Intra- and Inter-seasonal Variation in the Socio-Spatial Behavior of Adult Male Collared Lizards, Crotaphytus collaris (Reptilia, Crotaphytidae)

When individuals maintain strong inter‐seasonal philopatry to the same territories, males may be able to re‐establish territory occupancy without intense intra‐sexual aggression, and instead spend more time courting females early in the reproductive season. Furthermore, when some males have prior experience defending the same territories, it may be necessary for young males to exhibit higher levels of aggression because they are establishing a territory for the first time. We tested these hypotheses by examining within‐season (1992 and 1997) temporal variation in the social behavior of adult male collared lizards of known age and prior territorial experience in a population where inter‐season philopatry to territories is high. Contrary to expectations, the frequency of aggression exhibited by males with and without prior territorial experience did not differ. The frequency of intra‐sexual aggression was higher in 1992 than in 1997, perhaps because male competitors were more abundant in 1992. Although there was an interactive effect of year, male display and patrol were low at the beginning of the reproductive season in Apr. and May, reached peaks during midseason in June, and then decreased as reproduction ended in July. The size of territories showed a similar pattern, with males defending larger areas in June. Our data support the philopatry hypothesis in that the establishment of territories occurred without high levels of aggression early in the season, perhaps because territory boundaries have been well defined by high rates of patrol and advertisement during the middle of the previous season. Inter‐sexual interactions were most frequent in June rather than at the beginning of the reproductive season. Adult females are producing their second clutches and yearling females are producing their first clutches in June. The high rate of inter‐sexual encounters in June supports the hypothesis that males allocate more time to courtship when females are receptive because there are more reproductively active females at this time. The temporal pattern of activities in adult Crotaphytus collaris appears to function as a compromise between competing intra‐ and inter‐sexual social demands on males, allowing males to maximize mating opportunities as well as maintain future access to productive territories.     

Predation Cost of Conspicuous Male Coloration in Collared Lizards (Crotaphytus collaris): An Experimental Test Using Clay-Covered Model Lizards

Animal color patterns are a compromise between sexual selection pressures that increase advantages accrued from conspicuousness, and natural selection pressures that decrease those advantages through reduced survivorship. Predation pressure, as a mode of natural selection, often is invoked as a counter‐selective force to sexual selection, yet few studies have demonstrated empirically that more conspicuous individuals experience higher rates of predation. We quantified predator attacks on models of collared lizards, Crotaphytus collaris, in three well‐studied populations (Oklahoma, USA). These populations differ in coloration and in visual backgrounds against which the lizards are viewed by conspecifics and predators. Attack frequencies varied considerably among study sites but at all sites the models exhibiting the strongest color contrast with local rocks were detected and attacked most often. By comparison, inconspicuous models of females were never attacked at any of the sites. These results suggest a survival cost of conspicuous coloration in collared lizards, and reiterate the importance of considering the visual environment as well as differences among populations when examining the influence of predation on the evolution of animal color patterns.     

Femoral glands of the lizard, Crotaphytus collaris

The anatomy of the femoral glands in an iguanid lizard, Crotaphytus collaris collaris (Say), is described. The 48 lizards (including three embryos) from which glands were examined were obtained throughout their season of activity at one locality in Kansas. In animals of both sexes the glands lie in a linear series on the ventral aspect of each thigh. They are composed of branching tubes and tubules of epidermal and dermal origin. The row of femoral pores is the only external manifestation of the glands. Post hatching, the glands of males increase in size and complexity; little onto-genetic change occurs in the glands of females. The relative length of the glands appears to vary seasonally in adult males suggesting variation in their activity. The greatest relative sizes occur in the breeding season. At times a stratum corneum, continuous with the stratum corneum of the skin, occurs in the duct of the gland internal to part of the secretion plug. Formation of the stratum corneum seems to be initiated in the autumn prior to hibernation, and the stratum corneum removes the outer part of the secretion plug in the next ecdysis; meanwhile, production of a new secretion plug is initiated. The anatomy of the femoral glands in Crotaphytus is similar to that of the described glands of other species of lizards.     

