Commensal interaction; Disturbance; Ecological network; Second extinction; Stability; Tropical rainforest; Ecological networks; High intensity; Individual-based; Interspecies interactions; Nestedness; Network structures; Tropical rain forest; Forestry; Nature and Landscape Conservation; Management, Monitoring, Policy and Law
Abstract :
[en] Interspecies interactions deserve more attention in biodiversity conservation since the elimination of only one species can indirectly impede the dependent species through ecological networks. Phorophytes, which provide physical support, constitute the basis for the occurrence of epiphytes. Epiphytes and their host phorophytes thus form a typical commensal interaction network. However, the impacts of phorophyte removals on the diversity and stability of epiphyte communities are poorly understood. Such understanding may illuminate guidance on forest protection and management. In this study, two species-based networks (raw species-based network and standardized species-based network) and one raw individual-based network between vascular epiphytes and phorophytes were analyzed in a tropical rainforest in Southwest China. Based on the construction of second extinction models, the robustness of epiphyte community and the dynamic of network structure were calculated for raw species-based network and individual-based network under different phorophyte removal scenarios. As a result, all three epiphyte-phorophyte networks exhibited low connectivity and moderate modularity; the nestedness of the standardized species-based network was lower than that of the raw species-based network, but remained higher than that of the raw individual-based network. The removal of the strongest interactor could lead to the rapid collapse of epiphytic communities, while the reverse order increased community robustness. Most importantly, for raw species-based and individual-based networks, we found the curves of modularity and nestedness started changing drastically and fluctuated frequently when the phorophytes’ removal rate approaches 80%. Our results suggest that the keystone phorophytes (such as generalists, large individuals and abundant species) should receive special attention in conservation efforts to sustain tropical epiphytic systems; and when subject to removal, the intensity of phorophyte removal should be kept below certain threshold to achieve long-term stability of epiphytic communities.
Hu, Hai-Xia; CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China ; University of Chinese Academy of Sciences, Beijing, China
Mo, Yu-Xuan; CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China ; University of Chinese Academy of Sciences, Beijing, China
Shen, Ting ; Université de Liège - ULiège > Integrative Biological Sciences (InBioS) ; CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China
Wu, Yi; CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China
Shi, Xian-Meng; CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China ; Ailaoshan Station for Subtropical Forest Ecosystem Studies, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Jingdong, China
Ai, Yan-Yu; CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China ; University of Chinese Academy of Sciences, Beijing, China
Lu, Hua-Zheng; CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China
Zakari, Sissou; Laboratory of Hydraulics and Environmental Modeling, Faculté d'Agronomie, Université de Parakou, Parakou, Benin
Li, Su; CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China ; Ailaoshan Station for Subtropical Forest Ecosystem Studies, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Jingdong, China
Song, Liang; CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China ; Ailaoshan Station for Subtropical Forest Ecosystem Studies, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Jingdong, China
Language :
English
Title :
Simulated high-intensity phorophyte removal mitigates the robustness of epiphyte community and destroys commensal network structure
This work was supported by the National Natural Science Foundation of China [ 32171529 ]; the Yunnan Natural Science Foundation [ 202101AT070059 ]; the Candidates of the Young and Middle Aged Academic Leaders of Yunnan Province [ 2019HB040 ]; and the Yunnan High Level Talents Special Support Plan [ YNWR-QNBJ-2020-066 ].We thank the National Forest Ecosystem Research Station at Xishuangbanna for providing canopy crane platform and plot survey data. We are grateful to Mr. Ji Wang and Mr. Jin-Long Dong for their assistance in field work. We also thank Dr. Gbadamassi G.O. Dossa for his revisions to the manuscript. This work was supported by the National Natural Science Foundation of China [32171529]; the Yunnan Natural Science Foundation [202101AT070059]; the Candidates of the Young and Middle Aged Academic Leaders of Yunnan Province [2019HB040]; and the Yunnan High Level Talents Special Support Plan [YNWR-QNBJ-2020-066].
