Quantitative assessment of plant-arthropod interactions in forest canopies: A plot-based approach


Autoři: Martin Volf aff001;  Petr Klimeš aff001;  Greg P. A. Lamarre aff001;  Conor M. Redmond aff001;  Carlo L. Seifert aff001;  Tomokazu Abe aff004;  John Auga aff005;  Kristina Anderson-Teixeira aff006;  Yves Basset aff001;  Saul Beckett aff007;  Philip T. Butterill aff001;  Pavel Drozd aff009;  Erika Gonzalez-Akre aff006;  Ondřej Kaman aff001;  Naoto Kamata aff010;  Benita Laird-Hopkins aff001;  Martin Libra aff001;  Markus Manumbor aff005;  Scott E. Miller aff012;  Kenneth Molem aff005;  Ondřej Mottl aff001;  Masashi Murakami aff004;  Tatsuro Nakaji aff013;  Nichola S. Plowman aff001;  Petr Pyszko aff009;  Martin Šigut aff009;  Jan Šipoš aff014;  Robert Tropek aff001;  George D. Weiblen aff017;  Vojtech Novotny aff001
Působiště autorů: Biology Centre of the Czech Academy of Sciences, Ceske Budejovice, Czech Republic aff001;  German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany aff002;  Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic aff003;  Faculty of Science, Chiba University, Chiba, Japan aff004;  New Guinea Binatang Research Center, Madang, Papua New Guinea aff005;  Conservation Ecology Center, Smithsonian Conservation Biology Institute; Front Royal, VA, United States of America aff006;  ForestGEO, Smithsonian Tropical Research Institute, Panama City, Panama aff007;  Maestria de Entomologia, Universidad de Panama, Panama City, Panama aff008;  Faculty of Science, University of Ostrava, Ostrava, Czech Republic aff009;  Graduate School of Agricultural and Life Sciences, The University of Tokyo, Furano, Japan aff010;  School of Biological Sciences, University of Bristol, Bristol, United Kingdom aff011;  National Museum of Natural History, Smithsonian Institution, Washington, DC, United States of America aff012;  Tomakomai Experimental Forest, Hokkaido University, Tomakomai, Japan aff013;  Institute of Botany, Czech Academy of Sciences, Brno, Czech Republic aff014;  Department of Zoology, Fisheries, Hydrobiology and Apiculture, Mendel University in Brno, Brno, Czech Republic aff015;  Department of Ecology, Faculty of Science, Charles University, Prague, Czech Republic aff016;  Bell Museum and Department of Plant & Microbial Biology, University of Minnesota, Saint Paul, MN, United States of America aff017
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222119

Souhrn

Research on canopy arthropods has progressed from species inventories to the study of their interactions and networks, enhancing our understanding of how hyper-diverse communities are maintained. Previous studies often focused on sampling individual tree species, individual trees or their parts. We argue that such selective sampling is not ideal when analyzing interaction network structure, and may lead to erroneous conclusions. We developed practical and reproducible sampling guidelines for the plot-based analysis of arthropod interaction networks in forest canopies. Our sampling protocol focused on insect herbivores (leaf-chewing insect larvae, miners and gallers) and non-flying invertebrate predators (spiders and ants). We quantitatively sampled the focal arthropods from felled trees, or from trees accessed by canopy cranes or cherry pickers in 53 0.1 ha forest plots in five biogeographic regions, comprising 6,280 trees in total. All three methods required a similar sampling effort and provided good foliage accessibility. Furthermore, we compared interaction networks derived from plot-based data to interaction networks derived from simulated non-plot-based data focusing either on common tree species or a representative selection of tree families. All types of non-plot-based data showed highly biased network structure towards higher connectance, higher web asymmetry, and higher nestedness temperature when compared with plot-based data. Furthermore, some types of non-plot-based data showed biased diversity of the associated herbivore species and specificity of their interactions. Plot-based sampling thus appears to be the most rigorous approach for reconstructing realistic, quantitative plant-arthropod interaction networks that are comparable across sites and regions. Studies of plant interactions have greatly benefited from a plot-based approach and we argue that studies of arthropod interactions would benefit in the same way. We conclude that plot-based studies on canopy arthropods would yield important insights into the processes of interaction network assembly and dynamics, which could be maximised via a coordinated network of plot-based study sites.

