Its Only Been Two Months Since My Chameleon Laid Eggs

• Periodical List
• Proc Natl Acad Sci U S A
• v.105(26); 2008 Jul 1
• PMC2449350

Proc Natl Acad Sci U South A. 2008 Jul 1; 105(26): 8980–8984.

Development

A unique life history among tetrapods: An annual chameleon living mostly as an egg

Kristopher B. Karsten

*Department of Zoology, Oklahoma State University, Stillwater, OK 74078;

Laza N. Andriamandimbiarisoa

^‡Département de Biologie Animale, Université d'Antananarivo, BP 906, Antananarivo 101, Madagascar; and

Stanley F. Fox

*Department of Zoology, Oklahoma Country University, Stillwater, OK 74078;

Christopher J. Raxworthy

^§American Museum of Natural History, Central Park Due west at 79th Street, New York, NY 10024

Abstract

The ≈28,300 species of tetrapods (iv-limbed vertebrates) almost exclusively take perennial life spans. Here, we study the discovery of a remarkable annual tetrapod from the arid southwest of Madagascar: the chameleon Furcifer labordi, with a posthatching life span of simply 4–5 months. At the start of the active flavor (November), an age cohort of hatchlings emerges; larger juveniles or adults are not present. These hatchlings abound quickly, reach sexual maturity in less than two months, and reproduce in Jan–February. After reproduction, senescence appears, and the active flavour concludes with population-wide adult death. Consequently, during the dry flavour, the entire population is represented by developing eggs that incubate for 8–nine months earlier synchronously hatching at the onset of the post-obit rainy flavour. Remarkably, this chameleon spends more than of its brusque annual life cycle within the egg than outside of information technology. Our review of tetrapod longevity (>1,700 species) finds no others with such a short life span. These findings suggest that the notorious rapid decease of chameleons in captivity may, for some species, actually stand for the natural adult life span. Consequently, a new appraisal may be warranted concerning the viability of chameleon breeding programs, which could have special significance for species of conservation business organisation. Additionally, because F. labordi is closely related to other perennial species, this chameleon group may prove also to be peculiarly well suited for comparative studies that focus on life history evolution and the ecological, genetic, and/or hormonal determinants of crumbling, longevity, and senescence.

Keywords: Madagascar, lizard, longevity, semelparity, senescence

Although there are almost limitless theoretical combinations of life history traits, they are remarkably constrained to a continuum of high reproductive rates, rapid growth, and short life spans on one terminate and the opposite set of traits on the other (1). Because of this, life history theory makes predictions of how traits should evolve for a given prepare of parameters. For example, organisms experiencing increased developed mortality rates should evolve shorter life spans, and those experiencing increased juvenile mortality rates should evolve longer life spans (2–8). Any alter in fecundity, age at maturity, or historic period-specific mortality that reduces the value of adults and increases the value of juveniles volition cause an evolutionary shift from the stop of the continuum with slower growth, iteroparity, and longer life span toward the other end with faster growth, semelparity, and shorter life bridge (vii, 9).

Almost all of the well-nigh thirty,000 species of tetrapods (iv-limbed vertebrates) have perennial life spans. Inside tetrapods, some species with slow growth and delayed maturity exhibit exceptionally long life spans of up to 100+ years (10). At the other extreme, rapid sexual maturity and almanac life spans are surprisingly rare. Amongst endotherms (mammals and birds), near-annual longevity is known merely in nine species of marsupials in the families Didelphidae and Dasyuridae, where it is restricted to males, and may also be facultative (xi–17). There are no examples of annual amphibians (18). Among reptiles, lizards exhibit the shortest life spans (19), although the shortest-lived are capable of longevity >1 year with multiple clutches per lifetime (20, 21). All the same, nosotros know very fiddling nigh taxa such equally chameleons, which accept proved hard to study in the field because of poor visibility in forest canopies, compounded by the secretive and cryptic beliefs of the animals themselves (22).

Hither, based on five seasons of field data, we report the surprising discovery of an annual tetrapod from the arid southwest of Madagascar: the chameleon Furcifer labordi, which has a posthatching life span of just iv–five months that concludes with synchronous adult population-broad death (Fig. i). Consequently, F. labordi spends the majority of its lifetime as a developing embryo, and, except for the brief period when adults and their recently laid eggs are both present, the entire population is a single age cohort. This life history is more reminiscent of ephemeral insects than that of a typical tetrapod. We also compare this life history with a sympatric but perennial chameleon, Furcifer verrucosus.

