Sceloporus Jarrovi Research Articles

The structure of the thermal landscape determined behavioural and physiological responses to simulated predation risk

Abstract Although predators can deter an animal from regulating its body temperature by basking or shuttling, this response to predation should depend on the spatial distribution of thermal resources. By simulating predation risk, we showed that movement, thermoregulation and corticosterone of male lizards (Sceloporus jarrovi) depended on the spatial distribution of shade. Simulated risk caused lizards to move less, thermoregulate worse and circulate more corticosterone than they did without risk. However, a patchier distribution of shade enabled lizards to move more, thermoregulate better and circulate less corticosterone when exposed to a simulated predator. In the absence of simulated risk, lizards in patchier environments moved less, thermoregulated better and circulated less corticosterone, indicating the distribution of shade also affected the energetic cost of thermoregulation. This study provides the first test of a spatial theory of thermoregulation under the perceived risk of predation. Read the free Plain Language Summary for this article on the Journal blog.

Lizards perceived abiotic and biotic stressors independently when competing for shade in terrestrial mesocosms

Hormones such as glucocorticoids and androgens enable animals to respond adaptively to environmental stressors. For this reason, circulating glucocorticoids became a popular biomarker for estimating the quality of an environment, and circulating androgens are frequently used to indicate social dominance. Here, we show that access to thermal resources influence the hormones and behavior of male lizards (Sceloporus jarrovi). We exposed isolated and paired males to different thermal landscapes, ranging from one large patch of shade to sixteen smaller patches. Both the presence of a competitor and the patchiness of the thermal environment influenced hormone concentrations and movement patterns. When shade was concentrated in space, paired lizards competed more aggressively and circulated more corticosterone. Even without competitors, lizards circulated more corticosterone in landscapes with fewer patches of shade. Conversely, shifts in circulating testosterone depended only on the relative body size of a lizard; when paired, large males and small males circulated more and less testosterone, respectively. Furthermore, isolated males moved the farthest and covered the most area when shade was concentrated in a single patch, but paired males did the opposite. Because the total area of shade in each landscape was the same, these hormonal and behavioral responses of lizards reflect the ability to access shade. Thus, circulating glucocorticoids should reflect the thermal quality of an environment when researchers have controlled for other factors. Moreover, a theory of stress during thermoregulation would help ecologists anticipate physiological and behavioral responses to changing climates.

Competition during thermoregulation altered the body temperatures and hormone levels of lizards

Summary Every organism must thermoregulate to maximize its performance, but competing organisms limit access to preferred microclimates. Such competition often creates hierarchies in which dominant individuals have more access to limited resources than subordinate individuals. To assess the costs of competition during thermoregulation, we measured thermoregulation, movement, and hormones of male lizards (Sceloporus jarrovi) when alone and when paired with a smaller or larger conspecific. Large males were 31% closer to the heat source when paired than when alone, resulting in a higher mean body temperature (35·7 vs. 33·9 °C). Conversely, small males were 40% farther from the heat source when paired, resulting in lower mean body temperature (32·1 vs. 33·6 °C). When paired, large and small males circulate 26 and 44% more corticosterone, respectively. Conversely, large males circulated 26% more testosterone when paired, whereas small males circulated 26% less testosterone. Both dominant and subordinate males incurred costs when paired, including poorer thermoregulation, more movement and greater physiological stress. Thus, competition for thermal resources should feature more prominently in ecological and evolutionary models of thermoregulation. A lay summary is available for this article.

Scanning electron microscopy of the placental interface in the viviparous lizard Sceloporus jarrovi (Squamata: Phrynosomatidae)

Placental membranes mediate maternal-fetal exchange in all viviparous reptilian sauropsids. We used scanning electron microscopy to examine the placental interface in the mountain spiny lizard, Sceloporus jarrovi (Phrynosomatidae). From the late limb bud stage until birth, the conceptus is surrounded by placental membranes formed from the chorioallantois and yolk sac omphalopleure. The chorioallantois lies directly apposed to the uterine lining with no intervening shell membrane. Both fetal and maternal sides of the chorioallantoic placenta are lined by continuous layers of flattened epithelial cells that overlie dense capillary networks. The chorioallantoic placenta shows specializations that enhance respiratory exchange, as well as ultrastructural evidence of maternal secretion and fetal absorption. The yolk sac placenta contains enlarged fetal and maternal epithelia with specializations for histotrophic nutrient transfer. This placenta lacks intrinsic vascularity, although the vascular allantois lies against its inner face, contributing to an omphallantoic placenta. In a specialized region at the abembryonic pole, uterine and fetal tissues are separated by a compact mass of shed shell membrane, yolk droplets, and cellular debris. The omphalopleure in this region develops elongate folds that may contribute to sequestration and absorption of this material. Fetal membrane morphogenesis and composition in S. jarrovi are consistent with those of typical squamates. However, this species exhibits unusual placental specializations characteristic of highly placentotrophic lizards.

