal size (Figs. 5 and 9). Lateral hook measurements: A 38–50
(42 ± 4; 11; 21), B 80–113 (88 ± 9; 11; 20), C 75–113 (85 ± 10; 11; 17), D 113–158 (127 ± 11; 11; 20). Medial hook
measurements: A’ 38–48 (40 ± 3; 11; 22), B’ 85–125 (95 ± 11; 11; 22), C’ 75–115 (87 ± 11; 11; 21), D’ 113–160 (129
± 11; 11; 22).
FIGURES 4–8. Holotype of Acanthobothrium ppdeleoni n. sp. (CNHE–11253): 4. Scolex. Note: the black arrow tip show the
presence of velum; 5. Hooks; 6. Mature proglottid; 7. Terminal mature proglottid; 8. Genitalia. Scale bars: 4, 6, 7 and 8 = 100
μm; 5. = 50 μm.
Cephalic peduncle 300–925 (645 ± 181; 13; 13) long by 60–125 (81 ± 18; 13; 13) wide, covered with microtriches (Fig. 11). Proglottids acraspedote. Immature proglottids 4–9 (6 ± 2; 9; 9) in number, 65–170 (103 ± 29; 13;
13) long by 100–168 (131 ± 22; 13; 13) wide; mature proglottids 3–5 (4 ± 1; 9; 9) in number, 338–1,025 (544 ±
191; 13; 13) long by 140–210 (179 ± 22; 13; 13) wide (Figs. 1 and 6), terminal mature proglottids 650–1,055 (920
± 183; 4; 4) long by 135–210 (183 ± 33; 4; 4) wide (Figs. 1 and 7). Gravid proglottids not observed. Genital pore
marginal, irregularly alternating, 46–64% (56± 5; 13; 13) of proglottid length from anterior end. Testes arranged in
two irregular columns, one column on each side of the uterus anterior to ovarian isthmus (Fig. 6), 28–38 (34 ± 3;
9; 18) long by 33–53 (41 ± 6; 9; 18) wide (Fig. 6); testes 20–44 (33 ± 7; 9; 14) in total number, 11–25 (18 ± 4; 9;
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ZARAGOZA-TAPIA ET AL.
14) aporal, 6–16 (11 ± 3; 9; 14) preporal, 3–5 (4 ± 1; 9; 14) postporal, no testes posterior to ovarian isthmus. Cirrus
sac pyriform, extending anteriorly (Figs. 6–8 and 12), 113–148 (131 ± 18; 7; 7) long by 63–88 (75 ± 13; 7; 7) wide
in mature proglottids, 113–148 (131 ± 18; 3; 3) long by 63–88 (75 ± 13; 3; 3) wide in terminal proglottids. Cirrus
armed with spinitriches. Vagina relatively thick walled covered with gland cells, extending along medial line of
proglottid from oӧtype, reaching to anterior of cirrus sac to common genital atrium; vaginal sphincter absent; seminal receptacle not seen. Ovary occupying posterior of proglottid, asymmetrical; poral lobe 220–350 (282 ± 45; 7;
7) long in mature proglottids, reaching cirrus sac; aporal lobe 213–438 (329 ± 79; 7; 7) long in mature proglottids,
reaching anterior margin of cirrus sac (Figs. 6 and 7), inverted A-shaped in frontal view (Figs. 1, 6–7), lobulated,
ovarian isthmus posterior to mid-point of ovary; Mehlis’ gland posterior to ovarian isthmus. Vitellarium follicular,
in two columns, on each lateral side of proglottid, extending from near anterior margin of proglottid, to near posterior margin of proglottid, interrupted by vagina and cirrus sac (Figs. 6 and 7); follicles 13–15 (13 ± 1; 9; 15) long by
13–30 (20 ± 7; 9; 15). Uterus thin-walled, sacciform, occupying midline of proglottid, extends from ovarian isthmus
to near anterior margin of proglottid. Excretory ducts lateral. Eggs not seen.
FIGURES 9–12. Light microscope photographs of holotype of Acanthobothrium ppdeleoni n. sp. (CNHE–11253): 9. Scolex;
10. Details of bothridium; 11. Details of peduncle cephalic; 12. Genitalia. Scale bars: 9 = 100 μm; 10 and 11 = 10 μm; 12 = 50
μm. Abbreviations: vl, velum; mt, microtriches; vg, vagina; cs ,cirrus sac; gp, genital pore.
