Impact of rainforest conversion into monoculture plantation systems on pseudoscorpion density, diversity and trophic niches
DOI:
https://doi.org/10.25674/so93iss2id147Keywords:
stable isotopes, soil, predation, Indonesia, land-use change, rubber, oil palmAbstract
Indonesia’s biodiversity is at risk due to large forest areas being transformed into rubber and oil palm monoculture plantations. The effects of this land-use change on local fauna have been studied in a variety of organisms, including invertebrates from leaf litter and soil habitats. Litter and soil organisms are important drivers of essential ecosystem functions, such as nutrient cycling and carbon sequestration, which are impacted heavily by monoculture plantations. Pseudoscorpions (Arachnida: Pseudoscorpiones) are predatory arthropods in such litter and soil habitats and are an ubiquitous, although typically not very abundant, component of the soil animal food web. Since virtually nothing is known on their functional role diversity in tropical soil food webs, this study aims at contributing filling this gap of knowledge. We studied the impact of the conversion of rainforest into rubber and oil palm plantations on the density and diversity of pseudoscorpions in two landscapes of Jambi province, Sumatra, Indonesia, and applied stable isotope analysis to investigate changes in their trophic niches. Among 266 sorted individuals, only one described species was recorded, while the others were sorted to a total of nine morphospecies. Pseudoscorpions in the study region predominantly colonized mineral soil rather than the litter layer. As expected, the density declined from rainforest to rubber (-83%) and oil palm (-87%), and the number of species declined from rainforest to rubber (-37%) but in particular to oil palm (-47%). The density in riparian areas was five times lower than in non-riparian sites, however, species richness was almost the same. Further, the community composition of pseudoscorpions differed between land-use systems and landscapes; no species was present across all land-use systems, and the majority of species was only present in one land-use system indicating high habitat dependence. Stable isotope analysis suggested that the pseudoscorpion community shifted from species associated with the detritus-based energy channel in rainforest to species associated with the plant-based energy channel in monoculture plantations, indicating shifts in the use of basal resources by the soil community cascading up into predators. Overall, the results indicate that tropical pseudoscorpion communities comprise high-level predators that prefere to inhabit soil rather than litter and respond sensitively to land-use change. Due to this sensitivity, pseudoscorpion abundance may serve as bioindicator for ecosystem changes in the tropics. To mitigate negative effects of changes in land use in tropical ecosystems on cryptic and unexplored soil biodiversity, reduced herbicide use resulting in increased understory vegetation and mulching practices might be adopted.
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References
Adis, J. U. (1981): Comparative ecological Studies of the terrestrial arthropod fauna in Central Amazonian Inundation-Forests. – Amazoniana: Limnologia et Oecologia Regionalis Systematis Fluminis Amazonas, AMAZONIA 7(2): 87–173.
Adis, J. U. & V. Mahnert (1985): On the natural history and ecology of Pseudoscorpiones (Arachnida) from an Amazonian blackwater inundation forest. – Amazoniana: Limnologia et Oecologia Regionalis Systematis Fluminis Amazonas 9/3: 297–314.
Allen, K., M. D. Corre, A. Tjoa & E. Veldkamp (2015): Soil nitrogen-cycling responses to conversion of lowland forests to oil palm and rubber plantations in Sumatra, Indonesia. – PLoS ONE 10/7 [https://doi.org/10.1371/journal.pone.0133325].
Ashton-Butt, A., A. A. K. Aryawan, A. S. C. Hood, M. Naim, D. Purnomo, Suhardi, R. Wahyuningsih, S. Willcock, G. M.Poppy, J.-P. Caliman, E. C. Turner, W. A. Foster,
K. S.-H. Peh & J. L. Snaddon (2018): Understory Vegetation in Oil Palm Plantations Benefits Soil Biodiversity and Decomposition Rates. – Frontiers in Forests and Global Change 1 [https://doi.org/10.3389/ffgc.2018.00010].
