Live fast and prosper: early territory defence is not costly in male collared lizards (Crotaphytus collaris)

Live fast and prosper: early territory defence is not costly in male collared lizards... Abstract Males often exhibit subordinate social tactics and grow at high rates when young, but changes in local social conditions may accelerate opportunities to acquire dominant territorial social status. Early territory defence, however, might trade off high energetic costs of advertisement and aggression against requirements for growth; therefore, the accelerated acquisition of dominant social status might carry prohibitive evolutionary costs. I tested this hypothesis by recording data on social behaviour and life-history traits in male collared lizards that acquired territories during their first season with those that remained non-territorial. I used principal components analysis (PCA) to synthesize these variables while controlling for male body size. Principal components analysis revealed four axes that summarized 89.4% of the total variance among males. As expected, first-year males that ascended to territorial status early had higher PCA scores on a social advertisement axis that included behaviour traits demanding expenditure of energy. Surprisingly, energetic investment in advertisement did not reduce male scores on a life-history PCA axis that included rates of growth, foraging and lifespan. My results indicate that accelerated territory acquisition did not impose long-term costs, suggesting that it might be an adaptive ontogenetic option for males in this population of collared lizards. INTRODUCTION Territory defence is favoured by natural selection when the benefits accrued through access to resources exceed the cumulative costs of repelling competitors (Davies & Houston, 1984; Stamps, 1994; Moore et al., 2014). Males, in particular, defend territories to access females and increase mating success (Trivers, 1972; Emlen & Oring, 1977). Defence of breeding territories, however, is likely also to impose one or more costs, which can include reduced foraging (Peres, 1989) and decreased time available to interact with females (Pryke, 1979; Nolet & Rosell, 1994; Baird, Sloan & Timanus, 2001; Eason & Switzer, 2004). Increased energy expenditure on advertisement and aggression may also reduce rates of growth (Godfrey, 2003; Amsler, 2010) and, perhaps, decrease survival (Marler & Moore, 1989; Marler et al., 1995). Territory defence may also increase predation risk if advertisement displays render males conspicuous (Magnhagen, 1991; Amsler, 2010; Catano et al., 2015). In many vertebrates, including some lizards, variation in the ability of individual males to repel same-sex competitors (i.e. resource holding power, RHP; Parker, 1974) is hypothesized to play a major role in determining the ontogenetic schedule (age) at which males attempt to defend territories (Calsbeek & Sinervo, 2002; Baird, 2013a). Male RHP can be influenced by numerous phenotypic factors, including morphological (e.g. body size, coloration), behavioural (e.g. display frequency, intensity) and performance (e.g. strength, speed) attributes (Hardy & Briffa, 2013). Such traits typically increase as males age, making it advantageous for young males to delay attempts to acquire territories until they attain sufficient RHP that energy investment in contest competition is cost effective (LeBoeuf, 1974; Baird & Curtis, 2010). During the interim, even though they are sexually mature, it is common for smaller males to allocate maximal energy to growth by avoiding confrontations with territory owners and using stealth tactics to interact with females (Kwiatkowski & Sullivan, 2002; Wikelski et al., 2005; Baird, 2008; York & Baird, 2015). Males then switch to dominant social tactics later, when they can compete effectively using aggression (e.g. Wikelski et al., 2005; Baird & Curtis, 2010; Baird, Baird & Shine, 2012). As males that control territories typically display strong philopatry, the ability of individuals to defend a particular space will probably depend on their RHP relative to that of rivals within local neighbourhoods (Zamudio & Sinervo, 2003). Dynamic ecological parameters within each local social milieu, therefore, will almost certainly play an important role in determining the age at which individual males may have opportunities to ascend successfully to territorial social status (Baird & Curtis, 2010). Mortality of established territory owners during or after the reproductive season sometimes provides opportunities for males to acquire territories early, instead of delaying territory acquisition (Baird & Curtis, 2010). Adopting territorial tactics earlier may result in a trade-off between the high energetic demands of defence and investments in rapid growth, which may decrease body condition (Metcalfe & Monoghan, 2001) and perhaps survival (Marler & Moore, 1989; Marler et al., 1995). The potential trade-off between energy allocation to growth vs. territory defense when males are young therefore prompts the question of whether or not accelerated acquisition of territories is an adaptive ontogenetic tactic for individual males. I addressed this question using longitudinal demographic and behavioural data on male collared lizards (Crotaphytus collaris), which allowed comparison of fitness correlates in individuals that adopted territorial social tactics during their first season with those that delayed territory acquisition. Longitudinal studies since 1990 have shown that, although collared lizard males attain sexual maturity at the beginning of their first spring, they usually delay efforts to defend territories throughout this first season (Baird & Timanus, 1998; Baird, Timanus & Sloan, 2003; York & Baird, 2015). The social tactics of first-year males, however, are conditional upon the presence or absence of older, larger territorial males. Mortality of territorial males from predation or winter kill sometimes allows first-year males to establish territories, which is exemplified by their abruptly increasing rates of travel, advertisement displays and aggression (Baird & Hews, 2007; Baird & Curtis, 2010). Opportunities for first-year males to acquire territories increased in my study population beginning in 2008 and continued through 2013. The 2007 cohort of territorial males was particularly old, such that many died that winter. Also, additional suitable lizard habitat was constructed for flood control in the winter of 2008 and colonized by lizards beginning in the spring of that year. I used these opportunities to test the influence of early territory acquisition on variables that might be related to fitness by comparing body size and condition at the beginning of the season, growth rate and lifespan in males that established and defended territories during their first activity season vs. those that maintained non-territorial tactics throughout their first season. Given that territorial activities might also influence the effectiveness of sit-and-wait foraging tactics that collared lizards use (Baird, 2008), I also compared frequencies of foraging strikes by first-year males that adopted these two social ontogenies to assess the potential trade-off with foraging. MATERIAL AND METHODS Study population This research was conducted at the Arcadia Lake Dam flood control spillway (hereafter AL), 9.6 km east of Edmond, OK (35°39′, −97°21′), where I have studied collared lizards during each adult (from 20 March to 