Trophic and non-trophic interactions in a biodiversity experiment assessed by next- generation sequencing

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Tiede, Julia ^a,d   Wemheuer, Bernd ^a   Traugott, Michael ^b   Daniel, Rolf ^a   Tscharntke, Teja ^a   Ebeling, Anne ^c   Scherber, Christoph ^a,d  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF INNSBRUCK   (Austria)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA 18S; PLANT DNA;

ADULT; ARTICLE; BIODIVERSITY; CARABIDAE; CONTROLLED STUDY; DNA DETERMINATION; NEXT GENERATION SEQUENCING; NONHUMAN; ORGANISMAL INTERACTION; PLANTAGO; PREDATION RISK; PTEROSTICHUS MELANARIUS; RANUNCULUS; RUMEX; SPECIES DIVERSITY; SPECIES RICHNESS; VEGETATION; ANIMAL; BEETLE; CHEMISTRY; FEEDING BEHAVIOR; FOOD CHAIN; GENETICS; HIGH THROUGHPUT SEQUENCING; PHYSIOLOGY; PLANT;

ANIMALS; BEETLES; BIODIVERSITY; DNA, PLANT; FEEDING BEHAVIOR; FOOD CHAIN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; PLANTS;

EID: 84959333637     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0148781     Document Type: Article

References (84)

1. Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, et al. Global biodiversity scenarios for the year 2100. Science. 2000; 287: 1770-1774. doi:10.1126/science.287.5459.1770 PMID: 10710299.
2. Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature. 2012; 486: 105-108. doi:10.1038/nature11118 PMID: 22678289.
3. Newbold T, Hudson LN, Hill SLL, Contu S, Lysenko I, Senior RA, et al. Global effects of land use on local terrestrial biodiversity. Nature. 2015; 520: 45-50. doi:10.1038/nature14324 PMID: 25832402.
4. Grace JB, Adler PB, Stanley Harpole W, Borer ET, Seabloom EW. Causal networks clarify productivity- richness interrelations, bivariate plots do not. Funct Ecol. 2014; 28: 787-798. doi:10.1111/1365-2435.12269.
5. Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr. 2005; 75: 3-35. doi:10.1890/04-0922.
6. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, et al. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature. 2006; 443: 989-992. doi:10.1038/nature05202 PMID: 17066035.
7. 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. 2014; 5: 5351. doi:10.1038/ncomms6351 PMID: 25350947.
8. Scherber C, Eisenhauer N, Weisser WW, Schmid B, Voigt W, Fischer M, et al. Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature. 2010; 468: 553-556. doi:10.1038/nature09492 PMID: 20981010.
9. Ebeling A, Meyer ST, Abbas M, Eisenhauer N, Hillebrand H, Lange M, et al. Plant diversity impacts decomposition and herbivory via changes in aboveground arthropods. PLoS ONE. 2014; 9: e106529. doi:10.1371/journal.pone.0106529 PMID: 25226237.
10. Haddad NM, Crutsinger GM, Gross K, Haarstad J, Knops JMH, Tilman D. Plant species loss decreases arthropod diversity and shifts trophic structure. Ecol Lett. 2009; 12: 1029-1039. doi:10.1111/j.1461-0248.2009.01356.x PMID: 19702636.
11. Knops JMH, Tilman D, Haddad NM, Naeem S, Mitchell EAD, Haarstad J, et al. Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecol Lett. 1999; 2: 286-293. doi:10.1046/j.1461-0248.1999.00083.x.
12. Bohan DA, Caron-Lormier G, Muggleton S, Raybould A, Tamaddoni-Nezhad A. Automated discovery of food webs from ecological data using logic-based machine learning. Plos One. 2011; 6: e29028. doi:10.1371/journal.pone.0029028 PMID: 22242111.
13. Gibb H, Stoklosa J, Warton DI, Brown AM, Andrew NR, Cunningham SA. Does morphology predict trophic position and habitat use of ant species and assemblages? Oecologia. 2015; 177: 519-531. doi:10.1007/s00442-014-3101-9 PMID: 25288056.
14. Wimp GM, Murphy SM, Lewis D, Douglas MR, Ambikapathi R, Van-Tull L, et al. Predator hunting mode influences patterns of prey use from grazing and epigeic food webs. Oecologia. 2012; 171: 505-515. doi:10.1007/s00442-012-2435-4 PMID: 22926724.
