Caretta

Meylan, Peter A., Meylan, Anne B. & Gray, Jennifer A., 2011, The Ecology And Migrations Of Sea Turtles 8. Tests Of The Developmental Habitat Hypothesis, Bulletin of the American Museum of Natural History 2011 (357), pp. 1-70 : 53-61

Caretta

SECRETARY, PANAMA: The smallest loggerheads observed at Secretary (45–50 cm SCL) were similar in size to the smallest individuals reported from other benthic developmental sites (table 12). The appearance of Caretta at benthic developmental sites at sizes larger than those reported for Chelonia , Eretmochelys , and Lepidochelys kempii is now generally recognized as a result of an extended epipelagic stage in this species ( Bolten, 2003).

Loggerheads that were relatively small (55–60 cm) were not reported as foreign recaptures for longer periods of time than those that were larger at their last capture at the study site. This is consistent with the hypothesis that the intervening years were likely spent at the study site where they would have continued to grow before departing for presumed adult foraging range. At least three of the six foreign recaptures of Secretary loggerheads could be assumed to have been immature at last capture at Secretary, two on the basis of size (both were 57.5 cm SCL) and one based on laparoscopy. The maturity status of the 72.6, 73.3, and 74 cm SCL animals is uncertain, but they are likely to have been immature as well, given their sizes. Thus, it appears that Caretta enter benthic developmental habitat in Chiriqui Lagoon at about 45–50 cm SCL. They no longer use this site by the time they reach about 75 cm.

THE LITERATURE: Nearly all studies of loggerheads at foraging sites in the West Atlantic (table 12) report turtles in the 40– 50 cm SCL size range as the minimum size observed in their study. Exceptions include a study in Georgia that used strandings ( Frazer, 1987) and a long-term study of Chesapeake Bay that included four outliers ( Lutcavage and Musick, 1985; fig. 26C).

Although generalizations can be made from the literature about first arrival of Caretta into benthic developmental habitats, polymodal foraging by immatures and adults, and frequent occurrence of adults at immature-dominated foraging sites, make recognition of a final developmental migration to adult foraging range very difficult. However, studies of Caretta like those conducted by Limpus et al. (1994b) at Moreton Bay, Australia, and Schroeder et al. (1998) in Florida Bay, suggest that certain areas might be characterized as adult foraging range for this species and these sites seem to have few immatures. Thus, at some point in their lives, Caretta in the Atlantic (but perhaps not in the Pacific; see above) are likely to switch from more immature-dominated to more adult-dominated foraging areas when feeding near shore. However, this transition in the life cycle of Caretta may be more variable than for other species and perhaps should be incorporated into the relaxed life history model for Caretta proposed by Casale et al. (2008).

CONTRADICTORY EVIDENCE

Evidence against the existence of a separate, immature-dominated, benthic developmental stage, distinct from the adult foraging stage, would include the discovery of foraging sites with a well-mixed composition of adults and immatures, or data showing that immature-dominated aggregations are artifacts of modern fishing pressure. The strongest evidence that the immature-dominated benthic developmental stage is not a worldwide pattern for nonpelagic cheloniid sea turtle species comes from C. mydas in the Pacific. Mixed aggregations of immature and adult green turtles occur together on the same foraging grounds at a number of sites in the Pacific, including Australia, Baja California, Galapagos, Hawaii, and Peru. In Australia, both adult and immature (as small as 36 cm CCL) C. mydas are resident around Heron Island and Wistari Reef in the southern Great Barrier Reef system ( Limpus and Walter, 1980; Limpus and Reed, 1985a). Moreton Bay, Queensland, also fits this pattern ( Limpus et al., 1994a). In this bay, 10.9 % of 393 laparoscoped females were mature, another 2.5 % were pubescent; of 206 laparoscoped males, 3.9 % were mature and 1.0 % pubescent. However, large and small turtles were found to have different distributions among the banks within the bay. The area of Flathead Gutter in Moreton Bay, for example, appeared to have resident immature C. mydas that were captured there for periods of up to 3–4 years (Brand- Gardner et al., 1999).

