Skin lipids of the striped plateau lizard (Sceloporus virgatus) correlate with female receptivity and reproductive quality alongside visual ornaments
Sex pheromones can perform a variety of functions ranging from revealing the location of suitable mates to being honest signals of mate quality, and they are used in the mate selection process by many species of reptile. In this study, we determined whether the skin lipids of female striped plateau lizards (Sceloporus virgatus) can predict the reproductive quality of females, thereby having the potential to serve as pheromones. Using gas chromatography/mass spectrometry, we identified 17 compounds present in skin lipids of female lizards. Using principal component analysis to compare the skin lipid profile of receptive and non-receptive females, we determined that an uncharacterized compound may allow for chemical identification of receptive mates. We also compared extracted principal components to measures of female fitness and reproductive qualities and found that the level of two 18 carbon fatty acids present in a female’s skin lipids may indicate her clutch size. Finally, we compared the information content of the skin lipids to that of female-specific color ornaments to assess whether chemical and visual cues transmit different information or not. We found that the chroma of a female’s orange throat patch is also related to her clutch size, suggesting that chemical signals may reinforce the information communicated by visual ornamentation in this species which would support the “backup signals” hypothesis for multiple signals.
KeywordsChemical cues Lizards Multimodal communication Pheromones Reptilian Skin lipids
Chemical signature mixtures and pheromones come in various forms and can transmit myriad messages between conspecific organisms. For example, they have been shown to reveal the location of an individual to conspecifics, mark territory boundaries, and transmit information regarding the quality of potential mates (Johanssen and Jones 2007; Wyatt 2014). Signature mixtures are blends of compounds that transmit information to conspecifics without an evolutionarily derived signaling function whereas pheromones are chemical compounds with a signaling function that is the result of selection acting upon both signalers and receivers (Wyatt 2014). Both forms of chemical cues are understudied in the sexual selection literature (Penn and Potts 1998), as research has emphasized the role of striking visual and auditory displays (Moore et al. 2016).
Reptiles, like many other animals, mediate social interactions with chemical cues (Houck 2009). Inter-species and inter-population variation in chemical profiles is known to drive species identification, reproductive isolation, and speciation in both snakes (LeMaster and Mason 2002) and lizards (Barbosa et al. 2006). Inter-individual variation also plays an important role in mate choice by honestly signaling phenotypic information (LeMaster and Mason 2002). Reptilian pheromones can originate from many physiological sources (Weldon et al. 2008), yet prior research with lizards has focused on the secretions of the femoral glands (Alberts 1990; Mártin et al. 2013). The femoral glands are more productive during the breeding season, suggesting they play a role in mating (Martins et al. 2006). In many species, femoral glands are only active in males and play a role in rival assessment (Carazo et al. 2007), species identification (Gabriot et al. 2010), and mate assessment (Mártin et al. 2007). Less is known about the role of female chemical signals in the reproductive behavior of lizards.
The striped plateau lizard (Sceloporus virgatus) is a medium-sized lizard native to the Chiricahua Mountains of Arizona, USA. Males of the genus Sceloporus usually have bright colored ornamentation, yet S. virgatus has recently lost this ancestral trait (Wiens 1999). Instead, females possess orange throat patches which signal reproductive quality to conspecifics and influence male behavior (Weiss 2002; Weiss 2006; Weiss et al. 2009). The loss of male visual ornamentation in S. virgatus has been linked to higher rates of chemosensory behaviors (Hews et al. 2011), suggesting that chemical communication may play a greater role in this species than in related species. Consistent with this idea, S. virgatus males frequently tongue flick the flanks of females during courtship (Weiss, personal observation), and behavioral evidence has been found suggesting that information regarding female body size is transmitted via chemical cues (Fritzche and Weiss 2012). Despite this, little progress has been made in elucidating the composition of chemical cues in S. virgatus.
Females of this species lack active femoral glands, thus making skin lipids a likely source for female pheromones although others certainly exist. The primary function of skin lipids is believed to be preventing water loss (Roberts and Lillywhite 1980), yet they are also known to function as pheromones in some species (Weldon et al. 2008). Components of the epidermal lipids in female red-sided garter snakes (Thamnophis sirtalis parietalis) produced only during the mating season (Uhrig et al. 2012) serve as an attractiveness pheromone communicating phenotypic information to conspecifics (Mason et al. 1989) whereas differences between the skin lipids of male and female leopard geckos mediate sex recognition (Mason and Gutzke 1990).
