Advertisement

Ecosystems

, Volume 21, Issue 5, pp 930–942 | Cite as

Landuse Change in Savannas Disproportionately Reduces Functional Diversity of Invertebrate Predators at the Highest Trophic Levels: Spiders as an Example

  • Grant S. Joseph
  • Evans V. Mauda
  • Colleen L. Seymour
  • Thinandavha C. Munyai
  • Ansie Dippenaar-Schoeman
  • Stefan H. Foord
Article

Abstract

Predators play a disproportionately positive role in ensuring integrity of food webs, influencing ecological processes and services upon which humans rely. Predators tend to be amongst the first species to be affected by anthropogenic disturbance, however. Spiders impact invertebrate population dynamics and stabilise food webs in natural and agricultural systems (potentially mitigating against crop pests and reduced yields). Africa’s savannas are undergoing continent-wide conversion from low-density rangelands to villages and croplands, as human populations burgeon. Despite limited research, and evidence of deleterious impacts to biodiversity, African savannas are earmarked by prominent international organisations for conversion to cropland. Given the key role of spiders in food webs, they can have beneficial impacts in agroecosystems. Furthermore, functional diversity (FD) reflects ecosystem pattern and processes better than species diversity, so we evaluated impacts of large-scale landuse change on both species richness and FD. We surveyed spiders using pitfall traps at 42 sites (14 replicates each in rangeland, cropland, and villages) in South African savannas, investigating effects of landuse, season, and habitat variables on spider species diversity and FD. Species richness was lowest in villages. FD was lowest in cropland, however, with reduced representation of traits associated with hunting of larger invertebrates. Furthermore, there were fewer specialists in croplands. These findings suggest that even when cropland does not impact species diversity, loss of FD can still occur. As savanna systems transform, impacts on invertebrate population dynamics may increase the possibility of a breakdown in pest control in natural and agricultural systems, given changes in FD of invertebrate predators.

Keywords

agriculture cropland epigaeic spider species food security food web functional diversity functional traits pest control 

Notes

Acknowledgements

We thank the NRF and Department of Science &Technology through the South African Research Chairs Initiative Chair on Biodiversity Value and Change in the Vhembe Biosphere Reserve, hosted by the University of Venda. This project was supported by the German Federal Government, BMBF (SPACES programme: Limpopo Living Landscapes Project). We thank the editors and two anonymous reviewers for comments that improved this manuscript.

Supplementary material

10021_2017_194_MOESM1_ESM.docx (52 kb)
Appendix 1. Table of spider traits (DOCX 52 kb)
10021_2017_194_MOESM2_ESM.docx (24 kb)
Appendix 2. Spider abundance as a function of landuse (DOCX 23 kb)
10021_2017_194_MOESM3_ESM.xlsx (317 kb)
Supplementary material 3 (XLSX 317 kb)
10021_2017_194_MOESM4_ESM.xlsx (47 kb)
Supplementary material 4 (XLSX 47 kb)
10021_2017_194_MOESM5_ESM.xlsx (47 kb)
Supplementary material 5 (XLSX 46 kb)

