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Organic vs. organic – soil arthropods as bioindicators of ecological sustainability in greenhouse system experiment under Mediterranean conditions

  • Suzana Madzaric (a1) (a2), F.G. Ceglie (a2), L. Depalo (a3), L. Al Bitar (a2), G. Mimiola (a2), F. Tittarelli (a4) and G. Burgio (a3)...


Organic greenhouse (OGH) production is characterized by different systems and agricultural practices with diverse environmental impact. Soil arthropods are widely used as bioindicators of ecological sustainability in open field studies, while there is a lack of research on organic production for protected systems. This study assessed the soil arthropod abundance and diversity over a 2-year crop rotation in three systems of OGH production in the Mediterranean. The systems under assessment differed in soil fertility management: SUBST – a simplified system of organic production, based on an input substitution approach (use of guano and organic liquid fertilizers), AGROCOM – soil fertility mainly based on compost application and agroecological services crops (ASC) cultivation (tailored use of cover crops) as part of crop rotation, and AGROMAN – animal manure and ASC cultivation as part of crop rotation. Monitoring of soil fauna was performed by using pitfall traps and seven taxa were considered: Carabidae, Staphylinidae, Araneae, Opiliones, Isopoda, Myriapoda, and Collembola. Results demonstrated high potential of ASC cultivation as a technique for beneficial soil arthropod conservation in OGH conditions. SUBST system was dominated by Collembola in all crops, while AGROMAN and AGROCOM had more balanced relative abundance of Isopoda, Staphylinidae, and Aranea. Opiliones and Myriapoda were more affected by season, while Carabidae were poorly represented in the whole monitoring period. Despite the fact that all three production systems are in accordance with the European Union regulation on organic farming, findings of this study displayed significant differences among them and confirmed the suitability of soil arthropods as bioindicators in protected systems of organic farming.


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Andre, H.M., Duarme, X. & Lebrum, P. (2002) Soil biodiversity: myth, reality or conning? Oikos 96, 324.
Ayres, E., Steltzer, H., Simmons, B.L., Simpson, R.T., Steinweg, J.M., Wallenstein, M.D., Mellor, N., Parton, W.J., Moore, J.C. & Wall, D.H. (2009) Home-field advantage accelerates leaf litter decomposition in forests. Soil Biology and Biochemistry 41, 606610.
Bell, J.R., Traugott, M., Sunderland, K.D., Skirvin, D.J., Mead, A., Kravar-Garde, L., Reynolds, K., Fenlon, J.S. & Symondson, W.O.C. (2008) Beneficial links for the control of aphids: the effects of compost applications on predators and prey. Journal of Applied Ecology 45, 12661273.
Bengtsson, J., Ahnström, J., Weibull, A. & Weibull, A.C. (2005) The effects of organic agriculture on biodiversity and abundance: a meta-analysis. Journal of Applied Ecology 42, 261269.
Biaggini, M., Consorti, R., Dapporto, L., Dellacasa, M., Paggetti, E. & Corti, C. (2007) The taxonomic level order as a possible tool for rapid assessment of arthropod diversity in agricultural landscapes. Agriculture, Ecosystem & Environment 122, 183191.
Birkhofer, K., Bezemer, T.M., Bloem, J., Bonkowski, M., Christensen, S., Dubois, D., Ekelund, F., Fliessbach, A., Gunst, L., Hedlund, K., Mader, P., Mikola, J., Robin, C., Setala, H., Tatin-Froux, F., Van der Putten, W.H. & Scheu, S. (2008) Long term organic farming fosters below and aboveground biota: implications for soil quality, biological control and productivity. Soil Biology and Biochemistry 40, 22972308.
Bohac, J. (1999) Staphylinid beetles as bioindicators. Agriculture, Ecosystem & Environment 74, 357372.
Burgio, G., Campanelli, G., Leteo, F., Ramilli, F., Depalo, L., Fabbri, R. & Sgolastra, F. (2015) Ecological sustainability of an organic four-year vegetable rotation system: carabids and other soil arthropods as bioindicators. Agroecology and Sustainable Food Systems 39, 295316.
