Marcel Holyoak

A movement ecology paradigm for unifying organismal movement research.

Movement of individual organisms is fundamental to life, quilting our planet in a rich tapestry of phenomena with diverse implications for ecosystems and humans. Movement research is both plentiful and insightful, and recent methodological advances facilitate obtaining a detailed view of individual movement. Yet, we lack a general unifying paradigm, derived from first principles, which can place movement studies within a common context and advance the development of a mature scientific discipline. This introductory article to the Movement Ecology Special Feature proposes a paradigm that integrates conceptual, theoretical, methodological, and empirical frameworks for studying movement of all organisms, from microbes to trees to elephants. We introduce a conceptual framework depicting the interplay among four basic mechanistic components of organismal movement: the internal state (why move?), motion (how to move?), and navigation (when and where to move?) capacities of the individual and the external factors affecting movement. We demonstrate how the proposed framework aids the study of various taxa and movement types; promotes the formulation of hypotheses about movement; and complements existing biomechanical, cognitive, random, and optimality paradigms of movement. The proposed framework integrates eclectic research on movement into a structured paradigm and aims at providing a basis for hypothesis generation and a vehicle facilitating the understanding of the causes, mechanisms, and spatiotemporal patterns of movement and their role in various ecological and evolutionary processes. ”Now we must consider in general the common reason for moving with any movement whatever.“ (Aristotle, De Motu Animalium, 4th century B.C.)

CONNECTING THEORETICAL AND EMPIRICAL STUDIES OF TRAIT‐MEDIATED INTERACTIONS

Trait-mediated interactions (TMIs), in which trophic and competitive inter- actions depend on individual traits as well as on overall population densities, have inspired large amounts of research, but theoretical and empirical studies have not been well con- nected. To help mitigate this problem, we review and synthesize the theoretical literature on TMIs and, in particular, on trait-mediated indirect interactions, TMIIs, in which the presence of one species mediates the interaction between a second and third species. (1) In models, TMIs tend to stabilize simple communities; adding further biological detail often reduces stability in models, but populations may persist even if their dynamics become mathematically unstable. (2) Short- and long-term changes in population density caused by TMIs depend even more on details, such as the curvature of functional responses and trade-offs, which have rarely been measured. (3) The effects of TMIs in multipredator communities depend in a straightforward way on the specificity of prey defenses. (4) Tritrophic and more complex communities are theoretically difficult; few general conclu- sions have emerged. Theory needs new kinds of experiments as a guide. The most critical needs are experiments that measure curvatures of trade-offs and responses, and experiments that (combined with theory) allow us to scale from short- to long-term responses of com- munities. Anecdotal evidence from long-term and large-scale studies suggests that TMIs may affect community dynamics at practical management scales; community models in- corporating TMIs are necessary and require closer collaborations between theory and ex-

Trends and missing parts in the study of movement ecology

Movement is important to all organisms, and accordingly it is addressed in a huge number of papers in the literature. Of nearly 26,000 papers referring to movement, an estimated 34% focused on movement by measuring it or testing hypotheses about it. This enormous amount of information is difficult to review and highlights the need to assess the collective completeness of movement studies and identify gaps. We surveyed 1,000 randomly selected papers from 496 journals and compared the facets of movement studied with a suggested framework for movement ecology, consisting of internal state (motivation, physiology), motion and navigation capacities, and external factors (both the physical environment and living organisms), and links among these components. Most studies simply measured and described the movement of organisms without reference to ecological or internal factors, and the most frequently studied part of the framework was the link between external factors and motion capacity. Few studies looked at the effects on movement of navigation capacity, or internal state, and those were mainly from vertebrates. For invertebrates and plants most studies were at the population level, whereas more vertebrate studies were conducted at the individual level. Consideration of only population-level averages promulgates neglect of between-individual variation in movement, potentially hindering the study of factors controlling movement. Terminology was found to be inconsistent among taxa and subdisciplines. The gaps identified in coverage of movement studies highlight research areas that should be addressed to fully understand the ecology of movement.

