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Non-invasive measurements of physical traits in wildlife: photogrammetry applied to deer antlers
Abstract
Photogrammetry has great potential in animal ecology because it can be used to obtain measurements of animal features such as antler, horn, and body size from photographs in a remote, non-invasive fashion. Little use of photogrammetry has been made so far, however, mostly limited by the need to get sufficiently close to the target animal or have an object of known size in frame to scale it. Here, I aim to unleash the further potential of photogrammetry by validating it for measuring more complex traits using three-dimensional deer antlers for the first time. I calibrated and validated two different photogrammetric systems by measuring an object of known size in photographs from distances up to 200 meters. I then demonstrated the high accuracy of my photogrammetry in measuring a suite of antler features from dozens of roe and fallow deer antlers attached to skulls placed at various distances to emulate a free-living animal. I also developed and validated an efficient correction protocol to deal with curved and tilted antler features. My antler measurement estimates were characterised by mean errors lower than 5% when compared to true antler sizes, with my correction protocol for antlers particularly effective and validated with independent antler sizes. Most importantly, the ecological meaning of my antler estimates was not altered by my approach, because the ranking of the deer based on true antler sizes was identical to the ranking estimated by photogrammetry. My procedures can be followed to estimate highly precise and accurate antler sizes. As I was able to obtain highly precise and accurate measurements of deer antler features with photogrammetry, these techniques can be transferred to measure other complex traits (e.g., horn size) and body size in general (e.g., shoulder height). As photogrammetry is non-invasive, remote, and fast, it fits perfectly into modern wildlife conservation and management techniques. The technique is particularly suited to (but not limited to) the establishment of long-term studies that allow repeated measurements of individuals without the need to capture and handle them.
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The measurement of physical traits of animals is an important topic in animal ecology and wildlife management, but it is quite difficult to achieve an acceptable level of accuracy, especially for free‐ranging wild animals. As a non‐invasive method, camera trapping has become a common tool for detecting and monitoring wild animals. In this study, we combined camera‐trapping images and a photogrammetry technique to present a camera trap‐based photogrammetric estimation (CTPE) approach for robust measurement of morphological traits of animals. We first tested our method in a captive population of fallow deer (Dama dama) and compared the estimated shoulder heights by CTPE with corresponding hand measurements. The results revealed a remarkable accuracy, with an expected measurement error within ± 5 cm. Second, we mainly demonstrated a field application of CTPE in a wild population of Altai wapiti (Cervus elaphus sibiricus) in the Kanas National Nature Reserve, Xinjiang, China. For wapiti, we found that the average shoulder height of males was 135 ± 9 cm (mean ± sd, n = 30) and that of females was 125 ± 6 cm (n = 37), with all data significantly fitting a normal distribution. We did not find any differences in CTPE results among cameras, between photograph types (colour vs. black and white) or temperatures. No significant difference existed between our results and the hand‐measured shoulder heights of wapiti from deer farms. Finally, we discussed the strengths, limitations and potential extensions of the method. We suggest that the combination of camera trapping and the photogrammetry technique is quite promising and that CTPE has great potential in wildlife field investigations.
The increasing availability of 3D-imaging technology provides new opportunities for measuring morphology. Photogrammetry enables easy 3D-data acquisition compared to conventional methods and here we assess its accuracy for measuring the size of deer antlers, a complex morphological structure. Using a proprietary photogrammetry software, we generated 3D images of antlers for 92 individuals from 29 species of cervids that vary widely in antler size and shape and used these to measure antler volume. By repeating the process, we found that the relative error averaged 8.5% of object size. Errors in converting arbitrary voxel units into real volumetric units accounted for 70% of the measurement variance and can therefore be reduced by replicating the conversion. We applied the method to clay models of known volume and found no indication of bias. The estimation was robust against variation in imaging device, distance and operator, but approximately 40 images per specimen were necessary to achieve good precision. We used the method to show that conventional measures of main-beam length are relatively poor estimators of antler volume. Using loose antlers of known weight, we also showed that the volume may be a relatively poor predictor of antler weight due to variation in bone density across species. We conclude that photogrammetry can be an efficient and accurate tool for measuring antlers, and likely many other complex morphological traits.
In species with sexual size dimorphism, the offspring of the larger sex usually have greater energy requirements and may lead to greater fitness costs for parents. The effects of offspring sex on maternal longevity, however, have only been tested in humans. Human studies produced mixed results and considerable debate mainly owing to the difficulty of distinguishing the effects of sexual dimorphism from sociocultural factors. To advance this debate, we examined how the relative number of sons influenced maternal longevity in four species of free-living ungulates (Soay sheep Ovis aries; bighorn sheep, Ovis canadensis; red deer, Cervus elaphus; mountain goat, Oreamnos americanus), with high male-biased sexual size dimorphism but without complicating sociocultural variables. We found no evidence for a higher cumulative cost of sons than of daughters on maternal longevity. For a given number of offspring, most females with many sons in all four populations lived longer than females with few sons. The higher cost of sons over daughters on maternal lifespan reported by some human studies may be the exception rather than the rule in long-lived iteroparous species.
Theoretical support exists for an exaggerated male structure to serve as both a weapon for intrasexual competition and as an ornament to signal quality and promote female choice. However, there is little, if any, evidence to support this theory in maleemale competition breeding systems. Using white-tailed deer, Odocoileus virginianus, as a model species, we manipulated antler size on males while controlling for body size and age and allowed 25 oestrous females the opportunity to choose between pairs of segregated males with either large or small antlers. By segregating males, we were able to remove any intrasexual male competition and isolate the effects of female choice. Using various behavioural indications of female choice, we demonstrate that females prefer males with large antlers to those with small antlers. Because antler size is heritable in deer, this female preference for larger antlers may be adaptive by increasing the reproductive success of her male offspring. Our unique antler manipulation study supports the armament-ornament model where male weapons can simultaneously serve as ornaments to females and weapons in maleemale competition breeding systems.
