Recommendations for photo‐identification methods used in capture‐recapture models with cetaceans

Capture‐recapture methods are frequently employed to estimate abundance of cetaceans using photographic techniques and a variety of statistical models. However, there are many unresolved issues regarding the selection and manipulation of images that can potentially impose bias on resulting estimates. To examine the potential impact of these issues we circulated a test data set of dorsal fin images from bottlenose dolphins to several independent research groups. Photo‐identification methods were generally similar, but the selection, scoring, and matching of images varied greatly amongst groups. Based on these results we make the following recommendations. Researchers should: (1) determine the degree of marking, or level of distinctiveness, and use images of sufficient quality to recognize animals of that level of distinctiveness; (2) ensure that markings are sufficiently distinct to eliminate the potential for “twins” to occur; (3) stratify data sets by distinctiveness and generate a series of abundance estimates to investigate the influence of including animals of varying degrees of markings; and (4) strive to examine and incorporate variability among analysts into capture‐recapture estimation. In this paper we summarize these potential sources of bias and provide recommendations for best practices for using natural markings in a capture‐recapture framework.     

Improved methods for estimating abundance and related demographic parameters from mark‐resight data

Over the past decade, there has been much methodological development for the estimation of abundance and related demographic parameters using mark‐resight data. Often viewed as a less‐invasive and less‐expensive alternative to conventional mark recapture, mark‐resight methods jointly model marked individual encounters and counts of unmarked individuals, and recent extensions accommodate common challenges associated with imperfect detection. When these challenges include both individual detection heterogeneity and an unknown marked sample size, we demonstrate several deficiencies associated with the most widely used mark‐resight models currently implemented in the popular capture‐recapture freeware Program MARK. We propose a composite likelihood solution based on a zero‐inflated Poisson log‐normal model and find the performance of this new estimator to be superior in terms of bias and confidence interval coverage. Under Pollock's robust design, we also extend the models to accommodate individual‐level random effects across sampling occasions as a potentially more realistic alternative to models that assume independence. As a motivating example, we revisit a previous analysis of mark‐resight data for the New Zealand Robin (Petroica australis) and compare inferences from the proposed estimators. For the all‐too‐common situation where encounter rates are low, individual detection heterogeneity is non‐negligible, and the number of marked individuals is unknown, we recommend practitioners use the zero‐inflated Poisson log‐normal mark‐resight estimator as now implemented in Program MARK.     

How has the remnant population of the threatened frog Leiopelma pakeka (Anura: Leiopelmatidae) fared on Maud Island,New Zealand,over the past 25 years?

Despite widespread global reports of declining amphibian populations, supporting long‐term census data are few, limiting opportunities to study changes in numbers and survival over time. However, in New Zealand, for the past 25 years (1983–2008), we studied Leiopelma pakeka, a threatened, terrestrial frog that inhabits rocky boulder banks under forest on Maud Island. Using night sampling at least annually on two 12 × 12 m plots, we had 5390 captures of 1000+ individuals, 327 on one plot (grid 1), 751 on the other (grid 2). The mean (±SE) number of frogs found per night was 11.3 (±0.6) on grid 1 and 25.6 (±1.4) on grid 2. We used capture‐recapture models to estimate population size, proportion of animals remaining beneath the surface and survival rate. The mean (±SE) population estimate was 131 (±14.7) frogs on grid 1 and 367 (±38.7) on grid 2. Over 25 years the estimated population increased on grid 1 and fluctuated on grid 2. Some frogs were captured on most sampling visits, others less often, evidently failing to emerge from cover each visit. Using a combination of open and closed population models, we estimated the mean (±SE) proportion remaining underground was 0.63 (±0.12) on grid 1 and 0.53 (±0.07) on grid 2. Our research represents one of the longest‐run population studies of any frog, and we recorded significant longevity, two males reaching 35+ and 37+ years, a female 34+ years. No significant differences occurred between mean annual survival rates of apparent females and males, or between the two sites. The number of toes clipped for individual identification had little influence on the return rate, once the effect of time of first capture was removed.     

