Abstract
Chemicals, which mediate the interactions between aphids, ladybirds and ants, are reviewed. Special emphasis is laid on autogenous and plant-derived chemical defence in aphids and ladybirds. Evidences for chemical cues used during foraging and oviposition in ladybirds are assessed. Possible mutualistic interaction between plants and the third trophic level is illustrated by the as yet few reports of indirect plant-defence volatiles induced by aphids or coccids attracting parasitoids or ladybirds. The use of chemical signals allowing aphid parasitoids or ladybirds to squeeze into ant–aphid mutualistic association is briefly described. Questions are raised and hypotheses suggested which could stimulate further research on aphid host-plant influence on ladybird foraging behaviour and fitness, and on the cues used by aphid-web partners for their mutual recognition.
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Al Abassi S, Birkett MA, Petterson J, Pickett JA, Woodcok CM (1998) Ladybird beetle odour identified and found to be responsible for attraction between adults. Cell Mol Life Sci 54:876–879
Al Abassi S, Birkett MA, Petterson J, Pickett JA, Wadhams LJ, Woodcock CM (2000) Response of the seven-spot ladybird to an alarm pheromone and an alarm pheromone inhibitor is mediated by paired olfactory cells. J Chem Ecol 26:1765–1771
Al Abassi S, Birkett MA, Petterson J, Pickett JA, Wadhams LJ, Woodcock CM (2001) Response of the ladybird parasitoid, Dinocampus coccinellae, to toxic alkaloids from the seven-spot ladybird, Coccinella septempunctata. J Chem Ecol 27:33–43
Agarwala BK, Dixon AFG (1992) Laboratory study of cannibalism and interspecific predation in ladybirds. Ecol Entomol 17:303–309
Agarwala BK, Bhattacharya S, Bardhanroy P (1998) Who eats whose eggs? Intra- versus inter-specific interactions in starving ladybird beetles predaceous on aphids. Ethol Ecol Evol 10:361–368
Arnonson JT, Guillet G, Durst T (2004) Phytochemical diversity of insect defenses in tropical and temperate plant families. In: Cardé RT, Millar JC (eds) Advances in chemical ecology. Cambridge University Press, Cambridge, pp 1–20
Bertschy C, Turlings TCJ, Bellotti AC, Dorn S (2001) The role of mealybug-induced cassava plant volatiles in the attraction of the encyrtid parasitoids Aenasius vexans and Apoanagyrus diversicornis. J Insect Behav 14:363–371
Budenberg WJ, Powell W (1992) The role of honeydew as an ovipositional stimulant for two species of syrphids. Entomol exp appl 64:57–61
Cottrell TE, Yeargan KV (1998) Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae) and a native lady beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). J Kans Entomol Soc 71:159–163
Daloze D, Braekman JC, Pasteels JM (1995) Ladybird defence alkaloids: structure, chemotaxonomic and biosynthetic aspects (Col.: Coccinellidae). Chemoecology 5/6:173–183
Dettner K, Liepert C (1994) Chemical mimicry and camouflage. Annu Rev Entomol 39:129–154
Dicke M, Sabelis MW (1988) Infochemical terminology: based on cost–benefit analyses rather than origin of compounds. Funct Ecol 2:131–139
Dixon AFG (1958) The escape responses shown by certain aphids to the presence of the coccinellid beetle Adalia decempunctata (L.). Trans R Entomol Soc London 110:319–334
Dixon AFG (1997) Patch quality and fitness in predatory ladybirds. In: Dettner K, Bauer G, Volkl (eds) Vertical food web interactions. Evolutionary patterns and driving forces. Ecol Stud 130:205–223
Dixon AFG (2000) Insect predator–prey dynamics. Ladybird beetles and biological control. Cambridge University Press, Cambridge
Doumbia M, Hemptinne JL, Dixon AFG (1998) Assessment of patch quality by ladybirds: role of larval tracks. Oecologia 118:197–202
Du Y, