Generalisation and specialisation in hoverfly (Syrphidae) grassland pollen transport networks revealed by DNA metabarcoding

Lucas, Andrew; Bodger, Owen; Brosi, Berry J.; Ford, Col R.; Forman, Dan W.; Greig, Carolyn; Hegarty, Matthew J.; Neyland, Penelope J.; Vere, Natasha de

doi:10.1111/1365-2656.12828

Cited by 83 publications

(90 citation statements)

References 81 publications

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“…The different approaches we used in this study reveal a quite paradoxical view of pollination and a functional complementarity into networks. On the one hand, consistent with previous findings (Banza, Belo, & Evans, ; Lucas et al, ; Tur, Vigalondo, Trøjelsgarrd, Olensen, & Traveset, ) our observations based on surveys of the occurrence of links revealed that individuals and particularly species of pollinators had large food niches (high L i and L sp ); that is, they interacted with many plant species. Individual ( i ‐sp N link ) and species (sp‐sp N link ) networks were therefore also highly generalized, regardless of R. ferrugineum density.…”

Section: Discussionsupporting

confidence: 92%

“…We investigated pollinator food niches and networks by using DNA metabarcoding data that were obtained in a previous study at the site (Pornon, Andalo, Burrus, & Escaravage, 2017). Metabarcoding has already been shown in several studies to successfully identify plant taxa in pollen mixtures (Cornman, Otto, Iwanowicz, & Pettis, 2015;Galimberti et al, 2014;Galliot et al, 2017;Lucas et al, 2018;Macgregor et al, 2019;Pornon et al, 2016;Richardson et al, 2019) at a higher taxonomic resolution than microscopy (Vamosi, Gong, Adamowicz, & Packer, 2017). A recent meta-analysis (Lamb et al, 2018) concluded on a significant quantitative positive linear relationship between the proportion of sequence reads and the proportion of species in original mixtures from very different origins (stomach contents, feces, airborne pollen, etc.).…”

Section: Introductionmentioning

confidence: 99%

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Pollinator specialization increases with a decrease in a mass‐flowering plant in networks inferred from DNA metabarcoding

Pornon

Baksay

Escaravage

et al. 2019

Ecology and Evolution

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How native mass‐flowering plants affect the specialization of insects at individual and species levels and the consequences for pollination networks have received much less attention than for mass‐flowering crops or alien species and basically remain unexplored. Using existing DNA metabarcoding data on the pollen loads of 402 flower‐visiting insects, we assessed the effects of a native mass‐flowering plant of high reward quality, the shrub Rhododendron ferrugineum, on pollination networks by investigating: (a) the food niches of individual pollinators and pollinator species and (b) the structure of individual and species networks in subalpine heathland patches with extremely contrasted densities of R. ferrugineum. Relative to its high abundance in high‐density patches, the shrub was greatly underrepresented and did not dominate individual's or species' generalized networks, rather individual and species specialization increased with a decrease in R. ferrugineum density. Furthermore, individuals of the more generalist dipteran Empididae species tended to extend exclusive interactions with rare plant species in low‐density networks. The same trend was observed in the more specialist Apidea but toward rare species in high‐density networks. Our results reveal a quite paradoxical view of pollination and a functional complementarity within networks. Niche and network indices mostly based on the occurrence of links showed that individual pollinators and pollinator species and networks were highly generalized, whereas indices of link strength revealed that species and above all individuals behave as quite strict specialists. Synthesis. Our study provides insights into the status of a native mass‐flowering plant in individual's and insect species' food niches and pollination networks. It revealed that a generalist pollinator species can be highly specialized at the individual level and how rare plant species coexisting with mass‐flowering plants may nevertheless be visited.

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Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Pollinator specialization increases with a decrease in a mass‐flowering plant in networks inferred from DNA metabarcoding

Pornon

Baksay

Escaravage

et al. 2019

Ecology and Evolution

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“…Anderson & Hubricht, , Heinrich, , Kochmer & Handel, , Morales, Dodge, & Inouye, , Makrodimos, Blionis, Krigas, & Vokou, , Craine, Wolkovich, Towne, & Kembel, ). Studies show that individuals respond to increases in floral diversity by visiting more plant species within a foraging bout (Flanagan, Mitchell, & Karron, ; Kunin, ; Lucas et al, ). However, if some bees (e.g.…”

