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Shift in trophic niches of soil microarthropods with conversion of tropical rainforest into plantations as indicated by stable isotopes (15N, 13C)


Autoři: Alena Krause aff001;  Dorothee Sandmann aff001;  Sarah L. Bluhm aff001;  Sergey Ermilov aff002;  Rahayu Widyastuti aff003;  Noor Farikhah Haneda aff004;  Stefan Scheu aff001;  Mark Maraun aff001
Působiště autorů: University of Göttingen, J.F. Blumenbach Institute of Zoology and Anthropology, Göttingen, Germany aff001;  Tyumen State University, Tyumen, Russia aff002;  Bogor Agricultural University-IPB, Department of Soil Sciences and Land Resources, Bogor, Indonesia aff003;  Bogor Agricultural University-IPB, Department of Silviculture; Faculty of Forestry, Bogor, Indonesia aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224520

Souhrn

Land-use change is threatening biodiversity worldwide, affecting above and below ground animal communities by altering their trophic niches. However, shifts in trophic niches with changes in land use are little studied and this applies in particular to belowground animals. Oribatid mites are among the most abundant soil animals, involved in decomposition processes and nutrient cycling. We analyzed shifts in trophic niches of six soil-living oribatid mite species with the conversion of lowland secondary rainforest into plantation systems of different land-use intensity (jungle rubber, rubber and oil palm monoculture plantation) in two regions of southwest Sumatra, Indonesia. We measured stable isotope ratios (13C/12C and 15N/14N) of single oribatid mite individuals and calculated shifts in stable isotope niches with changes in land use. Significant changes in stable isotope ratios in three of the six studied oribatid mite species indicated that these species shift their trophic niches with changes in land use. The trophic shift was either due to changes in trophic level (δ15N values), to changes in the use of basal resources (δ13C values) or to changes in both. The trophic shift generally was most pronounced between more natural systems (rainforest and jungle rubber) on one side and monoculture plantations systems (rubber and oil palm plantations) on the other, reflecting that the shifts were related to land-use intensity. Although trophic niches of the other three studied species did not differ significantly between land-use systems they followed a similar trend. Overall, the results suggest that colonization of very different ecosystems such as rainforest and intensively managed monoculture plantations by oribatid mite species likely is related to their ability to shift their trophic niches, i.e. to trophic plasticity.

Klíčová slova:

Ecosystems – Predation – Oil palm – Rubber – Mites – Rainforests – Stable isotopes – Jungles


Zdroje

1. Dirzo R, Raven PH. Global state of biodiversity and loss. Annu Rev Environ Resour. 2003;28: 137–167. doi: 10.1146/annurev.energy.28.050302.105532

2. Foley JA, Defries R, Asner GP, Barford C, Bonan G, Carpenter SR, et al. Global consequences of land use. Science (80-). 2005;309: 570–574. doi: 10.1126/science.1111772 16040698

3. Gibbs HK, Ruesch AS, Achard F, Clayton MK, Holmgren P, Ramankutty N, et al. Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. Proc Natl Acad Sci USA. 2010;107: 16732–16737. doi: 10.1073/pnas.0910275107 20807750

4. Newbold T, Hudson LN, Hill SLL, Contu S, Lysenko I, Senior R a., et al. Global effects of land use on local terrestrial biodiversity. Nature. 2015;520: 45–50. doi: 10.1038/nature14324 25832402

5. Wilcove DS, Giam X, Edwards DP, Fisher B, Koh LP. Navjot’s nightmare revisited: Logging, agriculture, and biodiversity in Southeast Asia. Trends Ecol Evol. Elsevier Ltd; 2013;28: 531–540. doi: 10.1016/j.tree.2013.04.005 23764258

6. Sodhi NS, Posa MRC, Lee TM, Bickford D, Koh LP, Brook BW. The state and conservation of Southeast Asian biodiversity. Biodivers Conserv. 2010;19: 317–328. doi: 10.1007/s10531-009-9607-5

