Springtail diversity in South Africa
Keywords:
Collembola, fynbos, decomposition, invasive species, barcoding
Abstract
Despite their significance in soil ecosystems and their use for investigations of soil ecosystem functioning and in bioindication elsewhere, springtails (Collembola) have not been well investigated in South Africa. Early recognition of their role in soil systems and sporadic systematic work has essentially characterised knowledge of the southern African fauna for some time. The situation is now changing as a consequence of systematic and ecological work on springtails. To date this research has focused mostly on the Cape Floristic Region and has revealed a much more diverse springtail fauna than previously known (136 identifiable species and an estimated 300 species for the Cape Floristic Region in total), including radiations in genera such as the isotomid Cryptopygus. Quantitative ecological work has shown that alpha diversity can be estimated readily and that the group may be useful for demonstrating land use impacts on soil biodiversity. Moreover, this ecological work has revealed that some disturbed sites, such as those dominated by Galenia africana, may be dominated by invasive springtail species. Investigation of the soil fauna involved in decomposition in Renosterveld and Fynbos has also revealed that biological decomposition has likely been underestimated in these vegetation types, and that the role of fire as the presumed predominant source of nutrient return to the soil may have to be re-examined. Ongoing research on the springtails will provide the information necessary for understanding and conserving soils: one of southern Africa’s major natural assets.References
1. Wardle DA. Communities and ecosystems: Linking the aboveground and belowground components. Princeton, NJ: Princeton University Press; 2002.
2. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van der Putten WH, Wall DH. Ecological linkages between aboveground and belowground biota. Science. 2004;304:1629–1633. http://dx.doi.org/10.1126/science.1094875, PMid:15192218
3. Hopkin S. Biology of the springtails. Insecta: Collembola. Oxford: Oxford University Press; 1997.
4. Rusek J. Soil microstructures-contributions on specific soil organisms. Quest Ent. 1985;21:497–514.
5. Scheu S, Treenhaus A, Jones TH. Links between the detritivore and the herbivore system: Effects of earthworms and Collembola on plant growth and aphid development. Oecologia. 1999;119:541–551. http://dx.doi.org/10.1007/s004420050817
6. Deharveng L. Soil Collembola diversity, endemism, and reforestation: A case study in the Pyrenees (France). Conserv Biol. 1996;10:74–84. http://dx.doi.org/10.1046/j.1523-1739.1996.10010074.x
7. Cassagne N, Gauquelin T, Bal-Serin M-C, Gers C. Endemic Collembola, privileged bioindicators of forest management. Pedobiologia. 2006;50:127–134. http://dx.doi.org/10.1016/j.pedobi.2005.10.002
8. Van Straalen NM, Van Gestel CAM. Soil invertebrates and microorganisms. In: Calow P, editor. Handbook of ecotoxicology. Oxford: Blackwell; 2009.
9. Rusek J. Biodiversity of Collembola and their functional role in the ecosystem. Biodiv Conserv. 1998;7:1207–1219. http://dx.doi.org/10.1023/A:1008887817883
10. Deharveng L. Recent advances in Collembola systematics. Pedobiologia. 2004;48:415–433. http://dx.doi.org/10.1016/j.pedobi.2004.08.001
11. Petersen H, Luxton M. A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos. 1982;39:287–388. http://dx.doi.org/10.2307/3544689
12. Ulrich W, Fiera C. Environmental correlates of species richness of European springtails (Hexapoda: Collembola). Acta Oecol. 2009;35:45–52. http://dx.doi.org/10.1016/j.actao.2008.07.007
13. Robertson HG. Afrotropical ants (Hymenoptera: Formicidae): Taxonomic progress and estimation of species richness. J Hymen Res. 2000;9:74–84.