30 July) and juvenile (from late July to 15 October) activity season from 1990 to the present (Baird, 2013b). Study subjects were permanently marked soon after hatching as neonates using unique toe-clip combinations, and for identification from a distance by applying coloured paint dots (acrylic) to the dorsum. Lizard subjects occupied five patches of granite rocks or broken concrete slab used to construct flood control/drainage channels. These habitat patches are mapped to scale using GIS measurements (± 1 m) of markers arranged in grids. As individuals maintain strong philopatry to home ranges and territories, this homogeneous substratum promotes observation of lizard behaviour and survival, and recapture of known lizards to monitor growth rates (Baird, 2013b). Males attain sexual maturity during their first season at 70–75 mm snout-to-vent length (SVL), as indicated by presence of mature spermatozoa in smears from extruded hemipenes (Baird & Timanus, 1998; Baird, 2013b). Males that survive their first season typically live 2–3 years, although maximal recorded male lifespan in this population is six seasons (T. A. Baird, unpublished data). Male growth rate, body condition and lifespan Beginning with the first capture of hatchlings and then repeatedly at each recapture, I measured male SVL (± 1 mm) and total body mass (± 0.5 g) and recorded capture location on scale-drawn maps (Baird, 2013b). The growth rate of each male subject during the first reproductive season was calculated as the change in SVL from the first (20 April–1 May) to last (1–15 July) capture up to the end of the reproductive season (15 July) divided by the number of days separating those measurements. I used the residuals from a regression of log10 body mass on log10 SVL to estimate male body condition, as in other lizard studies involving species having body shapes similar to collared lizards (López & Martín, 2002; Warner et al., 2008; Cox et al., 2010). Advertisement and aggressive activities by males diminish significantly after females have laid their last clutches of the season (Baird et al., 2001). Therefore, for first-year males that survived beyond the end of reproduction, I also recorded both SVL and body mass from 15 July until 31 August to determine post-reproductive growth rate. I determined male lifespan as reproductively mature adults to the nearest 0.5 months by determining the presence or absence of individuals during recaptures, censuses and focal observations (described below) throughout the first and subsequent adult activity seasons (from 20 April to 31 August). For lizards that survived into one or more subsequent seasons, I included the interim months of inactivity in estimates of total lifespan. Males were considered to have died during the activity season when they were abruptly and repeatedly absent from their previous home ranges/territories and not sighted elsewhere throughout the study site. Given that adult males emerged from hibernacula during the last 2 weeks of March, the maximal number of months survived during the first adult activity season was 9.5 (15 March to December), whereas the maximum for all subsequent years was 12 months. Male social and foraging behaviour I recorded behavioural data on a total of 155 sexually mature males from 1998 to 2004 and from 2008 to 2013, during their first activity season as adults (hereafter first-year males). In 1998–2004, many of the first-year males present on the site were involved in other experiments (Baird & Hews, 2007; Baird, 2008, 2009; Baird & Curtis, 2010). Therefore, for the present study, I limited my observations during these seasons to only males that were not involved in other studies. Throughout the 2008–2013 seasons, all data collection on first-year males was focused on the present study. I recorded two types of socio-spatial data by conducting censuses and focal observations throughout May and June, which is the collared lizard reproductive season in central Oklahoma (Baird, 2013b). Censuses involved recording the locations of all emergent marked lizards on maps at least four times per week, and capturing those that had moulted for repainting and measurement. I recorded focal observations (sensuAltmann, 1974) on first-year males throughout this 2 month period as long as they survived or until a maximum of 15 observations (20 min on separate days) were recorded (range = 5−15). I recorded only one focal observation per day on individual males, and observations were recorded at randomized times from 09.00 to 13.00 h when substrate temperature was optimal (30–38 °C) for lizard activity (Baird et al., 2001). The number of focal observations per male varied because it was common for first-year males to die of natural causes before the end of their first reproductive season. The cause of mortality was most likely to be predation, because each season we have witnessed near-miss attacks by raptors (Ictinia) and snakes (Masticophis) and four predation events by roadrunners (Geococcyx). Previous studies have demonstrated that five focal observations per individual recorded on separate days provide an accurate estimate of male display and travel rates (Baird & Hews, 2007; York & Baird, 2015), the two most important variables for distinguishing male social status in this population (see next paragraph). Neither variable was correlated with the number of focal observations per individual in either territorial or non-territorial males (F-values = 0.03–1.81; P-values = 0.18–0.87). During focal observations, I recorded the paths of travel and all social behaviour patterns that focal male subjects initiated (described below) on scale-drawn maps (Baird et al., 2003; Baird, 2013b). Territorial vs. non-territorial male social tactics are readily distinguished in AL collared lizards by marked differences in rates of travel and the frequencies with which individuals perform broadcast displays (York & Baird, 2015, 2017). I determined the rate of travel (in metres per hour) by using a digital planimeter (Planix 2000) to measure mapped traces recorded during focal observations, and dividing the cumulative distance travelled by the total observation time on each male. Broadcast displays are stereotypical movements performed when focal males are ≥ 5 m from the nearest conspecific of either sex (Baird & Curtis, 2010; Baird, 2013c; York & Baird, 2015). Most displays involve extension of all four legs to elevate the laterally compressed torso while the dewlap is extended (full shows), and flexion of the legs, which raises and lowers the head and torso, one to 12 times (= push-ups) in succession (Baird, 2013c). Broadcast displays also occasionally involve males walking stereotypically in a tight circular or figure-eight pattern while remaining on a single elevated perch (Baird et al., 2003; Baird, 2013c; York & Baird, 2015). I determined the frequency of broadcast displays per hour for each male by dividing the total number of displays given by the total observation time on each individual. First-year males classified as territorial vs. non-territorial had travel and broadcast display frequencies similar to those recorded during other studies of male behaviour in this population (Baird & Curtis, 2010; York & Baird, 2015). The subordinate social status of most non-territorial males was confirmed by their fleeing and hiding when approached by territory owners independent of their age. Collared lizard foraging acts were also readily recorded during