Effects of sex, age, and season on plasma steroids in free-ranging Texas horned lizards (Phrynosoma cornutum)

doi:10.1016/j.ygcen.2007.10.005

General and Comparative Endocrinology

Volume 155, Issue 3, 1 February 2008, Pages 589-596

https://doi.org/10.1016/j.ygcen.2007.10.005 Get rights and content

Abstract

The Texas horned lizard (Phrynosoma cornutum) is protected in several states due to its apparently declining numbers; information on its physiology is therefore of interest from both comparative endocrine and applied perspectives. We collected blood samples from free-ranging P. cornutum in Oklahoma from April to September 2005, spanning their complete active period. We determined plasma concentrations of the steroids, progesterone (P), testosterone (T), and corticosterone (CORT) by radioimmunoassay following chromatographic separation and 17β-estradiol (E2) by direct radioimmunoassay. T concentrations in breeding males were significantly higher than in non-breeding males. P showed no significant seasonal variation within either sex. CORT was significantly higher during the egg-laying season compared to breeding and non-breeding seasons for adult females and it was marginally higher in breeding than in non-breeding males (P = 0.055). CORT concentrations also significantly increased with handling in non-breeding males and egg-laying females. Perhaps most surprisingly, there were no significant sex differences in plasma concentrations of P and E2. Furthermore, with respect to seasonal differences, plasma E2 concentrations were significantly higher in breeding females than in egg-laying or non-breeding females, and they were significantly higher in breeding than in non-breeding males. During the non-breeding season, yearling males exhibited higher E2 concentrations than adult males; no other differences between the steroid concentrations of yearlings and adults were detected. In comparison to other vertebrates, the seasonal steroid profile of P. cornutum exhibited both expected and unexpected patterns, and our results illustrate the value of collecting such baseline data as a springboard for appropriate questions for future research.

Introduction

Temporal changes in plasma hormones, particularly steroids, frequently interact with changes in physiology, ecology, and behavior. For example, plasma testosterone concentrations often exhibit positive correlations with home-range size (e.g., Denardo and Sinervo, 1994) and agonistic behavior in male lizards (e.g., Fox, 1983). Although such generalities are useful, it is important to keep in mind that plasma steroids can vary in their effects on different species as well (Bern, 1990). For example, male red-sided garter snakes (Thamnophis sirtalis parietalis) exhibit peak testosterone concentrations the season before mating (Crews, 1984, Krohmer, 2004). Thus to understand the potential effects of hormones for any given species, it remains useful to first collect data on endogenous steroid concentrations.

We documented the steroid profile of the Texas horned lizard (Phrynosoma cornutum) in Oklahoma during its active period from April to September. This species ranges from the south-central United States to northern Mexico and has an adult size of 70–120 mm snout-vent length, with two occipital horns that point upward and dorsally located spines (Sherbrooke, 2003). The reproductive strategy of P. cornutum has been described as late maturing with one large clutch per year (Ballinger, 1974, Pianka and Parker, 1975, Tinkle et al., 1970), although P. cornutum, in areas of southern Texas, can have two clutches per year (Burrow, 2000; Kazmaier, unpub). Breeding occurs after individuals emerge from hibernation in late March to early April through May, when adult males and females are found with mature spermatids and yolked follicles, respectively (Ballinger, 1974, Howard, 1974). The non-breeding period occurs after breeding and continues until individuals enter hibernation in late September to early October (Endriss et al., 2007, Sherbrooke, 2003). Adult males, which are not territorial, increase their movements and cover a greater area during the breeding season, when they are searching for mates (Stark et al., 2005). Females have been reported to oviposit primarily in June with an average clutch size of 17 eggs (Endriss et al., 2007). The eggs hatch 49–68 days later, depending on weather conditions (Endriss et al., 2007). Hatchlings do not become reproductively active until the second summer following their birth when they are at least 19 months of age (Sherbrooke, 2003).

The population size of Texas horned lizards apparently has declined over the last several decades and, as a result, is listed as a Species of Special Concern in many states, including Oklahoma (Carpenter et al., 1993). In spite of broad interest in and need for information about P. cornutum, surprisingly little is known about its physiology. Most papers published on this species focus on behavior (e.g., Cahn, 1926; e.g., Milne and Milne, 1950, Sherbrooke and Middendorf, 2004) and ecology (e.g., Burrow et al., 2001, Donaldson et al., 1994, Fair and Henke, 1997); none have been published on endocrinology. On a larger scale, considering published endocrine studies across vertebrate species, few have comprehensively described steroid profiles for yearlings and adults of both sexes.

