MTN 152:8-10 Evidence of a Green Turtle Starting its Post-nesting Migration Without Laying all its Vitellogenic Follicles

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Evidence of a Green Turtle Starting its Post-nesting Migration Without Laying all its Vitellogenic Follicles

Nathan J. Robinson^1,2, Frank V. Paladino² & Pilar Santidrián Tomillo^1,3
¹The Leatherback Trust, Goldring-Gund Marine Biology Station, Playa Grande, Guanacaste, Costa Rica (E-mail: nathan@leatherback.org);
²Department of Biology, Indiana University-Purdue University Fort Wayne, Fort Wayne, Indiana, USA (E-mail: paladino@ipfw.edu);
³Population Ecology Group, Institut Mediterrani d’ Estudis Avançats, IMEDEA (CSIC-UIB), Miquel Marquès, 21, 07190, Esporles, Mallorca, Spain (E-mail: b_santidrian_tomillo@hotmail.com)

Ultrasonography is an invaluable tool for non-invasively monitoring the reproductive status of a wide-variety of organisms. In sea turtles, ultrasonography can be used to infer whether a nesting female will continue to lay more clutches of eggs in a given nesting season or whether she will begin migrating to post-nesting foraging areas (Blanco et al. 2012; Robinson 2014; Patel et al. 2015). Specifically, if multiple (> 10) vitellogenic follicles are present it is assumed that the turtle will lay one or more clutches that season. Alternatively, if only a few (< 10) vitellogenic follicles are present and there are numerous atretic follicles, it is assumed that the turtle will not nest further and will shortly begin its post-nesting migration (Rostal et al. 1996; Blanco et al. 2012). These assumptions seem logical, as it would appear to be a waste of time and energy for a nesting turtle to not shell and lay those vitellogenic follicles that have already been produced if there are presumably enough for a successful nest. Here, however, we used a combination of satellite telemetry and ultrasonography to describe an occurrence of a green sea turtle that began its post-nesting migration with numerous unlaid vitellogenic follicles still present in its ovaries. We also provide four potential hypotheses to explain this phenomenon.

Figure 1. Ultrasonographic images of left and right ovaries of an East Pacific green turtle immediately after nesting on Playa Cabuyal, Costa Rica and before it began its post-nesting migration. In both images, numerous vitellogenic follicles (vf) may be seen. Depth of the image is 20 cm. As the image is cross-sectional, it does not capture all the vitellogenic follicles that were observed in the ovary.

We were conducting a study that employed satellite telemetry to uncover the inter-nesting movements of the green turtles nesting on Playa Cabuyal on the Pacific coast of Costa Rica. To determine whether nesting turtles had more clutches to lay that season, and decide which females would be suitable for the attachment of a satellite transmitter, we scanned the ovaries of each turtle using a Sonosite 180 Plus real-time portable ultrasound (Sonosite, Bothell, Washington, USA). On 9 March 2015, which is towards the end of the nesting season for green turtles at Playa Cabuyal (August to April, Santidrián Tomillo et al. 2015), we encountered a turtle that had >10 vitellogenic follicles in both ovaries (Fig. 1). In addition, there was no evidence that atretic follicles were present and, as identified by her PIT tags, this was the first clutch that this turtle has been observed laying this season. Assuming that this turtle would therefore lay a subsequent clutch, we decided to deploy a SPOT5 satellite transmitter on the turtle (Wildlife Computers, Redmond, Washington, USA) (for details on the transmitter attachment see Clyde-Brockway 2014). The satellite tracking data were relayed using the Argos Satellite System and daily location estimates were generated using a Bayesian State Space Model as described in Jonsen et al. (2013).

Figure 2. Post-nesting migration of an East Pacific green turtle from Cabuyal, Costa Rica. The large black circles represent the tagging location and the white circles represent subsequent daily locations.

