Agroforestry Systems

, Volume 93, Issue 6, pp 2067–2083 | Cite as

Agroforestry impacts the seasonal and diurnal activity of dominant predatory arthropods in organic vegetable crops

  • Ambroise Martin-ChaveEmail author
  • Camille Béral
  • Christophe Mazzia
  • Yvan Capowiez


Agroforestry can improve predator recruitment by increasing the diversity of microhabitats and modifying the microclimate. Four treatment plots were defined with three tree-shading levels in a 20 years old agroforestry system combining organic vegetable crops with hybrid walnut trees. Temperature and canopy openness were recorded in each treatment in July and September 2015 and arthropods were sampled using pitfall traps at two dates (2 weeks in July and 2 weeks in September). The daily activity pattern of the main taxa was then estimated using dry pitfall traps for 7 days in July and 8 days in September. Agroforestry significantly limited the daily temperature extremes in the day and night (± 1.5 °C). We observed a significant effect of treatment on species distribution. In July, the main xerophilic species, Pseudoophonus rufipes (Coleoptera, Carabidae), was less abundant in the two most shaded plots (− 25%). Pardosa hortensis (Arachnida, Lycosidae) showed significant differences in activity-density and diurnal activity between treatments. This spider was more active between 10:00 and 14:00 in the two most shaded treatments especially in tomatoes (more than 20% of the daily activity) compared to the control (13%). The activity-density of this species was also higher in the two shaded treatments than in the control (> 20%). Our results highlight that agroforestry, by buffering climate extremes, is likely to modify predatory arthropod activity and possibly the associated services such as biocontrol.


Arachnids Biodiversity Ground beetles Microclimate Sylvo-arable system 



We thank the foundations Fondation de France, Fondation Humus, Terra Symbiosis and Fondation Picard who financially supported the ARBRATATOUILLE project. We wish to express considerable thanks to Virginie and Denis Florès who actively participated in the project and gave us permission to work on their farm.


