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Published 15 September 2023
DOI: 10.1645/23-32
Contents and archives available through www.bioone.org or www.jstor.org
Journal of Parasitology
journal homepage: www.journalofparasitology.org
TAPEWORMS (CESTODA: OPHIOTAENIA) FROM THE NORTHERN COTTONMOUTH
(AGKISTRODON PISCIVORUS)
Toma
´s
ˇScholz
1
, Alain de Chambrier
2
, Chris T. McAllister
3
, Vasyl V. Tkach
4
, and Roman Kuchta
1
1
Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05 České Bud
ejovice, Czech Republic.
2
Department of Invertebrates, Natural History Museum, P.O. Box 6434, CH-1211 Geneva 6, Switzerland.
3
Division of Natural Sciences, Northeast Texas Community College, 2886 FM 1735, Chapel Hill Road, Mt. Pleasant, Texas 75455.
4
University of North Dakota, Grand Forks, North Dakota 58202.
Correspondence should be sent to T. Scholz (https://orcid.org/0000-0002-6340-3750) at: tscholz@paru.cas.cz
KEY WORDS ABSTRACT
Morphology
Taxonomy
Redescription
Synonymy
Ophidia
Reptiles
North America
The northern cottonmouth, Agkistrodon piscivorus (Lace
´pe
`de, 1789) (Viperidae: Crotalinae), occurs
in the southeastern United States and is one of the few semiaquatic vipers in the world. Three pro-
teocephalid tapeworms of the genus Ophiotaenia La Rue, 1911 (Cestoda), have been described
from this venomous snake. A critical evaluation of type specimens and tapeworms recently col-
lected from A. piscivorus has revealed that only 2 species, Ophiotaenia marenzelleri (Barrois, 1898)
and Ophiotaenia grandis La Rue, 1911 (new synonym Ophiotaenia agkistrodontis [Harwood, 1933]),
are specific parasites of this crotaline viper; both species are redescribed here. Ophiotaenia grandis
was originally described from a mixture of 2 species: ‘true’ O. grandis, which is indistinguishable
from O. agkistrodontis described 22 yr later and thus considered to be a junior synonym of O. gran-
dis, and O. marenzelleri.Ophiotaenia marenzelleri, also reported from the pygmy rattlesnake,
Sistrurus miliarius (Linnaeus, 1766), is a larger tapeworm with a massive scolex, a large cirrus sac,
a very large, annular vaginal sphincter near the equatorial gonopore, and an oval, 3-layered
embryophore surrounded by a nearly square hyaline outer membrane. Ophiotaenia grandis is much
smaller and more slender and has a narrower scolex, a smaller cirrus sac and vaginal sphincter, a
2-layered embryophore, and a distinctly pre-equatorial gonopore. In addition to O. marenzelleri
and O. grandis, other Ophiotaenia species typical of semiaquatic snakes (Colubridae: Natricinae)
may be present in the northern cottonmouth, which serves only as a postcyclic or occasional host.
There is also a tabular summary of 18 species of Ophiotaenia from semiaquatic snakes worldwide,
with information on their hosts, distribution, and taxonomically important characters, including
key measurements.
Snakes (Squamata: Ophidia) serve as definitive hosts of a vari-
ety of tapeworms (Cestoda), especially the proteocephalids
(Onchoproteocephalidea). No fewer than 70 species of 6 proteo-
cephalid genera were reported from snakes, with 56 taxa classified
in Ophiotaenia La Rue, 1911, but the distribution of these tape-
worms in different snake groups and across zoogeographic
regions is highly inconsistent (de Chambrier et al., 2017). Overall,
proteocephalids are more common in aquatic and semiaquatic
snakes, probably because of the easier transmission of their larval
stages (metacestodes), which develop in planktonic crustaceans
(copepods); in addition, fish and frogs, which serve as paratenic
hosts, may be the main source of infection for snakes (Thomas,
1934a, 1934b, 1941; Freze, 1965).
The cestode fauna of North American snakes is relatively
depauperate (Brooks, 1978); de Chambrier et al. (2021) reported
only 7 valid species of proteocephalids from snakes in the
Nearctic. The northern cottonmouth or water moccasin, Agkis-
trodon piscivorus (Lace
´pe
`de, 1789) (Viperidae: Crotalinae), is one
of the few semiaquatic vipers in the world (Gloyd and Conant,
1990). Three proteocephalid species, namely, Ophiotaenia maren-
zelleri (Barrois, 1898), Ophiotaenia grandis La Rue, 1911, and
Ophiotaenia agkistrodontis (Harwood, 1933), have been described
from this venomous snake, which occurs in the southeastern
United States (Uetz et al., 2022).
Although Brooks (1978) has provided a morphological charac-
terization of all 3 cestode species, their distinction remains prob-
lematic, primarily for 3 reasons: (1) the original description of
O. grandis casts doubt on the species affiliation of the specimens
used by La Rue (1914); (2) Brooks (1978) used tapeworms from
colubrid semiaquatic snakes, Nerodia cyclopion (Dume
´ril, Bibron
and Dume
´ril, 1854) and Nerodia floridana (Goff, 1936) (Colubridae:
Natricinae), for the morphological characterization of O. grandis,
464
Journal of Parasitology 2023 109(5) 464–479
ÓAmerican Society of Parasitologists 2023
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i.e., not from the type host, northern cottonmouth; and (3) Brooks
(1978) did not mention some taxonomically important structures,
such as a vaginal sphincter, for O. agkistrodontis and O. marenzelleri,
although they are present (see below).
Recently, we collected extensive material of proteocephalids
of A. piscivorus and re-examined all types and some voucher
specimens of all species deposited in the National Museum of
Natural History, Smithsonian Institution (USNM), Washing-
ton, D.C. This material allowed us to critically evaluate the
species diversity of the tapeworms that parasitize northern cot-
tonmouths. Therefore, the objective of the present study was
(1) to clarify the taxonomic status of Ophiotaenia species
reported from the northern cottonmouth, (2) to redescribe the
species recognized as valid, and (3) to list additional parasites
of this viperid host.
MATERIALS AND METHODS
Tapeworms deposited in museum collections (detailed below)
and new material from the northern cottonmouth in Arkansas,
Mississippi, and Oklahoma collected by 2 of the authors (CTM
and VVT; for details, see “Material studied” in redescriptions of
each species) were studied.
Snakes were handled as described in previous reports by the
present authors (e.g., de Chambrier et al., 2021; Diard et al.,
2022). Tapeworms removed from the host intestine were placed
in saline (0.9% NaCl solution) and carefully cleared of intesti-
nal contents. They were heat killed with a near-boiling 4%
formaldehyde solution or 70% DNA grade ethanol for future
molecular studies. They were then stained with Mayer’s car-
mine, dehydrated in an ethanol series, cleared in clove oil, and
permanently mounted in Canada balsam (for more details see
de Chambrier et al., 2021; Diard et al., 2022). Several scolices
were used for scanning electron microscopy (SEM); they were
processed according to the protocol described by Kuchta and
Caira (2010). Scanning electron micrographs were taken with a
JEOL JSM-7401F field emission scanning electron microscope
(JEOL Ltd., Tokyo, Japan). Eggs collected from the uterus of
unstained worms preserved in 70% ethanol were examined in dis-
tilled water.
All measurements in the morphological descriptions are in micro-
meters (mm) unless otherwise indicated (Tables I, II). Common and
scientific names of snakes follow the Reptile Database (Uetz et al.,
2022). Acronyms of museum collections are as follows: HWML—
Harold W. Manter Laboratory, University of Nebraska, Lincoln,
Nebraska; IPCAS—Institute of Parasitology, Biology Centre of the
Czech Academy of Sciences, C
ˇeske
´Bud
ejovice, Czech Republic;
MHNG-PLAT—Natural History Museum, Geneva, Switzerland;
USNM—National Museum of Natural History, Smithsonian Insti-
tution, Washington, D.C.
RESULTS
Evaluation of all available type specimens (holotype of
O. agkistrodontis and syntypes of O. grandis), vouchers of
O. grandis and O. marenzelleri from the USNM, and newly col-
lected material from A. piscivorus has revealed that only 2 species,
O. marenzelleri, and O. grandis, actually occur as specific and
common parasites in the northern cottonmouth. They are rede-
scribed below, based on newly collected specimens from Arkan-
sas, Mississippi, and Oklahoma. Ophiotaenia agkistrodontis is
synonymized with O. grandis, which was described from a mix-
ture of 2 species.
REDESCRIPTION
Ophiotaenia marenzelleri (Barrois, 1898) La Rue, 1911
(Figs. 1–5)
Synonyms: Ichthyotaenia marenzelleri Barrois, 1898; Crepido-
bothrium marenzelleri (Barrois, 1898) Meggitt, 1927; Proteocepha-
lus marenzelleri (Barrois, 1898) Brooks, 1978; Ophiotaenia grandis
La Rue, 1911 (in partim; new synonym).