Inter-nesting green turtles generally stay close to the nesting beach (Blanco et al. 2013, Clyde-Brockway 2014); however, this turtle immediately migrated north from Cabuyal and continued on a northerly trajectory for 17 d (Fig. 2). During this time, the turtle traveled at an average speed of 26 km d^-1, covering a total distance of 400 km. In addition, there were no high-quality locations (Location Class 1, 2, or 3) that would indicate that the turtle returned to land to nest again. Eventually the turtle reached the northern extent of the mouth of the Gulf of Fonseca, which has been identified as the most common foraging areas for the green turtles that nest on Cabuyal (Clyde-Brockway 2014). Upon reaching the Gulf of Fonseca on 26 March 2015, the turtle’s movement speed dropped to an average of 7 km d^-1 and it appeared to take up residence. The turtle remained in the mouth of the Gulf of Fonseca for 4 days, until which point the transmitter stopped relaying information. Once again no high-quality locations were recorded over land in the Gulf of Fonseca that would suggest that the turtle was nesting here. In total, the transmitter was active for 21 days.

The tracking data suggest that this turtle began its post-nesting migration immediately after it was encountered nesting on Playa Cabuyal. Thus, this turtle must have eventually atrophied and reabsorbed its remaining vitellogenic follicles. While we only provide evidence of a single animal that migrated without laying all of its available vitellogenic follicles, this may be a relatively common phenomenon in sea turtles. Indeed, other scientists have reported finding mature follicles in the ovaries of female turtles that have just returned from their breeding areas (Miller &Limpus 1993).

It is not immediately clear why a sea turtle would commence a post-nesting migration without laying all its vitellogenic follicles. Indeed, sea turtles invest significant resources into egg production (Wallace et al. 2006) and any vitellogenic follicle that is not laid could represent a waste of resources. Nevertheless, we suggest four non-mutually exclusive hypotheses to explain this phenomenon.

1) In sea turtles, vitellogenesis begins 8 to 11 months before ovulation (Rostal et al. 1998, Hamann et al. 2002). This means that females must allocate a large proportion of their resources to vitellogenesis before commencing their pre-nesting migrations. Sea turtles also commonly do not feed during the breeding season (Houghton et al. 2002; Plot et al. 2013). Gravid turtles may therefore run the risk of not retaining large enough energy stores to ensure survival during pre- and post-nesting migrations if they over invest in egg-production. We propose that to safe-guard against over-investing in egg production, turtles might retain the ability to reabsorb some vitellogenic follicles if their energy reserves drop below a threshold value. By reabsorbing the vitellogenic follicles, it might be possible to mobilize the resorbed lipids for other metabolic needs (Kuchling & Bradshaw 1993) or reduce the time spent in the nesting area by not laying an entire clutch of eggs. If this is the case, then it might be expected that turtles would pre-emptively begin their post-nesting migrations and would also exhibit signs of emaciation, which were not observed in this instance.

2) Egg production, ovulation, and the initiation of migratory behavior all appear to be influenced by the production of a mix of hormones, including follicle-stimulating hormone, luteinizing hormone, progesterone, and testosterone (Wibbels et al. 1990; Wibbels et al. 1992). If there is a premature change in the hormones instigating migration, then turtles might migrate with many remaining vitellogenic follicles.

3) Shelling vitellogenic follicles requires a substantial investment of calcium (Bilinski et al. 2001). Thus, turtles might occasionally not shell all vitellogenic follicles in order to prevent calcium depletion and thus maintain healthy Ca:P ratios.

4) The epoxy method for attaching satellite transmitters, as used in this study, requires that the turtle is restrained for approximately 45 minutes to let the epoxy harden. It is possible that the handling stress could have elicited a ‘flight’ response in the nesting turtle causing it to return prematurely to its foraging area and abandon any attempts at future nesting events.

We recommend that future studies assess the regularity of sea turtles migrating with numerous vitellogenic follicles in combination with evaluations of physiologic status (e.g., body condition, blood chemistry, hormone levels, etc.) to conclusively determine if this is a common phenomenon and to explain its biological function. Understanding how sea turtles balance the costs of reproduction and survival could explain much about sea turtles’ life-history.

Acknowledgements. Jennifer Swiggs provided assistance in the field. We thank Roger Blanco and the Area de Conservación Guanacaste for supporting this research. Financial support for this project was provided by Seeds of Change and The Leatherback Trust. The study was conducted under research permits from The Ministry of Environment and Energy (MINAE) of Costa Rica (#ACG-PI-050-2014). This research was performed in accordance with the Purdue University Animal Care and Use Committee.

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