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Facilitating comparable research in seedling functional ecology

Ecologists have worked to ascribe function to the variation found in plant populations, communities and ecosystems across environments for at least the past century. The vast body of research in functional ecology has drastically improved understanding of how individuals respond to their environment, communities are assembled and ecosystems function. However, with limited exceptions, few studies have quantified differences in plant function during the earliest stages of the plant life cycle, and fewer have tested how this early variability shapes populations, communities and ecosystems. Drawing from the literature and our collective experience, we describe the current state of knowledge in seedling functional ecology and provide examples of how this subdiscipline can enrich our fundamental understanding of plant function across levels of organisation. To inspire progressive work in this area, we also outline key considerations involved in seedling functional research (who, what, when, where and how to measure seedling traits) and identify remaining challenges and gaps in understanding around methodological approaches. Within this conceptual synthesis, we highlight three critical areas in seedling ecology for future research to target. First, given wide variation in the definition of a ‘seedling’, we provide a standard definition based on seed reserve dependence while emphasising the need to measure ontogenetic variation more clearly both within and following the seedling stage. Second, studies demonstrate that seedlings can be studied in multiple media (e.g. soil, agar, filter paper) and conditions (e.g. field, greenhouse, laboratory). We recommend that researchers select methods based on explicit goals, yet follow standard guidelines to reduce methodological noise across studies. Third, research is critically needed to assess the implications of different methodologies on trait measurement and compatibility across studies. By highlighting the importance of seedling functional ecology and suggesting pathways to address key challenges, we aim to inspire future research that generates useful and comparable data on seedling functional ecology. This work is critical to explain variation within and among populations, communities and ecosystems and integrate this most vulnerable stage of plant life into ecological frameworks.

Methods in Ecology & Evolution

Dispersive currents explain patterns of population connectivity in an ecologically and economically important fish

How to identify the drivers of population connectivity remains a fundamental question in ecology and evolution. Answering this question can be challenging in aquatic environments where dynamic lake and ocean currents coupled with high levels of dispersal and gene flow can decrease the utility of modern population genetic tools. To address this challenge, we used RAD-Seq to genotype 959 yellow perch ( Perca flavescens ), a species with an ~40-day pelagic larval duration (PLD), collected from 20 sites circumscribing Lake Michigan. We also developed a novel, integrative approach that couples detailed biophysical models with eco-genetic agent-based models to generate “predictive” values of genetic differentiation. By comparing predictive and empirical values of genetic differentiation, we estimated the relative contributions for known drivers of population connectivity (e.g., currents, behavior, PLD). For the main basin populations (i.e., the largest contiguous portion of the lake), we found that high gene flow led to low overall levels of genetic differentiation among populations ( F ST = 0.003). By far the best predictors of genetic differentiation were connectivity matrices that were derived from periods of time when there were strong and highly dispersive currents. Thus, these highly dispersive currents are driving the patterns of population connectivity in the main basin. We also found that populations from the northern and southern main basin are slightly divergent from one another, while those from Green Bay and the main basin are highly divergent ( F ST = 0.11). By integrating biophysical and eco-genetic models with genome-wide data, we illustrate that the drivers of population connectivity can be identified in high gene flow systems.

Lake Michigan

MASTREE+: Time-series of plant reproductive effort from six continents

Significant gaps remain in understanding the response of plant reproduction to environmental change. This is partly because measuring reproduction in long-lived plants requires direct observation over many years and such datasets have rarely been made publicly available. Here we introduce MASTREE+, a data set that collates reproductive time-series data from across the globe and makes these data freely available to the community. MASTREE+ includes 73,828 georeferenced observations of annual reproduction (e.g. seed and fruit counts) in perennial plant populations worldwide. These observations consist of 5971 population-level time-series from 974 species in 66 countries. The mean and median time-series length is 12.4 and 10 years respectively, and the data set includes 1122 series that extend over at least two decades (≥20 years of observations). For a subset of well-studied species, MASTREE+ includes extensive replication of time-series across geographical and climatic gradients. Here we describe the open-access data set, available as a.csv file, and we introduce an associated web-based app for data exploration. MASTREE+ will provide the basis for improved understanding of the response of long-lived plant reproduction to environmental change. Additionally, MASTREE+ will enable investigation of the ecology and evolution of reproductive strategies in perennial plants, and the role of plant reproduction as a driver of ecosystem dynamics.