Body mass dynamics of animals can indicate critical associations between extrinsic factors and population vital rates. Photogrammetry can be used to estimate mass of individuals in species whose life histories make it logistically difficult to obtain direct body mass measurements. Such studies typically use equations to relate volume estimates from photogrammetry to mass; however, most fail to identify the sources of error between the estimated and actual mass. Our objective was to identify the sources of error that prevent photogrammetric mass estimation from directly predicting actual mass, and develop a methodology to correct this issue. To do this, we obtained mass, body measurements, and scaled photos for 56 sedated Weddell seals (Leptonychotes weddellii). After creating a three-dimensional silhouette in the image processing program PhotoModeler Pro, we used horizontal scale bars to define the ground plane, then removed the below-ground portion of the animal’s estimated silhouette. We then re-calculated body volume and applied an expected density to estimate animal mass. We compared the body mass estimates derived from this silhouette slice method with estimates derived from two other published methodologies: body mass calculated using photogrammetry coupled with a species-specific correction factor, and estimates using elliptical cones and measured tissue densities. The estimated mass values (mean ± standard deviation 345±71 kg for correction equation, 346±75 kg for silhouette slice, 343±76 kg for cones) were not statistically distinguishable from each other or from actual mass (346±73 kg) (ANOVA with Tukey HSD post-hoc, p>0.05 for all pairwise comparisons). We conclude that volume overestimates from photogrammetry are likely due to the inability of photo modeling software to properly render the ventral surface of the animal where it contacts the ground. Due to logistical differences between the “correction equation”, “silhouette slicing”, and “cones” approaches, researchers may find one technique more useful for certain study programs. In combination or exclusively, these three-dimensional mass estimation techniques have great utility in field studies with repeated measures sampling designs or where logistic constraints preclude weighing animals.
Growth and body condition can be used as indices of health and fitness, but are difficult to collect for populations of conservation concern where individuals cannot be captured. We incorporated a laser photogrammetry system into boat-based photo-identification surveys that underpin individual-based studies of cetacean populations. These data were integrated with >25 years of observations from a temperate bottlenose dolphin population in Scotland to investigate the influence of sex on growth patterns, effects of birth order on calf size and the longer term consequences of variation in early growth. Field measurements of the distance from the blowhole to the dorsal fin were made in multiple years from 87 dolphins that had been followed from birth, ranging in age from newborn to 26 years. These estimates were validated against direct measurements of 12 individuals that had previously been captured and released in Florida and two study individuals that subsequently stranded. Using relationships derived from other stranded individuals, age-specific body lengths were used to produce growth curves that were based entirely upon remote observations. Multilevel regression growth curve analyses suggested males and females showed similar patterns of growth, unlike bottlenose dolphins in sub-tropical areas, and growth was best described by a Richards’ growth curve. Newborn length was unrelated to sex, however females’ first calves were shorter than subsequent calves. Sample sizes remain small, yet there was evidence of fitness consequences of variation in calf length; calves that died in their first winter were significantly shorter than those that survived. The incorporation of this simple-to-use and inexpensive method into individual-based photo-identification studies provides new opportunities to non-invasively investigate drivers of variation in growth and the demographic consequences of variation in early growth in cetaceans from protected populations.
Intra‐class correlations ( ICC ) and repeatabilities ( R ) are fundamental statistics for quantifying the reproducibility of measurements and for understanding the structure of biological variation. Linear mixed effects models offer a versatile framework for estimating ICC and R . However, while point estimation and significance testing by likelihood ratio tests is straightforward, the quantification of uncertainty is not as easily achieved.
A further complication arises when the analysis is conducted on data with non‐Gaussian distributions because the separation of the mean and the variance is less clear‐cut for non‐Gaussian than for Gaussian models. Nonetheless, there are solutions to approximate repeatability for the most widely used families of generalized linear mixed models (GLMMs).
Here, we introduce the R package rptR for the estimation of ICC and R for Gaussian, binomial and Poisson‐distributed data. Uncertainty in estimators is quantified by parametric bootstrapping and significance testing is implemented by likelihood ratio tests and through permutation of residuals. The package allows control for fixed effects and thus the estimation of adjusted repeatabilities (that remove fixed effect variance from the estimate) and enhanced agreement repeatabilities (that add fixed effect variance to the denominator). Furthermore, repeatability can be estimated from random‐slope models. The package features convenient summary and plotting functions.
Besides repeatabilities, the package also allows the quantification of coefficients of determination R ² as well as of raw variance components. We present an example analysis to demonstrate the core features and discuss some of the limitations of rptR.
Positive relationships between age, sexually selected traits, and male reproductive success have been reported for a number of polygynous ungulates; however, relatively little is known about the factors influencing male reproductive success in ungulate species whose mating system is characterized by tending-bond behaviors. Broad interest in the genetic consequences of selective harvest supports a greater understanding of the role of these factors as determinants of male reproductive success in important game species (e.g., white-tailed deer [Odocoileus virginianus]), that exhibit tending-bond behaviors. We investigated male reproductive success in white-tailed deer across a range of sex ratios and age structures using a known population of deer housed in a 175-ha enclosure in central Alabama, USA. We measured age, annual antler size, and annual body size of male white-tailed deer and assigned paternity to 143 known-age offspring during 2007–2014. Reproductive success was attributed to a high proportion of males during each of the 6 breeding seasons. Our most supported model indicated that annual body size and antler size of the individual were positively associated with annual male breeding success. The effects of annual antler size were sensitive to changes in mean male age of the herd, with antler size having the greatest effect on male reproductive success under older male age structures. Young (≤1.5 yr) males reproduced most frequently when male age structure was youngest (which correlated with female-biased sex ratios in this population). Our results suggest that male age structure and sex ratio played a key role in establishing patterns of male reproductive success in white-tailed deer. Management practices that encourage balanced adult sex ratios and older male age structures (e.g., Quality Deer Management) may promote a highly competitive environment where sexually selected traits are of increased importance to male breeding success. However, the ability of managers to alter herd genetics in a positive or negative direction through selective harvest is limited in white-tailed deer because of the high proportion of reproducing males.
The ability to accurately measure morphological characteristics of wild primates in the field is challenging, yet critical for understanding fundamental aspects of their biology and behavior. Recent studies have shown that digital photogrammetry can be used to non-invasively measure morphological traits of wild primates, as it allows for the determination of geometric properties of objects remotely from photographic images. We report here on a rare opportunity to test this methodology by comparing measurements obtained directly from living great apes to those obtained from photographs. We test the accuracy and precision of two independent photogrammetric techniques, employing the use of parallel lasers and a distance meter, respectively, for obtaining measurements of static objects and captive western lowland gorillas (Gorilla gorilla gorilla) (n=4) at Zoo Atlanta. For static objects, the mean percent error between corresponding measurements collected by the same observer directly versus using photogrammetry was 0.49-0.74% for the parallel laser method and 0.62-0.76% for the distance meter method. For gorillas, mean percent error between corresponding direct and remote measurements was 2.72-5.20% for the parallel laser method and 2.20-7.51% for the distance meter method. Correlations between direct measurements and corresponding parallel laser and distance meter measurements of gorillas were highly significant with R2 values and slopes approaching 1.0 (parallel lasers: R2=0.9989, P<0.0001; distance-meter: R2=0.9990, P<0.0001). Further, variation between measurements of the same targets collected repeatedly by the same observer, and between different observers, was uniformly low across methods (CV, range=0.003-0.013). While errors are slightly higher for the distance meter technique, both methods show great promise for addressing a wide range of questions requiring the non-invasive collection of morphological data from wild primates.
