Mesocoelium monas

López-García, Ashley Samara & García-Prieto, Luis, 2017, A reevaluation of the specimens of Mesocoelium (Trematoda: Mesocoeliidae) in the Colección Nacional de Helmintos, Mexico, Zootaxa 4273 (2), pp. 151-176 : 153-161

Monas body type

Mesocoelium danforthi CNHE-875 (1 slide: four specimens) ( Figure 1 ), ex R. marina . ( Anura : Bufonidae ) from Valle de Antón, Panama.

M. cf. danforthi CNHE-1528c (1 slide: one specimen) ( Figure 2 ), ex R. marina from Laguna El Zacatal , Veracruz , Mexico.

Mexico City.

Original identification CNHE Body type Present determination

Mesocoelium travassosi Pereira & 875 (n=4) monas M. danforthi Hoffman, 1935

Cuocolo, 1940 M. danforthi Hoffman, 1935 M. danforthi Hoffman, 1935 M. danforthi Hoffman, 1935 876 (n=1) mesembrinum M. cf. microon Nicoll, 1914 876a (n=2) carli Mesocoelium sp.

Mesocoelium sp.

876b (n=1) leiperi Mesocoelium sp.

876c (n=2) Not assigned Mesocoelium sp.

Not assigned Mesocoelium sp.

1067a (n=1) monas M. americanum Harwood, 1932 1067b leiperi M. cf. gonocephali Singh, 1967 1067c (n=2) carli Mesocoelium sp.

Mesocoelium sp.

1067d (n=2) leiperi Mesocoelium sp.

Mesocoelium sp.

1067e (n=2) Not assigned Mesocoelium sp.

Mesocoelium sp.

Mesocoelium leiperi Bhalerao, 1936 1068 (n=7) carli Mesocoelium sp.

Mesocoelium sp.

Mesocoelium sp.

Mesocoelium sp.

Mesocoelium sp.

Mesocoelium sp.

Mesocoelium sp.

1068a (n=1) Not assigned Mesocoelium sp.

Mesocoelium monas Rudolphi, 1819 1528 (n=1) monas M. americanum Harwood, 1932 1528a (n=2) mesembrinum M. meggitti Bhalerao, 1927

M. meggitti Bhalerao, 1927 Mesocoelium sp.

1529 (n=3) Not assigned Mesocoelium sp.

Not assigned Mesocoelium sp.

Characterization. Based on 5 specimens. Body oval, covered with numerous spines that gradually diminish to the posterior end and disappear before anterior end of ventral sucker; oral sucker spherical; prepharynx very short, almost absent; pharynx wider than long. Esophagus short, slightly visible; cecal bifurcation slightly posterior to mid-forebody; intestinal ceca surpass ovary posteriorly, end near mid-body. Testes slightly diagonal at level of ventral sucker; cirrus sac between pharynx and anterior end of ventral sucker. Genital pore prebifurcal, submedian, dextral. Ovary dextral or sinistral and postesticular. Uterus widely distributed but located mostly under ventral sucker. Excretory vesicle visible only in posterior region, branches of vesicle not visible ( Table 3).

Remarks. The four specimens in the catalogue number CNHE-875 were originally identified as M. travassosi by Caballero et al. (1956); this species was recently synonymized with M. meggitti by Dronen et al. (2012). However, this material differs from M. meggitti (= M. travassosi ) by the position of the genital pore (prebifurcal and submedian, which places it within the monas body type vs. prebifurcal and medial, as seen with the mesembrinum body type). In addition, the body in M. meggitti is attenuated, typically clavate, and widest at the forebody level; in the CNHE specimens, the body is oval; finally, the seminal vesicle in M. meggitti is tripartite (vs. bipartite in the studied specimens). Among the 12 species of monas body type to which our material belongs, it presented the diagnostic characteristics of M. danforthi , particularly in body length (1.95 in CNHE specimens vs. 1.3–2.1 in the re-description), the distribution (anterior and posterior) of the vitelline fields, the position of gonads related to the ventral sucker, the length of the eggs (0.034 x 0.019 in CNHE vs. 0.032–0.038 x 0.018–0.023 in the re-description), post-ovarian space length (1.16 in CNHE vs. 0.64–1.30 in the re-description), the ratio of oral sucker width to ventral sucker width (1: 1.3 in CNHE vs. 1:1.3–1: 1.9 in the re-description), the percentage of post-ovarian space occupied in relation to the total body length (59.7 in CNHE vs. 50–62 in the re-description), the size of the ovary (0.18 x 0.19 in CNHE vs. 0.12–0.22 x 0.09–0.23 in the re-description) and testicles (0.21 x 0.21 in CNHE vs. 0.08– 0.23 x 0.09–0.25 in the re-description), the percentage occupied by the cirrus sac related to the total body length (8.2 in CNHE vs. 8–11 in the re-description), and the percentage of ceca that surpasses the ovary into the postovarian space (28.8 in CNHE vs. 27–32 in the re-description).