focal observations. Lizards scan for prey by sitting motionless on rock perches at the grass–rock interface, with their heads elevated to inspect for approaching arthropods. When prey approach to ≤ 3 m, lizards descend their perches and begin walking slowly towards prey while crouching, or making a sudden forward lunge/chase (= strikes) in an attempt to capture prey in the mouth (Baird, 2008). I calculated the number of foraging acts per hour by dividing the number of strikes by the total observation time on each male subject. Statistical analyses Variation in the body size of males at the beginning of their first reproductive season, as well annual variation (year), might influence the results of comparisons between first-year males that displayed territorial tactics (N = 80) vs. those that remained non-territorial (N = 75). I used general linear models (GLM) to test the influence of both variables on all dependent behavioural and life-history variables. There was no significant effect of year on any of the dependent variables, and male SVL influenced only growth rate during the reproductive season (see Results). Therefore, I included male SVL as a covariate in a principal components analysis (PCA) used to synthesize variation in six dependent variables [broadcast displays per hour, travel rate (in metres per hour), growth rate (in millimetres per day), foraging acts per hour, lifespan (in months), and estimated body condition] in first-year males that adopted early territorial tactics vs. those that remained non-territorial. I then compared the scores of individual males on significant PCA factors using two-sample t-tests when data met the assumptions of parametric tests and Wilcoxon rank-sum tests when data did not meet these assumptions despite log10 transformation (see also Baird et al., 2007). I used two-sample t-tests to examine the influence of social ontogeny on post-reproductive growth rates in the subset of males (total N = 64) that survived beyond the end of reproduction (10 July) to the end of the activity season (30 August), and lifespan (in months) in the subset of males (N = 58) that survived their first winter. Ethical note All procedures involving live lizards were approved by the Institutional Animal Care and Use Committee of the University of Central Oklahoma (IACUC permit number 13009) and the Oklahoma Department of Wildlife (permit number 5553). I have conducted longitudinal studies on lizard behaviour, growth and survival in this population for > 25 seasons. These studies have involved capturing hatchling lizards by noose, clipping the terminal phalanges of three digits for permanent identification, applying non-toxic acrylic paint for identification of individuals from a distance, palpating female abdomens to monitor reproduction and recording morphometric measurements to determine growth rates. Normal locomotory, foraging and thermoregulatory behaviour together with very rapid growth in hundreds of toe-clipped hatchlings have confirmed that these techniques do not harm collared lizards (Baird, 2013b). RESULTS Principal components analysis identified four factors that individually explained ≥ 12% and collectively explained 84.9% of the total variance in the behavioural and life-history parameters of 155 first-year males. Rates of travel and frequency of broadcast displays loaded highest on factor 1 (advertisement), which explained 33.9% of the variance (Table 1). Three likely life-history correlates of fitness, foraging and growth rates, and lifespan loaded highest on factor 2 (life history), which explained 20.8% of the total variance. Only body condition loaded highest on factor 3 (17.7% of variance), but the loading was negative, indicating low body condition estimates. Positive body condition loaded alone on factor 4, which explained 12.5% of the total variance (Table 1). Scores for first-year males that acquired territories were higher on the advertisement (z – normal approximation154 = 9.10, P < 0.0001) and negative body condition axes (z154 = 3.18, P = 0.0018) than scores for first-year males that remained non-territorial (Table 2). Territorial and non-territorial males had similar scores on both the life-history (t154 = 0.56, P = 0.58) and positive body condition axes (t154 = 0.29, P = 0.77; Table 2). Table 1. Principal component analysis factor loadings for behavioural and life-historical variables in all first-year males (N = 155) Variable  Principal component analysis factor  1  2  3  4  Travel (m/h)  0.620  0.052  0.245  −0.121  Broadcast displays/h  0.613  0.140  0.210  −0.063  Growth rate (mm/day)  −0.384  0.468  −0.001  −0.220  Lifespan (months)  −0.027  0.676  0.289  0.623  Body condition  0.252  −0.046  −0.752  0.525  Foraging acts/h  0.167  0.547  −0.487  −0.515  Percentage of variance explained  33.9  20.8  17.7  12.5  Variable  Principal component analysis factor  1  2  3  4  Travel (m/h)  0.620  0.052  0.245  −0.121  Broadcast displays/h  0.613  0.140  0.210  −0.063  Growth rate (mm/day)  −0.384  0.468  −0.001  −0.220  Lifespan (months)  −0.027  0.676  0.289  0.623  Body condition  0.252  −0.046  −0.752  0.525  Foraging acts/h  0.167  0.547  −0.487  −0.515  Percentage of variance explained  33.9  20.8  17.7  12.5  Highest positive loadings are indicated using boldface font. View Large Table 2. Comparison of principal component analysis factor scores for males that acquired territories during their first season vs. those that remained non-territorial throughout their first seasons Principal component analysis axis  Territorial males    Non-territorial males  (N = 80)    (N = 75)  Advertisement  0.094 (0.016)  *  −0.113 (0.069)  Life history  0.009 (0.013)  NS  −0.002 (0.015)  Negative body condition  0.025 (0.013)  *  −0.030 (0.011)  Positive body condition  −0.003 (0.010)  NS  0.002 (0.011)  Principal component analysis axis  Territorial males    Non-territorial males  (N = 80)    (N = 75)  Advertisement  0.094 (0.016)  *  −0.113 (0.069)  Life history  0.009 (0.013)  NS  −0.002 (0.015)  Negative body condition  0.025 (0.013)  *  −0.030 (0.011)  Positive body condition  −0.003 (0.010)  NS  0.002 (0.011)  Data are mean factor scores (± 1.0 SE). Asterisks indicate significant differences (0.0001) between means of territorial vs. non-territorial males. NS denotes not significant. View Large For the 64 males that survived past the end of reproduction until at least 31 August, post-reproduction growth rates of subjects that had defended territories during the reproductive season (mean mm/day ± 1.0 SE = 0.19 ± 0.02) and those that had remained non-territorial (0.22 ± 0.02) were similar (t63 = 1.30, P = 0.20). For the 58 males that survived their first winter, lifespan of those that had defended territories (mean months ± 1.0 SE = 18.9 ± 2.4) and those that had remained non-territorial (20.1 ± 1.6) was also similar (t57 = 0.43, P = 0.67). DISCUSSION As expected, social variables associated with territorial advertisement (patrol and broadcast display) loaded together on the advertisement PCA axis that explained the most variation among first-year males, and scores for males that acquired territories during their first seasons were higher than those for males that remained non-territorial. It is surprising that accelerated territorial activities did not reduce scores on the life-history PCA axis that best synthesized male growth rates, foraging rates and lifespan. Increased travel is intuitively expected to diminish the energy that can be allocated