Hostname: page-component-848d4c4894-8kt4b Total loading time: 0 Render date: 2024-06-24T05:31:10.177Z Has data issue: false hasContentIssue false
  • English
  • Français

Monitoring green sea turtles in Brazilian feeding areas: relating body condition index to fibropapillomatosis prevalence

Published online by Cambridge University Press:  10 September 2019

Silmara Rossi Open the ORCID record for Silmara Rossi [Opens in a new window] ,
Angélica María Sánchez-Sarmiento Open the ORCID record for Angélica María Sánchez-Sarmiento [Opens in a new window] ,
Robson Guimarães dos Santos Open the ORCID record for Robson Guimarães dos Santos [Opens in a new window] ,
Roberta Ramblas Zamana ,
Fabiola Eloisa Setim Prioste ,
Marco Aurélio Gattamorta Open the ORCID record for Marco Aurélio Gattamorta [Opens in a new window] ,
Pablo Felipe Cruz Ochoa ,
José Henrique Hildebrand Grisi-Filho Open the ORCID record for José Henrique Hildebrand Grisi-Filho [Opens in a new window]  and
Eliana Reiko Matushima Open the ORCID record for Eliana Reiko Matushima [Opens in a new window]
Silmara Rossi*
Affiliation:
Universidade Federal do Rio Grande do Norte (UFRN), Centro de Biociências, Departamento de Morfologia, Laboratório de Morfofisiologia Comparada, Campus Universitário UFRN, Lagoa Nova, CEP 59072-970, Natal/Rio Grande do Norte, Brazil Grupo de Pesquisa sobre Fibropapilomatose em Tartarugas Marinhas, Universidade de São Paulo (USP), Av. Prof. Dr Orlando Marques de Paiva 87, Cidade Universitária, CEP 05508-270, São Paulo/São Paulo, Brazil
Angélica María Sánchez-Sarmiento
Affiliation:
Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo (USP), Av. Prof. Dr Orlando Marques de Paiva 87, Cidade Universitária, CEP 05508-270, São Paulo/São Paulo, Brazil
Robson Guimarães dos Santos
Affiliation:
Laboratório de Biologia Marinha e Conservação, Instituto de Ciências Biológicas e da Saúde, Universidade Federal de Alagoas, Av. Lourival Melo Mota, S/N, Tabuleiro do Martins, CEP 57072-970, Maceió/Alagoas, Brazil
Roberta Ramblas Zamana
Affiliation:
Grupo de Pesquisa sobre Fibropapilomatose em Tartarugas Marinhas, Universidade de São Paulo (USP), Av. Prof. Dr Orlando Marques de Paiva 87, Cidade Universitária, CEP 05508-270, São Paulo/São Paulo, Brazil Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo (USP), Av. Prof. Dr Orlando Marques de Paiva 87, Cidade Universitária, CEP 05508-270, São Paulo/São Paulo, Brazil
Fabiola Eloisa Setim Prioste
Affiliation:
Grupo de Pesquisa sobre Fibropapilomatose em Tartarugas Marinhas, Universidade de São Paulo (USP), Av. Prof. Dr Orlando Marques de Paiva 87, Cidade Universitária, CEP 05508-270, São Paulo/São Paulo, Brazil Universidade São Judas, Rua Taquari, 546, Mooca, CEP 03166-000, São Paulo/SP, Brazil
Marco Aurélio Gattamorta
Affiliation:
Grupo de Pesquisa sobre Fibropapilomatose em Tartarugas Marinhas, Universidade de São Paulo (USP), Av. Prof. Dr Orlando Marques de Paiva 87, Cidade Universitária, CEP 05508-270, São Paulo/São Paulo, Brazil Escola de Engenharia e Arquitetura, Faculdades Metropolitanas Unidas (FMU), Av. Liberdade 899, Liberdade, CEP 01503-001, São Paulo/São Paulo, Brazil
Pablo Felipe Cruz Ochoa
Affiliation:
Bioparque Los Ocarros, Km 3 via Restrepo, Villavicencio/Meta, Colombia
José Henrique Hildebrand Grisi-Filho
Affiliation:
Laboratório de Epidemiologia e Estatística (LEB), Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo (USP), Av. Prof. Dr Orlando Marques de Paiva 87, Cidade Universitária, CEP 05508-270, São Paulo/São Paulo, Brazil
Eliana Reiko Matushima
