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Checklist of sea turtles endohelminth in Neotropical region

Open Access
|Jul 2016

Full Article

Introduction

The Neotropical region corresponds to Central and South America, where five species of sea turtles are found: Green turtle (Chelonia mydas Linnaeus, 1758), loggerhead turtle (Caretta caretta Linnaeus, 1758), hawksbill turtle (Eretmochelys imbricata Linnaeus, 1766), Olive ridley turtle (Lepidochelys olivacea Eschscholtz, 1829) and leatherback turtle (Dermochelys coriacea Vandelli, 1761) (Lutz & Musick, 1996). The International Union for Conservation of Nature (IUCN, 2015) considers C. caretta, C. mydas and L. olivacea as endangered and both D. coriacea and E. imbricata as critically threatened.

Parasitological analyses of sea turtles have been conducted for many years and the results have contributed to a better understanding of the helminths of this group of hosts. Thus, the aim of this paper was to offer a comprehensive bibliographic review of the species of endohelminths found in sea turtles in the Neotropics.

Material and Methods

This checklist was developed using only scientific papers on endohelminths identified in sea turtles published between 1911 and 2016. Dissertations, theses and abstracts from conferences were not considered.

The data are presented in two forms: The first part of the paper presents a list of helminths (and synonyms) separated by family, genus and species and includes the infection site, location, infected host and author of the reference. The second part presents the hosts and a list of helminths reported in these hosts. For the classification, the taxonomic proposal presented by the World Register of Marine Species (WoRMS, 2015) was used.

Results

This checklist records the occurrence of 79 taxa of parasites. Seventy six represent the phylum Platyhelminthes (one from the order Aspidogastrida, 11 from the order Diplostomida and 64 from the order Plagiorchiida) represented by 14 families. Three represent the phylum Nematoda, in which two families have been found in the sea turtles C. mydas, C. caretta, E. imbricata, L. olivacea and D. coriacea. Overall helminths are reported in 12 countries and three are reported for the region in which the present study took place (i.e. the Caribbean Sea).

Parasite-Host list

  • Phylum Platyhelminthes Gegenbaur, 1859

  • Class Trematoda Rudolphi, 1808

  • Subclass Aspidogastrea Faust & Tang, 1936

  • Order Aspidogastrida Skrjabin & Guschanskaja, 1962

  • Superfamily Apidogastroidea Poche, 1907

  • Family Aspidogastridae Poche, 1907

  • Lophotaspis vallei (Stossich, 1899)

  • Site of infection: Esophagus and stomach.

  • Host and distribution: C. caretta from Brazil (Araújo, 1941)

  • Suborder Hemiurata Markevitsch 1951

  • Superfamily Hemiuroidea Looss, 1899

  • Family Sclerodistomidae Odner, 1927

  • Prosorchis psenopsis Yamaguti, 1934

  • Site of infection: Stomach.

  • Host and distribution: L. olivacea from México (Pérez-Ponce de Leon et al., 1996).

  • Suborder Pronocephalata Olson, Cribb, Tkach, Bray & Littlewood, 2003

  • Superfamily Paramphistomoidea Fischoeder, 1901

  • Family Cladorchiidae Fischoeder, 1901

  • Schizamphistomum erratumBlair, 1983 (Synonym: Schizamphistomoides erratumBlair, 1983)

  • Site of infection: Intestine.

  • Host and distribution: C. mydas from Costa Rica (Santoro et al., 2006).

  • Schizamphistomoides spinulosum (Looss, 1901) Stunkard, 1925

  • Site of infection: Large intestine.

  • Host and distribution: C. mydas from Panamá (Caballero et al., 1955).

  • Family Microscaphidiidae Looss, 1900

  • Angiodictyum anteroporum Chattopadhyaya, 1972 (Taxon inquirendum)

  • Site of infection: Large intestine.

  • Host and distribution: E. imbricata from Puerto Rico (Dyer et al., 1995a).

  • Angiodictyum parallelum (Looss, 1901) Looss, 1902 (Synonym: Microscaphidium parallelum Looss, 1901)

  • Site of infection: Small and large intestine.

  • Host and distribution:, C. mydas from Brazil (Werneck & Silva, 2015) and Puerto Rico (Dyer et al., 1991) and E. imbricata from Puerto Rico (Dyer et al., 1995c).

  • Deuterobaris cheloneiGupta, 1961.

  • Site of infection: Intestine.

  • Host and distribution: C. mydas from Trinidad (The West India) (Gupta, 1961).

  • Deuterobaris intestinalis Mehrotra, 1973

  • Site of infection: Intestine.

  • Host and distribution: C. mydas from Costa Rica (Santoro et al., 2006).

  • Microscaphidium aberrans Looss, 1902

  • Site of infection: Intestine.

