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- . - ~ ; ~ - - ~ A. [~ ~ [:~ 5 Nalural Mortality and Critical Life Stages his chapter summarizes current information on the causes and mag- nitude of natural mortality of sea turtles, and discusses how sea tur- tles at different life stages contribute to the population or to the reproductive value. Recent analyses of loggerhead populations and reproduction (Crouse et al., 1987) are especially useful for making decisions about conservation of sea turtles, because they help to identify life stages in which reduced mortality can have the greatest influence on the maintenance or recovery of endangered or threatened sea turtle pop ulations. From models developed by Frazer (1983a), female loggerheads proba- bly first nest when about 22 years old, and survivors continue nesting every few years until they are about 54. Most mature female loggerheads nest every second or third year and deposit several clutches of eggs dur- ing a nesting season. Thus, an individual is estimated to lay on the aver- age 80 eggs each year for 30 years. The eggs and hatchlings have high mortality rates, but as the survivors grow, natural mortality declines markedly. About 80% of the nesting females studied for many years at Little Cumberland Island survive from one year to the next. (Chapter 2 presented variations on the pattern of life history of the several species of sea turtles.) These general patterns of mortality and reproduction form a 61

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62 Decline of the Sea Turtles basis for the insight needed to devise a rational program for sea turtle conservation (Crouse et al., 19871. Sea turtles are killed by various animals and environmental phenome- na. Nests and eggs are destroyed by predators, erosion, and inundation by rain or tides. After hatching, turtles of all ages, both at sea and on land, are consumed by predators. They are also subject to debilitating parasites and diseases and are killed by various abiotic factors, including hurricanes and thermal stress. However, quantitative accounts of sea tur- tle mortality in the wild are few. Some of the apparently natural factors that are lethal to sea turtles are associated with human activities. For example, sea turtles are subject to predation by wild, formerly domestic animals introduced by humans (hogs and dogs) or wild, nondomesticated animals introduced by humans (mongoose) or enhanced by human activities (raccoons). Beach erosion is a natural source of mortality that has also been altered by human activi- ties. Predation BIOTIC SOURCES OF MORTALllY Many species, from ants to jaguars, prey on sea turtles. Excellent reviews (which include lists of predators) by Hirth (1971), Stancyk (1982), Witzell (1983), and Dodd (1988) categorize predators by the life stage of sea turtles on which they prey, and the following presentation below fol- lows that pattern. Eggs and Hatchlings on the Becch Predators of the Kemp's ridley at Rancho Nuevo, Mexico, include coy- otes, raccoons, coatis, skunks, ghost crabs, and ants (Marquez M. et al., 19899. Some predators, such as the black vulture, feed on eggs from nests already opened by other predators or erosion. Hatchling Kemp's ridleys are caught and eaten on the beach by ghost crabs, vultures, grack- les, caracaras, hawks, coyotes, raccoons, skunks, coatis, and badgers (Marquez M., in prep.~. The major loggerhead egg predator in the southeastern United States is the raccoon (Dodd, 19881. Before protective efforts were initiated, rac- coons destroyed nearly all the nests at Canaveral National Seashore, Flori- da (Ehrhart, 1979), and at Cape Sable, Florida, raccoons destroyed 85% of