Alarcón, R., Waser, N.M., Ollerton, J., Year-to-year variation in the topology of a plant-pollinator interaction network. Oikos 117 (2008), 1796–1807, 10.1111/j.0030-1299.2008.16987.x.
Almeida-Neto, M., Guimaraes, P., Guimaraes, P.R. Jr, Loyola, R.D., Ulrich, W., A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117 (2008), 1227–1239, 10.1111/j.0030-1299.2008.16644.x.
Almeida-Neto, M., Ulrich, W., A straightforward computational approach for measuring nestedness using quantitative matrices. Environ. Modell. Software 26 (2011), 173–178, 10.1016/j.envsoft.2010.08.003.
Bascompte, J., Jordano, P., Melian, C.J., Olesen, J.M., The nested assembly of plant-animal mutualistic networks. Proc. Natl. Acad. Sci. USA 100 (2003), 9383–9387, 10.1073/pnas.1633576100.
Bastazini, V.A.G., Debastiani, V.J., Azambuja, B.O., Guimaraes, P.R. Jr, Pillar, V.D., Loss of generalist plant species and functional diversity decreases the robustness of a seed dispersal network. Environ. Conserv. 46 (2019), 52–58, 10.1017/s0376892918000334.
Bates, D., Machler, M., Bolker, B.M., Walker, S.C., Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67 (2015), 1–48, 10.18637/jss.v067.i01.
Baumgartner, M.T., Connectance and nestedness as stabilizing factors in response to pulse disturbances in adaptive antagonistic networks. J. Theor. Biol., 486, 2020, 110073, 10.1016/j.jtbi.2019.110073.
Bluthgen, N., Menzel, F., Bluthgen, N., Measuring specialization in species interaction networks. BMC Ecol., 6, 2006, 9, 10.1186/1472-6785-6-9.
Böhnert, T., Wenzel, A., Altenhövel, C., Beeretz, L., Tjitrosoedirdjo, S.S., Meijide, A., Rembold, K., Kreft, H., Effects of land-use change on vascular epiphyte diversity in Sumatra (Indonesia). Biol. Conserv. 202 (2016), 20–29, 10.1016/j.biocon.2016.08.008.
Borrvall, C., Ebenman, B., Tomas Jonsson, T.J., Biodiversity lessens the risk of cascading extinction in model food webs. Ecol. Lett. 3 (2000), 131–136, 10.1046/j.1461-0248.2000.00130.x.
Burgos, E., Ceva, H., Perazzo, R.P., Devoto, M., Medan, D., Zimmermann, M., Maria Delbue, A., Why nestedness in mutualistic networks?. J. Theor. Biol. 249 (2007), 307–313, 10.1016/j.jtbi.2007.07.030.
Ceballos, S.J., Chacoff, N.P., Malizia, A., Interaction network of vascular epiphytes and trees in a subtropical forest. Acta Oecol.-Int. J. Ecol. 77 (2016), 152–159, 10.1016/j.actao.2016.10.007.
Colwell, R.K., Chao, A., Gotelli, N.J., Lin, S.Y., Mao, C.X., Chazdon, R.L., Longino, J.T., Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J. Plant Ecol. 5 (2012), 3–21, 10.1093/jpe/rtr044.
Cortes-Anzures, O.B., Corona-Lopez, M.A., Damon, A., Mata-Rosas, M., Flores-Palacios, A., Phorophyte type determines epiphyte-phorophyte network structure in a Mexican oak forest. Flora, 272, 2020, 151704, 10.1016/j.flora.2020.151704.
Dáttilo, W., Aguirre, A., Quesada, M., Dirzo, R., Pratt, S.C., Tropical forest fragmentation affects floral visitors but not the structure of individual-based palm-pollinator networks. PLoS ONE, 10, 2015, e0121275, 10.1371/journal.pone.0121275.