to growth, and more frequent broadcast display would seem to increase conspicuousness to predators. The finding of similar foraging rates in collared lizard males that increased territorial activities is also counter to findings of other studies (Peres, 1989; Amsler, 2010). Increased travel would seem to detract from the ability of males to wait motionless on perches to locate and ambush prey (Baird, 2008), but similar foraging scores suggest that territory acquisition did not decrease foraging opportunities in male collared lizards. Increased travel and scanning for shorter periods from different vantage points is also apparently an effective foraging tactic, perhaps because it increases encounters with prey. First-year males that acquired territories early and those that remained non-territorial also had similar growth rates after reproduction ceased and had similar lifespan in analyses of all males and only those that survived their first winter. Together, these results suggest that diverting energy to increased travel and display to promote early territory acquisition during the first season did not impose a fitness cost for these individuals. There appear to be almost no other longitudinal studies of free-living vertebrates where males vary in the ontogenetic schedules of alternative social tactics that can be used for comparison of the fitness impact with that in collared lizards. My results showing insignificant effects on growth and survival differ markedly from findings of field studies on another iguanian lizard, Sceloporus jarrovi, in which heightened territorial behaviour decreased male survival (Marler & Moore, 1989; Marler et al., 1995). These opposing results might be a consequence of an important difference in experimental design. Increased aggression in S. jarrovi males was induced before the reproductive season by supplementing circulating testosterone concentrations (Marler & Moore, 1989; Marler et al., 1995). In contrast, the collared lizard males that adopted territorial tactics did so of their own volition during the natural reproductive season. Males that sought territorial social status early were larger (SVL), which might indicate a positive relationship between accelerated territory acquisition and RHP, specifically the ability of males to sustain heightened energetic costs. Nevertheless, the observed pattern of loadings on PCA factors related to body condition did not support this hypothesis. Scores on the positive body condition axis (factor 4) were similar in territorial vs. non-territorial males, whereas males that adopted territorial tactics had higher scores on the negative body condition axis (factor 3). My sampling did not allow determination of whether non-surviving first-year males (59% territorial, 75% non-territorial) were taken by predators before they entered hibernacula or died over the winter because of insufficient energy storage. A previous study (Baird, 2009) revealed almost no mortality of first-year collared lizard males during the reproductive season, suggesting little predation even though one experimental group was painted brightly to increase visual conspicuousness to potential predators (Baird, 2009). This result, coupled with those of the present study showing that neither body condition nor post-reproductive growth rate was impacted by early territory acquisition, suggests that variation in survival while burrowed over the winter is a significant factor influencing total lifespan. Similar to results on collared lizards, decreased survival in male S. jarrovi also appeared to be a consequence of energy deficits instead of predation (Marler & Moore, 1989; Marler et al., 1995). There also appear to be few, if any, empirical field measurements of total lifespan in relationship to different age-specific social ontogenies such as those displayed by male collared lizards, even though lifespan is obviously related to fitness in iteroparous species. Once they establish territory occupancy, male collared lizards defend their areas for life, apparently at a reduced cost owing to ‘dear-enemy’ effects (Fox & Baird, 1992; Husak & Fox, 2003) and reduced aggression through prior residency effects gained through repeatedly defending familiar territories (Schwartz, Baird & Timanus, 2007). Results showing that accelerated territory acquisition did not decrease growth rate, foraging opportunities, body condition or longevity all strongly suggest that this schedule of social behaviour does not impose long-term costs. Early territory acquisition, therefore, might be an adaptive tactic if it increases reproductive output. Accelerated opportunistic territory acquisition is particularly interesting in view of recent genetic parentage studies that measure the reproductive success of territorial vs. non-territorial males in the AL population. Socially subordinate but sexually mature first-year males are poised to ascend rapidly (2 days) to territorial status when opportunities arise through removal of territory owners experimentally or by predators (Baird et al., 2003; Baird & Curtis, 2010) or by new habitat becoming available (present study). Nevertheless, genetic parentage results over several seasons show clearly that first-year and older males displaying both territorial and non-territorial tactics sire similar numbers of offspring (York & Baird, 2017). Non-territorial males are successful at the AL site because the human-constructed habitat allows them to avoid displacement by territory owners and to copulate successfully using stealth tactics, prompting questions about the adaptive value of territory defense in this population (York & Baird, 2017). Maintenance of territory defence in AL males might simply be a consequence of selective inertia favouring these tactics that evolved on the ancestral rock outcropping/wash microhabitats, where mate monopolization was likely to be more feasible (York & Baird, 2017). On the contrary, the fitness advantage gained through territorial defence might not be revealed by comparing only the number of hatchlings that males sired each season, because this metric does not measure the number of offspring that survive (York & Baird, 2017). During the 2007–2009 seasons, survivorship of offspring sired by territorial males was positively correlated with the frequency that these males performed broadcast displays, a behaviour pattern that females can readily assess. In contrast, there was no such correlation in non-territorial males, probably because they display much less frequently (York & Baird, 2017). Territory acquisition during the first season is closely linked with increased broadcast display (present study; Baird & Curtis, 2010; Baird, 2013c). Males that acquire territories early might increase the number of reproductive seasons when they can use this prominent behavioural signal to advertise their genetic qualities to females (York & Baird, 2017). Earlier advertisement, therefore, could be under strong selection unless this tactic shortens lifespan. My results show that accelerated territory acquisition did not shorten lifespan, suggesting that this ontogentic tactic is adaptive because it does not impose prohibitive long-term fitness costs and appears to accelerate ascent to a social position allowing maximal intersexual advertisement. ACKNOWLEDGEMENTS Funding for this research was provided by the Office of Sponsored Research at the University of Central Oklahoma. 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Live fast and prosper: early territory defence is not costly in male collared lizards (Crotaphytus collaris)

