Mark-recapture Methodology Research Articles

A Cretaceous peak in family-level insect diversity estimated with mark-recapture methodology.

The history of insects' taxonomic diversity is poorly understood. The two most common methods for estimating taxonomic diversity in deep time yield conflicting results: the 'range through' method suggests a steady, nearly monotonic increase in family-level diversity, whereas 'shareholder quorum subsampling' suggests a highly volatile taxonomic history with family-level mass extinctions occurring repeatedly, even at the midpoints of geological periods. The only feature shared by these two diversity curves is a steep increase in standing diversity during the Early Cretaceous. This apparent diversification event occurs primarily during the Aptian, the pre-Cenozoic interval with the most described insect occurrences, raising the possibility that this feature of the diversity curves reflects preservation and sampling biases rather than insect evolution and extinction. Here, the capture-mark-recapture (CMR) approach is used to estimate insects' family-level diversity. This method accounts for the incompleteness of the insect fossil record as well as uneven sampling among time intervals. The CMR diversity curve shows extinctions at the Permian/Triassic and Cretaceous/Palaeogene boundaries but does not contain any mass extinctions within geological periods. This curve also includes a steep increase in diversity during the Aptian, which appears not to be an artefact of sampling or preservation bias because this increase still appears when time bins are standardized by the number of occurrences they contain rather than by the amount of time that they span. The Early Cretaceous increase in family-level diversity predates the rise of angiosperms by many millions of years and can be better attributed to the diversification of parasitic and especially parasitoid insect lineages.

From Transient to Sedentary? Changes in the Home Range Size and Environmental Patterns of Movements of European Eels (Anguilla anguilla) in a Mediterranean River

Abstract: The habitat use of eels during the development of sedentary behavior, which depends on the animals’ body size, is unknown. Our objective was to analyze, for two years, the changes in the home range of a population of European eel (Anguilla anguilla, Linnaeus, 1758) in Southern Europe in relation to the animals’ body length (TL), and the influence of environmental factors (water temperature and flow) on the local movements of this population through observation of their sedentary behavior. We used a previously-validated mark–recapture methodology, obtaining a low deviation in the estimation of the extension of the eels’ movements. Our results revealed relatively short movements in relation to other populations, and we hypothesize that this could be related to the high habitat diversity and low eel population density in the study area. The home range size showed a high variability and dispersion among the smallest eels, however, as TL increased, the variability of home range size decreased, and home ranges were larger. These changes could be associated with the acquisition of a sedentary lifestyle. Once eels had become sedentary, an environmental pattern was observed between their movements and the water temperature and flow, with larger movements observed as the flow increased and water temperature decreased. This suggests that the temporal and spatial scales of observation are of crucial importance for monitoring eel populations and for the study of population size structure, population dynamics, and biology, which can be used to improve conservation strategies.

TRYPANOSOMA CRUZI IN FREE-RANGING MAMMALIAN POPULATIONS IN SOUTH TEXAS, USA.

Chagas disease, also known as American trypanosomiasis, is caused by the flagellate protozoan Trypanosoma cruzi. It is a significant health concern in South and Central America, where millions of people are infected or at risk of infection, and is an emerging health concern in the US. The occurrence of Chagas disease in natural environments is supported by mammal host species, but those primary species may vary based on geographic location. In South Texas, the primary host species for the disease is poorly understood, and required a field study to determine the spatial distribution of T. cruzi prevalence in free-ranging mammals. Our study objectives were to determine the spatial distribution and prevalence of T. cruzi parasites in free-ranging mammals. We compared T. cruzi prevalence among species, among vegetative communities, and among different topographies (i.e., floodplain versus upland). From December 2011 through December 2013, 450 blood and tissue samples from geolocated free-ranging wildlife mammal species were analyzed with the use of polymerase chain reaction to detect protozoan T. cruzi DNA. We also calculated mammal abundance with the use of mark-recapture methodology and recorded capture-site characteristics such as vegetation structure. We found that animals in grasslands had a significantly lower infection rate when summed across all species compared with animals in dense hardwoods and semi-improved woodlands (P=0.001). A higher percentage of infections were found in the lower-elevation floodplain-65% (28/43) of animals sampled, compared to upland areas-25% (9/36) of animals sampled. Our study suggested that common free-ranging meso-mammals supported T. cruzi in natural environments and are of public health concern in South Texas. Mitigation strategies should consider a range of management activities to include vegetation management, selective application of insecticides, and changes in human behavior in high-risk areas.

