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Temporal changes in arthropod activity in tropical anthropogenic forests

Published online by Cambridge University Press:  14 February 2018

G.-J. Brandon-Mong ,
J.E. Littlefair ,
K.-W. Sing ,
Y.-P. Lee ,
H.-M. Gan ,
E.L. Clare  and
J.-J. Wilson
G.-J. Brandon-Mong
Affiliation:
Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia Biodiversity Research Center, Academia Sinica, No. 28, Lane 70, Section 2, Yanjiuyuan Road, Nangang District, Taipei City, 115, Taiwan
J.E. Littlefair
Affiliation:
School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Rd., London, E1 4NS, UK Department of Biology, McGill University, 1205 Docteur Penfield, Montréal, Québec H3A 1B1, Canada
K.-W. Sing
Affiliation:
South China DNA Barcoding Center, Kunming Institute of Zoology, Chinese Academy of Sciences, 32 Jiaochang Donglu, 650223 Kunming, Yunnan, P. R. China
Y.-P. Lee
Affiliation:
School of Science, Monash University Malaysia, Jalan Lagoon Selatan, Bandar Sunway, 47500 Petaling Jaya, Selangor, Malaysia Monash University Malaysia Genomics Facility, Monash University Malaysia, Jalan Lagoon Selatan, Bandar Sunway 47500 Petaling Jaya, Selangor, Malaysia
H.-M. Gan
Affiliation:
School of Science, Monash University Malaysia, Jalan Lagoon Selatan, Bandar Sunway, 47500 Petaling Jaya, Selangor, Malaysia Monash University Malaysia Genomics Facility, Monash University Malaysia, Jalan Lagoon Selatan, Bandar Sunway 47500 Petaling Jaya, Selangor, Malaysia Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong, Victoria 3220, Australia
E.L. Clare
Affiliation:
School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Rd., London, E1 4NS, UK
J.-J. Wilson*
Affiliation:
International College Beijing, China Agricultural University, Beijing, 100083, P. R. China School of Applied Sciences, Faculty of Computing, Engineering and Science, University of South Wales, Pontypridd, CF37 4DB, United Kingdom Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok 65000, Thailand
*
*Author for correspondence Phone: +447456690249 E-mail: wilso04@gmail.com; johnjameswilson@qq.com
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Abstract

Arthropod communities in the tropics are increasingly impacted by rapid changes in land use. Because species showing distinct seasonal patterns of activity are thought to be at higher risk of climate-related extirpation, global warming is generally considered a lower threat to arthropod biodiversity in the tropics than in temperate regions. To examine changes associated with land use and weather variables in tropical arthropod communities, we deployed Malaise traps at three major anthropogenic forests (secondary reserve forest, oil palm forest, and urban ornamental forest (UOF)) in Peninsular Malaysia and collected arthropods continuously for 12 months. We used metabarcoding protocols to characterize the diversity within weekly samples. We found that changes in the composition of arthropod communities were significantly associated with maximum temperature in all the three forests, but shifts were reversed in the UOF compared with the other forests. This suggests arthropods in forests in Peninsular Malaysia face a double threat: community shifts and biodiversity loss due to exploitation and disturbance of forests which consequently put species at further risk related to global warming. We highlight the positive feedback mechanism of land use and temperature, which pose threats to the arthropod communities and further implicates ecosystem functioning and human well-being. Consequently, conservation and mitigation plans are urgently needed.