  1. Allegro G, Sciaky R (2003) Assessing the potential role of ground beetles (Coleoptera, Carabidae) as bioindicators in poplar stands, with a newly proposed ecological index (FAI). For Ecol Manag 175:275–284CrossRefGoogle Scholar
  2. Atienza JC, Farinos GP, Zaballos JP (1996) Role of temperature in habitat selection and activity patterns in the ground beetle Angoleus nitidus. Pedobiologia 40:240–250Google Scholar
  3. Batish D, Kohli R, Jose S, Singh H (eds) (2007) Ecological basis of agroforestry. CRC Press, Boca RatonGoogle Scholar
  4. Berthe SCF, Derocles SAP, Lunt DH, Kimball BA, Evans DM (2015) Simulated climate-warming increases Coleoptera activity-densities and reduces community diversity in a cereal crop. Agric Ecosyst Environ 210:11–14. CrossRefGoogle Scholar
  5. Bianchi FJJ, Booij CJ, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc R Soc B Biol Sci 273:1715–1727. CrossRefGoogle Scholar
  6. Buchholz S, Rolfsmeyer D, Schirmel J (2013) Simulating small-scale climate change effects-lessons from a short-term field manipulation experiment on grassland arthropods: simulating small-scale climate change effects. Insect Sci 20:662–670. CrossRefPubMedGoogle Scholar
  7. Chen J, Saunders SC, Crow TR, Naiman RJ, Brosofske KD, Mroz GD, Brookshire BL, Franklin JF (1999) Microclimate in forest ecosystem and landscape ecology variations in local climate can be used to monitor and compare the effects of different management regimes. Bioscience 49:288–297CrossRefGoogle Scholar
  8. Collins KL, Boatman ND, Wilcox A, Holland JM, Chaney K (2002) Influence of beetle banks on cereal aphid predation in winter wheat. Agric Ecosyst Environ 93:337–350CrossRefGoogle Scholar
  9. Coulon J, Pupier R, Quénnec E, Ollivier E, Richoux P (2011) Faune de France n°94 Coléoptères carabiques: complément et mise à jour volume 1. Fédération Française des Sociétés de Sciences Naturelles, 352 pGoogle Scholar
  10. Coulon J, Pupier R, Quénnec E, Ollivier E, Richoux P (2012) Faune de France n°95 Coléoptères carabiques: complément et mise à jour. Fédération Française des Sociétés de Sciences Naturelles, 337 pGoogle Scholar
  11. De Frenne P, Rodriguez-Sanchez F, Coomes DA, Baeten L, Verstraeten G, Vellend M, Bernhardt-Romermann M, Brown CD, Brunet J, Cornelis J, Decocq GM, Dierschke H, Eriksson O, Gilliam FS, Hedl R, Heinken T, Hermy M, Hommel P, Jenkins MA, Kelly DL, Kirby KJ, Mitchell FJG, Naaf T, Newman M, Peterken G, Petrik P, Schultz J, Sonnier G, Van Calster H, Waller DM, Walther G-R, White PS, Woods KD, Wulf M, Graae BJ, Verheyen K (2013) Microclimate moderates plant responses to macroclimate warming. Proc Natl Acad Sci 110:18561–18565. CrossRefPubMedGoogle Scholar
  12. Diffenbaugh NS, Pal JS, Giorgi F, Gao X (2007) Heat stress intensification in the Mediterranean climate change hotspot. Geophys Res Lett. CrossRefGoogle Scholar
  13. Dondale CD, Redner JH, Semple RB (1972) Diel activity periodicities in meadow arthropods. Can J Zool 50:1155–1163. CrossRefGoogle Scholar
  14. Edgar WD (1969) Prey and feeding behaviour of adult females of the wolf spider Pardosa amentata (Clerck). Neth J Zool 20:487–491CrossRefGoogle Scholar
  15. Eichhorn MP, Paris P, Herzog F, Incoll LD, Liagre F, Mantzanas K, Mayus M, Moreno G, Papanastasis VP, Pilbeam DJ, Pisanelli A, Dupraz C (2006) Silvoarable Systems in Europe—Past, Present and Future Prospects. Agrofor Syst 67:29–50. CrossRefGoogle Scholar
  16. Frampton GK, Van den Brink PJ, Wratten SD (2001) Diel activity patterns in an arable collembolan community. Appl Soil Ecol 17:63–80. CrossRefGoogle Scholar
  17. Fuhrer J, Gregory PJ, International CAB (eds) (2014) Climate change impact and adaptation in agricultural systems. CABI climate change series. CABI, BostonGoogle Scholar
  18. Ghahari H, Avgin SS, Ostovan H (2010) Carabid beetles (Coleoptera: Carabidae) collected from different ecosystems in Iran with new records. Turk. J, Entomol, p 34Google Scholar
  19. Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Glob Planet Change 63:90–104. CrossRefGoogle Scholar
