The provision of refuges for natural enemies could be a key aspect for the management of the woolly apple aphid [Eriosoma lanigerum (Hausmann, 1802)] (Hemiptera: Aphididae) in apple orchards. The present study assesses the effects of Pyracantha coccinea (Rosaceae) (firethorn) adjacent to apple orchards as this extra-orchard habitat would positively affect the abundance of natural enemies and control of E. lanigerum. Abundances were evaluated for the pest, the parasitoid, Aphelinus mali (Haldeman, 1851) (Hymenoptera: Aphelinidae) (during two seasons) and generalist predators (only during the second season). The assessments were conducted at different distances from P. coccinea located at the edge of the apple orchards. Additionally, parasitism rates by A. mali were examined using a categorical and two quantitative methods. Results indicate that P. coccinea hedges promoted an early colonization by A. mali in apple orchards especially during the first season. However, parasitism rates by A. mali were not affected at the beginning of the season, but as the season progressed, the rates increased on the apple trees in comparison with the hedges. Additionally, during the second season, the interaction between certain natural enemies had a stronger effect on the population growth rates of E. lanigerum in orchards with P. coccinea compared to control orchards. Based on these results, we conclude that P. coccinea hedges may promote the early colonization by A. mali in the orchards and have a positive effect on the abundance of spiders, but had no effect on coccinelid, carabids, earwigs and syrphids.
This is a preview of subscription content, log in to check access.
Buy single article
Instant unlimited access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Altieri MA (1999) The ecological role of biodiversity in agroecosystems. Agric Ecosyst Environ 74:19–31. https://doi.org/10.1016/S0167-8809(99)00028-6
Altieri MA, Schmidt LL (1986) The dynamics of colonizing arthropod communities at the interface of abandoned, organic and commercial apple orchards and adjacent woodland habitats. Agric Ecosyst Environ 16:29–43
Asante SK (1995) Functional responses of the European earwig and two species of coccinellids to densities of Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae). J Aust Entomol Soc 34:105–109. https://doi.org/10.1111/j.1440-6055.1995.tb01295.x
Asante SK, Danthanarayana W (1993) Sex ratios in natural populations of Aphelinus mali (Hym.: Aphelinidae) in relation to host size and host density. Entomophaga 38:391–403. https://doi.org/10.1007/BF02374457
Begg GS, Cook SM, Dye R et al (2016) A functional overview of conservation biological control. Crop Prot 97:145–158. https://doi.org/10.1016/j.cropro.2016.11.008
Bianchi FJJA, van Wingerden WKRE, Griffioen AJ et al (2005) Landscape factors affecting the control of Mamestra brassicae by natural enemies in Brussels sprout. Agric Ecosyst Environ 107:145–150. https://doi.org/10.1016/j.agee.2004.11.007
Bianchi FJJA, Booij CJH, 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. https://doi.org/10.1098/rspb.2006.3530
Blackman RL, Eastop VF (2006) Volume 1: host lists and keys? In: Blackman RL, Eastop VF (eds) Aphids on the world’s herbaceous plants and shrubs. The Natural History Museum, Wiley, Hoboken, pp 1–1024
Budenberg WJ (1990) Honeydew as a contact kairomone for aphid parasitoids. Entomol Exp Appl 55:139–148. https://doi.org/10.1111/j.1570-7458.1990.tb01357.x
Cardinale BJ, Duffy JE, Gonzalez A et al (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67. https://doi.org/10.1038/nature11148
Cohen H, Horowitz AR, Nestel D, Rosen D (1996) Susceptibility of the woolly apple aphid parasitoid, Aphelinus mali (Hym.: Aphelinidae), to common pesticides used in apple orchards in Israel. Entomophaga 41:225–233. https://doi.org/10.1007/BF02764248
Corbett A, Rosenheim JA (1996) Impact of a natural enemy overwintering refuge and its interaction with the surrounding landscape. Ecol Entomol 21:155–164. https://doi.org/10.1111/j.1365-2311.1996.tb01182.x
