Slower environmental cycles maintain greater life-history variation within populations.

Populations in nature are comprised of individual life histories, whose variation underpins ecological and evolutionary processes. Yet the forces of environmental selection that shape intrapopulation life-history variation are still not well-understood, and efforts have largely focused on random (stochastic) fluctuations of the environment. However, a ubiquitous mode of environmental fluctuation in nature is cyclical, whose periodicities can change independently of stochasticity. Here, we test theoretically based hypotheses for whether shortened ('Fast') or lengthened ('Slow') environmental cycles should generate higher intrapopulation variation of life history phenotypes. We show, through a combination of agent-based modelling and a multi-generational laboratory selection experiment using the tidepool copepod Tigriopus californicus, that slower environmental cycles maintain higher levels of intrapopulation variation. Surprisingly, the effect of environmental periodicity on variation was much stronger than that of stochasticity. Thus, our results show that periodicity is an important facet of fluctuating environments for life-history variation.

Reconciling empirical interactions and species coexistence.

Coexistence in ecological communities is governed largely by the nature and intensity of species interactions. Countless studies have proposed methods to infer these interactions from empirical data, yet models parameterised using such data often fail to recover observed coexistence patterns. Here, we propose a method to reconcile empirical parameterisations of community dynamics with species-abundance data, ensuring that the predicted equilibrium is consistent with the observed abundance distribution. To illustrate the approach, we explore two case studies: an experimental freshwater algal community and a long-term time series of displacement in an intertidal community. We demonstrate how our method helps recover observed coexistence patterns, capture the core dynamics of the system, and, in the latter case, predict the impacts of experimental extinctions. Collectively, these results demonstrate an intuitive approach for reconciling observed and empirical data, improving our ability to explore the links between species interactions and coexistence in natural systems.

Integrating the invisible fabric of nature into fisheries management.

Overfishing and environmental change have triggered many severe and unexpected consequences. As existing communities have collapsed, new ones have become established, fundamentally transforming ecosystems to those that are often less productive for fisheries, more prone to cycles of booms and busts, and thus less manageable. We contend that the failure of fisheries science and management to anticipate these transformations results from a lack of appreciation for the nature, strength, complexity, and outcome of species interactions. Ecologists have come to understand that networks of interacting species exhibit nonlinear dynamics and feedback loops that can produce sudden and unexpected shifts. We argue that fisheries science and management must follow this lead by developing a sharper focus on species interactions and how disrupting these interactions can push ecosystems in which fisheries are embedded past their tipping points.

Historical baselines and the future of shell calcification for a foundation species in a changing ocean.

Seawater pH and the availability of carbonate ions are decreasing due to anthropogenic carbon dioxide emissions, posing challenges for calcifying marine species. Marine mussels are of particular concern given their role as foundation species worldwide. Here, we document shell growth and calcification patterns in Mytilus californianus, the California mussel, over millennial and decadal scales. By comparing shell thickness across the largest modern shells, the largest mussels collected in the 1960s-1970s and shells from two Native American midden sites (∼1000-2420 years BP), we found that modern shells are thinner overall, thinner per age category and thinner per unit length. Thus, the largest individuals of this species are calcifying less now than in the past. Comparisons of shell thickness in smaller individuals over the past 10-40 years, however, do not show significant shell thinning. Given our sampling strategy, these results are unlikely to simply reflect within-site variability or preservation effects. Review of environmental and biotic drivers known to affect shell calcification suggests declining ocean pH as a likely explanation for the observed shell thinning. Further future decreases in shell thickness could have significant negative impacts on M. californianus survival and, in turn, negatively impact the species-rich complex that occupies mussel beds.

Intraspecific leaf chemistry drives locally accelerated ecosystem function in aquatic and terrestrial communities.

Resource patchiness influences consumer foraging, movement, and physiology. Fluxes across ecosystem boundaries can extend these effects to otherwise distinct food webs. Intraspecific diversity of these cross-ecosystem subsidies can have large consequences for recipient systems. Here, we show intraspecific variation in leaf defensive chemistry of riparian trees drives local adaptation among terrestrial and riverine decomposers that consume shed leaf litter. We found extensive geographic structuring of ellagitannins, diarylheptanoids, and flavonoids in red alder trees. Ellagitannins, particularly those with strong oxidative activity, drive aquatic leaf decomposition. Further, spatial variation in these leaf components drives local ecological matching: in experiments using artificial food sources distinguished only by the chemical content of individual trees, we found decomposers both on land and in rivers more quickly consumed locally derived food sources. These results illustrate that terrestrial processes can change the chemistry of cross-ecosystem subsidies in ways that ultimately alter ecosystem function in donor and recipient systems.

What Can Interaction Webs Tell Us About Species Roles?

The group model is a useful tool to understand broad-scale patterns of interaction in a network, but it has previously been limited in use to food webs, which contain only predator-prey interactions. Natural populations interact with each other in a variety of ways and, although most published ecological networks only include information about a single interaction type (e.g., feeding, pollination), ecologists are beginning to consider networks which combine multiple interaction types. Here we extend the group model to signed directed networks such as ecological interaction webs. As a specific application of this method, we examine the effects of including or excluding specific interaction types on our understanding of species roles in ecological networks. We consider all three currently available interaction webs, two of which are extended plant-mutualist networks with herbivores and parasitoids added, and one of which is an extended intertidal food web with interactions of all possible sign structures (+/+, -/0, etc.). Species in the extended food web grouped similarly with all interactions, only trophic links, and only nontrophic links. However, removing mutualism or herbivory had a much larger effect in the extended plant-pollinator webs. Species removal even affected groups that were not directly connected to those that were removed, as we found by excluding a small number of parasitoids. These results suggest that including additional species in the network provides far more information than additional interactions for this aspect of network structure. Our methods provide a useful framework for simplifying networks to their essential structure, allowing us to identify generalities in network structure and better understand the roles species play in their communities.

Cascading effects of induced terrestrial plant defences on aquatic and terrestrial ecosystem function.

Herbivores induce plants to undergo diverse processes that minimize costs to the plant, such as producing defences to deter herbivory or reallocating limited resources to inaccessible portions of the plant. Yet most plant tissue is consumed by decomposers, not herbivores, and these defensive processes aimed to deter herbivores may alter plant tissue even after detachment from the plant. All consumers value nutrients, but plants also require these nutrients for primary functions and defensive processes. We experimentally simulated herbivory with and without nutrient additions on red alder (Alnus rubra), which supplies the majority of leaf litter for many rivers in western North America. Simulated herbivory induced a defence response with cascading effects: terrestrial herbivores and aquatic decomposers fed less on leaves from stressed trees. This effect was context dependent: leaves from fertilized-only trees decomposed most rapidly while leaves from fertilized trees receiving the herbivory treatment decomposed least, suggesting plants funnelled a nutritionally valuable resource into enhanced defence. One component of the defence response was a decrease in leaf nitrogen leading to elevated carbon : nitrogen. Aquatic decomposers prefer leaves naturally low in C : N and this altered nutrient profile largely explains the lower rate of aquatic decomposition. Furthermore, terrestrial soil decomposers were unaffected by either treatment but did show a preference for local and nitrogen-rich leaves. Our study illustrates the ecological implications of terrestrial herbivory and these findings demonstrate that the effects of selection caused by terrestrial herbivory in one ecosystem can indirectly shape the structure of other ecosystems through ecological fluxes across boundaries.

Local adaptation of stream communities to intraspecific variation in a terrestrial ecosystem subsidy.

Cross-ecosystem fluxes can intertwine otherwise disparate food webs, but the effects of biodiversity at the genotypic level on fluxes across ecosystems boundaries is not known. Fresh leaves, which vary in traits such as defensive compounds against terrestrial herbivores, drop off trees and enter streams, providing a vital resource for riverine organisms. We demonstrate substantial variation in decomposition rates among individual trees in four different rivers in the Olympic Peninsula of Washington State, USA. We show that locally derived red alder leaf litter decomposes on average 24% faster than red alder leaf litter introduced from other riparian zones. Within rivers, leaves downstream of their parent trees decompose nearly as quickly as leaves from local trees. Leaves upstream of the parent tree decomposed as slowly as leaves from trees growing alongside different rivers. Over time, aquatic decomposer communities have locally adapted to the specific trees supplying the riparian subsidies. In energy-limited environments, such as small shaded streams, consumers must be efficient foragers. Our results indicate that this pressure for efficiency has led to adaptation at a particularly fine scale. More broadly, these results illustrate how genetic diversity and the effects of selection in one ecosystem can indirectly shape the structure of other ecosystems through ecological fluxes across boundaries.

