Relative species abundance successfully predicts nestedness and interaction frequency of monthly pollination networks in an alpine meadow

Autoři: Lei Hu aff001;  Yuran Dong aff001;  Shucun Sun aff001
Působiště autorů: Department of Ecology, School of Life Sciences, Nanjing University, Nanjing, Jiangsu Province, China aff001;  Center for Ecological Studies, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan Province, China aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224316


Plant-pollinator networks have been repeatedly reported as cumulative ones that are described with >1 years observations. However, such cumulative networks are composed of pairwise interactions recorded at different periods, and thus may not be able to reflect the reality of species interactions in nature (e.g., early-flowering plants typically do not compete for shared pollinators with late-flowering plants, but they are assumed to do so in accumulated networks). Here, we examine the monthly sampling structure of an alpine plant-pollinator bipartite network over a two-year period to determine whether relative species abundance and species traits better explain the network structure of monthly networks than yearly ones. Although community composition and species abundance varied from one month to another, the monthly networks (as well as the yearly networks described with annual pooled data) had a highly nested structure, in which specialists directly interact with generalist partners. Moreover, relative species abundance predicted the nestedness in both the monthly and yearly networks and accounted for a statistically significant percentage of the variation (i.e., 20%-44%) in the pairwise interactions of monthly networks, but not yearly networks. The combination of relative species abundance and species traits (but not species traits only) showed a similar prediction power in terms of both network nestedness and pairwise interaction frequencies. Considering the previously recognized structural pattern and associated mechanisms of plant-pollinator networks, we propose that relative species abundance may be an important factor influencing both nestedness and interaction frequency of pollination networks.

Klíčová slova:

Flowering plants – Flowers – Plants – Pollination – Species diversity – Species interactions – Theoretical ecology – Plant-insect interactions


1. Bascompte J, Jordano P, Melián CJ, Olesen JM. The nested assembly of plant-animal mutualistic networks. Proc Nat Acad Sci. 2003; 100: 9383–9387. doi: 10.1073/pnas.1633576100 12881488

2. Olesen JM, Bascompte J, Dupont YL, Jordano P. The modularity of pollination networks. Proc Nat Acad Sci. 2007; 104: 19891–19896. doi: 10.1073/pnas.0706375104 18056808

3. Bascompte J, Jordano P, Olesen JM. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science. 2006; 312: 431–433. doi: 10.1126/science.1123412 16627742

4. Levine JM, Bascompte J, Adler PB, Allesina S. Beyond pairwise mechanisms of species coexistence in complex communities. Nature. 2017; 546: 56–64. doi: 10.1038/nature22898 28569813

5. Fortuna MA, Stouffer DB, Olesen JM, Jordano P, Mouillot D, Krasnov BR, et al. Nestedness versus modularity in ecological networks: two sides of the same coin? J Anim Ecol. 2010; 79: 811–817. doi: 10.1111/j.1365-2656.2010.01688.x 20374411

6. Ponisio LC, Gaiarsa MP, Kremen C. Opportunistic attachment assembles plant-pollinator networks. Ecol Lett. 2017; 20: 1261–1272. doi: 10.1111/ele.12821 28921857

7. Vázquez DP, Blüthgen N, Cagnolo L, Chacoff NP. Uniting pattern and process in plant–animal mutualistic networks: a review. Ann Bot. 2009; 103: 1445–1457. doi: 10.1093/aob/mcp057 19304996

8. Vázquez DP, Chacoff NP, Cagnolo L. Evaluating multiple determinants of the structure of plant-animal mutualistic networks. Ecology. 2009; 90: 2039–2046. doi: 10.1890/08-1837.1 19739366

9. Olito C, Fox JW. Species traits and abundances predict metrics of plant-pollinator network structure, but not pairwise interactions. Oikos. 2015; 124: 428–436.

10. Jordano P, Bascompte J, Olesen JM. Invariant properties in coevolutionary networks of plant–animal interactions. Ecology letters. 2003, 6: 69–81.

11. Dupont YL, Hansen DM, Olesen JM. Structure of a plant-flower-visitor network in the high-altitude sub‐alpine desert of Tenerife, Canary Islands. Ecography. 2003; 26: 301–310.

12. Lewinsohn TM, Inácio PP, Jordano P, Jordano P, Bascompte J, Olesen J. Structure in plant-animal interaction assemblages. Oikos. 2006; 113: 174–184.

13. Krishna A, Guimaraes JPR, Jordano P, Bascompte J. A neutral-niche theory of nestedness in mutualistic networks. Oikos. 2008; 117: 1609–1618.

14. Chacoff NP, Resasco J, Vázquez DP. Interaction frequency, network position, and the temporal persistence of interactions in a plant-pollinator network. Ecology. 2018; 99: 21–28. doi: 10.1002/ecy.2063 29082521

15. Canard EF, Mouquet N, Mouillot D, Stanko M, Miklisova D, Gravel D. Empirical evaluation of neutral interactions in host-parasite networks. Am Naturalist. 2014; 183: 468–479.

16. Kaiser-Bunbury CN, Vazquez DP, Stang M, Ghazoul J. Determinants of the microstructure of plant-pollinator networks. Ecology. 2014; 95: 3314–3324.

