- Email: [email protected]
Alligator physiology and life history: the importance of temperature
Experimental Gerontology 38 (2003) 801–805 www.elsevier.com/locate/expgero
Alligator physiology and life history: the importance of temperature Valentine A. Lance* Center for Reproduction of Endangered Species, Zoological society of San Diego, P.O. Box 120551, San Diego, CA 92112, USA
Abstract Alligators are the most northerly distributed of the extant Crocodilia. Reproducing populations are found as far north as 358 latitude in the freshwater marshes and rivers of coastal North Carolina, and as far south as 258 latitude in the Florida Keys. Thus different populations are exposed to very different annual thermal cycles. Alligators stop eating when ambient temperature drops below 16 8C. This anorexia lasts at least 6 months at 358 latitude. In southwest Louisiana alligators stop feeding in October and do not resume feeding until late March or early April. It is only during the warmer months when actively feeding that growth occurs. Even with this restricted growing season Louisiana alligators grow about 30 cm a year for the first 6 years. When alligators reach sexual maturity at about 1.85 m total length growth slows in both sexes, but is significantly slower in females than males. As a result of differences in thermal regime sexual maturity is estimated at around 18 years in North Carolina and about 10 years in Louisiana. Females lay one clutch of around 40 eggs in June, but the time of nesting is also tightly linked to temperature. In a cool spring nesting can occur as late as July 5th, and in a warm spring as early as June 5th. Immature male alligators undergo a seasonal hormonal cycle similar to fully mature breeding males, but testosterone levels differ by an order of magnitude. The number of mature females reproducing each year is rarely greater than 50%, but data on internest interval is lacking. Immature female alligators show no seasonal hormonal cycle. q 2003 Elsevier Science Inc. All rights reserved. Keywords: Temperature; Growth; Reproduction; Alligator; Crocodile
1. Introduction
2. Growth and sexual maturity
Crocodilians, ‘the last of the ruling reptiles’ (Neill, 1971), are descended from the dinosaur stock that gave rise to mammals and birds. They occupy an important position in the evolution of vertebrates in that they exhibit anatomical features found only in dinosaurs, and features common to birds and mammals (Brochu, 2001). They differ from other reptiles in a number of important ways, and are closer to birds both anatomically and biochemically than they are to lizards and snakes. Captive crocodiles and alligators have been reported to live well into their ninth decade (Pellegrin, 1937), and a large number of very old animals of uncertain age are currently being held in zoological collections (ISIS, N. Flesnes, personal communication). Information on longevity in wild crocodilians is lacking. As is typical of long-lived vertebrates sexual maturity is delayed and reproduction continues for decades in crocodiles. At what age crocodilians cease reproduction in not known, but there is anecdotal evidence that very large (and presumably very old) female alligators are senescent (T. Joanen, personal communication).
Accurate records of very large crocodiles in excess of 6 m and weighing more than 1000 kg have been published (Neill, 1971). The age of these large individuals is not known with any degree of accuracy. Techniques to age crocodiles using bone annual growth zones have been published (Peabody, 1961; Buffrenil, 1980; Hutton, 1986) and are fairly reliable in animals up to about 10 years of age, but in females, because of extensive bone remodeling during egg-shell formation (Wink and Elsey, 1986) and in very old individuals the method fails. Telomere length analysis may be of help in this area (see paper by Vleck). Growth in crocodilians is indeterminate. They are reported to continue growing well into old age, but solid data are rare. A surprisingly large number of studies on growth and estimated age at sexual maturity in the different species have been published (see refs in Wilkinson and Rhodes, 1997). Among these, the animal about which we have the most information is the American alligator. Growth in alligators (and crocodiles, but again data are scarce) is critically dependent on temperature. The American alligator, Alligator mississippiensis, is the most northerly distributed of the Crocodilia, ranging from 358 latitude in coastal North
* Tel.: þ1-619-557-3944; fax: þ 1-619-557-3959. E-mail address: [email protected] (V.A. Lance).