Assessing predictions of population viability analysis: Peregrine Falcon populations in California.

Population viability analysis (PVA) has been an important tool for evaluating species extinction risk and alternative management strategies, but there is little information on how well PVA predicts population trajectories following changes in management actions. We tested previously published predictions from a stage-structured PVA of Peregrine Falcons (Falco peregrinus) in California, USA (Wootton and Bell 1992), against population trajectories following the 1992 termination of statewide, active management (population supplementation of captive-reared young). In the absence of extensive post-management monitoring, we developed surrogate estimates of breeding population size by calibrating several citizen science data sets (Christmas Bird Count, CBC; and North American Breeding Bird Survey, BBS) to intensive population surveys taken primarily during the active management period. CBC abundance data standardized by observer effort exhibited a strong relationship to intensive survey data (r2 = 0.971), indicated significantly reduced annual population growth rates after management was terminated (λ = 0.023 ± 0.013 SE) than when supplementation occurred (λ = 0.089 ± 0.023 SE), and demonstrated an increasing population as predicted by the PVA. The population trajectory fell within the 95% CI of stochastic simulations of the model either with or without density dependence and assuming either measurement error or process error, but models with process error were most strongly supported by the data. These results indicate that PVA can quantitatively anticipate population trajectories following changes in management, highlight the importance of post-management monitoring of species of concern, and illustrate the benefits of using management changes as large-scale experiments to more rigorously test PVA.

Experimental separation of genetic and demographic factors on extinction risk in wild populations.

When populations reach small size, an extinction risk vortex may arise from genetic (inbreeding depression, genetic drift) and ecological (demographic stochasticity, Allee effects, environmental fluctuation) processes. The relative contribution of these processes to extinction in wild populations is unknown, but important for conserving endangered species. In experimental field populations of a harvested kelp (Postelsia palmaeformis), in which we independently varied initial genetic diversity (completely inbred, control, outbred) and population size, ecological processes dominated the risk of extinction, whereas the contribution of genetic diversity was slight. Our results match theoretical predictions that demographic processes will generally doom small populations to extinction before genetic effects act strongly, prioritize detailed ecological analysis over descriptions of genetic structure in assessing conservation of at-risk species, and highlight the need for field experiments manipulating both demographics and genetic structure on long-term extinction risk.

The mixed mating system of the sea palm kelp Postelsia palmaeformis: few costs to selfing.

Naturally isolated populations have conflicting selection pressures for successful reproduction and inbreeding avoidance. These species with limited seasonal reproductive opportunities may use selfing as a means of reproductive assurance. We quantified the frequency of selfing and the fitness consequences for inbred versus outcrossed progeny of an annual kelp, the sea palm (Postelsia palmaeformis). Using experimentally established populations and microsatellite markers to assess the extent of selfing in progeny from six founding parents, we found the frequency of selfing was higher than expected in every population, and few fitness costs were detected in selfed offspring. Despite a decline in heterozygosity of 30 per cent in the first generation of selfing, self-fertilization did not affect individual size or reproduction, and correlated only with a marginally significant decline in survival. Our results suggest both that purging of deleterious recessive alleles may have already occurred and that selfing may be key to reproductive assurance in this species with limited dispersal. Postelsia has an alteration of a free-living diploid and haploid stage, where the haploid stage may provide increased efficiency for purging the genetic load. This life history is shared by many seaweeds and may thus be an important component of mating system evolution in the sea.

Predicting community responses to perturbations in the face of imperfect knowledge and network complexity.