Material studied: One immature specimen, Biloxi, Harrison Co.,
Mississippi, collected in August 1931 (USNM 1321306); numerous
fragments of 1 or more specimens, Marion, Perry Co., Alabama, col-
lected in September 1979 by J. F. Detterline (given name not known;
USNM 1373420); 1 specimen without scolex and cross sections from
host USA 1 (hologenophore—MHNG-PLAT-0032847); 1 specimen
from host USA 1y (MHNG-PLAT-0035543); 1 specimen from host
USA 1z (MHNG-PLAT-0035544); 1 specimen without scolex (holo-
genophore) from host USA 1a (MHNG-PLAT-0035545); 1 speci-
men from host USA 1 SEM (MHNG-PLAT-0035546), all from
Stone Co., Mississippi, 15 May 2000, Vasyl V. Tkach (¼VVT); 1
specimen from host USA 26, Jackson Co., Mississippi, May 2001,
VVT (MHNG-PLAT-0063344); 6 specimens from hosts USA 47–52,
Biloxi, Harrison Co., Mississippi, 4 September 1997, Robin M.
Overstreet (MHNG-PLAT-0069445–069450); 2 specimens and
cross sections from host US 957, Butcherknife Creek, Polk
Co., Arkansas, 17 August 2019, Chris T. McAllister (¼CTM)
(IPCAS C-930; USNM 1690934); 1 specimen and cross sections
from host US 1119, Hochatown, McCurtain Co., Oklahoma, 1 May
2021, CTM (HWML-216961, IPCAS C-930, MHNG-PLAT-0150171,
USNM 1690932); 1 specimen and cross sections (scolex and pro-
glottids) from host US 1121, Polk Co., Ouachita Mountains Bio-
logical Station, Arkansas, 23 June 2021, CTM (HWML-216963,
IPCAS C-930, MHNG-PLAT-0150175, USNM 1690931); 1 specimen
and cross sections from host US 1122b, Polk Co., Ouachita Mountains
Biological Station, Arkansas, 22 June 2021, CTM (IPCAS C-930,
MHNG-PLAT-0150178); 1 specimen from host US 1123a, Polk Co.,
Ouachita Mountains Biological Station, Arkansas, 27 June 2021, CTM
(IPCAS C-930, MHNG-PLAT-0150181); 1 specimen and cross sec-
tions from host US 1123b, Polk Co., Ouachita Mountains Biologi-
cal Station, Arkansas, 27 June 2021, CTM (HWML-216964, IPCAS
C-930, MHNG-PLAT-0150181, USNM 1690930); 1 specimen in
vial from host US 1123c, Polk Co., Ouachita Mountains Biological
Station, Arkansas, 27 June 2021, CTM; 1 specimen and eggs from
host US 1124, Polk Co., Ouachita Mountains Biological Station,
Arkansas, 27 June 2021, CTM (IPCAS C-930, MHNG-PLAT-
0150183); 1 specimen in vial from host US 1125, Hochatown,
McCurtain Co., Oklahoma, 5 September 2020, CTM; specimens
from McCurtain Co., Lukfata, Oklahoma, 8 October 2014, CTM
(HWML-101840); specimens from Calhoun Co., Locust Bayou,
Arkansas, 22 April 2016, CTM (HWML-110878) (all samples from
A. piscivorus); fragments of 1 or more specimens from Sistrurus
SCHOLZ ET AL.—TAPEWORMS OF NORTHERN COTTONMOUTH 465
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Table I. Measurements of proteocephalid tapeworms from the northern cottonmouth, Agkistrodon piscivorus (Lace
´pe
`de, 1789) (Viperidae) in the United States. Measurements taken by the
present authors from illustrations in La Rue (1914) and Brooks (1978) in brackets; mean and number of measurements in parentheses.
Species
Ophiotaenia marenzelleri
(Barrois, 1898)
Ophiotaenia marenzelleri
(Barrois, 1898)
Ophiotaenia ‘grandis’
La Rue, 1911 (¼mixture
of 2 species; see the text)
Ophiotaenia ‘grandis’
La Rue, 1911 (¼mixture
of 2 species; see the text)
Ophiotaenia agkistrodontis
Harwood, 1933 (¼new
synonym of O. grandis)
Ophiotaenia agkistrodontis
Harwood, 1933 (¼new
synonym of O. grandis)
Ophiotaenia sp.
(“small scolex”)
Reference Barrois (1898), Schwarz
(1908), Woodland (1925)
This study La Rue (1911, 1914) This study (observations
of holotype)
Harwood (1933) This study This study
Host field code A. piscivorus A. piscivorus USA 1, US
956, 957, 1120–1123
A. piscivorus A. piscivorus A. piscivorus A. piscivorus US 957, 1120,
1122, 1124
A. piscivorus US 953
State Southern United States Arkansas, Mississippi,
Oklahoma, Texas
National Zoo,
Washington, D.C.
National Zoo,
Washington, D.C.
Texas Arkansas, Oklahoma Oklahoma
Collector Calmette V. V. Tkach, C. T.
McAllister
S. S. Shawhan S. S. Shawhan P. D. Harwood V. V. Tkach, C. T.
McAllister
C. T. McAllister
Date of collection 22 December 1897 2000–2021 18 November 1907 18 November 1907 4 May 1932 2000–2021 23 June 2019
Specimens deposited None MHNG-PLAT, IPCAS
C-9
USNM 1323355 USNM 1323355 USNM 1321332 MHNG-PLAT, IPCAS MHNG-PLAT-0130136
Total length (mm) 350–400 Up to 535 300–400 ? [193] 129–143 215
Maximum width (mm) 1.2–3.1 3.04 2.72–4.25 4.255 0.9 0.84 0.89
Scolex length*
1
N/A 920–930 [670] 500–890 550–650 380–450 88
Scolex width 1,600–2,000 1,410–1,760 1,000–1,200 815–1,170 850–950 540–700 215
Sucker width 600–913 640–820 340–360 350–395 250–300 210–290 85–90
Sucker diameter/scolex width
ratio
N/A 48–57% (51%; 7) [30–33%] 31–41% 26–35% 36–43% (39%; 9) 39–41%
Testis number (mean; n) 150–240 215–298 200–250 240–277 (258; 3) 90–110 90–150 (117; 16) 169–247 (190; 5)
Testis size 60–70 60–90 N/A 75–125 340–50 35–75 35–55 35–55 330–50
No. of testis fields 2 2 2 2 2 2 2
Cirrus sac—relative length*
2
25–33% 26–34% 20–33% 23–34% (29%;4) 26–34% (29%; 4) 25–32% (29%; 26) 17–23% (21%; 10)
Genital pore—position*
3
About 50% [41%] 47–56% Near middle 51–54% 20–25% 25–35% 27–35% (30%; 9)
Ovary—relative width*
4
[61%] 57–72% 53% 53–58% [78%] 62–72% (68%; 25) 76–82% (78%; 8)
Ovary—surface ratio*
5
[5.7%] 4.0–6.1% [2.7%] 2.3–3.0% [5.4%] 3.4–5.7% 4.8%
Ovary—relative length*
6
[15–16%] 8.7–12.1% [8.3–9.7%] 8.1–9.8% [10.1–11.9%] 8.7–12.5% 7.2–12.5%
Mehlis’ gland – width N/A 100–130 N/A 105–155 N/A 60–120 55–80
Mehlis’ gland – relative size*
7
N/A 4.1–7.2% N/A 5.7–6.7% N/A 7.7–14% (10.6%; 23) 7.1–11.5% (8.7%; 7)
Vagina—position to cirrus sac Anterior-posterior Anterior-posterior Anterior-posterior Anterior-posterior Anterior-posterior Anterior-posterior Anterior-posterior
Vaginal sphincter N/A Present Present Present N/A Present Present
Aporal vitelline follicles—
relative length*
8
[93%] 86–94% [83–93%] 91–95% [84%] 84–94% 86–94%
Poral vitelline follicles—
relative length*
9
[94%] 91–94% [88–92%] 90–95% [85%] 82–94% 88–93%
Uterine diverticula on each
side
20–30 40–59 40–60 28–45 25–30 30–38 22–32
Embryophore diameter 22 45–55 327–30 26–37*
10
N/A N/A 22–25 26–33
Oncosphere diameter 11 15–16 15–16*
10
N/A N/A 14–17 13–14
Type of uterus formation*
11
[1] 1 N/A 1 N/A 2 2
* According to de Chambrier et al. (2021, see their Table 1);
1
distance from the anterior extremity to the posterior margin of the suckers;
2
cirrus sac length to proglottid width ratio;
3
relative
position of the genital pore to the proglottid length;
4
ovary width to proglottid width ratio;
5
ovary surface area to proglottid area ratio (see de Chambrier et al., 2012);
6
ovary length to proglottid
length ratio;
7
width of Mehlis’ gland to proglottid width ratio;
8,9
length of bands of vitelline follicles to proglottid length ratio on the aporal and poral sides, respectively;
10
measured in whole
mounts;
11
see de Chambrier et al. (2004) for type of uterine development; N/A—not available.
