Some Digenetic Trematodes Found in a Loggerhead Sea Turtle (Caretta Caretta) from Brazil.

This paper reports three recovered species of digeneans from an adult loggerhead sea turtle - Caretta caretta (Testudines, Cheloniidae) in Brazil. These trematodes include Diaschistorchis pandus (Pronocephalidae), Cymatocarpus solearis (Brachycoeliidae) and Rhytidodes gelatinosus (Rhytidodidae) The first two represent new geographic records. A list of helminths reported from the Neotropical region, Gulf of Mexico and USA (Florida) is presented.

Introduction

During the last century sea turtle populations worldwide have been declining mostly due to human activities, but also due to natural dangers, such as predation and infections caused by several pathogens, like parasites. According to the International Union for Conservation of Nature, the loggerhead turtle is considered a vulnerable specie and all the populations of sea turtles have become threatened (IUCN, 2017). Therefore, it is important to study these factors in order to know its impact on these threatened species.

Studies of the helminth fauna from sea turtles have already been carried out for many years and, possibly, loggerhead sea turtles (Caretta caretta) are the most studied specie, with a large number of parasites already reported in different parts of the world (Sey, 1977, Aznar et al., 1998, Werneck et al., 2008; Valente et al., 2009; Santoro et al., 2010; Gracan et al., 2012; Karaa et al., 2019; Greiner, 2013). However, in Brazil a small amount of research on loggerhead sea turtles parasites has been done (Werneck & Silva, 2016; Werneck et al., 2018; Werneck et al., 2019). Therefore, the present article brings new knowledge on loggerheads’ trematodes parasites from Brazil.

Material and Methods

In March 22, 2014 an adult female loggerhead sea turtle measuring 97.9 cm in curved carapace length was found in the Camburi beach (20° 16’ 0.120” S, 40° 16’ 59.880” W), municipality of Vitória in the state of Espírito Santo, Brazil. The turtle was found dead on the beach during a monitoring expedition and it was frozen.

At necropsy, performed in April 29, 2014 several trematodes were found in the stomach. The contents were cleansed and concentrated with sieves (mesh sizes: 0.3 mm and 0.150 mm) and examined under a stereomicroscope. The parasites were placed in a Petri dish, preserved in 70 % alcohol, stained with carmine, and cleared with eugenol. Morphometric data was collected with the aid of a Global optics microscope using the S-EYE software program. Measurements are reported in micrometers, except when indicated, with the mean and standard deviation followed by the range in parenthesis. The analyses of the parasites were authorized by federal licenses for activities with scientific purposes (SISBIO 30600–1). The helminths were deposited in the Helminthological Collection of the Instituto Oswaldo Cruz in the state of Rio de Janeiro, Brazil (CHIOC).

The classification used in this report followed the taxonomic proposal presented by the World Register of Marine Species (WoRMS, 2020).

Ethical Approval and/or Informed Consent

For this study formal consent is not required.

Results and Discussion

Three species of digeneans including 23 Diaschistorchis pandus (Pronocephalidae), 36 Cymatocarpus solearis (Brachycoeliidae) and 2 Rhytidodes gelatinosus (Rhytidodidae) were found in the stomach of the loggerhead turtle. The first two trematodes have new geographic records.

TREMATODA

Family: Pronocephalidae Looss, 1899

1. Diaschistorchis pandus (Braun, 1901) Johnstone, 1913 (Fig. 1) Site of infection: stomach.

Fig. 1

Diaschistorchis pandus (Braun, 1901) Johnstone, 1913 (Digenea: Pronocephalidae) found in a loggerhead turtle from Brazil, ventral view (scale bar = 1.0 mm)

Voucher specimen deposited: CHIOC 38973.

Remarks: This trematode has been found in loggerheads sea turtles from Australia (Braun, 1901), USA (Pratt, 1914; Greiner, 2013), Egypt (Sey, 1977) and Tunisia (Karaa et al., 2019). In Green sea turtles (Chelonia mydas) from Australia (Johnstone, 1913), USA (Greiner, 2013). In Halksbill sea turtles (Eretmocheys imbricata from Australia (Johnstone, 1913) and India (Chattopadhyaya, 1972; Mehrotra & Gupta, 1976). In the Neotropical region (Central and South America), this trematode was already found in green sea turtles from Brazil (Werneck & Silva, 2015), in hawksbills sea turtles from Bermuda (Barker, 1922), Cuba (Vigueras, 1955), Puerto Rico (Fischthal & Acholonu, 1976; Dyer et al., 1995) and Brazil (Werneck et al., 2015) and loggerhead sea turtle from Brazil (present report).