The use of both visual and chemical cues by S. virgatus females presents the unique opportunity to study the information content of female cues in separate sensory modalities. Theoretical models have shown that when a species utilizes multiple displays, the displays can signal different information (multiple messages) or strengthen transmission of another signal (backup signals; Johnstone 1996). Thus, by relating measures of female color with phenotypic measures, we set out to determine if communication via skin lipids could serve as a backup to visual ornamentation, or signal a separate message.
In this study, we address three questions regarding the epidermal lipids of S. virgatus females: (1) what is the chemical makeup of their skin lipids? (2) does the profile of the skin lipids indicate a female’s receptivity? and (3) can a female’s skin lipid profile predict her phenotype/reproductive quality? We also examined the information content of a female’s color ornament following Weiss (2006) and compared this to the information content of her skin lipid profile.
Materials and methods
Lizard collection and maintenance
Sceloporus virgatus females (hereafter “lizards”) were captured by noose from the vicinity of the Southwestern Research Station (SWRS, Portal, AZ) on May 26 (N = 8), June 7 (N = 6), and June 20 (N = 7) 2010. Lizards (total N = 21) were housed individually in terraria (22.9 × 15.2 × 16.5 cm) on a screened porch, allowing for natural light and temperature fluctuations for 7 days. Additional heat was provided by a 40 W incandescent bulb in a metal reflector on a 12:12 light:dark cycle. Lizards were fed crickets (Acheta sp., Fluker Farms) and provided access to water twice during this period; feedings occurred in separate 10-gal glass terraria to control the duration of exposure to prey-borne chemicals.
Upon capture, lizards were weighed to determine body mass, measured with a transparent ruler to determine body size (snout to vent length, SVL), and had the number of trombiculid and pterygosomatid mites on their body counted. The residuals of a regression of SVL and body mass were used as the measure of body condition (Weiss 2006). Following euthanization and extraction of skin lipids (detailed below), females were dissected in order to classify the reproductive state of each female as non-reproductive (NR, N = 7), vitellogenic (V, N = 5), or gravid (G, N = 9). NR females were those that had not yet reached sexual maturity. Reproductive females are vitellogenic before ovulation occurs whereas after ovulation, females become gravid and are no longer sexually receptive. The ovaries of V females were weighed and the number of enlarged follicles was counted. For G females, the egg-containing oviducts were removed, weighed for mass, and the number of eggs was counted.
On the 8th day following capture, the right throat patch of each female was photographed along with a small ruler using an Olympus C-5050 ZOOM 5-megapixel digital camera set to macro mode with a Super Bright zoom F1.8 lens under standardized indoor lighting. Ornament area was measured by selecting orange pixels from the photograph using the “color range” command of Adobe Photoshop 9.0 (Weiss 2006) and determining the area of the selected pixels (in mm2) in National Institutes of Health ImageJ 1.60. The value (relative lightness or darkness) and chroma (degree of saturation) of the ornament were determined by matching the orange color of females to Munsell color chips; SLW performed all color matches under standardized light conditions following Weiss (2006). Each Munsell color chip is classified by separate measures of hue, value, and chroma. All reproductive females were matched to Munsell hue 10R but varied in both value (range 4.0–6.0) and chroma (range 10.0–16.0). Higher numbers for value and for chroma indicate lighter and more saturated color, respectively. Spectrometry shows that the female orange color is non-reflective in the UV spectrum (Weiss et al. 2012) and is similar in shape to that of the matching Munsell color chip (Weiss, unpublished data).
Immediately following color measurements, lizards were euthanized with 0.1 mL of 50 mg/mL pentobarbital solution. Euthanized lizards were then placed in glass jars, covered to the neck in hexane, and soaked for 12 h. Hexane was decanted into 32-mL storage vials and left to dry overnight in a fume hood. Vials were then weighed, wrapped in aluminum foil, and transported to the University of Puget Sound, Tacoma, WA, where they were stored at − 70 °C until analysis began in February 2013. Lipids collected from lizards captured on June 20 were not dried or weighed at SWRS due to time constraints. These samples were transported and stored with the others, then dried under reduced pressure via rotary evaporation at 45 °C in March 2013. Control samples (N = 6) of hexane subjected to the above procedure were prepared (on 29 June 2010), transported, and stored along with the lipid samples.
