Extensive behavioral data contained within existing ecological datasets.

Long-term ecological datasets contain vast behavioral data, enabling the quantification of among-individual behavioral variation at unprecedented spatiotemporal scales. We detail how behaviors can be extracted and describe how such data can be used to test new hypotheses, inform population and community ecology, and address pressing conservation needs.

Long-term, large-scale experiment reveals the effects of seed limitation, climate, and anthropogenic disturbance on restoration of plant communities in a biodiversity hotspot.

Ecological restoration is essential for maintaining biodiversity in the face of dynamic, global changes in climate, human land use, and disturbance regimes. Effective restoration requires understanding bottlenecks in plant community recovery that exist today, while recognizing that these bottlenecks may relate to complex histories of environmental change. Such understanding has been a challenge because few long-term, well-replicated experiments exist to decipher the demographic processes influencing recovery for numerous species against the backdrop of multiyear variation in climate and management. We address this challenge through a long-term and geographically expansive experiment in longleaf pine savannas, an imperiled ecosystem and biodiversity hotspot in the southeastern United States. Using 48 sites at three locations spanning 480 km, the 8-y experiment manipulated initial seed arrival for 24 herbaceous plant species and presence of competitors to evaluate the impacts of climate variability and management actions (e.g., prescribed burning) on plant establishment and persistence. Adding seeds increased plant establishment of many species. Cool and wet climatic conditions, low tree density, and reduced litter depth also promoted establishment. Once established, most species persisted for the duration of the 8-y experiment. Plant traits were most predictive when tightly coupled to the process of establishment. Our results illustrate how seed additions can restore plant diversity and how interannual climatic variation affects the dynamics of plant communities across a large region. The significant effects of temperature and precipitation inform how future climate may affect restoration and conservation via large-scale changes in the fundamental processes of establishment and persistence.

Daily activity timing in the Anthropocene.

Animals are facing novel 'timescapes' in which the stimuli entraining their daily activity patterns no longer match historical conditions due to anthropogenic disturbance. However, the ecological effects (e.g., altered physiology, species interactions) of novel activity timing are virtually unknown. We reviewed 1328 studies and found relatively few focusing on anthropogenic effects on activity timing. We suggest three hypotheses to stimulate future research: (i) activity-timing mismatches determine ecological effects, (ii) duration and timing of timescape modification influence effects, and (iii) consequences of altered activity timing vary biogeographically due to broad-scale variation in factors compressing timescapes. The continued growth of sampling technologies promises to facilitate the study of the consequences of altered activity timing, with emerging applications for biodiversity conservation.

Plant induced defenses that promote cannibalism reduce herbivory as effectively as highly pathogenic herbivore pathogens.

Plant induced defenses may benefit plants by increasing cannibalism among insect herbivores. However, the general efficacy of plant defenses that promote cannibalism remains unclear. Using a generalist Lepidopteran herbivore (Helicoverpa zea), we examined whether plant induced defenses in Solanum lycopersicum increased cannibalism among H. zea and whether defense-mediated cannibalism benefits both the plant and the cannibal. In a separate experiment, we also examined whether defense-mediated cannibalism has effects on H. zea herbivory that are comparable to the effects of pathogenic virus of H. zea (HzSNPV) and whether defense-mediated cannibalism modified pathogen efficacy. We found that both plant defenses and cannibalism decreased herbivory: H. zea consumed less plant material if plants were induced, if dead conspecifics were provided, or both. Cannibalism increased cannibal growth rate: cannibals effectively overcome the costs of plant defenses by eating conspecifics. Inoculating half of H. zea with virus strongly reduced caterpillar survival. Cannibalism occurred sooner among virus-inoculated groups of H. zea, and all caterpillars in virus-inoculated treatments died before the end of the 7-day experiment. Although the rise in mortality caused by HzSNPV occurred more rapidly than the rise in mortality due to defense-mediated cannibalism, overall H. zea mortality at the end of the experiment was equal among virus-inoculated and induced-defense groups. Defense-mediated cannibalism and viral inoculation equally reduced herbivory on S. lycopersicum. Our results provide evidence that defense-mediated increases in cannibalism can be as effective as other forms of classic herbivore population regulation, and that both viral pathogens and defense-induced cannibalism can have significant benefits for plants.

The important role of animal social status in vertebrate seed dispersal.

