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Morphological characterization of the digestive tube of hawksbill sea turtle (Eretmochelys imbricata) hatchlings

Published online by Cambridge University Press:  05 September 2022

Radan Elvis Matias de Oliveira*
Affiliation:
Postgraduate Program in Animal Science, Federal University of the Semi-Arid Region, Mossoró, Rio Grande do Norte 59625-900, Brazil Center for Environmental Studies and Monitoring – CEMAM, Areia Branca, Rio Grande do Norte 59655-000, Brazil. Cetáceos da Costa Branca Project, University of the State of Rio Grande do Norte – PCCB-UERN, Mossoró, Rio Grande do Norte 59610-210, Brazil
Fernanda Loffler Niemeyer Attademo
Affiliation:
Center for Environmental Studies and Monitoring – CEMAM, Areia Branca, Rio Grande do Norte 59655-000, Brazil.
Ana Caroline Freitas Caetano de Sousa
Affiliation:
Department of Animal Sciences, Federal University of the Semi-Arid Region, Mossoró, Rio Grande do Norte 59625-900, Brazil
João Vitor de Oliveira Gurgel
Affiliation:
Department of Animal Sciences, Federal University of the Semi-Arid Region, Mossoró, Rio Grande do Norte 59625-900, Brazil
Marcela dos Santos Magalhães
Affiliation:
Department of Morphology, Federal University of Amazonas, Manaus, Amazonas 69080-900, Brazil
Carlos Eduardo Bezerra de Moura
Affiliation:
Postgraduate Program in Animal Science, Federal University of the Semi-Arid Region, Mossoró, Rio Grande do Norte 59625-900, Brazil
Ana Bernadete Lima Fragoso
Affiliation:
Center for Environmental Studies and Monitoring – CEMAM, Areia Branca, Rio Grande do Norte 59655-000, Brazil. Cetáceos da Costa Branca Project, University of the State of Rio Grande do Norte – PCCB-UERN, Mossoró, Rio Grande do Norte 59610-210, Brazil
Flávio José de Lima Silva
Affiliation:
Center for Environmental Studies and Monitoring – CEMAM, Areia Branca, Rio Grande do Norte 59655-000, Brazil. Cetáceos da Costa Branca Project, University of the State of Rio Grande do Norte – PCCB-UERN, Mossoró, Rio Grande do Norte 59610-210, Brazil Doctoral Program in Development and Environment (PRODEMA), Federal University of Rio Grande do Norte (UFRN), Natal, Rio Grande do Norte 59064-741, Brazil
Moacir Franco de Oliveira
Affiliation:
Postgraduate Program in Animal Science, Federal University of the Semi-Arid Region, Mossoró, Rio Grande do Norte 59625-900, Brazil
*
*Corresponding author: Radan Elvis Matias de Oliveira, E-mail: radan_elvis@hotmail.com
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Abstract

Morphological studies concerning the digestive system can further information on animal diets, thus aiding in the understanding of feeding behavior. Given the scarcity of information on sea turtle digestive system morphology, the aim of the present study was to describe the digestive tube (DT) morphology of Eretmochelys imbricata hatchlings to further understand the diet of these individuals in the wild. DT samples from 10 stillborn turtles (undefined sex) were analyzed at the macro and microscopic levels. The esophagus, stomach, small intestine (SI), and large intestine (LI) are described. Histologically, the DT is formed by four tunics, the mucosa, submucosa, muscular, and adventitia or serosa. The esophagus is lined by keratinized stratified squamous epithelium, while the remainder of the DT is lined by a simple columnar epithelium. The esophagus mucosa is marked by conical, pointed papillae. The stomach comprises three regions, the cardiac, fundic, and pyloric and is covered by neutral mucous granular cells. The intestinal mucosa presents absorptive cells with microvilli, neutral and acidic goblet cells, and mucosa-associated lymphoid tissue. The SI is significantly longer than the LI (p value = 0.006841). These morphological findings are strong indications of adaptations to a carnivorous diet in this hawksbill turtle age group.