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Abstract

Abstract Males often exhibit subordinate social tactics and grow at high rates when young, but changes in local social conditions may accelerate opportunities to acquire dominant territorial social status. Early territory defence, however, might trade off high energetic costs of advertisement and aggression against requirements for growth; therefore, the accelerated acquisition of dominant social status might carry prohibitive evolutionary costs. I tested this hypothesis by recording data on social behaviour and life-history traits in male collared lizards that acquired territories during their first season with those that remained non-territorial. I used principal components analysis (PCA) to synthesize these variables while controlling for male body size. Principal components analysis revealed four axes that summarized 89.4% of the total variance among males. As expected, first-year males that ascended to territorial status early had higher PCA scores on a social advertisement axis that included behaviour traits demanding expenditure of energy. Surprisingly, energetic investment in advertisement did not reduce male scores on a life-history PCA axis that included rates of growth, foraging and lifespan. My results indicate that accelerated territory acquisition did not impose long-term costs, suggesting that it might be an adaptive ontogenetic option for males in this population of collared lizards. INTRODUCTION Territory defence is favoured by natural selection when the benefits accrued through access to resources exceed the cumulative costs of repelling competitors (Davies & Houston, 1984; Stamps, 1994; Moore et al., 2014). Males, in particular, defend territories to access females and increase mating success (Trivers, 1972; Emlen & Oring, 1977). Defence of breeding territories, however, is likely also to impose one or more costs, which can include reduced foraging (Peres, 1989) and decreased time available to interact with females (Pryke, 1979; Nolet & Rosell, 1994; Baird, Sloan & Timanus, 2001; Eason & Switzer, 2004). Increased energy expenditure on advertisement and aggression may also reduce rates of growth (Godfrey, 2003; Amsler, 2010) and, perhaps, decrease survival (Marler & Moore, 1989; Marler et al., 1995). Territory defence may also increase predation risk if advertisement displays render males conspicuous (Magnhagen, 1991; Amsler, 2010; Catano et al., 2015). In many vertebrates, including some lizards, variation in the ability of individual males to repel same-sex competitors (i.e. resource holding power, RHP; Parker, 1974) is hypothesized to play a major role in determining the ontogenetic schedule (age) at which males attempt to defend territories (Calsbeek & Sinervo, 2002; Baird, 2013a). Male RHP can be influenced by numerous phenotypic factors, including morphological (e.g. body size, coloration), behavioural (e.g. display frequency, intensity) and performance (e.g. strength, speed) attributes (Hardy & Briffa, 2013). Such traits typically increase as males age, making it advantageous for young males to delay attempts to acquire territories until they attain sufficient RHP that energy investment in contest competition is cost effective (LeBoeuf, 1974; Baird & Curtis, 2010). During the interim, even though they are sexually mature, it is common for smaller males to allocate maximal energy to growth by avoiding confrontations with territory owners and using stealth tactics to interact with females (Kwiatkowski & Sullivan, 2002; Wikelski et al., 2005; Baird, 2008; York & Baird, 2015). Males then switch to dominant social tactics later, when they can compete effectively using aggression (e.g. Wikelski et al., 2005; Baird & Curtis, 2010; Baird, Baird & Shine, 2012). As males that control territories typically display strong philopatry, the ability of individuals to defend a particular space will probably depend on their RHP relative to that of rivals within local neighbourhoods (Zamudio & Sinervo, 2003). Dynamic ecological parameters within each local social milieu, therefore, will almost certainly play an important role in determining the age at which individual males may have opportunities to ascend successfully to territorial social status (Baird & Curtis, 2010). Mortality of established territory owners during or after the reproductive season sometimes provides opportunities for males to acquire territories early, instead of delaying territory acquisition (Baird & Curtis, 2010). Adopting territorial tactics earlier may result in a trade-off between the high energetic demands of defence and investments in rapid growth, which may decrease body condition (Metcalfe & Monoghan, 2001) and perhaps survival (Marler & Moore, 1989; Marler et al., 1995). The potential trade-off between energy allocation to growth vs. territory defense when males are young therefore prompts the question of whether or not accelerated acquisition of territories is an adaptive ontogenetic tactic for individual males. I addressed this question using longitudinal demographic and behavioural data on male collared lizards (Crotaphytus collaris), which allowed comparison of fitness correlates in individuals that adopted territorial social tactics during their first season with those that delayed territory acquisition. Longitudinal studies since 1990 have shown that, although collared lizard males attain sexual maturity at the beginning of their first spring, they usually delay efforts to defend territories throughout this first season (Baird & Timanus, 1998; Baird, Timanus & Sloan, 2003; York & Baird, 2015). The social tactics of first-year males, however, are conditional upon the presence or absence of older, larger territorial males. Mortality of territorial males from predation or winter kill sometimes allows first-year males to establish territories, which is exemplified by their abruptly increasing rates of travel, advertisement displays and aggression (Baird & Hews, 2007; Baird & Curtis, 2010). Opportunities for first-year males to acquire territories increased in my study population beginning in 2008 and continued through 2013. The 2007 cohort of territorial males was particularly old, such that many died that winter. Also, additional suitable lizard habitat was constructed for flood control in the winter of 2008 and colonized by lizards beginning in the spring of that year. I used these opportunities to test the influence of early territory acquisition on variables that might be related to fitness by comparing body size and condition at the beginning of the season, growth rate and lifespan in males that established and defended territories during their first activity season vs. those that maintained non-territorial tactics throughout their first season. Given that territorial activities might also influence the effectiveness of sit-and-wait foraging tactics that collared lizards use (Baird, 2008), I also compared frequencies of foraging strikes by first-year males that adopted these two social ontogenies to assess the potential trade-off with foraging. MATERIAL AND METHODS Study population This research was conducted at the Arcadia Lake Dam flood control spillway (hereafter AL), 9.6 km east of Edmond, OK (35°39′, −97°21′), where I have studied collared lizards during each adult (from 20 March to 30 July) and