References

  1. Bates D, Maechler M, Bolker BM, Walker S. 2015. ‘Fitting linear mixed-effects models using lme4.’ ArXiv e-print. J Stat Software, http://arxiv.org/abs/14065823.
  2. Bolger DT, Suarez A, Crooks K, Morrison S, Case T. 2000. Arthropods in urban habitat fragments in southern California: area, age, and edge effects. Ecol Appl 10(10):1230–48.CrossRefGoogle Scholar
  3. Bonte D, Vandenbroecke N, Lens L, Maelfait J. 2003. Low propensity for aerial dispersal in specialist spiders from fragmented landscapes. Proc R Soc B Biol Sci 270:1601–7.CrossRefGoogle Scholar
  4. Botha M, Siebert SJ, van den Berg J. 2016. Grass abundance maintains positive plant-arthropod diversity relationships in maize fields and margins in South Africa. Agric For Entomol. http://doi.wiley.com/10.1111/afe.12195.
  5. Botha M, Siebert SJ, van den Berg J, Maliba BG, Ellis SM. 2015. Plant and arthropod diversity patterns of maize agro-ecosystems in two grassy biomes of South Africa. Biodivers Conserv 24:1797–824.CrossRefGoogle Scholar
  6. Buchholz S. 2010. Ground spider assemblages as indicators for habitat structure in inland sand ecosystems. Biodivers Conserv 19:2565–95.CrossRefGoogle Scholar
  7. Cardoso P, Pekár S, Jocqué R, Coddington JA. 2011. Global patterns of guild composition and functional diversity of spiders. PLoS ONE 6:1–10.Google Scholar
  8. Cardoso P, Silva I, De Oliveira NG, Serrano ARM. 2004. Indicator taxa of spider (Araneae) diversity and their efficiency in conservation. Biol Conserv 120:517–24.CrossRefGoogle Scholar
  9. Carter PE, Rypstra AL. 1995. Top-down effects in soybean agroecosystems: spider density affects herbivore damage. Oikos 72:433–9.CrossRefGoogle Scholar
  10. Carvalho FMV, De Marco P, Ferreira LG. 2009. The Cerrado into-pieces: Habitat fragmentation as a function of landscape use in the savannas of central Brazil. Biol Conserv 142:1392–403.CrossRefGoogle Scholar
  11. Cattin M, Blandenier G, Banas ěk-Richter C, Bersier L. 2003. The impact of mowing as a management strategy for wet meadows on spider (Araneae) communities. Biol Conserv 113:179–88.CrossRefGoogle Scholar
  12. Coe M, Cumming D, Phillipson J. 1976. Biomass and production of large Africa herbivores in relation to rainfall and primary production. Oecologia 22:341–54.CrossRefPubMedGoogle Scholar
  13. Colwell R. 2006. EstimateS: statistical estimation of species richness and shared species from samples. http://purl.oclc.org/estimates.
  14. Colwell RK, Coddington J. 1994. Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc B Biol Sci 345:101–18.CrossRefGoogle Scholar
  15. Cornwell W, Ackerly D. 2009. Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr 79:109–26.CrossRefGoogle Scholar
  16. Cortez J, Garnier E, Perez-Harguindeguy NDM, Gillon D. 2007. Plant traits, litter quality and decomposition in a Mediterranean old-field succession. Plant Soil 296:19–34.CrossRefGoogle Scholar
  17. Dennis P, Young M, Bentley C. 2001. The effects of varied grazing management on epigeal spiders, harvestmen and pseudoscorpions of Nardus stricta grassland in upland Scotland. Agric Ecosyst Environ 86:39–57.CrossRefGoogle Scholar
  18. Dias SC, Carvalho LS, Bonaldo AB, Brescovit AD. 2009. Refining the establishment of guilds in Neotropical spiders (Arachnida: Araneae). J Nat Hist 44:219–39.CrossRefGoogle Scholar
  19. Diaz S, Cabido M. 2001. Vive la difference: plant functional diversity matters to ecosystem processes: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–55.CrossRefGoogle Scholar
