Plant-animal Mutualisms Research Articles

Effects of Habitat and Fruit Scent on the Interactions between Short-tailed Fruit Bats and Piper Plants.

Piper is a mega-diverse genus of pioneer plants that contributes to the maintenance and regeneration of tropical forests. In the Neotropics, Carollia bats use olfaction to forage for Piper fruit and are a main disperser of Piper seeds via consumption and subsequent defecation during flight. In return, Piper fruits provide essential nutrients for Carollia year-round. There is evidence that the types and diversity of Piper frugivores are influenced by the primary habitat type of different Piper species (forest and gap), with forest Piper depending more on bats for seed dispersal; however, this pattern has not been tested broadly. We aimed to characterize and compare the interactions between Carollia and Piper across forested and gap habitats, and further investigate whether differences in fruit traits relevant to bat foraging (i.e., scent) could underlie differences in Carollia-Piper interactions. We collected nightly acoustic ultrasonic recordings and 24 h camera trap data in La Selva, Costa Rica across 12 species of Piper (six forest, six gap) and integrated this information with data on Carollia diet and Piper fruit scent. Merging biomonitoring modalities allowed us to characterize ecological interactions in a hierarchical manner: from general activity and presence of bats, to visitations and inspections of plants, to acquisition and consumption of fruits. We found significant differences in Carollia-Piper interactions between forested and gap habitats; however, the type of biomonitoring modality (camera trap, acoustics, diet) influenced our ability to detect these differences. Forest Piper were exclusively visited by bats, whereas gap Piper had a more diverse suite of frugivores; the annual diet of Carollia, however, is dominated by gap Piper since these plants produce fruit year-round. We found evidence that fruit scent composition significantly differs between forest and gap Piper, which highlights the possibility that bats could be using chemical cues to differentially forage for gap vs. forest Piper. By integrating studies of Piper fruit scent, plant visitation patterns, and Carollia diet composition, we paint a clearer picture of the ecological interactions between Piper and Carollia, and plant-animal mutualisms more generally.

The turnover of plant-frugivore interactions along plant range expansion: consequences for natural colonization processes.

Plant-animal mutualisms such as seed dispersal are key interactions for sustaining plant range shifts. It remains elusive whether the organization of interactions with seed dispersers is reconfigured along the expansion landscape template and, if so, whether its effects accelerate or slow colonization. Here we analyse plant-frugivore interactions in a scenario of rapid population expansion of a Mediterranean juniper. We combined network analyses with field surveys, sampling interactions between individual plants and frugivores by DNA-barcoding and phototrapping over two seasons. We assess the role of intrinsic and extrinsic intraspecific variability in shaping interactions and we estimate the individual plant contributions to the seed rain. The whole interaction network was highly structured, with a distinct set of modules including individual plants and frugivore species arranged concordantly along the expansion gradient. The modular configuration was partially shaped by individual neighbourhood context (density and fecundity) and phenotypic traits (cone size). Interaction reconfiguration resulted in a higher and more uneven propagule contribution, with most effective dispersers having a prominent role at the colonization front stand, where a distinct subset of early arriving plants dominated the seed rain. Our study offers new insights into the key role of mutualistic interactions in colonization scenarios by promoting fast plant expansion processes.

Symbiotic ant traits produce differential host-plant carbon and water dynamics in a multi-species mutualism.

Cooperative interactions may frequently be reinforced by "partner fidelity feedback," in which high- or low-quality partners drive positive feedbacks with high or low benefits for the host, respectively. Benefits of plant-animal mutualisms for plants have been quantified almost universally in terms of growth or reproduction, but these are only two of many sinks to which a host-plant allocates its resources. By investigating how partners to host-plants impact two fundamental plant resources, carbon and water, we can better characterize plant-partner fidelity and understand how plant-partner mutualisms may be modulated by resource dynamics. In Laikipia, Kenya, four ant species compete for Acacia drepanolobium host-plants. These ants differ in multiple traits, from nectar consumption to host-plant protection. Using a 5-year ant removal experiment, we compared carbon fixation, leaf water status, and stem non-structural carbohydrate concentrations for adult ant-plants with and without ant partners. Removal treatments showed that the ants differentially mediate tree carbon and/or water resources. All three ant species known to be aggressive against herbivores were linked to benefits for host-plant resources, but only the two species that defend but do not prune the host, Crematogaster mimosae and Tetraponera penzigi, increased tree carbon fixation. Of these two species, only the nectivore C. mimosae increased tree simple sugars. Crematogaster nigriceps, which defends the tree but also castrates flowers and prunes meristems, was linked only to lower tree water stress approximated by pre-dawn leaf water potential. In contrast to those defensive ants, Crematogaster sjostedti, a poor defender that displaces other ants, was linked to lower tree carbon fixation. Comparing the effects of the four ant species across control trees suggests that differential ant occupancy drives substantial differences in carbon and water supply among host trees. Our results highlight that ant partners can positively or negatively impact carbon and/or water relations for their host-plant, and we discuss the likelihood that carbon- and water-related partner fidelity feedback loops occur across ant-plant mutualisms.

Passive directed dispersal of plants by animals

Conceptual gaps and imprecise terms and definitions may obscure the breadth of plant-animal dispersal relationships involved in directed dispersal. The term 'directed' indicates predictable delivery to favourable microsites. However, directed dispersal was initially considered uncommon in diffuse mutualisms (i.e. those involving many species), partly because plants rarely influence post-removal propagule fate without specialized adaptations. This rationale implies that donor plants play an active role in directed dispersal by manipulating vector behaviour after propagule removal. However, even in most classic examples of directed dispersal, participating plants do not influence animal behaviour after propagule removal. Instead, such plants may take advantage of vector attraction to favourable plant microsites, indicating a need to expand upon current interpretations of directed dispersal. We contend that directed dispersal can emerge whenever propagules are disproportionately delivered to favourable microsites as a result of predictably skewed vector behaviour. Thus, we propose distinguishing active and passive forms of directed dispersal. In active directed dispersal, the donor plant achieves disproportionate arrival to favourable microsites by influencing vector behaviour after propagule removal. By contrast, passive directed dispersal occurs when the donor plant takes advantage of vector behaviour to arrive at favourable microsites. Whereas predictable post-removal vector behaviour is dictated by characteristics of the donor plant in active directed dispersal, characteristics of the destination dictate predictable post-removal vector behaviour in passive directed dispersal. Importantly, this passive form of directed dispersal may emerge in more plant-animal dispersal relationships because specialized adaptations in donor plants that influence post-removal vector behaviour are not required. We explore the occurrence and consequences of passive directed dispersal using the unifying generalized gravity model of dispersal. This model successfully describes vectored dispersal by incorporating the influence of the environment (i.e. attractiveness of microsites) on vector movement. When applying gravity models to dispersal, the three components of Newton's gravity equation (i.e. gravitational force, object mass, and distance between centres of mass) become analogous to propagules moving towards a location based on characteristics of the donor plant, the destination, and relocation processes. The generalized gravity model predicts passive directed dispersal in plant-animal dispersal relationships when (i) animal vectors are predictably attracted to specific destinations, (ii) animal vectors disproportionately disperse propagules to those destinations, and (iii) those destinations are also favourable microsites for the dispersed plants. Our literature search produced evidence for these three conditions broadly, and we identified 13 distinct scenarios where passive directed dispersal likely occurs because vector behaviour is predictably skewed towards favourable microsites. We discuss the wide applicability of passive directed dispersal to plant-animal mutualisms and provide new insights into the vulnerability of those mutualisms to global change.

Predation risk can modify the foraging behaviour of frugivorous carnivores: Implications of rewilding apex predators for plant-animal mutualisms.

Apex predators play key roles in food webs and their recovery can trigger trophic cascades in some ecosystems. Intra‐guild competition can reduce the abundances of smaller predators and perceived predation risk can alter their foraging behaviour thereby limiting seed dispersal by frugivorous carnivores. However, little is known about how plant–frugivore mutualisms could be disturbed in the presence of larger predators.We evaluated the top‐down effect of the regional superpredator, the Iberian lynx Lynx pardinus, on the number of visits and fruits consumed by medium‐sized frugivorous carnivores, as well as the foraging behaviour of identified individuals, by examining the consumption likelihood and the foraging time.We carried out a field experiment in which we placed Iberian pear Pyrus bourgaeana fruits beneath fruiting trees and monitored pear removal by frugivorous carnivores, both inside and outside lynx ranges. Using camera traps, we recorded the presence of the red fox Vulpes vulpes, the Eurasian badger Meles meles and the stone marten Martes foina, as well as the number of fruits they consumed and their time spent foraging.Red fox was the most frequent fruit consumer carnivore. We found there were fewer visits and less fruit consumed by foxes inside lynx ranges, but lynx presence did not seem to affect badgers. We did not observe any stone marten visits inside lynx territories. The foraging behaviour of red foxes was also altered inside lynx ranges whereby foxes were less efficient, consuming less fruit per unit of time and having shorter visits. Local availability of fruit resources, forest coverage and individual personality also were important variables to understand visitation and foraging in a landscape of fear.Our results show a potential trophic cascade from apex predators to primary producers. The presence of lynx can reduce frugivorous carnivore numbers and induce shifts in their feeding behaviour that may modify the seed dispersal patterns with likely consequences for the demography of many fleshy‐fruited plant species. We conclude that knowledge of the ecological interactions making up trophic webs is an asset to design effective conservation strategies, particularly in rewilding programs.

