Eur. J. Entomol. 120: 59-69, 2023 | DOI: 10.14411/eje.2023.009

Perennial alternative crops for biogas production increase arthropod abundance and diversity after harvest - results of suction sampling and metabarcodingOriginal article

Johannes BURMEISTER ORCID...1, Bernd PANASSITI ORCID...1, Franziska HEINE2, Sebastian WOLFRUM ORCID...1, Jerome MORINIERE ORCID...3
1 Bavarian State Research Center for Agriculture (LfL), Lange Point 6, 85354 Freising, Germany; e-mails: johannes.burmeister@lfl.bayern.de, bernd.panassiti@lfl.bayern.de, sebastian.wolfrum@lfl.bayern.de
2 School Center Wangen - Agricultural Schools, Jahnstraße 19, 88239 Wangen im Allgäu, Germany; e-mail: franziska.heine94@web.de
3 Advanced Identification Methods - AIM GmbH, Leipzig, Germany; e-mail: jerome.moriniere@aim.science

The effects of novel perennial energy crops on arthropod abundance and diversity were tested using three field trials in Bavaria. Established cup plant (Silphium perfoliatum), Virginia mallow (Sida hermaphrodita) and tall wheat grass (Thinopyrum ponticum) plots were sampled in autumn using a modified leaf blower and their arthropod faunas compared with that recorded in maize plots. At the time of sampling, maize, cup plant and Virginia mallow had already been harvested and samples from the remaining stubble were compared with those from open ground. Collembola were the most abundant group. The highest abundance and diversity of arthropods was recorded in tall wheat grass, with Hemiptera and Aranea especially benefitting from the green and taller vegetation. Post-harvest cup plant and Virginia mallow plots harboured a more diverse and more abundant arthropod assemblage than maize plots. Stubble was identified as a suitable habitat for arthropods in agricultural fields. In conclusion, the integration of perennial energy crops into existing biogas production systems could play an important role in supporting arthropods in agricultural landscapes by providing crucial structures and resources, such as the grassy vegetation of tall wheat grass in autumn and the long-lasting stubbles of cup plant and Virginia mallow.

Keywords: Insects, ground dwelling, perennial, biogas substrate, cup plant, Virigina mallow, tall wheat grass, next generation sequencing

Received: July 29, 2022; Revised: February 21, 2023; Accepted: February 21, 2023; Published online: March 22, 2023  Show citation

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BURMEISTER, J., PANASSITI, B., HEINE, F., WOLFRUM, S., & MORINIERE, J. (2023). Perennial alternative crops for biogas production increase arthropod abundance and diversity after harvest - results of suction sampling and metabarcoding. EJE, 120, Article 59-69. https://doi.org/10.14411/eje.2023.009
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    References

    1. Baines M., Hambler C., Johnson P.J., Macdonald D.W. & Smith H. 1998: The effects of arable field margin management on the abundance and species richness of Araneae (spiders). - Eco­graphy 21: 74-86. Go to original source...
    2. Bates D., Mächler M., Bolker B. & Walker S. 2015: Fitting linear mixed-effects models using lme4. - J. Stat. Soft. 67: 1-48. Go to original source...
    3. Bertrand C., Burel F. & Baudry J. 2016: Spatial and temporal heterogeneity of the crop mosaic influences carabid beetles in agricultural landscapes. - Landsc. Ecol. 31: 451-466. Go to original source...
    4. Boström U. 1995: Earthworm populations (Lumbricidae) in ploughed and undisturbed leys. - Soil Tillage Res. 35: 125-133. Go to original source...
    5. Burmeister J. 2021: Promotion of ground beetles by integrating perennial energy crops into existing agricultural landscapes. - Biomass Bioener. 146: 105973, 11 pp. Go to original source...
    6. Burmeister J. & Panasitti B. 2022: Sample Species Richness Accounting for Different Determination Depth. URL: https://doi.org/10.6084/m9.figshare.21324372.v3 Go to original source...
    7. Chao A., Gotelli N.J., Hsieh T.C., Sander E.L., Ma K.H., Colwell R.K. & Ellison A.M. 2014: Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. - Ecol. Monogr. 84: 45-67. Go to original source...
    8. Chmelíková L. & Wolfrum S. 2019: Mitigating the biodiversity footprint of energy crops - A case study on arthropod diversity. - Biomass Bioener. 125: 180-187. Go to original source...