Photographic identification of individuals of a free‐ranging,small terrestrial vertebrate

Recognition of individuals within an animal population is central to a range of estimates about population structure and dynamics. However, traditional methods of distinguishing individuals, by some form of physical marking, often rely on capture and handling which may affect aspects of normal behavior. Photographic identification has been used as a less‐invasive alternative, but limitations in both manual and computer‐automated recognition of individuals are particularly problematic for smaller taxa (<500 g). In this study, we explored the use of photographic identification for individuals of a free‐ranging, small terrestrial reptile using (a) independent observers, and (b) automated matching with the Interactive Individual Identification System (I³S Pattern) computer algorithm. We tested the technique on individuals of an Australian skink in the Egernia group, Slater's skink Liopholis slateri, whose natural history and varied scale markings make it a potentially suitable candidate for photo‐identification. From ‘photographic captures’ of skink head profiles, we designed a multi‐choice key based on alternate character states and tested the abilities of observers — with or without experience in wildlife survey — to identify individuals using categorized test photos. We also used the I³S Pattern algorithm to match the same set of test photos against a database of 30 individuals. Experienced observers identified a significantly higher proportion of photos correctly (74%) than those with no experience (63%) while the I³S software correctly matched 67% as the first ranked match and 83% of images in the top five ranks. This study is one of the first to investigate photo identification with a free‐ranging small vertebrate. The method demonstrated here has the potential to be applied to the developing field of camera‐traps for wildlife survey and thus a wide range of survey and monitoring applications.     

How common is common? Rapidly assessing population size and structure of the frog Mantidactylus betsileanus at a site in east‐central Madagascar

Population‐level data are urgently needed for amphibians in light of the ongoing amphibian extinction crisis. Studies focused on population dynamics are not only important for rare species but also for common species which shape ecosystems to a greater degree than those that are rare. Some of the greatest global amphibian species diversity is found in Madagascar, yet there are few studies on the ecology of frog species on the island. We carried out a mark‐recapture study on the widespread frog Mantidactylus betsileanus (Mantellidae: Mantellinae: Mantidactylus) at two adjacent rainforest sites in east‐central Madagascar to assess its population size and structure. To do so, we validated and implemented an individual identification protocol using photographs of the ventral patterns of frogs and identified individuals with photographic‐matching software. Using this rapid, non‐invasive survey method, we were able to estimate a density of 26 and 28 frogs per 100 m² at each of the two sites sampled. Our results show the rainforests near the village of Andasibe, Madagascar support remarkably high amphibian abundance, helping illustrate the significant ecological role of frogs in this ecosystem. Further, individual frog markings allowed us to develop more precise estimates than traditional survey methods. This study provides a blueprint to augment existing population studies or develop new monitoring programs in Madagascar and beyond.     

Genotyping validates photo‐identification by the head scale pattern in a large population of the European adder (Vipera berus)

Capture‐mark‐recapture procedures are a basic tool in population studies and require that individual animals are correctly identified throughout their lifetime. A method that has become more and more popular uses photographic records of natural markings, such as pigmentation pattern and scalation configuration. As with any other marking tool, the validity of the photographic identification technique should be evaluated thoroughly. Here, we report on a large‐scale double‐marking study in which European adders (Vipera berus) were identified by both microsatellite genetic markers and by the pattern of head scalation. Samples that were successfully genotyped for all nine loci yielded 624 unique genotypes, which matched on a one‐to‐one basis with the individual assignments based on the head scalation pattern. Thus, adders considered as different individuals by their genotypes were also identified as different individuals by their head scalation pattern, and vice versa. Overall, variation in the numbers, shape, and arrangement of the head scales enabled us to distinguish among 3200+ photographed individual snakes. Adders that were repeatedly sequenced genetically over intervals of 2–3 years showed no indication whatsoever for a change in the head scale pattern. Photographic records of 900+ adders that were recaptured over periods of up to 12 years showed a very detailed and precise match of the head scale characteristics. These natural marks are thus robust over time and do not change during an individual's lifetime. With very low frequency (0.3%), we detected small changes in scalation that were readily discernible and could be attributed to physical injury or infection. Our study provides a conclusive validation for the use of photo‐identification by head scale patterns in the European adder.     

Estimating Alpine ibex Capra ibex abundance from photographic sampling

Monitoring procedures for Alpine ibex Capra ibex are limited in habitats with reduced visibility and when physical capture and marking of the animals is not intended. Photographic sampling, involving using camera‐trap data and identifying ibex from natural markings, was adopted with capture‐recapture models to estimate the abundance of ibex in Austria. The software CAPTURE's model produced an average capture probability of 0.44 with an estimate of 34–51 ibex and a mean population size of 38 ibex. This first study showed the applicability of photographic capture‐recapture techniques to estimate the abundance of ibex based on their natural markings.     