Cowgill SE, Wratten SD, Sotherton NW (1993) The effect of weeds on the numbers of hoverfly (Diptera: Syrphidae) adults and the distribution and composition of their eggs in winter wheat. Ann Appl Biol 123:499–515. https://doi.org/10.1111/j.1744-7348.1993.tb04922.x
De Moraes CM, Lewis WJ, Paré PW et al (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573. https://doi.org/10.1038/31219
De Villalobos AE, Vázquez DP, Martin JL (2010) Soil disturbance, vegetation cover and the establishment of the exotic shrub Pyracantha coccinea in southern France. Biol Invasions 12:1023–1029. https://doi.org/10.1007/s10530-009-9519-z
Derocles SAP, Le Ralec A, Besson MM et al (2014) Molecular analysis reveals high compartmentalization in aphid-primary parasitoid networks and low parasitoid sharing between crop and noncrop habitats. Mol Ecol 23:3900–3911. https://doi.org/10.1111/mec.12701
Duarte GT, Santos PM, Cornelissen TG et al (2018) The effects of landscape patterns on ecosystem services: meta-analyses of landscape services. Landsc Ecol 33:1247–1257. https://doi.org/10.1007/s10980-018-0673-5
Duflot R, Daniel H, Aviron S et al (2018) Adjacent woodlands rather than habitat connectivity influence grassland plant, carabid and bird assemblages in farmland landscapes. Biodivers Conserv 27:1925–1942. https://doi.org/10.1007/s10531-018-1517-y
Eilenberg J, Hajek A, Lomer C (2001) Suggestions for unifying the terminology in biological control. Biocontrol 46:387–400. https://doi.org/10.1023/A:1014193329979
Erb M, Foresti N, Turlings TCJ (2010) A tritrophic signal that attracts parasitoids to host-damaged plants withstands disruption by non-host herbivores. BMC Plant Biol 10:1–11. https://doi.org/10.1186/1471-2229-10-247
Geiger F, Wäckers FL, Bianchi FJJA (2009) Hibernation of predatory arthropods in semi-natural habitats. Biocontrol 54:529–535. https://doi.org/10.1007/s10526-008-9206-5
Giller KE, Beare MH, Lavelle P et al (1997) Agricultural intensification, soil biodiversity and agroecosystem function. Appl Soil Ecol 6:3–16. https://doi.org/10.1016/S0929-1393(96)00149-7
Gillespie MAK, Gurr GM, Wratten SD (2016) Beyond nectar provision: the other resource requirements of parasitoid biological control agents. Entomol Exp Appl 159:207–221. https://doi.org/10.1111/eea.12424
Gontijol LM, Cockfield SD, Beers EH (2012) Natural enemies of woolly apple aphid (Hemiptera: Aphididae) in Washington state. Environ Entomol 41:1364–1371. https://doi.org/10.1603/EN12085
Grez AA, Torres C, Zaviezo T et al (2010) Migration of coccinellids to alfalfa fields with varying adjacent vegetation in Central Chile. Cienc e Investig Agrar 37:111–121. https://doi.org/10.4067/S0718-16202010000200011
Gurr GM, Liu J, Read DMY et al (2011) Parasitoids of Asian rice planthopper (Hemiptera: Delphacidae) pests and prospects for enhancing biological control by ecological engineering. Ann Appl Biol 158:149–176. https://doi.org/10.1111/j.1744-7348.2010.00455.x
Harrison XA, Donaldson L, Correa-Cano ME, Evans J, Fisher DN, Goodwin CED, Robinson BS, Hodgson DJ, Inger R (2018) A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 6:e4794. https://doi.org/10.7717/peerj.4794
Helsen H, Vaal F, Blommers L (1998) Phenology of the common earwig Forficula auricularia L. (Dermaptera: Forficulidae) in an apple orchard. Int J Pest Manag 44:75–79. https://doi.org/10.1080/096708798228356
Horton DR, Lewis TM (2000) Seasonal distribution of Anthocoris spp. and Deraeocoris brevis (Heteroptera: Anthocoridae, Miridae) in orchard and non-orchard habitats of Central Washington. Ann Entomol Soc Am 93:476–485. https://doi.org/10.1603/0013-8746(2000)093%5b0476:sdoasa%5d2.0.co;2
Howard LO (1929) Aphelinus Mali and its travels. Ann Entomol Soc Am 22:341–368
Lamb RJ, Wellington WG (1975) Life history and population characteristics of the European earwig, Forficula auricularia (Dermaptera: Forficulidae), at Vancouver, British Columbia. Can Entomol 107:819–824. https://doi.org/10.4039/Ent107819-8
Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201. https://doi.org/10.1146/annurev.ento.45.1.175