Remarks: Acanthobothrium ppdeleoni n. sp. is a Category 2 species (sensus Ghoshroy & Caira 2001): Species
have a total length ≤ 15 mm (2.5–5.95 mm); number of proglottids ≤ 50 proglottids (6–14 proglottids); the number
of testes per proglottids ≤ 80 (20–44 testes per proglottid); and with an asymmetrical ovary. The new species is the
fifth species of Acanthobothrium reported from H. dipterurus being preceded by A. bullardi; A. dasi and A. rajivi
that have been reported as Category 2 species and A. soberoni Ghoshroy & Caira, 2001 that has been reported as
Category 6 species. There are currently 41 described Category 2 species (Table 1). Acanthobothrium ppdeleoni n.
sp. differs from all but A. campbelli; A. coquimbensis; A. dasi; A. olseni and A. vargasi. The botridia of the new
species is shorter than that of A. coquimbensis (188–263 x 78–125 vs. 312–480 x 136–200), the length of the cirrus
sacs in mature proglottids of the new species is shorter than that of A. coquimbensis (80–125 vs. 200–400) and, the
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width of the testes in mature proglottids is grater than that of A. coquimbensis (33–53 vs. 12–24). The new species
can be distinguished from A. campbelli by the total length of the whole worms that is longer than A. campbelli
(2.5–5.95 vs. 0.99–1.80 mm), and A. campbelli has bases (handles) of the medial hooks shorter than those of A. ppdeleoni n. sp. (14–33 vs. 38–48). The new species differs from A. dasi by the length of the scolex proper (225–365
vs. 525–1,075), the length of bothridia is shorter than that of A. dasi (188–263 vs. 293–410) and A. ppdeleoni n. sp.
has abaxial prong lengths slightly longer than those of A. dasi (75–113 vs. 50–75). The width of the cirrus sacs in
mature proglottids of the new species is shorter than that of A. olseni (38–75 vs. 84–168), and the length of the testes
of A. ppdeleoni n. sp. is shorter than that of A. olseni (28–38 vs. 43–72). The new species differs from A. vargasi in
the width of the scolex proper (160–250 vs. 378 n=1), and the length of the bothridia (188–263 vs. 293–362).
Acanthobothrium hypanus n. sp.
(Figs. 2, 13–21)
urn:lsid:zoobank.org:act:318691F1-20CD-4EC5-9F2B-A19C5E680927
Type host: Hypanus longus (Myliobatiformes: Dasyatidae).
Type locality: La Puntilla, Mazatlán, Sinaloa, Mexico.
Site of infection: Spiral intestine.
Deposited material: Holotype (CNHE–11255), 3 paratypes (CNHE–11256), and 3 paratypes (HWML–
216261).
ZooBank registration: The Life Science Identifier (LSID) urn:lsid:zoobank.org:act:318691F1-20CD-4EC59F2B-A19C5E680927
Etymology: The species is named for the genus of the type host, Hypanus.
Description. Based on whole mounts of 5 mature worms and 3 incomplete specimens. Entire worms 3–6.5
mm (4.46 ± 1.41; 5; 5) long (Fig. 2), greatest width at level of mature proglottids, euapolytic; 18–22 (20 ± 2; 5; 5)
proglottids per worm (Fig. 2). Scolex consisting of scolex proper and cephalic peduncle, scolex proper with four
bothridia, 300–350 (331 ± 16; 8; 8) long by 250–300 (264 ± 22; 6; 6) wide. Maximum width of scolex at level of
posterior margin of anterior loculus (Figs. 13 and 18); surfaces of scolex covered with microtriches (Fig. 19). Bothridia free posteriorly, 238–270 (253 ± 11; 8; 14) long by 113–150 (128 ± 14; 6; 14) wide, each with 3 loculi separated by two transverse septa, and specialized anterior region in form of muscular pad (Figs. 13 and 18). Muscular
pad 54–66 (63 ± 4; 6; 12) long by 100–113 (106 ± 5; 6; 12) wide, with apical sucker 24–30 (27 ± 2; 7; 13) long by
43–55 (48 ± 4; 7; 13) wide, each with one pair of bipronged hooks at posterior margin (Figs. 13 and 18). Anterior
loculus of bothridia 125–150 (134 ± 8; 7; 14) long; middle loculus 50–70 (60 ± 14; 7; 6) long; posterior loculus
43–75 (60 ± 10; 7; 14) long (Figs. 13 and 18); loculus length ratio (anterior:middle:posterior) 1:0.45:0.45. Velum
present between medial margins of bothridia at posterior margin of posterior loculus (Figs. 13 and 18).
