Skip to main content
SpringerLink
Log in

Antipredator Behavioral Traits of some Agriotes Wireworms (Coleoptera: Elateridae) and their Potential Implications for Species Identification

  • Published:
Journal of Insect Behavior Aims and scope Submit manuscript

Abstract

Many insects show a typical antipredator behavior. The two simplest tactics are immobilization and flight. The antipredator behavior of wireworms, the soil-dwelling polyphagous larvae of click beetles, has not yet been investigated. Birds are known to attack wireworms. Our experimental method (picking up and dropping wireworms) mimics the first attack of a predator, such as a bird. In Europe, some Agriotes species are of particular importance as crop pests. As these species differ considerably, in ecology, damage threshold, and pathogen resistance, knowing more about the species specific biology and behavior will support the establishment of successful control measures. In an extensive microcosm study, we observed the antipredator behavior of wireworms belonging to four different Agriotes species (A. lineatus, A. obscurus, A. sordidus, and A. ustulatus) before and during digging into the soil after a startle-stimulus. We recorded wireworm immobility frequency and duration, and locomotor activity at three temperatures. We also analyzed genetic and morphologic attributes of A. lineatus larvae from two different origins. Following behavior types were found reflecting different escape tactics: (a) distinct tonic immobility (A. lineatus), (b) brief/inconsistent tonic immobility (A. obscurus, A. sordidus), and (c) immediate fleeing/burying (A. ustulatus). Additionally, we found small but significant differences in morphology, behavior, and genetics (PCR results) between A. lineatus larvae originating from the Netherlands and those originating from Germany. The biological information we gathered about each species will further increase the understanding of these insects and improve interpretation of future experimental data. In addition, the described behavioral differences between Agriotes obscurus and A. lineatus wireworms may represent a useful additional criterion in morphological species identification.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Acheampong S, Mitchell BK (1997) Quiescence in the Colorado potato beetle, Leptinotarsa decemlineata. Entomol Exp Appl 82:83–89

    Article  Google Scholar 

  • Beaudoin-Ollivier L, Prior RNB, Laup S (2000) Simplified field key to identify larvae of some rhinoceros beetles and associated scarabs (Coleoptera: Scarabaeoidea) in Papua New Guinea coconut developments. Ann Entomol Soc Am 93:90–95

    Article  Google Scholar 

  • Benefer CM, van Herk WG, Ellis JS, Blackshaw RP, Vernon RS, Knight ME (2012) The molecular identification and genetic diversity of economically important wireworm species (Coleoptera: Elateridae) in Canada. J Pest Sci 86:19–27

    Article  Google Scholar 

  • Berg MB, Merritt RW (2003) Growth, individual. In: Resh VH, Cardé RT (eds) Encyclopedia of insects, 2nd edn. Academic Press, San Diego, pp 431–434

  • Brunner N, Hann P, Trska C, Kromp B (2011) How does wireworm damage in potato fields correlate with elaterid species as well as environmental and cultivation parameters? IOBC/WPRS Bull 66:487–490

    Google Scholar 

  • Camhi JM, Tom W, Volman S (1978) The escape behavior of the cockroach Periplaneta americana. II Detection of natural predators by air displacement. J Comp Physiol 128:203–212

    Article  Google Scholar 

  • Chapman RF (1998) The insects: structure and function, 4th edn. Cambridge University Press, UK

    Book  Google Scholar 

  • Danner BJ, Joern A (2003) Stage-specific behavioral responses of Ageneotettix deorum (Orthoptera: Acrididae) in the presence of lycosid spider predators. J Insect Behav 16:453–464

    Article  Google Scholar 

  • Dedryver CA, Robin N, Taupin P, Thibord JB (2009) Lutte contre les taupins. 2009 April, France, INRA-Avaris, pp 1–26

  • de Mendiburu F (2013) Agricolae: statistical procedures for agricultural research. R package version 1.1–6. http://CRAN.R-project.org/package=agricolae. Accessed 16 April 2015

  • Falconer DS (1945a) On the behaviour of wireworms of the genus Agriotes Esch. (Coleoptera, Elateridae) in relation to temperature. J Exp Biol 21:17–32