This paper discusses a general framework for smoothing parameter estimation
for models with regular likelihoods constructed in terms of unknown smooth
functions of covariates. Gaussian random effects and parametric terms may also
be present. By construction the method is numerically stable and convergent,
and enables smoothing parameter uncertainty to be quantified. The latter
enables us to fix a well known problem with AIC for such models. The smooth
functions are represented by reduced rank spline like smoothers, with
associated quadratic penalties measuring function smoothness. Model estimation
is by penalized likelihood maximization, where the smoothing parameters
controlling the extent of penalization are estimated by Laplace approximate
marginal likelihood. The methods cover, for example, generalized additive
models for non-exponential family responses (for example beta, ordered
categorical, scaled t distribution, negative binomial and Tweedie
distributions), generalized additive models for location scale and shape (for
example two stage zero inflation models, and Gaussian location-scale models),
Cox proportional hazards models and multivariate additive models. The framework
reduces the implementation of new model classes to the coding of some standard
derivatives of the log likelihood.
It is not always practical to hand-measure body size of free-ranging animals. In recent years, parallel-laser photogrammetry has become increasingly common for obtaining remote estimates of body size. However, it is unknown how well this technique might capture variation in body size of curvilinear features or whether the distance between parallel-laser calipers is altered when projected onto a curved surface. We describe a photogrammetric system that may be useful for obtaining body-size measurements from unrestrained large mammals that permit approach. We tested the use of parallel-laser photogrammetry to estimate the size of curvilinear features in domestic horses (Equus ferus caballus) and identified morphometrics that explained variation in body weight. Despite projecting the lasers onto a curved surface (the barrel of a horse), we achieved accurate photogrammetric estimates of linear hand-measurements. The curvilinear hand-measurements also showed strong correlations (R2 ≥ 0.996) with their respective linear photogrammetric estimates, and most photogrammetric estimates had high reliability. Using 3 variables of body size, photogrammetric estimates and hand-measurements explained 86.0% and 96.2% of the variation in weight, respectively. © 2015 The Wildlife Society.
Body condition has a strong influence on reproduction and survival. Consequently, understanding spatiotemporal variation in body condition may help identify processes that determine life history, and thus demography. The effect of environmental variables on individuals' body condition, although widely documented, is generally achieved by investigating habitat, plant phenology, or density separately, such that cumulative or interactive effects can rarely be considered. We investigated how spatial and annual variation in habitat composition, deer density, and vegetation productivity influenced white-tailed deer (Odocoileus virginianus) body condition during the breeding period. We detailed changes in body condition using several indices, including body mass, peroneus muscle mass, rump fat, kidney fat index, and antler size in >4,000 male and female deer of different ages harvested during September-December, 2002-2006 on Anticosti Island, Quebec, Canada. Overall, females and yearlings harvested in fir forests were in poorer condition than those harvested in peatlands or spruce forests, whereas body condition of adult males was greater when open habitats were highly available. High deer density reduced autumn gains in fat, muscle mass, and body mass in males and yearlings, and in fat for females. Surprisingly, density positively affected the size of male antlers. High density at birth favored fat accumulation in adult females, suggesting strong selective pressure that removed low-quality individuals in early age at high deer density. Low Normalized Difference Vegetation Index (NDVI) in spring was associated with delayed but rapid spring green-up, and favored higher body condition in autumn. Reproduction affected most parameters of body condition; lactating females had less mass, fat, and muscle than non-lactating females, whereas mass and fat of males >4 years old steeply declined during the rut. Body mass and fat reserves showed a stronger response to density, habitat, NDVI, and reproduction than muscle mass. Body mass was a good integrating measure of fat and muscle mass, although allocation between muscle growth and energy storage was confounded. Our study highlighted the influence of environmental conditions on individual fat reserves, muscle mass, and body mass in autumn, with potential effects on reproduction and winter survival. Appropriate monitoring of body-condition indices in the fall can track the effect of environmental variables and management practices on animal populations. (C) 2014 The Wildlife Society
Morphological features correlate with many life history traits and are therefore of high interest to behavioral and evolutionary biologists. Photogrammetry provides a useful tool to collect morphological data from species for which measurements are otherwise difficult to obtain. This method reduces disturbance and avoids capture stress. Using the Galapagos sea lion (Zalophus wollebaeki) as a model system, we tested the applicability of single-camera photogrammetry in combination with laser distance measurement to estimate morphological traits which may vary with an animal's body position. We assessed whether linear morphological traits estimated by photogrammetry can be used to estimate body length and mass. We show that accurate estimates of body length (males: ±2.0%, females: ±2.6%) and reliable estimates of body mass are possible (males: ±6.8%, females: 14.5%). Furthermore, we developed correction factors that allow the use of animal photos that diverge somewhat from a flat-out position. The product of estimated body length and girth produced sufficiently reliable estimates of mass to categorize individuals into 10 kg-classes of body mass. Data of individuals repeatedly photographed within one season suggested relatively low measurement errors (body length: 2.9%, body mass: 8.1%). In order to develop accurate sex- and age-specific correction factors, a sufficient number of individuals from both sexes and from all desired age classes have to be captured for baseline measurements. Given proper validation, this method provides an excellent opportunity to collect morphological data for large numbers of individuals with minimal disturbance.