Effect of juvenile hormone on senescence in males with terminal investment

Senescence, a decline in survival and reproductive prospects with age, is controlled by hormones. In insects, juvenile hormone (JH) is involved in senescence with captive individuals, but its effect under natural conditions is unknown. We have addressed this gap by increasing JH levels in young and old wild males of the damselfly Hetaerina americana. We assessed survival in males that were treated with a JH analogue (methoprene), which is known to promote sexual activity, and an immune challenge, which is known to promote terminal investment in reproduction in the studied species. We replicated the same procedure in captivity (to control for environmental variation), where males were deprived of any activity or food. We expected old males to show the lowest survival after being treated with JH and immune‐challenged, because the effect of terminal investment on senescence would be exacerbated by JH. However, this should be the case for wild animals, but not for captive animals, as the effects of JH and immune challenge should lead to an increase in high energetic‐demanding activities only occurring in the wild. Old animals died sooner compared with young animals in both the wild and captivity, confirming that males are subject to senescence. In wild but not captive animals, JH decreased survival in young males and increased it in old males, confirming that JH is sensitive to the environment when shaping animal senescence. Immune challenge had no effect on survival, suggesting no effect of terminal investment on senescence. Additionally, contrary to the expected effects of terminal investment, with an immune challenge, recapture rates increased in young males and decreased in old males. Our results show that male senescence in the wild is mediated by JH and that terminal investment does not cause senescence. One explanation is that animals undergoing senescence and terminal investment modify their feeding behaviour to compensate for their physiological state.     

Spatial capture–recapture models allowing Markovian transience or dispersal

Spatial capture–recapture (SCR) models are a relatively recent development in quantitative ecology, and they are becoming widely used to model density in studies of animal populations using camera traps, DNA sampling and other methods which produce spatially explicit individual encounter information. One of the core assumptions of SCR models is that individuals possess home ranges that are spatially stationary during the sampling period. For many species, this assumption is unlikely to be met and, even for species that are typically territorial, individuals may disperse or exhibit transience at some life stages. In this paper we first conduct a simulation study to evaluate the robustness of estimators of density under ordinary SCR models when dispersal or transience is present in the population. Then, using both simulated and real data, we demonstrate that such models can easily be described in the BUGS language providing a practical framework for their analysis, which allows us to evaluate movement dynamics of species using capture–recapture data. We find that while estimators of density are extremely robust, even to pathological levels of movement (e.g., complete transience), the estimator of the spatial scale parameter of the encounter probability model is confounded with the dispersal/transience scale parameter. Thus, use of ordinary SCR models to make inferences about density is feasible, but interpretation of SCR model parameters in relation to movement should be avoided. Instead, when movement dynamics are of interest, such dynamics should be parameterized explicitly in the model.     

Stabilizing natural selection on the early expression of a secondary sexual trait in a passerine bird

Natural selection is a central tenet of evolutionary theory, yet the estimation of the direction and intensity of selection remains problematic. Here, we assess the strength of selection on the early expression of a secondary sexual ornament, bill colour, in male European blackbirds (Turdus merula) using 5 years of capture-mark-recapture (CMR) data. The best-fitting model consisted of a quadratic relationship between survival rate and bill colour, indicating stabilizing natural selection on the early expression of a secondary sexual trait. There was no evidence for sexual selection acting on bill colour in the first year. We suggest that the consideration of early selection and the adoption of refined statistical methods may reveal patterns of selection in the wild that have, as yet, remained undetected.     

Estimating the proportion of identifiable individuals and group sizes in photographic identification studies

Simple Bayesian statistical models are introduced to estimate the proportion of identifiable individuals and group sizes in photographic identification, or photo‐ID, studies of animals that are found in groups. The models require a simple random photographic sampling of animals, where the photographic captures are treated as sampling with replacement within each group. The total number of images, including those that cannot be identified, and the number of images that contain identifiable individuals are used to make inference about the proportion of identifiable individuals within each group and as the population when a number of groups are sampled. The numbers of images for individuals within each group are used to make inference about the group size. Based on analyses of simulated and real data, the models perform well with respect to accuracy and precision of posterior distributions of the parameters. Widths of posterior intervals were affected by the number of groups sampled, sampling duration, and the proportion of identifiable individuals in each group that was sampled. The structure of the models can accommodate covariates, which may affect photographic efficiency, defined in this study as the probability of photographically capturing individuals.     