Food consumption does not affect the preferred body temperature of Yarrow's spiny lizard ( Sceloporus jarrovi)

When animals consume less food, they must reduce their body temperature to maximize growth. However, high temperatures enhance locomotion and other performances that determine survival and reproduction. Therefore, thermoregulatory behaviors during different metabolic states reveal the relative importance of conserving energy and sustaining performance. Using artificial thermal gradients, we measured preferred body temperatures of male spiny lizards ( Sceloporus jarrovi) in fed and fasted states. Both the mean and maximal body temperatures (33° and 35 °C, respectively) were unaffected by metabolic state. This finding suggests that the benefits of foraging effectively, evading predators, and defending territory outweigh the energetic cost of a high body temperature during fasting.

Functionally opposing effects of testosterone on two different types of parasite: implications for the immunocompetence handicap hypothesis

Summary 1. The immunocompetence handicap hypothesis (ICHH) proposes that androgen‐dependent sexual traits are honest indicators of male quality because androgens are thought to suppress the immune system’s ability to combat parasitic infection. Yet, recent work suggests that the relationship between androgens and parasitism is more complex, as androgens may have different effects on the various types of parasites. 2. We explored this issue in free‐living mountain spiny lizards, Sceloporus jarrovi, by measuring the prevalence of four endoparasite species and one ectoparasite species in castrated, sham‐operated and testosterone (T)‐implanted males. 3. We found that effects of T manipulation accounted for the greatest amount of variability in the abundance of Trombiculid mites and two gastrointestinal nematodes (Physaloptera retusa and Spauligodon giganticus). Plasma T levels were positively associated with mite loads, negatively associated with P. retusa loads and not associated with S. giganticus load. We also found that T treatment had little effect on the abundances of two species of blood‐borne endoparasites (Plasmodium chiricahuae and an unidentified haemogregarine). Instead, the prevalence of these two parasites was mostly influenced by other physiological or seasonal factors, such as corticosterone levels, body condition, fat stores or time between capture events. 4. Our data illustrate that T can have functionally distinct and opposing effects on different parasite species. This finding supports the hypothesis that T does not depress the immune system in a way that causes an across‐the‐board increase in parasitism. 5. We speculate that T modifies select behavioural and physiological factors that govern parasite accumulation. Evolutionarily, our data also imply that the net ‘cost of T’ with respect to elevated ectoparasitism may be at least partially offset by concomitant reductions in helminth load.

Placental specializations of the mountain spiny lizard Sceloporus jarrovi

The lizard Sceloporus jarrovi (Phrynosomatidae) is one of the most widely studied viviparous reptiles of North America. Past research has assumed that placentation in this species is relatively simple and functions mainly in gas exchange. Our examination of the late stage placenta via transmission electron microscopy reveals that S. jarrovi has a unique combination of placental characteristics, with unusual specializations for secretion and absorption. In the chorioallantoic placenta, chorionic and uterine tissues are directly apposed through eggshell loss, and their epithelia are greatly attenuated, enhancing gas exchange; this placenta shows evidence of both nutrient transfer and endocrine function. Contrary to past inferences, a yolk sac placenta forms from the avascular omphalopleure and persists through the end of gestation. The uterine epithelium is enlarged and secretory, and the fetal omphalopleure shows branching absorptive channels and other specializations for uptake. Elsewhere, the omphalopleure develops elongated folds that protrude into a coagulum of degenerating shell membrane and other organic material. Uterine tissue in this region shows specializations for absorption. Placental features in S. jarrovi have unexpected functional implications, and challenge assumptions that specializations for nutrient transfer are confined to matrotrophic species.

