Abstract
Maintaining biodiversity in agricultural systems is essential, as it plays a key role in ecosystem services provision. However, it is declining at an unprecedented rate. Several methods can contribute to increasing species diversity in agroecosystems, including the use of artificial microhabitats. Studies focusing on biodiversity in vineyards have been carried out recently, mainly in Europe and North America, but are scarce in South America. In this study, we investigate whether introduced environmental variability and habitat complexity, using corrugated cardboard bands, enhances spider abundance and diversity in vineyards. Spiders were collected from grapevine plants, using two collecting methods (foliage beating and direct collection). Plants with and without cardboard bands (N = 30) were sampled in three different phenological stages of the vineyard (veraison, maturity and postharvest). Overall, we collected 904 spiders belonging to 35 species. We found that spider abundance and species richness significantly increased with cardboard bands. In addition, we identified particular species that prefer cardboard bands to build their shelters. Results suggest that cost-effective habitat manipulation can increase spider abundance in vineyards, which implies higher biodiversity conservation value and potential for improving biological control.
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The authors confirm that the data supporting the findings of this study are available from the corresponding author (GP), upon reasonable request.
References
Addante R, Di Gioia S, Calculli C, Pollice A (2008) The impact of spiders (Araneae) on Lobesia botrana (Denis & Schiffermüller) population density. IOBC/WPRS Bull 36:221–231
Alderweireldt M (1994) Habitat manipulations increasing spider densities in agroecosystems: possibilities for biological control? J App Entomol 118(1–5):10–16
Altieri MA, Nicholls CI (2004) Biodiversity and pest management in agroecosystems. CRC Press, Boca Raton
Altieri MA, Ponti L, Nicholls CI (2005) Enhanced pest management through soil health: toward a blow ground habitat management strategy. Biodynamics 253:33–40
Barzola-Elizagaray P, Engelman A (2020) La vitivinicultura en Mendoza desde 1990: entre la globalización y el desarrollo regional. Íconos Rev Cs Social 66:191–212 (In Spanish)
Baydizada N, Tóthová A, Pekár S (2020) Tracing the evolution of trophic specialization and mode of attack behaviour in the ground spider family Gnaphosidae. Org Divers Evol. https://doi.org/10.1007/s13127-020-00453-0
Birkhofer K, Entling MH, Lubin Y (2013) Agroecology: trait composition, spatial relationships, trophic interactions. In: Penney D (ed) Spider research in the 21st century: trends & perspectives. Siri Scientific Press, Rochdale, pp 200–228
Bogya S, Szinetár C, Markó V (1999) Species composition of spider (Araneae) assemblages in apple and pear orchards in the Carpathian Basin. Acta Phytopathol Entomol Hung 34(1/2):99–122
Bradley RA (2012) Common spiders of North America. Univ of California Press, Berkeley
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. J Insect Sci 12(1):61
Cardoso P, Pekár S, Jocqué R, Coddington JA (2011) Global patterns of guild composition and functional diversity of spiders. PLoS ONE 6(6):e21710
Gotelli JE, Colwell RK (2009) Estimating species richness. In: Magurran AE, McGill BJ (eds) Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford, pp 39–54
Daane KM, Vincent C, Isaacs R, Ioriatti C (2018) Entomological opportunities and challenges for sustainable viticulture in a global market. Annu Rev Entomol 63:193–214