Affiliation:
Grupo de Pesquisa sobre Fibropapilomatose em Tartarugas Marinhas, Universidade de São Paulo (USP), Av. Prof. Dr Orlando Marques de Paiva 87, Cidade Universitária, CEP 05508-270, São Paulo/São Paulo, Brazil Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo (USP), Av. Prof. Dr Orlando Marques de Paiva 87, Cidade Universitária, CEP 05508-270, São Paulo/São Paulo, Brazil
*
Author for correspondence: Silmara Rossi, E-mail: smara.rossi@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Fibropapillomatosis (FP) can be an important conservation threat to green sea turtles (Chelonia mydas) due to its widespread distribution and complex aetiology. Thus, understanding the impacts of FP in sea turtle populations is a research priority towards conservation efforts. The body condition index (BCI), based on straight carapace length (SCL) and body mass (BM), is an accurate indicator of body-nutritional condition that can be used in routine green turtle health evaluations. This study aimed to compare BCI in FP-free (N = 369) and FP-affected (N = 518) green turtles from Brazilian feeding areas. Body condition indices were evaluated in terms of the South-west Atlantic Fibropapillomatosis Score – FPSSWA (mild, moderate and severe), study sites (five Brazilian states), origin (intentional capture, fishery, stranding and afloat) and sex (when known). Curved and straight carapace lengths, and body mass were recorded in order to calculate BCI. Statistical analysis revealed significant differences in BCI among green turtles from different study areas (P = 0.02), and lower BCI values in FP-free than in FP-positive individuals (P < 0.0001). With regards to origin, the highest BCI was found in the intentional capture group (N = 245; 1.47 ± 0.16), followed by fishery (N = 180; 1.46 ± 0.20). Analysis according to sex revealed a higher mean BCI among females than males (P < 0.017). This study provides relevant data on the health and nutritional status of green turtles along the Brazilian coast, in important feeding areas for this species.

Keywords

Brazilian coastChelonia mydasconservationtumours
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 8 , December 2019 , pp. 1879 - 1887
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adnyana, W, Ladds, PW and Blair, D (1997) Observations of fibropapillomatosis in green turtles (Chelonia mydas) in Indonesia. Australian Veterinary Journal 75, 737–742.Google Scholar
Aguirre, AA and Lutz, PL (2004). Marine turtles as sentinels of ecosystem health: is fibropapillomatosis an indicator? EcoHealth 1, 275–283.Google Scholar
Aguirre, AA, Balazs, GH, Spraker, TR and Gross, TS (1995) Adrenal and hematological responses to stress in juvenile green turtles (Chelonia mydas) with and without fibropapillomas. Physiological Zoology 68, 831–854.Google Scholar
Anderson, ET, Harms, CA, Stringer, EM and Cluse, WM (2011) Evaluation of hematology and serum biochemistry of cold-stunned green sea turtles (Chelonia mydas) in North Carolina, USA. Journal of Zoo and Wildlife Medicine 42, 247–255.Google Scholar
Arthur, KE, Boyle, MC and Limpus, CL (2008) Ontogenetic changes in diet and habitat use in green sea turtle (Chelonia mydas) life history. Marine Ecology Progress Series 362, 303–311.Google Scholar
Baptistotte, C (2007) Caracterização espacial e temporal da fibropapilomatose em tartarugas marinhas da costa brasileira (PhD thesis). Escola Superior de Agricultura Luiz de Queiroz and Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, Piracicaba, Brazil.Google Scholar