Seed dispersal directly affects plant establishment, gene flow and fitness. Understanding patterns in seed dispersal is, therefore, fundamental to understanding plant ecology and evolution, as well as addressing challenges of extinction and global change. Our ability to understand dispersal is limited because seeds may be dispersed by multiple agents, and the effectiveness of these agents can be highly variable both among and within species. We provide a novel framework that links seed dispersal to animal social status, a key component of behaviour. Because social status affects individual resource access and movement, it provides a critical link to two factors that determine seed dispersal: the quantity of seeds dispersed and the spatial patterns of dispersal. Social status may have unappreciated effects on post-dispersal seed survival and recruitment when social status affects individual habitat use. Hence, environmental changes, such as selective harvesting and urbanisation, that affect animal social structure may have unappreciated consequences for seed dispersal. This framework highlights these exciting new hypotheses linking environmental change, social structure and seed dispersal. By outlining experimental approaches to test these hypotheses, we hope to facilitate studies across a wide diversity of plant-animal networks, which may uncover emerging hotspots or significant declines in seed dispersal.

Exome sequencing of deer mice on two California Channel Islands identifies potential adaptation to strongly contrasting ecological conditions.

Understanding the forces that drive genotypic and phenotypic change in wild populations is a central goal of evolutionary biology. We examined exome variation in populations of deer mice from two of the California Channel Islands: Peromyscus maniculatus elusus from Santa Barbara Island and P. m. santacruzae from Santa Cruz Island exhibit significant differences in olfactory predator recognition, activity timing, aggressive behavior, morphology, prevalence of Sin Nombre virus, and population densities. We characterized variation in protein-coding regions using exome capture and sequencing of 25 mice from Santa Barbara Island and 22 mice from Santa Cruz Island. We identified and examined 386,256 SNPs using three complementary methods (BayeScan, pcadapt, and LFMM). We found strong differences in molecular variation between the two populations and 710 outlier SNPs in protein-coding genes that were detected by all three methods. We identified 35 candidate genes from this outlier set that were related to differences in phenotypes between island populations. Enrichment analyses demonstrated that patterns of molecular variation were associated with biological processes related to response to chemical stimuli and regulation of immune processes. Candidate genes associated with olfaction (Gfy, Tlr2, Vmn13r2, numerous olfactory receptor genes), circadian activity (Cry1), anxiety (Brca1), immunity (Cd28, Eif2ak4, Il12a, Syne1), aggression (Cyp19a, Lama2), and body size (Bc16, Syne1) exhibited non-synonymous mutations predicted to have moderate to large effects. Variation in olfaction-related genes, including a stop codon in the Santa Barbara Island population, suggests loss of predator-recognition traits at the molecular level, consistent with a lack of behavioral aversion to fox feces. These findings also suggest that divergent pathogen prevalence and population density may have influenced adaptive immunity and behavioral phenotypes, such as reduced aggression. Overall, our study indicates that ecological differences between islands are associated with signatures of selection in protein-coding genes underlying phenotypes that promote success in those environments.

Sin Nombre virus prevalence from 2014-2017 in wild deer mice, Peromyscus maniculatus, on five of the California Channel Islands.

Sin Nombre virus (SNV) is a zoonotic virus that is highly pathogenic to humans. The deer mouse, Peromyscus maniculatus, is the primary host of SNV, and SNV prevalence in P. maniculatus is an important indicator of human disease risk. Because the California Channel Islands contain permanent human settlements, receive hundreds of thousands of visitors each year, and can have extremely high densities of P. maniculatus, surveillance for SNV in island P. maniculatus is important for understanding the human risk of zoonotic disease. Despite the importance of surveillance on these heavily utilized islands, SNV prevalence (i.e. the proportion of P. maniculatus that test positive to antibodies to SNV) has not been examined in the last 13-27 years. We present data on 1,610 mice sampled for four consecutive years (2014-2017) on five of the California Channel Islands: East Anacapa, Santa Barbara, Santa Catalina, San Nicolas, and San Clemente. Despite historical data indicating SNV-positive mice on San Clemente and Santa Catalina, we detected no SNV-positive mice on these islands, suggesting very low prevalence or possible loss of SNV. Islands historically free of SNV (East Anacapa, Santa Barbara, and San Nicolas) remained free of SNV, suggesting that rates of pathogen introduction from other islands and/or the mainland are low. Although continued surveillance is warranted to determine whether SNV establishes on these islands, our work helps inform current human disease risk in these locations and suggests that SNV prevalence on these islands is currently very low.

