Restoring plant-pollinator communities: using a network approach to monitor pollination function

This is the final version. Available from IUCN via the link in this recordEcological restoration is a common tool to mitigate the loss of species and habitats, ultimately aiming to restore ecosystem functioning. Large-scale experimental evidence is lacking, however, on whether standard management techniques, e.g. the removal of invasive alien plants, indeed restore ecosystem functions at the community level. One key ecosystem function is animal mediated pollination. Based on findings from an experimental network study on rocky outcrops (inselbergs) on the island of Mahé in the Seychelles, I present recommendations for conservation practitioners about how to incorporate a network approach into an evaluation of management effectiveness. Responses to restoration actions by plant19 pollinator communities and pollination functions lead to several conclusions regarding the resilience of native fauna and flora and ecosystem functioning. Pollination network structure appears to be directly related to the quality and resilience of pollination services, which suggests that network analysis can be used to monitor management efficacy. I present recommendations and provide advice to encourage the uptake of a network approach by conservation practitioners seeking to restore ecosystem functions.German Research Foundatio

Ecosystem restoration strengthens pollination network resilience and function.

Land degradation results in declining biodiversity and the disruption of ecosystem functioning worldwide, particularly in the tropics. Vegetation restoration is a common tool used to mitigate these impacts and increasingly aims to restore ecosystem functions rather than species diversity. However, evidence from community experiments on the effect of restoration practices on ecosystem functions is scarce. Pollination is an important ecosystem function and the global decline in pollinators attenuates the resistance of natural areas and agro-environments to disturbances. Thus, the ability of pollination functions to resist or recover from disturbance (that is, the functional resilience) may be critical for ensuring a successful restoration process. Here we report the use of a community field experiment to investigate the effects of vegetation restoration, specifically the removal of exotic shrubs, on pollination. We analyse 64 plant-pollinator networks and the reproductive performance of the ten most abundant plant species across four restored and four unrestored, disturbed mountaintop communities. Ecosystem restoration resulted in a marked increase in pollinator species, visits to flowers and interaction diversity. Interactions in restored networks were more generalized than in unrestored networks, indicating a higher functional redundancy in restored communities. Shifts in interaction patterns had direct and positive effects on pollination, especially on the relative and total fruit production of native plants. Pollinator limitation was prevalent at unrestored sites only, where the proportion of flowers producing fruit increased with pollinator visitation, approaching the higher levels seen in restored plant communities. Our results show that vegetation restoration can improve pollination, suggesting that the degradation of ecosystem functions is at least partially reversible. The degree of recovery may depend on the state of degradation before restoration intervention and the proximity to pollinator source populations in the surrounding landscape. We demonstrate that network structure is a suitable indicator for pollination quality, highlighting the usefulness of interaction networks in environmental management

Tracing coco de mer's reproductive history: Pollen and nutrient limitations reduce fecundity

This is the final version of the article. Available from Wiley Open Access via the DOI in this record.Habitat degradation can reduce or even prevent the reproduction of previously abundant plant species. To develop appropriate management strategies, we need to understand the reasons for reduced recruitment in degraded ecosystems. The dioecious coco de mer palm (Lodoicea maldivica) produces by far the largest seeds of any plant. It is a keystone species in an ancient palm forest that occurs only on two small islands in the Seychelles, yet contemporary rates of seed production are low, especially in fragmented populations. We developed a method to infer the recent reproductive history of female trees from morphological evidence present on their inflorescences. We then applied this method to investigate the effects of habitat disturbance and soil nutrient conditions on flower and fruit production. The 57 female trees in our sample showed a 19.5-fold variation in flower production among individuals over a seven-year period. Only 77.2% of trees bore developing fruits (or had recently shed fruits), with the number per tree ranging from zero to 43. Flower production was positively correlated with concentrations of available soil nitrogen and potassium and did not differ significantly between closed and degraded habitat. Fruiting success was positively correlated with pollen availability, as measured by numbers and distance of neighboring male trees. Fruit set was lower in degraded habitat than in closed forest, while the proportion of abnormal fruits that failed to develop was higher in degraded habitat. Seed size recorded for a large sample of seeds collected by forest wardens varied widely, with fresh weights ranging from 1 to 18 kg. Synthesis: Shortages of both nutrients and pollen appear to limit seed production of Lodoicea in its natural habitat, with these factors affecting different stages of the reproductive process. Flower production varies widely amongst trees, while seed production is especially low in degraded habitat. The size of seeds is also very variable. We discuss the implications of these findings for managing this ecologically and economically important species.Deutsche Forschungsgemeinschaft. Grant Number: KA 3349/2‐1. Eidgenössische Technische Hochschule Zürich. Grant Number: ETH‐37 12‐