Responses to Femoral Gland Secretions by Visually Adept Male and Female Collared Lizards

Although visually transmitted social signals are well documented in many diurnal iguanians, including collared lizards, secretory femoral glands also suggest a role of chemical signals in intraspecific communication. We conducted laboratory trials to test the extent to which male and female collared lizards responded by tongue‐flicking femoral gland secretions, neutral (water), and odoriferous (cologne) control substances, males distinguished self‐secretions from those produced by unfamiliar rival males, and females distinguish secretions from unfamiliar vs. familiar males. Both males and females spent similar amounts of time in four arena quadrants each with a Petri dish treated with one of the four test compounds. Males gave more tongue flicks/trial to secretions produced by unfamiliar rivals and cologne than they tongue‐flicked their own secretions and water. By contrast, the number of tongue flicks by females on control substances and familiar and unfamiliar males was similar. Results support the hypothesis that femoral gland secretions function in intrasexual signaling among male collared lizards, perhaps allowing them to distinguish unfamiliar rivals. Females tongue‐flicked secretions from familiar and unfamiliar males with similar frequency that was high relative to that of males, suggesting a possible role of secretions in assessment of males. Ours is the first evidence of a signaling role of femoral gland secretions in collared lizards and adds to a growing body of evidence that chemical signaling has evolved in diurnal lizards that also have highly developed visual‐based signaling.     

Interannual Variation in Timing of Parturition and Growth of Collared Pikas (Ochotona collaris) in the Southwest Yukon

The length of the snow-free season has a significant influenceon reproduction and growth in northern alpine environments,and these life history traits may provide sensitive indicatorsof the responses of organisms to climate change. We examinedgrowth rates and timing of parturition of collared pikas (Ochotonacollaris) from 1995–2002 in the Ruby Range, Yukon Territory,Canada. Growth rates were best described using a Gompertz model,in which the asymptotic mass, determined from the average maleand female weights, was 157 g, the growth rate constant (K)was 0.0557, and the age at inflection (I) was 18.12 days, fora birth weight of 10 g. The maximum growth rate for North Americanpikas (O. collaris and O. princeps) increased with latitude,with maximum growth rates being approximately one-third greaterin northern populations where the snow-free season is less thanthree months long. The mean parturition date varied significantlyamong years from 3 June to 3 July, and delayed parturition wascorrelated with indices of high snow accumulation and, to alesser extent, late spring snowmelt. However, parturition datedid not significantly affect the subsequent over-winter survivalof juveniles in this population, suggesting that pikas are ableto adjust to seasonal uncertainty associated with highly variablespring conditions.     

Oviductal morphology and egg shelling in the oviparous lizards Crotaphytus collaris and Eumeces obsoletus

Morphological changes occurring in the oviduct and epithelial cells of the lizards Crotaphytus collaris and Eumeces obsoletus during the natural reproductive cycle were examined and quantified. Additionally, development of the eggshell at different stages of gravidity was described. The anterior uterus of each species has a distinct glandular type which differs between species: in E. obsoletus, the glands are tubular and in C. collaris, branched saccular. The branched saccular glands in the anterior uterus of C. collaris produce collagen-like material that forms the fibers of the shell membranes. However, fibers from the eggshell of E. obsoletus did not stain for collagen. The shell of both species is composed of a multilayered inner boundary covered externally by fibers of varying thickness. Initial layers are composed of thick fibers all lying along the same general axis. Outer layers of fibers are progressively thinner and an external surface layer composed of glycosaminoglycans (GAGs) is also present. In C. collaris, calcium, which is deposited in relatively small amounts on the shell surface, appears to be secreted by the epithelium of the anterior uterus. The nonciliated secretory epithelial cells covering the villi-like folds of the posterior infundibulum secrete GAGs. Epithelial cell height of the infundibular villi is greatest during early gravidity. A functional relationship may exist between luteal activity and oviductal secretory activity because the activity of the glandular epithelium varied as gravidity progressed.     