Barnes, A. D., M. Jochum, S. Mumme, N. F. Haneda, A. Farajallah, T. H. Widarto & U. Brose (2014): Consequences of tropical land use for multitrophic biodiversity and ecosystem functioning. – Nature Communications 5/1: 5351 [https://doi.org/10.1038/ncomms6351].
Basset, Y., L. Cizek, P. Cuénoud, R. K. Didham, V. Novotny, F. Ødegaard, T. Roslin, A. K. Tishechkin, J. Schmidl, N. N. Winchester & et al (2015): Arthropod Distribution in a Tropical Rainforest: Tackling a Four Dimensional Puzzle. – PLOS ONE 10/12: e0144110 [https://doi.org/10.1371/journal.pone.0144110].
Bates, D., M. Mächler, B. Bolker & S. Walker (2015): Fitting Linear Mixed-Effects Models Using {lme4}. – Journal of Statistical Software 67/1 [https://doi.org/10.18637/jss.v067.i01].
Battirola, L. D., G. G. Brizzola dos Santos, E. Meurer, A. C. C Castilho, V. Mahnert, A. D. Brescoyit & M. I. Marques (2017): Soil and canopy Pseudoscorpiones (Arthropoda, Arachnida) in a monodominant forest of Attalea phalerata Mart. (Arecaceae) in the Brazilian Pantanal, – Studies on Neotropical Fauna and Environment 52/2: 87–94 [https://doi.org/10.1080/01650521.2017.1282210].
Beier, M. (1932): Das Tierreich: Pseudoscorpionidea I: Subord. Chthoniinea et Neobisiinea. – De Gruyter 254/57: 89–96.
Bilde, T., J. A. Axelsen & S. Toft (2000): The value of Collembola from agricultural soils as food for a generalist predator. – Journal of Applied Ecology 37/4: 672–683 [https://doi.org/10.1046/j.1365-2664.2000.00527.x.].
Briones, M. J. I. (2018): The serendipitous value of soil fauna in ecosystem functioning: The unexplained explained. – Frontiers in Environmental Science 6 [https://doi.org/10.3389/fenvs.2018.00149].
Brose, U. & S. Scheu (2014): Into darkness: unravelling the structure of soil food webs. – Oikos 123/10: 1153–1156 [https://doi.org/10.1111/oik.01768].
Clough, Y., V. V. Krishna, M. D. Corre, K. Darras, L. H. Denmead, A. Meijide, S. Moser, O. Musshoff, S. Steinebach, E. Veldkamp & et al. (2016): Land-use choices follow profitability at the expense of ecological functions in Indonesian smallholder landscapes. – Nature Communications 7/1 [13137. https://doi.org/10.1038/ncomms13137].
Cullen, K. & M. Harvey (2008): Short-range endemism in hypogean environments: The pseudoscorpion genera Tyrannochthonius and Lagynochthonius (Pseudoscorpiones: Chthoniidae) in the semiarid zone of Western Australia. – Invertebrate Systematics 22: 259–293 [https://doi.org/10.1071/IS07025].
Darras, K. F. A., M. D. Corre, , G. Formaglio, A. Tjoa, A. Potapov, F. Brambach, K. T. Sibhatu, I. Grass, A. Rubiano, D. Buchori & et al. (2019): Reducing Fertilizer and Avoiding Herbicides in Oil Palm Plantations — Ecological and Economic Valuations. – Frontiers in Forests and Global Change 2 [https://doi.org/10.3389/ffgc.2019.00065].
Dennis, P., M. R. Young & C. Bentley (2001): The effects of varied grazing management on epigeal spiders, harvestmen and pseudoscorpions of Nardus stricta grassland in upland Scotland. – Agriculture, Ecosystems & Environment 86/1: 39–57 [https://doi.org/10.1016/S0167-8809(00)00263-2].