How best to predict the effects of perturbations to ecological communities has been a long-standing goal for both applied and basic ecology. This quest has recently been revived by new empirical data, new analysis methods, and increased computing speed, with the promise that ecologically important insights may be obtainable from a limited knowledge of community interactions. We use empirically based and simulated networks of varying size and connectance to assess two limitations to predicting perturbation responses in multispecies communities: (1) the inaccuracy by which species interaction strengths are empirically quantified and (2) the indeterminacy of species responses due to indirect effects associated with network size and structure. We find that even modest levels of species richness and connectance (-25 pairwise interactions) impose high requirements for interaction strength estimates because system indeterminacy rapidly overwhelms predictive insights. Nevertheless, even poorly estimated interaction strengths provide greater average predictive certainty than an approach that uses only the sign of each interaction. Our simulations provide guidance in dealing with the trade-offs involved in maximizing the utility of network approaches for predicting dynamics in multispecies communities.

Field parameterization and experimental test of the neutral theory of biodiversity.

Ecologists would like to explain general patterns observed across multi-species communities, such as species-area and abundance-frequency relationships, in terms of the fundamental processes of birth, death and migration underlying the dynamics of all constituent species. The unified neutral theory of biodiversity and related theories based on these fundamental population processes have successfully recreated general species-abundance patterns without accounting for either the variation among species and individuals or resource-releasing processes such as predation and disturbance, long emphasized in ecological theory. If ecological communities can be described adequately without estimating variation in species and their interactions, our understanding of ecological community organization and the predicted consequences of reduced biodiversity and environmental change would shift markedly. Here, I introduce a strong method to test the neutral theory that combines field parameterization of the underlying population dynamics with a field experiment, and apply it to a rocky intertidal community. Although the observed abundance-frequency distribution of the system follows that predicted by the neutral theory, the neutral theory predicts poorly the field experimental results, indicating an essential role for variation in species interactions.

Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset.

Increasing global concentrations of atmospheric CO(2) are predicted to decrease ocean pH, with potentially severe impacts on marine food webs, but empirical data documenting ocean pH over time are limited. In a high-resolution dataset spanning 8 years, pH at a north-temperate coastal site declined with increasing atmospheric CO(2) levels and varied substantially in response to biological processes and physical conditions that fluctuate over multiple time scales. Applying a method to link environmental change to species dynamics via multispecies Markov chain models reveals strong links between in situ benthic species dynamics and variation in ocean pH, with calcareous species generally performing more poorly than noncalcareous species in years with low pH. The models project the long-term consequences of these dynamic changes, which predict substantial shifts in the species dominating the habitat as a consequence of both direct effects of reduced calcification and indirect effects arising from the web of species interactions. Our results indicate that pH decline is proceeding at a more rapid rate than previously predicted in some areas, and that this decline has ecological consequences for near shore benthic ecosystems.

Treatment-based Markov chain models clarify mechanisms of invasion in an invaded grassland community.

What are the relative roles of mechanisms underlying plant responses in grassland communities invaded by both plants and mammals? What type of community can we expect in the future given current or novel conditions? We address these questions by comparing Markov chain community models among treatments from a field experiment on invasive species on Robinson Crusoe Island, Chile. Because of seed dispersal, grazing and disturbance, we predicted that the exotic European rabbit (Oryctolagus cuniculus) facilitates epizoochorous exotic plants (plants with seeds that stick to the skin an animal) at the expense of native plants. To test our hypothesis, we crossed rabbit exclosure treatments with disturbance treatments, and sampled the plant community in permanent plots over 3 years. We then estimated Markov chain model transition probabilities and found significant differences among treatments. As hypothesized, this modelling revealed that exotic plants survive better in disturbed areas, while natives prefer no rabbits or disturbance. Surprisingly, rabbits negatively affect epizoochorous plants. Markov chain dynamics indicate that an overall replacement of native plants by exotic plants is underway. Using a treatment-based approach to multi-species Markov chain models allowed us to examine the changes in the importance of mechanisms in response to experimental impacts on communities.

Experimental species removal alters ecological dynamics in a natural ecosystem.

Theory predicts that species extinction or invasion can affect the temporal dynamics of ecological communities by altering feedback patterns and by damping or amplifying environmental variation via changes in the network of species interactions, but because of the logistical challenges of investigating temporal dynamics, evidence from natural ecosystems is lacking. In a long-term experimental manipulation of a rocky intertidal community on Tatoosh Island, Washington, U.S.A., chronic removal of the dominant species Mytilus californianus altered the dynamics of the system, causing reductions in the temporal variability of three subdominant species but no consistent change in the spectral characteristics or the order of density dependence across experimental replicates. This pattern of results suggests that Mytilus californianus impacted the temporal dynamics by amplifying environmental stochasticity, rather than by changing feedback pathways as is emphasized in most theoretical predictions and laboratory studies. Hence, further investigation of the mechanisms and implications of transmission of environmental stochasticity in natural ecosystems is merited.