Although C. mydas in Australia may not have a separate immature-dominated benthic developmental stage, size composition varies among foraging grounds ( Lanyon et al., 1989). Large immatures and adults predominate in certain bays (Moreton Bay, Repulse Bay, Shoalwater Bay; Limpus and Reed, 1985b), while in certain coral reef habitats, small- to medium-sized immatures dominate ( Limpus and Reed, 1985a; Parmenter, 1980). On the reef at Heron Island, more than 80 % of the turtles (of all species) are immature green turtles 40–90 cm CCL (Limpus, 1980). Some adult C. mydas are present, but they are not nearly as prevalent as they are in the lagoons, where 50–80 % of the green turtles encountered are adults. Limpus (1980: 9) summarized this early life history stage of C. mydas in Australia as follows:

The young turtles reappear at about the size of a large dinner plate…. [They] take up residence in the shallow water habitats of the continental shelf…these immature turtles may remain in the one feeding ground for extended periods, perhaps years before moving to another major area. At least several such shifts occur in the life of the turtle in this coastal shallow water benthic-feeding stage.

In Baja California at Bahia de Los Angeles, Seminoff et al. (2002) reported a foraging aggregation dominated by C. mydas $ 65 cm SCLn-t, the size at which green turtles in this region near maturity. But about 10 % of the turtles in this foraging aggregation were less than 65 cm. Other sites on the Baja Peninsula were dominated by smaller size classes ( Koch et al., 2006; Senko et al., 2010), but at these sites small numbers of potentially mature (based on size alone) individuals were present. Thus, for C. mydas in Baja California, there also appears to be a less complete separation between late benthic developmental sites and adult foraging range than may be present at some Atlantic sites.

In the Galapagos, Green (1993) reported that C. mydas ranging in size from 46.2– 89.5 cm SCLn-t were marked and recaptured on the same foraging grounds. A minimum size of maturation of 66.7 cm (based on nesting) indicated that roughly two-thirds of the animals recaptured were mature. Additional examples of mixed adult and immature foraging areas are known from Hawaii ( Balazs, 1982) and in the eastern Pacific near Pisco, Peru. At the latter site, Brown and Brown (1982) used the term developmental habitat for an area from which 89 % of a sample of 416 C. mydas was immature, based on an assumed size at sexual maturity of 80 cm. Even if some animals over 80 cm were actually immature, their observations of 27 males with elongate tails and the occasional female with shelled eggs, indicate that adult foraging range overlaps that of immatures along this coast.

There is an alternative interpretation for the immature-dominated foraging assemblages reported here. The work of Limpus and colleagues ( Limpus and Reed, 1985a; Limpus et al., 1994a; Limpus and Walter, 1980) suggested the possibility that survivorship patterns of sea turtle species could produce some of the observed immaturedominated foraging assemblages. Their work on foraging grounds shared by immatures and adults indicated that large numbers of immatures must be present on shared foraging grounds that produce even a relatively small number of breeding adults. Their observations would explain what appear to be developmental habitats as foraging grounds that were historically shared by adults and immatures, but from which the adults were largely or entirely extirpated. It might be expected at these sites that adults would appear in samples taken over long periods of time, especially if associated nesting beach populations were protected. The Bermuda Turtle Project (begun in 1968) may be the best example of a site where protection has existed long enough that if mature C. mydas were going to reappear, they would have done so by now. Other foraging sites with similar circumstances include: the Indian River Lagoon ( Ehrhart et al., 1996, 2007), Inagua, Bahamas, ( Bjorndal and Bolten, 1996), and Wuvulu Island, New Guinea ( Hirth et al., 1992).

The benthic developmental phase is also absent in Lepidochelys olivacea , which may be completely pelagic (but see McMahon et al., 2007). The evolution of a pelagic sea turtle could occur through an intermediate step in which the benthic developmental stage is used intermittently to supplement a pelagic foraging mode. Caretta models such an intermediate condition. Polymodal foraging (Reich et al., 2010) could represent an intermediate evolutionary step before the complete loss of the benthic developmental stage and loss of benthic foraging in adults. Thus, the benthic developmental stage is absent in Lepidochelys olivacea , alternates with a pelagic foraging mode in some Atlantic Caretta , and appears to be absent in Pacific Caretta . However, evidence compiled in this paper provides corroboration of a separate benthic developmental stage in C. mydas , Eretmochelys , and Lepidochelys kempii .

