Comp. Parasitol.

82(2), 2015, pp. 262–268

A New Species of Serendip (Cestoda: Tetraphyllidea: Serendipeidae)

in Rhinoptera steindachneri (Chondrichthyes: Myliobatidae) from
the Pacific Coast of Mexico

SCOTT MONKS,1,3 FRANCISCO ZARAGOZA-TAPIA,1 GRISELDA PULIDO-FLORES,1 AND

JUAN VIOLANTE-GONZÁLEZ2
1
Laboratorio de Morfologı́a Animal, Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo,
Apartado Postal 1-10, Pachuca, Hidalgo, C.P. 42001, México (e-mail: scottmonks@hotmail.com; gpflores6@hotmail.com)
and
2
Unidad Académica de Ecologı́a Marina, Universidad Autónoma de Guerrero, Gran Vı́a Tropical No. 20, Fracc. Las Playas,
C.P. 39390, Acapulco, Guerrero, México (e-mail: viojuang@yahoo.com.mx)

ABSTRACT: A species of Serendip Brooks and Barriga, 1995, Serendip danbrooksi n. sp., is described from Mexico as
a parasite of Rhinoptera steindachneri Evermann and Jenkins, 1891. The new species differs from Serendip deborahae, the
type and only other known member of the genus, by having bothridia subdivided by 2 septa, 1 simple and 1 bifurcating,
rather than 3 septa, 2 simple and 1 bifurcating, and by having 37–61 testes versus 64–116 testes, respectively. In general,
S. danbrooksi n. sp. is smaller than S. deborahae in the number of proglottids (average 77 vs. 150, respectively) and length
(maximum length 15.3 mm vs. 60.0 mm, respectively). Clarification of the details of some previously described structures is
discussed.
KEY WORDS: Serendipeidae, Serendip danbrooksi n. sp., Rhinoptera steindachneri, Myliobatidae.

The majority of surveys of helminths of elasmo- MATERIALS AND METHODS

branchs from Mexico have focused on species that
inhabit the Gulf of California (also known as the Mar
de Cortez or the Sea of Cortez) (Caira, 1985; Tyler
and Caira, 1999; Ruhnke et al., 2000; Caira and
Bruge, 2001; Caira and Zahner, 2001; Ghoshroy and
Caira, 2001; Olson and Caira, 2001; Ruhnke and
Seaman, 2009). Others have reported species that
inhabit elasmobranchs from Pacific waters outside of
the Gulf of California (Caballero y Caballero, 1945;
Bravo-Hollis, 1969; Monks et al., 1996; Gómez del
Prado-Rosas and Euzet, 1999), but members of
Serendip Brooks and Barriga, 1995, have never been
reported. During a continuing survey of the metazoan
parasites of elasmobranchs of Mexico, a new species
of this little-known genus in cownose rays (Rhinop-
tera steindachneri) was discovered in Bahı́a de
Acapulco, Acapulco, Guerrero, Mexico. Previously
collected, but unprocessed, material from other
localities off the Pacific coast of Mexico were
revisited, resulting in the discovery of additional
specimens consistent with the new species. The new
species of Serendip is described and discussed
herein, the nature of the apical sucker is clarified,
and some problematic aspects of our current un-
derstanding of the relationships of the Serendipeidae
are pointed out.
3
Corresponding author.
Specimens of the new species were found attached to the
inner surface of the wall of the spiral valve of 7 of 25
individual cownose rays, Rhinoptera steindachneri Ever-
mann and Jenkins, 1891 (Chondrichthyes: Myliobatiformes:
Myliobatidae), that were collected by fishermen from waters
off Playa Las Hamacas, Bahı́a de Acapulco, Guerrero
(16u51910.800N; 99u53959.020W) during February to June
2011. In addition, specimens also had been collected
previously (January 2004) from 1 of 3 cownose rays obtained
from fishermen in El Embarcadero, La Piedra, Mazatlán,
Sinaloa (23u129180N; 106u249370W).
Worms were placed temporarily in saline solution (6.5 g
NaCl/1.0 liter distilled water), killed in hot water, fixed in
alcohol-formalin-acetic acid (AFA) for 24 hr, and stored in
70% ethyl alcohol. Worms were stained with Mayer’s
carmalum or Delafield’s hematoxylin, cleared in methyl
salicylate, mounted on slides in Canada balsam as
permanent mounts, and examined using a compound
microscope (Leica DM-LB2) with differential interference
contrast (DIC-Nomarski) illumination. Histological sections
were prepared from the scolex and mature proglottids of
a complete specimen of Serendip danbrooksi n. sp. and from
a partial worm as follows: Scolex and proglottids were
embedded in paraplast and sectioned at 8 mm intervals using
a Leica RM2135 rotary microtome. Sections were stained
with Mayer’s hematoxylin, Biebrich scarlet, phosphotungs-
tic/phosphomolybdic acid solution, and Aniline blue
(recipes according to Luna, 1968), cleared in xylene, and
mounted with coverslips on glass slides in Canada balsam.
The remainder of the strobila of the complete specimen was
prepared as a whole mount. Measurements were taken using
a calibrated ocular micrometer and are reported in micro-
meters (mm) unless stated otherwise; for some traits, ranges
are given, followed in parentheses by mean values 6 1
standard deviation and sample size (n). A paratype of