Section: Introductionmentioning

confidence: 99%

Specialist foragers in forest bee communities are small, social or emerge early

Smith

Weinman

Gibbs

et al. 2019

Journal of Animal Ecology

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Individual pollinators that specialize on one plant species within a foraging bout transfer more conspecific and less heterospecific pollen, positively affecting plant reproduction. However, we know much less about pollinator specialization at the scale of a foraging bout compared to specialization by pollinator species. In this study, we measured the diversity of pollen carried by individual bees foraging in forest plant communities in the mid‐Atlantic United States. We found that individuals frequently carried low‐diversity pollen loads, suggesting that specialization at the scale of the foraging bout is common. Individuals of solitary bee species carried higher diversity pollen loads than did individuals of social bee species; the latter have been better studied with respect to foraging bout specialization, but account for a small minority of the world’s bee species. Bee body size was positively correlated with pollen load diversity, and individuals of polylectic (but not oligolectic) species carried increasingly diverse pollen loads as the season progressed, likely reflecting an increase in the diversity of flowers in bloom. Furthermore, the seasonal increase in pollen load diversity was stronger for bees visiting trees and shrubs than for bees visiting herbaceous plants. Overall, our results showed that both plant and pollinator species’ traits as well as community‐level patterns of flowering phenology are likely to be important determinants of individual‐level interactions in plant–pollinator communities.

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“…For instance, it is still not clear which plant species are 81 the most valuable food resources and how plant species vary in value across pollinator 82 species, over time, and in different environmental conditions. It is also not well understood 83 whether the addition of floral resources might draw pollinators away from pollinator-84 dependent crop plants (Morandin & Kremen, 2013), or whether floral enhancement will alter 85 levels of plant-target specialism, at the levels of insect species and of individual insects, 86 resulting in changes in pollination efficiency (Lucas et al, 2018;Morales & Traveset, 2008). 87 88 Therefore, a crucial technical challenge for understanding plant-pollinator interactions is a 89 method to identify and quantify the species of pollen that are consumed by pollinators.…”

mentioning

confidence: 99%

Semi-quantitative characterisation of mixed pollen samples using MinION sequencing and Reverse Metagenomics (RevMet)

Peel

Dicks

Heavens

et al. 2019

Preprint

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The ability to identify and quantify the constituent plant species that make up a mixed‐species sample of pollen has important applications in ecology, conservation, and agriculture. Recently, metabarcoding protocols have been developed for pollen that can identify constituent plant species, but there are strong reasons to doubt that metabarcoding can accurately quantify their relative abundances. A PCR‐free, shotgun metagenomics approach has greater potential for accurately quantifying species relative abundances, but applying metagenomics to eukaryotes is challenging due to low numbers of reference genomes. We have developed a pipeline, RevMet (Reverse Metagenomics) that allows reliable and semi‐quantitative characterization of the species composition of mixed‐species eukaryote samples, such as bee‐collected pollen, without requiring reference genomes. Instead, reference species are represented only by ‘genome skims’: low‐cost, low‐coverage, short‐read sequence datasets. The skims are mapped to individual long reads sequenced from mixed‐species samples using the MinION, a portable nanopore sequencing device, and each long read is uniquely assigned to a plant species. We genome‐skimmed 49 wild UK plant species, validated our pipeline with mock DNA mixtures of known composition, and then applied RevMet to pollen loads collected from wild bees. We demonstrate that RevMet can identify plant species present in mixed‐species samples at proportions of DNA ≥ 1%, with few false positives and false negatives, and reliably differentiate species represented by high versus low amounts of DNA in a sample. RevMet could readily be adapted to generate semi‐quantitative datasets for a wide range of mixed eukaryote samples. Our per‐sample costs were £90 per genome skim and £60 per pollen sample, and new versions of sequencers available now will further reduce these costs.

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Generalisation and specialisation in hoverfly (Syrphidae) grassland pollen transport networks revealed by DNA metabarcoding

Cited by 83 publications

References 81 publications

Pollinator specialization increases with a decrease in a mass‐flowering plant in networks inferred from DNA metabarcoding

Pollinator specialization increases with a decrease in a mass‐flowering plant in networks inferred from DNA metabarcoding

Specialist foragers in forest bee communities are small, social or emerge early

Semi-quantitative characterisation of mixed pollen samples using MinION sequencing and Reverse Metagenomics (RevMet)

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