Amer. Zool., 20:597-608 (1980)

The Ecological Strategies of Sea Turtles1

John R. Hendrickson Departmentof Ecology and EvolutionaryBiology, University of Arizona, Tucson, Arizona 85721

Synopsis. By employing concepts such as "option" and "strategy" from game theory, this study derives an ecologically-oriented dendrogram of the probable evolutionary history and the present relationships of sea turtles. An "armored tank" strategy is seen as differ- entiating the first ancestral testudines from the stem reptiles and providing enduring advantages while simultaneously imposing basic restrictions on all later forms. A "flipper" strategy is postulated as basic to development of the sea turtle line, again imposing limi- tations while conferring selective advantage. Modern sea turtle species are grouped into three lineages representing strategies of habitat-type resource partitioning (a split-habitat, migratory pattern, a neritic residence pattern, and a pelagic residence pattern). Within the split-habitat, migratory group, further resource-partitioning by food-type separates the herbivorous Chelonia mydas populations from omnivorous Eretmochelysimbricata and the (apparently) carnivorous Chelonia depressa. Herbivory is seen as integral to the split- habitat, migratory strategy and C. mydas is considered the most "traditional" species, with the migratory habit secondarily lost in the other two. At the same time, the enhanced philopatry selected for by the migration strategy is viewed as responsible for the fact that C. mydasseems to have the most active race-formation ofthe three species. Further habitat- type partitioning in the neritic group, together with food-type partitioning, separates Caretta caretta from the two Lepidochelysspecies. L. kempi is represented as a consequence of Panamanian separation from L. olivacea following the last establishment of the isthmus as a land barrier. The third, pelagic residence, strategy is represented by Dermochelys coriacea, with little further differentiation of the line. The paper attempts to show that the evolution of sea turtles has been ecologically logical, that most conceivable niches for marine turtles are presently filled successfully, and that some predictions may be made with regard to gaps in our existing information.

Introduction gained currency in discussion of ecological and recent Although I suspect that few biologists evolutionary phenomena; pub? lications 1957, is the earliest will be in much doubt about the subject of (Waddington, reference I to know this discussion, the title itself is trouble- happen about) speak some because of the use of the word "strat? of reproductive strategies, foraging strat? sex ratio and r and egies." The word stems from the Greek egies, gene strategies, K and stratos (army, host) and agein (to lead); its strategies, ecological evolutionary even and English meaning is either strictly military strategies, community ecosystem ... all with reference to entities or a transferred meaning from this, and it strategies and which we cannot make is misused here. It implies rational choice, processes agree rational choices. Louw and an example of correct usage is a com- (1979) correctly ment on the conduct of medical research points out that these usages of the word are and attributed by Bates (1951) to Alan Gregg "strategy" semantically wrong I of Rockefeller Foundation: "Strategy is the philosophically misleading?besides, that most of the users art of deciding when and on what one will strongly suspect mean trick for engage his strength, and tactics is the skill, "stratagem" (synonym: a rather than economy, promptitude and grace with achieving goal) "strategy" of What we are which one utilizes his strength to attain the (art deciding, etc). really about in most cases are ends chosen by strategy." Yet the word has talking complexes of adaptive evolutionary changes, each of which has relative positive and negative 1 values in any one ecological circumstance. From the Symposium on Behavioral and Reproduc? These adaptive tive Biology of Sea Turtles presented at the Annual complexes (phenotypes) are moves in an "existential Meeting of the American Society of Zoologists, 27- game" (Slo- 30 December 1979, at Tampa, Florida. bodkin and Rapoport, 1974), the rules of 597 598 John R. Hendrickson which are the principles of natural selec? tral lines, and include speculation in the tion and probability, and the object of form of "best guesses" when describing the which is to "turn resources into babies" ecological niches of extant species. The (Colinvaux, 1973) so that recruitment rate point is to present, not documented fact, at least equals death rate; past moves, pos? but a way of thinking about sea turtles sibly under different ecological circum? which is consistent with present evolution? stances, place varying limitations on pres? ary and ecological theory and which ent options; there are clearly defined squares in a logical way with sea turtle bi? losers, and the winner's reward is the op- ology as we presently understand it. If the portunity to keep on playing. There is no main framework is correct, it should ac- cognition, no rational choice, no predic? cept embellishment in detail without dam? tion?chance and necessity are all-control- age, and it may in itself predict the content ling. of various information gaps which now ex? Smith (1979) coins the term "phenotype ist. It is conceivable that a haemoglobin set" which I would have preferred to chemist or an endocrinologist might weave "strategy," but then goes on to give this the same fabric from different lines of evi? useful phrase a distinct hierarchical con? dence. text and to speak of the possible behavioral The General Chelonian "Strategy" strategies within the phenotype set. Mitch- ell and Williams (1979) note the difference Obviously, the extant species of sea tur? between the dictionary definition and the tles did not have unlimited possibilities for biological usage of the word "strategy," but developing the phenotypes (ecological pat? then go on to consolidate the usage. I re- terns and attendant morphologies) which luctantly agree with Murtagh (1979) that they show today; earlier "options" selected it is a necessary evil for lack of a simpler during their evolutionary