Preliminary analysis revealed that the skin lipids were primarily composed of triacylglycerides, the precise structures of which are hard to obtain from direct analysis; thus, samples were derivatized to allow for the identification of fatty acids within lipid samples using gas chromatography/mass spectrometry. An aliquot of lipid (too small to be accurately weighed) was scraped from storage vials with a metal spatula and dissolved in 0.2 mL toluene. 1.5 mL anhydrous methanol and 0.3 mL of 8% HCl in methanol were added (Ichihara and Fukubayashi 2010). The mixture was then heated to 120 °C for 10 min. This reaction breaks triacylglycerides into fatty acid methyl esters (FAMEs) and glycerol. FAMEs were then separated by adding 10 mL distilled water followed by 1 mL hexane and shaking in a separatory funnel. The hexane layer (FAME containing) was dried over sodium sulfate and concentrated to 200 μL under a stream of dry nitrogen before 50 μL MSTFA (N-methyl-N-trimethylsilyl-trifluoroacetamide) was added. This solution was then heated to 110 °C for 1 h. The final product was reduced to 100 μL under a stream of nitrogen before being analyzed immediately using GC/MS. Residue from control vials was subjected to this procedure as well. Samples from multiple individuals were never pooled. All chemical reagents and standards used were purchased from Sigma-Aldrich (St. Louis, MO) and used without further refinement or derivatization except when stated below. All reactions were heated in pressure vials using a microwave reactor (CEM Corporation, Matthews, NC).
Gas chromatography and mass spectrometry
Mean (± standard deviation) for the % TIC of each compound identified in the skin lipids from females of each reproductive state. Sample sizes for mean % are 7 (NR), 5 (V), and 9 (G) except when a peak was not found in all individuals of a given reproductive state; for these exceptions, n is shown in parentheses. For unidentified compounds, m/z of notable peaks are shown in parentheses
0.88 ± 0.18
0.52 ± 0.16
0.61 ± 0.16
32.96 ± 4.68
24.41 ± 6.41
28.97 ± 4.88
0.63 ± 0.07
0.54 ± 0.16
0.67 ± 0.15
Putative octadecadienoic acida
0.83 ± 0.53
0.48 ± 0.24
0.63 ± 0.18
2.84 ± 0.92
2.10 ± 0.77
2.67 ± 0.34
15.90 ± 3.31
13.24 ± 3.92
17.69 ± 2.76
2.58 ± 0.57
2.13 ± 0.54
2.95 ± 0.39
2.12 ± 0.94
1.21 ± 0.36
2.27 ± 0.79
0.66 ± 0.20
0.69 ± 0.22
0.61 ± 0.13
0.35 ± 0.05 (4)
0.37 ± 0.08 (3)
0.49 ± 0.10
13.02 ± 3.96
14.22 ± 6.56
14.24 ± 2.11
0.51 ± 0.23 (6)
0.50 ± 0.33
0.94 ± 0.19
Unidentified steroid (343, 367, 382, 395, 413, 457, 472)
0.93 ± 0.58
0.78 ± 0.67
1.34 ± 0.35
0.66 ± 0.42
1.05 ± 0.68
1.19 ± 0.28
Unidentified steroid (215, 305, 383, 398, 473, 488)
0.45 ± N/A (1)
0.65 ± 0.32 (4)
0.57 ± 0.14
Putative triacontanoic acida (367, 423, 466)
0.32 ± 0.08 (4)
0.24 ± 0.05 (2)
0.44 ± 0.13
Unidentified compound (393, 451, 494)
0.25 ± 0.11 (2)
0.40 ± 0.17
Skin lipids as indicators of receptivity
Eigenvalue, percent of variance explained, one-way ANOVA across reproductive state results, and variable loadings for the three PCs extracted. PCA includes compounds found in all three reproductive states
% of variance explained
F statistic (ANOVA)
Skin lipids as predictors of reproductive quality
Eigenvalues, percent of variance explained, and variable loadings for the five PCs used in multiple regression models. PCA includes only compounds found in V and G females
% of variance explained
Orange coloration as predictors of reproductive quality
To determine if orange coloration can predict the reproductive quality of reproductively mature (V and G) females, we used multivariate regression to determine if the measurements of female color (area, value, and chroma) are correlated with any phenotypic variables (Weiss 2006). NR females were excluded from this analysis as they do not possess color ornaments. Control variables identified above were included when they met the criteria described above. Variance inflation factors were calculated to determine that multicolinearity was not an issue with any model.
