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First Approximation to Congenital Malformation Rates in Embryos and Hatchlings of Sea Turtles

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First Approximation to Congenital Malformation Rates in Embryos and Hatchlings of Sea Turtles First Approximation to Congenital Malformation Rates in Embryos and Hatchlings of Sea Turtles Annelisse Barcenas-Ibarra 1, Horacio de la Cueva2, Isaias Rojas-Lleonart3, F. Alberto Abreu-Grobois4, Rogelio Ivan Lozano-Guzman 5, Eduardo Cuevas6, and Alejandra Garcıa-Gasca*1 Background: Congenital malformations in sea turtles have been considered these, 38 are new reports; 35 for wild sea turtles, three for vertebrates. Thirty- sporadical. Research carried out in the Mexican Pacific revealed high levels one types were found in hawksbill, 23 in green, and 59 in olive ridley. The of congenital malformations in the olive ridley, but little or no information is head region showed a higher number of malformation types. Malformation available for other species. We present results from analyses of external levels in the olive ridley were higher than previously reported. Conclusion: congenital malformations in olive ridley, green, and hawskbill sea turtles from Olive ridleys seem more prone to the occurrence of congenital malformations Mexican rookeries on the Pacific coast and Gulf of Mexico. METHODS: We than the other two species. Whether the observed malformation levels are examined 150 green and hawksbill nests and 209 olive ridley nests during normal or represent a health problem cannot be currently ascertained without the 2010 and 2012 nesting seasons, respectively. Olive ridley eggs were long-term assessments. transferred to a hatchery and incubated in styrofoam boxes. Nests from the other two species were left in situ. Number of eggs, live and dead hatchlings, Birth Defects Research (Part A) 103:203–224, 2015. and eggs with or without embryonic development were registered. VC 2015 Wiley Periodicals, Inc. Malformation frequency was evaluated with indices of prevalence and severity. Results: Mortality levels, prevalence and severity were higher in olive Key words: congenital malformations; mortality; hatching success; sea turtles; ridley than in hawksbill and green sea turtles. Sixty-three types of congenital endangered species malformations were observed in embryos, and dead or live hatchlings. Of Introduction urally occurring congenital malformations in animals con- Congenital malformations figure prominently in human sists primarily of isolated case reports or grey literature. pathology, and domesticated or laboratory animals (Lei- The scarce surveys have used data from different sources pold, 1980; Kalter, 2003), but in wildlife they are mostly and considerable variation in methodological techniques unknown and neglected (Barcenas-Ibarra and Maldonado- and nomenclature (diagnostic criteria) exist. For example, Gasca, 2009; Sant’Anna et al., 2013). in laboratory mammals there are at least 466 specific con- Because congenital malformations are relatively rare genital malformation categories with structural defects, and sporadic in wildlife, they have probably been over- and among these, multiple variants have also been looked in a large number of surveys (Scott and Camh, described (Markis et al., 2009). 1925; Bellairs, 1965; Barcenas-Ibarra and Maldonado- Existing reports of congenital malformations in wildlife Gasca, 2009; Sant’Anna et al., 2013). The literature on nat- focus on fishes (Dethlefesen et al., 1996; Burgos-Alvarado, 1999; Hevia-Hormazabal et al., 2011), mammals (Scott and Camh, 1925; Stills and Bullock, 1981; Rojas-Lleonart and Additional Supporting Information may be found in the online version of this article. Silveira-Prado, 2007, 2012; Rojas-Lleonart et al., 2011), birds (Scott and Camh, 1925; Ryder and Chamberlain, 1Centro de Investigacion en Alimentacion y Desarrollo, Mazatlan, Sinaloa, Mexico 1972; Ohlendorf et al., 1986; Hoffman et al., 1998; Pourlis, 2Centro de Investigacion Cientıfica y de Educacion Superior de Ensenada, 2011), amphibians (Blaustein and Johnson, 2003; Garcıa- Carretera Ensenada-Tijuana 3918 Zona Playitas, Ensenada, Baja California, Munoz~ et al., 2010; Henle et al., 2012), and reptiles Mexico (Blatchley, 1906; Scott and Camh, 1925; Bellairs, 1965; 3 Universidad Central “Marta Abreu” de Las Villas, Santa Clara, Villa Clara, Frye, 1991; Rodrıguez-Soberon et al., 2002; Sant’Anna Cuba 4Unidad Academica Mazatlan, Instituto de Ciencias del Mar y Limnologıa, et al., 2013). Universidad Nacional Autonoma de Mexico, Mazatlan, Sinaloa, Mexico Emerging awareness of congenital malformations in 5Instituto Tecnologico de Ciudad. Victoria, Ciudad Victoria, Tamaulipas, wild populations has attracted public and scientific con- Mexico cern because of the probable underlying environmental 6Pronatura Penınsula de Yucatan, A.C., Merida, Yucatan, Mexico health risks to both wildlife