14. Parr CL, Robertson HG, Biggs HC, Chown SL. Response of African savanna ants to long-term fire regimes. J Appl Ecol. 2004;41:630–642. http://dx.doi.org/10.1111/j.0021-8901.2004.00920.x
15. Botes A, McGeoch MA, Robertson HG, Van Niekerk A, Davids HP, Chown SL. Ants, altitude and change in the northern Cape Floristic Region. J Biogeogr. 2006;33:71–90. http://dx.doi.org/10.1111/j.1365-2699.2005.01336.x
16. Braschler B, Kirsten M, Karenyi N, Gaston KJ, Chown SL. Realizing a synergy between research and education: How participation in ant monitoring helps raise biodiversity awareness in a resource-poor country. J Insect Cons. 2010;14:19–30. http://dx.doi.org/10.1007/s10841-009-9221-6
17. Lawrence RF. The biology of the cryptic fauna of forests, with special reference to the indigenous forests of South Africa. Cape Town: Balkema; 1953.
18. Womersley H. On some Collembola Arthropleona from South Africa and southern Rhodesia. Ann S Afr Mus. 1934;30:441–475.
19. Paclt J. Collembola. In: Hanstrom B, Brinck P, Rudebeck G, editors. South African animal life. Results of the Lund University Expedition in 1950–1951. Vol. VI. Uppsala: Almqvist & Wiksells Boktryckeri AB, 1959; p. 24–78.
20. Yosii R. Collembola fauna of the Cape Province, with special reference to the genus Seira Lubbock. In: Biological results of the Japanese Antarctic ResearchExpedition 6. Kyoto: Siraham, Wakayam-Ken, 1959; p. 1–23.
21. Coates TJ. The Collembola of South Africa – 1: The genus Neanura. J Ent Soc Sth Afr. 1968;31:185–195.
22. Coates TJ. The Collembola of South Africa – 2: The genus Seira. J Ent Soc Sth Afr. 1968;31:435–462.
23. Coates TJ. The Collembola of South Africa – 3: The genus Lepidokrugeria. J Ent Soc Sth Afr. 1969;32:87–89.
24. Coates TJ. Check-list of the Collembola of South African Parks (Part 1). Koedoe. 1970;13:181–184.
25. Weiner WM, Najt J. Collembola Poduromorpha of South Africa. Bonn Zool Beitr. 1991;42:369–387.
26. Barra J-A. Nouveaux Collemboles Poduromorphes de la Province du Natal (Rép. Sud Africaine) (Insecta: Collembola). [New Poduromorpha Collembola from Natal Province (Republic of South Africa) (Insecta: Collembola)]. J Afr Zool. 1994;108:181–189. French.
27. Barra J-A. Nouveaux Collemboles Poduromorphes des sables littoraux (partie terrestre) de la Province du Natal (Rép. Sud Africaine) (Insecta : Collembola). [New Poduromorpha Collembola from the sand coasts (terrestrial part) from Natal Province (Republic of South Africa) (Insecta: Collembola)]. J Afr Zool. 1995;109:125–139. French.
28. Barra J-A. Nouveaux Collemboles Entomobryomorphes des sables littoraux (partie terrestre) de la Province du Natal (Rép. Sud Africaine) (Insecta : Collembola). [New Entomobryomorpha Collembola from the sand coasts (terrestrial part) of the Natal Province (Republic of South Africa) (Insecta : Collembola)]. J Afr Zool. 1997;111:465–480. French.
29. McGeoch MA. The selection, testing and application of terrestrial insects as bioindicators. Biol Rev. 1998;73:181–201. http://dx.doi.org/10.1017/S000632319700515X
30. Reinecke AJ, Albertus RMC, Reinecke SA, Larink O. The effects of organic and conventional management practices on feeding activity of soil organisms in vineyards. Afr Zool. 2008;43:66–74. http://dx.doi.org/10.3377/1562-7020(2008)43[66:TEOOAC]2.0.CO;2
31. Chown SL, Froneman PW. The Prince Edward Islands. Land-sea interactions in a changing climate. Stellenbosch: African Sun Media; 2008.