Skin lipid profile
We identified 17 compounds in the derivatized lipid samples (see Table 1). The three most prevalent compounds were hexadecanoic acid, octadecanoic acid, and cholesterol. The other compounds were identified as long-chain and very long-chain fatty acids (FA) ranging from 14 to 28 carbons in size. Two 18 carbon unsaturated FA were identified as octadecenoic acid and octadecadienoic acid. The sterols cholesterol and beta-sitosterol were identified along with two putative sterols of unknown structures. The structure of one compound remains unknown altogether.
Skin lipids as indicators of receptivity
Skin lipids as predictors of reproductive quality
Statistics for multiple linear regression models of skin lipid profile versus phenotype. Phenotype variables were predicted by multiple predictors simultaneously. Full model statistics (F) are shown alongside β coefficients for specific predictors. P values associated with each model statistic are shown in parentheses. Values in italics are significant at P < 0.05 level
Full model statistic
− 0.12 (0.38)
− 0.14 (0.74)
− 0.19 (0.82)
− 0.001 (0.99)
− 0.13 (0.44)
− 0.51 (0.13)
− 0.06 (0.86)
− 0.47 (0.86)
− 0.21 (0.78)
< 0.01 (0.71)
− 0.15 (0.22)
− 0.25 (0.16)
− 0.23 (0.30)
− 0.62 (0.58)
− 1.40 (0.29)
− 0.45 (0.81)
− 0.74 (0.74)
Average egg mass
10.91 (< 0.01)
− 0.01 (0.15)
− 0.01 (0.62)
− 0.001 (0.92)
− 0.02 (0.07)
− 0.01 (0.65)
− 0.13 (0.06)
− 0.08 (0.73)
− 0.01 (0.98)
Orange coloration as a predictor of reproductive quality
Statistics of multiple regression models comparing color ornaments to phenotype. Model statistics are shown in the same fashion as Table 4
Full model statistic
− 0.09 (0.80)
− 0.19 (0.18)
− 1.06 (0.40)
Average egg mass
8.30 (< 0.01)
− 0.01 (0.56)
− 0.01 (0.61)
− 0.15 (< 0.01)
− 0.92 (0.07)
− 0.37 (0.44)
1.61 (< 0.01)
All compounds identified in the skin lipids of S. virgatus females were previously identified in the skin lipids of female Iberian wall lizards Podarcis hispanica (Font et al. 2012). Although the identities of the compounds present in the skin lipids of these two species are similar, the relative proportions of these compounds differ substantially between them. For example, in P. hispanica, the most prevalent compound was octadecanoic acid (Font et al. 2012), whereas hexadecanoic acid was the primary component of S. virgatus skin lipids. One of the compounds identified in our samples (beta-sitosterol) is a phytosterol (Piironen et al. 2000). The presence of phytosterols in the skin of predatory reptiles has been documented before and thus our observation is not entirely unexpected (Ahern and Downing 1974; Weldon et al. 2008). Diet has been demonstrated to influence components of human skin lipids (Meinke et al. 2013) and this relationship may also exist for reptiles, but has yet to be directly investigated.
Some notable compounds were absent in the skin lipids of S. virgatus. For example, long-chain methyl ketones, which function as the attractiveness pheromone of red-sided garter snakes (Mason et al. 1989), were absent. Methyl ketones have also been identified in the skin lipids of the brown tree snake (Boiga irregularis; Jones et al. 1991), leopard gecko (Eublepharis macularius, Mason and Gutzke 1990), and Florida indigo snake (Drymarchon coarais; Ahern and Downing 1974). We also identified no squalenes or hydrocarbons in the skin lipids of S. virgatus. Hydrocarbons are a common component of reptilian skin lipids (Weldon et al. 2008) and the triterpene hydrocarbon, squalene, mediates sex recognition in the red-sided garter snake (Mason et al. 1989); this finding may be an artifact of our methodology, which was not equipped to quantify volatile compounds.