15. Davey JS, Vaughan IP, Andrew King R, Bell JR, Bohan DA, Bruford MW, et al. Intraguild predation in winter wheat: prey choice by a common epigeal carabid consuming spiders. J Appl Ecol. 2013; 50: 271-279. doi:10.1111/1365-2664.12008.
16. Wallinger C, Staudacher K, Schallhart N, Mitterrutzner E, Steiner E-M, Juen A, et al. How generalist herbivores exploit belowground plant diversity in temperate grasslands. Mol Ecol. 2014; 23: 3826- 3837. doi:10.1111/mec.12579 PMID: 24188592.
17. Wolkovich EM, Allesina S, Cottingham KL, Moore JC, Sandin SA, de Mazancourt C. Linking the green and brown worlds: The prevalence and effect of multichannel feeding in food webs. Ecology. 2014; 95: 3376-3386. doi:10.1890/13-1721.1.
18. Pompanon F, Deagle BE, Symondson WOC, Brown DS, Jarman SN, Taberlet P. Who is eating what: diet assessment using next generation sequencing. Mol Ecol. 2012; 21: 1931-1950. doi:10.1111/j.1365-294X.2011.05403.x PMID: 22171763.
19. Symondson WOC. The molecular revolution: Using polymerase chain reaction based methods to explore the role of predators in terrestrial food webs. In: Gurr GM, Wratten SD, Snyder WE, Read DMY, editors. Biodiversity and Insect Pests. John Wiley & Sons, Ltd; 2012. pp. 166-184. Available: http://onlinelibrary.wiley.com/doi/10.1002/9781118231838.ch10/summary.
20. Traugott M, Kamenova S, Ruess L, Seeber J, Plantegenest M. Empirically characterising trophic networks: What emerging DNA-based methods, stable isotope and fatty acid analyses can offer. In: Woodward G, Bohan DA, editors. Ecological Networks in an Agricultural World. Academic Press; 2013.
21. Lundgren JG, Fergen JK. Predator community structure and trophic linkage strength to a focal prey. Mol Ecol. 2014; 23: 3790-3798. doi:10.1111/mec.12700 PMID: 24612337.
22. Symondson WOC, Harwood JD. Special issue on molecular detection of trophic interactions: Unpicking the tangled bank. Mol Ecol. 2014; 23: 3601-3604. doi:10.1111/mec.12831 PMID: 25051891.
23. Valentini A, Pompanon F, Taberlet P. DNA barcoding for ecologists. Trends Ecol Evol. 2009; 24: 110- 117. doi:10.1016/j.tree.2008.09.011 PMID: 19100655.
24. Clare EL. Molecular detection of trophic interactions: emerging trends, distinct advantages, significant considerations and conservation applications. Evol Appl. 2014; 7: 1144-1157. doi:10.1111/eva.12225 PMID: 25553074.
25. Pompanon F, Samadi S. Next generation sequencing for characterizing biodiversity: promises and challenges. Genetica. 2015; 143: 133-138. doi:10.1007/s10709-015-9816-7 PMID: 25613325.
26. O'Rorke R, Lavery S, Chow S, Takeyama H, Tsai P, Beckley LE, et al. Determining the diet of larvae of western rock lobster (Panulirus cygnus) using high-throughput DNA sequencing techniques. PLoS ONE. 2012; 7: e42757. doi:10.1371/journal.pone.0042757 PMID: 22927937.
27. Clare EL, Symondson WOC, Broders H, Fabianek F, Fraser EE, MacKenzie A, et al. The diet of Myotis lucifugus across Canada: assessing foraging quality and diet variability. Mol Ecol. 2014; 23: 3618- 3632. doi:10.1111/mec.12542 PMID: 24274182.
28. Kéfi S, Berlow EL, Wieters EA, Joppa LN, Wood SA, Brose U, et al. Network structure beyond food webs: mapping non-trophic and trophic interactions on Chilean rocky shores. Ecology. 2015; 96: 291- 303. doi:10.1890/13-1424.1 PMID: 26236914.
29. Thiele HU. Carabid beetles in their environments: a study on habitat selection by adaptations in physiology and behaviour. 1st ed. Berlin, Heidelberg, New York: Springer-Verlag; 1977.
30. Hengeveld R. Polyphagy, oligophagy and food specialization in ground beetles (Coleoptera, Carabidae). Neth J Zool. 1979; 30: 564-584. doi:10.1163/002829679X00197.