Caballero-López, B., Blanco-Moreno, J.M., Pérez, N., Pujade-Villar, J., Ventura, D., Oliva, F. & Sans, F.X. (2010) A functional approach to assessing plant–arthropod interaction in winter wheat. Agriculture, Ecosystem & Environment 137, 288293.
Canali, S., Diacono, M., Campanelli, G. & Montemurro, F. (2015) Organic no-till with roller crimpers: agro-ecosystem services and applications in organic Mediterranean vegetable productions. Sustainable Agriculture Research 4, 6675.
Cárdenas, M., Castro, J. & Campos, M. (2012) Short-term response of soil spiders to cover-crop removal in an organic olive orchard in a Mediterranean setting. Journal of Insect Science 12, 118.
Ciaccia, C., Testani, E., Campanelli, G., Sestili, S., Leteo, F., Tittarelli, F., Riva, F., Canali, S. & Trinchera, A. (2015) Ecological service providing crops effect on melon-weed competition and allelopathic interactions. Organic Agriculture 5, 199207.
Clough, Y., Holzschuh, A., Gabriel, D., Purtauf, T., Kleijn, D., Kruess, A., Steffan-Dewenter, I. & Tscharntke, T. (2007a) Alpha and beta diversity of arthropods and plants in organically and conventionally managed wheat fields. Journal of Applied Ecology 44, 804812.
Clough, Y., Kruess, A. & Tscharntke, T. (2007b) Organic versus conventional arable farming systems: functional grouping helps understand Staphylinid response. Agriculture, Ecosystem & Environment 118, 285290.
Collins, K.L., Boatman, N.D., Wilcox, A., Holland, J.M. & Chaney, K. (2002) Influence of beetle banks on cereal aphid predation in winter wheat. Agriculture, Ecosystem & Environment 93, 337350.
Depalo, L., Burgio, G., Von Fragstein, P., Kristensen, H.L., Bavec, M., Robačer, M., Campanelli, G. & Canali, S. (2016) Impact of living mulch on arthropod fauna: analysis of pest and beneficial dynamics on organic cauliflower (Brassica oleracea L. var. botrytis) in different European scenarios. Renewable Agriculture and Food Systems 32, 18.
Diekötter, T., Wamser, S., Wolters, V. & Birkhofer, K. (2010) Landscape and management effects on structure and function of soil arthropod communities in winter wheat. Agriculture, Ecosystem & Environment 137, 108112.
Drinkwater, L.E. (2002) Cropping systems research: reconsidering agricultural experimental approaches. HortTechnology 12, 355361.
Ebeling, A., Pompe, S., Baade, J., Eisenhauer, N., Hillebrand, H., Proulx, R., Roscher, C., Schmid, B., Wirth, C. & Weisser, W.W. (2014) Plant diversity impacts decomposition and herbivory via changes in aboveground arthropods. PLoS ONE 9, e106529.
EC [European Council] (2007) Council regulation (EC) No 834/2007 on organic production and labeling of organic products and repealing Regulation (EEC) No 2092/91. O.J. of the European Union of the 20/07/2007 L 189/1.
Eisenhauer, N., Sabais, A.C.W. & Scheu, S. (2011) Collembola species composition and diversity effects on ecosystem functioning vary with plant functional group identity. Soil Biology and Biochemistry 43, 16971704.
Ekroos, J., Hyvonen, T., Tiainen, J. & Tiira, M. (2010) Responses in plant and carabid communities to farming practises in boreal landscapes. Agriculture, Ecosystem & Environment 135, 288293.
Endlweber, K. & Scheu, S. (2007) Interactions between myccorhizal fungi and Collembola: effects on root structure of competing plant species. Biology and Fertility of Soils 43, 741749.
Frampton, G.K., Van Den Brink, P.J. & Gould, P.J.L. (2000) Effects of spring drought and irrigation on farmland arthropods in southern Britain. Journal of Applied Ecology 37, 865883.
Gkisakis, V., Volakakis, N., Kollaros, D., Barberi, P. & Kabourakis, E.M. (2016) Soil arthropod community in the olive agroecosystem: determined by environment and farming practices in different management systems and agroecological zones. Agriculture, Ecosystem & Environment 218, 178189.