Research on wildlife movement, physiology, and reproductive biology often requires capture and handling of animals. Such invasive treatment can alter behavior, which may bias results or invalidate assumptions regarding representative behaviors. To assess the impacts of handling on mule deer (Odocoileus hemionus), a focal species for research in North America, we investigated pre- and post-recapture movements of collared individuals, and compared them to deer that were not recaptured (controls). We compared pre- and post-recapture movement rates (m/hr) and 24-hour straight-line displacement among recaptured and control deer. In addition, we examined the time it took recaptured deer to return to their pre-recapture home range. Both daily straight-line displacement and movement rate were marginally elevated relative to monthly averages for 24 hours following recapture, with non-significant elevation continuing for up to 7 days. Comparing movements averaged over 30 days before and after recapture, we found no differences in displacement, but movement rates demonstrated seasonal effects, with faster movements post- relative to pre-recapture in March and slower movements post- relative to pre-recapture in December. Relative to control deer movements, recaptured deer movement rates in March were higher immediately after recapture and lower in the second and third weeks following recapture. The median time to return to the pre-recapture home range was 13 hours, with 71% of deer returning in the first day, and 91% returning within 4 days. These results indicate a short period of elevated movements following recaptures, likely due to the deer returning to their home ranges, followed by weaker but non-significant depression of movements for up to 3 weeks. Censoring of the first day of data post-capture from analyses is strongly supported, and removing additional days until the individual returns to its home range will control for the majority of impacts from capture.
In red deer, yearling antler length is a largely nutrition-mediated phenotypic character, and is therefore sometimes used as an indirect estimate of range quality and population condition. However, the parameters affecting yearling antler length have been little studied. We analyse the contributions of density, weather and maternal effects on yearling antler length of 581 individual stags born 1970-1996 on the Isle of Rum (Scotland). We show that antler length is a good measure of yearling condition: the probability of overwinter survival in yearlings that developed antlers was 3 times higher than for yearlings that did not develop antlers, and yearling antler length was correlated with the number of antler points the following year. Between years, variation in yearling antler length was best explained by variation in red deer density and June temperature at 12 months of age. Both of these variables were negatively correlated with antler length, and most likely this effect is due to changes in nutrient availability. Population density affects biomass availability for the individual, while low temperatures in early summer prolong the availability of high forage quality. At the individual level, antler length increased with birth weight and decreased with birth date, reflecting the persistent and pervasive influence of conditions in early life.
The acquisition of accurate information on the size of traits in animals is fundamental for the study of animal ecology and evolution and their management. We demonstrate how morphological traits of free-ranging animals can reliably be estimated on very large observation distances of several hundred meters by the use of ordinary digital photographic equipment and simple photogrammetric software. In our study, we estimated the length of horn annuli in free-ranging male Alpine ibex (Capra ibex) by taking already measured horn annuli of conspecifics on the same photographs as scaling units. Comparisons with hand-measured horn annuli lengths and repeatability analyses revealed a high accuracy of the photogrammetric estimates. If length estimations of specific horn annuli are based on multiple photographs measurement errors of <5.5 mm can be expected. In the current study the application of the described photogrammetric procedure increased the sample size of animals with known horn annuli length by an additional 104%. The presented photogrammetric procedure is of broad applicability and represents an easy, robust and cost-efficient method for the measuring of individuals in populations where animals are hard to capture or to approach.
Shoulder height is considered a reliable indicator of age for African elephants that grow throughout their lifetime (Lindeque and van Jaarsveld 1993, Shrader et al. 2006b). Many techniques have been used to estimate elephant age, including back length (Laws 1969, Croze 1972), posterior foot print (Western 1983), progressive molar growth (Laws 1966), as well as characteristics identifiable through direct observation (Moss 1996). Among these latter, body size, appearance of jaws (at ca two-three yr old) and their growth, markings that arise with older age (ears turning outwards, snout elongation, etc.), and shoulder height (Laws 1966, Douglas-Hamilton 1972, Laws et al. 1975, Jachmann 1988, Lee and Moss 1995) have been fre-quently used in population studies of these mammals.Currently, the majority of studies on elephants still depend on the assessment of body size to reconstruct the age structure of wild populations (Wittemyer 2001, Morgan and Lee 2003). My aims in this paper are (i) to compare two alternative and simple models (one based on the employment of a linear regression method, and the other based on digital photo-grammetry and laser rangefinder (Shrader et al. 2006a) to evaluate their performance with estimates of ele-phant heights in the field, and (ii) to validate these models How tall is an elephant? Two methods for estimating elephant height
Photogrammetry can be used to measure the body dimensions of a variety of mammals. We developed a digital photogrammetry technique and used an infrared laser rangefinder to measure the shoulder heights of African elephants (Loxodonta africana). Measures of the height of objects of known size using digital photogrammetry were between 0.7% shorter to 0.6% taller than the real values. The rangefinder recorded values that ranged from 0.8% to 3.6% larger than the real height. When we applied digital photogrammetry to tame elephants, measured shoulder heights were 1.6% to 3.4% shorter than those recorded using a cus- tom-made calliper. For these elephants, the rangefinder recorded shoulder heights that were 3.8 to 9.4% smaller than the real values. The digital photogrammetric technique described here is less time-consuming and as or more precise than other techniques used to measure African elephants.
Cause for spatial variation in phenotypic quality of white-tailed deer (Odocoileus virginianus) populations is of great interest to wildlife managers. Relating phenotypic variation of populations to large-scale land-use patterns may provide insight into why populations exhibit spatial variation and elucidate how management can influence population phenotype. We used an information-theoretic approach to relate average antler size of 203 deer populations to composition and structure of the habitat occupied by those populations. We used interspersion, edge, and diversity indices to represent habitat structure and percentage of area in vegetation types to represent habitat composition. Landscape composition was a better predictor of deer population antler size than was landscape structure. Percentages of the management unit in agriculture, pasture, and pine forest were variables commonly found in the region-specific set of best models. Model-averaged estimates of agriculture and pasture parameters were always positive and estimates of pine forest parameters were always negative, which suggests that land-use types that promote growth of early successional herbaceous plants will positively influence antler size and, most likely, body growth and reproduction of white-tailed deer populations. Conversely, our findings suggest landscapes dominated by pine forests did not provide optimal amounts of quality forages for white-tailed deer. Pine forest effects should be mitigated using a combination of increased harvest to lower deer density and silvicultural practices like thinning, prescribed burning, and selective herbicide applications that stimulate growth of high-quality forages beneath the forest canopy to improve deer phenotypic quality.