Dejean, A., Azémar, F., Petitclerc, F., Delabie, J.H.C., Corbara, B., Leroy, C., Céréghino, R., Compin, A., Highly modular pattern in ant-plant interactions involving specialized and non-specialized myrmecophytes. Sci. Nat., 105, 2018, 43, 10.1007/s00114-018-1570-0.
Díaz, I.A., Sieving, K.E., Peña-Foxon, M.E., Larraín, J., Armesto, J.J., Epiphyte diversity and biomass loads of canopy emergent trees in Chilean temperate rain forests: A neglected functional component. For. Ecol. Manage. 259 (2010), 1490–1501, 10.1016/j.foreco.2010.01.025.
Dormann, C.F., 2019. Using bipartite to describe and plot two-mode networks in R. R package version 4.0.1.
Dormann, C.F., Fründ, J., Blüthgen, N., Gruber, B., Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol. J. 2 (2009), 7–24, 10.2174/1874213000902010007.
Dormann, C.F., Strauss, R., Peres-Neto, P., A method for detecting modules in quantitative bipartite networks. Methods Ecol. Evol. 5 (2014), 90–98, 10.1111/2041-210X.12139.
Dunne, J.A., Williams, R.J., Martinez, N.D., Food-web structure and network theory: The role of connectance and size. Proc. Natl. Acad. Sci. USA 99 (2002), 12917–12922, 10.1073/pnas.192407699.
Dunne, J.A., Williams, R.J., Cascading extinctions and community collapse in model food webs. Philos. Trans. Roy. Soc. B-Biol. Sci. 364 (2009), 1711–1723, 10.1098/rstb.2008.0219.
Dunne, J.A., Williams, R.J., Martinez, N.D., Network structure and biodiversity loss in food webs: robustness increases with connectance. Ecol. Lett. 5 (2002), 558–567, 10.1046/j.1461-0248.2002.00354.x.
Francisco, T.M., Couto, D.R., Evans, D.M., Garbin, M.L., Ruiz-Miranda, C.R., Structure and robustness of an epiphyte-phorophyte commensalistic network in a neotropical inselberg. Austral Ecol. 43 (2018), 903–914, 10.1111/aec.12640.
Francisco, T.M., Couto, D.R., Garbin, M.L., Muylaert, R.L., Ruiz-Miranda, C.R., Low modularity and specialization in a commensalistic epiphyte–phorophyte network in a tropical cloud forest. Biotropica 51 (2019), 509–518, 10.1111/btp.12670.
Gaiarsa, M.P., Guimaraes, J.P.R., Interaction strength promotes robustness against cascading effects in mutualistic networks. Sci. Rep. 9 (2019), 787–793, 10.1038/s41598-018-35803-8.
Gilljam, D., Curtsdotter, A., Ebenman, B., Adaptive rewiring aggravates the effects of species loss in ecosystems. Nat. Commun., 6, 2015, 8412, 10.1038/ncomms9412.
Ginestet, C., ggplot2: Elegant graphics for data analysis. J. Roy. Statist. Soc.: Series A (Statistics in Society) 174 (2011), 245–246, 10.1111/j.1467-985X.2010.00676_9.x.
Gotelli, N., Colwell, R., Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4 (2001), 379–391, 10.1046/j.1461-0248.2001.00230.x.
Grilli, J., Rogers, T., Allesina, S., Modularity and stability in ecological communities. Nat. Commun., 7, 2016, 12031, 10.1038/ncomms12031.
Hu, H.X., Shen, T., Quan, D.L., Nakamura, A., Song, L., Structuring interaction networks between epiphytic bryophytes and their hosts in Yunnan, SW China. Front. Forests Global Change, 4, 2021, 716278, 10.3389/ffgc.2021.716278.
Kaiser-Bunbury, C.N., Muff, S., Memmott, J., Muller, C.B., Caflisch, A., The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol. Lett. 13 (2010), 442–452, 10.1111/j.1461-0248.2009.01437.x.
Kassambara, A., 2019. ggpubr: 'ggplot2' Based Publication Ready Plots. R package version 0.2.4., https://CRAN.R-project.org/package=ggpubr.