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63 Natural Mortality and Critical Life Stages the nests in 1972 and 75% in 1973 (Davis and Whiting, 19779. The high rate of predation might have resulted from the unusually large raccoon populations, which were augmented by such human activities as habitat alteration, food supplements (garbage), and removal of natural predators of the raccoon (Carr, 1973; pers. comm., L. Ehrhart, University of Central Florida, 19891. Not all nesting beaches in Florida suffer such high losses from raccoons; for example, only seven of 97 nests on Melbourne Beach, Florida, were destroyed by raccoons in 1985 (Withering/on, 19861. Other nest predators are ghost crabs, hogs, foxes, fish crows, and ants (Dodd, 19881. From 1980 to 1982, nonhuman predators destroyed up to 80% of the loggerhead clutches laid on two barrier islands in South Carolina (Hopkins and Murphy, 19831. Management practices have eliminated nearly all the beach predation of Kemp's ridleys at Rancho Nuevo, and reduced predation significantly on most of the important loggerhead nesting beaches. Hatchlings as They Leave the Beach Once in the ocean, Kemp's ridley hatchlings are eaten by a large vari- ety of predatory birds and fish (Marquez M., in prep.~. Loggerhead hatch- lings at this time in their lives also fall prey to a similar array of predators, including gulls, terns, sharks, and other predatory fish (Dodd, 19881. Many Atlantic sharpnose sharks captured in a commercial fishery off Flori- da during the turtle hatching season in 1988 had loggerhead hatchlings in their stomachs (pers. comm., A. Bolten, University of Florida, 19891. Larger Juveniles and Adults in the Water Sharks-and other large predatory fish are important predators of Kemp's ridleys in all oceanic life stages (Marquez M. et al., 19891. Tiger sharks might be selective predators of large cheloniid sea turtles; analyses of stomach contents of 404 tiger sharks showed that 21% of the sharks with food in their stomachs had eaten large turtles (Witzell, 19871. Balazs (1980) has summarized data on predation of juvenile and adult green tur- tles in Hawaii by tiger sharks; turtles were found in 7-75% of tiger sharks sampled in Hawaiian waters inhabited by sea turtles. Nesting Females on the Beach There is no evidence of nonhuman predation of adult loggerhead females on U.S. nesting beaches, but it might have occurred in the past. Reported predators of leatherbacks, green turtles, and hawksbills are similar to those of loggerheads and Kemp's ridleys at each life history stage (Hirth, 1971; Pritchard, 1971; Fowler, 1979; Balazs, 1980; Stancyk,

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64 Decline of the Sea Turtles 1982; Bjorndal et al., 1985; Witzell, 19871. The actual predator species change with geographic region, but are from the same feeding guilds. Diseases and Parasites Most reported diseases in sea turtles have been described in captive animals (Kinne, 19851. Diseases induced by stress or improper diet in captivity and not known to occur in wild sea turtles (Glazebrook, 1980; Kinne 1985; Lauckner 1985) will not be discussed here. An excellent 7 7 . 1 , ~. . 1 1 ~1 ~_ 1 review or the diseases ancl parasites of sea turtles can [~e rouna In LaucK- ner (1985), and specific parasites of sea turtles are identified in the reviews by Hirth (1971), Witzell (1983), and Dodd (19881. Cutaneous fibropapillomatosis, a disease of green turtles, has been recorded infrequently in Florida waters for many years (Smith and Coates, However, large numbers of green turtles have recently contracted the disease in the Indian River lagoon system in east-central Florida (Witherington and Ehrhart, 1989b) and the Hawaiian Islands (Balazs, 19861. In the Indian River, 40-52% of the green turtles captured in 1983- 1988 had fibropapillomas. In Hawaii, 10% of the nesting females at French Frigate Shoals had fibropapillomas, as did 35% of 51 stranded green turtles in 1985 (Balazs, 19861. Recaptured turtles have demonstrat- ed further proliferation of the fibropapillomas, although in other cases regression occurs (Witherington and Ehrhart, 1989a). Tumors can cause mortality indirectly. Turtles whose vision is blocked by tumors are unable to feed normally, and turtles with fibropapillomas are more prone to entanglement in monofilament line and other debris (Balazs, 1986; With- erington and Ehrhart, 1989a). Research on the cause of the disease is in progress (Jacobson et al., 19891. Spirorchidiasis has been reported in loggerheads (Wolke et al., 19821. Severe infestations of spirorchids (blood flukes) result in emaciation, ane- mia, and enteritis, or conversely, emaciation and anemia could make a turtle more susceptible to spirorchid infestation. Three genera of blood flukes were identified in 14 of 43 loggerheads stranded or floating dead from Florida to Massachusetts (Wolke et al., 19821. Spirorchidiasis can result in death or make turtles more susceptible to succumb to other stresses (Wolke et al., 19821. A macrochelid mite (Macrocheles sp.) has been found on Kemp's ridley hatchlings emerging from relocated nests (Mast and Carr, 19851. Mites of the same genus, considered to be nonparasitic, were found on loggerhead hatchlings in South Carolina (Baldwin and Lofton, 19591. Bacterial and fungal infections of eggs can be a major source of mortal 93 ~- -- , --- D - ' ' _ A .