Knowledge of whale length is important to ecological studies. However, photographic techniques to measure sperm whales traditionally require high vantage points or a complicated stereo system. Furthermore, these traditional techniques require an alongside approach that often prevents individual identification. For simple and fast size measurements at sea, I used a laser range finder alongside a digital camera to obtain distance to the fluke at the same time as photo-identification. The camera/lens and laser range finder were calibrated on objects of known lengths. The coefficient of variation (CV) for test objects was low (CV = 0.21%). Forty-seven individually identified sperm whales were measured repetitively on up to 12 different occasions, and the CV was lower (CV = 1.3%) than for other photogrammetric techniques (CV = 4.4%–5.1%). A regression of log fluke span to log total length from whaling and stranding data yielded an r 2 of 0.87 (CV of residuals = 6.7%). Thirty-eight female/immature sperm whales were measured in the Gulf of Mexico (median = 9.3 m, range = 7.1–12.3 m), 167 in the Gulf of California (median = 10.7 m, range = 8.4–13.1 m) and 13 bachelor males off Kaikoura, New Zealand (median = 14.2, range = 11.7–15.8 m). The results were within known sperm whale size and suggested that the population in the Gulf of Mexico was made up of smaller animals than that of the Gulf of California. This technique is easy to implement and allows the measurement of identified individuals.
Size and symmetry of secondary sexual traits are supposed to be honest signals of male phenotypic quality in vertebrates. Antler size and symmetry, male quality and mating success have not been fully demonstrated to be correlated in cervids. Such correlations can be particularly intriguing in the case of species adopting costly mating strategies, which imply territorial defence without feeding. In these cases, body condition appears to be crucial at the onset of the rut, and large and symmetrical antlers may be borne by successful males. For these reasons, during four consecutive years, we analysed growth rate, size and symmetry of 26 fallow bucks’ antlers in relation to individual mating strategy and success in a lekking population. Territorial (T) males, which gained higher mating success in the lek, showed a faster antler growth (about 10 g/d per antler) than non-territorial (NT) males (3.6–5.2 g/d per antler) during the velvet period, and this was likely because of optimized foraging strategies. At the onset of the rut, when antler growth was completed, T males had larger antlers than NT males. Possibly because of worsened body conditions, NT males showed a pronounced antler directional asymmetry, while T males did not. However, no direct link between antler symmetry and mating success was found, thus confirming the ambiguous role of antler asymmetry as an indicator of fitness. The faster the antler growth, the larger its final size and the higher its beholder’s mating success. Our results confirmed that, like groaning and scent marking, antler size reflects social status and dominance in male fallow deer, and therefore represents an honest advertisement of phenotypic quality.
Little is known about traits under sexual selection in territorial mammals with low sexual size dimorphism. We examined the potential for sexual selection on male body mass and antler length in the European roe deer Capreolus capreolus, a territorial ungulate in which males are less than 10% heavier than females. Independently, both body mass and antler length (irrespective of age) had a positive effect on male yearly breeding success. However, when corrected for body mass, antler length at a given mass only had a slight effect on male breeding success. This suggests that: (1) ‘bigger is better’ and (2) sexual selection is responsible for at least part of the observed variation in body mass and antler length in roe deer. High body mass and large antlers may be advantageous to males for two reasons: (1) they enhance fighting ability and dominance, so allowing males to defend better their territory and hence access mates, and (2) they attract females because they are honest signals of male phenotypic quality. This suggests that, even in weakly dimorphic ungulate species, sexual selection may lead to a marked influence of body mass on male breeding success, as long as body mass is also strongly selected in females.
Summary 1. A major current challenge in ageing research is to understand why senescence rates vary between individuals, populations and species in wild populations. 2. Recent studies clearly illustrate that senescent declines in key demographic and life-history traits can be observed in many wild animal systems. 3. Here, we summarize the key challenges facing researchers working to understand senescence in the wild. We concentrate on: (i) limited data availability, (ii) the substantial individual heterogeneity typical of wild populations, (iii) incomplete capture histories, and (iv) trade-offs across the life span. 4. We discuss analytical methods to overcome these challenges. We advocate the use of Capture- Mark-Recapture models to remove likely bias associated with re-sampling rates of less than one. We also illustrate that ageing trajectories may vary between different traits in wild populations. Wherever possible, researchers should examine ageing patterns in multiple traits. 5. Numerous models are available to describe the rate and shape of senescence in free-living populations, but there is currently little consensus regarding which is most appropriate in analyses of wild organisms. 6. We argue that only longitudinal studies of marked or recognizable individuals provide reliable sources of information in the study of senescence. Senescence is a within-individual process and only longitudinal studies allow researchers to separate within-individual ageing patterns from between-individual heterogeneity. 7. We examine two analytical approaches to measure ageing using longitudinal data from wild populations: a jack-knifing approach, well-suited to modelling survival probability, and a mixed- effects model approach. Both methods control for sources of between-individual heterogeneity to allow more accurate measurement of within-individual ageing patterns.
Animal ecology research could benefit from the measurement of individual morphological traits. In bovids, male horn size often correlates with annual reproductive success, is sensitive to resource abundance, and could be a predictor of survival. However, live captures are costly, involve some risk of injury or substantial disturbance to the animals, and are impossible in many situations. To remotely measure horn growth of free-ranging Alpine ibex (Capra ibex), I designed an aluminum frame that holds parallel laser pointers and a digital camera. I took digital pictures of ibex horns and calculated horn growth based on the fixed distance between the 2 laser points. This simple and accurate technique could benefit many ecological studies that require linear measurements, such as shoulder height, body length, leg length, or fin length. It could also help measure body features (e.g., fur or skin patterns, scars), increasing the reliability of individual photographic identification.
Male contests for access to receptive females are thought to have selected for the larger male body size and conspicuous weaponry frequently observed in mammalian species. However, when females copulate with multiple males within an oestrus, male reproductive success is a function of both pre- and postcopulatory strategies. The relative importance of these overt and covert forms of sexual competition has rarely been assessed in wild populations. The Soay sheep mating system is characterized by male contests for mating opportunities and high female promiscuity. We find that greater horn length, body size and good condition each independently influence a male's ability to monopolize receptive females. For males with large horns at least, this behavioural success translates into greater siring success. Consistent with sperm-competition theory, we also find that larger testes are independently associated with both higher copulation rates and increased siring success. This advantage of larger testes emerges, and strengthens, as the number of oestrous females increases, as dominant males can no longer control access to them all. Our results thus provide direct quantitative evidence that male reproductive success in wild populations of mammals is dependent upon the relative magnitude of both overt contest competition and covert sperm competition.