  20. Dippenaar-Schoeman AS. 2013. Field guide to the spiders of southern Africa. Cape Town: Lapa Publishers.Google Scholar
  21. Dobson A, Lodge D, Alder J, Cumming GS, Keymer J, McGlade J, Mooney H, Rusak J, Sala O, Wolters V, Wall D, Winfree R, Xenopoulos M. 2006. Habitat loss, trophic collapse, and the decline of ecosystem services. Ecology 87:1915–24.CrossRefPubMedGoogle Scholar
  22. Elias DO, Land BR, Mason AC, Hoy RR. 2006. Measuring and quantifying dynamic visual signals in jumping spiders. J Comp Physiol A 192:785–97.CrossRefGoogle Scholar
  23. Elias DO, Mason AC, Hoy RR. 2004. The effect of substrate on the efficacy of seismic courtship signal transmission in the jumping spider Habronattus dossenus (Araneae: Salticidae). J Exp Biol 207:4105–10.CrossRefPubMedGoogle Scholar
  24. Elmqvist T, Folke C, Nyström M, Peterson G, Bengtsson J, Walker B, Norberg J, Elmqvist T, Folke C, Walker B, Nystrm M, Peterson G, Bengtsson J. 2003. Diversity. Ecosyst Change Resil 1:488–94.Google Scholar
  25. Finke DL, Denno RF. 2004. Predator diversity dampens trophic cascades. Nature 429:407–10.CrossRefPubMedGoogle Scholar
  26. Flynn DFB, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, Simpson N, Mayfield MM, DeClerck F. 2009. Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12:22–33.CrossRefPubMedGoogle Scholar
  27. FAO. 2009. Food and Agricultural Organisation of the United Nations. Africa’s sleeping giant. http://www.fao.org/news/story/en/item/20964/icode/.
  28. Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O’Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill J, Monfreda C, Polasky S, Rockström J, Sheehan J, Siebert S, Tilman D, Zaks DPM, O’Connell C. 2011. Solutions for a cultivated planet. Nature 478:337–42.CrossRefPubMedGoogle Scholar
  29. Foord S, Dippenaar-Schoeman A, Haddad C, Lotz L, Lyle R. 2011. The faunistic diversity of spiders Savanna Biome in South African. Trans R Soc S Afr 66:170–201.CrossRefGoogle Scholar
  30. Forster L. 1977. A qualitative analysis of hunting behaviour in jumping spiders (Araneae: Salticidae). New Zeal J Zool 4:51–62.CrossRefGoogle Scholar
  31. Garnier E, Cortez J, Billès G, Navas M, Roumet C. 2004. Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–7.CrossRefGoogle Scholar
  32. Gerland P, Raftery A, Ševčíková H, Li N, Gu D, Spoorenberg T, Alkema L, Fosdick BK, Chunn J, Lalic N, Bay G, Buettner T, Heilig G, Wilmoth J, Gerland P, Raftery A. 2014. World population stabilization unlikely this century. Science 346:234–7.CrossRefPubMedPubMedCentralGoogle Scholar
  33. GlobCover. 2010. The GlobCover 2009 Project. http://dup.esrin.esa.it/globcover/.
  34. Gotelli NJ, Rohde K. 2002. Co-occurence of ectoparasites of marine fishes: a null model analysis. Ecol Lett 5:86–94.CrossRefGoogle Scholar
  35. Greenstone MH. 1984. Determinants of web spider species diversity: vegetation structural diversity vs. prey availability. Oecologia 62:299–304.CrossRefPubMedGoogle Scholar
  36. Greenstone MH, Morgan CE, Hultsch A-L, Farrow RA, Dowse JE. 1987. Ballooning spiders in Missouri, USA, and New South Wales, Australia: family and mass distributions. J Arachnol 15:163–70.Google Scholar
  37. Joseph GS, Makumbe M, Seymour CL, Cumming GS, Mahlangu Z, Cumming DHM. 2015. Termite mounds mitigate against 50 years of herbivore-induced reduction of functional diversity of savanna woody plants. Landsc Ecol 30:2161–74.CrossRefGoogle Scholar
  38. Joseph GS, Seymour CL, Cumming GS, Cumming DHM, Mahlangu Z. 2014. Termite mounds increase functional diversity of woody plants in African savannas. Ecosystems 17:808–19.CrossRefGoogle Scholar