Discrimination of chemical stimuli in conspecific fecal pellets by a visually adept iguanid lizard,Crotaphytus collaris

Iguanid lizards are known for visual acuity and a diminished vomeronasal organ, which has led to mixed conclusions on whether iguanids use chemical cues. The collared lizard, Crotaphytus collaris, is a territorial iguanid that lives in open rocky habitats. Fecal pellets placed prominently on open rocky perches may provide an ideal mechanism for intraspecific chemical signaling. In order to determine whether collared lizards can discriminate between chemical stimuli found in conspecific fecal pellets, we collected 24 males and 25 females to analyze sex-specific behavioral responses via tongue-flicks and a newly observed behavior for the species, gular pumps, to cotton swabs containing water, cologne, chemical stimuli from conspecific male and female fecal pellets, and the lizard’s own fecal pellet. Both sexes were able to discriminate chemical stimuli from water via at least one behavior. Male collared lizards exhibited greater rates of response (tongue-flick and gular pumps) toward male fecal pellets when compared to the negative water control. Our results also suggest individuals may be able to discriminate between fecal pellets, as indicated by generally greater (but non-significant) counts of male tongue-flick responses to male fecal pellets when compared to their own. Collared lizard chemical discrimination appears to utilize tongue-flick and gular pump behaviors, possibly associated with distinct chemosensory modes (vomerolfaction and olfaction). Based on this study, we suggest that chemical signals may play a greater role in intraspecific communication than previously thought in this highly visual lizard.     

Isolation and characterization of 11 polymorphic microsatellite loci in collared lizards (Crotaphytus collaris)

We identified 11 polymorphic microsatellite loci in collared lizards (Crotaphytus collaris). Polymorphism assessment in 512 individuals from 52 populations sampled across much of the species distribution revealed a fairly high degree of genetic diversity (six to 20 alleles per locus) and a wide range of average expected heterozygosity values (0.143–0.530). We found no evidence for linkage, very few deviations from HW expectation (two of 572 possible population/locus analyses) and thus no evidence for null alleles. There was a tendency for reduced polymorphism towards the northern periphery.     

Luteal morphology, atresia, and plasma progesterone concentrations during the reproductive cycle of two oviparous lizards, Crotaphytus collaris and Eumeces obsoletus

From ovulation to oviposition, the corpora lutea of the oviparous lizards Crotaphytus collaris and Eumeces obsoletus exhibit three stages of luteal development: 1) luteogenesis, 2) luteal maturity, and 3) luteal regression. Each stage exhibits distinct characteristics, involving changes in: 1) luteal volume, 2) nuclear diameter of cells within the luteal cell mass, and 3) thecal development. Plasma progesterone concentration is greatest during luteogenesis and is positively correlated with ovarian atresia, although atresia occurred throughout the period of gravidity. These data suggest that in these two species, the corpora lutea secrete high amounts of progesterone immediately following ovulation and exhibit morphologically distinct stages of growth and regression.     

Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris)

In territorial polygynous taxa, reproductive success reflects phenotypic variation. Using Crotaphytus collaris, a sexually dimorphic lizard in which males use the head (i.e., jaws and associated musculature) as a weapon when territorial interactions escalate to fights, we tested the hypothesis that weapon performance (i.e., bite force) is a better predictor of fitness than body or weapon size. Bite-force performance predicted the number of female home ranges overlapped, estimated mating success, and potential reproductive output. However, no body or weapon size measure correlated with these estimates of fitness, and only one weapon dimension (head width) correlated with bite force. These results indicate that weapon performance has far stronger effects on fitness than body or weapon size, likely because it directly influences fight outcomes. As such, it is desirable that the use of morphology as a proxy for performance and its presumed extensions to fitness be based on empirical morphology-performance relationships.     