The specimen with the catalogue number CNHE-1528c, originally identified as M. monas by Guillén- Hernández et al. (2000), differs from M. monas by the posterior extent of the vitelline fields, which do not surpass the intestinal ends in M. monas (Dronen et al. 2012) and notably surpass them in the CNHE specimen. Additionally, the posterior extent of the intestinal ends of M. monas do not surpass the ovary posteriorly (Dronen et al. 2012), while in the studied material, the intestinal ends surpasses the ovary, occupying 28.75% of the postovarian space. Almost all traits observed in this specimen fit with the diagnosis of M. danforthi presented by Dronen et al. (2012); however, based on the presence of a tripartite seminal vesicle and due to differences observed in some measurements, we preferred to assign this specimen as Mesocoelium cf. danforthi .

The records of M. danforthi come from the Neotropical Realm ( Puerto Rico, Jamaica and Panama), where it was recorded as a parasite of Diploglossus pleii Duméril & Bibron ( Squamata : Diploglossidae ), Anolis lineatopus Gray ( Squamata : Dactyloidae ), and R. marina ( Anura : Bufonidae ) (Dronen et al. 2012).

Mesocoelium americanum CNHE-1067a (1 slide: one specimen) ( Figure 3 ), Plestiodon sp. (= Eumeces sp.) ( Squamata : Scincidae ) from Cuicatlán, Oaxaca, Mexico.

Mesocoelium americanum CNHE-1528 (1 slide: one specimen) ( Figure 4 ), R. marina ( Anura : Bufonidae ) from Laguna El Zacatal , Veracruz , Mexico.

Mesocoelium americanum CNHE-3309 (1 slide: one specimen) ( Figure 5 ), Smilisca baudinii Duméril & Bibron ( Anura : Hylidae ) from Laguna Escondida , Veracruz , Mexico.

Mesocoelium americanum CNHE-5403 (1 slide: one specimen) ( Figure 6 ), R. marina ( Anura : Bufonidae ) from Presa Temascal, Oaxaca, Mexico.

Mesocoelium cf. americanum CNHE-1528b (1 slide: one specimen) ( Figure7 ), R. marina ( Anura : Bufonidae ) from Laguna El Zacatal , Veracruz , Mexico.

Mesocoelium cf. americanum CNHE-5403a (1 slide: one specimen) ( Figure 8 ), R. marina ( Anura : Bufonidae ) from Presa Temascal, Oaxaca, Mexico.

Characterization. Based on 6 specimens. Body oval, covered with numerous spines that gradually diminish to posterior end and disappear near mid-region of postovarian space, except in specimen CNHE-3309, which has no tegumental spines; oral sucker spherical in specimen CNHE-3309 and subspherical in remaining specimens; prepharynx very short, almost absent; pharynx wider than long; cecal bifurcation slightly posterior to midforebody; intestinal ceca surpass ovary posteriorly and end near mid-body. Testes slightly diagonal at level of ventral sucker; cirrus sac between pharynx and ventral sucker; the vitelline fields extends from the posterior margin of oral sucker until surpass the cecal ends and enter the postovarian space; seminal vesicle bipartite in all specimens, except for CNHE-1528b and CNHE-5403a, which has a tripartite seminal vesicle. Genital pore prebifurcal, submedian, sinistral; ovary dextral. Uterus widely distributed but located mostly under ventral sucker. Excretory system not visible (CNHE-3309 and CNHE-5403a) or visible partially (CNHE-1067a, CNHE-1528, CNHE-5403 and CNHE-1528b) ( Table 4).