  • Host and distribution: C. mydas from Panamá (Caballero, 1954)

  • Octangium sagitta (Looss, 1899) Looss, 1902

  • [Synonym: Microscapha sagitta Looss, 1899, Octangium hasta Looss, 1902, Octangium takanoi Kobayashi, 1921 (see Blair, 1987)].

  • Site of infection: Stomach and small and large intestine.

  • Host and distribution: C. mydas from Puerto Rico (Dyer et al., 1991) and E. imbricata from Puerto Rico (Fischthal & Acholonu, 1976; Dyer et al., 1995c).

  • Cricocephalus americanusVigueras, 1955

  • Site of infection: Stomach.

  • Host and distribution: E. imbricata from Cuba (Viegueras, 1955).

  • Cricocephalus resectus Looss, 1902

  • Site of infection: Esophagus and stomach.

  • Host and distribution: C. mydas from Costa Rica (Santoro et al., 2006).

  • Cricocephalus vitallani (Gupta, 1962)

  • (Synonym: Neocricocephalus vitallaniGupta, 1962)

  • Site of infection: Intestine.

  • Host and distribution: C. mydas from Caribbean Sea (Gupta, 1962).

  • Pleurogonius chelonii Mehra, 1939

  • (Synonym: Pleurogonius mehraiRuiz, 1946).

  • Site of infection: Intestine.

  • Host and distribution: C. mydas from Trinidad (The West Indies) (Gupta, 1961).

  • Pleurogonius sindhii Mehra, 1939

  • [Synonym: Pyelosomum sindhii (Mehra, 1939)].

  • Site of infection: Intestine.

  • Host and distribution: C. mydas from Costa Rica (Santoro et al., 2006) and Panamá (Caballero et al., 1955).

  • Pleurogonius solidus Looss, 1901

  • [Synonym: Pyelosomum solidum (Looss, 1901); Glyphicephalus solidus Looss, 1901].

  • Site of infection: Intestine.

  • Host and distribution: C. mydas from Costa Rica (Santoro et al., 2006) and E. imbricata from Cuba (Vigueras, 1955).

  • Pyelosomum renicapite (Leidy, 1856)

  • [Synonym: Astrorchis renicapite (Leidy, 1856), Monostomum nephrocephalum Diesing, 1858, Monostomum sphargidis MacCallum, 1921 and Pyelosomum longicaecum Luhman, 1935]

  • Site of infection: Small and large intestine.

  • Host and distribution: C. caretta from Brazil (Werneck et al., 2008a); D. coriacea from Brazil and Uruguay (Werneck et al., 2012) and Puerto Rico (Dyer et al., 1995b); L. olivacea from México (Pérez-Ponce de Leon et al., 1996).

  • Suborder Xiphidiata Olson Cribb, Tkach, Bray & Littlewood, 2003

  • Superfamily Gorgoderoidea Looss, 1901

  • Family Gorgoderidae Looss, 1899

  • Subfamily Anaporrhutinae Looss, 1901

  • Plesiochorus cymbiformis (Rudolphi, 1819) Looss, 1901

  • [Synonym: Phyllodistomum cymbiforme (Rudolphi, 1819; Plesiochorus cymbiformis elongatus Pigulevsky, 1953]

  • Site of infection: Urinary bladder and small intestine.

  • Host and distribution: C. mydas from Brazil (Binoti et al., 2016) and Panamá (Caballero, 1954); E. imbricata from Puerto Rico (Fischthal & Acholonu, 1976); L. olivacea from Costa Rica (Santoro & Morales, 2007).

  • Superfamily Plagiorchioidea Lühe, 1901

  • Family Brachycoeliidae Looss, 1899

  • Cymatocarpus solearis (Braun, 1899) Braun, 1901 (probably Synonym: Cymatocarpus undulatus Looss, 1899)

  • Site of infection: Esophagus, stomach and small intestine.

  • Host and distribution: C. mydas from Brazil (Werneck & Silva, 2015) and Mexico (Caballero, 1959); E. imbricata from Brazil (Werneck et al., 2015b)

  • Order Diplostomida Olson, Cribb, Tkach, Bray & Littlewood, 2003

  • Suborder Diplostomata Olson, Cribb, Tkach, Bray & Littlewood, 2003

  • Superfamily Schistosomatoidea Stiles & Hassall, 1898

  • Family Spirorchiidae Stunkard, 1921

  • Amphiorchis amphiorchis Price, 1934

  • Site of infection: Blood vessels of large intestine.

  • Host and distribution: E. imbricata from Puerto Rico (Fischthal & Acholonu, 1976).

  • Hapalotrema synorchis Luhman, 1935

  • Site of infection: Heart.

  • Host and distribution: E. imbricata from Puerto Rico (Fischthal & Acholonu, 1976).

  • Neospirorchis sp.