Global Change Biology

The role of climate in the dynamics of a hybrid zone in Appalachian salamanders

I examined the potential influence of climate change on the dynamics of a previously studied hybrid zone between a pair of terrestrial salamanders at the Coweeta Hydrologic Laboratory, U.S. Forest Service, in the Nantahala Mountains of North Carolina, USA. A 16-year study led by Nelson G. Hairston, Sr. revealed that Plethodon teyahalee and Plethodon shermani hybridized at intermediate elevations, forming a cline between 'pure' parental P. teyahalee at lower elevations and 'pure' parental P. shermani at higher elevations. From 1974 to 1990 the proportion of salamanders at the higher elevation scored as 'pure' P. shermani declined significantly, indicating that the hybrid zone was spreading upward. To date there have been no rigorous tests of hypotheses for the movement of this hybrid zone. Using temperature and precipitation data from Coweeta, I re-analyzed Hairston's data to examine whether the observed elevational shift was correlated with variation in either air temperature or precipitation from the same time period. For temperature, my analysis tracked the results of the original study: the proportion of 'pure' P. shermani at the higher elevation declined significantly with increasing mean annual temperature, whereas the proportion of 'pure' P. teyahalee at lower elevations did not. There was no discernable relationship between proportions of 'pure' individuals of either species with variation in precipitation. From 1974 to 1990, low-elevation air temperatures at the Coweeta Laboratory ranged from annual means of 11.8 to 14.2 °C, compared with a 55-year average (1936-1990) of 12.6 °C. My re-analyses indicate that the upward spread of the hybrid zone is correlated with increasing air temperatures, but not precipitation, and provide an empirical test of a hypothesis for one factor that may have influenced this movement. My results aid in understanding the potential impact that climate change may have on the ecology and evolution of terrestrial salamanders in montane regions.

Global Change Biology

Worldwide phylogenetic relationship of avian poxviruses

Poxvirus infections have been found in 230 species of wild and domestic birds worldwide in both terrestrial and marine environments. This ubiquity raises the question of how infection has been transmitted and globally dispersed. We present a comprehensive global phylogeny of 111 novel poxvirus isolates in addition to all available sequences from GenBank. Phylogenetic analysis of the Avipoxvirus genus has traditionally relied on one gene region (4b core protein). In this study we expanded the analyses to include a second locus (DNA polymerase gene), allowing for a more robust phylogenetic framework, finer genetic resolution within specific groups, and the detection of potential recombination. Our phylogenetic results reveal several major features of avipoxvirus evolution and ecology and propose an updated avipoxvirus taxonomy, including three novel subclades. The characterization of poxviruses from 57 species of birds in this study extends the current knowledge of their host range and provides the first evidence of the phylogenetic effect of genetic recombination of avipoxviruses. The repeated occurrence of avian family or order-specific grouping within certain clades (e.g., starling poxvirus, falcon poxvirus, raptor poxvirus, etc.) indicates a marked role of host adaptation, while the sharing of poxvirus species within prey-predator systems emphasizes the capacity for cross-species infection and limited host adaptation. Our study provides a broad and comprehensive phylogenetic analysis of the Avipoxvirus genus, an ecologically and environmentally important viral group, to formulate a genome sequencing strategy that will clarify avipoxvirus taxonomy.

Journal of Virology

Causes, consequences, and conservation of ungulate migration

Our understanding of ungulate migration is advancing rapidly due to innovations in modern animal tracking. Herein, we review and synthesize nearly seven decades of work on migration and other long-distance movements of wild ungulates. Although it has long been appreciated that ungulates migrate to enhance access to forage, recent contributions demonstrate that their movements are fine tuned to dynamic landscapes, where forage, snow, and drought change seasonally. Researchers are beginning to understand how ungulates navigate migrations, with the emerging view that animals blend gradient tracking with spatial memory, some of which is socially learned. Although migration often promotes abundant populations—with broad effects on ecosystems—many migrations around the world have been lost or are currently threatened by habitat fragmentation, climate change, and barriers to movement. Fortunately, new efforts that use empirical tracking data to map migrations in detail are facilitating effective conservation measures needed to maintain ungulate migration.

Annual Review of Ecology, Evolution, and Systemati

Characterizing species interactions to understand press perturbations: What is the community matrix?

