Effects of sex, age, and season on plasma steroids in free-ranging Texas horned lizards (Phrynosoma cornutum)
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; F1,24=0.40, P = 0.531), P (Fig. 1; F1,33 = 2.40, P = 0.131), or CORT (Fig. 1; F1,33 = 3.26, P = 0.080). However, breeding males had higher plasma T concentrations than breeding females (Fig. 1; F1,31 = 44.57, P < 0.001). Also, there were no differences between non-breeding males and females for E2 (Fig. 1; F1,57 = 0.10, P = 0.751), P (Fig. 1; F1,71 = 0.18, P = 0.669), or CORT (Fig. 1; F1,71 = 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.
References (68)
- et al.
Sex steroid levels in developing and adult male and female zebra finches (Poephila guttata)
Gen. Comp. Endocrinol.
(1990) - et al.
Does male sexual behavior require progesterone?
Brain Res. Rev.
(2006) - et al.
Sex steroids levels in the plasma and testis during the reproductive cycle of lizard Podarcis sicula sicula raf
Gen. Comp. Endocrinol.
(1992) - et al.
Annual androgen rhythm in the spiny-tailed lizard, Uromastix hardwicki
Gen. Comp. Endocrinol.
(1978) - et al.
Autoregulation of estrogen and androgen receptor mRNAs and downregulation of androgen receptor mRNA by estrogen in primary cultures of lizard testis cells
Gen. Comp. Endocrinol.
(1998) - et al.
Plasma vitellogenin and 17-beta estradiol levels during the annual reproductive cycle of Podarcis sicula sicula raf
Gen. Comp. Endocrinol.
(1991) Conservation and behavioral neuroendocrinology
Horm. Behav.
(2005)Gamete production, sex hormone secretion, and mating behavior uncoupled
Horm. Behav.
(1984)- et al.
Effects of corticosterone on social behavior of male lizards
Horm. Behav.
(1993) - et al.
Effects of steroid–hormone interaction on activity and home-range size of male lizards
Horm. Behav.
(1994)
Changes in plasma progesterone, estrogen, and testosterone concentrations throughout the reproductive cycle in female viviparous blue-tongued skinks, Tiliqua nigrolutea (Scincidae), in Tasmania
Gen. Comp. Endocrinol.
Male morphs in tree lizards have different testosterone responses to elevated levels of corticosterone
Gen. Comp. Endocrinol.
Is corticosterone involved in the reproductive processes of the male lizard, Podarcis sicula sicula
Horm. Behav.
Plasma androgens and their association with the reproductive cycle of the male fence lizard, Sceloporus undulatus
Comp. Biochem. Physiol. Part A
Stress-induced inhibition of sexual behavior: corticosterone inhibits courtship behaviors of a male amphibian (Taricha granulosa)
Horm. Behav.
Stress, reproduction, and adrenocortical modulation in amphibians and reptiles
Horm. Behav.
Regulation of male sexual behavior by progesterone receptor, sexual experience, and androgen
Horm. Behav.
Pattern of plasma sex steroid hormone levels during reproductive cycles of male and female tropical lizard, Calotes versicolor
Gen. Comp. Endocrinol.
Differential effects of testosterone and progesterone on the activation and retention of courtship behavior in sexual and parthenogenetic whiptail lizards
Horm. Behav.
Estrogen synthesis and secretion in the brown-headed cowbird (Molothrus ater)
Gen. Comp. Endocrinol.
Effects of corticosterone treatment on male aggressive behavior in a lizard (Anolis sagrei)
Horm. Behav.
Relationships between corticosterone concentration and season, time of day and confinement in a wild reptile (tuatara, Sphenodon punctatus)
Gen. Comp. Endocrinol.
Circulating estradiol and the activation of male and female copulatory behavior in Japanese quail (Coturnix-Japonica)
Gen. Comp. Endocrinol.
The determination of five steroids in avian plasma by radioimmunoassay and competitive protein-binding
Steroids
Female territorial aggression and steroid hormones in mountain spiny lizards
Anim. Behav.
Plasma corticosterone response to an acute stressor varies according to reproductive condition in female tree lizards (Urosaurus ornatus)
Gen. Comp. Endocrinol.
The effects of progesterone on sexual behavior in male green anole lizards (Anolis carolinensis)
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
Cited by (24)
Sex steroids are correlated with environmental factors and body condition during the reproductive cycle in females of the lizard Sceloporus torquatus
2021, General and Comparative EndocrinologyCitation Excerpt :Concentrations from June to September were similar; however, they were significantly higher in November (Fig. 3b and Fig. 4) because this period corresponds to the LV and PO stages. A similar pattern of this estrogen has been reported in species such as Cnemidophorus inornatus (Moore et al., 1984), Eublepharius macularius (Rhen et al., 2000), Calotes versicolor (Radder et al., 2001), S. virgatus (Weiss et al., 2002), Phrynosoma cornutum (Wack et al., 2008), Chameleo calyptratus (Kummrow et al., 2010), Salvator merianae (Zena et al., 2019), and Mabuya sp. (Barbosa-Moyano et al., 2020). We observed a positive correlation between E2 and follicular diameters.
Validation of an enzyme immunoassay for the quantification of testosterone in green iguana males (Iguana iguana)
2020, General and Comparative EndocrinologyCitation Excerpt :These steroid hormones are synthesized from cholesterol in the gonads, and transported via blood freely or in association with globulins and/or albumins, inducing the synthesis of proteins in the target tissues, for example, the synthesis of vitellogenin in the liver of the females (Licht, 1979; Jones, 2015). The study of sex hormones in reptiles has demonstrated their relationship and regulation with reproductive stages, e.g., vitellogenesis, mating, ovulation, and uterine secretory activities in Podarcis sicula (Mosconi et al., 1991), Tiliqua nigrolutea (Edwards et al., 2003), Chelonia mydas (Al-Habsi et al., 2006), Phrynosoma cornutum (Wack et al., 2008), Hemidactylus flaviviridis (Al-Amri et al., 2012) among others. Additionally, the relationship between the variation of these steroid hormones and the behavior of reptiles have also been demonstrated the effects of P4 and T in the organization and activation of sexual behavior of males in courtship and in females’ action of E2 and P4 to control sexual receptivity (Crews and Moore, 2005).
The impacts of invaders: Basal and acute stress glucocorticoid profiles and immune function in native lizards threatened by invasive ants
2012, General and Comparative EndocrinologyAmbient temperature and pregnancy influence cortisol levels in female guinea pigs and entail long-term effects on the stress response of their offspring
2011, General and Comparative EndocrinologyCitation Excerpt :Such results are important for comparative purposes because plasma levels of glucocorticoids vary greatly among amniotes depending upon taxonomy and reproductive strategy [63]. For example, average baseline levels are low in certain species (e.g. 5 ng ml−1 for the non-breeding Texas horned lizard, Phrynosoma cornutum; [75]; 2 ng ml−1 for house sparrows, Passer domesticus, [48]), but they are extremely elevated in others (e.g. 1270 ng ml−1 in the fruit bat, Pteropus hypomelanus, [78]; and 3000–8000 ng ml−1 in the Lemming, Lemmus trimucronatus, [63]). Statistical analyses were performed using R7.1. (
Hormones and Reproductive Cycles in Lizards
2011, Hormones and Reproduction of Vertebrates - Volume 3Stress and Reproduction in Reptiles
2011, Hormones and Reproduction of Vertebrates - Volume 3