Hooks bipronged, hollow, with tubercle on proximal surface of 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
slightly longer than abaxial prongs (Figs. 13–14 and 18). Bases (handles) of medial and lateral hooks touching each
other (Fig. 14). Lateral hook measurements: A 40–43 (41 ± 1; 6; 12), B 75–85 (79 ± 3; 6; 12), C 75–80 (77 ± 2; 6;
11), D 113–118 (114 ± 2; 6; 12). Medial hook measurements: A’ 38–43 (40 ± 1; 6; 12), B’ 80–85 (81 ± 2; 6; 12), C’
75–75 (75 ±0; 6; 12), D’ 110–118 (114 ± 2; 6; 11).
Cephalic peduncle 450–1,900 (728 ± 481; 8; 8) long by 90–150 (128 ± 21; 8; 8) wide, covered with microtriches
(Fig. 20). Proglottids craspedote. Immature proglottids 11–16 (14 ± 2; 5; 5) in number, 50–150 (88 ± 29; 8; 22) long
by 175–315 (228 ± 38; 8; 22) wide; mature proglottids 4–7 (5 ± 1; 5; 5) in number, 275–813 (485 ± 167; 8; 14) long
by 230–313 (268 ± 20; 8; 14) wide (Figs. 2 and 15), terminal mature proglottids 750–1,075 (910 ± 133; 5; 5) long
by 285–385 (322 ± 38; 5; 5) wide (Figs. 2 and 16). Gravid proglottids not observed. Genital pores marginal, irregularly alternating, 34–64% (55 ± 7; 8; 14) of proglottid length from anterior end in mature proglottids. Testes oval in
frontal view, arranged irregularly anterior to ovarian lobes, two layer deep, 28–38 (30 ± 2; 7; 20) long by 38–68 (53
± 8; 7; 20) wide (Fig. 15); testes 36–47 (42 ± 3; 8; 16) in total number,19–24 (22 ± 2; 8; 16) aporal,12–17 (15 ± 2;
8; 16) preporal, 4–6 (6 ± 1; 8; 16) postporal, no testes posterior to ovarian isthmus. Cirrus sac pyriform (Figs. 15–17
and 21), 100–138 (119 ± 12; 8; 12) long by 28–70 (45 ± 13; 8; 12) wide in mature proglottids. Cirrus expanded at
base, armed with spinitriches. Vagina thick walled covered with gland cells, extending along medial line of pro-
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glottid from oӧtype, reaching to anterior margin of cirrus sac to common genital atrium; vaginal sphincter absent;
seminal receptacle not seen. Ovary asymmetrical; poral lobe 150–285 (192 ± 40; 8; 9) long in mature proglottids,
reaching to cirrus sac; aporal lobe 225–388 (263 ± 52; 8; 9) long, reaching to anterior margin of cirrus sac (Figs.
15 and 16), inverted A-shaped in frontal view (Figs. 2, 15–16), lobulated, ovarian isthmus posterior to mid-point of
ovary. Mehlis’ gland posterior to ovarian isthmus. Vitellarium follicular, comprised of two lateral band, 1–2 small
follicules wide on each lateral band, extending from near anterior margin of proglottid to near posterior margin of
proglottid, interrupted by vagina and cirrus sac (Figs. 15 and 16); follicles 5–10 (7 ± 1; 8; 24) long by 15–30 (22 ±
5; 8; 24) wide. Uterus thin-walled, sacciform, extends from near anterior part of proglottid to near oӧtype. Excretory
ducts lateral. Eggs not seen.
FIGURES 13–17. Holotype of Acanthobothrium hypanus n. sp. (CNHE–11255): 13. Scolex. Note: the black arrow tip show
the presence of velum; 14. Hooks; 15. Mature proglottid; 16. Terminal mature proglottid; 17. Genitalia. Scale bars: 13, 15, 16
and 17 = 100 μm; 14. = 50 μm.
Remarks: Acanthobothrium hypanus n. sp. is a Category 2 species (sensus Ghoshroy & Caira 2001): Species
have a total length ≤ 15 mm (3–6.5 mm); number of proglottids ≤ 50 proglottids (18–22 proglottids); the number
of testes per proglottids ≤ 80 (36–47 testes per proglottid); and with an asymmetrical ovary. The new species is the
seventh species of Acanthobothrium reported from H. longus in the world being preceded by A. cimari; A. costarricense; A. puntarenasense and A. vargasi that have been reported as Category 2 species (see Table 1); A. cleofanus
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Monks, Brooks & Lonce de Leon, 1996, that has been reported as Category 3 species, and A. obuncus Marques,
Brooks & Barriga, 1997 that has been reported as Category 6 species. There are currently 42 described Category 2
species (including A. ppdeleoni n. sp.). Acanthobothrium hypanus n. sp. differs from all but A. bullardi; A. cimari
and A. olseni. The new species can be distinguished from A. bullardi by the length of the scolex proper (250–300
vs. 633–943), the new species has abaxial prong lengths longer than that of A. bullardi (75–85 vs. 40–68), and the
width of cirrus sacs in mature proglottids is shorter than that of A. bullardi (28–70 vs. 100–153). Acanthobothrium
hypanus n. sp. has the length of bothridia shorter than that of A. cimari (238–270 vs. 321–438), the length of the
cirrus sacs in mature proglottids is shorter than that of A. cimari (100–138 vs. 145–180), and width of the testes
is smaller than that of A. cimari (28–38 vs. 44–72). The new species differs from A. olseni by the diameter of the
accessory sucker (43–55 vs. 24–34), and by the width of the cirrus sacs in mature proglottids (28–70 vs. 84–168).
