Temporal variation in abundance of leaf litter beetles and ants in an Australian lowland tropical rainforest is driven by climate and litter fall

Abstract

Determining if the seasonality of leaf litter invertebrate populations in tropical rainforests is driven by climate or availability of litter, or both, is important to more accurately predict the vulnerability of litter invertebrates to climate change. Here we used two approaches to disentangle these effects. First, the influence of climatic seasonality was quantified by sampling a fixed volume of litter monthly over 4 years and counting extracted beetles and ants. Second, litter volume was experimentally manipulated (addition and exclusion) to test the influence of litter quantity independently of climatic variation. There were significant seasonal peaks for both beetle and ant abundance and these were positively correlated with rainfall, temperature and litter volume. As abundance was measured on a ‘per litter volume’ basis we conclude that there was a significant effect of climate on abundance. The litter manipulation experiment showed that beetle and ant abundance per litter volume were also influenced by litter volume, when it was low. We recognise that other factors such as litter structure or complexity may have affected temporal ant abundance. Beetle and ant abundance were depressed in litter exclusion plots but did not differ significantly between control and addition plots, suggesting a possible ceiling in the effect of litter volume on population sizes. We conclude that seasonality in climate and litter quantity are driving most temporal variation in insect abundance and that there may be some resilience among leaf litter insects to cope with higher temperatures. However, future responses by plants to increased climatic variability and higher CO2 concentrations may alter litter fall dynamics and thus temporal patterns in litter insect abundances.

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References

  1. Abbott KL, Green PT (2007) Collapse of an ant-scale mutualism in a rainforest on Christmas Island. Oikos 116:1238–1246

    Article  Google Scholar 

  2. Andrew NR, Hart RA, Jung M-P, Hemmings Z, Terblanche JS (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. J Insect Physiol 59:870–880

    Article  PubMed  CAS  Google Scholar 

  3. Anu A, Sabu TK (2007) Seasonal variation in the litter chemical quality of a wet evergreen forest in the Western Ghats. Curr Sci 93:391–394

    CAS  Google Scholar 

  4. Armbrecht I, Perfecto I, Vandermeer J (2004) Enigmatic biodiversity correlations: ant diversity responds to diverse resources. Science 304:284–286

    Article  PubMed  CAS  Google Scholar 

  5. Basu P (1997) Seasonal and spatial patterns in ground foraging ants in a rain forest in the western Ghats, India. Biotropica 29:489–500

    Article  Google Scholar 

  6. Bluethgen N, Stork NE, Fiedler K (2004) Bottom-up control and co-occurrence in complex communities: honeydew and nectar determine a rainforest ant mosaic. Oikos 106:344–358

    Article  Google Scholar 

  7. Brasell HM, Unwin GL, Stocker GC (1980) Quantity, temporal distribution and mineral-element content of litterfall in two forest types at two sites in tropical Australia. J Ecol 68:123–139

    Article  CAS  Google Scholar 

  8. Burghouts T, Ernsting G, Korthals G, De Vires T (1992) Litterfall, leaflitter decomposition and litter invertebrates in primary and selectively logged dipterocarp forests in Sabah, Malaysia. In: Marshall AG, Swaine MD (eds) Tropical rainforest: disturbance and recovery. Philosophical Transactions of the Royal Society of London, London, pp 407–416

    Google Scholar 

  9. Chave J, Navarrete D, Almeida S, Alvarez E, Aragao L, Bonal D, Chatelet P, Silva-Espejo JE, Goret JY, von Hildebrand P, Jimenez E, Patino S, Penuela MC, Phillips OL, Stevenson P, Malhi Y (2010) Regional and seasonal patterns of litterfall in tropical South America. Biogeosciences 7:43–55

    Article  Google Scholar 

  10. Colwell RK, Brehm G, Cardelus CL, Gilman AC, Longino JT (2008) Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322:258–261

    Article  PubMed  CAS  Google Scholar 

  11. Corlett RT (2011) Impacts of warming on tropical lowland rainforests. Trends Ecol Evol 26:606–613

    Article  PubMed  Google Scholar 

  12. Delsinne T, Arias-Penna T, Leponce M (2013) Effect of rainfall exclusion on ant assemblages in montane rainforests of Ecuador. Basic Appl Ecol 14(4):357–365

    Article  Google Scholar 

  13. Diamond SE, Sorger DM, Hulcr J, Pelini SL, Toro ID, Hirsch C, Oberg E, Dunn RR (2012) Who likes it hot? A global analysis of the climatic, ecological, and evolutionary determinants of warming tolerance in ants. Glob Change Biol 18:448–456

    Article  Google Scholar 

  14. Didham RK, Springate N (2003) Determinants of temporal variation in canopy arthropod community structure. In: Basset Y, Novotny V, Miller SE, Kitching RL (eds) Arthropods of tropical forests. Spatio-temporal dynamics and resource use in the canopy. Cambridge University Press, Cambridge, pp 28–39