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Table II. Species of Ophiotaenia La Rue, 1911, from semi-aquatic snakes worldwide. Measurements taken in this study in parentheses.
Parasite Host Country Total length Scolex width
Testis
number
Relative
length
of cirrus-sac Gonopore
Vagina—
position
Vaginal
sphincter
Uterine
diverticula
Apical
organ
Relative size
of ovary
Embryophore
—diameter
Embryophore
—layers
Uterine
type
Ophiotaenia
agkistrodontis
(Harwood, 1933)
(¼new synonym
of O. grandis; see
the text)
Agkistrodon
piscivorus
United States 193 mm
(129–143 mm)
850–950
(540–700)
90–110
(90–150)
20–25%
(25–32%)
20–25%
(25–35%)
Ant-post Present 25–30
(30–38)
No 4.5–6.3%
(3.4–5.7%)
(22–25) ? 2
Ophiotaenia arandasi
Santos and Rolas,
1973
Liophis miliaris Brazil 80 mm 390 70 41–42% 35–45% Ant-post ? Env. 60 No 5.1% ? ? 2
Ophiotaenia europaea
Odening, 1963
Natrix natrix Germany 280–540 mm 222–313 189–344 25–43% 33–66% Post Absent 28–73 No (?) 12.7% 18–22 ? 2
Ophiotaenia faranciae
(MacCallum, 1921)
Farancia
abacura
United States .180 mm 500 390–420 25% (?) 16–25% Post ? 30–50 Yes 2.1% ? ? ?
Ophiotaenia gilberti
Ammann and de
Chambrier, 2008
Thamnodynastes
pallidus
Paraguay 60–120 mm 140–145 57–91 15–23% 42–50% Ant-post Present 28–41 Yes 3.7% 27–28 Bi-layered 1
Ophiotaenia ‘grandis’
La Rue, 1911
(mixture of
2 species; see
the text)
Agkistrodon
piscivorus
United States 300–400 mm 1,000–1,200 200–250 20–33% 50% (?) Ant-post Present 40–60 No 2.1% 21–23 Bi–layered ?
Ophiotaenia habanensis
Freze and Rysavy,
1976
Tropidophis
pardalis
Cuba 57–67 mm 360 31–51 .50% 60% Post Present 26–33 No 2.7% 22–28 ? ?
Ophiotaenia hyalina
Rudin, 1917
Coluber’ sp.
(¼Liophis
sp.)
Brazil 120 mm 680–800 50–55 50% 33% (?) Ant-post Present ? No 5.5% ? ? 2
Ophiotaenia japonensis
Yamaguti, 1935
Rhabdophis
tigrinum
Japan 400 mm 330–500 90–130 ?25% 50% Ant-post Present (?) 20–30 No (?) 1.9% 39 ? ?
Ophiotaenia marenzelleri
(Barrois, 1898)
Agkistrodon
piscivorus
United States 400 mm (up to
535 mm)
1.2–2.0 mm
(1.41–1.76
mm)
150–240
(215–298)
25–33%
(26–34%)
50%
(47–56%)
Ant
(ant-post)
(Present) 20–30
(40–59)
Yes 2.6%
(4.0–6.1%)
20 (45–55 3
27–30)
Bi-layered 1
Ophiotaenia
paraguayensis
Rudin, 1917
Hydrodynastes
gigas
Paraguay 550–600 mm 240 238–344 12–19% 27–39% Ant-post Present 20–36 No 3.3% 21–24 ? 2
Ophiotaenia perspicua
La Rue, 1911
Natrix
rhombifer
United States 360 mm
(200 mm)
255–410 150–215 25–33% 33–50% Anterior Present 20–30 Yes 2.3% ? Bi-layered 2
Ophiotaenia
rhabdophidis
(Burt, 1937)
Natrix stolata Sri Lanka 250 mm 130–187 110–140 20–25% 33–50% Ant-post ? 30–45 Yes 3.1% 22–27 ? ?
Ophiotaenia
sanbernardinensis
Rudin, 1917
Helicops
leopardinus
Paraguay 100–120 mm 230–250 70–102 ? 20–40% Ant-post Present 27–33 No 5.0% 22–23 ? 2
Ophiotaenia sinensis
Cheng and Lin,
2002
Rhabdophis
tigrina
lateralis
China 460–694 mm 247–325 256–320 25% 45% ? ? ? ? 2.5% ? ? 1 (?)
Ophiotaenia spasskii
Freze and
Sharpilo, 1965
Vipera berus Russia 70–90 mm 295–355 179–271 20–25% 30% Ant-post Present 19–31 ? 9.1% ? ? ?
Ophiotaenia tessellata
Gamil and Fouad,
2022
Natrix tessellata Egypt 230–550 mm 280–320 65–135 21–33% 41–51% Ant-post Present 18–30 No 4.1% 29–33 Bi-layered 1
Ophiotaenia variabilis
(Brooks, 1978)
Natrix cyclopion United States 300 mm 170–200 77–253 22–33% 15–30% Ant-post absent 25–45 No 2.8% 30–40 ? 2 (?)
SCHOLZ ET AL.—TAPEWORMS OF NORTHERN COTTONMOUTH 467
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miliarius (Linnaeus), National Zoological Garden, Washington,
D.C. (USNM 1332621); Ophiotaenia ‘grandis’ (likely O. maren-
zelleri)exA. piscivorus, Biloxi, Mississippi, 4 September 1997,
sequenced by Zehnder and Mariaux (1999) and Hyps
ˇa et al.
(2005).
Redescription (based on 9 specimens from USNM 1373420,
1373421, USA 01, US 957, 1119, 1121, 1122; composite measure-
ments of Barrois (1898), Schwarz (1908), Woodland (1925), and
Brooks (1978) in brackets; Table I): Proteocephalidae. Very
large worms, up to 535 mm long [400 mm], up to 4.25 mm wide
Figure 1. Scolices of species of Ophiotaenia La Rue, 1911, from Agkistrodon piscivorus (Lace
´pe
`de, 1789) in the United States. (A–C)Ophiotaenia
marenzelleri (Barrois, 1898), Arkansas (host US 957), Louisiana (USNM 1380488), and Arkansas (US 1121); (D)Ophiotaenia agkistrodontis
(Harwood, 1933) (¼new synonym of O. grandis), Texas, holotype (USNM 1321332); (E–G)Ophiotaenia grandis La Rue, 1911, syntypes (USNM
1323355); (H–L)O. grandis, Oklahoma (US 956) and Arkansas (US 957); (M, N)Ophiotaenia sp., Arkansas (US 1122) and Oklahoma (US 953).
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[1.60–3.07 mm], flattened dorsoventrally, mature proglottids longer
than wide, up to 4.45 mm [5.75 mm] long. Immature proglottids
wider than long to longer than wide (length: width ratio 0.23–1.69);
mature proglottids longer than wide (length: width ratio 1.55–1.74);
pregravid proglottids longer than wide (length: width ratio 1.53–
3.28); gravid proglottids longer than wide (length: width ratio 2.68–
3.64). Tegument thick, 9–15 in thickness.
Scolex large, slightly pedunculate, aspinose, 920–930 long
(measured from anterior extremity to posterior margin of
suckers), 1.41–1.76 mm wide [1.2–2.0 mm], wider than neck, with
4 large uniloculate suckers (Figs. 1A–C, 2A–C), 640–820 [600–
700] in diameter; apical organ small, difficult to see in mounted
specimens, 55–65 long by 75–100 wide (Fig. 1B, C). Neck up to
980 wide; zone posterior to scolex long (up to 18 mm).
Inner longitudinal musculature weakly developed, consisting of
few small bundles of muscle fibers (Fig. 3F–H); transverse mus-
cles well developed, in cortical parenchyma and sometimes reach-
ing margins of proglottid (Fig. 3F). Osmoregulatory canals run
Figure 2. Scanning electron micrographs of scolices of species of Ophiotaenia La Rue, 1911 from Agkistrodon piscivorus (Lace
´pe
`de, 1789) in the
United States. (A–C)Ophiotaenia marenzelleri (Barrois, 1898), Mississippi (host USA 1); (D–F)Ophiotaenia grandis La Rue, 1911, Arkansas (US
1124, US 957), and Mississippi (USA 27); (G–I)Ophiotaenia sp., Arkansas (US 1122).
