Interaction strength in plant-pollinator networks: Are we using the right measure?

English version

Autoři: Roberto Novella-Fernandez ^aff001; Anselm Rodrigo ^aff002; Xavier Arnan ^aff003; Jordi Bosch ^aff003
Působiště autorů: School of Biological Sciences, University of Southampton, Southampton, England, United Kingdom ^aff001; Universitat Autònoma Barcelona, Cerdanyola del Vallès, Catalunya, Spain ^aff002; CREAF, Cerdanyola del Vallès, Catalunya, Spain ^aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225930

Souhrn

Understanding how ecological networks are assembled is important because network structure reflects ecosystem functioning and stability. Quantitative network analysis incorporates measures of interaction strength as an estimate of the magnitude of the effect of interaction partners on one another. Most plant-pollinator network studies use frequency of interaction between individual pollinators and individual plants (encounter) as a surrogate of interaction strength. However, the number of flowers visited per encounter may strongly vary among pollinator and plant species, and therefore not all encounters are quantitatively equivalent. We sampled plant-pollinator interactions in a Mediterranean scrubland and tested whether using a measure of interaction strength based on the number of flowers visited resulted in changes in species (species strength, interaction species asymmetry, specialization) and network descriptors (nestedness, H2’, interaction evenness, plant generality, pollinator generality) compared to the encounter-based measure. Several species (including some of the most abundant ones) showed important changes in species descriptors, notably in specialization. These changes were especially important in plant species with large floral displays, which became less specialized with the visit-based measure of interaction strength. At the network level we found significant changes in all properties analysed. With the encounter-based approach plant generality was much higher than pollinator generality (high specialization asymmetry between trophic levels). However, with the visit-based approach plant generality was greatly reduced so that plants and pollinators had similar levels of generalization. Interaction evenness also decreased strongly with the visit-based approach. We conclude that accounting for the number of flowers visited per encounter provides a more ecologically relevant measure of interaction strength. Our results have important implications for the stability of pollination networks and the evolution of plant-pollinator interactions. The use of a visit-based approach is especially important in studies relating interaction network structure and ecosystem function (pollination and/or exploitation of floral resources).

Klíčová slova:

Community structure – Flowering plants – Flowers – Network analysis – Plants – Pollen – Species interactions – Trophic interactions

Zdroje

1. Johnson MTJ, Stinchcombe JR. An emerging synthesis between community ecology and evolutionary biology. Trends Ecol Evol. 2007;22: 250–257. doi: 10.1016/j.tree.2007.01.014 17296244

2. Bascompte J, Jordano P. Plant-Animal Mutualistic Networks: The Architecture of Biodiversity. Annu Rev Ecol Evol Syst. 2007;38: 567–593. doi: 10.1146/annurev.ecolsys.38.091206.095818

3. Vázquez DP, Bluthgen 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

4. Landi P, Minoarivelo HO, Brännström Å, Hui C, Dieckmann U. Complexity and stability of adaptive ecological networks: A survey of the theory in community ecology. Popul Ecol. 2018;60: 319–345. doi: 10.1007/978-3-319-71486-8_12

5. Guimarães PR, Jordano P, Thompson JN. Evolution and coevolution in mutualistic networks. Ecol Lett. 2011;14: 877–885. doi: 10.1111/j.1461-0248.2011.01649.x 21749596

6. Gómez JM, Perfectti F, Jordano P. The Functional Consequences of Mutualistic Network Architecture. PLoS One. 2011;6: 1435–1439. doi: 10.1371/Citation

7. Jordano P, Bascompte J, Olesen JM. The ecological consequences of complex topology and nested structure in pollination webs. In: Waser N.M. & Ollerton J, editor. Complex plant-pollinator networks. Chicago: University of Chicago Press; 2006. pp. 173–199. Available: http://books.google.com/books?hl=ca&lr=&id=Fbl5c9fUxTIC&pgis=1

8. Bascompte J, Jordano P, Olesen JM. Asymetric Coevolutionary Networks Facilitate Biodiversity Maintenance. Science (80-). 2006;312: 431–433. doi: 10.1126/science.1123412 16627742

9. Kaiser-Bunbury CN, Muff S, Memmott J, Müller CB, Caflisch A. The robustness of pollination networks to the loss of species and interactions: A quantitative approach incorporating pollinator behaviour. Ecol Lett. 2010;13: 442–452. doi: 10.1111/j.1461-0248.2009.01437.x 20100244

10. Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J. The impact of an alien plant on a native plant-pollinator network: An experimental approach. Ecol Lett. 2007;10: 539–550. doi: 10.1111/j.1461-0248.2007.01055.x 17542933