262
 MONKS ET AL.—NEW SPECIES OF SERENDIP FROM MEXICO
Serendip deborahae (Museum of Natural History, Geneva,
Switzerland, MNGH-INVE18254) was examined. Speci-
mens were deposited in the Colección Nacional de
Helmintos, Instituto de Biologı́a, Universidad Nacional
Autonóma de México (IBUNAM), Mexico (holotype CNHE
9725, and paratypes CNHE-9726 to CNHE-9727); the
Harold W. Manter Laboratory, University of Nebraska,
Lincoln, Nebraska, U.S.A (HWML-75091 to HWML-
75104, paratypes); and the Museum of Natural History,
Geneva, Switzerland (MNGH-PLAT-90513 to MHNG-
PLAT-90515, paratypes).
RESULTS
Serendip danbrooksi n. sp.
(Figs. 1–7)
Updated generic diagnosis: Eucestoda; Tetraphyl-
lidea. Scolex composed of 4 triangular bothridia,
each subdivided by septa extending radially from
base, dividing bothridial face but lacking distinct
loculi. Bothridia with marginal loculi and thin velum;
apical suckers lacking. Bothridia fused to form
a single platelike structure giving bothridial faces
a dorsal rather than lateral aspect; pedicels lacking.
Vestigial apical sucker centrally located in tissue of
scolex apex, wider than long. Proglottids apolytic,
protandric. Testes in 2 layers, in 2 fields, extending
throughout proglottid; postovarian testes present,
some positioned between ovarian digitiform pro-
cesses in mature proglottids. Cirrus sac spherical;
cirrus armed. Genital pore pre-equatorial. Vagina
passing anteriorly to cirrus sac. Ovary in frontal view
with radiating lobes, tetra-lobed in cross section, with
digitiform processes extending laterally. Vitellarium
follicular, medullary, in 2 lateral fields extending
length of proglottid ventrally; vitelline fields con-
verging dorsally in each proglottid, except for areas
of ovarian and terminal genitalia.
Description (based on 4 complete adult and 23
incomplete specimens, 12 immature worms, and
histological sections of 6 free proglottids and
1 scolex): Strobila slightly craspedote, apolytic,
11.0–23.3 mm (15.3 mm 6 6.9 mm; 3) long,
composed of 57–103 (77 6 24; 3) proglottids. Scolex
1,275–2,675 (2,168 6 385; 27) long by 1,500–3,000
(2,168 6 385; 27) wide. Vestigial sucker (sensu
Brooks and Barriga, 1995) located centrally in apical
tissue of scolex 55–93 (65 6 10; 17) long by 125–205
(151 6 21; 17) wide (Figs. 1, 3). Pedicels lacking.
Bothridia symmetrical, 700–1,500 (1,054 6 197;
104) long by 800–1,825 (1,251 6 214; 104) wide,
fused anteriorly by a muscular velum and posteriorly
by a thinner flexible velum into single, anteriorly
directed, structure. Bothridia subdivided by poster-
263
iorly diverging, muscular septa; 1 simple (lateral) and
