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Seed dispersal is key to the persistence and spread of plant populations. Because the majority of plant species rely on animals to disperse their seeds, global change drivers that directly affect animals can cause cascading impacts on plant communities. In this review, we synthesize studies assessing how disperser loss alters plant populations, community patterns, multitrophic interactions, and ecosystem functioning. We argue that the magnitude of risk to plants from disperser loss is shaped by the combination of a plant species’ inherent dependence on seed dispersal and the severity of the hazards faced by their dispersers. Because the factors determining a plant species’ risk of decline due to disperser loss can be related to traits of the plants and dispersers, our framework enables a trait-based understanding of change in plant community composition and ecosystem functioning. We discuss how interactions among plants, among dispersers, and across other trophic levels also mediate plant community responses, and we identify areas for future research to understand and mitigate the consequences of disperser loss on plants globally., This work was supported by the National Socio-Environmental Synthesis Center’s Postdoctoral Fellowship to E.C.F. under funding received from the National Science Foundation (DBI1639145), the Alexander von Humboldt Foundation Fellowship to I.D., and the Spanish Ministry of Science to A.T. (project CGL2017-88122-P).

Current understanding of mutualistic networks is grounded largely in data on interaction frequency, yet mutualistic network dynamics are also shaped by interaction quality—the functional outcomes of individual interactions on reproduction and survival. The difficulty of obtaining data on functional outcomes has resulted in limited understanding of functional variation among a network's pairwise species interactions, of the study designs that are necessary to capture major sources of functional variation, and of predictors of functional variation that may allow generalization across networks. In this community‐scale study, we targeted a key functional outcome in plant–frugivore networks: the impact of frugivore gut passage on seed germination. We used captive frugivore feeding trials and germination experiments in an island ecosystem, attaining species‐level coverage across all extant native frugivores and the plants they consume to (a) assess sources of functional variation, (b) separate effects of pulp removal from those of scarification via gut passage, and (c) test trait‐based correlates of gut passage effect sizes. We found antagonistic seed predation effects of a frugivore previously assumed to be a seed disperser, highlighting the need to consider functional outcomes rather than interaction frequency alone. The other frugivores each exhibited similar impacts for individual plant species, with benefits primarily caused by pulp removal rather than scarification, supporting the use of animal functional groups in this context. In contrast, plant species varied widely in impacts of gut passage on germination. Species with smaller seeds and more frugivore partners had larger benefits of gut passage, showing promise for network metrics and functional traits to predict functional variation among plants. Synthesis. Combining network and demographic approaches, we assessed the degree and sources of variation in a key functional outcome of plant–frugivore interactions across an entire network. Using a detailed study design, our work shows how simpler study designs can capture primary sources of functional variation and that functional traits and network metrics may allow generalization across networks. Efficiently measuring and generalizing sources of functional variation within mutualistic networks will strengthen our ability to model network dynamics and predict mutualist responses to global change.

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. This article is protected by copyright. All rights reserved.

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., Seed dispersal is fundamental to the structure and function of plant communities, but its complexity and heterogeneity impede mechanistic understanding and quantitative prediction of seed dispersal processes and their disruption. In this Special Issue, we consider the current state of seed dispersal ecology and identify collaborative research needs. The diversity of disciplines, geographic regions and expertise represented in this Special Issue yield a range of perspectives and insights and, we hope, will stimulate further collaborations to advance seed dispersal ecology and conservation.

How can hundreds of tree species coexist in a single hectare of tropical forest when the environmental conditions, as well as the species’ basic requirements, appear so similar? A leading explanation, particularly in tropical forests, is called the Janzen–Connell hypothesis after the two ecologists who proposed it in the early 1970s (1, 2). In this mechanism, specialized predators and pathogens concentrated near adult plants differentially reduce survival and growth of conspecific offspring relative to seedlings of other species. These natural enemies limit regeneration of common species and confer a relative advantage to rare species because they have more enemy-free regeneration sites. This has driven decades of empirical work to understand whether enemies are specialized enough in nature to cause this pattern and allow coexistence by this mechanism, and a recent metaanalysis supports the prediction that seed or seedling survival is greater away from conspecific adults (3). In PNAS, Eck et al. (4) show that natural enemies can be even more specialized, specializing on individual genotypes within a wild population. Through simulation models exploring the theoretical implications of this field result, Eck et al. (4) show that this greater specialization may weaken the stabilizing effects of natural enemies on species coexistence but also may select for greater dispersal over evolutionary time. The body of theory developed since the original formulation of the Janzen–Connell hypothesis has primarily asked ( i ) How specialized must the natural enemies be? and ( ii ) At what scale must these patterns operate? With regard to natural enemies, a long-standing conclusion is that species specificity of natural enemies allows coexistence. If a rare plant species shares a generalist enemy with an abundant plant species, then this abundant generalist enemy could extirpate the rare species from the community. With regard to patterns, the spatial scale matters—both in terms of enemy … [↵][1]1To whom correspondence should be addressed. Email: haldre{at}iastate.edu. [1]: #xref-corresp-1-1