  • Site of infection: Small intestine, liver, heart, lung, body wash. Host and distribution: C. mydas from Brazil (Werneck & Silva, 2015).

  • Phylum Nematoda Rudolphi, 1808

  • Class Chromadorea Inglis, 1983

  • Subclass Chromadoria Adamson, 1987

  • Order Rhabditida Chitwood, 1933

  • Suborder Spirurina Railliet & Henry, 1915

  • Infraorder Ascaridomorpha De Ley & Blaxter 2002

  • Superfamily Ascaridoidea Baird, 1853

  • Family Anisakidae Skrjabin e Karokhin, 1945

  • Sulcascaris sulcata (Rudolphi, 1819)

  • Site of infection: Esophagus, stomach and small intestine.

  • Host and distribution: C. caretta from Brazil (Werneck et al., 2008a) and Uruguay (Lent & Teixeira de Freitas, 1948); C. mydas from Brazil (Teixeira de Freitas & Lent, 1946).

  • Anisakis larvae

  • Site of infection: Body wash.

  • Host and distribution: E. imbricata from (Werneck et al., 2015b).

  • Superfamily Cosmocercoidea Travassos, 1935

  • Family Kathlaniidae Travassos, 1918

  • Kathlania leptura (Rudolphi, 1819)

  • Site of infection: Small and large intestine.

  • Host and distribution: C. caretta from Brazil (Werneck et al., 2008a); C. mydas from Brazil (Travassos, 1918).

  • Nematode larvae

  • Site of infection: Esophagus, stomach, small and large intestine, liver.

  • Host and distribution: C. mydas from Brazil (Werneck & Silva, 2015).

Host-Parasite list
Chelonia mydas

Digeneans

Family Calycodidae

  • Calycodes anthos

Family Rhytidodidae

  • Rhytidodes gelatinosus

  • Rhytidodoides intestinalis

  • Rhytidodoides similis

Family Cladorchiidae

Schizamphistomum erratum

Schizamphistomum scleroporum

Schizamphistomoides spinulosum

Family Microscaphidiidae

  • Angiodictyum longum

  • Angiodictyum parallelum

  • Deuterobaris chelonei

  • Deuterobaris intestinalis

  • Deuterobaris proteus

  • Microscaphidium aberrans

  • Microscaphidium reticulare

  • Microscaphidium warui

  • Neoctangium travassosi

  • Octangium hyphalum

  • Octangium sagitta

  • Polyangium linguatula

Family Pronocephalidae

  • Adenogaster serialis

  • Charaxicephaloides polyorchis

  • Charaxicephalus robustus

  • Cricocephalus albus

  • Cricocephalus megastomum

  • Cricocephalus resectus

  • Cricocephalus vitallani

  • Desmogonius desmogonius

  • Diaschistorchis pandus

  • Metacetabulum invaginatum

  • Pleurogonius americanus

  • Pleurogonius chelonii

  • Pleurogonius grocotti

  • Pleurogonius linearis

  • Pleurogonius longiusculus

  • Pleurogonius sindhii

  • Pleurogonius solidus

  • Pleurogonius tortugueroi

  • Pleurogonius trigonocephalus

  • Pleurogonius lobatus

  • Pronocephalus obliquus

  • Pronocephalus trigonocephalus

  • Pyelosomum cochlear

  • Pyelosomum crassum

  • Pyelosomum posterorchis

  • Rameshwarotrema uterocrescens

  • Ruicephalus minutus

Family Gorgoderidae

  • Plesiochorus cymbiformis

Family Pachypsolidae

  • Pachypsolus irroratus

Family Brachycoeliidae

  • Cymatocarpus solearis

Family Plagiorchiidae

  • Enodiotrema reductumFamily Telorchiidae

  • Orchidasma amphiorchisFamily Spirorchiidae

  • Amphiorchis indicus

  • Amphiorchis solus

  • Carettacola stunkardi

  • Hapalotrema postorchis

  • Learedius learedi

  • Learedius orientalis

  • Monticellius indicum

  • Neospirorchis schistosomatoides

Nematodes

FamilyAnisakidae

  • Sulcascaris sulcata

Family Kathlaniidae

  • Kathlania leptura.