Type
Micrographia
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

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References

Allen, A, Flemström, G, Garner, A & Kivilaakso, E (1993). Gastroduodenal mucosal protection. Physiol Rev 73, 823857.CrossRefGoogle ScholarPubMed
Andrady, AL (2011). Microplastics in the marine environment. Mar Pollut Bull 62, 15961605.CrossRefGoogle ScholarPubMed
Balesienfer, DC & Vogt, RC (2006). Diet of Podocnemis unifilis (Testudines, Podocnemididae) during the dry season in the Mamirauá Sustainable Development Reserve, Amazonas, Brazil. Chelonian Conserv Biol 5, 312317.CrossRefGoogle Scholar
Behmer, OA, Tolosa, EMC & Freitas Neto, AG (1976). Manual de técnicas para histologia normal e patológica. São Paulo, SP: Editora da Universidade de São Paulo.Google Scholar
Bell, FR (1979). The relevance of the new knowledge of gastrointestinal hormones to veterinary science. Vet Res Commun 2, 305314.CrossRefGoogle Scholar
Blaker, PA & Irving, P (2014). Physiology and function of the small intestine. In Advanced Nutrition and Dietetics in Gastroenterology, Lomer, M (Ed.), pp. 2127. Nova Jersey, EUA: John Wiley & Sons.CrossRefGoogle Scholar
Bowen, BW (1995). Tracking marine turtles with genetic makers – voyages of ancient mariners. Bioscience 45, 528534.CrossRefGoogle Scholar
Bugoni, L, Krause, L & Petry, MV (2001). Marine debris and human impacts on sea turtles in southern Brazil. Mar Pollut Bull 42, 13301334.CrossRefGoogle ScholarPubMed
Calais Junior, A, David, JAO & Nunes, LC (2016). Caracterização morfológica do esôfago de tartarugas-verdes (chelonia mydas). Arq Bras Med Vet Zootec 68, 127135.CrossRefGoogle Scholar
Carrión-Cortez, J, Canales-Cerro, C, Arauz, R & Riosmena-Rodríguez, R (2013). Habitat use and diet of juvenile eastern pacific hawksbill turtles (Eretmochelys imbricata) in the North Pacific Coast of Costa Rica. Chelonian Conserv Biol 12, 235245.CrossRefGoogle Scholar
Chen, H, Ye, M, Lu, Y, Duan, J, Li, P & Gu, H (2015). Structure and function of the gastrointestinal tract of the green turtle (Chelonia mydas) hatchling. Asian Herpetol 6, 317330.Google Scholar
Croix, JA, Carbonero, F, Nava, GM, Russell, M, Greenberg, E & Gaskins, HR (2011). On the relationship between sialomucin and sulfomucin expression and hydrogenotrophic microbes in the human colonic mucosa. PLoS One 6, e24447.CrossRefGoogle ScholarPubMed
Eichholz, A & Crane, RK (1965). Studies on the organization of the brush border in intestinal epithelial cells. J Cell Biol 26, 687691.CrossRefGoogle ScholarPubMed
Farias, DSD, Rossi, S, Bomfim, AC, Fragoso, ABL, Santos-Neto, EB, Silva, FJL, Lailson-Brito, J, Navoni, JA, Gavilan, SA & Amaral, VS (2022). Bioaccumulation of total mercury, copper, cadmium, silver, and selenium in green turtles (Chelonia mydas) stranded along the Potiguar Basin, northeastern Brazil. Chemosphere 299, 19.Google Scholar
Fujihara, J, Kunito, T, Kubota, R & Tanabe, S (2003). Arsenic accumulation in livers of pinnipeds, seabirds, and sea turtles: Subcellular distribution and interaction between arsenobetaine and glycine betaine. Comp Biochem Physiol C Toxicol Pharmacol 136, 287296.CrossRefGoogle ScholarPubMed
Gad, A (1982). Pathophysiology of gastrointestinal mucins. Adv Physiol Sci 29, 161183.Google Scholar
Hildebrand, M (1995). Analise da Estrutura dos Vertebrados. São Paulo, SP: Atheneu.Google Scholar