    Google Scholar 

  • Falconer DS (1945b) On the movement of wireworms of the genus Agriotes Esch. (Coleoptera, Elateridae) on the surface of the soil and their sensitivity to light. J Exp Biol 21:33–38

    Google Scholar 

  • Feare CJ (1974) Ecological studies of the rook (Corvus frugilegus L.) in north-East Scotland. Damage and its control. J Appl Ecol 11:897–914

    Article  Google Scholar 

  • Freude H, Harde KW, Lohse GA (eds) (1979) Volume 6: Diversicornia (Lycidae - Byrrhidae). In: die Käfer Mitteleuropas. (the beetles of Central Europe.). Spektrum Akademischer Verlag, Heidelberg, Germany, pp. 103–186

    Google Scholar 

  • Furlan L (2014) IPM thresholds for Agriotes wireworm species in maize in Southern Europe. J Pest Sci 87:609–617

    Article  Google Scholar 

  • Furlan L (2004) The biology of Agriotes sordidus Illiger (Col., Elateridae). J Appl Entomol 128:696–706

    Article  Google Scholar 

  • Furlan L (1998) The biology of Agriotes ustulatus Schäller (Col., Elateridae). II. Larval development, pupation, whole cycle description and practical implications. J Appl Entomol 122:71–78

    Article  Google Scholar 

  • Furlan L, Tóth M, Parker WE, Ivezic M, Pancic S, Brmez Z, Voigt D, Carollo G (Editor) 2001 The efficacy of the new Agriotes sex pheromone traps in detecting wireworm population levels in different European countries. Proceedings of XXI IWGO Conference, 27 October–3 November 2001, Legnaro, Italy: Tadiotto a; Lavezzo I, pp 293–304

  • Gras H, Hörner M (1992) Wind-evoked escape running of the cricket Gryllus bimaculatus: I. Behav Anal J Exp Biol 171:189–214

    Google Scholar 

  • Hoffmann G (1991) Verband Deutscher Landwirtschaftlicher Untersuchungs- und Forschungsanstalten Methodenbuch. Band I. Die Untersuchung von Böden, 4th edn. VDLUFA-Verlag, Darmstadt, Germany

    Google Scholar 

  • Holmes SJ (1906) Death-feigning in Ranatra. J Comp Neurol Psychol 16:200–216

    Article  Google Scholar 

  • Honek A, Furlan L (1995) Colour polymorphism in Agriotes ustulatus (Coleoptera: Elateridae): absence of geographic and temporal variation. Eur J Entomol 92:437–442

    Google Scholar 

  • Hozumi N, Miyatake T (2005) Body-size dependent difference in death-feigning behavior of adult Callosobruchus chinensis. J Insect Behav 18:557–566

    Article  Google Scholar 

  • Jander R (1963) Grundleistungen der Licht-und Schwereorientierung von Insekten. Z vergl Physiol 47:381–430

    Article  Google Scholar 

  • Jones MP, Pierce KE Jr, Ward D (2007) Avian vision: a review of form and function with special consideration to birds of prey. J Exot Pet Med 16:69–87

    Article  Google Scholar 

  • Kabaluk JT, Ericsson JD (2007) Environmental and behavioral constraints on the infection of wireworms by Metarhizium anisopliae. Environ Entomol 36:1415–1420

    Article  PubMed  Google Scholar 

  • Kennedy TF, Connery J (2008) An investigation of seed treatments for the control of crow damage to newly-sown wheat. Irish J Agric Food Res 47:79–91

    Google Scholar 

  • King BH, Leaich HR (2006) Variation in propensity to exhibit thanatosis in Nasonia vitripennis (Hymenoptera: Pteromalidae). J Insect Behav 19:241–249

    Article  Google Scholar 

  • Kiyotake H, Matsumoto H, Nakayama S, Sakai M, Miyatake T, Ryuda M, Hayakawa Y (2014) Gain of long tonic immobility behavioral trait causes the red flour beetle to reduce anti-stress capacity. J Insect Physiol 60:92–97

    Article  CAS  PubMed  Google Scholar 

  • Klausnitzer K (1994) Familie Elateridae. In: Klausnitzer BE. Die Larven der Käfer Mitteleuropas. Gustav Fischer Verlag, Jena, Germany, pp 118–189