Krishna, A., Guimaraes, J.P.R., Jordano, P., Bascompte, J., A neutral-niche theory of nestedness in mutualistic networks. Oikos 117 (2008), 1609–1618, 10.1111/j.1600-0706.2008.16540.x.
Liu, L.L., Yang, B., Lu, H.Z., Wu, Y., Meng, X.J., Zhang, Y.J., Song, L., Dry-season fog water utilization by epiphytes in a subtropical montane cloud forest of southwest China. Water, 13, 2021, 3237, 10.3390/w13223237.
Mazziotta, A., Vizentin-Bugoni, J., Tottrup, A.P., Bruun, H.H., Fritz, O., Heilmann-Clausen, J., Interaction type and intimacy structure networks between forest-dwelling organisms and their host trees. Basic Appl. Ecol. 24 (2017), 86–97, 10.1016/j.baae.2017.08.003.
Memmott, J., Waser, N.M., Price, M.V., Tolerance of pollination networks to species extinctions. Proc. R. Soc. Lond. B 271 (2004), 2605–2611, 10.1098/rspb.2004.2909.
Messeder, J.V.S., Guerra, T.J., Dattilo, W., Silveira, F.A.O., Searching for keystone plant resources in fruit-frugivore interaction networks across the Neotropics. Biotropica 52 (2020), 857–870, 10.1111/btp.12804.
Morrison, B.M.L., Brosi, B.J., Dirzo, R., Gomez, J.M., Agricultural intensification drives changes in hybrid network robustness by modifying network structure. Ecol. Lett. 23 (2020), 359–369, 10.1111/ele.13440.
Morrison, B.M.L., Dirzo, R., Distinct responses of antagonistic and mutualistic networks to agricultural intensification. Ecology, 101, 2020, e03116, 10.1002/ecy.3116.
Naranjo, C., Iriondo, J.M., Riofrio, M.L., Lara-Romero, C., Evaluating the structure of commensalistic epiphyte-phorophyte networks: a comparative perspective of biotic interactions. Aob Plants, 11, 2019, plz011, 10.1093/aobpla/plz011.
Neff, F., Brändle, M., Ambarlı, D., Ammer, C., Bauhus, J., Boch, S., Hölzel, N., Klaus, V.H., Kleinebecker, T., Prati, D., Schall, P., Schäfer, D., Schulze, E.-D., Seibold, S., Simons, N.K., Weisser, W.W., Pellissier, L., Gossner, M.M., Changes in plant-herbivore network structure and robustness along land-use intensity gradients in grasslands and forests. Sci. Adv., 7, 2021, eabf3985, 10.1126/sciadv.abf3985.
Olesen, J.M., Bascompte, J., Dupont, Y.L., Jordano, P., The modularity of pollination networks. Proc. Natl. Acad. Sci. USA 104 (2007), 19891–19896, 10.1073/pnas.0706375104.
Osie, M., Shibru, S., Dalle, G., Nemomissa, S., Habitat fragmentation effects on vascular epiphytes diversity in Kafa biosphere reserve and nearby coffee agroecosystem, southwestern Ethiopia. Trop. Ecol., 2022, 10.1007/s42965-022-00223-3.
Piazzon, M., Larrinaga, A.R., Santamaría, L., Romanuk, T.N., Are nested networks more robust to disturbance? A test using epiphyte-tree, comensalistic networks. PLoS ONE, 6, 2011, e19637, 10.1371/journal.pone.0019637.
Pocock, M.J.O., Evans, D.M., Memmott, J., The robustness and restoration of a network of ecological networks. Science 335 (2012), 973–977, 10.1126/science.1214915.
R Core Team, R: A language and environment for statistical computing. 2021, R Foundation for Statistical Computing, Vienna, Austria https://www.R-project.org/.
Sanger, J.C., Kirkpatrick, J.B., Moss and vascular epiphyte distributions over host tree and elevation gradients in Australian subtropical rainforest. Aust. J. Bot. 63 (2015), 696–704, 10.1071/bt15169.
