Insights from plant reproductive trade-offs and plant-pollinator interactions at contrasting ecological scales - Dataset
The dataset consists of information compiled on 17 reproductive traits for more than 1506 flowering plants from 64 plant-pollinator networks distributed across the globe to explore plant reproductive trade-offs and how they influence interactions with floral visitors.
The dataset is arranged by chapter and consists of:
Chapter 1 Reproductive traits. Raw data of this chapters is in the path "Data/Trait_data_raw/".
Chapter 2 Functionalmotifs. This chapter uses the same raw data as chapter 1 and is in the same path on this folder ""Data/Trait_data_raw/".
Chapter 3 Hp_pollen_experiment. Raw data to produce this chapter is in two different folders, "Data/species_seed_set" (all files, the data reported there is per species, n=10) and "trait_all.csv" in the file path "Data/csv".
Chapter 4 Plantdiv. Raw data can be found in "Data/Csv/Data_Plantdiv.csv" and in "Data/RData/df_all.RData".
Non-bee insects are important contributors to global crop pollination
Wild and managed bees are well documented as effective pollinators of global crops of economic importance. However, the contributions by pollinators other than bees have been little explored despite their potential to contribute to crop production and stability in the face of environmental change. Non-bee pollinators include flies, beetles, moths, butterflies, wasps, ants, birds, and bats, among others. Here we focus on non-bee insects and synthesize 39 field studies from five continents that directly measured the crop pollination services provided by non-bees, honey bees, and other bees to compare the relative contributions of these taxa. Non-bees performed 25-50% of the total number of flower visits. Although non-bees were less effective pollinators than bees per flower visit, they made more visits; thus these two factors compensated for each other, resulting in pollination services rendered by non-bees that were similar to those provided by bees. In the subset of studies that measured fruit set, fruit set increased with non-bee insect visits independently of bee visitation rates, indicating that non-bee insects provide a unique benefit that is not provided by bees. We also show that non-bee insects are not as reliant as bees on the presence of remnant natural or seminatural habitat in the surrounding landscape. These results strongly suggest that non-bee insect pollinators play a significant role in global crop production and respond differently than bees to landscape structure, probably making their crop pollination services more robust to changes in land use. Non-bee insects provide a valuable service and provide potential insurance against bee population declines.
Delivery of crop pollination services is an insufficient argument for wild pollinator conservation
There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.
Covariation among reproductive traits in flowering plants shapes their interactions with pollinators
- Globally, plants display enormous variation in life-history strategies and trait combinations. However, evidence suggests that evolutionary and physiological constraints limit the number of plant ecological strategies. Although there have been recent advances in understanding correlations among plant traits, reproductive traits are rarely considered, despite their key role in shaping plant life-history strategies and interactions with pollinators.
- Here, using a global dataset of 18 reproductive traits for 1506 species, we investigate the reproductive spectrum of flowering plants to identify how it shapes interactions with pollinators.
- We show that over 50% of all trait variation is explained by the first two reproductive axes, which represent the negative correlation between flower number and flower size, and the negative correlation between autonomous selfing and floral display size. In addition, these reproductive axes were associated with the identity and number of visits of the distinct pollinator guilds. However, reproductive axes explain a relatively small amount of variance in pollinator interactions highlighting the need to incorporate other factors along with reproductive traits to fully explain large-scale patterns of plant-pollinator interactions.
- Our study identifies the major reproductive trait correlations in flowering plants and their role in shaping plant-pollinator interactions at a macro-ecological scale. These findings emphasise the importance of considering reproductive traits in the global spectrum of plant form and function, and the need to explore beyond floral morphological traits to broaden our understanding of plant-pollinator interactions.
Insights from Plant Reproductive Trade-offs and Plant-pollinator Interactions at Contrasting Ecological Scales
Global change is threatening both plant and pollinator species, leading to a rapid loss of ecological interactions. Surprisingly, our knowledge of plant reproductive ecology and plant-pollinator interactions remains largely disconnected and there is a need to better understand how plant reproductive strategies affect, and are affected by, the structure of plant-pollinator interactions. This thesis tries to progress knowledge by investigating (i) plant reproductive trade-offs; (ii) how these tradeoffs determine plant-pollinator interactions; (iii) the effects of pollinator sharing for plant reproduction; and (iv) methods to assess the state of vegetation communities, as this can influence the condition of pollinator communities.