0531-5565/03/$ - see front matter q 2003 Elsevier Science Inc. All rights reserved. doi:10.1016/S0531-5565(03)00112-8
802
V.A. Lance / Experimental Gerontology 38 (2003) 801–805
Carolina to 258 latitude in the Florida Keys. The seasonal temperature variation at these extremes is marked. In Florida the monthly mean temperature is above 16 8C every month of the year, whereas in the northern extreme of the range, the mean temperature is well below 168 for at least 6 months of the year (Fig. 1). A temperature of 16 8C is the temperature below which alligator metabolism is inhibited and assimilation of food is not possible; therefore, the animals stop eating and stop growing. The months in the year in which the temperature exceeds 16 8C have been described as growing months (Joanen and McNease, 1989), thus in southern Florida there are 12 growing months, and in North Carolina six. In Louisiana (Fig. 1) on average, there are seven. The temperature given by Joanen and McNease (1989) as the temperature below which alligators stop feeding and growing was confirmed nicely in a recent publication. Seebacher et al. (2003) implanted temperature data loggers into the body cavity of seven alligators in Louisiana in winter (February) and seven alligators in summer (July). The loggers were recovered and the data showed that the mean body temperature of alligators in winter was 15.66 ^ 0.43 and 29.34 ^ 0.21 8C in summer. Given these numbers we would expect alligators in Florida to reach sexual maturity in far less time than in North Carolina. The observations, however, do not fit our predictions. In Louisiana alligators in the wild grow at about 30 cm/year for the first 6 years of life and attain sexual maturity at about 10 years (Joanen and McNease, 1989). In captivity alligators can grow as much as 150 cm/year (Coulson et al., 1973) and reach sexual maturity in 6 years (Joanen and McNease, 1989). In recent years, however, climate change may be affecting alligator behavior. Wildlife biologists in Louisiana have recently (2003), observed alligators feeding in January and February when the weather was exceptionally warm (R. Elsey, personal
communication), months during which no feeding activity has previously been reported. In Louisiana sexual maturity is reached at about 10 years and in North Carolina at about 18 years. In southern Florida, however, sexual maturity is estimated at 12 –14 years (Dalrymple, 1996). The reason for these differences is in quality of habitat. Louisiana alligators have an abundant food supply whereas in the Florida Everglades food is scarce and thus alligators in this region are in much poorer condition than those in other regions. Clutch size is smaller and they are reported to reach sexual maturity at a smaller size than alligators in Louisiana (Dalrymple, 1996). In conditions of extreme nutritional deprivation crocodiles probably fail to reach sexual maturity until very advanced ages, estimated as more than 20 years (Webb, 1985). There are populations of crocodiles living under such extreme conditions. In Mauritania there are small populations of Nile crocodiles surviving in the extremely limited ephemeral wetlands in the Sahara desert. These recently discovered relict populations (Shine et al., 2001) are miniature versions of the formidable monsters that kill cattle, wildebeests and humans in Tanzania and other parts of East Africa. Not only is the size at sexual maturity of these desert crocodiles much smaller, but their eggs and neonates are also smaller than East African Nile crocodiles. Some behavioral differences have also been documented (Shine, personal communication). Similarly, there are relict, isolated populations of the Australian crocodile, Crocodylus johnstoni in Arnhem Land, northern Australia, that also exhibit very slow growth and a very small size at sexual maturity (Webb, 1985). Even though barely surviving (they appear emaciated) and growing at a very slow rate, these animals do eventually attain sexual maturity at about one half the size, and probably twice the age of their counterparts in better habitats. The complex interrelationship between growth and
Fig. 1. Mean monthly temperature from weather station in coastal North Carolina, Key West, Florida, and Rockefeller Wildlife Refuge in coastal southwest Louisiana. The line across the graph is approximately 16 8C, the temperature below which alligators do not eat or grow.
