Hostname: page-component-848d4c4894-xm8r8 Total loading time: 0 Render date: 2024-07-01T06:16:09.601Z Has data issue: false hasContentIssue false

Aphid alarm pheromone alters larval behaviour of the predatory gall midge, Aphidoletes aphidimyza and decreases intraguild predation by anthocorid bug, Orius laevigatus

Published online by Cambridge University Press:  05 March 2021

Mojtaba Hosseini
Affiliation:
Institute of Ecology, Friedrich-Schiller-University, Jena, Germany
Mohsen Mehrparvar*
Affiliation:
Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran
Sharon E. Zytynska
Affiliation:
Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, Centre for Food and Life Sciences Weihenstephan, Technical University of Munich, Freising, Germany
Eduardo Hatano
Affiliation:
Institute of Ecology, Friedrich-Schiller-University, Jena, Germany
Wolfgang W. Weisser
Affiliation:
Institute of Ecology, Friedrich-Schiller-University, Jena, Germany Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, Centre for Food and Life Sciences Weihenstephan, Technical University of Munich, Freising, Germany
*
Author for correspondence: Mohsen Mehrparvar, Email: mehrparvar@aphidology.com; mehrparvar@kgut.ac.ir

Abstract

Intraguild predation is the killing and consuming of a heterospecific competitor that uses similar resources as the prey, and also benefit from preying on each other. We investigated the foraging behaviour of the gallmidge, Aphidoletes aphidimyza, a predator of aphids used for biological control that is also the intraguild prey for most other aphid natural enemies. We focus on how aphid alarm pheromone can alter the behaviour of the gallmidge, and predation by the anthocorid bug Orius laevigatus (O. laevigatus). We hypothesised that gallmidges would respond to the presence of (E)-β-farnesene (EBF) by leaving the host plant. Since feeding by Aphidoletes gallmidge larvae does not induce EBF emission by aphids, this emission indicates the presence of an intraguild predator. We found that gallmidge larvae reduced their foraging activities and left the plant earlier when exposed to EBF, particularly when aphids were also present. Contrastingly, gallmidge females did not change the time visiting plants when exposed to EBF, but lay more eggs on plants that had a higher aphid density. Lastly, EBF reduced the number of attacks of the intraguild predator, O. laevigatus, on gallmidge larvae, potentially because more gallmidges stopped aphid feeding and moved off the plant at which point O. laevigatus predated on aphids. Our work highlights the importance of understanding how intraguild predation can influence the behaviour of potential biological control agents and the impact on pest control services when other natural enemies are also present.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Present address: Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran.

Present address: Department of Evolution, Ecology and Behaviour, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool, UK.

Present address: Department of Entomology, Schal's Lab, North Carolina State University, Raleigh, North Carolina, USA.

