Jeffrey A. Spendelow

Chapter 3 Modeling Individual Animal Histories with Multistate Capture–Recapture Models

Summary Many fields of science begin with a phase of exploration and description, followed by investigations of the processes that account for observed patterns. The science of ecology is no exception, and recent decades have seen a focus on understanding key processes underlying the dynamics of ecological systems. In population ecology, emphasis has shifted from the state variable of population size to the demographic processes responsible for changes in this state variable: birth, death, immigration, and emigration. In evolutionary ecology, some of these same demographic processes, rates of birth and death, are also the determinants of fitness. In animal population ecology, the estimation of state variables and their associated vital rates is especially problematic because of the difficulties in sampling such populations and detecting individual animals. Indeed, early capture–recapture models were developed for the purpose of estimating population size, given the reality that all animals are not caught or detected at any sampling occasion. More recently, capture–recapture models for open populations were developed to draw inferences about survival in the face of these same sampling problems. The focus of this paper is on multi‐state mark–recapture models (MSMR), which first appeared in the 1970s but have undergone substantial development in the last 15 years. These models were developed to deal explicitly with biological variation, in that animals in different “states” (classes defined by location, physiology, behavior, reproductive status, etc.) may have different probabilities of survival and detection. Animal transitions between states are also stochastic and themselves of interest. These general models have proven to be extremely useful and provide a way of thinking about a remarkably wide range of important ecological processes. These methods are now at a stage of refinement and sophistication where they can readily be used by biologists to tackle a wide range of important issues in ecology. In this paper, we draw together information on the state of the art in multistate mark–recapture methods, explaining the models and illustrating their use. We provide a modeling philosophy and a series of general principles on how to conduct analyses. We cover key issues and features, and we anticipate the ways in which we expect the models to develop in the years ahead. In particular: – MSMR can now be used in a straightforward fashion by population biologists, thanks to the development of sound goodness‐of‐fit procedures, reliable parameter identifiability diagnostics, and robust user‐friendly computer software.Constrained models and model selection procedures can be used in the ANOVA‐like philosophy commonly used over the last 15 years for survival models, to answer a variety of biological questions. We develop as an example a treatment of meadow vole Microtus pennsylvanicus data. – As in survival models, random effects should be an integral part of this philosophy. Some simple approaches to random effects are illustrated. – States can be defined in a very general way, for example, by combining several criteria, such as sites and reproductive states, and can include nonobservable states. We develop as an example a multisite recruitment model of roseate terns Sterna dougallii . – MSMR models appear as a natural framework for combining different sources of information, viewed as different events that can be organized into mutually exclusive alternatives. – With the available developments, MSMR models are becoming a standard tool in population biology, as shown by a rapid growth of their use in the literature. In particular, given the ease with which a variety of constrained models can now be developed, MSMR models appear as less data hungry than was often feared. – MSMR models make it also possible to unify a large array of methodology, and, as such, are both a step towards further unification in a “mother of all” model, and a sound basis for further generalizations. – Future developments concern a variety of generalizations such as the reverse time approach and population size estimation. “Multievent” models, accounting for uncertainty in state determination, and integrated state–space models are key generalizations already in full development.

Estimating Annual Survival and Movement Rates of Adults within a Metapopulation of Roseate Terns

Several multistratum capture-recapture models were used to test various hypotheses about possible geographic and temporal variation in survival, movement, and recapture/resighting probabilities of 2399 adult Roseate Terns (Sterna dougallii) color-banded from 1988 to 1992 at the sites of the four largest breeding colonies of this species in the northeastern USA. Linear-logistic ultrastructural models also were developed to investigate possible correlates of geographic variation in movement probabilities. Based on goodness-of-fit tests and comparisons of Akaikes Information Criterion (AIC) values, the fully parameterized model (Model A) with time- and location-specific survival, movement, and capture probabilities, was selected as the most appropriate model for this metapopulation structure. With almost all movement accounted for, on average >90% of the surviving adults from each colony site returned to the same site the following year. Variations in movement probabilities were more closely associated with the identity of the destination colony site than with either the identity of the colony site of origin or the distance between colony sites. The average annual survival estimates (0.74-0.84) of terns from all four sites indicate a high rate of annual mortality relative to that of other species of marine birds.