First, I compiled information on 17 reproductive traits for more than 1506 flowering plants from 64 plant-pollinator networks distributed across the globe to explore plant reproductive trade-offs and how they influence interactions with floral visitors. Second, using 60 of these plant-pollinator networks, I examined the structural properties of network motifs (subsets of interactions) that describe both direct and indirect interactions among plants and pollinators. I then assessed over- and under-representation of the different plant and floral visitor functional groups on the distinct motif positions and position combinations. Third, I explored one of the consequences of indirect interactions, heterospecific pollen deposition on floral stigmas, by creating an experimental co-flowering community with heterogeneous traits and contrasting phylogenetic relatedness. This allowed me to investigate the impact, mechanisms and competitive structure of heterospecific pollen arrival. Finally, because plant and pollinator species interactions depend on the state of natural systems, I investigated the performance of three remotely sensed metrics (two cover metrics and one novel indicator of ecological condition) to assess the state of vegetation across environmental gradients.
Of the flowering plants recorded, two main reproductive trade-offs were evident (‘flower number - flower size’ and ‘pollinator dependence’) that explained over half of the reproductive trait variation. These plant reproductive trade-offs determined their interactions with floral visitors worldwide. The analysis of network motifs revealed that the structure of motifs in real plant-pollinator networks is non-random. Further, the different floral visitor functional groups associated with distinct motif positions describe contrasting ecological roles. Interestingly, the combination of functional groups within motifs cannot be retrieved by their observed probabilities indicating the presence of underlying ecological processes that constrain motif composition. In the experimental plant communities, heterospecific pollen deposition showed a prevailing negative effect on seed production. These impacts were mainly driven by pollen recipient traits and specific pollen recipient - pollen donor combinations of traits. In addition, the structure of pollen competition was hierarchical with clear ‘winner’ and ‘loser’ species. Lastly, the different remote sensing metrics tested to assess vegetation cover and condition indicated good performance on tree-dominated communities but they were not reliable for specific ecosystem types from arid regions.
Greater understanding of plant reproductive ecology is clearly essential to progress knowledge on the global spectrum of plant trait variation, but also to understand the structure of plant-pollinator interactions (e.g., pollination syndromes). Further, pollinator-mediated interactions among plants (e.g., competitive or facilitative processes) and the consequences for plant fitness need to be considered to disentangle the main ecological drivers of species coexistence. Finally, there is an urgent need to develop precise indices that can capture the state of vegetation for species conservation and enable better understanding of the different ecological processes that mediate plant-pollinator interactions.
A global synthesis reveals biodiversity-mediated benefits for crop production
Human land use threatens global biodiversity and compromises multiple ecosystem functions critical to food production. Whether crop yield-related ecosystem services can be maintained by a few dominant species or rely on high richness remains unclear. Using a global database from 89 studies (with 1475 locations), we partition the relative importance of species richness, abundance, and dominance for pollination; biological pest control; and final yields in the context of ongoing land-use change. Pollinator and enemy richness directly supported ecosystem services in addition to and independent of abundance and dominance. Up to 50% of the negative effects of landscape simplification on ecosystem services was due to richness losses of service-providing organisms, with negative consequences for crop yields. Maintaining the biodiversity of ecosystem service providers is therefore vital to sustain the flow of key agroecosystem benefits to society.
Linking species functional roles to their network roles
Species roles in ecological networks combine to generate their architecture, which contributes to their stability. Species trait diversity also affects ecosystem functioning and resilience, yet it remains unknown whether species' contributions to functional diversity relate to their network roles. Here, we use 21 empirical pollen transport networks to characterise this relationship. We found that, apart from a few abundant species, pollinators with original traits either had few interaction partners or interacted most frequently with a subset of these partners. This suggests that narrowing of interactions to a subset of the plant community accompanies pollinator niche specialisation, congruent with our hypothesised trade-off between having unique traits vs. being able to interact with many mutualist partners. Conversely, these effects were not detected in plants, potentially because key aspects of their flowering traits are conserved at a family level. Relating functional and network roles can provide further insight into mechanisms underlying ecosystem functioning.
