Windborne migration amplifies insect-mediated pollination services

  1. Huiru Jia
  2. Yongqiang Liu
  3. Xiaokang Li
  4. Hui Li
  5. Yunfei Pan
  6. Chaoxing Hu
  7. Xianyong Zhou
  8. Kris AG Wyckhuys
  9. Kongming Wu

  • Curated by eLife

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    Evaluation Summary:

    Hoverflies are a group of insects that provide crucial ecosystem services such as pollination and crop protection. Their migratory behavior in western countries is well characterized, but in eastern Asia, the annual summer monsoon provides a 'highway' of favorable winds for the airborne transport of migratory organisms, and the migration of hoverflies in this large region has not been well studied. This study addresses hoverfly migration in this region and its consequences using a variety of suitable methods. The work will be of great interest to insect migration biologists and pollination ecologists.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1, Reviewer #2 and Reviewer #3 agreed to share their name with the authors.)

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Abstract

Worldwide, hoverflies (Syrphidae: Diptera) provide crucial ecosystem services such as pollination and biological pest control. Although many hoverfly species exhibit migratory behavior, the spatiotemporal facets of these movement dynamics, and their ecosystem services implications are poorly understood. In this study, we use long-term (16-year) trapping records, trajectory analysis, and intrinsic (i.e., isotope, genetic, pollen) markers to describe migration patterns of the hoverfly Episyrphus balteatus in northern China. Our work reveals how E. balteatus migrate northward during spring–summer and exhibits return (long-range) migration during autumn. The extensive genetic mixing and high genetic diversity of E. balteatus populations underscore its adaptive capacity to environmental disturbances, for example, climate change. Pollen markers and molecular gut analysis further illuminate how E. balteatus visits min. 1012 flowering plant species (39 orders) over space and time. By thus delineating E. balteatus transregional movements and pollination networks, we advance our understanding of its migration ecology and facilitate the design of targeted strategies to conserve and enhance its ecosystem services.

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  1. Version published to 10.7554/elife.76230 on eLife
  2. eLife

    Evaluation Summary:

    Hoverflies are a group of insects that provide crucial ecosystem services such as pollination and crop protection. Their migratory behavior in western countries is well characterized, but in eastern Asia, the annual summer monsoon provides a 'highway' of favorable winds for the airborne transport of migratory organisms, and the migration of hoverflies in this large region has not been well studied. This study addresses hoverfly migration in this region and its consequences using a variety of suitable methods. The work will be of great interest to insect migration biologists and pollination ecologists.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1, Reviewer #2 and Reviewer #3 agreed to share their name with the authors.)

  3. eLife

    Reviewer #1 (Public Review):

    The authors of this study conducted a long-term ecological study using a night-trap to determine how Episyrphus balteatus migrates in China. Furthermore, stable isotope analysis was used to identify the heterogeneous origins of migrant hoverflies. The authors also employed population genetics to demonstrate that hoverfly populations are not locally isolated, consequently supporting indirect migration events of E. balteatus as well. Several approaches support the same conclusion. Overall, the authors provide sufficient evidence to indicate that E balteatus migrates seasonally. It is, however, difficult to understand what the authors want to express in the later part of the manuscript (from Figure 5 to Figure 8). Lastly, it is still unclear whether hoverflies migrate at night on purpose or if other factors influenced their behavior at night.

  4. eLife

    Reviewer #2 (Public Review):

    This study of the migration ecology of the hoverfly Episyrphus balteatus is quite exceptional in both the long-term nature of the study, and in the diverse array of techniques applied to the study. The authors should be congratulated on their ambition and comprehensive approach, as in more than 20 years of research in this field I have never seen a paper with quite so many techniques used to support their conclusions. Firstly, a long-term dataset (16 years) of nightly light-trap catches from a small island in the centre of the Bohai Gulf, East China, at least 40 km from the nearest mainland, is used to explore the seasonal and annual patterns of nocturnal over-sea migratory flights of this species - the data clearly demonstrate that the species is an abundant migrant, commonly engaging in nocturnal flights over the sea. Secondly, the authors document that the migrants feed on, and frequently transport, a very diverse array of plant pollen using two complementary techniques (morphological identification of pollen grains on the body surface, and DNA barcoding of ingested pollen), which shows that this species is a very important provider of pollination services. Thirdly, the authors employ a variety of techniques to demonstrate that the hoverflies captured on the island are long-range migrants either from south of the trapping location (during the spring migration period) or from north of the trapping location (during the autumn migration period). These techniques include: (1) atmospheric trajectory simulations; (2) identification of pollen from plants only found in distant regions; (3) stable isotope analyses of wing material; and (4) population genetics.

    The authors come to three important conclusions, two of which are strongly supported by the data, but one isn't supported in my opinion. Firstly, they conclusively demonstrate that this species of hoverfly is a highly abundant, consistent, bi-directional long-range migrant which makes annual movements through East China. Their data provides very strong support for this finding, and it matches previous findings on this species in Western Europe (Wotton et al. 2019; Gao et al. 2020); it is very interesting to see similar patterns of migration at opposite ends of the Eurasian landmass. Secondly they demonstrate the importance of this species for pollination in East Asia, and their pollen analyses provide excellent support for this aspect, again confirming the previous findings from Western Europe (Wotton et al. 2019). Thirdly, they conclude that nocturnal migration is an important feature of the migration ecology of this species, something which has not been discussed elsewhere in the literature; for reasons I will explain in the more detailed comments, I do not believe their data support this third contention, and I think this part of the manuscript needs to be rewritten.

    My overall opinion of this manuscript is that it contains some highly interesting and important data which strongly support the previous studies of this species, and demonstrate that the migrations of this hoverfly are an important component of agro-ecosystem in East Asia. However, in my opinion the manuscript suffers from having too many strands, none of which are afforded the space necessary to fully explain and explore their findings. While I applaud the ambition of the authors and the extremely comprehensive nature of the study, I think there is basically too much material for a single paper. My advice would be to split the paper into at least two studies, and I provide suggestions for this in the more detailed comments to the authors.

  5. eLife

    Reviewer #3 (Public Review):

    Little known about the migration of hoverfly in eastern Asia, and this paper delineated the trans-regional movement of hoverfly in China with very solid evidences from various ways, including searchlight trapping, stable hydrogen isotope, population genetics, pollen marker and molecular gut-content. Overall, this is a wonderful work and a great example of scientific detective work to understand insect long-distance migration. Here, I provide some comments that I hope can improve the paper.

    1. "Given the substantial night-time dispersal of E. balteatus, this species possibly adopts a 'dual' migration strategy". Because Beihuang Island is an island about 44 km away from the mainland of Liaoning Province, and 60 km away from the mainland of Shandong Province. Through the distance is not much very far, it is still possible that the catches of hoverfly take daytime migration and have to continue their journey in nighttime over sea.

    2. The authors present a great deal of work, and they tried to show all results they have obtained. I think some of the result could be moved into the Supplementary Material, and some key conclusions need further explanation. For example, Figs. 6-8 are three large figures but accompanied only a very short paragraph that describes them. I think each figure could be simplified, and more description and more explanation would be welcome.

    3. The presentation of the narrative could be improved.

  6. Version published to 10.1101/2022.02.01.478668v1 on bioRxiv