V.A. Lance / Experimental Gerontology 38 (2003) 801–805
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The annual reproductive cycle of the American alligator is closely linked to the annual thermal cycle. When water and air temperatures increase in late March or early April, male alligators move from their winter dens and begin feeding. Occasional bellowing by both males and females is heard during this time. As the temperature increases bellowing frequency increases and courtship activity starts. During this time the testes are fully spermatogenic and reach their greatest mass by May. Mating is completed by mid May. In early June at the completion of spermiogenesis, testosterone levels drop from a peak of about 75 ng/ml to a mean of about 2ng/ml (Fig. 2.). This annual testicular cycle is similar to that seen in seasonally breeding birds, where testis mass can vary by a factor of 10 during the year. Paired testis mass in alligators also drops precipitously from a peak of over 100 g to less than 20 g by July. Hormone levels remain low until September –October when there is a slight increase, but spermatogenesis does not begin again until early in the following year (Lance, 1989). The timing of this cycle may vary from year to year depending on temperature. Male American alligators are generally considered to reach sexual maturity when they reach a total body length of about 1.8 m (Joanen and McNease, 1989). This estimate is based on examination of reproductive tracts or by checking for the presence of sperm in the penile groove during the breeding season. Although alligators in the size range of 1.8– 2.2 m are producing spermatozoa it is unlikely that they succeed in breeding. Larger males, especially those in excess of 2.6 m will chase off smaller males and mate with a number of different females (T. Joanen, personal communication). Some females,
however, do mate with more than one male. Genetic analysis of blood from all of the neonates taken from nests at which the female was caught and a blood sample taken has revealed that many clutches are fathered by more than one male (Davis et al., 2001). Nothing is known on the fecundity of very old and very large male alligators. A large female alligator kept in captivity with a 4 m male in southern Louisiana continued to build nests and lay large clutches (, 50) of infertile eggs for several years. The cause of the infertility, male or female, was never determined (Lance, unpublished). While there is considerable information on growth in alligators it is not known if circulating testosterone levels correlate with presumed size of sexual maturity in males. Blood samples were collected from wild caught male alligators at the Rockefeller Wildlife Refuge, a 76,000 acre refuge located in coastal southwestern Louisiana. Samples were collected over a 2 year period in every month of the year. Blood samples were taken from the cervical sinus from noosed animals immediately upon capture and analyzed for testosterone by radioimmunoassay (RIA). A total of over 1100 blood samples were collected from male alligators as small as 0.9 m and as large as 3.56 m total length during this study. The large breeding males . 2.28 m showed a distinct seasonal variation in circulating testosterone, with peak levels occurring during April. Elevated levels continued during April and May, but were followed by a dramatic decline in June, with low levels continuing throughout the summer and fall. Smaller males in all size classes also demonstrated a seasonal variation in hormone levels, but peak testosterone values in April and May only reached 2 ng/ml in the smallest animals sampled (61 –89 cm) and around 5 ng/ml in the 122– 150 cm size class (Fig. 3). In the larger alligators, a seasonal increase in testis mass was correlated with the rise in testosterone levels (Lance, 1989), but the testes of sub-adult alligators have not been studied. These results demonstrate that there is a clear positive
Fig. 2. Mean plasma testosterone values for adult male alligators in southwest Louisiana in each month of the year. The lines above the bars represent the standard error of the mean. Sample size is five or greater for all months except December in which only four samples were collected.
Fig. 3. Mean plasma testosterone in juvenile male alligators in southwest Louisiana in each month of the year. Sample size ranged from a low of 14 to a high of 39. Note the difference in values between the adults in Fig. 1, a peak of about 75 ng/ml and the juveniles, a peak of about 5 ng/ml.
sexual maturity in these long-lived reptiles remains poorly understood.
3. Male reproduction
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V.A. Lance / Experimental Gerontology 38 (2003) 801–805
association between total body length and plasma testosterone, and that immature alligators show a similar seasonal pattern of circulating testosterone as the adults. There is also a correlation of peak paired testis mass with body size, values as high as 300 g in alligators greater than 3.3 m were recorded (Lance, 1989).