Modelling postfledging survival and age-specific breeding probabilities in species with delayed maturity: A case study of Roseate Terns at Falkner Island, Connecticut

We modelled postfledging survival and age-specific breeding probabilities in endangered Roseate Terns ( Sterna dougallii ) at Falkner Island, Connecticut, USA using capture-recapture data from 1988-1998 of birds ringed as chicks and as adults. While no individuals bred as 2-year-olds during this period, about three-quarters of the young that survived and returned as 3-year-olds nested, and virtually all surviving birds had begun breeding by the time they reached 5 years of age. We found no evidence of temporal variation age of first breeding of birds from different cohorts. There was significant temporal variation in the annual survival of adults and the survival over the typical 3-year maturation period of prebreeding birds, with extremely low values for both groups from the 1991 breeding season. The estimated overwinter survival rate (0.62) for adults from 1991-1992 was about three-quarters the usual rate of about 0.83, but the low survival of fledglings from 1991 resulted in less than 25% of the otherwise expected number of young from that cohort returning as breeding birds; this suggests that fledglings suffered a greater proportional decrease in survival than did adults. The survival estimates of young from 1989 and 1990 show that these cohorts were not negatively influenced by the events that decimated the young from 1991, and the young from 1992 and 1993 had above-average survival estimates. The apparent decrease since 1996 in development of fidelity of new recruits to this site is suspected to be due mainly to nocturnal disturbance and predation of chicks causing low productivity.

Variations in growth of Roseate Tern chicks

We measured growth parameters of Roseate Tem (Sterna dougallii) chicks at two contrasting colonies: Bird Island, Massachusetts, and Falkner Island, Connecticut, from 1987 through 1990. Differences in growth parameters among individual chicks are used to explore differences in parental performance, whereas differences in average growth parameters among colonies and years are used to explore differences in average environmental conditions. Chicks were marked at hatching and weighed at one- or two-day intervals. For each chick that survived to fledging, we calculated two measures of growth: linear growth rate and asymptotic mass. There were no significant differences between growth parameters of first-hatched chicks in broods of one and two. Both measures of growth were significantly lower and more variable for second-hatched chicks than for first-hatched chicks. Both measures were significantly positively related to egg mass and negatively related to hatch date. After controlling for these variables, differences between colonies and among years were relatively small and inconsistent. Mean survival of second-hatched chicks was positively correlated with the mean growth rate of survivors across colonies and years. These findings are consistent with a general hypothesis that growth of chicks reflects individual parental performance and parental quality

ESTIMATION OF SEX‐SPECIFIC SURVIVAL FROM CAPTURE–RECAPTURE DATA WHEN SEX IS NOT ALWAYS KNOWN

Many animals lack obvious sexual dimorphism, making assignment of sex difficult even for observed or captured animals. For many such species it is possible to assign sex with certainty only at some occasions; for example, when they exhibit certain types of behavior. A common approach to handling this situation in capture–recapture studies has been to group capture histories into those of animals eventually identified as male and female and those for which sex was never known. Because group membership is dependent on the number of occasions at which an animal was caught or observed (known sex animals, on average, will have been observed at more occasions than unknown-sex animals), survival estimates for known-sex animals will be positively biased, and those for unknown animals will be negatively biased. In this paper, we develop capture–recapture models that incorporate sex ratio and sex assignment parameters that permit unbiased estimation in the face of this sampling problem. We demonstrate the magnitude...

VARIATIONS IN GROWTH OF ROSEATE TERN CHICKS: II. EARLY GROWTH AS AN INDEX OF PARENTAL QUALITY'

We measured growth of Roseate Tern (Sterna dougallii) chicks at a colony in Connecticut in 10 successive years, 1987-1996. Data on body mass during the first 3-4 days of life were fitted to a quadratic regression model, yielding three parameters of early growth for each of 1,551 chicks: mass at hatching, linear growth, and quadratic growth. First chicks in each brood (A-chicks) exceeded second chicks (B-chicks) in each of the three growth parameters; A-chicks from broods of two grew faster during the first 3 days than single chicks. The three parameters of early growth depended upon egg mass, hatch order, hatch date, and year, but not on parental age after controlling for effects of the other vari- ables. The linear and quadratic growth parameters were negatively correlated. Subsequent growth and survival of chicks were predicted by all three parameters of early growth. After controlling for effects of early growth, none of the other variables measured (hatch date, egg mass, parental age, hatching asynchrony, female-female pairing, or trapping) contributed significantly to explaining later growth or survival. Year effects were substantial in only 2 of the 10 years of study. Individual pairs were consistent in performance (as indexed by early growth) in successive years. These results suggest that growth and survival of Roseate Tern chicks are determined primarily by parental quality; much of the information about parental quality is expressed by the time the eggs are laid, and most of it is expressed by the time the chicks are three days old.