Holmberg, A, Kaim, J, Persson, A, Jensen, J, Wang, T & Holmgren, S (2002). Effects of digestive status on the reptilian gut. Comp Biochem Physiol A Mol Integr Physiol 133, 499518.CrossRefGoogle ScholarPubMed
International Committee on Veterinary Gross Anatomical Nomenclature (2017). Nomina Anatomica Veterinaria. Knoxville, TX: World Association of Veterinary Anatomists.Google Scholar
Junqueira, LC & Carneiro, J (2017). Histologia Básica. Rio de Janeiro, RJ: Guanabara Koogan.Google Scholar
Krause, WJ (1981). Morphological and histochemical observations on the duodenal glands of eight wild ungulate species native to North America. Am J Anat 162, 167181.CrossRefGoogle ScholarPubMed
Ku, SK, Lee, HS, Lee, JH & Park, KD (2001). An immunohistochemical study on the endocrine cells in the alimentary tract of the Red-eared slider (Trachemys scripta elegans). Anat Histol Embryol 30, 3339.CrossRefGoogle Scholar
Lutz, PL & Musick, JA (1997). The Biology of Sea Turtles. Boca Raton, FL: CRC Press.Google Scholar
Lynch, MJ, Raphael, SS, Mellor, LD, Spare, PD & Inwood, JH (1972). Métodosde Laboratorio. Ciudad de México, MXC: Interamericana.Google Scholar
Magalhães, MS, Freitas, ML, Silva, NB & Moura, CEB (2010). Morfologia do tubo digestório da tartaruga-verde (Chelonia mydas) [Morphology of the digestive tube of the green turtle (Chelonia mydas)]. Pesq Vet Bras 30, 676684.CrossRefGoogle Scholar
Magalhães, MS, Santos, AJB, Silva, NB & Moura, CEB (2012). Anatomy of the digestive tube of sea turtles (Reptilia: Testudines). Zoologia 29, 7076.CrossRefGoogle Scholar
Magalhães, MS, Vogt, RC, Barcellos, JFM, Moura, CEB & Silveira, RD (2014). Morphology of the digestive tube of the Podocnemididae in the Brazilian Amazon. Herpetologica 70, 449463.CrossRefGoogle Scholar
Mortimer, JA & Donnelly, M (2008). Eretmochelys imbricata, Hawksbill Turtle (IUCN SSC Marine Turtle Specialist Group). The IUCN Red List of Threatened Species.Google Scholar
Nelms, SE, Duncan, EM, Broderick, AC, Galloway, TS, Godfrey, MH, Hamann, M, Lindeque, PK & Godley, BJ (2016). Plastic and marine turtles: A review and call for research. ICES J Mar Sci 73, 165181.CrossRefGoogle Scholar
Oliveira, REM, Attademo, FLN, Freire, ACB, Pires, JML, Farias, DSD, Bomfim, AC, Oliveira, RM, Gavilan, SA, Silva, FJL & Oliveira, MF (2021). Pathoanatomical findings of a green turtle (Chelonia mydas) victim of collision with a motorboat. Acta Vet 71, 490499.CrossRefGoogle Scholar
Ontiveros-Tlachi, R, Muñoz-Tenería, FA & Anzaldúa-Arce, SR (2014). Histological and histochemical features of the small intestine in loggerhead sea turtle hatchlings (Caretta caretta). Veterinaria México OA 1, 115.CrossRefGoogle Scholar
Perez-Eman, JL & Paollilo, OA (1997). Diet of the Pelomedusid turtle Peltocephalus dumerilianus in the Venezuelan Amazon. J Herpetol 31, 173179.CrossRefGoogle Scholar
Rahman, MS & Sharma, DK (2014). Morphometric, anatomical and histological features of gastrointestinal tract (GIT) of freshwater turtle. Pangshura Tentoria. Int J Sci Eng Res 5, 9094.Google Scholar
Reich, KJ, Bjorndal, KA & Bolten, AB (2007). The “lost years” of green turtles: Using stable isotopes to study cryptic life stages. Biol Lett 3, 712714.CrossRefGoogle Scholar
Ricklefs, RE (2003). A Economia da Natureza. Rio de Janeiro, RJ: Guanabara Koogan.Google Scholar