Measurements: (n = 23) Body 7.75 ± 1.07 (6.46 – 9.33) mm long by 3.23 ± 0.35 (2.83 – 3.66) mm wide; oral sucker 961.9 ± 143.8 (727 – 1,201) long by 984 ± 143.9 (871 – 1,220) wide; testis number 16.6 ± 0.89 (16 – 18); ovary 318 ± 48.0 (252 – 364) long by 342.8 ± 82.4 (232 – 430) wide; cirrus sac 680.4 ± 109.6 (575 – 900) long by 225.3 ± 54.5 (156 – 302)

The morphological characteristics are compatible with the taxonomic key proposed by Blair (2005a) and Mehrotra and Gupta (1976), comparisons were made with the article by Dyer et al. (1995). Our specimens are comparable to those described, except the size of the body width and oral sucker, that are larger than those reported by Dyer et al. (1995).

Family: Brachycoeliidae Looss, 1899

2. Cymatocarpus solearis (Braun, 1899) Braun, 1901 (Fig. 2) (probably Synonym: Cymatocarpus undulatus Looss, 1899) Site of infection: stomach.

Fig. 2

Cymatocarpus solearis (Braun, 1899) Braun, 1901 (Digenea: Brachycoeliidae) found in a loggerhead turtle from Brazil, ventral view (scale bar=1.0 mm)

Voucher specimen deposited: CHIOC 38975.

Remarks: According to Blair and Limpus (1982), C. solearis has already been found in loggerheads sea turtles from the Mediterranean coast of Egypt and from USA (Florida) (Looss, 1899; Linton, 1910; Pratt, 1914; Luhman, 1935), in olive ridleys from Japan (Oguro, 1942) and green sea turtles from Mexico (Caballero, 1959). In Brazil it has already been reported in green sea turtles (Werneck & Silva, 2015), hawksbills sea turtles (Werneck et al., 2015) and in loggerhead sea turtle (present report).

Measurements: (n = 36) Body 4.86 ± 0.83 (3.36 – 5.89) mm long by 1.30 ± 0.12 (1.12 – 1.47) mm wide; oral sucker 198.3 ± 50.1 (133 – 245) long by 231.5 ± 55.2 (161 – 291) wide; ventral sucker 262.5 ± 46.7 (171 – 301) long by 275.2 ± 55.9 (196 – 327) wide; pharynx 275.7 ± 187.6 (157 – 492) long by 72.5 ± 25.5 (46 – 107) wide; oesophagus 1,094.8 ± 149.3 (936 – 1296) long by 79 ± 18.7 (61 – 98) wide; anterior testis 249.2 ± 56.2 (183 – 310) long by 238.7 ± 50.0 (168 – 290); posterior testis 256 ± 60.7 (176 – 338) long by 249.6 ± 30.3 (217 – 281); ovary 204.3 ± 64.2 (142 – 321) long by 208.5 ± 49.8 (118 – 267) wide

The morphological characteristics are compatible with the taxonomic key proposed by Pojmanska (2008) and comparisons were made with the article by Blair and Limpus (1982), Caballero (1959) and Grano-Maldonado and Álvarez-Cadena (2010). The morphometric analyses of our specimens are comparable to those described by Blair and Limpus (1982) and Caballero (1959) although they were larger than largest fluke by Grano-Maldonado and Álvarez-Cadena (2010). Principal variations occurred for the size of ventral sucker, pharynx and ovary from those described by Blair and Limpus (1982).

Family: Rhytidodidae Odhner, 1926

3. Rhytidodes gelatinosus (Rudolphi, 1819) Looss, 1901 (Fig. 3) Site of infection: stomach.

Fig. 3

Rhytidodes gelatinosus (Rudolphi, 1819) Looss, 1901 (Digenea: Rhytidodidae) found in a loggerhead turtle from Brazil, ventral view (scale bar=1.0 mm).

Voucher specimen deposited: CHIOC 38974.

Remarks: R. gelatinosus is a wide distributed trematode. It has been reported from loggerheads sea turtles, green sea turtles and halksbill sea turtles, from Mediterranean sea, Morocco, USA, Puerto Rico, Cuba, Panama, India, Pakistan, New Guinea and Australia (see revision in Blair & Limpus 1982), also reported in loggerheads sea turtles from Brazil (Viana, 1924; Travassos et al., 1969, present report), Egypt (Looss, 1901; Looss, 1902; Sey, 1977), USA (Greiner, 2013), , More recently in Italy (Manfredi et al., 1998; Santoro et al., 2010; Gracan et al., 2012) and Portugal (Madeira Archipelago); Valente et al., 2009), in green sea turtle from Brazil, (Werneck & Silva, 2015).