Pollinator size and its consequences: Robust estimates of body size in pollinating insects
Body size is an integral functional trait that underlies pollination-related ecological processes, yet it is often impractical to measure directly. Allometric scaling laws have been used to overcome this problem. However, most existing models rely upon small sample sizes, geographically restricted sampling and have limited applicability for non-bee taxa. Allometric models that consider biogeography, phylogenetic relatedness, and intraspecific variation are urgently required to ensure greater accuracy. We measured body size as dry weight and intertegular distance (ITD) of 391 bee species (4,035 specimens) and 103 hoverfly species (399 specimens) across four biogeographic regions: Australia, Europe, North America, and South America. We updated existing models within a Bayesian mixed-model framework to test the power of ITD to predict interspecific variation in pollinator dry weight in interaction with different co-variates: phylogeny or taxonomy, sexual dimorphism, and biogeographic region. In addition, we used ordinary least squares regression to assess intraspecific dry weight ~ ITD relationships for ten bees and five hoverfly species. Including co-variates led to more robust interspecific body size predictions for both bees and hoverflies relative to models with the ITD alone. In contrast, at the intraspecific level, our results demonstrate that the ITD is an inconsistent predictor of body size for bees and hoverflies. The use of allometric scaling laws to estimate body size is more suitable for interspecific comparative analyses than assessing intraspecific variation. Collectively, these models form the basis of the dynamic R package, "pollimetry," which provides a comprehensive resource for allometric pollination research worldwide.
Native bees buffer the negative impact of climate warming on honey bee pollination of watermelon crops
If climate change affects pollinator-dependent crop production, this will have important implications for global food security because insect pollinators contribute to production for 75% of the leading global food crops. We investigate whether climate warming could result in indirect impacts upon crop pollination services via an overlooked mechanism, namely temperature-induced shifts in the diurnal activity patterns of pollinators. Using a large data set on bee pollination of watermelon crops, we predict how pollination services might change under various climate change scenarios. Our results show that under the most extreme IPCC scenario (A1F1), pollination services by managed honey bees are expected to decline by 14.5%, whereas pollination services provided by most native, wild taxa are predicted to increase, resulting in an estimated aggregate change in pollination services of +4.5% by 2099. We demonstrate the importance of native biodiversity in buffering the impacts of climate change, because crop pollination services would decline more steeply without the native, wild pollinators. More generally, our study provides an important example of how biodiversity can stabilize ecosystem services against environmental change.
Recipient and donor characteristics govern the hierarchical structure of heterospecific pollen competition networks
- Pollinator sharing can have negative consequences for plant fitness via competition for visits as well as with the arrival of heterospecific pollen. Plant traits and relatedness of donor and recipient species have been suggested to drive the observed variation in plant fitness effects of both processes, but how they shape the structure of interspecific pollen competition networks has been overlooked at the community level.
- To understand the importance of reproductive traits and relatedness to the impact of heterospecific pollen, we conducted a controlled glasshouse experiment with an artificial co-flowering community. We performed 2,200 hand pollination crosses by experimentally transferring conspecific pollen alone or with 50% and 100% foreign pollen among 10 species belonging to three different plant families.
- Relative to conspecific pollen alone, there was a significant reduction in seed set with 50% heterospecific pollen for 67% of the crosses. This effect is driven largely by recipient traits and the interaction between recipient and donor traits under specific circumstances of trait matching. In general, species with shorter styles, smaller stigmas and lower pollen:ovule ratios were more impacted by heterospecific pollen. These traits and their differences among species led to a hierarchical (or transitive) structure of pollen competition with clear winners and losers. However, phylogenetic distance among recipient and donor species did not explain the effects.
- Synthesis. Our study shows that specific traits and trait combinations between donor and recipient species are important in determining seed production outcomes with heterospecific pollen receipt. Moreover, the differences in traits between species lead to a competitive structure with clear 'winners' or 'losers' species. The results of this study highlight the importance of specific traits in understanding the position of the competitive hierarchy of the species and the mechanisms underlying heterospecific pollen impacts upon plant reproductive success.