Identifying factors shaping secondary sexual traits is essential in understanding how their variation may influence male fitness. Little information is available on the allocation of resources to antler growth in territorial ungulates with low sexual size dimorphism. We investigated phenotypic and environmental factors affecting both absolute and relative antler size of male roe deer in three contrasting populations in France and Sweden. In the three populations, we found marked age-specific variation in antler size, with an increase in both absolute and relative antler size between yearling and prime-age stages, followed by a decrease (senescence) for males older than 7 years. Antler size increased allometrically with body mass. This increase was particularly strong for senescent males, suggesting the evolution of two reproductive tactics: heavy old males invested particularly heavily in antler growth (potentially remaining competitive for territories), whereas light old males grew small antlers (potentially abandoning territory defense). Finally, environmental conditions had little effect on antler size: only population density negatively affected absolute antler size in one of the three populations. Antler size may therefore provide an honest signal of male phenotypic quality in roe deer. We discuss the implications of these results in terms of territory tenure and mating competition.
Investigating sexual dimorphism is important for our understanding of its influence on reproductive strategies including male-male competition, mate choice, and sexual conflict. Measuring physical traits in wild animals can be logistically challenging and disruptive for the animals. Therefore body size and ornament variation in wild primates have rarely been quantified. Gorillas are amongst the most sexually dimorphic and dichromatic primates. Adult males (silverbacks) possess a prominent sagittal crest, a pad of fibrous and fatty tissue on top of the head, have red crest coloration, their saddle appears silver, and they possess a silverline along their stomach. Here we measure levels of sexual dimorphism and within-male variation of body length, head size, and sexual dichromatism in a population of wild western gorillas using photogrammetry. Digital photogrammetry is a useful and precise method to measure sexual dimorphism in physical traits yielding sexual dimorphism indices (ISD), similar to those derived from traditional measurements of skeletal remains. Silverbacks were on an average 1.23 times longer in body length than adult females. Sexual dimorphism of head size was highest in measures of crest size (max ISD: 60.4) compared with measures of facial height (max ISD: 24.7). The most sexually dimorphic head size measures also showed the highest within-sex variation. We found no clear sex differences in crest coloration but there was large sexual dichromatism with high within-male variation in saddle coloration and silverline size. Further studies should examine if these sexually dimorphic traits are honest signals of competitive ability and confer an advantage in reproductive success.
An animal's social environment can influence individual physiological and reproductive status, which might have implications for the success of ex situ conservation programs. This study investigated the relationship between an individual's position in the social hierarchy, body and antler size, testosterone concentration, and seminal traits in male pampas deer maintained in all-male groups. The study was performed in a semi-captive population in Uruguay during the rut. Data were collected over a 4 year period from 18 different males kept in five groups each of 4-7 adult males (2-7 y old). An index of individual hierarchical success (hierarchical index; HI) was determined based on agonistic interactions with other males within the group. Males positioned higher in the social hierarchy had larger antlers (p = 0.02). In three out of four groups, testosterone was positively correlated with HI (p < 0.0001). Semen vitality was negatively related to HI in three groups (p < 0.0001); however, a positive relationship was observed in another group (p < 0.0001). In conclusion, position in the social hierarchy of semi-captive male pampas deer was positively related to antler size, and in most groups negatively related to semen vitality.
Numerous studies have shown that dyadic fights are regularly disrupted by the intervention of third-party group members. Empirical and theoretical attention with respect to these interventions have focused predominantly on the fitness advantages that accrue to the intervening individual; conversely, little attention has been given to studying the fitness implications of suffering from third-party intervention behaviour. Therefore, we investigated this issue by examining the relationship between variation in individual mating success and suffering third-party interventions during a fallow deer, Dama dama, rut. Mating success was analysed using a ‘hurdle’ model against three explanatory variables: daily variation in suffering an intervention, dominance rank and fight rate. The lower, logistic level of the model indicated a negative interaction between variation in suffering an intervention and fight rate in relation to whether a mating was achieved or not. Further investigation of this interaction showed that the proportion of matings achieved by males declined as interventions suffered increased regardless of whether males had a high (five or more fights per day) investment in fighting. There was no meaningful effect observed in the upper level of the model. We also investigated whether there was evidence for a temporal association between suffering interventions and mating success: two models investigated interventions suffered on a previous day and the cumulative sum of interventions suffered over 2 days in relation to mating success. Neither model showed a meaningful association at the lower or upper level indicating that the effects of intervention behaviour are temporally limited in this population. Our results underline the complex nature of the relationships at play during third-party interventions in relation to mating success. We suggest that there is a need for greater empirical investigation and wider theoretical scrutiny with respect to suffering intervention.
This paper discusses a general framework for smoothing parameter estimation for models with regular likelihoods constructed in terms of unknown smooth functions of covariates. Gaussian random effects and parametric terms may also be present. By construction the method is numerically stable and convergent, and enables smoothing parameter uncertainty to be quantified. The latter enables us to fix a well known problem with AIC for such models, thereby improving the range of model selection tools available. The smooth functions are represented by reduced rank spline like smoothers, with associated quadratic penalties measuring function smoothness. Model estimation is by penalized likelihood maximization, where the smoothing parameters controlling the extent of penalization are estimated by Laplace approximate marginal likelihood. The methods cover, for example, generalized additive models for non-exponential family responses (for example beta, ordered categorical, scaled t distribution, negative binomial and Tweedie distributions), generalized additive models for location scale and shape (for example two stage zero inflation models, and Gaussian location-scale models), Cox proportional hazards models and multivariate additive models. The framework reduces the implementation of new model classes to the coding of some standard derivatives of the log likelihood.
In the area of deer antler evaluation for trophy homologation, as well as in the obtaining of biometric databases for later analysis in the field of Geometric Morphometrics, different linear biometric tools have traditionally been used. In this study we used two sets of antlers from 29 Iberian red deer (Cervus elaphus hispanicus) to develop and establish a new photogrammetric technique which creates the 3D model of the antler using a parametric 3D Computer-Aided Design (CAD). This simple and reliable method for deer hunting trophy homologation was compared with the other two more extensively used methods of antler measurement, the traditional measuring tape and the Articulated Arm Coordinate Measuring Machine (AACMM or CMA). The advantage of this innovative photogrammetric method is the use of only two photographs to obtain both the 3D model and the dimensions required for antler evaluation. A procedure was performed to compare lengths and antler evaluation as hunting trophy. The three methods showed similar reliability, although the photogrammetric process using the 3D CAD system was much faster and more functional than both the traditional measuring tape and Articulated Arm methods. Since this method only requires two photographs per individual, it makes possible the study of a high percentage of antlers in the field. This new photogrammetric method has been successfully used in the biometrics area, but it could become a more extensively used method in this and other fields because of its ease of operation, speed and accuracy of data collection.