    9. Cumplido-Marin L., Graves A.R., Burgess P.J., Morhart C., Paris P., Jablonowski N.D., Facciotto G., Bury M., Martens R. & Nahm M. 2020: Two novel energy crops: Sida hermaphrodita (L.) Rusby and Silphium perfoliatum L. - state of knowledge. - Agronomy 10: 928, 67 pp. Go to original source...
    10. Dauber J., Jones M.B. & Stout J.C. 2010: The impact of biomass crop cultivation on temperate biodiversity. - GCB Bioenergy 2: 289-309. Go to original source...
    11. Dauber J., Cass S., Gabriel D., Harte K., Åström S., O'Rourke E. & Stout J.C. 2015: Yield-biodiversity trade-off in patchy fields of Miscanthus × giganteus. - GCB Bioenergy 7: 455-467. Go to original source...
    12. Ebeling A., Hines J., Hertzog L.R., Lange M., Meyer S.T., Simons N.K. & Weisser W.W. 2018: Plant diversity effects on arthropods and arthropod-dependent ecosystem functions in a biodiversity experiment. - Basic Appl. Ecol. 26: 50-63. Go to original source...
    13. Erktan A., Or D. & Scheu S. 2020: The physical structure of soil: Determinant and consequence of trophic interactions. - Soil Biol. Biochem. 148: 107876, 17 pp. Go to original source...
    14. Emmerling C., Ruf T., Audu V., Werner W. & Udelhoven T. 2021: Earthworm communities are supported by perennial bioenergy cropping systems. - Eur. J. Soil Biol. 105: 103331, 11 pp. Go to original source...
    15. Fachagentur für Nachwachsende Rohstoffe e. V. 2022: Basisdaten Bioenergie Deutschland 2021. URL: https://www.fnr.de/fileadmin/Projekte/2020/Mediathek/broschuere_basisdaten_bioenergie_2020_web.pdf (last accessed 29 Apr. 2022).
    16. Fadl A., Purvis G. & Towey K. 1996: The effect of time of soil cultivation on the incidence of Pterostichus melanarius (Illig.) (Coleoptera: Carabidae) in arable land in Ireland. - Ann. Zool. Fenn. 33: 207-214
    17. Fahrig L., Baudry J., Brotons L., Burel F.G., Crist T.O., Fuller R.J., Sirami C., Siriwardena G.M. & Martin J.-L. 2011: Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. - Ecol. Lett. 14: 101-112. Go to original source...
    18. Faith D.P. 1992: Conservation evaluation and phylogenetic diversity. - Biol. Conserv. 61: 1-10. Go to original source...
    19. Förster L., Burmeister J., Walter R., Ebertseder F., Solbach J., Parzefall S., Hartmann A. & Fritz M. 2021: Ertragsstabilität, Etablierung und Umweltparameter mehrjähriger Energiepflanzen - Dauerkulturen II. - Berichte TFZ 71: 312 pp.
    20. Gevers J., Høye T.T., Topping C.J., Glemnitz M. & Schröder B. 2011: Biodiversity and the mitigation of climate change through bioenergy: impacts of increased maize cultivation on farmland wildlife. - GCB Bioenergy 3: 472-482. Go to original source...
    21. Grass I., Loos J., Baensch S., Batáry P., Librán-Embid F., Ficiciyan A., Klaus F., Riechers M., Rosa J., Tiede J., Udy K., Westphal C., Wurz A. & Tscharntke T. 2019: Land-sharing/-sparing connectivity landscapes for ecosystem services and biodiversity conservation. - People Nat. 1: 262-272. Go to original source...
    22. Grunwald D., Panten K., Schwarz A., Bischoff W.-A. & Schittenhelm S. 2020: Comparison of maize, permanent cup plant and a perennial grass mixture with regard to soil and water protection. - GCB Bioenergy 12: 694-705. Go to original source...
    23. Hallmann C.A., Sorg M., Jongejans E., Siepel H., Hofland N., Schwan H., Stenmans W., Müller A., Sumser H., Hörren T., Goulson D. & de Kroon H. 2017: More than 75 percent decline over 27 years in total flying insect biomass in protected areas. - PLoS ONE 12(10): e0185809, 21 pp. Go to original source...
    24. Harrison T. & Berenbaum M.R. 2013: Moth diversity in three biofuel crops and native prairie in Illinois. - Insect Sci. 20: 407-419. Go to original source...
    25. Hartig F. 2021: DHARMa: Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. URL: https://CRAN.R-project.org/package=DHARMa (last accessed 29 Apr. 2022).