Keywords

Insectsbiodiversityglobal warmingland-useMalaise trapmetabarcoding
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 6 , December 2018 , pp. 792 - 799
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Copyright
Copyright © Cambridge University Press 2018 

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References

Akhiri, M.F.M. & Yong, J.C. (2011) Seasonal variation of water characteristics during inter-monsoon along the east coast of Johor. Journal of Sustainability Science and Management 6, 206–214.Google Scholar
Alvey, A.A. (2006) Promoting and preserving biodiversity in the urban forest. Urban Forestry and Urban Greening 5, 195–201.Google Scholar
Andrew, N.R., Hart, R.A., Jung, M.P., Hemmings, Z. & Terblanche, J.S. (2013) Can temperate insects take the heat? A case study of the physiological and behavioural responses in a common ant, Iridomyrmex purpureus (Formicidae), with potential climate change. Journal of Insect Physiology 59, 870–880.Google Scholar
Aneni, T.I., Aisagbonhi, C.I., Iloba, B.N., Adaigbe, V.C. & Ogbebor, C.O. (2014) Influence of weather factors on seasonal population dynamics of Coelaenomenodera elaeidis (Coleoptera: Chrysomelidae) and its natural enemies in NIFOR, Nigeria. American Journal of Plant Sciences 5, 42–47.Google Scholar
Anu, A., Sabu, T.K. & Vineesh, P.J. (2009) Seasonality of litter insects and relationship with rainfall in a wet evergreen forest in South Western Ghats. Journal of Insect Science 9, 46.Google Scholar
Austin, K.G., Kasibhatla, P.S., Urban, D.L., Stolle, F. & Vincent, J. (2015) Reconciling oil palm expansion and climate change mitigation in Kalimantan, Indonesia. PLoS ONE 10, e0127963.Google Scholar
Bale, J.S. & Hayward, S.A. (2010) Insect overwintering in a changing climate. The Journal of Experimental Biology 213, 980–994.Google Scholar
Beng, K.C., Tomlinson, K.W., Shen, X.H., Surget-Groba, Y., Hughes, A.C., Corlett, R.T. & Slik, J.W. (2016) The utility of DNA metabarcoding for studying the response of arthropod diversity and composition to land-use change in the tropics. Scientific Reports 6, 24965.Google Scholar
Benoit, J.B. & Denlinger, D.L. (2010) Meeting the challenges of on-host and off-host water balance in blood-feeding arthropods. Journal of Insect Physiology 56, 1366–1376.Google Scholar
Brandon-Mong, G.J., Gan, H.M., Sing, K.W., Lee, P.S., Lim, P.E. & Wilson, J.J. (2015) DNA metabarcoding of insects and allies: an evaluation of primers and pipelines. Bulletin of Entomological Research 105, 717–727.Google Scholar
Colinet, H., Sinclair, B.J., Vernon, P. & Renault, D. (2015) Insects in fluctuating thermal environments. Annual Review of Entomology 60, 123–140.Google Scholar
Corlett, R.T. (2011) Impacts of warming on tropical lowland rainforests. Trends in Ecology and Evolution 26, 606–613.Google Scholar
Corley, R.H.V. & Tinker, P.B.H. (2016) The oil Palm. 5th edn. Chapter 14. p. 458. UK, John Wiley & Sons, Ltd.Google Scholar
Crawley, M.J. (2012) The R Book. 2nd edn. Chapter 9, p. 393. UK, John Wiley & Sons, Ltd.Google Scholar
Fayle, T.M., Turner, E.C., Snaddon, J.L., Chey, V.K., Chung, A.Y.C., Eggleton, P. & Foster, W.A. (2010) Oil palm expansion into rain forest greatly reduces ant biodiversity in canopy, epiphytes and leaf-litter. Basic and Applied Ecology 11, 337–345.Google Scholar
Fitzherbert, E.B., Struebig, M.J., Morel, A., Danielsen, F., Brühl, C.A., Donald, P. F. & Phalan, B. (2008) How will oil palm expansion affect biodiversity? Trends in Ecology and Evolution 23, 538–545.Google Scholar
Foottit, R.G. & Adler, P.H. (2009) Insect Biodiversity Science and Society. Chapter 2. p. 8. UK, John Wiley & Sons Ltd.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Forestry Department Peninsular Malaysia, Kuala Lumpur, Malaysia. (2016) Forestry Statistics Peninsular Malaysia 2014. Link: http://www.forestry.gov.my/jpsm/index.php/my/pusat-sumber/2016-06-07-03-12-29 (accessed 11 January 2017).Google Scholar