Mechanisms of Coexistence in Competitive Metacommunities

Although there is a large body of theory on spatial competitive coexistence, very little of it involves comparative analyses of alternative mechanisms. We thus have limited knowledge of the conditions under which multiple spatial mechanisms can operate or of emergent properties arising from interactions between mechanisms. Here we present a mathematical framework that allows for comparative analysis of spatial coexistence mechanisms. The basis for comparison is mechanisms operating in spatially homogeneous competitive environments (e.g., life‐history trade‐offs) versus mechanisms operating in spatially heterogeneous competitive environments (e.g., source‐sink dynamics). Our comparative approach leads to several new insights about spatial coexistence. First, we show that spatial variation in the expression of a life‐history trade‐off leads to a unique regional pattern that cannot be predicted by considering trade‐offs or source‐sink dynamics alone. This result represents an instance where spatial heterogeneity constrains rather than promotes coexistence, and it illustrates the kind of counterintuitive emergent properties that arise due to interactions between different classes of mechanisms. Second, we clarify the role of dispersal mortality in spatial coexistence. Previous studies have shown that coexistence can be constrained or facilitated by dispersal mortality. Our broader analysis distinguishes situations where dispersal mortality is not necessary for coexistence from those where such mortality is essential for coexistence because it preserves spatial variation in the strength of competition. These results form the basis for two important future directions: evolution of life‐history traits in spatially heterogeneous environments and elucidation of the cause and effect relationship(s) between biodiversity and ecosystem functioning.

The role of dispersal in predator-prey metapopulation dynamics

We report the role of dispersal in the metapopulation dynamics of a protist predator-prey pair, the predaceous ciliate Didinium nasutum Muller feeding on the bacterivorous ciliate Colpidium cf. striatum Stokes. In previous work we showed that this extinction-prone pair persisted as metapopulations in subdivided habitats. An experiment assessed the effects of habitat subdivision on persistence and dynamics. Undivided habitats were 270 or 750 mL in volume, and subdivided habitats (arrays) were sets of nine or 25 linked 30mL bottles (270 or 750mL total volume), each replicated three times. Undivided microcosms allowed maximum dispersal, whereas subdivision reduced dispersal. Within arrays, bottles with more connecting tubes allowed more dispersal. Nine and 25 bottle arrays also differed in the mean number of connections per bottle. The effects of dispersal on predator-prey dynamics were tested by comparing subdivided vs. undivided microcosms, bottles with different numbers of connecting tubes, and nine vs. 25 bottle arrays. We tested the following predictions from metapopulation theory. (i) Predator and prey persistence and predator abundance will be greatest at intermediate dispersal rates. (ii) Prey abundance, local population variability and asynchrony in population fluctuations will be greatest at low dispersal rates. (iii) Predator :prey ratios will be greatest at high dispersal rates. Predictions were confirmed, except for the following. (i) Two measures of synchrony differed in whether they showed the expected pattern. Spatial synchrony (estimated via correlation of densities among patches within sampling dates) showed high variance and did not vary with dispersal rates. However, spatial variability (CV of density across adjacent pairs of linked bottles), showed the predicted decrease with increased dispersal. (ii) Evidence that dispersal increases predator :prey ratios was inconclusive. Predator :prey ratios were lower in undivided 750mL microcosms than in 750mL arrays, possibly because predators over-exploited prey in undivided microcosms, so that both became scarce. Conversely, within arrays, predator :prey ratios were greatest in bottles that allowed the most dispersal, as predicted. This work generally confirms the predicted effects of dispersal on predator-prey metapopulation dynamics. It also demonstrates the need for models to include more realism, e.g. the possibility of over-exploitation with very high dispersal.

RECONCILING EMPIRICAL ECOLOGY WITH NEUTRAL COMMUNITY MODELS

Neutral community models embody the idea that individuals are ecologically equivalent, having equal fitness over all environmental conditions, and describe how the spatial dynamics and speciation of such individuals can produce a wide range of patterns of distribution, diversity, and abundance. Neutral models have been controversial, provoking a rush of tests and comments. The debate has been spurred by the suggestion that we should test mechanisms. However, the mechanisms and the spatial scales of interest have never clearly been described, and consequently, the tests have often been only peripherally relevant. At least two mechanisms are present in spatially structured neutral models. Dispersal limitation causes clumping of a species, which increases the strength of intraspecific competition and reduces the strength of interspecific competition. This may prolong coexistence and enhance local and regional diversity. Speciation is present in some neutral models and gives a donor-controlled input of new species, many of which remain rare or are short lived, but which directly add to species diversity. Spatial scale is an important consideration in neutral models. Ecological equivalence and equal fitness have implicit spatial scales because dispersal limitation and its emergent effects operate at population levels, and populations and communities are defined at a chosen spatial scale in recent neutral models; equality is measured relative to a metacommunity, and this necessitates defining the spatial scale of that metacommunity. Furthermore, dispersal has its own scales. Thorough empirical tests of neutral models will require both tests of mechanisms and pattern-producing ability, and will involve coupling theoretical models and experiments.