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., Invasive brown treesnakes decimated the forest bird community on the island of Guam. Now, Rogers and colleagues document the indirect effects of the snake on trees, linking snake-initiated bird loss to reduced seed dispersal and plant recruitment on Guam compared to nearby uninvaded islands.

The Mariana islands have a species-poor but functionally diverse and largely endemic bird assemblage that varies due to biogeographic legacy and anthropogenic impacts. The largest island in the chain, Guam, is the setting for one of the most extreme examples of recent avian population declines, indicating the capacity for avifaunal collapse and loss of function in neighboring islands. We performed a systematic survey of resident land birds in remnant karst forest on the Mariana Islands' 3 largest islands following Guam to assess the status of the avifauna in this habitat, characterize inter-island heterogeneity in bird communities, and consider the resulting differences in the functional roles of birds across the archipelago's native forests. We identified significantly greater functional diversity on Rota than either Saipan or Tinian, but lower bird population densities, species richness, and Shannon diversity. We recommend continued monitoring of avian population trends across the archipelago and assessments of ecosystem functions like pollination, seed dispersal, and food web dynamics.

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., Seed dispersal is critical to plant fitness and plant community dynamics. However, measuring and tracking all factors that influence seed dispersal effectiveness for any potential seed-disperser relationship would require an unrealistically large amount of time, materials and financial resources. Building on current frameworks, we suggest that seed dispersal ecology quantify seed dispersal at the scale of plant functional groups, in order to reduce complexity to manageable levels. Based on functional group classifications, plant species can be distinguished by their level of dependence on seed dispersal and its mechanisms.

[Aim] Biogeographical comparisons of interaction networks help to elucidate differences in ecological communities and ecosystem functioning at large scales. Neotropical ecosystems have higher diversity and a different composition of frugivores and fleshy-fruited plants compared with Afrotropical systems, but a lack of intercontinental comparisons limits understanding of (a) whether plant–frugivore networks are structured in a similar manner, and (b) whether the same species traits define the roles of animals across continents., [Location] Afrotropics and Neotropics., [Time period] 1977-2015., [Taxa] Fleshy-fruited plants and frugivorous vertebrates., [Methods] We compiled a dataset comprising 17 Afrotropical and 48 Neotropical weighted seed-dispersal networks quantifying frugivory interactions between 1,091 fleshy-fruited plant and 665 animal species, comprising in total 8,251 interaction links between plants and animals. In addition, we compiled information on the body mass of animals and their degree of frugivory. We compared four standard network-level metrics related to interaction diversity and specialization, accounting for differences related to sampling effort and network location. Furthermore, we tested whether animal traits (body mass, degree of frugivory) differed between continents, whether these traits were related to the network roles of species and whether these relationships varied between continents., [Results] We found significant structural differences in networks between continents. Overall, Neotropical networks were less nested and more specialized than Afrotropical networks. At the species level, a higher body mass and degree of frugivory were associated with an increasing diversity of plant partners. Specialization of frugivores increased with the degree of frugivory, but only in the Neotropics., [Main conclusions] Our findings show that Afrotropical networks have a greater overlap in plant partners among vertebrate frugivores than the more diverse networks in the Neotropics that are characterized by a greater niche partitioning. Hence, the loss of frugivore species could have stronger impacts on ecosystem functioning in the more specialized Neotropical communities compared with the more generalized Afrotropical communities., We thank Beth A. Kaplin and Norbert J. Cordeiro for their guidance and support for P.J.D., who received a travel grant by The Center for Tropical Studies and Conservation (CTEC). L.C. and I.G. were supported by the Robert Bosch Foundation. D.M.D. (DE 2754/1‐1), F.S. (HE 3041/20‐1), M.Q., V.S., E.L.N. (Research Unit 823‐825), and K.B.G., M.S. and M.G.R.V. (FOR 1246) thank the German Research Foundation (DFG) for funding. F.A.F.J. acknowledges funding by a CAPES scholarship, N.F. and D.G.S. by the Robert Bosch Foundation, M.G., C.E., A.P. and M.A.P. by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2010/52315‐7; 2015/15172‐7; 2016/18355‐8) and Conselho Nacional de Desenvolvimento Científico (CNPq), M.C.M. by Doctoral Fellowships from COLCIENCIAS and Rufford, M.S.S. by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and FONCyT (PICT2013‐2759 and PICT2016‐0608), P.G.B. by CONICET (PIP 2014‐592) and FONCyT (PICT 2013‐1280), R.A.R. by a Doctoral Fellowship from CONICET, R.H. and S.T. (IF/00441/2013) and M.C. (SFRH/BD/96050/2013) by Fundação para a Ciência e Tecnologia, Portugal, and A.T. (CGL2013‐44386‐P) and D.G. (CGL2015‐68963‐C2‐2‐R) by the Spanish government. T.

