Skip to main content
Log in

Carabid patterns in olive orchards and woody semi-natural habitats: first implications for conservation biological control against Bactrocera oleae

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The role of carabids (Coleoptera: Carabidae) for pest control service in perennial crop systems has been scarcely investigated. We addressed this knowledge gap exploring activity patterns and traits of adult carabids dwelling olive orchard agroecosystems as potential natural enemies of third instar larvae and pupae of Bactrocera oleae (Diptera: Tephritidae). Olive orchard supported a well-structured carabid assemblage, whose species phenologies revealed a temporal overlapping within the pest cycle. The assemblage of adjacent woody semi-natural habitats is more of conservation interest, but may play a weaker role in B. oleae control provisioning. We suggest the identification of carabids main traits for B. oleae conservation biological control as a cost-effective strategy for addressing future attention and resources only to those predators that satisfy basic requirements. This research may open new scenarios on management interventions to both conserve predators and encourage alternative approaches against olive orchards pest.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen RT (1979) The occurrence and importance of ground beetles in agricultural and surrounding habitats. In: Erwin TL, Ball GE, Whitehead DR, Halpern AL (eds) Carabid beetles. Springer, Dordrecht, pp 485–505

    Chapter  Google Scholar 

  • Altieri MAA, Nicholls CI (2004) Biodiversity and pest management in agroecosystems, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  • Amvrazi EG, Albanis TA (2009) Pesticide residue assessment in different types of olive oil and preliminary exposure assessment of Greek consumers to the pesticide residues detected. Food Chem 113:253–261

    Article  CAS  Google Scholar 

  • Andersen A (1997) Densities of overwintering carabids and staphylinids (Col., Carabidae and Staphylinidae) in cereal and grass fields and their boundaries. J Appl Entomol 121:77–80

    Article  Google Scholar 

  • Bàrberi P, Burgio G, Dinelli G, Moonen AC, Otto S, Vazzana C, Zanin G (2010) Functional biodiversity in the agricultural landscape: relationships between weeds and arthropod fauna. Weed Res 50:388–401

    Article  Google Scholar 

  • Barbosa P (2003) Conservation Biological Control. Academic Presss, San Diego

    Google Scholar 

  • Bertacchi A, Sani A, Tomei PE (2004) La vegetazione del Monte Pisano. Felici Editore, Pisa

    Google Scholar 

  • Blake S, Foster GN, Eyre MD, Luff ML (1994) Effects of habitat type and grassland management practices on the body size distribution of carabid beetles. Pedobiologia 38:502–512

    Google Scholar 

  • Boccaccio L, Petacchi R (2009) Landscape effects on the complex of Bactrocera oleae parasitoids and implications for conservation biological control. BioControl 54:607–616

    Article  Google Scholar 

  • Brandmayr P (1983) The main axes of the coenoclinal continuum from macroptery to brachyptery in carabid communities of the temperate zone. In: Brandmayr P, den Boer PJ, Weber F (eds) The synthesis of field study and laboratory experiment in carabids. Report of the IV European Carabidologists Meeting, pp 147–169

  • Brandmayr P, Zetto T, Pizzolotto R (2005) I coleotteri carabidi per la valutazione ambientale e la conservazione della biodiversità: manuale operativo. Apat, Manuali e Linee Guida 34/2005, Roma

  • Bryan KM, Wratten SD (1984) The responses of polyphagous predators to prey spatial heterogeneity: aggregation by carabid and staphylinid beetles to their cereal aphid prey. Ecol Entomol 9:251–259

    Article  Google Scholar 

  • Burgio G, Sommaggio D, Marini M, Puppi G, Chiarucci A, Landi S, Fabbri R, Pesarini F, Genghini M, Ferrari R, Muzzi E (2015) The influence of vegetation and landscape structural connectivity on butterflies (Lepidoptera: Papilionoidea and Hesperiidae), Carabids (Coleoptera: Carabidae), Syrphids (Diptera: Syrphidae), and Sawflies (Hymenoptera: Symphyta) in Northern Italy farmland. Environ Entomol 44:1299–1307

    Article  PubMed  Google Scholar 

  • Cavalloro R, Delrio G (1975) Osservazioni sulla distribuzione e sopravvivenza delle pupe di Dacus oleae Gmelin nel terreno. Redia 56:167–175

    Google Scholar 

  • Clark MS, Gage SH, Spence JR (1997) Habitats and management associated with common ground beetles (Coleoptera: Carabidae) in a Michigan agricultural landscape. Environ Entomol 26:519–527