Baptistotte, C (2016) Fibropapillomatosis in sea turtles from South America – Brazil, Uruguay, and Argentina. In Hargrove, S, Work, T, Brunson, S, Foley, AM and Balazs, G (eds), Proceedings of the 2015 International Summit on Fibropapillomatosis: Global Status, Trends, and Population Impacts. Honolulu: U.S. Department of Commerce, NOAA Tech. Memo., pp. 22–25. NOAA-TM-NMFS-PIFSC-54, 87 pp. doi: 10.7289/V5/TM-PIFSC-54.Google Scholar
Bjorndal, KA (1997) Foraging ecology and nutrition of sea turtles. In Lutz, PL and Musick, JA (eds), The Biology of Sea Turtles, Vol. I. London: CRC Press, pp. 199–231.Google Scholar
Bjorndal, KA, Bolten, AB and Chaloupka, MY (2000) Green turtle somatic growth model: evidence for density dependence. Ecological Applications 10, 269–282.Google Scholar
Bolten, AB (2003) Variation in sea turtle life history patterns: neritic vs oceanic development stages. In Lutz, PL, Musick, JA and Wyneken, J (eds), The Biology of Sea Turtles, Vol. II. New York, NY: CRC Press, pp. 243–257.Google Scholar
Bolten, AB and Bjorndal, KA (1992) Blood profiles for a wild population of green turtles (Chelonia mydas) in the Southern Bahamas: size-specific and sex-specific relationships. Journal of Wildlife Diseases 28, 407–413.Google Scholar
Carr, A (1982) Notes on the behavioral ecology of sea turtles. In Bjorndal, KA (ed.), Biology and Conservation of Sea Turtles, vol. I. Washington, DC: Smithsonian Institute Press, pp. 19–26.Google Scholar
Chaloupka, M, Limpus, C and Miller, J (2004) Green turtle somatic growth dynamics in a spatially disjunct Great Barrier Reef metapopulation. Coral Reefs 23, 325–335.Google Scholar
Deem, SL, Dierenfeld, ES, Sounguet, GP, Alleman, AR, Cray, C, Poppenga, RH, Norton, TM and Karesh, WB (2006) Blood values in free-ranging nesting leatherback sea turtles (Dermochelys coriacea) on the coast of the Republic of Gabon. Journal of Zoo and Wildlife Medicine 37, 464–471.Google Scholar
Dinno, A (2017) Dunn-test: Dunn's test of multiple comparisons using rank sums. Available at https://cran.r-project.org/package=dunn.test (Accessed 28 August 2018).Google Scholar
Duarte, A, Faisca, P, Loureiro, NS, Rosado, R, Gil, S, Pereira, N and Tavares, L (2012) First histological and virological report of fibropapilloma associated with herpesvirus in Chelonia mydas at Príncipe Island, West Africa. Archives of Virology 157, 1155–1159.Google Scholar
Ene, A, Su, M, Lemaire, S, Rose, C, Schaff, S, Moretti, R, Lenz, J and Herbst, LH (2005) Distribution of chelonid fibropapillomatosis associated herpesvirus variants in Florida: molecular genetic evidence for infection of turtles following recruitment to neritic developmental habitats. Journal of Wildlife Diseases 41, 489–497.Google Scholar
Flint, M, Morton, JM, Limpus, CJ, Patterson-Kane, JC, Murray, PJ and Mills, PC (2010) Development and application of biochemical and haematological reference intervals to identify unhealthy green sea turtles (Chelonia mydas). Veterinary Journal 185, 299–304.Google Scholar
Fong, CL, Chen, HC and Cheng, IJ (2010) Blood profiles from wild populations of green sea turtles in Taiwan. Journal of Veterinary Medicine and Animal Health 2, 8–10.Google Scholar
Gattamorta, MA (2015) Ecologia, prevalência e caracterização molecular de Chelonid fibropapilloma-associated herpesvirus (CFPHV) em Tartarugas verdes (Chelonia mydas) em áreas da costa brasileira, 2015. Piracicaba: Tese (Doutor em Ciências) – Escola Superior de Agricultura ‘Luiz de Queiroz’ – Centro de Energia Nuclear na Agricultura, Universidade de São Paulo, 122 pp.Google Scholar
