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.

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.

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.

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.

Integrative modelling reveals mechanisms linking productivity and plant species richness.

How ecosystem productivity and species richness are interrelated is one of the most debated subjects in the history of ecology. Decades of intensive study have yet to discern the actual mechanisms behind observed global patterns. Here, by integrating the predictions from multiple theories into a single model and using data from 1,126 grassland plots spanning five continents, we detect the clear signals of numerous underlying mechanisms linking productivity and richness. We find that an integrative model has substantially higher explanatory power than traditional bivariate analyses. In addition, the specific results unveil several surprising findings that conflict with classical models. These include the isolation of a strong and consistent enhancement of productivity by richness, an effect in striking contrast with superficial data patterns. Also revealed is a consistent importance of competition across the full range of productivity values, in direct conflict with some (but not all) proposed models. The promotion of local richness by macroecological gradients in climatic favourability, generally seen as a competing hypothesis, is also found to be important in our analysis. The results demonstrate that an integrative modelling approach leads to a major advance in our ability to discern the underlying processes operating in ecological systems.

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.

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.

Herbivores and nutrients control grassland plant diversity via light limitation.

Human alterations to nutrient cycles and herbivore communities are affecting global biodiversity dramatically. Ecological theory predicts these changes should be strongly counteractive: nutrient addition drives plant species loss through intensified competition for light, whereas herbivores prevent competitive exclusion by increasing ground-level light, particularly in productive systems. Here we use experimental data spanning a globally relevant range of conditions to test the hypothesis that herbaceous plant species losses caused by eutrophication may be offset by increased light availability due to herbivory. This experiment, replicated in 40 grasslands on 6 continents, demonstrates that nutrients and herbivores can serve as counteracting forces to control local plant diversity through light limitation, independent of site productivity, soil nitrogen, herbivore type and climate. Nutrient addition consistently reduced local diversity through light limitation, and herbivory rescued diversity at sites where it alleviated light limitation. Thus, species loss from anthropogenic eutrophication can be ameliorated in grasslands where herbivory increases ground-level light.

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.

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.

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.

Plants eavesdrop on cues produced by snails and induce costly defenses that affect insect herbivores.

Although induced defenses are widespread in plants, the degree to which plants respond to herbivore kairomones (incidental chemicals that herbivores produce independent of herbivory), the costs and benefits of responding to cues of herbivory risk, and the ecological consequences of induced defenses remain unclear. We demonstrate that undamaged tomatoes, Solanum lycopersicum, induce defenses in response to a kairomone (locomotion mucus) of snail herbivores (Helix aspersa). Induced defense had significant costs and benefits for plants: plants exposed to snail mucus or a standard defense elicitor (methyl jasmonate, MeJA) exhibited slower growth, but also experienced less herbivory by an insect herbivore (Spodoptera exigua). We also find that kairomones from molluscan herbivores lead to deleterious effects on insect herbivores mediated through changes in plant defense, i.e., mucus-induced defenses of Solanum lycopersicum-reduced growth of S. exigua. These results suggest that incidental cues of widespread generalist herbivores might be a mechanism creating variation in plant growth, plant defense, and biotic interactions.

Invasive exotic shrub modifies a classic animal-habitat relationship and alters patterns of vertebrate seed predation.

Recent evidence suggests that invasive exotic plants can provide novel habitats that alter animal behavior. However, it remains unclear whether classic animal-habitat associations that influence the spatial distribution of plant-animal interactions, such as small mammal use of downed woody debris, persist in invaded habitats. We removed an invasive exotic shrub (buckthorn, Rhamnus cathartica) from 7 of 15 plots in Wisconsin. In each plot, we deployed 200 tagged Quercus rubra seeds in November 2014. After five months, tags were recovered to track spatial patterns of small mammal seed predation. Most recovered tags were associated with consumed seeds (95%); live-trapping, ancillary camera-trapping, and previous behavioral studies suggest that white-footed mice (Peromyscus leucopus) were responsible for most seed predation. In habitats without R. cathartica, most seed predation occurred near woody debris. In habitats with R. cathartica, small mammals rarely consumed seeds near woody debris, and seed predation occurred farther from the plot center and was less spatially clustered. Our results illustrate that invasive exotic shrubs can disrupt an otherwise common animal-habitat relationship. Failing to account for changes in habitat use may diminish our ability to predict animal distributions and outcomes of species interactions in novel habitats created by invasive exotic plants.