1 bifurcating (medial), but not divided in separate
loculi. Peripheral margins of bothridia with 13–15
small loculi (13 loculi on 3 of 44 bothridia, 14 on 6 of
44, 15 on 35 of 44; n 5 44 bothridia), and medial
margin with thin, contractile, velum-like membrane
(Fig. 1). Interseptal marginal loculi variable in
number, region A: 3–4; regions B and C: 2–3; and
region D: 4–5 (Fig. 1). Peduncle 875–5,250 (2,479 6
1,010; 25) long, 125–600 (326 6 123; 25) wide.
Immature proglottids wider than long; mature pro-
glottids wider than long to square (Fig. 2). Endmost
mature proglottids longer than wide, 570–850 (723 6
121; n 5 4) long by 430–750 (570 6 139; n 5 4)
wide (Fig. 4). Gravid proglottids not observed. Testes
in 2 irregular longitudinal fields, in 2 layers,
extending length of proglottid, 37–61 (47 6 6; 53)
in total number; 2–9 (5 6 1; 53) preporal, 12–27
(18 6 3; 53) postporal, 18–29 (24 6 2; 53) aporal
(Figs. 2, 4). Maturing proglottids with 4–8 postovar-
ian testes; often with testes located between ovarian
processes. Testes wider than long, 20–63 (32 6 10;
43) long by 18–93 (49 6 15; 43) wide, (Fig. 7).
Genital atrium deep, opening 15–30% (23 6 4%; 64)
from anterior end in mature proglottids, and 18–29%
(24 6 5%; 4) in terminal proglottids (Figs. 2, 4).
Cirrus sac 110–275 (192 6 46; 57) long by 40–125
(85 6 21; 57) wide in mature proglottids, containing
eversible cirrus armed with obvious microtriches.
Vas deferens extensively coiled, on poral side of
cirrus sac dorsal to testicular fields, with some coils
aporal to cirrus sac (not illustrated); joining cirrus
sac near posterior end. Vagina anterior to cirrus sac,
passing medially, curving ventrally around posterior
aporal side of cirrus sac and then around dorsal side
of vas deferens. Vagina glandular (Figs. 2, 4).
Ovary in frontal view with radiating lobes, tetra-
lobed in cross section, with digitiform processes
extending laterally past osmoregulatory ducts, 75–
135 (89 6 19; 15) long by 250–340 (295 6 64; 15)
wide. Vitelline follicles medullary, lateral, confluent
dorsally except dorsal to ovary and to terminal
genitalia (Fig. 5); ventrally extending medially to
excretory ducts from anterior extent of testicular
fields to anterior end of ovary, interrupted near
genital pore (Figs. 5, 6). Vitelline follicles 10–40
(20 6 7; 31) long by 10–20 (10 6 2; 31) wide.
Uterus in mature and terminal proglottids glandular,
sinuous sac-like, extending ventrally from ovary to
near anterior end of proglottid. Eggs not observed.
Excretory ducts as paired dorsal and ventral osmo-
regulatory canals.
264 COMPARATIVE PARASITOLOGY, 82(2), JULY 2015

