Compartmentalization of specialized metabolites across vegetative and reproductive tissues in two sympatric Psychotria species.

PREMISE: The specialized metabolites of plants are recognized as key chemical traits in mediating the ecology and evolution of sundry plant-biotic interactions, from pollination to seed predation. Intra- and interspecific patterns of specialized metabolite diversity have been studied extensively in leaves, but the diverse biotic interactions that contribute to specialized metabolite diversity encompass all plant organs. Focusing on two species of Psychotria shrubs, we investigated and compared patterns of specialized metabolite diversity in leaves and fruit with respect to each organ's diversity of biotic interactions. METHODS: To evaluate associations between biotic interaction diversity and specialized metabolite diversity, we combined UPLC-MS metabolomic analysis of foliar and fruit specialized metabolites with existing surveys of leaf- and fruit-centered biotic interactions. We compared patterns of specialized metabolite richness and variance among vegetative and reproductive tissues, among plants, and between species. RESULTS: In our study system, leaves interact with a far larger number of consumer species than do fruit, while fruit-centric interactions are more ecologically diverse in that they involve antagonistic and mutualistic consumers. This aspect of fruit-centric interactions was reflected in specialized metabolite richness-leaves contained more than fruit, while each organ contained over 200 organ-specific specialized metabolites. Within each species, leaf- and fruit-specialized metabolite composition varied independently of one another across individual plants. Contrasts in specialized metabolite composition were stronger between organs than between species. CONCLUSIONS: As ecologically disparate plant organs with organ-specific specialized metabolite traits, leaves and fruit can each contribute to the tremendous overall diversity of plant specialized metabolites.

Short-term plant-soil feedback experiment fails to predict outcome of competition observed in long-term field experiment.

Mounting evidence suggests that plant-soil feedbacks (PSF) may determine plant community structure. However, we still have a poor understanding of how predictions from short-term PSF experiments compare with outcomes of long-term field experiments involving competing plants. We conducted a reciprocal greenhouse experiment to examine how the growth of prairie grass species depended on the soil communities cultured by conspecific or heterospecific plant species in the field. The source soil came from monocultures in a long-term competition experiment (LTCE; Cedar Creek Ecosystem Science Reserve, MN, USA). Within the LTCE, six species of perennial prairie grasses were grown in monocultures or in eight pairwise competition plots for 12 years under conditions of low or high soil nitrogen availability. In six cases, one species clearly excluded the other; in two cases, the pair appeared to coexist. In year 15, we gathered soil from all 12 soil types (monocultures of six species by two nitrogen levels) and grew seedlings of all six species in each soil type for 7 weeks. Using biomass estimates from this greenhouse experiment, we predicted coexistence or competitive exclusion using pairwise PSFs, as derived by Bever and colleagues, and compared model predictions to observed outcomes within the LTCE. Pairwise PSFs among the species pairs ranged from negative, which is predicted to promote coexistence, to positive, which is predicted to promote competitive exclusion. However, these short-term PSF predictions bore no systematic resemblance to the actual outcomes of competition observed in the LTCE. Other forces may have more strongly influenced the competitive interactions or critical assumptions that underlie the PSF predictions may not have been met. Importantly, the pairwise PSF score derived by Bever et al. is only valid when the two species exhibit an internal equilibrium, corresponding to the Lotka-Volterra competition outcomes of stable coexistence and founder control. Predicting the other two scenarios, competitive exclusion by either species irrespective of initial conditions, requires measuring biomass in uncultured soil, which is methodologically challenging. Subject to several caveats that we discuss, our results call into question whether long-term competitive outcomes in the field can be predicted from the results of short-term PSF experiments.

Resistance Genes Affect How Pathogens Maintain Plant Abundance and Diversity.