7. Meijide A, Badu CS, Moyano F, Tiralla N, Gunawan D, Knohl A. Impact of forest conversion to oil palm and rubber plantations on microclimate and the role of the 2015 ENSO event. Agric For Meteorol. 2018;252: 208–2019. doi: 10.1016/j.agrformet.2018.01.013

8. Laumonier Y, Uryu Y, Stüwe M, Budiman A, Setiabudi B, Hadian O. Eco-floristic sectors and deforestation threats in Sumatra: Identifying new conservation area network priorities for ecosystem-based land use planning. Biodivers Conserv. 2010;19: 1153–1174. doi: 10.1007/s10531-010-9784-2

9. Miettinen J, Shi C, Liew SC. Deforestation rates in insular Southeast Asia between 2000 and 2010. Glob Chang Biol. 2011;17: 2261–2270. doi: 10.1111/j.1365-2486.2011.02398.x

10. Margono BA, Potapov P V., Turubanova S, Stolle F, Hansen MC. Primary forest cover loss in indonesia over 2000–2012. Nat Clim Chang. 2014;4: 730–735. doi: 10.1038/nclimate2277

11. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GA, Kent J. Biodiversity hotspots for conservation priorities. Nature. 2000;403: 853–8. doi: 10.1038/35002501 10706275

12. Drescher J, Rembold K, Allen K, Beckscha P, Buchori D, Clough Y, et al. Ecological and socio-economic functions across tropical land use systems after rainforest conversion. Philos Trans R Soc Lond B Biol Sci. 2016;231: 1–7. doi: 10.1098/rstb.2015.0275 27114577

13. Klarner B, Winkelmann H, Krashevska V, Maraun M, Widyastuti R, Scheu S. Trophic niches, diversity and community composition of invertebrate top predators (Chilopoda) as affected by conversion of tropical lowland rainforest in Sumatra (Indonesia). PLoS One. 2017; 1–17. doi: 10.1371/journal.pone.0180915 28763453

14. Lavelle P, Decaëns T, Aubert M, Barot S, Blouin M, Bureau F, et al. Soil invertebrates and ecosystem services. Eur J Soil Biol. 2006;42. doi: 10.1016/j.ejsobi.2006.10.002

15. Lavelle P, Bignell D, Lepage M, Wolters W, Roger P, Ineson P, et al. Soil function in a changing world: The role of invertebrate ecosystem engineers. Eur J Soil Biol. 1997;33: 159–193. doi: 35400007052344.0010

16. Whalen J, Sampedro L. Soil ecology and management. CAB International. CABI; 2010.

17. Erdmann G, Otte V, Langel R, Scheu S, Maraun M. The trophic structure of bark-living oribatid mite communities analysed with stable isotopes (15N,13C) indicates strong niche differentiation. Exp Appl Acarol. 2007;41: 1–10. doi: 10.1007/s10493-007-9060-7 17333459

18. Maraun M, Scheu S. The structure of oribatid mite communities (Acari, Oribatida): Patterns, mechanisms and implications for future research. Source: Ecography. 2000;23: 374–383. doi: 10.1139/x03-284

19. Bardgett R. The biology of soil: A community and ecosystem approach. Oxford University Press; 2005.

20. Subías LS, Shtanchaeva UY, Arillo A. Listado de los ácaros oribátidos (Acariformes, Oribatida) de las diferentes regiones biogeográficas del mundo (6 actzalización). 2018;1939: 1–874.

21. Walter DE, Proctor HC. Mites: Ecology, Evolution & Behaviour. 2013. p. 494.

22. Maraun M, Schatz H, Scheu S. Awesome or ordinary? Global diversity patterns of oribatid mites. Ecography (Cop). 2007;30: 209–216.

23. Scheu S, Illig J, Eissfeller V, Krashevska V, Sandmann D, Maraun M. The soil fauna of a tropical mountain rainforest in southern Ecuador: Structure and functioning. Gradstein S. R., Homeier J., D. G (eds., editor. The tropical mountain forest. Patterns and Processes in a Biodiversity Hotspots. Biodiversity and Ecology Series 2. Göttingen, Universitätsverlag; 2008. pp. 79–96.