  • Tonaudia freitasi

Eretmochelys imbricata

Digeneans

Family Calycodidae

  • Calycodes caborojoensis

Familia Rhytidodidae

  • Rhytidodes gelatinosus

Family Cladorchiidae

  • Schizamphistomum scleroporum

Family Microscaphidiidae

  • Angiodictyum anteroporum

  • Angiodictyum mooreae

  • Angiodictyum parallelum

  • Neoctangium travassosi

  • Octangium sagitta

Family Pronocephalidae

  • Adenogaster serialis

  • Cricocephalus albus

  • Cricocephalus americanus

  • Cricocephalus megastomum

  • Diaschistorchis pandus

  • Metacetabulum invaginatum

  • Pleurogonius laterouteus

  • Pleurogonius latus

  • Pleurogonius linearis

  • Pleurogonius lobatus

  • Pleurogonius longibursatus

  • Pleurogonius puertoricensis

  • Pleurogonius solidus

  • Pleurogonius trigonocephalus

  • Pleurogonius stenobursatum

  • Pronocephalus obliquus

  • Pyelosomum crassum

  • Pyelosomum posterorchis

  • Rameshwarotrema uterocrescens

Family Gorgoderidae

  • Plesiochorus cymbiformis

Family Pachypsolidae

  • Pachypsolus irroratus

Family Brachycoeliidae

  • Cymatocarpus solearis

Family Plagiorchiidae

  • Enodiotrema megachondrus

  • Enodiotrema reductum

Family Styphlotrematidae

  • Styphlotrema solitaria

Family Telorchiidae

  • Orchidasma amphiorchis

Family Spirorchiidae

  • Amphiorchis amphiorchis

  • Amphiorchis caborojoensis

  • Carettacola stunkardi

  • Hapalotrema postorchis

  • Hapalotrema synorchis

  • Learedius learedi

  • Learedius orientalis

  • Monticellius indicum

Nematodes

FamilyAnisakidae

  • Anisakis larvae

Lepidochelys olivacea

Digeneans

Family Calycodidae

  • Calycodes anthos

Family Sclerodistomidae

  • Prosorchis psenopsis

Family Pronocephalidae

  • Adenogaster serialis

  • Pleurogoius lobatus

  • Pyelosomum cochlear

  • Pyelosomum renicapite

Family Gongoderidae

  • Plesiochorus cymbiformis

Family Pachypsolidae

  • Pachypsolus irroratus

Family Plagiorchiidae

  • Enodiotrema megachondrus

Family Telorchiidae

  • Orchidasma amphiorchis

Caretta caretta

Aspidogastrids Family Aspidogastridae

  • Lophotaspis vallei

Digeneans Family Calycodidae

  • Calycodes anthos

Familia Rhytidodidae

  • Rhytidodes gelatinosus

Family Pronocephalidae

  • Pronocephalus trigonocephalus

  • Pyelosomum renicapite

Family Telorchiidae

  • Orchidasma amphiorchis

Nematodes

FamilyAnisakidae

  • Sulcascaris sulcata

Family Kathlaniidae

  • Kathlania leptura

Dermochelys coriacea

Digeneans Family Calycodidae

  • Calycodes anthos

Family Pronocephalidae

  • Pyelosomum renicapite

Discussion

This checklist demonstrates the occurrence of 79 taxa of helminthes parasites. Seventy six represent the phylum Platyhelminthes (one from the order Aspidogastrida, 11 from the order Diplostomida and 64 from the order Plagiorchiida) represented by 14 families. Three represent the phylum Nematoda, Five species of sea turtles (C. mydas, C. caretta, E. imbricata, L. olivacea and D. coriacea) had records of helminths in the Neotropical region. The host with the largest number of records of parasites was C. mydas (records of only the genus were excluded from the calculation), representing 62 parasite species, followed by E. imbricata (42 species), L. olivacea (10 species), C. caretta (8 species) and D. coriacea (2 species). Overall helminths are reported in 12 countries and three are reported for the region in which the present study took place (i.e. the Caribbean Sea).

Among the countries in which helminths are reported, Brazil, Costa Rica and Panamá have the largest number of records for C. mydas. Lepidochelys olivacea is the best studied sea turtle from Mexico, with eight records of parasite species. Porto Rico stands out for the large number of parasite species reported in E. imbricata, such as C. caborojoensis, A. anteroporum, A. mooreae, P. laterouterus, P. puertoricensis, P. latus, P. sternobursatum, A. amphiorchis and H. synorchis, which are only found in this country in this region.

Dermochelys coriacea had the fewest reports of parasites from the region with only C. anthos and P. renicapite) being detected. This species of turtle has been studied the least of all marine turtles regarding its parasites around the world (see Werneck et al., 2012). This paper presents the largest compilation of data on helminth parasites in sea turtles in the Neotropical region published to date.

DOI: https://doi.org/10.1515/helmin-2016-0045 | Journal eISSN: 1336-9083 | Journal ISSN: 0440-6605
Language: English
Page range: 211 - 223
Submitted on: Dec 17, 2015
Accepted on: May 6, 2016
Published on: Jul 22, 2016
Published by: Slovak Academy of Sciences, Mathematical Institute
In partnership with: Paradigm Publishing Services
Publication frequency: 4 times per year

© 2016 M. R. Werneck, R. J. Da Silva, published by Slovak Academy of Sciences, Mathematical Institute
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.