  • Klemola T, Tanhuanpää M, Korpimäki E, Ruohomäki K (2002) Specialist and generalist natural enemies as an explanation for geographical gradients in population cycles of northern herbivores. Oikos 99:83–94

    Article  Google Scholar 

  • Kölliker U, Biasio L, Jossi W (2011) Potential control of Swiss wireworms with entomopathogenic fungi. IOBC/WPRS Bull 66:517–520

  • Kuriwada T, Kumano N, Shiromoto K, Haraguchi D (2010) The effect of mass-rearing on death-feigning behaviour in the sweet potato weevil (Coleoptera: Brentidae). J Appl Entomol 134:652–658

    Google Scholar 

  • Langenbuch R (1932) Beiträge zur Kenntnis der Biologie von Agriotes lineatus L. und Agriotes obscurus L. Z Angew Entomol 19:278–300

    Article  Google Scholar 

  • Lees AD (1943a) On the behaviour of wireworms of the genus Agriotes Esch. (Coleoptera, Elateridae) I. Reactions to humidity. J Exp Biol 20:43–53

    Google Scholar 

  • Lees AD (1943b) On the behaviour of wireworms of the genus Agriotes Esch. (Coleoptera, Elateridae) II. Reactions to moisture. J Exp Biol 20:54–60

    Google Scholar 

  • Lehmhus J, Niepold F (2013) New finds of the click beetle Agriotes sordidus (Illiger, 1807) and an overview on its current distribution in Germany. J Kult 65:309–314

    Google Scholar 

  • Lehmhus J, Niepold F (2015) Identification of Agriotes wireworms - are they always what they appear to be? J Kult 67:129–138

    Google Scholar 

  • Lima SL (1998) Stress and decision-making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv Study Behav 27:215–290

    Article  Google Scholar 

  • Marler P, Hamilton WJ (1966) Mechanisms of animal behavior. John Wiley, Sons, New York

    Google Scholar 

  • Matthews RW, Matthews JR (2010) Insect behavior. Springer, Dordrecht, The Netherlands

    Book  Google Scholar 

  • Miles HW (1942) Wireworms and agriculture. J R Agric Soc Engl 102:1–13

    Google Scholar 

  • Miyatake T (2001a) Diurnal periodicity of death-feigning in Cylas formicarius (Coleoptera: Brentidae). J Insect Behav 14:421–432

    Article  Google Scholar 

  • Miyatake T (2001b) Effects of starvation on death-feigning in adults of Cylas formicarius (Coleoptera: Brentidae). Ann Entomol Soc Am 94:612–616

    Article  Google Scholar 

  • Miyatake T, Katayama K, Takeda Y, Nakashima A, Sugita A, Mizumoto M (2004) Is death-feigning adaptive? Heritable variation in fitness difference of death-feigning behaviour. Proc R Soc Lond [Biol] 271:2293–2296

    Article  Google Scholar 

  • Miyatake T, Okada K, Harano T (2008a) Negative relationship between ambient temperature and death-feigning intensity in adult Callosobruchus maculatus and Callosobruchus chinensis. Physiol Entomol 33:83–88

    Article  Google Scholar 

  • Miyatake T, Tabuchi K, Sasaki K, Okada K, Katayama K, Moriya S (2008b) Pleiotropic antipredator strategies, fleeing and feigning death, correlated with dopamine levels in Tribolium castaneum. Anim Behav 75:113–121

    Article  Google Scholar 

  • Nakamuta K, van Tol RW, Visser JH (2005) An olfactometer for analyzing olfactory responses of death-feigning insects. Appl Entomol Zool 40:173–175

    Article  Google Scholar 

  • Nishino H, Sakai M (1996) Behaviorally significant immobile state of so-called thanatosis in the cricket Gryllus bimaculatus DeGeer: its characterization, sensory mechanism and function. J Comp Physiol A Sens Neural Behav Physiol 179:613–624

    Article  Google Scholar 

  • Ohno T, Miyatake T (2007) Drop or fly? Negative genetic correlation between death-feigning intensity and flying ability as alternative anti-predator strategies. Proc R Soc Lond [Biol] 274:555–560

    Article  Google Scholar 

  • Parker WE, Howard JJ (2001) The biology and management of wireworms (Agriotes spp.) on potato with particular reference to the UK. Agric For Entomol 3:85–98