  39. Laliberte E, Legendre P. 2010. A distance-based framework for measuring functional diversity from multiple traits: A distance-based framework for measuring from multiple traits functional diversity. Ecology 91:299–305.CrossRefPubMedGoogle Scholar
  40. Laliberté E, Shipley B. 2011. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-11. http://CRAN.R-project.org/package=FD.
  41. Larsen TH, Williams NM, Kremen C. 2005. Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol Lett 8:538–47.CrossRefPubMedGoogle Scholar
  42. Lavorel S, Grigulis K, McIntyre S, Williams NSG, Garden D, Dorrough J, Berman S, Quétier F, Thébault A, Bonis A. 2008. Assessing functional diversity in the field—methodology matters!. Funct Ecol 22:134–47.Google Scholar
  43. Lemessa D, Hambäck PA, Hylander K. 2015. The effect of local and landscape level land-use composition on predatory arthropods in a tropical agricultural landscape. Landsc Ecol 30:167–80.CrossRefGoogle Scholar
  44. Losey JE, Denno RF. 1998. Positive predator-predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology 79:2143–52.Google Scholar
  45. Malumbres-Olarte J, Barratt BIP, Vink CJ, Paterson AM, Cruickshank RH, Ferguson CM, Barton DM. 2014. Big and aerial invaders: dominance of exotic spiders in burned New Zealand tussock grasslands. Biol Invasions 16:2311–22.CrossRefGoogle Scholar
  46. Mauda EV, Joseph GS, Seymour CL, Munyai TC, Foord SH. 2017. Changes in landuse alter ant diversity, assemblages and dominant functional groups in African savannas. Biodivers Conserv (in press).Google Scholar
  47. McIntyre B., Herren H, Wakhungu J, Watson R. 2009. International Assessment of Agricultural Knowledge, Science and Technology for Development (IAASTD): global report. Washington DC.Google Scholar
  48. Midega CAO, Khan ZR, Van Den Berg J, Ogol CKPO, Dippenaar-Schoeman AS, Pickett JA, Wadhams LJ. 2008. Response of ground-dwelling arthropods to a ‘push-pull’ habitat management system: Spiders as an indicator group. J Appl Entomol 132:248–54.CrossRefGoogle Scholar
  49. Modiba R, Joseph GS, Seymour C, Fouché P, Foord S. 2017. Restoration of riparian systems through clearing of invasive plant species improves functional diversity of Odonate assemblages. Biol Conserv 214:46–54.CrossRefGoogle Scholar
  50. Moring J, Stewart K. 1994. Habitat partitioning by the Wolf Spider (Araneae, Lycosidae) Guild in Streamside and Riparian Vegetation Zones of the Conejos River, Colorado. J Arachnol 22:205–17.Google Scholar
  51. Mucina L, Rutherford MC. 2006. The vegetation of South Africa, Lesotho and Swaziland. In: Pretoria: South African National Biodiversity Institute. pp 492–3.Google Scholar
  52. Munyai TC, Foord SH. 2015. Temporal patterns of ant diversity across a mountain with climatically contrasting aspects in the tropics of Africa. PLoS ONE 10:1–16.CrossRefGoogle Scholar
  53. Naeem S, Li S. 1997. Africa appears to have been dominated by tetanurans, including Biodiversity enhances ecosystem reliability. Nature 390:507–9.CrossRefGoogle Scholar
  54. Nakagawa S, Schielzeth H. 2013. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–42.CrossRefGoogle Scholar
  55. Nyffeler M, Birkhofer K. 2017. An estimated 400–800 million tons of prey are annually killed by the global spider community. Sci Nat 104:30.CrossRefGoogle Scholar
  56. Nyffeler M, Sunderland K. 2003. Composition, abundance and pest control potential of spider communities in agroecosystems: a comparison of European and US studies. Agric Ecosyst Environ 95:579–612.CrossRefGoogle Scholar