Habitat Patch Arrangement and Metapopulation Persistence of Predators and Prey

This study tests whether spatial dynamics can stabilize metapopulations with a small number of patches and tests the influence of patch arrangement. I measured persistence of predator and prey protists in replicated microcosms with two to four patches. Predators persisted for 85–437 generations (26–130 d). As predicted by single‐species and/or predator‐prey metapopulation models, substantial variation in predator metapopulation persistence was accounted for by the amount of patches or habitat, number of dispersal corridors, maximum interpatch distance, and proportion of patches providing colonists (which depends on the explicit spatial arrangement of patches). Contrary to expectation, persistence was not influenced by loops of patches or patch similarity. Persistence was also shorter in four‐patch loops than three‐patch loops, indicating an interaction between patch number and arrangement, which is not predicted by published models. Spatial synchrony of density fluctuations was central to predator persistence but had complex effects on extinction‐colonization dynamics, rescue effects, and predator‐prey interaction strength. Levins’s model, containing only extinction‐colonization dynamics, predicted patch occupancy for prey but not predators. Predators did, however, show rescue effects and changes in interaction strength. This work illustrates the need to combine experimentation with modeling to understand the mechanisms of spatial dynamics.

Omnivory and the stability of simple food webs

Abstract Traditional ecological theory predicts that the stability of simple food webs will decline with an increasing number of trophic levels and increasing amounts of omnivory. These ideas have been tested using protozoans in laboratory microcosms. However, the results are equivocal, and contrary to expectation, omnivory is common in natural food webs. Two recent developments lead us to re-evaluate these predictions using food webs assembled from protists and bacteria. First, recent modelling work suggests that omnivory is actually stabilizing, providing that interactions are not too strong. Second, it is difficult to evaluate the degree of omnivory of some protozoan species without explicit experimental tests. This study used seven species of ciliated protozoa and a mixed bacterial flora to assemble four food webs with two trophic levels, and four webs with three trophic levels. Protist species were assigned a rank for their degree of omnivory using information in the literature and the results of experiments that tested whether the starvation rate of predators was influenced by the amount of bacteria on which they may have fed and whether cannibalism (a form of omnivory) occurred. Consistent with recent modelling work, both bacterivorous and predatory species with higher degrees of omnivory showed more stable dynamics, measured using time until extinction and the temporal variability of population density. Systems with two protist species were less persistent than systems with one protist species, supporting the prediction that longer food chains will be less stable dynamically.

DISTINGUISHING STRESSORS ACTING ON LAND BIRD COMMUNITIES IN AN URBANIZING ENVIRONMENT

Urbanization has profound influences on ecological communities, but our understanding of causal mechanisms is limited by a lack of attention to its component stressors. Published research suggests that at landscape scales, habitat loss and fragmentation are the major drivers of community change, whereas at local scales, human activity and vegetation management are the primary stressors. Little research has focused on whether urbanization stressors may supplant natural factors as dominant forces structuring communities. We used model selection to determine the relative importance of urban development, human activity, local and landscape vegetation, topography, and geographical location in explaining land bird species richness, abundance, and dominance. We analyzed the entire community and groups of species based on ecological characteristics, using data collected in remnant forests along a gradient of urban development in the Lake Tahoe basin, California and Nevada, USA. Urbanization stressors were consistently among the principal forces structuring the land bird community. Strikingly, disturbance from human activity was the most important factor for richness in many cases, surpassing even habitat loss from development. Landscape-scale factors were consistently more important than local-scale factors for abundance. In demonstrating considerable changes in land bird community structure, our results suggest that ecosystem function in urban areas may be severely compromised. Such changes compel local- and landscape-scale management, focused research, and long-term monitoring to retain biodiversity in urban areas to the extent possible.

Transcontinental Crashes of Insect Populations

1. Department of Ecology and Evolutionary Biology, University factors that may be operating within the populations. Beof California, Irvine, California 92697 cause our focus was on the drought, we also obtained 2. Department of Entomology, University of California, Davis, records of annual precipitation for the regions where California 95616-8584 each insect population occurs for the period 1978–1996. We located time-series data for 10 insect taxa, repreSubmitted December 4, 1997; Accepted March 17, 1998 senting a wide range of life histories, habitats, and geographic regions in North America (references in fig. 1 legend): gypsy moth (Lymantria dispar, Lepidoptera: Lymantriidae) in Massachusetts; a multispecies complex of