Use of Photo-Identification and Mark-Recapture Methodology to Assess Basking Shark (Cetorhinus maximus) Populations.

Following centuries of exploitation, basking sharks (Cetorhinus maximus) are considered by IUCN as Endangered in the Northeast Atlantic, where they have now been substantially protected for over two decades. However, the present size of this population remains unknown. We investigated the use of photo-identification of individuals’ dorsal fins, combined with mark-recapture methodology, to investigate the size of populations of basking shark within the west coast of Scotland. From a total of 921 encounters photographed between 2004 and 2011, 710 sharks were found to be individually identifiable based on dorsal fin damage and natural features. Of these, only 41 individuals were re-sighted, most commonly both within days of, and close to the site of, the initial encounter. A smaller number were re-sighted after longer periods of up to two years. A comparison of the distinguishing features of individuals on first recording and subsequent re-sighting showed that in almost all cases these features remained little changed, suggesting the low re-sighting rate was not due to a loss of distinguishing features. Because of the low number of re-sighting we were not able to produce reliable estimates for the long-term regional population. However, for one 50 km diameter study area between the islands of Mull, Coll and Tiree, we were able to generate closed-population estimates for 6–9 day periods in 2010 of 985 (95% CI = 494–1683), and in 2011 of 201 (95% CI = 143–340). For the same 2011 period an open-population model generated a similar estimate of 213 (95% CI = 111–317). Otherwise the low rate and temporal patterning of re-sightings support the view that such local basking shark populations are temporary, dynamic groupings of individuals drawn from a much larger regional population than previously supposed. The study demonstrated the feasibility and limitations of photo-identification as a non-invasive technique for identifying individual basking sharks.

Survival and abundance of short‐finned pilot whales in the archipelago of Madeira, NE Atlantic

AbstractEstimates of population parameters for the short‐finned pilot whale, Globicephala macrorhynchus, are scarce in literature, contributing to an International Union for Conservation of Nature (IUCN) status of Data Deficient. In this study, photo‐identification data collected over 7 yr from Madeira were used to estimate for the first time survivorship, capture probability, and abundance in this species using mark‐recapture methodology. The Cormack‐Jolly‐Seber model estimated that the adult island‐associated (i.e., resident and regular visitor) whales had a constant survival rate of 0.960 (95% CI: 0.853–0.990) and an annual capture probability varying between 0.372 (CI: 0.178–0.619) and 0.843 (CI: 0.619–0.947). A parameterization of the Jolly‐Seber model estimated that 140 island‐associated whales (CI: 131–151) used the area throughout the course of the study. Based on a closed population model, the most precise (lower CV) annual estimate of the total number of pilot whales using the southern and eastern waters of Madeira (~900 km2) in a 3 mo period covering summer/autumn was 334 animals (CI: 260–437). No trend was observed. Despite including biases, the approach used in this study provided plausible estimates of population parameters, which can contribute to the regional conservation strategies.

Postnatal development in the big-footed bat, Myotis macrodactylus: wing morphology, echolocation calls, and flight

We studied the postnatal development of wing morphology and echolocation calls during flight in a free-ranging population of the big-footed bat, Myotis macrodactylus, using the mark-recapture methodology. Young bats were reluctant to move until 7 days of age and started fluttering at a mean age of 10 days. The wingspan and wing area of pups followed a linear pattern of growth until 22 days of age, by which time the young bats exhibited flapping flight, with mean growth rates of 0.62 mm/day and 3.15 mm2/day, for wingspan and area, respectively, after which growth rates decreased. Pups achieved sustained flight at 40 days of age. Of the three nonlinear growth models (logistic, Gompertz, and von Bertalanffy), the logistic equation provided the best fit to the empirical curves for wingspan and wing area. Neonates emitted long echolocation calls with multiple harmonics. The duration of calls decreased significantly between flutter (19 days) and flight (22 days) stages. The peak and start frequency of calls increased significantly over the 3-week period of development, but the terminal frequency did not change significantly over the development period.