history con- way to label evolutionary designs in con? ferred certain. genetic parameters within text with present-day thought on the sub? which the present species had to develop. ject. It has become jargon, and, while I la- Whether of positive, negative, or neutral ment the birth of this bastard in our family value in any one life circumstance, these of words, I have little choice but to ac? parameters from the past are basic to what knowledge its existence as a counterpart of we can detect today. the nomina conservanda of The selected the " systematics. prime "option" by 'When I use a word/ Humpty Dumpty sprawl-legged ancestral chelonian line said, in rather a scornful tone, 'it means more than 200 million years ago was the just what I choose it to mean?neither "armored tank" mode of body form?the more nor less'^Carroll, 1935). drastic modification of the entire anatomy In the discussion which follows, I at? to provide for encasement in a rigid box tempt an heuristic approach to the evolu? of defensive armor, presumably for de? tionary history of sea turtles, speaking as fense against large, toothed predators. of a complex game played with nature Pritchard (1979) gives a succinct account over the past 200 million years. I try to of early chelonian evolution and mentions show how, given various mixes of oppor- a number of important references. I cher- tunities and limitations implicit in each ish Romer's (1945) statement that: "The "move" of the game, and given the strat? chelonians are the most bizarre, and yet in egies "chosen" by the ancestral sea turtle many respects the most conservative, of line, a logical outcome seems to be the reptilian groups. Because they are still liv? present mix of species and their various ing, turtles are commonplace objects to us; niche spaces. Limited knowledge and lim? were they entirely extinct, their shells?the ited space permit no more than an account most remarkable defensive armor ever as? which hits only the high spots of the game sumed by a tetrapod?would be a cause for and is simplistic in many respects?I con? wonder. From the Triassic the turtles have sider only a few major aspects of body come down to present times practically un- form and attendant function in the ances- changed; they have survived all the vicis- Ecological Strategies of Sea Turtles 599 situdes which have swamped most of the mode to occupy new niche-space, it did reptilian groups and are in as flourishing produce a new set of life challenges a condition today as at any time in the which?under natural selection?had to be past." (In 1945, and with his long view of accommodated by further phenotypic paleontological history, Romer can hardly "strategy." The fossil record appears to be faulted for not recognizing the disas- give evidence of a number of separate at? trous effects of man on these otherwise- tempts by chelonian lines to invade the flourishing species.) sea; I believe that a single group was ul- The highly successful "armored tank" timately successful to the extent of having defense mode adopted by the ancestral representatives living today.2 chelonians involved a number of drastic Compared with the swamp, river, and anatomical modifications which committed land habitats in which the chelonian "ar? the line irrevocably to several important mored tank" strategy proved so successful, limitations on their evolutionary future the vast extent of the ocean environment (see Zangerl, 1969). About a dozen verte- and its relative monotony (lack of local spa? brae were eliminated from the trunk re? tial heterogeneity) must have presented a gion; the ribs were freed from the sternum major new challenge; mobility must have and spread laterally, and the limb girdles become a prime factor for selection. Given were drastically modified to lie partly in? the irrevocable loss of trunk musculature, side the rib elements. In the process of fus- etc. mentioned above, the best adaptation ing the axial skeleton to the bony shell box, (phenotypic "strategy") to provide the req- practically all the dorsal trunk musculature uisite swimming speed and efficiency was lost and the remnants of the ventral seems to be the limb modifications we see trunk musculature were modified for res? in all living sea turtles (see Zangerl and piratory action to make up for the loss of Sloan, 1960). The stiffened, elongate fore- the expansible thoracic cage. The tail was flippers which enable the animals to "fly" drastically shortened to permit retraction through the water with forward propul? into the bony box. With these changes, all sion from both up and down strokes, with possibilities for resuming undulatory the rudder and elevator action provided swimming motion were lost. Expansion by the modified hindflippers, meet the room in the cloacal area was severely lim? need in a rather elegant way. Given the ited by the bony box and the necessary anatomical circumstances imposed by the conditions for giving birth to large, living chelonian mode, I can think of no superior young (as in the ichthyosaurs and most sea adaptation for covering large distances. A snakes) could not be met in the chelonian number of other morphological and phys? line, so they remained tied to the land for iological modifications (e.g., the curious, deposition of cleidoic eggs. cornified papillae lining the esophagus, It is interesting (albeit somewhat myste- etc.) also come to mind in association with rious to me) that, as in the evolution of the commitment to marine life, but these birds, when the anterior appendages be? appear to be subordinate to the major came sufficiently modified for other pur? change in flipper form and function. poses to no longer serve efficiently for And the penalties of success? With the grasping and anchoring prey, while at the full development of the swimming flippers same time there was broad amplification of as a strategy for life in the spacious sea, all keratin formation by the epidermis, cor- possibility of any reasonably efficient mo- nified beak structures appeared and teeth disappeared?presumably forever. 