Elsevier

Crop Protection

Volume 65, November 2014, Pages 71-76
Crop Protection

Aggregation behavior in the European earwig: Response to impregnated shelters

https://doi.org/10.1016/j.cropro.2014.07.005Get rights and content

Highlights

  • Aggregation behavior of European earwig was confirmed in field conditions in apple orchards.

  • The number of earwigs required to impregnate a shelter and the duration of such impregnation was determined.

  • A shelter impregnated by 0.2 individuals/cm2 over one week was observed to attract earwigs during 5 weeks.

  • Such impregnated shelters could be used to promote earwigs in pip fruit orchards and to remove them from stone fruit ones.

Abstract

The European earwig Forficula auricularia Linnaeus (Dermaptera: Forficulidae) is a key predator of pests in pip fruit orchards; however, this insect can also cause economic damage in stone fruit crops. Pheromone-impregnated shelters may be useful to promote earwigs in orchards devoted to pip fruit and also to capture them in those used for stone fruit production. By using corrugated cardboard traps in four orchards during two years, we observed the aggregation behavior of European earwig in canopies. Under laboratory conditions, corrugated cardboard shelters impregnated by 0.2 individuals/cm2 over one week attracted earwigs for 5 weeks within a range of 50 cm. Future field work should examine the potential of impregnated shelters to promote earwigs in pip fruit orchards and to remove them from stone fruit ones.

Introduction

The European earwig, Forficula auricularia Linnaeus (Dermaptera: Forficulidae), is an important predator in pip fruit (Asante, 1995, He et al., 2008, Lenfant et al., 1994, Nicholas et al., 2005), kiwifruit (Hill et al., 2005) and citrus (Piñol et al., 2010, Piñol et al., 2009) orchards. However, given its omnivorous regime, this insect can damage shoots, leaves, flowers and fruits (Pollini, 2010), becoming a pest of stone fruit crops (Albouy and Caussanel, 1990, Cranshaw, 2000, Flint, 2012, Grafton-Cardwell et al., 2003, Kuthe, 1996) and vineyards, where in addition to its direct damage on berries, its frass can negatively influence the aroma and flavor of some wines (Burdet et al., 2013, Huth et al., 2011). The incidence and severity of earwig outbreaks has recently increased in peaches (Prunus persica (L.) Batsch var. persica), nectarines (P. persica (L.) Batsch var. nectarine (Aiton) Maxim. and P. persica (L.) Batsch var. nucipersica (Borkh.) Schneider), apricots (Prunus armeniaca L.) and cherries (Prunus avium L.), reaching in some cases 10–15% of damage in Mediterranean areas (Asteggiano and Vittone, 2013, Pollini, 2010, Saladini et al., 2012; Servei de Sanitat Vegetal, 2013). Therefore, earwig management practices should be adopted in accordance with the fruit crop. To control them in conventional production, growers spray orchards with commonly used pesticides such as chlorpyrifos and spinosad that have been reported to have lethal effects on European earwig (Fountain et al., 2013, Peusens and Gobin, 2008, Vogt et al., 2010). In organic production, alternative strategies such as mass trapping and exclusion by setting glue around the base of trunks are used (Alston and Tebeau, 2011, Saladini et al., 2012).

The European earwig is a thigmotactic insect that shelters during the day and forages at night (Albouy and Caussanel, 1990, Burnip et al., 2002). It is usually found in clusters across the orchard, taking refuge in shelters previously occupied by earwigs (Sauphanor and Sureau, 1993). In laboratory experiments, this insect has been observed to aggregate, which is postulated to be elicited by a pheromone (Evans and Longépé, 1996, Hehar et al., 2008, Sauphanor, 1992, Sauphanor and Sureau, 1993, Walker et al., 1993). Gregarious behavior confers protection against predators, increases mate encounters, and enhances juvenile growth and development (Antony et al., 1985, Fuchs et al., 1985, Sauphanor and Sureau, 1993, Walker et al., 1993).