Estimating Sample Size for Landscape-Scale Mark-Recapture Studies of North American Migratory Tree Bats

Concern for migratory tree-roosting bats in North America has grown because of possible population declines from wind energy development. This concern has driven interest in estimating population-level changes. Mark-recapture methodology is one possible analytical framework for assessing bat population changes, but sample size requirements to produce reliable estimates have not been estimated. To illustrate the sample sizes necessary for a mark-recapture-based monitoring program we conducted power analyses using a statistical model that allows reencounters of live and dead marked individuals. We ran 1,000 simulations for each of five broad sample size categories in a Burnham joint model, and then compared the proportion of simulations in which 95% confidence intervals overlapped between and among years for a 4-year study. Additionally, we conducted sensitivity analyses of sample size to various capture probabilities and recovery probabilities. More than 50,000 individuals per year would need to be captured and released to accurately determine 10% and 15% declines in annual survival. To detect more dramatic declines of 33% or 50% survival over four years, then sample sizes of 25,000 or 10,000 per year, respectively, would be sufficient. Sensitivity analyses reveal that increasing recovery of dead marked individuals may be more valuable than increasing capture probability of marked individuals. Because of the extraordinary effort that would be required, we advise caution should such a mark-recapture effort be initiated because of the difficulty in attaining reliable estimates. We make recommendations for what techniques show the most promise for mark-recapture studies of bats because some techniques violate the assumptions of mark-recapture methodology when used to mark bats.

Assessment of the fishing impact on the silver eel stock in the Baltic using survival analysis

Restoration of the depleted stock of the European eel (Anguilla anguilla (L.)) requires anthropogenic impacts to be quantified, reduced, and controlled. In this article, we assess the impact of the silver eel fishery on the Baltic Coast in Sweden, applying survival analysis to 60 years of mark–recapture experiments, involving 8000 recaptures out of 18 000 releases. The hazard of being recaptured (overall 46%) varies along the coast and declined substantially over the decades. But, most notably, the hazard for the individual diminishes strongly after the first kilometres en route. This individualized hazard disqualifies the more traditional mark–recapture methodology, which assumes random recaptures. We advocate the general use of survival analysis for conventional mark–recapture data. The result of our analysis indicates that the impact of the fishery just prior the 2009 fishing restrictions was in the order of 10%—in itself well within sustainability limits, though only but one of the factors contributing to the mortality in the Baltic Sea.

Estimating Abundance of the Endangered Houston Toad on a Primary Recovery Site

Abstract The Griffith League Ranch is one of the primary recovery sites for the endangered Houston toad Bufo (Anaxyrus) houstonensis. New recovery initiatives have recently been implemented to increase Houston toad abundance; however, no robust estimate of population size has been conducted in the last decade of study, nor from this recovery site. To assist with inferences regarding efficacy of current and future management actions, we estimated adult Houston toad abundance on the Griffith League Ranch. Houston toads were sampled at breeding ponds during the 2010 breeding season using a mark–recapture methodology. We analyzed the data using a modified Jolly–Seber open population model in Program MARK. Models were built whereby the probability of capture remained constant, the apparent survival varied with time or was constant, and the probability of entry varied with time. Model averaging was used to account for uncertainty and the derived adult male Houston toad abundance ranged from 201 to 307 individuals. Using a previously determined Griffith League Ranch Houston toad functional sex ratio of 5∶1, we estimated the abundance of the total adult Houston toad population on this primary recovery site to be from 241 to 368 individuals. This study is the first to report a robust abundance estimate of a Houston toad population and provides a foundation for further research to quantify the impact of current and future management actions.