We found evidence that receptive V females possess less of an unidentified steroid in their skin lipids relative to non-receptive NR and G females. Given that a phytosterol (beta-sitosterol) was identified, it is possible that the unknown compound is also a plant sterol obtained via diet. Reproductive state is known to affect dietary behavior in captive S. virgatus, with V females eating more than G females (Weiss 2001), yet diet composition in the wild has not been examined. Given this, it is possible that reproduction-associated dietary shifts are the source of skin lipid variation. Furthermore, phytosterols have important physiological functions (Piironen et al. 2000) and diverting them to the skin to serve as pheromones may impose a cost, yet receptive (V) females do not bear this cost since they store lower levels of the compound in their skin lipids. Low levels of campesterol are known to be transported into the yolk of developing chicken eggs (Elkin 2007). A similar mechanism may be present here, whereby V females divert dietary sterols to their developing follicles, thus maintaining low skin-borne levels as an indicator of receptivity via physiological constraints. Future studies may wish to examine if NR and G females benefit from reduced male harassment via expression of chemical profiles indicative of their non-receptive state. Specific blends of triacylglycerides are known to function as suppressive sex pheromones in a species of desert-dwelling fruit fly (Chin et al. 2014). It is possible that triacylglycerides containing the fatty acids we identified may be performing a similar role; however, the precise arrangement of these fatty acids within triacylglycerides is likely important to their information content and thus must be determined before behavioral assays can confirm their signaling function.
We also found evidence linking octadecanoic acid and octadecenoic acid, a monounsaturated fatty acid, to female clutch size, a reliable metric for female phenotypic quality (Weiss 2006). Previous work has shown that scent marks (femoral pore secretions) deposited by male Carpetane wall lizards (Ibolacerta cyreni) are most attractive when they contain high levels of oleic acid ((Z)-9-octadecenoic acid; Mártin and López 2010). Contrary to the results of Mártin and López (2010), our results show that lower—not higher—levels of octadecanoic acid and octadecenoic acid correlate with higher quality phenotype. This is contradictory to theory which states that higher quality signals must be costly to produce, and the primary cost of chemical signals is diversion of compounds from metabolic functions (Mártin and López 2008). Future studies will wish to examine if in fact male S. virgatus will exhibit stronger chemosensory responses to skin lipids with lower levels of octadecenoic acid and octadecanoic acid. Should this be the case, it will also be necessary to investigate the costs of storing low levels of these compounds in skin lipids in order to understand how the honesty of this potential signal is maintained.
We found that both the levels of octadecenoic and octadecanoic acid in a female’s skin lipids and the chroma of her orange ornament correlate with her clutch size. This suggests that both chemical and visual cues in this species can potentially communicate the same information. These results fit with the “backup signals” hypothesis which states that multiple signals can remain stable when they enhance the accuracy by which the receiver assesses a single signal’s quality (Johnstone 1996). Our support for the backup signals hypothesis contradicts the notion that there is a trade-off between visual and chemical signaling in iguanid lizards (Hews et al. 2011) as we have shown that information transfer through a visual signal does not preclude the redundant use of chemical signals; however, our results do not conclusively rule out the possibility of a trade-off. Skin lipids and orange coloration do not correlate with each other despite both independently correlating with clutch size; this could be due to the correlations being driven by “visually signaling” and “chemically signaling” subsets of females, but may also be due to our small sample size.
It is also notable that our results differ from those of Weiss (2006) which found that both orange patch area and chroma correlated with a number of the phenotypic variables we analyzed here and did not correlate with clutch size. This may be the result of true annual variation in the information content of indicator traits (Chaine and Lyon 2008). Therefore, future studies may benefit from comparing female fitness correlates and male preference for female signals across years.
This study has laid the groundwork for a wide range of future studies. Most importantly, behavioral studies should be used to determine how variation in the skin lipid profile—both natural and experimental—influences the mate choice of males. Prior work typically focused on chemosensory responses to standards of compounds found in chemical ornaments (Mártin and López 2010). This is an effective method for determining which compounds in a mixture elicit chemosensory behaviors, yet studies linking response to natural variation in skin lipid composition are required to fully understand the information content and ecological roles of such complex chemical signals. Studies such as these will allow us to determine if female skin lipids are sexually selected chemical signals or simply signature mixtures that males learn to recognize (Wyatt 2014). A preliminary study on S. virgatus suggests that increasing the lipids on a female’s skin may reduce the interest of males (Gill, Goldberg, and Weiss, unpublished data), and future studies will further disentangle the relationship between chemical signal structure, female condition, and male behavior.
We thank Eric Scharrer and John Hanson for their help with chemical analysis, James Bernhard for statistical help, and Mark Martin for helpful comments on an early draft of the manuscript. We also thank all the staff and volunteers at the Southwestern Research Station.