Keeping it in the family: strong fine-scale genetic structure and inbreeding in Lodoicea maldivica, the largest-seeded plant in the world

This is the author accepted manuscript. The final version is available from Springer via the DOI in this recordThe fine-scale spatial genetic structure (FSGS) of plant populations is strongly influenced by patterns of seed dispersal. An extreme case of limited dispersal is found in the charismatic yet endangered palm Lodoicea maldivica, which produces large fruits (up to 20 kg) dispersed only by gravity. To investigate patterns of seed dispersal and FSGS in natural populations we sampled 1252 individual adults and regenerating offspring across the species’ natural range in the Seychelles archipelago, and characterised their genotypes at 12 microsatellite loci. The average dispersal distance was 8.7 ± 0.7 m. Topography had a significant effect on seed dispersal, with plants on steep slopes exhibiting the longest distances. FSGS was intense, especially in younger cohorts. Contrary to what might be expected in a dioecious species, we found high levels of inbreeding, with most neighbouring pairs of male and female trees (≤10 m) being closely related. Nonetheless, levels of genetic diversity were relatively high and similar in the various sampling areas, although these differed in disturbance and habitat fragmentation. We discuss potential trade-offs associated with maternal resource provisioning of progeny, seed dispersal and inbreeding, and consider the implications of our findings for managing this globally significant flagship species

Impacts of invasive ants on pollination of native plants are similar in invaded and restored plant communities

This is the final version. Available on open access from Elsevier via the DOI in this recordData availability: Data will be made available on request.Ants are amongst the most successful invaders worldwide and can markedly modify invaded communities through biotic interactions. Invasive ants, for example, can compete with native pollinators for resources, act as legitimate pollinators, or disrupt plant-pollinator mutualistic interactions, thereby affecting native plant reproduction. Ecological restoration aims to mitigate the impact of invasive species and restore ecological communities and ecosystem functioning. Here we investigated the combined effects of two invasive ant species, the yellow crazy ant (Anoplolepis gracilipes) and white-footed ant (Technomyrmex albipes), on the pollination and reproduction of native plants in the context of a large-scale plant community restoration experiment. We conducted ant exclusion experiments and pollinator observations to obtain data on plant reproduction and pollination of four plant species. The experiments were conducted across eight granitic inselbergs on the island of Mahé, Seychelles, four of which are undergoing restoration since 2011 and four remained as invaded control sites (unrestored). Our findings indicate that native plants on Seychelles’ inselbergs relied primarily on flying flower visitors for pollination, considering that the contribution of ants to fruit set was generally small and substantially lower than that of flying pollinators. Moreover, while flying pollinators approached flowering plants irrespective of invasive ant presence, the number of probed flowers per visit was reduced, in both restored and unrestored communities. Therefore, native plant reproduction was negatively affected by the presence of invasive ants and this effect was similar in restored and unrestored plant communities. Our research suggests that invasive ants may contribute to changes in plant communities by deterring legitimate pollinators of native plants, an impact that is unlikely to be alleviated through early stages of ecological restoration.Deutsche Forschungsgemeinschaft (DFG)Portuguese Foundation for Science and Technolog

Seed dispersal by frugivores from forest remnants promotes the regeneration of adjacent invaded forests in an oceanic island