31. Lovei GL, Sunderland KD. Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annu Rev Entomol. 1996; 41: 231-256. doi:10.1146/annurev.en.41.010196.001311 PMID: 15012329.
32. Waldner T, Traugott M. DNA-based analysis of regurgitates: a noninvasive approach to examine the diet of invertebrate consumers. Mol Ecol Resour. 2012; 12: 669-675. doi:10.1111/j.1755-0998.2012.03135.x PMID: 22443278.
33. Raso L, Sint D, Mayer R, Plangg S, Recheis T, Brunner S, et al. Intraguild predation in pioneer predator communities of alpine glacier forelands. Mol Ecol. 2014; 23: 3744-3754. doi:10.1111/mec.12649 PMID: 24383765.
34. O'Rorke R, Lavery S, Jeffs A. PCR enrichment techniques to identify the diet of predators. Mol Ecol Resour. 2012; 12: 5-17. doi:10.1111/j.1755-0998.2011.03091.x PMID: 22145916.
35. Vestheim H, Jarman SN. Blocking primers to enhance PCR amplification of rare sequences in mixed samples-a case study on prey DNA in Antarctic krill stomachs. Front Zool. 2008; 5: 12. doi:10.1186/1742-9994-5-12 PMID: 18638418.
36. Piñol J, Mir G, Gomez-Polo P, Agustí N. Universal and blocking primer mismatches limit the use of high-throughput DNA sequencing for the quantitative metabarcoding of arthropods. Mol Ecol Resour. 2014; 819-830. doi:10.1111/1755-0998.12355 PMID: 25454249.
37. Piñol J, San Andrés V, Clare EL, Mir G, Symondson WOC. A pragmatic approach to the analysis of diets of generalist predators: The use of next-generation sequencing with no blocking probes. Mol Ecol Resour. 2013; 18-26. doi:10.1111/1755-0998.12156 PMID: 23957910.
38. Roscher C, Schumacher J, Baade J, Wilcke W, Gleixner G, Weisser WW, et al. The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community. Basic Appl Ecol. 2004; 5: 107-121. doi:10.1078/1439-1791-00216.
39. Ebeling A, Pompe S, Baade J, Eisenhauer N, Hillebrand H, Proulx R, et al. A trait-based experimental approach to understand the mechanisms underlying biodiversity-ecosystem functioning relationships. Basic Appl Ecol. 2014; 15: 229-240.
40. Draper NR, Smith H. Applied regression analysis. Wiley; 1998.
41. Bates ST, Berg-Lyons D, Lauber CL, Walters WA, Knight R, Fierer N. A preliminary survey of lichen associated eukaryotes using pyrosequencing. The Lichenologist. 2012; 44: 137-146. doi:10.1017/S0024282911000648.
42. Walters WA, Caporaso JG, Lauber CL, Berg-Lyons D, Fierer N, Knight R. PrimerProspector: de novo design and taxonomic analysis of barcoded polymerase chain reaction primers. Bioinformatics. 2011; 27: 1159-1161. doi:10.1093/bioinformatics/btr087 PMID: 21349862.
43. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012; gks1219. doi:10.1093/nar/gks1219.
44. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7: 335-336. doi:10.1038/nmeth.f.303 PMID: 20383131.
45. Bragg L, Stone G, Imelfort M, Hugenholtz P, Tyson GW. Fast, accurate error-correction of amplicon pyrosequences using Acacia. Nat Methods. 2012; 9: 425-426.
46. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMB Net. journal. 2011; 17: pp. 10-12. doi:10.14806/ej.17.1.200.
47. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. 2011; 27: 2194-2200. doi:10.1093/bioinformatics/btr381 PMID: 21700674.
48. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010; 26: 2460-2461. doi:10.1093/bioinformatics/btq461 PMID: 20709691.
49. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009; 10: 421. doi:10.1186/1471-2105-10-421 PMID: 20003500.
50. Wright AJ, Ebeling A, de Kroon H, Roscher C, Weigelt A, Buchmann N, et al. Flooding disturbances increase resource availability and productivity but reduce stability in diverse plant communities. Nat Commun. 2015; 6: 6092. doi:10.1038/ncomms7092 PMID: 25600177.
51. Deagle BE, Chiaradia A, McInnes J, Jarman S. Pyrosequencing faecal DNA to determine diet of little penguins: is what goes in what comes out? Conserv Genet. 2010; 11: 2039-2048. doi:10.1007/s10592-010-0096-6.