Acanthobothrium hypanus n. sp. can be distinguished from A. ppdeleoni n. sp. by the number of proglottids (16–22
vs. 6–14), presents proglottids craspedote vs. proglottids acraspedote respectively, the width of the scolex proper is
greater than that of A. ppdeleoni n. sp. (300–350 vs. 160–250) and the width of the accessory sucker is greater than
that of A. ppdeleoni n. sp. (43–55 vs. 25–38).
FIGURES 18–21. Light microscope photographs of holotype of Acanthobothrium hypanus n. sp. (CNHE–11255): 18. Scolex;
19. Details of bothridium; 20. Details of peduncle cephalic; 21. Genitalia. Scale bars: 18 = 100 μm; 19 and 20 = 10 μm; 21 = 50
μm. Abbreviations: vl, velum; mt, microtriches; vg, vagina; cs, cirrus sac; gp, genital pore.
Acanthobothrium sinaloaensis n. sp.
(Figs. 3, 22–30)
urn:lsid:zoobank.org:act:835CD0CA-6412-444D-8322-B5CBCB9FE584
Type host: Hypanus longus (Myliobatiformes: Dasyatidae).
Type locality: La Puntilla, Mazatlán, Sinaloa, Mexico.
Site of infection: Spiral intestine.
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Deposited material: Holotype (CNHE–11257), 6 paratypes (CNHE–11258), and 5 paratypes (HWML–
216262).
ZooBank registration: The Life Science Identifier (LSID) urn:lsid:zoobank.org:act:835CD0CA-6412-444D8322-B5CBCB9FE584
Etymology: The species name refers to the state of Sinaloa, México where the type specimen was collected.
Description. Based on whole mounts of 11 mature worms and 2 incomplete specimens. Entire worms 1.5–2.75
mm (1.85 ± 0.38; 11 ;11) long, greatest width at level of mature proglottids (Fig. 3), euapolytic; 6–9 (7 ± 2; 11; 11)
proglottids per worm (Fig. 3). Scolex consisting of scolex proper and cephalic peduncle, scolex proper with four
bothridia, 210–300 (267 ± 24; 11; 11) long, 175–200 (189 ± 11; 11; 11) wide. Maximum width of scolex at level of
posterior margin of anterior loculus (Figs. 22 and 27); surfaces of scolex covered with microtriches (Fig. 28). Bothridia free posteriorly, 193–250 (214 ± 13; 11; 21) long by 75–113 (88 ± 8; 11; 21) wide; each with 3 loculi separated
by two transverse septa, and specialized anterior region in form of muscular pad (Figs. 22 and 27). Muscular pad
54–60 (58 ± 3; 11; 23) long by 75–100 (90 ± 7; 11; 23) wide, with apical sucker 22–24 (23 ± 1; 11; 22) long by
38–43 (40 ± 2; 11; 22), each with one pair of bipronged hooks at posterior margin (Figs. 22 and 27). Anterior loculus
of bothridia 113–163 (134 ± 12; 10; 20) long; middle loculus 30–50 (41 ± 5; 10; 20) long; posterior loculus 30–50
(38 ± 5; 10; 20) long (Figs. 22 and 27); loculus length ratio (anterior:middle:posterior) 1:0.31:0.28. Velum absent
(Fig. 22).
Hooks bipronged, hollow, with tubercle on proximal surface of axial prong; internal channels of axial and abaxial prongs continuous, smooth, and base and anterior part of each hook embedded in muscular pad, axial and abaxial
hooks approximately equal in size (Figs. 22–23 and 27). Bases (handles) of medial and lateral hooks articulated each
another (Fig. 23). Lateral hook measurements: A 38–45 (40 ± 3; 11; 21), B 65–98 (78 ± 7; 11; 21), C 70–93 (79 ± 6;
11; 21), D 95–133 (110 ± 9; 11; 21). Medial hook measurements: A’ 33–43 (37 ± 3; 11; 23), B’ 68–100 (82 ± 9; 11;
27), C’ 68–100 (79 ±7; 11; 23), D’ 100–140 (115 ± 10; 11; 27).