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65 Natural Mortality and Critical Life Stages ity. Bacteria and fungi are implicated as a major cause of death of olive ridley eggs at Nancite, Costa Rica, where hatching success averages only 5% (Cornelius, 1986; Mo, 19881. Microbial pathogens are believed to cause mortality of loggerhead embryos (Wyneken et al., 19881. Other Nesting Turdes Eggs and emerging hatchlings are sometimes killed when their nest is dug into by a nesting female of either the same or a different species. Bustard and Tognetti (1969) described this activity as a density-dependent mortality factor. Although a thorough study of the relationship between nesting density and this mortality factor has not been carried out, clearly the greater the number of nesting females in a given area, the greater the likelihood of a female disturbing an earlier nest. In most areas, this is a minor source of mortality because most nesting populations have densi- ties that are relatively low. However, during the mass nestings (arrib- adas) of olive ridleys, large numbers of nests can be destroyed. Cor- nelius (1986) estimated that 7% of the nests of the olive ridley colony at Nancite, Costa Rica, were destroyed by other females' digging in the same arribada, and another 10% were destroyed by females' digging in subsequent arribadas. In contrast, at Tortuguero, Costa Rica, of 587 green turtle nests monitored, none was destroyed by nesting activities of other turtles (Fowler, 19791. At Mon Repos, Australia, an average of 0.43% of the total seasonal egg production in five consecutive seasons was destroyed by nesting loggerheads (Limpus, 19851. Vegetation Although usually a minor cause of death, plant roots can invade turtle nests and cause mortalities. Invasion by roots of beach morning glory (Ipomoca pes-caprae) and sea oats (Uniola paniculata) killed 275 embryos in three of 97 loggerhead nests on Melbourne Beach, Florida (Withering/on, 1986), and at Cape Romaine, South Carolina, 5% of the eggs laid among sea oats were destroyed by the roots (Baldwin and Lofton, 19593. Destruction of marine turtle nests by sea oat roots also has been reported by Raymond (19841. Plants can also entrap sea turtles. Hatchlings get entangled on their way to the sea (Limpus, 1985) and adult females sometimes become fatal- ly trapped in vegetation or by logs washed onto the nesting beach (Pritchard, 1971; Cornelius, 19861.

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66 Decline of the Sea Turtles ABIOTIC SOURCES OF MORTAU1Y Erosion, Accretion, and Tidal Inundafion In almost every nesting colony, some nests are lost to erosion, accre- tion, and tidal inundation. The extent of mortality varies widely among beaches, years, and species. Nests deposited on shifting beaches are more susceptible to destruction from erosion or accretion. In each species, some turtles deposit nests below the high-tide line. Leatherbacks often nest in areas vulnerable to erosion or inundation: 40-60% of the nests in Surinam were in such areas, compared with 12% of green turtles on the same beach (Whitmore and Dutton, 1985), the Guianas, and St. Croix (Eckert, 1987), but less than 3% in Malaysia (Mrosovsky, 19831. Erosion and inundation destroyed 3-25% of the loggerhead nests deposit- ed each year on two barrier islands in South Carolina in 1980-1982 (Hop- kins and Murphy, 1983), and on Melbourne Beach, Florida, 17 of 97 log- gerhead nests in 1985 were lost to erosion, accretion, and surf action (Withering/on, 19869. Heavy Rains Heavy rain can destroy large numbers of nests. Ragotzkie (1959) reported that all embryos in 15 of the 17 loggerhead nests deposited on Sapelo Island, Georgia, in 1955 and 1957 were drowned by heavy rain. Kraemer and Bell (1978) also reported heavy loggerhead egg and hatch- ling mortality in Georgia resulting from heavy rains. At Tortuguero, Costa Rica, heavy rains and high groundwater drowned all embryos in many green turtle nests in 1986 and 1988 (Horikoshi, 19891. Thermal Stress Hypothermia in sea turtles causes a comatose condition and can result in death. Perhaps the best-documented events are those that occurred in recent years in Long Island Sound, New York (Meylan and Sadove, 1986), and in the Indian River lagoon system, in Florida (Wilcox, 1986; Wither- ington and Ehrhart, 1989b). Both areas can act as natural "traps," because of their geographic configurations (Witherington and Ehrhart, 1989b). Of 52 turtles (41 Kemp's ridleys, nine loggerheads, and two green turtles) stranded in Long Island Sound in the winter of 1985-1986, 18 were alive when discovered and 11 (nine ridleys, one loggerhead, and one green