SCHOLZ ET AL.—TAPEWORMS OF NORTHERN COTTONMOUTH 469
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Figure 3. Proglottids (A–E) and cross sections (F–L) of species of Ophiotaenia La Rue, 1911, from Agkistrodon piscivorus (Lace
´pe
`de, 1789) in the
United States. (A) Mature proglottid of Ophiotaenia marenzelleri (Barrois, 1898), Mississippi (host USA 1), ventrally; (B, C) pregravid and gravid pro-
glottids of Ophiotaenia ‘grandis’ La Rue, 1911 (¼O. marenzelleri), syntypes (USNM 1323355), ventrally and dorsally; most testes and vitelline follicles
not illustrated; (D) mature proglottid of O. grandis, Arkansas (US 1124), dorsally; (E) pregravid proglottid of Ophiotaenia sp., Oklahoma (US 953),
dorsally; (F–H)O. marenzelleri (Barrois, 1898), Mississippi (USA 1), sections at level of ovary (F) and vaginal sphincter (G, H); (I, J)Ophiotaenia sp.,
Oklahoma (US 953), sections at level of testes (I) and ovary (J); (K, L)O. grandis, Arkansas (US 1120); sections at level of testes (K) and ovary (L).
470 THE JOURNAL OF PARASITOLOGY, VOL. 109, NO. 5, OCTOBER 2023
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alongside testicular fields, slightly dividing them, situated 13–19% of
proglottid width from lateral margins. Ventral canals thin-walled,
10–20 in diameter; dorsal canals thick-walled, 4–5 in diameter,
never reaching vitelline follicles laterally, often median to ventral
canals. Terminal genitalia between osmoregulatory canals.
Testes spherical, 60–90 in diameter [70 long 360 wide], 215–
298 in number (x¼256, n ¼8) [230–240], in 1 layer, in 2 lateral
fields on both sides of uterine stem (Fig. 3A). Anteriorly, testes
reaching almost anterior margin of proglottids; posteriorly, testes
not reaching posterior margin of proglottids, but reaching to
ovary posteriorly and laterally (Fig. 3A). Vas deferens strongly
coiled, reaching mid-line of proglottid, without overlapping it,
occupying small elongated area (Figs. 3A, 4A). Cirrus sac mas-
sive, oval to pyriform, thick-walled, 500–860 [448–680] long, i.e.,
26–34% (x¼28%, n ¼10) of proglottid width, 160–260 wide
(Figs. 3A, 4A). Cirrus robust, especially in distal end, occupies
72–91% of length of cirrus sac (Fig. 4A). Genital atrium deep;
genital pores irregularly alternating, equatorial, situated at 47–56%
(x¼49%, n ¼8) [“near the middle of segment margin”] of pro-
glottid length (Fig. 3A).
Ovary bilobed, 1,140–1,700 wide, occupying 57–72% (x¼
66%, n ¼10) of proglottid width (Fig. 3A–C); relative size of
ovary, i.e., ratio of surface of ovary to surface of proglottid (see
de Chambrier et al., 2012) 4.0–6.1% [5.7%; taken from Fig. 12 in
Schwarz (1908)]. Ovary length represents 8.7–12.1% of proglottid
length. Vagina anterior (32% of proglottids counted) or posterior
(68%, n ¼100) to cirrus sac, with powerful vaginal sphincter,
150–200 in diameter and 75–150 thick/wide, vaginal canal lined
with layer of stained cells in its terminal (distal) part (Fig. 4A).
Mehlis’ gland 100–130 in diameter, representing 4.1–7.2% (x¼
5.6%, n ¼7) of proglottid width.
Vitelline follicles small, spherical to oval, arranged in 2 lateral,
longitudinal bands (Fig. 3A), interrupted at level of terminal geni-
talia (cirrus sac and vagina; Fig. 4A). Follicles not reaching ante-
rior or posterior margin of proglottids, with bands occupying 91–
94% and 86–94% of proglottid length on poral and aporal sides,
respectively (Fig. 3A). Vitelline follicles do not overlap ovarian
lobes laterally.
Primordium of uterine stem ventral. Formation of uterus of
type 1 of de Chambrier et al. (2004), with uterine diverticula
formed before appearance of first eggs in uterus (uterine stem pre-
sent as a tube with thin wall and lumen), occupying about 5–6%
of proglottid width in mature proglottids. In pregravid proglottids,
diverticula occupy up to 6–32% of proglottid width. In gravid pro-
glottids, diverticula occupy up to 74% of proglottid width. Number
of lateral branches (diverticula) variable, depending on shape
Figure 4. Terminal genitalia (cirrus sac and vagina) of species of Ophiotaenia La Rue, 1911, from Agkistrodon piscivorus (Lace
´pe
`de, 1789) in the United
States. (A)Ophiotaenia marenzelleri (Barrois, 1898), Arkansas (host US 1121), ventrally; (B)Ophiotaenia ‘grandis’LaRue,1911(¼O. marenzelleri), syn-
type (USNM 1323355), dorsally; (C)Ophiotaenia agkistrodontis (Harwood, 1933) (¼new synonym of O. grandis), Texas, holotype (USNM 1321332), dor-
sally; (D)O. grandis, Arkansas (US 1124), dorsally; (E)Ophiotaenia sp., Oklahoma (US 953), dorsally.
SCHOLZ ET AL.—TAPEWORMS OF NORTHERN COTTONMOUTH 471
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of proglottids and their development, with only 16–17 diverticula
in early gravid proglottids, but as many as 40–59 [20–30] divertic-
ula on each side in last proglottids. Eggs large, formed by outer
hyaline envelope of nearly cubic shape (Fig. 5A–E), about 200 3
170, with elongate oval tri-layered embryophore 45–55 327–30
[20] possessing 2 polar button-shaped structures (Fig. 5A–E), and
oncospheres 15–16 [11] in diameter with 3 pairs of embryonic
hooks about 6–8 long (Fig. 5D, E).
Taxonomic summary
Type host: Northern cottonmouth, Agkistrodon piscivorus
(Lace
´pe
`de, 1789) (Viperidae: Crotalinae).
Possible additional host: Pygmy rattlesnake, Sistrurus miliarius (Lin-
naeus, 1766) (Viperidae: Crotalinae) (not verified by molecular data).
Type locality: Not specified (host reported to be “propre a
`la
partie me
´ridionale des Etats-Unis.”).
Distribution: USA (Alabama, Arkansas—new geographical record,
California, Louisiana, North Carolina, Oklahoma, Texas); record
from unknown locality in the Catskill Mountains, New York (Fan-
tham and Porter, 1954) is doubtful because A. piscivorus does not
occur in this state (Uetz et al., 2022).
Records: Barrois (1898), Schwarz (1908), Beddard (1913),
Woodland (1925), Harwood (1933), Fantham and Porter (1954),
Collins (1969), Brooks (1978), Detterline et al. (1984), Fontenot
and Font (1996), McAllister et al. (2015), present study.
Figure 5. Eggs of species of Ophiotaenia La Rue, 1911, from Agkistrodon piscivorus (Lace
´pe
`de, 1789) in the United States. (A–C) microphotographs
of eggs of Ophiotaenia marenzelleri (Barrois, 1898) from Arkansas (US 1124, US 1122) and Oklahoma (US 1119); (D, E) line drawings of eggs of
O. marenzelleri, Arkansas (US 1122); (F, J)Ophiotaenia sp., Oklahoma (US 953); (G–I)Ophiotaenia grandis La Rue, 1911, Arkansas (US 1122).
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Type material: Does not exist.
Prevalence and intensity of infection: 15 of 18 cottonmouths
examined by the present authors were infected, i.e., prevalence
83%; intensity of infection 1–3 (x¼1.4; n ¼15).
Representative DNA sequences and phylogenetic relation-
ships: Zehnder and Mariaux (1999) and Hyps
ˇa et al. (2005) pub-
lished sequences of tapeworms found in A. piscivorus from Biloxi,
Mississippi,collectedbyR.M.Overstreeton4September1997,that
were identified as O. grandis: sequence accession nos. AY551164
(ITS2), AY551128 (V4-18S rDNA), AJ389514 (16S rDNA), and
AJ388632 (28S rDNA). However, an examination of morphological
vouchers has shown that O. marenzelleri has been misidentified as O.
grandis. In phylogenetic analyses, O. marenzelleri is clustered with
Ophiotaenia species from tropical snakes (Zehnder and Mariaux,
1999; de Chambrier et al., 2004), i.e., in the “terrestrial” clade of
Hyps
ˇa et al. (2005) or clade K of de Chambrier et al. (2015). Mem-
bersofthesecladesarelargeandsharetype1uterinedevelopment
according to de Chambrier et al. (2004); most species parasitize
snakes, but only 2, O. gilberti Ammann and de Chambrier, 2008, and
O. tessellata Gamil and Fouad, 2022, were found in colubrids (de
Chambrier et al., 2015; this study).
Remarks
This species is one of the largest known proteocephalids
(total length of more than 50 cm and maximum width .4 mm;
Table I). It was described as Ichthyotaenia marenzelleri by Bar-
rois (1898), who examined tapeworms from Trigonocephalus
piscivorus (¼Agkistrodon piscivorus). The original description
was brief and did not include illustrations, being only a prelimi-
nary note (Barrois, 1898). The author promised to provide a
more detailed description later, but it was never published.
