Predicting plant-pollinator interactions: concepts, methods, and challenges.

Plant-pollinator interactions are ecologically and economically important, and, as a result, their prediction is a crucial theoretical and applied goal for ecologists. Although various analytical methods are available, we still have a limited ability to predict plant-pollinator interactions. The predictive ability of different plant-pollinator interaction models depends on the specific definitions used to conceptualize and quantify species attributes (e.g., morphological traits), sampling effects (e.g., detection probabilities), and data resolution and availability. Progress in the study of plant-pollinator interactions requires conceptual and methodological advances concerning the mechanisms and species attributes governing interactions as well as improved modeling approaches to predict interactions. Current methods to predict plant-pollinator interactions present ample opportunities for improvement and spark new horizons for basic and applied research.

Mate-choice for close kin is associated with improved offspring survival in Lodoicea maldivica, the largest-seeded plant in the world.

We studied spatial patterns of kinship in the offspring of the endangered Lodoicea maldivica, a dioecious palm that produces the largest seed of any plant. Previous research has suggested that restricted seed and pollen dispersal in populations resulted in strong spatial genetic structure. We used microsatellites to genotype young plants and their potential parents at four sites across the species' entire natural range. We determined the most likely parents of each young plant based on the spatial separation of each parent pair, their genetic relatedness, and the level of correlated paternity. We identified both parents (43 female, 54 male) for 139 of 493 young plants. Mean distance between parental pairs was 26.8 m. Correlated paternity was low (0.168), indicating that mother trees were often pollinated by several fathers. Parental pairs were more closely related than expected by chance, suggesting outbreeding depression. Our results highlight the apparent strong mate choice for close kin in parent pairs of surviving offspring. We discuss the alternative biological processes that could lead to this, including the potential for break-up of favourable allelic combinations necessary for the development of the palm's very large seed. Management implications include germinating seeds where they naturally fall, using a diverse range of male plants as pollen donors for hand pollination, and protecting the native community of gecko pollinators.

Rapid monitoring of ecological persistence.

Effective conservation of ecological communities requires accurate and up-to-date information about whether species are persisting or declining to extinction. The persistence of an ecological community is supported by its underlying network of species interactions. While the persistence of the network supporting the whole community is the most relevant scale for conservation, in practice, only small subsets of these networks can be monitored. There is therefore an urgent need to establish links between the small snapshots of data conservationists can collect, and the "big picture" conclusions about ecosystem health demanded by policymakers, scientists, and societies. Here, we show that the persistence of small subnetworks (motifs) in isolation-that is, their persistence when considered separately from the larger network of which they are a part-is a reliable probabilistic indicator of the persistence of the network as a whole. Our methods show that it is easier to detect if an ecological community is not persistent than if it is persistent, allowing for rapid detection of extinction risk in endangered systems. Our results also justify the common practice of predicting ecological persistence from incomplete surveys by simulating the population dynamics of sampled subnetworks. Empirically, we show that our theoretical predictions are supported by data on invaded networks in restored and unrestored areas, even in the presence of environmental variability. Our work suggests that coordinated action to aggregate information from incomplete sampling can provide a means to rapidly assess the persistence of entire ecological networks and the expected success of restoration strategies.

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

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. A free Plain Language Summary can be found within the Supporting Information of this article.

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

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.

Pollination effectiveness of specialist and opportunistic nectar feeders influenced by invasive alien ants in the Seychelles.

PREMISE: Opportunistic nectar-feeders may act as effective pollinators; nonetheless, we still lack information on whether these opportunistic species differ in their pollination effectiveness from specialized nectarivorous vertebrates and insects. Many nectar specialists have coevolved with the plants on which they feed; therefore, we would expect higher pollination effectiveness in specialists than in opportunistic feeders. Here, we assessed quantity and quality components of pollination effectiveness in specialist and opportunistic vertebrate nectarivores and insects, focusing on three plants from the Seychelles: Thespesia populnea, Polyscias crassa, and Syzygium wrightii. METHODS: We determined the quantity component (QNC) of pollination effectiveness with pollinator observations, and the quality component (QLC) by measuring fruit and seed set resulting from single visits by each pollinator. To detect potential negative effects of invasive ants on native plant-pollinator interactions, we classified pollinator visits (quantity component) as disturbed (>6 ants/30 min) vs. undisturbed. RESULTS: All focal plants were visited by insects, and vertebrate specialist and opportunist nectarivores, yet their pollination effectiveness differed. Flying insects were the most effective pollinators of T. populnea. The other two plants were most effectively pollinated by vertebrates; i.e., sunbirds (nectar specialists) in S. wrightii and Phelsuma geckos (nectar opportunists) in P. crassa, despite marked variation in QNC and QLC. Ant presence was associated with lower pollinator visitation rate in P. crassa and S. wrightii. CONCLUSIONS: Our study highlights the importance of all pollinator guilds, including opportunist nectarivorous vertebrates as pollinators of island plants, and the vulnerability of such interactions to disruption by nonnative species.