Digel, C., A. Curtsdotter, J. Riede, B. Klarner & U. Brose (2014): Unravelling the complex structure of forest soil food webs: higher omnivory and more trophic levels. – Oikos, 123/10: 1157–1172 [https://doi.org/10.1111/oik.00865].
Drescher, J., K. Rembold, K. Allen, P. Beckschäfer, D. Buchori, Y. Clough, H. Faust, A. M. Fauzi, D. Gunawan, D. Hertel & et al. (2016): Ecological and socio-economic functions across tropical land use systems after rainforest conversion. – Philosophical Transactions of the Royal Society B: Biological Sciences 371/1694: 20150275 [https://doi.org/10.1098/rstb.2015.0275].
Drogla, R. & K. Lippold (2004): Zur Kenntnis der Pseudoskorpion-Fauna von Ostdeutschland (Arachnida, Pseudoscorpiones). – Arachnologische Mitteilungen 27/28: 1–54 [https://doi.org/10.5431/aramit2701].
Eisenhauer, N. (2010): The action of an animal ecosystem engineer: Identification of the main mechanisms of earthworm impacts on soil microarthropods. – Pedobiologia 53/6:
–352 [https://doi.org/10.1016/j.pedobi.2010.04.003].
FAO (2020): (Food Agric. Organ.). 2020. Crops. FAOSTAT statistical database, Rome, updated September 14, 2020 [http://www.fao.org/faostat/en/#data/QC. – Retrieved October 13, 2020, from http://www.fao.org/faostat/en/#data/QC].
Ferlian, O., N. Eisenhauer, M. Aguirrebengoa, M. Camara, I. Ramirez‐Rojas, F. Santos, K. Tanalgo & M. P. Thakur (2018): Invasive earthworms erode soil biodiversity: A meta-analysis. – Journal of Animal Ecology 87/1: 162–172 [https://doi.org/10.1111/1365-2656.12746].
Grass, I., C. Kubitza, V. V. Krishna, M. D. Corre, O. Mußhoff, P. Pütz, J. Drescher, K. Rembold, E. S. Ariyanti, A. D. Barnes & et al. (2020): Trade-offs between multifunctionality and profit in tropical smallholder landscapes. – Nature Communications 11/1: 1186. https://doi.org/10.1038/s41467-020-15013-5.
Guillaume, T., M. Damris & Y. Kuzyakov (2015): Losses of soil carbon by converting tropical forest to plantations: erosion and decomposition estimated by δ13C. – Global Change Biology 21/9: 3548–3560 [https://doi.org/10.1111/gcb.12907].
Harvey, M. S. (1988): The systematics and biology of pseudoscorpions – In: Austin, A. D. & N. W. Heather (eds): Australian Arachnology, Miscellanious Publication No.5 - The Australian Entomological Society, Brisbane: 75–85. – Australian Enthomological Society.
Harvey, M. S. (1992): The phylogeny and classification of the Pseudoscorpionida (Chelicerata : Arachnida). – Invertebrate Systematics 6/6: 1373–1435 (CSIRO PUBLISHING) [https://doi.org/10.1071/it9921373].
Harvey, M. S. & E. Volschenk (2007): Systematics of the Gondwanan pseudoscorpion family Hyidae (Pseudoscorpiones : Neobisioidea): new data and a revised phylogenetic hypothesis. – Invertebrate Systematics 21: 365–406 [https://doi.org/10.1071/IS05030].
Harvey, M. S. (2011): Pseudoscorpions of the World, version 1.2. Western Australian Museum, Perth [http://www.museum.wa.gov.au/catalogues/pseudoscorpions (Retrieved November 27, 2019)].
Haubert, D., M. M. Häggblom, R. Langel, S. Scheu & L. Ruess (2006): Trophic shift of stable isotopes and fatty acids in Collembola on bacterial diets. – Soil Biology and Biochemistry 38/7: 2004–2007 [https://doi.org/10.1016/j.soilbio.2005.11.031].
