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Figure 1. The capture site of the green x loggerhead hybrid along with major nesting areas for green and loggerhead turtles in Brazil.

The Trident Submarine Turning Basin is a riprap-lined embayment that the University of Central Florida Marine Turtle Research Group has monitored since 1993 to assess juvenile green turtle (Chelonia mydas) abundance and demographics (Redfoot & Ehrhart 2013). A 35.0 cm straight carapace length (SCL) juvenile turtle with intermediate morphology was captured via dipnet on 18 January 2016. The juvenile resembled a green turtle in many respects (Figs. 2 and 3). However, it also exhibited some characteristics typical of loggerhead turtles (Caretta caretta), such as the presence of five lateral scutes, jagged marginal scutes, and a mid-dorsal ridge (Wyneken 2001). The prefrontal scales were partially subdivided and therefore intermediate between a single pair expected for greens and two pairs expected for loggerheads. Overall, these characteristics suggested a possible hybrid origin for this individual.

We assessed the possible hybrid identity through sequencing of maternally inherited mitochondrial DNA and fingerprinting of bi-parentally inherited nuclear microsatellite markers. An 817 base pair fragment of the mitochondrial control region was amplified using PCR primers LCM15382 and H950 (Abreu-Grobois et al. 2006) and sequenced as previously described (Shamblin et al. 2014). The sample was genotyped at six microsatellite loci that are species informative between loggerhead and green turtles (Shamblin et al. 2007, 2009; Shamblin, B.M. & C.J. Nairn, unpubl. data), using an Applied Biosystems 3730xl capillary DNA Analyzer at the Georgia Genomics Facility, University of Georgia. Four markers are species diagnostic in that green turtle alleles fall entirely outside of loggerhead microsatellite arrays or fall between loggerhead bins such that no alleles are shared between the species (CcP1H11, Cc1G03, Cc7H04, Cc7E11). Two additional markers have partially overlapping arrays where some alleles are species-specific and others are shared between the two species (CcP1B03, Cc2H12). Allele sizes reflect DNA fragment lengths to the nearest base pair amplified from directly labeled, newly designed primers for these loci (Shamblin et al. 2017).

Table 1. Microsatellite genotypes expressed as base pair allele lengths for the juvenile green turtle x loggerhead hybrid captured at Trident Basin, Florida, USA. * indicates species informative markers. ** indicates species diagnostic markers. Cm alleles have been detected in green turtles only. Cc alleles have been detected in loggerheads only.

Figure 2. Carapace of the green turtle x loggerhead turtle hybrid illustrating five costal scutes and jagged marginal scutes typical of juvenile loggerhead turtles. Photo by D.A. Bagley.

Figure 3. Head of the green turtle x loggerhead turtle hybrid illustrating typical green morphology, with the exception of the prefrontal scales. Photo by C.A. Long.

The juvenile turtle carried maternally inherited loggerhead mitochondrial haplotype CC-A4.2, the dominant haplotype in all Brazilian loggerhead rookeries and not known to occur in any other nesting populations (Shamblin et al. 2014). All microsatellite genotypes yielded one species-specific allele at each marker (Table 1). The combination of markers indicated that the juvenile was a first generation hybrid between a male green turtle and female loggerhead and suggested that it originated from a Brazilian loggerhead turtle nesting beach. Hybridization between a male green turtle and female loggerhead was previously reported from a clutch of eggs sampled in Bahia, Brazil (Karl et al. 1995). These investigators hypothesized that hybridization may arise due to the difficulty of finding conspecific mates when one species is abundant and the other is relatively rare. The primary loggerhead turtle nesting beaches in Brazil occur along the continental coast from Sergipe to Rio de Janeiro, with the highest densities along the northern coast of Bahia (Fig. 1) (Marcovaldi & Chaloupka 2007). Conversely, the major green turtle nesting sites in Brazil are on oceanic islands: Trindade Island, 1,100 km off the southeastern coast and the archipelagos of Atol das Rocas and Fernando de Noronha off the northeastern coast (Marcovaldi & Marcovaldi 1999). Nonetheless, small numbers of green turtle nests are recorded in Bahia (Dow et al. 2007), raising the possibility that rare courting green turtle males in typical loggerhead courtship areas may mate with the more abundant receptive loggerhead females.

Juvenile loggerheads from Brazil have rarely been detected in the North Atlantic. To date, there have been only two observations of loggerheads found in the North Atlantic with flippers tags from Brazil (Lima et al. 2014). In genetic surveys, loggerhead haplotype CC-A4 was recorded in one of 389 oceanic juveniles in the Northwest Atlantic (LaCasella et al. 2013), one of 329 oceanic juveniles in the Northeast Atlantic (Monzón-Argüello et al. 2009), and one of 1,437 neritic juveniles foraging along the southeastern United States coast (Bowen et al. 2004). Similarly, neritic juvenile green turtles of South Atlantic origin are also rare along the southeastern United States coast, with mixed stock analyses suggesting Ascension and/or West African rookeries rather than Brazilian contributions to account for individuals carrying CM-A8 (Bass et al. 2006).

