, Volume 64, Issue 6, pp 685–696 | Cite as

Effect of local and landscape factors on abundance of ground beetles and assessment of their role as biocontrol agents in the olive growing area of southeastern Madrid, Spain

  • Esther Lantero
  • Marta Ortega
  • Ismael Sánchez-Ramos
  • Manuel González-Núñez
  • Cristina E. Fernández
  • Alejandro  J Rescia
  • Beatriz Matallanas
  • Carmen Callejas
  • Susana PascualEmail author


Designing biological control strategies for the olive fruit fly (Bactrocera oleae (Rossi)) by predators requires the study of their biology and effectiveness. In this work, we have studied the relationship between ground beetle activity density and local (soil condition) and landscape factors in the olive area of southeastern Madrid, as well as the efficiency of the most abundant species, Orthomus barbarus (Dejean) (Coleoptera: Carabidae) by functional response experiments. Also, O. barbarus has been described for the first time by molecular methods through the barcode gene COI. The two dominant species, O. barbarus and Pterostichus globosus (Fabricius) (Coleoptera: Carabidae) showed different responses to landscape structure, but soil condition was more relevant than landscape structure for both species, and for activity density of ground beetles as a whole. P. globosus is more efficient than O. barbarus, and it is possible that in the study area other taxa are relevant as B. oleae predators.


Bactrocera oleae Barcode gene COI Landscape Orthomus barbarus Pterostichus globosus Soil condition 



This work received financial support from the Ministerio de Economía y Competitividad of Spain and the European Regional Development Fund by project RTA2013-00039-C03-03: Biological control of Bactrocera oleae: Effect of landscape structure and importance of predation. We extend our sincere thanks to Luis M. Carrascal (MNCN, CSIC, Madrid) for statistical advice and Sergio Pérez (Faculty of Biological Sciences, UCM, Madrid) for carabid determination. We also thank Pablo Blas (RECESPAÑA Cooperative, Villarejo de Salvanés, Madrid), Esther Alonso (UCAM - Union of Madrid Agricultural Cooperatives) and the owners of the sampled olive groves.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human and/or animal participants

No animals have been used.