Apparent survival of tropical birds in a wet,premontane forest in Costa Rica

Despite the importance of tropical birds in the development of life history theory, we lack information about demographic rates and drivers of population dynamics for most species. We used a 7‐year (2007–2013) capture‐mark‐recapture dataset from an exceptionally wet premontane forest at mid‐elevation in Costa Rica to estimate apparent survival for seven species of tropical passerines. For four of these species, we provide the first published demographic parameters. Recapture probabilities ranged from 0.21 to 0.53, and annual estimates of apparent survival varied from 0.23 to 1.00. We also assessed the consequences of inter‐annual variation in rainfall on demographic rates. Our results are consistent with inter‐annual rainfall increasing estimates of apparent survival for two species and decreasing estimates for three species. For the three species where we could compare our estimates of apparent survival to estimates from drier regions, our estimates were not consistently higher or lower than those published previously. The temporal and spatial variability in demographic rates we document within and among species highlights the difficulties of generalizing life history characteristics across broad biogeographic gradients. Most importantly, this work emphasizes the context‐specific role of precipitation in shaping tropical avian demographic rates and underscores the need for mechanistic studies of environmental drivers of tropical life histories.     

oSCR: a spatial capture–recapture R package for inference about spatial ecological processes

Spatial capture–recapture (SCR) methods have become widely applied in ecology. The immediate adoption of SCR is due to the fact that it resolves some major criticisms of traditional capture–recapture methods related to heterogeneity in detectabililty, and the emergence of new technologies (e.g. camera traps, non‐invasive genetics) that have vastly improved our ability to collection spatially explicit observation data on individuals. However, the utility of SCR methods reaches far beyond simply convenience and data availability. SCR presents a formal statistical framework that can be used to test explicit hypotheses about core elements of population and landscape ecology, and has profound implications for how we study animal populations. In this software note, we describe the technical basis and analytical workflow of oSCR, an R package for analyzing spatial encounter history data using a multi‐session sex‐structured likelihood. The impetus for developing oSCR was to create an accessible and transparent analysis tool that allows users to conveniently and intuitively formulate statistical models that map directly to fundamental processes of interest in spatial population ecology (e.g. space use, resource selection, density and connectivity). We have placed an emphasis on creating a transparent and accessible code base that is coupled with a logical workflow that we hope stimulates active participation in further technical developments.     

High juvenile annual survival probabilities in Southern Rockhopper Penguins Eudyptes chrysocome are independent of individual fledging traits

Juvenile survival is an important demographic parameter. Southern Rockhopper Penguins Eudyptes chrysocome have undergone a dramatic population decline in the past century across their distribution, but the demographic processes are poorly understood. To estimate juvenile annual survival probabilities, Rockhopper Penguin chicks from two cohorts on New Island, Falkland Islands, were marked with transponders and recorded in subsequent years using an automated gateway. We first estimated annual survival and detection probabilities using a Cormack‐Jolly‐Seber (CJS) model, and found that both probabilities were extremely high (81% in the first and 98% in the second, third and fourth years of life), even in comparison with adult birds. Because detection probability after 3 years was effectively 1, and our sample size (n = 114) was too small to explore the effects of individual traits on survival in a CJS model, we assessed whether sex, cohort, body mass and laying sequence affected whether juveniles returned to the colony during their first 3 years of life using a simple generalized linear model that assumed perfect detection. Juveniles from the first cohort and males showed a higher return probability than juveniles from the second cohort and females. There was no clear effect of fledging body mass on return rate, probably related to the favourable environmental conditions during the study period. The laying sequence did not markedly affect the return probability of chicks, indicating that, once fledged, first‐laid A‐chicks have the same probability to return as second‐laid B‐chicks despite a much larger initial maternal investment in B‐eggs in this species. This study demonstrates extraordinarily high juvenile survival probabilities and will help to understand the recent changes in the population dynamics of the Falkland Islands Southern Rockhopper Penguins.     

Apomorphine as an emetic for insectivorous songbirds: effectiveness and post‐release effects on survival and mass change

Emetics can be used to obtain food samples from birds, but they can harm birds during or after treatment. Studies to date suggest that apomorphine is a safe emetic for songbirds, but information is needed about possible post‐release deleterious effects. From March to July 2012, we collected food samples from insectivorous songbirds using apomorphine. We treated 67 Moustached Warblers (Acrocephalus melanopogon), 56 Reed Warblers (Acrocephalus scirpaceus), 15 Great Reed Warblers (Acrocephalus arundinaceus), and 12 Savi's Warblers (Locustella luscinoides). Effectiveness in inducing regurgitation was high (76.7%) and varied among species, being significantly more effective with Reed Warblers (91.1%). No birds died during treatment. To check for possible post‐release negative effects, we considered 53 treated Moustached Warblers and 37 treated Reed Warblers and selected an equal number of untreated individuals (simply captured, banded, and measured). We found no support for differences in survival or recapture probabilities between treated and untreated birds of either species within 21 d after administering apomorphine. We calculated body mass changes of all Moustached Warblers subsequently recaptured (within 21 d) and found no difference between treated (N = 8) and untreated (N = 22) birds, suggesting normal foraging activity after release. Our results suggest that apomorphine is a safe emetic, with no negative effect on survival at least in the short term. The effectiveness of apomorphine with insectivorous songbirds in our study contrasts with the results of some previous studies and confirms the differences in effectiveness among different taxa of songbirds. As with differences in effectiveness among species in our study, this variability in sensitivity to the emetic could be caused by morphological and physiological differences among different taxa.     