4. Female reproduction Growth in male and female alligators is not significantly different for the first 6 years of life. On reaching sexual maturity however, the rates of growth differ markedly. Both sexes show a pronounced slowing of the growth rate when they attain a length of about 1.8 m, but males continue to grow at a significantly greater rate than females (Jacobsen and Kushlan, 1989). Male alligators also attain a much larger body size than females. Females over 3 m are extremely rare whereas males of 4 m are not uncommon. The reason for this difference may be due to the enormous drain on body reserves the female experiences during reproduction. In the wild less that 50% of female alligators over 1.8 m in length reproduce in a given year (Joanen and McNease, 1989; Lance, 1989). This means that most females lack the body reserves to produce a clutch of eggs each year. In captivity, however, female alligators are able to reproduce every year. The large amounts of food that captive alligators consume as compared to wild alligators is clear when body weights are compared. Captive-reared alligators are significantly heavier than wild alligators of similar length, have more body fat, grow at a faster rate than wild alligators, and continue to grow at a faster rate for one or 2 years even after being released into the wild (Elsey et al., 1992). Wild alligators, therefore, even in the best environments, can rarely get enough food to sustain reproduction every year. There is no published information on the intervals between nesting in the wild, but some anecdotal evidence suggest a range of 2 – 4 years (R. Elsey, personal communication). The ovary of the alligator is grossly similar in appearance to that of the chicken, but unlike the chicken is paired, the right ovary contains more follicles and is generally larger than the left. No actively diving germ cells, such as are seen in the ovaries of lizards and snakes, have been seen in crocodilian ovaries. It is likely, therefore, that alligators and crocodiles hatch with a complete complement of germ cells as do birds (see Holmes this issue). Old senescent, female alligators probably do exist, but have yet to be described in a scientific publication. The reproductive cycle of the female alligator is closely synchronized with that of the male, and like the male is closely tied to the annual thermal cycle. In unusually warm years in south Louisiana nesting may commence as early as June 5th, and in unusually cool years nesting may not begin until July 5th (Joanen and McNease, 1989). Crocodilians
lack a photosensitive pineal organ and thus appear to regulate their reproductive cycle independently of photoperiod. In Louisiana when the temperature goes above 16 8C in late March or early April females emerge from their winter dens, estradiol levels start to increase, vitellogenesis commences and active courtship begins. The vitellogenic period is relatively brief, lasting about 5– 6 weeks. Unlike males in which immature animals exhibit a seasonal cycle in plasma testosterone, there is no indication of any such pattern in immature females. Plasma estradiol in immature female alligators remains low (20 – 60 pg/ml) throughout the year. Shortly after copulation the females move to small isolated ponds in the open marsh and begin nest construction. It is during this period between ovulation and oviposition, estimated at 2 12 –3 weeks, that the albumin layer and the hard calcified shell is deposited. In south Louisiana a clutch of about 40 eggs, each averaging 70 g is deposited in one night. Egg mass among individuals can vary from 50 to 90 g. First time nesters usually lay around 20 eggs, and usually of lower fertility than eggs from larger females. The amount of calcium to produce 40 egg shells, each containing an estimated 5 g of calcium cannot be met by dietary intake (females generally do not eat during nesting) and thus has to be taken from bone (Wink and Elsey, 1986). Once the eggs are deposited the female remains in the vicinity guarding the nest throughout the 65– 75 day incubation period. When the eggs hatch and the young start vocalizing, the female opens the nests and carries the young to water. Alligators like all other crocodilians studied produce only one clutch of eggs a year. Some crocodiles in captivity have produced two clutches in a year, but this is rare. As can be seen from this brief overview there are a number of questions in alligator biology that need to be addressed. If, as appears to be the case, crocodilians hatch with a fixed complement of oocytes, are they similar to birds in that waves of atresia occur prior to, and after hatching among the germ cells and primary follicles? Do alligators continue to grow when they reach very advanced ages? Do male alligators become senescent? For how many years can a female alligator continue to reproduce? If female alligators become senescent how long do they live post-reproductively? Can the age of alligators be estimated by use of telomere length analysis? These long-lived ‘exemplars’ of that great radiation known as the age of reptiles have a number of unique features that have enabled them to survive for millions of years, and features that enable them to survive long periods without food and long periods of drought. As a model for a long-lived vertebrate they offer a number of physiological and endocrinological adaptations that challenge the investigator and should stimulate research for years to come.
V.A. Lance / Experimental Gerontology 38 (2003) 801–805
Acknowledgements I would like to thank Dr Ruth M. Elsey, Phillip Trosclair III and the staff of Rockefeller Refuge for their help in collecting blood samples and all other aspects of research on alligators. The testosterone data presented in this paper are part of a larger data set to be published elsewhere with R. M. Elsey and P. Trosclair.