  1. Albertini A, Pizoloto R, Petacchi R (2017) Carabid patterns in olive orchards and woody semi-natural habitats: first implications for conservation biological control against Bactrocera oleae. BioControl 62:71–83Google Scholar
  2. Avgin SS, Luff ML (2009) Biodiversity of carabid beetles (Coleoptera: Carabidae) from crops in Turkey. Proc Entomol Soc Wash 111:326–334Google Scholar
  3. Baguette M, Hance T (1997) Carabid beetles and agricultural practices: influence of soil ploughing. Biol Agric Hortic 15:185–190Google Scholar
  4. Balzan MV, Bocci G, Moonen AC (2016) Landscape complexity and field margin vegetation diversity enhance natural enemies and reduce herbivory by Lepidoptera pests on tomato crop. BioControl 61:141–154Google Scholar
  5. Benhadi-Marin J, Pereira JA, Barreales D, Sousa JP, Santos SAP (2018) A simulation-based method to compare the pest suppression potential of predators: a case study with spiders. Biol Control 123:87–96Google Scholar
  6. Boccaccio L, Petacchi R (2009) Landscape effects on the complex of Bactrocera oleae parasitoids and implications for conservation biological control. BioControl 54:607–616Google Scholar
  7. Bolker B (2008) Ecological models and data in R. Princeton University Press, Princeton, New JerseyGoogle Scholar
  8. Cárdenas AM, Hidalgo JM (1998) Data on the biological cycle of Steropus globosus (Coleoptera Carabidae) in the south west of Iberian Peninsula. Vie Et Milieu-Life Environ 48:35–39Google Scholar
  9. 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):18Google Scholar
  10. Cárdenas M, Pascual F, Campos M, Pekar S (2015) The spider assemblage of olive groves under three management systems. Environ Entomol 44:509–518PubMedGoogle Scholar
  11. Carpio AJ, Castro J, Tortosa FS (2019) Arthropod biodiversity in olive groves under two soil management systems: presence versus absence of herbaceous cover crop. Agric For Entomol 21:58–68Google Scholar
  12. Cotes B, Castro J, Cárdenas M, Campos M (2009) Responses of epigeal beetles to the removal of weed cover crops in organic olive orchards. Bull Insectol 62:47–52Google Scholar
  13. da Silva PM, Oliveira J, Ferreira A, Fonseca F, Pereira JA, Aguiar CAS, Serrano ARM, Sousa JP, Santos SAP (2017) Habitat structure and neighbor linear features influence more carabid functional diversity in olive groves than the farming system. Ecol Indic 79:128–138Google Scholar
  14. Dainese M, Martin EA, Aizen M, 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, Tscharntke T, Andersson GKS, Badenhausser I, Baensch S, Bezerra ADM, Bianchi FJJA, Boreux V, Bretagnolle V, Caballero-Lopez B, Cavigliasso P, Cetkovic A, Chacoff NP, Classen A, Cusser S, Silva e Silva FDd, de Groot GA, Dudenhoffer JH, Ekroos J, Fijen T, Franck P, Freitas BM, Garratt MPD, Gratton C, Hipolito J, Holzschuh A, Hunt L, Iverson AL, Jha S, Keasar T, Kim TN, Kishinevsky M, Klatt BK, Klein A, Krewenka KM, Krishnan S, Larsen AE, Lavigne C, Leire H, Maas B, Nesper M, Mallinger RE, Martinez E, Martinez-Salinas A, Meehan TD, Mitchell MGE, Molina GAR, Nilsson L, O’Rourke M, Peters MK, Plecas M, Potts SG, Ramos DdL, Rosenheim JA, Rundlof M, Rusch A, Saez A, Scheper J, Schleuning M, 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, Wilcox BK, Wratten SD, Yoshioka A, Zaragoza C, Zhang W, Zou Y, Steffan-Dewenter I (2019) A global synthesis reveals biodiversity-mediated benefits for crop production. Biorxiv (in press).
  15. D’Alberto CF, Hoffmann AA, Thomson LJ (2012) Limited benefits of non-crop vegetation on spiders in Australian vineyards: regional or crop differences? BioControl 57:541–552Google Scholar
  16. Dinis AM, Pereira JA, Benhadi-Marin J, Santos SAP (2016a) Feeding preferences and functional responses of Calathus granatensis and Pterostichus globosus (Coleoptera: Carabidae) on pupae of Bactrocera oleae (Diptera: Tephritidae). Bull Entomol Res 106:701–709PubMedGoogle Scholar