Laboratory experiments revealed that females, males, and nymphs produce and respond to an airborne aggregation pheromone; however, its source and composition are still under debate (Evans and Longépé, 1996, Hehar et al., 2008, Sauphanor, 1992, Walker et al., 1993). Sauphanor (1992) suggested that the pheromone was segregated on tibial glands, while Walker et al. (1993) associated it with fecal excreta and cuticular lipids. Evans and Longépé (1996) reported that leg extracts were not active and pointed to the body cuticle as the source of the pheromone, whereas Hehar et al. (2008) observed that neither fresh frass extracts nor body washes elicited significant responses. Although the source and composition of the pheromone remains unclear, Hehar et al. (2008) proposed that this chemical cue is perceived by olfaction rather than by contact chemoreception, and Evans and Longépé (1996) had already determined that it was detectable by the antennae.

Evans and Longépé, 1996, Sauphanor and Sureau, 1993 and Hehar et al. (2008) observed that filter papers, cardboard shelters, and paper-towel disks previously in contact with European earwig individuals elicited aggregation behavior. In this regard, the use of corrugated cardboard shelters in pear orchards has been reported to increase populations of European earwig which results in a reduction of the densities of pear psylla Cacopsylla pyri L. (Hemiptera: Psyllidae) (Solomon et al., 1999). Suckling et al. (2006) suggested that high populations of earwigs may significantly contribute to biological control. Earwigs have been shown to be predators of pests such as woolly apple aphid (WAA) Eriosoma lanigerum Hausmann (Asante, 1995, Mueller et al., 1988, Nicholas et al., 2005), and green apple aphid Aphis pomi DeGeer (both Hemiptera: Aphididae) (Carroll and Hoyt, 1984, Hagley and Allen, 1990), apple leaf-curling midge Dasineura mali Kieffer (Diptera: Cecidomyiidae) (He et al., 2008) and diaspidid scale insects (Hemiptera: Diaspididae) (Hill et al., 2005, Logan et al., 2007).

In pip fruit, growers have tried with little success up to now, to enhance earwig populations (Moerkens et al., 2009). While the pheromone emitted by earwigs is not commercially available, shelters impregnated with the aggregation pheromone by maintaining earwig individuals in contact with them for some time may be useful for this purpose. Impregnated shelters might be also useful to capture individuals in stone fruit orchards. However, such applications are hindered because there is no method to ensure long-term impregnation of shelters for this purpose.

Here we evaluated the aggregation behavior of the European earwig in field conditions; determined in the laboratory the number of earwigs required to impregnate a shelter, the duration of such impregnation, and the distance at which the insect can respond to the pheromonal signal emitted by these shelters.

Section snippets

Aggregation behavior in field conditions

The trials were performed in the following four apple orchards located in Catalonia (NE Spain): Les Borges Blanques (41°30′23.06″N; 0°51′05.93″E), Mollerussa (41°36′51.13″N; 0°52′22.75″E), Ivars d'Urgell (41°41′06.19″N; 0°58′06.09″E), and Miralcamp (41°36'31.89″N; 0°52'24.62″E). All orchards were under organic management. To evaluate earwig aggregation behavior, 10 cardboard traps per orchard were set up in the canopy of trees (one trap per tree). For this purpose, a piece of corrugated

Aggregation behavior in field conditions

European earwig nymphs in field traps were observed from April to the beginning of June, whereas adults were mainly found from June to August (Fig. 1a–b). Nymph density peaked at the end of May, with an average of 23.78 ± 4.89 (mean ± SE) individuals per trap in 2012 and 14.68 ± 3.18 individuals per trap in 2013 (Fig. 1a–b). The number of adults per trap had one peak (37.53 ± 7.1) in June 2012 and two similar peaks in June–July 2013 (23.34 ± 4.65 and 21.41 ± 5.38) (Fig. 1a–b). From April to mid

Aggregation behavior

Earwigs in tree traps were observed from April to August, with higher densities between May and June. Similar results were observed by Romeu-Dalmau et al. (2011) under Mediterranean climates, while in colder areas of Central-Northern Europe they tend to appear later in the season, with density peaks in June–July (Gobin et al., 2008, Helsen et al., 1998, Moerkens et al., 2011, Moerkens et al., 2009). These differences between warmer and colder areas may be explained by earwigs being highly

Acknowledgments

We thank Anna Geli and Lourdes Zazurca for technical support. This work was funded by the Spanish project AGL2010-17486. We would also like to thank two anonymous reviewers and the editor for their constructive comments, which improved this manuscript.