REFINEMENT OF THE DEVELOPMENTAL HABITAT CONCEPT

The goal of this paper has been to test the hypothesis that an ‘‘immature-dominated, benthic developmental stage’’ is a regular part of the life cycle of most species of cheloniid sea turtles. Having assembled the evidence, we believe that the concept is a valid one that can be characterized by the following traits, which are usually exhibited.

BENTHIC FEEDING: Turtles at this stage feed mostly on benthic food items, such as sea grasses, algae, and benthic macroinvertebrates. In the previous, epipelagic stage, they are feeding at the surface or in the water column (Ogren, 1989). Control of buoyancy must be well developed before a turtle can enter the benthic developmental habitat stage. This feature helps to define the lower limit of the stage, but not the upper limit because adults of the species that have this stage are also benthic feeders.

IMMATURES ‘‘ONLY’’: Examination of the hypothesis that certain foraging areas are occupied exclusively or nearly exclusively by postpelagic immatures requires knowledge of the maturity status of the animals. Collection of these data requires laparoscopy in most cases. In too many studies, assessment of maturity is based on size alone. Often the minimum size of sexual maturity for the species is used as an indicator of maturity. This is problematic in species where the size at sexual maturation is highly variable. Furthermore, there is sexual size dimorphism in the green turtle that has gone undocumented until recently ( Godley et al., 2002), so using one minimum size for both sexes compounds the error. In studies where laparoscopy has been used, the existence of all-immature populations has been corroborated.

RESIDENCY AND SITE FIDELITY: Immatures of some species previously described as itinerant or transient are now thought to exhibit both residency and site fidelity at some sites. Carr and Caldwell (1956) and Carr (1967) viewed the green turtle population at Cedar Key as itinerant. They considered the site a station on a ‘‘developmental migration.’’ Similarly, Mowbry and Caldwell (1958) identified Bermuda as a site where immature green turtles occurred but thought they were transient. Shaver (1994) interpreted the data set from the Mansfield Channel, Texas, to indicate that C. mydas there probably remain in the area for a few days to a few months, and do not return to the area after that time. She considered her sample to consist of seasonally resident individuals plus transient animals.

Mendonca (1981) recognized that some degree of residency (up to 2 yr) existed for green turtles in benthic developmental habitats on the east coast of Florida. Mendonca and Ehrhart (1982) described mud covering the margins of shells on 43 % of the green turtles they saw in January 1977, and suggested that these turtles may bury themselves during cold weather. But these authors thought that Caretta at their study site were more transient than C. mydas . Mendonca (1983) tracked C. mydas in Mosquito Lagoon and discovered significant differences in movement patterns between winter and summer months. She attributed extensive erratic winter movements to attempts to depart the mostly enclosed Mosquito Lagoon system.

Turtles in the benthic developmental stage appear to be resident, at least in the case of Chelonia and Eretmochelys in tropical waters in the Western Atlantic. Caretta , Lepidochelys kempii , and a small number of C. mydas that use seasonally available resources travel up and down the east coast of the United States on a regular schedule ( Epperly et al., 1995; Morreale and Standora, 2005; Mansfield et al., 2009; McClellan and Read, 2009). They are probably not itinerant as implied by Carr (1980).

In addition to being resident, C. mydas and E. imbricata at some sites exhibit site fixity. The green turtles in Bermuda were the subject of homing experiments ( Burnett-Herkes, 1974; Ireland, 1979, 1980). The results of those studies and results reported here suggest that individuals of this species can and do return to specific grass flats if removed from them.