Gill, S.E., Handley, J.F., Ennos, A.R. & Pauleit, S. (2007) Adapting cities for climate change: the role of the green infrastructure. Built Environment 33, 115–133.Google Scholar
Gunarso, P., Hartoyo, M.E., Agus, F. & Killeen, T.J. (2013) Oil palm and land use change in Indonesia, Malaysia and Papua New Guinea. pp. 65–88. in Killeen, T. J. & Goon, J. (Eds) Reports From the Technical Panels of the Second RSPO GHG Working Group, Roundtable for Sustainable Palm Oil – RSPO. Kuala Lumpur. The Netherlands: Tropenbos International.Google Scholar
Hafezatul Rasyidah, O. (2010) Wind environment evaluation on major town of Malaysia. (Unpublished bachelor's thesis). Faculty of civil engineering & earth resources, Universiti Malaysia Pahang, Pahang, Malaysia.Google Scholar
Haines-Young, R. & Potschin, M. (2010) The links between biodiversity, ecosystem services and human well-being. Chapter 6. pp. 1–31. in Raffaelli, D. & Frid, C. (Eds) Ecosystem Ecology: A New Synthesis. BES Ecological Reviews Series. Cambridge, CUP, in press.Google Scholar
Jaworski, T. & Hilszczański, J. (2013) The effect of temperature and humidity changes on insects development their impact on forest ecosystems in the expected climate change. Forest Research Papers 74, 345–355.Google Scholar
Koh, L.P. (2008) Can oil palm plantations be made more hospitable for forest butterflies and birds? Journal Applied Ecology 45, 1002–1009.Google Scholar
Lachin, J.M. (1981) Introduction to sample size determination and power analysis for clinical trials. Controlled Clinical Trials 2, 93–113.Google Scholar
Lahondère, C. & Lazzari, C.R. (2012) Mosquitoes cool down during blood feeding to avoid overheating. Current Biology 22, 40–45.Google Scholar
Lease, H.M., Goelst, K., Seely, M.K. & Mitchell, D. (2014) Evidence of temperature-independent metabolic rates in diurnal Namib Desert tenebrionid beetles. Physiological Entomology 39, 254–262.Google Scholar
Lee, P.S., Gan, H.M., Clements, G.R. & Wilson, J.J. (2016) Field calibration of blowfly-derived DNA against traditional methods for assessing mammal diversity in tropical forests. Genome 59, 1008–1022.Google Scholar
Leray, M. & Knowlton, N. (2016) Visualizing patterns of marine eukaryotic diversity from metabarcoding data using QIIME. Methods in Molecular Biology 1452, 219–235.Google Scholar
Leray, M., Yang, J.Y., Meyer, C.P., Mills, S.C., Agudelo, N., Ranwez, V., Boehm, J.T. & Machida, R.J. (2013) A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Frontiers in Zoology 10, 34.Google Scholar
Liow, L.H., Sodhi, N. S. & Elmqvist, T. (2001) Bee diversity along a disturbance gradient in tropical lowland forests of South-East Asia. Journal of Applied Ecology 38, 180–192.Google Scholar
Luskin, M.S. & Potts, M.D. (2011) Microclimate and habitat heterogeneity through the oil palm lifecycle. Basic and Applied Ecology 12, 540–551.Google Scholar
McMurdie, P.J. & Holmes, S. (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Computational Biology 10, e1003531.Google Scholar
Mora, C., Frazier, A.G., Longman, R.J., Dacks, R.S., Walton, M.M., Tong, E.J., Sanchez, J.J., Kaiser, L.R., Stender, Y.O., Anderson, J.M., Ambrosino, C.M., Fernandez-Silva, I., Giuseffi, L.M. & Giambelluca, T.W. (2013) The projected timing of climate departure from recent variability. Nature 502, 183–187.Google Scholar
MPOB (2016) Malaysia: Distribution of oil palm planted area by state and sector in 2014. Link: http://www.data.gov.my/data/en_US/dataset/malaysia-distribution-of-oil-palm-planted-area-by-state-and-sector-in-2014/resource/9b6fcd3b-f361-42c2-ae6f-e668f4efcf11 (accessed 11 January 2017).Google Scholar