Remarks. Zerecero (1951) identified the specimen CNHE 1067a as M. meggitti (= M. travassosi ). However, this material cannot be included in M. meggitti based on the position of genital pore (prebifurcal and submedian in Zerecero´s material vs. prebifurcal and medial in M. meggitti ), the body shape (attenuated, typically clavate, and widest at the forebody level in M. meggitti and oval in the CNHE specimen) and because the seminal vesicle in M. meggitti is tripartite but is bipartite in the studied digenean. The specimens included in the catalogue numbers CNHE 1528, 1528b, 3309, 5403 and 5403a were assigned to M. monas by Guillén-Hernández et al. (2000), Pérez- Ponce de León et al. (2000), and Espínola-Novelo & Guillén-Hernández (2008). Nonetheless, in M. monas , the posterior extent of the vitelline fields terminates well anterior to the cecal end, from near the mid-level to approximately 3/4 of the cecal length, and the posterior extent of the vitelline fields do not surpass the ovary posteriorly. In the specimens held at CNHE, the vitelline fields surpass the cecal ends, and in turn, the cecal ends surpass the ovary and reach almost mid-level of the hindbody. These specimens further differ from M. monas by having the genital pore anterior to the mid-level of esophagus, just above the level of the cecal bifurcation compared with the genital pore located from the level of the posterior margin of the pharynx to near the mid-level of esophagus (Dronen et al. 2012).

Considering the characteristics described above, the specimens CNHE 1067a, 1528, 3309, and 5403 are consistent with M. americanum , especially in the distribution (anterior and posterior) of the vitelline fields, the position of the gonads related to the ventral sucker, the percentage represented by the forebody in relation with total body length (37.87 in CNHE-1067a, 29.84 in CNHE-1528, 31.25 in CNHE-3309 and 26.37 in CNHE-5403 vs. 24– 37 in the re-description), the percentage occupied by the cirrus sac related to the total body length (6.43 in CNHE- 1067a, 6.06 in CNHE-1528, 11.25 in CNHE-3309 and 9.91 in CNHE-5403 vs. 6–10 in the re-description), egg size (0.036 x 0.026 in CNHE-1067a, 0.034 x 0.023 in CNHE-1528, 0.032 x 0.025 in CNHE-3309 and 0.032 x 0.021 in CNHE-5403 vs. 0.035–0.044 x 0.020–0.026 in the re-description), post-ovarian space length (2.57 in CNHE- 1067a, 2.27 in CNHE-1528, 0.87 in CNHE-3309 and 1.11 in CNHE-5403 vs. 0.67–2.62 in the re-description), the ratio of oral sucker width to ventral sucker width (1: 1.5 in CNHE-1067a, 1: 1.5 in CNHE-1528, 1: 1.2 in CNHE- 3309 and 1: 1.2 in CNHE-5403 vs. 1:1.2–1: 1.7 in the re-description), the ratio of oral sucker width to pharynx width (1: 2.5 in CNHE-1067a, 1: 2.7 in CNHE-1528, 1: 2.3 in CNHE-3309 and 1: 1.9 in CNHE-5403 vs. 1:2.1–1: 2.5 in the re-description) and the percentage of post-ovarian space occupied in relation to the total body length (60.60 in CNHE-1067a, 60.57 in CNHE-1528, 56.61 in CNHE-3309 and 54.97 in CNHE-5403 vs. 51–65 in the redescription) (Dronen et al. 2012).