52. Deagle BE, Thomas AC, Shaffer AK, Trites AW, Jarman SN. Quantifying sequence proportions in a DNA-based diet study using Ion Torrent amplicon sequencing: which counts count? Mol Ecol Resour. 2013; 13: 620-633. doi:10.1111/1755-0998.12103 PMID: 23590207.
53. Ruggiero MA, Gordon DP, Orrell TM, Bailly N, Bourgoin T, Brusca RC, et al. A higher level classification of all living organisms. PLoS ONE. 2015; 10: e0119248. doi:10.1371/journal.pone.0119248 PMID: 25923521.
54. Draganova S, Takov D, Doychev D. Naturally-occurring entomopathogenic fungi on three bark beetle species (Coleoptera: Curculionidae) in Bulgaria. Pestic Fitomedicina. 2010; 25: 59-63. doi:10.2298/PIF1001059D.
55. Sienkiewicz P, Lipa JJ. Prevalence of eugregarines (Apicomplexa: Eugregarinida) parasitizing in ground beetles (Coleoptera, Carabidae) in various habitats. Pol J Entomol. 2009; 4. Available: https://www.infona.pl/resource/bwmeta1.element.agro-99bcbf94-5925-4fc9-866f-dd55d41ee133.
56. Petit S, Boursault A, Bohan DA. Weed seed choice by carabid beetles (Coleoptera: Carabidae): Linking field measurements with laboratory diet assessments. Eur J Entomol. 2014; doi:10.14411/eje.2014.086.
57. Bohan DA, Bohan AC, Glen DM, Symondson WOC, Wiltshire CW, Hughes L. Spatial dynamics of predation by carabid beetles on slugs. J Anim Ecol. 2000; 69: 367-379. doi:10.1046/j.1365-2656.2000.00399.x.
58. McKemey AR, Symondson WOC. Effects of slug size on predation by Pterostichus melanarius (Coleoptera: Carabidae). Biocontrol Sci Technol. 2001; 11: 81-91. doi:10.1080/09583150020029763.
59. Symondson WOC, Glen DM, Erickson ML, Liddell JE, Langdon CJ. Do earthworms help to sustain the slug predator Pterostichus melanarius (Coleoptera: Carabidae) within crops? Investigations using monoclonal antibodies. Mol Ecol. 2000; 9: 1279-1292. doi:10.1046/j.1365-294x.2000.01006.x PMID: 10972768.
60. Prasad RP, Snyder WE. Polyphagy complicates conservation biological control that targets generalist predators. J Appl Ecol. 2006; 43: 343-352. doi:10.1111/j.1365-2664.2006.01129.x.
61. Specht J, Scherber C, Unsicker SB, Köhler G, Weisser WW. Diversity and beyond: plant functional identity determines herbivore performance. J Anim Ecol. 2008; 77: 1047-1055. doi:10.1111/j.1365-2656.2008.01395.x PMID: 18844757.
62. Parker JR, Wakeland CC. Grasshopper egg pods destroyed by larvae of bee flies, blister beetles, and ground beetles. 1st ed. Washington, D.C.: U.S. Department of Agriculture; 1957.
63. Foltan P, Sheppard S, Konvicka M, Symondson WOC. The significance of facultative scavenging in generalist predator nutrition: detecting decayed prey in the guts of predators using PCR. Mol Ecol. 2005; 14: 4147-4158. doi:10.1111/j.1365-294X.2005.02732.x PMID: 16262865.
64. Fain A, Noti MI, Dufrêne M. Observations on the mites (Acari) associated with Carabidae (Coleoptera) in Belgium. I. Annotated list of the species. Int J Acarol. 1995; 21: 107-122. doi:10.1080/01647959508684051.
65. Lundgren JG, Lehman RM. Bacterial gut symbionts contribute to seed digestion in an omnivorous beetle. PLoS ONE. 2010; 5: e10831. doi:10.1371/journal.pone.0010831 PMID: 20520762.
66. Lundgren JG, Lehman RM, Chee-Sanford J. Bacterial communities within digestive tracts of ground beetles (Coleoptera: Carabidae). Ann Entomol Soc Am. 2007; 100: 275-282. doi:10.1603/0013-8746(2007)100[275:BCWDTO]2.0.CO;2.
67. Lilleskov EA, Bruns TD. Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs. Mycologia. 2005; 97: 762-769. doi:10.3852/mycologia.97.4.762 PMID: 16457345.
