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Hawai‘i forest review: Synthesizing the ecology, evolution, and conservation of a model system

As the most remote archipelago in the world, the Hawaiian Islands are home to a highly endemic and disharmonic biota that has fascinated biologists for centuries. Forests are the dominant terrestrial biome in Hawai‘i, spanning complex, heterogeneous climates across substrates that vary tremendously in age, soil structure, and nutrient availability. Species richness is low in Hawaiian forests compared to other tropical forests, as a consequence of dispersal limitation from continents and adaptive radiations in only some lineages, and forests are dominated by the widespread Metrosideros species complex. Low species richness provides a relatively tractable model system for studies of community assembly, local adaptation, and species interactions. Moreover, Hawaiian forests provide insights into predicted patterns of evolution on islands, revealing that while some evidence supports “island syndromes,” there are exceptions to them all. For example, Hawaiian plants are not as a whole less defended against herbivores, less dispersible, more conservative in resource use, or more slow-growing than their continental relatives. Clearly, more work is needed to understand the drivers, sources, and constraints on phenotypic variation among Hawaiian species, including both widespread and rare species, and to understand the role of this variation for ecological and evolutionary processes, which will further contribute to conservation of this unique biota. Today, Hawaiian forests are among the most threatened globally. Resource management failures – the proliferation of non-native species in particular – have led to devastating declines in native taxa and resulted in dominance by novel species assemblages. Conservation and restoration of Hawaiian forests now rely on managing threats including climate change, ongoing species introductions, novel pathogens, lost mutualists, and altered ecosystem dynamics through the use of diverse tools and strategies grounded in basic ecological, evolutionary, and biocultural principles. The future of Hawaiian forests thus depends on the synthesis of ecological and evolutionary research, which will continue to inform future conservation and restoration practices.

Hawaii

Phylogeny and species traits predict bird detectability

Avian acoustic communication has resulted from evolutionary pressures and ecological constraints. We therefore expect that auditory detectability in birds might be predictable by species traits and phylogenetic relatedness. We evaluated the relationship between phylogeny, species traits, and field‐based estimates of the two processes that determine species detectability (singing rate and detection distance) for 141 bird species breeding in boreal North America. We used phylogenetic mixed models and cross‐validation to compare the relative merits of using trait data only, phylogeny only, or the combination of both to predict detectability. We found a strong phylogenetic signal in both singing rates and detection distances; however the strength of phylogenetic effects was less than expected under Brownian motion evolution. The evolution of behavioural traits that determine singing rates was found to be more labile, leaving more room for species to evolve independently, whereas detection distance was mostly determined by anatomy (i.e. body size) and thus the laws of physics. Our findings can help in disentangling how complex ecological and evolutionary mechanisms have shaped different aspects of detectability in boreal birds. Such information can greatly inform single‐ and multi‐species models but more work is required to better understand how to best correct possible biases in phylogenetic diversity and other community metrics.

Ecography

An old tree and its many‐shaped leaves

Plant leaf shape is highly variable. The beauty of leaves can be purely aesthetic, but also derives from the mystery of adaptive significance. This mystery is especially compelling for species with strongly varying leaf shape on a single tree. The desert poplar (Populus euphratica Oliv.) is an ancient and protected species, and forms riparian forests in deserts of mid and west Asia, north Africa and southern Europe. More than half of all desert poplar forest is found along the Tarim River within the Taklamakan, a desert in northwest China. The Taklamakan is in the rain shadow of the Himalayas and the world’s second largest shifting sand desert. There, forest extent has been greatly reduced, mostly due to flow diversion for agriculture, but many old trees persist. The tree in the picture is the oldest recorded living desert poplar. The innermost ring in a core dates back to 1709 or earlier. The leaves on this tree vary widely in shape, from smooth to dentate, from narrow to broad, and from linear to lanceolate to ovate. Drought is a dominant stressor in this hyperarid environment with highly variable temperature and soil salinity. Leaf shape may relate to tradeoffs among water conservation, thermoregulation and growth rate. Is this extremely wide variation in leaf shape on a single tree an adaptation to the large temporal fluctuations in the environment? Alternatively, could leaf polymorphism be a neutral and thus non-adaptive consequence of variable gene expressions related to developmental stages. Answers to these questions can enrich the ecological and evolutionary understanding of trees and ecological drought.

