Maricela Villagrán-Santa Cruz

Erosion of lizard diversity by climate change and altered thermal niches

Demise of the Lizards Despite pessimistic forecasts from recent studies examining the effects of global climate change on species, and observed extinctions in local geographic areas, there is little evidence so far of global-scale extinctions. Sinervo et al. (p. 894; see the Perspective by Huey et al.) find that extinctions resulting from climate change are currently reducing global lizard diversity. Climate records during the past century were synthesized with detailed surveys of Mexican species at 200 sites over the past 30 years. Temperature change has been so rapid in this region that rates of adaptation have not kept pace with climate change. The models were then extended to all families of lizards at >1000 sites across the globe, and suggest that climate change-induced extinctions are currently affecting worldwide lizard assemblages. A historical record of lizard populations in Mexico is used to parameterize models that predict global effects of climate change. It is predicted that climate change will cause species extinctions and distributional shifts in coming decades, but data to validate these predictions are relatively scarce. Here, we compare recent and historical surveys for 48 Mexican lizard species at 200 sites. Since 1975, 12% of local populations have gone extinct. We verified physiological models of extinction risk with observed local extinctions and extended projections worldwide. Since 1975, we estimate that 4% of local populations have gone extinct worldwide, but by 2080 local extinctions are projected to reach 39% worldwide, and species extinctions may reach 20%. Global extinction projections were validated with local extinctions observed from 1975 to 2009 for regional biotas on four other continents, suggesting that lizards have already crossed a threshold for extinctions caused by climate change.

CONTINUOUS SPERMATOGENESIS IN THE LIZARD SCELOPORUS BICANTHALIS (SAURIA: PHRYNOSOMATIDAE) FROM HIGH ELEVATION HABITAT OF CENTRAL MEXICO

Sceloporus bicanthalis is a viviparous lizard that inhabits high altitude temperate zone habitats in México. Our histological observations indicate that adult males exhibit spermatogenesis and spermiogenesis throughout the year; no seasonal differences were found in testes mass, height of epididymal epithelial cells, and number of layers of spermatogonia, primary and secondary spermatocytes, and spermatids. Seminiferous tubules exhibited slight, but statistically significant, seasonal variation in diameter. Continuous spermatogenesis and spermiogenesis of S. bicanthalis differ from the cyclical pattern exhibited by most species of lizards and from lizard species sympatric with S. bicanthalis. Continuous reproductive activity of males of S. bicanthalis, and maturation at a relatively small size, is associated with a female reproductive activity in which vitellogenic or pregnant females are present in the population during all months of the year. As a consequence, males can encounter potential mates as soon as they mature. Resumen Sceloporus bicanthalis es una lagartija vivípara que habita en elevaciones altas de ambientes templados en México. De acuerdo al análisis histológico, los machos adultos presentan espermatogénesis y espermiogénesis continuas; no se encontraron diferencias estacionales en el peso testicular, altura del epitelio de los conductos del epidídimo, número de capas de espermatogonias, espermatocitos primarios y secundarios y espermátidas. En contraste, se encontró variación estacional en el diámetro de los túbulos seminíferos. El patrón reproductor continuo de S. bicanthalis es atípico cuando se compara con los ciclos reproductores de otras lagartijas, incluyendo especies simpátricas. Aparentemente, la actividad reproductora continua de los machos de S. bicanthalis y su madurez sexual temprana, están asociadas con la actividad reproductora de las hembras, en el cual la vitelogénesis o preñez se presentan durante todo el año. En consecuencia, los machos pueden aparearse una vez que alcanzan la madurez sexual.

Body Temperatures of Female Sceloporus grammicus: Thermal Stress or Impaired Mobility?

Females of some lizard species exhibit lower body temperatures (Tbs) when reproductive (gravid or pregnant) than when not reproductive. Two hypotheses have been invoked to explain this phenomenon. One, the thermal stress hypothesis, is that the thermal optimum for embryos is lower than that of the female, and females thus actively select relatively low Tbs. The other, the encumbrance hypothesis, is that females are encumbered by their clutch/litter and thus passively accept relatively low Tbs. We collected field data on the thermal biology of Sceloporus grammicus at a high elevation site in Mexico during two seasons. In March, when thermoregulation was facilitated by high ambient temperature, lizards had high Tbs overall, and reproductive females had significantly lower Tbs than males; these observations were in accord with the thermal stress hypothesis. In June/July, when thermoregulation was difficult as a result of low ambient temperatures, lizards had low Tbs overall, and reproductive females had considerably lower Tbs than nonreproductive females. Thus, when thermal opportunities were limited, reproductive females had more difficulty thermoregulating than did nonreproductive females. These observations were in accord with the encumbrance hypothesis. The encumbrance hypothesis was also supported by the observation that females grew more slowly when reproductive than when nonreproductive. Thus, we suggest that the thermal stress and the encumbrance hypotheses are not alternatives but are complementary explanations for the thermal behavior of female Sceloporus.