32. Deharveng L. Collemboles des iles subantarctiques de l’Océan Indien Mission J. Travé 1972–1973. [Collembola of the sub-Antarctic islands of the IndianOcean Mission J. Travé 1972–1973]. Com Nat Fr Rech Antarct. 1981;48:33-108. French.
33. Gabriel AGA, Chown SL, Barendse J, et al. Biological invasions on Southern Ocean islands: The Collembola of Marion Island as a test of generalities. Ecography. 2001;24:421–430. http://dx.doi.org/10.1034/j.1600-0587.2001.d01-198.x
34. Chown SL, Slabber S, McGeoch MA, Janion C, Leinaas HP. Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proc R Soc Lond B. 2007;274:2661–2667. http://dx.doi.org/10.1098/rspb.2007.0772, PMid:17686728, PMCid:2275886
35. Myburgh M, Chown SL, Daniels SR, Jansen van Vuuren B. Population structure, propagule pressure, and conservation biogeography in the sub-Antarctic:Lessons from indigenous and invasive springtails. Divers Distrib. 2007;13:143–154.
36. Janion C, Leinaas H-P, Terblanche JS, Chown SL. Trait means and reaction norms: The consequences of climate change/invasion interactions at the organism level. Evol Ecol. 2010;24:1365–1380. http://dx.doi.org/10.1007/s10682-010-9405-2
37. Samways MJ. Insect conservation biology. London: Chapman & Hall; 1994.
38. Greenslade P. Collembola. In: Houston VWK, editor. Zoological catalogue of Australia. Volume 22. Protura, Collembola, Diplura. Melbourne: CSIRO, 1994; p. 19–138.
39. Potapov M, Janion C, Deharveng L. Two new species of Parisotoma (Collembola: Isotomidae) from the Western Cape, South Africa. Zootaxa. 2011;2771:17–24. PMid:21547000, PMCid:3086760
40. Janion C, Bedos A, Deharveng L. The genus Ectonura, Cassagnau 1980 in South Africa (Collembola: Neanuridae: Neanurinae), with a key to South AfricanNeanurinae. ZooKeys. 2011;136:31–45.
41. Scholtz CH, Chown SL. Insects in southern Africa: How many species are there? S Afr J Sci. 1995;91:124–126.
42. Bengtsson J, Janion C, Chown SL, Leinaas HP. Variation in decomposition rates in the fynbos biome, South Africa: The role of plant species and plant stoichiometry. Oecologia. 2011;165:225–235. http://dx.doi.org/10.1007/s00442-010-1753-7, PMid:20827492, PMCid:3015188
43. Fjellberg A. The Collembola of Fennoscandia and Denmark. Part I: Poduromorpha. Fauna Entomologica Scandinavica 35. Leiden: Brill; 1998.
44. Colwell RK. EstimateS: Statistical estimation of species richness and shared species from samples (software and user’s guide). Version 8.2.0. Storrs, CT:University of Connecticut; 2009.
45. Seastedt TR. The role of microarthropods in decomposition and mineralization processes. Annu Rev Entomol. 1984;29:25–46.
46. Verhoef H, Brussaard L. Decomposition and nitrogen mineralization in natural and agro-ecosystems: The contribution of soil animals. Biogeochemistry. 1990;11:175–211. http://dx.doi.org/10.1007/BF00004496
47. Barrios E. Soil biota, ecosystem services and land productivity. Ecol Econ. 2007;64:269–285.
48. Ettema CH, Wardle DA. Spatial soil ecology. Trends Ecol Evol. 2002;17:177–183. http://dx.doi.org/10.1016/S0169-5347(02)02496-5
49. Ayres E, Steltzer H, Simmons BL, et al. Home-field advantage accelerates leaf litter decomposition in forests. Soil Biol Biochem. 2009;41:606–610.
50. Van Wilgen BW. The evolution of fire and invasive alien plant management practices in fynbos. S Afr J Sci. 2009;105:335–342.