Lavandero B, Wratten S, Hagler J, Jervis M (2004) The need for effective marking and tracking techniques for monitoring the movements of insect predators and parasitoids. Int J Pest Manag 50:147–151. https://doi.org/10.1080/09670870410001731853
Lavandero B, Wratten S, Shishehbor P, Worner S (2005) Enhancing the effectiveness of the parasitoid Diadegma semiclausum (Helen): movement after use of nectar in the field. Biol Control 34:152–158. https://doi.org/10.1016/j.biocontrol.2005.04.013
Lavandero B, Figueroa CC, Franck P, Mendez A (2011) Estimating gene flow between refuges and crops: a case study of the biological control of Eriosoma lanigerum by Aphelinus mali in apple orchards. PLoS ONE 6:e26694. https://doi.org/10.1371/journal.pone.0026694
Leroy P, Capella Q, Haubruge E (2009) L’impact du miellat de puceron au niveau des relations tritrophiques entre les plantes-hôtes, les insectes ravageurs et leurs ennemis naturels. Biotechnol Agron Soc Environ 13:325–334
Letourneau DK, Jedlicka JA, Bothwell SG, Moreno CR (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu Rev Ecol Evol Syst 40:573–592. https://doi.org/10.1146/annurev.ecolsys.110308.120320
Letourneau DK, Allen SGB, Kula RR et al (2015) Habitat eradication and cropland intensification may reduce parasitoid diversity and natural pest control services in annual crop fields. Elem Sci Anth 3:000069. https://doi.org/10.12952/journal.elementa.000069
Liang KY, Zeger SL (1986) Longitudinal data analysis using generalized linear models. Biometrika 73:13–22. https://doi.org/10.1093/biomet/73.1.13
Lordan J, Alegre S, Gatius F et al (2015a) Woolly apple aphid Eriosoma lanigerum Hausmann ecology and its relationship with climatic variables and natural enemies in Mediterranean areas. Bull Entomol Res 105:60–69. https://doi.org/10.1017/S0007485314000753
Lordan J, Alegre S, Moerkens R et al (2015b) Phenology and interspecific association of Forficula auricularia and Forficula pubescens in apple orchards. Span J Agric Res 13:1–12. https://doi.org/10.5424/sjar/2015131-6814
Mehrnejad MR, Copland MJW (2006) Behavioral responses of the parasitoid Psyllaephagus pistaciae (Hymenoptera: Encyrtidae) to host plant volatiles and honeydew. Entomol Sci 9:31–37. https://doi.org/10.1111/j.1479-8298.2006.00151.x
Miliczky ER, Horton DR (2005) Densities of beneficial arthropods within pear and apple orchards affected by distance from adjacent native habitat and association of natural enemies with extra-orchard host plants. Biol Control 33:249–259. https://doi.org/10.1016/j.biocontrol.2005.03.002
Miliczky E, Horton DR (2007) Natural enemy fauna (Insecta, Araneae) found on native sagebrush steppe plants in eastern Washington with reference to species also found in adjacent apple and pear orchards. Pan-Pac Entomol 83:50–65. https://doi.org/10.3956/0031-0603-83.1.50
Moerkens R, Leirs H, Peusens G, Gobin B (2009) Are populations of European earwigs, Forficula auricularia, density dependent? Entomol Exp Appl 130:198–206. https://doi.org/10.1111/j.1570-7458.2008.00808.x
Mols PJM, Boers JM (2001) Comparison of a Canadian and a Dutch strain of the parasitoid Aphelinus mali (Hald) (Hym., Aphelinidae) for control of woolly apple aphid Eriosoma lanigerum (Haussmann) (Hom., Aphididae) in the Netherlands: a simulation approach. J Appl Entomol 125:255–262. https://doi.org/10.1046/j.1439-0418.2001.00543.x
Nicholas AH, Spooner-Hart RN, Vickers RA (2005) Abundance and natural control of the woolly aphid Eriosoma lanigerum in an Australian apple orchard IPM program. Biocontrol 50:271–291. https://doi.org/10.1007/s10526-004-0334-2
Ortiz-Martínez SA, Ramírez CC, Lavandero B (2013) Host acceptance behavior of the parasitoid Aphelinus mali and its aphid-host Eriosoma lanigerum on two Rosaceae plant species. J Pest Sci 86:659–667. https://doi.org/10.1007/s10340-013-0518-6
Pan W (2001) Akaike’s information criterion in generalized estimating equations. Biometrics 57:120–125
R Development Core Team (2010) R: a language and environment for statistical computing. Computer programme. http://www.R-project.org/. Accessed 5 Oct 2018
Rand TA, Tylianakis JM, Tscharntke T (2006) Spillover edge effects: the dispersal of agriculturally subsidized insect natural enemies into adjacent natural habitats. Ecol Lett 9:603–614. https://doi.org/10.1111/j.1461-0248.2006.00911.x