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.

Rewilding is an approach aiming at restoring ecosystems to a self-sustaining state by restoring ecological function through active reintroductions or passive management. Locations for most rewilding-through-reintroduction efforts today are selected based on the suitability of the habitat for the reintroduced species, often with little consideration of where the ecological function is most needed. We developed the Spatial Planning of Rewilding Effort (Spore) framework to identify priority locations for rewilding projects through simultaneous consideration of habitat suitability and provisioning of ecological function. We use the island of Guam as a case study for a potential rewilding project, as the island has functionally lost all native seed dispersers as a result of the invasive brown treesnake ( Boiga irregularis ). The Såli (Micronesian starling, Aplonis opaca ) is a good candidate for rewilding to restore ecological function, because it is an effective seed disperser with a localized remnant population. Using Spore, we identify three priority areas for the restoration of seed dispersal, each subdivided into management units. By recognizing the influence of landscape structure and the behaviour of the reintroduced species on the spatial pattern of the function provided by that species, this approach should lead to improved ecological outcomes.

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.

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.

In healthy forests, vertebrate frugivores move seeds from intact to degraded forests, aiding in the passive regeneration of degraded forests. Yet vertebrate frugivores are declining around the world, and little is known about the impact of this loss on regeneration of degraded areas. Here, we use a unique natural experiment to assess how complete vertebrate frugivore loss affects native seed rain in degraded forest. All native vertebrate frugivores (which were primarily avian frugivores) have been functionally extirpated from the island of Guam by the invasive brown tree snake (Boiga irregularis), whereas the nearby island of Saipan has a relatively intact vertebrate frugivore community. We captured seed rain along transects extending from intact into degraded forest and compared the species richness, density and condition of the seed rain from native bird-dispersed tree species between the two islands. Considering seeds from native bird-dispersed species, approximately 1.66 seeds landed per 26 days in each square meter of degraded forest on Saipan, whereas zero seeds landed per 26 days per square meter in degraded forest on Guam. Additionally, on Saipan, 69% of native bird-dispersed seeds in intact forest and 77% of seeds in degraded forest lacked fleshy fruit pulp, suggesting ingestion by birds, compared to 0% of all seeds on Guam. Our results show an absence of seed rain in degraded forests on Guam, correlated with the absence of birds, whereas on Saipan, frugivorous birds regularly disperse seeds into degraded forests, providing a mechanism for re-colonization by native plants. These results suggest that loss of frugivores will slow regeneration of degraded forests on Guam.

