Arpat Ozgul

Coupled dynamics of body mass and population growth in response to environmental change

Environmental change has altered the phenology, morphological traits and population dynamics of many species. However, the links underlying these joint responses remain largely unknown owing to a paucity of long-term data and the lack of an appropriate analytical framework. Here we investigate the link between phenotypic and demographic responses to environmental change using a new methodology and a long-term (1976–2008) data set from a hibernating mammal (the yellow-bellied marmot) inhabiting a dynamic subalpine habitat. We demonstrate how earlier emergence from hibernation and earlier weaning of young has led to a longer growing season and larger body masses before hibernation. The resulting shift in both the phenotype and the relationship between phenotype and fitness components led to a decline in adult mortality, which in turn triggered an abrupt increase in population size in recent years. Direct and trait-mediated effects of environmental change made comparable contributions to the observed marked increase in population growth. Our results help explain how a shift in phenology can cause simultaneous phenotypic and demographic changes, and highlight the need for a theory integrating ecological and evolutionary dynamics in stochastic environments.

The Dynamics of Phenotypic Change and the Shrinking Sheep of St. Kilda

Little Lambs In changing environments, ecological and evolutionary dynamics are intimately intertwined. However, understanding the dynamics of phenotypic traits under natural conditions is still rudimentary. Ozgul et al. (p. 464; published online 2 July) dissected the dynamics of a phenotypic trait in the context of the contributing ecological and evolutionary processes. In a wild population of Soay sheep where mean body size has fluctuated substantially over the past 25 years and has, on average, gotten smaller, an ecological response to environmental variation is the major driver of the dynamics; evolutionary change has contributed relatively little: The sheep have become smaller because climate change has modified the way that density-dependence influences lamb growth rates. Environmental change has led to decreasing body size in a sheep population over 20 years, despite selection for increased size. Environmental change, including climate change, can cause rapid phenotypic change via both ecological and evolutionary processes. Because ecological and evolutionary dynamics are intimately linked, a major challenge is to identify their relative roles. We exactly decomposed the change in mean body weight in a free-living population of Soay sheep into all the processes that contribute to change. Ecological processes contribute most, with selection—the underpinning of adaptive evolution—explaining little of the observed phenotypic trend. Our results enable us to explain why selection has so little effect even though weight is heritable, and why environmental change has caused a decline in the body size of Soay sheep.

The ecological forecast horizon, and examples of its uses and determinants

Forecasts of ecological dynamics in changing environments are increasingly important, and are available for a plethora of variables, such as species abundance and distribution, community structure and ecosystem processes. There is, however, a general absence of knowledge about how far into the future, or other dimensions (space, temperature, phylogenetic distance), useful ecological forecasts can be made, and about how features of ecological systems relate to these distances. The ecological forecast horizon is the dimensional distance for which useful forecasts can be made. Five case studies illustrate the influence of various sources of uncertainty (e.g. parameter uncertainty, environmental variation, demographic stochasticity and evolution), level of ecological organisation (e.g. population or community), and organismal properties (e.g. body size or number of trophic links) on temporal, spatial and phylogenetic forecast horizons. Insights from these case studies demonstrate that the ecological forecast horizon is a flexible and powerful tool for researching and communicating ecological predictability. It also has potential for motivating and guiding agenda setting for ecological forecasting research and development.

How Life History Influences Population Dynamics in Fluctuating Environments

A major question in ecology is how age-specific variation in demographic parameters influences population dynamics. Based on long-term studies of growing populations of birds and mammals, we analyze population dynamics by using fluctuations in the total reproductive value of the population. This enables us to account for random fluctuations in age distribution. The influence of demographic and environmental stochasticity on the population dynamics of a species decreased with generation time. Variation in age-specific contributions to total reproductive value and to stochastic components of population dynamics was correlated with the position of the species along the slow-fast continuum of life-history variation. Younger age classes relative to the generation time accounted for larger contributions to the total reproductive value and to demographic stochasticity in “slow” than in “fast” species, in which many age classes contributed more equally. In contrast, fluctuations in population growth rate attributable to stochastic environmental variation involved a larger proportion of all age classes independent of life history. Thus, changes in population growth rates can be surprisingly well explained by basic species-specific life-history characteristics.

