The role of alien species on plant-floral visitor network structure in invaded communities

English version

Autoři: Víctor Parra-Tabla ^aff001; Diego Angulo-Pérez ^aff001; Cristopher Albor ^aff001; María José Campos-Navarrete ^aff002; Juan Tun-Garrido ^aff003; Paula Sosenski ^aff001; Conchita Alonso ^aff004; Tia-Lynn Ashman ^aff005; Gerardo Arceo-Gómez ^aff006
Působiště autorů: Departamento de Ecología Tropical, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán,Mérida, Yucatán, México ^aff001; División de Estudios de Posgrado e Investigación, Instituto Tecnológico de Tizimín, Tecnológico Nacional de México,Tizimín, Yucatán, México ^aff002; Departamento de Botánica, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Mérida, Yucatán, México ^aff003; Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas (CSIC), Avda, Sevilla, Spain ^aff004; Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, United States of America ^aff005; Department of Biological Sciences, East Tennessee State University, Johnson City, TN, United States of America ^aff006
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0218227

Souhrn

The interactions between pairs of native and alien plants via shared use of pollinators have been widely studied. Community level studies however, are necessary in order to fully understand the factors and mechanisms that facilitate successful plant invasion, but these are still scarce. Specifically, few community level studies have considered how differences in invasion level (alien flower abundance), and degree of floral trait similarity between native and invasive species, mediate effects on native plant-pollinator communities. Here, we evaluated the role of alien species on overall plant-floral visitor network structure, and on species-level network parameters, across nine invaded coastal communities distributed along 205 km in Yucatán, México that vary in alien species richness and flower abundance. We further assessed the potential the role of alien plant species on plant-floral visitor network structure and robustness via computational simulation of native and invasive plant extinction scenarios. We did not find significant differences between native and alien species in their functional floral phenotypes or in their visitation rate and pollinator community composition in these invaded sites. Variation in the proportion of alien plant species and flower abundance across sites did not influence plant-pollinator network structure. Species-level network parameters (i.e., normalized degree and nestedness contribution) did not differ between native and alien species. Furthermore, our simulation analyses revealed that alien species are functionally equivalent to native species and contribute equally to network structure and robustness. Overall, our results suggest that high levels of floral trait similarity and pollinator use overlap may help facilitate the integration of alien species into native plant-pollinator networks. As a result, alien species may also play a similar role than that of natives in the structure and stability of native plant and pollinator communities in the studied coastal sand dune ecosystem.

Klíčová slova:

Plants – Network analysis – Species interactions – Flowering plants – Flowers – Invasive species – Species extinction – Pollination

Zdroje

1. Powell KI, Chase JM, Knigth T (2011) A synthesis of plant invasion effects on biodiversity across spatial scales. Am J Bot. 98, 539–548. doi: 10.3732/ajb.1000402 21613145

2. Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, et al. (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol. 28, 58–66. doi: 10.1016/j.tree.2012.07.013 22889499

3. Traveset A, Richardson DM (2014) Mutualistic interactions and biological invasions. Annu Rev Ecol Evol Syst. 45, 89–113.

4. Morales CL, Traveset A (2009) A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of coflowering native plants. Ecol Lett. 12, 716–728. doi: 10.1111/j.1461-0248.2009.01319.x 19453616

5. Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, et al. (2011) Ecological impact of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett. 14, 702–708. doi: 10.1111/j.1461-0248.2011.01628.x 21592274

6. Thijs K, Brys R, Verboven H, Hermy M (2012) The influence of an invasive plant species on the pollination success and reproductive output of three riparian plant species. Biol Invas. 14, 355–365.

7. Charlebois KA, Sargent RD (2017) No consistent pollinator-mediated impacts of alien plants on natives. Ecol Lett. 20, 1479–1490. doi: 10.1111/ele.12831 28901037

8. Powell K, Krakos K, Knight T (2011) Comparing the reproductive success and pollination biology of an invasive plant to its rare and common native congeners: a case study in the genus Cirsium (Asteraceae). Biol Invas. 13, 905–917.

9. Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol. 6, e31. doi: 10.1371/journal.pbio.0060031 18271628

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

11. Albrecht M, Padrón B, Bartomeus I, Traveset A (2014) Consequences of plant invasions on compartmentalization and species’ roles in plant–pollinator networks. P R Soc B. 281, 20140773.

12. Stout JC, Tiedeken EJ (2017) Direct interactions between invasive plants and native pollinators: evidence, impacts and approaches. Funct Ecol. 31, 38–46.

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

14. Gómez JM, Perfectti F, Jordano P (2011) The functional consequences of mutualistic network architecture. PLoS One 6, e16143. doi: 10.1371/journal.pone.0016143 21283583

15. Morales CL, Traveset A (2008) Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. CRC Crit Rev Plant Sci. 27: 221–238.

16. Kaiser-Bunbury CN, Valentin T, Mougal J, Matatiken D, Ghazoul J (2011) The tolerance of island plant–pollinator networks to alien plants. J Ecol. 99, 202–213.