51. Mitchell DT, Coley PGF, Webb S, Allsopp N. Litter fall and decomposition processes in the coastal fynbos vegetation, south-western Cape, South Africa. JEcol. 1986;74:977–993.
52. Mitchell DT, Coley PGF. Litter production and decomposition from shrubs of Protea repens growing in sand plain lowland and mountain fynbos, south western Cape. S Afr J Bot. 1987;53:25–31.
53. Stock WD, Allsopp N. Functional perspective of ecosystems. In: Cowling RM, editor. The ecology of fynbos: Nutrients, fire and diversity. Cape Town: Oxford University Press, 1992; p. 241–259.
54. Chown SL. Temporal biodiversity change in transformed landscapes: A southern African perspective. Phil Trans R Soc B. 2010;365:3729–3742.
2. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van der Putten WH, Wall DH. Ecological linkages between aboveground and belowground biota. Science. 2004;304:1629–1633. http://dx.doi.org/10.1126/science.1094875, PMid:15192218
3. Hopkin S. Biology of the springtails. Insecta: Collembola. Oxford: Oxford University Press; 1997.
4. Rusek J. Soil microstructures-contributions on specific soil organisms. Quest Ent. 1985;21:497–514.
5. Scheu S, Treenhaus A, Jones TH. Links between the detritivore and the herbivore system: Effects of earthworms and Collembola on plant growth and aphid development. Oecologia. 1999;119:541–551. http://dx.doi.org/10.1007/s004420050817
6. Deharveng L. Soil Collembola diversity, endemism, and reforestation: A case study in the Pyrenees (France). Conserv Biol. 1996;10:74–84. http://dx.doi.org/10.1046/j.1523-1739.1996.10010074.x
7. Cassagne N, Gauquelin T, Bal-Serin M-C, Gers C. Endemic Collembola, privileged bioindicators of forest management. Pedobiologia. 2006;50:127–134. http://dx.doi.org/10.1016/j.pedobi.2005.10.002
8. Van Straalen NM, Van Gestel CAM. Soil invertebrates and microorganisms. In: Calow P, editor. Handbook of ecotoxicology. Oxford: Blackwell; 2009.
9. Rusek J. Biodiversity of Collembola and their functional role in the ecosystem. Biodiv Conserv. 1998;7:1207–1219. http://dx.doi.org/10.1023/A:1008887817883
10. Deharveng L. Recent advances in Collembola systematics. Pedobiologia. 2004;48:415–433. http://dx.doi.org/10.1016/j.pedobi.2004.08.001
11. Petersen H, Luxton M. A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos. 1982;39:287–388. http://dx.doi.org/10.2307/3544689
12. Ulrich W, Fiera C. Environmental correlates of species richness of European springtails (Hexapoda: Collembola). Acta Oecol. 2009;35:45–52. http://dx.doi.org/10.1016/j.actao.2008.07.007
13. Robertson HG. Afrotropical ants (Hymenoptera: Formicidae): Taxonomic progress and estimation of species richness. J Hymen Res. 2000;9:74–84.
14. Parr CL, Robertson HG, Biggs HC, Chown SL. Response of African savanna ants to long-term fire regimes. J Appl Ecol. 2004;41:630–642. http://dx.doi.org/10.1111/j.0021-8901.2004.00920.x
15. Botes A, McGeoch MA, Robertson HG, Van Niekerk A, Davids HP, Chown SL. Ants, altitude and change in the northern Cape Floristic Region. J Biogeogr. 2006;33:71–90. http://dx.doi.org/10.1111/j.1365-2699.2005.01336.x
16. Braschler B, Kirsten M, Karenyi N, Gaston KJ, Chown SL. Realizing a synergy between research and education: How participation in ant monitoring helps raise biodiversity awareness in a resource-poor country. J Insect Cons. 2010;14:19–30. http://dx.doi.org/10.1007/s10841-009-9221-6
17. Lawrence RF. The biology of the cryptic fauna of forests, with special reference to the indigenous forests of South Africa. Cape Town: Balkema; 1953.