AbstractSpecialized pathogens are thought to maintain plant community diversity; however, most ecological studies treat pathogens as a black box. Here we develop a theoretical model to test how the impact of specialized pathogens changes when plant resistance genes (R-genes) mediate susceptibility. This work synthesizes two major hypotheses: the gene-for-gene model of pathogen resistance and the Janzen-Connell hypothesis of pathogen-mediated coexistence. We examine three scenarios. First, R-genes do not affect seedling survival; in this case, pathogens promote diversity. Second, seedlings are protected from pathogens when their R-gene alleles and susceptibility differ from those of nearby conspecific adults, thereby reducing transmission. If resistance is not costly, pathogens are less able to promote diversity because populations with low R-gene diversity suffer higher mortality, putting those populations at a disadvantage and potentially causing their exclusion. R-gene diversity may also be reduced during population bottlenecks, creating a priority effect. Third, when R-genes affect survival but resistance is costly, populations can avoid extinction by losing resistance alleles, as they cease paying a cost that is unneeded. Thus, the impact pathogens can have on tree diversity depends on the mechanism of plant-pathogen interactions. Future empirical studies should examine which of these scenarios most closely reflects the real world.

Investigating the direct and indirect effects of forest fragmentation on plant functional diversity.

Ongoing habitat loss and fragmentation alter the functional diversity of forests. Generalising the magnitude of change in functional diversity of fragmented landscapes and its drivers is challenging because of the multiple scales at which landscape fragmentation takes place. Here we propose a multi-scale approach to determine whether fragmentation processes at the local and landscape scales are reducing functional diversity of trees in the East Usambara Mountains, Tanzania. We employ a structural equation modelling approach using five key plant traits (seed length, dispersal mode, shade tolerance, maximum tree height, and wood density) to better understand the functional responses of trees to fragmentation at multiple scales. Our results suggest both direct and indirect effects of forest fragmentation on tree functional richness, evenness and divergence. A reduction in fragment area appears to exacerbate the negative effects resulting from an increased amount of edge habitat and loss of shape complexity, further reducing richness and evenness of traits related to resource acquisition and favouring tree species with fast growth. As anthropogenic disturbances affect forests around the world, we advocate to include the direct and indirect effects of forest fragmentation processes to gain a better understanding of shifts in functional diversity that can inform future management efforts.

Individual variation in dispersal and fecundity increases rates of spatial spread.

Dispersal and fecundity are two fundamental traits underlying the spread of populations. Using integral difference equation models, we examine how individual variation in these fundamental traits and the heritability of these traits influence rates of spatial spread of populations along a one-dimensional transect. Using a mixture of analytic and numerical methods, we show that individual variation in dispersal rates increases spread rates and the more heritable this variation, the greater the increase. In contrast, individual variation in lifetime fecundity only increases spread rates when some of this variation is heritable. The highest increases in spread rates occur when variation in dispersal positively co-varies with fecundity. Our results highlight the importance of estimating individual variation in dispersal rates, dispersal syndromes in which fecundity and dispersal co-vary positively and heritability of these traits to predict population rates of spatial spread.

Introduction to the Special Issue: The role of seed dispersal in plant populations: perspectives and advances in a changing world.

Despite the importance of seed dispersal as a driving process behind plant community assembly, our understanding of the role of seed dispersal in plant population persistence and spread remains incomplete. As a result, our ability to predict the effects of global change on plant populations is hampered. We need to better understand the fundamental link between seed dispersal and population dynamics in order to make predictive generalizations across species and systems, to better understand plant community structure and function, and to make appropriate conservation and management responses related to seed dispersal. To tackle these important knowledge gaps, we established the CoDisperse Network and convened an interdisciplinary, NSF-sponsored Seed Dispersal Workshop in 2016, during which we explored the role of seed dispersal in plant population dynamics (NSF DEB Award # 1548194). In this Special Issue, we consider the current state of seed dispersal ecology and identify the following collaborative research needs: (i) the development of a mechanistic understanding of the movement process influencing dispersal of seeds; (ii) improved quantification of the relative influence of seed dispersal on plant fitness compared to processes occurring at other life history stages; (iii) an ability to scale from individual plants to ecosystems to quantify the influence of dispersal on ecosystem function; and (iv) the incorporation of seed dispersal ecology into conservation and management strategies.

Advancing an interdisciplinary framework to study seed dispersal ecology.

