Ophiotaenia crotali

Trindade, Luiz Felipe Ferreira, Jos, Adriano, F, e Silva, elix, Reb, Gabriel Lima, elo, Neves, Jorge Kevin Silva, Paix ˜ ao, Deivyson Jo ˜ ao Malcher, Dias-Souza, Marcos Roberto, Costa-Campos, Carlos Eduardo, Santos, Jeannie Nascimento & Melo, Francisco Tiago Vasconcelos, 2024, Ophiotaenia karipuna n. sp. (Eucestoda: Proteocephalidae), a parasite of Erythrolamprus miliaris (Linnaeus, 1758), with redescription of Ophiotaenia arandasi (Santos and Rolas, 1973) from the Brazilian Amazon, International Journal for Parasitology: Parasites and Wildlife 24, pp. 100930-100930 : 100930-

8 O. crotali Crotalus durissus Viperidae Venezuela

O. elongata Snake ND Brazil

O. euzeti Bothrops jararaca Viperidae Brazil

O. ecuadorensis Boana geographicus Hylidae Ecuador

O. flava Coluber sp Colubridae Brazil

O. gilberti Thamnodynastes Dipsadidae Paraguay pallidus

O. habanensis Tropidophis pardalis Tropidophiidae Cuba

O. hernandezi Rana sp. Ranidae Guatemala

O. hyalina Coluber sp. Colubridae Brazil

O. jarara Bothrops jararaca Viperidae Brazil

O. joanae Xenodon neuwiedii Dipsadidae Brazil

O. macrobothria Micrurus corallinus Elapidae Brazil O. micruricola Micrurus diastema Elapidae Mexico

O. nattereri Coluber sp. Colubridae Brazil

O. noei Calyptocephalella Calyptocephalellidae Chile gayi

O. nicolae Thecadactylus Phyllodactylidae Ecuador rapicauda

O. olseni Boana geographica Hylidae Ecuador

630–735 present 88–212 17–26% 40–55% ant–post

730 absent 46–58 ND 33% posterior

300 present 120–140 23–26% 32–34% ND

280–385 absent 100–177 15–24% 15–29% anterior

740 absent 180–220 20% 44–48% ant/post

700 absent ND 16–20% 38% ND 225–296 absent 34–60 20–38% 25–50% ant/post 1000–1300 absent 130–160 17–25% 50% posterior

990–1220 present 107–158 14–22% 40–54% ant–post

ND ND 308–412 7–12% 41–43% ND

ND ND 26–44 ND 50% ND

300–310 absent 116–141 25–34% 24–42% ant-post

450 present 92–121 23–32% 42–45% posterior 500–600 absent 45–60 50% 20–40% ant-post 140–145 present 57–91 15–23% 42–50% ant–post

360 absent 31–51> 50% 60% ND

880 absent 59–78 24–26% 17–18% posterior 680–800 absent 50–55 50% 33% ant-post 1100–1200 present 150 27–34% 50% anterior

480–790 present 147–210 14–25% 28–56% ant–post

400–500 absent 50–60> 50% 20–33% ant-post 720–760 absent 121–169 14–20% 48–56% posterior

250 absent 80–100 28–33% <50% ant-post

410–580 absent 200–250 22–27% 39% ant-post

325–340 present 142–204 21–33% 34–53% ant–post

430–490 absent 126–160 19% 59% posterior

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eggs. Finally, we observed type 1 uterine development in both materials of Ophiotaenia arandasi , contrary to Scholz et al. (2023b) that assigned type 2 for this species. All this newly provided data confirm that Ophiotaenia arandasi is a valid taxon.

Intraspecific variations have been reported in other Ophiotaenia species, mainly in characters such as: number of uterine diverticula, size of scolex, number and average size of testes ( Rego, 1962; Scholz et al., 2023a). However, we did not find intraspecific variation in the morphometric data among specimens of the present study, re-examination of type series and measurements provided in the original description of Santos and Rolas (1973) from E. miliaris . Additionally, despite some studies suggest that Ophiotaenia spp. exihibit host specificity ( Ammann and de Chambrier, 2008; de Chambrier et al., 2015), there are some reports of Ophiotaenia species in multiple congeneric hosts ( Santos and Rolas, 1973; de Chambrier, Vaucher and Renaud, 1992; de Chambrier et al., 2023). Our findings and those previous reports suggest that the host specificity of Ophiotaenia might be less strict than it was previously assumed.