17. Maruyama PK, Vizentin-Bugoni J, Sonne J, González AM, Schleuning M, Araujo AC, et al. (2016) The integration of alien plants in mutualistic plant–hummingbird networks across the Americas: the importance of species traits and insularity. Divers Distrib. 22, 672–681.

18. Tylianakis JM, and Morris R J (2017) Ecological networks across environmental gradients. Annu Rev Ecol Evol Syst. 48:25–48.

19. Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. P R Soc B. 271, 2605–2611.

20. Burgos E, Ceva H, Perazzo RPJ, Devoto M, Medan D, Zimmermann M, et al. (2007) Why nestedness in mutualistic networks? J Theor Biol. 249, 307–313. doi: 10.1016/j.jtbi.2007.07.030 17897679

21. Padrón B, Traveset A, Biedenweg T, Díaz D, Nogales M, Olesen JM (2009) Impact of alien plant invaders on pollination networks in two archipelagos. PLoS One 4, e6275. doi: 10.1371/journal.pone.0006275 19609437

22. Olesen JM, Eskildsen LI, Venkatasamy S (2002) Invasion of pollination networks on oceanic islands: importance of invader complexes and endemic super generalists. Divers Distrib. 8, 181–192.

23. Bosch J, Martín González AM, Rodrigo A, Navarro D (2009) Plant–pollinator networks: adding the pollinator’s perspective. Ecol Lett. 12:409–19 doi: 10.1111/j.1461-0248.2009.01296.x 19379135

24. Sargent RD, Ackerly DD (2008) Plant–pollinator interactions and the assembly of plant communities. Trends Ecol. Evol. 23:123–30 doi: 10.1016/j.tree.2007.11.003 18262307

25. Gibson MR, Richardson DM, Pauw A (2012) Can floral traits predict an invasive plant’s impact on native plant-pollinator communities? J Ecol. 100: 1216–1223.

26. Bartomeus I, Vilá M, Santamaría L (2008) Contrasting effects of invasive plants in plant–pollinator networks. Oecologia 155, 761–770. doi: 10.1007/s00442-007-0946-1 18188603

27. Russo L, Nichol C, Shea K (2015) Pollinator floral provisioning by a plant invader: quantifying beneficial effects of detrimental species. Divers Distrib. 22, 189–198.

28. Valtonen A, Jantunen J, Saarinen K (2006) Flora and lepidoptera fauna adversely affected by invasive Lupinus polyphyllus along road verges. Biol Conserv. 133, 389–396.

29. Morón D, Lenda M, Skórka P, Szentgyörgyi H, Settele J, Woyciechowski M (2009) Wild pollinator communities are negatively affected by invasion of alien goldenrods in grassland landscapes. Biol Conserv. 142, 1322–1332.

30. Hanula JL, Horn S (2011) Removing an invasive shrub (Chinese privet) increases native bee diversity and abundance in riparian forests of the southeastern United States. Insect Conserv Diver. 4, 275–283.

31. Del Vecchio S, Pizzo L, Buffa G (2015) The response of plant community diversity to alien invasion: evidence from a sand dune time series. Biodivers Conserv. 24, 371–392.

32. Espejel I (1987) A phytogeographical analysis of coastal vegetation in the Yucatan Peninsula. J Biogeogr. 14, 499–519.

33. Parra-Tabla V, Albor-Pinto C, Tun-Garrido J, Angulo-Pérez D, Barajas C, Silveira R, et al. (2018) Spatial patterns of species diversity in sand dune plant communities in Yucatan, México: the importance of invasive species in the species dominance patterns. Plant Ecol Divers. In press.

34. Barajas DC (2018) Red de interacciones y diversidad functional planta-polinizador en una vegetación de duna costeras costeras de la Reseva de la Biósfera Ría Celestún, Yucatán. BScC thesis. Universidad de Guadalajara, Zapopan, Jalisco.

35. Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol. 21, 208–216. doi: 10.1016/j.tree.2006.01.006 16701087

36. Miranda F (1959) Vegetación de la Península de Yucatán. Colegio de Postgraduados de Chapingo, Texcoco, México.

37. Zhao YH, Ren ZX, Lázaro A, Wang H, Bernhardt P, Li HD, et al. (2016). Floral traits influence pollen vectors’ choices in higher elevation communities in the Himalaya‐Hengduan Mountains. BMC Ecol. 16, 26. doi: 10.1186/s12898-016-0080-1 27221235

38. Kantsa A, Raguso RA, Dyer AG, Sgardelis SP, Olesen JM, Petanidou T (2017). Community‐wide integration of floral colour and scent in a Mediterranean scrubland. Nature Ecol and Evol, 1(10), 1502–1510. https://doi.org/10.1038/s41559-017-0298-0

39. Caruso CM (2000). Competition for pollination influences selection on floral traits of Ipomopsis aggregata. Evolution, 54, 1546–1557. doi: 10.1111/j.0014-3820.2000.tb00700.x 11108583

40. Chittka L (1992). The colour hexagon: A chromaticity diagram based on photoreceptor excitations as a generalized representation of colour opponency. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 170, 533–543. https://doi.org/10.1007/BF00199331)

41. Campos-Navarrete MJ, Parra-Tabla V, Ramos-Zapata J, Díaz-Castelazo C, Reyes-Novelo E (2013) Structure of plant–Hymenoptera networks in two coastal shrub sites in Mexico. Arthropod-Plant Inter. 7, 607–617.