2I disagree with Pritchard's (1979) phylogenetic The Marine Commitment diagram showing separation between dermochelyid While the move into the marine world and cheloniid lines in the Jurassic. I follow Ernst and Barbour in that the ancestors of Der? the ancestors of marine turtles un- (1972) believing by mochelysevolved much later from the cheloniid line, an favor? doubtedly exploited important, probably in Eocene times (see also Zangerl and Turn- able opportunity for the general chelonian bull, 1955; Romer, 1956; Gaffney, 1975). 600 JOHN R- Hendrickson bility on land had to be sacrificed. Not only of nesting beach selection with which we was flight from land predators made ridic- are familiar. ulously inefficient, but the necessary hy? The required production of large num? pertrophy of the pectoral muscles for pow- bers of eggs, combined with the necessity ering the foreflippers interfered with for long distance travel to reach nesting complete retraction of the head, partially beaehes offering the requisite isolation, invalidating the original "armored tank" poses a general problem in energetics. It advantage. Maternal care of a nest (as in seems that all sea turtles must have a rel? crocodilians) became virtually impossible, atively large body mass to solve the im- yet the animals remained tied to terrestrial posed problem of energy allocation for re? egg deposition. production?apparently, there can be no There must have been strong selection small-sized marine turtles as we know at this time for the development of behav? them. ior patterns leading to choices of isolated The foregoing describes what I believe beaches for nesting, where there were Smith (1979) would call the "phenotype minimal risks of predation by land animals set" of the living sea turtles?the complex on the vulnerable adults and the unpro- of morphological and behavioral charac? tected nests. It is interesting to note that ters common to all seven species. They are the and Zangerl Sloan (1960) account of all large animals with elongate, "flying" the primitive cheloniid Desmatochelys lowi front flippers and "rudder" hind flippers Williston from the Cretaceous not only for efficient, sustained, long-distance trav? its analyzes primitive "flying" flipper de? el in the sea; all have unusually high fe? veloped from the ancestral chelonian type, cundity by reptilian standards, with pre? but also describes the fossil site as probably cocial young suffering high initial mortality, an island in the Benton Sea which then etc. From this point onward, the story is of covered the South Dakota region where radiation within the major set and the for? the fossil was found. mation of minor, species-level phenotype nests mean Unprotected precocial young sets or strategies fitted to different ecolog? which must meet, unassisted, the chal- ical niches. There is no reason to doubt of the lenges environment. For baby sea that this process, which I view as essentially turtles leaving the nest and crawling to the one of resource partitioning in the broad this sea, implies the devastating early mor? sense, has gone on continually since the tality rates so characteristic of marine time true sea turtles first appeared. In A species. strongly concave survivorship terms of the "game" paradigm employed with curve, high mortality during the early here, this amounts to the constant testing life stages, was presumably inescapable un? of the opponent (the changing environ? der such circumstances (see Pearl, 1929; ment) through secular time by deployment Krebs, 1972). of new minor variants of the sea turtle I believe it was here in the evolutionary mode, with continual extinctions of some history of sea turtles, coincident with the phenotypes and establishment of others, "flipper commitment," that the reproduc? but with some group of sets always surviv? tive strategy common to all living sea tur? ing to continue the testing. The forms liv? tles All our developed. living species pro? ing today are the temporary membership duce large numbers of eggs which are of this changing series. deposited, one oviducal load following The Modern Species of Sea Turtles another, in a sequential series of subter- ranean nests the dug by female under con? The seven presently recognized species ditions of and then left of peril without fur? sea turtles are placed in five genera, rep? ther attention. I believe there was no resenting two families. It is useful to visu- alternative but to resort to this "numbers alize a branching evolutionary tree which game" so different from that shown by al? extends into the present time-slice at seven most all other and to reptiles, develop the points and has n twigs terminating in times (sometimes complex) behavioral patterns past. The names we apply are only labels Ecological Strategies of Sea Turtles 601 hung on various lower branches and twig- other. Biological energy fluxes and asso? ends, placed to indicate meaningful rela? ciated possibilities for food resources are tionships, but nevertheless arbitrary. I highest in the continental shelf habitat- have no argument with the common, mod- type with its input of nutrients from the ern placement of family labels (see Foot- adjacent continental land masses, lower in note 2, preceding); I am reasonably con? the coastal waters of oceanic islands, and tent with the four generic labels on the lowest of all in the open ocean pelagic cheloniid branchlets and the single label waters. At the same time, the general sea on the dermochelyid branchlet, but I be- turtle phenotype set places high value on long to a sizable company of students who isolated beaehes for nesting because of the have strong doubts that all the extant twig- requirement for reduced terrestrial pre? ends are suitably hung with species labels. dation pressure. One strategy for coping Present studies in my laboratory (Hen? advantageously with this situation, partic? drickson, 1980) on the chemical composi? ularly for herbivores whose richest pastur- tion of the shell keratins from different age (sea grasses) is usually in shallow areas populations indicate that Chelonia mydas of coastal deposition where isolated island carrinegra Caldwell, for instance, should be beaehes with few predators are scarce, is reinstated and elevated to full species sta? development of structural, physiological tus (a fitting action for the present sym? and behavioral adaptations to permit mi? posium honoring Archie Carr!). In the gration between