This is the final version. Available on open access from Wiley via the DOI in this recordForest remnants often act as refuges for native plant species within a degraded and highly fragmented forest matrix. Understanding whether these native patches can function as feeding grounds for frugivores and seed sources for native plant dispersal into the surrounding forest can provide critical information on ecosystem functions on a landscape scale and guidance on forest restoration. We used a large-scale natural system of eight granitic inselbergs in the Seychelles and recorded the identity and transport direction of seeds retrieved from the droppings of mist-netted birds across an invasion gradient. We found that inselberg forest remnants are important feeding areas for frugivores, acting as a source of native propagules to the surrounding invaded forests and potentially limiting the progression of non-native plant invasion. Two dominant non-native plant species (Cinnamomum verum and Clidemia hirta) were highly integrated into the frugivores' diets, competing with native plants for dispersal services. Despite the high non-native propagule pressure, the spill-over effect of native seeds into the invaded forest seemed to have a more durable positive effect on native plant recruitment fading out with distance to the inselberg edge. Our findings illustrate that remnant forest patches can generate positive spill-over of native seeds into degraded surrounding forests through directed seed transport by frugivores. This cross-boundary transport may slow down plant invasion and contribute to the recovery of adjacent degraded ecosystems. Forest remnants and avian frugivores therefore play a key role in the maintenance of native biodiversity and act as insurance for future restoration efforts.German Research Foundation (DFG)Portuguese Foundation for Science and Technolog

Seasonal variation in impact of non‐native species on tropical seed dispersal networks

This is the final version. Available on open access from Wiley via the DOI in this recordData availability statement: Data available at the Dryad Digital Repository https://doi.org/10.5061/dryad.wm37pvmqw (Costa, Heleno, Dufrene, Huckle, Gabriel, Harrison, et al., 2022).Invasive non-native species can alter animal-mediated seed dispersal interactions and ultimately affect the stability of recipient communities. The degree of such disturbances, however, is highly variable and depends on several factors, two of which have received little attention: the relative timing of native and non-native fruiting phenologies, and the associated variation in relative resource availability across the fruiting period. Both are likely to alter plant–seed disperser interactions threatened by biological invasions. Here we investigated the impact of plant invasions on the seasonal dynamics of frugivory and seed dispersal networks across a large-scale experimental setup and a plant invasion gradient on a tropical island. We recorded fruit and frugivore abundances, and plant–frugivore interactions across eight inselbergs (i.e. rocky outcrops) with different levels of plant invasion during 10 months on the island of Mahé, Seychelles. By combining four sampling methods of plant–frugivore interactions we constructed quantitative seed dispersal networks at all sites across two 5-month seasons: the on-peak and off-peak fruiting season. Our findings showed that, by fruiting mostly synchronously with natives, non-native plants compete with natives for dispersal services, predominantly carried out by native frugivores. Variation in native seed dispersal was driven by plant invasion and seasonality. Specifically, native seed dispersal declined with the degree of invasion; dispersal frequency increased with fruit abundance more strongly during the off-peak fruiting season; and networks became increasingly specialised during off-peak. These results indicated that during the main fruiting peak seed dispersal services were saturated, which likely intensified the competition between native and non-native fruits. When resources were scarce during off-peak fruiting season, native and non-native frugivores were more selective in their fruit choice at sites dominated by non-native plants. We showed that native plant and frugivore populations and native seed dispersal interactions were more vulnerable in invaded plant communities, where non-native plants compete with natives for dispersal services potentially reducing native recruitment. As invasive non-native plants dominate many ecosystems world-wide, particularly on islands, our findings showed that controlling plant invasions in vulnerable native communities can be critical to maintain native ecosystem functions and biodiversity.German Research Foundation (DFG)Portuguese Foundation for Science and Technolog

The role of asymmetric interactions on the effect of habitat destruction in mutualistic networks

