Linking animal migration and ecosystem processes: Data-driven simulation of propagule dispersal by migratory herbivores.

Animal migration is a key process underlying active subsidies and species dispersal over long distances, which affects the connectivity and functioning of ecosystems. Despite much research describing patterns of where animals migrate, we still lack a framework for quantifying and predicting how animal migration affects ecosystem processes. In this study, we aim to integrate animal movement behavior and ecosystem functioning by developing a predictive modeling framework that can inform ecosystem management and conservation.We propose a framework to model individual-level migration trajectories between populations' seasonal ranges as well as the resulting dispersal and fate of propagules carried by the migratory animals, which can be calibrated using empirical data at every step of the modeling process. As a case study, we applied our framework to model the spread of guava seeds, Psidium guajava, by a population of migratory Galapagos tortoises, Chelonoidis porteri, across Santa Cruz Island. Galapagos tortoises are large herbivores that transport seeds and nutrients across the island, while Guava is one of the most problematic invasive species in the Galapagos archipelago.Our model can predict the pattern of spread of guava seeds alongside tortoises' downslope migration range, and it identified areas most likely to see establishment success. Our results show that Galapagos tortoises' seed dispersal may particularly contribute to guava range expansion on Santa Cruz Island, due to both long gut retention time and tortoise's long-distance migration across vegetation zones. In particular, we predict that tortoises are dispersing a significant amount of guava seeds into the Galapagos National Park, which has important consequences for the native flora.The flexibility and modularity of our framework allow for the integration of multiple data sources. It also allows for a wide range of applications to investigate how migratory animals affect ecosystem processes, including propagule dispersal but also other processes such as nutrient transport across ecosystems. Our framework is also a valuable tool for predicting how animal-mediated propagule dispersal can be affected by environmental change. These different applications can have important conservation implications for the management of ecosystems that include migratory animals.

Seasonal species richness of birds on the world's islands and its geographical correlates.

The presence of migratory birds on islands results in seasonal variation in species richness. These patterns and their geographical correlates within the context of island biogeography theory have not been examined. We used 21 years of bird observations on 690 islands from eBird to determine how seasonal species richness estimates vary as a function of island area, isolation and latitude. Species richness was highest on islands within the northern mid-latitudes during migration and on islands within tropical latitudes during the non-breeding season. Area defined positive, nonlinear relationships with species richness across seasons, with the steepest slopes occurring with islands greater than 1100 km2. Distance to mainland defined negative, nonlinear relationships with species richness across seasons, with the strongest slopes occurring with islands located greater than 150 km from the mainland. Species-area relationships were weakest for the most remote islands and strongest for islands at intermediate distances to the mainland. Intermediate proximity to other islands was a poor predictor of species richness. Our findings emphasize the presence of seasonally dynamic geographical relationships, the enhanced role of evolutionary processes on larger islands, the unique ecology of the world's most remote islands, and the importance of islands as stopover sites and wintering grounds for migratory bird species.

The overlooked complexity of avian brood parasite-host relationships.

The relationships between avian brood parasites and their hosts are widely recognised as model systems for studying coevolution. However, while most brood parasites are known to parasitise multiple species of host and hosts are often subject to parasitism by multiple brood parasite species, the examination of multispecies interactions remains rare. Here, we compile data on all known brood parasite-host relationships and find that complex brood parasite-host systems, where multiple species of brood parasites and hosts coexist and interact, are globally commonplace. By examining patterns of past research, we outline the disparity between patterns of network complexity and past research emphases and discuss factors that may be associated with these patterns. Drawing on insights gained from other systems that have embraced a multispecies framework, we highlight the potential benefits of considering brood parasite-host interactions as ecological networks and brood parasitism as a model system for studying multispecies interactions. Overall, our results provide new insights into the diversity of these relationships, highlight the stark mismatch between past research efforts and global patterns of network complexity, and draw attention to the opportunities that more complex arrangements offer for examining how species interactions shape global patterns of biodiversity.

Bayesian Skyline Plots disagree with range size changes based on Species Distribution Models for Holarctic birds.

During the Quaternary, large climate oscillations impacted the distribution and demography of species globally. Two approaches have played a major role in reconstructing changes through time: Bayesian Skyline Plots (BSPs), which reconstruct population fluctuations based on genetic data, and Species Distribution Models (SDMs), which allow us to back-cast the range occupied by a species based on its climatic preferences. In this paper, we contrast these two approaches by applying them to a large data set of 102 Holarctic bird species, for which both mitochondrial DNA sequences and distribution maps are available, to reconstruct their dynamics since the Last Glacial Maximum (LGM). Most species experienced an increase in effective population size (Ne , as estimated by BSPs) as well as an increase in geographical range (as reconstructed by SDMs) since the LGM; however, we found no correlation between the magnitude of changes in Ne and range size. The only clear signal we could detect was a later and greater increase in Ne for wetland birds compared to species that live in other habitats, a probable consequence of a delayed and more extensive increase in the extent of this habitat type after the LGM. The lack of correlation between SDM and BSP reconstructions could not be reconciled even when range shifts were considered. We suggest that this pattern might be linked to changes in population densities, which can be independent of range changes, and caution that interpreting either SDMs or BSPs independently is problematic and potentially misleading.