Frontiers in Ecology and the Environment

Improving ecological data science with workflow management software

Pressing environmental research questions demand the integration of increasingly diverse and large-scale ecological datasets as well as complex analytical methods, which require specialized tools and resources. Computational training for ecological and evolutionary sciences has become more abundant and accessible over the past decade, but tool development has outpaced the availability of specialized training. Most training for scripted analyses focuses on individual analysis steps in one script rather than creating a scripted pipeline, where modular functions comprise an ecosystem of interdependent steps. Although current computational training creates an excellent starting place, linear styles of scripting can risk becoming labor- and time-intensive and less reproducible by often requiring manual execution. Pipelines, however, can be easily automated or tracked by software to increase efficiency and reduce potential errors. Ecology and evolution would benefit from techniques that reduce these risks by managing analytical pipelines in a modular, readily parallelizable format with clear documentation of dependencies. Workflow management software (WMS) can aid in the reproducibility, intelligibility and computational efficiency of complex pipelines. To date, WMS adoption in ecology and evolutionary research has been slow. We discuss the benefits and challenges of implementing WMS and illustrate its use through a case study with the targets r package to further highlight WMS benefits through workflow automation, dependency tracking and improved clarity for reviewers. Although WMS requires familiarity with function-oriented programming and careful planning for more advanced applications and pipeline sharing, investment in training will enable access to the benefits of WMS and impart transferable computing skills that can facilitate ecological and evolutionary data science at large scales.

Methods in Ecology and Evolution

The ecology of extinctions in kelp forest communities

We recognize three levels of extinction–global, local, and ecological – and provide examples of each. The protection and recovery of sea otters (Enhydra lutris) has provided abundant evidence of the consequences of their local extinction from kelp forest communities in the North Pacifc Ocean. These consequences include release of benthic invertebrate populations from limitation by predation; deforestation of kelp beds due to increased grazing by herbivorous sea urchins, one of the otter's main prey; and various cascading effects resulting from the biological and physical importance of kelp in coastal ecosystems. These interactions probably were important agents of selection for certain species. Two other examples are discussed: Steller's sea cow (Hydrodamalis gigas), a case of global extinction, and spiny lobsters, a possible case of ecological extinction. We speculate that grazing by sea cows was an important disturbance to surface-canopy-forming kelps and other algae in the littoral zones, but also point out that any such interactions probably acted in concert with physical disturbances by ocean waves. The ecological and evolutionary importance of sea cow grazing probably will remain a matter of speculation and conjecture because the species is globally extinct. Predation by spiny lobsters limits a variety of littoral and sublittoral invertebrate populations, particularly mollusks In one remarkable example, the reduction or local extinction of spiny lobsters enabled predutory whelks to increase in size and abundance, ultimately resulting in a predutor-prey role reversal. From these and other case studies we can clued that (1) the extinction of consumers may have brad and sometimes unexpected influences on kelp forest ecosystems; (2) direct or indirect interactions with now-extinct species probably exerted important selective influences on many extant forms; (3) such ecological and evolutionary influences are best understood where local or ecological extinctions, followed by recoveries, have provided comparisons in space or time; and (4) because of various ecological and behavioral barriers, local extinctions and their ecological consequences may not be simply reversed by protecting or reintroducing depleted or locally extinct species.

Conservation Biology

Spatial personalities: A meta-analysis of consistent individual differences in spatial behavior

Individual variation in behavior, particularly consistent among-individual differences (i.e., personality), has important ecological and evolutionary implications for population and community dynamics, trait divergence, and patterns of speciation. Nevertheless, individual variation in spatial behaviors, such as home range behavior, movement characteristics, or habitat use has yet to be incorporated into the concepts or methodologies of ecology and evolutionary biology. To evaluate evidence for the existence of consistent among-individual differences in spatial behavior – which we refer to as “spatial personality” – we performed a meta-analysis of 200 repeatability estimates of home range size, movement metrics, and habitat use. We found that the existence of spatial personality is a general phenomenon, with consistently high repeatability (r) across classes of spatial behavior (r = 0.67–0.82), taxa (r = 0.31–0.79), and time between repeated measurements (r = 0.54–0.74). These results suggest: 1) repeatable spatial behavior may either be a cause or consequence of the environment experienced and lead to spatial personalities that may limit the ability of individuals to behaviorally adapt to changing landscapes; 2) interactions between spatial phenotypes and environmental conditions could result in differential reproduction, survival, and dispersal, suggesting that among-individual variation may facilitate population-level adaptation; 3) spatial patterns of species' distributions and spatial population dynamics may be better understood by shifting from a mean field analytical approach towards methods that account for spatial personalities and their associated fitness and ecological dynamics.

