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Lack of Xenoestrogen-Induced Vitellogenin in Male Olive Ridley Sea Turtles (Lepidochelys Olivacea) from the Pacific Coast of Costa Rica

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Lack of Xenoestrogen-Induced Vitellogenin in Male Olive Ridley Sea Turtles (Lepidochelys Olivacea) from the Pacific Coast of Costa Rica Lack of xenoestrogen-induced vitellogenin in male olive ridley sea turtles (Lepidochelys olivacea) from the Pacific coast of Costa Rica Roldán A. Valverde1*, Kyle W. Selcer2, Luis Rólier Lara3 & Jeffrey Alejandro Sibaja-Cordero3 1. Department of Biological Sciences, Southeastern Louisiana University, Hammond, LA 70402 2. Department of Biological Sciences, Duquesne University, Pittsburgh, PA 15282 3. Centro de Investigaciones en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, 2060 San José, Costa Rica * Corresponding author: [email protected] Received 04-VI-2007. Corrected 06-VI-2008. Accepted 03-VII-2008. Abstract: Olive ridley sea turtles (Lepidochelys olivacea) distribute widely throughout Eastern Pacific (EP) waters. During reproduction these animals aggregate near coastal waters where they may be exposed to indus- trial or agrochemical environmental pollutants that may disrupt the endocrine system of these reptiles. One group of compounds of concern is the persistent organic pollutants (POPs), some of which have been detected in Costa Rican waters. Some of these POPs, such as polychlorinated biphenyls and DDT and its metabolites, exhibit estrogenic activity in reptiles. It is unknown whether olive ridleys are exposed to endocrine disruptive doses of these POPs throughout their life in EP waters. Consequently, this study was conducted to determine whether there is evidence of exposure of male olive ridleys to estrogenic compounds. During the study a total of 35 males were hand-captured while mating off the coast of Ostional, Costa Rica, a major nesting beach for this species. The captured turtles were brought aboard a small boat, and blood samples taken with a hypodermic syringe. Turtles were carefully released in the water after the blood samples were taken. In the laboratory, blood collected from these males was analyzed by Western blot using an antibody developed against red-eared slider turtle vitellogenin. Vitellogenin is a female-specific protein that is induced by estrogen during gonadal recrudes- cence. Estrogenic compounds have been shown to induce this protein in reptilian species. Results of this study indicate the lack of evidence of vitellogenin in the blood of olive ridley males as shown by Western blot analysis. This study demonstrates the feasibility of using the slider’s vitellogenin antibody to detect the presence of the protein in the olive ridley sea turtle, L. olivacea. Rev. Biol. Trop. 56 (Suppl. 4): 49-57. Epub 2009 June 30. Key words: Lepidochelys olivacea, olive ridley turtle, vitellogenin, marine pollution, endocrine disruption, Eastern Pacific, Costa Rica. Many industrial and agricultural activities may contribute to local wildlife extinctions. An result in the discard of environmental pollut- important group of endocrine disruptors is that ants that may pose a significant threat to sea of the persistent organic pollutants (POPs) that, turtles due to their toxicity or to their abil- because of their hydrophobicity and persistence ity to behave as endocrine disruptors, i.e., as in the environment, tend to bioaccumulate in exogenous chemicals that may interfere with fatty tissues of invertebrates and vertebrates endocrine physiology by either mimicking or and to biomagnify through the food chain blocking endogenous hormonal signals (Crews (Lindström et al., 2004). Two widely distributed et al., 2000). Indeed a recent review on endo- POPs are 1,1-dichloro-2,2-bis(p-chlorophenyl) crine disruption in wildlife by Cheek (2006) ethylene (DDE) and polychlorinated biphenyls suggests that this phenomenon, in combina- (PCBs). DDE is a highly toxic pesticide and tion with other stressors such as habitat loss, PCBs are industrial pollutants whose pres- over-harvesting, and global climate change, ence has been detected in aquatic ecosystems Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (Suppl. 5): 49-57, December 2008 49 in Costa Rica, including the Pacific coast (De The olive ridley sea turtle (Lepidochelys la Cruz, 1994; Spongberg, 2004b; Spongberg, olivacea) is an endangered species with a pan- 2004c; Spongberg, 2004a). DDE has been tropical distribution. Its abundance is greatest detected in bivalves in Costa Rican estuaries on the east coast of India and on the west coast (De la Cruz, 1994). Both DDE and PCBs have of Mexico and Central America (Cornelius, been detected in tissues of carnivorous marine 1982). The species exhibits a mass nesting turtles, including ridleys and loggerheads in behavior, also known as arribada, which is the EP and in other regions (Lake et al., 1994; characterized by the synchronous nesting of Gardner et al., 2003; Keller et al., 2004). These thousands of conspecifics in a relatively small organochlorinated compounds are known to be section of beach (Valverde et al., 1998). An endocrine disruptors, having estrogenic activ- extensive tagging program conducted in the ity in turtles and being capable of reversing the