Identification of sex-linked markers in the sexually cryptic coco de mer: are males and females produced in equal proportions?

Lodoicea maldivica (coco de mer) is a long-lived dioecious palm in which male and female plants are visually indistinguishable when immature, only becoming sexually dimorphic as adults, which in natural forest can take as much as 50 years. Most adult populations in the Seychelles exhibit biased sex ratios, but it is unknown whether this is due to different proportions of male and female plants being produced or to differential mortality. In this study, we developed sex-linked markers in Lodoicea using ddRAD sequencing, enabling us to reliably determine the gender of immature individuals. We screened 589 immature individuals to explore sex ratios across life stages in Lodoicea. The two sex-specific markers resulted in the amplification of male-specific bands (Lm123977 at 405 bp and Lm435135 at 130 bp). Our study of four sub-populations of Lodoicea on the islands of Praslin and Curieuse revealed that the two sexes were produced in approximately equal numbers, with no significant deviation from a 1:1 ratio before the adult stage. We conclude that sex in Lodoicea is genetically determined, suggesting that Lodoicea has a chromosomal sex determination system in which males are the heterogametic sex (XY) and females are homogametic (XX). We discuss the potential causes for observed biased sex ratios in adult populations, and the implications of our results for the life history, ecology and conservation management of Lodoicea.

The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study.

Background and Aims: Large clades of angiosperms are often characterized by diverse interactions with pollinators, but how these pollination systems are structured phylogenetically and biogeographically is still uncertain for most families. Apocynaceae is a clade of >5300 species with a worldwide distribution. A database representing >10 % of species in the family was used to explore the diversity of pollinators and evolutionary shifts in pollination systems across major clades and regions. Methods: The database was compiled from published and unpublished reports. Plants were categorized into broad pollination systems and then subdivided to include bimodal systems. These were mapped against the five major divisions of the family, and against the smaller clades. Finally, pollination systems were mapped onto a phylogenetic reconstruction that included those species for which sequence data are available, and transition rates between pollination systems were calculated. Key Results: Most Apocynaceae are insect pollinated with few records of bird pollination. Almost three-quarters of species are pollinated by a single higher taxon (e.g. flies or moths); 7 % have bimodal pollination systems, whilst the remaining approx. 20 % are insect generalists. The less phenotypically specialized flowers of the Rauvolfioids are pollinated by a more restricted set of pollinators than are more complex flowers within the Apocynoids + Periplocoideae + Secamonoideae + Asclepiadoideae (APSA) clade. Certain combinations of bimodal pollination systems are more common than others. Some pollination systems are missing from particular regions, whilst others are over-represented. Conclusions: Within Apocynaceae, interactions with pollinators are highly structured both phylogenetically and biogeographically. Variation in transition rates between pollination systems suggest constraints on their evolution, whereas regional differences point to environmental effects such as filtering of certain pollinators from habitats. This is the most extensive analysis of its type so far attempted and gives important insights into the diversity and evolution of pollination systems in large clades.

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

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.

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.

Development of 12 polymorphic microsatellite loci for the endangered Seychelles palm Lodoicea maldivica (Arecaceae).

PREMISE OF THE STUDY: The evolutionarily and ecologically distinct coco de mer palm Lodoicea maldivica (Arecaceae) is endemic to two islands in the Seychelles. Before colonization of the islands by man, the endangered palm formed large monodominant stands, but its natural range is now restricted to four main populations and several patches of isolated individuals. Microsatellite markers were designed to investigate the genetic structure of the remaining natural populations of L. maldivica. METHODS AND RESULTS: We developed 12 polymorphic and three monomorphic microsatellite markers for this species, with a mean number of alleles per locus of 13.2 (range 5-21) and expected heterozygosity values ranging from 0.31-0.91 for the polymorphic loci. CONCLUSIONS: These markers enable us to study the patterns of genetic diversity, contemporary seed dispersal, and the fine-scale spatial genetic structure of this important conservation flagship species.