Cephalic peduncle 260–640 (357 ± 104; 13; 13) long by 60–95 (77 ± 12; 13; 13) wide, covered with microtriches (Fig. 29). Proglottids craspedote. Immature proglottids 2–6 (4 ± 1; 11; 11) in number, 50–195 (96 ± 34; 10;
17) long by 113–175 (134 ± 20; 10; 17) wide; mature proglottids 3–4 (3 ± 0.5; 11; 11) in number, 215–400 (286 ±
74; 5; 6) long by 123–153 (141 ± 11; 5; 6) wide (Figs. 3 and 24), terminal mature proglottids 500–710 (577 ± 63;
11; 10) long by 170–240 (197 ± 24; 11; 10) wide (Figs. 3 and 25). Gravid proglottids not observed. Genital pores
marginal, irregularly alternating, 50–56% (52 ± 3%; 11; 5) of proglottid length from anterior end in mature proglottids. Testes oval in frontal view, arranged in two regular columns anterior to ovarian isthmus, 13–33 (21 ± 5; 11; 31)
long by 25–55 (36 ± 9; 11; 31) wide (Figs. 3, 24–25); testes 21–32 (27 ± 3; 11; 17) in total number, 10–17 (14 ± 2;
11; 17) aporal, 8–11 (10 ± 1; 11; 17) preporal, 3–4 (4 ± 1; 11; 17) postporal, no testes posterior to ovarian isthmus.
Cirrus sac pyriform, extending medially (Figs. 24–26, 30), 50–110 (73 ± 17; 10; 10) long by 18–38 (26 ± 8; 10; 10)
wide in mature proglottids. Cirrus armed with spinitriches. Vagina narrow and relatively thick walled covered with
gland cells, reaching to anterior of cirrus sac to common genital atrium; vaginal sphincter absent; seminal receptacle
not seen. Ovary asymmetrical; poral lobe 70–145 (100 ± 26; 9; 9) long in mature proglottids, reaching to cirrus sac;
aporal lobe 95–188 (131 ± 36; 9; 9) long, reaching to anterior margin of cirrus sac (Figs. 24, 25), inverted A-shaped
in frontal view (Figs. 24 and 25), lobulated, ovarian isthmus posterior to mid-point of ovary. Mehlis’ gland posterior
to ovarian isthmus. Vitellarium follicular, follicles arranged in two lateral bands; each band consisting of oval follicles; extending from near anterior margin of proglottid to near posterior margin of proglottid, interrupted by vagina
and cirrus sac (Fig. 25); follicles 8–13 (10 ± 2; 10; 22) long by 13–20 (15 ± 2; 10; 22) wide. Uterus thin-walled,
sacciform, extends from near anterior margin of proglottid to near to near oӧtype. Excretory ducts lateral. Eggs not
seen.
Remarks: Acanthobothrium sinaloaensis n. sp. is a Category 2 species (sensus Ghoshroy & Caira 2001):
Species have a total length ≤ 15 mm (1.5–2.75 mm); number of proglottids ≤ 50 proglottids (6–9 proglottids); the
number of testes per proglottids ≤ 80 (21–32 testes per proglottid); and with an asymmetrical ovary. The new species is the eighth species of Acanthobothrium reported from H. longus in the world being preceded by A. cimari;
A. hypanus n. sp.; A. puntarenasense and A. vargasi that have been reported as Category 2 species (see Table 1);
A. cleofanus that has been reported as Category 3 species, and A. obuncus that has been reported as Category 6
species. There are currently 43 described Category 2 species (including A. hypanus n. sp. and A. ppdeleoni n. sp.).
Acanthobothrium sinaloaensis n. sp. differs from all but A. campbelli; A. dasi; A. olseni; A. vargasi, and two of them
described above. The new species can be distinguished from A. campbelli, A. dasi, A. hypanus n. sp., and A. vargasi
THREE NEW SPECIES OF ACANTHOBOTHRIUM BLANCHARD, 1848
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165
by the width of the scolex proper (175–200 vs. 211–255, 213–288, 300–350 and 378 n=1, respectively). The width
of the accessory sucker of the new species is shorter than that of A. hypanus n. sp. (38–43 vs. 43–55) and greater
than that of A. olseni and A. ppdeleoni n. sp. (38–43 vs. 24–34 and 25–38). The length of the bothridia of the new
species is shorter than that of A. dasi and A. vargasi (193–250 vs. 293–410, 293–362); the width of the bothridia of
the new species is shorter than that of A. hypanus n. sp., A. olseni and A. vargasi (80–105 vs. 113–150, 120–168 and
121–145, respectively). The width of the cirrus sacs in mature proglottids of the new species is shorter than that of A.