early 1980s at Nancite and Ostional, the two sex of turtles with temperature-dependent sex most important arribada beaches on the Pacific determination (Bergeron et al., 1994; Palmer coast of Costa Rica, revealed that these nest- and Palmer, 1995; Willingham and Crews, ing assemblages distribute widely through- 1999). Another sign of endocrine disruption out the Eastern Pacific (EP), between Baja in oviparous vertebrates by organochlorinated California and northern Peru (Cornelius, 1986). hydrocarbons is the ability of these compounds Tag recoveries indicate that this species distrib- to induce vitellogenin, a phospholipoglycopro- utes along the coast and also travels as far as tein precursor of egg yolk proteins, from the 3,200 km off the Costa Rican coast, which is liver (Heppell et al., 1995). Vitellogenin is a consistent with its pelagic behavior (Cornelius female-specific protein normally present in the and Robinson, 1986). This ample distribution blood of females with recrudescing gonads, but in the EP, including highly productive coastal not in juveniles or males. Interestingly, it has and estuarine areas, provides an extensive for- been shown that males and immature turtles are aging area for this carnivorous species along also capable of producing vitellogenin when the coast (Reichart, 1993). It is in these coastal exposed to exogenous sources of estradiol areas where ridleys are most impacted by (Palmer and Palmer, 1995; Irwin et al., 2001; anthropogenic activities including direct and Sifuentes-Romero et al., 2006). Thus, the pres- incidental take in various fisheries, poaching ence of vitellogenin in male blood has been of eggs at the nesting beaches and several used as evidence of exposure to estrogenic industries, among other threats. The impact of compounds, like organochlorinated chemicals environmental pollutants on sea turtle popula- (Heppell et al., 1995). Such exposure may lead tions remains to be demonstrated. to negative impacts on physiological processes The objective of this study is to establish that may be deleterious to endangered wildlife whether there is evidence of endocrine disrup- populations such as sea turtles. A clear case tion in olive ridley sea turtles in Costa Rica as of relevance of endocrine disruption at the a function of estrogenic contaminants. population level is that of alligators in Lake Apopka. Exposure to high concentrations of Materials AND METHODS organochlorinated compounds led to reproduc- tive dysfunction and a decline in the alligator Olive ridleys were captured over a period population (Guillette et al., 1994). Declines of three years off the coast of the Ostional of sea turtle populations in Costa Rica have National Wildlife Refuge, Pacific coast of been documented, although the specific causes Costa Rica. Ostional beach is one of the have not been elucidated (Valverde et al., world’s most important mass nesting beaches 1998). Thus, we undertook an exploratory for the olive ridley sea turtle (Fig.1a). Turtles study searching for evidence of endocrine dis- were captured during the months of June or ruption in marine turtles in Costa Rica. July over a period of three years, just before 50 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (Suppl. 5): 49-57, December 2008 the beginning of the heavy nesting period in Each sampling trip lasted an effective time Costa Rica (July-November), when mating is of no more than four hours. All animals were believed to be most frequent. All animals were marked using a water-proof marker to avoid captured during mating by means of the turtle recapture during the same season. rodeo technique (Limpus, 1985). Briefly, upon Blood samples of 5 ml were collected from sighting a mating pair a diver leaps off the boat, each individual from the cervical sinus using captures the animals and brings them onboard. heparinized vacutainers with 21G, 2.5 inch Fig. 1a. Mass nesting event (arribada) at Ostional National Wildlife Refuge, Costa Rica. This arribada took place in November of 2006, and was estimated at 64,388 ± 4,951 females. Arribadas like this are characteristic of this beach (photo taken by Diana Solís). Fig. 1b. Blood sampling of a male olive ridley captured by means of the turtle rodeo technique during mating off the coast of Ostional Beach, Costa Rica (photo taken by J. Sibaja). Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 56 (Suppl. 5): 49-57, December 2008 51 needles (Fig. 1b). The turtles were released fractionated for each sample on a 4 % to 12% to the sea after the blood samples were taken. gradient precast (Invitrogen) polyacrylamide Blood samples were placed on ice and centri- gel under reducing conditions. A molecular fuged shortly after collection while still on the weight marker (BlueRanger; Pierce) was also boat using a portable 12 V centrifuge, or shortly included as a signal reference. After fraction- after landing. Before aliquoting into cryovials ation, proteins were transferred to Immobilon-P all plasma samples were supplemented with (Millipore) polyvinylidene fluoride (PVDF) approximately 50 µl of the wide spectrum pro- membranes using a semi-dry transfer cell (Bio- tease inhibitor aprotinin to prevent vitellogenin Rad), with a solution of NuPage transfer buffer degradation.
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