The effects of dispersal, herbivory, and competition on plant community assembly.

Dispersal is a key process in community assembly but is often considered separately from downstream assembly processes (e.g., competition, herbivory). However, dispersal varies by species and can interact with other assembly processes through establishment as species enter communities. Here, we sought to distinguish the role of dispersal in community assembly and its interaction with two biotic assembly processes: competition and herbivory. We used a tallgrass prairie restoration experiment that manipulated the competitive and herbivore environments while allowing for natural dispersal and establishment from a diverse regional species pool into areas of low diversity. Dispersal, competition, and herbivory all influenced local communities. By tracking the spread of four target species across the plots, we found interspecific and intraspecific differences in establishment patterns, with herbivores influencing the number of individuals present and the distances species moved. At the community level, only dispersal and competition significantly influenced alpha diversity, but all three processes additively influenced community composition. There was also evidence of herbivore-competition and herbivore-colonization trade-offs in our experiment. Some species that could tolerate herbivory were less likely to establish in competitive environments, while others that could tolerate herbivory were more likely to disperse greater distances. More work is needed to understand the contexts under which dispersal variation affects community assembly and its synergy with other processes.

Optimizing trilateration estimates for tracking fine-scale movement of wildlife using automated radio telemetry networks.

A major advancement in the use of radio telemetry has been the development of automated radio tracking systems (ARTS), which allow animal movements to be tracked continuously. A new ARTS approach is the use of a network of simple radio receivers (nodes) that collect radio signal strength (RSS) values from animal-borne radio transmitters. However, the use of RSS-based localization methods in wildlife tracking research is new, and analytical approaches critical for determining high-quality location data have lagged behind technological developments. We present an analytical approach to optimize RSS-based localization estimates for a node network designed to track fine-scale animal movements in a localized area. Specifically, we test the application of analytical filters (signal strength, distance among nodes) to data from real and simulated node networks that differ in the density and configuration of nodes. We evaluate how different filters and network configurations (density and regularity of node spacing) may influence the accuracy of RSS-based localization estimates. Overall, the use of signal strength and distance-based filters resulted in a 3- to 9-fold increase in median accuracy of location estimates over unfiltered estimates, with the most stringent filters providing location estimates with a median accuracy ranging from 28 to 73 m depending on the configuration and spacing of the node network. We found that distance filters performed significantly better than RSS filters for networks with evenly spaced nodes, but the advantage diminished when nodes were less uniformly spaced within a network. Our results not only provide analytical approaches to greatly increase the accuracy of RSS-based localization estimates, as well as the computer code to do so, but also provide guidance on how to best configure node networks to maximize the accuracy and capabilities of such systems for wildlife tracking studies.

The effects of defaunation on plants' capacity to track climate change.

Half of all plant species rely on animals to disperse their seeds. Seed dispersal interactions lost through defaunation and gained during novel community assembly influence whether plants can adapt to climate change through migration. We develop trait-based models to predict pairwise interactions and dispersal function for fleshy-fruited plants globally. Using interactions with introduced species as an observable proxy for interactions in future novel seed dispersal networks, we find strong potential to forecast their assembly and functioning. We conservatively estimate that mammal and bird defaunation has already reduced the capacity of plants to track climate change by 60% globally. This strong reduction in the ability of plants to adapt to climate change through range shifts shows a synergy between defaunation and climate change that undermines vegetation resilience.

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.

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.

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.

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.

Rapid changes in seed dispersal traits may modify plant responses to global change.

When climatic or environmental conditions change, plant populations must either adapt to these new conditions, or track their niche via seed dispersal. Adaptation of plants to different abiotic environments has mostly been discussed with respect to physiological and demographic parameters that allow local persistence. However, rapid modifications in response to changing environmental conditions can also affect seed dispersal, both via plant traits and via their dispersal agents. Studying such changes empirically is challenging, due to the high variability in dispersal success, resulting from environmental heterogeneity, and substantial phenotypic variability of dispersal-related traits of seeds and their dispersers. The exact mechanisms that drive rapid changes are often not well understood, but the ecological implications of these processes are essential determinants of dispersal success, and deserve more attention from ecologists, especially in the context of adaptation to global change. We outline the evidence for rapid changes in seed dispersal traits by discussing variability due to plasticity or genetics broadly, and describe the specific traits and biological systems in which variability in dispersal is being studied, before discussing some of the potential underlying mechanisms. We then address future research needs and propose a simulation model that incorporates phenotypic plasticity in seed dispersal. We close with a call to action and encourage ecologists and biologist to embrace the challenge of better understanding rapid changes in seed dispersal and their consequences for the reaction of plant populations to global change.