    Google Scholar 

  15. Donoso DA, Johnston MK, Kaspari M (2010) Trees as templates for tropical litter arthropod diversity. Oecologia 164:201–211

    Article  PubMed  Google Scholar 

  16. Edwards W, Liddell MJ, Franks P, Nichols C, Laurance SGW (2017) Seasonal patterns in rainforest litterfall: detecting endogenous and environmental influences from long-term sampling. Austral Ecol 43:225–235

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  18. Frith D, Frith C (1990) Seasonality of litter invertebrate populations in an Australian upland tropical rainforest. Biotropica 22:181–190

    Article  Google Scholar 

  19. Frouz J, Jilkova V (2008) The effect of ants on soil properties and processes (Hymenoptera: Formicidae). Myrmecol News 11:191–199

    Google Scholar 

  20. Gonzalez G, Seastedt TR (2001) Soil fauna and plant litter decomposition in tropical and subalpine forests. Ecology 82:955–964

    Article  Google Scholar 

  21. Grimbacher PS, Stork NE (2009) Seasonality of a diverse beetle assemblage inhabiting lowland tropical rainforest in Australia. Biotropica 41:328–337

    Article  Google Scholar 

  22. Hamilton AJ, Basset Y, Benke KK, Grimbacher PS, Miller SE, Novotny V, Samuelson A, Stork NE, Weiblen GD, Yen JDL (2010) Quantifying uncertainty in estimation of global arthropod species richness. Am Nat 176:90–95

    Article  PubMed  Google Scholar 

  23. Hansen RA (2000) Effects of habitat complexity and composition on a diverse litter microarthropod assemblage. Ecology 81:1120–1132

    Article  Google Scholar 

  24. Hattenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition interrestrial ecosystems. Annu Rev Ecol Evol S 36:191–218

    Article  Google Scholar 

  25. Hopkins MS, Head J, Ash JE, Hewett RK, Graham AW (1996) Evidence of a Holocene and continuing recent expansion of lowland rain forest in humid, tropical North Queensland. J Biogeogr 23:737–745

    Article  Google Scholar 

  26. Isbell RF (2002) The Australian soil classification. CSIRO Publishing, Collingwood

    Google Scholar 

  27. Jones R, Gilliver R, Robson S, Edwards W (2014) S-plus for the analysis of biological data. James Cook University, Townsville

    Google Scholar 

  28. Kampichler C, Bruckner A (2009) The role of microarthropods in terrestrial decomposition: a meta-analysis of 40 years of litterbag studies. Biol Rev 84:375–389

    Article  PubMed  Google Scholar 

  29. Kaspari M, Yanoviak SP (2009) Biogeochemistry and the structure of tropical brown food webs. Ecology 90:3342–3351

    Article  PubMed  Google Scholar 

  30. Klimes P, Janda M, Ibalim S, Kua J, Novotny V (2011) Experimental suppression of ants foraging on rainforest vegetation in New Guinea: testing methods for a whole-forest manipulation of insect communities. Ecol Entomol 36:94–103

    Article  Google Scholar 

  31. Laidlaw M, Kitching RL, Goodall K, Small A, Stork NE (2007) Temporal and spatial variation in an Australian tropical rainforest. Austral Ecol 32:10–20

    Article  Google Scholar 

  32. Lavelle P, Blanchart E, Martin A, Martin S, Spain A, Toutain F, Barois I, Schaefer R (1993) A hierarchical model for decomposition in terrestrial ecosystems—application to soils of the humid tropics. Biotropica 25:130–150

    Article  Google Scholar 

  33. Lessard JP, Sackett TE, Reynolds WN, Fowler DA, Sanders NJ (2011) Determinants of the detrital arthropod community structure: the effects of temperature and resources along an environmental gradient. Oikos 120:333–343

    Article  Google Scholar 

  34. Levings SC, Windsor DM (1984) Litter moisture content as a determinant of litter arthropod distribution and abundance during the dry season on Barro Colorado Island, Panama. Biotropica 16:125–131

    Article  Google Scholar 

  35. Levings SC, Windsor DM (1985) Litter arthropod populations in a tropical deciduous forest—relationships between years and arthropod groups. J Anim Ecol 54:61–69

    Article  Google Scholar 

  36. Lyra A, Imbach P, Rodriguez D, Chou SC, Georgiou S, Garofolo L (2017) Projections of climate change impacts on central America tropical rainforest. Clim Change 141:93–105

    Article  CAS  Google Scholar 

  37. McGlynn TP, Salinas DJ, Dunn RR, Wood TE, Lawrence D, Clark DA (2007) Phosphorus limits tropical rain forest litter fauna. Biotropica 39:50–53