42. R Development Core TEAM. (2012). A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved from http://www.Rproject.org

43. Albor C, García-Franco J, Parra-Tabla V, Díaz-Castelazo C, Arceo-Gomez G (2019) Taxonomic and functional diversity of the co-flowering community differentially affect Cakile edentula pollination at different spatial scales. J Ecol. https://doi.org/10.1111/1365-2745.13183

44. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol. 26, 32–46

45. Oksanen J, Guillaume Blanchet F, Kindt R, Legendre P, Minchin Pr, O’Hara RB, et al. (2015) Vegan: community ecology package. Rpackage version 2.0–7. http://CRAN.R-project.org/package=vegan

46. SAS (2002) SAS, Version 9.1. SAS Institute Inc., Cary, NC.

47. Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for Mixed Models, 2nd edn. SAS Institute Inc., Cary, North Carolina Little

48. Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst. 38, 567–593.

49. Dormann CF, Gruber B, Frund J (2008) Introducing the bipartite package: analyzing ecological networks. R News. 8, 8–11.

50. Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interactions networks. BMC Ecol. 6, 9 doi: 10.1186/1472-6785-6-9 16907983

51. Guimarães P, Guimarães PR (2005) Aninhado 1.0. (https://pypi.org/project/aninhado/).

52. Guimera R, Sales-Pardo M, Amaral LAN (2004) Modularity from fluctuations in random graphs and complex networks. Phys Rev E. 70, 025101.

53. Marquitti FMD, Guimarães PR, Pires MM, Bittencourt LF (2014) MODULAR: software for the autonomous computation of modularity in large network sets. Ecography. 37, 221–224.

54. Bascompte J, Jordano P, Melian C, Olesen JM (2003) The nested assembly of plant-animal mutualistic networks. P Natl Acad Sci. USA 16, 9383–9387.

55. Colwell RK (2009) EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples (Software), Version 8. 2. 0. http://viceroy.eeb.uconn.edu/estimates.

56. Saavedra S, Stouffer DB, Uzzi B, Bascompte J (2011) Strong contributors to network persistence are the most vulnerable to extinction. Nature 478, 233–235. doi: 10.1038/nature10433 21918515

57. Hedges LV, Olkin I (1985) Statistical Methods for Meta-analysis. Academic Press, New York

58. Valdovinos FS, Ramos-Jiliberto R, Flores JD, Espinoza C, López G (2009) Structure and dynamics of pollination networks: the role of alien plants. Oikos 118, 1190–1200.

59. Bastolla U, Fortuna MA, Pascual-García A, Ferrera A, Luque B, Bascompte J (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458, 1018–1020. doi: 10.1038/nature07950 19396144

60. Vilà M, Bartomeus I, Dietzsch AC, Petanidou T, Steffan-Dewenter I, Stout J.C., et al. (2009) Invasive plant integration into native plant–pollinator networks across Europe. P R Soc B. 276, 3887–3893.

61. Traveset A, Castro-Urgal R, Rotllàn-Puig X, Lázaro A (2017) Effects of habitat loss on the plant-flower visitor network structure of a dune community. Oikos 127, 45–55.

62. Koski MH, Meindl GA, Arceo-Gómez G, Wolowski M, Le Croy KA, Ashman T-L (2015) Plant-flower visitor networks in a serpentine metacommunity: assessing traits associated with keystone plant species. Arthropod-Plant Inter. 9: 9–21.

63. Minnaar C, Anderson B, de Jager ML, Karron JD (2019) Plant–pollinator interactions along the pathway to paternity. Ann Bot. 123: 225–245. doi: 10.1093/aob/mcy167 30535041

64. Emer C, Vaughan IP, Hiscock S, Memmott J (2015) The impact of the invasive alien plant, Impatiens glandulifera, on pollen transfer networks. PLoS One 10: e0143532. doi: 10.1371/journal.pone.0143532 26633170

65. Johnson ALJ, Ashman T-L (2019) Consequences of invasion for pollen transfer and pollination revealed in a tropical island ecosystem. New Phyt. 221, 142–154.

66. Arceo-Gómez G, Ashman T-L (2016) Invasion status and phylogenetic relatedness predict cost of heteroespecific pollen receipt: implications for native biodiversity decline. J Ecol 104, 1003–1008.

67. Bjerkens A-L, Totland Ø, Hegland SJ, Nielsen A (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Cons. 138, 1–12.

68. Carvalheiro LG, Biesmeijer JC, Benadi G, Fründ J, Stang M, Bartomeus I, et al. (2014) The potential for indirect effects between co-flowering plants via shared pollinators depends on resource abundance, accessibility and relatedness. Ecol Lett. 11: 1389–1399.

The role of alien species on plant-floral visitor network structure in invaded communities

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz