First report of Rhytidodes gelatinosus (Rudolphi, 1819) Looss, 1901 (Digenea: Rhytidodidae) in an olive-ridley Turtle Lepidochelys olivacea (Eschscholtz, 1829) from Brazil

The family Rhytidodidae corresponds to a group of digenetic trematodes described in sea turtles, which currently includes only two genera: Rhytidodes Looss, 1901 (with four accepted species: Rhytidodes gelatinosus (Rudolphi, 1819) Looss, 1901; Rhytidodes indicus Simha and Chattopadhyaya, 1969; Rhytidodes secundus Pratt, 1914 and Rhytidodes srivastavai Ghosh, 1996 and Rhytidodoides Price, 1939 (also with four accepted species: Rhytidodoides similis Price, 1939; Rhytidodoides intestinalis Price, 1939; Rhytidodoides pricei Mehrotra & Gupta, 1978 and Rhytidodoides cheloniae Wang, 1983 (Blair, 2005; WoRMS, 2023).

Rhytidodes gelatinosus was originally described by Rudolphi (1819) as Distomum gelatinosum Rudolphi, 1819 found in the intestine of “Testudinnis mydae” – green turtle – now Chelonia mydas. It was later described in different parts of the world in green turtles, in addition to loggerhead turtles, Caretta caretta and hawksbill turtles, Eretmochelys imbricata (Rudolphi, 1819; Limpus and Blair, 1980; Blair, 2005).

Thus, the purpose of this note is to describe the first occurrence of specimens of R. gelatinosus in an olive turtle, Lepidochelys olivacea (Eschscholtz, 1829) found on the Brazilian coast.

In March 2019, a female olive-ridley (observed during necropsy with visualization of the ovaries) considered to be an adult (with a curvilinear carapace length of 67.3 cm) was found dead on Mosqueiro beach in the municipality of Aracaju (11°01′57″S, 37°05′00″W) in the State of Sergipe, Brazil. Necropsy was performed immediately and four specimens of R. gelatinosus were found in the small intestine.

The collected trematodes were preserved in ethanol 70 %, stained with carmine, and cleared with eugenol. Morphometric data was collected with the aid of a Global optics light microscope using the S-EYE software program. Measurements are reported in micrometers, except when indicated, with the mean followed by the range in parenthesis. The helminths were deposited in the Helminthological Collection of the Instituto Oswaldo Cruz in the state of Rio de Janeiro (number requested), Brazil.

The identification used in this report followed the genus taxonomic key proposal by Blair (2005), the original description by Looss (1901), comments by Blair and Limpus (1982) and redescription by Caballero and Caballero (1954). The morphometric comparison (Table 1) was made using the works of Caballero and Caballero (1954), Bilqees (1974), Blair and Limpus (1982) and Cavaco et al. (2021).

For this study, formal consent is not required.

Parasite description (Fig. 1, Table 1): elongated parasites with slightly rounded ends, terminal oral sucker showing lateral projections, pharynx present; long oesophagus and pre-acetabular caecal bifurcation, thin cecum running along the body ending near the posterior end of the body; acetabulum in the initial third of the body; rounded pre-testicular ovary; intercaecal uterus between ovary and acetabulum; preacetabular cirrus sac; two slightly oval testicles in tandem; genital pore anterior to the acetabulum; vitelline follicles similar to thin threads that occupy the lateral area of the body, covering the cecum in almost its entirety and occupying the region immediately after the acetabulum to the posterior end of the body.

Fig. 1.

The specimens analyzed in this note presented the acetabulum in the anterior third of the body, testicles in tandem in the post-equatorial region and the distribution of vitelline follicles that are compatible with the genus Rhytidodes, according to the gender identification key proposed by Blair (2005).

Our specimens differ from R. secundus by having a smaller acetabulum (360 in diameter in R. secundus), in addition to smaller egg dimensions, however, our specimens are as small as those presented by Pratt (1914).

Our specimens also differ from R. indicus by having smaller eggs. It was not possible to visualize the cirrus [which according to Simha and Chattopadhyaya (1969) in R. indicus was described as “a long and muscular cirrus, protruding out of the genital pore, whereas in the type species it is small” see page 98]. In addition, the authors also note: “(…) having a sucker like structure, situated at a distance of 1.94 – 1.96 mm from the posterior testis”. Such structure was not observed in our specimens.

The size of the egg of the specimens corresponded to those found in R. gelatinosus, a measure that was even used by Ghosh (1994) together with the shape and extent of the cirrus sac and the positioning of the vitelline follicles to differentiate R. srivastavai from R. gelatinosus.