Figures 1–7. Serendip danbrooksi n. sp. 1. Bothridium of scolex indicating interseptal regions A, B, C, and D (medial to
lateral, respectively); medial velum anterior to small marginal loculi. 2. Mature proglottid. 3. Immature specimen. 4. Terminal
attached proglottid; only 31 of 39 testes were drawn. 5. Outline of terminal attached proglottid showing ventral arrangement of
vitellaria. 6. Outline of terminal attached proglottid showing dorsal arrangement of vitellaria. 7. Testis of terminal attached
proglottid showing internal features. Abbreviations: vm, medial velum; p, peduncle; gp, genital pore. Scale bars in mm.

Taxonomic summary Other reported hosts: none.

Type host: Rhinoptera steindachneri Evermann Site of infection: Spiral intestine.
and Jenkins, 1891 (Chondrichthyes: Myliobatiformes: Type locality: Bahı́a de Acapulco, Playa Las Hamacas
Myliobatidae). (16u519110N; 99u539590W), Guerrero, Mexico.
 MONKS ET AL.—NEW SPECIES OF SERENDIP FROM MEXICO
Other localities: Mazatlán (23u129N; 106u249W),
Sinaloa, Pacific coast of Mexico.
Specimens deposited: Holotype (CNHE-9725) and
15 paratypes (CNHE-9726 to CNHE-9727); 3 para-
types (MNGH-PLAT-90513 to MHNG-PLAT-90515);
15 paratypes (HWML-75091 to HWML-75104).
Etymology: The species is named after Daniel R.
Brooks of the Harold W. Manter Laboratory, who
collected the first known member of the genus.
Remarks
Serendip was established by Brooks and Barriga
(1995) for S. deborahae, a parasite of R. steindach-
neri from southeastern Ecuador. Until this study, the
genus has remained monotypic. The diagnosis of the
genus includes having a scolex composed of 4
triangular bothridia, each subdivided by septa
extending radially but not dividing the bothridia into
distinct loculi. The margins of each bothridia are set
off by marginal loculi, and the bothridia, without
pedicels, are fused at the apex and are united distally
by a velum. A small, nonmuscular, internal apical
sucker is located in the tissues of the scolex between
the bothridia. Serendip danbrooksi n. sp. also has
these characteristics, indicating that it should be
assigned to the genus Serendip. The new species is
similar to S. deborahae in general appearance but can
be distinguished from that species by having
bothridia that are subdivided by 2 septa (1 simple
and 1 bifurcating) rather than 3 septa (2 simple and 1
bifurcating). Peripheral margins of the bothridia of
the new species have 13–15 small loculi (13 loculi on
3 of 44 bothridia, 14 on 6 of 44, 15 on 35 of 44; n 5 44
bothridia), while the specimens of S. deborahae that
we examined had from 22 to 27 marginal loculi; the
number of loculi is different between species, so no
direct comparison of loculi per septa can be made.
Serendip danbrooksi n. sp. also can be distinguished
from S. deborahae by the number of testes (37 to 61
testes [mean 47] vs. 64 to 116, respectively).
The individuals of the new species generally are
smaller than those of S. deborahae, although there is
overlap in the upper limit of the range of some characters.
As a result, the new species is shorter with fewer
proglottids (maximum length 15.3 vs. 60.0 mm; mean
number of proglottids 77 vs. 150), and the peduncle is
shorter (2,479 vs. 8,250), while some structures (e.g.,
accessory sucker, bothridia, size of proglottids) are
approximately the same size. The proglottid morphology
of the 2 species is similar except for the number of
testes and the extent of the vitellaria (Figs. 5, 6).
265
The scanning electron micrograph of Brooks and
Barriga (1995) (their figs. 1–4) shows a specimen
with only 2 septa, 1 simple and 1 bifurcate, rather
than the arrangement presented for S. deborahae. A
paratype of S. deborahae (MNGH-INVE18254) was
examined, and that specimen was as discussed in the
formal description by Brooks and Barriga (1995) and
depicted in their fig. 5, having 2 simple septa and 1
bifurcated septa.
DISCUSSION
The study of the helminths of elasmobranchs in
Mexico goes back at least until the 1940s and 1950s
with the works published by Caballero y Caballero
(1945), Bravo-Hollis (1954), and Winter (1959); see
Lamothe-Argumedo et al. (1997) and references
therein. While such a situation might lead one to
think that there are few new discoveries to be made in
this region, these early studies were occasional in
nature and reported only the digeneans and mono-