Although dispersal is generally viewed as a crucial determinant for the fitness of any organism, our understanding of its role in the persistence and spread of plant populations remains incomplete. Generalizing and predicting dispersal processes are challenging due to context dependence of seed dispersal, environmental heterogeneity and interdependent processes occurring over multiple spatial and temporal scales. Current population models often use simple phenomenological descriptions of dispersal processes, limiting their ability to examine the role of population persistence and spread, especially under global change. To move seed dispersal ecology forward, we need to evaluate the impact of any single seed dispersal event within the full spatial and temporal context of a plant's life history and environmental variability that ultimately influences a population's ability to persist and spread. In this perspective, we provide guidance on integrating empirical and theoretical approaches that account for the context dependency of seed dispersal to improve our ability to generalize and predict the consequences of dispersal, and its anthropogenic alteration, across systems. We synthesize suitable theoretical frameworks for this work and discuss concepts, approaches and available data from diverse subdisciplines to help operationalize concepts, highlight recent breakthroughs across research areas and discuss ongoing challenges and open questions. We address knowledge gaps in the movement ecology of seeds and the integration of dispersal and demography that could benefit from such a synthesis. With an interdisciplinary perspective, we will be able to better understand how global change will impact seed dispersal processes, and potential cascading effects on plant population persistence, spread and biodiversity.

Seed-to-seedling transitions exhibit distance-dependent mortality but no strong spacing effects in a Neotropical forest.

Patterns of seed dispersal and seed mortality influence the spatial structure of plant communities and the local coexistence of competing species. Most seeds are dispersed in proximity to the parent tree, where mortality is also expected to be the highest, because of competition with siblings or the attraction of natural enemies. Whereas distance-dependent mortality in the seed-to-seedling transition was often observed in tropical forests, few studies have attempted to estimate the shape of the survival-distance curves, which determines whether the peak of seedling establishment occurs away from the parent tree (Janzen-Connell pattern) or if the peak attenuates but remains at the parent location (Hubbell pattern). In this study, we inferred the probability density of seed dispersal and two stages of seedling establishment (new recruits, and seedlings 20 cm or taller) with distance for 24 tree species present in the 50-ha Forest Dynamics Plot of Barro Colorado Island, Panama. Using data from seed traps, seedling survey quadrats, and tree-census records spanning the 1988-2014 period, we fit hierarchical Bayesian models including parameters for tree fecundity, the shape of the dispersal kernel, and overdispersion of seed or seedling counts. We combined predictions from multiple dispersal kernels to obtain more robust inferences. We find that Hubbell patterns are the most common and Janzen-Connell patterns are very rare among those species; that distance-dependent mortality may be stronger in the seed stage, in the early recruit stage, or comparable in both; and that species with larger seeds experience less overall mortality and less distance-dependent mortality. Finally, we describe how this modeling approach could be extended at a community scale to include less abundant species.

Intrinsic and extrinsic drivers of intraspecific variation in seed dispersal are diverse and pervasive.

There is growing realization that intraspecific variation in seed dispersal can have important ecological and evolutionary consequences. However, we do not have a good understanding of the drivers or causes of intraspecific variation in dispersal, how strong an effect these drivers have, and how widespread they are across dispersal modes. As a first step to developing a better understanding, we present a broad, but not exhaustive, review of what is known about the drivers of intraspecific variation in seed dispersal, and what remains uncertain. We start by decomposing 'drivers of intraspecific variation in seed dispersal' into intrinsic drivers (i.e. variation in traits of individual plants) and extrinsic drivers (i.e. variation in ecological context). For intrinsic traits, we further decompose intraspecific variation into variation among individuals and variation of trait values within individuals. We then review our understanding of the major intrinsic and extrinsic drivers of intraspecific variation in seed dispersal, with an emphasis on variation among individuals. Crop size is the best-supported and best-understood intrinsic driver of variation across dispersal modes; overall, more seeds are dispersed as more seeds are produced, even in cases where per seed dispersal rates decline. Fruit/seed size is the second most widely studied intrinsic driver, and is also relevant to a broad range of seed dispersal modes. Remaining intrinsic drivers are poorly understood, and range from effects that are probably widespread, such as plant height, to drivers that are most likely sporadic, such as fruit or seed colour polymorphism. Primary extrinsic drivers of variation in seed dispersal include local environmental conditions and habitat structure. Finally, we present a selection of outstanding questions as a starting point to advance our understanding of individual variation in seed dispersal.