  20. Greenwood O, Mossman HL, Suggitt AJ, Curtis RJ, Maclean IMD (2016) Using in situ management to conserve biodiversity under climate change. J Appl Ecol 53:885–894. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Griffiths GJK, Holland JM, Bailey A, Thomas MB (2008) Efficacy and economics of shelter habitats for conservation biological control. Biol Control 45:200–209. CrossRefGoogle Scholar
  22. Guenat S, Kaartinen R, Jonsson M (2017) Shade trees decrease pest abundances on brassica crops in Kenya. Syst, Agrofor. CrossRefGoogle Scholar
  23. Guo K, Hao S-G, Sun OJ, Kang L (2009) Differential responses to warming and increased precipitation among three contrasting grasshopper species. Glob Change Biol 15:2539–2548. CrossRefGoogle Scholar
  24. Honek A (2013) The effect of temperature on the activity of Carabidae (Coleoptera) in a fallow field. EJE 94:97–104Google Scholar
  25. Jeannel R (1941) Faune de France n°39, Coléoptères carabiques. Fédération Française des Sociétés de Sciences Naturelles, 575 pGoogle Scholar
  26. Jeannel R (1942) Faune de France n°40, Coléoptères carabiques. Fédération Française des Sociétés de Sciences Naturelles, 606 pGoogle Scholar
  27. Jones M, Sinclair FL, Grime VL (1998) Effect of tree species and crown pruning on root length and soil water content in semi-arid agroforestry. Plant Soil 201:197–207CrossRefGoogle Scholar
  28. Joyce KA, Holland J, Doncaster C (1999) Influences of hedgerow intersections and gaps on the movement of carabid beetles. Bull Entomol Res. CrossRefGoogle Scholar
  29. Karungi J, Nambi N, Ijala AR, Jonsson M, Kyamanywa S, Ekbom B (2015) Relating shading levels and distance from natural vegetation with hemipteran pests and predators occurrence on coffee. J Appl Entomol 139:669–678. CrossRefGoogle Scholar
  30. Kranz AJ, Wolz KJ, Miller JR (2018) Effects of shrub crop interplanting on apple pest ecology in a temperate agroforestry system. Syst, Agrofor. CrossRefGoogle Scholar
  31. Kromp B (1999) Carabid beetles in sustainable agriculture: a review on pest control efficacy, cultivation impacts and enhancement. Agric Ecosyst Environ 74:187–228CrossRefGoogle Scholar
  32. Krumpalova Z, Tuf IH (2013) Circadian rhythms of ground living spiders: mechanisms of coexistence strategy based on the body size. Pol J Ecol 61:575–586Google Scholar
  33. Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-33.
  34. Lasco RD, Delfino RJP, Espaldon MLO (2014) Agroforestry systems: helping smallholders adapt to climate risks while mitigating climate change. Wiley Interdiscip Rev Clim Change 5:825–833. CrossRefGoogle Scholar
  35. Leather SR (ed) (2005) Insect sampling in forest ecosystems. Methods in ecology. Blackwell Pub, MaldenGoogle Scholar
  36. Lin BB (2007) Agroforestry management as an adaptive strategy against potential microclimate extremes in coffee agriculture. Agric For Meteorol 144:85–94. CrossRefGoogle Scholar
  37. Lindberg N, Engtsson JB, Persson T (2002) Effects of experimental irrigation and drought on the composition and diversity of soil fauna in a coniferous stand. J Appl Ecol 39:924–936CrossRefGoogle Scholar
  38. Malézieux E, Crozat Y, Dupraz C, Laurans M, Makowski D, Ozier-Lafontaine H, Rapidel B, Tourdonnet S, Valantin-Morison M (2009) Mixing plant species in cropping systems: concepts, tools and models. A review. Agron Sustain Dev 29:43–62. CrossRefGoogle Scholar
  39. Mariño YA, Pérez M-E, Gallardo F, Trifilio M, Cruz M, Bayman P (2016) Sun vs. shade affects infestation, total population and sex ratio of the coffee berry borer (Hypothenemus hampei) in Puerto Rico. Agric Ecosyst Environ 222:258–266. CrossRefGoogle Scholar
  40. Miñarro M, Dapena E (2003) Effects of groundcover management on ground beetles (Coleoptera: Carabidae) in an apple orchard. Appl Soil Ecol 23:111–117. CrossRefGoogle Scholar
  41. Moreno G, Aviron S, Berg S, Crous-Duran J, Franca A, de Jalón SG, Hartel T, Mirck J, Pantera A, Palma JHN, Paulo JA, Re GA, Sanna F, Thenail C, Varga A, Viaud V, Burgess PJ (2017) Agroforestry systems of high nature and cultural value in Europe: provision of commercial goods and other ecosystem services. Syst, Agrofor. CrossRefGoogle Scholar
  42. Musolin DL (2007) Insects in a warmer world: ecological, physiological and life-history responses of true bugs (Heteroptera) to climate change. Glob Change Biol 13:1565–1585. CrossRefGoogle Scholar