The community matrix is among ecology's most important mathematical abstractions, formally encapsulating the interconnected network of effects that species have on one another's populations. Despite its importance, the term `community matrix' has been applied to matrices having differing interpretations. This has hindered the application of theory for understanding community structure and perturbation responses, particularly in the contexts of ecosystem-based management and conservation. Here we clarify the correspondence and distinctions between the Interaction matrix, the Alpha matrix and the Jacobian matrix, terms which are frequently used interchangeably and have numerous synonyms, including the term Community matrix. We illustrate how these matrices correspond to different ways of characterizing interaction strengths, how they permit insights regarding different types of press perturbations of species growth rates or abundances, and how these are related by a simple scaling relationship. Connections to additional interaction strength characterizations encapsulated by the Beta matrix, the Gamma matrix, and the Removal matrix are also discussed. Our synthesis highlights the empirical challenges that remain in using these mathematical tools to understand actual communities.

Ecology, Evolution, and Systematics

Evolutionary ecology of fire

Fire has been an ecosystem process since plants colonized land over 400 million years ago. Many diverse traits provide a fitness benefit following fires, and these adaptive traits vary with the fire regime. Some of these traits enhance fire survival, while others promote recruitment in the postfire environment. Demonstrating that these traits are fire adaptations is challenging, since many arose early in the paleontological record, although increasingly better fossil records and phylogenetic analysis make timing of these trait origins to fire more certain. Resprouting from the base of stems is the most widely distributed fire-adaptive trait, and it is likely to have evolved under a diversity of disturbance types. The origins of other traits like serotiny, thick bark, fire-stimulated germination, and postfire flowering are more tightly linked to fire. Fire-adaptive traits occur in many environments: boreal and temperate forests, Mediterranean-type climate (MTC) shrublands, savannas, and other grasslands. MTC ecosystems are distinct in that many taxa in different regions have lost the resprouting ability and depend solely on postfire recruitment for postfire recovery. This obligate seeding mode is perhaps the most vulnerable fire-adaptive syndrome in the face of current global change, particularly in light of increasing anthropogenic fire frequency.

Annual Review of Ecology, Evolution, and Systemati

Functional ecology of free-living nitrogen fixation: A contemporary perspective

Nitrogen (N) availability is thought to frequently limit terrestrial ecosystem processes, and explicit consideration of N biogeochemistry, including biological N 2 fixation, is central to understanding ecosystem responses to environmental change. Yet, the importance of free-living N 2 fixation—a process that occurs on a wide variety of substrates, is nearly ubiquitous in terrestrial ecosystems, and may often represent the dominant pathway for acquiring newly available N—is often underappreciated. Here, we draw from studies that investigate free-living N 2 fixation from functional, physiological, genetic, and ecological perspectives. We show that recent research and analytical advances have generated a wealth of new information that provides novel insight into the ecology of N 2 fixation as well as raises new questions and priorities for future work. These priorities include a need to better integrate free-living N 2 fixation into conceptual and analytical evaluations of the N cycle's role in a variety of global change scenarios.

Annual Review of Ecology, Evolution, and Systemati

Observed and potential range shifts of native and non-native species with climate change

There is broad concern that the range shifts of global flora and fauna will not keep up with climate change, increasing the likelihood of population declines and extinctions. Many populations of nonnative species already have advantages over native species, including widespread human-aided dispersal and release from natural enemies. But do nonnative species also have an advantage with climate change? Here, we review observed and potential range shifts for native and nonnative species globally. We show that nonnative species are expanding their ranges orders of magnitude faster than native species, reflecting both traits that enable rapid spread and ongoing human-mediated introduction. We further show that nonnative species have large potential ranges and range expansions with climate change, likely due to a combination of widespread introduction and broader climatic tolerances. With faster spread rates and larger potential to persist or expand, nonnative populations have a decided advantage in a changing climate.