References

Agarwala, BK, Bardhanroy, P, Yasuda, H and Takizawa, T (2003) Effects of conspecific and heterospecific competitors on feeding and oviposition of a predatory ladybird: a laboratory study. Entomologia Experimentalis Et Applicata 106, 219226.CrossRefGoogle Scholar
Arim, M and Marquet, PA (2004) Intraguild predation: a widespread interaction related to species biology. Ecology Letters 7, 557564.CrossRefGoogle Scholar
Boulanger, F-X, Jandricic, S, Bolckmans, K, Wäckers, FL and Pekas, A (2019) Optimizing aphid biocontrol with the predator Aphidoletes aphidimyza, based on biology and ecology. Pest Management Science 75, 14791493.CrossRefGoogle ScholarPubMed
Bowers, WS, Webb, RE, Nault, LR and Dutky, SR (1972) Aphid alarm pheromone: Isolation, identification, synthesis. Science 177, 11211122.CrossRefGoogle ScholarPubMed
Christensen, RK, Enkegaard, A and Brodsgaard, HF (2002) Intraspecific interactions among the predators Orius majusculus and Aphidoletes aphidimyza. IOBC/WPRS Bulletin 25, 5760.Google Scholar
Dicke, M and Grostal, P (2001) Chemical detection of natural enemies by arthropods: an ecological perspective. Annual Review of Ecology and Systematics 32, 123.CrossRefGoogle Scholar
Dixon, AFG (2000) Foraging behavior. In Dixon, AFG (ed.), Insect Predator-Prey Dynamics: Ladybird Beetles and Biological Control. Cambridge: Cambridge University Press, pp. 82129.Google Scholar
Ferreira, JAM, Cunha, DFS, Pallini, A, Sabelis, MW and Janssen, A (2011) Leaf domatia reduce intraguild predation among predatory mites. Ecological Entomology 36, 435441.CrossRefGoogle Scholar
Ferris, G and Rudolf, VW (2007) Response of larval dragonflies to conspecific and heterospecific predator cues. Ecological Entomology 32, 283288.CrossRefGoogle Scholar
Frago, E and Godfray, HCJ (2014) Avoidance of intraguild predation leads to a long-term positive trait-mediated indirect effect in an insect community. Oecologia 174, 943952.CrossRefGoogle Scholar
Hatano, E, Kunert, G, Bartram, S, Boland, W, Gershenzon, J and Weisser, WW (2008) Do aphid colonies amplify their emission of alarm pheromone? Journal of Chemical Ecology 34, 11491152.CrossRefGoogle ScholarPubMed
Hemptinne, JL, Lognay, G, Doumbia, M and Dixon, AFG (2001) Chemical nature and persistence of the oviposition deterring pheromone in the tracks of the larvae of the two spot ladybird, Adalia bipunctata (Coleoptera : Coccinellidae). Chemoecology 11, 4347.CrossRefGoogle Scholar
Humphreys, RK and Ruxton, GD (2019) Dropping to escape: a review of an under-appreciated antipredator defence. Biological Reviews 94, 575589.CrossRefGoogle ScholarPubMed
Kislow, C and Edwards, LJ (1972) Repellent odour in aphids. Nature 235, 108109.CrossRefGoogle Scholar
Klingauf, F (1967) Abwehr- und Meidereaktionen von Blattla üsen (Aphididae) bein Bedrohung durch Raüber und parasiten. Zeitschrift für Angewandte Entomologie 60, 269317.CrossRefGoogle Scholar
Kunert, G and Weisser, WW (2003) The interplay between density- and trait-mediated effects in predator-prey interactions: a case study in aphid wing polymorphism. Oecologia 135, 304312.CrossRefGoogle ScholarPubMed
Kunert, G, Otto, S, Rose, USR, Gershenzon, J and Weisser, WW (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecology Letters 8, 596603.CrossRefGoogle Scholar
Lucas, E (2005) Intraguild predation among aphidophagous predators. European Journal of Entomology 102, 351364.CrossRefGoogle Scholar
Lucas, E and Brodeur, J (1999) Oviposition site selection by the predatory midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Environmental Entomology 28, 622627.CrossRefGoogle Scholar
Lucas, E and Brodeur, J (2001) A fox in sheep's clothing: furtive predators benefit from the communal defense of their prey. Ecology 82, 32463250.CrossRefGoogle Scholar
Lucas, E, Coderre, D and Brodeur, J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79, 10841092.CrossRefGoogle Scholar
Markkula, M, Tiittanen, K, Hämäläinen, M and Forsberg, A (1979) The aphid midge Aphidoletes aphidimyza (Diptera, Cecidomyiidae) and its use in biological control of aphids. Annales Entomologica Fennica 45, 8998.Google Scholar
Martinou, AF, Raymond, B, Milonas, PG and Wright, DJ (2010) Impact of intraguild predation on parasitoid foraging behaviour. Ecological Entomology 35, 183189.CrossRefGoogle Scholar
Messelink, GJ, Bloemhard, CM, Cortes, JA, Sabelis, MW and Janssen, A (2011) Hyperpredation by generalist predatory mites disrupts biological control of aphids by the aphidophagous gall midge Aphidoletes aphidimyza. Biological Control 57, 246252.CrossRefGoogle Scholar
Minoretti, N and Weisser, WW (2000) The impact of individual ladybirds (Coccinella septempunctata, Coleoptera: Coccinellidae) on aphid colonies. European Journal of Entomology 97, 475479.CrossRefGoogle Scholar
Montgomery, ME and Nault, LR (1977) Comparative response of aphids to the alarm pheromone, (E)-beta-farnesene. Entomologia Experimentalis Et Applicata 22, 236242.CrossRefGoogle Scholar
Mortensen, L and Richardson, JML (2008) Effects of chemical cues on foraging in damselfly larvae, Enallagma antennatum. Journal of Insect Behavior 21, 285295.CrossRefGoogle Scholar