SPATIOTEMPORAL VARIATION IN SURVIVAL RATES: IMPLICATIONS FOR POPULATION DYNAMICS OF YELLOW-BELLIED MARMOTS

Spatiotemporal variation in age-specific survival rates can profoundly influence population dynamics, but few studies of vertebrates have thoroughly investigated both spatial and temporal variability in age-specific survival rates. We used 28 years (1976-2003) of capture-mark-recapture (CMR) data from 17 locations to parameterize an age-structured Cormack-Jolly-Seber model, and investigated spatial and temporal variation in age-specific annual survival rates of yellow-bellied marmots (Marmota flaviventris). Survival rates varied both spatially and temporally, with survival of younger animals exhibiting the highest degree of variation. Juvenile survival rates varied from 0.52 +/- 0.05 to 0.78 +/- 0.10 among sites and from 0.15 +/- 0.14 to 0.89 +/- 0.06 over time. Adult survival rates varied from 0.62 +/- 0.09 to 0.80 +/- 0.03 among sites, but did not vary significantly over time. We used reverse-time CMR models to estimate the realized population growth rate (lamda), and to investigate the influence of the observed variation in age-specific survival rates on lamda. The realized growth rate of the population closely covaried with, and was significantly influenced by, spatiotemporal variation in juvenile survival rate. High variability in juvenile survival rates over space and time clearly influenced the dynamics of our study population and is also likely to be an important determinant of the spatiotemporal variation in the population dynamics of other mammals with similar life history characteristics.

Influence of local demography on asymptotic and transient dynamics of a yellow-bellied marmot metapopulation

Despite recent advances in biodemography and metapopulation ecology, we still have limited understanding of how local demographic parameters influence short‐ and long‐term metapopulation dynamics. We used long‐term data from 17 local populations, along with the recently developed methods of matrix metapopulation modeling and transient sensitivity analysis, to investigate the influence of local demography on long‐term (asymptotic) versus short‐term (transient) dynamics of a yellow‐bellied marmot metapopulation in Colorado. Both long‐ and short‐term dynamics depended primarily on a few colony sites and were highly sensitive to changes in demography at these sites, particularly in survival of reproductive adult females. Interestingly, the relative importance of sites differed between long‐ and short‐term dynamics; the spatial structure and local population sizes, while insignificant for asymptotic dynamics, were influential on transient dynamics. However, considering the spatial structure was uninformative about the relative influence of local demography on metapopulation dynamics. The vital rates that were the most influential on local dynamics were also the most influential on both long‐ and short‐term metapopulation dynamics. Our results show that an explicit consideration of local demography is essential for a complete understanding of the dynamics and persistence of spatially structured populations.

THE INFLUENCE OF DISTURBANCE EVENTS ON SURVIVAL AND DISPERSAL RATES OF FLORIDA BOX TURTLES

Disturbances have the potential to cause long-term effects to ecosystem structure and function, and they may affect individual species in different ways. Long-lived vertebrates such as turtles may be at risk from such events, inasmuch as their life histories preclude rapid recovery should extensive mortality occur. We applied capture-mark-recapture models to assess disturbance effects on a population of Florida box turtles (Terrapene carolina bauri) on Egmont Key, Florida, USA. Near the midpoint of the study, a series of physical disturbances affected the island, from salt water overwash associated with several tropical storms to extensive removal of nonindigenous vegetation. These disturbances allowed us to examine demographic responses of the turtle population and to determine if they affected dispersal throughout the island. Adult survival rates did not vary significantly either between sexes or among years of the study. Survival rates did not vary significantly between juvenile and adult turtles, or among years of the study. Furthermore, neither adult nor juvenile survival rates differed significantly between pre- and post-disturbance. However, dispersal rates varied significantly among the four major study sites, and dispersal rates were higher during the pre-disturbance sampling periods compared to post-disturbance. Our results suggest few long-term effects on the demography of the turtle population. Florida box turtles responded to tropical storms and vegetation control by moving to favorable habitats minimally affected by the disturbances and remaining there. As long as turtles and perhaps other long-lived vertebrates can disperse to non-disturbed habitat, and high levels of mortality do not occur in a population, a long life span may allow them to wait out the impact of disturbance with potentially little effect on long-term population processes.