References Brochu, C.A., 2001. Congruence between physiology, phylogentics and the fossil record on crocodilian historical biogeography. In: Grigg, G.C., Seebacher, F., Franklin, C.E. (Eds.), Crocodilian Biology and Evolution, Surrrey Beatty, Chipping Norton, NSW, pp. 9–28. Buffrenil, V.de., 1980. Donne´es pre´liminaries sur la structure des marques de croissance squelettiques ches les crocodilians actuels et fossils. Bull. Soc. Zool. Fr. 105 (2), 355–361. Coulson, T.D., Coulson, R.A., Hernandez, T., 1973. Some observations on the growth of captive alligators. Zoologica 58, 47– 52. Dalrymple, G.H., 1996. Growth of American alligators in the Shark Valley region of Everglades National Park. Copeia, 212 –216. Davis, L.M., Glenn, T.C., Elsey, R.M., Dessauer, C., Sawyer, R., 2001. Multiple paternity and mating patterns in the American alligator, Alligator mississippiensis. Mol. Ecol. 10, 1011–1024. Elsey, R.M., Joanen, T., McNease, L., Kinler, N., 1992. Growth rates and body condition factors of Alligator mississipiensis in coastal Louisiana
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wetlands: a comparison of wild and farm released juveniles. Comp. Biochem. Physiol. 103A, 667–672. Hutton, J.M., 1986. Age determination of living Nile crocodiles from the cortical stratification of bone. Copeia (2), 332–341. Jacobsen, T., Kushlan, J.A., 1989. Growth dynamics in the American alligator (Alligator mississippiensis). J. Zool. Lond. 219, 309–328. Joanen, T., McNease, L., 1989. Ecology and physiology of nesting and early development of the American alligator. Am. Zool. 29, 987– 998. Lance, V.A., 1989. Reproductive cycle of the American alligator. Am. Zool. 29, 999–1018. Neill, W.T., 1971. The Last of the Ruling Reptiles, Alligators, Crocodiles and their Kin, Columbia University Press, New York. Peabody, F.E., 1961. Annual growth zones in living and fossil vertebrates. J. Morphol. 108, 11–62. Pellegrin, J., 1937. Mort d’un alligator presume avoir vecu 85 ans a la menegerie des reptiles. Bull. Mus. Hist. Nat. Paris, 2nd Ser. 9, 176– 177. Seebacher, F., Guderley, H., Elsey, R.M., Trosclair, P.L. III, 2003. Seasonal acclimation of muscle metabolic enzymes in a reptile (Alligator mississippiensis). J. Exp. Biol. 206 (7), 1193–1200. Shine, T.S., Bo¨hme, W., Nickel, H., Thies, D.F., Wilms, T., 2001. Rediscovery of relict populations of the Nile crocodile Crocodylus niloticus in south-eastern Mauritania, with observations on their natural history. Oxyx 35, 260–262. Webb, J.G.W., 1985. Survey of a pristine population of freshwater crocodiles in the Liverpool River, Arnhem Land, Australia. National Geographic Society, Research Reports: 1979 Projects, pp. 841–852. Wilkinson, P.M., Rhodes, W.E., 1997. Growth rate of American alligators in coastal South Carolina. J. Wildl. Manage. 61, 397–402. Wink, C., Elsey, R.M., 1986. Changes in femoral bone morphology during egg-lying in Alligator mississippiensis. J. Morphol. 189, 183– 188.
Alligator physiology and life history: the importance of temperature Valentine A. Lance* Center for Reproduction of Endangered Species, Zoological society of San Diego, P.O. Box 120551, San Diego, CA 92112, USA
Abstract Alligators are the most northerly distributed of the extant Crocodilia. Reproducing populations are found as far north as 358 latitude in the freshwater marshes and rivers of coastal North Carolina, and as far south as 258 latitude in the Florida Keys. Thus different populations are exposed to very different annual thermal cycles. Alligators stop eating when ambient temperature drops below 16 8C. This anorexia lasts at least 6 months at 358 latitude. In southwest Louisiana alligators stop feeding in October and do not resume feeding until late March or early April. It is only during the warmer months when actively feeding that growth occurs. Even with this restricted growing season Louisiana alligators grow about 30 cm a year for the first 6 years. When alligators reach sexual maturity at about 1.85 m total length growth slows in both sexes, but is significantly slower in females than males. As a result of differences in thermal regime sexual maturity is estimated at around 18 years in North Carolina and about 10 years in Louisiana. Females lay one clutch of around 40 eggs in June, but the time of nesting is also tightly linked to temperature. In a cool spring nesting can occur as late as July 5th, and in a warm spring as early as June 5th. Immature male alligators undergo a seasonal hormonal cycle similar to fully mature breeding males, but testosterone levels differ by an order of magnitude. The number of mature females reproducing each year is rarely greater than 50%, but data on internest interval is lacking. Immature female alligators show no seasonal hormonal cycle. q 2003 Elsevier Science Inc. All rights reserved. Keywords: Temperature; Growth; Reproduction; Alligator; Crocodile
1. Introduction
2. Growth and sexual maturity
Crocodilians, ‘the last of the ruling reptiles’ (Neill, 1971), are descended from the dinosaur stock that gave rise to mammals and birds. They occupy an important position in the evolution of vertebrates in that they exhibit anatomical features found only in dinosaurs, and features common to birds and mammals (Brochu, 2001). They differ from other reptiles in a number of important ways, and are closer to birds both anatomically and biochemically than they are to lizards and snakes. Captive crocodiles and alligators have been reported to live well into their ninth decade (Pellegrin, 1937), and a large number of very old animals of uncertain age are currently being held in zoological collections (ISIS, N. Flesnes, personal communication). Information on longevity in wild crocodilians is lacking. As is typical of long-lived vertebrates sexual maturity is delayed and reproduction continues for decades in crocodiles. At what age crocodilians cease reproduction in not known, but there is anecdotal evidence that very large (and presumably very old) female alligators are senescent (T. Joanen, personal communication).