Klíčová slova:

Ants – Arthropoda – Forests – Cherries – Interaction networks – Leaves – Trees – Herbivory


Zdroje

1. Lowman MD, Schowalter TD, Franklin J. Methods in Forest Canopy Research: Univ of California Press; 2012.

2. Hamilton AJ, Novotny V, Waters EK, Basset Y, Benke KK, Grimbacher PS, et al. Estimating global arthropod species richness: refining probabilistic models using probability bounds analysis. Oecologia. 2013;171(2):357–65. doi: 10.1007/s00442-012-2434-5 22968292

3. Erwin TL. Tropical forests: their richness in Coleoptera and other arthropod species. The Coleopterists Bulletin. 1982;36(1):74–5.

4. Lowman M. An assessment of techniques for measuring herbivory: is rainforest defoliation more intense than we thought? Biotropica. 1984;16(4):264–8.

5. Basset Y, Aberlenc HP, Delvare G. Abundance and stratification of foliage arthropods in a lowland rain forest of Cameroon. Ecological Entomology. 1992;17(4):310–8.

6. Novotny V, Miller SE, Hrcek J, Baje L, Basset Y, Lewis OT, et al. Insects on plants: Explaining the paradox of low diversity within specialist herbivore guilds. American Naturalist. 2012;179(3):351–62. doi: 10.1086/664082 22322223

7. Godfray HCJ, Lewis OT, Memmott J. Studying insect diversity in the tropics. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences. 1999;354(1391):1811–24.

8. Lowman M, Foster R, Wittman P, Rinker H. Herbivory and insect loads on epiphytes, vines and host trees in the rain forest canopy of French Guiana. In: Hallé F, editor. Biologie d’une canopée de forêt equatoriale–III Rapport de la mission d’exploration scientifique de la Canopée de Guyane. Paris, Lyon: Pro-Natura International & Operation Canopee; 1996. p. 116–128.

9. Díaz I, Sieving K, Peña-Foxon M, Armesto J. A field experiment links forest structure and biodiversity: epiphytes enhance canopy invertebrates in Chilean forests. Ecosphere. 2012;3(1):1–17.

10. Wardhaugh CW, Stork NE, Edwards W. Canopy invertebrate community composition on rainforest trees: Different microhabitats support very different invertebrate communities. Austral Ecology. 2014;39(4):367–77.

11. Basset Y, Hammond PM, Barrios H, Holloway JD, Miller SE. Vertical stratification of arthropod assemblages. In: Basset Y, Novotny V, Miller SE, Kitching R, editors. Arthropods of Tropical Forests: Spatio-Temporal Dynamics and Resource Use in the Canopy. Cambridge: Cambridge University Press; 2003. p. 17–27.

12. Murakami M, Yoshida K, Hara H, Toda MJ. Spatio-temporal variation in Lepidopteran larval assemblages associated with oak, Quercus crispula: the importance of leaf quality. Ecological Entomology. 2005;30(5):521–31.

13. Basset Y. Species abundance and body size relationships in insect herbivores associated with New Guinea forest trees, with particular reference to insect host-specificity. In: Stork NE, Adis J, Didham RK, editors. Canopy Arthropods. London, New York: Chapman & Hall; 1997. p. 237–64.

14. Novotny V, Basset Y. Host specificity of insect herbivores in tropical forests. Proceedings of the Royal Society of London B: Biological Sciences. 2005;272(1568):1083–90.

15. Kress WJ, García-Robledo C, Uriarte M, Erickson DL. DNA barcodes for ecology, evolution, and conservation. Trends in Ecology & Evolution. 2015;30(1):25–35.

16. Klimes P, Fibich P, Idigel C, Rimandai M. Disentangling the diversity of arboreal ant communities in tropical forest trees. PLOS One. 2015;10(2):e0117853. doi: 10.1371/journal.pone.0117853 25714831

17. Basset Y, Cizek L, Cuenoud P, Didham RK, Guilhaumon F, Missa O, et al. Arthropod Diversity in a Tropical Forest. Science. 2012;338(6113):1481–4. doi: 10.1126/science.1226727 23239740

18. Ødegaard F. Species richness of phytophagous beetles in the tropical tree Brosimum utile (Moraceae): the effects of sampling strategy and the problem of tourists. Ecological Entomology. 2004;29(1):76–88.

19. Wardhaugh CW, Stork NE, Edwards W, Grimbacher PS. The overlooked biodiversity of flower-visiting invertebrates. PLOS One. 2012;7(9):e45796. doi: 10.1371/journal.pone.0045796 23029246

20. Corff JL, Marquis RJ. Differences between understorey and canopy in herbivore community composition and leaf quality for two oak species in Missouri. Ecological Entomology. 1999;24(1):46–58.