11. Aizen MA, Morales CL, Morales JM. Invasive mutualists erode native pollination webs. PLoS Biol. 2008;6: 0396–0403. doi: 10.1371/journal.pbio.0060031 18271628

12. Memmott J, Waser NM, Price M V. Tolerance of pollination networks to species extinctions. Proc Biol Sci. 2004;271: 2605–2611. doi: 10.1098/rspb.2004.2909 15615687

13. Tylianakis JM, Tscharntke T, Lewis OT. Habitat modification alters the structure of tropical host-parasitoid food webs. Nature. 2007;445: 202–205. doi: 10.1038/nature05429 17215842

14. Weiner CN, Werner M, Linsenmair KE, Blüthgen N. Land-use impacts on plant-pollinator networks: Interaction strength and specialization predict pollinator declines. Ecology. 2014;95: 466–474. doi: 10.1890/13-0436.1 24669739

15. Osorio S, Arnan X, Bassols E, Vicens N, Bosch J. Local and landscape effects in a host-parasitoid interaction network along a forest-cropland gradient. Ecol Appl. 2015;25: 1869–1879. doi: 10.1890/14-2476.1 26591453

16. Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø. How does climate warming affect plant-pollinator interactions? Ecol Lett. 2009;12: 184–195. doi: 10.1111/j.1461-0248.2008.01269.x 19049509

17. Memmott J, Craze PG, Waser NM, Price M V. Global warming and the disruption of plant-pollinator interactions. Ecol Lett. 2007;10: 710–717. doi: 10.1111/j.1461-0248.2007.01061.x 17594426

18. Jordano P. Patterns of Mutualistic Interactions in Pollination and Seed Dispersal: Connectance, Dependence Asymetries, and Coevolution. Am Nat. 1987;129: 657–677.

19. Laska MS, Wootton JT. Theoretical concepts and empirical approaches to measuring interaction strength. Ecology. 1998;79: 461–476. doi: 10.1890/0012-9658(1998)079[0461:TCAEAT]2.0.CO;2

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

21. Almeida-Neto M, Ulrich W. A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Model Softw. 2011;26: 173–178. doi: 10.1016/j.envsoft.2010.08.003

22. Bersier LF, Banašek-Richter C, Cattin MF. Quantitative descriptors of food-web matrices. Ecology. 2002;83: 2394–2407. doi: 10.1890/0012-9658(2002)083[2394:QDOFWM]2.0.CO;2

23. Blüthgen N, Menzel F, Blüthgen N. Measuring specialization in species interaction networks. BMC Ecol. 2006;6: 1–12. doi: 10.1186/1472-6785-6-1 16412253

24. Poisot T, Canard E, Mouquet N, Hochberg ME. A comparative study of ecological specialization estimators. Methods Ecol Evol. 2012;3: 537–544. doi: 10.1111/j.2041-210X.2011.00174.x

25. Herrera CM. Components of Pollinator “Quality”: Comparative Analysis of a Diverse Insect Assemblage. Oikos. 1987;50: 79–90. doi: 10.2307/3565403

26. Herrera CM. Pollinator abundance, morphology, and flower visitation rate: analysis of the “quantity” component in a plant-pollinator system. Oecologia. 1989;80: 241–248. doi: 10.1007/BF00380158 28313114

27. Vázquez DP, Morris WF, Jordano P. Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol Lett. 2005;8: 1088–1094. doi: 10.1111/j.1461-0248.2005.00810.x

28. Wilson P, Thomson JD. Heterogeneity Among Floral Visitors Leads to Discordance Between Removal and Deposition of Pollen. Ecology. 1991;72: 1503–1507.

29. Ne’Eman G, Jürgens A, Newstrom-Lloyd L, Potts SG, Dafni A. A framework for comparing pollinator performance: Effectiveness and efficiency. Biol Rev. 2010;85: 435–451. doi: 10.1111/j.1469-185X.2009.00108.x 20015317

30. King C, Ballantyne G, Willmer PG. Why flower visitation is a poor proxy for pollination: Measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods Ecol Evol. 2013;4: 811–818. doi: 10.1111/2041-210X.12074

31. Santiago-Hernández MH, Martén-Rodríguez S, Lopezaraiza-Mikel M, Oyama K, González-Rodríguez A, Quesada M. The role of pollination effectiveness on the attributes of interaction networks: from floral visitation to plant fitness. Ecology. 2019;100: 1–15. doi: 10.1002/ecy.2803 31240696