Hille Ris Lambers, J., P. B. Adler, W. S. Harpole, J. M. Levine & M. M. Mayfield (2012): Rethinking community assembly through the lens of coexistence theory. – Annual Review of Ecology, Evolution, and Systematics 43/1: 227–248 [https://doi.org/10.1146/annurev-ecolsys-110411-160411].
Hothorn, T., F. Bretz, P. Westfall, R. M. Heiberger, A. Schuetzenmeister & S. Scheibe (2021): multcomp: Simultaneous Inference in General Parametric Models. – Biometrical Journal 50/3: 346–363 [http://doi.wiley.com/10.1002/bimj.200810425].
Huang, C.-Y., K. L. Tully, D.A. Clark, S. F. Oberbauer & T. P. McGlynn (2012): The δ15N signature of the detrital food web tracks a landscape-scale soil phosphorus gradient in a Costa Rican lowland tropical rain forest. – Journal of Tropical Ecology 28/4: 395–403 [https://doi.org/10.1017/S0266467412000284].
Khasanah, N., M. van Noordwijk, M. Slingerland, M. Sofiyudin, D. Stomph, A. F. Migeon & K. Hairiah (2020): Oil Palm Agroforestry Can Achieve Economic and Environmental Gains as Indicated by Multifunctional Land Equivalent Ratios. – Frontiers in Sustainable Food Systems 3 [https://doi.org/10.3389/fsufs.2019.00122].
Kempson, D., M. Lloyd & R. Ghelardi (1963): A new extractor for woodland litter. – Pedobiologia 3/1: 1–21.
Klarner, B., H. Winkelmann, V. Krashevska, M. Maraun, R. Widyastuti & S. Scheu (2017): Trophic niches, diversity and community composition of invertebrate top predators (Chilopoda) as affected by conversion of tropical lowland rainforest in Sumatra (Indonesia). – PLOS ONE 12/8: e0180915 [https://doi.org/10.1371/journal.pone.0180915].
Kotowska, M. M., C. Leuschner, T. Triadiati & D. Hertel (2016): Conversion of tropical lowland forest reduces nutrient return through litterfall, and alters nutrient use efficiency and seasonality of net primary production. – Oecologia 180/2: 601–618 [https://doi.org/10.1007/s00442-015-3481-5].
Krashevska, V., E. Malysheva, B. Klarner, Y. Mazei, M. Maraun, R. Widyastuti & S. Scheu (2018): Micro-decomposer communities and decomposition processes in tropical lowlands as affected by land use and litter type. – Oecologia 187/1: 255–266 [https://doi.org/10.1007/s00442-018-4103-9].
Krause, A., D. Sandmann, S. L. Bluhm, S. Ermilov, R. Widyastuti, N. F. Haneda, S. Scheu & M. Maraun (2019): Shift in trophic niches of soil microarthropods with conversion of tropical rainforest into plantations as indicated by stable isotopes (15N, 13C). – PLOS ONE 14/10: e0224520 [https://doi.org/10.1371/journal.pone.0224520].
Lencinas, M. V., G. Kreps, R. Soler, P. L. Peri, A. Porta, M. Ramírez & G. M. Pastur (2015): Neochelanops michaelseni (Pseudoscorpiones: Chernetidae) as a potential bioindicator in managed and unmanaged Nothofagus forests of Tierra del Fuego. – The Journal of Arachnology 43/3: 406–412 [https://doi.org/10.1636/0161-8202-43.3.406]
Maraun, M., G. Erdmann, B. M. Fischer, M. M. Pollierer, R. A. Norton, Schneider, K. & S. Scheu (2011): Stable isotopes revisited: Their use and limits for oribatid mite trophic ecology. – Soil Biology and Biochemistry 43/5: 877–882 [https://doi.org/10.1016/j.soilbio.2011.01.003].