    26. Hawlitschek O., Morinière J., Lehmann G.U.C., Lehmann A.W., Kropf M., Dunz A., Glaw F., Detcharoen M., Schmidt S., Hausmann A., Szucsich N.U., Caetano-Wyler S.A. & Haszprunar G. 2017: DNA barcoding of crickets, katydids and grasshoppers (Orthoptera) from Central Europe with focus on Austria, Germany and Switzerland. - Mol. Ecol. Res. 17: 1037-1053. Go to original source...
    27. Hsieh T.C., Ma K.H. & Chao A. 2020: iNEXT: iNterpolation and EXTrapolation for Species Diversity. URL: https://CRAN.R-Project.org/package=iNEXT (last accessed 29 Apr. 2022).
    28. Isaacs R., Tuell J., Fiedler A., Gardiner M. & Landis D. 2009: Maximizing arthropod-mediated ecosystem services in agricultural landscapes: the role of native plants. - Front. Ecol. Environ. 7: 196-203. Go to original source...
    29. Kleijn D., Kohler F., Báldi A., Batáry P., Concepción E.D., Clough Y., Díaz M., Gabriel D., Holzschuh A., Knop E., Kovács A., Marshall E.J.P., Tscharntke T. & Verhulst J. 2009: On the relationship between farmland biodiversity and land-use intensity in Europe. - Proc. R. Soc. (B) 276: 903-909. Go to original source...
    30. Lask J., Magenau E., Ferrarini A., Kiesel A., Wagner M. & Lewandowski I. 2020: Perennial rhizomatous grasses: Can they really increase species richness and abundance in arable land? - A meta-analysis. - GCB Bioenergy 12: 968-978. Go to original source...
    31. Lefcheck J.S. 2016: piecewiseSEM: Piecewise structural equation modelling in r for ecology, evolution, and systematics. - Methods Ecol. Evol. 7: 573-579. Go to original source...
    32. Lenth R. 2019: emmeans: Estimated Marginal Means, aka Least-Squares Means. URL: https://CRAN.R-project.org/package=emmeans (last accessed 29 Apr. 2022).
    33. Leray M., Yang J.Y., Meyer C.P., Mills S.C., Agudelo N., Ranwez V., Boehm J.T. & Machida R.J. 2013: A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. - Front. Zool. 10: 34, 14 pp. Go to original source...
    34. Marja R., Tscharntke T. & Batáry P. 2022: Increasing landscape complexity enhances species richness of farmland arthropods, agri-environment schemes also abundance - A meta-analysis. - Agric. Ecosyst. Environ. 326: 107822, 7 pp. Go to original source...
    35. Martin M. 2011: Cutadapt removes adapter sequences from high-throughput sequencing reads. - EMBnet J. 17(1): 10, 3 pp. Go to original source...
    36. Mommerts S., Schauer C., Kösters N., Lang A. & Filser J. 1996: A comparison of D-Vac suction, fenced and unfenced pitfall trap sampling of epigeal arthropods in agro-ecosystems. - Ann. Zool. Fenn. 33: 117-124.
    37. Morinière J., Cancian de Araujo B., Lam A.W., Hausmann A., Balke M., Schmidt S., Hendrich L., Doczkal D., Fartmann B., Arvidsson S. & Haszprunar G. 2016: Species identification in Malaise trap samples by DNA barcoding based on NGS technologies and a scoring matrix. - PLoS ONE 11(5): e0155497, 14 pp. Go to original source...
    38. Morinière J., Balke M., Doczkal D., Geiger M.F., Hardulak L.A., Haszprunar G., Hausmann A., Hendrich L., Regalado L., Rulik B., Schmidt S., Wägele J.-W. & Hebert P.D.N. 2019: A DNA barcode library for 5,200 German flies and midges (Insecta: Diptera) and its implications for metabarcoding-based biomonitoring. - Mol. Ecol. Res. 19: 900-928. Go to original source...
    39. Mueller A.L. & Dauber J. 2016: Hoverflies (Diptera: Syrphidae) benefit from a cultivation of the bioenergy crop Silphium perfoliatum L. (Asteraceae) depending on larval feeding type, landscape composition and crop management. - Agric. For. Entomol. 18: 419-431. Go to original source...
    40. Nardi D., Lami F., Pantini P. & Marini L. 2019: Using species-habitat networks to inform agricultural landscape management for spiders. - Biol. Conserv. 239: 108275, 8 pp. Go to original source...