24. Illig J, Langel R, Norton RA., Scheu S, Maraun M. Where are the decomposers? Uncovering the soil food web of a tropical montane rain forest in southern Ecuador using stable isotopes (15N). J Trop Ecol. 2005;21: 589–593. doi: 10.1017/S0266467405002646

25. Maaß S, Maraun M, Scheu S, Rillig MC, Caruso T. Environmental filtering vs. resource-based niche partitioning in diverse soil animal assemblages. Soil Biol Biochem. Elsevier Ltd; 2015;85: 145–152. doi: 10.1016/j.soilbio.2015.03.005

26. Schneider K, Migge S, Norton RA, Scheu S, Langel R, Reineking A, et al. Trophic niche differentiation in soil microarthropods (Oribatida, Acari): Evidence from stable isotope ratios (15N/14N). Soil Biol Biochem. 2004;36: 1769–1774. doi: 10.1016/j.soilbio.2004.04.033

27. Powers JS, Montgomery R a., Adair EC, Brearley FQ, Dewalt SJ, Castanho CT, et al. 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. 2009;97: 801–811. doi: 10.1111/j.1365-2745.2009.01515.x

28. Hooper DU, Chapin F, Ewel J, Hector A, Inchausti P, Lavorel S, et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr. 2005;10: 3–35. doi: 10.1890/04-0922

29. Wada E, Mizutani H, Minagawa M. The use of stable isotopes for food web analysis. Crit Rev Food Sci Nutr. 1991;30(4): 361–371. doi: 10.1080/10408399109527547 1910519

30. Potapov AM, Tiunov A V., Scheu S. Uncovering trophic positions and food resources of soil animlas using bulk natural stable isotope composition. Biol Rev. 2019;94: 37–59. doi: 10.1515/jpem-2016-0111

31. Boecklen WJ, Yarnes CT, Cook BA, James AC. On the use of stable isotopes in trophic ecology. Annu Rev Ecol Evol Syst. 2011;42: 411–440. doi: 10.1146/annurev-ecolsys-102209-144726

32. Post DM. Using stable isotopes to estimate trophic position: Models, methos, and assumptions. Ecology. 2002;83: 703–718. doi: 10.2307/3071875

33. McCutchan JH, Lewis WM, Kendall C, McGrath CC. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos. 2003;102: 378–390. doi: 10.1034/j.1600-0706.2003.12098.x

34. DeNiro MJ, Epstein S. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta. 1978;45: 341–351. doi: 10.1016/0016-7037(81)90244-1

35. Kreipe V, Corral-Hernández E, Scheu S, Schaefer I, Maraun M. Phylogeny and species delineation in European species of the genus Steganacarus (Acari, Oribatida) using mitochondrial and nuclear markers. Exp Appl Acarol. Springer International Publishing; 2015; 173–186. doi: 10.1007/s10493-015-9905-4 25860859

36. Scheu S, Falca M. The soil food web of two beech forests (Fagus sylvatica) of contrasting humus type: Stable isotope analysis of a macro- and a mesofauna-dominated community. Oecologia. 2000;123: 285–296. doi: 10.1007/s004420051015 28308733

37. Halaj J, Peck RW, Niwa CG. Trophic structure of a macroarthropod litter food web in managed coniferous forest stands: A stable isotope analysis with δ15N and δ13C. Pedobiologia (Jena). 2005;49: 109–118. doi: 10.1016/j.pedobi.2004.09.002

38. Maraun M, Erdmann G, Fischer BM, Pollierer MM, Norton RA, Schneider K, et al. Stable isotopes revisited: Their use and limits for oribatid mite trophic ecology. Soil Biol Biochem. Elsevier Ltd; 2011;43: 877–882. doi: 10.1016/j.soilbio.2011.01.003

