Community- and trophic-level responses of soil nematodes to removal of a non-native tree at different stages of invasion

English version

Autoři: Guadalupe Peralta ^aff001; Ian A. Dickie ^aff002; Gregor W. Yeates ^aff001; Duane A. Peltzer ^aff001
Působiště autorů: Manaaki Whenua Landcare Research, Lincoln, New Zealand ^aff001; Bio-Protection Research Centre, School of Biological Sciences, University of Canterbury, Christchurch, New Zealand ^aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0227130

Souhrn

Success of invasive non-native plant species management is usually measured as changes in the abundance of the invasive plant species or native plant species following invader management, but more complex trophic responses to invader removal are often ignored or assumed. Moreover, the effects of invader removal at different stages of the invasion process is rarely evaluated, despite a growing recognition that invader impacts are density or stage-dependent. Therefore, the effectiveness of invasive species management for restoring community structure and function across trophic levels remains poorly understood. We determined how soil nematode diversity and community composition respond to removal of the globally invasive tree species Pinus contorta at different stages of invasion by reanalysing and expanding an earlier study including uninvaded vegetation (seedlings removed continuously), early invader removal (saplings removed), late removal (trees removed), and no removal (invaded). These treatments allowed us to evaluate the stage-dependent belowground trophic responses to biological invasion and removal. We found that invaded plots had half the nematode taxa richness compared to uninvaded plots, and that tree invasion altered the overall composition of the nematode community. Differences in nematode community composition between uninvaded nematode communities and those under the tree removal strategy tended to dilute higher up the food chain, whereas the composition of uninvaded vs. sapling removal strategies did not differ significantly. Conversely, the composition of invaded compared to uninvaded nematode communities differed across all trophic levels, altering the community structure and function. Specifically, invaded communities were structurally simplified compared to uninvaded communities, and had a higher proportion of short life cycle nematodes, characteristic of disturbed environments. We demonstrate that a shift in management strategies for a globally invasive tree species from removing trees to earlier removal of saplings is needed for maintaining the composition and structure of soil nematode communities to resemble uninvaded conditions.

Klíčová slova:

Community structure – Ecosystems – Seedlings – Life cycles – Plant communities – Invasive species – Pines – Food web structure

Zdroje

1. Hulme PE. Invasion pathways at a crossroad: policy and research challenges for managing alien species introductions. J Appl Ecol. 2015;52 : 1418–1424. doi: 10.1111/1365-2664.12470

2. Pearson DE, Ortega YK, Runyon JB, Butler JL. Secondary invasion: the bane of weed management. Biol Conserv. 2016;197 : 8–17. doi: 10.1016/j.biocon.2016.02.029

3. Manchester SJ, Bullock JM. The impacts of non-native species on UK biodiversity and the effectiveness of control. J Appl Ecol. 2000;37 : 845–864. doi: 10.1046/j.1365-2664.2000.00538.x

4. Gardener MR, Atkinson R, Rentería JL. Eradications and People: lessons from the Plant Eradication Program in Galapagos. Restor Ecol. 2010;18 : 20–29. doi: 10.1111/j.1526-100X.2009.00614.x

5. van Wilgen BW, Forsyth GG, Le Maitre DC, Wannenburgh A, Kotzé JDF, van den Berg E, et al. An assessment of the effectiveness of a large, national-scale invasive alien plant control strategy in South Africa. Biol Conserv. 2012;148 : 28–38. doi: 10.1016/j.biocon.2011.12.035

6. Reid AM, Morin L, Downey PO, French K, Virtue JG. Does invasive plant management aid the restoration of natural ecosystems? Biol Conserv. 2009;142 : 2342–2349. doi: 10.1016/j.biocon.2009.05.011

7. Simberloff D. Biological invasions: What’s worth fighting and what can be won? Sustain Restor. 2014;65 : 112–121. doi: 10.1016/j.ecoleng.2013.08.004