Nevertheless, the species was characterized in more detail by
Schwarz (1908), who studied the original material of Barrois
(1898) and provided 3 illustrations of this species, including a
drawing of the large scolex with the prominent suckers (fig. 11
in Schwarz, 1908).
Beddard (1913) described the morphology of immature tape-
worms (up to 25 cm long) found in an A. piscivorus that died in
the London Zoological Gardens. Woodland (1925) provided fur-
ther data based on a large specimen (total length of about 35 cm)
from a northern cottonmouth that also died in the London Zoo-
logical Gardens. He indicated the presence of a very long strobila
with immature proglottids that were always wider than long,
while the mature proglottids were nearly square, and pregravid
and gravid proglottids that were wider than long and longer than
wide (length to width ratio 0.59–1.88). Later Harwood (1933)
found 10 specimens of O. marenzelleri in a single northern cotton-
mouth that also harbored O. agkistrodontis, which he described
as a new species (see below), but refrained from a morphological
description of these tapeworms because they corresponded well
with those described by earlier authors.
We also add some new measurements of O. marenzelleri,
such as the relative size of the Mehlis’ gland and ovary and the
size and morphology of the eggs (Table I). Frontal sections of
the scolex also confirmed the presence of a small apical organ
that is difficult to observe in stained specimens because of the
size of the scolex and has not been described by previous
authors, except for Brooks (1978), who illustrated this organ in
his Fig. 35. One of the most remarkable features of O. maren-
zelleri is the morphology of its eggs, which are unique among
proteocephalid tapeworms with their nearly cubic shape of the
outer (hyaline) envelope and the oval shape of the embryo
phore (Fig. 5A–E). Molecular data suggest that O. marenzelleri
(as O. grandis—Zehnder and Mariaux, 1999; Hyps
ˇa et al.,
2005) should be placed in a different genus, together with
Ophiotaenia species from snakes forming clade K of de Chamb-
rier et al. (2015).
Ophiotaenia grandis La Rue, 1911
(Figs. 1–5)
New synonyms: Ophiotaenia marenzelleri (Barrois, 1898) La Rue,
1911 (in partim—see below); Proteocephalus agkistrodontis Har-
wood, 1933; Ophiotaenia ancistrodontis Harwood, 1933, in Freze
(1965); Ophiotaenia agkistrodontis (Harwood, 1933) Freze, 1965.
Material studied: Syntypes of O. grandis—17 slides with anterior
parts with 4 scolices and immature proglottids (¼‘true’ O. grandis)
and numerous fragments of strobilae with wide pregravid and
gravid proglottids (¼O. marenzelleri), National Zoological Park,
Washington, D.C. (USNM 1323355); 4 wide immature proglottids
of O. grandis (¼O. marenzelleri), New Orleans, Louisiana, col-
lected on 24 January 1916 by P. Viosca (given name not known;
USNM 1348628); 2 specimens of O. grandis (¼O. marenzelleri)
with scolices 1.58 and 1.77 mm wide, suckers 660–720 lm and 770–
780 lm wide, and apical organ 150 lm long by 100 lmwide,San
Diego, California, March 1963, L. F. Conti (given name not
known; USNM 1343215); holotype of O. agkistrodontis (¼O. gran-
dis), 1 complete specimen on 7 slides, Houston, Harris Co., Texas,
4 May 1932, Paul D. Harwood (USNM 1321332); 1 specimen iden-
tified as O. agkistrodontis (¼O. grandis), Head of Island, Living-
stone Parish, Louisiana, September 1989, Lance W. Fontenot
(USNM 1380488); 1 specimen from host USA 1, Stone Co., Missis-
sippi, 15 May 2000, VVT (MHNG-PLAT-0035542); 1 specimen
and 1 scolex for SEM studies from host USA 27, Jackson Co., Mis-
sissippi, May 2001, VVT (MHNG-PLAT-0063345); 2 specimens
and cross sections from host US 956, McCurtain Co., off US 259
and US 259a road junction, Oklahoma, 17 August 2019, CTM
(IPCAS C-931, MHNG-PLAT-0130135, USNM 1690937); 4 speci-
mens and cross sections from host US 957, Butcherknife Creek,
Polk Co., Arkansas, 17 August 2019, CTM (IPCAS C-931;
MHNG-PLAT-0130133; USNM 1690933); 1 specimen and cross
sections (scolex and proglottids) from host US 1120, Polk Co.,
Ouachita Mountains Biological Station, Arkansas, 24 May 2021,
CTM (HWML-216962; IPCAS C-931, MHNG-PLAT-0150174, USNM
1690936); 1 specimen and 21 cross sections from host US 1122a, Polk
Co., Ouachita Mountains Biological Station, Arkansas, 22 June 2021,
CTM (IPCAS C-931; MHNG-PLAT-0150180); 2 specimens and
eggs from host US 1124, Polk Co., Ouachita Mountains Biological
Station, Arkansas, 27 June 2021, CTM (IPCAS C-931; MHNG-
PLAT-0150185; USNM 1690935) (all samples from A. piscivorus);
1 specimen identified as O. marenzelleri from Sistrurus miliarius, National
Zoological Garden, Washington, D.C. (USNM 1332621), with scolex
815 mm wide and suckers 340 mm in diameter (¼O. grandis).
Redescription (based on 9 specimens from hosts nos. USA 1, 27,
US 956, 957, 1120, 1122, 1124—see above; measurements of
Harwood (1933) in brackets; Table I): Proteocephalidae. Large,
slender worms, 129–143 mm [193 mm] long, up to 0.84 mm
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[0.90 mm] wide, flattened dorsoventrally, with proglottids quad-
rate to elongated.
Immature proglottids wider than long to longer than wide
(length: width ratio 0.32–2.54); mature proglottids longer than
wide (length: width ratio 1.85–3.41); pregravid proglottids longer
than wide (length: width ratio 2.34–5.96); gravid proglottids lon-
ger than wide (length: width ratio 2.71–4.46). Tegument thick, 5–
8 in thickness.
Scolex rounded to pyramidal, aspinose (Figs. 1D–L, 2D–F),
380–450 long [550-650] (measured from anterior extremity to pos-
terior margin of suckers), 540–700 wide [850–950], narrower than
neck, with 4 uniloculate, elongated suckers (Fig. 2D–F), 210–290
[250–300] in diameter; apical organ absent (Fig. 1D–L). Neck up
to 645 wide; unsegmented zone posterior to scolex to first recog-
nizable proglottids long (up to 18 mm).
Inner longitudinal musculature weakly developed, consisting of
few small bundles of muscle fibers (Fig. 3K, L). Osmoregulatory
canals run alongside lateral testes fields, slightly dividing them,
situated 18–31% of proglottid width from lateral margins (Fig.
3D). Ventral canals thin-walled, 15–20 in diameter; dorsal canals
thick-walled, about 4–5 in diameter, never reaching vitelline folli-
cle level.
Testes spherical, 35–55 [35–75] in diameter, 90–150 (x¼117, n ¼
16) [90–100] in number, in 1 layer, in 2 lateral fields on both sides
of uterine stem (Fig. 3D). Vas deferens strongly coiled, reaching
mid-line of proglottid (Fig. 3D), sometimes slightly overlapping it.
Cirrus sac pyriform, thick-walled, 160–230 long, i.e., 25–32%
(x¼29%, n ¼26) of proglottid width, 60–90 wide (Figs. 3D, 4C,
D). Genital atrium shallow; genital pores irregularly alternating,
pre-equatorial, situated at 25–35% (x¼29%, n ¼25) [21–25%] of
proglottid length (Fig. 3D).
Ovary bilobed, 355–555 wide, occupying 62–72% (x¼68%, n ¼
25) [73–78%] of proglottid width (Fig. 3D); relative size of ovary,
i.e., ratio of surface of ovary to surface of proglottid (see de Chamb-
rier et al., 2012), 3.4–5.7% [4.5–6.3%]. Ovary length represents 8.7–
12.5% [10.1–11.9%] of proglottid length. Vagina anterior (25% of
proglottids examined) or posterior (75%, n ¼51) to cirrus sac, with
ring-like vaginal sphincter 15–35 in diameter and 30–40 thick/wide
(Fig. 4C, D), lined with layer of intensely stained cells in its terminal
(distal) part (Fig. 4D). Mehlis’ gland 60–120 in diameter, represent-
ing 7.7–14% (x¼10.6%, n ¼23)ofproglottidwidth.