References (52)

  • V. Albouy et al.

    Dermaptères ou Perce-Oreilles. Fédération Française des Sociétés de Sciences Naturelles

    (1990)
  • D. Alston et al.

    Utah pest fact sheet: European earwig (Forficula auricularia), in: University, U.S

  • C. Antony et al.

    Compared behavioral responses of male Drosophila melanogaster (Canton S) to natural and synthetic aphrodisiacs

    J. Chem. Ecol.

    (1985)
  • S.K. Asante

    Functional responses of the European earwig and 2 species of coccinellids to densities of Eriosoma lanigerum (Hausmann) (Hemiptera: Aphididae)

    J. Aust. Entomol. Soc.

    (1995)
  • S.K. Asante et al.

    Spatial and temporal distribution of the Eriosoma lanigerum on apple

    Environ. Entomol.

    (1993)
  • L. Asteggiano et al.

    Albicocche e nettarine, come contenere i danni delle forficule

    Frutticoltura

    (2013)
  • J.P. Burdet et al.

    Occurrence of earwigs in vineyards and their impact on aroma and flavour of “Chasselas” and “Pinot Noir” wines

    IOBC-WPRS Bull.

    (2013)
  • G.M. Burnip et al.

    European earwig phenology and effect of understorey management on population estimation

    N. Z. Plant Prot.

    (2002)
  • D.P. Carroll et al.

    Augmentation of European earwigs (Dermaptera, Forficulidae) for biological control of apple aphid (Homoptera, Aphididae) in an apple orchard

    J. Econ. Entomol.

    (1984)
  • W.S. Cranshaw

    European earwig: habits and management

    Pest alert

    (2000)
  • S.E. Crumb et al.

    The European earwig

    United States Dep. Agric. Tech. Bull.

    (1941)
  • M. Eizaguirre et al.

    Diapause induction in the stem corn borer, Sesamia nonagrioides (Lepidoptera: Noctuidae)

    Entomol. Gen.

    (1992)
  • K.A. Evans et al.

    The European earwig: getting the best of both worlds?

  • M.L. Flint

    Pest Notes: Earwigs UC ANR Publication 74102,UC Statewide IPM Program

    (2012)
  • M.T. Fountain et al.

    Importance of naturally occurring predators for pear sucker control

    IOBC-WPRS Bull.

    (2013)
  • M.E.A. Fuchs et al.

    Carboxylic acids in the feces of Blattella germanica (L.) and their possible role as part of the aggregation pheromone

    J. Appl. Entomol.

    (1985)
  • B. Gobin et al.

    Enhancing earwig populations in Belgian orchards

    Commun. Agric. Appl. Biol. Sci.

    (2006)
  • B. Gobin et al.

    Understanding earwig phenology in top fruit orchards. Proceedings of the International Conferenceon Cultivation Technique and Phytopathological Problems in Organic Fruit growing

  • E.E. Grafton-Cardwell et al.

    Photographic Guide to Citrus Fruit Scarring. Oakland (CA): Division of Agriculture and Natural Resources

    (2003)
  • E.A.C. Hagley et al.

    The green apple aphid Aphis pomi DeGeer (Homoptera, Aphididae), as prey of polyphagous arthropod predators in Ontario

    Can. Entomol.

    (1990)
  • X.Z. He et al.

    European earwig as a potential biological control agent of apple leaf-curling midge

    N. Z. Plant Prot.

    (2008)
  • G. Hehar et al.

    Re-analysis of pheromone-mediated aggregation behaviour of European earwigs

    Can. Entomol.

    (2008)
  • H. Helsen et al.

    Phenology of the common earwig Forficula auricularia L. (Dermaptera: Forficulidae) in an apple orchard

    Int. J. Pest Manag.

    (1998)
  • M.G. Hill et al.

    A technique for measuring growth rate and survival of armoured scale insects

    N. Z. Plant Prot.

    (2005)
  • C. Huth et al.

    A beneficial species becomes a pest – the common earwig Forficula auricularia (Linnaeus 1758)

    IOBC-WPRS Bull.

    (2011)
  • S. Ishii et al.

    Aggregation of german cockroach (Blattella germanica) nymphs

    Experientia

    (1968)
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