Good, J.A. & Giller, P.S. (1991) The effect of cereal and grass management on Staphylinid (Coleoptera) assemblages in South West Ireland. Journal of Applied Ecology 28, 810826.
Goldberger, J.R. (2011) Conventionalization, civic engagement, and the sustainability of organic agriculture. Journal of Rural Studies 27, 288296.
Hall, A. & Mogyorody, V. (2001) Organic farmers in Ontario: an examination of the conventionalization argument. Sociologia Ruralis 41, 399422.
Hole, D.G., Perkins, A.J., Wilson, J.D., Alexander, I.H., Grice, P.V. & Evans, A.D. (2005) Does organic farming benefit biodiversity? Biological Conservation 122, 113130.
Hopkin, S.P. (1997) Biology of the Springtails (Insecta: Collembola). New York, Oxford University Press.
Høye, T. T. & Forchhammer, M. C. (2008) The influence of weather conditions on the activity of high arctic arthropods inferred from long-term observations. BMC Ecology 8, 8.
Jabbour, R., Pisani-Gareau, T., Smith, R.G., Mullen, C. & Barbercheck, M. (2016) Cover crop and tillage intensities alter ground-dwelling arthropod communities during the transition to organic production. Renewable Agriculture and Food Systems 31, 361374.
Kampichler, C. & Geissen, V. (2005) Temporal predictability of soil microarthropod communities in temperate forests. Pedobiologia 49, 4150.
Kikas, A. & Luik, A. (2002) The influence of different mulches on strawberry yield and beneficial entomofauna. Acta Horticulturae 567, 701704.
Kotze, D.J., Brandmayr, P., Casale, A., Dauffy-Richard, E., Dekoninck, W., Koivula, M.J., Lövei, G.L., Mossakowski, D., Noordijk, J., Paarmann, W., Pizzolotto, R., Saska, P., Schwerk, A., Serrano, J., Szyszko, J., Taboada, A., Turin, H., Venn, S., Vermeulen, R. & Zetto, T. (2005) Forty years of carabid beetle research in Europe - from taxonomy, biology, ecology and population studies to bioindication, habitat assessment and conservation. ZooKeys 100, 55148.
Kracht, M. & Schrader, S. (1997) Collembola and Acari in compacted soil of agricultural land under different soil tillage systems. Braunschweiger Naturkundliche Schriften 5, 425440.
Kromp, B. (1999) Carabid beetles in sustainable agriculture: a review on pest control efficacy, cultivation impacts and enhancement. Journal of Applied Ecology 74, 187228.
Lensing, J.R., Todd, S. & Wise, D.H. (2005) The impact of altered precipitation on spatial stratification and activity-densities of springtails (Collembola) and spiders (Araneae). Ecological Entomology 30, 194200.
Lindberg, N., Engtsson, J.B. & Persson, T. (2002) Effects of experimental irrigation and drought on the composition and diversity of soil fauna in a coniferous stand. Journal of Applied Ecology 39, 924936.
Mathews, C.R., Bottrell, D.G. & Brown, M.W. (2004) Habitat manipulation of the apple orchard floor to increase ground-dwelling predators and predation of Cydia pomonella (L.) (Lepidoptera: Tortricidae). Biological Control 30, 265273.
Milcu, A., Partsch, S., Langel, R. & Scheu, S. (2006) The response of decomposers (earthworms, springtails and microorganisms) to variations in species and functional group diversity of plants. Oikos 112, 513524.
Nasir, S., Akram, W., Zahid, F.M., Ahmed, F., Hussain, S.M. & Nasir, I. (2015) Effect of crop type and production systems (conventional and organic agriculture) on the density of rove beetles (Staphylinidae: Coleoptera) in the Punjab, Pakistan. Journal of the Kansas Entomological Society 88, 19.
Paoletti, M.G. & Bressan, M. (1996) Soil invertebrates as bioindicators of human disturbance. Critical Reviews in Plant Sciences 15, 2162.