George, RH (1997) Health problems and diseases of sea turtles. In Lutz, PL and Musick, JA (eds), The Biology of Sea Turtles, Vol. I. Boca Raton, FL: CRC Press, pp. 363–385.Google Scholar
Hamann, M, Schauble, CS, Simon, T and Evans, S (2006) Demographic and health parameters of green sea turtles Chelonia mydas foraging in the Gulf of Carpentaria, Australia. Endangered Species Research 2, 81–88.Google Scholar
Hamann, M, Godfrey, MH, Seminoff, JA, Arthur, K, Barata, PCR, Bjorndal, KA, Bolten, AB, Broderick, AC, Campbell, LM, Carreras, C, Casale, P, Chaloupka, M, Chan, SKF, Coyne, MS, Crowder, LB, Diez, CE, Dutton, PH, Epperly, SP, FitzSimmons, NN, Formia, A, Girondot, M, Hays, GC, Cheng, IJ, Kaska, Y, Lewison, R, Mortimer, JA, Nichols, WJ, Reina, RD, Shanker, K, Spotila, JR, Tomás, J, Wallace, BP, Work, TM, Zbinden, J and Godley, BJ (2010) Global research priorities for sea turtles: informing management and conservation in the 21st century. Endangered Species Research 11, 245–269.Google Scholar
Hargrove, S, Work, T, Brunson, S, Foley, AM and Balazs, G (2016) Proceedings of the 2015 international summit on fibropapillomatosis: global status, trends, and population impacts. U.S. Department of Commerce, NOAA Tech. Memo., NOAA-TM-NMFS-PIFSC-54, 87 pp. doi: 10.7289/V5/TM-PIFSC-54.Google Scholar
Hasbún, CR, Lawrence, AJ, Naldo, J, Samour, JH and Al-Ghais, SM (1998) Normal blood chemistry of free-living green sea turtles, Chelonia mydas, from the United Arab Emirates. Comparative Haematology International 8, 174–177.Google Scholar
Herbst, LH (1994) Fibropapillomatosis of marine turtles. Annual Review of Fish Diseases 4, 389–425.Google Scholar
Herbst, LH and Jacobson, ER (2003) Practical approaches for studying sea turtle health and disease. In Lutz, P, Musick, JA and Wyneken, J (eds), The Biology of Sea Turtles, Vol. II. New York, NY: CRC Press, pp. 385–410.Google Scholar
Herbst, LH, Greiner, EC, Ehrhart, LM, Bagley, DA and Klein, PA (1998) Serological association between spirorchidiasis, herpesvirus infection, and fibropapillomatosis in green turtles from Florida. Journal of Wildlife Diseases 34, 496–507.Google Scholar
Hirama, S and Ehrhart, LM (2007) Description, prevalence and severity of green turtle fibropapillomatosis in three developmental habitats on the east coast of Florida. Florida Scientist 70, 435–448.Google Scholar
Hirama, S, Ehrhart, LM, Rea, LD and Kiltie, RA (2014) Relating fibropapilloma tumor severity to blood parameters in green turtles Chelonia mydas. Diseases of Aquatic Organisms 111, 61–68.Google Scholar
Jesus, HC, Costa, EA, Mendonça, ASF and Zandonade, E (2004) Distribuição de metais pesados em sedimentos do sistema estuarino da ilha de Vitória-ES. Quimica Nova 27, 378–386.Google Scholar
Kassambara, A (2017) ggpubr: ‘ggplot2’ Based Publication Ready Plots. Available at https://cran.r-project.org/package=ggpubr (Accessed 28 August 2018).Google Scholar
Keller, JM, Balazs, GH, Nilsen, F, Rice, M, Work, TM and Jensen, BA (2014) Investigating the potential role of persistent organic pollutants in Hawaiian green sea turtle fibropapillomatosis. Environmental Science & Technology 48, 7807–7816.Google Scholar
Labrada-Martagón, V, Méndez-Rodriguez, LC, Gardner, SC, López-Castro, M and Zenteno-Savin, T (2010 a) Health indices of the green turtle (Chelonia mydas) along the Pacific coast of Baja California Sur, Mexico. I. Blood biochemistry values. Chelonian Conservation and Biology 9, 162–172.Google Scholar