feeding and remote nest? present paper, however, I shall confine my ing areas across the intervening expanses remarks to the seven "official" species list? of open water. A good example is the Che? ed in most current works, merging carri? lonia mydas (L.) population which feeds on negra with the rest of species mydas in the the Brazilian coast and nests on Ascension genus Chelonia. Island (see Carr, 1975). This appears to be The seven species have a great deal in the strategy adopted by the group of common, as described above, but they also species which Zangerl (1958) places in his show considerable differences in their re? Tribus Chelonini on the basis of what he alized ecological nices along with related, interprets as "pelagic" modifications. The minor differences in morphology. I find it remainder of the cheloniids are placed by useful to view these differences as the con- Zangerl (1958) in his Tribus Carettini, sequence of a partitioning of the spectrum which he considers to be less modified for of resources available to the sea turtle phe? open ocean travel. To me this latter group notype set in past and present times, and represents the alternative option available will attempt description of each species in to carnivores unrestricted by distribution this context. of pasturage plants; they can maintain res? Schoener (1974) concluded that niche idence in continental neritic waters and segregation by resource partitioning ac? trade off the advantages of remote nesting cording to habitat-type dimensions is in for the metabolic savings implicit in not general more important than partitioning making extensive migrations. by food-type dimensions, which is in turn Zangerl's (1958) separation of cheloniids more important than partitioning by tem? into tribes, based largely on paleontologi- poral dimensions. This seems to apply to cal evidence, is acceptable to me as a broad the ecological evolution of sea turtles, and separation of niche space. He places it in to have an attractive correspondence with Oligocene/Miocene times, although other Zangerl's (1958) and Zangerl and Turn- workers might place it earlier (see Ernst bull's (1955) arrangement ofthe cheloniid and Barbour, 1972). sea turtles according to paleontological evi? In Zangerl's (1958) Tribus Chelonini be? dence. long Chelonia mydas (Linnaeus), C. depressa A basic division of the habitat resources Garman, and Eretmochelys imbricata (Lin? in the world ocean may be made between naeus). In his Tribus Carettini belong Car? the neritic waters of continental shelves etta caretta (Linnaeus), Lepidochelys olivacea and oceanic islands on the one hand and (Eschscholtz) and L. kempi (Garman). He the vast spaces of open, deep sea on the does not consider Dermochelys coriacea (Lin- 602 John R. Hendrickson

Dermochelys Eretmochelys Chelonia Chelonia coriacea Imbricata mydas depressa (race ft>HJIM)

"jj|lly" Omni^ory Herbivory Carftivory Anti-TrSpical Tropical Tr%phic (Molldtecs) (Crustaceans) Cfc%,1n

PELAGIC SPLIT-pABITAT, NERlllC St^iiGY migr|tory STRAlfGY% STR/|irEGY (Caretfini) (Chellnini)

CHEfpNIOID "Flipper" (Carettoohelyoids) \ STRATEGY (Pleurodires) (Trionyehoids)

TESfJDINE "Armoied Tank" STR|TEGY

Stem R|ptiles Fig. 1. Ecological strategies in sea turtle evolution.

naeus); I conceive of this species as an tioning and sometimes significantly alter- aberrant, highly specialized offshoot from ing the original niche-space. Such later the chelonioid stem which adopted a third change seems to have been particularly option with regard to habitat partitioning common in the chelonins (Tribus Chelon- among sea turtles, possibly in Eocene times ini), presumably because the development (Romer, 1956; Ernst and Barbour, 1972; of highly directed, philopatric migration Gaffney, 1975). The strategy for Dermoche? behavior enhanced the genetic isolation of lys consists of forsaking benthic feeding populations and provided greater oppor- grounds entirely and specializing in ad? tunity for fixation of new strategic "moves" aptations for planktonic feeding and per- at the population level. It is difficult to ex? manent residence in the open ocean waters plain in any other way the chelonin group (except for the obligate terrestrial nesting tendency toward race-formation and spe? common to all testudines); this is discussed ciation in a connected world ocean. Such further in the species account for Der? radiation, originally contributed-to by the mochelys. Figure 1 illustrates my concept of migrational habit, apparently included in the evolution of ecological strategies in sea a number of instances a reversal of the turtles preceding and following this major base trait and adoption of non-migratory three-part division. habits where shifts in diet permitted sur? Further habitat specializations presum? vival without the energy-expensive migra? ably occurred subsequent to the above-de- tions (see below). scribed strategic "choices" made by the In the species accounts which follow, I ancestors of modern sea turtles, often shall treat the taxa and lesser population coincident with food-type resource parti- units from the above point of view, delin- Ecological Strategies of Sea Turtles 603 eating their individual ecological niches parent incompetence for dealing with solid (strategies) as I see these on the basis of obstacles; captive juveniles which I reared available information on sea turtle natural for up to 18 mo seemed to have no "re? history. verse gear," reacting to contact with the solid walls of their tanks by swimming har- der and battering themselves unceasingly coriacea (Linnaeus), Dermochelys against the obstacle. Limited success in the turtle leathery captive maintenance was possible only by This is a true pelagic animal, highly building an inner wall of flexible, polyeth- adapted for life in the open ocean. Among ylene film in a circular tank and creating the more obvious morphological adapta? a strong rotary flow in the water mass. tions of Dermochelys coriacea for pelagic life The behavioral adaptations for pelagic are its powerfully developed swimming life make the general testudine group con? flippers (differently proportioned and dif? straint of terrestrial nesting even more of ferently structured from those of other sea a challenge for this species