39. Tiunov A V. Stable isotopes of carbon and nitrogen in soil ecological studies. Biol Bull. 2007;34: 395–407. doi: 10.1134/S1062359007040127

40. Martin A, Balesdent J, Mariotti A. Earthworm diet related to soil organic matter dynamics through 13C measurments. Oecologia. 1992;91: 23–29. doi: 10.1007/BF00317236 28313369

41. Rosumek FB, Blüthgen N, Brückner A, Menzel F, Gebauer G, Heethoff M. Unveiling community patterns and trophic niches of tropical and temperate ants using an integrative framework of field data, stable isotopes and fatty acids. PeerJ. 2018;6. doi: 10.7717/peerj.5467 30155364

42. Chahartaghi M, Langel R, Scheu S, Ruess L. Feeding guilds in Collembola based on nitrogen stable isotope ratios. Soil Biol Biochem. 2005;37: 1718–1725. doi: 10.1016/j.soilbio.2005.02.006

43. Klarner B, Maraun M, Scheu S. Trophic diversity and niche partitioning in a species rich predator guild—Natural variations in stable isotope ratios (13C/12C, 15N/14N) of mesostigmatid mites (Acari, Mesostigmata) from Central European beech. Soil Biol Biochem. Elsevier Ltd; 2013;57: 327–333. doi: 10.1016/j.soilbio.2012.08.013

44. Minor MA, Ermilov SG, Tiunov A V. Taxonomic resolution and functional traits in the analysis of tropical oribatid mite assemblages. Exp Appl Acarol. Springer International Publishing; 2017;73: 365–381. doi: 10.1007/s10493-017-0190-2 29128984

45. Lagerlöf J, Maribie C, John JM. Trophic interactions among soil arthropods in contrasting land-use systems in Kenya, studied with stable isotopes. Eur J Soil Biol. 2017;79: 31–39. doi: 10.1016/j.ejsobi.2017.01.002

46. Flynn DFB, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, et al. Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett. 2009;12: 22–33. doi: 10.1111/j.1461-0248.2008.01255.x 19087109

47. Koh LP, Wilcove DS. Is oil palm agriculture really destroying tropical biodiversity? Conserv Lett. 2008;1: 60–64. doi: 10.1111/j.1755-263X.2008.00011.x

48. Barnes AD, Jochum M, Mumme S, Haneda NF, Farajallah A, Widarto TH, et al. Consequences of tropical land use for multitrophic biodiversity and ecosystem functioning. Nat Commun. Nature Publishing Group; 2014;5: 1–7. doi: 10.1038/ncomms6351 25350947

49. Bowen SH, Allanson BR. Behavioral and trophic plasticity of juvenile Tilapia mossambica in utilization of the unstable littoral habitat. Environ Biol Fishes. 1982;7: 357–362. doi: 10.1007/BF00005570

50. Almeida D, Almodóvar A, Nicola GG, Elvira B, Grossman GD. Trophic plasticity of invasive juvenile largemouth bass Micropterus salmoides in Iberian streams. Fish Res. Elsevier B.V.; 2012;113: 153–158. doi: 10.1016/j.fishres.2011.11.002

51. Drymon JM, Powers SP, Carmichael RH. Trophic plasticity in the Atlantic sharpnose shark (Rhizoprionodon terraenovae) from the north central Gulf of Mexico. Environ Biol Fishes. 2012;95: 21–35. doi: 10.1007/s10641-011-9922-z

52. Riera P. Trophic plasticity of the gastropod Hydrobia ulvae within an intertidal bay (Roscoff, France): A stable isotope evidence. J Sea Res. Elsevier B.V.; 2010;63: 78–83. doi: 10.1016/j.seares.2009.10.001

53. Langel R, Dyckmans J. Combined 13C and 15N isotope analysis on small samples using a near-conventional elemental analyzer/isotope ratio mass spectrometer setup. Rapid Commun Mass Spectrom. 2014;28: 1019–1022. doi: 10.1002/rcm.6878 24677523