Labrada-Martagón, V, Méndez-Rodriguez, LC, Gardner, SC, Cruz-Escalona, VH and Zenteno-Savin, T (2010 b) Health indices of the green turtle (Chelonia mydas) along the Pacific coast of Baja California Sur, Mexico. II. Body condition index. Chelonian Conservation and Biology 9, 173–183.Google Scholar
Lackovich, JK, Brown, DR, Homer, BL, Garber, RL, Mader, DR, Moretti, RH, Patterson, AD, Herbst, LH, Oros, J, Jacobson, ER, Curry, SS and Klein, PA (1999) Association of herpesvirus with fibropapillomatosis of the green turtle Chelonia mydas and the loggerhead turtle Caretta caretta in Florida. Diseases of Aquatic Organisms 37, 89–97.Google Scholar
Lewbart, GA, Hirschfeld, M, Denkinger, J, Vasco, K, Guevara, N, García, J, Muñoz, J and Lohmann, KJ (2014) Blood gases, biochemistry, and hematology of Galapagos green turtles (Chelonia mydas). PLoS ONE 9, e96487.Google Scholar
Limpus, CJ and Limpus, DJ (2000) Mangroves in the diet of Chelonia mydas in Queensland, Australia. Marine Turtle Newsletter 89, 13–15.Google Scholar
Limpus, CJ, Limpus, DJ, Arthur, KE and Parmenter, CJ (2005) Monitoring Green Turtle Population Dynamics in Shoalwater Bay: 2000–2004. Great Barrier Reef Marine Park Authority and Environmental Protection Agency, Queensland Parks and Wildlife Service.Google Scholar
López-Castro, MC, Koch, V, Mariscal-Loza, A and Nichols, WJ (2010) Long-term monitoring of black turtles Chelonia mydas at coastal foraging areas off the Baja California Peninsula. Endangered Species Research 11, 35–45.Google Scholar
Matushima, ER, Filho, AL, Di Loretto, C, Kanamura, CT, Sinhorini, IL, Gallo, B and Baptistotte, C (2001) Cutaneous papillomas of green turtles: a morphological, ultra-structural and immunohistochemical study in Brazilian individuals. Brazilian Journal of Veterinary Research and Animal Science 38, 51–54.Google Scholar
Meylan, AB and Meylan, PA (2000) Introducción a la evolución, historias de vida y biología de las tortugas marinas. In Eckert, KL, Bjorndal, KA, Abreu-Grobois, FA and Donnelly, M (eds), Técnicas de Investigación y Manejo para la Conservación de las Tortugas Marinas. Grupo Especialista en Tortugas Marinas UICN/CSE Publicación No. 4 (Español). Blanchard, PA: Consolidated Graphic Communications, pp. 3–5.Google Scholar
Meylan, AB, Bowen, BW and Avise, JC (1990) A genetic test of the natal homing versus social facilitation models for green turtle migration. Science 248, 724–727.Google Scholar
Millard, SP (2013) EnvStats: An R Package for Environmental Statistics. New York, NY: Springer.Google Scholar
Monezi, T, Mehnert, DU, Moura, EMM, Müller, N, Garrafa, P, Matushima, ER, Werneck, MR and Borella, MI (2016) Chelonid herpesvirus 5 in secretions and tumor tissues from green turtles (Chelonia mydas) from Southeastern Brazil: a ten-year study. Veterinary Microbiology 186, 150–156.Google Scholar
Mortimer, J (1982) Feeding ecology of sea turtles. In Bjorndal, KA (ed.), Biology and Conservation of Sea Turtles. Washington, DC: Smithsonian Institution Press, pp. 103–109.Google Scholar
Musick, JA and Limpus, CJ (1997) Habitat utilization and migration in juvenile sea turtles. In Lutz, P and Musick, JA (eds), The Biology of Sea Turtles, Vol. I. Boca Raton, FL: CRC Press, pp. 137–163.Google Scholar
Osborne, AG, Jacobson, ER, Bresette, MJ, Singewald, DA, Scarpino, RA and Bolten, AB (2010) Reference intervals and relationships between health status, carapace length, body mass, and water temperature and concentrations of plasma total protein and protein electrophoretogram fractions in Atlantic loggerhead sea turtles and green turtles. Journal of the American Veterinary Medical Association 237, 561–567.Google Scholar