Margono, B. A., S. Turubanova, I. Zhuravleva, P. Potapov, A. Tyukavina, A. Baccini, S. Goetz & M. C. Hansen (2012): Mapping and monitoring deforestation and forest degradation in Sumatra (Indonesia) using Landsat time series data sets from 1990 to 2010. – Environmental Research Letters 7/3: 034010 [https://doi.org/10.1088/1748-9326/7/3/034010].
Marsden, C., A. Martin-Chave, J. Cortet, M. Hedde & Y. Capowiez (2020): How agroforestry systems influence soil fauna and their functions - a review. – Plant and Soil 453/1: 29–44 [https://doi.org/10.1007/s11104-019-04322-4].
Mumme, S., M. Jochum, U. Brose, N. F. Haneda & A. D. Barnes (2015): Functional diversity and stability of litter-invertebrate communities following land-use change in Sumatra, Indonesia. – Biological Conservation 191: 750–758 [https://doi.org/10.1016/j.biocon.2015.08.033].
Muster, C. & T. Blick (2015): Pseudoscorpions (Arachnida: Pseudoscorpiones) in strict forest reserves in Hesse (Germany). – Arachnologische Mitteilungen 50: 37–50 [https://doi.org/10.5431/aramit5006].
Nazarreta, R., T. R. Hartke, P. Hidayat, S. Scheu, B. Damayanti & J. Drescher (2020): Rainforest conversion to smallholder plantations of rubber or oil palm leads to species loss and community shifts in canopy ants (Hymenoptera: Formicidae). – Myrmecological News 30: 175–186 [https://doi.org/10.25849/MYRMECOL.NEWS_030:175].
Oelbermann, K. & S. Scheu (2010): Trophic guilds of generalist feeders in soil animal communities as indicated by stable isotope analysis (15N/14N). – Bulletin of Entomological Research 100/5: 511–520 [https://doi.org/10.1017/S0007485309990587].
Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos & et al. (2020): vegan: Community Ecology Package.
Paoletti, A., K. Darras, H. Jayanto, I. Grass, M. Kusrini & T. Tscharntke (2018): Amphibian and reptile communities of upland and riparian sites across Indonesian oil palm, rubber and forest. – Global Ecology and Conservation 16: e00492 [https://doi.org/10.1016/j.gecco.2018.e00492].
Pollierer, M. M., R. Langel, C. Körner, M. Maraun & S. Scheu (2007): The underestimated importance of belowground carbon input for forest soil animal food webs. – Ecology Letters 10/8: 729–736 [https://doi.org/10.1111/j.1461-0248.2007.01064.x].
Pollierer, M. M., R. Langel, S. Scheu & M. Maraun (2009): Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15N/14N and 13C/12C). – Soil Biology and Biochemistry 41/6: 1221–1226 [https://doi.org/10.1016/j.soilbio.2009.03.002].
Post, D. M. (2002): Using stable isotopes to estimate trophic position: Models, methods, and assumptions. – Ecology 83/3: 703–718 [https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2].
Potapov, A. M., A. V. Tiunov & S. Scheu (2019a): Uncovering trophic positions and food resources of soil animals using bulk natural stable isotope composition. – Biological Reviews 94/1: 37–59 [https://doi.org/10.1111/brv.12434].
Potapov, A. M., B. Klarner, D. Sandmann, R. Widyastuti & S. Scheu (2019b): Linking size spectrum, energy flux and trophic multifunctionality in soil food webs of tropical land-use systems. – Journal of Animal Ecology 88/12: 1845–1859.[https://doi.org/10.1111/1365-2656.13027].
Potapov, A. M., U. Brose, S. Scheu & A. V. Tiunov (2019c): Trophic position of consumers and size structure of food webs across aquatic and terrestrial ecosystems. – The American Naturalist 194/6: 823–839 [https://doi.org/10.1086/705811].