The morphometric analysis of the specimens in the present study demonstrated that the body width, oesophageal width, cirrus sac length and egg length and width are smaller when compared to previously published data, while the pharyngeal values are bigger. These data do not preclude the identification of the specimens and probably reflect only variation within the species.

Observation of the genital pore reveals the opening in a protuberance located directly in front of and slightly to the right of the ventral sucker (Fig. 2). This protuberance had already been observed, initially by Looss (1902) and later by Blair and Limpus (1982).

Fig. 2.

Rhytidodes gelatinosus has already been reported in several parts of the world and in three of the seven species of sea turtles. Blair and Limpus (1982) offer an extensive review of the species, occurring in loggerhead turtles in the Adriatic Sea (Trieste and Egypt), USA, Mediterranean coast of France, New Guinea, Australia and Brazil; in green turtles in the Adriatic Sea (Rimini), Panama, Mexico, Pakistan and New Guinea; and in hawksbill turtles in Cuba, India and Puerto Rico.

Later Manfredi et al. (1998) analyzed 14 specimens of loggerhead turtles from the Adriatic Sea (Mediterranean Sea) and in 11 of them the presence of parasites was observed. Specimens of R. gelatinosus were collected from the stomach, intestine and liver of four analyzed turtles (28.6 %) and had an abundance of 32.6 (intensity 0 – 392 specimens).

Valente et al. (2009) analyzed fifty-seven specimens of logger-head turtles found in the Madeira archipelago, Portugal. 45.6 % of the specimens were parasitized. R. gelatinosus was found in the intestines of two turtles (3.5 %), with an average abundance of 0.04 (±0.19) and an average intensity of 1.5 (1 – 2) specimens. Santoro et al. (2010) analyzed 182 loggerhead turtles from six sites on the west and central Mediterranean coasts. Specimens of R. gelatinosus were found in the stomach and intestine. The highest prevalence was recorded in the Campania region (9.4 %), followed in descending order by Sicily - Tyrrhenian Sea (5.6 %), Spanish Balearic Islands (5.6 %), Sicily - Ionian Sea (4.5 %) and Valencia (2.3 %). The highest mean intensity of infection was recorded in the region of Valencia (22.0), followed by Campania (13.3 (1.0 – 20.7)), Sicily – Tyrrhenian Sea (2.0), Sicily – Ionian Sea (2.0) and Spanish Balearic Islands (1.0).

Gracan et al. (2012) analyzed 70 loggerhead turtles from the East Adriatic Sea, of which 49 were infected. Rhytidodes gelatinosus was identified in the gut of 19 turtles (27.1 %) with an abundance of 8.3 and mean intensity of 30.5 (13.8 – 79.1) specimens.

Greiner (2013) reported the presence of R. gelatinosus in the gut of four species of Florida sea turtles. In 44 loggerhead turtles, he found 3703 specimens of R. gelatinosus in 23 turtles (52.6 %), with an average intensity of 16.1 (1 – 882); in 74 green turtles, he found 101 specimens of this trematode in ten turtles (13.5 %), with an average intensity of 10.1 (1 – 49); in four hawksbill turtles he found 54 specimens in three turtles (75 %), with an average intensity of 16 (9 – 45); finally, in four Kemp turtles, he found 2 specimens in one animal (25 %).

In Brazil, Werneck and Silva (2015) evaluated 136 loggerhead turtles. They found an only specimen of R. gelatinosus. They registered a prevalence of 0.7 % (0 – 3.9) and mean abundance of 0.00735 (0 – 0.0221).

Pace et al. (2019) investigated the presence of eggs in 30 faecal samples from loggerhead turtles from Italy and recorded a 10 % prevalence of Rhytidodes spp.

Gentile et al. (2021) analyzed 64 loggerhead turtles from various locations along the coast of Italy. 31 turtles had parasites. The highest prevalence of R. gelatinosus was recorded in the Tyrrhenian Sea (34.6 %), followed by the Adriatic Sea (33.3 %) and finally the Ionian Sea (6.4 %).

The last report of R. gelatinosus was made by Cavaco et al. (2021), who found two specimens in the stomach of a loggerhead turtle in Brazil.

In the present report we present the occurrence of R. gelatinosus in a specimen of L. olivacea found in Brazil. This parasite had already been described in other sea turtles in different locations (see Table 2).

Unfortunately, reports of parasitological analysis of olive turtles on the Brazilian coast are scarce, noting up to the present moment only two parasites reported in this host: Werneck et al. (2015) report the occurrence of Pyelosomum cochlear Looss, 1899 (Pronocephalidae) and Jerdy et al. (2019) describe lesions in the urinary bladder resulting from the parasitism of Plesiochorus cymbiformis (Rudolphi, 1819) Looss, 1901 (Gorgoderidae). The present work adds L. olivacea as a host for R. gelatinosus.