Annual Review of Ecology, Evolution, and Systemati

Interactions among invasive plants: Lessons from Hawai‘i

Most ecosystems have multiple-plant invaders rather than single-plant invaders, yet ecological studies and management actions focus largely on single invader species. There is a need for general principles regarding invader interactions across varying environmental conditions, so that secondary invasions can be anticipated and managers can allocate resources toward pretreatment or postremoval actions. By reviewing removal experiments conducted in three Hawaiian ecosystems (a dry tropical forest, a seasonally dry mesic forest, and a lowland wet forest), we evaluate the roles environmental harshness, priority effects, productivity potential, and species interactions have in influencing secondary invasions, defined here as invasions that are influenced either positively (facilitation) or negatively (inhibition/priority effects) by existing invaders. We generate a conceptual model with a surprise index to describe whether long-term plant invader composition and dominance is predictable or stochastic after a system perturbation such as a removal experiment. Under extremely low resource availability, the surprise index is low, whereas under intermediate-level resource environments, invader dominance is more stochastic and the surprise index is high. At high resource levels, the surprise index is intermediate: Invaders are likely abundant in the environment but their response to a perturbation is more predictable than at intermediate resource levels. We suggest further testing across environmental gradients to determine key variables that dictate the predictability of postremoval invader composition.

Hawai'i

Threshold changes in winter temperature and precipitation drive threshold responses across nine global climate zones and associated biomes

Globally, winter temperatures are rising, and snowpack is shrinking or disappearing entirely. Despite previous research and published literature reviews, it remains unknown whether biomes across the globe will cross important thresholds in winter temperature and precipitation that will lead to significant ecological changes. Here, we combine the widely used Köppen–Geiger climate classification system with worst-case-scenario projected changes in global monthly temperature and precipitation to illustrate how multiple climatic zones across Earth may experience shifting winter conditions by the end of this century. We then examine how these shifts may affect ecosystems within corresponding biomes. Our analysis demonstrates potential widespread losses of extreme cold (<−20°C) in Arctic, boreal, and cool temperate regions. We also show the possible disappearance of freezing temperatures (<0°C) and large decreases in snowfall in warm temperate and dryland areas. We identify important and potentially irreversible ecological changes associated with crossing these winter climate thresholds.

Annual Review of Ecology, Evolution, and Systemati

A multiscale, hierarchical model of pulse dynamics in arid-land ecosystems

Ecological processes in arid lands are often described by the pulse-reserve paradigm, in which rain events drive biological activity until moisture is depleted, leaving a reserve. This paradigm is frequently applied to processes stimulated by one or a few precipitation events within a growing season. Here we expand the original framework in time and space and include other pulses that interact with rainfall. This new hierarchical pulse-dynamics framework integrates space and time through pulse-driven exchanges, interactions, transitions, and transfers that occur across individual to multiple pulses extending from micro to watershed scales. Climate change will likely alter the size, frequency, and intensity of precipitation pulses in the future, and arid-land ecosystems are known to be highly sensitive to climate variability. Thus, a more comprehensive understanding of arid-land pulse dynamics is needed to determine how these ecosystems will respond to, and be shaped by, increased climate variability.

Annual Review of Ecology, Evolution, and Systemati

Marine infectious disease ecology

To put marine disease impacts in context requires a broad perspective on the roles infectious agents have in the ocean. Parasites infect most marine vertebrate and invertebrate species, and parasites and predators can have comparable biomass density, suggesting they play comparable parts as consumers in marine food webs. Although some parasites might increase with disturbance, most probably decline as food webs unravel. There are several ways to adapt epidemiological theory to the marine environment. In particular, because the ocean represents a three-dimensional moving habitat for hosts and parasites, models should open up the spatial scales at which infective stages and host larvae travel. In addition to open recruitment and dimensionality, marine parasites are subject to fishing, filter feeders, dosedependent infection, environmental forcing, and death-based transmission. Adding such considerations to marine disease models will make it easier to predict which infectious diseases will increase or decrease in a changing ocean.

Annual Review of Ecology, Evolution, and Systemati

Are diseases increasing in the ocean?

Many factors (climate warming, pollution, harvesting, introduced species) can contribute to disease outbreaks in marine life. Concomitant increases in each of these makes it difficult to attribute recent changes in disease occurrence or severity to any one factor. For example, the increase in disease of Caribbean coral is postulated to be a result of climate change and introduction of terrestrial pathogens. Indirect evidence exists that ( a ) warming increased disease in turtles; ( b ) protection, pollution, and terrestrial pathogens increased mammal disease; ( c ) aquaculture increased disease in mollusks; and ( d ) release from overfished predators increased sea urchin disease. In contrast, fishing and pollution may have reduced disease in fishes. In other taxa (e.g., sea grasses, crustaceans, sharks), there is little evidence that disease has changed over time. The diversity of patterns suggests there are many ways that environmental change can interact with disease in the ocean.