68. Boyer S, Cruickshank RH, Wratten SD. Faeces of generalist predators as "biodiversity capsules": A new tool for biodiversity assessment in remote and inaccessible habitats. Food Webs. 2015; 3: 1-6.
69. Waldner T, Sint D, Juen A, Traugott M. The effect of predator identity on post-feeding prey DNA detection success in soil-dwelling macro-invertebrates. Soil Biol Biochem. 2013; 63: 116-123. doi:10.1016/j.soilbio.2013.03.030.
70. Sheppard SK, Bell J, Sunderland KD, Fenlon J, Skervin D, Symondson WOC. Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. Mol Ecol. 2005; 14: 4461-4468. doi:10.1111/j.1365-294X.2005.02742.x PMID: 16313606.
71. Forsythe TG. Feeding mechanisms of certain ground beetles (Coleoptera: Carabidae). Coleopt Bull. 1982; 36: 26-73.
72. Gross J, Müller C, Vilcinskas A, Hilker M. Antimicrobial activity of exocrine glandular secretions, hemolymph, and larval regurgitate of the mustard leaf beetle Phaedon cochleariae. J Invertebr Pathol. 1998; 72: 296-303. PMID: 9784354.
73. Olckers T. Biology and physiological host range of four species of Platyphora gistel (Coleoptera: Chrysomelidae) associated with Solanum mauritianum scop. (Solanaceae) in South America. Coleopt Bull. 2000; 54: 497-510. doi:10.1649/0010-065X(2000)054[0497:BAPHRO]2.0.CO;2.
74. Robertson IC. Relative abundance of Nicrophorus pustulatus (Coleoptera: Silphidae) in a burying beetle community, with notes on its reproductive behavior. Psyche J Entomol. 1992; 99: 189-198. doi:10.1155/1992/85675.
75. Lymbery A, Bailey W. Regurgitation as a possible anti-predator defensive mechanism in the grasshopper Goniaea sp. (Acrididae, Orthoptera). Aust J Entomol. 1980; 19: 129-130. doi:10.1111/j.1440-6055.1980.tb00973.x.
76. Grant JB. Diversification of gut morphology in caterpillars is associated with defensive behavior. J Exp Biol. 2006; 209: 3018-3024. doi:10.1242/jeb.02335 PMID: 16857885.
77. Tilman D. The ecological consequences of changes in biodiversity: a search for general principles. Ecology. 1999; 80: 1455-1474. doi:10.1890/0012-9658(1999)080[1455:TECOCI]2.0.CO;2.
78. Hector A, Joshi J, Scherer-Lorenzen M, Schmid B, Spehn EM, Wacker L, et al. Biodiversity and ecosystem functioning: reconciling the results of experimental and observational studies. Funct Ecol. 2007; 21: 998-1002. doi:10.1111/j.1365-2435.2007.01308.x.
79. Brose U. Bottom-up control of carabid beetle communities in early successional wetlands: mediated by vegetation structure or plant diversity? Oecologia. 2003; 135: 407-413. doi:10.1007/s00442-003-1222-7 PMID: 12721831.
80. Hunter MD. Trophic promiscuity, intraguild predation and the problem of omnivores. Agric For Entomol. 2009; 11: 125-131. doi:10.1111/j.1461-9563.2008.00427.x.
81. Toberman H, Freeman C, Evans C, Fenner N, Artz RRE. Summer drought decreases soil fungal diversity and associated phenol oxidase activity in upland Calluna heathland soil. FEMS Microbiol Ecol. 2008; 66: 426-436. doi:10.1111/j.1574-6941.2008.00560.x PMID: 18662311.
82. Stefan G, Cornelia B, Jörg R, Michael B. Soil water availability strongly alters the community composition of soil protists. Pedobiologia. 2014; 57: 205-213. doi:10.1016/j.pedobi.2014.10.001.
83. Lefcheck JS, Byrnes JEK, Isbell F, Gamfeldt L, Griffin JN, Eisenhauer N, et al. Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nat Commun. 2015; 6. doi:10.1038/ncomms7936.
84. Vesterinen EJ, Lilley T, Laine VN, Wahlberg N. Next generation sequencing of fecal DNA reveals the dietary diversity of the widespread insectivorous predator daubenton's bat (Myotis daubentonii) in Southwestern Finland. PLoS ONE. 2013; 8: e82168. doi:10.1371/journal.pone.0082168 PMID: 24312405.