Integrating network ecology with applied conservation: a synthesis and guide to implementation.

Ecological networks are a useful tool to study the complexity of biotic interactions at a community level. Advances in the understanding of network patterns encourage the application of a network approach in other disciplines than theoretical ecology, such as biodiversity conservation. So far, however, practical applications have been meagre. Here we present a framework for network analysis to be harnessed to advance conservation management by using plant-pollinator networks and islands as model systems. Conservation practitioners require indicators to monitor and assess management effectiveness and validate overall conservation goals. By distinguishing between two network attributes, the 'diversity' and 'distribution' of interactions, on three hierarchical levels (species, guild/group and network) we identify seven quantitative metrics to describe changes in network patterns that have implications for conservation. Diversity metrics are partner diversity, vulnerability/generality, interaction diversity and interaction evenness, and distribution metrics are the specialization indices d' and [Formula: see text] and modularity. Distribution metrics account for sampling bias and may therefore be suitable indicators to detect human-induced changes to plant-pollinator communities, thus indirectly assessing the structural and functional robustness and integrity of ecosystems. We propose an implementation pathway that outlines the stages that are required to successfully embed a network approach in biodiversity conservation. Most importantly, only if conservation action and study design are aligned by practitioners and ecologists through joint experiments, are the findings of a conservation network approach equally beneficial for advancing adaptive management and ecological network theory. We list potential obstacles to the framework, highlight the shortfall in empirical, mostly experimental, network data and discuss possible solutions.

The nutrient economy of Lodoicea maldivica, a monodominant palm producing the world's largest seed.

The iconic Lodoicea maldivica palm appears to invest heavily in reproduction, with females bearing the world's largest seeds and males producing copious pollen. We asked how these palms, which grow in extremely poor soils, obtain sufficient nutrients to support such high levels of reproductive function. Our study site was the Vallée de Mai UNESCO Site on Praslin, Seychelles. We measured the trees' allocations of dry matter, nitrogen (N) and phosphorus (P) to aboveground growth and reproduction, quantified stemflow and throughfall, and measured availabilities of N and P in the soil. We show that the nutrient costs of reproduction are very high in male and female plants, and for P far exceed those of vegetative growth. We describe how the palm leaves form a huge funnel that intercepts particulate material, especially pollen, which is flushed to the base of the trunk when it rains. In this way, Lodoicea improves its nutrient supply and that of its dispersal-limited offspring. Lodoicea shares many functional characteristics with dominant trees of other monodominant forests in the humid tropics. It also exhibits unique features, including its huge seed, effective funnelling mechanism and diverse community of closely associated animals, suggesting a long evolutionary history under relatively stable conditions.

Genetic connectivity of the moth pollinated tree Glionnetia sericea in a highly fragmented habitat.

Long-distance gene flow is thought to be one prerequisite for the persistence of plant species in fragmented environments. Human influences have led to severe fragmentation of native habitats in the Seychelles islands, with many species surviving only in small and isolated populations. The endangered Seychelles endemic tree Glionnetia sericea is restricted to altitudes between 450 m and 900 m where the native forest vegetation has been largely lost and replaced with exotic invasives over the last 200 years. This study explores the genetic and ecological consequences of population fragmentation in this species by analysing patterns of genetic diversity in a sample of adults, juveniles and seeds, and by using controlled pollination experiments. Our results show no decrease in genetic diversity and no increase in genetic structuring from adult to juvenile cohorts. Despite significant inbreeding in some populations, there is no evidence of higher inbreeding in juvenile cohorts relative to adults. A Bayesian structure analysis and a tentative paternity analysis indicate extensive historical and contemporary gene flow among remnant populations. Pollination experiments and a paternity analysis show that Glionnetia sericea is self-compatible. Nevertheless, outcrossing is present with 7% of mating events resulting from pollen transfer between populations. Artificial pollination provided no evidence for pollen limitation in isolated populations. The highly mobile and specialized hawkmoth pollinators (Agrius convolvuli and Cenophodes tamsi; Sphingidae) appear to promote extensive gene flow, thus mitigating the potential negative ecological and genetic effects of habitat fragmentation in this species. We conclude that contemporary gene flow is sufficient to maintain genetic connectivity in this rare and restricted Seychelles endemic, in contrast to other island endemic tree species with limited contemporary gene flow.