than for the turtles), its sculptured carapace ridges others. Leathery turtles nest, for the most (which I take to be adaptations for han? part, on mainland beaches with deep water dling problems of laminar flow associated approaches where strong, on-shore cur? with sustained swimming at speed), and its rents produce steep-fronted beach pro? large size with consequent low surface-to- files; such circumstances permit access to mass ratio permitting maintenance of ad? nesting elevations above high tide levels by equate core body temperatures in cool comparatively short crawls. The extreme waters (Frair et al., 1972). All these fea? difficulty which this incomparable swim- tures support a wide-ranging life on the mer experiences during land locomotion high seas, where accessible food items of accounts, I suggest, for the fact that Der? suitable size are sparsely distributed or mochelys shows the most exteme stereotypy patchy. I view this line as an early branch of all sea turtles during its period of emer? off the chelonin stem which found a food gence from the sea for nesting. niche in the open ocean and rapidly evolved for sustained residence there. Chelonia Dermochelys coriacea has become so spe? mydas (Linnaeus), the sea turtle cialized that it is more strictly limited to its green open sea habitat and specialized diet than As noted above, although the C. mydas the other living sea turtles are tied to their migrating between Brazilian feeding particular niches. It is apparently an obli- grounds and Ascension Island nesting gate jelly-feeder (medusae and other ge- beaches are considered here to typify the latinous plankton); little other food has "chelonin option" of long distance travel been found in stomachs, and captive between separated habitats, there are nu? young animals do poorly on other diets. It merous variations on this pattern. The is interesting to note that this specialized Costa Rican/Nicaraguan population so diet, on first consideration seeming so un? thoroughly studied by Archie Carr (see a likely source of adequate sustenance for Carr et al., 1978 and earlier papers cited such a giant, probably places the leathery there) shows well-defined migration, but turtle at the top of a distinctive marine remains coastally oriented and does not food chain based upon nannoplankton re? cross open ocean waters to reach its nest? sponsible for more than half of the total ing ground on the (relatively isolated) primary production of pelagic waters, mainland bar beach at Tortuguero. The which chain is largely independent of the Hawaiian and Galapagos populations ap? more commonly recognized trophic sys? pear to be permanent residents of these tems supporting whales, tunas, etc. (Greve oceanic island groups, feeding mainly on and Parsons, 1977). algae instead of sea grasses. A number of Behaviorally, leathery turtles demon? other variations on the presumed standard strate the extent of their adaptation to a pattern have been described, but these ex? three-dimensional, liquid world by an ap- amples serve to illustrate the point. This 604 John R. Hendrickson species appears to be more clearly divided known about it is contained in reports by into distinct, variant populations than are Bustard and Limpus (1969), Limpus other sea turtles. (1971), and Bustard (1973, 1979). I believe Broadly speaking, it is possible to char? it is a population which evolved to species acterize the species mydas as one distinctive status on the northern coasts of Australia by its herbivory. All populations, regard- and has since spread south ward along both less of their variation from the migratory eastern and western coasts to occur sym- pattern postulated for the original chelo- patrically with C. mydas in some areas. The nin strategy, appear to show strong phil- main elements of C. depressa's ecological opatric behavior and remarkable site-fixity strategy appear to be related to non-mi? in nesting. Another behavioral feature gratory habitation of an especially isolated which seems to distinguish green sea tur? region of shallow coastal waters where the tles from the other sea turtles is the dig- nesting beaches were free of large, terres? ging of a distinct "body pit" as deep as or trial carnivores. There is no firm infor? deeper than the carapace, in which the fe? mation on diet, but some aborigines be? male rests in an approximately horizontal lieve the flatback feeds largely on sea position before beginning the excavation cucumbers (Cogger and Lindner, 1969, of the discrete cavity in which the eggs are cited in Bustard, 1973), and several re? deposited. The end result seems to be the ports indicate that the flesh is unpleasant positioning of the egg mass at a relatively by comparison with green turtle flesh?an lower level in the beach sand than in other observation commonly made when green species, sizes of the ovipositing females turtle diets tend toward carnivory. One being approximately equal. also recalls the relatively large head of C. All green sea turtle hatchlings are dis- depressa and the tendency toward large- tinctively countershaded black above and headedness in the carnivorous carettins clear white below?a feature in which they (see below). differ from other cheloniid hatchlings and Evolving in the absence of placental car? which Bustard (1970) interprets as adap? nivores (before the advent of the dingo tive for juvenile life on the open ocean. with aboriginal man), the principal verte? There is still much uncertainty about brate predators on flatback nesting beach? nesting cycles of sea turtles (see Hughes, es were presumably birds, important 1980) but I expect that, when more facts threats only to hatchlings. The flatback has are available, it will be found that C. mydas apparently lost most of its heavy, keratin- tends to lay more eggs per season, with ous armor, to the point where fairly light longer periods between nestings, than do scratches will draw blood. Bustard (1973, other sea turtle species. (Hirth, 1971, ar- 1979) indicates that it is frequently a day- rives at a trial calculation of 17% of body nester, influenced more by tides than by weight for the eggs a female C. mydas de? ambient light. It lays a smaller clutch of posits during one nesting season.) Such a larger-sized eggs