The objective of this study was to document plasma concentrations of 17β-estradiol (E2), progesterone (P), testosterone (T), and corticosterone (CORT) in adult and yearling Texas horned lizards. Specifically, we addressed the following questions: (1) Do steroid concentrations differ by sex or age? (2) Do steroid concentrations differ between reproductive and non-reproductive periods? and (3) Does brief capture and handling affect CORT concentration? This descriptive study should contribute to development of an effective conservation management program; endocrine data on gonadal steroids serve as a foundation for further research, and data on glucocorticoid concentrations can reveal how a species is responding to environmental stressors and human disturbance (Cockrem, 2005).

Section snippets

Sampling methods

We collected data on free-ranging male and female P. cornutum during sampling trips occurring every two weeks from 15 April to 18 September 2005. All work was conducted as approved by the Oklahoma State University Institutional Animal Care and Use Committee (Animal Care and Use Protocol No. AS059). Individuals were sampled from two sites, one located at Tinker Air Force Base in Oklahoma County, OK (35°24′58′′N and 97°24′41′′W) and the other in Payne County, OK (36°06′30′′N and 97°01′30′′W). We

Sex differences in plasma steroid concentrations

There were no differences between breeding males and females for E2 (Fig. 1; F_1,24=0.40, P = 0.531), P (Fig. 1; F_1,33 = 2.40, P = 0.131), or CORT (Fig. 1; F_1,33 = 3.26, P = 0.080). However, breeding males had higher plasma T concentrations than breeding females (Fig. 1; F_1,31 = 44.57, P < 0.001). Also, there were no differences between non-breeding males and females for E2 (Fig. 1; F_1,57 = 0.10, P = 0.751), P (Fig. 1; F_1,71 = 0.18, P = 0.669), or CORT (Fig. 1; F_1,71 = 3.19, P = 0.078). However, non-breeding males had

Discussion

The seasonal steroid profile of P. cornutum exhibited several traditional and non-traditional hormone-behavior relationships. E2 concentrations typically elevate in female lizards during the breeding season when vitellogenesis is occurring and reach peak concentrations just before ovulation when vitellogenic follicles are large (Alberts et al., 2004, Carnevali et al., 1991, Edwards and Jones, 2001a, Radder et al., 2001). The E2 profile of female P. cornutum suggests that a similar pattern is

Acknowledgments

We thank Raymond Moody for giving us access to horned lizards on Tinker AFB. Dr. Jerry Chmielewski provided statistical advice. Thanks to Sarah Woodley and Timothy O’Connell for helpful comments on the manuscript. Debora Endriss and Crystal Stanley were instrumental in helping us find horned lizards in the field, and Jennifer Doyle spent many hours helping us with lab work. This work was supported in part by Tinker AFB and the Department of Zoology at Oklahoma State University.

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Effects of sex, age, and season on plasma steroids in free-ranging Texas horned lizards (Phrynosoma cornutum)

Abstract

Introduction

Section snippets

Sampling methods

Sex differences in plasma steroid concentrations

Discussion

Acknowledgments

Gen. Comp. Endocrinol.

Brain Res. Rev.

Gen. Comp. Endocrinol.

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Comp. Biochem. Physiol. Part A

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Horm. Behav.

Horm. Behav.

Gen. Comp. Endocrinol.

Horm. Behav.

Gen. Comp. Endocrinol.

Horm. Behav.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Steroids

Anim. Behav.

Gen. Comp. Endocrinol.

Horm. Behav.

Reproduction of the Texas horned lizard, Phrynosoma cornutum

Herpetologica

Activational and organizational effects of estradiol on male behavioral neuroendocrine function

Scand. J. Psychol.

The new endocrinology—its scope and its impact

Am. Zool.

Steroids control the aromatase gene expression in purified germ cells from the adult male rat

J. Mol. Endocrinol.

The physiological ecology of desert horned lizards (Phrynosoma platyrhinos) in the Mojave Desert

The effect of prescribed burning and grazing on the threatened Texas horned lizard (Phrynosoma cornutum) in the western Rio Grande Plains