Dainese M, Martin EA, Aizen MA, Albrecht M, Bartomeus I, Bommarco R, Carvalheiro LG, Chaplin-Kramer R, Gagic V, Garibaldi LA, Ghazoul J, Grab H, Jonsson M, Karp DS, Kennedy CM, Kleijn D, Kremen C, Landis DA, Letourneau DK, Marini L, Poveda K, Rader R, Smith HG, Tscharnke T, Andersson GKS, Badenhausser I, Baensch S, Bezerra AD, Bianchi FJJA, Boreux V, Bretagnolle V, Caballero-Lopez B, Cavigliasso P, Cetkovic A, Chacoff NP, Classen A, Cusser S, da Silva FD, de Groot GA, Dudenhöffer JH, Ekroos J, Fijen T, Franck P, Freitas BM, Garratt MPD, Gratton C, Hipólito J, Holzschuh A, Hunt L, Iverson AL, Jha S, Keasar T, Kim TN, Kishinevsky M, Klatt BK, Klein AM, Krewenka KM, Krishnan S, Larsen AE, Lavigne C, Liere H, Mass B, Mallinger RE, Martinez Pachon E, Martinez-Salinas A, Meehan TD, Mitchell MGE, Molina GAR, Nesper M, Nilsson L, O’Rourke ME, Peters MK, Plecas M, Potts SG, Ramos DL, Rosenheim JA, Schmack J, Sciligo AR, Seymour C, Stanley DA, Stewart R, Stout JC, Sutter L, Takada MB, Taki H, Tamburini G, Tschumi M, Viana BF, Westphal C, Willcox BK, Wratten SD, Yoshioka A, Zaragoza-Trello C, Zhang W, Zou I, Steffan-Dewenter I (2019) A global synthesis reveals biodiversity-mediated benefits for crop production. Sci Adv 5(10):eaax0121
Emmerson M, Morales MB, Oñate JJ, Batary P, Berendse F, Liira J, Aavik T, Guerrero I, Bommarco R, Eggers S, Tscharntke T, Weisser WW, Clément L, Bengtsson J (2016) How agricultural intensification affects biodiversity and ecosystem services. In: Dumbrell AJ, Kordas RL (eds) Advances in ecological research, vol 55. Academic Press, Cambridge, pp 43–97
Ferreira JAM, Cunha DFS, Pallini A, Sabelis MW, Janssen A (2011) Leaf domatia reduce intraguild predation among predatory mites. Ecol Entomol 36:435–441
Fiedler AK, Landis DA, Wratten SD (2008) Maximizing ecosystem services from conservation biological control: the role of habitat management. Biol Control 45(2):254–271
Geiger F, Wäckers FL, Bianchi FJJA (2009) Hibernation of predatory arthropods in semi-natural habitats. BioControl 54:529–535
Halaj J, Cady AB, Uetz GW (2000) Modular habitat refugia enhance generalist predators and lower plant damage in soybeans. Environ Entomol 29(2):383–393
Havlova L, Hula V, Niedobova J, Michalko R (2017) Effect of adjacent steppe-like habitats on spider diversity in vine plants. BioControl 62(6):757–768
Horton DR, Miliczky ER, Broers DA, Lewis RR, Calkins CO (2001) Numbers, diversity, and phenology of spiders (Araneae) overwintering in cardboard bands placed in pear and apple orchards of central Washington. Ann Entomol Soc Am 94(3):405–414
Isaia M, Bona F, Badino G (2006a) Comparison of polyethylene bubble wrap and corrugated cardboard traps for sampling tree-inhabiting spiders. Environ Entomol 35(6):1654–1660
Isaia M, Bona F, Badino G (2006b) Influence of landscape diversity and agricultural practices on spider assemblage in Italian vineyards of Langa Astigiana (Northwest Italy). Environ Entomol 35(2):297–307
Isaia M, Beikes S, Paschetta M, Sarvajayakesavalu SN, Badino G (2010) Spiders as biological controller in apple orchards infested by Cydia spp. In XXIV European congress of arachnology. Natural History Museum, Bern, pp 79–88
James DG, Seymour L, Lauby G, Buckley K (2015) Beauty with benefits: butterfly conservation in Washington State, USA, wine grape vineyards. J Insect Conserv 19(2):341–348
Korenko S, Pekár S (2010) Is there intraguild predation between winter-active spiders (Araneae) on apple tree bark? Biol Control 54(3):206–212
Landis DA (2017) Designing agricultural landscapes for biodiversity-based ecosystem services. Basic Appl Ecol 18:1–12
Langellotto GA, Denno RF (2004) Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis. Oecologia 139:1–10
Lombardini L, Harris MK, Glenn DM (2005) Effects of particle film application on leaf gas exchange, water relations, nut yield, and insect populations in mature pecan trees. Hort Sci 40(5):1376–1380
Marc P, Canard A, Ysnel F (1999) Spiders (Araneae) useful for pest limitation and bioindication. Agric Ecosyst Environ 74:229–273
McCravy KW (2018) A review of sampling and monitoring methods for beneficial arthropods in agroecosystems. Insects 9(4):170
Mendoza G, Sánchez J, Becerra V (2014) Impacto ambiental de tres estrategias fitosanitarias para el control de Lobesia botrana. In: 37th World congress of vine and wine and 12th general assembly of the OIV (Part 2). EDP Sciences. p 05009 (In Spanish)