The hosts registered for O. arandasi are phylogenetically related and their geographical distributions overlap ( Entiauspe-Neto et al., 2021). E. taeniogaster is more abundant in the Amazon and the northern Atlantic Forest, while E. miliaris is widely distributed in the Atlantic Forest, and other regions in brazilian territory, except Pampas Grasslands ( Nogueira et al., 2019). Our results support that sympatric hosts, might share some cestode taxa since they are exposed to similar ecological and phylogenetic conditions ( Aho, 1990; Krasnov et al., 2011).

Ophiotaenia karipuna n. sp. is the third species described parasitizing Erythrolamprus miliaris in Brazil. Although, O. arandasi and O. hyalina parasitize the same host species, they differ in various morphological aspects, primarily in the absence of the apical organ, present in O. karipuna .

Our study provides an ultrastructural analysis for O. karipuna n. sp. and O. arandasi . The SEM images showed details of the distribution of microtrichia on the tegument surface, on the upper edge of the sucker, luminal region of the suckers, and tegument surface between the suckers and the neck in both species. Additionally, it was possible to observe the presence of a vestigial apical sucker in O. karipuna n. sp., a unique characteristic of the new species compared to its Neotropical congeners.

The morphological data obtained by light and scanning electron microscopy strongly support the independent species-status of O. karipuna n. sp. from Erythrolamprus miliaris . The taxonomic validity of O. arandasi is confirmed based on a re-examination of the type series, and new collected specimens. We also provide the first ultrastructural analysis of the species, and new host and locality records. Therefore, considering the great diversity of snakes and the comparatively small number of Ophiotaenia species in Brazil, future studies of proteocephalids are valuable insights into the systematics and evolutionary history of the group.

Ethics approval

All procedures contributing to this work comply with all applicable institutional, national, and international guidelines for animal care and use Animal Research Ethics Committee, Federal University of Par´a, under license N8341260821CEUA/UFPa. The present study was approved by Instituto Chico Mendes de Conservaç˜ao da Biodiversidade (ICMBio), Brazil, and host specimens were collected under license number SISBIO: 53,527–4.

Funding

This study was supported by PROPESP/UFPA (PAPQ), CAPES/ PPGZOOL/UFPa, Fundaç˜ao Amazˆonia de Amparo a Estudos e Pesquisa (FAPESPA) (01/2021 – PROGRAMA DE APOIO A NÚCLEOS EMER- GENTES) and Conselho Nacional de Desenvolvimento Científico e Tecnol´ogico (CNPq) Research productivity scholarship of CNPq to

9

COSTA–CAMPOS, C.E (Process number 307697/2022–3); MELO , F.T.V. (Process number 314116/2021–4) and SANTOS, J.N. (Process number 305552/2019–8).

CRediT authorship contribution statement

Luiz Felipe Ferreira Trindade: Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing. Adriano Jose´Silva F´elix: Conceptualization, Data curation, Formal analysis, Methodology, Resources, Writing – review & editing. Gabriel Lima Rebˆelo: Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing. Jorge Kevin Silva Neves: Data curation, Formal analysis, Writing – original draft, Writing – review & editing. Deivyson Joao ˜Malcher Paix˜ao: Investigation, Data curation, Formal analysis, Writing – review & editing. Marcos Roberto Dias-Souza: Data curation, Methodology, Visualization, Writing – review & editing. Carlos Eduardo Costa-Campos: Conceptualization, Funding acquisition, Methodology, Resources, Visualization, Writing – review & editing. Jeannie Nascimento Santos: Conceptualization, Funding acquisition, Methodology, Supervision, Writing – review & editing. Francisco Tiago Vasconcelos Melo : Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Writing – original draft, Writing – review & editing.