    41. Narimanov N., Kempel A., van Kleunen M. & Etnling m. H. 2021: Unexpected sensitivity of the highly invasive spider Mermessus trilobatus to soil disturbance in grasslands. - Biol. Invas. 23: 1-6. Go to original source...
    42. Norris S.L., Blackshaw R.P., Critchley C.N.R., Dunn R.M., Smith K.E., Williams J., Randall N.P. & Murray P.J. 2018: Intercropping flowering plants in maize systems increases pollinator diversity. - Agric. For. Entomol. 20: 246-254. Go to original source...
    43. Paradis E. 2010: pegas: an R package for population genetics with an integrated-modular approach. - Bioinformatics 26: 419-420. Go to original source...
    44. Paradis E. & Schliep K. 2019: ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. - Bioinformatics 35: 526-529. Go to original source...
    45. Platen R., Konrad J. & Glemnitz M. 2017: Novel energy crops: an opportunity to enhance the biodiversity of arthropod assemblages in biomass feedstock cultures? - Int. J. Biodiv. Sci. Ecosyst. Serv. Manag. 13: 162-171. Go to original source...
    46. Porter T.M. & Hajibabaei M. 2018: Automated high throughput animal CO1 metabarcode classification. - Sci. Rep. 8(1): 4226, 10 pp. Go to original source...
    47. Potapov A.A., Semenina E.E., Korotkevich A.Y., Kuznetsova N.A. & Tiunov A.V. 2016: Connecting taxonomy and ecology: Trophic niches of collembolans as related to taxonomic identity and life forms. - Soil Biol. Biochem. 101: 20-31. Go to original source...
    48. Radzikowski P., Matyka M. & Berbeæ A.K. 2020: Biodiversity of weeds and arthropods in five different perennial industrial crops in Eastern Poland. - Agriculture 10(12): 636, 27 pp. Go to original source...
    49. Raupach M.J., Hannig K., Morinière J. & Hendrich L. 2019: About Notiophilus Duméril, 1806 (Coleoptera, Carabidae): Species delineation and phylogeny using DNA barcodes. - Dtsch. Entomol. Z. 66: 63-73. Go to original source...
    50. Robertson B.A., Porter C., Landis D.A. & Schemske D.W. 2012: Agroenergy crops influence the diversity, biomass, and guild structure of terrestrial arthropod communities. - Bioenerg. Res. 5: 179-188. Go to original source...
    51. Roßberg D. 2016: Erhebungen zur Anwendung von Pflanzenschutzmitteln im Ackerbau. - J. Kulturpfl. 68: 25-37.
    52. Rosenfield M.F., Brown L.M. & Anand M. 2022: Increasing cover of natural areas at smaller scales can improve the provision of biodiversity and ecosystem services in agroecological mosaic landscapes. - J. Environ. Manag. 303: 114248, 7 pp. Go to original source...
    53. R Core Team 2021: R: A Language and Environment for Statistical Computing. Vienna, URL: https://www.R-project.org/.
    54. Rognes T., Flouri T., Nichols B., Quince C. & Mahé F. 2016: VSEARCH: a versatile open source tool for metagenomics. - PeerJ 4: e2584, 22 pp. Go to original source...
    55. Saitou N. & Nei M. 1987: The neighbor-joining method: a new method for reconstructing phylogenetic trees. - Mol. Biol. Evol. 4: 406-425.
    56. Salman I.N., Gavish-Regev E., Saltz D. & Lubin Y. 2019: The agricultural landscape matters: spider diversity and abundance in pomegranate orchards as a case study. - BioControl 64: 583-593. Go to original source...
    57. Sánchez-Bayo F. & Wyckhuys K.A.G. 2019: Worldwide decline of the entomofauna: A review of its drivers. - Biol. Conserv. 232: 8-27. Go to original source...
    58. Sánchez-Bayo F. & Wyckhuys K.A.G. 2021: Further evidence for a global decline of the entomofauna. - Austral Entomol. 60: 9-26. Go to original source...
    59. Sanders D. & Entling M.H. 2011: Large variation of suction sampling efficiency depending on arthropod groups, species traits, and habitat properties. - Entomol. Exp. Appl. 138: 234-243. Go to original source...
    60. Schaafsma A.W., Meloche F. & Pitblado R.E. 1996: Effect of mowing corn stalks and tillage on overwintering mortality of European corn borer (Lepidoptera: Pyralidae) in field corn. - J. Econ. Entomol. 89: 1587-1592. Go to original source...
