The demographic contributions of connectivity versus local dynamics to population growth of an endangered bird.

Conservation and management increasingly focus on connectivity, because connectivity driven by variation in immigration rates across landscapes is thought to be crucial for maintaining local population and metapopulation persistence. Yet, efforts to quantify the relative role of immigration on population growth across the entire range of species and over time have been lacking. We assessed whether immigration limited local and range-wide population growth of the endangered snail kite Rostrhamus sociabilis in Florida, USA, over 18 years using multi-state, reverse-time modelling that accounts for imperfect detection of individuals and unobservable states. Demographic contributions of immigration varied depending on the dynamics and geographic position of the local populations, were scale-dependent and changed over time. By comparing the relative contributions of immigration versus local demography for periods of significant change in local abundance, we found empirical evidence for a disproportionately large role of immigration in facilitating population growth of a centrally located population-a connectivity 'hub'. The importance of connectivity changed depending of the spatial scale considered, such that immigration was a more important driver of population growth at small versus large spatial scales. Furthermore, the contribution of immigration was much greater during time periods when local population size was small, emphasizing abundance-dependent rescue effects. Our findings suggest that efforts aimed at improving local breeding habitat will likely be most effective at increasing snail kite population growth. More broadly, our results provide much needed information on the role of connectivity for population growth, suggesting that connectivity conservation may have the greatest benefits when efforts focus on centrally located habitat patches and small populations. Furthermore, our results highlight that connectivity is highly dynamic over time and that interpreting the effects of connectivity at local scales may not transfer to region-wide dynamics.

Rapid morphological change of a top predator with the invasion of a novel prey.

Invasive exotic species are spreading rapidly throughout the planet. These species can have widespread impacts on biodiversity, yet the ability for native species, particularly long-lived vertebrates, to respond rapidly to invasions remains mostly unknown. Here we provide evidence of rapid morphological change in the endangered snail kite (Rostrhamus sociabilis) across its North American range with the invasion of a novel prey, the island apple snail (Pomacea maculata), a much larger congener of the kite's native prey. In less than one decade since invasion, snail kite bill size and body mass increased substantially. Larger bills should be better suited to extracting meat from the larger snail shells, and we detected strong selection on increased size through juvenile survival. Using pedigree data, we found evidence of both genetic and environmental influences on trait expression and discovered that additive genetic variation in bill size increased with invasion. However, trends in predicted breeding values emphasize that recent morphological changes have been driven primarily by phenotypic plasticity rather than micro-evolutionary change. Our findings suggest that evolutionary change may be imminent and underscore that even long-lived vertebrates can respond quickly to invasive species. Furthermore, these results highlight that phenotypic plasticity may provide a crucial role for predators experiencing rapid environmental change.

Counteracting effects of a non-native prey on the demography of a native predator culminate in positive population growth.

Identifying impacts of non-native species on native populations is central to conservation and ecology. While effects of non-native predators on native prey populations have recently received much attention, impacts of introduced prey on native predator populations are less understood. Non-native prey can influence predator behavior and demography through direct and indirect pathways, yet quantitative assessments of the relative impacts of multiple, potentially counteracting, effects on native predator population growth remain scarce. Using ≈20 years of range-wide monitoring data, we tested for effects of a recently introduced, rapidly spreading non-native prey species (Pomacea maculata) on the behavior and demography of the endangered Snail Kite (Rostrhamus sociabilis). Previous studies found that food-handling difficulties caused by the large size of P. maculata (relative to the native P. paludosa) can lead to energetic deficiencies in juvenile kites, suggesting the potential for evolutionary traps to occur. However, high densities of P. maculata populations could facilitate kites by providing supplemental food resources. Contrary to prior hypotheses, we found that juvenile apparent survival increased ≈50% in wetlands invaded by non-native snails. Breeding rates and number of young fledged/successful nests were also positively associated with non-native snail presence, suggesting direct trophic benefits to kites. We found no direct effects of the invasive snail on adult survival or daily nest survival rates. Kite movements and breeding distribution closely tracked the spread of non-native snail populations. Since 2005, kites have been heavily concentrated in northern regions where non-native snails have established. This geographic shift has had hidden costs, as use of northern regions is associated with lower adult survival. Despite negative impacts to this key vital rate, matrix population modeling indicated that the multifarious effects of the non-native snail invasion on kites culminated in increased population growth rates, likely lowering short-term extinction risks. Results suggest that considering only particular components of behavior or demography may be inadequate to infer the population-dynamic importance of non-native prey on native predators, including their role in creating potential evolutionary traps. Our findings provide information pertinent to Everglades restoration, highlighting potential management trade-offs for non-native species that may aid imperiled species recovery yet disrupt other native communities.

Spatio-Temporal Variation in Age Structure and Abundance of the Endangered Snail Kite: Pooling across Regions Masks a Declining and Aging Population.