geneans of elasmobranchs off the Pacific coast. More
recent studies of the cestode fauna of elasmobranchs
have been limited to particular regions, such as
Jalisco, Mexico (Monks et al., 1996), or the Gulf of
California (see, for example, Tyler and Caira, 1999;
Ruhnke et al., 2000; Caira and Zahner, 2001;
Ghoshroy and Caira, 2001; Fyler et al., 2006; Tyler,
2006). The only report of nematodes is that of
Hoberg et al. (1998), from a stingray from the
southeastern Pacific coast of Mexico. Thus, although
there are studies on a variety of helminths from the
area, there are still many regions of the Pacific coast
where the helminths of elasmobranchs have not been
studied. This is the first report of a cestode from
elasmobranchs of Guerrero.
It is interesting that Serendip has not been reported
from the Gulf of California, despite the concentration
of reports of cestodes from R. steindachneri from that
region (see references above). Curran and Overstreet
(2000) mention that over 800 elasmobranchs from the
Gulf of California were examined as part of the study
in which they were involved, and Tyler (2001)
mentioned specifically that 19 specimens of R.
steindachneri were examined for his report. None
of the publications stemming from that impressive
study reported specimens of Serendip, although it is
possible that they were collected but have never been
identified. Using the reasoning of Tyler (2000), this
suggests that individuals from the populations in the
Gulf of California that have been sampled may not be
leaving that region to mix with other members of the
more southern ray populations along the Mexican
266 COMPARATIVE PARASITOLOGY, 82(2), JULY 2015
coast. Sandoval-Castillo et al. (2004) and Sandoval-
Castillo and Rocha-Olivares (2011) discovered ge-
netic divergence between populations of Rhinobatos
productus (Ayres, 1854) and R. steindachneri,
respectively, on the Pacific coast of Baja California
and the Gulf of California. In both studies, it was
suggested that the populations of the individuals of
each species within the Gulf of California might
represent cryptic species. Castillo-Páez et al. (2014)
noted that populations of Zapteryx exasperata
(Jordan y Gilbert, 1880) were genetically isolated
from others in the northern Mexican Pacific.
However, the distribution of the new species reported
herein suggests that cownose rays move between
Mazatlán and Acapulco (much farther apart than the
Gulf of California and Mazatlán); whether they are
moving southward, northward, or in both directions is
unknown. Based on the scanning electron micro-
graphs of Brooks and Barriga (1995, their figs. 1–4)
of a specimen that can now be identified as S.
danbrooksi n. sp., it is interesting to note that at least
some individuals of R. steindachneri do appear to be
moving (migrating?) between Mexico and at least as
far south as Ecuador, carrying with them the new
species. Further studies of the helminth fauna of the
Pacific coasts of Mexico and Central America are
necessary before the distribution of the new species is
known. Nevertheless, as seen from studies of other
species of elasmobranch (Marie and Justine, 2005;
Richards et al., 2009; citations within Sandoval-
Castillo and Rocha-Olivares, 2011; Castillo-Páez
et al., 2014), we are far from an understanding the
distributions of elasmobranchs.
Brooks and Barriga (1995) noted that the members
of the genus have proglottids that are apolytic and
protandric. The terminal proglottid they described
was similar to those of our specimens, but proglottids
this mature were found on only a few (n 5 4 of 27)
adult individuals; no free proglottids of this species
were found in the intestines of any of the cownose
rays that were collected. The male reproductive
structures in the proglottids of this species develop
earlier (i.e., in the more anterior proglottids) than the
female structures, which were still not fully de-
veloped in the posteriormost proglottids, and no
gravid proglottids were found. This suggests that
these species might be hyperapolytic (Fyler, 2011;
Pickering and Caira, 2012) rather than only apolytic.
A paratype of S. deborahae (Museum of Natural
History, Geneva, Switzerland, MNGH-INVE18254)
was examined and found to have the same bothridial
structure as that described and drawn by Brooks and