Sáyago, R., Lopezaraiza-Mikel, M., Quesada, M., Álvarez-Añorve, M.Y., Cascante-Marín, A., Bastida, J.M., Evaluating factors that predict the structure of a commensalistic epiphyte–phorophyte network. Proc. R. Soc. B., 280, 2013, 20122821, 10.1098/rspb.2012.2821.
Sheykhali, S., Fernández-Gracia, J., Traveset, A., Ziegler, M., Voolstra, C.R., Duarte, C.M., Eguíluz, V.M., Robustness to extinction and plasticity derived from mutualistic bipartite ecological networks. Sci. Rep., 10, 2020, 9783, 10.1038/s41598-020-66131-5.
Shinohara, N., Uchida, K., Yoshida, T., Contrasting effects of land-use changes on herbivory and pollination networks. Ecol. Evol. 9 (2019), 13585–13595, 10.1002/ece3.5814.
Silva, I.A., Ferreira, A.W.C., Lima, M.I.S., Soares, J.J., Networks of epiphytic orchids and host trees in Brazilian gallery forests. J. Trop. Ecol. 26 (2010), 127–137, 10.1017/s0266467409990551.
Spiesman, B.J., Inouye, B.D., Habitat loss alters the architecture of plant-pollinator interaction networks. Ecology 94 (2013), 2688–2696, 10.1890/13-0977.1.
Taylor, A., Saldaña, A., Zotz, G., Kirby, C., Díaz, I., Burns, K., Composition patterns and network structure of epiphyte-host interactions in Chilean and New Zealand temperate forests. N. Z. J. Botan. 54 (2016), 204–222, 10.1080/0028825x.2016.1147471.
Vanbergen, A.J., Woodcock, B.A., Heard, M.S., Chapman, D.S., Brody, A., Network size, structure and mutualism dependence affect the propensity for plant-pollinator extinction cascades. Funct. Ecol. 31 (2017), 1285–1293, 10.1111/1365-2435.12823.
Vergara-Torres, A.C., Pacheco-Alvarez, C.M., Flores-Palacios, A., Host preference and host limitation of vascular epiphytes in a tropical dry forest of central Mexico. J. Trop. Ecol. 26 (2010), 563–570, 10.1017/s0266467410000349.
Woods, C.L., Cardelús, C.L., DeWalt, S.J., Piper, F., Microhabitat associations of vascular epiphytes in a wet tropical forest canopy. J. Ecol. 103 (2015), 421–430, 10.1111/1365-2745.12357.
Xi, X., Gong, X., Zhang, S., Yang, N., Sun, S., Structure and robustness of “pollinators-plants-herbivores” network in the alpine meadow of the Northwestern Sichuan Province (in Chinese). Scientia Sinica Vitae 52 (2021), 449–458, 10.1360/ssv-2021-0150.
Zhao, M., Geekiyanage, N., Xu, J., Khin, M.M., Nurdiana, D.R., Paudel, E., Harrison, R.D., Bond-Lamberty, B., Structure of the epiphyte community in a tropical montane forest in SW China. PLoS ONE, 10, 2015, e0122210, 10.1371/journal.pone.0122210.
Zotarelli, H.G.S., Molina, J.M.P., Ribeiro, J.E.L.S., Sofia, S.H., A commensal network of epiphytic orchids and host trees in an Atlantic Forest remnant: A case study revealing the important role of large trees in the network structure. Austral Ecol. 44 (2019), 114–125, 10.1111/aec.12659.
Zotz, G., The systematic distribution of vascular epiphytes - a critical update. Bot. J. Linn. Soc. 171 (2013), 453–481, 10.1111/boj.12010.
Zotz, G., Weigelt, P., Kessler, M., Kreft, H., Taylor, A., EpiList 1.0: a global checklist of vascular epiphytes. Ecology, 102, 2021, e03326, 10.1002/ecy.3326.