Even in areas where immature green turtles occur with adults, they show residency. Sixty-nine of the 71 immatures recaptured by Balazs (1982) were taken in the same ‘‘resident area.’’ Additional residency data come from the work of Brand-Gardner et al. (1999) in Moreton Bay where more that onethird of the C. mydas involved in a feeding study had been marked at the site 3–4 yrs earlier. Strong philopatry was noted on the part of some individuals during the course of the study, with some individuals being observed in the same 0.05 km 2 area up to four times in one week.

MATURATION OCCURS ELSEWHERE: Laparoscopic examinations indicated that maturation was not occurring in the benthic developmental habitats that were studied in Bermuda and Panama. Mendonca and Ehrhart (1982) wrote that immature Chelonia and Caretta in the Mosquito Lagoon might remain resident there until ‘‘they approach maturity.’’ Ehrhart (1983) suggested that the Indian River provided ‘‘a good demonstration of developmental habitat’’ for Chelonia and Caretta , and that ‘‘these turtles move elsewhere to mature.’’ This idea of maturation occurring elsewhere is reiterated by Ehrhart and Witherington (1992) and is supported by the laparoscopy and tag-return data collected in Bermuda and Panama for this study. It is also supported by the work of Limpus (1992) on hawksbills in the southern Great Barrier Reef. However, Ehrhart and colleagues provided data that indicated that at least a small percentage of male loggerheads appear to mature in developmental habitat in the Indian River Lagoon system. Of the 430 Caretta handled during the first 14 years of their study, 14 (3.3 %) were noted as being ‘‘either a maturing male or possibly a maturing male based on relative tail length’’ ( Ehrhart et al., 1996). After 24 years of study, they had seen a total of 704 different loggerheads of which 18 (2.6 %) were likely maturing males ( Ehrhart et al., 2007).

Boulon and Frazer (1990) also recognized that the maturation process occurs away from their study site in the U.S. Virgin Islands. They studied growth in C. mydas at St. Thomas and St. Johns based on the recapture of 41 individuals that were 25.6– 62.3 cm SCL at first capture. They noted the absence of larger individuals and suggested that green turtles were completing the maturation process after departing from the habitats in their study area.

Although some authors have suggested that maturity precedes migration to the adult foraging range (van Dam and Diez, 1998a: 22), the studies reported here that incorporate laparoscopy suggest that maturation typically occurs away from benthic developmental habitat. The onset of puberty occurs at about the same size as departure from developmental habitat in Bermuda and in other studies, suggesting the possibility that the maturation process itself might prompt a developmental migration to the adult foraging range.

When immature C. mydas depart from study sites in Bermuda and Panama, they reappear at foraging grounds (mostly in Nicaragua) known to support adults. The best explanation for the observed pattern of departure and tag-return data is that these turtles will complete the maturation process at these sites, where they will reside as adults. That is to say, the maturation process is completed at the adult foraging range, not in benthic developmental habitats. Bresette et al. (2010) provided evidence for this conclusion at their study area west of Key West, Florida. On the eastern Quicksands, large subadults occur with adults (composite size range 65– 105 cm SCL) and they are geographically separated from the nearest foraging concentration of immatures (25–65 cm SCL) at Mooney Harbor.

RELATIVELY HIGH GENETIC DIVERSITY: Turtles on foraging grounds are drawn from multiple genetic populations. Howev- er, the data available for C. mydas in the West Atlantic indicate that aggregations occupying benthic developmental habitats (n 5 4) show higher genetic diversity than the one studied adult foraging range in Nicaragua ( Bass et al., 2006: table 2). Lahanas et al. (1998) described the pooling effect of the ‘‘lost year’’ stage of sea turtle life history whereby turtles from multiple nesting beaches become mixed in the pelagic environment. This pooled diversity is clearly maintained into the extended pelagic stage of Atlantic Caretta ( Bolten et al., 1998) . It also appears to be maintained into the benthic developmental habitat stage at other benthic developmental foraging aggregations studied so far ( Bass et al., 2006: table 2; Sears et al., 1995; Engstrom et al., 2002; Blumenthal et al., 2009; Velez-Zuazo et al., 2008). When turtles of varying genotypes depart from benthic developmental habitats for adult foraging habitat, there may be geographic sorting that results in individuals occupying adult foraging range with better proximity to nesting beaches for the population to which they belong.