    Article  Google Scholar 

  38. McGlynn TP, Fawcett RM, Clark DA (2009) Litter biomass and nutrient determinants of ant density, nest size, and growth in a Costa Rican tropical wet forest. Biotropica 41:234–240

    Article  Google Scholar 

  39. Milton Y, Kaspari M (2007) Bottom-up and top-down regulation of decomposition in a tropical forest. Oecologia 153:163–172

    Article  PubMed  Google Scholar 

  40. Novotný V, Basset Y (1998) Seasonality of sap-sucking insects (Auchenorrhyncha, Hemiptera) feeding on Ficus (Moraceae) in a lowland rain forest in New Guinea. Oecologia 115:514–522

    Article  PubMed  Google Scholar 

  41. Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson G, Solymos P, Stevens MHH, Wagner H (2010) Vegan: community ecology package. R package version 1.17-4

  42. Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stenevs HH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4-4. https://cran.r-project.org, https://github.com/vegandevs/vegan

  43. Ozanne CMP, Anhuf D, Boulter SL, Keller M, Kitching RL, Körner C, Meinzer FC, Mitchell AW, Nakashizuka T, Silva Dias PL, Stork NE, Wright SJ, Yoshimura M (2003) Biodiversity meets the atmosphere: a global view of forest canopies. Science (Washington, DC) 301:183–186

    Article  CAS  Google Scholar 

  44. Pachauri RK, Meyer L, Plattner G-K, Stocker T (2015) IPCC, 2014: climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC

  45. Parsons SA, Shoo LP, Williams SE (2009) Volume measurements for quicker determination of forest litter standing crop. J Trop Ecol 25:665–669

    Article  Google Scholar 

  46. Pearson DL, Derr JA (1986) Seasonal patterns of lowland forest floor arthropod abundance in southeastern Peru. Biotropica 18:244–256

    Article  Google Scholar 

  47. Powers JS, Montgomery RA, Adair EC, Brearley FQ, DeWalt SJ, Castanho CT, Chave J, Deinert E, Ganzhorn JU, Gilbert ME, Gonzalez-Iturbe JA, Bunyavejchewin S, Grau HR, Harms KE, Hiremath A, Iriarte-Vivar S, Manzane E, de Oliveira AA, Poorter L, Ramanamanjato JB, Salk C, Varela A, Weiblen GD, Lerdau MT (2009) Decomposition in tropical forests: a pan-tropical study of the effects of litter type, litter placement and mesofaunal exclusion across a precipitation gradient. J Ecol 97:801–811

    Article  CAS  Google Scholar 

  48. Proctor J, Anderson JM, Fogden SCL, Vallack HW (1983) Ecological-studies in 4 contrasting lowland rain forests in Gunung-Mulu-National-Park, Sarawak. 2. Litterfall, litter standing crop and preliminary-observations on herbivory. J Ecol 71:261–283

    Article  Google Scholar 

  49. R Core Team (2017) R package stats: a language and environment for statistical computing. Vienna. https://www.R-project.org/

  50. R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  51. Roderstein M, Hertel D, Leuschner C (2005) Above- and below-ground litter production in three tropical montane forests in southern Ecuador. J Trop Ecol 21:483–492

    Article  Google Scholar 

  52. Sakchoowong W, Hasin S, Pachey N, Amornsak W, Bunyavejchewin S, Kongnoo P, Basset Y (2015) Influence of leaf litter composition on ant assemblages in a lowland tropical rainforest in Thailand. Asian Myrmecol 7:57–71

    Google Scholar 

  53. Sayer EJ (2006) Using experimental manipulation to assess the roles of leaf litter in the functioning of forest ecosystems. Biol Rev 81:1–31

    Article  PubMed  Google Scholar 

  54. Sayer EJ, Sutcliffe LME, Ross RIC, Tanner EVJ (2010) Arthropod abundance and diversity in a lowland tropical forest floor in Panama: the role of habitat space vs. nutrient concentrations. Biotropica 42:194–200

    Article  Google Scholar 

  55. Shik JZ, Kaspari M (2010) More food, less habitat: how necromass and leaf litter decomposition combine to regulate a litter ant community. Ecol Entomol 35:158–165

    Article  Google Scholar 

  56. Stocker GC, Thompson WA, Irvine AK, Fitzsimon JD, Thomas PR (1995) Annual patterns of litterfall in a lowland and tableland rainforest in tropical Australia. Biotropica 27:412–420

    Article  Google Scholar 

  57. Stork NE, Grimbacher PS (2006) Beetle assemblages from an Australian tropical rainforest show that the canopy and the ground strata contribute equally to biodiversity. Proc R Soc B Biol Sci 273:1969–1975