Accurate records of very large crocodiles in excess of 6 m and weighing more than 1000 kg have been published (Neill, 1971). The age of these large individuals is not known with any degree of accuracy. Techniques to age crocodiles using bone annual growth zones have been published (Peabody, 1961; Buffrenil, 1980; Hutton, 1986) and are fairly reliable in animals up to about 10 years of age, but in females, because of extensive bone remodeling during egg-shell formation (Wink and Elsey, 1986) and in very old individuals the method fails. Telomere length analysis may be of help in this area (see paper by Vleck). Growth in crocodilians is indeterminate. They are reported to continue growing well into old age, but solid data are rare. A surprisingly large number of studies on growth and estimated age at sexual maturity in the different species have been published (see refs in Wilkinson and Rhodes, 1997). Among these, the animal about which we have the most information is the American alligator. Growth in alligators (and crocodiles, but again data are scarce) is critically dependent on temperature. The American alligator, Alligator mississippiensis, is the most northerly distributed of the Crocodilia, ranging from 358 latitude in coastal North
* Tel.: þ1-619-557-3944; fax: þ 1-619-557-3959. E-mail address: [email protected] (V.A. Lance).
0531-5565/03/$ - see front matter q 2003 Elsevier Science Inc. All rights reserved. doi:10.1016/S0531-5565(03)00112-8
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V.A. Lance / Experimental Gerontology 38 (2003) 801–805
Carolina to 258 latitude in the Florida Keys. The seasonal temperature variation at these extremes is marked. In Florida the monthly mean temperature is above 16 8C every month of the year, whereas in the northern extreme of the range, the mean temperature is well below 168 for at least 6 months of the year (Fig. 1). A temperature of 16 8C is the temperature below which alligator metabolism is inhibited and assimilation of food is not possible; therefore, the animals stop eating and stop growing. The months in the year in which the temperature exceeds 16 8C have been described as growing months (Joanen and McNease, 1989), thus in southern Florida there are 12 growing months, and in North Carolina six. In Louisiana (Fig. 1) on average, there are seven. The temperature given by Joanen and McNease (1989) as the temperature below which alligators stop feeding and growing was confirmed nicely in a recent publication. Seebacher et al. (2003) implanted temperature data loggers into the body cavity of seven alligators in Louisiana in winter (February) and seven alligators in summer (July). The loggers were recovered and the data showed that the mean body temperature of alligators in winter was 15.66 ^ 0.43 and 29.34 ^ 0.21 8C in summer. Given these numbers we would expect alligators in Florida to reach sexual maturity in far less time than in North Carolina. The observations, however, do not fit our predictions. In Louisiana alligators in the wild grow at about 30 cm/year for the first 6 years of life and attain sexual maturity at about 10 years (Joanen and McNease, 1989). In captivity alligators can grow as much as 150 cm/year (Coulson et al., 1973) and reach sexual maturity in 6 years (Joanen and McNease, 1989). In recent years, however, climate change may be affecting alligator behavior. Wildlife biologists in Louisiana have recently (2003), observed alligators feeding in January and February when the weather was exceptionally warm (R. Elsey, personal
communication), months during which no feeding activity has previously been reported. In Louisiana sexual maturity is reached at about 10 years and in North Carolina at about 18 years. In southern Florida, however, sexual maturity is estimated at 12 –14 years (Dalrymple, 1996). The reason for these differences is in quality of habitat. Louisiana alligators have an abundant food supply whereas in the Florida Everglades food is scarce and thus alligators in this region are in much poorer condition than those in other regions. Clutch size is smaller and they are reported to reach sexual maturity at a smaller size than alligators in Louisiana (Dalrymple, 1996). In conditions of extreme nutritional deprivation crocodiles probably fail to reach sexual maturity until very advanced ages, estimated as more than 20 years (Webb, 1985). There are populations of crocodiles living under such extreme conditions. In Mauritania there are small populations of Nile crocodiles surviving in the extremely limited ephemeral wetlands in the Sahara desert. These recently discovered relict populations (Shine et al., 2001) are miniature versions of the formidable monsters that kill cattle, wildebeests and humans in Tanzania and other parts of East Africa. Not only is the size at sexual maturity of these desert crocodiles much smaller, but their eggs and neonates are also smaller than East African Nile crocodiles. Some behavioral differences have also been documented (Shine, personal communication). Similarly, there are relict, isolated populations of the Australian crocodile, Crocodylus johnstoni in Arnhem Land, northern Australia, that also exhibit very slow growth and a very small size at sexual maturity (Webb, 1985). Even though barely surviving (they appear emaciated) and growing at a very slow rate, these animals do eventually attain sexual maturity at about one half the size, and probably twice the age of their counterparts in better habitats. The complex interrelationship between growth and
Fig. 1. Mean monthly temperature from weather station in coastal North Carolina, Key West, Florida, and Rockefeller Wildlife Refuge in coastal southwest Louisiana. The line across the graph is approximately 16 8C, the temperature below which alligators do not eat or grow.