17. Machado-de-Souza T, Campos RP, Devoto M, Varassin IG. Local drivers of the structure of a tropical bird-seed dispersal network. Oecologia. 2019; 189: 421–433. doi: 10.1007/s00442-018-4322-0 30612225

18. Price MV, Waser NM, Irwin RE, Campbell DR, Brody AK. Temporal and spatial variation in pollination of a montane herb: a seven‐year study. Ecology. 2005; 86: 2106–2116.

19. Gonzalez O, Loiselle BA. Species interactions in an Andean bird-flowering plant network: phenology is more important than abundance or morphology. Peer J. 2016; 4: e2789. doi: 10.7717/peerj.2789 27994982

20. Vizentinbugoni J, Maruyama PK, Sazima M. Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird-plant network. Proc. R. Soc. B. 2014; 281(1780):86–108.

21. Fang Q, Huang SQ. Relative stability of core groups in pollination networks in a biodiversity hotspot over four years. PLoS ONE. 2012; 7: e32663. doi: 10.1371/journal.pone.0032663 22412902

22. Burkle LA, Alarcón R. The future of plant-pollinator diversity: understanding interaction networks across time, space, and global change. Amer J Bot. 2011; 98: 528–538.

23. Olesen JM, Bascompte J, Elberling H, Jordano P. Temporal dynamics in a pollination network. Ecology. 2008; 89: 1573–1582. doi: 10.1890/07-0451.1 18589522

24. Basilio AM, Medan D, Torretta JP, Bartoloni NJ. A year-long plant-pollinator network. Austral Ecol. 2006; 31: 975–983.

25. Li G, Liu Y, Frelich LE, Sun S. Experimental warming induces degradation of a Tibetan alpine meadow through trophic interactions. J Appl Ecol. 2011; 48: 659–667.

26. Xi X, Dong Y, Tian X, Xu H, Zhou Q, Niklas KJ, et al. Domestic honeybees affect the performance of pre-dispersal seed predators in an alpine meadow. Oecologia. 2018; 187: 113–122. doi: 10.1007/s00442-018-4095-5 29492691

27. Memmott J. The structure of a plant-pollinator food web. Ecol Lett. 1999; 2: 276–280.

28. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994; 3: 294–299. 7881515

29. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016; 33: 1870–1874. doi: 10.1093/molbev/msw054 27004904

30. Kwaiser KS, Hendrix SD. Diversity and abundance of bees (Hymenoptera: Apiformes) in native and ruderal grasslands of agriculturally dominated landscapes. Agr Ecosyst Environ. 2008; 124: 200–204.

31. Jönsson AM, Ekroos J, Dänhardt J, Andersson GK, Olsson O, Smith HG. Sown flower strips in southern Sweden increase abundances of wild bees and hoverflies in the wider landscape. Biol Conserv. 2015; 184: 51–58.

32. Ramette A. Multivariate analyses in microbial ecology. FEMS Microbiol Ecol. 2007; 62: 142–160. doi: 10.1111/j.1574-6941.2007.00375.x 17892477

33. Osorio-Canadas S, Arnan X, Bassols E, Vicens N, Bosch J. Seasonal dynamics in a cavity-nesting bee-wasp community: Shifts in composition, functional diversity and host-parasitoid network structure. PLoS ONE. 2018; 13: e0205854. doi: 10.1371/journal.pone.0205854 30325966

34. Almeida-Neto M, Ulrich W. A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Modell Soft. 2011; 26: 173–178.

35. Almeida‐Neto M, Guimaraes P, Guimaraes PR Jr, Loyola RD, Ulrich W. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos. 2008; 117: 1227–1239.

36. Rodríguez‐Gironés MA, Santamaría L. A new algorithm to calculate the nestedness temperature of presence-absence matrices. J Biogeogr. 2006; 33: 924–935.

37. Dormann CF, Gruber B, Fründ J. Introducing the bipartite package: analysing ecological networks. interaction, 2008, 1: 0.2413793.

38. Vitória RS, Vizentin-Bugoni J, DS Duarte L. Evolutionary history as a driver of ecological networks: a case study of plant-hummingbird interactions. Oikos. 2017; 127: 561–569.

39. Alarcón R, Waser N M, Ollerton J. Year‐to‐year variation in the topology of a plant-pollinator interaction network. Oikos. 2008; 117: 1796–1807.

40. Fox J. Current food web models cannot explain the overall topological structure of observed food webs. Oikos. 2006; 115: 97–109.

41. Vizentin-Bugoni J, Maruyama PK, Sazima M. Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird-plant network. Proc Roy Soc B-Biol Sci. 2014; 281: 1–8.

42. Sazatornil FD, Moré M, Benitez-Vieyra S, Cocucci AA, Kitching IJ, Schlumpberger BO, et al. Beyond neutral and forbidden links: morphological matches and the assembly of mutualistic hawkmoth-plant networks. J Anim Ecol. 2016; 85: 1586–1594. doi: 10.1111/1365-2656.12509 26931495

43. Vázquez DP, Aizen MA. Asymmetric specialization: a pervasive feature of plant-pollinator interactions. Ecology. 2004; 85: 1251–1257.

Článek vyšel v časopise


2019 Číslo 10