The total dispersal kernel: a review and future directions.

The distribution and abundance of plants across the world depends in part on their ability to move, which is commonly characterized by a dispersal kernel. For seeds, the total dispersal kernel (TDK) describes the combined influence of all primary, secondary and higher-order dispersal vectors on the overall dispersal kernel for a plant individual, population, species or community. Understanding the role of each vector within the TDK, and their combined influence on the TDK, is critically important for being able to predict plant responses to a changing biotic or abiotic environment. In addition, fully characterizing the TDK by including all vectors may affect predictions of population spread. Here, we review existing research on the TDK and discuss advances in empirical, conceptual modelling and statistical approaches that will facilitate broader application. The concept is simple, but few examples of well-characterized TDKs exist. We find that significant empirical challenges exist, as many studies do not account for all dispersal vectors (e.g. gravity, higher-order dispersal vectors), inadequately measure or estimate long-distance dispersal resulting from multiple vectors and/or neglect spatial heterogeneity and context dependence. Existing mathematical and conceptual modelling approaches and statistical methods allow fitting individual dispersal kernels and combining them to form a TDK; these will perform best if robust prior information is available. We recommend a modelling cycle to parameterize TDKs, where empirical data inform models, which in turn inform additional data collection. Finally, we recommend that the TDK concept be extended to account for not only where seeds land, but also how that location affects the likelihood of establishing and producing a reproductive adult, i.e. the total effective dispersal kernel.

The effects of habitat loss and fragmentation on plant functional traits and functional diversity: what do we know so far?

Habitat loss and fragmentation result in significant landscape changes that ultimately affect plant diversity and add uncertainty to how natural areas will respond to future global change. This uncertainty is important given that the loss of biodiversity often includes losing key ecosystem functions. Few studies have explored the effects of landscape changes on plant functional diversity and evidence so far has shown far more pervasive effects than previously reported by species richness and composition studies. Here we present a review on the impact of habitat loss and fragmentation on (1) individual functional traits-related to persistence, dispersal and establishment-and (2) functional diversity. We also discuss current knowledge gaps and propose ways forward. From the literature review we found that studies have largely focused on dispersal traits, strongly impacted by habitat loss and fragmentation, while traits related to persistence were the least studied. Furthermore, most studies did not distinguish habitat loss from spatial fragmentation and were conducted at the plot or fragment-level, which taken together limits the ability to generalize the scale-dependency of landscape changes on plant functional diversity. For future work, we recommend (1) clearly distinguishing the effects of habitat loss from those of fragmentation, and (2) recognizing the scale-dependency of predicted responses when functional diversity varies in time and space. We conclude that a clear understanding of the effects of habitat loss and fragmentation on functional diversity will improve predictions of the resiliency and resistance of plant communities to varying scales of disturbance.

Consequences of intraspecific variation in seed dispersal for plant demography, communities, evolution and global change.

As the single opportunity for plants to move, seed dispersal has an important impact on plant fitness, species distributions and patterns of biodiversity. However, models that predict dynamics such as risk of extinction, range shifts and biodiversity loss tend to rely on the mean value of parameters and rarely incorporate realistic dispersal mechanisms. By focusing on the mean population value, variation among individuals or variability caused by complex spatial and temporal dynamics is ignored. This calls for increased efforts to understand individual variation in dispersal and integrate it more explicitly into population and community models involving dispersal. However, the sources, magnitude and outcomes of intraspecific variation in dispersal are poorly characterized, limiting our understanding of the role of dispersal in mediating the dynamics of communities and their response to global change. In this manuscript, we synthesize recent research that examines the sources of individual variation in dispersal and emphasize its implications for plant fitness, populations and communities. We argue that this intraspecific variation in seed dispersal does not simply add noise to systems, but, in fact, alters dispersal processes and patterns with consequences for demography, communities, evolution and response to anthropogenic changes. We conclude with recommendations for moving this field of research forward.