V.A. Lance / Experimental Gerontology 38 (2003) 801–805
803
The annual reproductive cycle of the American alligator is closely linked to the annual thermal cycle. When water and air temperatures increase in late March or early April, male alligators move from their winter dens and begin feeding. Occasional bellowing by both males and females is heard during this time. As the temperature increases bellowing frequency increases and courtship activity starts. During this time the testes are fully spermatogenic and reach their greatest mass by May. Mating is completed by mid May. In early June at the completion of spermiogenesis, testosterone levels drop from a peak of about 75 ng/ml to a mean of about 2ng/ml (Fig. 2.). This annual testicular cycle is similar to that seen in seasonally breeding birds, where testis mass can vary by a factor of 10 during the year. Paired testis mass in alligators also drops precipitously from a peak of over 100 g to less than 20 g by July. Hormone levels remain low until September –October when there is a slight increase, but spermatogenesis does not begin again until early in the following year (Lance, 1989). The timing of this cycle may vary from year to year depending on temperature. Male American alligators are generally considered to reach sexual maturity when they reach a total body length of about 1.8 m (Joanen and McNease, 1989). This estimate is based on examination of reproductive tracts or by checking for the presence of sperm in the penile groove during the breeding season. Although alligators in the size range of 1.8– 2.2 m are producing spermatozoa it is unlikely that they succeed in breeding. Larger males, especially those in excess of 2.6 m will chase off smaller males and mate with a number of different females (T. Joanen, personal communication). Some females,
however, do mate with more than one male. Genetic analysis of blood from all of the neonates taken from nests at which the female was caught and a blood sample taken has revealed that many clutches are fathered by more than one male (Davis et al., 2001). Nothing is known on the fecundity of very old and very large male alligators. A large female alligator kept in captivity with a 4 m male in southern Louisiana continued to build nests and lay large clutches (, 50) of infertile eggs for several years. The cause of the infertility, male or female, was never determined (Lance, unpublished). While there is considerable information on growth in alligators it is not known if circulating testosterone levels correlate with presumed size of sexual maturity in males. Blood samples were collected from wild caught male alligators at the Rockefeller Wildlife Refuge, a 76,000 acre refuge located in coastal southwestern Louisiana. Samples were collected over a 2 year period in every month of the year. Blood samples were taken from the cervical sinus from noosed animals immediately upon capture and analyzed for testosterone by radioimmunoassay (RIA). A total of over 1100 blood samples were collected from male alligators as small as 0.9 m and as large as 3.56 m total length during this study. The large breeding males . 2.28 m showed a distinct seasonal variation in circulating testosterone, with peak levels occurring during April. Elevated levels continued during April and May, but were followed by a dramatic decline in June, with low levels continuing throughout the summer and fall. Smaller males in all size classes also demonstrated a seasonal variation in hormone levels, but peak testosterone values in April and May only reached 2 ng/ml in the smallest animals sampled (61 –89 cm) and around 5 ng/ml in the 122– 150 cm size class (Fig. 3). In the larger alligators, a seasonal increase in testis mass was correlated with the rise in testosterone levels (Lance, 1989), but the testes of sub-adult alligators have not been studied. These results demonstrate that there is a clear positive
Fig. 2. Mean plasma testosterone values for adult male alligators in southwest Louisiana in each month of the year. The lines above the bars represent the standard error of the mean. Sample size is five or greater for all months except December in which only four samples were collected.
Fig. 3. Mean plasma testosterone in juvenile male alligators in southwest Louisiana in each month of the year. Sample size ranged from a low of 14 to a high of 39. Note the difference in values between the adults in Fig. 1, a peak of about 75 ng/ml and the juveniles, a peak of about 5 ng/ml.
sexual maturity in these long-lived reptiles remains poorly understood.
3. Male reproduction
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association between total body length and plasma testosterone, and that immature alligators show a similar seasonal pattern of circulating testosterone as the adults. There is also a correlation of peak paired testis mass with body size, values as high as 300 g in alligators greater than 3.3 m were recorded (Lance, 1989).