Life histories of annual and perennial chameleon species. Shown are the study region climate and life history of two chameleons: the almanac F. labordi (Lower) and a hatchling accomplice of the perennial F. verrucosus (Upper) over xv months in southwest Madagascar. Toliara rainfall (bluish line) and temperature (ruddy line) are shown (57). Life history phases are: incubating eggs with a suspected diapause (open up), juvenile growth (blood-red), courting (yellow), menses of courting and egg laying overlap (green), egg-laying and senescence (blue), juvenile aestivation (gray). The life span of F. labordi is a single year, with most of this fourth dimension spent every bit a developing egg.

Results

After the cool, dry, inactive season, nosotros observed no F. labordi until the outset emergence of hatchlings on November 11, with the onset of the wet flavor. Over the following 38 days, all F. labordi were a single age accomplice of hatchlings and hatchlings-turned-juveniles, with no adults present until December xx (Table 1). An annual species with synchronous hatching of a single cohort should prove a strong, positive correlation between size and appointment during the growth phase for the entire population; and we found this pattern for F. labordi. Between Nov 11 and Jan 3, SVL (snout–vent length) was positively correlated with engagement in both males (north = 163, r = 0.745, P < 0.001) and females (northward = 112, r = 0.759, P < 0.001; Fig. 2 A). F. verrucosus differed from F. labordi in that SVL was non significantly correlated with date for either males or females (n = 119, r = −0.024, P = 0.793; n = 96, r = 0.170, P = 0.097, respectively; Fig. two B). Juvenile F. labordi growth was exceptionally high: marked-recaptured males increased mean body mass by four.1% daily (n = 24, hateful ± 1 SE = 0.32 ± 0.07 g per day) and mean SVL by 1.86% daily (north = 24, 1.36 ± 0.eleven mm per day). Female F. labordi also exhibited impressive growth rates during the same portion of the active season: marked-recaptured females increased mean body mass by 2.0% daily (n = 3, 0.09 ± 0.10 g per solar day) and mean SVL by 1.86% daily (n = iii, 1.26 ± 0.65 mm per day). The maximum growth rate observed in this species was as high as 2.6 mm per solar day. All posthatching growth was restricted to a period of <threescore days.

Tabular array ane.

Population demography of two chameleon species at Ranobe, Madagascar

Period of agile flavor	northward	Percentage of population
		Hatchling	Juvenile	Adult
F. labordi
November 11–Nov 29	23	100	0	0
Nov 30–Dec 6	28	32	68	0
Dec 7–Dec 16	146	ane	99	0
December 17–December 29	83	0	24	76
Dec 29–Mar five	138	0	0	100
F. verrucosus
November 5–Nov 30	48	ii	79	19
December one–December 20	174	29	42	29
Feb 13–Mar 5	104	0	88	xiii

Cohorts of annual and perennial chameleon species. (A) Composite data (1995, 2003–2006) for SVL and date in the almanac F. labordi cohort: unsexed hatchlings <26 mm SVL (+); males (filled symbols); females (open symbols); sexed hatchlings, juveniles, and prereproductive adults (circles); and sexually reproductive adults (triangles). (B) Composite information (2005–2006) for SVL and date for multiple cohorts of the perennial F. verrucosus: hatchlings <30 mm SVL (+); prereproductive (circles) and sexually reproductive (triangles) individuals; males (filled symbols); females (open symbols). Data beyond 21 December are truncated to exclude biased sampling efforts. Still, juveniles were nowadays throughout the entire agile season (meet Table 1).

We start observed reproductive behavior on January 10, and after this date all individuals exhibited developed morphology (Table one), and growth ceased (Fig. ii A) and was even negative within individuals. Although growth is largely considered irreversible in vertebrates, negative reptile growth has been reported for marine iguanas during periods of poor nutrient availability and stress (23). When reproduction in F. labordi began, we observed negative growth in a small set of marked-recaptured males (n = 6, −0.26 ± 0.xxx mm per day). Within the population, growth ceased for both developed males (n = 61, r = −0.085, P = 0.517) and females (n = 55, r = −0.654, P < 0.001; Fig. two A).

We observed no aestivation behavior by adults of F. labordi: none emerging at the commencement of the active season and none inbound aestivation at the cease of the active season. In dissimilarity, we take observed both emerging and aestivation behavior multiple times in F. verrucosus and other arid-adapted chameleons. Additional museum specimens with known collecting dates and field records (run into Materials and Methods) support these conclusions. Developed F. labordi have never been constitute in the field betwixt May and Nov, whereas F. verrucosus have been collected in all months except July and August. In the perennial F. verrucosus, we observed adults, juveniles, and hatchlings oftentimes throughout the commencement of the agile flavor (Fig. 2 B and Tabular array i). Based on size classes, F. verrucosus comprises at least three age cohorts once hatchlings emerge: (i) hatchlings, (two) subadults and adults from the previous twelvemonth's hatch, and (iii) older adults (Fig. 2 B).