A lek is an aggregated male display that females attend for the purpose of fertilization. A male needs to climb the relative
hierarchy to be available for mating when the peak of female estrus occurs. We analyzed the link between timing of lek use
by males in relation to age, phenotype, territoriality, and mating success. For more than a decade, we collected radio-tracking
data and behavioral observations of a lekking mammal, the fallow deer (Dama dama). Competitively stronger males (i.e., older and heavier males with larger antlers) moved to the lek before less competitive
ones. However, an early arrival did not guarantee the territory defense for a longer period nor higher mating success. The
early arrival seemed to be a necessary but not sufficient condition to be a successful male in a lek. In fact, the ability
to defend a territory for longer was related to age, body mass, antler length but not arrival time. We accordingly argue that
males move to the lek early because they need to engage in male–male interactions and scent-marking activities. Successful
males left the lek later than unsuccessful ones. The latter did not attempt to compensate for their low mating success by
remaining in the lek, likely adopting alternative strategies outside of it. Adult males seeking for a chance to defend the
territory and mate have to move to the lek early and stay there until the end of the rut, though this does not guarantee them
a higher mating success.
The first edition of this book has established itself as one of the leading references on generalized additive models (GAMs), and the only book on the topic to be introductory in nature with a wealth of practical examples and software implementation. It is self-contained, providing the necessary background in linear models, linear mixed models, and generalized linear models (GLMs), before presenting a balanced treatment of the theory and applications of GAMs and related models. The author bases his approach on a framework of penalized regression splines, and while firmly focused on the practical aspects of GAMs, discussions include fairly full explanations of the theory underlying the methods. Use of R software helps explain the theory and illustrates the practical application of the methodology. Each chapter contains an extensive set of exercises, with solutions in an appendix or in the book’s R data package gamair, to enable use as a course text or for self-study.
Capture myopathy can be a significant cause of mortality for white-tailed deer (Odocoileus virginianus) and other ungulates. Capture and handling may affect rates of myopathy. During 1988-92 we captured 415 white-tailed deer with rocket-nets and Clover traps as part of a deer mortality study in northcentral Missouri. We placed radiotransmitters on 250 of these deer and assumed capture myopathy was the cause of death for 23 deer that died within 26 days of capture. All myopathy suspects were captured with rocket-nets. We examined differences in 6 handling variables for rocket-net-captured deer that died within 26 days of capture and those that lived more than 26 days. We fit a Cox proportional hazard model to these data to determine the capture variables most affecting myopathy for deer captured with rocket-nets. Survival of captured deer was most influenced by the number of deer captured together. Process times should be minimized to reduce stress to captured deer.
Wildlife research often requires the capture, chemical immobilization, and handling of free-ranging animals. These activities have been documented to yield detrimental effects among some study subjects and may bias study results. We developed an empirical censoring protocol that investigated the postcapture movement rates of 89 white-tailed deer (Odocoileus virginianus) outfitted with global positioning system (GPS) collars to identify data that should be censored from analyses due to postcapture recovery and acclimation. Average daily postcapture movement rates were significantly lower than average daily movement rates for a given calendar day for approximately 14 days postcapture. We tested the influence of biased data in a simple random walk simulation and found that net displacement values were significantly lower after 1,000 iterations when an uncensored data set was used than for data sets that did not include the first 2 weeks of GPS locations. Our results indicate that study animals exhibited sublethal effects of capture, handling, and instrument acclimation (reduced movement rates) for approximately 14 days postcapture. We recommend that all studies involving marked animals assess the influence of capture, handling, and instrumentation on postcapture movements to guard against data sets that are not representative of normal movement behavior. Inclusion of these data in movement analyses may bias results, especially when data sets are small (<90 days).
Abstract Capture-related injuries or deaths of wildlife study subjects pose concerns to researchers, from considerations for animal welfare to inflated project costs and biased data. Capture myopathy (CM) is an injury that can affect an animal's survival ≤30 days postrelease, but is often difficult to detect without close monitoring and immediate necropsy. We evaluated the influence of capture and handling on postcapture movement in an attempt to characterize movement rates of animals suffering from CM. We captured and global positioning system-collared 95 white-tailed deer (Odocoileus virginianus) in central and northern New York during 2006-2008. Six juveniles died within 30 days postrelease, and necropsy reports indicated that two suffered CM (2%). We compared postcapture movement rates for juveniles that survived >30 days with those that died ≤30 days postcapture. Survivor movement rates (43.74 m/hr, SD = 3.53, n = 28) were significantly higher than rates for deer that died within 30 days (17.70 m/hr, SD = 1.57, n = 6) (P<0.01). Additionally, movement rates of juveniles that died of CM (15.1 m/hr) were 5.1 m/hr lower than those for juveniles that died of other causes ≤30 days postcapture (20.2 m/hr), but we were unable to evaluate this statistically because of insufficient sample size. We found no difference in vital rates (temperature, heart rate, respiration rate) during handling between survivors and juveniles that died within 30 days postcapture but observed that survivors were in better body condition at capture. These results suggest that deer likely to die within the 30-day CM window can be identified soon after capture, provided that intensive movement data are collected. Further, even if necropsy reports are unavailable, these animals should be censored from analysis because their behavior is not representative of movements of surviving animals.
New insights into anti-predator adaptations and ways of quantifying antler mass in relation to neonatal investment allow a test of the hypothesis that antler size in male deer tracks the inherent reproductive capacity in females. Cursorialism (speedy and enduring running) as an anti-predator strategy maximizes perinatal investment by the female. In deer it leads to maximum antler size in males. In saltatorial hiders (species that avoid detection by hiding and escape by rapid leaping over obstacles and by taking cover), neonates secret themselves away in cover. This reduces the need for perinatal investment, or for large antler size in males. The capacity to spare nutrients from body growth is reflected in females in reproduction and in males in antler growth which permits females to choose males with the best capacity to spare nutrients from growth, or with the best capacity to forage. Female choice is expected to be proportional to the need of neonates to run from predators soon after birth. Courtship, but not dominance displays by male deer, varies interspecifically in proportion to antler size.