    Article  Google Scholar 

  • Coombes DS, Sotherton NW (1986) The dispersal and distribution of polyphagous predatory Coleoptera in cereals. Ann Appl Biol 108:461–474

    Article  Google Scholar 

  • Daane KM, Johnson MW (2010) Olive fruit fly: managing an ancient pest in modern times. Annu Rev Entomol 55:151–169

    Article  CAS  PubMed  Google Scholar 

  • Den Boer PJ, den Boer-Daanje W (1990) On life history tactics in carabid beetles: are there only spring-and autumn-breeders? In: Stork NE (ed) The role of ground beetles in ecological and environmental studies. Intercept, Andover, pp 247–258

    Google Scholar 

  • Dennis P, Fry GLA (1992) Field margins: can they enhance natural enemy population densities and general arthropod diversity on farmland? Agric Ecosyst Environ 40:95–115

    Article  Google Scholar 

  • Dimou I, Koutsikopoulos C, Economopoulos AP, Lykakis J (2003) Depth of pupation of the wild olive fruit fly, Bactrocera (Dacus) oleae (Gmel.) (Dipt., Tephritidae), as affected by soil abiotic factors. J Appl Entomol 127:12–17

    Article  Google Scholar 

  • Dinis AM, Pereira JA, Pimenta MC, Oliveira J, Benhadi-Marín J, Santos SAP (2016) Suppression of Bactrocera oleae (Diptera: Tephritidae) pupae by soil arthropods in the olive grove. J Appl Entomol 140:677–687

    Article  Google Scholar 

  • Duelli P, Obrist MK (2003) Regional biodiversity in an agricultural landscape: the contribution of seminatural habitat islands. Basic Appl Ecol 4:129–138

    Article  Google Scholar 

  • Duflot R, Aviron S, Ernoult A, Fahrig L, Burel F (2015) Reconsidering the role of “semi-natural habitat” in agricultural landscape biodiversity: a case study. Ecol Res 30:75–83

    Article  Google Scholar 

  • Geiger F, Wäckers FL, Bianchi FJJA (2009) Hibernation of predatory arthropods in semi-natural habitats. Biol Control 54:529–535

    Google Scholar 

  • Gkisakis VD, Kollaros D, Bàrberi P, Livieratos IC, Kabourakis EM (2015) Soil arthropod diversity in organic, integrated, and conventional olive orchards and different agroecological zones in Crete, Greece. Agroecol Sustain Food Syst 39:276–294

    Article  Google Scholar 

  • Gonçalves MF, Pereira JA (2012) Abundance and diversity of soil arthropods in the olive grove ecosystem. J Insect Sci 12:1–14

    Article  Google Scholar 

  • Gotelli NJ, Colwell RK (2010) Estimating species richness. In: Magurran AE, McGill BJ (eds) Biological diversity. Oxford University Press, Oxford, pp 39–54

    Google Scholar 

  • Greenslade PJM (1964) Pitfall trapping as a method for studying populations of Carabidae (Coleoptera). J Anim Ecol 33:301–310

    Article  Google Scholar 

  • Hance T, Gregoire-Wibo C, Lebrun P (1990) Agriculture and ground-beetles populations: the consequence of crop types and surrounding habitats on activity and species composition. Pedobiologia 34:337–346

    Google Scholar 

  • Hendrickx F, Maelfait JP, van Wingerden W, Schweiger O, Speelmans M, Aviron S, Augenstein I, Billeter R, Bailey D, Bukacek R, Burel F (2007) How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J Appl Ecol 44:340–351

    Article  Google Scholar 

  • Holland JM (2002) The agroecology of carabid beetles. Intercept, Andover

    Google Scholar 

  • Holland JM, Luff ML (2000) The effects of agricultural practices on Carabidae in temperate agroecosystems. Integr Pest Manag Rev 5:109–129

    Article  Google Scholar 

  • Holland J, Bianchi FJJA, Entling MH, Moonen AC, Smith BM, Jeanneret P (2016) Structure, function and management of semi-natural habitats for conservation biological control: a review of European studies. Pest Manag Sci 72:1638–1651

    Article  CAS  PubMed  Google Scholar 

  • Homburg K, Homburg N, Schäfer F, Schuldt A, Assmann T (2014) Carabids.org: a dynamic online database of ground beetle species traits (Coleoptera, Carabidae). Insect Conserv Divers 7:195–205

    Article  Google Scholar 

  • Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586

    Article  Google Scholar 

  • Keddy PA (1992) A pragmatic approach to functional ecology. Funct Ecol 6:621–626