Vitelline follicles spherical to oval, arranged in 2 lateral, longitu-
dinal columns on lateral side of proglottid (Fig. 3D), interrupted at
level of terminal genitalia (cirrus sac and vagina; Fig. 4C, D). Folli-
cles not reaching anterior or posterior margin of proglottids, with
bands occupying 82–94% and 84–94% of proglottid length on
poral and aporal sides, respectively (Fig. 3D). Vitelline follicles
sometimes overlap lateral margin of ovary.
Primordium of uterine stem ventral, consists of diffuse cells,
with 30–28 [25–30] lateral branches (diverticula) on each side.
Formation of uterus of type 2 of de Chambrier et al. (2004), with
uterine diverticula formed after appearance of first eggs in uterus,
occupying about 25% of proglottid width in mature proglottids.
In pregravid proglottids, diverticula occupy up to 30% of proglottid
width. In gravid proglottids, diverticula occupy up to 60% of pro-
glottid width. Uterus does not reach anterior or posterior part of
proglottids and does not cross ovarian isthmus. Uterine pores rarely
present, more often present as a full-length ventral aperture.
Eggs (measured in distilled water; Fig. 5G–I) with outer enve-
lope 65–90 in diameter, bilayered embryophore 29–32 in diameter
and oncospheres 15–17 in diameter, with 3 pairs of embryonic
hooks about 6–8 long (Fig. 5G–I).
Taxonomic summary
Type host: Northern cottonmouth, Agkistrodon piscivorus (Lace
´-
pe
`de, 1789) (Viperidae: Crotalinae) (as Ancistrodon piscivorus).
Additional host: Pygmy rattlesnake, Sistrurus miliarius (Linnaeus,
1766) (Viperidae: Crotalinae) (not verified by molecular data).
Type locality: Not specified (host was kept in the National
Zoological Park, Washington, D.C.).
Distribution: United States (Alabama, Arkansas—new geographi-
cal record, Florida, Louisiana, Mississippi—new geographical record,
Oklahoma, and Texas).
Records: La Rue (1911, 1914—in part as O. grandis), Harwood
(1932, 1933), Roberts (1956), Brooks (1978), Detterline et al.
(1984), Fontenot and Font (1996), Ernst and Ernst (2006).
Type material: USNM 1321332 (holotype); no paratypes were
deposited.
Prevalence and intensity of infection: Ophiotaenia grandis was
found in 8 of 18 cottonmouths examined, i.e., with prevalence
44%; intensity of infection 1–6 (x¼3.7; n ¼9).
Representative DNA sequences and phylogenetic relationships: No
molecular data are available because sequences published by
Zehnder and Mariaux (1999—AJ389514, AJ388632) and Hyps
ˇa
et al. (2005—AY551164, AY551128) were those of O. marenzelleri;
see above.
Remarks
The species was originally described by La Rue (1911) but was
not morphologically characterized until 3 yr later (La Rue, 1914).
The morphological description of O. grandis was based on
numerous fragments: “Six or 8 heads together with numerous
pieces in a bottle bearing the U. S. Bureau of Animal Industry
number 14854 were labeled ‘Ichthyotaenia: host Ancistrodon
piscivorous; location, intestine; locality Nat. Zoo. Park, collected
S. S. Shawhan. Nov. 18, 1907.’” La Rue (1914) distinguished the
new species from O. marenzelleri by the alleged possession of a
smaller head (width 1.0–1.2 vs. 1.5–2.0 mm in the latter species),
smaller suckers (diameter 340–360 vs. 600–700 lm), larger pro-
glottids (length up to 8 mm in O. grandis), greater width (4.25 vs.
2.0 mm), more testes (200–250 vs. 150–240), and more uterine
diverticula (40–60 vs. 20–25).
Examination of all type specimens (syntypes) of O. grandis
(USNM 1323355) on 17 slides revealed that La Rue (1911, 1914)
confused 2 different species. Five slides contain fragments of 4
tapeworms with scolices and undifferentiated strobilae, including
some immature proglottids with distinct pre-equatorial gonopores
(normally in the anterior third of the proglottid). In the specimen
with scolex illustrated by La Rue (1914; his Fig. 38), the first recog-
nizable gonopores are on 28–31% (n ¼3) of the proglottid length.
In another syntype with scolex, the gonopores are located on 27–
33% (x¼30%; n ¼6), which corresponds to the position of the
gonopores in O. agkistrodontis (see below and Table I).
All 4 scolices of the syntypes of O. grandis are partially
deformed, with the posterior part and the neck region unnaturally
inflated, as reported by La Rue (1914). The width of these scolices
is 815, 877, 900, and 1,170 mm, respectively, which agrees well
with the width of the scolex of the holotype of O. agkistrodontis
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(830 mm). These scolices also bear small suckers (diameter 350–
395 mm), which are much smaller than those of O. marenzelleri
(compare Figs. 1D–L and 1A–C, 2A–C). One syntype consists of
10 immature, deformed proglottids with testicular primordia that
are difficult to count (ca. 109 in the last proglottid). In another
early immature proglottid, 96–137 testes could be counted, i.e., a
similar number as in the holotype of O. agkistrodontis (86–117
testes; x¼103, n ¼9) and in the new material (90–150 testes; x¼
117; n ¼16). Gonopores are located on 22–46% of the proglottid
length in immature proglottids (x¼35%; n ¼19). Based on the
information summarized above, it is evident that these syntypes
of O. grandis do indeed belong to O. agkistrodontis.
The 10 slides with the remaining syntypes of O. grandis consist
of 1 slide with immature proglottids and 9 slides with gravid pro-
glottids up to 4.25 mm wide; no mature proglottids are present.
These proglottids have approximately equatorially located gono-
pores (x¼51%; range 42–62%; n ¼30), contain numerous testes
(236–277; x¼259; n ¼6), a large cirrus sac (585–650 lmlong)
with a massive cirrus, and the vaginal canal surrounded by a large,
annular sphincter (diameter up to 200 mm; thickness/width about
80 lm) near the genital atrium. The size, shape, and internal anat-
omy of these gravid proglottids do not differ from those of O. mar-
enzelleri redescribed above (see Fig. 3A–C; Table I).
Ophiotaenia agkistrodontis (¼O. grandis; new synonym) was
described by Harwood (1933) as Proteocephalus (Ophiotaenia)
agkistrodontis, based on 14 mostly immature specimens from a
northern cottonmouth caught near Houston, Harris Co., Texas, in
May 1932. The original description was relatively detailed, but only 1
mature proglottid was illustrated. The new species was distinguished
from O. marenzelleri and O. grandis (¼mixture of 2 species) by a con-
spicuous pre-equatorial position of the gonopore (at 20–25% of the
proglottid length according to Harwood, 1933). Re-examination of
the holotype of O. agkistrodontis (¼O. grandis) allowed us to illus-
trate the scolex and confirm the pre-equatorial position of the gono-
pores, which are at 21–25% of the proglottid length.
Based on the present study, it can be concluded that La Rue
(1911, 1914) confused 2 different species: large gravid proglottids
belong to O. marenzelleri, whereas scolices with few immature pro-
glottids are indistinguishable from tapeworms later described by
Harwood (1933) as O. agkistrodontis. These tapeworms are consid-
ered as ‘true’ O. grandis and O. agkistrodontis is a junior synonym
of O. grandis based on the priority of the former taxon (Interna-
tional Trust for Zoological Nomenclature, 1999). Both O. maren-
zelleri and O. grandis have weakly developed inner longitudinal
musculature, making their proglottids easily detached. In our expe-
rience, most tapeworms found in a northern cottonmouth are frag-
mented, and it is difficult to find a complete specimen of a species.
Tapeworms identified as O. grandis have been reported from
northern cottonmouths in Oklahoma (Roberts, 1956; McAllister
et al., 2021). They have also been reported from the colubrids
Mississippi green water snake, Nerodia cyclopion (Dume
´ril,
Bibron, and Dume
´ril); Florida green water snake, Nerodia flori-
dana (Goff); northwestern garter snake, Thamnophis ordinoides
(Baird and Girard); and common garter snake, Thamnophis sirta-
lis (Linnaeus) in Florida, Louisiana, Mississippi, Oklahoma,
Texas, and Saskatchewan, Canada (La Rue, 1914; Roberts, 1956;
Brooks, 1978; Ernst and Ernst, 2006). The species affiliation of
these tapeworms remains unclear, and it cannot be ruled out that
at least some species of Ophiotaenia reported from watersnakes
(Colubridae) have been misidentified (see below).
Differential characteristics of O. marenzelleri and O. grandis
are summarized in Table III.
Ophiotaenia sp. (“small scolex”)
(Figs. 1M, N, 2G–I, 3E, I, J, 4E, 5F, J)
Material studied: One complete specimen from host US 953,
Hochatown, McCurtain Co., Oklahoma, 23 June 2019, C. T.