  17. Dinis AM, Pereira JA, Pimenta MC, Oliveira J, Benhadi-Marin J, Santos SAP (2016b) Suppression of Bactrocera oleae (Diptera: Tephritidae) pupae by soil arthropods in the olive grove. J Appl Entomol 140:677–687Google Scholar
  18. Ehler LE (1998) Conservation biological control: Past, present, and future. In: Barbosa P (ed) Conservation biological control. Academic Press, USA, pp 1–8Google Scholar
  19. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  20. Gardiner MM, Landis DA, Gratton C, DiFonzo CD, O’Neal M, Chacon JM, Wayo MT, Schmidt NP, Mueller EE, Heimpel GE (2009) Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecol Appl 19:143–154PubMedGoogle Scholar
  21. Gkisakis V, Volakakis N, Kollaros D, Barberi P, Kabourakis EM (2016) Soil arthropod community in the olive agroecosystem: determined by environment and farming practices in different management systems and agroecological zones. Agric Ecosyst Environ 218:178–189Google Scholar
  22. Gkisakis VD, Barberi P, Kabourakis EM (2018) Olive canopy arthropods under organic, integrated, and conventional management. The effect of farming practices, climate and landscape. Agroecol Sustain Food 42:843–858Google Scholar
  23. Goncalves MF, Pereira JA (2012) Abundance and diversity of soil arthropods in the olive grove ecosystem. J Insect Sci 12(1):20PubMedPubMedCentralGoogle Scholar
  24. Goncalves F, Carlos C, Aranha J, Torres L (2018) Does habitat heterogeneity affect the diversity of epigaeic arthropods in vineyards? Agric For Entomol 20:366–379Google Scholar
  25. González-Núñez M, Sánchez-Ramos I, Ortega M, Rescia AJ, Pascual S (2015) Ecosystem services for the control of Bactrocera oleae in different landscape spatial contexts. IOBC/WPRS Bull 121:143–148Google Scholar
  26. Grilli MP, Pedemonte ML, Bruno M, Fachinetti R (2015) The effect of landscape structure on two species of different trophic levels in an arid environment. Landsc Ecol. 30:1335–1349Google Scholar
  27. Happe AK, Roquer-Beni L, Bosch J, Alins G, Mody K (2018) Earwigs and woolly apple aphids in integrated and organic apple orchards: responses of a generalist predator and a pest prey to local and landscape factors. Agric Ecosyst Environ 268:44–51Google Scholar
  28. Hawro V, Ceryngier P, Tscharntke T, Thies C, Gagic V, Bengtsson J, Bommarco R, Winqvist C, Weisser WW, Clement LW, Japoshvili G, Ulrich W (2015) Landscape complexity is not a major trigger of species richness and food web structure of European cereal aphid parasitoids. BioControl 60:451–461Google Scholar
  29. Juliano SA (2001) Nonlinear curve fitting: predation and functional response curves. In: Scheiner S, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman & Hall, New York, pp 178–196Google Scholar
  30. Karp DS, Chaplin-Kramer R, Meehan TD, Martin EA, DeClerck F, Grab H, Gratton C, Hunt L, Larsen AE, Martinez-Salinas A, O’Rourke ME, Rusch A, Poveda K, Jonsson M, Rosenheim JA, Schellhorn NA, Tscharntke T, Wratten SD, Zhang W, Iverson AL, Adler LS, Albrecht M, Alignier A, Angelella GM, Anjum MZ, Avelino J, Batary P, Baveco JM, Bianchi F, Birkhofer K, Bohnenblust EW, Bommarco R, Brewer MJ, Caballero-Lopez B, Carrière Y, Carvalheiro LG, Cayuela L, Centrella M, Cetkovic A, Henri DC, Chabert A, Costamagna AC, De la Mora A, de Kraker J, Desneux N, Diehl E, Diekotter T, Dormann CF, Eckberg JO, Entling MH, Fiedler D, Franck P, van Veen FJF, Frank T, Gagic V, Garratt MPD, Getachew A, Gonthier DJ, Goodell PB, Graziosi I, Groves RL, Gurr GM, Hajian-Forooshani Z, Heimpel GE, Herrmann JD, Huseth AS, Inclan DJ, Ingrao AJ, Iv P, Jacot K, Johnson GA, Jones L, Kaiser M, Kaser JM, Keasar T, Kim TN, Kishinevsky M, Landis DA, Lavandero B, Lavigne C, Le Ralec A, Lemessa D, Letourneau