First Report of Pyelosomum Cochlear Looss 1899 (Digenea: Pronocephalidae) in a Hawksbill Turtle - Eretmochelys Imbricata L. Found in Brazilian Coast.

Pyelosomum cochlear Looss 1899 (Digenea: Pronocephalidae) is a parasite exclusive to sea turtles, having been described in the green turtle (Chelonia mydas) in Egypt, the USA, Panama, Costa Rica and Brazil as well as the olive ridley turtle (Lepidochelys olivacea) in Brazil. The present note describes the first occurrence of P. cochlear in a hawksbill turtle (Eretmochelys imbricata) found on the coast of Brazil.

Introduction

Looss (1899) erected the genus Pyelosomum (type species: P. cochlear Looss 1899) based on two specimens found in the urinary bladder of a green turtle (Chelonia mydas Linnaeus 1758) from Egypt. The parasite was later described in the same host in the United States (including from Puerto Rico) (Nigrelli, 1940, 1941; Dyer et al., 1991, 1995), Panama (Caballero, 1954), Costa Rica (Santoro et al., 2006) and Brazil (Werneck and Silva 2015) as well as in an olive ridley turtle (Lepidochelys olivacea Eschscholtz 1829) in Brazil (Werneck et al., 2015a). However, there are no previous reports of the occurrence of this parasite in the hawksbill turtle (Eretmochelys imbricata Linnaeus 1766).

Therefore, the present note describes the first occurrence of P. cochlear in a hawksbill turtle found on the coast of Brazil.

Materials and Methods

In December 2018, a hawksbill turtle was found dead after stranding on Brava Beach (23° 0’33.42”S / 44°29’3.00”W) in the city of Angra dos Reis, State of Rio de Janeiro, Brazil. The sea turtle measured 76.4 cm in curvilinear length and weighed 49.5 kg. During necropsy, the specimen was determined to be female, but the collection of samples for histopathological analysis was not possible due to the advanced state of decomposition of the carcass. However, the analysis of the urinary bladder revealed the presence of a single specimen of P. cochlear found in the mucosa of the organ.

The parasite was placed in saline solution, fixed in 70 % alcohol, stained with carmine and cleared with eugenol. The specimen was measured under a microscope (Nikon Eclipse 80i, Kurobane Nikon Co., Ltd., Otawara, Tochigi, Japan) with the aid of the NIS-Elements BR software and deposited in the Helminthological Collection of the Instituto Oswaldo Cruz (CHIOC number 38588) in the state of Rio de Janeiro, Brazil.

The identification of the parasite was based on the taxonomic genus key proposed by Blair (2005) and the phylogenetic study by Pérez-Ponce de León and Brooks (1995) as well as the description (Looss, 1899) and redescription (Caballero, 1954) of the species and other reports of the parasite (Nigrelli, 1940; Werneck et al., 2015a).

The following were the characteristics of the specimen (Fig. 1): anterior extremity tapered, with evident cephalic collar; posterior extremity rounded, measuring 4,282 μm in length by 3,409 μm in width; oral sucker subterminal, measuring 658 μm in length by 780 μm in width; esophagus short; ceca sinuous, near side of body, moving to mid region of body before testes, extending beyond the testes and terminating in fundus of cecum between testes near posterior extremity of body; cirrus sac partially covered by uterine loops, but clearly intercecal; vitellaria composed of two groups of follicles, extra-cecal, bordering side of body, beginning in anterior third near posterior extremity of cirrus sac and ending at ovary level, oval shape, right side with 11 follicles and left side with 12, some points surpass ceca; uterus begins at level of ovary and occupies practically entire medial (inter-cecal) area; uterine loops reach various points laterally to follicle area and anteriorly surpass cirrus sac area; testes in posterior region of body, extracecal, with slightly rounded and weakly lobed shape; right testicle measuring 852 μm in length by 807 μm in width; left testicle measuring 704 μm in length by 620 μm in width; ovary with irregular shape, anterior to Mehlis’ gland, measuring 588 μm in length by 470 μm in width; Mehlis’ gland measuring 374 μm in length by 223 μm in width; genital pore in anterior third of body at distance of 1209 μm from anterior extremity; eggs with polar processes (10 measured

Fig. 1

Pyelosomum cochlear Looss 1899 (Digenea: Pronocephalidae) found in Eretmochelys imbricata Linnaeus 1766 (Testudines: Cheloniadae) from Brazil. Ventral view (scale bar 1 mm).

without polar processes), ranging from 29 to 34 μm (mean: 31 μm) in length and from 13 to 18 μm (mean: 15 μm) in width. It was not possible to define the number of polar processes in each egg due to the quantity of eggs in the uterine loops.

Ethical Approval and/or Informed Consent

For this study formal consent is not required.

Discussion

Pyelosomum cochlear is a parasite exclusive to sea turtles and, according to the majority of reports, preferably occupies the urinary bladder of the host. The species was described based on two specimens found in the urinary bladder of green sea turtles found in Egypt (Looss, 1899).

Four decades later, Nigrelli (1940) cited the occurrence of P. cochlear, unfortunately, the author did not describe the number of individuals found, but presented morphometric data on length (0.5 to 2.5 mm), width (2.5 to 5 mm) and egg length (0.0763 to 0.253 mm) as well as some morphological characteristics. Analyzing 50 green sea turtles the following year, the author cited the occurrence of 16 species of parasites, including P. cochlear collected from the urinary bladder, but did not describe any morphometric/morphological characteristics or report the prevalence (Nigrelli, 1941).

Analyzing 12 green sea turtles found in Panama, Caballero (1954) redescribed P. cochlear based on a specimen found in the urinary bladder. Sometime later, Dyer et al. (1991) described the occurrence of P. cochlear in the cloaca of a green turtle found in Puerto Rico.

Dailey et al. (1992) reported the occurrence of immature individuals of P. cochlear in the urinary bladder of a green sea turtle found in Oahu, Hawaii. Dyer et al. (1995) reported the occurrence of two specimens of P. cochlear in two of a total of four green sea turtles analyzed in Puerto Rico.

Santoro et al. (2006) analyzing 40 adult green turtles and described the occurrence of P. cochlear in 57.5 % of the hosts, with a mean intensity of 1.8 ± 1.1 (range: 1 to 4). In an analysis of 136 juvenile green turtles from the coast of Brazil, P. cochlear was found in only one host (Werneck and Silva, 2015). More recently, Werneck et al. (2015a) reported the occurrence of a specimen of P. cochlear in the urinary bladder of an olive ridley turtle in southern Brazil.

The specimen analyzed in the present study was consistent with the original description by Looss (1899) and redescription by Caballero (1954) and had the majority of characteristics described by Pérez-Ponce de León and Brooks (1995), with the presence of uterine loops exceeding the limits of the cirrus sac (i.e., autapomorphy found only in P. cochlear). However, it was not possible to determine/describe the filament number in each egg, development of the prostatic complex or degree of glandulation of the metraterm due to the large number of eggs in the uterine loops.

The morphometric analysis revealed that the oral sucker, right testicle, length of the left testicle, length of Mehlis’ gland and ovary dimensions were larger than previously published data and the egg dimensions were smaller than previously published data (Looss, 1899; Nigrelli, 1940; Caballero, 1954; Werneck et al., 2015a). Such findings likely correspond merely to individual variations of the specimens

The helminth fauna of the hawksbill turtle correspond to approximately 60 species distributed among 11 families (see Dyer et al., 1995; Greiner, 2013; Santoro et al., 2015; Werneck et al., 2014, 2015b, 2015c). The present study adds P. cochlear to this list.