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67 Natural Mortality and Critical Life Stages turtle) survived after gradual warming at rehabilitation centers (Meylan and Sadove, 19861. Morning surface water temperatures below 8C in 1977, 1978, 1981, 1985, and 1986 caused hypothermic stunning of sea turtles in the Indian River lagoon system, in Florida (Witherington and Ehrhart, 1989b). Those events involved 342 green turtles (25-75 cm SCL), 123 loggerheads (44-91 cm), and two Kemp's ridleys (55-63 cm). Among the stranded turtles, a greater proportion of green turtles than of loggerheads died, and smaller turtles were more susceptible to hypothermia. Most of the turtles were released alive, and many were recaptured months or years later. We have no way of estimating the mortality that would have occurred without human intervention (Witherington and Ehrhart, 1989b). QUANTITATIVE STUDIES OF NAVAL MORTAUh The only life stage for which natural mortality of sea turtles has been quantified is the egg and hatchling stage, including the brief period when hatchlings emerge from the nest and make their way down the beach to the water. Percentage of emergence of hatchlings is measured and report- ed in the literature in two ways. In the first, egg clutches are marked as they are laid and followed through the season; that results in an emer- gence percentage for eggs in all clutches laid. In the second, the emer- gence success of hatchlings from clutches that successfully produce hatch- lings is determined. The former value is the best measure of survivorship. Results in Table 5-1 indicate the range of survivorship values for the egg stage. Of necessity, some studies include sources of mortality related to human activities for example, predation by humans, formerly domestic animals, and wild animals introduced by humans. The rate of mortality resulting from predation is assumed to be much higher for eggs and very small turtles than for larger turtles, because the lists of predators on eggs and hatchlings are much longer than those of predators on larger juveniles and adults. However, there are no quantita- tive studies of predation away from the nesting beach, so the assumption, although a reasonable one, has not been tested. The value of an individual of a particular age or life stage can be stated according to its expected production of offspring, hence the term "repro- ductive value." Reproductive value is the relative contribution of an indi- vidual of a given age to the growth rate of the population (see Mertz, 1970, for a description of reproductive value). The more offspring an individual is expected to produce, the higher its reproductive value. The life stages that we consider below are eggs and hatchlings, small juveniles,

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68 Decline of the Sea Turtles TABLE 5-1 Emergence success of sea turtle egg clutches presented as mean (range). Emer- gence success is the percentage of eggs that produce hatchlings that reach the surface of the sand above the nest chamber. Data are presented only for natural nests (nests not moved or protected) from studies that included those clutches that produced no hatchlings. Clutches Emergence Species and Location (Number) Success (%) Reference loggerhead Tongaland 72 78 (0-99) Hughes, 1974 Brevard Co., Florida 97 56 (0-99) Witherington, 1986 Cape Canaveral (1982) 310 1 (0-90) McMurtray, 1982 Cape Canaveral (1983) 76 3 (0-?) McMurtray, 1986 Green turtles Bigisanti, Sur~nam 57 84 Schulz, 1975 Hawaii 40 71 (0-93) Balazs, 1980 Tortuguero, Costa Rica 318 35 (0-?) Horikoshi, 1989 Florida 25 57 (0-94) Witherington, 1986 Hawlesbill U.S. Virgin Islands 61 60 (0-100) Small, 1982 U.S. Virgin Islands 88 81 Hillis and Mackay, 1989a Tortuguero, Costa Rica 5 36 (0-94) Bjorndal et al., 1985 Antigua, West Indies (1987) 99 79 (0-100) Corliss et al., 1989 Antigua, West Indies (1988) 156 85 (0-100) Corliss et al., 1989 Leatherback Bigisanti, Surinam 52 50 Schulz, 1975 Culebra, Puerto Rico 429 71 (0-100) Tucker, 1989b St. Crow (1983) 98 25 (0-95) Eckert and Eckert, 1983 St. Croix (1984) 123 26 (0-97) Eckert et al., 1984 large juveniles, subadults, and nesting adults (breeders). The life stage with the highest reproductive value is the one for which greater protec- tion can contribute the most to the maintenance or recovery of a popula- tion. Reproductive value can be estimated with population models. Those models have a long history in population ecology, perhaps beginning with Lotka (19221. The models traditionally combine information on age- specific fecundity and age-specific survivorship to yield population pro- jections where survivorship is the percentage of individuals that survived the year and fecundity is the average number of eggs produced per female. Other important factors in the calculations are the number of years required for an animal to reach its reproductive age and the ratio of females to males in the population.