While variation in age structure over time and space has long been considered important for population dynamics and conservation, reliable estimates of such spatio-temporal variation in age structure have been elusive for wild vertebrate populations. This limitation has arisen because of problems of imperfect detection, the potential for temporary emigration impacting assessments of age structure, and limited information on age. However, identifying patterns in age structure is important for making reliable predictions of both short- and long-term dynamics of populations of conservation concern. Using a multistate superpopulation estimator, we estimated region-specific abundance and age structure (the proportion of individuals within each age class) of a highly endangered population of snail kites for two separate regions in Florida over 17 years (1997-2013). We find that in the southern region of the snail kite-a region known to be critical for the long-term persistence of the species-the population has declined significantly since 1997, and during this time, it has increasingly become dominated by older snail kites (> 12 years old). In contrast, in the northern region-a region historically thought to serve primarily as drought refugia-the population has increased significantly since 2007 and age structure is more evenly distributed among age classes. Given that snail kites show senescence at approximately 13 years of age, where individuals suffer higher mortality rates and lower breeding rates, these results reveal an alarming trend for the southern region. Our work illustrates the importance of accounting for spatial structure when assessing changes in abundance and age distribution and the need for monitoring of age structure in imperiled species.

Consistent scaling of population structure across landscapes despite intraspecific variation in movement and connectivity.

Understanding the spatial scale of population structure is fundamental to long-standing tenets of population biology, landscape ecology and conservation. Nonetheless, identifying such scales has been challenging because a key factor that influences scaling - movement among patches or local populations - is a multicausal process with substantial phenotypic and temporal variation. We resolve this problem via a novel application of network modularity. When applied to movements, modularity provides a formal description of the functional aggregation of populations and identifies potentially critical scales for ecological and evolutionary dynamics. We first test for modularity using several different types of biologically relevant movements across the entire geographic range of an endangered bird, the snail kite (Rostrhamus sociabilis plumbeus). We then ask whether variation in movement based on (i) age, (ii) sex and (iii) time (annual, seasonal and within-season movements) influences spatial population structure (i.e. modularity) in snail kites. We identified significant modularity in annual dispersal of snail kites (all adults, males only, females only, and juveniles only) and in within-breeding season movements of adults, yet no evidence of modularity in seasonal (non-breeding) movements. For those movements with observed modular structure, we found striking similarities in the spatial configuration of population structure, even though movement properties varied considerably among these different types of movements. Our results suggest that the emergence of modularity in population networks can be robust despite movement heterogeneity and differences in patch-based measures of connectivity. Furthermore, our comparison of the population structure and connectivity across multiple movement phases helps to identify wetland patches most critical to population connectivity at multiple spatiotemporal scales. We argue that understanding modularity in populations may provide a robust complement to existing measures of population structure and connectivity and will help to clarify the limiting roles of movement for populations. Such information is increasingly needed for interpreting population persistence and guiding effective conservation strategies with ongoing environmental change.

Affinity for natal environments by dispersers impacts reproduction and explains geographical structure of a highly mobile bird.

Understanding dispersal and habitat selection behaviours is central to many problems in ecology, evolution and conservation. One factor often hypothesized to influence habitat selection by dispersers is the natal environment experienced by juveniles. Nonetheless, evidence for the effect of natal environment on dispersing, wild vertebrates remains limited. Using 18 years of nesting and mark-resight data across an entire North American geographical range of an endangered bird, the snail kite (Rostrhamus sociabilis), we tested for natal effects on breeding-site selection by dispersers and its consequences for reproductive success and population structure. Dispersing snail kites were more likely to nest in wetlands of the same habitat type (lacustrine or palustrine) as their natal wetland, independent of dispersal distance, but this preference declined with age and if individuals were born during droughts. Importantly, dispersing kites that bred in natal-like habitats had lower nest success and productivity than kites that did not. These behaviours help explain recently described population connectivity and spatial structure across their geographical range and reveal that assortative breeding is occurring, where birds are more likely to breed with individuals born in the same wetland type as their natal habitat. Natal environments can thus have long-term and large-scale effects on populations in nature, even in highly mobile animals.

Network modularity reveals critical scales for connectivity in ecology and evolution.

For nearly a century, biologists have emphasized the profound importance of spatial scale for ecology, evolution and conservation. Nonetheless, objectively identifying critical scales has proven incredibly challenging. Here we extend new techniques from physics and social sciences that estimate modularity on networks to identify critical scales for movement and gene flow in animals. Using four species that vary widely in dispersal ability and include both mark-recapture and population genetic data, we identify significant modularity in three species, two of which cannot be explained by geographic distance alone. Importantly, the inclusion of modularity in connectivity and population viability assessments alters conclusions regarding patch importance to connectivity and suggests higher metapopulation viability than when ignoring this hidden spatial scale. We argue that network modularity reveals critical meso-scales that are probably common in populations, providing a powerful means of identifying fundamental scales for biology and for conservation strategies aimed at recovering imperilled species.