18. Womersley H. On some Collembola Arthropleona from South Africa and southern Rhodesia. Ann S Afr Mus. 1934;30:441–475.
19. Paclt J. Collembola. In: Hanstrom B, Brinck P, Rudebeck G, editors. South African animal life. Results of the Lund University Expedition in 1950–1951. Vol. VI. Uppsala: Almqvist & Wiksells Boktryckeri AB, 1959; p. 24–78.
20. Yosii R. Collembola fauna of the Cape Province, with special reference to the genus Seira Lubbock. In: Biological results of the Japanese Antarctic ResearchExpedition 6. Kyoto: Siraham, Wakayam-Ken, 1959; p. 1–23.
21. Coates TJ. The Collembola of South Africa – 1: The genus Neanura. J Ent Soc Sth Afr. 1968;31:185–195.
22. Coates TJ. The Collembola of South Africa – 2: The genus Seira. J Ent Soc Sth Afr. 1968;31:435–462.
23. Coates TJ. The Collembola of South Africa – 3: The genus Lepidokrugeria. J Ent Soc Sth Afr. 1969;32:87–89.
24. Coates TJ. Check-list of the Collembola of South African Parks (Part 1). Koedoe. 1970;13:181–184.
25. Weiner WM, Najt J. Collembola Poduromorpha of South Africa. Bonn Zool Beitr. 1991;42:369–387.
26. Barra J-A. Nouveaux Collemboles Poduromorphes de la Province du Natal (Rép. Sud Africaine) (Insecta: Collembola). [New Poduromorpha Collembola from Natal Province (Republic of South Africa) (Insecta: Collembola)]. J Afr Zool. 1994;108:181–189. French.
27. Barra J-A. Nouveaux Collemboles Poduromorphes des sables littoraux (partie terrestre) de la Province du Natal (Rép. Sud Africaine) (Insecta : Collembola). [New Poduromorpha Collembola from the sand coasts (terrestrial part) from Natal Province (Republic of South Africa) (Insecta: Collembola)]. J Afr Zool. 1995;109:125–139. French.
28. Barra J-A. Nouveaux Collemboles Entomobryomorphes des sables littoraux (partie terrestre) de la Province du Natal (Rép. Sud Africaine) (Insecta : Collembola). [New Entomobryomorpha Collembola from the sand coasts (terrestrial part) of the Natal Province (Republic of South Africa) (Insecta : Collembola)]. J Afr Zool. 1997;111:465–480. French.
29. McGeoch MA. The selection, testing and application of terrestrial insects as bioindicators. Biol Rev. 1998;73:181–201. http://dx.doi.org/10.1017/S000632319700515X
30. Reinecke AJ, Albertus RMC, Reinecke SA, Larink O. The effects of organic and conventional management practices on feeding activity of soil organisms in vineyards. Afr Zool. 2008;43:66–74. http://dx.doi.org/10.3377/1562-7020(2008)43[66:TEOOAC]2.0.CO;2
31. Chown SL, Froneman PW. The Prince Edward Islands. Land-sea interactions in a changing climate. Stellenbosch: African Sun Media; 2008.
32. Deharveng L. Collemboles des iles subantarctiques de l’Océan Indien Mission J. Travé 1972–1973. [Collembola of the sub-Antarctic islands of the IndianOcean Mission J. Travé 1972–1973]. Com Nat Fr Rech Antarct. 1981;48:33-108. French.
33. Gabriel AGA, Chown SL, Barendse J, et al. Biological invasions on Southern Ocean islands: The Collembola of Marion Island as a test of generalities. Ecography. 2001;24:421–430. http://dx.doi.org/10.1034/j.1600-0587.2001.d01-198.x
34. Chown SL, Slabber S, McGeoch MA, Janion C, Leinaas HP. Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proc R Soc Lond B. 2007;274:2661–2667. http://dx.doi.org/10.1098/rspb.2007.0772, PMid:17686728, PMCid:2275886
35. Myburgh M, Chown SL, Daniels SR, Jansen van Vuuren B. Population structure, propagule pressure, and conservation biogeography in the sub-Antarctic:Lessons from indigenous and invasive springtails. Divers Distrib. 2007;13:143–154.