dasi and A. olseni (18–38 vs. 43–90 and 84–168). The total number of testes per mature proglottid in A. sinaloaensis
n. sp. is less than that of A. hypanus n. sp. (21–32 vs. 36–47). The number of aporal testes in mature proglottids of
the new species is less than those of A. dasi and A. hypanus n. sp. (10–17 vs. 22–37 and 19–24). The length of the
poral lobe of the ovary in the mature proglottids of the new species is shorter than that of A. dasi, A. hypanus n. sp.,
A. ppdeleoni n. sp. and A. vargasi (70–145 vs. 178–335, 150–285, 220–350 and 158–381, respectively). The number
of immature proglottids in the A. sinaloaensis n. sp. is less than that of A. hypanus n. sp. (2–6 vs. 11–16). Finally,
A. sinaloaensis n. sp. does no present velum between of bothridia and A. ppdeleoni n. sp. and A. hypanus n. sp. has
velum between medial margins of bothridia.
FIGURES 22–26. Holotype of Acanthobothrium sinaloaensis n. sp. (CNHE–11257): 22. Scolex; 23. Hooks; 24. Mature proglottid; 25. Terminal mature proglottid; 26. Genitalia. Scale bars: 22 = 100 μm; 23, 24, 25 and 26 = 50 μm.
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ZARAGOZA-TAPIA ET AL.
THREE NEW SPECIES OF ACANTHOBOTHRIUM BLANCHARD, 1848
TABLE 1. Species of Acanthobothrium reported within of Category 2 species.
Acanthobothrium species
Type host
Type locality
Source
A. annapinkiensis Carvajal & Goldstein, 1971
Zearaja chilensis (Guichenot)
Anna Pink Bay, Chile
Carvajal-G. & Goldstein (1971)
A. benedenii (Lönnberg, 1889)
Raja clavata Linnaeus
Mediterranean Sea
Lönnberg (1889)
A. bobconniorum Fyler & Caira, 2010
Rhynchobatus laevis (Bloch & Schneider)
Gove Harbor, Gulf of Carpentaria, Northern Territory, Australia
Fyler & Caira (2010)
A. brachyacanthum Riser, 1955
Raja stellulata (Gilbert)
Monterey Bay, California, USA
Riser (1955)
A. brayi Campbell & Beveridge, 2002
Sutorectus tentaculatus (Peters)
Eastern Shoal, South Australia
Campbell & Beveridge (2002)
A. brevissime Linton, 1909
Hypanus say (Lesueur)
Dry Tortugas, Florida, USA
Linton (1908)
A. bullardi Ghoshroy & Caira, 2001
Hypanus dipterurus (Jordan & Gilbert)
Bahía de Los Angeles, Gulf of California,
Mexico
Ghoshroy & Caira (2001)
A. campbelli Marques, Brooks & Monks, 1995
Urotrygon chilensis (Günther)
Costa de Pajaros, Puntarenas, Costa Rica
Marques et al. (1995)
A. chisholmae Campbell & Beveridge, 2002
Pastinachus sephen (Forsskål)
Nickol Bay, Western Australia
Campbell & Beveridge (2002)
Zootaxa 4766 (1) © 2020 Magnolia Press ·
A. cimari Marques, Brooks & Monks, 1995
Hypanus longus (Garman)
Punta Morales, Puntarenas Province, Costa Rica
Marques et al. (1995)
A. coquimbensis Carvajal & Jeges, 1980
Myliobatis chilensis Philippi
Antofagasta, Chile
Carvajal-G. & Jeges-G. (1980)
A. costarricense Marques, Brooks & Monks, 1995
H. longus
Punta Morales, Puntarenas Province, Costa Rica
Marques et al. (1995)
A. dasi Ghoshroy & Caira, 2001
H. dipterurus
Puertecitos, Gulf of California, Mexico
Ghoshroy & Caira (2001)
A. dujardini van Beneden, 1850
R. clavata
English Channel,Belgium
Goldstein (1967)
A. edwardsi Williams, 1969
Leucoraja fullonica (Linnaeus)
West coast of Britain, United Kingdom
Williams (1969)
A. gloveri Campbell & Beveridge, 2002
Trygonorrhina fasciata Müller & Henle
Goolwa, South Australia
Campbell & Beveridge (2002)
A. guanghaiense Yang, Sun, Zhi, Iwaki,
Reyda & Yang, 2016
Hemitrygon akajei (Müller & Henle)
Off Guanghai Port, Taishan, Guangdong Province, China
Yang et al. (2016)
A. lasti Campbell & Beveridge, 2002
Rhynchobatus djiddensis (Forsskål)
Broome, Western Australia
Campbell & Beveridge (2002)
A. lilium Baer & Euzet, 1962
Dasyatis sp.