21. Volf M, Pyszko P, Abe T, Libra M, Kotásková N, Šigut M, et al. Phylogenetic composition of host plant communities drives plant‐herbivore food web structure. Journal of Animal Ecology. 2017;86(3):556–65. doi: 10.1111/1365-2656.12646 28146344

22. Whitfeld TJS, Novotny V, Miller SE, Hrcek J, Klimes P, Weiblen GD. Predicting tropical insect herbivore abundance from host plant traits and phylogeny. Ecology. 2012;93(8):S211–S22.

23. Redmond CM, Auga J, Gewa B, Segar ST, Miller SE, Molem K, et al. High specialization and limited structural change in plant‐herbivore networks along a successional chronosequence in tropical montane forest. Ecography. 2019;42(1):162–72.

24. Reynolds BC, Crossley D Jr. Spatial variation in herbivory by forest canopy arthropods along an elevation gradient. Environmental Entomology. 1997;26(6):1232–9.

25. Kitching R, Bergelson J, Lowman M, McIntyre S, Carruthers G. The biodiversity of arthropods from Australian rainforest canopies: general introduction, methods, sites and ordinal results. Austral Ecology. 1993;18(2):181–91.

26. Lowman MD. Leaf growth dynamics and herbivory in five species of Australian rain-forest canopy trees. Journal of Ecology. 1992;80(3):433–47.

27. Schowalter TD, Zhang Y. Canopy arthropod assemblages in four overstory and three understory plant species in a mixed-conifer old-growth forest in California. Forest Science. 2005;51(3):233–42.

28. Klimes P, Idigel C, Rimandai M, Fayle TM, Janda M, Weiblen GD, et al. Why are there more arboreal ant species in primary than in secondary tropical forests? Journal of Animal Ecology. 2012;81(5):1103–12. doi: 10.1111/j.1365-2656.2012.02002.x 22642689

29. Volf M, Julkunen‐Tiitto R, Hrcek J, Novotny V. Insect herbivores drive the loss of unique chemical defense in willows. Entomologia Experimentalis et Applicata. 2015;156(1):88–98.

30. Volf M, Segar ST, Miller SE, Isua B, Sisol M, Aubona G, et al. Community structure of insect herbivores is driven by conservatism, escalation and divergence of defensive traits in Ficus. Ecology Letters. 2018;21:83–92. doi: 10.1111/ele.12875 29143434

31. Volf M, Hrcek J, Julkunen‐Tiitto R, Novotny V. To each its own: differential response of specialist and generalist herbivores to plant defence in willows. Journal of Animal Ecology. 2015;84(4):1123–32. doi: 10.1111/1365-2656.12349 25649252

32. Anderson‐Teixeira KJ, Davies SJ, Bennett AC, Gonzalez‐Akre EB, Muller‐Landau HC, Joseph Wright S, et al. CTFS‐ForestGEO: a worldwide network monitoring forests in an era of global change. Global Change Biology. 2015;21(2):528–49. doi: 10.1111/gcb.12712 25258024

33. Novotny V, Miller SE. Mapping and understanding the diversity of insects in the tropics: past achievements and future directions. Austral Entomology. 2014;53(3):259–67.

34. Novotny V, Basset Y. Seasonality of sap-sucking insects (Auchenorrhyncha, Hemiptera) feeding on Ficus (Moraceae) in a lowland rain forest in New Guinea. Oecologia. 1998;115(4):514–22. doi: 10.1007/s004420050549 28308272

35. Ribeiro DB, Freitas AV. Large-sized insects show stronger seasonality than small-sized ones: a case study of fruit-feeding butterflies. Biological Journal of the Linnean Society. 2011;104(4):820–7.

36. Basset Y, Charles E, Novotny V. Insect herbivores on parent trees and conspecific seedlings in a Guyana rain forest. Selbyana. 1999;20(1):146–58.

37. Basset Y, Horlyck V, Wright SJ. Studying forest canopies from above: the International Canopy Crane Network. Panama City: Smithsonian Tropical Research Institute and UNEP; 2003.

38. Abràmoff MD, Magalhães PJ, Ram SJ. Image processing with ImageJ. Biophotonics International. 2004;11(7):36–42.

39. Miller SE, Hrcek J, Novotny V, Weiblen GD, Hebert PD. DNA barcodes of caterpillars (Lepidoptera) from Papua New Guinea. Proceedings of the Entomological Society of Washington. 2013;115(1):107–10.

