The diversity of population responses to environmental change

This is the final version. Available from Wiley via the DOI in this record.Data available from the Dryad Digital Repository: https:// doi.org/10.5061/dryad.d5f54s7The current extinction and climate change crises pressure us to predict population dynamics with ever-greater accuracy. Although predictions rest on the well-advanced theory of age-structured populations, two key issues remain poorly explored. Specifically, how the age-dependency in demographic rates and the year-to-year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age-specific demographic rates and when ages are reduced to stages. We find that stage- vs. age-based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival-fecundity-trade-offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age-specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.Max Planck Society, Marie Curie FellowshipERCGerman Research FoundationSwiss National Science FoundationNational Science FoundationNational Institute of AgingRamon y Cajal Research GrantWenner-Gren FoundationLeakey FoundationNational Geographic SocietyZoological Society of San DiegoUniversity of PennsylvaniaArgentinean National Council of Researc

Factors influencing terrestriality in primates of the Americas and Madagascar

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (bodymass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use

Factors influencing terrestriality in primates of the Americas and Madagascar

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use

Metamodels for transdisciplinary analysis of wildlife population dynamics.

Wildlife population models have been criticized for their narrow disciplinary perspective when analyzing complexity in coupled biological - physical - human systems. We describe a "metamodel" approach to species risk assessment when diverse threats act at different spatiotemporal scales, interact in non-linear ways, and are addressed by distinct disciplines. A metamodel links discrete, individual models that depict components of a complex system, governing the flow of information among models and the sequence of simulated events. Each model simulates processes specific to its disciplinary realm while being informed of changes in other metamodel components by accessing common descriptors of the system, populations, and individuals. Interactions among models are revealed as emergent properties of the system. We introduce a new metamodel platform, both to further explain key elements of the metamodel approach and as an example that we hope will facilitate the development of other platforms for implementing metamodels in population biology, species risk assessments, and conservation planning. We present two examples - one exploring the interactions of dispersal in metapopulations and the spread of infectious disease, the other examining predator-prey dynamics - to illustrate how metamodels can reveal complex processes and unexpected patterns when population dynamics are linked to additional extrinsic factors. Metamodels provide a flexible, extensible method for expanding population viability analyses beyond models of isolated population demographics into more complete representations of the external and intrinsic threats that must be understood and managed for species conservation

Population trajectories for a prey species subjected to different levels of predation.

<p>Mean prey population size through time is predicted by a single-species PVA model that assumed a fixed predator population size. Simulations were run for predator populations of 50, 60, 70, 80, and 100 individuals. The prey population was sustained at a size of N = 10000 or more if there were 80 or fewer predators.</p

Population trajectories for a predator species at different levels of prey availability.

<p>Mean predator population size through time is predicted by a single-species PVA model that assumed a fixed prey population size. Simulations were run for prey populations of 5000, 6000, 7000, 8000, 10000, and 15000 individuals. Approximately 6000 prey was sufficient to sustain growth of the predator population from its initial N = 50 to more than 100.</p

Mean predator-prey dynamics in coupled metamodels that (A) did not include and (B) did include stochastic variation.

<p>Mean population densities (N/K) for a predator and a prey species are predicted by a two-species metamodel, which assumed that the density of one species would impact the other species. In (A), externally driven sources of stochasticity (e.g., environmental variation, catastrophes) and inbreeding did not impact either population, and we found that the predator population grew rapidly, causing collapse of the prey population followed by collapse of the predator population. In (B), externally driven stochasticity and inbreeding depression could impact each population. For this scenario, the average trajectory shows that the predator population grew, followed by a decline in prey, causing subsequent decline in the predator, eventually resulting in a possibly stable state in which a reduced prey population sustained a reduced predator population.</p

Metapopulation dynamics influenced by dispersal.

<p>Metapopulation size is projected by (A) a PVA model in <i>Vortex</i> assuming varied rates of dispersal, annual fluctuations in demographic rates, and inbreeding depression; (B) a metamodel that linked a PVA model in <i>Vortex</i> to an infectious disease model in <i>Outbreak</i>, assuming varied rates of dispersal, minimal annual fluctuations in demographic rates, and no inbreeding depression; and (C) a metamodel that linked a PVA in <i>Vortex</i> to an infectious disease model in <i>Outbreak</i>, assuming varied rates of dispersal, annual fluctuations in demographic rates, and inbreeding depression. In (A), higher rates of dispersal increase growth and stability of the metapopulation because stochastic effects in local subpopulations are dampened. When disease was introduced but stochasticity was removed, as in (B), higher rates of dispersal depress population size because of the faster spread of disease. Finally, when stochasticity, disease, and dispersal were considered in (C), higher dispersal initially reduced population size because of the faster spread of disease. In later years, disease was largely eliminated from the system, and higher rates of dispersal stabilized the population against stochastic fluctuations. During a few years in the middle of the simulation, disease and stochastic processes were equally important, and intermediate rates of dispersal led to the highest population size.</p

Examples of data structure and program flow implemented by <i>MetaModel</i><i>Manager</i>.

<p>(A) Nested data representing a species in a metamodel. Global state variables (GSvar), population state variables (PSvar), and individual state variables (ISvar) are descriptors of the overall system, each population, and each individual, respectively. (B) Flow of control among component models. Curved arrows represent access to and modification of data. Block arrows represent control passed among models. (C) A two-species metamodel, with one modifier and one translator model acting on one species and two modifier models acting on the second species. Control alternates between the species, as illustrated by solid block arrows. Each system, modifier, and translator model has access to change any property of its populations and individuals as well as any shared global state variables.</p

Metamodel that integrates demography, landscape change, dispersal, and disease status.

<p>A PVA program acts as the system model (solid outline) to simulate individual survival and reproduction based on individual and population state variables (shown in italics) passed from other models. Modifier models (dashed outlines) simulate habitat dynamics, individual movements, and individual transitions in disease status. A central facilitator program passes state variables between the system and modifier models at appropriate time steps. The ultimate results are measures of population dynamics and extinction risk for a species impacted by habitat change and disease.</p