Potapov, A. M., N. Dupérré, M. Jochum, K. Dreczko, B. Klarner, A. D. Barnes, V. Krashevska, K. Rembold, H. Kreft, U. Brose, R. Widyastuti, D. Harms & S. Scheu (2020): Functional losses in ground spider communities due to habitat structure degradation under tropical land-use change. – Ecology 101/3: e02957 [https://doi.org/10.1002/ecy.2957].
Potapov, A. M., I. Schaefer, M. Jochum, R. Widyastuti, N. Eisenhauer & S. Scheu (2021): Oil palm and rubber expansion facilitates earthworm invasion in Indonesia. – Biological Invasions [https://doi.org/10.1007/s10530-021-02539-y].
R Core Team (2018): R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria [https://www.R-project.org/. – httg://www.R-project.org/. Retrieved February 25, 2020, from https://www.r-project.org/].
Riede, J. O ., U. Brose, B. Ebenman, U. Jacob, R. Thompson, C. R. Townsend & T. Jonsson (2011a): Stepping in Elton’s footprints: a general scaling model for body masses and trophic levels across ecosystems. – Ecology Letters 14/2: 169–178 [https://doi.org/10.1111/j.1461-0248.2010.01568.x].
Rooney, N., K. McCann, G. Gellner & J. C. Moore (2006): Structural asymmetry and the stability of diverse food webs. – Nature 442/7100: 265–269 [https://doi.org/10.1038/nature04887].
Sahner, J., S. W. Budi, H. Barus, N. Edy, M. Meyer, M. D. Corre & A. Polle (2015): Degradation of root community traits as indicator for transformation of tropical lowland rain forests into oil palm and rubber plantations. – PLOS ONE 10/9: e0138077 [https://doi.org/10.1371/journal.pone.0138077].
Scheu, S. (2002): The soil food web: structure and perspectives. – European Journal of Soil Biology 38/1: 11–20 [https://doi.org/10.1016/S1164-5563(01)01117-7].
Sodhi, N. S., L. P. Koh, B. W. Brook & P. K. L. Ng (2004): Southeast Asian biodiversity: an impending disaster. – Trends in Ecology & Evolution 19/12: 654–660 [https://doi.org/10.1016/j.tree.2004.09.006].
Susanti, W. I., M. W. Pollierer, R. Widyastuti, S. Scheu & A. Potapov (2019): Conversion of rainforest to oil palm and rubber plantations alters energy channels in soil food webs. – Ecology and Evolution 9/16: 9027–9039 [https://doi.org/10.1002/ece3.5449].
Villarreal, E., N. Martínez & C. Romero-Ortiz (2019): Diversity of Pseudoscorpiones (Arthropoda: Arachnida) in two fragments of dry tropical forest in the colombian Caribbean region. – Caldasia 41/1: 139–151 [https://doi.org/10.15446/caldasia.v41n1.72189].
Weygoldt, P. (1969): The biology of Pseudoscorpions. – 168 pp. (Harvard University Press).
Wickham, H., W. Chang, L. Henry, T. L. Pedersen, K. Takahashi, C. Wilke, K. Woo, H. Yutani, D. Dunnington & RStudio (2020): ggplot2: Create Elegant Data Visualisations Using the Grammar of Graphics.
Yamamoto, T., N. Nakagoshi & Y. Touyama (2001): Ecological study of pseudoscorpion fauna in the soil organic layer in managed and abandoned secondary forests: Pseudoscorpions and forest management. – Ecological Research 16/3: 593–601 [https://doi.org/10.1046/j.1440-1703.2001.00422.x].
Yang, X., M. Warren & X. Zou (2007): Fertilization responses of soil litter fauna and litter quantity, quality, and turnover in low and high elevation forests of Puerto Rico. – Applied Soil Ecology 37/1–2: 63–71 [https://doi.org/10.1016/j.apsoil.2007.03.012].
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