Likelihood-based genetic mark–recapture estimates when genotype samples are incomplete and contain typing errors

Genotypes produced from samples collected non-invasively in harsh field conditions often lack the full complement of data from the selected microsatellite loci. The application to genetic mark–recapture methodology in wildlife species can therefore be prone to misidentifications leading to both ‘true non-recaptures’ being falsely accepted as recaptures (Type I errors) and ‘true recaptures’ being undetected (Type II errors). Here we present a new likelihood method that allows every pairwise genotype comparison to be evaluated independently. We apply this method to determine the total number of recaptures by estimating and optimising the balance between Type I errors and Type II errors. We show through simulation that the standard error of recapture estimates can be minimised through our algorithms. Interestingly, the precision of our recapture estimates actually improved when we included individuals with missing genotypes, as this increased the number of pairwise comparisons potentially uncovering more recaptures. Simulations suggest that the method is tolerant to per locus error rates of up to 5% per locus and can theoretically work in datasets with as little as 60% of loci genotyped. Our methods can be implemented in datasets where standard mismatch analyses fail to distinguish recaptures. Finally, we show that by assigning a low Type I error rate to our matching algorithms we can generate a dataset of individuals of known capture histories that is suitable for the downstream analysis with traditional mark–recapture methods.

Estimating brush-tailed rock-wallaby population size using individual animal recognition

We undertook surveys of brush-tailed rock-wallabies (Petrogale penicillata) at four colonies in Oxley Wild Rivers National Park, north-eastern New South Wales, with the aim of developing a technique based upon individual animal recognition that could be used to obtain robust population estimates for rock-wallaby colonies. We identified individuals on the basis of distinct morphological characters in each colony using visual observations, and used the data within a ‘mark–recapture’ (or sight–resight) framework to estimate population size. More than 37 h of observations were made over 10 sampling days between 18 May and 9 June 2010. We could identify 91.7% of all rock-wallabies that were independently sighted (143 of 156 sightings of 35 animals). A small percentage of animals could not be identified during a visit because they were seen only fleetingly, were in dense cover, or were partly obscured by rock. The number of new animals sighted and photographed declined sharply at the midpoint of the survey, and there was a corresponding increase in resighting of known individuals. Population estimates using the mark–recapture methodology were nearly identical to estimates of total animals seen, suggesting that this method was successful in obtaining a complete census of rock-wallabies in each colony.

Individual differences in reproductive costs examined using multi-state methods

1. Trade-offs among life-history traits are common because individuals have to partition limited resources between multiple traits. Reproductive costs are generally assumed to be high, resulting in reduced survival and fecundity in the following year. However, it is common to find positive rather than negative correlations between life-history traits. 2. Here, we use a data set from the individual-based study of red deer on the Isle of Rum to examine how these costs vary between individuals and at different ages, using multi-state mark-recapture methodology. 3. Females that had reproduced frequently in the past incurred lower costs of reproduction in terms of survival in the following year and were more likely to reproduce in two consecutive years. Older individuals and those that had not reproduced frequently exhibited higher costs. 4. These results highlight the importance of considering heterogeneity and individual quality when examining trade-offs and demonstrate the effectiveness of using detailed long-term data sets to explore life-history strategies using multi-state mark-recapture models.

HIGH SURVIVAL OF IMMATURES IN A LONG-LIVED SEABIRD: INSIGHTS FROM A LONG-TERM STUDY OF THE ATLANTIC PUFFIN (FRATERCULA ARCTICA)

Abstract Survival from fledging to maturity is an important life-history parameter in long-lived species such as seabirds. However, because of the long period of unobservability following fledging, few studies have reported reliable estimates of survival rates for immatures. We estimated survival to maturity of two cohorts of Atlantic Puffin (Fratercula arctica) fledglings from Hornoya in northern Norway using capture–mark–recapture methodology. By considering only juveniles that actually left their nest burrows, we arrived at unbiased estimates of survival rates for immatures. Contrary to many previous studies, annual survival of immatures was not depressed in relation to adult survival. By the age of five years, more than two-thirds of all fledglings are still estimated to be alive. Averaged over this period, annual survival of immatures is estimated as 0.933 (95% confidence interval: 0.806–0.993). This compares to an annual adult survival of 0.943 (0.909–0.965) during the same period. The survival esti...