Behavioral Ecology

Comparing marine and terrestrial ecosystems: Implications for the design of coastal marine reserves

Concepts and theory for the design and application of terrestrial reserves is based on our understanding of environmental, ecological, and evolutionary processes responsible for biological diversity and sustainability of terrestrial ecosystems and how humans have influenced these processes. How well this terrestrial -based theory can be applied toward the design and application of reserves in the coastal marine environment depends, in part, on the degree of similarity between these systems. Several marked differences in ecological and evolutionary processes exist between marine and terrestrial ecosystems as ramifications of fundamental differences in their physical environments (i.e., the relative prevalence of air and water) and contemporary patterns of human impacts. Most notably, the great extent and rate of dispersal of nutrients, materials, holoplanktonic organisms, and reproductive propagules of benthic organisms expand scales of connectivity among near-shore communities and ecosystems . Consequently, the "openness" of marine populations, communities, and ecosystems probably has marked influences on their spatial, genetic, and trophic structures and dynamics in ways experienced by only some terrestrial species. Such differences appear to be particularly significant for the kinds of organisms most exploited and targeted for protection in coastal marine ecosystems (fishes and macroinvertebrates). These and other differences imply some unique design criteria and application of reserves in the marine environment. In explaining the implications of these differences for marine reserve design and application, we identify many of the environmental and ecological processes and design criteria necessary for consideration in the development of the analytical approaches developed elsewhere in this Special Issue.

Ecological Applications

Legacy introductions and climatic variation explain spatiotemporal patterns of invasive hybridization in a native trout

Hybridization between invasive and native species, a significant threat to worldwide biodiversity, is predicted to increase due to climate-induced expansions of invasive species. Long-term research and monitoring are crucial for understanding the ecological and evolutionary processes that modulate the effects of invasive species. Using a large, multi-decade genetics dataset (N = 582 sites, 12,878 individuals) with high-resolution climate predictions and extensive stocking records, we evaluate the spatiotemporal dynamics of hybridization between native cutthroat trout and invasive rainbow trout, the world’s most widely introduced invasive fish, across the northern Rocky Mountains of the United States. Historical effects of stocking and contemporary patterns of climatic variation were strongly related to the spread of hybridization across space and time. The probability of occurrence, extent of, and temporal changes in hybridization increased at sites in close proximity to historical stocking locations with greater rainbow trout propagule pressure, warmer water temperatures, and lower spring precipitation. Although locations with warmer water temperatures were more prone to hybridization, cold sites were not protected from invasion; 58% of hybridized sites had cold mean summer water temperatures (<11 ° C). Despite cessation of stocking over 40 years ago, hybridization increased over time at half (50%) of the locations with long-term data, the vast majority of which (74%) were initially non-hybridized, emphasizing the chronic, negative impacts of human-mediated hybridization. These results show that effects of climate change on biodiversity must be analyzed in the context of historical human impacts that set ecological and evolutionary trajectories.

Global Change Biology

Representing plant diversity in land models: An evolutionary approach to make ‘Functional Types’ more functional

Plants are critical mediators of terrestrial mass and energy fluxes, and their structural and functional traits have profound impacts on local and global climate, biogeochemistry, biodiversity, and hydrology. Yet Earth System Models (ESMs), our most powerful tools for predicting the effects of humans on the coupled biosphere-atmosphere system, simplify the incredible diversity of land plants into a handful of coarse categories of ‘Plant Functional Types’ (PFTs) that often fail to capture ecological dynamics such as biome distributions. The inclusion of more realistic functional diversity is a recognized goal for ESMs, yet there is currently no consistent, widely accepted way to add diversity to models, i.e. to determine what new PFTs to add and with what data to constrain their parameters. We review approaches to representing plant diversity in ESMs and draw on recent ecological and evolutionary findings to present an evolution-based functional type approach for further disaggregating functional diversity. Specifically, the prevalence of niche conservatism, or the tendency of closely related taxa to retain similar ecological and functional attributes through evolutionary time, reveals that evolutionary relatedness is a powerful framework for summarizing functional similarities and differences among plant types. We advocate that Plant Functional Types based on dominant evolutionary lineages (‘Lineage Functional Types’) will provide an ecologically defensible, tractable, and scalable framework for representing plant diversity in next-generation ESMs, with the potential to improve parameterization, process representation, and model benchmarking. We highlight how the importance of evolutionary history for plant function can unify the work of disparate fields to improve predictive modeling of the Earth system.