DK, Liere H, Lu YH, Lubin Y, Luttermoser T, Maas B, Mace K, Madeira F, Mader V, Cortesero AM, Marini L, Martinez E, Martinson HM, Menozzi P, Mitchell MGE, Miyashita T, Molina GAR, Molina-Montenegro MA, O’Neal ME, Opatovsky I, Ortiz-Martinez S, Nash M, Ostman O, Ouin A, Pak D, Paredes D, Parsa S, Parry H, Perez-Alvarez R, Perovic DJ, Peterson JA, Petit S, Philpott SM, Plantegenest M, Plecas M, Pluess T, Pons X, Potts SG, Pywell RF, Ragsdale DW, Rand TA, Raymond L, Ricci B, Sargent C, Sarthou JP, Saulais J, Schackermann J, Schmidt NP, Schneider G, Schuepp C, Sivakoff FS, Smith HG, Whitney KS, Stutz S, Szendrei Z, Takada MB, Taki H, Tamburini G, Thomson LJ, Tricault Y, Tsafack N, Tschumi M, Valantin-Morison M, Trinh MV, van der Werf W, Vierling KT, Werling BP, Wickens JB, Wickens VJ, Woodcock BA, Wyckhuys K, Xiao HJ, Yasuda M, Yoshioka A, Zou Y (2018) Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proc Natl Acad Sci USA 115:7863–7870Google Scholar
  31. Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201PubMedPubMedCentralGoogle Scholar
  32. Lantero E, Matallanas B, Dolores Ochando M, Pascual S, Callejas C (2017) Specific and sensitive primers for the detection of predated olive fruit flies, Bactrocera oleae (Diptera: Tephritidae). Span J Agric Res 15, article e1002, 7 ppGoogle Scholar
  33. Lantero E, Pascual S, Ortega M, Rescia A, Gonzalez-Núñez M, Sánchez-Ramos I, Pérez S, Matallanas B, Callejas C (2019) Post mortem gut content analysis for determining the contribution of different soil predators to control Bactrocera oleae. IOBC/WPRS Bull 141:161–167Google Scholar
  34. Lefebvre M, Franck P, Toubon J-F, Bouvier J-C, Lavigne C (2016) The impact of landscape composition on the occurrence of a canopy dwelling spider depends on orchard management. Agric Ecosyst Environ 215:20–29Google Scholar
  35. Marko V, Elek Z, Kovacs-Hostyanszki A, Korosi A, Somay L, Foldesi R, Varga A, Ivan A, Baldi A (2017) Landscapes, orchards, pesticides-abundance of beetles (Coleoptera) in apple orchards along pesticide toxicity and landscape complexity gradients. Agric Ecosyst Environ 247:246–254Google Scholar
  36. Miñarro A, Dapena T (2003) Effects of groundcover management on ground beetles (Coleoptera: Carabidae) in an apple orchard. Appl Soil Ecol 23:111–117Google Scholar
  37. Monzo C, Molla O, Vanaclocha P, Monton H, Melic A, Castanera P, Urbaneja A (2011) Citrus-orchard ground harbours a diverse, well-established and abundant ground-dwelling spider fauna. Span J Agric Res 9:606–616Google Scholar
  38. Neuenschwander P, Bigler E, Delucchi V, Michelakis S (1983) Natural enemies of preimaginal stages of Dacus oleae Gmel. (Dipt. Tephritidae) in Western Crete. I. Bionomics and phenologies. Boll Lab Entomol Agrar Filippo Silvestri 40:3–32Google Scholar
  39. Ortega M, Pascual S (2014) Spatio-temporal analysis of the relationship between landscape structure and the olive fruit fly Bactrocera oleae (Diptera: Tephritidae). Agric For Entomol 16:14–23Google Scholar
  40. Ortega M, Sanchez-Ramos I, Gonzalez-Nunez M, Pascual S (2018) Time course study of Bactrocera oleae (Diptera: Tephritidae) pupae predation in soil: the effect of landscape structure and soil condition. Agric For Entomol 20:201–207Google Scholar
  41. Paredes D, Cayuela L, Campos M (2013) Synergistic effects of ground cover and adjacent vegetation on natural enemies of olive insect pests. Agric Ecosyst Environ 173:72–80Google Scholar
  42. Paredes D, Cayuela L, Gurr GM, Campos M (2015) Is ground cover vegetation an effective biological control enhancement strategy against olive pests? PLoS ONE 10(2):e0117265PubMedPubMedCentralGoogle Scholar
  43. Picchi MS, Bocci G, Petacchi R, Ending MH (2016) Effects of local and landscape factors on spiders and olive fruit flies. Agric Ecosyst Environ 222:138–147Google Scholar