Plant-pollinator mutualistic networks are asymmetric in their interactions: specialist plants are pollinated by generalist animals, while generalist plants are pollinated by a broad involving specialists and generalists. It has been suggested that this asymmetric ---or disassortative--- assemblage could play an important role in determining the equal susceptibility of specialist and generalist plants under habitat destruction. At the core of the argument lies the observation that specialist plants, otherwise candidates to extinction, could cope with the disruption thanks to their interaction with generalist pollinators. We present a theoretical framework that supports this thesis. We analyze a dynamical model of a system of mutualistic plants and pollinators, subject to the destruction of their habitat. We analyze and compare two families of interaction topologies, ranging from highly assortative to highly disassortative ones, as well as real pollination networks. We found that several features observed in natural systems are predicted by the mathematical model. First, there is a tendency to increase the asymmetry of the network as a result of the extinctions. Second, an entropy measure of the differential susceptibility to extinction of specialist and generalist species show that they tend to balance when the network is disassortative. Finally, the disappearance of links in the network, as a result of extinctions, shows that specialist plants preserve more connections than the corresponding plants in an assortative system, enabling them to resist the disruption.Comment: 14 pages, 7 figure

Seeing through the static: the temporal dimension of plant–animal mutualistic interactions

This is the final version. Available from Wiley via the DOI in this record. Most studies of plant–animal mutualistic networks have come from a temporally static perspective. This approach has revealed general patterns in network structure, but limits our ability to understand the ecological and evolutionary processes that shape these networks and to predict the consequences of natural and human-driven disturbance on species interactions. We review the growing literature on temporal dynamics of plant–animal mutualistic networks including pollination, seed dispersal and ant defence mutualisms. We then discuss potential mechanisms underlying such variation in interactions, ranging from behavioural and physiological processes at the finest temporal scales to ecological and evolutionary processes at the broadest. We find that at the finest temporal scales (days, weeks, months) mutualistic interactions are highly dynamic, with considerable variation in network structure. At intermediate scales (years, decades), networks still exhibit high levels of temporal variation, but such variation appears to influence network properties only weakly. At the broadest temporal scales (many decades, centuries and beyond), continued shifts in interactions appear to reshape network structure, leading to dramatic community changes, including loss of species and function. Our review highlights the importance of considering the temporal dimension for understanding the ecology and evolution of complex webs of mutualistic interactions.National Science FoundationAlexander von Humboldt‐StiftungFP7 People: Marie‐Curie ActionsDeutsche ForschungsgemeinschaftDeutscher Akademischer AustauschdienstFondo para la Investigación Científica y TecnológicaHelmholtz AssociationHelmholtz‐GemeinschaftSeventh Framework Programm

Envisioning a resilient future for biodiversity conservation in the wake of the COVID-19 pandemic

This is the final version. Available on open access from Wiley via the DOI in this record. As the COVID-19 pandemic continues to affect societies across the world, the ongoing economic and social disruptions are likely to present fundamental challenges for current and future biodiversity conservation. We review the literature for outcomes of past major societal, political, economic and zoonotic perturbations on biodiversity conservation, and demonstrate the complex implications of perturbation events upon conservation efforts. Building on the review findings, we use six in-depth case studies and the emerging literature to identify positive and negative outcomes of the COVID-19 pandemic, known and anticipated, for biodiversity conservation efforts around the world. A number of similarities exist between the current pandemic and past perturbations, with experiences highlighting that the pandemic-induced declines in conservation revenue and capacity, livelihood and trade disruptions are likely to have long-lasting and negative implications for biodiversity and conservation efforts. Yet, the COVID-19 pandemic also brought about a global pause in human movement that is unique in recent history, and may yet foster long-lasting behavioural and societal changes, presenting opportunities to strengthen and advance conservation efforts in the wake of the pandemic. Enhanced collaborations and partnerships at the local level, cross-sectoral engagement, local investment and leadership will all enhance the resilience of conservation efforts in the face of future perturbations. Other actions aimed at enhancing resilience will require fundamental institutional change and extensive government and public engagement and support if they are to be realised. The pandemic has highlighted the inherent vulnerabilities in the social and economic models upon which many conservation efforts are based. In so doing, it presents an opportunity to reconsider the status quo for conservation, and promotes behaviours and actions that are resilient to future perturbation.European Union Horizon 2020Natural Environment Research Council (NERC)Darwin InitiativeFondation BertarelliThe Orangutan ProjectArcus FoundationOrangutan Appeal UKUS Fish and Wildlife Service Great Ape Conservation FundOcean Parks Conservation FoundationEuropean Outdoor Conservation Association and Global Wildlife Conservatio