The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness.

Co-flowering plant species commonly share flower visitors, and thus have the potential to influence each other's pollination. In this study we analysed 750 quantitative plant-pollinator networks from 28 studies representing diverse biomes worldwide. We show that the potential for one plant species to influence another indirectly via shared pollinators was greater for plants whose resources were more abundant (higher floral unit number and nectar sugar content) and more accessible. The potential indirect influence was also stronger between phylogenetically closer plant species and was independent of plant geographic origin (native vs. non-native). The positive effect of nectar sugar content and phylogenetic proximity was much more accentuated for bees than for other groups. Consequently, the impact of these factors depends on the pollination mode of plants, e.g. bee or fly pollinated. Our findings may help predict which plant species have the greatest importance in the functioning of plant-pollination networks.

Specialization of mutualistic interaction networks decreases toward tropical latitudes.

Species-rich tropical communities are expected to be more specialized than their temperate counterparts. Several studies have reported increasing biotic specialization toward the tropics, whereas others have not found latitudinal trends once accounting for sampling bias or differences in plant diversity. Thus, the direction of the latitudinal specialization gradient remains contentious. With an unprecedented global data set, we investigated how biotic specialization between plants and animal pollinators or seed dispersers is associated with latitude, past and contemporary climate, and plant diversity. We show that in contrast to expectation, biotic specialization of mutualistic networks is significantly lower at tropical than at temperate latitudes. Specialization was more closely related to contemporary climate than to past climate stability, suggesting that current conditions have a stronger effect on biotic specialization than historical community stability. Biotic specialization decreased with increasing local and regional plant diversity. This suggests that high specialization of mutualistic interactions is a response of pollinators and seed dispersers to low plant diversity. This could explain why the latitudinal specialization gradient is reversed relative to the latitudinal diversity gradient. Low mutualistic network specialization in the tropics suggests higher tolerance against extinctions in tropical than in temperate communities.

The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour.

Species extinctions pose serious threats to the functioning of ecological communities worldwide. We used two qualitative and quantitative pollination networks to simulate extinction patterns following three removal scenarios: random removal and systematic removal of the strongest and weakest interactors. We accounted for pollinator behaviour by including potential links into temporal snapshots (12 consecutive 2-week networks) to reflect mutualists' ability to 'switch' interaction partners (re-wiring). Qualitative data suggested a linear or slower than linear secondary extinction while quantitative data showed sigmoidal decline of plant interaction strength upon removal of the strongest interactor. Temporal snapshots indicated greater stability of re-wired networks over static systems. Tolerance of generalized networks to species extinctions was high in the random removal scenario, with an increase in network stability if species formed new interactions. Anthropogenic disturbance, however, that promote the extinction of the strongest interactors might induce a sudden collapse of pollination networks.

Indirect interactions between invasive and native plants via pollinators.

In generalised pollination systems, the presence of alien plant species may change the foraging behaviour of pollinators on native plant species, which could result in reduced reproductive success of native plant species. We tested this idea of indirect interactions on a small spatial and temporal scale in a field study in Mauritius, where the invasive strawberry guava, Psidium cattleianum, provides additional floral resources for insect pollinators. We predicted that the presence of flowering guava would indirectly and negatively affect the reproductive success of the endemic plant Bertiera zaluzania, which has similar flowers, by diverting shared pollinators. We removed P. cattleianum flowers within a 5-m radius from around half the B. zaluzania target plants (treatment) and left P. cattleianum flowers intact around the other half (control). By far, the most abundant and shared pollinator was the introduced honey bee, Apis mellifera, but its visitation rates to treatment and control plants were similar. Likewise, fruit and seed set and fruit size and weight of B. zaluzania were not influenced by the presence of P. cattleianum flowers. Although other studies have shown small-scale effects of alien plant species on neighbouring natives, we found no evidence for such negative indirect interactions in our system. The dominance of introduced, established A. mellifera indicates their replacement of native insect flower visitors and their function as pollinators of native plant species. However, the pollination effectiveness of A. mellifera in comparison to native pollinators is unknown.