Page-Karjian, A, Norton, TM, Krimer, P, Groner, M, Nelson, SE and Gottdenker, NL (2014) Factors influencing survivorship of rehabilitating green sea turtles (Chelonia mydas) with fibropapillomatosis. Journal of Zoo and Wildlife Medicine 45, 507–519.Google Scholar
Patricio, AR, Herbst, LH, Duarte, A, Veles-Zuazo, X, Loureiro, NS, Pereira, N, Tavares, L and Toranzos, GA (2012) Global phylogeography and evolution of chelonid fibropapilloma-associated herpesvirus. Journal of General Virology 93, 1035.Google Scholar
Quackenbush, SL, Casey, RN, Murcek, RJ, Paul, TA, Work, TM, Limpus, CJ, Chaves, A, Dutoit, L, Vasconcelos Peres, J, Aguirre, AA, Spraker, RT, Horrocks, JÁ, Vermeer, LA, Balazs, GH and Casey, JW (2001) Quantitative analysis of herpesvirus sequences from normal tissue and fibropapillomas of marine turtles with real time PCR. Virology 287, 105–111.Google Scholar
R Core Team (2016) A Language and Environment for Statistical Computing. Available at https://www.r-project.org/ (Accessed 24 September 2018).Google Scholar
Rodenbusch, CR, Baptistotte, C, Werneck, MR, Pires, TT, Melo, MTD, Ataíde, MW, Reis, KDHL, Testa, P, Alieve, MM and Canal, CW (2014) Fibropapillomatosis in green turtles Chelonia mydas in Brazil: characteristics of tumors and virus. Diseases of Aquatic Organisms 111, 207–217.Google Scholar
Rossi, S, Sánchez-Sarmiento, AM, Santos, RG, Prioste, FES, Mott, C, Grisi Filho, JHH and Matushima, ER (2015) Analysis of corporal condition and fibropapillomatosis manifestation in Chelonia mydas (Testudines Cheloniidae) studied at Brazilian feeding areas. In Soler-Tovar, D and Navas-Suárez, PE (eds), Proceedings of Salud y Enfermedades de la Vida Silvestre. Wildlife Disease Association – Latin American Section (WDA-LA). Bogotá: Asociación de Veterinarios de Vida Silvestre, September 2015.Google Scholar
Rossi, S, Sánchez-Sarmiento, AM, Vanstreels, RET, Santos, RG, Prioste, FES, Gattamorta, MA, Grisi-Filho, JHH and Matushima, ER (2016) Challenges in evaluating the severity of fibropapillomatosis: a proposal for objective index and score system for green sea turtles (Chelonia mydas) in Brazil. PLoS ONE 11, e0167632.Google Scholar
Sales, G, Giffoni, B and Barata, PCR (2008) Incidental catch of sea turtles by the Brazilian pelagic longline fishery. Journal of the Marine Biological Association of the United Kingdom 88, 853–864.Google Scholar
Samour, JH, Hewlett, JC, Silvanose, C, Hasbún, CR and AlpGhais, SM (1998) Normal haematology of free-living green sea turtles (Chelonia mydas) from the United Arab Emirates. Comparative Haematology International 8, 102–107.Google Scholar
Sánchez-Sarmiento, AM, Rossi, S, Vanstreels, RET, Santos, RG, Marigo, J, Bertozzi, CP, Baptistotte, C, Becker, JH and Matushima, ER (2012) Comparison between corporal subjetive classification and body condition index (BCI) for Chelonia mydas (Testudines, Cheloniidae) caught in Brazilian coast. Proceedings of the Second Congresso Latino-Americano de Reabilitação de Fauna Marinha, CRAM-Museu Oceanográfico Prof. Eliézer de C. Rios-FURG. Rio Grande, 3–6 September 2012.Google Scholar
Santos, RG, Martins, AS, Torezani, E, Baptistotte, C, Farias, JN, Horta, PA, Work, TM and Balazs, GH (2010) Relationship between fibropapillomatosis and environmental quality: a case study with Chelonia mydas of Brazil. Diseases of Aquatic Organisms 89, 87–95.Google Scholar