Michalko R, Petráková L, Senstenská L, Pekár S (2017) The effect of increased habitat complexity and density-dependent non-consumptive interference on pest suppression by winter-active spiders. Agric Ecosyst Environ 242:26–33
Michalko R, Pekár S, Dul’a M, Entling MH (2019) Global patterns in the biocontrol efficacy of spiders: a meta-analysis. Glob Ecol Biogeogr 28(9):1366–1378
Paiola A, Assandri G, Brambilla M, Zottini M, Pedrini P, Nascimbene J (2020) Exploring the potential of vineyards for biodiversity conservation and delivery of biodiversity-mediated ecosystem services: a global-scale systematic review. Sci Total Environ 706:135839
Pennington T, Kolb S, Kaiser J, Hoffmann C, Entling MH (2019) Does minimal pruning and reduced fungicide use impact spiders in the grapevine canopy? J Arachnol 47(3):381–384
Pfingstmann A, Paredes D, Buchholz J, Querner P, Bauer T, Strauss P, Kratschmer S, Winter S, Zaller J (2019) Contrasting effects of tillage and landscape structure on spiders and springtails in vineyards. Sustainability 11(7):2095
Pinzón J, Spence JR (2010) Bark-dwelling spider assemblages (Araneae) in the boreal forest: dominance, diversity, composition and life-histories. J Insect Conserv 14:439–458
Pompozzi G, Marrero HJ, Haedo J, Fritz L, Torretta JP (2019) Non-cropped fragments as important spider reservoirs in a Pampean agro-ecosystem. Ann App Biol 175(3):326–335
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.r-project.org/
Ricci B, Franck P, Toubon JF, BouvierJC SB, Lavigne C (2009) The influence of landscape on insect pest dynamics: a case study in southeastern France. Landsc Ecol 24(3):337–349
Rosas-Ramos N, Baños-Picón L, Tobajas E, de Paz V, Tormos J, Asís JD (2018) Value of ecological infrastructure diversity in the maintenance of spider assemblages: a case study of Mediterranean vineyard agroecosystems. Agric Ecosyst Environ 265:244–253
Rypstra AL, Carter PE, Balfour RA, Marshall SD (1999) Architectural features of agricultural habitats and their impact on the spider inhabitants. J Arachnol 27:371–377
Salman IN, 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(5):583–593
Salman IN, Ferrante M, Möller DM, Gavish-Regev E, Lubin Y (2020) Trunk refugia: a simple, inexpensive method for sampling tree trunk arthropods. J Insect Sci 20(2):5
Serra G, Lentini A, Verdinelli M, Delrio G (2006) Effects of cover crop management on grape pests in a Mediterranean environment. IOBC/WPRS Bull 29(11):209–214
Sunderland K (1999) Mechanisms underlying the effects of spiders on pest populations. J Arachnol 27:308–316
Thomson LJ, Hoffmann AA (2013) Spatial scale of benefits from adjacent woody vegetation on natural enemies within vineyards. Biol Control 64(1):57–65
Uetz GW, Halaj J, Cady AB (1999) Guild structure of spiders in major crops. J Arachnol 27:270–280
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
Wilson H, Miles AF, Daane KM, Altieri MA (2015) Landscape diversity and crop vigor influence biological control of the western grape leafhopper (E. elegantula Osborn) in vineyards. PLoS ONE 10(11):e0141752
Acknowledgments
We thank two anonymous reviewers and the editor for their helpful comments that greatly improved the manuscript. We would like to thank Bruno Alzugaray for his help in the field. This study was supported by grant SIIP TIPO 1 (A109) provided by Universidad Nacional de Cuyo to EA.
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GP conceived the study and wrote the first draft of the manuscript. GP, SC, FFC analyzed the data. All authors conducted field work and contributed to the improvement of the manuscript.
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Pompozzi, G., Copperi, S., Fernández Campón, F. et al. The use of artificial habitats increases spider abundance and richness in a vineyard of Argentina. BioControl 66, 217–226 (2021). https://doi.org/10.1007/s10526-020-10056-5
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DOI: https://doi.org/10.1007/s10526-020-10056-5