Large ecosystem-scale effects of restoration fail to mitigate impacts of land-use legacies in longleaf pine savannas.

Ecological restoration is a global priority, with potential to reverse biodiversity declines and promote ecosystem functioning. Yet, successful restoration is challenged by lingering legacies of past land-use activities, which are pervasive on lands available for restoration. Although legacies can persist for centuries following cessation of human land uses such as agriculture, we currently lack understanding of how land-use legacies affect entire ecosystems, how they influence restoration outcomes, or whether restoration can mitigate legacy effects. Using a large-scale experiment, we evaluated how restoration by tree thinning and land-use legacies from prior cultivation and subsequent conversion to pine plantations affect fire-suppressed longleaf pine savannas. We evaluated 45 ecological properties across four categories: 1) abiotic attributes, 2) organism abundances, 3) species diversity, and 4) species interactions. The effects of restoration and land-use legacies were pervasive, shaping all categories of properties, with restoration effects roughly twice the magnitude of legacy effects. Restoration effects were of comparable magnitude in savannas with and without a history of intensive human land use; however, restoration did not mitigate numerous legacy effects present prior to restoration. As a result, savannas with a history of intensive human land use supported altered properties, especially related to soils, even after restoration. The signature of past human land-use activities can be remarkably persistent in the face of intensive restoration, influencing the outcome of restoration across diverse ecological properties. Understanding and mitigating land-use legacies will maximize the potential to restore degraded ecosystems.

Large-scale patterns of seed removal by small mammals differ between areas of low- versus high-wolf occupancy.

Because most tree species recruit from seeds, seed predation by small-mammal granivores may be important for determining plant distribution and regeneration in forests. Despite the importance of seed predation, large-scale patterns of small-mammal granivory are often highly variable and thus difficult to predict. We hypothesize distributions of apex predators can create large-scale variation in the distribution and abundance of mesopredators that consume small mammals, creating predictable areas of high and low granivory. For example, because gray wolf (Canis lupus) territories are characterized by relatively less use by coyotes (C. latrans) and greater use by foxes (Vulpes vulpes, Urocyon cinereoargentus) that consume a greater proportion of small mammals, wolf territories may be areas of reduced small-mammal granivory. Using large-scale, multiyear field trials at 22 sites with high- and low-wolf occupancy in northern Wisconsin, we evaluated whether removal of seeds of four tree species was lower in wolf territories. Consistent with the hypothesized consequences of wolf occupancy, seed removal of three species was more than 25% lower in high-wolf-occupancy areas across 2 years and small-mammal abundance was more than 40% lower in high-wolf areas during one of two study years. These significant results, in conjunction with evidence of seed consumption in situ and the absence of significant habitat differences between high- and low-wolf areas, suggest that top-down effects of wolves on small-mammal granivory and seed survival may occur. Understanding how interactions among carnivores create spatial patterns in interactions among lower trophic levels may allow for more accurate predictions of large-scale patterns in seed survival and forest composition.

Proportional fitness loss and the timing of defensive investment: a cohesive framework across animals and plants.

The risk of consumption is a pervasive aspect of ecology and recent work has focused on synthesis of consumer-resource interactions (e.g., enemy-victim ecology). Despite this, theories pertaining to the timing and magnitude of defenses in animals and plants have largely developed independently. However, both animals and plants share the common dilemma of uncertainty of attack, can gather information from the environment to predict future attacks and alter their defensive investment accordingly. Here, we present a novel, unifying framework based on the way an organism's ability to defend itself during an attack can shape their pre-attack investment in defense. This framework provides a useful perspective on the nature of information use and variation in defensive investment across the sequence of attack-related events, both within and among species. It predicts that organisms with greater proportional fitness loss if attacked will gather and respond to risk information earlier in the attack sequence, while those that have lower proportional fitness loss may wait until attack is underway. This framework offers a common platform to compare and discuss consumer effects and provides novel insights into the way risk information can propagate through populations, communities, and ecosystems.

Why do entomologists and plant pathologists approach trophic relationships so differently? Identifying biological distinctions to foster synthesis.