NASA. Link: http://climate.nasa.gov/vital-signs/global-temperature/ (accessed 7 April 2015).Google Scholar
National Physical Plan-2 (2010) Federal Department of Town and Country Planning. Ministry of Housing and Local Government. Link: http://www.townplan.gov.my/download/National%20Physical%20Plan(kecik).pdf (accessed 27 January 2017).Google Scholar
Nazareth, T., Seixas, G. & Sousa, C.A. (2016) Climate Change and Mosquito-Borne Diseases. Part of the Series Climate Change Management. pp. 187–199. Switzerland: Springer International Publishing.Google Scholar
Nichols, E., Spector, S., Louzada, J., Larsen, T., Amezquita, S. & Favila, M.E. & The Scarabaeinae Research Network. (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation 141, 1461–1474.Google Scholar
Pacifici, M., Foden, W.B., Visconti, P., Watson, J.E.M., Butchart, S.H.M., Kovacs, K.M., Scheffers, B.R., Hole, D.G., Martin, T.G., Akçakaya, H.R., Corlett, R.T., Huntley, B., Bickford, D., Carr, J.A., Hoffmann, A.A., Midgley, G.F., Pearce-Kelly, P., Pearson, R.G., Williams, S.E., Willis, S.G. & Young, B. & Rondinini, C. (2015) Assessing species vulnerability to climate change. Nature Climate Change 5, 215–224.Google Scholar
Pincebourde, S., Sinoquet, H., Combes, D. & Casas, J. (2007) Regional climate modulates the canopy mosaic of favourable and risky microclimates for insects. Journal of Animal Ecology 76, 424–438.Google Scholar
Pinheiro, F., Diniz, I.R., Coelho, D. & Bandeira, M.P.S. (2002) Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecology 27, 132–136.Google Scholar
Piyaphongkul, J., Pritchard, J. & Bale, J. (2012) Can tropical insects stand the heat? A case study with the brown planthopper Nilaparvata lugens (Stål). PLoS ONE 7, e29409.Google Scholar
Plant, A.R., Surin, C., Saokhod, R. & Srisuka, W. (2011). Higher taxon diversity, abundance and community structure of Empididae, Hybotidae and Brachystomatidae (Diptera: Empidoidea) in tropical forests - results of mass sampling in Thailand. Studia dipterologica 18, 121–149.Google Scholar
Porter, E.E., Forschner, B.R. & Blair, R.B. (2001) Woody vegetation and canopy fragmentation along a forest-to-urban gradient. Urban Ecosystem 5, 131–151.Google Scholar
Price, P.W., Denno, R.F., Eubanks, M.D., Finke, D.L. & Kaplan, I. (2011) Ecosystem Processes. Chapter 1.7. In: Insect Ecology: Behavior, Populations and Communities. UK: Cambridge University Press.Google Scholar
Putz, F.E., Zuidema, P.A., Pinard, M.A., Boot, R.G., Sayer, J.A., Sheil, D., Sist, P., Elias, & Vanclay, J.K. (2008) Improved tropical forest management for carbon retention. PLoS Biology 6, e166.Google Scholar
Ratnasingham, S. & Hebert, P.D.N. (2007) BOLD: the Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes 7, 355–364.Google Scholar
Roberts, D.L., Cooper, R.J. & Petit, L.J. (2000) Use of premontane moist forest and shade coffee agroecosystems by army ants in western Panama. Conservation Biology 14, 192–199.Google Scholar
Schmieder, R. & Edwards, R. (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27, 863–864.Google Scholar
Schneider, A., Mertes, C.M., Tatem, A.J., Tan, B., Sulla-Menashe, D., Graves, S.J., Patel, N.N., Horton, J.A., Gaughan, A.E. & Rollo, J.T. (2015) A new urban landscape in East–Southeast Asia, 2000–2010. Environmental Research Letters 10, 3.Google Scholar
Senior, M.J.M., Hamer, K.C., Bottrell, S., Edwards, D.P., Fayle, T.M., Lucey, J.M., Mayhew, P.J., Newton, R., Peh, K.S.H., Sheldon, F.H., Stewart, C., Styring, A.R., Thom, M.D.F., Woodcock, P. & Hill, J.K. (2013) Trait-dependent declines of species following conversion of rain forest to oil palm plantations. Biodiversity and Conservation 22, 253–268.Google Scholar