    Article  Google Scholar 

  • Pic M, Pierre E, Martinez M, Genson G, Rasplus JY, Albert H, AFPP (Editor) (2008) Les taupins du genre Agriotes démasqués par leurs empreintes génétiques. AFPP. Colloque Biodiversité et Changements Climatiques. 8ème Conférence Internationale sur les Ravageurs en Agriculture, 22–23 October 2008, Montpellier, France, pp 23–32

  • Pienkowski RL (1976) Behavior of the adult alfalfa weevil in diapause. Ann Entomol Soc Am 69:155–157

    Article  Google Scholar 

  • Prohammer LA, Wade MJ (1981) Geographic and genetic variation in death-feigning behavior in the flour beetle, Tribolium castaneum. Behav Genet 11:395–401

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.r-project.org. Accessed 16 April 2015

  • Reisenman CE, Lazzari CR, Giurfa M (1998) Circadian control of photonegative sensitivity in the haematophagous bug Triatoma infestans. J Comp Physiol A Sens Neural Behav Physiol 183:533–541

    Article  Google Scholar 

  • Ritter C, Richter E (2013) Control methods and monitoring of Agriotes wireworms (Coleoptera: Elateridae). J Plant Dis Protect 120:4–15

    Article  CAS  Google Scholar 

  • Ritter C, Richter E, Knölck I, Katroschan K-U (2014) Laboratory studies on the effect of calcium cyanamide on wireworms (Agriotes ustulatus, Coleoptera: Elateridae). J Plant Dis Protect 121:133–137

    Article  CAS  Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford, UK

    Book  Google Scholar 

  • Scheid C, Range F, Bugnyar T (2007) When, what, and whom to watch? Quantifying attention in ravens (Corvus corax) and jackdaws (Corvus monedula). J Comp Psychol 121:380–386

    Article  PubMed  Google Scholar 

  • Sonnemann I, Grunz S, Wurst S (2014) Horizontal migration of click beetle (Agriotes spp.) larvae depends on food availability. Entomol Exp Appl 150:174–178

    Article  Google Scholar 

  • Stacey DA, Fellowes MDE (2002) Influence of temperature on pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae) resistance to natural enemy attack. Bull Entomol Res 92:351–357

    CAS  PubMed  Google Scholar 

  • Staudacher K, Pitterl P, Furlan L, Cate PC, Traugott M (2011a) PCR-based species identification of Agriotes larvae. Bull Entomol Res 101:201–210

    Article  CAS  PubMed  Google Scholar 

  • Staudacher K, Schallhart N, Pitterl P, Wallinger C, Brunner N, Landl M, Traugott M (2011b) Occurrence of Agriotes wireworms in Austrian agricultural land. J Pest Sci 86:33–39

    Article  Google Scholar 

  • Staudacher K, Schallhart N, Thalinger B, Wallinger C, Juen A, Traugott M (2013) Plant diversity affects behavior of generalist root herbivores, reduces crop damage, and enhances crop yield. Ecol Appl 23:1135–1145

    Article  PubMed  Google Scholar 

  • Steiniger F (1936) Die Biologie der sog. „tierischen Hypnose“. Springer, Heidelberg, Germany, pp 348–451

  • Strobbe F, McPeek MA, de Block M, Stoks R (2010) Survival selection imposed by predation on a physiological trait underlying escape speed. Funct Ecol 24:1306–1312

    Article  Google Scholar 

  • Sufyan M, Neuhoff D, Furlan L (2014) Larval development of Agriotes obscurus under laboratory and seminatural conditions. Bull Insectol 67:227–235

  • Therneau T, Atkinson B, Ripley B (2013) Rpart: recursive partitioning. R package version 4.1–4. http://CRAN.R-project.org/package=rpart. Accessed 16 April 2015

  • Traugott M, Benefer CM, Blackshaw RP, van Herk WG, Vernon RS (2015) Biology, ecology, and control of elaterid beetles in agricultural land. Annu Rev Entomol 60:313–334

    Article  CAS  PubMed  Google Scholar 

  • van Herk WG, Vernon RS (2013) Categorization and numerical assessment of wireworm mobility over time following exposure to bifenthrin. J Pest Sci 86:115–123