  43. Nentwig W, Blick T, Gloor D, Hänggi A, Kropf C (2015) Spiders of Europe. Version 10.2015. Accessed Oct 2015
  44. Oger P (2015) Les araignées de Belgique et de France. Accessed Oct 2015
  45. Park O (1941) Concerning Community Symmetry. Ecology 22:164. CrossRefGoogle Scholar
  46. Petit S, Boursault A, Bohan DA (2014) Weed seed choice by carabid beetles (Coleoptera: Carabidae): Linking field measurements with laboratory diet assessments. Eur J Entomol 111:615CrossRefGoogle Scholar
  47. Pezzopane JRM, de Souza PS, Rolim GDS, Gallo PB (2011) Microclimate in coffee plantation grown under grevillea trees shading. Acta Sci Agron. CrossRefGoogle Scholar
  48. Pfannenstiel RS, Yeargan KV (2002) Identification and diel activity patterns of predators attacking Helicoverpa zea (Lepidoptera: Noctuidae) eggs in soybean and sweet corn. Environ Entomol 31:232–241. CrossRefGoogle Scholar
  49. Poeydebat C, Tixier P, De Lapeyre De Bellaire L, Carval D (2017) Plant richness enhances banana weevil regulation in a tropical agroecosystem by affecting a multitrophic food web. Biol Control 114:125–132. CrossRefGoogle Scholar
  50. Pumariño L, Sileshi GW, Gripenberg S, Kaartinen R, Barrios E, Muchane MN, Midega C, Jonsson M (2015) Effects of agroforestry on pest, disease and weed control: a meta-analysis. Basic Appl Ecol 16:573–582. CrossRefGoogle Scholar
  51. Quinkenstein A, Wöllecke J, Böhm C, Grünewald H, Freese D, Schneider BU, Hüttl RF (2009) Ecological benefits of the alley cropping agroforestry system in sensitive regions of Europe. Environ Sci Policy 12:1112–1121. CrossRefGoogle Scholar
  52. Rainio J, Niemelä J (2003) Ground beetles (Coleoptera: Carabidae) as bioindicators. Biodivers Conserv 12:487–506CrossRefGoogle Scholar
  53. Ranjha MH, Irmler U (2014) Movement of carabids from grassy strips to crop land in organic agriculture. J Insect Conserv 18:457–467. CrossRefGoogle Scholar
  54. Saska P, Vodde M, Heijerman T, Westerman P, van der Werf W (2007) The significance of a grassy field boundary for the spatial distribution of carabids within two cereal fields. Agric Ecosyst Environ 122:427–434. CrossRefGoogle Scholar
  55. Saska P, van der Werf W, Hemerik L, Luff ML, Hatten TD, Honek A (2013) Temperature effects on pitfall catches of epigeal arthropods: a model and method for bias correction. J Appl Ecol 50:181–189. CrossRefPubMedGoogle Scholar
  56. Simon S, Bouvier J-C, Debras J-F, Sauphanor B (2010) Biodiversity and pest management in orchard systems. A review. Agron Sustain Dev 30:139–152CrossRefGoogle Scholar
  57. Thiele H-U (1977) Carabid beetles in their environments. Springer, BerlinCrossRefGoogle Scholar
  58. Tscharntke T, Clough Y, Bhagwat SA, Buchori D, Faust H, Hertel D, Hölscher D, Juhrbandt J, Kessler M, Perfecto I, Scherber C, Schroth G, Veldkamp E, Wanger TC (2011) Multifunctional shade-tree management in tropical agroforestry landscapes—a review. J Appl Ecol 48:619–629. CrossRefGoogle Scholar
  59. Tuf IH, Dedek P, Vesely M (2012) Does the diurnal activity pattern of carabid beetles depend on season, ground temperature and habitat? Arch Biol Sci. CrossRefGoogle Scholar
  60. Vucic-Pestic O, Ehnes RB, Rall BC, Brose U (2011) Warming up the system: higher predator feeding rates but lower energetic efficiencies. Glob Change Biol 17:1301–1310. CrossRefGoogle Scholar
  61. Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefGoogle Scholar
  62. Weber DC, Pfannenstiel RS, Lundgren JG (2008) Diel predation pattern assessment and exploitation of sentinel prey: new interpretations of community & individual behaviors. In: Proceedings of the third international symposium on biological control of arthropods, Christchurch, New Zealand, pp 485–494Google Scholar
  63. Zehnder G, Gurr GM, Kühne S, Wade MR, Wratten SD, Wyss E (2007) Arthropod pest management in organic crops. Annu Rev Entomol 52:57–80. CrossRefPubMedGoogle Scholar
  64. Zuur AF (ed) (2009) Mixed effects models and extensions in ecology with R. Statistics for biology and health. Springer, New YorkGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.AGROOFAnduzeFrance
  2. 2.UAPV, UMR 7263 CNRS-IRDInstitut Méditerranéen de Biodiversité et EcologieAvignon cedex 09France
  3. 3.INRAUR EMMAHAvignonFrance

Personalised recommendations