The frequency of gravid F. labordi females peaked from late January to tardily February. We observed a radio-tracked female excavating a nest and depositing a clutch of 11 eggs on February 3: mean egg length was 11.seven mm (15.2% of her SVL), and total clutch mass was 4.iv m (36.7% of her preoviposition mass) (24). We did not observe any gravid females after March two. Nosotros estimate that egg laying in F. labordi occurs generally in February, and incubation spans viii–9 months with hatching in November, similar to the 10-month incubation period observed in captivity (25, 26). No species in the genus Furcifer are known to accept incubation periods shorter than eight months. These long incubation periods that are common among chameleons are the result of embryos being in diapause at the time of oviposition. Diapause terminates after several months, simply development remains arrested by common cold torpor until nest temperature increases as the wet season approaches (27–31). Consequently, the eggs resume development, and hatchlings synchronously emerge at the onset of the wet flavour in November (Fig. 1). Some other reptile species may hatch before emergence and overwinter inside the nest as hatchlings (32). However, in chameleons, this scenario appears unlikely because the group is mostly characterized by long incubation periods; delayed nest emergence, afterwards hatching, has never been observed for whatsoever captive chameleon (26, 28).

In 2004, the terminal active adults (both species) were institute on February 11, merely in 1995 agile adults were nerveless as late as March 28 (see Materials and Methods). Thus, the termination of the active season likely varies among years, falling approximately between February and Apr. After egg laying, the agile season for F. labordi concludes with senescence and population-wide adult death. Developing eggs (incubating for 8–9 months) represent the unabridged population during the prolonged dry season, which is considerably longer than the posthatching life span of 4–5 months (Fig. 1). Withal, adult and subadult F. verrucosus aestivate over the dry out season.

Word

No other tetrapod species, including short-lived marsupials (11, 12, 17, 33) and lizards, are known to have a life history similar to that of F. labordi. Previous reviews of other lizards (20, 21, 34) study eleven species every bit putatively almanac. However, in all species in which survivorship was quantified past the original authors (cf. extrapolated from anecdotal literature), maximal postembryonic longevity was actually greater than 1 year, and none exhibited obligate annual population turnover. Our review of longevity in tetrapods, which included >1,700 species and 194 publications (available on request from the respective author), did not find obligate almanac population turnover for whatsoever other tetrapod species, nor did we find whatever other tetrapod with a postembryonic life span of simply four–five months. F. labordi is also unique among tetrapods in that it spends the bulk of its life cycle inside the egg, a life history more reminiscent of ephemeral insects or aquatic vertebrates than of other terrestrial tetrapods.

At the stop of the active season, radio-tracked and marked-recaptured F. labordi exhibited worsening body condition, including physical characteristics typical of senescence such equally reduced mass, slower locomotion, and reduced strength when gripping branches. For example, males lost an average of 0.30 ± 0.xvi g per mean solar day at the end of the breeding flavor (n = 6), and we too observed multiple instances of radio-tracked chameleons falling from trees, for unknown reasons, during normal locomotor activeness. Additionally, from January 20—February x, two of seven radio-tracked individuals were establish dead of unknown causes merely with no signs of mutilation. We also establish several non-radio-tracked and unmarked dead F. labordi in a similar unmutilated status toward the end of the active season. Conversely, for F. verrucosus, individuals continued to announced robust and salubrious at the end of the breeding flavour, and none were establish expressionless unmutilated.