than other Chelonia, and trend toward "big-bang" reproduction these hatch into significantly larger hatch? would be consistent with the heavy energy lings, too large for the available bird pred? investment implicit in the chelonin migra? ators to swallow comfortably (Bustard, tory pattern which I consider to be best 1973). The hatchlings differ markedly represented among extant species by the from C. mydas hatchlings in coloration as green sea turtle. well as in morphology, being gray dorsally rather than black. Bustard (1970) inter- prets this to mean that young flatbacks do Chelonia Garman, depressa not go to open, pelagic waters for juvenile the flatback turtle residence?a feature which would accord This distinctive, large-headed Austra? with a non-migratory strategy. I expect lian species with a depressed and reflexed that, when data from tagging programs on carapace is presumed here to represent a the flatback become available, the species fairly recent offshoot from the C. mydas will be found to show a high frequency of line (see Fig. 1). Most of what little is annual nesters. Ecological Strategies of Sea Turtles 605

Eretmochelys imbricata (Linnaeus), that hawksbills are largely solitary nesters the hawksbill turtle which show exceptional alertness and free- dom from stereotypy during the nesting The hawksbill is represented here as process (Carr et al, 1960). another specialized offshoot from the Che? Caretta caretta lonia line, probably separated from the (Linnaeus), the turtle main stem for a longer period than C. de- loggerhead pressa, but still having a strong genetic sim? This species and the two species of Lep? ilarity to C. mydas. Intergeneric mating can idochelys belong in Zangerl's (1958) Tribus produce viable offspring. Earlier this year, Carettini and represent what I consider to I had the opportunity to examine a group be the third major strategic choice made of about 18 animals on the Cayman Turtle by ancient sea turtles?neritic residence Farm which were clearly the results of a with adoption (continuation?) of carnivory hybrid cross between Chelonia mydas and (Fig. 1). Between the genera Caretta and Eretmochelys imbricata. The turtles (some- Lepidochelys there seems to have been a thing over 2 yr old when I saw them) had two-fold partitioning of resources, divid- hatched from a batch of wild-laid eggs im? ing both habitat regions and principal food ported from Surinam in a routine ship? items. Both genera show less evidence of ment for farm stock during the period be? race-formation than do the chelonin gen? fore the farm stopped all recruitment era. from the wild. The 5-8 kg individuals The ecological strategy of the logger? showed wide gradations and mixes of head appears to be one of antitropical dis? characters between C. mydas and E. imbri? tribution and mollusc-feeding. Although cata (one wonders if they will be fertile loggerheads range widely and appear to when mature?!). tolerate low temperatures better than any The hawksbill's strategy for survival other species except the leathery turtle, seems to be that of a coral-reef-scroung- their main concentrations are over pro? ing-omnivore tied closely to coral reef hab? ductive sea bottoms on the eastern sides of itats which supply both feeding and nest? continental masses where the general ing requirements within a small spatial water movement is from the tropics to? range. Most ofthe adequately documented ward cooler regions (exception: the Med- reports of human poisoning after con? iterranean populations). Loggerheads sumption of sea turtle flesh relate back to characteristically nest on mainland beaches this species, no doubt in correlation with (exception: the Japanese populations). its omnivorous food habits. Although While there do seem to be migrational there is a regrettable lack of quantitative movements in this species, they appear to information on hawksbills from tagging be more a seasonal drift-and-return pro? programs, there is general agreement that cess than directed movement between dis- it is basically a solitary nester which does tinctly different habitats as in the chelonin not engage in distant migration. Bustard mode. The heavy head and jaw structure (1979) reports hawksbill populations in the of the loggerhead are presumably direct Torres Straits which nest on coral cays only adaptations to their molluscan diet, al? a few miles apart, yet are "readily distin- though there are numerous reports of Ca? guishable on carapace morphology, color? retta feeding on other prey, including jel- ation, and shell thickness." The strategy lies at the sea surface and mangrove leaves tying the species strongly to coral reef in the shallows. areas is adequate to explain why hawksbills olivacea are found nesting mainly, but not only, on Lepidochelys (Eschscholtz), the olive turtle islands. The general pattern of living ridley where the reefs are would provide less So little is known of the non-nesting life consistent isolation from land predators of the olive ridley that any attempt to de- than is common for the other species; this, scribe its full ecological niche, or strategy, in turn, conforms with the observations must necessarily resort to educated guess- 606 John R. Hendrickson work with regard to some important de? annual nestings, conforming with the ca- tails. The species shows an interesting rettin mode of less energy expenditure for complementary distribution and diet to its major migrations leaving more energy fellow carettin, the loggerhead, in that L. available for reproductive effort. olivacea is strongly tropical in distribution (Garman), (at least for nesting) and seems to feed Lepidochelys kempi the turtle mainly on decapod crustaceans (Fig. 1). Kemp ridley Like Caretta, both species of Lepidochelys I view this species as a special, recent off- are, for the most part, mainland nesters. shoot of the L. olivacea line following final The olive ridley apparently resides farther emergence of the Panamanian land bar? offshore than the loggerhead during the rier and isolation from the major East Pa? non-breeding portion of its life; many re? cific populations of L. olivacea. The Kemp ports of "green turtles" far out at sea in ridley is confined to the Gulf of Mexico as the Eastern Pacific are, I