Sing, K.W., Syaripuddin, K. & Wilson, J.J. (2013) Changing perspectives on the diversity of bats (Chiroptera) at Ulu Gombak since the establishment of the Field Studies Centre in 1965. Raffles Bulletin of Zoology S29, 211–217.Google Scholar
Sing, K.W., Jusoh, W.F.A., Hashim, N.R. & Wilson, J.J. (2016a) Urban parks: refuges for tropical butterflies in Southeast Asia? Urban Ecosystems 19, 1131–1147.Google Scholar
Sing, K.W., Dong, H., Wang, W.Z. & Wilson, J.J. (2016b) Can butterflies cope with city life? Butterfly diversity in a young megacity in southern China. Genome 59, 751–761.Google Scholar
Sittichaya, W., Thaochan, N. & Tasen, W. (2013) Powderpost beetle communities (Coleoptera: Bostrichidae) in durian-based agricultural areas in southern Thailand. Kasetsart Journal: Natural Science 47, 374–386.Google Scholar
Sugiura, S., Tanaka, R., Taki, H. & Kanzaki, N. (2013) Differential responses of scavenging arthropods and vertebrates to forest loss maintain ecosystem function in a heterogeneous landscape. Biological Conservation 159, 206–213.Google Scholar
Syaripuddin, K., Sing, K.W. & Wilson, J.J. (2015) Comparison of butterflies, bats and beetles as bioindicators based on four key criteria and DNA barcodes. Tropical Conservation Science 8, 138–149.Google Scholar
Tangang, F.T., Liew, J., Salimun, E., Kwan, M.S., Loh, J.L. & Muhamad, H. (2012) Climate change and variability over Malaysia: gaps in science and research information. Sains Malaysiana 41, 1355–1366.Google Scholar
Teuscher, M., Gérard, A., Brose, U., Buchori, D., Clough, Y., Ehbrecht, M., Hölscher, D., Irawan, B., Sundawati, L., Wollni, M. & Kreft, H. (2016) Experimental biodiversity enrichment in Oil-palm-dominated landscapes in Indonesia. Frontiers in Plant Science 7, 1538.Google Scholar
Uno, S., Cotton, J. & Philpott, S.M. (2010) Diversity, abundance, and species composition of ants in urban green spaces. Urban Ecosystems 13, 425–441.Google Scholar
Vanbergen, A. J. (2013) Threats to an ecosystem service: pressures on pollinators. Frontiers in Ecology and the Environment 5, 251–259.Google Scholar
Verdú, J.R., Díaz, A. & Galante, E. (2004) Thermoregulatory strategies in two closely related sympatric Scarabaeus species (Coleoptera: Scarabaeinae). Physiological Entomology 29, 32–38.Google Scholar
Verdú, J.R., Alba-Tercedor, J. & Jiménez-Manrique, M. (2012) Evidence of different thermoregulatory mechanisms between two sympatric Scarabaeus species using infrared thermography and micro-computer tomography. PLoS ONE 7, e33914.Google Scholar
Weisser, W.W. & Siemann, E. (2004) The various effects of insects on ecosystem functioning. pp. 3–24. in Insects and Ecosystem Function. Berlin Heidelberg, Springer.Google Scholar
Wilby, R.L. & Perry, G.L.W. (2006) Climate change, biodiversity and the urban environment: a critical review based on London, UK. Progress in Physical Geography 30, 73–98.Google Scholar
Wilson, J.J., Sing, K.W., Lee, P.S. & Wee, A.K. (2016) Application of DNA barcodes in wildlife conservation in tropical East Asia. Conservation Biology 30, 982–989.Google Scholar
Wong, M.M., Lim, C.L. & Wilson, J.J. (2015) DNA barcoding implicates 23 species and four orders as potential pollinators of Chinese knotweed (Persicaria chinensis) in Peninsular Malaysia. Bulletin of Entomological Research 105, 515–520.Google Scholar
Zeale, M.R.K., Butlin, R.K., Barker, G.L.A., Lees, D.C. & Jones, G. (2011) Taxon-specific PCR for DNA barcoding arthropod prey in bat faeces. Molecular Ecology Resources 11, 236–244.Google Scholar
Zhang, K., Lin, S.L., Ji, Y.Q., Yang, C.X., Wang, X.Y., Yang, C.Y., Wang, H., Jiang, H., Harrison, R.D. & Yu, D.W. (2016) Plant diversity accurately predicts insect diversity in two tropical landscapes. Molecular Ecology 25, 4407–4419.Google Scholar
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