Reintroducing a keystone burrowing rodent to restore an arid North American grassland: challenges and successes

Prairie dogs (Cynomys spp.) are important ecosystem engineers in North America's central grasslands, and are a key prey base for numerous predators. Prairie dogs have declined dramatically across their former range, prompting reintroduction efforts to restore their populations and ecosystem functions, but the success of these reintroductions is rarely monitored rigorously. Here, we reintroduced 2,400 Gunnison's prairie dogs (C. gunnisoni) over a period of 6 years to the Sevilleta National Wildlife Refuge, in central New Mexico, U.S.A., a semi‐arid grassland ecosystem at the southern edge of their range. We evaluated the population dynamics of prairie dogs following their reintroduction, and their consequent effects on grassland vertebrates. We found postrelease survival of prairie dogs stabilized at levels typical for the species (ca. 50%) after approximately 1 month, while average annual recruitment was ca. 0.35 juveniles per female, well below what was required for a self‐sustaining, stable population. Extreme drought conditions during much of the study period may have contributed to low recruitment. However, recruitment increased steadily over time, indicating that the reintroduced colony may simply need more time to establish in this arid system. We also found well‐known associates of prairie dog colonies, such as American badgers (Taxidea taxus) and burrowing owls (Athene cunicularia), were significantly more common on the colonies than off. After 7 years, we have yet to meet our goal of establishing a self‐sustaining population of Gunnison's prairie dogs in this semi‐arid grassland. But despite the uncertainty and challenges, our work shows that reestablishing keystone species can promote ecosystem restoration.     

genecap: a program for analysis of multilocus genotype data for non‐invasive sampling and capture‐recapture population estimation

We created genecap to facilitate analysis of multilocus genotype data for use in non‐invasive DNA sampling and genetic capture‐recapture studies. genecap is a Microsoft excel macro that uses multilocus genetic data to match samples with identical genotypes, calculate frequency of alleles, identify sample genotypes that differ by one and two alleles, calculate probabilities of identity, and match probabilities for matching samples. genecap allows the user to include background data and samples with missing genotypes for multiple loci. Capture histories for each user‐defined sampling period are output in formats consistent with commonly employed population estimation programs.     

Survival probability in a small shorebird decreases with the time an individual carries a tracking device

Effects of tracking devices on survival are generally considered to be small. However, most studies to date have been conducted over a time-period of only one year, neglecting the possible accumulation of negative effects and consequently stronger negative impacts on survival when the individuals have carried the tracking devices for longer periods. We studied the effects of geolocators in a closely monitored and colour-ringed southern dunlin Calidris alpina schinzii population breeding in Finland. Our capture–recapture data spans 2002–2018 and includes individual histories of 338 colour-ringed breeding adult dunlins (the term ‘recapture' includes resightings of colour-ringed and individually recognizable birds). These data include 53 adults that were fitted with leg-flag mounted geolocators in 2013–2014. We followed their fates together with other colour-ringed birds not equipped with geolocators until 2018. Geolocators were removed within 1–2 years of attachment or were not removed at all, which allowed us to examine whether carrying a geolocator reduces survival and whether the reduction in survival becomes stronger when geolocators are carried for more than one year. We fit multi-state open population capture–recapture models to the encounter history data. When assessing geolocator effects, we accounted for recapture probabilities, time since marking, and sex and year effects on survival. We found that carrying a geolocator reduced survival, which contrasts with many studies that examined return rates after one year. Importantly, survival declined with the time the individual had carried a geolocator, suggesting that the negative effects accumulate over time. Hence, the longer monitoring of birds carrying a geolocator may explain the difference from previous studies. Despite their larger mass, females tended to be more strongly affected by geolocators than males. Our results warrant caution in conducting tracking studies and suggest that short-term studies examining return rates may not reveal all possible effects of tracking devices on survival.