believe, based on a reproducing entity, and the entire breed? sightings of olive ridleys. Apparently, this ing population nests on a limited section animal dives deeply to feed on benthic of coastline in the state of Tamaulipas, crustaceans in neritic waters, but I suspect Mexico. Scattered reports of stomach con? that it also may spend long periods floating tents from Kemp ridleys indicate a diet on favorable currents over deep abyssal consisting mainly of portunid swimming waters, feeding on crustaceans such as the crabs. Like the olive ridley, the Kemp rid? red lobsterette (Pleuroncodes) which come ley is prone to formation of massive nest? to the surface at night, as well as on larger ing arribadas, but these characteristically plankton it may contact during the day. If take place during the day for L. kempi in? this be true, the species is tending to move stead of at night, as in L. olivacea. out of the initial carettin neritic habitat and One interesting feature of the ecological into the pelagic world of Dermochelys, but niche of L. kempi involves the question of only in a strictly tropical zone. whether the Panamanian isolation which One of the more remarkable features of presumably triggered its evolution as a dis? both L. olivacea and its sibling species L. tinct species carried with it a major nega? kempi is the reproductive strategy of pred- tive effect. While the Atlantic and Pacific ator-swamping by aggregating in large ocean systems were connected across what groups offshore and, upon suitable stim? is now the Panamanian Isthmus, the west- ulus provided by wind or stormy weather, ward flow of the Atlantic North Equatorial coming ashore en masse to nest in a satu? Current presumably "spilled" into the Pa? ration maneuver on one section of beach. cific system. With the emergence of the Anyone who has endured the conditions isthmus barrier in early-to-middle Pliocene on an exposed beach during a high wind (about 3.5 to 4 million years ago), the en? is probably willing to believe that most of ergy generated by deflection from this bar? the large land carnivores would shun the rier must have made the Florida Current beach at such times, and can testify to the and Gulf Stream more powerful flows, rapidity with which the turtle tracks (and, moving water out of the Gulf of Mexico presumably, odors) are obliterated in the habitat of L. kempi and into the north At? wind-swept sands. The turtles are quite ca? lantic circulation (Berggren and Hollister, pable of nesting individually or in small 1974). At the present time, there are abun? groups, but these massive arribadas (ar- dant records of L. kempi on the eastern rivals) seem to be typical whenever there U.S. seaboard and even in western Eu? are large numbers of individuals in the rope. One must ask whether these individ? nesting population. Richard and Hughes uals, carried outside their critical habitat (1972) suggest that the sites chosen for ar? into what must be highly disadvantageous ribadas may be more a matter of focus by environments, are ever able to make their current patterns than philopatry or site way back to the Gulf of Mexico to join in fixity on the part of the turtles. Tagging the reproductive effort of the species. Or returns indicate a fairly high frequency of is this a gigantic "leak" in the system, con- Ecological Strategies of Sea Turtles 607 tinually extracting an important fraction nesting beaches. From this line, by re? of the population and making such waifs, source partitioning of habitat space and reproductively speaking, "dead" to the diet came Caretta caretta and the two Lepi? species? The majority of the animals re? dochelys species. With the rise of the Pana- corded are well beyond the small juvenile manian barrier, Lepidochelys kempi differ? stages and, therefore, past the early period entiated in the Gulf of Mexico, leaving the of high mortality; they are valuable indi? remaining world population as L. olivacea. viduals in terms of potential recruitment The third group, represented by the pe? to the breeding population. lagic Dermochelys coriacea, has undergone no further speciation by our existing stan? Summary dards. In an attempt to understand the com- I conclude that, not only does the evo? plexities of sea turtle evolution and inter- lutionary history of sea turtles make good pret the histories and relationships of the ecological sense, but that the group meets extant seven species of sea turtles, it is use? the logical expectation of successfully fill? ful to employ a technique of game theory, ing all the major niche space available to treating the various conceivable evolution? sea turtles at present. ary possibilities as options and the selected adaptations of populations and species as ACKNOWLEDGMENTS this it is strategies. Following approach, While all errors in fact and in interpre? possible to identify a basic "testudine op- tation here are mine alone, I must ac- or which had survival tion," strategy, great knowledge the stimulus provided by my value but also certain imposed permanent wife and by former students to set down limitations on descendants ofthe line (e.g., in writing an agglomeration of ideas on for possibilities undulatory swimming which I have expounded privately for were cleidoic became man- forfeited, eggs many years. In particular, I must congrat- When the successful descen? datory, etc). ulate Dr. David Owens on the diplomatic dants of the testudine line invaded the and supportive (and successful!) manner oceanic the successful strat? major habitat, in which he persuaded me into a "put-up- also carried distinctive limitations egy (re? or-shut-up" situation, and Lupe Hendrick? with quired high fecundity precocial son must receive major credit for skilled and massive Fur? young early mortality). assistance with language and form as well ther of the line in a development changing as a ready supply of resolve when my own environment three strat? produced major faltered. E. Balasingam, L. Brongersma, egy classes by a process of resource parti? R. Bustard, A. Carr, S. De Silva, G. The first identifiable from tioning. group, Hughes, and J. Schulz are prominent fossil for evidence, developed adaptations among other "old turtlers" whose findings, in mainland shallow waters com? herbivory insights, and speculations appear here in bined with to energy-expensive migrations one form or another, as filtered through remote islands for From this nesting. my own mind. group, by further ecological strategies, or adaptations, have come Chelonia mydas?a References "orthodox" Eret? relatively descendant, Bates, M. 1951. The nature of natural history. Chap- mochelys imbricata?a variant which has giv? man & Hall, London. W. A. and C. D. Hollister. 