Functional roles of frugivores and plants shape hyper‐diverse mutualistic interactions under two antagonistic conservation scenarios

AbstractDisentangling the structure of plant–animal mutualisms shed light on how species are organized, and allow us to infer about resilience, specificity, and ultimately the consequences of the loss of functions to the ecosystem. Here we gathered fruit–frugivore interactions for all the major vertebrate taxa interacting with plants in two conservation states in the Brazilian Atlantic forest: a small patch and a continuous forest. Using a network approach, we identified individual roles played by vertebrates and plants, as well as the most relevant functional traits determining the network structure. The most important vertebrates in the continuous forest were the frugivorous characterized by the ability to swallow fruits containing small to large seeds, but they also were the first to be vanished from the small patch decades ago. Animal gape/gullet size, but not body mass, together with the greatest degrees of frugivory contributed to structure the conserved community. In the forest patch, where specialization degrees (in terms of number of interactions performed) were lost, small generalist birds and the only still living primate, along with small lipid‐rich fruits, were central in maintaining community structure. This study brings insights on the potential of conserved forests to hold important species‐rich interactions, at the same time that small patches count on small birds and small fruits with increased energetic rewards to maintain structuring under human degradation threats. Our results reemphasize the importance of preserving large continuous forest remnants to support important mutualistic interactions subjected to functional traits already lost in small degraded patches.Abstract in Portuguese is available with online material.

Hunting pressure modulates the composition and size structure of terrestrial and arboreal vertebrates in Amazonian forests

Overhunting is a leading contemporary driver of tropical forest wildlife loss. The absence or extremely low densities of large-bodied vertebrates disrupts plant-animal mutualisms and consequently degrades key ecosystem services. Understanding patterns of defaunation is therefore crucial given that most tropical forests worldwide are now “half-empty”. Here we investigate changes in vertebrate community composition and size structure along a gradient of marked anthropogenic hunting pressure in the Médio Juruá region of western Brazilian Amazonia. Using a novel camera trapping grid design deployed both in the understorey and the forest canopy, we estimated the aggregate biomass of several functional groups of terrestrial and arboreal species at 28 sites along the hunting gradient. Generalized linear models (GLMs) identified hunting pressure as the most important driver of aggregate biomass for game, terrestrial, and arboreal species, as well as nocturnal rodents, frugivores, and granivores. Local hunting pressure affected vertebrate community structure as shown by both GLM and ordination analyses. The size structure of vertebrate fauna changed in heavily hunted areas due to population declines in large-bodied species and apparent compensatory increases in nocturnal rodents. Our study shows markedly altered vertebrate community structure even in remote but heavily settled areas of continuous primary forest. Depletion of frugivore and granivore populations, and concomitant density-compensation by seed predators, likely affect forest regeneration in persistently overhunted tropical forests. These findings contribute to a better understanding of how cascading effects induced by historical defaunation operate, informing wildlife management policy in tropical peri-urban, rural and wilderness areas.

Nectar biosynthesis is conserved among floral and extrafloral nectaries.