36. Janion C, Leinaas H-P, Terblanche JS, Chown SL. Trait means and reaction norms: The consequences of climate change/invasion interactions at the organism level. Evol Ecol. 2010;24:1365–1380. http://dx.doi.org/10.1007/s10682-010-9405-2
37. Samways MJ. Insect conservation biology. London: Chapman & Hall; 1994.
38. Greenslade P. Collembola. In: Houston VWK, editor. Zoological catalogue of Australia. Volume 22. Protura, Collembola, Diplura. Melbourne: CSIRO, 1994; p. 19–138.
39. Potapov M, Janion C, Deharveng L. Two new species of Parisotoma (Collembola: Isotomidae) from the Western Cape, South Africa. Zootaxa. 2011;2771:17–24. PMid:21547000, PMCid:3086760
40. Janion C, Bedos A, Deharveng L. The genus Ectonura, Cassagnau 1980 in South Africa (Collembola: Neanuridae: Neanurinae), with a key to South AfricanNeanurinae. ZooKeys. 2011;136:31–45.
41. Scholtz CH, Chown SL. Insects in southern Africa: How many species are there? S Afr J Sci. 1995;91:124–126.
42. Bengtsson J, Janion C, Chown SL, Leinaas HP. Variation in decomposition rates in the fynbos biome, South Africa: The role of plant species and plant stoichiometry. Oecologia. 2011;165:225–235. http://dx.doi.org/10.1007/s00442-010-1753-7, PMid:20827492, PMCid:3015188
43. Fjellberg A. The Collembola of Fennoscandia and Denmark. Part I: Poduromorpha. Fauna Entomologica Scandinavica 35. Leiden: Brill; 1998.
44. Colwell RK. EstimateS: Statistical estimation of species richness and shared species from samples (software and user’s guide). Version 8.2.0. Storrs, CT:University of Connecticut; 2009.
45. Seastedt TR. The role of microarthropods in decomposition and mineralization processes. Annu Rev Entomol. 1984;29:25–46.
46. Verhoef H, Brussaard L. Decomposition and nitrogen mineralization in natural and agro-ecosystems: The contribution of soil animals. Biogeochemistry. 1990;11:175–211. http://dx.doi.org/10.1007/BF00004496
47. Barrios E. Soil biota, ecosystem services and land productivity. Ecol Econ. 2007;64:269–285.
48. Ettema CH, Wardle DA. Spatial soil ecology. Trends Ecol Evol. 2002;17:177–183. http://dx.doi.org/10.1016/S0169-5347(02)02496-5
49. Ayres E, Steltzer H, Simmons BL, et al. Home-field advantage accelerates leaf litter decomposition in forests. Soil Biol Biochem. 2009;41:606–610.
50. Van Wilgen BW. The evolution of fire and invasive alien plant management practices in fynbos. S Afr J Sci. 2009;105:335–342.
51. Mitchell DT, Coley PGF, Webb S, Allsopp N. Litter fall and decomposition processes in the coastal fynbos vegetation, south-western Cape, South Africa. JEcol. 1986;74:977–993.
52. Mitchell DT, Coley PGF. Litter production and decomposition from shrubs of Protea repens growing in sand plain lowland and mountain fynbos, south western Cape. S Afr J Bot. 1987;53:25–31.
53. Stock WD, Allsopp N. Functional perspective of ecosystems. In: Cowling RM, editor. The ecology of fynbos: Nutrients, fire and diversity. Cape Town: Oxford University Press, 1992; p. 241–259.
54. Chown SL. Temporal biodiversity change in transformed landscapes: A southern African perspective. Phil Trans R Soc B. 2010;365:3729–3742.