8. Stewart G, Cox E, Le Duc M, Pakeman R, Pullin A, Marrs R. Control of Pteridium aquilinum: meta-analysis of a multi-site Study in the UK. Ann Bot. 2008;101 : 957–970. doi: 10.1093/aob/mcn020 18337356

9. Kettenring KM, Adams CR. Lessons learned from invasive plant control experiments: a systematic review and meta-analysis. J Appl Ecol. 2011;48 : 970–979. doi: 10.1111/j.1365-2664.2011.01979.x

10. Pyšek P, Jarošík V, Hulme PE, Pergl J, Hejda M, Schaffner U, et al. A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Glob Change Biol. 2012;18 : 1725–1737. doi: 10.1111/j.1365-2486.2011.02636.x

11. Myers JH, Simberloff D, Kuris AM, Carey JR. Eradication revisited: dealing with exotic species. Trends Ecol Evol. 2000;15 : 316–320. doi: 10.1016/s0169-5347(00)01914-5 10884695

12. Rinella MJ, Maxwell BD, Fay PK, Weaver T, Sheley RL. Control effort exacerbates invasive-species problem. Ecol Appl. 2009;19 : 155–162. doi: 10.1890/07-1482.1 19323180

13. Musil CF, Milton SJ, Davis GW. The threat of alien invasive grasses to lowland Cape floral diversity: an empirical appraisal of the effectiveness of practical control strategies. South Afr J Sci. 2005;101 : 337–344.

14. Firn J, House APN, Buckley YM. Alternative states models provide an effective framework for invasive species control and restoration of native communities. J Appl Ecol. 2010;47 : 96–105. doi: 10.1111/j.1365-2664.2009.01741.x

15. Barney JN, Tekiela DR, Barrios-Garcia MN, Dimarco RD, Hufbauer RA, Leipzig-Scott P, et al. Global Invader Impact Network (GIIN): toward standardized evaluation of the ecological impacts of invasive plants. Ecol Evol. 2015;5 : 2878–2889. doi: 10.1002/ece3.1551 26306173

16. Dickie IA, St John MG, Yeates GW, Morse CW, Bonner KI, Orwin K, et al. Belowground legacies of Pinus contorta invasion and removal result in multiple mechanisms of invasional meltdown. AoB PLANTS. 2014;6: plu056–plu056. doi: 10.1093/aobpla/plu056 25228312

17. Reid ML, Emery SM. Scale-dependent effects of Gypsophila paniculata invasion and management on plant and soil nematode community diversity and heterogeneity. Biol Conserv. 2018;224 : 153–161. doi: 10.1016/j.biocon.2018.05.026

18. Seibold S, Cadotte MW, MacIvor JS, Thorn S, Müller J. The necessity of multitropic approaches in community ecology. Trends Ecol Evol. 2018; doi: 10.1016/j.tree.2018.07.001 30146326

19. Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, et al. Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions. 1999;1 : 3–19. doi: 10.1023/A:1010034312781

20. Kumschick S, Gaertner M, Vilà M, Essl F, Jeschke JM, Pyšek P, et al. Ecological impacts of alien species: quantification, scope, caveats, and recommendations. BioScience. 2015;65 : 55–63. doi: 10.1093/biosci/biu193

21. Hejda M, Hanzelka J, Kadlec T, Štrobl M, Pyšek P, Reif J. Impacts of an invasive tree across trophic levels: species richness, community composition and resident species’ traits. Divers Distrib. 2017;23 : 997–1007. doi: 10.1111/ddi.12596

22. Gebremikael MT, Steel H, Buchan D, Bert W, De Neve S. Nematodes enhance plant growth and nutrient uptake under C and N-rich conditions. Sci Rep. 2016;6 : 32862. doi: 10.1038/srep32862 27605154

23. Ferris H, Bongers T, Goede RGM. A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol. 2001;18 : 13–29.

24. Dickie IA, Yeates GW, St. John MG, Stevenson BA, Scott JT, Rillig MC, et al. Ecosystem service and biodiversity trade-offs in two woody successions: Ecosystem service trade-offs. J Appl Ecol. 2011;48 : 926–934. doi: 10.1111/j.1365-2664.2011.01980.x