Nectar is a primary reward mediating plant–animal mutualisms to improve plant fitness and reproductive success. Four distinct trichomatic nectaries develop in cotton (Gossypium hirsutum), one floral and three extrafloral, and the nectars they secrete serve different purposes. Floral nectar attracts bees for promoting pollination, while extrafloral nectar attracts predatory insects as a means of indirect protection from herbivores. Cotton therefore provides an ideal system for contrasting mechanisms of nectar production and nectar composition between different nectary types. Here, we report the transcriptome and ultrastructure of the four cotton nectary types throughout development and compare these with the metabolomes of secreted nectars. Integration of these datasets supports specialization among nectary types to fulfill their ecological niche, while conserving parallel coordination of the merocrine-based and eccrine-based models of nectar biosynthesis. Nectary ultrastructures indicate an abundance of rough endoplasmic reticulum positioned parallel to the cell walls and a profusion of vesicles fusing to the plasma membranes, supporting the merocrine model of nectar biosynthesis. The eccrine-based model of nectar biosynthesis is supported by global transcriptomics data, which indicate a progression from starch biosynthesis to starch degradation and sucrose biosynthesis and secretion. Moreover, our nectary global transcriptomics data provide evidence for novel metabolic processes supporting de novo biosynthesis of amino acids secreted in trace quantities in nectars. Collectively, these data demonstrate the conservation of nectar-producing models among trichomatic and extrafloral nectaries.

Mismatch managed? Phenological phase extension as a strategy to manage phenological asynchrony in plant–animal mutualisms

Species‐specific shifts in phenology (timing of periodic life cycle events) are occurring with climate change and are already disrupting interactions within and among trophic levels. Phenological phase duration (e.g. beginning to end of flowering) and complementarity (patterns of nonoverlap), and their responses to changing conditions, will be important determinants of species' adaptive capacity to these shifts. Evidence indicates that extension of phenological duration of mutualistic partners could buffer negative impacts that occur with phenological shifts. Therefore, we suggest that techniques to extend the length of phenological duration will contribute to management of systems experiencing phenological asynchrony. Techniques of phenological phase extension discussed include the role of abiotic heterogeneity, genetic and species diversity, and alteration of population timing. We explore these approaches with the goal of creating a framework to build adaptive capacity and address phenological asynchrony in plant–animal mutualisms under climate change.

The resource‐mediated modular structure of a non‐symbiotic ant–plant mutualism

1. Plant–animal mutualisms are key processes that influence community structure, dynamics, and function. They reflect several neutral and niche‐based mechanisms related to plant–animal interactions.2. However, the strength with which these processes influence community structure depends on functional traits that influence the interactions between mutualistic partners. In mutualisms involving plants and ants, nectar is the most common reward, and traits such as quantity and quality can affect ant species' responses by influencing their recruitment rates and aggressiveness.3. In this study, nectar traits that mediate ant–plant defensive mutualisms were manipulated to test whether resource quantity and quality affect the structure of ant–plant interaction networks. A downscaling approach was used to investigate the interaction network between ant species and individual plants of the extrafloral nectary‐bearing terrestrial orchid Epidendrum secundum.4. We found a short‐term reorganization of the ant assemblage that caused the interaction networks to become more specialised and modular in response to a more rewarding nectar gradient. Furthermore, the ant species tended to narrow their foraging range by limiting their associations to one or a few individual plants.5. This study shows that ant species' responses to variable resource traits play an important role in the structure of the ant–plant interaction network. We suggest that more rewarding nectar enhanced aggressiveness and a massive recruitment of some ant species, leading to lower niche overlap and thus a less connected and more specialised network.

Regeneration of a keystone semiarid shrub over its range in Spain: habitat degradation overrides the positive effects of plant-animal mutualisms.

Global change drivers are currently affecting semiarid ecosystems. Because these ecosystems differ from others in biotic and abiotic filters, cues for plant regeneration and management derived from elsewhere may not be applicable to semiarid ecosystems. We sought to determine the extent to which regional variation in regeneration prospects of a long-lived semiarid keystone shrub depends on anthropogenic habitat degradation, plant-animal interactions and climate determinants. We investigated the regeneration ability (via population size structure, juvenile density and juvenile/adult ratio), fruit set and seed dispersal of Ziziphus lotus in 25 localities spanning the range of its threatened habitats in Spain. We dissected the relative contribution of different regeneration determinants using multiple regression and structural equationmodelling. Population regeneration was extremely poor, and size structures were biased towards large classes and low juvenile densities and juvenile/adult ratios. Poor regeneration was often coincident with seed dispersal collapse. However, the positive effect of seed dispersal on population regeneration disappeared after considering its relationship with habitat degradation. Protected areas did have juveniles. Together, these data suggest that habitat degradation directly impacts juvenile establishment. Our results provide insights into habitat and species management at the regional level. Z.lotus populations are currently driven by persistence-based dynamics through the longevity of the species. Nonetheless, collapsed seed dispersal, poor regeneration and the removal of adults from their habitats forecast extinction of Z.lotus in many remnants. The extreme longevity of Z.lotus provides opportunities for recovery of its populations and habitats through effective enforcement of regulations.