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69 . Natural Mortality and Critical Life Stages The concept of a mathematical value for reproductive value arose from Cole's use of demographic models (Fisher, 19581. A reproductive value of 1 is assigned to a newly laid egg, and all other ages receive valuations rel- ative to that. The idea of reproductive value is fundamental to conserva- tion biology, because it helps to identify the age classes of most signifi- cance for determining future population size. Population modeling is also useful in assessing whether a particular population is growing or declining and at what rate. Its greatest useful" ness, however, might be in sensitivity analysis (Cole, 1954), the estimation of the magnitude of change in the growth rate of the population for each of several changes in such factors as fecundity and survivorship. A sensi- tivity analysis can evaluate, for example, whether a 10% increase in sur- vivorship could have the same effect on population growth as a 50% increase in fecundity. If it did, then the growth of the population would be 5 times more sensitive to survivorship changes than to fecundity changes. Sensitivity analysis is also useful for predicting which of several life stages would be most responsive to a particular management tool. The loggerhead is the sea turtle whose demographics are best known, because loggerheads nest in sufficient numbers along the southeastern U.S. coast to be accessible to scientists, and because one nesting popula- tion on Little Cumberland Island, Georgia, has been subject to intensive tagging since 1964 (Richardson and Hillestad, 1978; Richardson and Richardson, 19821. Frazer has conducted an exhaustive analysis of the Cumberland loggerhead population (Frazer, 1983a,b; 1984; 1986; 1987; Frazer and Ehrhart, 1985; Frazer and Richardson, 1985a,b; 1986) and has provided the algebraic notation for the standard age-based population model of Lotka (19221. Survivorship and fecundity in loggerheads are best estimated by life history stages (eggs, hatchlings, small pelagic juveniles, large coastal juve- niles, subadults, and adults), rather than years of age, so Crouse et al. (1987) used Frazer's demographic data from Cumberland Island logger- heads to apply a stage-based demographic technique for analyzing popu- lation dynamics. The approach, as developed by Werner and Caswell (1977), is analogous to the traditional age-based life-table analysis, but does not require age-specific information. Population factors (Table 5-2, columns 1-4) used by Crouse et al. (1987) in the analyses were calculated by Frazer (1983a). Predictions for reproductive value (column 5) and sensitivity (column 6) were derived from the model of Crouse et al. (19871. Five life stages are represented. Annual survivorship is lowest in eggs and hatchlings-67% per year and in large juveniles-68%. Large juveniles are the dominant size group (55- 75 cm) of the turtles stranded on the beaches of North Carolina (Crouse et