Extreme weather and experience influence reproduction in an endangered bird.

Extreme weather events, such as droughts and heat waves, are expected to become more severe and more frequent in the coming years, and understanding their impacts on demographic rates is of increasing interest to both evolutionary ecologists and conservation practitioners. An individual's breeding probability can be a sensitive indicator of the decision to initiate reproductive behavior under varying environmental conditions, has strong fitness consequences, and can be considered the first step in a life history trade-off between allocating resources for breeding activities or self-survival. Using a 14-year time series spanning large variation in climatic conditions and the entirety of a population's breeding range, we estimated the effects of extreme weather conditions (drought) on the state-specific probabilities of breeding and survival of an endangered bird, the Florida Snail Kite (Rostrhamus sociabilis plumbeus). Our analysis accounted for uncertainty in breeding status assignment, a common source of uncertainty that is often ignored when states are based on field observations. Breeding probabilities in adult kites (> 1 year of age) decreased during droughts, whereas the probability of breeding in young kites (1 year of age) tended to increase. Individuals attempting to breed showed no evidence of reduced future survival. Although population viability analyses of this species and other species often implicitly assume that all adults will attempt to breed, we find that breeding probabilities were significantly < 1 for all 13 estimable years considered. Our results suggest that experience is an important factor determining whether or not individuals attempt to breed during harsh environmental conditions and that reproductive effort may be constrained by an individual's quality and/or despotic behavior among individuals attempting to breed.

Social network models predict movement and connectivity in ecological landscapes.

Network analysis is on the rise across scientific disciplines because of its ability to reveal complex, and often emergent, patterns and dynamics. Nonetheless, a growing concern in network analysis is the use of limited data for constructing networks. This concern is strikingly relevant to ecology and conservation biology, where network analysis is used to infer connectivity across landscapes. In this context, movement among patches is the crucial parameter for interpreting connectivity but because of the difficulty of collecting reliable movement data, most network analysis proceeds with only indirect information on movement across landscapes rather than using observed movement to construct networks. Statistical models developed for social networks provide promising alternatives for landscape network construction because they can leverage limited movement information to predict linkages. Using two mark-recapture datasets on individual movement and connectivity across landscapes, we test whether commonly used network constructions for interpreting connectivity can predict actual linkages and network structure, and we contrast these approaches to social network models. We find that currently applied network constructions for assessing connectivity consistently, and substantially, overpredict actual connectivity, resulting in considerable overestimation of metapopulation lifetime. Furthermore, social network models provide accurate predictions of network structure, and can do so with remarkably limited data on movement. Social network models offer a flexible and powerful way for not only understanding the factors influencing connectivity but also for providing more reliable estimates of connectivity and metapopulation persistence in the face of limited data.

Natal location influences movement and survival of a spatially structured population of snail kites.

Despite the accepted importance of the need to better understand how natal location affects movement decisions and survival of animals, robust estimates of movement and survival in relation to the natal location are lacking. Our study focuses on movement and survival related to the natal location of snail kites in Florida and shows that kites, in addition to exhibiting a high level of site tenacity to breeding regions, also exhibit particular attraction to their natal region. More specifically, we found that estimates of movement from post-dispersal regions were greater toward natal regions than toward non-natal regions (differences were significant for three of four regions). We also found that estimates of natal philopatry were greater than estimates of philopatry to non-natal regions (differences were statistically significant for two of four regions). A previous study indicated an effect of natal region on juvenile survival; in this study, we show an effect of natal region on adult survival. Estimates of adult survival varied among kites that were hatched in different regions. Adults experienced mortality rates characteristic of the region occupied at the time when survival was measured, but because there is a greater probability that kites will return to their natal region than to any other regions, their survival was ultimately influenced by their natal region. In most years, kites hatched in southern regions had greater survival probabilities than did kites hatched in northern regions. However, during a multiregional drought, one of the northern regions served as a refuge from drought, and during this perturbation, survival was greater for birds hatched in the north. Our study shows that natal location may be important in influencing the ecological dynamics of kites but also highlights the importance of considering temporal variation in habitat conditions of spatially structured systems when attempting to evaluate the conservation value of habitats.

Importance of well-designed monitoring programs for the conservation of endangered species: case study of the snail kite.