Elevated atmospheric carbon dioxide concentrations promote ant tending of aphids.

Animal mutualisms, which involve beneficial interactions between individuals of different species, are common in nature. Insect-insect mutualism, for example, is widely regarded as a keystone ecological interaction. Some mutualisms are anticipated to be modified by climate change, but the focus has largely been on plant-microbe and plant-animal mutualisms rather than those between animals. Ant-aphid mutualisms, whereby ants tend aphids to harvest their honeydew excretions and, in return, provide protection for the aphids, are widespread. The mutualism is heavily influenced by the quality and quantity of honeydew produced by aphids, which is directly affected by host plant quality. As predicted increases in concentrations of atmospheric carbon dioxide (eCO2 ) are widely reported to affect plant nutritional chemistry, this may also alter honeydew quality and hence the nature of ant-aphid mutualisms. Using glasshouse chambers and field-based open-top chambers, we determined the effect of eCO2 on the growth and nutritional quality (foliar amino acids) of lucerne (Medicago sativa). We determined how cowpea aphid (Aphis craccivora) populations and honeydew production were impacted when feeding on such plants and how this affected the tending behaviour of ants (Iridomyrmex sp.). eCO2 stimulated plant growth but decreased concentrations of foliar amino acids by 29% and 14% on aphid-infested plants and aphid-free plants, respectively. Despite the deterioration in host plant quality under eCO2 , aphids maintained performance and populations were unchanged by eCO2 . Aphids induced higher concentrations of amino acids (glutamine, asparagine, glutamic acid and aspartic acid) important for endosymbiont-mediated synthesis of essential amino acids. Aphids feeding under eCO2 also produced over three times more honeydew than aphids feeding under ambient CO2 , suggesting they were imbibing more phloem sap at eCO2 . The frequency of ant tending of aphids more than doubled in response to eCO2 . To our knowledge, this is the first study to demonstrate the effects of atmospheric change on an ant-aphid mutualism. In particular, these results highlight how impending changes to concentrations of atmospheric CO2 may alter mutualistic behaviour between animals. These could include positive impacts, as reported here, shifts from mutualism to antagonism, partner switches and mutualism abandonment.

An ant-plant mutualism through the lens of cGMP-dependent kinase genes.

In plant-animal mutualisms, how an animal forages often determines how much benefit its plant partner receives. In many animals, foraging behaviour changes in response to foraging gene expression or activation of the cGMP-dependent protein kinase (PKG) that foraging encodes. Here, we show that this highly conserved molecular mechanism affects the outcome of a plant-animal mutualism. We studied the two PKG genes of Allomerus octoarticulatus, an Amazonian ant that defends the ant-plant Cordia nodosa against herbivores. Some ant colonies are better 'bodyguards' than others. Working in the field in Peru, we found that colonies fed with a PKG activator recruited more workers to attack herbivores than control colonies. This resulted in less herbivore damage. PKG gene expression in ant workers correlated with whether an ant colony discovered an herbivore and how much damage herbivores inflicted on leaves in a complex way; natural variation in expression levels of the two genes had significant interaction effects on ant behaviour and herbivory. Our results suggest a molecular basis for ant protection of plants in this mutualism.

Seed dispersal by macaws shapes the landscape of an Amazonian ecosystem

Seed dispersal is one of the most studied plant–animal mutualisms. It has been proposed that the dispersal of many large-seeded plants from Neotropical forests was primarily conducted by extinct megafauna, and currently by livestock. Parrots can transport large fruits using their beaks, but have been overlooked as seed dispersers. We demonstrate that three macaws (Ara ararauna, A. glaucogularis and A. severus) are the main dispersers of the large-seeded motacú palm Attalea princeps, which is the biomass-dominant tree in the Bolivian Amazonian savannas. Macaws dispersed fruits at high rates (75–100% of fruits) to distant (up to 1200 m) perching trees, where they consumed the pulp and discarded entire seeds, contributing to forest regeneration and connectivity between distant forests islands. The spatial distribution of immature palms was positively associated to the proximity to macaws’ perching trees and negatively to the proximity to cattle paths. The disperser role of livestock, presumably a substitute for extinct megafauna, had little effect due to soil compaction, trampling and herbivory. Our results underscore the importance of macaws as legitimate, primary dispersers of large-seeded plants at long distances and, specifically, their key role in shaping the landscape structure and functioning of this Amazonian biome.