Plant interactions with herbivores and pathogens are among the most widespread ecological relationships, and show many congruent properties. Despite these similarities, general models describing how plant defenses function in ecosystems, and the prioritization of responses to emerging challenges such as climate change, invasive species and habitat alteration, often differ markedly between entomologists and plant pathologists. We posit that some fundamental distinctions between how insects and pathogens interact with plants underlie these differences. We propose a conceptual framework to help incorporate these distinctions into robust models and research priorities. The most salient distinctions include features of host-searching behavior, evasion of plant defenses, plant tolerance to utilization, and sources of insect and microbial population regulation. Collectively, these features lead to relatively more diffuse and environmentally mediated plant-insect interactions, and more intimate and genetically driven plant-pathogen interactions. Specific features of insect vs pathogen life histories can also yield different patterns of spatiotemporal dynamics. These differences can become increasingly pronounced when scaling from controlled laboratory to open ecological systems. Integrating these differences alongside similarities can foster improved models and research approaches to plant defense, trophic interactions, coevolutionary dynamics, food security and resource management, and provide guidance as traditional departments increase collaborations, or merge into larger units.

Transgenerational Plasticity in Human-Altered Environments.

Our ability to predict how species will respond to human-induced rapid environmental change (HIREC) may depend upon our understanding of transgenerational plasticity (TGP), which occurs when environments experienced by previous generations influence phenotypes of subsequent generations. TGP evolved to help organisms cope with environmental stressors when parental environments are highly predictive of offspring environments. HIREC can alter conditions that favored TGP in historical environments by reducing parents' ability to detect environmental conditions, disrupting previous correlations between parental and offspring environments, and interfering with the transmission of parental cues to offspring. Because of the propensity to produce errors in these processes, TGP will likely generate negative fitness outcomes in response to HIREC, though beneficial fitness outcomes may occur in some cases.

Ongoing accumulation of plant diversity through habitat connectivity in an 18-year experiment.

Deleterious effects of habitat fragmentation and benefits of connecting fragments could be significantly underestimated because changes in colonization and extinction rates that drive changes in biodiversity can take decades to accrue. In a large and well-replicated habitat fragmentation experiment, we find that annual colonization rates for 239 plant species in connected fragments are 5% higher and annual extinction rates 2% lower than in unconnected fragments. This has resulted in a steady, nonasymptotic increase in diversity, with nearly 14% more species in connected fragments after almost two decades. Our results show that the full biodiversity value of connectivity is much greater than previously estimated, cannot be effectively evaluated at short time scales, and can be maximized by connecting habitat sooner rather than later.

Predator-Prey Interactions in the Anthropocene: Reconciling Multiple Aspects of Novelty.

Ecological novelty, when conditions deviate from a historical baseline, is increasingly common as humans modify habitats and communities across the globe. Our ability to anticipate how novelty changes predator-prey interactions will likely hinge upon the explicit evaluation of multiple forms of novelty, rather than a focus on single forms of novelty (e.g., invasive predators or climate change). We provide a framework to assess how multiple forms of novelty can act, alone or in concert, on components shared by all predator-prey interactions (the predation sequence). Considering how novelty acts throughout the predation sequence could improve our understanding of predator-prey interactions in an increasingly novel world, identify important knowledge gaps, and guide conservation decisions in the Anthropocene.

Agricultural land-use history does not reduce woodland understory herb establishment.

Agricultural land use is a leading cause of habitat degradation, leaving a legacy of ecological impacts long after agriculture has ceased. Yet the mechanisms for legacy effects, such as altered plant community composition, are not well understood. In particular, whether plant community recovery is limited by an inability of populations to establish within post-agricultural areas, owing to altered environmental conditions within these areas, remains poorly known. We evaluated this hypothesis of post-agricultural establishment limitation through a field experiment within longleaf pine woodlands in South Carolina (USA) and a greenhouse experiment using field-collected soils from these sites. In the field, we sowed seeds of 12 understory plant species associated with remnants (no known history of agriculture) into 27 paired remnant and post-agricultural woodlands. We found that post-agricultural woodlands supported higher establishment, resulting in greater species richness of sown species. These results were context dependent, however, with higher establishment in post-agricultural woodlands only when sites were frequently burned, had less leaf litter, or had less sandy soils. In the greenhouse, we found that agricultural history had no impact on plant growth or survival, suggesting that establishment limitation is unlikely driven by differences in soils associated with agricultural history when environmental conditions are not stressful. Rather, the potential for establishment in post-agricultural habitats can be higher than in remnant habitats, with the strength of this effect determined by fire frequency and soil characteristics.