Presently, it is unclear why F. labordi exhibits such a baroque and extreme life history compared with other tetrapods. One hypothesis is that the harsh environs with extreme seasonality contributes to life history extremes. For example, brusque-lived, annual killifish deposit eggs in the mud, and they survive the harsh, dry flavor by entering a diapause, an adaptation to the highly fluctuating environment. Annualism is likely the ancestral graphic symbol state; however, it has been evolutionarily lost by lineages found in more stable environments (35). The climate of Madagascar is highly variable (36): ecology unpredictability is much greater than other tropical areas, specially in the southwest, which exhibits unusually high interannual variability in rainfall. In response to stochastic climate fluctuations, many mammals of Madagascar differ from close relatives in more than stable environments in that the Malagasy species showroom more extreme versions of either "short-lived" or "long-lived" life histories (36). Dewar and Richard (36) suggested that both responses are possible "solutions" to the same evolutionary "problem." Concordant with life history theory, the best solution depends on how environmental instability affects historic period-specific mortality (vii, 8). Among several Malagasy mammals (carnivores, primates, tenrecs, and rodents), reduced juvenile survivorship due to environmental variability resulted in the evolution of longer life spans (37), whereas stochastic climatic variables that reduced adult survivorship resulted in the evolution of shorter life spans (36, 38). If environmental unpredictability differentially affected historic period-specific survivorship in chameleons, this may assist explain why F. labordi is almanac whereas other sympatric chameleons are perennial.

An culling, and not mutually exclusive, caption may sally at the interface between life history theory and hormone–beliefs relationships. Loftier adult bloodshed rates tin drive the development of rapid growth and earlier age of reproduction (two–7), with the cost being decreased longevity, frequently equally a result of a trade-off between resources allocated to somatic cell maintenance compared with reproduction (6, 7, x, 39–41). Hormones tin can command these trade-offs (42). For case, increased androgens in both natural populations and by experimental manipulation can be correlated with mating success (43, 44) merely are too known to contribute to traits typically associated with increased adult bloodshed rates (eastward.k., reduced survival, increased parasite loads, increased energetic expenditure) (45–50). It seems possible that a change in the social structure in ancestral F. labordi, to a social system characterized by increased androgen levels or sensitivity, could contribute to increased intrinsic and/or extrinsic adult mortality. Indeed, F. labordi is characterized by physically intense combat and agonistic courtship (unpublished data). A similar mode of evolutionary selection appears to have played a office in the evolution of semelparity in at least one other tetrapod, the marsupial Phascogale calura (33). Accounting for hormonal regulation of physiology and behavior is critical to a comprehensive understanding of life history evolution (1, 42). Although our hypothesis is plausible, the function of hormones, and even behavior to a lesser extent, is unexplored in chameleons. Our hypothesis can exist tested by quantifying seasonal hormone profiles, social systems, and sexual selection inside a phylogenetic comparative framework.

Mortality is loftier during the cursory mating phase of the active season: four of 7 radio-tracked individuals died from predation or unknown causes from January 20 to February 10. The physically intense social system of this species, the harsh and unpredictable environment it inhabits, with a brief active season and where adult mortality is already high, may exacerbate the compression of life into such a brief menses. In accordance with life history theory, the outcome would be evolutionary selection for reduced life span, smaller body size, and earlier historic period of reproduction (2–8). This may be advantageous for two reasons. Beginning, because F. labordi is sympatric with other larger, just closely related (51, 52), perennial chameleons, a shift in body size and age of reproduction may alleviate some dimensions of niche overlap. Second, the metabolic theory of ecology states that smaller organisms take more resources to allocate to reproduction than their larger-bodied counterparts, relative to body mass, producing new individuals and genes at faster rates (53).

F. labordi has a life history like no other tetrapod, but information technology still conforms to predictions of life history theory: it experiences high adult bloodshed, is the smallest chameleon within a closely related group, exhibits rapid growth, and has an early age of reproduction. What makes this species unique among tetrapods is how farthermost it has compressed its suite of life history traits into a single, cursory season and that it spends the majority of its life cycle in a more benign and anticipated environment: the egg. In fact, its unabridged life span is shorter than the age of sexual maturity in many other chameleons (26). Our findings propose that the notorious rapid death of chameleons in captivity may, for some species, really stand for the natural adult life span. Consequently, a new appraisal may be warranted apropos the viability of chameleon breeding programs, which could have special significance for species of conservation concern. Additionally, if chameleons become a meliorate studied group, information technology will likewise be possible to construct life history tables to test empirically the evolution of semelparity in some species and why iteroparity is nowadays in others. Because F. labordi is closely related to other perennial species, this chameleon group may show also to be especially well suited for comparative studies that focus on life history evolution and the ecological, genetic, and/or hormonal determinants of aging, longevity, and senescence.