Annual Review of Ecology, Evolution, and Systemati

Individual-based modeling of ecological and evolutionary processes

Individual-based models (IBMs) allow the explicit inclusion of individual variation in greater detail than do classical differential-equation and difference-equation models. Inclusion of such variation is important for continued progress in ecological and evolutionary theory. We provide a conceptual basis for IBMs by describing five major types of individual variation in IBMs: spatial, ontogenetic, phenotypic, cognitive, and genetic. IBMs are now used in almost all subfields of ecology and evolutionary biology. We map those subfields and look more closely at selected key papers on fish recruitment, forest dynamics, sympatric speciation, metapopulation dynamics, maintenance of diversity, and species conservation. Theorists are currently divided on whether IBMs represent only a practical tool for extending classical theory to more complex situations, or whether individual-based theory represents a radically new research program. We feel that the tension between these two poles of thinking can be a source of creativity in ecology and evolutionary theory.

Annual Review of Ecology, Evolution, and Systemati

Genetic diversity and connectivity of chemosynthetic cold seep mussels from the U.S. Atlantic margin

Background Deep-sea mussels in the subfamily Bathymodiolinae have unique adaptations to colonize hydrothermal-vent and cold-seep environments throughout the world ocean. These invertebrates function as important ecosystem engineers, creating heterogeneous habitat and promoting biodiversity in the deep sea. Despite their ecological significance, efforts to assess the diversity and connectivity of this group are extremely limited. Here, we present the first genomic-scale diversity assessments of the recently discovered bathymodioline cold-seep communities along the U.S. Atlantic margin, dominated by Gigantidas childressi and Bathymodiolus heckerae . Results A Restriction-site Associated DNA Sequencing (RADSeq) approach was used on 177 bathymodiolines to examine genetic diversity and population structure within and between seep sites. Assessments of genetic differentiation using single-nucleotide polymorphism (SNP) data revealed high gene flow among sites, with the shallower and more northern sites serving as source populations for deeper occurring G. childressi . No evidence was found for genetic diversification across depth in G. childressi , likely due to their high dispersal capabilities. Kinship analyses indicated a high degree of relatedness among individuals, and at least 10–20% of local recruits within a particular site. We also discovered candidate adaptive loci in G. childressi and B. heckerae that suggest differences in developmental processes and depth-related and metabolic adaptations to chemosynthetic environments. Conclusions These results highlight putative source communities for an important ecosystem engineer in the deep sea that may be considered in future conservation efforts. Our results also provide clues into species-specific adaptations that enable survival and potential speciation within chemosynthetic ecosystems.

Atlantic Ocean, Baltimore Canyon Seep, Blake Ridge

Native amphibian toxin reduces invasive crayfish feeding with potential benefits to stream biodiversity

Background Biodiversity is generally reduced when non-native species invade an ecosystem. Invasive crayfish, Procambarus clarkii , populate California freshwater streams, and in the Santa Monica Mountains (Los Angeles, USA), their introduction has led to trophic cascades due to omnivorous feeding behavior and a rapid rate of population growth. The native California newt, Taricha torosa , possesses a neurotoxin, tetrodotoxin (TTX), that affects freshwater animal behavior. Given P. clarkii has a limited evolutionary history with TTX, we hypothesized that TTX may affect crayfish feeding behaviors. To determine if TTX affects P. clarkii behavior, we measured cumulative movement and various feeding behaviors of P. clarkii exposed to (i) waterborne, ecologically realistic concentrations of TTX (~ 3.0 × 10 − 8 moles/L), (ii) an anuran chemical cue to account for intraguild cues, or (iii) a T. torosa chemical cue with quantitated TTX in it (~ 6.2 × 10 − 8 moles/L). Results We found that the presence of TTX in any form significantly reduced crayfish movement and decreased the amount of food consumed over time. Crayfish responses to the anuran treatment did not significantly differ from controls. Conclusion Our laboratory results show that naturally occurring neurotoxin from native California newts limits invasive crayfish foraging and feeding rates, which may play a role in preserving local stream ecosystems by limiting invasive crayfish behaviors that are detrimental to biodiversity.

California