Extreme cold consistently reduces seedling growth but has species-specific effects on browse tolerance in summer.

PREMISE OF THE STUDY: Extreme weather events can injure plants, causing decreased survival. However, we may underestimate the ecological importance of extreme events if they have strong sublethal effects that manifest after several months. We tested the hypothesis that late-winter extreme-cold events decrease the ability of woody plants to grow and tolerate stem removal in summer. METHODS: Seedlings from four temperate tree species (Abies balsamea, Pinus resinosa, P. strobus, Quercus rubra) were acclimated to winter conditions in growth chambers, and experienced 1 week of warm temperatures before being exposed to one of three 24-h extreme-cold events (minimum temperature: 8°C control, -8°C, or -16°C). Seedlings were then transferred to a greenhouse where we monitored survival and growth. Three months after the extreme-cold event, we mimicked an herbivore attack by removing either 25% or 75% of new stem growth from seedlings of two species (P. resinosa, Q. rubra). KEY RESULTS: While extreme cold had no immediate effect on seedling survival, the coldest temperature treatment reduced stem growth 51% relative to controls. Stem removal decreased P. resinosa survival in the -16°C treatment, but stem removal treatment had no effect on P. resinosa survival in the intermediate -8°C treatment or 8°C control. Stem removal did not alter Q. rubra survival. CONCLUSIONS: Ephemeral late-winter cold temperatures can have unappreciated effects on growing-season seedling dynamics, including growth and herbivory. For predicting how extreme-cold events might alter large-scale patterns of tree distribution, seedlings should be monitored throughout the growing season following extreme late-winter frosts.

Error management theory and the adaptive significance of transgenerational maternal-stress effects on offspring phenotype.

It is well established that circulating maternal stress hormones (glucocorticoids, GCs) can alter offspring phenotype. There is also a growing body of empirical work, within ecology and evolution, indicating that maternal GCs link the environment experienced by the mother during gestation with changes in offspring phenotype. These changes are considered to be adaptive if the maternal environment matches the offspring's environment and maladaptive if it does not. While these ideas are conceptually sound, we lack a testable framework that can be used to investigate the fitness costs and benefits of altered offspring phenotypes across relevant future environments. We present error management theory as the foundation for a framework that can be used to assess the adaptive potential of maternal stress hormones on offspring phenotype across relevant postnatal scenarios. To encourage rigorous testing of our framework, we provide field-testable hypotheses regarding the potential adaptive role of maternal stress across a diverse array of taxa and life histories, as well as suggestions regarding how our framework might provide insight into past, present, and future research. This perspective provides an informed lens through which to design and interpret experiments on the effects of maternal stress, provides a framework for predicting and testing variation in maternal stress across and within taxa, and also highlights how rapid environmental change that induces maternal stress may lead to evolutionary traps.

A judgment and decision-making model for plant behavior.

Recently plant biologists have documented that plants, like animals, engage in many activities that can be considered as behaviors, although plant biologists currently lack a conceptual framework to understand these processes. Borrowing the well-established framework developed by psychologists, we propose that plant behaviors can be constructively modeled by identifying four distinct components: (1) a cue or stimulus that provides information, (2) a judgment whereby the plant perceives and processes this informative cue, (3) a decision whereby the plant chooses among several options based on their relative costs and benefits, and (4) action. Judgment for plants can be determined empirically by monitoring signaling associated with electrical, calcium, or hormonal fluxes. Decision-making can be evaluated empirically by monitoring gene expression or differential allocation of resources. We provide examples of the utility of this judgment and decision-making framework by considering cases in which plants either successfully or unsuccessfully induced resistance against attacking herbivores. Separating judgment from decision-making suggests new analytical paradigms (i.e., Bayesian methods for judgment and economic utility models for decision-making). Following this framework, we propose an experimental approach to plant behavior that explicitly manipulates the stimuli provided to plants, uses plants that vary in sensory abilities, and examines how environmental context affects plant responses. The concepts and approaches that follow from the judgment and decision-making framework can shape how we study and understand plant-herbivore interactions, biological invasions, plant responses to climate change, and the susceptibility of plants to evolutionary traps.