The assignation of the specimens CNHE-1528b and CNHE-5403a to M. cf. americanum was based on their differences with M. americanum in characteristics such as the percentage of postovarian space occupied by ceca (45.12 in CNHE-1528b and 23.07 in CNHE-5403 vs. 26–38 in the re-description), egg length (0.031 in CNHE- 1528b and 0.032 in CNHE-5403 vs. 26–38 in the re-description), the ratio of oral sucker width to pharynx width in CNHE-1528b (1:3.0 in CNHE vs. 1:2.1–1: 2.5 in the re-description) and the presence of a tripartite seminal vesicle in both specimens.

The host range of M. americanum include amphibian species such as Storeria dekayi texana Trapido ( Squamata : Colubridae ), Scincella lateralis Say ( Squamata : Scincidae ), Plestiodon fasciatus Linnaeus ( Squamata : Scincidae ), Anolis sagrei Duméril & Bibron ( Squamata : Dactyloidae ), Hyla cinerea Schneider ( Anura : Hylidae ) and Smilisca baudinii ( Anura : Hylidae ) in Florida, Texas ( USA), and Veracruz ( Mexico) (Calhoun & Dronen 2012; Dronen et al. 2012). In addition, M. cf. americanum was recorded as a parasite of Anolis gingivinus Cope ( Squamata : Dactyloidae ), Duttaphrynus melanostictus Schneider ( Anura : Bufonidae ) and Peltophryne fustiger Schwartz ( Anura : Bufonidae ) in the Caribbean and Malaysia (Calhoun & Dronen 2012; Dronen et al. 2012). The specimen recorded with the catalogue number CNHE-1067a was collected in the reptile Eumeces sp.; however, according to Uetz & Hošek (2015), this genus is not distributed in Mexico. The records of Eumeces spp. in this country were re-assigned to the genera Mesoscincus or Plestiodon (CONABIO 2012) based on the current distribution of both genera; the host species involved in the record of M. americanum in Oaxaca state, Mexico could belong to Plestiodon brevirostris Günther , Plestiodon ochoterenae Taylor or Plestiodon sumichrasti Cope , whose distribution includes this state of the country ( Uetz & Hošek 2015). The specimens CNHE-3309, CNHE- 5403, CNHE-1528b and CNHE-5403a were collected in the bufonid R. marina , one of the most widespread amphibians in America ( Easteal 1981); to the best of our knowledge, this represents the first record of M. cf. americanum and M. americanum in the cane toad.

Figures

FIGURES 1 – 2. 1. Mesocoelium danforthi (CNHE- 875) parasite of Rhinella marina from Valle de Antón, Panama. Ventral view of the specimen (A) and detail of the cirrus sac (B). 2. Mesocoelium cf. danforthi (CNHE- 1528 c) parasite of Rhinella marina from El Zacatal, Veracruz, Mexico. Ventral view of the specimen (A) and detail of the cirrus sac (B).

FIGURES 3 – 4. 3. Mesocoelium americanum (CNHE- 1067 a) parasite of Plestiodon sp. (= Eumeces sp.) from Cuicatlán, Oaxaca, Mexico. Ventral view of the specimen (A) and detail of the cirrus sac (B). 4. Mesocoelium americanum (CNHE- 1528) parasite of Rhinella marina from Laguna El Zacatal, Veracruz, Mexico. Ventral view of the specimen (A) and detail of the cirrus sac (B).

FIGURES 5 – 6. 5. Mesocoelium americanum (CNHE- 3309) parasite of Smilisca baudinii from Laguna Escondida, Veracruz, Mexico. Ventral view of the specimen (A) and detail of the cirrus sac (B). 6. Mesocoelium americanum (CNHE- 5403) parasite of Rhinella marina from Presa Temascal, Oaxaca, Mexico. Ventral view of the specimen (A) and detail of the cirrus sac (B).

FIGURES 7 – 8. 7. Mesocoelium cf. americanum CNHE- 1528 b parasite of Rhinella marina from Laguna El Zacatal, Veracruz, Mexico. Ventral view of the specimen (A) and detail of the cirrus sac (B). 8. Mesocoelium cf. americanum CNHE- 5403 a parasite of Rhinella marina from Presa Temascal, Oaxaca, Mexico. Ventral view of the specimen (A) and detail of the cirrus sac (B).