The combination of small-scale manipulative experiments and large-scale natural experiments provides a powerful approach for demonstrating the importance of top-down trophic control on the ecosystem scale. The most compelling natural experiments have come from studies examining the landscape-scale loss of apex predators like sea otters, wolves, fish and land crabs. Birds are dominant apex predators in terrestrial systems around the world, yet all studies on their role as predators have come from small-scale experiments; the top-down impact of bird loss on their arthropod prey has yet to be examined at a landscape scale. Here, we use a unique natural experiment, the extirpation of insectivorous birds from nearly all forests on the island of Guam by the invasive brown tree snake, to produce the first assessment of the impacts of bird loss on their prey. We focused on spiders because experimental studies showed a consistent top-down effect of birds on spiders. We conducted spider web surveys in native forest on Guam and three nearby islands with healthy bird populations. Spider web densities on the island of Guam were 40 times greater than densities on islands with birds during the wet season, and 2.3 times greater during the dry season. These results confirm the general trend from manipulative experiments conducted in other systems however, the effect size was much greater in this natural experiment than in most manipulative experiments. In addition, bird loss appears to have removed the seasonality of spider webs and led to larger webs in at least one spider species in the forests of Guam than on nearby islands with birds. We discuss several possible mechanisms for the observed changes. Overall, our results suggest that effect sizes from smaller-scale experimental studies may significantly underestimate the impact of bird loss on spider density as demonstrated by this large-scale natural experiment.

[Special section on vanishing fauna][1] The rate at which animals are vanishing from this planet is one of the signatures of this age, as sure a sign of human dominance as our impact on Earth's nitrogen, phosphorus, and carbon cycles. This disappearance of animals from the world's ecosystems is generally a by-product of human activity, not an intentional act. Animals do matter to people, but on balance, they matter less than food, jobs, energy, money, and development. As long as we continue to view animals in ecosystems as irrelevant to these basic demands, animals will lose. ![Figure][2] PHOTO: NEXUS 2014/WATER FOOD CLIMATE AND ENERGY CONFERENCE If we accept that humans now shape the future of this planet, the future for existing and extirpated fauna will depend on vision as much as on science. What type of world do we want to pass on, and what role do animals have in that world? ![Figure][2] PHOTO:SUSANNAH BARR A responsible vision must include the dominating influence of people on the planet. The near future is likely to include 8 to 9 billion people, 3 billion more people in the middle class, a doubling of the terrestrial footprint of cities, and a transformation of global food and energy systems. A vision that includes a vital future for animals requires thinking beyond “restoration” and even beyond “rewilding.” To maintain the animal diversity of the present and restore the animal abundance of the past, we must place animals squarely in a world where human systems are integrated with functioning natural systems. We cannot focus on recreating the ecosystems of the past—our impacts are making this untenable in most places—but we must not give up on nature or wildness, either. To begin, we need to recognize the importance of animals in all socioecological systems, pristine and human-dominated, terrestrial and marine. When we consider the benefits of a world rich with animals, we should shift some of our focus to systems where many people depend on animals. As an example, 2.6 billion people depend on ocean animals for protein. ![Figure][2] “A vision that includes a vital future for animals requires thinking beyond ‘restoration’ and even beyond ‘rewilding.’” PHOTO: PAUL ROLLISON/FLICKR In addition, we will have to grapple with tricky issues, such as those associated with the management of novel ecosystems and species substitution. There is also the potential application of synthetic biology, but the positive and negative impacts must be fully explored. How do we reduce the risks of ecosystem-level experimentation? When considering whether to introduce a new species into a system to replace the loss of another, for example, we must weigh the consequences of no intervention against the consequences of actions taken to recover ecological function. This is not a trivial exercise, as the ecological, economic, and cultural impact of an animal within an ecosystem is dynamic, and often obscured by complex ecological dynamics, shifting baselines (what a natural system “should” be like), and changing cultural norms. A full understanding of the relevant natural history, as well as the values of the people with a stake in the outcome, will be essential to any path forward. This is not entirely new territory, as our successes and failures in biological control can serve as a guide. We cannot give up on the difficult species—the species that do not coexist well with people and require large areas for their survival. Conservation of these animals will hinge on recognition of their full value—ecological, economic, and cultural—by those with the power to protect them. A country with many large animals has as much right to development as a country without, and thus the global community must find pathways that would allow communities sharing their land with these animals to benefit from their presence. Defaunation is a global issue. A world without animals represents a loss to humanity as much as a loss to ecology. [1]: http://www.sciencemag.org/site/special/vanishing/index.xhtml [2]: pending:yes