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.

The role of trust in public attitudes toward invasive species management on Guam: A case study.

Public attitudes toward invasive alien species management and trust in managers' ability to effectively manage non-native species can determine public support for conservation action. The island of Guam has experienced widespread species loss and ecosystem transformation due to invasive species, most notably, the brown treesnake (Boiga irregularis). Despite Guam's long history with invasives and extensive efforts to eradicate them, we know little about the sociological context of invasive species and drivers of public support or opposition on the island. Using focused group discussions, we explore public attitudes toward invasive species management measures. Respondents were familiar with the common invasive species on Guam and recognized that they were not native. They expressed support for management activities, interest in more effective and frequent management initiatives, and desire to participate directly in conservation actions. Participants also expressed frustration with government institutions and lack of confidence in managers' ability to control invasive species. Perceptions of managers' trustworthiness, communication with managers, and positive personal experiences with managers were related to positive attitudes about management and support for existing initiatives, indicating the important role of trust and engagement for invasive species management.

Landscape-level bird loss increases the prevalence of honeydew-producing insects and non-native ants.

Bird exclusion experiments consistently show that birds exhibit strong top-down control of arthropods, including ants and the honeydew-producing insects (HPIs) that they tend. However, it remains unclear whether the results of these small-scale bird exclosure experiments can be extrapolated to larger spatial scales. In this study, we use a natural bird removal experiment to compare the prevalence of ants and HPIs between Guam, an island whose bird community has been extirpated since the 1980s due to the introduction of the brown tree snake, and two nearby islands (Rota and Saipan) that have more intact bird assemblages. Consistent with smaller-scale bird exclosure experiments, we show that (1) forest trees from Guam are significantly more likely to host HPIs than trees from Saipan and (2) ants are nearly four times as abundant on Guam than on both Saipan and Rota. The prevalence of HPIs varied slightly based on tree species identity, although these effects were not as strong as island-level effects associated with bird loss. Ant community composition differed between Guam and the other two islands. These results corroborate past observational studies showing increased spider densities on Guam and suggest that trophic changes associated with landscape-level bird extirpation may also involve alterations in the abundance of ants and HPIs. This study also provides a clear example of the strong indirect effects that invasive species can have on natural food webs.

Contrasting ecological roles of non-native ungulates in a novel ecosystem.

Conservation has long focused on preserving or restoring pristine ecosystems. However, understanding and managing novel ecosystems has grown in importance as they outnumber pristine ecosystems worldwide. While non-native species may be neutral or detrimental in pristine ecosystems, it is possible that even notorious invaders could play beneficial or mixed roles in novel ecosystems. We examined the effects of two long-established non-native species-Philippine deer (Rusa marianna) and feral pigs (Sus scrofa)-in Guam, Micronesia, where native vertebrate frugivores are functionally absent leaving forests devoid of seed dispersers. We compared the roles of deer and pigs on seedling survival, seed dispersal and plant community structure in limestone karst forests. Deer, even at low abundances, had pronounced negative impacts on forest communities by decreasing seedling and vine abundance. By contrast, pigs showed no such relationship. Also, many viable seeds were found in pig scats, whereas few were found in deer scats, suggesting that pigs, but not deer, provide an ecosystem function-seed dispersal-that has been lost from Guam. Our study presents a discrepancy between the roles of two non-native species that are traditionally managed as a single entity, suggesting that ecological function, rather than identity as a non-native, may be more important to consider in managing novel systems.

Defaunation leads to interaction deficits, not interaction compensation, in an island seed dispersal network.