How fragmentation and corridors affect wind dynamics and seed dispersal in open habitats.

Determining how widespread human-induced changes such as habitat loss, landscape fragmentation, and climate instability affect populations, communities, and ecosystems is one of the most pressing environmental challenges. Critical to this challenge is understanding how these changes are affecting the movement abilities and dispersal trajectories of organisms and what role conservation planning can play in promoting movement among remaining fragments of suitable habitat. Whereas evidence is mounting for how conservation strategies such as corridors impact animal movement, virtually nothing is known for species dispersed by wind, which are often mistakenly assumed to not be limited by dispersal. Here, we combine mechanistic dispersal models, wind measurements, and seed releases in a large-scale experimental landscape to show that habitat corridors affect wind dynamics and seed dispersal by redirecting and bellowing airflow and by increasing the likelihood of seed uplift. Wind direction interacts with landscape orientation to determine when corridors provide connectivity. Our results predict positive impacts of connectivity and patch shape on species richness of wind-dispersed plants, which we empirically illustrate using 12 y of data from our experimental landscapes. We conclude that habitat fragmentation and corridors strongly impact the movement of wind-dispersed species, which has community-level consequences.

Neighbor palatability generates associational effects by altering herbivore foraging behavior.

Despite increasing evidence that herbivory on a focal plant may hinge upon the identity of its neighbors, it is not clear whether predictable mechanisms govern the nature and magnitude of such associational effects. Using a factorial field experiment replicated at 14 sites across 80,000 hectares, we evaluated the mechanisms driving associational effects between two plant species mediated by grasshopper herbivores. Our experiment manipulated local neighborhood plant density (two levels) and frequency (three levels), nested within two larger-scale habitat contexts (habitats that did or did not have past agricultural land use). We found that the more palatable plant species, Solidago nemoralis, experienced reduced herbivory (associational resistance) when rare due mainly to reduced grasshopper foraging activity. Damage to the less palatable plant species, S. odora, was affected by the interaction between plant frequency and the land-use history of the site: it experienced increased damage (associational susceptibility) in even-frequency neighborhoods, but only in sites with a history of agricultural use. Behavioral assays generally corroborated the results from the field, further supporting the importance of foraging behavior in generating associational effects. In finding that associational effects are contingent upon relative palatability among plants and events in the distant past that modify contemporary habitat structure (i.e., past agricultural land use), our work suggests that foraging decisions made at the neighborhood level are important for generating associational effects and that in some cases these neighborhood interactions also depend on the larger-scale environmental context resulting from legacies of past land-use events.

Connectivity from a different perspective: comparing seed dispersal kernels in connected vs. unfragmented landscapes.

Habitat fragmentation can create significant impediments to dispersal. A technique to increase dispersal between otherwise isolated fragments is the use of corridors. Although previous studies have compared dispersal between connected fragments to dispersal between unconnected fragments, it remains unknown how dispersal between fragments connected by a corridor compares to dispersal in unfragmented landscapes. To assess the extent to which corridors can restore dispersal in fragmented landscapes to levels observed in unfragmented landscapes, we employed a stable-isotope marking technique to track seeds within four unfragmented landscapes and eight experimental landscapes with fragments connected by corridors. We studied two wind- and two bird-dispersed plant species, because previous community-based research showed that dispersal mode explains how connectivity effects vary among species. We constructed dispersal kernels for these species in unfragmented landscapes and connected fragments by marking seeds in the center of each landscape with 'IN and then recovering marked seeds in seed traps at distances up to 200 m. For the two wind-dispersed plants, seed dispersal kernels were similar in unfragmented landscapes and connected fragments. In contrast, dispersal kernels of bird-dispersed seeds were both affected by fragmentation and differed in the direction of the impact: Morella cerifera experienced more and Rhus copallina experienced less long-distance dispersal in unfragmented than in connected landscapes. These results show that corridors can facilitate dispersal probabilities comparable to those observed in unfragmented landscapes. Although dispersal mode may provide useful broad predictions, we acknowledge that similar species may respond uniquely due to factors such as seasonality and disperser behavior. Our results further indicate that prior work has likely underestimated dispersal distances of wind-dispersed plants and that factors altering long-distance dispersal may have a greater impact on the spread of species than previously thought.