Global Change Biology

Ecological community integration increases with added trophic complexity

The existence of functional biological organization at the level of multi-species communities has long been contested in ecology and evolutionary biology. I found that adding a trophic level to simulated ecological communities enhanced their ability to compete at the community level, increasing the likelihood of one community forcing all or most species in a second community to extinction. Community-level identity emerged within systems of interacting ecological networks, while competitive ability at the community level was enhanced by intense within-community selection pressure. These results suggest a reassessment of the nature of biological organization above the level of species, indicating that the drive toward biological integration, so prominent throughout the history of life, might extend to multi-species communities.

Ecological Complexity

Exploiting common senses: Sensory ecology meets wildlife conservation and management

Multidisciplinary approaches to conservation and wildlife management are often effective in addressing complex, multi-factor problems. Emerging fields such as conservation physiology and conservation behaviour can provide innovative solutions and management strategies for target species and systems. Sensory ecology combines the study of ‘how animals acquire’ and process sensory stimuli from their environments, and the ecological and evolutionary significance of ‘how animals respond’ to this information. We review the benefits that sensory ecology can bring to wildlife conservation and management by discussing case studies across major taxa and sensory modalities. Conservation practices informed by a sensory ecology approach include the amelioration of sensory traps, control of invasive species, reduction of human–wildlife conflicts and relocation and establishment of new populations of endangered species. We illustrate that sensory ecology can facilitate the understanding of mechanistic ecological and physiological explanations underlying particular conservation issues and also can help develop innovative solutions to ameliorate conservation problems.

Conservation Physiology

Tadpoles: the Biology of Anuran Larvae

The recent alarming declines in amphibian populations worldwide and the suitability of amphibians for use in answering research questions in disciplines as diverse as molecular systematics, animal behavior, ecology, and evolutionary biology have focused enormous attention on tadpoles. Yet despite this growing interest, relatively little is known about these fascinating creatures. n this invaluable reference, leading experts on tadpole biology relate what we currently know about tadpoles and what we might learn from them in the future. Tadpoles provides detailed summaries of tadpole morphology, development, behavior, ecology, and environmental physiology; explores the evolutionary consequences of the tadpole stage; synthesizes available information on their biodiversity, and presents a standardized terminology and an exhaustive literature review of tadpole biology.

Book

Overview of emerging amphibian pathogens and modeling advances for conservation-related decisions

One of the leading causes of global amphibian decline is emerging infectious disease. We summarize the disease ecology of four major emerging amphibian infectious agents: chytrids, ranaviruses, trematodes, and Perkinsea. We focus on recently developed quantitative advances that build on well-established ecological theories and aid in studying epizootic and enzootic disease dynamics. For example, we identify ecological and evolutionary selective forces that determine disease outcomes and transmission pathways by borrowing ideas from population and community ecology theory. We outline three topics of general interest in disease ecology: (i) the relationship between biodiversity and disease risk, (ii) individual, species, or environmental transmission heterogeneity, and (iii) pathogen coinfections. Finally, we identify specific knowledge gaps impeding the success of conservation-related decisions for disease mitigation and the future of amphibian conservation success.

Biological Conservation

Sampling in ecology and evolution - bridging the gap between theory and practice

Sampling is a key issue for answering most ecological and evolutionary questions. The importance of developing a rigorous sampling design tailored to specific questions has already been discussed in the ecological and sampling literature and has provided useful tools and recommendations to sample and analyse ecological data. However, sampling issues are often difficult to overcome in ecological studies due to apparent inconsistencies between theory and practice, often leading to the implementation of simplified sampling designs that suffer from unknown biases. Moreover, we believe that classical sampling principles which are based on estimation of means and variances are insufficient to fully address many ecological questions that rely on estimating relationships between a response and a set of predictor variables over time and space. Our objective is thus to highlight the importance of selecting an appropriate sampling space and an appropriate sampling design. We also emphasize the importance of using prior knowledge of the study system to estimate models or complex parameters and thus better understand ecological patterns and processes generating these patterns. Using a semi-virtual simulation study as an illustration we reveal how the selection of the space (e.g. geographic, climatic), in which the sampling is designed, influences the patterns that can be ultimately detected. We also demonstrate the inefficiency of common sampling designs to reveal response curves between ecological variables and climatic gradients. Further, we show that response-surface methodology, which has rarely been used in ecology, is much more efficient than more traditional methods. Finally, we discuss the use of prior knowledge, simulation studies and model-based designs in defining appropriate sampling designs. We conclude by a call for development of methods to unbiasedly estimate nonlinear ecologically relevant parameters, in order to make inferences while fulfilling requirements of both sampling theory and field work logistics. ?? 2010 The Authors.