and humans (Lemly, 1997; *Correspondence to: Alejandra Garcıa-Gasca, Centro de Investigacion en Blaustein and Johnson, 2003; Hu et al., 2009). Congenital Alimentacion y Desarrollo, Avenida Sabalo-Cerritos s/n, Mazatlan, Sinaloa, malformations may signal emerging pathological threats, 82100, Mexico. E-mail: [email protected] but whether the phenomena are broadly applicable Published online 10 March 2015 in Wiley Online Library (wileyonlinelibrary. across taxa, or have population-scale impacts, is unknown com). Doi: 10.1002/bdra.23342 (Kelly et al., 2010). The concern due to rising trends in VC 2015 Wiley Periodicals, Inc. 204 CONGENITAL MALFORMATIONS IN SEA TURTLES TABLE 1. Frequency of Congenital Malformations in Sea Turtles Sample size Prevalence (%) Severity (6SE) Reference Location Speciesa Nests Eggs Nests Eggs Nests Organism Fowler (1979) Costa Rica Cm 134 14,272 19 (26) 0.5 (69) — — McGehee (1979) United States Cc — 5,666 — 0.6 (34) — — Blanck and Sawyer (1981) United States Cc — 2,811 — <1.0 (NP) — — Miller (1982) Australia Cc — 90,000 — 0.2 (180) — — Drennen (1990) United States Cc 213 21,130 12 (25) 0.2 (37) — — Galvan (1991) Mexico Lo — 7,524 — 1 (92) — — Kaska and Downie (1999) Turkey Cc — 1,882 — 8 (153) — — Kaska and Downie (1999) Turkey Cm — 1,169 — 26 (267) — — Trejo (2000) Mexico Lo 381 37,155 — 2 (730) — — Gularte (2000) Guatemala Lo — 8,000 — 0.5 (43) — — Carswell and Lewis (2002) United States Cc — 29,420 — 0.2 (46) — — Ruiz (2002) Mexico Lo 63 4,225 — 1 (54) — — Barcenas-Ibarra and Mexico Lo 100 8,625 50 (50) 1.6 (139) 2.8 (60.5) 1.6 (60.1) Maldonado-Gasca (2009) Barcenas-Ibarra Mexico Lo 49 5,016 55 (27) 1 (52) 1.9 (61.2) 25 (61.5) (unpublished data, 2012) This study Mexico Ei 150 23,559 41 (62) 2 (464) 7.5 (61.5) 1.2 (60Á04) This study Mexico Cm 150 17,690 11 (16) 0.2 (27) 1.7 (60.3) 2.8 (60.4) This study Mexico Lo 209 20,257 67 (140) 2 (400) 2.9 (60.2) 3.1 (60.1) For prevalence values, the data in parentheses indicate the number of nests or eggs that showed congenital malformations of the total sampled aSpecies: Cm, Chelonia mydas; Cc, Caretta caretta; Lo, Lepidochelys olivacea; Ei, Eretmochelys imbricata. congenital malformation levels in animals is highlighted by Beckman, 1990; Jelinek, 2005; Ujhazy et al., 2012). The increased incidence of limb malformations in amphibians multifactorial/threshold hypothesis postulates that congen- caused mostly by augmented trematode infections and pol- ital malformations are the result of modulations from a lution in the wild probably leading to diminishing popula- continuum of genetic characteristics by intrinsic and tions (Kaiser, 1997; Reaser and Johnson, 1997; Gray, 2000; extrinsic (environmental) factors (Brent, 2004). The com- Cohen, 2001; Johnson et al., 2011; Pinya et al., 2012). Reli- mon human congenital malformations have familial distri- able measures of congenital malformations, at the popula- butions that cannot be accounted for by simple Mendelian tion or individual levels, are of great importance to models, but can be explained in terms of a continuous identify demographic, geographic, and temporal patterns variable - liability - with a threshold value above which to detect sudden increases in their occurrence (due per- individuals will be affected. Both genetic and environmen- haps to the presence of novel teratogens), and to evaluate tal factors determine liability, making the system multifac- the efficacy of prevention efforts (Kalter, 2003). Under- torial. Cleft palate is an example of a congenital standing the aetiology of congenital malformations is still malformation that has a clear multifactorial origin (see challenging within clinical and field conditions. During the Fraser, 1976). 1940s, Warkany’s work demonstrated for the first time Of the seven sea turtle species (Pritchard and Mor- that congenital malformations in mammals could be timer, 1999), all are listed under some degree of extinction induced by both genetic and environmental agents (War- risk in the IUCN Red List with exception of Natator depres- kany and Nelson, 1940; Warkany and Scharaffenberger, sus (considered data deficient, IUCN, 2013). One of the 1947). Hence, causes of congenital malformations are main causes of sea turtle population declines has been the divided in four categories (i) unknown (50%); (ii) genetic prolonged traditional use augmented by the particularly (20–25%); (iii) environmental (5–10%); and (iv) multifac- intense commercial exploitation in the middle of the last torial (Wilson, 1979; Kalter and Warkany, 1983; Brent and century. However, the level of unknown intrinsic or BIRTH DEFECTS RESEARCH (PART A) 103:203–224 (2015) 205 extrinsic factors (such as pathologies, egg pest infestation, hawksbills. Some general descriptions for green turtles marine pollution, and climate change) that could under- have been reported by Fowler (1979), Miller (1985), mine their
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