Compliance with Ethical Standards
This work was conducted under Arizona Game and Fish scientific collecting permit SP603461 and with University of Puget Sound IACUC approval (F0708-01). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
- Alberts AC (1990) Chemical properties of femoral gland secretions in the desert iguana Dipsosaurus dorsalis. J Chem Ecol 16:13–25. https://doi.org/10.1007/BF01021264
- Carazo P, Font E, Desfilis E (2007) Chemosensory assessment of rival competitive ability and scent-mark function in a lizard, Podarcis hispanica. Anim Behav 74:895–902. https://doi.org/10.1016/j.anbehav.2007.02.011
- Chin JSR, Ellis SR, Pham HT, Blanksby SJ, Mori K, Koh QL, Etges WJ, Yew JY (2014) Sex-specific triacylglycerides are widely conserved in Drosophila and mediate mating behavior. ELife 3:e01751. https://doi.org/10.7554/eLife.01751
- Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B (2003) Cuticular hydrocarbons mediate discrimination of reproductives and nonreproductives in the ant Myrmecia gulosa. PNAS 100:10341–10346. https://doi.org/10.1073/pnas.1834281100
- Fritzche AK, Weiss SL (2012) Effect of signaler body size on the response of male striped plateau lizards (Sceloporus virgatus) to conspecific chemical cues. J Herp 46(1):79–84. https://doi.org/10.1670/10-166
- Gabriot M, Castilla AM, López P, Mártin J (2010) Differences in chemical signals may explain species recognition between an island lizard, Podarcis atrata, and related mainland lizards, P. hispanica. Biochem Syst Ecol 38:521–528. https://doi.org/10.1016/j.bse.2010.05.008
- Hews DK, Date P, Hara E, Castellano MJ (2011) Field presentation of male secretions alters social display in Sceloporus virgatus but not S. undulatus lizards. Behav Ecol Sociobiol 65:1403–1410. https://doi.org/10.1007/s00265-011-1150-1
- Houck LD (2009) Pheromone communication in amphibians and reptiles. Annu Rev Physiol 75:161–176. https://doi.org/10.1146/annurev.physiol.010908.163134 CrossRefGoogle Scholar
- Jones T, Fales H, Mulata Y, Yeh H, Pannell L, Mason RT (1991) New ketodienes from the integumental lipids of the guam brown tree snake, Boiga irregularis. J Nat Prod 54:233–240. https://doi.org/10.1021/np50073a024
- Mártin J, Civantos E, Amo L, López P (2007) Chemical ornaments of male lizards Psammodromus algirus may reveal their parasite load and health state to females. Behav Ecol Sociobiol 62:173–179. https://doi.org/10.1007/s00265-007-0451-x
- Mártin J, Ortega J, López P (2013) Lipophilic compounds in femoral secretions of male collared lizards, Crotaphytus bicinctores (Iguania, Crotaphytidae). Biochem Syst Ecol 47:5–10. https://doi.org/10.1016/j.bse.2012.09.025
- Mason RT, Gutzke WHN (1990) Sex recognition in the leopard gecko Eublepharis macularius (Sauria: Gekkonidae) possible mediation by skin-derivied semiochemicals. J Chem Ecol 16:27–36Google Scholar
- R Core Team (2012) R: language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Uhrig EJ, Lutterschmidt DI, Mason RT, LeMaster MP (2012) Pheromonal mediation of intraseasonal declines in the attractivity of female red-sided garter snakes, Thamnophis sirtalis parietalis. J Chem Ecol 38:71–80. https://doi.org/10.1007/s10886-011-0054-x
- Weiss SL (2001) The effect of reproduction on food intake of a sit-and-wait foraging lizards, Sceloporus virgatus. Herpetologica 57:138–146Google Scholar
- Weiss SL (2002) Reproductive signals of female lizards: pattern of trait expression and male response. Ethology 108: 793–813Google Scholar
- Weiss SL (2006) Female-specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behav Ecol 17:726–732. https://doi.org/10.1093/beheco/arl001
- Weiss SL, Kennedy EA, Bernhard JA (2009) Female-specific ornamentation predicts offspring quality in the striped plateau lizard, Sceloporus virgatus. Behav Ecol 20:1063–1071. https://doi.org/10.1093/beheco/arp098
- Wyatt TD (2014) Pheromones and Animal Behavior. 2nd edition. Cambridge University PressGoogle Scholar