    Article  Google Scholar 

  • van Herk WG, Vernon RS, McGinnis S (2013) Response of the dusky wireworm, Agriotes obscurus (Coleoptera: Elateridae), to residual levels of bifenthrin in field soil. J Pest Sci 86:125–136

    Article  Google Scholar 

  • Vernon RS (2005) Aggregation and mortality of Agriotes obscurus (Coleoptera: Elateridae) at insecticide-treated trap crops of wheat. J Econ Entomol 98:1999–2005

    Article  PubMed  Google Scholar 

  • Vernon RS, Kabaluk T, Behringer A (2000) Movement of Agriotes obscurus (Coleoptera: Elateridae) in strawberry (Rosaceae) plantings with wheat (Gramineae) as a trap crop. Can Entomol 132:231–241

    Article  Google Scholar 

  • Vernon RS, van Herk WG (2013) Wireworms as pests of potato. In: Giordanengo P (ed) Insect pests of potato: global perspectives on biology and management, Academic, Amsterdam, pp 103–164

  • Wei YJ (2001) Nysius huttoni (Hemiptera: Lygaeidae): life history and some aspects of its biology and ecology in relation to wing development and flight. Dissertation, University of Canterbury, http://hdl.handle.net/10092/5856

Download references

Acknowledgments

We would like to thank the technical staff of the Vegetable Research and Information Center, especially Irena Knölck, Mona Knoll, and Karin Ohde, for their support in preparing the experiment. Furthermore, we greatly thank the staff of the JKI, especially Dörte Achilles, Ales Dolezal, Ruth Schaarschmidt and Dieter Gebelein for experimental assistance. We greatly thank Dr. Carly Benefer (School of Biological Sciences, Faculty of Science & Environment, United Kingdom) for her additional behavioral experiments on wireworms and click beetles and the supplied experimental data.

Most of all, we thank those who provided us with wireworms: Dr. Fanny Barsics (Department of Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, University of Liege, Gembloux, Belgium) in cooperation with the Arvalis Institute - Montardon (Pau, southern France), Hilfred Huiting (Applied Plant Research Wageningen UR, Lelystad, the Netherlands), the organic farm Gensheimer (Offenbach/Queich, Germany), Raphael Maurath (District Council Office Breisgau High Black Forest, Breisach, Germany), Udo Pfotenhauer and Dr. Andreas Gurgel (State Research Center of Agriculture and Fisheries Mecklenburg-Vorpommern, Gülzow, Germany), Dr. Jörn Lehmhus (Julius Kühn-Institute Braunschweig, Germany), and Dr. Lorenzo Furlan (Veneto Agricoltura, Legnaro, PD, Italy).

We would like to thank Editage (www.editage.com) for English language editing.

Finally, we are indebted to Dr. Frank Burghause (Dienstleistungszentrum Ländlicher Raum, Bad Kreuznach, Germany) for double-checking our morphologically determined wireworm species, and to Dr. Karin Staudacher for methodological advice on genetic species determination.

Author information

Authors and Affiliations

  1. State Research Center of Agriculture and Fisheries Mecklenburg-Vorpommern, Vegetable Research and Information Center, Dorfplatz 1, D-18276 Gülzow-Prüzen, Rostock, Germany

    Claudia Ritter & Kai-Uwe Katroschan

  2. Faculty of Agricultural and Environmental Sciences, University of Rostock, D-18051, Rostock, Germany

    Claudia Ritter, Friederike de Mol & Christine Struck

  3. Julius Kühn-Institute (JKI) - Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Horticulture and Forests, Messeweg 11/12, D-38104, Braunschweig, Germany

    Ellen Richter

Authors
  1. Claudia Ritter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Friederike de Mol
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ellen Richter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christine Struck
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kai-Uwe Katroschan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudia Ritter.

Ethics declarations

Financial Support

This work was financially supported by the German Federal Ministry of Food, Agriculture and Consumer Protection (BMELV) through the Federal Office for Agriculture and Food (BLE), grant number 2808HS005.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ritter, C., de Mol, F., Richter, E. et al. Antipredator Behavioral Traits of some Agriotes Wireworms (Coleoptera: Elateridae) and their Potential Implications for Species Identification. J Insect Behav 29, 214–232 (2016). https://doi.org/10.1007/s10905-016-9555-3

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10905-016-9555-3

Keywords

Search

Navigation