Mark–resight density estimation for American black bears in Hoopa, California

Accurate and precise population estimates are necessary to answer many management questions, but these estimates are generally unavailable for large carnivores because of their extensive movements, low densities, and secretive natures. These traits also often prevent the bounding of occupied areas necessary to estimate densities. We used a modified Petersen mark–recapture methodology to estimate black bear density in 1998 at 2 study sites on the Hoopa Valley Reservation, California, from mark–resight data. We used culvert traps to capture, radiocollar, and eartag bears, radio telemetry to establish closure, and remote cameras to collect resighting data. We calculated bear densities (90% confidence intervals) of 0.18 (0.09–0.32) and 1.33 (0.54–3.29) bears/km2 on the 2 sites. Knowledge of bear densities can now be incorporated into forest management actions and associated bear control measures on the Hoopa Valley Reservation.

ESTIMATING SPECIES-SPECIFIC SURVIVAL AND MOVEMENT WHEN SPECIES IDENTIFICATION IS UNCERTAIN

Incorporating uncertainty in the investigation of ecological studies has been the topic of an increasing body of research. In particular, mark-recapture methodology has shown that incorporating uncertainty in the probability of detecting individuals in populations enables accurate estimation of population-level processes such as survival, reproduction, and dispersal. Recent advances in mark-recapture methodology have included estimating population-level processes for biologically important groups despite the misassignment of individuals to those groups. Examples include estimating rates of apparent survival despite less than perfect accuracy when identifying individuals to gender or breeding state. Here we introduce a method for estimating apparent survival and dispersal in species that co-occur but that are difficult to distinguish. We use data from co-occurring populations of meadow voles (Microtus pennsylvanicus) and montane voles (M. montanus) in addition to simulated data to show that ignoring species uncertainty can lead to biased estimates of population processes. The incorporation of species uncertainty in mark-recapture studies should aid future research investigating ecological concepts such as interspecific competition, niche differentiation, and spatial population dynamics in sibling species.

Completeness and Validity of Cancer Registration in a Major Public Referral Hospital in Saudi Arabia

The 1994 Saudi National Cancer Registry (NCR), a population-based registry, showed a crude incidence rate (CIR) of 39/100,000 for all cancers in the Saudi population. The low CIR suggested possible under-reporting, especially during the early years of operation. This study as aimed at estimating the number of missed cases due to under-reporting, and to assess the validity of reported data from a major public referral hospital in Riyadh city. We compared cancer cases from the three data sources: medical records (MR), which were the original source of NCR cases; pathology reports (PR); and death certificates (DC). We estimated the missing cancer cases using the capture-recapture method with log-linear models of Fienberg to correct for interdependency between the three data sources. To assess the validity of the data, we reabstracted records of about 8% (39/4760 of previously reported cases from the same hospital. A total of 811 cancer cases were reported through the three sources, i.e., MR 611 (75.3%), PR 639 (78.8%) and DC 204 (25.2%). After fitting a series of log-linear models to the three sources of data, the three sources were found to be statistically dependent. Capture-repcapture method indicated that 384 cases were missed, giving an estimation of 1195 cancer cases to be reported. Using these 1195 estimated cases; the estimated ascertainment rates were 51% for medical records, 53% for pathology reports, 17% for death certificates, and 68% for the aggregated registry. In the validity assessment, major disagreement between the abstracted and reabstracted data was found to be highest for stage of disease (44%), followed by histology code and behavior (25.6%). Minor disagreements were most common for date of diagnosis (36%) and grade (36%). Overall, agreements were highest for laterality (95%), followed by primary site codes (90%) and basis of diagnosis (85%). Agreement of tumor description variables (site, histology, behavior, and stage) was 57%. Cancer registration will require substantial improvements in both completeness of reporting and data quality at the hospital level. Use of multiple data sources and estimation of missed cases will help ensure completeness of case registration.