Reproductive Cycle of the Lizard Sceloporus mucronatus with Comments on Intraspecific Geographic Variation

ABSTRACT. Sceloporus mucronatus is a viviparous lizard that inhabits high altitudes in central México. Lizards from Tecocomulco, Hidalgo, México, were collected monthly at 2500 m throughout one year. Macro- and microscopic evidence of gonads showed that both sexes reproduce synchronously during the fall. In males, after a short testicular quiescence in December, the recrudescence begins in winter (January) and continues through spring and summer (July), with maximum activity occurring from late summer to early fall (August–September). Regression takes place simultaneously with copulation during the fall (October–November). In females, vitellogenesis occurs during summer and fall (August–November), with ovulation in the fall (November–December). Gravid females were found throughout the winter, and parturition occurs during spring (May). Litter size was correlated with female snout-vent length. Female reproductive phenology of viviparous Sceloporus species seems to be highly conservative at different altitudes, but male reproductive phenology shifts between spring—summer (in populations higher than 2500 m) and summer—fall (in populations 2500 m or lower), as in the present study. The longer period of testicular recrudescence (January–July) in the studied population from Tecocomulco suggests plasticity in testicular activity.

Temporal germ cell development strategy during continuous spermatogenesis within the montane lizard, Sceloporus bicanthalis (Squamata; Phrynosomatidae)

Sceloporus bicanthalis is a viviparous lizard that lives at higher elevations in Mexico. Adult male S. bicanthalis were collected (n = 36) from the Nevado de Toluca, Mexico (elevation is 4200 m) during August to December, 2007 and January to July, 2008. Testes were extracted, fixed in Trumps, and dehydrated in a graded series of ethanol. Tissues were embedded, sectioned (2 μm), stained, and examined via a light microscope to determine the spermatogenic developmental strategy of S. bicanthalis. In all months examined, the testes were spermiogenically active; based on this, plus the presence of sperm in the lumina of seminiferous tubules, we inferred that S. bicanthalis had year-round or continuous spermatogenesis, unlike most reptiles that occupy a temperate or montane habitat. It was recently reported that seasonally breeding reptiles had a temporal germ cell development strategy similar to amphibians, where germ cells progress through spermatogenesis as a single population, which leads to a single spermiation event. This was much different than spatial development within the testis of other derived amniotes. We hypothesized that germ cell development was temporal in S. bicanthalis. Therefore, we wanted to determine whether reptiles that practice continuous spermatogenesis have a mammalian-like spatial germ cell development, which is different than the typical temperate reptile exhibiting a temporal development. In the present study, S. bicanthalis had a temporal development strategy, despite its continuous spermatogenic cycle, making them similar to tropical anoles.

Genetic Homogeneity between Populations of Aspidoscelis rodecki, a Parthenogenetic Lizard from the Yucatan Peninsula

Abstract We undertook skin-grafting between populations to determine whether Aspidoscelis rodecki originated from single, or multiple, parthenogenetically capable hybrids. We transplanted 292 skin grafts within and between the two most geographically distant populations, considering only grafts in animals surviving more than 45 days. Two hundred fifteen grafts were analyzed. Histocompatibility within (100%) and between (97.9%) populations suggests that A. rodecki was derived from a single, parthenogenetically capable, hybrid.

Reproductive Cycle of a High-Elevation, Oviparous Lizard (Sceloporus spinosus: Reptilia: Phrynosomatidae)