DEVELOPMENTAL MIGRATIONS LONGER THAN REPRODUCTIVE MIGRATIONS: The work at Bermuda reported here has led to the realization that green turtles and hawksbills must travel long distances to reach benthic developmental habitat there and likewise to move to adult foraging habitat assuming that is the next destination after leaving Bermuda. Extensive developmental migrations for Caretta are well documented (Bolton et al., 1998; Polovina et al., 2004) and consist of tens of thousands of kilometers of travel in some cases. But other species also appear to be capable of traveling long distances during developmental migrations. For example, green turtles hatched at Tortuguero, Costa Rica, are represented in benthic developmental foraging habitats as far away as Barbados, North Carolina, and Bermuda ( Bass et al., 2006; BTP, unpubl. data). These sites are about 2600, 2800, and 3000 km straight-line distance from the nesting beach, respectively. Migration from these sites to Nicaragua, the most likely adult foraging range for this population, would be nearly as long, resulting in a total developmental migration of well over 5000 km. As adults, most of these turtles are likely to make their reproductive migrations between Nicaragua and Costa Rica (500 km). The single international tag return in Grenada for a hawksbill tagged in Bermuda and transatlantic movements of Brazilian hawksbills (see above) suggest that some individuals of this species are making developmental migrations of similar magnitude.

FACTORS OBFUSCATING THE DEVELOPMENTAL HABITAT STAGE

Not all authors writing about sea turtle foraging aggregations recognize the benthic developmental habitat stage as it is considered here ( Lanyon et al., 1989; Miller, 1994). The spatial overlap of life history stages, either on a temporary or permanent basis, is a frequent obfuscating factor. The data on green turtles at Zapatilla Cays, Panama, presented above suggest that developmental habitat that is occupied by large immature green turtles year-round is shared annually with migratory adults from May to September (fig. 23A). A different type of overlap appears to exist for Caretta on the east coast of Florida. Henwood and Ogren (1987) described an immature assemblage of Caretta that dissipates annually when adults arrive to use nesting beaches. Any remaining immature Caretta must share their foraging grounds with internesting adult females and with adult males looking for mates (fig. 23B). Similar overlap appears to occur for both hawksbills and green turtles at American Samoa ( Grant et al., 1997). The hawksbills of Mona Island, Puerto Rico (van Dam and Diez, 1998a, 1998b, and references therein), provide another example where developmental habitat overlaps with internesting habitat and, to some extent, with adult foraging grounds.

Certain sampling methods may not be sensitive enough to detect details of distribution that might be required to recognize differences in habitat use by adult and immature individuals that live in proximity to one another. Among these methods might be rodeo, trawling with long tow times, and collection of data from strandings or certain fisheries.

A major complicating factor in the recognition of the benthic developmental stage along the eastern seaboard of the United States is that occupation of certain benthic developmental habitats is strictly seasonal. A number of studies cited above confirm that Caretta , Lepidochelys , and to a smaller extent, C. mydas , move up the eastern seaboard as the water warms each summer and then either move back south or seaward into warmer waters in the fall as water temperatures drop. Thus, although certain sounds and bays from Georgia to Massachusetts have predictable use by immature cheloniids, sometimes in fairly large numbers, year-round residency at these latitudes is limited by climatic factors.

A frequent reason for the failure to recognize a benthic developmental stage as separate from adult foraging stage is the assumption of the presence of mature animals because some individuals observed are above the minimum reproductive size for that species. Attainment of sexual maturity in sea turtles in not based on size alone. Limpus (1992) provided excellent evidence of the impact of this problem on the understanding of foraging ground ‘‘population’’ structure and the utility of laparoscopy in correcting it. In his sample of 152 Eretmochelys from the southern Great Barrier Reef, 20 animals were larger than the minimum size at sexual maturity (based on minimum size of nesting females). If only these data had been available, one might have assumed that this is a mixed adult and immature foraging aggregation. However, of 109 animals for which maturity status was assessed (including 16 of the ‘‘adult-sized’’ individuals), only one adult (0.9 %) was identified. This suggests the alternative possibility that immature-dominated, benthic developmental habitat exists for Eretmochelys in the southern Great Barrier Reef. In the Limpus (1992) study, the largest immature female was 3.5 cm larger than the average size of nesting females. This is a pointed example of the problem of using size at sexual maturity to extrapolate maturity status in a population of turtles.