Employing plant functional groups to advance seed dispersal ecology and conservation.

Seed dispersal enables plants to reach hospitable germination sites and escape natural enemies. Understanding when and how much seed dispersal matters to plant fitness is critical for understanding plant population and community dynamics. At the same time, the complexity of factors that determine if a seed will be successfully dispersed and subsequently develop into a reproductive plant is daunting. Quantifying all factors that may influence seed dispersal effectiveness for any potential seed-vector relationship would require an unrealistically large amount of time, materials and financial resources. On the other hand, being able to make dispersal predictions is critical for predicting whether single species and entire ecosystems will be resilient to global change. Building on current frameworks, we here posit that seed dispersal ecology should adopt plant functional groups as analytical units to reduce this complexity to manageable levels. Functional groups can be used to distinguish, for their constituent species, whether it matters (i) if seeds are dispersed, (ii) into what context they are dispersed and (iii) what vectors disperse them. To avoid overgeneralization, we propose that the utility of these functional groups may be assessed by generating predictions based on the groups and then testing those predictions against species-specific data. We suggest that data collection and analysis can then be guided by robust functional group definitions. Generalizing across similar species in this way could help us to better understand the population and community dynamics of plants and tackle the complexity of seed dispersal as well as its disruption.

Environment and past land use together predict functional diversity in a temperate forest.

Environment and human land use both shape forest composition. Abiotic conditions sift tree species from a regional pool via functional traits that influence species' suitability to the local environment. In addition, human land use can modify species distributions and change functional diversity of forests. However, it is unclear how environment and land use simultaneously shape functional diversity of tree communities. Land-use legacies are especially prominent in temperate forest landscapes that have been extensively modified by humans in the last few centuries. Across a 900-ha temperate deciduous forest in the northeastern United States, comprising a mosaic of different-aged stands due to past human land use, we used four key functional traits-maximum height, rooting depth, wood density, and seed mass-to examine how multiple environmental and land-use variables influenced species distributions and functional diversity. We sampled ~40,000 trees >8 cm DBH within 485 plots totaling 137 ha. Species within plots were more functionally similar than expected by chance when we estimated functional diversity using all traits together (multi-trait), and to a lesser degree, with each trait separately. Multi-trait functional diversity was most strongly correlated with distance from the perennial stream, elevation, slope, and forest age. Environmental and land-use predictors varied in their correlation with functional diversities of the four individual traits. Landscape-wide change in abundances of individual species also correlated with both environment and land-use variables, but magnitudes of trait-environment interactions were generally stronger than trait interactions with land use. These findings can be applied for restoration and assisted regeneration of human-modified temperate forests by using traits to predict which tree species would establish well in relation to land-use history, topography, and soil conditions.

Neighborhoods have little effect on fungal attack or insect predation of developing seeds in a grassland biodiversity experiment.

Numerous observational studies have documented conspecific negative density-dependence that is consistent with the Janzen-Connell Hypothesis (JCH) of diversity maintenance. However, there have been few experimental tests of a central prediction of the JCH: that removing host-specific enemies should lead to greater increases in per capita recruitment in areas of higher host density or lower relative phylogenetic diversity. Using spatially randomized plots of high and low host biomass in a temperate grassland biodiversity experiment, we treated developing seedheads of six prairie perennials to factorial applications of fungicide and insecticide. We measured predispersal seed production, seed viability, and seedling biomass. Results were highly species-specific and idiosyncratic. Effects of insect seed predators and fungal pathogens on predispersal responses varied with neither conspecific biomass nor phylogenetic diversity, suggesting that-at least at the predispersal stage and for the insect and fungal seed predators we were able to exclude-the JCH is not sufficient to contribute to negative conspecific density-dependence for these dominant prairie species.

The distribution of fruit and seed toxicity during development for eleven neotropical trees and vines in Central Panama.