Male collared lizards,Crotaphytus collaris (Sauria: Crotaphytidae), signal females by broadcasting visual displays

The signalling function of displays broadcast when animals are distant from conspecifics can be difficult to determine. I tested the extent to which visually transmitted broadcast displays given by free‐ranging territorial male collared lizards signalled same‐sex rivals or females. One test involved recording the frequency of broadcast displays, aggressive contests with rivals, and courtship encounters with females during ten reproductive seasons when local sex ratios varied markedly. The frequency of broadcast displays decreased as the ratio of male competitors to females increased. The frequency with which males initiated contests with rivals was not related to the ratio of competitors to females, whereas the frequency of courtship interactions decreased with sex ratio because there were fewer females to court. The behaviour of males that defended territories during two successive seasons showed a similar pattern. Broadcast display frequency was positively correlated with courtship frequency, but not with the frequency of contests with rivals. Lastly, individual males gave more broadcast displays during focal observations when they also engaged in courtship encounters with females than other observations when they engaged in aggressive conflicts with rival males. Although these results do not reject the possibility that broadcast displays may also signal male rivals, they support a major role of these displays in advertisement to females. © 2013 The Linnean Society of London     

Testing the adaptive significance of sex‐specific mating tactics in collared lizards (Crotaphytus collaris)

We tested whether territorial defence is adaptive in male collared lizards by examining the extent to which territory owners monopolize females. We also tested whether females benefit by mating with multiple males using alternative tactics when local sex ratios varied. Surprisingly, neither the number of offspring that males sired, nor the number of females that males mated with varied as a consequence of highly variable local sex ratios. Moreover, both the number of offspring sired and the number of female mates were independent of male social status. Courtship frequency was under positive directional sexual selection for mating success for territorial males. None of the phenotypic traits that we examined were targets of sexual selection in nonterritorial males. Although offspring survivorship decreased with the degree of multiple mating, females mated multiply with similar numbers of territorial and nonterritorial males during all three seasons. Females did not obtain material or genetic benefits that balanced the apparent offspring survival cost imposed by mating with multiple males. Instead, females appeared to be ‘making the best of a bad job’, perhaps because the abundance of hiding places used by subordinate males makes it difficult for females to avoid male harassment. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 423–436.     

Changes in oviducal vascularity during the reproductive cycle of three oviparous lizards (Eumeces obsoletus, Sceloporus undulatus and Crotaphytus collaris)

Histologically derived estimates and ink suspension vascular casts were used to examine oviducal vascular changes. Vascularity peaked during gravidity and was correlated with maximal plasma progesterone concentrations. The vascular increase in the oviducal tissue was attributed exclusively to increased capillary densities. The greatest change occurred in the anterior uterus where incubation and egg shell secretion occur. Similar patterns of change in vascularity occurred in the infundibulum, although not as extreme as that seen in the anterior uterus, whereas no significant alterations were noted in the posterior uterus. These modifications mimic the pattern of vascular change occurring in viviparous lizards during simple placentation. We suggest that major changes in uterine vascularity may not be required for the evolution of simple chorioallantoic placentae in lizards.     

Capital energy drives production of multiple clutches whereas income energy fuels growth in female collared lizards Crotaphytus collaris