Limpus et al. (1994a) provided another example of this phenomenon in their study of green turtles at Moreton Bay, Queensland, where they calculated that the number of mature females in the sample would have been overestimated by 42 % if maturity status were based on size alone. They pointed out that, on average, C. mydas does not mature at a minimum breeding size but rather at a size approaching the average breeding size for the population (average nesting size for females, average mating size for males). It seems clear that using the minimum size of sexual maturity to recognize ‘‘sexually mature’’ individuals will always greatly overestimate the number of mature individuals in the sample.

Finally, there is geographic variation within species in the degree to which a separate benthic developmental habitat stage exists. C. mydas in the Atlantic system provides some of the best evidence for the existence of a separate stage. However, in the Pacific there are few, if any, discrete allimmature, postpelagic foraging assemblages for this species. Similarly, Caretta in the Atlantic has a prolonged stage at sea in their early lives, but most individuals eventually enter benthic foraging habitats at sizes of about 45–50 cm ( Panama: this study; Indian River: Ehrhart et al., 1996, 2007; Chesapeake Bay: Lutcavage and Musick, 1985; etc.). However, no near shore developmental habitat has been reported for Caretta in the Pacific ( Limpus et al., 1994b). Individuals as large as 83 cm are present in the open North Pacific (Polovina et al., 2004), suggesting that in the Pacific, Caretta may remain pelagic until it is ready to enter the adult foraging range. This would agree with observations of recruitment of Caretta to Australian foraging grounds. Limpus (1994) and Limpus et al. (1994b) reported that Caretta recruits to two different foraging grounds at about 80 cm CCL, matures over the next 8–14 years, and then remains resident at these sites.

EVOLUTION OF A BENTHIC DEVELOPMENTAL STAGE

Why does a separate benthic developmental stage in the life history exist in this set of four cheloniid sea turtles ( Chelonia mydas , Eretmochelys imbricata , Lepidochelys kempii , and Caretta caretta )? Congdon et al. (1992) suggested that differential habitat use associated with age or size in turtles may result from changes in diet, distributions of food resources of appropriate size, size-specific risks of predation, or a combination of these factors. A shift in resource use is associated with the change from the epipelagic to the benthic developmental stage but not from the latter to the adult foraging range. For Chelonia , Eretmochelys , and L. kempii , there is no known shift in diet between these stages ( Bjorndal, 1997). Thus, a change in resource use can explain the shift from epiplegic to benthic foraging but does not explain why, in many cases, benthic developmental foraging sites are separate from adult foraging habitat.

Size-specific risk of predation appears to be an important factor that keeps smaller aquatic organisms of many species in shallower water. Congdon et al. (1992) reported that for certain freshwater turtles, there is a tendency for smaller individuals to use shallower water. Thus, an alternative reason for the existence of benthic developmental habitat separate from adult foraging range is that it offers enhanced refuge from predators to immatures that they do not enjoy in adult foraging habitat. Sharks are probably the single most important predator of sea turtles of all sizes ( Heithaus et al., 2002, 2005). Perhaps the shallower inshore areas that typically serve as benthic developmental habitat offer some additional protection from sharks. Estuarine foraging areas may provide a refuge from shark predation because of lower salinity. This is believed to be the case for the Chesapeake Bay (J. Musick, personal commun.) However, a study of tiger sharks in Western Australia showed that these known turtle predators prefer foraging in shallow waters and forage in shallows (, 4m) more frequently than expected based on several measures ( Heithaus et al., 2002). Thus, shallow waters alone may not serve to protect sea turtles from their predators.