A central aim of the study of animal communication is to identify the mode and content of information transferred between individuals. The lateral presentation of the antler palm between male fallow deer has been described as either a signal of individual quality or an attempt to avoid fighting. In the first case two phenotypic features have been proposed by which transmission of individual quality may be facilitated. These are antler size and antler symmetry. The alternative hypothesis proposes that the lateral presentation of antlers occurs as a consequence of averting a threatening posture and may signify a reluctance to fight. We examined whether mature fallow deer use lateral palm presentation as a display during fights to indicate antler size and symmetry. We found no relationship between presentation rate of the antler and antler size and symmetry. Furthermore, males did not preferentially present their larger antler to their opponent. We also investigated whether the rate at which males presented antlers laterally during a fight was related to their ability to win the fight. Our results show that the male who performed more presentations during a fight was more likely to lose it. There were behavioural differences in the way in which a bout of presentation ended; subsequent losers tended to turn their body away from their opponent and subsequent winners tended to lower their antlers to an opponent which we interpret as an invitation to continue fighting. We conclude that the lateral palm presentation serves to de-escalate fighting between mature fallow deer. It is not a mechanism by which to communicate individual quality but rather an indication that a male is less committed to continuing investment in the current contest.
The quantification of nutritional status (e.g., total body fat) of animals is difficult, because the linear dimension (body length) required for the calculation of proxy parameters, such as the physique or body mass indices, cannot be measured without capture. One solution is photogrammetry of body length, provided the following two criteria are met: (1) the camera axes and subject are oriented vertically, and (2) anatomical landmarks are easily identified with low measurement error. By modifying Mori's (Primates 20:371-397, 1979) approach, we devised an accurate photogrammetric method that uses a horizontal bar with an attached ruler for the monkey to traverse, and the anatomical landmarks of the eye and upper border of the ischial callosity to measure body length. We tested the applicability of this method on 11 adult female, habituated, free-ranging Japanese macaques (Macaca fuscata). Somatometric body length (crown-rump length and anterior trunk length) was statistically compared with the body length obtained using photogrammetry. The significant correlation of the photogrammetric body length with each somatometric measurement verified that the former could be employed to calculate various indices that are used to characterize fat mass (nutritional status) in Japanese macaques. The advantages and disadvantages of photogrammetry are also discussed.
To investigate a possible link of malignant hyperthermia to capture myopathy, between June 1990 and July 1993 we anesthetized four black-tailed deer (Odocoileus hemionus columbianus) and challenged them with halothane and succinylcholine. Halothane had no significant effect on oxygen consumption. Succinylcholine significantly (P < 0.05) increased cardiac output (mean +/- SD), from 2.94 +/- 1.05 l/min to 5.26 +/- 1.79 l/min, and oxygen consumption, from 5.5 +/- 2.1 ml/kg/min to 10.1 +/- 2.9 ml/kg/min. Muscle biopsy specimens tested for malignant hyperthermia susceptibility responded normally to halothane and caffeine. We conclude that these deer did not experience malignant hyperthermia; suggesting no link to capture myopathy.
Representation of generalized additive models (GAM's) using penalized regression splines allows GAM's to be employed in a straightforward manner using penalized regression methods. Not only is inference facilitated by this approach, but it is also possible to integrate model selection in the form of smoothing parameter selection into model fitting in a computationally efficient manner using well founded criteria such as generalized cross-validation. The current fitting and smoothing parameter selection methods for such models are usually effective, but do not provide the level of numerical stability to which users of linear regression packages, for example, are accustomed. In particular the existing methods cannot deal adequately with numerical rank deficiency of the GAM fitting problem, and it is not straightforward to produce methods that can do so, given that the degree of rank deficiency can be smoothing parameter dependent. In addition, models with the potential flexibility of GAM's can also present practical fitting difficulties as a result of indeterminacy in the model likelihood: Data with many zeros fitted by a model with a log link are a good example. In this article it is proposed that GAM's with a ridge penalty provide a practical solution in such circumstances, and a multiple smoothing parameter selection method suitable for use in the presence of such a penalty is developed. The method is based on the pivoted QR decomposition and the singular value decomposition, so that with or without a ridge penalty it has good error propagation properties and is capable of detecting and coping elegantly with numerical rank deficiency. The method also allows mixtures of user specified and estimated smoothing parameters and the setting of lower bounds on smoothing parameters. In terms of computational efficiency, the method compares well with existing methods. A simulation study compares the method to existing methods, including treating GAM's as mixed models.
The intensity of sexual selection predicts weapon size in male bovids
- J Bro-Jorgensen
- D Chapman
- N Chapman
Bro-Jorgensen, J. (2007). The intensity of sexual selection predicts weapon size in male bovids.
Evolution, 61(6), 1316-1326. doi:10.1111/j.1558-5646.2007.00111.x
Chapman, D., & Chapman, N. (1997). Fallow Deer: Their History, Distribution and Biology (2 ed.).
Machynlleth, Wales: Coch-y-Bonddu Books.
Mountain goats: ecology, behavior, and conservation of an alpine ungulate
- J W Durban
- K M Parsons
Durban, J.W. & Parsons, K.M. (2006). Laser-metrics of freeranging killer whales. Marine Mammal Science 22, 735.
Festa-Bianchet, M. & Côté, S.D. (2008) Mountain goats:
ecology, behavior, and conservation of an alpine ungulate.
Washington, DC: Island Press.
Fallow deer: their history, distribution and biology
- D Chapman
- N Chapman
Chapman, D. & Chapman, N. (1997) Fallow deer: their history,
distribution and biology. 2nd edn. Machynlleth, Wales: Cochy-Bonddu Books.
Hierarchical status and body traits and reproductive characteristics of male pampas deer (Ozotoceros bezoarticus) maintained in all-male groups
- C Vanpe
- J M Gaillard
- P Kjellander
- A Mysterud
- P Magnien
- D Delorme
- G Van Laere
- F Klein
- O Liberg
- A J M Hewison
- M Villagran
- F Beracochea
- L Bartos
- R Ungerfeld
Vanpe, C., Gaillard, J.M., Kjellander, P., Mysterud, A.,
Magnien, P., Delorme, D., Van Laere, G., Klein, F., Liberg,
O. & Hewison, A.J.M. (2007). Antler size provides an honest
signal of male phenotypic quality in roe deer. Am. Nat. 169,
481.
Villagran, M., Beracochea, F., Bartos, L. & Ungerfeld, R.
(2018). Hierarchical status and body traits and reproductive
characteristics of male pampas deer (Ozotoceros bezoarticus)
maintained in all-male groups. Appl. Anim. Behav. Sci. 207,
116.
Willisch, C.S., Marreros, N. & Neuhaus, P. (2013). Longdistance photogrammetric trait estimation in free-ranging
animals: A new approach. Mamma. Biol. 78, 351.