McAllister; 1 immature specimen from host US 1122b, Ouachita
Mountains Biological Station, Polk Co., Arkansas, 22 June 2021,
CTM (MHNG-PLAT-0150178, IPCAS C-930); “Proteocephalus
agkistrodontis,” Spanish Lake, Iberia Parish, Louisiana, 9 Septem-
ber 1989, Lance W. Fontenot (USNM 1380487; scolex 210 lm
wide, sucker diameter 92–93 lm) (all specimens from A. piscivorus).
Morphological description (based on 1 complete specimen from
host US 953; Table I): Proteocephalidae. Long, narrow worms,
215 mm long, up to 890 wide, flattened dorsoventrally, with proglot-
tids elongated, up to 2.6 mm long. Strobila acraspedote, anapolytic,
with about 250 immature proglottids, 6 mature proglottids, 11 pre-
gravid proglottids, about 10 gravid proglottids; in total 277 proglot-
tids in complete specimen (US 953). Immature proglottids wider
than long to longer than wide (length: width ratio 0.36–1.86); mature
proglottids longer than wide (length: width ratio 1.71–1.94); pregra-
vid proglottids longer than wide (length: width ratio 2.30–2.54);
gravid proglottids longer than wide (length: width ratio 3.28–3.34).
Tegument thick, 7–8 in thickness.
Scolex slightly flattened dorsoventrally, 88 long (measured
from anterior extremity to posterior margin of suckers), 215
wide, slightly wider than neck, with 4 uniloculate suckers (Figs.
1M, N, 2G–I), 85–90 in diameter; apical organ absent (Fig. 1M,
N). Neck up to 205 wide; unsegmented zone posterior to scolex
to first recognizable proglottids long (up to 10 mm).
Inner longitudinal musculature well developed, consisting of
numerous small bundles of muscle fibers. Osmoregulatory canals
run alongside lateral testes fields, slightly dividing them, situated
from 23 to 29% of lateral margins (Fig. 3E). Ventral canals thin-
walled, 8–15 in diameter, dorsal canals thick-walled, about 2–4 in
diameter, never reaching to vitelline follicle level (Fig. 3E). Termi-
nal genitalia between osmoregulatory canals.
Testes spherical to oval, 35–55 long, 30–50 wide, 169–247 in
number (x¼190, n ¼5), in 1 layer, in 2 lateral fields on both sides
of uterine stem (Fig. 3E). Testes do reach posterior margin of pro-
glottids, not reaching to ovary posteriorly, reaching anterior mar-
gin of proglottids (Fig. 3E). Vas deferens strongly coiled, reaching
to mid-line of proglottid, sometimes slightly overlapping it, occu-
pying rounded area (Fig. 3E). Cirrus sac pyriform, thin-walled,
145–185 long, i.e., 17–23% (x¼21%, n ¼10) of proglottid width,
75–100 wide (Fig. 3E). Cirrus occupies up to 80% of length of cir-
rus sac (Fig. 4E). Genital atrium shallow; genital pores irregularly
alternating, pre-equatorial, situated at 27–35% (x¼30%, n ¼9)
of proglottid length (Fig. 3E).
Ovary bilobed, 505–640 wide, occupying 76–82% (x¼78%,
n¼8) of proglottid width (Fig. 3E); relative size of ovary, i.e.,
ratio of surface of ovary to surface of proglottid (see de Chamb-
rier et al., 2012), 4.8%. Ovary length represents 7.2–12.5% of
proglottid length. Vagina anterior (71%) or posterior (29%, n ¼
34) to cirrus sac, with thin vaginal sphincter 30–50 in diameter
and 40–55 thick/wide, lined with thick layer of intensely stained
cells in its terminal (distal) part (Fig. 4E). Mehlis’ gland 55–80 in
diameter, representing 7.1–11.5% (x¼8.7%, n ¼7) of proglottid
width.
SCHOLZ ET AL.—TAPEWORMS OF NORTHERN COTTONMOUTH 475
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Vitelline follicles spherical to oval, arranged in 2 lateral, longitudi-
nal bands on lateral side of proglottid (Fig. 3E), interrupted at level
of terminal genitalia (cirrus sac and vagina; Figs. 3E, 4E). Follicles
closely approaching, but not reaching, anterior or posterior margin
of proglottids, with bands occupying 88–93% and 86–94% of pro-
glottid length on poral and aporal sides, respectively (Fig. 3E).
Vitelline follicles sometimes overlap ventrally lateral margin of
ovary.
Primordium of uterine stem ventral, with 22–32 lateral branches
(diverticula) on each side (Fig. 3E). Formation of uterus of type 2
of de Chambrier et al. (2004), with uterine diverticula formed
after appearance of first eggs in uterus, occupying about 21% of
proglottid width in mature proglottids. In pregravid proglottids,
diverticula occupy up to 27% of proglottid width. In gravid pro-
glottids, diverticula occupy up to 55% of proglottid width. Eggs
(measured in whole mount slides) with bilayered embryophore
26–33 in diameter and oncospheres 13–14 in diameter, with 3 pairs
of embryonic hooks, 4–6 long (Fig. 5F, J).
Remarks
In 2 of the 18 A. piscivorus examined by the present authors
(prevalence 11%), there were 2 tapeworms (1 immature) that
have a much smaller scolex compared to O. marenzelleri and
O. agkistrodontis (¼O. grandis) (Figs. 1, 2) and differ in other
characteristics as well (Table I and a key below). These tape-
worms resemble those of watersnakes (Nerodia spp.), including
Ophiotaenia perspicua La Rue, 1911, and Ophiotaenia variabilis
(Brooks, 1978). Preliminary molecular data suggest that the tape-
worm of the host US 953 is conspecific with tapeworms of the
plainbelly water snake, Nerodia erythrogaster (Forster, 1771),
the broad-banded water snake, Nerodia fasciata confluens (Blan-
chard, 1923), and the northern water snake, Nerodia sipedon
(Linnaeus, 1758) (O. Kudlai, unpubl. data). In the present
paper, the ‘small scolex’ tapeworms found in A. piscivorus are
morphologically characterized, but their systematic status will
be addressed in another paper focusing on proteocephalids par-
asitizing watersnakes (Colubridae) in North America, which is
in preparation.
Key to the identification of species of Ophiotaenia from
Agkistrodon piscivorus
1 (2) Large worms, .1 mm wide (usually about 3 mm);
scolex massive, large (width 1.4–2.0 mm), with large
suckers (.600 lm in diameter); vaginal sphincter
large, diameter .150 lm); genital pore equatorial;
eggs large, formed by outer hyaline envelope of
nearly cubic shape, with elongate-oval trilayered
embryophore ......................................... O. marenzelleri
2 (1) Slender worms, ,1 mm wide; scolex smaller (,1
mm), with smaller suckers (width ,300 lm); eggs of
‘typical’ shape, i.e., spherical, including spherical
bilayered embryophore (Fig. 5); vaginal sphincter
smaller (diameter ,55 lm); genital pore pre-equato-
rial .............................................................................. 3
3 (4) Scolex larger, .500 lm wide, bearing larger suck-
ers (width .200 lm); fewer testes (,150 per pro-
glottid) ........... O. grandis (new syn. O. agkistrodontis)
4 (3) Scolex smaller, ,220 lm wide, bearing smaller suck-
ers (width ,100 lm); more testes (.150, usually
about 200) ....................... Ophiotaenia sp. (‘small scolex’)
DISCUSSION
Agkistrodon Palisot de Beauvois, 1799, is a genus of venom-
ous pit vipers commonly known as American moccasins
(Crother, 2017). The genus is endemic to North and Central
America, ranging from the southern United States to northern
Costa Rica (McDiarmid et al., 1999). Eight species of Agkistrodon
are currently recognized (Burbrink and Guiher, 2014), but flat-
worms (tapeworms and trematodes) and acanthocephalans were
reported only from the northern cottonmouth (Detterline et al.,
1984; Gibson et al., 2005).
The following helminths have been found in A. piscivorus:
the acanthocephalan Macracanthorhynchus ingens (Linstow,
1879); the nematodes Cosmocercoides dukae (Holl, 1928), Kali-
cephalus rectiphilus Harwood, 1932, and Terranova caballeroi
Barus and Coy Otero, 1966; and the trematodes Alaria marcia-
nae (La Rue, 1917), Dasymetra villicaeca Byrd, 1935, Neodi-
plostomum cratera (Barker and Noll, 1915), Renifer laterotrema
Byrd and Denton, 1938, and Styphlodora magna Byrd and
Denton, 1938 (Collins, 1969; Rabalais, 1969; Detterline et al.,
1984; Fontenot and Font, 1996; Gibson et al., 2005; Ernst and
Ernst, 2006; Davis et al., 2016; McAllister et al., 2020, 2021).
The present study has shown that only 2 and not 3 species of
Ophiotaenia are typical, most probably specific parasites of
northern cottonmouth. They often occur simultaneously and
differ markedly in size and other morphological characters
Table III. Differential characteristics of Ophiotaenia marenzelleri (Barrois, 1898) and Ophiotaenia grandis La Rue, 1911, parasites of the northern
cottonmouth, Agkistrodon piscivorus (Lace
´pe
`de, 1789), based on the present study.