Secondary compounds in fruit mediate interactions with natural enemies and seed dispersers, influencing plant survival and species distributions. The functions of secondary metabolites in plant defenses have been well-studied in green tissues, but not in reproductive structures of plants. In this study, the distribution of toxicity within plants was quantified and its influence on seed survival was determined in Central Panama. To investigate patterns of allocation to chemical defenses and shifts in allocation with fruit development, I quantified variation in toxicity between immature and mature fruit and between the seed and pericarp for eleven species. Toxicity of seed and pericarp was compared to leaf toxicity for five species. Toxicity was measured as reduced hyphal growth of two fungal pathogens, Phoma sp. and Fusarium sp., and reduced survivorship of brine shrimp, Artemia franciscana, across a range of concentrations of crude extract. I used these measures of potential toxicity against generalist natural enemies to examine the effect of fruit toxicity on reductions of fruit development and seed survival by vertebrates, invertebrates, and pathogens measured for seven species in a natural enemy removal experiment. The seed or pericarp of all vertebrate- and wind-dispersed species reduced Artemia survivorship and hyphal growth of Fusarium during the immature and mature stages. Only mature fruit of two vertebrate-dispersed species reduced hyphal growth of Phoma. Predispersal seed survival increased with toxicity of immature fruit to Artemia during germination and decreased with toxicity to fungi during fruit development. This study suggests that fruit toxicity against generalist natural enemies may be common in Central Panama. These results support the hypothesis that secondary metabolites in fruit have adaptive value and are important in the evolution of fruit-frugivore interactions.

Linking fruit traits to variation in predispersal vertebrate seed predation, insect seed predation, and pathogen attack.

The importance of vertebrates, invertebrates, and pathogens for plant communities has long been recognized, but their absolute and relative importance in early recruitment of multiple coexisting tropical plant species has not been quantified. Further, little is known about the relationship of fruit traits to seed mortality due to natural enemies in tropical plants. To investigate the influences of vertebrates, invertebrates, and pathogens on reproduction of seven canopy plant species varying in fruit traits, we quantified reductions in fruit development and seed germination due to vertebrates, invertebrates, and fungal pathogens through experimental removal of these enemies using canopy exclosures, insecticide, and fungicide, respectively. We also measured morphological fruit traits hypothesized to mediate interactions of plants with natural enemies of seeds. Vertebrates, invertebrates, and fungi differentially affected predispersal seed mortality depending on the plant species. Fruit morphology explained some variation among species; species with larger fruit and less physical protection surrounding seeds exhibited greater negative effects of fungi on fruit development and germination and experienced reduced seed survival integrated over fruit development and germination in response to vertebrates. Within species, variation in seed size also contributed to variation in natural enemy effects on seed viability. Further, seedling growth was higher for seeds that developed in vertebrate exclosures for Anacardium excelsum and under the fungicide treatment for Castilla elastica, suggesting that predispersal effects of natural enemies may carry through to the seedling stage. This is the first experimental test of the relative effects of vertebrates, invertebrates, and pathogens on seed survival in the canopy. This study motivates further investigation to determine the generality of our results for plant communities. If there is strong variation in natural enemy attack among species related to differences in fruit morphology, then quantification of fruit traits will aid in predicting the outcomes of interactions between plants and their natural enemies. This is particularly important in tropical forests, where high species diversity makes it logistically impossible to study every plant life history stage of every species.

Identification and Characterization of a Carlavirus Causing Veinal Necrosis of Coleus.

A filamentous virus identified in coleus (Coleus × hybrida) in Minnesota and New York was found to cause veinal necrosis in coleus, although this symptom was observed only under certain conditions. The virus was transmitted readily by mechanical inoculation to coleus and Nicotiana spp. and was not transmitted by Myzus persicae. The particles of the coleus virus had a modal length of 640 nm and a single capsid protein with an estimated molecular mass of 34 kDa. The amino acid sequence of the coat protein region of the coleus virus genome had significant similarities only to the corresponding domain of carlaviruses. Based on virion morphology, capsid protein size, genome size and organization, amino acid sequence, and phylogenetic analyses, the coleus virus, which was named provisionally Coleus vein necrosis virus (CVNV), was concluded to be a new definitive member of the genus Carlavirus. A 2-kb fragment of the 3' terminus of the CVNV genome sequence is accessible under accession number DQ915963 in GenBank.