  57. Oksanen J, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens H, Szoecs E, Wagner H. 2016. Vegan, Community Ecology Package. R-CRAN https://cr.Google Scholar
  58. Otoshi M, Bichier P, Philpott SM. 2015. Local and landscape correlates of spider activity density and species richness in urban gardens. Environ Entomol 44:1–9.CrossRefGoogle Scholar
  59. Pan C, Zhao H, Feng Q, Liu J, Liu L, Cai Y, Liu C, Li J. 2015. Temporal variations of ground-dwelling arthropods in relation to grassland salinization. Eur J Soil Biol 68:25–32.CrossRefGoogle Scholar
  60. Patrick L, Kershner M, Fraser L. 2012. Epigeal spider responses to fertilization and plant litter: testing biodiversity theory at the ground level. American Arachnological Society 40:309–24.Google Scholar
  61. Pekar S, Lubin Y. 2003. Habitats and interspecific associations of Zodariidae spiders in the Negev (Araneae: Zodariidae). Isr J Zool 49:255–67.CrossRefGoogle Scholar
  62. Petchey OL, Gaston KJ. 2002. Functional diversity (FD), species richness and community composition. Ecol Lett 5:402–11.CrossRefGoogle Scholar
  63. Petchey OL, Gaston KJ. 2006. Functional diversity: Back to basics and looking forward. Ecol Lett 9:741–58.CrossRefPubMedGoogle Scholar
  64. Petráková L, Líznarová E, Pekár S, Haddad CR, Sentenská L, Symondson WOC. 2015. Discovery of a monophagous true predator, a specialist termite-eating spider (Araneae: Ammoxenidae). Sci Rep 5:14013. doi: 10.1038/srep14013.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Pinkus-Rendón MA, León-Cortés JL, Ibarra-Núñez G. 2006. Spider diversity in a tropical habitat gradient in Chiapas, Mexico. Divers Distrib 12:61–9.CrossRefGoogle Scholar
  66. Platnick N. 2017. World spider catalog version 18.0. Nat Hist Museum Bern.Google Scholar
  67. Pluess T, Opatovsky I, Gavish-Regev E, Lubin Y, Schmidt-Entling MH. 2010. Non-crop habitats in the landscape enhance spider diversity in wheat fields of a desert agroecosystem. Agric Ecosyst Environ 137:68–74.CrossRefGoogle Scholar
  68. Podani J. 1999. Extending Gower’s general coefficient of similarity to ordinal characters. Taxon 48:331–40.CrossRefGoogle Scholar
  69. Podani J, Schmera D. 2006. On dendrogram-based measures of functional diversity. Oikos 115:179–85.CrossRefGoogle Scholar
  70. R Core Team R. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, http://www.r-project.org/. http://www.r-project.org/.
  71. Riggio J, Jacobson A, Dollar L, Bauer H. 2013. The size of savannah Africa: a lion’s (Panthera leo) view. Biodivers Conserv 22:17–35.CrossRefGoogle Scholar
  72. Rypstra AL, Schmidt JM, Reif BD, Devito J, Matthew H, Rypstra AL, Schmidt JM, Reif BD, Devito J, Persons MH. 2007. Tradeoffs involved in site selection and foraging in a wolf spider: effects of substrate structure and predation risk. Oikos 116:853–63.CrossRefGoogle Scholar
  73. Sattler T, Borcard D, Arlettaz R, Bontadina F, Legendre P, Obrist M, Moretti M. 2010. Spider, bee, and bird communities in cities are shaped by environmental control and high stochasticity. Ecology 9:3343–53.CrossRefGoogle Scholar
  74. Schmidt MH, Lauer A, Purtauf T, Thies C, Schaefer M, Tscharntke T. 2003. Relative importance of predators and parasitoids for cereal aphid control. Proc R Soc B Biol Sci 270:1905–9.CrossRefGoogle Scholar
  75. Schmidt MH, Tscharntke T. 2005. Landscape context of sheetweb spider (Araneae: Linyphiidae) abundance in cereal fields. J Biogeogr 32:467–73.CrossRefGoogle Scholar
  76. Schmitz OJ. 2009. Effects of predator functional diversity on grassland ecosystem function. Ecology 90:2339–45.CrossRefPubMedGoogle Scholar