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71 Natural Mortality and Critical Life Stages al., 1987) and other beaches from Florida to North Carolina (Schroeder, 1987; Schroeder and Warner, 1988; Schroeder and Maley, 19891. Survivor- ship is estimated to be highest for nesting females 81% per year. Because they do not breed until they are 12-30 years old, and 22-33% die each year, few loggerheads reach reproductive age. The reproductive value of individual surviving turtles is greatest for breeders, which, once they reach maturity, can continue to breed for many years. Each individ- ual breeder's reproductive value is estimated to be about 584 times greater than that of an egg or hatchling. Few turtles, however, survive to adulthood and reproduce. As Crouse et al. (1987) noted, "By increasing the survival of large juveniles (who have already survived some of the worst years) a much larger number of turtles are likely to reach maturity, thereby greatly magnifying the input of the increased reproductive value of the adult stages." i, The analyses of Crouse et al. (1987) suggested that the greatest ncrease in growth rate of the Little Cumberland Island population could be achieved by increasing the survivorship of the large juveniles and subadults. Increasing fecundity or survivorship of eggs had less influence on population growth than increasing survivorship of older turtles. This conclusion was not especially sensitive to uncertainties in the parameter estimates. Because beach strandings of dead sea turtles are dominated by large juveniles (Crouse et al., 1987), reducing strandings would affect the very life stage whose increased survivorship could increase loggerhead population growth the most. No conservation effort can be successful without adequately protecting all stages in the life cycle, but the analyses of Crouse et al. (1987) strongly suggest that efforts to reduce mortality of larger juvenile and adult loggerheads will be more effective at promoting loggerhead population growth than efforts to increase the numbers of hatchlings leaving the beaches. The analyses also predict that efforts to protect eggs on nesting beaches and efforts at "headstarting" loggerheads would by themselves be insufficient to reverse the observed decline in the population of loggerheads nesting on Little Cumberland Island (Figure 3-14). Although the results of such population models clearly depend upon necessary assumptions regarding poorly known demographic characteris- tics, the general conclusions of the Crouse et al. (1987) model of the log- gerhead are robust. Of the poorly known demographic characteristics, age at sexual maturity is the one to which the model is most sensitive. But large changes in maturation rate and in other imprecisely known demographic characteristics did not alter the general conclusion that increasing the survivorship of juveniles and young adults would promote population growth far more than increasing survivorship of eggs and

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72 Decline of the Sea Turtles hatchlings. However, the imprecision of our knowledge of necessary demographic characteristics for loggerheads prevents us from specifying how many hatchlings would have to be spared to equal the effect of spar- ing the life of a single large juvenile, although we know that the number is large. Crouse et al. (1987) modeled only the loggerhead, but there are rea- sons to believe that aggregate reproductive value in Kemp's ridley and other sea turtles is also greater for larger juveniles and young adults than for earlier and later stages. The key demographic characteristics that lead to this pattern in how reproductive value varies with life stage are the rel- atively long time to sexual maturity and the extremely high mortality rate from birth to age of sexual maturity. Those characteristics ensure that reproductive value of individual hatchlings will be relatively low. To the degree that all sea turtles share those two traits with the loggerhead, the conclusion that reproductive value of hatchlings is relatively low will apply generally. The implication for conservation efforts, too, is general: Increasing survivorship of older juvenile and young adult sea turtles is the most effective means of increasing population sizes. Because mature sea turtles age without ceasing to reproduce, reproductive value will remain high until late in adult life, thus suggesting that continued protection of adult sea turtles will be an important conservation measure. However, if there are few or no hatchlings, there will inevitably be few or no adults ultimately. Therefore, relative reproductive values will be useful in man- agement decisions only if there is a certainty that large numbers of hatch- lings are being produced. SUMMARY Sea turtles lay great quantities of eggs throughout their life, particularly if mortality is low for adults. Predators consume many turtle eggs on most unprotected beaches. Demographic analyses suggest that the repro- ductive value of a turtle egg is low and that the sensitivity of population growth to the loss of an egg also is low; sea turtle populations under nor- mal conditions appear to be adapted to withstanding substantial egg loss. However, demographic analyses suggest that the reproductive value of a large juvenile, subadult, or adult sea turtle is higher than that of an egg. Because population growth is most sensitive to changes in survivorship of large juveniles and subadults, we conclude that reduction of human- induced mortality in these life stages will have a significantly greater effect on population growth than reduction of human-induced mortality of eggs and hatchlings.

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73 Natural Mortality and Critical Life Stages However, every age and life stage has value. Given that sea turtle species are threatened with extinction, every individual in every life stage becomes important to the survival of the species and protective efforts should be focused on all life stages, even those where individual repro- ductive values are relatively low.