Despite genetic data suggesting limited trans-equatorial dispersal in the western Atlantic, this connectivity is supported by oceanic juvenile loggerhead distributions and modeling from the Brazilian rookeries. Modeling under the assumption of passive drift suggests two strongly divergent trajectories for loggerhead turtle hatchlings departing the Bahia coast: a northern track that follows the Brazilian coastline into the Caribbean Sea with the possibility of entering the Caribbean or North Atlantic gyre and a southern track into the currents associated with the South Atlantic gyre (Mansfield & Putman 2013). Modeling the relative dispersal of oceanic juvenile loggerhead, hawksbill, and their hybrid offspring indicated that some divergence was temporally driven based on differences in nesting phenology among the parental types (Proietti et al. 2014). Most loggerheads hatching during peak season dispersed to the south, but later season hatchlings were more likely to follow the northern trajectory (Proietti et al. 2014). Satellite tracked oceanic stage loggerheads (10-29 cm carapace length) released early, mid- and late-hatching season from the Bahia rookery suggests that loggerhead turtles emerging late in the hatching season actively orient to remain offshore within currents favorable for transport north into the Northern Hemisphere (Mansfield et al. in prep.), consistent with model predictions. Although it is likely that the majority of Brazilian loggerheads remain in the South Atlantic throughout their lives (Reis et al. 2010), connectivity between Southwest Atlantic loggerhead rookeries and North Atlantic foraging areas may be more common than previous mixed stock analyses suggested from a foraging-centric perspective.

We believe this hybrid turtle was acting like a green turtle for three primary reasons. First, its size is similar to average size of the green turtle foraging population in the Trident Basin (31.7 cm SCL, Redfoot & Ehrhart 2013). Second, the hybrid turtle’s head morphology closely resembles that of a green turtle, with a relatively small head and a lack of powerful jaws (Fig. 3). Third, the Trident site is used almost exclusively by small juvenile green turtles (Redfoot & Ehrhart 2013), which feed on the macroalgae growing on the boulders that line the embayment (Holloway-Atkins & Hanisak 2017). From 1993 through 2011, there were 1,571 turtles captured during in-water studies, of which only 10 were loggerheads (Caretta caretta) and one a hawksbill turtle (Eretmochelys imbricata); the rest were green turtles (Redfoot & Ehrhart 2013).

That the Trident juvenile behaved like its paternal parent contrasts with the migratory behavior of the best-studied marine turtle hybrids, hawksbill x loggerhead turtles nesting in Brazil (Lara-Ruiz et al. 2006). Satellite tracks for five of six hybrid turtles nesting in Bahia identified foraging home ranges off the northern coast of Brazil (Marcovaldi et al. 2012), consistent with foraging areas previously identified for Bahia-nesting loggerhead turtles (Marcovaldi et al. 2010). All pure hawksbills traveled to foraging sites along the east coast of Brazil, and only one hybrid female migrated south to a foraging area in proximity of hawksbill foraging home ranges (Marcovaldi et al. 2012). These data suggest that most Brazilian hawksbill x loggerhead hybrids displayed migratory (and likely foraging) behavior consistent with their mothers despite more closely resembling their fathers morphologically. Nonetheless, the outlier also suggests that behavior may vary even among individuals with the same genetic makeup departing from the same nesting areas.
Hybridization may be fostered in areas where an abundant species and a rare species overlap (Karl et al. 1995). Biases in sex ratios across species sharing courtship areas can arise via temporal variation in nesting phenology. In cases where males are not resident near the nesting beach, they typically leave foraging areas and arrive in courtship areas prior to the arrival of females (James et al. 2005, Hays et al. 2010). Where nesting seasons may be asynchronous among species, males representing the later nesting species may arrive to find an abundance of females of the earlier nesting species. This scenario was invoked as a mechanism to explain the Brazilian hawksbill x loggerhead hybrid swarm (Vilaça et al. 2012) and would apply to green turtle x loggerhead hybridization as well, given the later nesting season for green turtles relative to loggerheads in areas where their nesting distributions overlap. This variation in nesting phenology among species may have important implications for colonization of novel nesting habitats where one species is already well established.

It is unclear whether green turtle x loggerhead hybrids are fertile. All such hybrids genetically characterized to date appear to represent first generation crosses between green turtle males and loggerhead females (Karl et al. 1995, James et al. 2004), implying that they may not be reproductively viable. Nuclear analyses of the Brazilian hybrids confirmed the fertility of first generation hawksbill x loggerhead hybrids and suggested introgression into both parental species (Vilaça et al. 2012). These analyses also identified a hatchling that contained loggerhead, hawksbill, and green turtle nuclear DNA, which was hypothesized to have been the offspring of mating between a male green turtle and a female hawksbill x loggerhead hybrid (Vilaça et al. 2012). The Brazilian data suggest that hybrids within marine turtle tribes may be fertile and capable of introgression. An adult male hawksbill x green turtle that was raised from wild-collected eggs at the Cayman Turtle Farm mated with green turtle females and had motile sperm (Karl et al. 1995), but the fertility of Chelonini x Carettini hybrids and their ability to produce viable offspring through parental species backcrosses remain unknown.

Nuclear analyses of the Brazilian hawksbill x loggerhead swarm suggest that despite some introgression, most of the hybridization between these species is recent and ongoing (Vilaça et al. 2012). It is unclear how common these hybridization events are outside of Brazil. Researchers, rehabilitators, and beach surveyors should be vigilant and document any unusual individuals during routine activities, and hybrid status of these individuals should be confirmed genetically where possible. Even if hybridization is rare and does not represent a threat in a conservation context, assessment of hybrid individuals will continue to offer insights into behavior and ecology of the parental species. Integration of genetic, stable isotopic, and tracking technologies in studying these hybrid individuals could prove particularly powerful in exploring natural history variation among the marine turtle species.

Acknowledgments. Funding for the in-water sampling was provided by the US Fish & Wildlife Service. Access to Trident Basin was facilitated by the Cape Canaveral Air Force Station, U.S. Air Force and Naval Ordnance Test Unit, U.S. Navy. All activities were conducted under IACUC-approved protocols and the following federal and state permits: NMFS Endangered Species permit #14506 and Florida Marine Turtle Permit #231.

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