FACTORS INFLUENCING MOVEMENT DISTANCES OF TWO SPECIES OF SYMPATRIC VOLES

Abstract We studied factors influencing home-range size in fluctuating populations of Microtus ochrogaster and M. pennsylvanicus in alfalfa, bluegrass, and tallgrass habitats over a 25-year period in east-central Illinois. Preferred food availability for both species was greatest in alfalfa and least in tallgrass, lesser during winter than other seasons in all 3 habitats, and greater in alfalfa during winter than in the other 2 habitats. Vegetative cover was sparse, especially during winter, in alfalfa and dense year-round in bluegrass and tallgrass. Movement distances of M. ochrogaster tended to be smaller in alfalfa than in bluegrass and tallgrass; movement distances of neither vole species differed between bluegrass and tallgrass. Within alfalfa, movement distances of both species were smaller during winter, when cover was sparse and food availability low. No seasonal difference was found in movement distances of either species within bluegrass and tallgrass, where cover was dense year-round, but food availability was low during winter. Movement distances of M. ochrogaster were not affected by supplemental feeding in bluegrass and tallgrass; those of M. pennsylvanicus were smaller in supplementally fed tallgrass. We conclude that cover, as an indicator of risk of predation, influenced home-range sizes of both species more than did food availability.

Social behavior drives the dynamics of respiratory disease in threatened tortoises

Since the early 1990s, morbidity and mortality in tortoise populations have been associated with a transmissible, mycoplasmal upper respiratory tract disease (URTD). Although the etiology, transmission, and diagnosis of URTD have been extensively studied, little is known about the dynamics of disease transmission in free-ranging tortoise populations. To understand the transmission dynamics of Mycoplasma agassizii, the primary etiological agent of URTD in wild tortoise populations, we studied 11 populations of free-ranging gopher tortoises (Gopherus polyphemus; n = 1667 individuals) over five years and determined their exposure to the pathogen by serology, by clinical signs, and by detection of the pathogen in nasal lavages. Adults tortoises (n = 759) were 11 times more likely to be seropositive than immature animals (n = 242) (odds ratio = 10.6, 95% CI = 5.7-20, P < 0.0001). Nasal discharge was observed in only 1.4% (4/296) of immature tortoises as compared with 8.6% (120/1399) of adult tortoises. Nasal lavages from all juvenile tortoises (n = 283) were negative by PCR for mycoplasmal pathogens associated with URTD. We tested for spatial segregation among tortoise burrows by size class and found no consistent evidence of clustering of either juveniles or adults. We suggest that the social behavior of tortoises plays a critical role in the spread of URTD in wild populations, with immature tortoises having minimal interactions with adult tortoises, thereby limiting their exposure to the pathogen. These findings may have broader implications for modeling horizontally transmitted diseases in other species with limited parental care and emphasize the importance of incorporating animal behavior parameters into disease transmission studies to better characterize the host-pathogen dynamics.

Proximate causes of natal dispersal in female yellow-bellied marmots, Marmota flaviventris

We investigated factors influencing natal dispersal in 231 female yearling yellow-bellied marmots (Marmota flaviventris) using comprehensive analysis of 10 years (1983-1993) of radiotelemetry and 37 years (1963-1999) of capture-mark-recapture data. Only individuals whose dispersal status was verified, primarily by radiotelemetry, were considered. Univariate analyses revealed that six of the 24 variables we studied significantly influenced dispersal: dispersal was less likely when the mother was present, amicable behavior with the mother and play behavior were more frequent, and spatial overlap was greater with the mother, with matriline females, and with other yearling females. Using both univariate and multivariate analyses, we tested several hypotheses proposed as proximate causes of dispersal. We rejected inbreeding avoidance, population density, body size, social intolerance, and kin competition as factors influencing dispersal. Instead, our results indicate that kin cooperation, expressed via cohesive behaviors and with a focus on the mother, influenced dispersal by promoting philopatry. Kin cooperation may be an underappreciated factor influencing dispersal in both social and nonsocial species.