Müller, CB and Brodeur, J (2002) Intraguild predation in biological control and conservation biology. Biological Control 25, 216223.CrossRefGoogle Scholar
Müller, CB, Adriaanse, ICT, Belshaw, R and Godfray, HCJ (1999) The structure of an aphid-parasitoid community. Journal of Animal Ecology 68, 346370.CrossRefGoogle Scholar
Nakashima, Y, Birkett, MA, Pye, BJ, Pickett, JA and Powell, W (2004) The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata, by the aphid parasitoid, Aphidius ervi. Journal of Chemical Ecology 30, 11031116.CrossRefGoogle ScholarPubMed
Nakashima, Y, Birkett, MA, Pye, BJ and Powell, W (2006) Chemically mediated intraguild predator avoidance by aphid parasitoids: interspecific variability in sensitivity to semiochemical trails of ladybird predators. Journal of Chemical Ecology 32, 19891998.CrossRefGoogle ScholarPubMed
Nedved, O, Fois, X, Ungerova, D and Kalushkov, P (2013) Alien vs. Predator – the native lacewing Chrysoperla carnea is the superior intraguild predator in trials against the invasive ladybird Harmonia axyridis. Bulletin of Insectology 66, 7378.Google Scholar
Perdikis, D, Lucas, E, Garantonakis, N, Giatropoulos, A, Kitsis, P, Maselou, D, Panagakis, S, Lampropoulos, P, Paraskevopoulos, A, Lykouressis, D and Fantinou, A (2014) Intraguild predation and sublethal interactions between two zoophytophagous mirids, Macrolophus pygmaeus and Nesidiocoris tenuis. Biological Control 70, 3541.CrossRefGoogle Scholar
Polis, GA, Myers, CA and Holt, RD (1989) The ecology and evolution of intraguild predation – potential competitors that eat each other. Annual Review of Ecology and Systematics 20, 297330.CrossRefGoogle Scholar
Raymond, B, Darby, AC and Douglas, AE (2000) Intraguild predators and the spatial distribution of a parasitoid. Oecologia 124, 367372.CrossRefGoogle ScholarPubMed
Rieger, JF, Binckley, CA and Resetarits, WJ (2004) Larval performance and oviposition site preference along a predation gradient. Ecology 85, 20942099.CrossRefGoogle Scholar
Rosenheim, JA (1998) Higher-order predators and the regulation of insect herbivore populations. Annual Review of Entomology 43, 421447.CrossRefGoogle ScholarPubMed
Rosenheim, JA, Wilhoit, LR and Armer, CA (1993) Influence of intraguild predation among generalist insect pedators on the suppression of an herbivore population. Oecologia 96, 439449.CrossRefGoogle ScholarPubMed
Rosenheim, JA, Kaya, HK, Ehler, LE, Marois, JJ and Jaffee, BA (1995) Intraguild predation among biological-control agents – theory and evidence. Biological Control 5, 303335.CrossRefGoogle Scholar
Ruzicka, Z (1998) Further evidence of oviposition-deterring allomone in chrysopids (Neuroptera: Chrysopidae). European Journal of Entomology 95, 3539.Google Scholar
Ruzicka, Z (2001a) Oviposition responses of aphidophagous coccinellids to tracks of ladybird (Coleoptera: Coccinellidae) and lacewing (Neuroptera: Chrysopidae) larvae. European Journal of Entomology 98, 183188.CrossRefGoogle Scholar
Ruzicka, Z (2001b) Response of chrysopids (Neuroptera) to larval tracks of aphidophagous coccinellids (Coleoptera). European Journal of Entomology 98, 283285.CrossRefGoogle Scholar
Ruzicka, Z (2003) Perception of oviposition-deterring larval tracks in aphidophagous coccinellids Cycloneda limbifer and Ceratomegilla undecimnotata (Coleoptera: Coccinellidae). European Journal of Entomology 100, 345350.CrossRefGoogle Scholar
Ruzicka, Z (2006) Oviposition-deterring effects of conspecific and heterospecific larval tracks on Cheilomenes sexmaculata (Coleoptera: Coccinellidae). European Journal of Entomology 103, 757763.CrossRefGoogle Scholar
Ruzicka, Z and Havelka, J (1998) Effects of oviposition-deterring pheromone and allomones on Aphidoletes aphidimyza (Diptera: Cecidomyiidae). European Journal of Entomology 95, 211216.Google Scholar
Sarmento, RA, Venzon, M, Pallini, A, Oliveira, EE and Janssen, A (2007) Use of odours by Cycloneda sanguinea to assess patch quality. Entomologia Experimentalis Et Applicata 124, 313318.CrossRefGoogle Scholar
Sato, S, Yasuda, H and Evans, EW (2005) Dropping behaviour of larvae of aphidophagous ladybirds and its effects on incidence of intraguild predation: interactions between the intraguild prey, Adalia bipunctata (L.) and Coccinella septempunctata (L.), and the intraguild predator, Harmonia Axyridis Pallas. Ecological Entomology 30, 220224.CrossRefGoogle Scholar
Sergio, F, Marchesi, L, Pedrini, P and Penteriani, V (2007) Coexistence of a generalist owl with its intraguild predator: distance-sensitive or habitat-mediated avoidance? Animal Behaviour 74, 16071616.CrossRefGoogle Scholar
Snyder, WE and Ives, AR (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82, 705716.CrossRefGoogle Scholar
Vet, LEM and Dicke, M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37, 141172.CrossRefGoogle Scholar
Yu, X-L, Feng, Y, Fu, W-Y, Sun, Y-X and Liu, T-X (2019) Intraguild predation between Harmonia axyridis and Aphidius gifuensis: effects of starvation period, plant dimension and extraguild prey density. BioControl 64, 5564.CrossRefGoogle Scholar