Ecography

Microsatellites: Evolutionary and methodological background and empirical applications at individual, population, and phylogenetic levels

The recent proliferation and greater accessibility of molecular genetic markers has led to a growing appreciation of the ecological and evolutionary inferences that can be drawn from molecular characterizations of individuals and populations (Burke et al. 1992, Avise 1994). Different techniques have the ability to target DNA sequences which have different patterns of inheritance, different modes and rates of evolution and, concomitantly, different levels of variation. In the quest for 'the right marker for the right job', microsatellites have been widely embraced as the marker of choice for many empirical genetic studies. The proliferation of microsatellite loci for various species and the voluminous literature compiled in very few years associated with their evolution and use in various research applications, exemplifies their growing importance as a research tool in the biological sciences. The ability to define allelic states based on variation at the nucleotide level has afforded unparalleled opportunities to document the actual mutational process and rates of evolution at individual microsatellite loci. The scrutiny to which these loci have been subjected has resulted in data that raise issues pertaining to assumptions formerly stated, but largely untestable for other marker classes. Indeed this is an active arena for theoretical and empirical work. Given the extensive and ever-increasing literature on various statistical methodologies and cautionary notes regarding the uses of microsatellites, some consideration should be given to the unique characteristics of these loci when determining how and under what conditions they can be employed.

Book chapter

Climate dipoles as continental drivers of plant and animal populations

Ecological processes, such as migration and phenology, are strongly influenced by climate variability. Studying these processes often relies on associating observations of animals and plants with climate variability indices, such as the El Niño–Southern Oscillation. A characteristic of climate indices is the simultaneous emergence of opposite extremes of temperature and precipitation across continental scales, known as climate dipoles. The role of climate dipoles in shaping ecological and evolutionary processes has been largely overlooked. We review emerging evidence that climate dipoles can entrain species dynamics, and offer a framework for identifying ecological dipoles using broad-scale biological data. Given future changes in climatic and atmospheric processes, climate and ecological dipoles will likely shift in their intensity, distribution, and timing.

Trends in Ecology and Evolution

Generalizing indirect defense and resistance of plants

Indirect defence, the adaptive top‐down control of herbivores by plant traits that enhance predation, is a central component of plant–herbivore interactions. However, the scope of interactions that comprise indirect defence and associated ecological and evolutionary processes has not been clearly defined. We argue that the range of plant traits that mediate indirect defence is much greater than previously thought, and we further organise major concepts surrounding their ecological functioning. Despite the wide range of plant traits and interacting organisms involved, indirect defences show commonalities when grouped. These categories are based on whether indirect defences boost natural enemy abundance via food or shelter resources, or, alternatively, increase natural enemy foraging efficiency via information or alteration of habitat complexity. The benefits of indirect defences to natural enemies should be further explored to establish the conditions in which indirect defence generates a plant–natural enemy mutualism. By considering the broader scope of plant–herbivore–natural enemy interactions that comprise indirect defence, we can better understand plant‐based food webs, as well as the evolutionary processes that have shaped them.

Ecology Letters

New trends in species distribution modelling

Species distribution modelling has its origin in the late 1970s when computing capacity was limited. Early work in the field concentrated mostly on the development of methods to model effectively the shape of a species' response to environmental gradients (Austin 1987, Austin et al. 1990). The methodology and its framework were summarized in reviews 10&ndash;15 yr ago (Franklin 1995, Guisan and Zimmermann 2000), and these syntheses are still widely used as reference landmarks in the current distribution modelling literature. However, enormous advancements have occurred over the last decade, with hundreds &ndash; if not thousands &ndash; of publications on species distribution model (SDM) methodologies and their application to a broad set of conservation, ecological and evolutionary questions. With this special issue, originating from the third of a set of specialized SDM workshops (2008 Riederalp) entitled 'The Utility of Species Distribution Models as Tools for Conservation Ecology', we reflect on current trends and the progress achieved over the last decade.

Ecography