The geographic distribution of seed-dispersal mutualisms in North America

It is often difficult to determine the relative importance of different sorts of species interactions in shaping community structure or how communities function because we lack basic information on patterns of occurrence of biotic interactions. Here we determine the geographic distribution of seed-dispersal mutualisms across North America, and then test the hypotheses that those patterns are correlated with mean annual precipitation and latitude. We analyze the floras of 197 sites across North America to identify which species of native seed plants are dispersed by animals in one of three types of plant-animal mutualisms: frugivory, scatter hoarding, and ants. We identified 1655 plant species that are involved in these seed-dispersal mutualisms. 16.5 ± 6.5% of all seed plants across North America are dispersed by animals; 10.0 ± 4.2% by frugivores, 3.7 ± 1.7% by scatter hoarders, and 3.9 ± 2.2% by ants. Secondary dispersal by a different mode and vector (e.g., wind dispersal followed by scatter hoarding, or ballistic dispersal followed by myrmecochory) occurred in 16.8% of all plant mutualist records. Although each mode of dispersal showed a different pattern, the prevalence of seed-dispersal mutualisms increased with mean annual precipitation. The prevalence of seed dispersal by frugivory and scatter-hoarding decreased with increasing latitude. The prevalence of seed-dispersal interactions varies dramatically across North America. The center of greatest diversity for all three types of seed-dispersal mutualisms is the eastern United States, roughly coincident with the eastern deciduous forest. Knowing the distribution of species interactions improves our understanding of how the structure and functioning of communities varies across environmental gradients.

A general framework for effectiveness concepts in mutualisms.

A core interest in studies of mutualistic interactions is the 'effectiveness' of mutualists in providing benefits to their partners. In plant-animal mutualisms it is widely accepted that the total effect of a mutualist on its partner is estimated as (1) a 'quantity' component multiplied by (2) a 'quality' component, although the meanings of 'effectiveness,' 'quantity,' and 'quality' and which terms are applied to these metrics vary greatly across studies. In addition, a similar quantity×quality=total effect approach has not been applied to other types of mutualisms, although it could be informative. Lastly, when a total effect approach has been applied, it has invariably been from a phytocentric perspective, focussing on the effects of animal mutualists on their plant partner. This lack of a common framework of 'effectiveness' of mutualistic interactions limits generalisation and the development of a broader understanding of the ecology and evolution of mutualisms. In this paper, we propose a general framework and demonstrate its utility by applying it to both partners in five different types of mutualisms: pollination, seed dispersal, plant protection, rhizobial, and mycorrhizal mutualisms. We then briefly discuss the flexibility of the framework, potential limitations, and relationship to other approaches.

An invasive slug exploits an ant-seed dispersal mutualism.

Plant-animal mutualisms, such as seed dispersal, are often vulnerable to disruption by invasive species. Here, we show for the first time how a non-ant invasive species negatively affects seed dispersal by ants. We examined the effects of several animal species that co-occur in a temperate deciduous forest-including native and invasive seed-dispersing ants (Aphaenogaster rudis and Myrmica rubra, respectively), an invasive slug (Arion subfuscus), and native rodents-on a native myrmecochorous plant, Asarum canadense. We experimentally manipulated ant, slug, and rodent access to seed depots and measured seed removal. We also video-recorded depots to determine which other taxa interact with seeds. We found that A. rudis was the main disperser of seeds and that A. subfuscus consumed elaiosomes without dispersing seeds. Rodent visitation was rare, and rodent exclusion had no significant effect on seed or elaiosome removal. We then used data obtained from laboratory and field mesocosm experiments to determine how elaiosome robbing by A. subfuscus affects seed dispersal by A. rudis and M. rubra. We found that elaiosome robbing by slugs reduced seed dispersal by ants, especially in mesocosms with A. rudis, which picks up seeds more slowly than M. rubra. Taken together, our results show that elaiosome robbing by an invasive slug reduces seed dispersal by ants, suggesting that invasive slugs can have profound negative effects on seed dispersal mutualisms.

Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests

Tropical forests are the global cornerstone of biological diversity, and store 55% of the forest carbon stock globally, yet sustained provisioning of these forest ecosystem services may be threatened by hunting-induced extinctions of plant-animal mutualisms that maintain long-term forest dynamics. Large-bodied Atelinae primates and tapirs in particular offer nonredundant seed-dispersal services for many large-seeded Neotropical tree species, which on average have higher wood density than smaller-seeded and wind-dispersed trees. We used field data and models to project the spatial impact of hunting on large primates by ∼ 1 million rural households throughout the Brazilian Amazon. We then used a unique baseline dataset on 2,345 1-ha tree plots arrayed across the Brazilian Amazon to model changes in aboveground forest biomass under different scenarios of hunting-induced large-bodied frugivore extirpation. We project that defaunation of the most harvest-sensitive species will lead to losses in aboveground biomass of between 2.5-5.8% on average, with some losses as high as 26.5-37.8%. These findings highlight an urgent need to manage the sustainability of game hunting in both protected and unprotected tropical forests, and place full biodiversity integrity, including populations of large frugivorous vertebrates, firmly in the agenda of reducing emissions from deforestation and forest degradation (REDD+) programs.

Scale‐dependent responses of pollination and seed dispersal mutualisms in a habitat transformation scenario

Summary Transformed habitats are the result of deliberate replacement of native species by an exotic monoculture, involving changes in biotic and abiotic conditions. Despite the fact that transformed habitats are becoming more common and constitute a major biodiversity change driver, little is known about the scale‐dependent responses of plant–animal mutualisms. Aiming to test the multiscale responses of pollination and seed dispersal in a habitat transformation scenario, we examined a gradient of native and transformed habitats at three spatial scales (0–50, 50–100 and 100–250 m) and focused on a highly specialized mutualistic system composed of a hemiparasitic mistletoe (Tristerix corymbosus) that is almost exclusively pollinated by a hummingbird (Sephanoides sephaniodes) and dispersed by an arboreal marsupial (Dromiciops gliroides). Even though mistletoes were found along the gradient, they were more abundant and more densely aggregated when the transformed habitat was dominant. Disperser and pollinator activity also increased as the transformed habitat becomes dominant, at the scale of 0–50 and 50–100 m, respectively. Furthermore, crop size and disperser activity covaried at broad and intermediate scales, whereas recruitment covaried at intermediate and fine scales. Moreover, disperser activity and the number of seedlings were spatially associated, stressing D. gliroides’ role in the recruitment of the mistletoe. Synthesis. This highly specialized mutualistic system seems to be responding positively to the habitat structure modifications associated with Eucalyptus plantations. However, the actual costs (e.g. reduced gene flow, increased herbivory) in these transformed habitats are yet to be assessed.

Are flowers red in teeth and claw? Exploitation barriers and the antagonist nature of mutualisms

The romantic perception of plant–animal mutualisms as a cooperative endeavour has been shattered in the last decades. While the classic theory of plant–pollinator coevolution assumed that partner coevolution is largely mutualistic, an increasing appreciation of the inherent conflict of interests between such partners has led to the realization that genes that confer a reproductive advantage to plants may have negative effects on their pollinators (and vice versa), giving rise to an apparent paradox: that antagonistic processes may drive coevolution among mutualistic partners. Under this new paradigm, mutualistic partners are bound by mutual interest but shaped by “selfish” antagonistic processes. Exploitation barriers mediated by resource competition among pollinators are a key element of this paradigm. Exploitation barriers involve traits such as tubular corollas, red flowers, toxic or deterrent rewards, and attractants of floral predators. Exploitation barriers result in resource partitioning, increasing floral fidelity of favoured pollinators and therefore plant fitness; but they often entail a physiological, behavioural or developmental cost for such favoured pollinators. Resource partitioning mediated by exploitation barriers is a very powerful driver of floral diversification, robust to variation in pollinator assemblages; hence, it may contribute to elucidating the occurrence of co-evolutionary changes in multi-species contexts. Exploitation barriers provide also a mechanistic basis for trait-based modelling of interaction networks, and represent a reason for caution in assuming fixed interaction identity or strength when modelling such networks (e.g. in rarefaction procedures used to estimate secondary extinctions). We propose to replace the misleading metaphor that depicts flowers and pollinators as cooperative partners by a metaphor in which plants and pollinator are traders, seeking to obtain different services from each other in complete disregard for the benefit of their mutualistic partner.