  77. Schmitz OJ, Hambäck P, Beckerman AP. 2000. Trophic cascades in terrestrial systems: a review of the effects of carnivore removals on plants. Am Nat 155:141–53.CrossRefPubMedGoogle Scholar
  78. Seymour CL, Joseph GS, Makumbe M, Cumming GS, Mahlangu Z, Cumming DHM. 2016. Woody species composition in an African savanna: determined by centuries of termite activity but modulated by 50 years of ungulate herbivory. J Veg Sci 27:824–33.CrossRefGoogle Scholar
  79. Seymour CL, Simmons RE, Joseph GS, Slingsby JA. 2015. On bird functional diversity: species richness and functional differentiation show contrasting responses to rainfall and vegetation structure in an arid landscape. Ecosystems 18:971–84.CrossRefGoogle Scholar
  80. Shochat E, Stefanov WL, Whitehouse MEA, Faeth SH. 2004. Urbanization and spider diversity: influences of human modification of habitat structure and productivity. Ecol Appl 14:268–80.CrossRefGoogle Scholar
  81. Snyder WE, Wise DH. 2001. Contrasting trophic cascades generated by a community of generalist predators. Ecology 82:1571–83.CrossRefGoogle Scholar
  82. Suding K, Lavorel S, Chapin F, Cornelissen J, Diaz S, Garnie E, Goldberg D, Hooper D, Jackson S, Navas M-L. 2008. Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Glob Chang Biol 14:1125–40.CrossRefGoogle Scholar
  83. Sunderland K, Samu F. 2000. Effects of agricultural diversification on the abundance, distribution, and pest control potential of spiders: a review. Entomol Exp Appl 95:1–13.CrossRefGoogle Scholar
  84. Tilman D. 2001. Functional diversity. Encycl Biodivers 3:109–20.CrossRefGoogle Scholar
  85. Uetz GW, Halaj J, Cady AB. 1999. Guild structure of spiders in major crops. J Arachnol 27:270–80.Google Scholar
  86. UNICEF. 2017. Child nutrition UNICEF DATA. https://data.unicef.org/topic/nutrition/malnutrition/.
  87. Walker B, Kinzig A, Langridge J. 1999. Plant attribute diversity, resilience, and ecosystem function: the nature and significance of dominant and minor species. Ecosystems 2:95–113.CrossRefGoogle Scholar
  88. Wu Y, Cai Q, Lin C, Chen Y, Li Y, Cheng X. 2009. Response of ground-dwelling spiders to four hedgerow species on sloped agricultural fields in Southwest China. Prog Nat Sci 19:337–46.CrossRefGoogle Scholar
  89. Zurek DB, Taylor AJ, Evans CS, Nelson XJ. 2010. The role of the anterior lateral eyes in the vision-based behaviour of jumping spiders. J Exp Biol 213:2372–8.CrossRefPubMedGoogle Scholar
  90. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. 2009. Mixed effects models and extensions in ecology with R. New York: Springer.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Grant S. Joseph
    • 1
    • 2
  • Evans V. Mauda
    • 1
    • 5
  • Colleen L. Seymour
    • 2
    • 3
  • Thinandavha C. Munyai
    • 4
  • Ansie Dippenaar-Schoeman
    • 1
  • Stefan H. Foord
    • 1
  1. 1.SARChI-Chair on Biodiversity Value and Change, Department of Zoology, School of Mathematical and Natural ScienceUniversity of VendaThohoyandouSouth Africa
  2. 2.Department of Biological Sciences, DST/NRF Centre of Excellence, Percy FitzPatrick Institute of African OrnithologyUniversity of Cape TownCape TownSouth Africa
  3. 3.Kirstenbosch Research CentreSouth African National Biodiversity InstituteClaremontSouth Africa
  4. 4.School of Life Science, College of Agriculture, Engineering and ScienceUniversity of KwaZulu-NatalScottsvilleSouth Africa
  5. 5.Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa

Personalised recommendations