    Article  Google Scholar 

  • Kotze DJ, O’Hara RB (2003) Species decline: but why? Explanations of carabid beetle (Coleoptera, Carabidae) declines in Europe. Oecologia 135:138–148

    Article  PubMed  Google Scholar 

  • Kotze DJ, Brandmayr P, Casale A, Dauffy-Richard E, Dekoninck W, Koivula MJ, Lövei GL, 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 (2011) Forty years of carabid beetle research in Europe-from taxonomy, biology, ecology and population studies to bioindication, habitat assessment and conservation. ZooKeys 100:55–148

    Article  Google Scholar 

  • Kromp B (1999) Carabid beetles in sustainable agriculture: a review on pest control efficacy, cultivation impacts and enhancement. Agric Ecosyst Environ 74:187–228

    Article  Google Scholar 

  • Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201

    Article  CAS  PubMed  Google Scholar 

  • Larochelle A (1990) The food of the Carabid beetles (Coleoptera: Carabidae, including Cicindelinae). Fabreries Suppl 5:1–132

    Google Scholar 

  • Lasinio PJ, Zapparoli M (1993) First data on the soil arthropod community in an olive grove in central Italy. In: Coleman DC, Foissner W, Paoletti MG (eds) Soil biota, nutrient cycling, and farming systems. CRC Press, Boca Raton, pp 113–121

    Google Scholar 

  • Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  Google Scholar 

  • Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge

    Google Scholar 

  • Lövei GL, Sunderland KD (1996) Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annu Rev Entomol 41:231–256

    Article  PubMed  Google Scholar 

  • Luff ML (1987) Biology of polyphagous ground beetles in agriculture. Agric Zool Rev 2:237–278

    Google Scholar 

  • Luff ML (2002) Carabid assemblage organization and species composition. In: Holland JM (ed) The agroecology of carabid beetles. Intercept, Andover, pp 41–79

    Google Scholar 

  • Malavolta C, Perdikis D (2012) Guidelines for integrated production of olive. IOBC/WPRS Bulletin 77:1–19

    Google Scholar 

  • Malheiro R, Casal S, Baptista P, Pereira JA (2015) A review of Bactrocera oleae (Rossi) impact in olive products: from the tree to the table. Trends Food Sci Technol 44:226–242

    Article  CAS  Google Scholar 

  • Marchi S, Guidotti D, Ricciolini M, Petacchi R (2016) Towards understanding temporal and spatial dynamics of Bactrocera oleae (Rossi) infestations using decade-long agrometeorological time series. Int J Biometeorol 60:1681–1694

    Article  PubMed  Google Scholar 

  • Marshall EJP, Moonen AC (2002) Field margins in northern Europe: integrating agricultural, environmental and biodiversity functions. Agric Ecosyst Environ 89:5–21

    Article  Google Scholar 

  • McGarigal K, Cushman S, Stafford S (2000) Multivariate statistics for wildlife and ecology research. Springer, Berlin

    Book  Google Scholar 

  • Neuenschwander P, Bigler F, Delucchi V, Michelakis S (1983) Natural enemies of preimmaginal stages of Dacus oleae Gmel. (Dipt. Tethritidae) in Western Crete. I. Bionomics and phenologies. Boll Lab Ent Agr Filippo Silvestri 40:3–32

    Google Scholar 

  • Niccolai M, Marchi S (2005) Il clima della Toscana. RaFT 2005: Rapporto sullo stato delle foreste in Toscana. Sherwood 124(2):16–21

    Google Scholar 

  • Orsini MM, Daane KM, Sime KR, Nelson EH (2007) Mortality of olive fruit fly pupae in California. BioControl Sci Technol 17:797–807

    Article  Google Scholar 

  • Pearson DL (1994) Selecting indicator taxa for the quantitative assessment of biodiversity. Philos Trans R Soc Lond B Biol Sci 345:75–79

    Article  CAS  PubMed  Google Scholar 

  • Pizzolotto R (2009) Characterization of different habitats on the basis of the species traits and eco-field approach. Acta Oecol 35:142–148

    Article  Google Scholar 

  • Pizzolotto R, Mazzei A, Belfiore T, Bonacci T, Odoguardi R, Scalercio S, Iannotta N, Brandmayr P (2009) Biodiversità dei Coleotteri Carabidi (Coleoptera: Carabidae) nell’agroecosistema oliveto in Calabria. Entomologica 41:5–11

    Google Scholar 

  • Pollard E (1968) Hedges. IV. A comparison between the Carabidae of a hedge and field site and those of a Woodland Glade. J Appl Ecol 12:649–657