    Article  Google Scholar 

  58. Tauber MJ, Tauber CA (1976) Insect seasonality: diapause maintenance, termination, and postdiapause development. Annu Rev Entomol 21:81–107

    Article  Google Scholar 

  59. Townsend AR, Asner GP, Cleveland CC (2008) The biogeochemical heterogeneity of tropical forests. Trends Ecol Evol 23:424–431

    Article  PubMed  Google Scholar 

  60. Tracey J (1982) Vegetation of the humid tropical region of North Queensland. CSIRO, Melbourne

    Google Scholar 

  61. Wall DH, Bradford MA, St John MG, Trofymow JA, Behan-Pelletier V, Bignell DDE, Dangerfield JM, Parton WJ, Rusek J, Voigt W, Wolters V, Gardel HZ, Ayuke FO, Bashford R, Beljakova OI, Bohlen PJ, Brauman A, Flemming S, Henschel JR, Johnson DL, Jones TH, Kovarova M, Kranabetter JM, Kutny L, Lin KC, Maryati M, Masse D, Pokarzhevskii A, Rahman H, Sabara MG, Salamon JA, Swift MJ, Varela A, Vasconcelos HL, White D, Zou XM (2008) Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent. Glob Change Biol 14:2661–2677

    Google Scholar 

  62. Wardhaugh CW, Stork NE, Edwards W (2012a) Feeding guild structure of beetles on Australian tropical rainforest trees reflects microhabitat resource availability. J Anim Ecol 81:1086–1094

    Article  PubMed  Google Scholar 

  63. Wardhaugh CW, Stork NE, Edwards W, Grimbacher PS (2012b) The overlooked biodiversity of flower-visiting invertebrates. PLoS ONE 7:e45796

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Wardhaugh CW, Edwards W, Stork NE (2013a) Body size variation among invertebrates inhabiting different canopy microhabitat: flower visitors are smaller. Ecol Entomol 38:101–111

    Article  Google Scholar 

  65. Wardhaugh CW, Stork NE, Edwards W (2013b) Specialization of rainforest canopy beetles to host trees and microhabitats: not all specialists are leaf-feeding herbivores. Biol J Lin Soc 109:215–228

    Article  Google Scholar 

  66. Wardhaugh CW, Edwards W, Stork NE (2015) The specialization and structure of antagonistic and mutualistic networks of beetles on rainforest canopy trees. Biol J Lin Soc 114:287–295

    Article  Google Scholar 

  67. Wolda H (1988) Insect seasonality: why? Annu Rev Ecol Syst 19:1–18

    Article  Google Scholar 

  68. Wood S (2006) Generalized additive models: an introduction with R. Chapman & Hall, Boca Raton

    Google Scholar 

  69. Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc Ser B 73:3–36

    Article  Google Scholar 

  70. Wood SN (2017) mgcv: mixed GAM computation vehicle with automatic smoothness. R package version 1.8-22. https://cran.r-project.org/web/packages/mgcv

  71. Wood TE, Lawrence D, Clark DA (2005) Variation in leaf litter nutrients of a Costa Rican rain forest is related to precipitation. Biogeochemistry 73:417–437

    Article  Google Scholar 

  72. Yang XD, Warren M, Zou XM (2007) Fertilization responses of soil litter fauna and litter quantity, quality, and turnover in low and high elevation forests of Puerto Rico. Appl Soil Ecol 37:63–71

    Article  CAS  Google Scholar 

  73. Zvereva EL, Kozlov MV (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant–herbivore interactions: a metaanalysis. Glob Change Biol 12:27–41

    Article  Google Scholar 

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Acknowledgements

We thank the Daintree Rainforest Observatory for access to the centres facilities and Marcin Skladaniec for laboratory work tallying ants. During the duration of the fieldwork and subsequent write up, PSG was funded by several organisations including the Rainforest Cooperative Research Centre, the Marine and Tropical Science Research Facility, Melbourne University and the Cooperative Research Centre for Forestry. This project was funded as part of the Marine and Tropical Science Research Facility. ML activities in the Daintree are supported by the Australian SuperSite Network, part of the Australian Government’s Terrestrial Ecosystem Research Network (www.tern.org.au).

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Correspondence to Nigel E. Stork.

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This article belongs to the Topical Collection: Forest and plantation biodiversity.

Communicated by David Hawksworth.

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Grimbacher, P.S., Edwards, W., Liddell, M.J. et al. Temporal variation in abundance of leaf litter beetles and ants in an Australian lowland tropical rainforest is driven by climate and litter fall. Biodivers Conserv 27, 2625–2640 (2018). https://doi.org/10.1007/s10531-018-1558-2

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Keywords

  • Leaf litter
  • Seasonality
  • Temporal variation
  • Beetles
  • Ants
  • Tropical forest
  • Climate change
  • Litter manipulation
  • Nutrient concentrations