Following defaunation, the loss of interactions with mutualists such as pollinators or seed dispersers may be compensated through increased interactions with remaining mutualists, ameliorating the negative cascading impacts on biodiversity. Alternatively, remaining mutualists may respond to altered competition by reducing the breadth or intensity of their interactions, exacerbating negative impacts on biodiversity. Despite the importance of these responses for our understanding of the dynamics of mutualistic networks and their response to global change, the mechanism and magnitude of interaction compensation within real mutualistic networks remains largely unknown. We examined differences in mutualistic interactions between frugivores and fruiting plants in two island ecosystems possessing an intact or disrupted seed dispersal network. We determined how changes in the abundance and behavior of remaining seed dispersers either increased mutualistic interactions (contributing to "interaction compensation") or decreased interactions (causing an "interaction deficit") in the disrupted network. We found a "rich-get-richer" response in the disrupted network, where remaining frugivores favored the plant species with highest interaction frequency, a dynamic that worsened the interaction deficit among plant species with low interaction frequency. Only one of five plant species experienced compensation and the other four had significant interaction deficits, with interaction frequencies 56-95% lower in the disrupted network. These results do not provide support for the strong compensating mechanisms assumed in theoretical network models, suggesting that existing network models underestimate the prevalence of cascading mutualism disruption after defaunation. This work supports a mutualist biodiversity-ecosystem functioning relationship, highlighting the importance of mutualist diversity for sustaining diverse and resilient ecosystems.

Seed dispersal as an ecosystem service: frugivore loss leads to decline of a socially valued plant, Capsicum frutescens.

Species interactions, both mutualistic and antagonistic, are widely recognized as providing important ecosystem services. Fruit-eating animals influence plant recruitment by increasing germination during gut passage and moving seeds away from conspecifics. However, relative to studies focused on the importance of frugivores for plant population maintenance, few studies target frugivores as ecosystem service providers, and frugivores are underappreciated as ecosystem service providers relative to other mutualists such as pollinators. Here, we use an accidental experiment to elucidate the role of seed dispersal by frugivores for maintaining a culturally and economically important plant, the donne' sali chili (Capsicum frutescens) in the Mariana Islands. One of the islands (Guam) has lost nearly all of its native forest birds due to an invasive snake (Boiga irregularis), whereas nearby islands have relatively intact bird populations. We hypothesized that frugivore loss would influence chili recruitment and abundance, which could have economic and cultural impacts. By using video cameras, we confirmed that birds were the primary seed dispersers. We used captive bird feeding trials to obtain gut-passed seeds to use in a seedling emergence experiment. The experiment showed that gut-passed seeds emerged sooner and at a higher proportion than seeds from whole fruits. Consistent with our findings that birds benefit chilies, we observed lower chili abundance on Guam than on islands with birds. In a survey questionnaire of island residents, the majority of residents reported an association between the wild chili and local cultural values and traditions. In addition, we identified a thriving market for chili products, suggesting benefits of wild chilies to people in the Marianas both as consumers and producers. Our study therefore documents seed dispersal as both a cultural and a supporting ecosystem service. We provide a comprehensive case study on how seed-dispersed plants decline in the absence of their disperser, and how to apply mixed-methods in ecosystem service assessments. Furthermore, we suggest that scientists and resource managers may utilize fruit-frugivore mutualisms concerning socially valuable plants to gather support for frugivore and forest conservation efforts.

Structured education to improve primary-care management of headache: how long do the benefits last? A follow-up observational study.

BACKGROUND AND PURPOSE: Our earlier study showed that structured education of general practitioners (GPs) improved their practice in headache management. Here the duration of this effect was assessed. METHODS: In a follow-up observational study in southern Estonia, subjects were the same six GPs as previously, managing patients presenting with headache as the main complaint. Data reflecting their practice were collected prospectively during a 1-year period commencing 2 years after the educational intervention. The primary outcome measure was referral rate (RR) to neurological services. Comparisons were made with baseline and post-intervention data from the earlier study. RESULTS: In 366 patients consulting during the follow-up period, the RR was 19.9%, lower than at baseline (39.5%; P < 0.0001) or post-intervention (34.7%; P < 0.0001). The RR was diagnosis-dependent: the biggest decline was for migraine. Use of headache diagnostic terms showed changes generally favouring specific terminology. In particular, the proportion of patients given migraine diagnoses greatly increased whilst use of the inappropriate M79.1 (Pericranial) myalgia almost disappeared. Requests for investigations, which had fallen from 26% (of patients seen) at baseline to 4% post-intervention, resurged to 23% (mostly laboratory investigations; requests for X-rays continued to dwindle). Initiation of treatment by the GPs remained at the post-intervention level of just over 80% (up from baseline 58%). CONCLUSIONS: Improvements in GPs' practice after a structured educational programme mostly last for ≥3 years, some showing further betterment. A few measures suggest the beginnings of a decline towards baseline levels. This policy-informing evidence for continuing medical education indicates that the educational programme needs repeating every 2-3 years.