Barriga (1995) for that species. Brooks and Barriga
(1995) described the central sucker of the scolex as
‘‘vestigial,’’ although the structure of the sucker
appears to be well defined. However, since we have
no method of determining the degree of function of
the structure, that terminology is maintained. In the
description of S. deborahae, the sucker was described
as being longer than wide, but their figures 1 and 2
show that the sucker is wider than long; this condition
was verified in paratype MNGH-INVE18254, the
only specimen of that species that was available for
study.
Serendipidae (sec. Brooks and Barriga, 1995), later
changed to Serendipeidae Brooks and Evenhuis, 1995,
because that name was occupied (Brooks and
Evenhuis, 1995), was considered to be the putative
sister clade of Dioecotaeniidae based on the shared
fusion of the bothridia that is present in all members of
those families: fusion of bothridia with each other
(Dioecotaenia Schmidt, 1969; Duplicibothrium Wil-
liams and Campbell, 1978; and Serendip) or fusion of
the bothridia with the scolex (Glyphobothrium Wil-
liams and Campbell, 1977). Brooks and Barriga
(1995) assigned Duplicibothrium, Glyphobothrium,
and Serendip to Serendipeidae and identified Dioeco-
taenia as the sole member of Dioecotaeniidae. Ruhnke
et al. (2000) also considered these relationships to be
supported by their more recent findings, as well as by
molecular studies (Caira et al., 1999; Olson and Caira,
1999). The putative sister relationship between
Duplicibothrium and Dioecotaenia was strongly
supported by Caira et al. (2014), but to date, none of
the other taxa assigned to or suggested as potential
members of Serendipeidae (see Ruhnke, 2011) has
been examined empirically as pertaining to the family.
Furthermore, Ruhnke et al. (2000) suggested that
Echeneibothrium javanicum Shipley and Hornell,
1906, and Tiarabothrium javanicum Shipley and
Hornell, 1906, both known only from Rhinoptera
javanica Müller and Henle, 1841, might also belong
to Serendipeidae. Serendip and these latter 2 species
are distributed in the Pacific and Indian Oceans,
respectively; Glyphobothrium is known only from the
Atlantic Ocean and the Gulf of Mexico (Pulido-
Flores and Monks, 2014), while Duplicibothrium has
been reported from both the Atlantic and Pacific
Oceans, suggesting that the historical aspects of the
family may not be simple (for a similar problem, see
the study of Pedibothrium Linton, 1909, in nurse
sharks by Caira and Euzet, 2001). It is possible that
these so phenetically distinct taxa represent relic
taxa (sensu Brooks and Bandoni, 1988) that are the
 MONKS ET AL.—NEW SPECIES OF SERENDIP FROM MEXICO
remnants of a once species-rich clade that had now-
extinct members with scoleces of types that would
provide transitional information about the evolution
of the extremely different forms found in the extant
genera. While some progress has been made in the
understanding of the relationships between these taxa
(see Healy et al., 2009, and references therein), it is
clear that but much more work is necessary to clarify
elasmobranch cestode associations.
ACKNOWLEDGMENTS
The authors thank all those who made possible the
collection and examination of specimens. Scott L.
Gardner and Gabor Racz, curator and collection
manager, respectively, at the HWML, and Mary
Hanson Pritchard, affiliate of the HWML, provided
access to material of the collection and literature in the
laboratory archives. Students from the Laboratorio de
Morfologı́a Animal, Universidad Autónoma del Estado
de Hidalgo, and the Unidad Académica de Ecologı́a
Marina, Universidad Autónoma de Guerrero, helped
with the collection of specimens. This study was
supported by funds from the project: Inventario
Ambiental y Establecimiento de Indicadores Regio-
nales de la Red Temática: Calidad Ambiental y
Desarrollo Sustentable (PROMEP-SEP). Part of this
manuscript was prepared during a postdoctoral research
visit to the HWML by S.M. and G.P.-F., supported by
funds from the Patronato Universitario (Gerardo Soza
Castelán, president), Universidad Autónoma del Estado
de Hidalgo (UAEH), and the Consorcio de Universi-
dades Mexicanas (CUMEX). The Consejo Nacional de
Ciencia y Tecnologı́a (CONACYT) provided a scholar-
ship (no. 432427) to F.Z.-T.
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