Steroid Hormone Metabolism by the Chorioallantoic Placenta of the Mountain Spiny LizardSceloporus jarrovias a Possible Mechanism for Buffering Maternal‐Fetal Hormone Exchange

The placenta provides a maternal-fetal exchange interface that maximizes the diffusion of gases, nutrients, and wastes. However, the placenta also may permit diffusion of lipid-soluble steroid hormones that influence processes such as sex-specific fetal development and maternal pregnancy maintenance. In mammals, placental steroid metabolism contributes to regulation of maternal and fetal hormone levels. Such mechanisms may be less highly developed in species that have recently evolved placentation, such as many reptiles. We therefore chose to investigate placental metabolism of steroids in the viviparous lizard Sceloporus jarrovi. In vitro tissue incubations tested the abilities of the chorioallantoic placenta to clear progesterone and corticosterone by converting them to other metabolites and to synthesize progesterone. Placental tissue rapidly cleared progesterone and corticosterone added to the incubation media, indicating that the tissue had converted the steroids to other products. Placental tissue also synthesized substantial concentrations of progesterone from the prohormone pregnenolone. Thus, even in a species with a simple, recently evolved placenta, steroid metabolism appears to be highly developed and could be critical for regulation of maternal and fetal hormone levels. This finding suggests that placental hormone metabolism may be critical to the successful evolution of placentation.

Testosterone and Daily Activity Period in Laboratory-Housed Mountain Spiny Lizards, Sceloporus jarrovi

Experimentally elevated testosterone has been shown to increase the daily activity period of free-ranging lizards, but it is unknown whether the effect depends upon additional factors present in nature (i.e., conspecific interactions) or whether it can be elicited in the laboratory. In a relatively simple laboratory environment, male Mountain Spiny Lizards (Sceloporus jarrovi) implanted with testosterone had significantly greater activity levels throughout the day than sham-implanted males. Differences were greatest during the morning and late afternoon, with testosterone-treated males more likely to be out earlier and to stay out later. This general result was repeated in both spring and fall experiments using separate groups of males. Although testosterone-treated males were more active (i.e., out in the open) than control males, there was not a significant difference in the frequency of movements (>20 cm), nor did the groups differ in selected body temperature in their home cages. Nonetheless, testosterone-implanted males lost significantly more body mass than controls over the course of the experiments. Because the effect of testosterone on daily activity period occurs in the laboratory as well as in the field, it is suggested that the effect is not dependent upon interactions with complex environmental stimuli.

NOCTURNAL ACTIVITY BY DIURNAL LIZARDS (SCELOPORUS JARROVI, S. VIRGATUS) EATEN BY SMALL OWLS (GLAUCIDIUM GNOMA, OTUS TRICHOPSIS)

Whiskered screech-owls (Otus trichopsis) and northern pygmy-owls (Glaucidium gnoma) delivered freshly caught Yarrow's spiny lizards (Sceloporus jarrovi) and striped plateau lizards (S. virgatus) to nestlings from dusk to dark in southeastern Arizona. This observation stimulated studies of the prey deliveries by the owls and lizard activity patterns, because the lizards are not known to be nocturnal. Lizards were more frequent prey of both owls than endothermic vertebrates but infrequent compared to arthropods, a pattern in the pygmy-owl that differs from its northern populations. Yarrow's spiny lizard, the most abundant and frequently captured lizard, was most active in the morning but also active in the evening. Striped plateau lizard, the second most abundant and depredated species, had morning and evening peaks of activity. Few lizards, including S. clarki and Urosaurus ornatus, but not Cnemidophorus exsanguis and C. sonorae, were active at or after dark, when relatively few were captured by the owls.

Placental buffering of maternal steroid hormone effects on fetal and yolk hormone levels: a comparative study of a viviparous lizard, Sceloporus jarrovi, and an oviparous lizard, Sceloporus graciosus

We investigated maternal-fetal hormone transfer in the mountain spiny lizard, Sceloporus jarrovi, a viviparous species with a simple chorioallantoic placenta. In one experiment, we examined the effect of elevated maternal progesterone on fetal and yolk hormone levels. Progesterone implants increased maternal progesterone nearly 100-fold; however, the resulting increase in fetal and yolk progesterone was only about 2% of that seen in mothers, providing evidence that the placenta buffers hormone diffusion. In addition, some effects of progesterone treatment differed between male and female fetuses, suggesting that this buffering may differ between the sexes. In a second experiment, we examined the relationship between maternal and fetal hormone levels in viviparous versus oviparous species. We measured endogenous progesterone, testosterone, estradiol, and corticosterone levels in pregnant S. jarrovi and their fetuses and neonates, and in gravid S. graciosus (an oviparous congener) and their fetuses and hatchlings. No clear relationship was identified between maternal and fetal or hatchling S. graciosus hormone levels. However, the data for S. jarrovi suggest that maternal hormones may inhibit perinatal hormone secretion. These findings indicate that, despite the relatively recent evolutionary origin and simple structure of the S. jarrovi placenta, mechanisms for placental mediation of the maternal-fetal endocrine relationship have evolved. Although the placenta appears to buffer hormone transport, maternal hormones can affect fetal and yolk hormone levels, suggesting that disruption of endocrine regulation could be a physiological cost of the evolution of viviparity.