Ceylon Pearl Bank, Sri Lanka
Baer & Euzet (1962)
A. masnihae Fyler & Caira, 2006
Urogymnus polylepis (Bleeker)
Kampung Abai, Kinabatangan River, Sabah,
Malaysia
Fyler & Caira (2006)
A. minus Tazerouti, Kechemir-Issad & Euzet, 2009
Raja asterias Delaroche
Cap Djinet, Algérie
Tazerouti et al. (2009)
A. mooreae Campbell & Beveridge, 2002
T. fasciata
Northhaven, South Australia
Campbell & Beveridge (2002)
A. ocallaghani Campbell & Beveridge, 2002
Aptychotrema vincentiana (Haacke)
Musgrave Shoal, South Australia
Campbell & Beveridge (2002)
A. olseni Dailey & Mudry, 1968
Pseudobatos productus (Ayres)
Newport Beach, California, USA
Dailey & Mudry (1968)
......continued on the next page
167
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TABLE 1. (Continued)
Acanthobothrium species
Type host
Type locality
Source
A. popi Fyler, Caira & Jensen, 2009
Urogymnus acanthobothrium Last, White
& Kyne
Arafura Sea, east of Wessel Islands, Northern
Territory, Australia.
Fyler et al. (2009)
A. puntarenasense Marques, Brooks & Monks,
1995
H. longus
Punta Morales, Puntarenas Province, Costa Rica
Marques et al. (1995)
A. quadripartitum Williams, 1968
Leucoraja naevus (Müller & Henle)
North Sea, off Aberdeen
Williams (1968)
A. rajivi Ghoshroy & Caira, 2001
H. dipterurus
Puertecitos, Gulf of California, Mexico
Ghoshroy & Caira (2001)
A. semnovesiculum Verma, 1928
P. sephen
Allahabad (Ganges and Jumna)
Verma (1928)
A. soniae Zaragoza-Tapia, Pulido-Flores,
Violante-Gonzalez & Monks, 2019
Narcine entemedor Jordan & Starks
Bahía de Acapulco, Playa Las Hamacas, Guerrero, Mexico
Zaragoza-Tapia et al. (2019)
A. sphaera Maleki, Malek & Palm, 2013
P. sephen
Persian Gulf, Iran
Maleki et al. (2013)
A. stevensi Campbell & Beveridge, 2002
T. fasciata
Marion Bay, South Australia
Campbell & Beveridge (2002)
A. tasajerasi Brooks, 1977
Styracura schmardae (Werner)
Caribbean Sea, La Cienaga, Magdalena, Colombia
Brooks (1977)
A. tetabuanense Reyda & Caira, 2006
Pateobatis uarnacoides (Bleeker)
Off Kampung Tetabuan, Sabah, Malaysia
Reyda & Caira (2006)
A. thomasae Campbell & Beveridge, 2002
A. vincentiana
Musgrave Shoal, South Australia
Campbell & Beveridge (2002)
A. tripartitum Williams, 1969
R. microocellata Montagu
English Channel, Plymouth
Williams (1969)
A. urotrygoni Brooks & Mayes, 1980
Urotrygon venezuelae Schultz
Cartagena, Colombia
Brooks & Mayes (1980)
A. vargasi Marques, Brooks & Monks, 1995
H. longus
Punta Morales, Puntarenas Province, Costa Rica
Marques et al. (1995)
A. walkeri Campbell & Beveridge, 2002
P. sephen
Nickol Bay, Western Australia
Campbell & Beveridge (2002)
A. woodsholei Baer, 1948
Bathytoshia centroura (Mitchill)
Woods Hole, Massachusetts, USA
Baer (1948)
A. zapterycum Ostrowski de Nuñez, 1971
Zapteryx brevirostris (Müller & Henle)
Mar del Plata, Buenos Aires, Argentina
Ostrowski de Núñez (1971)
ZARAGOZA-TAPIA ET AL.
FIGURES 27–30. Light microscope photographs of holotype of Acanthobothrium sinaloaensis n. sp. (CNHE–11257): 27.
Scolex; 28. Details of bothridium; 29. Details of peduncle cephalic; 30. Genitalia. Scale bars: 27 = 50 μm; 28, 29 and 30 = 10
μm. Abbreviations: mt, microtriches; vg, vagina; cs, cirrus sac; gp, genital pore.