Santos, AS, Almeida, AP, Santos, AJB, Gallo, B, Giffoni, B, Baptistotte, C, Coelho, CA, Lima, EHSM, Sales, G, Lopez, GG, Stahelin, G, Becker, H, Castilhos, JC, Thomé, JCA, Wanderlinde, J, Marcovaldi, MAAGD, Mendilaharsu, MLML, Damasceno, MT, Barata, PCR and Sforza, R. (2011) Chelonia mydas (Linnaeus, 1758). In Plano de Ação Nacional para Conservação das Tartarugas Marinhas (Orgs. Marcovaldi MAAGD, Santos AS, Sales G). Brasília: Instituto Chico Mendes de Conservação da Biodiversidade, pp. 32–35.Google Scholar
Santos, MRD, Martins, AS, Baptistotte, C and Work, TM (2015) Health condition of juvenile Chelonia mydas related to fibropapillomatosis in southeast Brazil. Diseases of Aquatic Organisms 115, 193–201.Google Scholar
Seminoff, JA, Jones, TT, Resendiz, A, Nichols, WJ and Chaloupka, MY (2003) Monitoring green turtles (Chelonia mydas) at a coastal foraging area in Baja California, Mexico: multiple indices to describe population status. Journal of the Marine Biological Association of the United Kingdom 83, 1355–1362.Google Scholar
Stamper, MA, Harms, C, Epperly, SP, Braun-McNeill, J and Stoskopf, MK (2005) Relationship between barnacle epibiotic load and hematologic parameters in loggerhead sea turtles (Caretta caretta), a comparison between migratory and residential animals in Pamlico Sound, North Carolina. Journal of Zoo and Wildlife Medicine 36, 635–641.Google Scholar
Stevenson, RD and Woods, WA Jr (2006) Condition indices for conservation: new uses for evolving tools. Integrative and Comparative Biology 46, 1169–1190.Google Scholar
Thomson, JA, Burkholder, D, Heithaus, MR and Dill, LM (2009) Validation of a rapid visual-assessment technique for categorizing the body condition of green turtles (Chelonia mydas) in the field. Copeia 2, 251–255.Google Scholar
Torezani, E, Baptistotte, C, Mendes, SL and Barata, PCR (2010) Juvenile green turtles (Chelonia mydas) in the effluent discharge channel of a steel plant, Espírito Santo, Brazil. Journal of the Marine Biological Association of the United Kingdom 90, 233–246.Google Scholar
Van Houtan, KS, Hargrove, SK and Balazs, GH (2010) Land use, macroalgae, and a tumor-forming disease in marine turtles. PLoS ONE 5, 1–8.Google Scholar
Vilca, FZ, Rossi, S, Olinda, RA, Sánchez-Sarmiento, AM, Prioste, FES, Matushima, ER and Tornisielo, VL (2018) Concentrations of polycyclic aromatic hydrocarbons in liver samples of juvenile green sea turtles from Brazil: can these compounds play a role in the development of fibropapillomatosis? Marine Pollution Bulletin 130, 215–222.Google Scholar
Whiting, SD, Guinea, ML, Limpus, CJ and Fomiatti, K (2007) Blood chemistry reference values for two ecologically distinct population of foraging green turtles, eastern Indian Ocean. Comparative Clinical Pathology 16, 109–118.Google Scholar
Wickham, H (2009) ggplot2: Elegant Graphics for Data Analysis. New York, NY: Springer-Verlag. Available at http://ggplot2.org (Accessed 24 September 2018).Google Scholar
Wickham, H and Bryan, J (2017) readxl: Read Excel Files. Available at https://cran.r-project.org/package=readxl (Accessed 24 September 2018).Google Scholar
Work, TM and Balazs, GH (1999) Relating tumor score to hematology in green turtles with fibropapillomatosis in Hawaii. Journal of Wildlife Diseases 35, 804–807.Google Scholar
Work, TM, Dagenais, J, Balazs, GH, Schumacher, J, Lewis, TD, Leong, JC, Casey, RN and Casey, JW (2009) In vitro biology of fibropapilloma-associated turtle herpesvirus and host cells in Hawaiian green turtles (Chelonia mydas). Journal of General Virology 90, 1943–1950.Google Scholar