Measurements: (n=2) Body 5.31 (4.94 – 5.68) mm long by 1.27 (1.20 – 1.34) mm wide; oral sucker 355 (318 – 392) long by 469 (403 – 535) wide; pharynx 180 (160 – 200) long by 167 (147 – 187) wide; oesophagus 834 (676 – 992) long by 76 (73 – 79) wide; acetabulum 234.5 (214 – 255) long by 187 (181 – 193); ovary 175 (169 – 181) long by 225 (204 – 246) wide; cirrus sac 309 long by 183; anterior testis 249.2 ± 56.2 (183 – 310) long by 238.7 ± 50.0 (168 – 290); posterior testis 371 (338 – 404) long by 272.5 (244 – 301);

The morphological characteristics are compatible with the taxonomic key proposed by Blair (2005b) and the original description by Looss (1901). Our specimens are similar to those described by Blair and Limpus (1982), except that they are smaller.

Published information concerning species of parasites of the loggerhead from the Neotropical region, Gulf of Mexico and USA (Florida) is summarized in Table 1 and Table 2. The present report contributes to the knowledge on marine loggerheads helminth fauna and their geographical distribution.

Table 1

Digeneans identified in loggerhead turtle from the Neotropical region, Gulf of Mexico and Florida.

Trematoda	Locality	Reference
Aspidogastridae
Lophotaspis vallei	Brazil, USA	Luhman, 1935; Araújo, 1941; Grenier, 2013
Brachycoeliidae
Cymatocarpus solearis	Brazil, USA	Linton, 1910; Pratt, 1914; Luhman, 1935; Greiner, 2013; Present report;
Calycodidae
Calycodes anthos	Brazil, USA	Werneck et al., 2008; Greiner, 2013
Gorgoderidae
Plesiochorus cymbiformis	Brazil, USA	Pratt, 1914; Cary, 1930; Luhman, 1935, Greiner, 2013; Werneck et al., 2018.
Pachypsolidae
Pachypsolus irroratus	USA	Linton, 1910; Greiner, 2013
Pachypsolus tertius	Gulf of Mexico	Pratt, 1914
Plagiorchiidae
Enodiotrema carettae	USA	Greiner, 2013
Enodiotrema megachondrus	Brazil	Werneck et al., 2019
Pachypsolus tertius	USA	Linton, 1910; Greiner, 2013
Pronocephalidae
Cricocephalus americanus	USA	Linton, 1910
Diaschistorchis ellipticus	Gulf of Mexico	Pratt, 1914
Diaschistorchis pandus	Brazil, USA	Greiner, 2013; Present report
Pleurogonius longiusculus	Brazil, USA	Luhman, 1935; Ernst and Ernst, 1977
Pleurogonius trigonocephalus	Brazil, USA	Luhman, 1935; Ernst and Ernst, 1977; Greiner, 2013
Pronocephalus trigonocephalus	Brazil	Viana, 1924
Pyelosomum chelonei	USA	Greiner, 2013
Pyelosomum renicapite	Brazil, USA	Luhman, 1935; Werneck et al., 2008; Greiner, 2013
Rhytidodidae
Rhytidodes gelatinosus	Brazil, USA	Viana, 1924; Travassos et al., 1969.; Luhman, 1935; Greiner, 2013; Present report
Rhytidodes secundus	USA	Pratt, 1914; Luhman, 1935
Spirorchiidae
Amphiorchis sp.	USA	Dutton, 2019
Carettacola bipora	USA	Manter and Larson, 1950; Stacy et al., 2010; Greiner, 2013
Carettacola sp.	USA	Jacobson et al., 2006
Hapalotrema mistroides	USA	Greiner, 2013; Dutton, 2019
Hapalotrema synorchis	Florida	Luhman, 1935
Hapalotrema pambanensis	USA	Stacy et al., 2010
Monticellius indicum	Brazil	Werneck et al., 2017
Neospirorchis pricei	USA	Manter and Larson, 1950; Stacy et al., 2010; Greiner, 2013
Neospirorchis sp.	USA	Jacobson et al., 2006
Styphlotrematidae
Styphlotrema solitaria	USA	Luhman, 1935; Greiner, 2013
Telorchiidae
Orchidasma amphiorchis	Argentina, Brazil, USA	Linton, 1910; Manter, 1931; Luhman, 1935; Boero and Led, 1974; Werneck et al., 2008; Greiner, 2013

Table 2

Nematodes and Cestodes identified in loggerhead turtle from the Neotropical region, Gulf of Mexico and Florida.

	Locality	Reference
Nematoda
Angiostomatidae
Angiostoma carettae	USA-	Bursey and Manire, 2006; Manire et al., 2008
Anisakidae
Sulcascaris sulcata	Uruguay, Brazil, USA	Lent and Teixeira de Freitas, 1948; Werneck et al., 2008; Greiner, 2013
Cucullanidae
Cucullanus carettae	USA	Greiner, 2013
Kathlaniidae
Kathlania leptura	Brazil, USA	Werneck et al., 2008; Greiner, 2013
Cestoda
Trypanorhynch cysts	USA	Greiner, 2013