Invertebrates are dominant species in primary tropical rainforests, where their abundance and diversity contributes to the functioning and resilience of these globally important ecosystems. However, more than one-third of tropical forests have been logged, with dramatic impacts on rainforest biodiversity that may disrupt key ecosystem processes. We find that the contribution of invertebrates to three ecosystem processes operating at three trophic levels (litter decomposition, seed predation and removal, and invertebrate predation) is reduced by up to one-half following logging. These changes are associated with decreased abundance of key functional groups of termites, ants, beetles and earthworms, and an increase in the abundance of small mammals, amphibians and insectivorous birds in logged relative to primary forest. Our results suggest that ecosystem processes themselves have considerable resilience to logging, but the consistent decline of invertebrate functional importance is indicative of a human-induced shift in how these ecological processes operate in tropical rainforests.

] Department of Life Sciences Imperial College London Silwood Park Campus Buckhurst Road Ascot SL5 7PY UK [2] Department of Zoology University of Cambridge Downing Street Cambridge CB2 3EJ UK

] Department of Life Sciences Imperial College London Silwood Park Campus Buckhurst Road Ascot SL5 7PY UK [2] Faculty of Science University of South Bohemia Branisovska 31 Ceske Budejovice CZ 370 05 Czech Republic [3] Institute of Entomology Biology Centre of Czech Academy of Sciences Branisovska 31 Ceske Budejovice CZ 370 05 Czech Republic

] Department of Life Sciences Imperial College London Silwood Park Campus Buckhurst Road Ascot SL5 7PY UK [2] Faculty of Science University of South Bohemia Branisovska 31 Ceske Budejovice CZ 370 05 Czech Republic [3] Institute of Entomology Biology Centre of Czech Academy of Sciences Branisovska 31 Ceske Budejovice CZ 370 05 Czech Republic [4] Institute for Tropical Biology and Conservation Universiti Malaysia Sabah Jln UMS Kota Kinabalu Sabah 88400 Malaysia

] Department of Life Sciences Imperial College London Silwood Park Campus Buckhurst Road Ascot SL5 7PY UK [2] Institute of Zoology Zoological Society of London Regent's Park London NW1 4RY UK

] Department of Life Sciences Imperial College London Silwood Park Campus Buckhurst Road Ascot SL5 7PY UK [2] School of Environmental Sciences University of Liverpool Liverpool L69 3GP UK [3] Centre for Invasion Biology Department of Zoology and Entomology University of Pretoria Pretoria 0002 South Africa

] School of Biological Sciences University of East Anglia Norwich NR4 7TJ UK [2] Department of Zoology University of Cambridge Downing Street Cambridge CB2 3EJ UK

Centre for Biological Sciences University of Southampton Southampton SO17 1BJ UK

Department of Animal and Plant Sciences University of Sheffield Western Bank Sheffield S10 2TN UK

Department of Life Sciences Imperial College London Silwood Park Campus Buckhurst Road Ascot SL5 7PY UK

Durrell Institute of Conservation and Ecology School of Anthropology and Conservation University of Kent Canterbury CT2 7NR UK

Entomology Department Natural History Museum Cromwell Road London SW7 5BD UK

Environmental Futures Research Institute and Griffith School of the Environment Griffith University Nathan Queensland 4111 Australia

Faculty of Sustainable Agriculture Universiti Malaysia Sabah Locked Bag No 3 Sandakan Sabah 90509 Malaysia

Forest Research Centre Sabah Forestry Department PO Box 1407 Sandakan Sabah 90715 Malaysia

Institute for Tropical Biology and Conservation Universiti Malaysia Sabah Jln UMS Kota Kinabalu Sabah 88400 Malaysia

School of Biological Sciences University of East Anglia Norwich NR4 7TJ UK

School of Rural Animal and Environmental Sciences Nottingham Trent University Brackenhurst Campus Southwell Nottinghamshire NG25 0QF UK

See more in PubMed

Wilson E. O. The little things that run the world (the importance and conservation of invertebrates). Conserv. Biol. 1, 344–346 (1987) .

Floren A., Biun A. & Linsenmair E. Arboreal ants as key predators in tropical lowland rainforest trees. Oecologia 131, 137–144 (2002) . PubMed

Janzen D. H. Seed predation by animals. Annu. Rev. Ecol. Syst. 2, 465–492 (1971) .