Seed dispersal increases local species richness and reduces spatial turnover of tropical tree seedlings.

Dispersal is thought to be a key process underlying the high spatial diversity of tropical forests. Just how important dispersal is in structuring plant communities is nevertheless an open question because it is very difficult to isolate dispersal from other processes, and thereby measure its effect. Using a unique situation, the loss of vertebrate seed dispersers on the island of Guam and their presence on the neighboring islands of Saipan and Rota, we quantify the contribution of vertebrate seed dispersal to spatial patterns of diversity of tree seedlings in treefall gaps. The presence of vertebrate seed dispersers approximately doubled seedling species richness within canopy gaps and halved species turnover among gaps. Our study demonstrates that dispersal plays a key role in maintaining local and regional patterns of diversity, and highlights the potential for ongoing declines in vertebrate seed dispersers to profoundly alter tropical forest composition.

Mutualistic strategies minimize coextinction in plant-disperser networks.

The global decline of mutualists such as pollinators and seed dispersers may cause negative direct and indirect impacts on biodiversity. Mutualistic network models used to understand the stability of mutualistic systems indicate that species with low partner diversity are most vulnerable to coextinction following mutualism disruption. However, existing models have not considered how species vary in their dependence on mutualistic interactions for reproduction or survival, overlooking the potential influence of this variation on species' coextinction vulnerability and on network stability. Using global databases and field experiments focused on the seed dispersal mutualism, we found that plants and animals that depend heavily on mutualistic interactions have higher partner diversity. Under simulated network disruption, this empirical relationship strongly reduced coextinction because the species most likely to lose mutualists depend least on their mutualists. The pattern also reduced the importance of network structure for stability; nested network structure had little effect on coextinction after simulations incorporated the empirically derived relationship between partner diversity and mutualistic dependence. Our results highlight a previously unknown source of stability in mutualistic networks and suggest that differences among species in their mutualistic strategy, rather than network structure, primarily accounts for stability in mutualistic communities.

Effects of an invasive predator cascade to plants via mutualism disruption.

Invasive vertebrate predators are directly responsible for the extinction or decline of many vertebrate species, but their indirect impacts often go unmeasured, potentially leading to an underestimation of their full impact. When invasives extirpate functionally important mutualists, dependent species are likely to be affected as well. Here, we show that the invasive brown treesnake, directly responsible for the extirpation of forest birds from the island of Guam, is also indirectly responsible for a severe decline in plant recruitment as a result of disrupting the fruit-frugivore mutualism. To assess the impact of frugivore loss on plants, we compare seed dispersal and recruitment of two fleshy-fruited tree species on Guam and three nearby islands with intact disperser communities. We conservatively estimate that the loss of frugivorous birds caused by the brown treesnake may have caused a 61-92% decline in seedling recruitment. This case study highlights the potential for predator invasions to cause indirect, pervasive and easily overlooked interaction cascades.

Secondary extinctions of biodiversity.

Extinctions beget further extinctions when species lose obligate mutualists, predators, prey, or hosts. Here, we develop a conceptual model of species and community attributes affecting secondary extinction likelihood, incorporating mechanisms that buffer organisms against partner loss. Specialized interactors, including 'cryptic specialists' with diverse but nonredundant partner assemblages, incur elevated risk. Risk is also higher for species that cannot either evolve new traits following partner loss or obtain novel partners in communities reorganizing under changing environmental conditions. Partner loss occurs alongside other anthropogenic impacts; multiple stressors can circumvent ecological buffers, enhancing secondary extinction risk. Stressors can also offset each other, reducing secondary extinction risk, a hitherto unappreciated phenomenon. This synthesis suggests improved conservation planning tactics and critical directions for research on secondary extinctions.