    61. Schorpp Q. & Schrader S. 2016: Earthworm functional groups respond to the perennial energy cropping system of the cup plant (Silphium perfoliatum L.). - Biomass Bioener. 87: 61-68. Go to original source...
    62. Schorpp Q. & Schrader S. 2017: Dynamic of nematode communities in energy plant cropping systems. - Eur. J. Soil Biol. 78: 92-101. Go to original source...
    63. Scordia D. & Cosentino S. 2019: Perennial energy grasses: Resilient crops in a changing European agriculture. - Agriculture 9(8): 169, 19 pp. Go to original source...
    64. Seibold S., Gossner M.M., Simons N.K., Blüthgen N., Müller J., Ambarli D., Ammer C., Bauhus J., Fischer M., Habel J.C., Linsenmair K.E., Nauss T., Penone C., Prati D., Schall P., Schulze E.-D., Vogt J., Wöllauer S. & Weisser W.W. 2019: Arthropod decline in grasslands and forests is associated with landscape-level drivers. - Nature 574: 671-674. Go to original source...
    65. Simons N.K., Gossner M.M., Lewinsohn T.M., Boch S., Lange M., Müller J., Pa¹aliæ E., Socher S.A., Türke M., Fischer M. & Weisser W.W. 2014: Resource-mediated indirect effects of grassland management on arthropod diversity. - PLoS ONE 9(9): e107033, 12 pp. Go to original source...
    66. Steidle J.L.M., Kimmich T., Csader M. & Betz O. 2022: Negative impact of roadside mowing on arthropod fauna and its reduction with 'arthropod-friendly' mowing technique. - J. Appl. Entomol. 146: 465-473. Go to original source...
    67. Theuerl S., Herrmann C., Heiermann M., Grundmann P., Landwehr N., Kreidenweis U. & Prochnow A. 2019: The future agricultural biogas plant in Germany: A vision. - Energies 12(3): 396, 32 pp. Go to original source...
    68. Tscharntke T., Grass I., Wanger T.C., Westphal C. & Batáry P. 2021: Beyond organic farming - harnessing biodiversity-friendly landscapes. - Trends Ecol. Evol. 36: 919-930. Go to original source...
    69. Uellendahl H., Wang G., Møller H.B., Jørgensen U., Skiadas I.V., Gavala H.N. & Ahring B.K. 2008: Energy balance and cost-benefit analysis of biogas production from perennial energy crops pretreated by wet oxidation. - Water Sci. Technol. 58: 1841-1847. Go to original source...
    70. Wagner D.L., Grames E.M., Forister M.L., Berenbaum M.R. & Stopak D. 2021: Insect decline in the Anthropocene: Death by a thousand cuts. - Proc. Natn. Acad. Sci. U.S.A. 118(2): e2023989118, 10 pp. Go to original source...
    71. Williams M.A., Feest A., Williams M.A. & Feest A. 2019: The effect of Miscanthus cultivation on the biodiversity of ground beetles (Coleoptera: Carabidae), spiders and harvestmen (Arachnida: Araneae and Opiliones). - Agric. Sci. 10: 903-917. Go to original source...
    72. Winter M., Devictor V. & Schweiger O. 2013: Phylogenetic diversity and nature conservation: where are we? - Trends Ecol. Evol. 28: 199-204. Go to original source...
    73. Wright E.S. 2016: Using DECIPHER v2.0 to analyze big biological sequence data in R. - The R Journal 8(1) 352, 8 pp. Go to original source...
    74. Xu J., Dang H., Wang M., Chai Y., Guo Y., Chen Y., Zhang C. & Yue M. 2019: Is phylogeny more useful than functional traits for assessing diversity patterns under community assembly processes? - Forests 10(12): 1159, 11 pp. Go to original source...
    75. Yang X., Liu Y., Thrän D., Bezama A. & Wang M. 2021: Effects of the German Renewable Energy Sources Act and environmental, social and economic factors on biogas plant adoption and agricultural land use change. - Energ. Sustain. Soc. 11(1), 22 pp. Go to original source...
    76. Yu G., Smith D.K., Zhu H., Guan Y. & Lam T.T. 2017: ggtree an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. - Methods Ecol. Evol. 8: 28-36. Go to original source...
    77. Zuur A., Ieno E.N., Walker N., Saveliev A.A. & Smith G.M. 2009: Mixed Effects Models and Extensions in Ecology with R. Springer, New York, 574 pp. Go to original source...

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