Contribution of research to management and recovery of the roseate tern: review of a twelve-year project

-The Northwest Atlantic population of the Roseate Tern (Sterna dougallii) is largely confined to a small breeding area along the northeast coast of the USA between 400 and 420N. This population was listed as endangered in the USA in 1987 because it was dangerously concentrated into a few breeding sites (85% on two islands in the 1980s). The nesting population in the area from Long Island, New York to Cape Cod, Massachusetts has been studied intensively since 1987, in conjunction with a program of management of the breeding colonies. This paper summarizes the results of the research program and discusses the extent to which it has contributed to effective management. The regional population now numbers about 4,000 breeding pairs and has been increasing slowly since 1987, except between 1991 and 1992 when it declined by about 17%. Noteworthy features of the demographic data collected since 1987 are: skewed adult sex-ratio (about 127 F to 100 M), high average productivity (1.0-1.2 fledglings per pair), low annual adult survival (0.83), and probably low survival from fledging to first breeding (about 0.2). This species is a specialized forager and may be limited within this region by the distribution of suitable feeding sites. When this regional population was listed as endangered in 1987, managers postulated that predation and displacement by gulls were important factors limiting numbers and productivity. Research since 1987 has suggested that the primary effect of gulls is to limit the number of secure sites available for nesting, and that high postfledging mortality and skewed sex-ratios are probably more important as limiting factors on population size. Research activities have contributed both directly and indirectly to management of the regional population, but it has taken longer than expected to obtain needed information on demographic parameters, causes of mortality, and other limiting factors. Received 5 February 1999, accepted 18 April 1999.

Predicting chick survival and productivity of Roseate Terns from data on early growth

-Early growth of Roseate Tern (Sterna dougallii) chicks is a strong predictor of chick survival and hence of productivity. Using data from a ten-year study at Falkner Island, Connecticut, we developed discriminant functions to predict chick survival from body-masses measured during the first three days of life. A discriminant function using only the mass of the B-chick (second-hatched in each brood) on day 2 of life yielded predictions of survival (83% correct classification) almost as good as any other. The correct classification rates were consistent across each of the 10 yr of the study. The simplest discriminant function gave good results (84% correct classification) in a limited test with a data set from another site. We derive a formula to estimate the total number of B-chicks raised to fledging from the number of individuals for which the discriminant function predicts survival. Productivity is estimated by assuming that almost all A-chicks (first-hatched in each brood) survive to fledging, and using the discriminant function and the formula to predict the number of B-chicks that survive. In the absence of predation, the resulting estimates of Roseate Tern chick survival and productivity are almost as good as those obtained by more intensive methods, but require less effort and less disturbance. This approach might be useful for other seabird species in which chick survival is determined primarily by parental performance. Received 29 May 1998, accepted 13 October 1998.

Sources of variation in loss rates of color bands applied to adult roseate terns (Sterna dougallii) in the western North Atlantic

ABSTRAcr.-A model-based analysis was done to test several hypotheses concerning the rates of loss of butt-ended color bands placed on adult Roseate Terns (Sterna dougallii) in the western North Atlantic. These birds were captured and color banded from 1987-1991 at four colony sites, and recaptured from 1989-1992 as part of a study of the population dynamics of this species. Two types of color bands, Darvic and celluloid, were used, but only one band type was used for each individual bird. Each bird was given three color bands. The estimated probability that a bird with all color bands present during one breeding season still had all color bands during the next breeding season was 0.87. The analysis provided no evidence that colony site, cohort, calendar year of banding, age of color band, or whether or not the bands were heat-sealed closed, were important sources of variation in band-retention prob

Individual foraging strategies of kleptoparasitic Roseate Terns

Abstract We describe the kleptoparasitic behavior of ten adult Roseate Terns (Sterna dougallii) breeding at a colony at Falkner Island, Connecticut, USA between 1995 and 1998. These birds were considered habitual kleptoparasites because they stole fish repeatedly from other terns in every year they were observed at the site. No other breeding individuals were observed attempting to steal fish during our study. Kleptoparasitic techniques included aerial piracy, ground-based attacks, and deceptive behavior, but with one exception, each individual used one method exclusively. Success varied among individuals, but overall, kleptoparasites obtained prey at a significantly higher rate than did “honest” foragers. Eight of the ten kleptoparasites were females, suggesting a sex-biased tendency in Roseate Terns to engage in this behavior. Our observations indicate that kleptoparasitism by Roseate Terns is a specialized behavior, used regularly by only a few individuals at this breeding colony. This conclusion is consistent with a recent theoretical prediction regarding kleptoparasitism in birds.