Interaction of Testosterone and Social Stimuli on the Feeding Behavior of Male Mountain Spiny Lizards, Sceloporus jarrovi

Experimental elevation of plasma testosterone during the nonbreeding season has previously been shown to reduce the survivorship of male mountain spiny lizards, Sceloporus jarrovi. The reduction in survivorship results from energetic stress caused, in part, by reduced foraging behavior. This study examines proximate explanations for this decreased foraging behavior. In particular, do testosterone-treated males engage in more social behaviors at the expense of feeding? This question was tested by observing the behavior of hormonally manipulated males in a large indoor arena in which both social and prey stimuli were present. Males were tested with social stimuli present during the nonbreeding season (male intruders, sexually unreceptive females, or a combination of male and females) and with stimuli encountered only during the breeding season (sexually receptive females). Testosterone-implanted males ate significantly fewer prey when a sexually receptive female was present, but control males did not. However, a difference in feeding was not observed in any of the nonbreeding stimulus conditions in spite of consistent increases in social behaviors, such as display frequencies. These results indicate that, although high levels of testosterone increase some aspects of social behavior, they do not necessarily lead to decreased feeding in the nonbreeding season.

Female territorial aggression and steroid hormones in mountain spiny lizards

In certain species, females are highly aggressive. For example, female mountain spiny lizards,Sceloporus jarrovi, express aggressive behaviours when defending their territories. Despite the occurrence of female aggression, relatively little is known about its underlying hormonal mediation. As a first step in understanding neuroendocrine mechanisms of female aggression, this study documented seasonal changes in territorial aggression, plasma steroid hormone levels, and reproductive condition in free-living female mountain spiny lizards. We determined how seasonal patterns of testosterone (T), oestradiol (E), dihydrotestosterone (DHT) and corticosterone (B) corresponded to seasonal patterns of aggression. At times of the year when females were most aggressive, plasma levels of T and E were elevated. At times of the year when females were least aggressive, plasma B was elevated. Furthermore, when levels of T were elevated, females were more aggressive, and when levels of B were elevated, females were less aggressive. Plasma levels of DHT were not associated with aggression. These seasonal patterns are consistent with the hypotheses that T, and perhaps E, promote female aggression, while B suppresses female aggression. Despite these associations of hormones and aggression, no hormone was associated with aggression in a one-to-one fashion. This suggests that if steroid hormones contribute to the expression of female aggression, they must interact with each other or with other factors (for example, other hormones, receptor levels, environmental factors) to mediate fully the expression of aggression.

Central Monoamines in Free-Ranging Lizards: Differences Associated with Social Roles and Territoriality

During the breeding season different social classes of field-active lizards, Sceloporus jarrovi, exhibit regionally specific changes in central monoaminergic activation. Changes in serotonergic content and turnover between lizards from different social classes are seen in forebrain structures (telencephalon and diencephalon) and reflect events associated with reproductive behaviors, stress and aggression. Males without territories (satellite males) exhibit higher forebrain serotonin (5-HT) system activation compared to territorial males and adult females. This serotonergic activation includes increased 5-hydroxyindoleacetic acid (5-HIAA) and 5-HIAA/5-HT ratio, suggesting increased release and catabolism. Satellite males also exhibit higher 5-HIAA/5-HT ratios (serotonergic turnover) compared to territorial males following agonistic interactions. Territorial males, immediately following aggressive defense of territories against intruder males, exhibit increased 5-hydroxytryptophan (5-HTP) levels, higher 5-HIAA levels and 5-HIAA/5-HT ratio, higher epinephrine levels, greater MHPG/NE, more DOPAC and larger DOPAC/DA ratio compared to territorial males that did not have an aggressive encounter. These differences suggest activation of 5-HT, norepinephrine (NE), and dopamine (DA) systems by the synthesis and release of more 5-HT and the release of more NE and DA during aggressive defense of territory. The highest activity of serotonergic systems is exhibited by satellite males compared to territorial males, perhaps reflecting stress in subordinate animals from social and ecological sources.

Influence of pregnancy on the thermal biology of the lizard, Sceloporus jarrovi: why do pregnant females exhibit low body temperatures?