Discussion
Members of a genus of ray commonly can be hosts to more than one species of Acanthobothrium; for example, four
species of Acanthobothrium have been described from H. dipterurus [synonym of Dasyatis brevis (Garman)] and
seven species from H. longus (Ghoshroy & Caira 2001; Marques et al. 1997; Marques et al. 1995; Monks et al.
1996). The present study adds one more species of Acanthobothrium to the list of parasites of H. dipterurus and two
more species of Acanthobothrium to that of H. longus.
The three species of the present study can be distinguished from each other by variations in characters, such as
the total length of whole worms, the width of the scolex proper and the width of the accessory sucker, the number
of testes, the number of immature proglottids, the length of the lobes of the ovary and the presence or absence of
velum between medial margin of bothridia. Some of these characters have been used in multiple comparisons between species of the genus (e.g. Maleki et al. 2015; Yang et al. 2016). However, we know that a deeper analysis of
the morphological diversity of the species of Acanthobothrium is needed to confirm whether the species belonging
to the different morphological categories are monophyletic. This also leads in the future to a more robust molecular
phylogenetic work to know the relationships between the more than 198 members of the genus that can allow a different way of comparing the species with its most phylogenetically related congenitals.
Based on information collected by Last et al. (2016), 66 species of rays (17 families) have distribution in the
Pacific coast of Mexico. Dasyatidae is represented in the coast of Mexico by 5 species and currently has only reports
of species of Acanthobothrium from H. dipterurus (5 species of Acanthobothrium including A. ppdeleoni n. sp.)
and H. longus (8 species of Acanthobothrium including A. hypanus n. sp. and A. sinaloaensis n. sp.), as mentioned
THREE NEW SPECIES OF ACANTHOBOTHRIUM BLANCHARD, 1848
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above in the section of remarks. The family with the largest number of species of rays distributed in the Pacific coast
of Mexico is Urotrygonidae with 13 species, of which 3 species have been reported as hosts of Acanthobothrium
campbelli Marques, Brooks & Monks, 1995, from Puntarenas, Costa Rica; A. minusculus Marques, Brooks & Barriga, 1997, from Provincia de El Oro, Ecuador and A. parviuncinatum Young, 1954, from California, USA, but there
are no reports of species of Acanthobothrium for these families of rays in the Pacific coast of Mexico. The family
with the second highest number of species with distribution in the Pacific coast of Mexico is Rajidae, with 11 species of rays and only A. brachyacanthum has been reported for that family in California, USA. Undoubtedly, there
is a great deal of work to be done in order to understand the diversity and phylogenetic relationships of the members
of Acanthobothrium as parasites of elasmobranchs.
Likewise, the present study adds three new species of Acanthobothrium to the 13 species that have been reported
from the Pacific coast of Mexico, A. bajaensis, A. bullardi, A. cleofanus, A. dasi, A. dollyae, A. maryanskii, A. puertecitense, A. rajivi, A. royi, A. santarosaliense, A. soberoni, A. soniae, and A. vidali (Appy & Dailey 1973; Monks et
al. 1996; Caira & Burge 2001; Caira & Zahner 2001; Ghoshroy & Caira 2001; Zaragoza-Tapia et al. 2019). To date,
of these, two species are members of Category 1, seven are Category 2 (including the three new species described
herein), two are Category 3, two are Category 4, one is Category 5, and two are Category 6; no representatives of
Categories 7–9 have been described from the Pacific coast. In addition, two other species have been reported from
the Mexican Coast of the Gulf of Mexico/Caribbean (A. cartagenensis Brooks & Mayes, 1980 and A. marquesi
Rodríguez-Ibarra, Pulido-Flores, Violante-González, & Monks, 2018) (Monks et al. 2015; Rodríguez-Ibarra et al.
2018) (Cetegories 1 y 3, respectively). Therefore, the descriptions of A. ppdeleoni n. sp., A. hypanus n. sp. and A.
sinaloaensis n. sp. brings the total number of species of Acanthobothrium to 16 from the Mexican coasts.
Acknowledgments
The authors would like to thank all those who made possible the collection and examination of specimens during
this study, particularly Gerardo Pérez-Ponce de León, IBUNAM. The authors also thank Luis García-Prieto, curator
of the CNHE, and Scott L. Gardner and Gabor Racz (curator and collection manager, respectively) of the HWML,
for providing access to laboratories, specimens, and literature. To Sergio Martínez-Lora was responsible for cataloging literature. To the Consejo Nacional de Ciencia y Tecnología (CONACYT) provided a scholarship (no. 432427)
to FZ-T. We also thank the editor and anonymous reviewers for their comments.
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