The role of habitat configuration in shaping animal population processes: a framework to generate quantitative predictions.

By shaping where individuals move, habitat configuration can fundamentally structure animal populations. Yet, we currently lack a framework for generating quantitative predictions about the role of habitat configuration in modulating population outcomes. To address this gap, we propose a modelling framework inspired by studies using networks to characterize habitat connectivity. We first define animal habitat networks, explain how they can integrate information about the different configurational features of animal habitats, and highlight the need for a bottom-up generative model that can depict realistic variations in habitat potential connectivity. Second, we describe a model for simulating animal habitat networks (available in the R package AnimalHabitatNetwork), and demonstrate its ability to generate alternative habitat configurations based on empirical data, which forms the basis for exploring the consequences of alternative habitat structures. Finally, we lay out three key research questions and demonstrate how our framework can address them. By simulating the spread of a pathogen within a population, we show how transmission properties can be impacted by both local potential connectivity and landscape-level characteristics of habitats. Our study highlights the importance of considering the underlying habitat configuration in studies linking social structure with population-level outcomes.

A general theory of avian migratory connectivity.

Birds exhibit a remarkable array of seasonal migrations. Despite much research describing migratory behaviour, the underlying forces driving how a species' breeding and wintering populations redistribute each year, that is, migratory connectivity, remain largely unknown. Here, we test the hypothesis that birds migrate in a way that minimises energy expenditure while considering intraspecific competition for energy acquisition, by developing a modelling framework that simulates an optimal redistribution of individuals between breeding and wintering areas. Using 25 species across the Americas, we find that the model accurately predicts empirical migration patterns, and thus offers a general explanation for migratory connectivity based on first ecological and energetic principles. Our model provides a strong basis for exploring additional processes underlying the ecology and evolution of migration, but also a framework for predicting how migration impacts local adaptation across seasons and how environmental change may affect population dynamics in migratory species.

Linking climate niches across seasons to assess population vulnerability in a migratory bird.

Global loss of biodiversity has placed new urgency on the need to understand factors regulating species response to rapid environmental change. While specialists are often less resilient to rapid environmental change than generalists, species-level analyses may obscure the extent of specialization when locally adapted populations vary in climate tolerances. Until recently, quantification of the degree of climate specialization in migratory birds below the species level was hindered by a lack of genomic and tracking information, but recent technological advances have helped to overcome these barriers. Here we take a genome-wide genetic approach to mapping population-specific migratory routes and quantifying niche breadth within genetically distinct populations of a migratory bird, the willow flycatcher (Empidonax traillii), which exhibits variation in the severity of population declines across its breeding range. While our sample size is restricted to the number of genetically distinct populations within the species, our results support the idea that locally adapted populations of the willow flycatcher with narrow climatic niches across seasons are already federally listed as endangered or in steep decline, while populations with broader climatic niches have remained stable in recent decades. Overall, this work highlights the value of quantifying niche breadth within genetically distinct groups across time and space when attempting to understand the factors that facilitate or constrain the response of locally adapted populations to rapid environmental change.

Author Correction: Simulation-based reconstruction of global bird migration over the past 50,000 years.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Simulation-based reconstruction of global bird migration over the past 50,000 years.

Migration is a widespread response of birds to seasonally varying climates. As seasonality is particularly pronounced during interglacial periods, this raises the question of the significance of bird migration during past periods with different patterns of seasonality. Here, we apply a mechanistic model to climate reconstructions to simulate the past 50,000 years of bird migration worldwide, a period encompassing the transition between the last glacial period and the current interglacial. Our results indicate that bird migration was also a prevalent phenomenon during the last ice age, almost as much as today, suggesting that it has been continually important throughout the glacial cycles of recent Earth history. We find however regional variations, with increasing migratory activity in the Americas, which is not mirrored in the Old World. These results highlight the strong flexibility of the global bird migration system and offer a baseline in the context of on-going anthropogenic climate change.

Movement and conformity interact to establish local behavioural traditions in animal populations.

The social transmission of information is critical to the emergence of animal culture. Two processes are predicted to play key roles in how socially-transmitted information spreads in animal populations: the movement of individuals across the landscape and conformist social learning. We develop a model that, for the first time, explicitly integrates these processes to investigate their impacts on the spread of behavioural preferences. Our results reveal a strong interplay between movement and conformity in determining whether locally-variable traditions establish across a landscape or whether a single preference dominates the whole population. The model is able to replicate a real-world cultural diffusion experiment in great tits Parus major, but also allows for a range of predictions for the emergence of animal culture under various initial conditions, habitat structure and strength of conformist bias to be made. Integrating social behaviour with ecological variation will be important for understanding the stability and diversity of culture in animals.