Novotny V. et al.. Predation risk for herbivorous insects on tropical vegetation: a search for enemy-free space and time. Aust. J. Ecol. 24, 477–483 (1999) .

Coley P. D. & Barone J. A. Herbivory and plant defenses in tropical forests. Annu. Rev. Ecol. Syst. 27, 305–335 (1996) .

Bawa K. S. Plant-pollinator interactions in tropical rain forests. Annu. Rev. Ecol. Syst. 21, 399–422 (1990) .

Ollerton J., Winfree R. & Tarrant S. How many flowering plants are pollinated by animals? Oikos 120, 321–326 (2011) .

Simon J. G. Saproxylic insect ecology and the sustainable management of forests. Annu. Rev. Ecol. Syst. 33, 1–23 (2002) .

Hamilton A. J. et al.. Quantifying uncertainty in estimation of tropical arthropod species richness. Am. Nat. 176, 90–95 (2010) . PubMed

Hamilton A. J. et al.. Correction. Am. Nat. 177, 544–545 (2011) .

Basset Y. et al.. Arthropod diversity in a tropical forest. Science 338, 1481–1484 (2012) . PubMed

Larsen T. H., Williams N. M. & Kremen C. Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol. Lett. 8, 538–547 (2005) . PubMed

Walker B. H. Biodiversity and ecological redundancy. Conserv. Biol. 6, 18–23 (1992) .

Hirota M., Holmgren M., Van Nes E. H. & Scheffer M. Global resilience of tropical forest and savanna to critical transitions. Science 334, 232–235 (2011) . PubMed

Ewers R. M. et al.. A large-scale forest fragmentation experiment: the Stability of Altered Forest Ecosystems Project. Phil. Trans. R. Soc. B-Biol. Sci. 366, 3292–3302 (2011) . PubMed PMC

Struebig M. et al.. Quantifying the biodiversity value of repeatedly logged rainforests: gradient and comparative approaches from Borneo. Adv. Ecol. Res. 48, 183–224 (2013) .

Burivalova Z., Şekercioğlu Ç. H. & Koh L. P. Thresholds of logging intensity to maintain tropical forest biodiversity. Curr. Biol. 24, 1893–1898 (2014) . PubMed

DeAngelis K. M. et al.. Changes in microbial dynamics during long-term decomposition in tropical forests. Soil Biol. Biochem. 66, 60–68 (2013) .

Lee-Cruz L., Edwards D. P., Tripathi B. M. & Adams J. M. Impact of logging and forest conversion to oil palm plantations on soil bacterial communities in Borneo. Appl. Environ. Microbiol. 79, 7290–7297 (2013) . PubMed PMC

Hartmann M. et al.. Resistance and resilience of the forest soil microbiome to logging-associated compaction. ISME J. 8, 226–244 (2014) . PubMed PMC

Snaddon J. L. et al.. Biodiversity hanging by a thread: the importance of fungal litter-trapping systems in tropical rainforests. Biol. Lett. 8, 397–400 (2012) . PubMed PMC

Hardwick S. R. et al.. The relationship between leaf area index and microclimate in tropical forest and oil palm plantation: forest disturbance drives changes in microclimate. Agric. For. Meteorol. 201, 187–195 (2015) . PubMed PMC

Cornelius M. L. & Osbrink W. L. A. Effect of soil type and moisture availability on the foraging behavior of the Formosan subterranean termite (Isoptera: Rhinotermitidae). J. Econ. Entomol. 103, 799–807 (2010) . PubMed

Senior M. M. et al.. Trait-dependent declines of species following conversion of rain forest to oil palm plantations. Biodiv. Conserv. 22, 253–268 (2013) .

Brodie J. F. & Giordano A. Lack of trophic release with large mammal predators and prey in Borneo. Biol. Conserv. 163, 58–67 (2013) .

Wearn O. R., Rowcliffe J. M., Carbone C., Bernard H. & Ewers R. M. Assessing the status of wild felids in a highly-disturbed commercial forest reserve in Borneo and the implications for camera trap survey design. PLoS ONE 8, e77598 (2013) . PubMed PMC

Hoffmann M. et al.. The impact of conservation on the status of the world's vertebrates. Science 330, 1503–1509 (2010) . PubMed

Gibson L. et al.. Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478, 378–381 (2011) . PubMed

Bicknell J. E., Struebig M. J., Edwards D. P. & Davies Z. G. Improved timber harvest techniques maintain biodiversity in tropical forests. Curr. Biol. 24, R1119–R1120 (2014) . PubMed

Berry N., Phillips O., Ong R. & Hamer K. Impacts of selective logging on tree diversity across a rainforest landscape: the importance of spatial scale. Landsc. Ecol. 23, 915–929 (2008) .