juvenile (from late July to 15 October) activity season from 1990 to the present (Baird, 2013b). Study subjects were permanently marked soon after hatching as neonates using unique toe-clip combinations, and for identification from a distance by applying coloured paint dots (acrylic) to the dorsum. Lizard subjects occupied five patches of granite rocks or broken concrete slab used to construct flood control/drainage channels. These habitat patches are mapped to scale using GIS measurements (± 1 m) of markers arranged in grids. As individuals maintain strong philopatry to home ranges and territories, this homogeneous substratum promotes observation of lizard behaviour and survival, and recapture of known lizards to monitor growth rates (Baird, 2013b). Males attain sexual maturity during their first season at 70–75 mm snout-to-vent length (SVL), as indicated by presence of mature spermatozoa in smears from extruded hemipenes (Baird & Timanus, 1998; Baird, 2013b). Males that survive their first season typically live 2–3 years, although maximal recorded male lifespan in this population is six seasons (T. A. Baird, unpublished data). Male growth rate, body condition and lifespan Beginning with the first capture of hatchlings and then repeatedly at each recapture, I measured male SVL (± 1 mm) and total body mass (± 0.5 g) and recorded capture location on scale-drawn maps (Baird, 2013b). The growth rate of each male subject during the first reproductive season was calculated as the change in SVL from the first (20 April–1 May) to last (1–15 July) capture up to the end of the reproductive season (15 July) divided by the number of days separating those measurements. I used the residuals from a regression of log10 body mass on log10 SVL to estimate male body condition, as in other lizard studies involving species having body shapes similar to collared lizards (López & Martín, 2002; Warner et al., 2008; Cox et al., 2010). Advertisement and aggressive activities by males diminish significantly after females have laid their last clutches of the season (Baird et al., 2001). Therefore, for first-year males that survived beyond the end of reproduction, I also recorded both SVL and body mass from 15 July until 31 August to determine post-reproductive growth rate. I determined male lifespan as reproductively mature adults to the nearest 0.5 months by determining the presence or absence of individuals during recaptures, censuses and focal observations (described below) throughout the first and subsequent adult activity seasons (from 20 April to 31 August). For lizards that survived into one or more subsequent seasons, I included the interim months of inactivity in estimates of total lifespan. Males were considered to have died during the activity season when they were abruptly and repeatedly absent from their previous home ranges/territories and not sighted elsewhere throughout the study site. Given that adult males emerged from hibernacula during the last 2 weeks of March, the maximal number of months survived during the first adult activity season was 9.5 (15 March to December), whereas the maximum for all subsequent years was 12 months. Male social and foraging behaviour I recorded behavioural data on a total of 155 sexually mature males from 1998 to 2004 and from 2008 to 2013, during their first activity season as adults (hereafter first-year males). In 1998–2004, many of the first-year males present on the site were involved in other experiments (Baird & Hews, 2007; Baird, 2008, 2009; Baird & Curtis, 2010). Therefore, for the present study, I limited my observations during these seasons to only males that were not involved in other studies. Throughout the 2008–2013 seasons, all data collection on first-year males was focused on the present study. I recorded two types of socio-spatial data by conducting censuses and focal observations throughout May and June, which is the collared lizard reproductive season in central Oklahoma (Baird, 2013b). Censuses involved recording the locations of all emergent marked lizards on maps at least four times per week, and capturing those that had moulted for repainting and measurement. I recorded focal observations (sensuAltmann, 1974) on first-year males throughout this 2 month period as long as they survived or until a maximum of 15 observations (20 min on separate days) were recorded (range = 5−15). I recorded only one focal observation per day on individual males, and observations were recorded at randomized times from 09.00 to 13.00 h when substrate temperature was optimal (30–38 °C) for lizard activity (Baird et al., 2001). The number of focal observations per male varied because it was common for first-year males to die of natural causes before the end of their first reproductive season. The cause of mortality was most likely to be predation, because each season we have witnessed near-miss attacks by raptors (Ictinia) and snakes (Masticophis) and four predation events by roadrunners (Geococcyx). Previous studies have demonstrated that five focal observations per individual recorded on separate days provide an accurate estimate of male display and travel rates (Baird & Hews, 2007; York & Baird, 2015), the two most important variables for distinguishing male social status in this population (see next paragraph). Neither variable was correlated with the number of focal observations per individual in either territorial or non-territorial males (F-values = 0.03–1.81; P-values = 0.18–0.87). During focal observations, I recorded the paths of travel and all social behaviour patterns that focal male subjects initiated (described below) on scale-drawn maps (Baird et al., 2003; Baird, 2013b). Territorial vs. non-territorial male social tactics are readily distinguished in AL collared lizards by marked differences in rates of travel and the frequencies with which individuals perform broadcast displays (York & Baird, 2015, 2017). I determined the rate of travel (in metres per hour) by using a digital planimeter (Planix 2000) to measure mapped traces recorded during focal observations, and dividing the cumulative distance travelled by the total observation time on each male. Broadcast displays are stereotypical movements performed when focal males are ≥ 5 m from the nearest conspecific of either sex (Baird & Curtis, 2010; Baird, 2013c; York & Baird, 2015). Most displays involve extension of all four legs to elevate the laterally compressed torso while the dewlap is extended (full shows), and flexion of the legs, which raises and lowers the head and torso, one to 12 times (= push-ups) in succession (Baird, 2013c). Broadcast displays also occasionally involve males walking stereotypically in a tight circular or figure-eight pattern while remaining on a single elevated perch (Baird et al., 2003; Baird, 2013c; York & Baird, 2015). I determined the frequency of broadcast displays per hour for each male by dividing the total number of displays given by the total observation time on each individual. First-year males classified as territorial vs. non-territorial had travel and broadcast display frequencies similar to those recorded during other studies of male behaviour in this population (Baird & Curtis, 2010; York & Baird, 2015). The subordinate social status of most non-territorial males was confirmed by their fleeing and hiding when approached by territory owners independent of their age. Collared lizard foraging acts were also readily recorded during focal