The Origin, Succession, and Predicted Metabolism of Bacterial Communities Associated with Leaf Decomposition.

Intraspecific variation in plant nutrient and defensive traits can regulate ecosystem-level processes, such as decomposition and transformation of plant carbon and nutrients. Understanding the regulatory mechanisms of ecosystem functions at local scales may facilitate predictions of the resistance and resilience of these functions to change. We evaluated how riverine bacterial community assembly and predicted gene content corresponded to decomposition rates of green leaf inputs from red alder trees into rivers of Washington State, USA. Previously, we documented accelerated decomposition rates for leaves originating from trees growing adjacent to the site of decomposition versus more distant locales, suggesting that microbes have a "home-field advantage" in decomposing local leaves. Here, we identified repeatable stages of bacterial succession, each defined by dominant taxa with predicted gene content associated with metabolic pathways relevant to the leaf characteristics and course of decomposition. "Home" leaves contained bacterial communities with distinct functional capacities to degrade aromatic compounds. Given known spatial variation of alder aromatics, this finding helps explain locally accelerated decomposition. Bacterial decomposer communities adjust to intraspecific variation in leaves at spatial scales of less than a kilometer, providing a mechanism for rapid response to changes in resources such as range shifts among plant genotypes. Such rapid responses among bacterial communities in turn may maintain high rates of carbon and nutrient cycling through aquatic ecosystems.IMPORTANCE Community ecologists have traditionally treated individuals within a species as uniform, with individual-level biodiversity rarely considered as a regulator of community and ecosystem function. In our study system, we have documented clear evidence of within-species variation causing local ecosystem adaptation to fluxes across ecosystem boundaries. In this striking pattern of a "home-field advantage," leaves from individual trees tend to decompose most rapidly when immediately adjacent to their parent tree. Here, we merge community ecology experiments with microbiome approaches to describe how bacterial communities adjust to within-species variation in leaves over spatial scales of less than a kilometer. The results show that bacterial community compositional changes facilitate rapid ecosystem responses to environmental change, effectively maintaining high rates of carbon and nutrient cycling through ecosystems.

Estimating nonlinear interaction strengths: an observation-based method for species-rich food webs.

Efforts to estimate the strength of species interactions in species-rich, reticulate food webs have been hampered by the multitude of direct and indirect interactions such systems exhibit and have been limited by an assumption that pairwise interactions display linear functional forms. Here we present a new method for directly measuring, on a per capita basis, the nonlinear strength of trophic species interactions within such food webs. This is an observation-based method, requiring three pieces of information: (1) species abundances, (2) predator and prey-specific handling times, and (3) data from predator-specific feeding surveys in which the number of individuals observed feeding on each of the predator's prey species has been tallied. The method offers a straightforward way to assess the completeness of one's sampling effort in accurately estimating interaction strengths through the construction of predator-specific prey accumulation curves. The method should be applicable to a variety of systems in which empirical estimates of direct interaction strengths have thus far remained elusive.

Understanding and predicting ecological dynamics: are major surprises inevitable?

Ecological surprises, substantial and unanticipated changes in the abundance of one or more species that result from previously unsuspected processes, are a common outcome of both experiments and observations in community and population ecology. Here, we give examples of such surprises along with the results of a survey of well-established field ecologists, most of whom have encountered one or more surprises over the course of their careers. Truly surprising results are common enough to require their consideration in any reasonable effort to characterize nature and manage natural resources. We classify surprises as dynamic-, pattern-, or intervention-based, and we speculate on the common processes that cause ecological systems to so often surprise us. A long-standing and still growing concern in the ecological literature is how best to make predictions of future population and community dynamics. Although most work on this subject involves statistical aspects of data analysis and modeling, the frequency and nature of ecological surprises imply that uncertainty cannot be easily tamed through improved analytical procedures, and that prudent management of both exploited and conserved communities will require precautionary and adaptive management approaches.