Animals invest energy in reproduction that is obtained at two distinct times relative to the reproductive cycle. Energy obtained during egg production is referred to as income energy whereas stored energy acquired prior to reproduction is capital energy. Similar to most ectotherms, squamate reptiles are generally hypothesized to be capital breeders. Nearly all squamates in which income/capital energy investment has been examined thus far produce only one clutch per reproductive season. Although it is likely that squamates producing multiple seasonal clutches fuel first clutches with capital energy, either capital or income energy may be used to produce later clutches. We first monitored female eastern collared lizards over 14 reproductive seasons to confirm that the number of clutches females produce seasonally is a plastic response to variable environmental parameters, and to examine the effects of female body condition at the beginning of the reproductive season on clutch production. Clutch production varied annually and both the size and number of clutches were positively correlated with body condition. We then tested the competing predictions of the income and capital hypotheses experimentally by supplementing the diets of female collared lizards in situ for one season. Diet‐supplementation had no effect on the number of clutches produced but increased growth rates of gravid females. We further tested the competing predictions of these two hypotheses by examining variation in maternal energy investment per clutch using preserved specimens collected near our primary field site. Clutch size was highly correlated with female body size. Together, our results suggest that variation in reproductive output by female collared lizards is linked to stored capital energy rather than income energy, similar to most ectotherms.     

Influence of Age and Prior Experience on Territorial Behavior and the Costs of Defense in Male Collared Lizards

In polygynous species where males maintain strong interseasonal philopatry to the same breeding territories, older individuals have prior experience defending their areas, whereas younger individuals are defending a territory for the first time. Theoretical and empirical studies predict that under such conditions the cumulative costs of defense may be lower for older experienced males as a consequence of familiarity with environmental and/or social conditions in their particular local habitats. We used quantitative data from focal observational studies and introduction experiments to test the hypothesis that older collared lizard males (Crotaphytus collaris) with prior territorial experience (3 yr+ males) acquire larger territories allowing them to court more, different females, with greater frequency without incurring higher defense costs. Consistent with this hypothesis, 3 yr+ males controlled significantly larger territories and courted more females, without having significantly higher rates of territory patrol, frequencies of advertisement display, or aggressive interactions with same‐sex competitors. Moreover, the intensity of responses to size‐ and age/experience‐matched tethered intruders by 3 yr+ males was lower than that by 2 yr males in their first season of territory defense. Our results support the hypothesis that age/prior occupancy of territories lowers defense costs allowing males to defend larger areas and increase opportunities to court females, perhaps increasing mating opportunities. By contrast, 2 yr males may need to respond more aggressively to intruders because their ownership of territories is tenuous as a consequence of shorter territory occupancy.     

Sexual dichromatism and differential conspicuousness in two populations of the common collared lizard (Crotaphytus collaris) from Utah and New Mexico, USA

The common collared lizard (Crotaphytus collaris) exhibits considerable geographical colour variation, particularly among males. Populations of this diurnal saxicolous iguanian inhabit patches of rocky habitat throughout the species’ broad distribution in North America and are anticipated to experience local differences in selective pressures that influence colouration. Specifically, while social interactions might favour conspicuous colouration, crypsis may be advantageous in interactions with visually orienting predator and prey species. To address the local relationship between lizard and substrate colouration we compared the reflectance spectra of two geographically distant and phenotypically divergent populations of collared lizards with the rocky substrates they inhabit. Our northern study population (C. c. auriceps in eastern Utah) occurs on red rocks, where males exhibit boldly coloured turquoise bodies and bright yellow heads. In contrast, our southern study population (C. c. fuscus in southern New Mexico) lives on grey and tan rocks, and males in this location exhibit subdued brown and tan dorsal colours. Spectral comparisons revealed that males in the northern population contrasted strongly with their local rocks, whereas males in the southern population matched their rock colours with reasonably good fidelity. This relationship held under a variety of lighting conditions. Females in both populations were less conspicuously coloured than males, although northern females contrasted more with their rocks than did southern females. In addition, sexual dichromatism was pronounced in the northern population but minimal in the southern population. Finally, sexual size and weight dimorphism was strong in the southern population while being virtually absent in the northern population. A comparison of the local predator and prey assemblages suggests that the conspicuous and sexually dichromatic colouration of the northern population may have evolved in response to reduced pressure from visually orienting predators as well as reduced dependence on saurian prey. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77 , 67–85