Raymond L, Ortiz-Martínez SA, Lavandero B (2015) Temporal variability of aphid biological control in contrasting landscape contexts. Biol Control 90:148–156. https://doi.org/10.1016/j.biocontrol.2015.06.011
Rega C, Bartual AM, Bocci G et al (2018) A pan-European model of landscape potential to support natural pest control services. Ecol Indic 90:653–664. https://doi.org/10.1016/j.ecolind.2018.03.075
Rojas S (2005) Control biológico de plagas en Chile: historia y avances. Instituto de Investigaciones Agropecuarias (INIA), Ministerio de Agricultura, Gobierno de Chile, Chile
Schmidt MH, Tscharntke T (2005) The role of perennial habitats for Central European farmland spiders. Agric Ecosyst Environ 105:235–242. https://doi.org/10.1016/j.agee.2004.03.009
Short BD, Bergh JC (2004) Feeding and egg distribution studies of Heringia calcarata (Diptera: Syrphidae), a specialized predator of woolly apple aphid (Homoptera: Eriosomatidae) in Virginia apple orchards. J Econ Entomol 97:813–819
Simon S, Bouvier JC, Debras JF, Sauphanor B (2010) Biodiversity and pest management in orchard systems. A review. Agron Sustain Dev 30:139–152. https://doi.org/10.1051/agro/2009013
Soler R, Harvey JA, Kamp AFD et al (2007) Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos 116:367–376. https://doi.org/10.1111/j.0030-1299.2007.15501.x
Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594. https://doi.org/10.1146/annurev.ento.47.091201.145240
Tscharntke T, Klein AM, Kruess A et al (2005) Landscape perspectives on agricultural intensification and biodiversity: ecosystem service management. Ecol Lett 8:857–874. https://doi.org/10.1111/j.1461-0248.2005.00782.x
Tylianakis JM, Didham RK, Wratten SD (2004) Improved fitness of aphid parasitoids receiving resource subsidies. Ecology 85:658–666. https://doi.org/10.1890/03-0222
Veres A, Petit S, Conord C, Lavigne C (2013) Does landscape composition affect pest abundance and their control by natural enemies? A review. Agric Ecosyst Environ 166:110–117. https://doi.org/10.1016/j.agee.2011.05.027
Wearing CH, Attfield BA, Colhoun K (2010) Biological control of woolly apple aphid, Eriosoma lanigerum (Hausmann), during transition to integrated fruit production for pipfruit in Central Otago, New Zealand. N Z J Crop Hortic Sci 38:255–273. https://doi.org/10.1080/01140671.2010.524189
White AJ, Wratten SD, Berry NA, Weigmann U (1995) Habitat manipulation to enhance biological control of Brassica pests by hover flies (Diptera: Syrphidae). J Econ Entomol 88:1171–1176. https://doi.org/10.1093/jee/88.5.1171
Woltz JM, Isaacs R, Landis DA (2012) Landscape structure and habitat management differentially influence insect natural enemies in an agricultural landscape. Agric Ecosyst Environ 152:40–49. https://doi.org/10.1016/j.agee.2012.02.008
Zhou H, Yu Y, Tan X et al (2014) Biological control of insect pests in apple orchards in China. Biol Control 68:47–56. https://doi.org/10.1016/j.biocontrol.2013.06.009
Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York
The authors very much thank Artzai Jauregui Solano for his assistance in the field work. Also, the authors would like to thank Cinthya Villegas for her advice during the process of the experiments and all orchard owners for providing us with the access to their apple orchards.
This study was funded by the Fondo Nacional de Desarrollo Científico y Tecnológico (Fondecyt) Postdoctoral Grant No. 3160233 and by Fondecyt Regular Grant No. 1140632.
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national and/or institutional guidelines for the care and use of animals were followed.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Communicated by M. Traugott.
About this article
Cite this article
Peñalver-Cruz, A., Alvarez, D. & Lavandero, B. Do hedgerows influence the natural biological control of woolly apple aphids in orchards?. J Pest Sci 93, 219–234 (2020) doi:10.1007/s10340-019-01153-1
- Woolly apple aphid
- Aphelinus mali
- Eriosoma lanigerum
- Generalist predators
- Apple orchards