Collapse of terrestrial mammal food webs since the Late Pleistocene.

Food webs influence ecosystem diversity and functioning. Contemporary defaunation has reduced food web complexity, but simplification caused by past defaunation is difficult to reconstruct given the sparse paleorecord of predator-prey interactions. We identified changes to terrestrial mammal food webs globally over the past ~130,000 years using extinct and extant mammal traits, geographic ranges, observed predator-prey interactions, and deep learning models. Food webs underwent steep regional declines in complexity through loss of food web links after the arrival and expansion of human populations. We estimate that defaunation has caused a 53% decline in food web links globally. Although extinctions explain much of this effect, range losses for extant species degraded food webs to a similar extent, highlighting the potential for food web restoration via extant species recovery.

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.

Accelerating homogenization of the global plant-frugivore meta-network.

Introductions of species by humans are causing the homogenization of species composition across biogeographic barriers1-3. The ecological and evolutionary consequences of introduced species derive from their effects on networks of species interactions4,5, but we lack a quantitative understanding of the impacts of introduced species on ecological networks and their biogeographic patterns globally. Here we address this data gap by analysing mutualistic seed-dispersal interactions from 410 local networks, encompassing 24,455 unique pairwise interactions between 1,631 animal and 3,208 plant species. We show that species introductions reduce biogeographic compartmentalization of the global meta-network, in which nodes are species and links are interactions observed within any local network. This homogenizing effect extends across spatial scales, decreasing beta diversity among local networks and modularity within networks. The prevalence of introduced interactions is directly related to human environmental modifications and is accelerating, having increased sevenfold over the past 75 years. These dynamics alter the coevolutionary environments that mutualists experience6, and we find that introduced species disproportionately interact with other introduced species. These processes are likely to amplify biotic homogenization in future ecosystems7 and may reduce the resilience of ecosystems by allowing perturbations to propagate more quickly and exposing disparate ecosystems to similar drivers. Our results highlight the importance of managing the increasing homogenization of ecological complexity.

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.

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.

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.

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.

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.

Measuring the demographic impact of conspecific negative density dependence.

Rare plant species often suffer stronger conspecific negative density dependence (CNDD) in studies that assess the impact of local conspecific density on individual survival. All else equal, this causes a relative disadvantage among rare species that appears inconsistent with the role of CNDD in coexistence. The resolution to this apparent paradox is for lower species abundance to decrease the frequency of conspecific interactions sufficiently to outweigh the disadvantage of stronger CNDD. Whether this occurs in natural systems is untested because existing metrics do not isolate demographic impacts of CNDD, and it is also uncertain for tropical forest trees because the greater spatial aggregation observed in rare species could cause higher frequency of conspecific interactions despite lower abundance on the landscape. We develop a new metric, effective density-dependent mortality (EDDM), to quantify the proportion of individuals that are killed by density-dependent effects. We apply EDDM to a long-term study of seed fall and recruitment at Barro Colorado Island, Panama. Rare species had stronger CNDD but lower conspecific densities, and EDDM increased with abundance. Lower abundance, thus, reduces the frequency of conspecific interaction and, consequently, mortality associated with CNDD. This mechanism allows rare species to avoid a disadvantage-when-rare that would, all else equal, result from stronger CNDD in rare species. Our work provides empirical support for a resolution to the apparently paradoxical findings that rare species experience stronger CNDD and may help reconcile contrasting findings for the relationship between the CNDD strength and abundance.

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.

The mechanical defence advantage of small seeds.

Seed size and toughness affect seed predators, and size-dependent investment in mechanical defence could affect relationships between seed size and predation. We tested how seed toughness and mechanical defence traits (tissue density and protective tissue content) are related to seed size among tropical forest species. Absolute toughness increased with seed size. However, smaller seeds had higher specific toughness both within and among species, with the smallest seeds requiring over 2000 times more energy per gram to break than the largest seeds. Investment in mechanical defence traits varied widely but independently of the toughness-mass allometry. Instead, a physical scaling relationship confers a toughness advantage on small seeds independent of selection on defence traits and without a direct cost. This scaling relationship may contribute to seed size diversity by decreasing fitness differences among large and small seeds. Allometric scaling of toughness reconciles predictions and conflicting empirical relationships between seed size and predation.

Gut passage and secondary metabolites alter the source of post-dispersal predation for bird-dispersed chili seeds.

Plants can influence the source and severity of seed predation through various mechanisms; the use of secondary metabolites for chemical defense, for example, is well documented. Gut passage by frugivores can also reduce mortality of animal-dispersed seeds, although this mechanism has gained far less attention than secondary metabolites. Apart from influencing the severity of seed predation, gut passage may also influence the source of seed predation. In Bolivia, we compared impacts of these two mechanisms, gut passage and secondary metabolites, on the source of seed predation in Capsicum chacoense, a wild chili species that is polymorphic for pungency (individual plants either produce fruits and seeds containing or lacking capsaicinoids). Using physical exclosures, we isolated seed removal by insects, mammals, and birds; seeds in the trials were from either pungent or non-pungent fruits and were either passed or not passed by seed-dispersing birds. Pungency had little influence on total short-term seed removal by animals, although prior work on this species indicates that capsaicin reduces mortality caused by fungi at longer time scales. Gut passage strongly reduced removal by insects, altering the relative impact of the three predator types. The weak impact of pungency on short-term predation contrasts with previous studies, highlighting the context dependence of secondary metabolites. The strong impact of gut passage demonstrates that this mechanism alone can influence which seed predators consume seeds, and that impacts of gut passage can be larger than those of secondary metabolites, which are more commonly acknowledged as a defense mechanism.

Multiple natural enemies cause distance-dependent mortality at the seed-to-seedling transition.

Specialised natural enemies maintain forest diversity by reducing tree survival in a density- or distance-dependent manner. Fungal pathogens, insects and mammals are the enemy types most commonly hypothesised to cause this phenomenon. Still, their relative importance remains largely unknown, as robust manipulative experiments have generally targeted a single enemy type and life history stage. Here, we use fungicide, insecticide and physical exclosure treatments to isolate the impacts of each enemy type on two life history stages (germination and early seedling survival) in three tropical tree species. Distance dependence was evident for five of six species-stage combinations, with each enemy type causing distance dependence for at least one species stage and their importance varying widely between species and stages. Rather than implicating one enemy type as the primary agent of this phenomenon, our field experiments suggest that multiple agents acting at different life stages collectively contribute to this diversity-promoting mechanism.

When condition trumps location: seed consumption by fruit-eating birds removes pathogens and predator attractants.

Seed ingestion by frugivorous vertebrates commonly benefits plants by moving seeds to locations with fewer predators and pathogens than under the parent. For plants with high local population densities, however, movement from the parent plant is unlikely to result in 'escape' from predators and pathogens. Changes to seed condition caused by gut passage may also provide benefits, yet are rarely evaluated as an alternative. Here, we use a common bird-dispersed chilli pepper (Capsicum chacoense) to conduct the first experimental comparison of escape-related benefits to condition-related benefits of animal-mediated seed dispersal. Within chilli populations, seeds dispersed far from parent plants gained no advantage from escape alone, but seed consumption by birds increased seed survival by 370% - regardless of dispersal distance - due to removal during gut passage of fungal pathogens and chemical attractants to granivores. These results call into question the pre-eminence of escape as the primary advantage of dispersal within populations and document two overlooked mechanisms by which frugivores can benefit fruiting plants.