    Article  Google Scholar 

  • Ponti L, Gutierrez AP, Ruti PM, Dell’Aquila A (2014) Fine-scale ecological and economic assessment of climate change on olive in the Mediterranean Basin reveals winners and losers. Proc Natl Acad Sci 111:5598–5603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porta A (1923) Fauna coleopterorum italica. Vol I Adephaga. Stabilimento Tipografico Piacentino, Piacenza

    Google Scholar 

  • Porta A (1934) Supplementum I. Stabilimento Tipografico Piacentino, Piacenza

    Google Scholar 

  • Reg. (UE) 1305/2013 URL https://www.politicheagricole.it/flex/cm/pages/ServeBLOB.php/L/IT/IDPagina/5091

  • Rejili M, Fernandes T, Dinis AM, Pereira JA, Baptista P, Santos SA, 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 106:1–5

    Article  Google Scholar 

  • Ribera I, Doledec S, Downie IS, Foster GN (2001) Effect of land disturbance and stress on species traits of ground beetle assemblages. Ecology 82:1112–1129

    Article  Google Scholar 

  • Ruano F, Lozano C, Tinaut A, Peña A, Pascual F, García P, Campos M (2001) Impact of pesticides on beneficial arthropod fauna of olive groves. IOBC/WPRS Bulletin 24:113–120

    Google Scholar 

  • Spence JR, Niemelä JK (1994) Sampling carabid assemblages with pitfall traps: the madness and the method. Can Entomol 126:881–894

    Article  Google Scholar 

  • Sunderland KD (2002) Invertebrate pest control by carabids. In: Holland JM (ed) The agroecology of carabid beetles. Intercept, Andover, pp 165–214

    Google Scholar 

  • R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Thiele HU (1977) Carabid beetles in their environments. A study on habitat selection by adaptation in physiology and behaviour. Springer, Berlin

    Book  Google Scholar 

  • Thomas CFG, Parkinson L, Griffiths GJK, Garcia AF, Marshall EJP (2001) Aggregation and temporal stability of carabid beetle distributions in field and hedgerow habitats. J Appl Ecol 38:100–116

    Article  Google Scholar 

  • Toft S, Bilde T (2002) Carabid diets and food value. In: Holland JM (ed) The agroecology of carabid beetles. Intercept, Andover, pp 81–110

    Google Scholar 

  • Trautner J, Geigenmüller K (1987) Tiger beetles, ground beetles. Illustrated key to the Cicindelidae and Carabidae of Europe. Margraf Publishing, Aichtal

    Google Scholar 

  • van den Bosch R, Stern VM (1962) The integration of chemical and biological control of arthropod pests. Annu Rev Entomol 7:367–386

    Article  Google Scholar 

  • Wheater CP (1988) Predator-prey size relationships in some Pterostichini (Coleoptera: Carabidae). Coleopt Bull 42:237–240

    Google Scholar 

  • Winqvist C, Bengtsson J, Öckinger E, Aavik T, Berendse F, Clement LW, Fischer C, Flohre A, Geiger F, Liira J, Thies C, Tscharntke T, Weisser WW, Bommarco R (2014) Species’ traits influence ground beetle responses to farm and landscape level agricultural intensification in Europe. J Insect Conserv 18:837–846

    Article  Google Scholar 

Download references

Acknowledgements

We express our gratitude to Prof. Pietro Brandmayr and Dr. Susanna Marchi for their valuable suggestions, to Dr. Diego Guidotti for statistical assistance and Dr. Gionata Bocci for botanical identification and statistical assistance. We thank Valentina Cantini, Antonio Coccina, Cristina Ghelardi, Gaia Monteforti, Malayka Picchi, Nathaly Castro Rodas for their field and laboratory assistances. We express particular acknowledgment and appreciation to landowners for allowing the access to their olive orchards and answering the questionnaires. We thank the anonymous reviewers and the editor for their comments to improve our manuscript. The research was inspired by the QuESSA project which received funding from the European Union’s Seventh Framework Programme for research, technological development and demonstration under grant agreement No. 311879. This work has been realized with the financial support of Scuola Superiore Sant’Anna, PhD Programme in Agrobiodiversity.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alice Albertini.

Additional information

Handling Editor: Dirk Babendreier

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 40 kb)

Supplementary material 2 (DOC 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Albertini, A., Pizzolotto, R. & Petacchi, R. Carabid patterns in olive orchards and woody semi-natural habitats: first implications for conservation biological control against Bactrocera oleae . BioControl 62, 71–83 (2017). https://doi.org/10.1007/s10526-016-9780-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-016-9780-x

Keywords

Navigation