LEAST TERN CHICK SURVIVAL ON THE LOWER MISSISSIPPI RIVER

Accurate population models for the endangered Interior Least Tern (Sterna antillarum) cannot be generated without age-specific survival estimates. Our purpose was to estimate chick survival from hatching to fledging, for Least Terns nesting at two sites on the Lower Mississippi River in Missouri, using mark-recapture methodology. We banded 110 Least Tern chicks during 1995 on sand island nesting colonies situated at river kilometers (Rkm) 1431 and 1481 on the Lower Mississippi River. We used Program JOLLY to compute survival point estimates, their associated variances, and goodness-of-fit tests for Jolly-Seber open population models (Pollock et al. 1990). The mean daily survival rate for Least Tern chicks at Rkm 1431 was 0.951 (SE = 0.03) with 95% confidence intervals of 0.899–1.003. Mean daily survival rate for Least Tern chicks at Rkm 1481 was 0.972 (SE = 0.03) with 95% confidence intervals of 0.911–1.034. Estimated survival of Least Tern chicks throughout the entire 17-d fledging interval was 0.43 at Rkm 1431 and 0.62 at Rkm 1481. Based on survival rate estimates and number of known pairs producing chicks we estimated 0.72 and 1.0 fledglings/pair were produced at Rkm 1431 and Rkm 1481, respectively.

APPLICATION OF MARK–RECAPTURE MODELS TO ESTIMATION OF THE POPULATION SIZE OF PLANTS

Mark-recapture models have been widely used in ecology to estimate pop- ulation sizes of animals. In contrast, estimation of plant population size has usually been assumed to be much easier. However, detection of individuals is difficult for perennial plants, such as the rare prairie plant Mead's milkweed ( Asclepias meadii), which does not produce aboveground parts every year and lives in dense vegetation where nonflowering stems are hard to observe. In these cases, a count of the number of plants observed in a particular year may greatly underestimate the true population size, just as a count of animals in traps does not adequately estimate the total number of animals in an area. Using a family of closed population models (CAPTURE), we applied mark-recapture methodology to estimate population size of A. meadii. Over a 4-yr period, a total of 129 patches (aggregated collections of stems) was observed, with 124 flowering in at least one year. In any one year, however, the number of flowering patches ranged from 15 to 105. Using model M th of CAPTURE with these data, the estimated number of patches capable of flowering was 219. Although the confidence interval is broad (95% confidence interval of 175-302), these results emphasize that the observed number of patches in any one year, or even over a 4-yr period, underestimates the actual population size.

Adjusting for missed tags in salmon escapement surveys

One of the assumptions in mark-recapture studies is that all tags recovered are correctly identified. In some cases, tags are overlooked, and a subsample of fish previously classified as untagged is examined to look for missed tags. In this paper, a method for estimating the salmon escapement using a mark-recapture methodology after correcting for missed tags is developed. The variance of the revised estimator is derived and the loss of efficiency compared with a Petersen estimate, where no tags are overlooked, is found. Optimal allocation of effort between the initial and second examination is considered. Finally, a numerical example using actual data from the 1994 Fraser River sockeye salmon (Oncorhynchus nerka) season is used to illustrate the results.

Fire and its impact on avian population dynamics

Survival rate, population size, recruitment and probability of capture, derived from a long-term study of 20 passerine species in wet sclerophyll forest near Canberra, were used to measure the impact of a high intensity wildfire which burnt 70% of the study area. The wildfire significantly affected the population size of 13 species for a period of up to six years following the fire. Survival and recruitment were the least sensitive measures of impact and indicated a significant response to fire for only 2 of 10 species. We detected measurable effects of the fire for 17 of the 20 species studied. Many of these species had returned to prefire levels within three years, but for nine species the effects were still apparent six years later. Mark-recapture methodology provides an effective way of measuring the impact of fire regimes in forest environments. Long-term monitoring programmes should be established in fire-prone forest environments to contribute toward our understanding of fire, and its effect on avian populations. Such programmes have resource implications and researchers are urged to encourage the participation of the amateur bird banding community to contribute to such projects.