32. Vázquez DP, Lomascolo SB, Belen Maldonado M, Chacoff NP, Dorado J, Stevani EL, et al. The strength of plant-pollinator interactions. Ecology. 2012;93: 719–725. doi: 10.1890/11-1356.1 22690622

33. Sahli HF, Conner JK. Characterizing ecological generalization in plant-pollination systems. Oecologia. 2006;148: 365–372. doi: 10.1007/s00442-006-0396-1 16514533

34. Castro-Urgal R, Tur C, Albrecht M, Traveset A. How different link weights affect the structure of quantitative flower-visitation networks. Basic Appl Ecol. 2012;13: 500–508. doi: 10.1016/j.baae.2012.08.002

35. Arnan X, Escolà A, Rodrigo A, Bosch J. Female reproductive success in gynodioecious Thymus vulgaris: Pollen versus nutrient limitation and pollinator foraging behaviour. Bot J Linn Soc. 2014;175: 395–408. doi: 10.1111/boj.12173

36. Herrera CM. Flower-to-seedling consequences of different pollination regimes in an insect-pollinated shrub. Ecology. 2000;81: 15–29. doi: 10.1890/0012-9658(2000)081[0015:FTSCOD]2.0.CO;2

37. Thompson JD. How do visitation patterns vary among pollinators in relation to floral display and floral design in a generalist pollination system? Oecologia. 2001;126: 386–394. doi: 10.1007/s004420000531 28547453

38. Ohashi K, Yahara T. Effects of Variation in Flower Number on Pollinator Visits in Cirsium purpuratum (Asteraceae). Am J Bot. 1998;85: 219–224. 21684905

39. Kaiser-Bunbury CN, Memmott J, Müller CB. Community structure of pollination webs of Mauritian heathland habitats. Perspect Plant Ecol Evol Syst. 2009;11: 241–254. doi: 10.1016/j.ppees.2009.04.001

40. Vázquez DP, Melián CJ, Williams NM, Blüthgen N, Krasnov BR, Poulin R. Species abundance and asymmetric interaction strength in ecological networks. Oikos. 2007;116: 1120–1127. doi: 10.1111/j.2007.0030–1299.15828.x

41. Dormann CF, Frund J, Bluthgen N, Gruber B. Indices, Graphs and Null Models: Analyzing Bipartite Ecological Networks. Open Ecol J. 2009;2: 7–24. doi: 10.2174/1874213000902010007

42. R core team. R: A language and environment for statistical computing. Vienna, Austria: R Core Team; 2019.

43. Bates D, Mächler M, Bolker BM, Walker SC. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. 2015;67: 1–48. doi: 10.18637/jss.v067.i01

44. Berlow EL, Neutel AM, Cohen JE, De Ruiter PC, Ebenman B, Emmerson M, et al. Interaction strengths in food webs: Issues and opportunities. J Anim Ecol. 2004;73: 585–598. doi: 10.1111/j.0021-8790.2004.00833.x

45. Jordano P. Sampling networks of ecological interactions. Funct Ecol. 2016;30: 1883–1893. doi: 10.1111/1365-2435.12763

46. Miranda PN, Ribeiro JEL da S, Luna P, Brasil I, Delabie JHC, Dáttilo W. The dilemma of binary or weighted data in interaction networks. Ecol Complex. 2019;38: 1–10. doi: 10.1016/j.ecocom.2018.12.006

47. Mitchell RJ, Karron JD, Holmquist KG, Bell JM. The influence of Mimulus ringens floral display size on pollinator visitation patterns. Funct Ecol. 2004;18: 116–124. doi: 10.1111/j.1365-2435.2004.00812.x

48. Miyake YC, Sakai S. Effects of number of flowers per raceme and number of racemes per plant on bumblebee visits and female reproductive success in Salvia nipponica (Labiatae). Ecol Res. 2005;20: 395–403. doi: 10.1007/s11284-004-0035-4

49. Abramson G, Trejo Soto CA, Oña L. The role of asymmetric interactions on the effect of habitat destruction in mutualistic networks. PLoS One. 2011;6: e21028. doi: 10.1371/journal.pone.0021028 21698298

50. Armbruster WS. The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Funct Ecol. 2017;31: 88–100. doi: 10.1111/1365-2435.12783

51. Mitchell RJ, Irwin RE, Flanagan RJ, Karron JD. Ecology and evolution of plant–pollinator interactions. Ann Bot. 2009;103: 1355–1363. doi: 10.1093/aob/mcp122 19482881

Interaction strength in plant-pollinator networks: Are we using the right measure?

Souhrn

Klíčová slova:

Zdroje

PLOS One

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií

Aktuální možnosti diagnostiky a léčby litiáz