Characteristic Ophiotaenia marenzelleri Ophiotaenia grandis (new syn. O. agkistrodontis)
Total length Up to 54 cm ,20 cm
Maximum width 4.3 mm 0.9 mm
Width of scolex .1.4 mm ,1.0 mm
Apical organ Present Absent
Diameter of suckers 0.64–0.82 mm 0.21–0.30 mm
Number of testes 215–298 90–150
Length of cirrus sac 500–860 mm 160–230 mm [Harwood, 1935: 230–270 mm]
Position of gonopore Equatorial (47–56% of proglottid length) Pre-equatorial (25–35% of proglottid length)
Diameter of vaginal sphincter 160–205 mm 30–40 mm
No. of layers of embryophore 3 2
Uterine development (see de Chambrier et al., 2004) Type 1 Type 2
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(Tables I, III), but because of weakly developed inner longitudi-
nal musculature, these cestodes are often fragmented even when
found in freshly examined hosts, and their differentiation is
not easy in unstained material. An examination of syntypes of
O. grandis has confirmed that it is a mixture of 2 different species
used by La Rue (1911, 1914) for his description of O. grandis. This
case once again emphasizes the importance of depositing type
specimens in solving taxonomic problems and in the stability of
nomenclature. Without the possibility of studying museum speci-
mens, it would not be possible to clarify the misidentification of
tapeworms that La Rue (1911, 1914) used for his description of the
supposedly new taxon.
In addition to the 2 species redescribed above, O. marenzelleri
and O. grandis, which are specific and common parasites of
the northern cottonmouth, another species of Ophiotaenia can
sometimes be found in this predatory snake. Brooks (1978) and
Fontenot and Font (1996) reported O. perspicua La Rue, 1911 in
A. piscivorus, but this identification should be verified. In the pre-
sent study, we found small, slender tapeworms with a very small
scolex (width ,250 mm) in A. piscivorus from Oklahoma and
Arkansas (Figs. 1M, N, 2G–I, 3E, 4E). They resembled some spe-
cies commonly found in watersnakes (Colubridae: Natricinae),
such as O. perspicua, but their identification was not possible
because of the taxonomic problems that exist with this tapeworm
group. Because these tapeworms are commonly found in semi-
aquatic snakes (species of Nerodia Baird and Girard, 1853 and
Thamnophis Fitzinger, 1843; McAllister et al., 2021), the northern
cottonmouth likely serves only as a postcyclic or incidental host,
because it frequently eats other snakes (Gloyd and Conant, 1990).
The present study does not include molecular data because a
more comprehensive molecular phylogenetic study of proteoce-
phalids belonging to clade D of de Chambrier et al. (2015) is
underway. However, preliminary data suggest that O. grandis
and tapeworms with small scolex from northern cottonmouth are
closely related to O. perspicua, the type species of the genus,
which would mean that they are indeed members of this genus
(O. Kudlai, unpublished data). In contrast, O. marenzelleri is not
closely related to tapeworms of this group and should be assigned
to a different genus.
Eighteen A. piscivorus were examined in the present study; 1
northern cottonmouth harbored all 3 species of Ophiotaenia (O.
marenzelleri,O. grandis, and Ophiotaenia sp.), 4 snakes harbored
2 species (O. marenzelleri and O. grandis), and 14 snakes were
infected with a single species of Ophiotaenia (103O. marenzelleri,
33O. grandis, and 13Ophiotaenia sp.).
Ophiotaenia was separated from Proteocephalus Weinland,
1858, by the presence of 2 testicular fields (La Rue, 1911; Freze,
1965; Rego, 1994). These 2 genera harbor more than half of all
nominal species recognized as valid in the family Proteocephali-
dae of the former order Proteocephalidea Mola, 1928 (87 species
of Ophiotaenia and 73 species of Proteocephalus out of a total of
316 species in the group according to de Chambrier et al., 2017).
However, none of these genera is monophyletic (Zehnder and
Mariaux, 1999; de Chambrier et al., 2004, 2017), and their species
appeared in 10 and 7 distinct lineages, respectively (de Chambrier
et al., 2015).
Most Ophiotaenia species of Nearctic and Palaearctic snakes
are morphologically similar (Freze, 1965). The most striking dif-
ference between them is in the relative size of the ovary, i.e., the
ratio of its surface area to the surface area of the proglottid.
Nearctic taxa have a smaller ovary, accounting for only 2.1–6.3%
of the proglottid surface area, whereas species from the Palaearc-
tic have a relatively larger ovary (9.1–12.7%; see de Chambrier
et al., 2012; Table II). Concerning uterine development (see de
Chambrier et al., 2004), 3 Ophiotaenia species from semiaquatic
snakes (O. gilberti Ammann and de Chambrier, 2008, O. maren-
zelleri Barrois, 1898, and O. tessellata Gamil and Fouad, 2022)
show type 1 uterine development, 7 species show type 2 uterine
development, and no information is available for the remaining 6
species (Table II) (Barrois, 1898; Ammann and de Chambrier,
2008; Gamil and Fouad, 2022).
Brooks (1978) studied tapeworms of North American semi-
aquatic snakes and provided morphological data on several spe-
cies of Ophiotaenia (erroneously synonymized with Proteocepha-
lus; see de Chambrier et al., 2015, 2017), including the type
species, O. perspicua La Rue, 1911, which he reported from no
fewer than 7 different species of colubrid snakes and also from
northern cottonmouth (see Table 2 in Brooks, 1978). This author
also described a new species, Ophiotaenia variabilis, from 2 differ-
ent hosts.
The broad host specificity of North American species of
Ophiotaenia in semiaquatic snakes assumed by Brooks (1978)
is not consistent with previous data from other zoogeographic
regions. Ammann and de Chambrier (2008) found that each
snake species from Central and South America (based on the
study of 170 snake species) harbors different species of Ophio-
taenia that are specific to a particular host. Strict host specific-
ity (oioxenous according to Euzet and Combes, 1980; strict
specialist according to Kuchta et al., 2020) has also been
observed in proteocephalids of amphibians, based on the para-
sitological study of 202 host species (see Table 2 in de Chamb-
rier et al., 2006), and in monitor lizards (Varanidae) from the
Australasian region (de Chambrier et al., 2020).
Therefore, it is necessary to verify Brooks’ (1978) assumption
of less strict host specificity of the Nearctic tapeworms of
snakes, other reptiles, and amphibians by evaluating new mate-
rial from different hosts using molecular data. A recent study of
Ophiotaenia tapeworms of ranid frogs in North America (Scholz
et al., 2023) suggests stenoxenous host specificity (congeneric
specialists after Kuchta et al., 2020). The present revision of
northern cottonmouth tapeworms suggests that records of tape-
worms typical of colubrid snakes may represent incidental infec-
tions in this viper that should be considered with caution when
evaluating host specificity.
ACKNOWLEDGMENTS
The authors thank 2 reviewers for helpful suggestions, Dr. Olena
Kudlai, Institute of Ecology, Nature Research Centre, Vilnius,
Lithuania, for providing preliminary unpublished molecular data,
and Dr. Anna Phillips and the staff of the USNM for the loan of
type and voucher specimens of the proteocephalids of A. piscivorus.
Special thanks are due to Dr. Anindo Choudhury, St. Norbert
College, De Pere, Wisconsin, for facilitating the loan from the
USNM and repeatedly hosting the first author in his laboratory. We
thank Dr. Stephen Curran and acknowledge the late Dr. Robin
Overstreet for granting collecting permits and their help in collecting
snakes in Mississippi. We also thank Janik Pralong and Christina
Lehmann-Graber for technical assistance and Gilles Roth (all
Geneva) for completing drawings, and Blanka S
ˇkorı
´kova
´(C
ˇeske
´
SCHOLZ ET AL.—TAPEWORMS OF NORTHERN COTTONMOUTH 477
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Bud
ejovice) for preparing plates with illustrations. The Arkansas
Game and Fish Commission and Oklahoma Department of
Wildlife Conservation issued Scientific Collecting Permits No.
040720225 and 1551646, respectively, to CTM. CTM thanks
Dr. Laurence Hardy of the Ouachita Mountain Biological Station,
Big Fork, Arkansas, for providing housing and laboratory space
free of charge. CTM also thanks Nikolas H. McAllister (North
Lamar High School, Paris, Texas) and Johnny C. Ray (Kiamichi
Tech Center, Idabel, Oklahoma) for assistance in collecting snakes.
This study was funded in part by the Institute of Parasitology,
Biology Centre of the Czech Republic (RVO: 60077344), Ministry
of Education, Youth and Sports of the Czech Republic (project
No. LUAUS23080), and National Science Foundation PBI
awards Nos. 0818696 and 0818823.
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HYPS
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