Monitoring natural populations is often a necessary step to establish the conservation status of species and to help improve management decisions. Nevertheless, many monitoring programs do not effectively address primary sources of variability in monitoring data, which ultimately may limit the utility of monitoring in identifying declines and improving management. To illustrate the importance of taking into account detectability and spatial variation, we used a recently proposed estimator of abundance (superpopulation estimator) to estimate population size of and number of young produced by the Snail Kite (Rostrhamus sociabilis plumbeus) in Florida. During the last decade, primary recovery targets set by the U.S. Fish and Wildlife Service for the Snail Kite that were based on deficient monitoring programs (i.e., uncorrected counts) were close to being met (by simply increasing search effort during count surveys). During that same period, the Snail Kite population declined dramatically (by 55% from 1997 to 2005) and the number of young decreased by 70% between 1992-1998 and 1999-2005. Our results provide a strong practical case in favor of the argument that investing a sufficient amount of time and resources into designing and implementing monitoring programs that carefully address detectability and spatial variation is critical for the conservation of endangered species.

Multiscale patterns of movement in fragmented landscapes and consequences on demography of the snail kite in Florida.

1. Habitat loss and fragmentation are major factors affecting vertebrate populations. A major effect of these habitat alterations is that they reduce movement of organisms. Despite the accepted importance of movement in driving the dynamics of many natural populations, movement of vertebrates in fragmented landscapes have seldom been estimated with robust statistical methods. 2. We estimated movement probabilities of snail kites Rosthramus sociabilis within the remaining wetlands in Florida. Using both radio-telemetry and banding information, we used a multistate modelling approach to estimate transition probabilities at two temporal scales (month; year) and multiple spatial scales. We examined kite movement among wetlands altered by three different levels of fragmentation: among wetlands separated by small physical barriers (e.g. road); among wetlands separated by moderate amount of matrix (< 5 km); and among wetlands separated by extensive matrix areas (> 15 km). 3. Kites moved extensively among contiguous wetlands (movement probability 0.29 per month), but significantly less among isolated wetlands (movement probability 0.10 per month). 4. Kites showed high levels of annual site fidelity to most isolated wetlands (probability ranged from 0.72 to 0.95 per year). 5. We tested the effects of patch size and interpatch distance on movement. Our modelling indicated an effect of both distance and patch size on juveniles' movement (but not adult) when examining movements among fragments. 6. Only a small proportion of kites escaped a regional drought by moving to refugia (wetlands less affected by drought). Many individuals died after the drought. During drought adult survival dropped by 16% while juvenile survival dropped by 86% (possibly because juveniles were less likely to reach refugia). 7. We hypothesize that fragmentation may decrease kite's resistance to drought by restricting exploratory behaviour.

Impacts of Citrus Development on Habitats of Southwest Florida.

Examining resource management needs at the landscape level has become critical for the conservation of ecosystems and the preservation of species. Geographic information systems (GIS) that allow for the integration of spatially referenced databases are a powerful tool that can be used by resource managers to examine potential impacts and develop strategies for regional planning. We applied a landscape-level approach to examine the potential impacts of citrus development on habitats and species in southwest Florida. We developed GIS models for panthers, Sandhill Cranes, and wading birds that reflect changes in potential habitats under a series of development scenarios. The models indicate that, under the maximum development scenario, 63% of potential panther habitat, 66% of potential Sandhill Crane habitat, and 67% and 33% of potential wading bird nesting and foraging habitats could be lost. In addition, the habitat that would remain would be severely fragmented. Several key areas were identified that will be critical to the continued existence of these species and to maintenance of regional biodiversity. The areas identified are habitats not represented on the existing public lands concentrated in the southern portion of the study area and/or that provide connections among existing natural areas. Impacto del desarrollo de cítricos en hábitats del suroeste de Florida.

Resumen: El exámen de las necesidades de manejo de los recursos a nivel del paisajese ha transformado en un elementeo crítico para la conservación de los ecosistemas y la preservación de las especies. Los Sistemas de Información Geográficos (SIG), que permiten la integración de las base de datos registrados espacialmente, constituyer una poderosa herramienta que puede ser utilizada por los administradores de recursos naturales para examinar los impactos potenciales y desarrollar estrategias de planificación a nivel regional. Aplicamos un enfoque a nivel de paisaje para examinar los impactos potenciales del desarrollo de los cítricos en especies y ambientes del sudoeste de la Florida. Desarrollamos modelos en SIG para panteras, grullas y aves zancudas que reflejan cambios en los hábitats potenciales bajo una serie de escenarios de desarrollo. Los modelos indican que bajo un escenario de máximo desarrollo 63% del hábitat potencial de la pantera, 66% del hábital potencial de la grulla y 67 y 33% del hábitat potencial para anidamiento y forestación de las aves zancudas se podrían perder. En forma adicional, el hábitat que quedara estaría severamente fragmentado. Se identificaron varias áreas claves que van a ser críticas para la supervivencia de estas especies y el mantenimiento de la biodiversidad a nivel regional. Las áreas identificadas, constituyen hábitats que no estan representados dentro de las tierras públicas existentes, y que se encuentran concentradas en la porción sur del área de estudio y/o proveen conecciones entre áreas naturales existentes.