Edwards D. P. et al.. Reduced-impact logging and biodiversity conservation: a case study from Borneo. Ecol. Appl. 22, 561–571 (2012) . PubMed

Reynolds G., Payne J., Sinun W., Mosigil G. & Walsh R. P. D. Changes in forest land use and management in Sabah, Malaysian Borneo, 1990-2010, with a focus on the Danum Valley region. Phil. Trans. R. Soc. B-Biol. Sci. 366, 3168–3176 (2011) . PubMed PMC

Marsh C. J. & Ewers R. M. A fractal-based sampling design for ecological surveys quantifying β-diversity. Methods Ecol. Evol. 4, 63–72 (2013) .

Sayer E. J., Tanner E. V. J. & Lacey A. L. Effects of litter manipulation on early-stage decomposition and meso-arthropod abundance in a tropical moist forest. For. Ecol. Manage. 229, 285–293 (2006) .

Meyer W. M. III, Ostertag R. & Cowie R. H. Macro-invertebrates accelerate litter decomposition and nutrient release in a Hawaiian rainforest. Soil Biol. Biochem. 43, 206–211 (2011) .

Schmidt P. et al.. Soil macrofauna and decomposition rates in southern Brazilian Atlantic rainforests. Ecotropica 14, 89–100 (2008) .

Ehnes R. B. et al.. Lack of energetic equivalence in forest soil invertebrates. Ecology 95, 527–537 (2014) . PubMed

Stork N. E. & Blackburn T. M. Abundance, body-size and biomass of arthropods in tropical forest. Oikos 67, 483–489 (1993) .

Barnes A. D. et al.. Consequences of tropical land use for multitrophic biodiversity and ecosystem functioning. Nat. Commun. 5, 5351 (2014) . PubMed PMC

Luke S. H., Fayle T. M., Eggleton P., Turner E. C. & Davies R. G. Functional structure of ant and termite assemblages in old growth forest, logged forest and oil palm plantation in Malaysian Borneo. Biodiv. Conserv. 23, 2817–2832 (2014) .

Hammond P. M. in Insects and the Rain Forests of South East Asia (Wallacea) eds Knight W. D., Holloway J. D. 197–254Royal Entomological Society (1990) .

Donovan S. E., Eggleton P. & Bignell D. E. Gut content analysis and a new feeding group classification of termites. Ecol. Entomol. 26, 356–366 (2001) .

Andersen A. N. in Ants—Standard Methods for Measuring and Monitoring Biodiversity eds Agosti D., Majer J. D., Alonso L. E., Schultz T. R. Smithsonian Institution (2000) .

Edwards F. A., Edwards D. P., Hamer K. C. & Davies R. G. Impacts of logging and conversion of rainforest to oil palm on the functional diversity of birds in Sundaland. Ibis 155, 313–326 (2013) .

Pfeifer M., Gonsamo A., Disney M., Pellikka P. & Marchant R. Leaf area index for biomes of the Eastern Arc Mountains: Landsat and SPOT observations along precipitation and altitude gradients. Remote Sens. Environ. 118, 103–115 (2012) .

Walsh R. P. D. & Newbery D. M. The ecoclimatology of Danum, Sabah, in the context of the world's rainforest regions, with particular reference to dry periods and their impact. Phil. Trans. R. Soc. B-Biol. Sci. 354, 1869–1883 (1999) . PubMed PMC

Bates D., Maechler M. & Bolker B. lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-39 (2011) .

R Core Team. R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing (2014) .

Hothorn T., Bretz F. & Westfall P. Simultaneous inference in general parametric models. Biom. J. 50, 346–363 (2008) . PubMed

Nakagawa S. & Schielzeth H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013) .

Bjørnstad O. & Falck W. Nonparametric spatial covariance functions: Estimation and testing. Environ. Ecol. Stat. 8, 53–70 (2001) .

Thresholds for adding degraded tropical forest to the conservation estate