4. Female reproduction Growth in male and female alligators is not significantly different for the first 6 years of life. On reaching sexual maturity however, the rates of growth differ markedly. Both sexes show a pronounced slowing of the growth rate when they attain a length of about 1.8 m, but males continue to grow at a significantly greater rate than females (Jacobsen and Kushlan, 1989). Male alligators also attain a much larger body size than females. Females over 3 m are extremely rare whereas males of 4 m are not uncommon. The reason for this difference may be due to the enormous drain on body reserves the female experiences during reproduction. In the wild less that 50% of female alligators over 1.8 m in length reproduce in a given year (Joanen and McNease, 1989; Lance, 1989). This means that most females lack the body reserves to produce a clutch of eggs each year. In captivity, however, female alligators are able to reproduce every year. The large amounts of food that captive alligators consume as compared to wild alligators is clear when body weights are compared. Captive-reared alligators are significantly heavier than wild alligators of similar length, have more body fat, grow at a faster rate than wild alligators, and continue to grow at a faster rate for one or 2 years even after being released into the wild (Elsey et al., 1992). Wild alligators, therefore, even in the best environments, can rarely get enough food to sustain reproduction every year. There is no published information on the intervals between nesting in the wild, but some anecdotal evidence suggest a range of 2 – 4 years (R. Elsey, personal communication). The ovary of the alligator is grossly similar in appearance to that of the chicken, but unlike the chicken is paired, the right ovary contains more follicles and is generally larger than the left. No actively diving germ cells, such as are seen in the ovaries of lizards and snakes, have been seen in crocodilian ovaries. It is likely, therefore, that alligators and crocodiles hatch with a complete complement of germ cells as do birds (see Holmes this issue). Old senescent, female alligators probably do exist, but have yet to be described in a scientific publication. The reproductive cycle of the female alligator is closely synchronized with that of the male, and like the male is closely tied to the annual thermal cycle. In unusually warm years in south Louisiana nesting may commence as early as June 5th, and in unusually cool years nesting may not begin until July 5th (Joanen and McNease, 1989). Crocodilians
lack a photosensitive pineal organ and thus appear to regulate their reproductive cycle independently of photoperiod. In Louisiana when the temperature goes above 16 8C in late March or early April females emerge from their winter dens, estradiol levels start to increase, vitellogenesis commences and active courtship begins. The vitellogenic period is relatively brief, lasting about 5– 6 weeks. Unlike males in which immature animals exhibit a seasonal cycle in plasma testosterone, there is no indication of any such pattern in immature females. Plasma estradiol in immature female alligators remains low (20 – 60 pg/ml) throughout the year. Shortly after copulation the females move to small isolated ponds in the open marsh and begin nest construction. It is during this period between ovulation and oviposition, estimated at 2 12 –3 weeks, that the albumin layer and the hard calcified shell is deposited. In south Louisiana a clutch of about 40 eggs, each averaging 70 g is deposited in one night. Egg mass among individuals can vary from 50 to 90 g. First time nesters usually lay around 20 eggs, and usually of lower fertility than eggs from larger females. The amount of calcium to produce 40 egg shells, each containing an estimated 5 g of calcium cannot be met by dietary intake (females generally do not eat during nesting) and thus has to be taken from bone (Wink and Elsey, 1986). Once the eggs are deposited the female remains in the vicinity guarding the nest throughout the 65– 75 day incubation period. When the eggs hatch and the young start vocalizing, the female opens the nests and carries the young to water. Alligators like all other crocodilians studied produce only one clutch of eggs a year. Some crocodiles in captivity have produced two clutches in a year, but this is rare. As can be seen from this brief overview there are a number of questions in alligator biology that need to be addressed. If, as appears to be the case, crocodilians hatch with a fixed complement of oocytes, are they similar to birds in that waves of atresia occur prior to, and after hatching among the germ cells and primary follicles? Do alligators continue to grow when they reach very advanced ages? Do male alligators become senescent? For how many years can a female alligator continue to reproduce? If female alligators become senescent how long do they live post-reproductively? Can the age of alligators be estimated by use of telomere length analysis? These long-lived ‘exemplars’ of that great radiation known as the age of reptiles have a number of unique features that have enabled them to survive for millions of years, and features that enable them to survive long periods without food and long periods of drought. As a model for a long-lived vertebrate they offer a number of physiological and endocrinological adaptations that challenge the investigator and should stimulate research for years to come.
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Acknowledgements I would like to thank Dr Ruth M. Elsey, Phillip Trosclair III and the staff of Rockefeller Refuge for their help in collecting blood samples and all other aspects of research on alligators. The testosterone data presented in this paper are part of a larger data set to be published elsewhere with R. M. Elsey and P. Trosclair.
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