25. Yeates GW. How plants affect nematodes. In: Macfadyen A, Ford ED, editors. Advances in Ecological Research. Academic Press; 1987. pp. 61–113. doi: 10.1016/S0065-2504(08)60244-5

26. Gundale MJ, Pauchard A, Langdon B, Peltzer DA, Maxwell BD, Nuñez MA. Can model species be used to advance the field of invasion ecology? Biol Invasions. 2014;16 : 591–607. doi: 10.1007/s10530-013-0610-0

27. Bongers T. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia. 1990;83 : 14–19. doi: 10.1007/BF00324627 28313236

28. Scherber C, Eisenhauer N, Weisser WW, Schmid B, Voigt W, Fischer M, et al. Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature. 2010;468 : 553. doi: 10.1038/nature09492 20981010

29. David P, Thébault E, Anneville O, Duyck P-F, Chapuis E, Loeuille N. Impacts of invasive species on food webs: a review of empirical data. In: Bohan DA, Dumbrell AJ, Massol F, editors. Advances in Ecological Research. Academic Press; 2017. pp. 1–60. doi: 10.1016/bs.aecr.2016.10.001

30. Ledgard N. The spread of lodgepole pine (Pinus contorta, Dougl.) in New Zealand. For Ecol Manag. 2001;141. doi: 10.1016/S0378-1127(00)00488-6

31. Whitehead AG, Hemming JR. A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Ann Appl Biol. 1965;55 : 25–38. doi: 10.1111/j.1744-7348.1965.tb07864.x

32. Yeates GW, Bongers T, De Goede RGM, Freckman DW, Georgieva SS. Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol. 1993;25 : 315–331. 19279775

33. Laliberté E, Kardol P, Didham RK, Teste FP, Turner BL, Wardle DA. Soil fertility shapes belowground food webs across a regional climate gradient. Ecol Lett. 2017;20 : 1273–1284. doi: 10.1111/ele.12823 28853198

34. Zhang P, Li B, Wu J, Hu S. Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta‐analysis. Seabloom E, editor. Ecol Lett. 2019;22 : 200–210. doi: 10.1111/ele.13181 30460738

35. Yeates GW. Modification and qualification of the nematode maturity index. Pedobiologia. 1994;38 : 97–101.

36. Bongers T, Bongers M. Functional diversity of nematodes. Appl Soil Ecol. 1998;10 : 239–251. doi: 10.1016/S0929-1393(98)00123-1

37. Sieriebriennikov B, Ferris H, de Goede RGM. NINJA: an automated calculation system for nematode-based biological monitoring. Eur J Soil Biol. 2014;61 : 90–93. doi: 10.1016/j.ejsobi.2014.02.004

38. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;26 : 32–46. doi: 10.1111/j.1442-9993.2001.01070.pp.x

39. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. 2017;

40. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. vegan: community ecology package. R Package Version 24–4. 2017; Available: https://CRAN.R-project.org/package=vegan

41. Martinez Arbizu P. pairwiseAdonis: pairwise multilevel comparison using adonis. R Package Version 001. 2017;

42. Anderson MJ. Distance-based tests for homogeneity of multivariate dispersions. Biometrics. 2006;62 : 245–253. doi: 10.1111/j.1541-0420.2005.00440.x 16542252

43. Cáceres MD, Legendre P. Associations between species and groups of sites: indices and statistical inference. Ecology. 2009;90 : 3566–3574. doi: 10.1890/08-1823.1 20120823

44. Nuñez MA, Chiuffo MC, Torres A, Paul T, Dimarco RD, Raal P, et al. Ecology and management of invasive Pinaceae around the world: progress and challenges. Biol Invasions. 2017;19 : 3099–3120. doi: 10.1007/s10530-017-1483-4