Energy efficiency drives the global seasonal distribution of birds.

The uneven distribution of biodiversity on Earth is one of the most general and puzzling patterns in ecology. Many hypotheses have been proposed to explain it, based on evolutionary processes or on constraints related to geography and energy. However, previous studies investigating these hypotheses have been largely descriptive due to the logistical difficulties of conducting controlled experiments on such large geographical scales. Here, we use bird migration-the seasonal redistribution of approximately 15% of bird species across the world-as a natural experiment for testing the species-energy relationship, the hypothesis that animal diversity is driven by energetic constraints. We develop a mechanistic model of bird distributions across the world, and across seasons, based on simple ecological and energetic principles. Using this model, we show that bird species distributions optimize the balance between energy acquisition and energy expenditure while taking into account competition with other species. These findings support, and provide a mechanistic explanation for, the species-energy relationship. The findings also provide a general explanation of migration as a mechanism that allows birds to optimize their energy budget in the face of seasonality and competition. Finally, our mechanistic model provides a tool for predicting how ecosystems will respond to global anthropogenic change.

A Physics-Inspired Mechanistic Model of Migratory Movement Patterns in Birds.

In this paper, we introduce a mechanistic model of migratory movement patterns in birds, inspired by ideas and methods from physics. Previous studies have shed light on the factors influencing bird migration but have mainly relied on statistical correlative analysis of tracking data. Our novel method offers a bottom up explanation of population-level migratory movement patterns. It differs from previous mechanistic models of animal migration and enables predictions of pathways and destinations from a given starting location. We define an environmental potential landscape from environmental data and simulate bird movement within this landscape based on simple decision rules drawn from statistical mechanics. We explore the capacity of the model by qualitatively comparing simulation results to the non-breeding migration patterns of a seabird species, the Black-browed Albatross (Thalassarche melanophris). This minimal, two-parameter model was able to capture remarkably well the previously documented migration patterns of the Black-browed Albatross, with the best combination of parameter values conserved across multiple geographically separate populations. Our physics-inspired mechanistic model could be applied to other bird and highly-mobile species, improving our understanding of the relative importance of various factors driving migration and making predictions that could be useful for conservation.

A global analysis of bird plumage patterns reveals no association between habitat and camouflage.

Evidence suggests that animal patterns (motifs) function in camouflage. Irregular mottled patterns can facilitate concealment when stationary in cluttered habitats, whereas regular patterns typically prevent capture during movement in open habitats. Bird plumage patterns have predominantly converged on just four types-mottled (irregular), scales, bars and spots (regular)-and habitat could be driving convergent evolution in avian patterning. Based on sensory ecology, we therefore predict that irregular patterns would be associated with visually noisy closed habitats and that regular patterns would be associated with open habitats. Regular patterns have also been shown to function in communication for sexually competing males to stand-out and attract females, so we predict that male breeding plumage patterns evolved in both open and closed habitats. Here, taking phylogenetic relatedness into account, we investigate ecological selection for bird plumage patterns across the class Aves. We surveyed plumage patterns in 80% of all avian species worldwide. Of these, 2,756 bird species have regular and irregular plumage patterns as well as habitat information. In this subset, we tested whether adult breeding/non-breeding plumages in each sex, and juvenile plumages, were associated with the habitat types found within the species' geographical distributions. We found no evidence for an association between habitat and plumage patterns across the world's birds and little phylogenetic signal. We also found that species with regular and irregular plumage patterns were distributed randomly across the world's eco-regions without being affected by habitat type. These results indicate that at the global spatial and taxonomic scale, habitat does not predict convergent evolution in bird plumage patterns, contrary to the camouflage hypothesis.

Mapping global diversity patterns for migratory birds.

Nearly one in five bird species has separate breeding and overwintering distributions, and the regular migrations of these species cause a substantial seasonal redistribution of avian diversity across the world. However, despite its ecological importance, bird migration has been largely ignored in studies of global avian biodiversity, with few studies having addressed it from a macroecological perspective. Here, we analyse a dataset on the global distribution of the world's birds in order to examine global spatial patterns in the diversity of migratory species, including: the seasonal variation in overall species diversity due to migration; the contribution of migratory birds to local bird diversity; and the distribution of narrow-range and threatened migratory birds. Our analyses reveal a striking asymmetry between the Northern and Southern hemispheres, evident in all of the patterns investigated. The highest migratory bird diversity was found in the Northern Hemisphere, with high inter-continental turnover in species composition between breeding and non-breeding seasons, and extensive regions (at high latitudes) where migratory birds constitute the majority of the local avifauna. Threatened migratory birds are concentrated mainly in Central and Southern Asia, whereas narrow-range migratory species are mainly found in Central America, the Himalayas and Patagonia. Overall, global patterns in the diversity of migratory birds indicate that bird migration is mainly a Northern Hemisphere phenomenon. The asymmetry between the Northern and Southern hemispheres could not have easily been predicted from the combined results of regional scale studies, highlighting the importance of a global perspective.