  44. Picchi MS, Marchi S, Albertini A, Petacchi R (2017) Organic management of olive orchards increases the predation rate of overwintering pupae of Bactrocera oleae (Diptera: Tephritidae). Biol Control 108:9–15Google Scholar
  45. Pizzolotto R, Mazzei A, Bonacci T, Scalercio S, Iannotta N, Brandmayr P (2018) Ground beetles in Mediterranean olive agroecosystems: their significance and functional role as bioindicators (Coleoptera, Carabidae). PLoS ONE 13(3):e0194551PubMedPubMedCentralGoogle Scholar
  46. Rejili M, Fernandes T, Dinis AM, Pereira JA, Baptista P, Santos SAP, Lino-Neto T (2016) A PCR-based diagnostic assay for detecting DNA of the olive fruit fly, Bactrocera oleae, in the gut of soil-living arthropods. Bull Entomol Res 106:695–699PubMedGoogle Scholar
  47. Rivers A, Barbercheck M, Govaerts B, Verhulst N (2016) Conservation agriculture affects arthropod community composition in a rainfed maize-wheat system in central Mexico. Appl Soil Ecol 100:81–90Google Scholar
  48. Rodríguez E, Gonzalez B, Campos M (2012) Natural enemies associated with cereal cover crops in olive groves. Bull Insectol 65:43–49Google Scholar
  49. Rogers D (1972) Random search and insect population models. J Anim Ecol 41:369–383Google Scholar
  50. Rusch A, Binet D, Delbac L, Thiery D (2016) Local and landscape effects of agricultural intensification on carabid community structure and weed seed predation in a perennial cropping system. Landsc Ecol 31:2163–2174Google Scholar
  51. Sadej W, Kosewska A, Sadej W, Nietupski M (2012) Effects of fertilizer and land-use type on soil properties and ground beetle communities. Bull Insectol 65:239–246Google Scholar
  52. Scalercio S, Brandmayr P, Iannotta N, Petacchi R, Boccaccio L (2012) Correlations between landscape attributes and ecological traits of Lepidoptera communities in olive groves. Eur J Entomol 109:207–216Google Scholar
  53. Shackelford G, Steward PR, Benton TG, Kunin WE, Potts SG, Biesmeijer JC, Sait SM (2013) Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops. Biol Rev 88:1002–1021PubMedGoogle Scholar
  54. Tamburini G, De Simone S, Sigura M, Boscutti F, Marini L (2016) Conservation tillage mitigates the negative effect of landscape simplification on biological control. J Appl Ecol 53:233–241Google Scholar
  55. Thiele HU (1977) Carabid beetles in their environments. A study on habitat selection by adaptation in physiology and behaviour. Springer, BerlinGoogle Scholar
  56. Trexler JC, McCulloch CE, Travis J (1988) How can the functional response best be determined. Oecologia 76:206–214PubMedGoogle Scholar
  57. Tscheulin T, Neokosmidis L, Petanidou T, Settele J (2011) Influence of landscape context on the abundance and diversity of bees in Mediterranean olive groves. Bull Entomol Res 101:557–564PubMedGoogle Scholar
  58. Winqvist C, Weisser WW, Clement LW, Japoshvili G, Ulrich W (2015) Landscape complexity is not a major trigger of species richness and food web structure of European cereal aphid parasitoids. BioControl 60:451–461Google Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2019

Authors and Affiliations

  • Esther Lantero
    • 1
  • Marta Ortega
    • 2
  • Ismael Sánchez-Ramos
    • 3
  • Manuel González-Núñez
    • 3
  • Cristina E. Fernández
    • 3
  • Alejandro  J Rescia
    • 2
  • Beatriz Matallanas
    • 1
  • Carmen Callejas
    • 1
  • Susana Pascual
    • 3
    Email author
  1. 1.Department of Genetics, Physiology and Microbiology, Faculty of Biological SciencesUniversidad Complutense de MadridMadridSpain
  2. 2.Department of Biodiversity, Ecology and EvolutionUniversidad Complutense de MadridMadridSpain
  3. 3.Entomology Group, Plant Protection DepartmentInstituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA)MadridSpain

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