Paoletti, M.G. & Hassall, M. (1999) Woodlice (Isopoda: Oniscidea): their potential for assessing sustainability and use as bioindicators. Journal of Applied Ecology 74, 157165.
Pinto da Rocha, R., Machado, G. & Giribet, G. (2007) Harvestman – The Biology of Opiliones. USA, Harvard University Press.
Randall, N.P. & James, K.L. (2012) The effectiveness of integrated farm management, organic farming and agri-environment schemes for conserving biodiversity in temperate Europe – a systematic map. Environmental Evidence 1, 121.
Razo-González, M., Castaño-Meneses, G., Callejas-Chavero, A., Pérez-Velázquez, D. & Palacios-Vargasa, J.G. (2014) Temporal variations of soil arthropods community structure in El Pedregal de San Ángel Ecological Reserve, Mexico City, Mexico. Applied Soil Ecology 83, 8894.
Sanguankeo, P.P. & León, R.G. (2011) Weed management practices determine plant and arthropod diversity and seed predation in vineyards. Weed Research 51, 404412.
Southwood, T.R.E. & Henderson, P.A. (2000). Ecological Methods. Oxford, Blackwell Science.
Scholberg, J.M.S., Dogliott, S., Zotarelli, L., Cherr, C.M., Leoni, C. & Rossing, W.A.H. (2010) Cover crops in agrosystems, innovations and applications. pp. 5998 in Lichtfouse, E. (ed.), Sustainable Agriculture Reviews 4: Genetic Engineering, Biofertilisation, Soil Quality and Organic Farming. Dordrecht, The Netherlands, Springer.
Smeding, F.W. & de Snoo, G.R. (2003) A concept of food-web structure in organic arable farming systems. Landscape and Urban Planning 65, 219236.
Snyder, B.A. & Hendrix, P.F. (2008) Current and potential roles of soil macroinvertebrates (earthworms, millipedes, and isopods) in ecological restoration. Restoration Ecology 16, 629636.
Sunderland, K. & Samu, F. (2000) Effects of agricultural diversification on the abundance, distribution, and pest control potential of spiders: a review. Entomologia Experimentalis et Applicata 95, 113.
Thiele, H. U. (1977). Carabid Beetles in Their Environment. New York, Springer.
Tittarelli, F., Ceglie, F.G., Ciaccia, C., Mimiola, G., Amodio, M.L. & Colelli, G. (2016) Organic strawberry in Mediterranean greenhouse: effect of different production systems on soil fertility and fruit quality. Renewable Agriculture and Food Systems First View, 113.
Tuovinen, T., Kikas, A., Tolonen, T. & Kivijärvi, P. (2006) Organic mulches vs. black plastic in organic strawberry: does it makes a difference for ground beetles (Col., Carabidae)? Journal of Applied Entomology 130, 495503.
Van Lenteren, J.C. (2000) A greenhouse without pesticides: fact or fantasy? Crop Protection 19, 375384.
Van Straalen, N.M. (1998) Evaluation of bioindicator systems derived from soil arthropod communities. Applied Soil Ecology 9, 429437.
Wang, S., Chen, H.Y., Tan, Y., Fan, H. & Ruan, H. (2016) Fertilizer regime impacts on abundance and diversity of soil fauna across a poplar plantation chronosequence in coastal Eastern China. Scientific Reports 6, 208216.
Wardle, D.A., Nicholson, K.S., Bonner, K.I. & Yeates, G.W. (1999) Effects of agricultural intensification on soil-associated arthropod population dynamics, community structure, diversity and temporal variability over a seven-year period. Soil Biology and Biochemistry 31, 16911706.
Woodcock, B.A., Redheada, J., Vanbergenb, A.J., Hulmesa, L., Hulmesa, S., Peytona, J., Nowakowskic, M., Pywella, R.F. & Hearda, M.S. (2010) Impact of habitat type and landscape structure on biomass, species richness and functional diversity of ground beetles. Journal of Applied Ecology 139, 181186.
Zhu, X. & Zhu, B. (2015) Diversity and abundance of soil fauna as influenced by long term fertilization in cropland of purple soil, China. Soil and Tillage Research 146, 3946.



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