Past agricultural land use and present-day fire regimes can interact to determine the nature of seed predation.

Historical agriculture and present-day fire regimes can have significant effects on contemporary ecosystems. Although past agricultural land use can lead to long-term changes in plant communities, it remains unclear whether these persistent land-use legacies alter plant-consumer interactions, such as seed predation, and whether contemporary disturbance (e.g., fire) alters the effects of historical agriculture on these interactions. We conducted a study at 27 sites distributed across 80,300 ha in post-agricultural and non-agricultural longleaf pine woodlands with different degrees of fire frequency to test the hypothesis that past and present-day disturbances that alter plant communities can subsequently alter seed predation. We quantified seed removal by arthropods and rodents for Tephrosia virginiana and Vernonia angustifolia, species of conservation interest. We found that the effects of land-use history and fire frequency on seed removal were contingent on granivore guild and microhabitat characteristics. Tephrosia virginiana removal was greater in low fire frequency sites, due to greater seed removal by rodents. Although overall removal of V. angustifolia did not differ among habitats, rodents removed more seeds than arthropods at post-agricultural sites and non-agricultural sites with low fire frequencies, but not at non-agricultural sites with high fire frequencies. Land-use history and fire frequency also affected the relationship between microhabitat characteristics and removal of V. angustifolia. Our results suggest that historical agriculture and present-day fire regimes may alter seed predation by shifting the impact of rodent and arthropod seed predators among habitats, with potential consequences for the establishment of rare plant species consumed by one or both predators.

Apparent competition and native consumers exacerbate the strong competitive effect of an exotic plant species.

Direct and indirect effects can play a key role in invasions, but experiments evaluating both are rare. We examined the roles of direct competition and apparent competition by exotic Amur honeysuckle (Lonicera maackii) by manipulating (1) L. maackii vegetation, (2) presence of L. maackii fruits, and (3) access to plants by small mammals and deer. Direct competition with L. maackii reduced the abundance and richness of native and exotic species, and native consumers significantly reduced the abundance and richness of native species. Although effects of direct competition and consumption were more pervasive, richness of native plants was also reduced through apparent competition, as small-mammal consumers reduced richness only when L. maackii fruits were present. Our experiment reveals the multiple, interactive pathways that affect the success and impact of an invasive exotic plant: exotic plants may directly benefit from reduced attack by native consumers, may directly exert strong competitive effects on native plants, and may also benefit from apparent competition.

Land-use history alters contemporary insect herbivore community composition and decouples plant-herbivore relationships.

Past land use can create altered soil conditions and plant communities that persist for decades, although the effects of these altered conditions on consumers are rarely investigated. Using a large-scale field study at 36 sites in longleaf pine (Pinus palustris) woodlands, we examined whether historic agricultural land use leads to differences in the abundance and community composition of insect herbivores (grasshoppers, families Acrididae and Tettigoniidae). We measured the cover of six plant functional groups and several environmental variables to determine whether historic agricultural land use affects the relationships between plant cover or environmental conditions and grasshopper assemblages. Land-use history had taxa-specific effects and interacted with herbaceous plant cover to alter grasshopper abundances, leading to significant changes in community composition. Abundance of most grasshopper taxa increased with herbaceous cover in woodlands with no history of agriculture, but there was no relationship in post-agricultural woodlands. We also found that grasshopper abundance was negatively correlated with leaf litter cover. Soil hardness was greater in post-agricultural sites (i.e. more compacted) and was associated with grasshopper community composition. Both herbaceous cover and leaf litter cover are influenced by fire frequency, suggesting a potential indirect role of fire on grasshopper assemblages. Our results demonstrate that historic land use may create persistent differences in the composition of grasshopper assemblages, while contemporary disturbances (e.g. prescribed fire) may be important for determining the abundance of grasshoppers, largely through the effect of fire on plants and leaf litter. Therefore, our results suggest that changes in the contemporary management regimes (e.g. increasing prescribed fire) may not be sufficient to shift the structure of grasshopper communities in post-agricultural sites towards communities in non-agricultural habitats. Rather, repairing degraded soil conditions and restoring plant communities are likely necessary for restoring grasshopper assemblages in post-agricultural woodlands.