Rincon-Diaz, MP, Diez, CE, van Dam, RP & Sabat, AM (2011). Effect of food availability on the abundance of Juvenile Hawksbill sea turtles (Eretmochelys imbricata) in inshore aggregation areas of the Culebra Archipelago, Puerto Rico. Chelonian Conserv Biol 10, 213221.CrossRefGoogle Scholar
Rizzi, M, Rodrigues, FL, Medeiros, L, Ortega, I, Rodrigues, L, Monteiro, DS, Kessler, F & Proietti, MC (2019). Ingestion of plastic marine litter by sea turtle in southern Brazil: Abundance, characteristics and potential selectivity. Mar Pollut Bull 140, 536548.CrossRefGoogle ScholarPubMed
Romer, AS & Parsons, TS (1986). The Vertebrate Body. Los Angeles, CA: Saunders College Pub.Google Scholar
Saeki, K, Sakakibara, H, Sakai, H, Kunito, T & Tanabe, S (2000). Arsenic accumulation in three species of sea turtles. BioMetals 13, 241250.CrossRefGoogle ScholarPubMed
Sakata, T & Engelhardt, W (1981). Luminar mucin in the large intestine of mice, rats and Guinea pigs. Cell Tissue Res 219, 629635.CrossRefGoogle Scholar
Sanderson, J & Mallinson, C (2002). Basic functions of the gut. In Food Allergy and Intolerance, Brostoff, J & Challacombe, S (Eds.), pp. 1735. London: Saunders.Google Scholar
Souza, AC & Vogt, RC (2008). Analysis of the stomach contents of two species of turtles of the Amazon: Peltocephalus dumerilianus and Podocnemis erythrocephala. In: Abstracts. 6th World Congress of Herpetology, Manaus.Google Scholar
Stevens, CE & Hume, ID (1998). Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78, 393427.CrossRefGoogle ScholarPubMed
Tarakçi, BG, Köprücü, SF & Yaman, M (2005). An immunohistochemical study on the endocrine cells in the gastrointestinal tract of the freshwater turtle, Mauremys caspica caspica. Turk J Vet Anim Sci 29, 581587.Google Scholar
Timmermans, JP, Scheuermann, DW, Gabriel, R, Adriaensen, D, Fekete, E & De Groodf-Lasseel, MHA (1991). The innervation of the gastrointestinal tract of a chelonian reptile, Pseudemys scripta elegans. I. Structure and topography of the enteric nerve plexuses using neuron-specific enolase immunohistochemistry. Histochemistry 95, 397402.CrossRefGoogle ScholarPubMed
Tolosa, EMC, Rodrigues, CJ, Behmer, OA & Freitas Neto, AG (2003). Manual de Técnicas para Histologia Normal e Patológica. Barueri, SP: Manole.Google Scholar
Vieira-Lopes, DA, Nascimento, AAD, Sales, A, Ventura, A, Novelli, IA, Sousa, BM & Pinheiro, NL (2014). Histology and histochemistry of the digestive tract of Phrynops geoffroanus (Testudines, Chelidae). Acta Amaz 44, 135142.CrossRefGoogle Scholar
Vogt, RC (2008). Tartarugas da Amazônia. Peru: Wust Ediciones.Google Scholar
Von Brandis, RG, Mortimer, JA, Reilly, BK, Van Soest, RWM & Branch, GM (2014). Diet composition of Hawksbill Turtles (Eretmochelys imbricata) in the Republic of Seychelles. Western Indian Ocean J Mar Sci 13, 8191.Google Scholar
Wilcox, C, Puckridge, M, Schuyler, QA, Townsend, K & Hardesty, BD (2018). A quantitative analysis linking sea turtle mortality and plastic debris ingestion. Sci Rep 8, 111.CrossRefGoogle ScholarPubMed
Work, TM (2000). Manual de Necropsia de Tortugas Marinas para Biologos en Refugios o Areas Remotas. Hawaii Field Station: National Wildlife Health Center.Google Scholar
Wyneken, J (2004). La Anatomía de las Tortugas Marinas. Miami, FL: U.S. Department of Commerce, NOAA Technical Memorandum NMFS-SEFSC-470.Google Scholar