Materials and Methods

The study site, Ranobe forest (23°01′30″ S, 43°36′36″ East), was located in southwestern Madagascar, ≈30 km north of Toliara. The forests of the southwest are spiny, and vegetation was typically xerophyllous thickets that included the family Didiereaceae and the genus Euphorbia (54). The region is classified as a "desert and xeric shrubland ecoregion" (55) and is the driest region in Madagascar, including during the wet, active season. Nigh rainfall is attributed to the brief and sporadic passage of tropical storms over the Indian Ocean (56). The mean almanac rainfall of Toliara is 420 mm, with the wet flavour typically from December to Feb (56): mean monthly atmospheric precipitation for these months is 89.9 mm (57). Mean almanac temperature is 24.2°C. Like most arid environments, daily (day vs. nighttime) and seasonal (wet vs. dry out) temperature differences are high. Data were nerveless over four field seasons: Feb 22–March 5, 2003; December 20, 2003–Jan 30, 2004; December five–December 16, 2005; and Nov 4–December 12, 2006. We reviewed historical atmospheric precipitation data for Toliara (1951–2005) and institute that the available data from the same periods every bit our study were within expected rainfall amounts in this dry out region (i.east., the years we nerveless life history data were not characteristic of excessive drought compared with normal).

F. labordi and F. verrucosus are sexually dimorphic chameleons, inhabit arid regions of Madagascar (58), and are seasonally agile only during the wet season. Both species have secondary sexual characters, merely they are more exaggerated in F. labordi. F. verrucosus males possess big cranial casques, whereas females do non. Male F. labordi take proportionately larger cranial casques than F. verrucosus (unpublished data) and large rostral appendages; these typically "male" traits are too present in females, simply to a lesser degree.

All specimens were collected past hand at night; they often sleep within 2 m of the footing. Upon capture, we marked locations, placed lizards individually in cloth, mesh bags, and transported them to a base of operations campsite where they experienced the same environmental conditions every bit they would in the forest. Nosotros suspended the mesh bags from narrow cord to prevent predation from arboreal, nocturnal snakes. The following morning, we measured torso size (SVL) and full length (TL) by property each chameleon so that maximal extension was credible (i.e., no observable curvature to the body or tail). These measurements were made to the nearest 0.1 mm with calipers. Nosotros measured mass by using spring scales to the nearest 0.ane m (≤ten g) or 1 g (>ten g). We returned all lizards to their point of capture inside 24 h and observed no agin signs of social or handling stress in any individuals. Because of the brief period in which nosotros possessed these individuals and because these chameleons do not drinkable except during sporadic periods of pelting, we did not provide any supplemental food or h2o.

We gave all individuals a permanent identification past toe-clipping the nigh distal phalanx in a iii-toe combination, with only ane toe clipped per human foot. Nosotros observed no adverse side furnishings of this marking process on the behavior and survivability of individuals, nor did we observe any partial or full-phalanx regrowth to confuse individual markings. Radio transmitters weighing <x% of the beast's torso mass were affixed to the dorsal ridge of seven F. labordi with liquid agglutinative. Nosotros located each lizard daily and made brief (<30-min) focal observations, iii or 4 times per day.

For both species, we classified each private as hatchling, juvenile, or developed. Nonetheless, because F. labordi is unique in comprising a single cohort that transitions from juveniles to adults that are not sexually active initially, nosotros besides classified adults in this species every bit either prereproductive or sexually reproductive. Prereproductive adults were those exhibiting fully adult secondary sexual characters and noticeably larger body size relative to the rest of the population, merely were present before courtship started in the population (January 10). After January x, adult females exhibited sexually receptive coloration and were sexually reproductive. All adult males exhibited hemipenal bulges. Hatchlings lacked secondary sexual characters (casque and dorsal crest, plus rostral bagginess in F. labordi), and juveniles represented all other individuals.

Nosotros queried additional museum collections for localities and collecting dates of F. labordi. Our search yielded eight specimens at the University of Michigan Museum of Zoology (UMMZ) nerveless by C.J.R. March 18–28, 1995, at Ranobe, and 34 others at UMMZ collected from throughout the species' range. No other specimens with usable locality and/or collection appointment data were constitute in other collections.

Acknowledgments.

Field studies in Madagascar were made possible by the assistance of the Ministries des Eaux et Forêts, the Association Nationale pour la Gestion des Aires Protégées, and the Université d'Antananarivo, Département de Biologie Animale. We thank D. Rakotondravony and O. Ramilijaona for assistance with the project and H. Thomas and D. Kidney for valuable logistical advice. We thank Thou. Lovern, T. A. Baird, M. Palmer, R. Voss, R. Lehtinen, R. A. Nussbaum, and G. Schneider for their contributions. Research was supported past National Science Foundation Grant DEB 99-84496 (to C.J.R.).

Footnotes

The authors declare no disharmonize of involvement.

This article is a PNAS Direct Submission.

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