45. Flory SL, Clay K. Invasive plant removal method determines native plant community responses. J Appl Ecol. 2009;46 : 434–442. doi: 10.1111/j.1365-2664.2009.01610.x

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

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

48. Čerevková A, Miklisová D, Bobuľská L, Renčo M. Impact of the invasive plant Solidago gigantea on soil nematodes in a semi-natural grassland and a temperate broadleaved mixed forest. J Helminthol. 2019; 1–14. doi: 10.1017/S0022149X17001201

49. Meisner A, Gera Hol WH, de Boer W, Krumins JA, Wardle DA, van der Putten WH. Plant–soil feedbacks of exotic plant species across life forms: a meta-analysis. Biol Invasions. 2014;16 : 2551–2561. doi: 10.1007/s10530-014-0685-2

50. Biederman LA, Boutton TW. Biodiversity and trophic structure of soil nematode communities are altered following woody plant invasion of grassland. Soil Biol Biochem. 2009;41 : 1943–1950. doi: 10.1016/j.soilbio.2009.06.019

51. Peralta G, Schon NL, Dickie IA, St John MG, Orwin KH, Yeates GW, et al. Contrasting responses of soil nematode communities to native and non-native woody plant expansion. Oecologia. 2019;190 : 891–899. doi: 10.1007/s00442-019-04456-3 31273519

52. Zavaleta ES, Hobbs RJ, Mooney HA. Viewing invasive species removal in a whole-ecosystem context. Trends Ecol Evol. 2001;16 : 454–459.

53. Funk JL, Cleland EE, Suding KN, Zavaleta ES. Restoration through reassembly: plant traits and invasion resistance. Trends Ecol Evol. 2008;23 : 695–703. doi: 10.1016/j.tree.2008.07.013 18951652

54. Corbin JD, D’Antonio CM. Gone but not forgotten? Invasive plants’ legacies on community and ecosystem properties. Invasive Plant Sci Manag. 2012;5 : 117–124. doi: 10.1614/IPSM-D-11-00005.1

55. Wubs ERJ, van der Putten WH, Bosch M, Bezemer TM. Soil inoculation steers restoration of terrestrial ecosystems. Nat Plants. 2016;2 : 16107. doi: 10.1038/nplants.2016.107 27398907

56. Van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, et al. Plant–soil feedbacks: the past, the present and future challenges. J Ecol. 2013;101 : 265–276. doi: 10.1111/1365-2745.12054

57. De Deyn GB, Raaijmakers CE, Zoomer HR, Berg MP, de Ruiter PC, Verhoef HA, et al. Soil invertebrate fauna enhances grassland succession and diversity. Nature. 2003;422 : 711–713. doi: 10.1038/nature01548 12700759

58. Coffey V, Otfinowski R. Legacies of afforestation on soil nematode community composition, structure, and diversity in a northern Canadian prairie. Plant Soil. 2019;435 : 437–447. doi: 10.1007/s11104-018-03906-w

59. Wardle DA, Yeates GW. The dual importance of competition and predation as regulatory forces in terrestrial ecosystems: evidence from decomposer food-webs. Oecologia. 1993;93 : 303–6. doi: 10.1007/BF00317685 28313621

60. Zhao J, Neher DA. Soil energy pathways of different ecosystems using nematode trophic group analysis: a meta analysis. Nematology. 2014;16 : 379–385. doi: 10.1163/15685411-00002771

61. Epanchin-Niell RS, Hastings A. Controlling established invaders: integrating economics and spread dynamics to determine optimal management. Ecol Lett. 2010;13 : 528–541. doi: 10.1111/j.1461-0248.2010.01440.x 20455926

62. Kerr NZ, Baxter PWJ, Salguero-Gómez R, Wardle GM, Buckley YM. Prioritizing management actions for invasive populations using cost, efficacy, demography and expert opinion for 14 plant species world-wide. J Appl Ecol. 2016;53 : 305–316. doi: 10.1111/1365-2664.12592 27478205

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