Interactions between large-scale and local factors influence seed predation rates and seed loss.

Herbivores often have highly variable impacts on plant fecundity. The relative contribution of different environmental factors operating at varying spatial scales in affecting this variability is often unclear. We examined how density-dependent seed predation at local scales and regional differences in primary productivity are associated with variation in the magnitude of pre-dispersal seed predation on Monarda fistulosa (Lamiaceae). Within M. fistulosa populations growing in a low-productivity region (LPR), Montana, USA, and a high-productivity region (HPR), Wisconsin, USA, we quantified the magnitude of pre-dispersal seed predation among individual plants differing in seed head densities. Out of a total of 303 M. fistulosa plants that were surveyed, we found half as many herbivores in seed heads in the LPR (n = 133 herbivores) compared to the HPR (n = 316). In the LPR, 30% of the seed heads were damaged in plants with low seed head density, while 61% of seed heads were damaged in plants with high seed head density. Seed head damage was consistently high in the HPR (about 49% across the range of seed head density) compared to the LPR (45% across a range of seed head density). However, the proportion of seeds per seed head that were destroyed by herbivores was nearly two times higher (~38% loss) in the LPR compared to HPR (22% loss). Considering the combined effects of probability of damage and seed loss per seed head, the proportion seed loss per plant was consistently higher in the HPR regardless of seed head density. Nevertheless, because of greater seed head production, the total number of viable seeds produced per plant was higher in HPR and high-density plants, despite being exposed to greater herbivore pressure. These findings show how large-scale factors can interact with local-scale factors to influence how strongly herbivores suppress plant fecundity.

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.

Evaluating unintended consequences of intentional species introductions and eradications for improved conservation management.

Increasingly intensive strategies to maintain biodiversity and ecosystem function are being deployed in response to global anthropogenic threats, including intentionally introducing and eradicating species via assisted migration, rewilding, biological control, invasive species eradications, and gene drives. These actions are highly contentious because of their potential for unintended consequences. We conducted a global literature review of these conservation actions to quantify how often unintended outcomes occur and to elucidate their underlying causes. To evaluate conservation outcomes, we developed a community assessment framework for systematically mapping the range of possible interaction types for 111 case studies. Applying this tool, we quantified the number of interaction types considered in each study and documented the nature and strength of intended and unintended outcomes. Intended outcomes were reported in 51% of cases, a combination of intended outcomes and unintended outcomes in 26%, and strictly unintended outcomes in 10%. Hence, unintended outcomes were reported in 36% of all cases evaluated. In evaluating overall conservations outcomes (weighing intended vs. unintended effects), some unintended effects were fairly innocuous relative to the conservation objective, whereas others resulted in serious unintended consequences in recipient communities. Studies that assessed a greater number of community interactions with the target species reported unintended outcomes more often, suggesting that unintended consequences may be underreported due to insufficient vetting. Most reported unintended outcomes arose from direct effects (68%) or simple density-mediated or indirect effects (25%) linked to the target species. Only a few documented cases arose from more complex interaction pathways (7%). Therefore, most unintended outcomes involved simple interactions that could be predicted and mitigated through more formal vetting. Our community assessment framework provides a tool for screening future conservation actions by mapping the recipient community interaction web to identify and mitigate unintended outcomes from intentional species introductions and eradications for conservation.

Evaluación de las Consecuencias Involuntarias de las Introducciones y Erradicaciones Intencionales de Especies para el Manejo Mejorado de la Conservación Resumen Actualmente se despliegan estrategias cada vez más intensas para mantener la biodiversidad y la función del ecosistema como respuesta a las amenazas antropogénicas mundiales, incluyendo la introducción y erradicación intencionales de especies por medio de la migración asistida, el retorno a la vida silvestre, el control biológico, la erradicación de especies invasoras y la genética dirigida. Estas acciones son muy polémicas por el potencial que tienen para generar consecuencias involuntarias. Realizamos una revisión de la literatura mundial sobre estas acciones de conservación para cuantificar cuán seguido ocurren las consecuencias involuntarias y cuáles son sus causas subyacentes. Para evaluar los resultados de conservación, desarrollamos un marco de trabajo de evaluación comunitaria para mapear sistemáticamente el rango de posibles interacciones para 111 estudios de caso. Con la aplicación de esta herramienta cuantificamos el número de tipos de interacción consideradas en cada estudio y documentamos la naturaleza y la fuerza de los resultados involuntarios. Se reportaron los resultados voluntarios en 51% de los casos, una combinación de resultados voluntarios e involuntarios en 26% de los casos y estrictamente los resultados involuntarios en el 10% de los casos. Por lo tanto, los resultados involuntarios fueron reportados en el 36% de todos los casos evaluados. En la evaluación general de los resultados de conservación (sopesando los efectos voluntarios y. los involuntarios), algunos efectos involuntarios fueron bastante inocuos en relación con el objetivo de conservación, mientras que otros resultaron en consecuencias involuntarias severas para las comunidades receptoras. Los estudios que evaluaron un mayor número de interacciones comunitarias con la especie objetivo reportaron resultados involuntarios con mayor frecuencia, lo que sugiere que las consecuencias involuntarias pueden estar subvaloradas debido al escrutinio insuficiente. La mayoría de los resultados involuntarios reportados surgieron de los efectos directos (68%) o de los efectos indirectos o mediados por la densidad (25%) vinculados con la especie diana. Solamente unos cuantos casos documentados surgieron de interacciones más complejas (7%). Por lo tanto, la mayoría de los resultados involuntarios involucran interacciones simples que podrían ser pronosticadas y mitigadas por medio de un escrutinio más formal. Nuestro marco de trabajo de evaluación comunitaria proporciona una herramienta para la revisión de las acciones de conservación en el futuro mediante el mapeo de la red de interacciones entre comunidades receptoras y para la mitigación de los resultados involuntarios surgidos de las introducciones y erradicaciones intencionales de especies a favor de la conservación.

Suitability of Formulated Entomopathogenic Fungi Against Hibiscus Mealybug, Nipaecoccus viridis (Hemiptera: Pseudococcidae), Deployed Within Mesh Covers Intended to Protect Citrus From Huanglongbing.

Mesh exclusion bags are increasingly being adopted by Florida citrus growers to protect young citrus trees from Asian citrus psyllid, Diaphorina citri Kuwayama, and Huanglongbing disease. These mesh bags exclude larger insects such as D. citri but may allow entry of minute insects. Hibiscus mealybugs, Nipaecoccus viridis (Newstead), have been observed thriving in the micro-habitat created by these covers on trees. Entomopathogenic fungi (EPF) and insect growth regulators (IGRs) are effective against several mealybug species under various growing conditions, but their efficacy against N. viridis or within the microclimate within exclusion bags is unknown. Therefore, we evaluated various formulations of entomopathogenic fungi with and without IGR against N. viridis using laboratory bioassays. We then conducted semifield bioassays to determine effectiveness of EPF formulations alone and in combination with an IGR applied to citrus trees enveloped within mesh bags under field conditions. Survival probabilities of N. viridis nymphs exposed to all Beauveria bassiana-based products tested were comparable to malathion under laboratory conditions and reduced survival as compared to controls (water only). Under field conditions, mortality of N. viridis nymphs on leaves sprayed with each fungal formulation tested was significantly greater than on control treatments (Water, Suffoil X, 435 oil) up to four weeks post application. There were no differences in the colony forming units per leaf area amongst all fungal treatments. Formulated B. bassiana-based products applied alone or combined with an IGR should be effective tools for managing N. viridis populations on young citrus trees protected with mesh exclusion bags.

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.

Effects of Lethal Bronzing Disease, Palm Height, and Temperature on Abundance and Monitoring of Haplaxius crudus.

Insect vector feeding preference and behavior play important roles in pathogen transmission, especially for pathogens that solely rely on insect vector transmission. This study aims to examine the effects of the 16SrIV-D phytoplasma, the causal agent of lethal bronzing (LB) disease of palms, on associated auchenorrhynchan insects. The numbers of auchenorrhynchans collected during weekly surveys during a yearlong study using yellow sticky traps were analyzed. The cumulative number of H. crudus was 4.5 times greater on phytoplasma-infected relative to non-infected palms. Other auchenorrhynchans showed no difference between phytoplasma-infected and non-infected palms or were greater on non-infected rather than on infected palms. Furthermore, we examined the effects of LB, palm height, temperature, and the interactive effects of these factors on H. crudus abundance. When the palms were infected with LB, at low temperature, H. crudus was more abundant on shorter than taller palms; however, H. crudus was more abundant on taller than shorter palms at the median and higher temperatures. These results may indicate that H. crudus prefers LB-infected palms over non-infected palms. The interactive effects of LB, palm heights, and temperature further suggest that vector monitoring and disease management should be optimized according to seasonal variation in temperature.