Another possible explanation for the existence of geographically separate benthic developmental habitat is resource partitioning by size (or age or maturity status). Because the diets of immature green turtles, hawksbills, Kemp’s ridleys, and loggerheads do not differ significantly from those of the adults, intraspecific competition with adults is possible and, in fact, likely. Classic Lotka- Volterra theory suggests that the ability of a local population (N 1) to increase is negatively affected by the number of individuals of that species already present, plus the number of competitors present, times their respective coefficients of competition. For species of the same approximate body size, if there is no significant ontogenetic shift in diet, it is likely that intraspecific competition will have a larger effect than interspecific competition. Thus, any reduction in N 1 will be an advantage to the population, but only if that reduction is not permanent and those individuals that leave are not lost from the population.

Intraspecific competition can be reduced by geographic partitioning of the habitat. If members of a population can use resources at a distant location (benthic developmental habitats) from the primary residence of a population (adult resident habitats), then the effect on population growth could be favorable. Natural selection should favor populations in which this partitioning takes place. If immatures can delay their return to the adult foraging range, more resources will be available for resident adults to invest in future generations of that population. Furthermore, immatures may be able to occupy habitats that do not contain sufficient resources to support larger adults. In any case, staying away from adult resident habitats may increase their own growth rate by reducing intraspecific competition with adults. Increased growth rate is an added benefit, as it should lead to higher rates of survivorship; most turtles show type III survivorship, with high mortality at the earliest stages that diminishes rapidly as the turtles grow ( Iverson, 1991). Bjorndal et al. (2000b) provided evidence for density-dependent growth in C. mydas , which indicates that intraspecific competition can limit growth rate in this species.

For most sea turtles species, geographic displacement to distant foraging areas is favored by the presence of the epipelagic stage. It is interesting to note that Natator , which is clearly primitive relative to other sea turtles in other life history traits (Van Buskirk and Crowder, 1994), should apparently also lack both an open-ocean pelagic stage and the benthic developmental stage of the life history. This suggests that an epipelagic stage may be a prerequisite for the evolution of an immature-dominated, benthic developmental stage of the life history.

RESEARCH AND MANAGEMENT SIGNIFICANCE OF THE BENTHIC DEVELOPMENTAL STAGE

Developmental habitat is a useful biological concept. Recognition of a separate benthic developmental stage further elucidates the complexity of the life cycle of cheloniid sea turtles and promotes discussion of why this complexity exists. It is also important for research and conservation efforts because each stage of a species’ life history needs to be identified and studied. As pointed out by Bjorndal and Bolten (1996) and illustrated by the fieldwork discussed here, turtles in benthic developmental habitats are easily captured and, with the continual replenishment due to recruits, might be harvested over time with no notable decline. The impact on nesting populations of the harvest of turtles at benthic developmental sites may not be seen at the nesting beach for several decades.

Recognition that life history stages overlap could help to explain unexpected results such as those of Godley et al. (2003). In this case, C. mydas from a single foraging ground showed two very different patterns of movements when satellite tracked. Laparoscopy might have shown that the smaller, more resident individuals were immature, and the large individuals that showed migratory tendencies were mature. Recognition of this stage also may be important in research design. For example, precautions should be taken in genetic studies when attempting to characterize the genetic diversity of an immature foraging aggregation that might be inflated by inclusion of transient adults (Wood, Hardy, Meylan, and Meylan, in prep.).

Recognition of the benthic developmental stage may also be important for the explanation of variance in genetic diversity among ‘‘foraging grounds’’ (see above). It appears likely that genetic diversity in adult resident habitat may be less than that in developmental habitat. The genetic diversity seen in benthic developmental habitats also suggests that losses at a single developmental site may impact multiple genetic populations.

Large immature sea turtles that are ready to depart from developmental habitat have survived the most dangerous years of their lives, and monitoring their numbers could provide a mechanism for predicting demographic shifts in a population. Turtles that complete this stage are demographically important because sea turtles appear to have type III survivorship. But before they can become reproductive adults they have to make a final developmental migration to the adult resident habitat. In some cases, this may be thousands of kilometers away. Tagreturn data from this study suggest that this may be a dangerous time for these turtles, and protection of subadults as they move into adult foraging ranges could be a productive objective of policy change for effective marine turtle conservation.