observations. Lizards scan for prey by sitting motionless on rock perches at the grass–rock interface, with their heads elevated to inspect for approaching arthropods. When prey approach to ≤ 3 m, lizards descend their perches and begin walking slowly towards prey while crouching, or making a sudden forward lunge/chase (= strikes) in an attempt to capture prey in the mouth (Baird, 2008). I calculated the number of foraging acts per hour by dividing the number of strikes by the total observation time on each male subject. Statistical analyses Variation in the body size of males at the beginning of their first reproductive season, as well annual variation (year), might influence the results of comparisons between first-year males that displayed territorial tactics (N = 80) vs. those that remained non-territorial (N = 75). I used general linear models (GLM) to test the influence of both variables on all dependent behavioural and life-history variables. There was no significant effect of year on any of the dependent variables, and male SVL influenced only growth rate during the reproductive season (see Results). Therefore, I included male SVL as a covariate in a principal components analysis (PCA) used to synthesize variation in six dependent variables [broadcast displays per hour, travel rate (in metres per hour), growth rate (in millimetres per day), foraging acts per hour, lifespan (in months), and estimated body condition] in first-year males that adopted early territorial tactics vs. those that remained non-territorial. I then compared the scores of individual males on significant PCA factors using two-sample t-tests when data met the assumptions of parametric tests and Wilcoxon rank-sum tests when data did not meet these assumptions despite log10 transformation (see also Baird et al., 2007). I used two-sample t-tests to examine the influence of social ontogeny on post-reproductive growth rates in the subset of males (total N = 64) that survived beyond the end of reproduction (10 July) to the end of the activity season (30 August), and lifespan (in months) in the subset of males (N = 58) that survived their first winter. Ethical note All procedures involving live lizards were approved by the Institutional Animal Care and Use Committee of the University of Central Oklahoma (IACUC permit number 13009) and the Oklahoma Department of Wildlife (permit number 5553). I have conducted longitudinal studies on lizard behaviour, growth and survival in this population for > 25 seasons. These studies have involved capturing hatchling lizards by noose, clipping the terminal phalanges of three digits for permanent identification, applying non-toxic acrylic paint for identification of individuals from a distance, palpating female abdomens to monitor reproduction and recording morphometric measurements to determine growth rates. Normal locomotory, foraging and thermoregulatory behaviour together with very rapid growth in hundreds of toe-clipped hatchlings have confirmed that these techniques do not harm collared lizards (Baird, 2013b). RESULTS Principal components analysis identified four factors that individually explained ≥ 12% and collectively explained 84.9% of the total variance in the behavioural and life-history parameters of 155 first-year males. Rates of travel and frequency of broadcast displays loaded highest on factor 1 (advertisement), which explained 33.9% of the variance (Table 1). Three likely life-history correlates of fitness, foraging and growth rates, and lifespan loaded highest on factor 2 (life history), which explained 20.8% of the total variance. Only body condition loaded highest on factor 3 (17.7% of variance), but the loading was negative, indicating low body condition estimates. Positive body condition loaded alone on factor 4, which explained 12.5% of the total variance (Table 1). Scores for first-year males that acquired territories were higher on the advertisement (z – normal approximation154 = 9.10, P < 0.0001) and negative body condition axes (z154 = 3.18, P = 0.0018) than scores for first-year males that remained non-territorial (Table 2). Territorial and non-territorial males had similar scores on both the life-history (t154 = 0.56, P = 0.58) and positive body condition axes (t154 = 0.29, P = 0.77; Table 2). Table 1. Principal component analysis factor loadings for behavioural and life-historical variables in all first-year males (N = 155) Variable  Principal component analysis factor  1  2  3  4  Travel (m/h)  0.620  0.052  0.245  −0.121  Broadcast displays/h  0.613  0.140  0.210  −0.063  Growth rate (mm/day)  −0.384  0.468  −0.001  −0.220  Lifespan (months)  −0.027  0.676  0.289  0.623  Body condition  0.252  −0.046  −0.752  0.525  Foraging acts/h  0.167  0.547  −0.487  −0.515  Percentage of variance explained  33.9  20.8  17.7  12.5  Variable  Principal component analysis factor  1  2  3  4  Travel (m/h)  0.620  0.052  0.245  −0.121  Broadcast displays/h  0.613  0.140  0.210  −0.063  Growth rate (mm/day)  −0.384  0.468  −0.001  −0.220  Lifespan (months)  −0.027  0.676  0.289  0.623  Body condition  0.252  −0.046  −0.752  0.525  Foraging acts/h  0.167  0.547  −0.487  −0.515  Percentage of variance explained  33.9  20.8  17.7  12.5  Highest positive loadings are indicated using boldface font. View Large Table 2. Comparison of principal component analysis factor scores for males that acquired territories during their first season vs. those that remained non-territorial throughout their first seasons Principal component analysis axis  Territorial males    Non-territorial males  (N = 80)    (N = 75)  Advertisement  0.094 (0.016)  *  −0.113 (0.069)  Life history  0.009 (0.013)  NS  −0.002 (0.015)  Negative body condition  0.025 (0.013)  *  −0.030 (0.011)  Positive body condition  −0.003 (0.010)  NS  0.002 (0.011)  Principal component analysis axis  Territorial males    Non-territorial males  (N = 80)    (N = 75)  Advertisement  0.094 (0.016)  *  −0.113 (0.069)  Life history  0.009 (0.013)  NS  −0.002 (0.015)  Negative body condition  0.025 (0.013)  *  −0.030 (0.011)  Positive body condition  −0.003 (0.010)  NS  0.002 (0.011)  Data are mean factor scores (± 1.0 SE). Asterisks indicate significant differences (0.0001) between means of territorial vs. non-territorial males. NS denotes not significant. View Large For the 64 males that survived past the end of reproduction until at least 31 August, post-reproduction growth rates of subjects that had defended territories during the reproductive season (mean mm/day ± 1.0 SE = 0.19 ± 0.02) and those that had remained non-territorial (0.22 ± 0.02) were similar (t63 = 1.30, P = 0.20). For the 58 males that survived their first winter, lifespan of those that had defended territories (mean months ± 1.0 SE = 18.9 ± 2.4) and those that had remained non-territorial (20.1 ± 1.6) was also similar (t57 = 0.43, P = 0.67). DISCUSSION As expected, social variables associated with territorial advertisement (patrol and broadcast display) loaded together on the advertisement PCA axis that explained the most variation among first-year males, and scores for males that acquired territories during their first seasons were higher than those for males that remained non-territorial. It is surprising that accelerated territorial activities did not reduce scores on the life-history PCA axis that best synthesized male growth rates, foraging rates and lifespan. Increased travel is intuitively expected to diminish the energy that can be allocated to