Abstract We studied the reproductive cycle of Sceloporus spinosus from Laguna La Preciosa, Puebla, Mexico, elevation 2,400 m. There was no sexual dimorphism in snout–vent length (males, 87.5 mm; females, 88.8 mm). Gonadal mass varied monthly and was related to snout–vent length; both sexes had a synchronous reproductive cycle that peaked in late winter and early spring. In males, recrudescence occurred November–January with abundant primary and secondary spermatocytes. Maximum testicular mass was in February when seminiferous tubules showed spermiogenesis and spermatozoa were in the lumen and epididymis. Regression was evident in April, when testicular mass decreased, and it continued in May, although spermatozoa were in seminiferous tubules and lumen of epididymal ducts. In July–September, testicular mass was less, and only spermatogonias, Sertoli cells, and remains of sperm were in seminiferous tubules. In females, vitellogenesis began in late autumn, maximum deposition of yolk was in March, and ovulation was in April. Oviductal eggs were present in April–June and oviposition was in June–July. In August–September, only previtellogenic and atretic follicles were present; hatchlings were present in September. Size of clutch was 6–17 eggs and correlated with snout–vent length. One clutch is produced per reproductive season. Reproductive activity in both sexes was distinct from spring-summer activity in tropical sceloporines from high elevations, but was similar to other lizards in northern temperate areas. Resumen Estudiamos el ciclo reproductor de Sceloporus spinosus de la laguna La Preciosa, Puebla, México, a una elevación de 2,400 m. No hubo dimorfismo sexual en la longitud hocico cloaca de machos (87.5 mm) y hembras (88.8 mm). La masa gonadal varió mensualmente y se correlacionó con la longitud hocico cloaca; ambos sexos tuvieron un ciclo reproductor sincrónico con una máxima actividad a fines del invierno y principios de la primavera. En los machos, la recrudescencia ocurrió de noviembre a enero con abundantes espermatocitos primarios y secundarios. La máxima masa testicular fue en febrero cuando los túbulos seminíferos mostraron espermiogénesis y espermatozoides se encontraron en la luz y en los conductos del epidídimo. La regresión fue evidente en abril, cuando decreció la masa testicular y se continuó en mayo, aunque espermatozoides estuvieron presentes en la luz de los túbulos seminíferos y en los conductos del epidídimo. De julio a septiembre la masa testicular se redujo y sólo espermatogonias, células de Sertoli y restos de espermatozoides permanecieron en los túbulos seminíferos. En las hembras la vitelogénesis inició a fines del otoño, el máximo depósito de vitelo fue en marzo y la ovulación en abril. Los huevos en el oviducto estuvieron presentes de abril a junio y la ovoposición fue en junio-julio. De agosto a septiembre sólo folículos previtelogénicos y atrésicos estuvieron presentes; los recién eclosionados aparecieron en septiembre. El tamaño de la puesta fue de 6 a 17 huevos y se correlacionó con la longitud hocico cloaca. Sólo una puesta es producida por estación reproductora. La actividad reproductora en ambos sexos fue diferente de la actividad de primavera–verano de sceloporinos tropicales de elevaciones altas, pero fue similar a la de otros lacertilios de áreas templadas norteñas.

REPRODUCTIVE BIOLOGY OF THE PARTHENOGENETIC LIZARD, ASPIDOSCELIS COZUMELA

The reproductive biology of the parthenogenetic lizard Aspidoscelis cozumela was studied from November 1994 to October 1995 on Cozumel Island, Quintana Roo, Mexico. Females exhibit a seasonal pattern with maximum reproductive activity during spring and summer (March to August) associated with day length. Clutch size averaged 1.8 (range 1–4) and was positively correlated with female body size. Females produced at least two clutches within the reproductive season.

Reproductive Activity in Females of the Oviparous Lizard Sceloporus aeneus

Abstract We studied the reproductive cycle of female Sceloporus aeneus from a population southeast of Mexico City (Milpa Alta), Mexico, from April 1993–March 1994. Females have a seasonal reproductive pattern with maximum activity in spring, a pattern typical of temperate oviparous species of the genus. Each female produces up to two clutches per breeding season, with a clutch size ranging from 4–10, which is not correlated with snout-vent length of females. Resumen De abril de 1993 a marzo de 1994 estudiamos el ciclo reproductor de las hembras de Sceloporus aeneus en una población al sureste de la Ciudad de México (Milpa Alta), México. Las hembras muestran un patrón reproductor estacional con actividad máxima en la primavera, un patrón típico de las especies ovíparas de ambiente templado del género. Cada hembra produce hasta dos nidadas por temporada reproductora, con un tamaño de puesta que varía de 4–10 huevos, el cual no se correlaciona con la longitud hocico-cloaca de las hembras.

Sperm Viability in the Reproductive Tract of Females in a Population of Sceloporus mucronatus Exhibiting Asynchronous Reproduction

ABSTRACT. Asynchronous reproduction is a common phenomenon in high-elevation populations of lizards from Central México. Sperm storage in the reproductive tract of females is the mechanism for making oocyte fertilization possible. Our study addresses questions related to functional oviductal sperm storage of females mating on different dates throughout the reproductive season. A population of Sceloporus mucronatus with copulation in the summer and ovulation in the fall was chosen for this experiment. Eleven females that copulated in the field during June and 13 females that copulated in captivity during August were maintained in the laboratory until parturition. The number of pregnant females and the litter sizes produced in each experimental group were indicative of the viability of the stored sperm. Sperm stored in the reproductive tract of females were able to fertilize eggs after 4 months. No significant differences were found in the number of pregnant females between the 2 experimental groups nor in the litter sizes that they produced. We found that the amount of time sperm were held in the female reproductive tract (ca. 3 months) had no effect on the capacity of sperm to fertilize eggs. Histological examination of 8 oviducts collected before the mating season eliminated the possibility of sperm storage from one year to the next. In this system, sperm retention could have evolved as a response mechanism to deal with the asynchrony between sexes in the reproductive cycles. However, we cannot rule out alternative hypotheses.