54. Guillaume T, Damris M, Kuzyakov Y. Losses of soil carbon by converting tropical forest to plantations: Erosion and decomposition estimated by δ13C. Glob Chang Biol. 2015;21: 3548–3560. doi: 10.1111/gcb.12907 25707391

55. Kempson D, Monte L, Ghelardi R. A new extractor for woodland litter. Pedobiologia 3, 1–21. 1963;

56. Balogh P, Balogh J. The soil mites of the world: Vol. 3: Oribatid mites of the neotropical region II. 3rd ed. Elsevier; 2012.

57. Coplen TB, Hopple JA, Boehike JK, Peiser HS, Rieder SE. Compilation of minimum and maximum isotope ratios of selected elements in naturally occurring terrestrial materials and reagents. 2002 pp. 1–110.

58. Vanderklift M a., Ponsard S. Sources of variation in consumer-diet δ15N enrichment: A meta-analysis. Oecologia. 2003;136: 169–182. doi: 10.1007/s00442-003-1270-z 12802678

59. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing,. Vienna, Austria, Austria; 2018.

60. Bates D, Maechler M, Bolker B, Walker S. Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw. 2015;67: 1–48.

61. Pinheiro J, Bates D, DebRoy S, Sarkar D. Linear and nonlinear mixed effects models. R Packag version. 2007;3: 1–89.

62. Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biometrical J. 2008;50: 346–363.

63. Fischer BM, Schatz H, Maraun M. Community structure, trophic position and reproductive mode of soil and bark-living oribatid mites in an alpine grassland ecosystem. Exp Appl Acarol. 2010;52: 221–237. doi: 10.1007/s10493-010-9366-8 20490626

64. Gan H, Zak DR, Hunter MD. Trophic stability of soil oribatid mites in the face of environmental change. Soil Biol Biochem. Elsevier Ltd; 2014;68: 71–77. doi: 10.1016/j.soilbio.2013.09.019

65. Perdomo G, Evans A, Maraun M, Sunnucks P, Thompson R. Mouthpart morphology and trophic position of microarthropods from soils and mosses are strongly correlated. Soil Biol Biochem. 2012;53: 56–63. doi: 10.1016/j.soilbio.2012.05.002

66. Pollierer MM, Langel R, Scheu S, Maraun M. Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15N/14N and13C/12C). Soil Biol Biochem. Elsevier Ltd; 2009;41: 1221–1226. doi: 10.1016/j.soilbio.2009.03.002

67. Heidemann K, Scheu S, Ruess L, Maraun M. Molecular detection of nematode predation and scavenging in oribatid mites: Laboratory and field experiments. Soil Biol Biochem. Elsevier Ltd; 2011;43: 2229–2236. doi: 10.1016/j.soilbio.2011.07.015

68. Heidemann K, Hennies A, Schakowske J, Blumenberg L, Ruess L, Scheu S, et al. Free-living nematodes as prey for higher trophic levels of forest soil food webs. Oikos. 2014;123: 1199–1211. doi: 10.1111/j.1600-0706.2013.00872.x

69. Rockett CL. Nematode predation by oribatid mites (Acari: Oribatida). Int J Acarol. 1980;6: 219–224. doi: 10.1080/01647958008683222

70. Bluhm C, Scheu S, Maraun M. Oribatid mite communities on the bark of dead wood vary with log type, surrounding forest and regional factors. Appl Soil Ecol. 2015;89: 102–112. https://doi.org/10.1016/j.apsoil.2015.01.013

71. Swift MJ, Heal OW, Anderson JM. Decomposition in terrestrial ecosystems. Decomposition in terrestrial ecosystems. Univ of California Press; 1979.