40. Miller SE, Rosati ME, Gewa B, Novotny V, Weiblen GD, Hebert PD. DNA Barcodes of Lepidoptera Reared from Yawan, Papua New Guinea. Proceedings of the Entomological Society of Washington. 2015;117(2):247–51.

41. Segar ST, Volf M, Isua B, Sisol M, Redmond CM, Rosati ME, et al. Variably hungry caterpillars: predictive models and foliar chemistry suggest how to eat a rainforest. Proceedings of the Royal Society of London B: Biological Sciences. 2017;284(1866):20171803.

42. Novotny V, Miller SE, Baje L, Balagawi S, Basset Y, Cizek L, et al. Guild-specific patterns of species richness and host specialization in plant-herbivore food webs from a tropical forest. Journal of Animal Ecology. 2010;79(6):1193–203. doi: 10.1111/j.1365-2656.2010.01728.x 20673235

43. Novotny V, Drozd P, Miller SE, Kulfan M, Janda M, Basset Y, et al. Why are there so many species of herbivorous insects in tropical rainforests? Science. 2006;313(5790):1115–8. doi: 10.1126/science.1129237 16840659

44. Novotny V, Miller SE, Leps J, Basset Y, Bito D, Janda M, et al. No tree an island: the plant-caterpillar food web of a secondary rain forest in New Guinea. Ecology Letters. 2004;7(11):1090–100.

45. Dormann CF, Gruber B, Fründ J. Introducing the bipartite package: analysing ecological networks. Interaction. 2008;1:0.2413793.

46. Bates D, Maechler M, Bolker B, Walker S. lme4: Linear mixed-effects models using Eigen and S4. R package version. 2014;1(7):1–23.

47. R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org; 2017.

48. Lewis OT, Memmott J, Lasalle J, Lyal CH, Whitefoord C, Godfray HCJ. Structure of a diverse tropical forest insect–parasitoid community. Journal of Animal Ecology. 2002;71(5):855–73.

49. Tylianakis JM, Tscharntke T, Lewis OT. Habitat modification alters the structure of tropical host–parasitoid food webs. Nature. 2007;445(7124):202–5. doi: 10.1038/nature05429 17215842

50. Straw N, Ludlow A. Small-scale dynamics and insect diversity on plants. Oikos. 1994;71(1):188–92.

51. Grandez-Rios JM, Bergamini LL, de Araújo WS, Villalobos F, Almeida-Neto M. The effect of host-plant phylogenetic isolation on species richness, composition and specialization of insect herbivores: A comparison between native and exotic hosts. PLOS One. 2015;10(9):e0138031. doi: 10.1371/journal.pone.0138031 26379159

52. Jorge LR, Prado PI, Almeida‐Neto M, Lewinsohn TM. An integrated framework to improve the concept of resource specialisation. Ecology Letters. 2014;17(11):1341–50. doi: 10.1111/ele.12347 25168335

53. Bagchi R, Gallery RE, Gripenberg S, Gurr SJ, Narayan L, Addis CE, et al. Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature. 2014;506(7486):85–8. doi: 10.1038/nature12911 24463522

54. Li HQ, Chen JY, Wang S, Xiong SZ. Evaluation of six candidate DNA barcoding loci in Ficus (Moraceae) of China. Molecular ecology resources. 2012;12(5):783–90. doi: 10.1111/j.1755-0998.2012.03147.x 22537273

55. Nakamura A, Kitching RL, Cao M, Creedy TJ, Fayle TM, Freiberg M, et al. Forests and their canopies: achievements and horizons in canopy science. Trends in Ecology & Evolution. 2017;32(6):438–51.

56. Grossman JJ, Vanhellemont M, Barsoum N, Bauhus J, Bruelheide H, Castagneyrol B, et al. Synthesis and future research directions linking tree diversity to growth, survival, and damage in a global network of tree diversity experiments. Environmental and Experimental Botany. 2018;152:68–89.

57. Ewers RM, Didham RK, Fahrig L, Ferraz G, Hector A, Holt RD, et al. A large-scale forest fragmentation experiment: the Stability of Altered Forest Ecosystems Project. Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2011;366(1582):3292–302. doi: 10.1098/rstb.2011.0049 22006969

58. Müller J, Brandl R. Assessing biodiversity by remote sensing in mountainous terrain: the potential of LiDAR to predict forest beetle assemblages. Journal of Applied Ecology. 2009;46(4):897–905.


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