Seedling recruitment correlates with seed input across seed sizes: implications for coexistence.

Understanding controls on recruitment is critical to predicting community assembly, diversity, and coexistence. Theory posits that at mean fecundity, recruitment of highly fecund small-seeded plants should be primarily microsite limited, which is indicated by a saturating recruitment function. In contrast, species that produce fewer large seeds are more likely to be seed-limited, which is characterized by a linear recruitment function. If these patterns hold in nature, seed predation that disproportionately affects larger-seeded species can limit their establishment. We tested these predictions by comparing recruitment functions among 16 co-occurring perennial forb species that vary by over two orders of magnitude in seed size. We also assessed how postdispersal seed predation by mice influenced recruitment. We added seeds at densities from zero to three times natural fecundity of each species to undisturbed plots and examined spatial variation in recruitment by conducting experiments across 10 grassland sites that varied in productivity and resource availability. Consistent across two replicated years, most species had linear recruitment functions across the range of added seed densities, indicative of seed-limited recruitment. Depending on year, the recruitment functions of only 19-37% of target species saturated near their average fecundity, and this was not associated with seed size. Recruitment was strongly inhibited by rodent seed predation for large-seeded species but not for smaller-seeded species. Proportional recruitment was more sensitive to spatial variation in recruitment conditions across sites for some small-seeded species than for large-seeded species. These results contradict the common belief that highly fecund small-seeded species suffer from microsite-limited recruitment. Rather, they imply that, at least episodically, recruitment can be strongly correlated to plant fecundity. However, proportional recruitment of small-seeded species was inhibited at productive sites to a greater extent than large-seeded species. Results also show that in a system where the dominant granivore prefers larger seeds, low-fecundity large-seeded species can suffer from even greater seed-limited recruitment than would occur in the absence of predators.

Population Variation, Environmental Gradients, and the Evolutionary Ecology of Plant Defense against Herbivory.

A central tenet of plant defense theory is that adaptation to the abiotic environment sets the template for defense strategies, imposing a trade-off between plant growth and defense. Yet this trade-off, commonly found among species occupying divergent resource environments, may not occur across populations of single species. We hypothesized that more favorable climates and higher levels of herbivory would lead to increases in growth and defense across plant populations. We evaluated whether plant growth and defense traits covaried across 18 populations of showy milkweed (Asclepias speciosa) inhabiting an east-west climate gradient spanning 25° of longitude. A suite of traits impacting defense (e.g., latex, cardenolides), growth (e.g., size), or both (e.g., specific leaf area [SLA], trichomes) were measured in natural populations and in a common garden, allowing us to evaluate plastic and genetically based variation in these traits. In natural populations, herbivore pressure increased toward warmer sites with longer growing seasons. Growth and defense traits showed strong clinal patterns and were positively correlated. In a common garden, clines with climatic origin were recapitulated only for defense traits. Correlations between growth and defense traits were also weaker and more negative in the common garden than in the natural populations. Thus, our data suggest that climatically favorable sites likely facilitate the evolution of greater defense at minimal costs to growth, likely because of increased resource acquisition.

Effects of Short- and Long-Term Variation in Resource Conditions on Soil Fungal Communities and Plant Responses to Soil Biota.

Soil biota can strongly influence plant performance with effects ranging from negative to positive. However, shifts in resource availability can influence plant responses, with soil pathogens having stronger negative effects in high-resource environments and soil mutualists, such as arbuscular mycorrhizal fungi (AMF), having stronger positive effects in low-resource environments. Yet the relative importance of long-term vs. short-term variation in resources on soil biota and plant responses is not well-known. To assess this, we grew the perennial herb Asclepias speciosa in a greenhouse experiment that crossed a watering treatment (wet vs. dry treatment) with a manipulation of soil biota (live vs. sterilized soil) collected from two geographic regions (Washington and Minnesota) that vary greatly in annual precipitation. Because soil biota can influence many plant functional traits, we measured biomass as well as resource acquisition (e.g., root:shoot, specific leaf area) and defense (e.g., trichome and latex production) traits. Due to their important role as mutualists and pathogens, we also characterized soil fungal communities in the field and greenhouse and used curated databases to assess fungal composition and potential function. We found that the experimental watering treatment had a greater effect than soil biota origin on plant responses; most plant traits were negatively affected by live soils under wet conditions, whereas responses were neutral or positive in live dry soil. These consistent differences in plant responses occurred despite clear differences in soil fungal community composition between inoculate origin and watering treatments, which indicates high functional redundancy among soil fungi. All plants grown in live soil were highly colonized by AMF and root colonization was higher in wet than dry soil; root colonization by other fungi was low in all treatments. The most parsimonious explanation for negative plant responses in wet soil is that AMF became parasitic under conditions that alleviated resource limitation. Thus, plant responses appeared driven by shifts within rather than between fungal guilds, which highlights the importance of coupling growth responses with characterizations of soil biota to fully understand underlying mechanisms. Collectively these results highlight how short-term changes in environmental conditions can mediate complex interactions between plants and soil biota.

Trait differences in responses to arbuscular mycorrhizal fungi are stronger and more consistent than fixed differences among populations of Asclepias speciosa.

PREMISE OF THE STUDY: Arbuscular mycorrhizal (AM) fungi can promote plant growth and reproduction, but other plant physiological traits or traits that provide defense against herbivores can also be affected by AM fungi. However, whether responses of different traits to AM fungi are correlated and whether these relationships vary among plants from different populations are unresolved. METHODS: In a common garden experiment, we grew Asclepias speciosa plants from seed collected from populations found along an environmental gradient with and without AM fungi to assess whether the responses of six growth and defense traits to AM fungi are correlated. KEY RESULTS: Although there was strong genetic differentiation in mean trait values among populations, AM fungi consistently increased expression of most growth and defense traits across all populations. Responses of biomass and root to shoot ratio to AM fungi were positively correlated, suggesting that plants that are more responsive to AM fungi allocated more biomass belowground. Responses of biomass and trichome density to AM fungi were negatively correlated, indicating a trade-off in responsiveness between a growth and defensive trait. CONCLUSIONS: Our results suggest that while there is substantial population differentiation in many traits of A. speciosa, populations respond similarly to AM fungi, and both positive and negative correlations among trait responses occur.

Corrigendum: Effects of Short- and Long-Term Variation in Resource Conditions on Soil Fungal Communities and Plant Responses to Soil Biota.

[This corrects the article DOI: 10.3389/fpls.2018.01605.].

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.

A Framework for Predicting Intraspecific Variation in Plant Defense.

One of the most well-supported theories regarding the evolution of plant defenses is the resource availability hypothesis (RAH). RAH posits that species from high-resource environments grow fast and allocate little to herbivore-resistance traits, whereas those species in low-resource environments grow slow and are highly resistant to herbivores. However, within species, how resources influence defense is unclear and existing theories make opposing predictions. Here, we review studies documenting intraspecific variation in plant defense across resource gradients and find little support for RAH. We outline why RAH does not apply intraspecifically and present a predictive framework for understanding how resources influence intraspecific variation in plant defense. Our framework provides an important step towards reconciling inter- versus intraspecific strategies of defense.

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.

Land-use history and contemporary management inform an ecological reference model for longleaf pine woodland understory plant communities.

Ecological restoration is frequently guided by reference conditions describing a successfully restored ecosystem; however, the causes and magnitude of ecosystem degradation vary, making simple knowledge of reference conditions insufficient for prioritizing and guiding restoration. Ecological reference models provide further guidance by quantifying reference conditions, as well as conditions at degraded states that deviate from reference conditions. Many reference models remain qualitative, however, limiting their utility. We quantified and evaluated a reference model for southeastern U.S. longleaf pine woodland understory plant communities. We used regression trees to classify 232 longleaf pine woodland sites at three locations along the Atlantic coastal plain based on relationships between understory plant community composition, soils (which broadly structure these communities), and factors associated with understory degradation, including fire frequency, agricultural history, and tree basal area. To understand the spatial generality of this model, we classified all sites together and for each of three study locations separately. Both the regional and location-specific models produced quantifiable degradation gradients-i.e., progressive deviation from conditions at 38 reference sites, based on understory species composition, diversity and total cover, litter depth, and other attributes. Regionally, fire suppression was the most important degrading factor, followed by agricultural history, but at individual locations, agricultural history or tree basal area was most important. At one location, the influence of a degrading factor depended on soil attributes. We suggest that our regional model can help prioritize longleaf pine woodland restoration across our study region; however, due to substantial landscape-to-landscape variation, local management decisions should take into account additional factors (e.g., soil attributes). Our study demonstrates the utility of quantifying degraded states and provides a series of hypotheses for future experimental restoration work. More broadly, our work provides a framework for developing and evaluating reference models that incorporate multiple, interactive anthropogenic drivers of ecosystem degradation.