72. Castellini M a., Rea LD. The biochemistry of natural fasting at its limits. Experientia. 1992;48: 575–582. doi: 10.1007/bf01920242 1612138

73. Gannes LZ, Brien DMO, Martinez C, Jun N. Stable isotopes in animal ecology: Assumptions, caveat, and a call for more laboratory experiments. Ecology. 2007;78: 1271–1276. doi: 10.1890/0012-9658(1997)078[1271:SIIAEA]2.0.CO;2

74. Heethoff M, Scheu S. Reliability of isotopic fractionation (Δ15N, Δ13C) for the delimitation of trophic levels of oribatid mites: Diet strongly affects Δ13C but not Δ15N. Soil Biol Biochem. 2016;101: 124–129. doi: 10.1016/j.soilbio.2016.07.013

75. Norton RA, Behan-Pelletier VM. Calcium carbonate and calcium oxalate as cuticular hardening agents in oribatid mites (Acari: Oribatida). Can J Zool. 1991;69: 1504–1511. https://doi.org/10.1139/z91-210

76. Pachl P, Domes K, Schulz G, Norton RA, Scheu S, Schaefer I, et al. Convergent evolution of defense mechanisms in oribatid mites (Acari, Oribatida) shows no “ghosts of predation past”. Mol Phylogenet Evol. 2012; 412–20.

77. Krashevska V, Sandmann D, Marian F, Maraun M, Scheu S. Leaf litter chemistry drives the structure and composition of soil testate amoeba communities in a tropical montane rainforest of the Ecuadorian Andes. Microb Ecol. Microbial Ecology; 2017;74: 681–690. doi: 10.1007/s00248-017-0980-4 28389728

78. Marian F, Sandmann D, Krashevska V, Maraun M, Scheu S. Leaf and root litter decomposition is discontinued at high altitude tropical montane rainforests contributing to carbon sequestration. Ecol Evol. 2017;7: 6432–6443. doi: 10.1002/ece3.3189 28861246

79. Butenschoen O, Krashevska V, Maraun M, Marian F, Sandmann D, Scheu S. Litter mixture effects on decomposition in tropical montane rainforests vary strongly with time and turn negative at later stages of decay. Soil Biol Biochem. Elsevier Ltd; 2014;77: 121–128. doi: 10.1016/j.soilbio.2014.06.019

80. Teuscher M, Gérard A, Brose U, Buchori D, Clough Y, Ehbrecht M, et al. Experimental biodiversity enrichment in oil-palm-dominated landscapes in Indonesia. Front Plant Sci. 2016;07: 1–15. doi: 10.3389/fpls.2016.01538 27799935

81. Gleixner G, Danier HJ, Werner RA, Schmidt HL. Correlations between the 13C content of primary and secondary plant products in different cell compartments and that in decomposing Basidiomycetes. Plant Physiol. 1993;102: 1287–1290. doi: 10.1104/pp.102.4.1287 12231905

82. Hobbie EA, Werner RA. Bulk carbon isotope patterns in C 3 and C 4 plants: a review and synthesis. New Phytol. 2004;161: 371–385. doi: 10.1046/j.1469-8137.2004.00970.x

83. Bowling DR, Pataki DE, Randerson JT. Carbon isotopes in terrestrial ecosystem pools and CO2 fluxes. New Phytol. 2008;178: 24–40. doi: 10.1111/j.1469-8137.2007.02342.x 18179603

84. Somerfield PJ, Clarke KR. Taxonomic levels, in marine community studies, revisited. Mar Ecol Prog Ser. 1995;127: 113–119.

85. Hirst AJ. Influence of taxonomic resolution on multivariate analyses of arthropod and macroalgal reef assemblages. Mar Ecol Prog Ser. 2006;324: 83–93.

86. Heino J. Taxonomic surrogacy, numerical resolution and responses of stream macroinvertebrate communities to ecological gradients: Are the inferences transferable among regions? Ecol Indic. 2014;36: 186–194.

87. Hanna C, Naughton I, Boser C, Holway D. Testing the effects of ant invasions on non-ant arthropods with high-resolution taxonomic data. Ecol Appl. 2015;25: 1841–1850. doi: 10.1890/14-0952.1 26591450


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