1. Selected body temperatures of female lizards, Sceloporus jarrovi, were measured on a photothermal gradient during late pregnancy and again when postpartum, and pregnant females were subjected to one of three fluctuating temperature regimes that simulated body temperatures of (1) pregnant females, (2) postpartum females or (3) allowed normal thermoregulation. 2. Overall, females selected lower body temperatures when pregnant (mean = 32·0°C) than when postpartum (mean = 33·5°C). 3. Females regulated body temperature more precisely when pregnant than when postpartum as judged by their smaller variances in body temperature throughout the day. 4. When pregnant, females selected a lower mean maximum body temperature (mean: pregnant = 32·8°C; postpartum = 34·5°C) than when postpartum, but selected mean minimum body temperatures did not differ. 5. None of the experimental temperature treatments was detrimental to pregnant females. Female body length increased during pregnancy but the rate of increase did not differ among treatments. Moreover, length‐adjusted body mass of postpartum females did not differ among treatments. 6. Pregnant females that experienced postpartum body temperatures produced neonates that were smaller in body mass and length than pregnant females that experienced pregnant body temperatures and females that were allowed to thermoregulate. 7. For neonates resulting from the postpartum body temperature treatment, the disparity in the body length, but not mass, was still observed at 9 days of age, although survival and growth of neonates was high and did not differ among treatments. 8. The results demonstrate that pregnant females could maintain higher postpartum body temperatures without compromising their physical condition, but select relatively low body temperatures, presumably to avoid decrements in offspring fitness.

Adrenergic and peptidergic innervation of the oviduct of Sceloporus jarrovi during the reproductive cycle

Adrenergic and peptidergic innervation of the oviduct of Sceloporus jarrovi during the reproductive cycle

Molecular Differentiation of Two New World Saurian Plasmodium Species in Different Host Species Using the Polymerase Chain Reaction

Several isolates of Plasmodium floridense obtained from naturally infected Anolis carolinensis and Anolis sagrei, and 2 isolates of Plasmodium chiricahuae obtained from Sceloporus jarrovi were characterized at the ribosomal DNA (rDNA) locus using the polymerase chain reaction and agarose gel electrophoresis. Enzymatic amplification of the rDNA locus from both Plasmodium species resulted in the generation of a 590-base pair (bp) DNA fragment. The results obtained with all isolates of P. floridense appeared as a doublet, with the second fragment being approximately 630 bp in size. Isolates of P. floridense obtained from A. carolinensis from ecologically different northern and southeastern Florida, and from A. sagrei a the same southeastern Florida site, were demonstrated to be molecularly similar. Plasmodium floridense and P. chiricahuae were molecularly distinct at the 18s rDNA locus, thus confirming their morphological and morphometrical distinction as taxonomic species. Anolis sagrei is a third natural host species for P. floridense in Florida.

Increased energy expenditure due to increased territorial defense in male lizards after phenotypic manipulation

Fitness tradeoffs are difficult to examine because many fitness variables are correlated and vary in the same direction. Phenotypic manipulation circumvents many of these difficulties, and here we used this technique to examine mechanisms for tradeoffs between increased aggression (territorial defense) and survivorship. The behavioral phenotype of male mountain spiny lizards (Sceloporus jarrovi) was manipulated with testosterone to increase territorial defense, a sexually selected trait. We previously demonstrated that increased territorial defense results in a decrease in survival caused by a lower ratio of energy intake to energy expenditure. Here we measured energy consumption of increased territorial aggression using the doubly labeled water technique in the field and compared males with and without testosterone implants (Fig. 1). In a supplementary study we measured standard metabolic rate using captive lizards given similar testosterone implants to examine if an increase in energy expenditure was a result of only an increase in standard metabolic rate (Fig. 3). Our results indicated that a primary contribution to tradeoffs between increased territorial defense and survivorship could be made by a 31% increase in energy expenditure in the field that is not due to an increase in standard metabolic rate.

Temporal and Spatial Variation in Individual Growth in the Spiny Lizard, Sceloporus jarrovi

Temporal and spatial variation in individual growth rates of Sceloporusjarrovi from three populations in the Chiricahua Mountains of southeastern Arizona were studied from 1973 to 1976. Annual variation in individual growth rate was observed only in the low-altitude population. Growth rates for individuals in the low-altitude population were lowest in 1974 (a year in which a drought occurred; 0.06 mm d-1), and yearlings in the low-altitude population had particularly low growth rates in 1974 relative to other years. Averaging over all years, two high-altitude populations (0.16 mm d-' in both populations) had significantly higher growth rates than the low-altitude population (0.12 mm d-'). Data on arthropod abundance and rainfall suggest that food availability can explain much of the observed temporal and spatial variation in individual growth

Survivorship in a High-Elevation Population of Sceloporus jarrovi during a Period of Drought

Survivorship in a High-Elevation Population of Sceloporus jarrovi during a Period of Drought