1974. Paleo- en up migration and turned to omnivory Berggren, as a member of the coral reef geography, paleobiogeography and the history community, of circulation in the Atlantic Ocean. In W. W. and Chelonia local form depressa?a adapt? Hay (ed.), Studies in paleo-oceanography,pp. 126- ed to a life without strong pressure from 186. Soc. Econ. Paleontologists and Mineralo- land carnivores and apparently itself gists, Special Publ. No. 20. Bustard, H. R. 1970. The of turned carnivorous. The second group, adaptive significance coloration in hatchling green sea turtles. Her? also identifiable from fossil evidence, petologica 26(2):224-227. to a carnivorous life on the con? adapted Bustard, H. R. 1973. Sea turtles, their natural history tinental shelves, without travel to distant and conservation. Taplinger, New York. 608 John R. Hendrickson

Bustard, H. R. 1979. Population dynamics of sea Conf On Sea Turtle Conservation. Smithson. Inst. turtles. In M. Harless and H. Morlock (eds.), Tur? Press, Wash., D.C. (In press) tles: Perspectives and research, pp. 523-540. John Krebs, C. J. 1972. Ecology: The experimentalanalysis of Wiley 8c Sons, New York. distributionand abundance. Harper & Row, New Bustard, H. R. and C. Limpus. 1969. Observations York. on the flatback turtle Chelonia depressa Garman. Limpus, C. 1971. The flatback turtle, Chelonia de? Herpetologica 25(l):29-34. pressa Garman in southeast Queensland, Austra? Carr, A. 1967a. Adaptive aspects of the scheduled lia. Herpetologica 27(4):431-446. travel of Chelonia. In R. Storm (ed.), Animal ori? Louw, G. 1979. Biological "strategies." Science entation and navigation, pp. 35-53. Oregon State 203:955. Univ. Press, Corvallis. Manton, M. L. 1979. Olfaction and behavior. In M. Carr, A. 1967ft. So excellent afishe. Natural History Harless and H. Morlock (eds.), Turtles: Perspec? Press, Garden City, New York. tives and research, pp. 289-301. John Wiley 8c Carr, A. 1975. The Ascension Island green turtle Sons, New York. colony. Copeia 1975:547-555. Mitchell, R. D. and M. S. Williams. 1979. Darwinian Carr, A., M. H. Carr, and A. B. Meylan. 1978. The analysis: The new natural history. In D. J. Horn, ecology and migrations of sea turtles, 7. The G. R. Stairs, and R. D. Mitchell (eds.), Analysis of West Caribbean green turtle colony. Bull. Amer. ecological systems, pp. 23-50. Ohio State Univ. Mus. Nat. Hist. 162(1): 1-46. Press, Columbus. Carr, A. and P. J. Coleman. 1974. Seafloor spread? Murtaugh, P. 1979. Strategy. Science 204:795. ing theory and the odyssey of the green turtle. Pearl, R. 1928. The rate of living. Being an account of Nature 249(5453): 128-130. some experimentalstudies on the biology of life dura? Carr, A., H. Hirth, and L. Ogren. 1966. The ecology tion. Knopf, New York. and migrations of sea turtles, 6. The hawksbill Pritchard, P. C. H. 1967. Living turtles of the world. turtle in the Caribbean Sea. Amer. Mus. Nov. T.F.H. Publ., Jersey City, New Jersey. 2248. Pritchard, P. C. H. 1979. Taxonomy, evolution and Carroll, L. 1935. Through the looking glass. Limited zoogeography. In M. Harless and H. Morlock Editions Club, New York. (eds.), Turtles: Perspectivesand research, pp. 1-42. Cogger, H. G. and D. Lindner. 1969. Marine turtles John Wiley 8c Sons, New York. in northern Australia. Australian Zool. 15:150- Richard, J. D. and D. A. Hughes. 1972. Some ob? 159. [Not seen; cited in Bustard, 1973.] servations on sea turtle nesting activity in Costa Colinvaux, P. A. 1973. Introduction to ecology. John Rica. Marine Biol. 16(4):297-309. Wiley 8c Sons, New York. Romer, A. S. 1956. Osteologyof the reptiles. Univ. of Ernst, C. H. and R. W. Barbour. 1972. Turtles ofthe Chicago Press, Chicago, Illinois. United States. Univ. Press of Kentucky, Lexing- Schoener, T. W. 1974. Resource partitioning in eco? ton. logical communities. Science 185:27-39. Frair, W., R. G. Ackman, and N. Mrosovsky. 1972. Slobodkin, L. B. 1964. The strategy of evolution. Body temperatures of Dermochelyscoriacea: Warm Amer. Sci. 52:342-357. turtle from cold water. Science 177:791-793. Slobodkin, L. B. and A. Rapoport. 1974. An optimal Frick, J. 1976. Orientation and behaviour of hatch? strategy of evolution. Q. Rev. Biol. 49(3): 181? ling green turtles (Chelonia mydas) in the sea. 200. Anim. Behav. 24:849-857. Smith, M. J. 1978. Optimization theory in evolution. Gaffney, E. S. 1975. A phylogeny and classification Ann. Rev. Ecol. Syst. 9:31-56. of the higher categories of turtles. Bull. Amer. Waddington, C. H. 1957. The strategy ofthe genes: A Mus. Nat. Hist. 155(5):391-436. discussion of some aspects of theoreticalbiology. Rus- Greve, W. and T. R. Parsons. 1977. Photosynthesis kin House, George Allen & Unwin, London. and fish production?hypothetical effects of cli- Zangerl, R. 1958. Die oligozanen Meerschildkroten matic change and pollution. Helg. Wiss. Meeres- von Glarus. Schweiz. Palaeontol. Abhandl. unters. 30(1-4):666-672. 73(3): 1-56. Hendrickson, J. R. 1980. Chemical discrimination of Zangerl, R. 1969. The turtle shell. In C. Gans (ed.), tortoiseshell materials and reptilian leathers. Fi? Biology of the Reptilia, Vol. 1, Morphology-A, pp. nal Rept., USFWS contract No. 14-16-0002-3701 311-339. Academic Press, London 8c New York. [to be published as USFWS Endangered Species Zangerl, R. and R. E. Sloan. 1960. A new specimen Report No. 7]. of Desmatochelyslowi Williston, a primitive che? Hirth, H. F. 1971. Synopsis of biological data on the loniid sea turtle from the Cretaceous of South green turtle (Chelonia mydas (Linnaeus) 1758). Dakota. Fieldiana, Geol. 14(2): 1-40. FAO Fisheries Synposis No. 85, Rome. Zangerl, R. and W. D. Turnbull. 1955. Procolpochelys Hughes, G. 1980. Nesting cycles in sea turtles?typ? grandaeva (Leidy), an early carettine sea turtle. ical or atypical? In K. Bjorndal (ed.), Proc. World Fieldiana, Zool. 37:345-382.