growth, and more frequent broadcast display would seem to increase conspicuousness to predators. The finding of similar foraging rates in collared lizard males that increased territorial activities is also counter to findings of other studies (Peres, 1989; Amsler, 2010). Increased travel would seem to detract from the ability of males to wait motionless on perches to locate and ambush prey (Baird, 2008), but similar foraging scores suggest that territory acquisition did not decrease foraging opportunities in male collared lizards. Increased travel and scanning for shorter periods from different vantage points is also apparently an effective foraging tactic, perhaps because it increases encounters with prey. First-year males that acquired territories early and those that remained non-territorial also had similar growth rates after reproduction ceased and had similar lifespan in analyses of all males and only those that survived their first winter. Together, these results suggest that diverting energy to increased travel and display to promote early territory acquisition during the first season did not impose a fitness cost for these individuals. There appear to be almost no other longitudinal studies of free-living vertebrates where males vary in the ontogenetic schedules of alternative social tactics that can be used for comparison of the fitness impact with that in collared lizards. My results showing insignificant effects on growth and survival differ markedly from findings of field studies on another iguanian lizard, Sceloporus jarrovi, in which heightened territorial behaviour decreased male survival (Marler & Moore, 1989; Marler et al., 1995). These opposing results might be a consequence of an important difference in experimental design. Increased aggression in S. jarrovi males was induced before the reproductive season by supplementing circulating testosterone concentrations (Marler & Moore, 1989; Marler et al., 1995). In contrast, the collared lizard males that adopted territorial tactics did so of their own volition during the natural reproductive season. Males that sought territorial social status early were larger (SVL), which might indicate a positive relationship between accelerated territory acquisition and RHP, specifically the ability of males to sustain heightened energetic costs. Nevertheless, the observed pattern of loadings on PCA factors related to body condition did not support this hypothesis. Scores on the positive body condition axis (factor 4) were similar in territorial vs. non-territorial males, whereas males that adopted territorial tactics had higher scores on the negative body condition axis (factor 3). My sampling did not allow determination of whether non-surviving first-year males (59% territorial, 75% non-territorial) were taken by predators before they entered hibernacula or died over the winter because of insufficient energy storage. A previous study (Baird, 2009) revealed almost no mortality of first-year collared lizard males during the reproductive season, suggesting little predation even though one experimental group was painted brightly to increase visual conspicuousness to potential predators (Baird, 2009). This result, coupled with those of the present study showing that neither body condition nor post-reproductive growth rate was impacted by early territory acquisition, suggests that variation in survival while burrowed over the winter is a significant factor influencing total lifespan. Similar to results on collared lizards, decreased survival in male S. jarrovi also appeared to be a consequence of energy deficits instead of predation (Marler & Moore, 1989; Marler et al., 1995). There also appear to be few, if any, empirical field measurements of total lifespan in relationship to different age-specific social ontogenies such as those displayed by male collared lizards, even though lifespan is obviously related to fitness in iteroparous species. Once they establish territory occupancy, male collared lizards defend their areas for life, apparently at a reduced cost owing to ‘dear-enemy’ effects (Fox & Baird, 1992; Husak & Fox, 2003) and reduced aggression through prior residency effects gained through repeatedly defending familiar territories (Schwartz, Baird & Timanus, 2007). Results showing that accelerated territory acquisition did not decrease growth rate, foraging opportunities, body condition or longevity all strongly suggest that this schedule of social behaviour does not impose long-term costs. Early territory acquisition, therefore, might be an adaptive tactic if it increases reproductive output. Accelerated opportunistic territory acquisition is particularly interesting in view of recent genetic parentage studies that measure the reproductive success of territorial vs. non-territorial males in the AL population. Socially subordinate but sexually mature first-year males are poised to ascend rapidly (2 days) to territorial status when opportunities arise through removal of territory owners experimentally or by predators (Baird et al., 2003; Baird & Curtis, 2010) or by new habitat becoming available (present study). Nevertheless, genetic parentage results over several seasons show clearly that first-year and older males displaying both territorial and non-territorial tactics sire similar numbers of offspring (York & Baird, 2017). Non-territorial males are successful at the AL site because the human-constructed habitat allows them to avoid displacement by territory owners and to copulate successfully using stealth tactics, prompting questions about the adaptive value of territory defense in this population (York & Baird, 2017). Maintenance of territory defence in AL males might simply be a consequence of selective inertia favouring these tactics that evolved on the ancestral rock outcropping/wash microhabitats, where mate monopolization was likely to be more feasible (York & Baird, 2017). On the contrary, the fitness advantage gained through territorial defence might not be revealed by comparing only the number of hatchlings that males sired each season, because this metric does not measure the number of offspring that survive (York & Baird, 2017). During the 2007–2009 seasons, survivorship of offspring sired by territorial males was positively correlated with the frequency that these males performed broadcast displays, a behaviour pattern that females can readily assess. In contrast, there was no such correlation in non-territorial males, probably because they display much less frequently (York & Baird, 2017). Territory acquisition during the first season is closely linked with increased broadcast display (present study; Baird & Curtis, 2010; Baird, 2013c). Males that acquire territories early might increase the number of reproductive seasons when they can use this prominent behavioural signal to advertise their genetic qualities to females (York & Baird, 2017). Earlier advertisement, therefore, could be under strong selection unless this tactic shortens lifespan. My results show that accelerated territory acquisition did not shorten lifespan, suggesting that this ontogentic tactic is adaptive because it does not impose prohibitive long-term fitness costs and appears to accelerate ascent to a social position allowing maximal intersexual advertisement. ACKNOWLEDGEMENTS Funding for this research was provided by the Office of Sponsored Research at the University of Central Oklahoma. 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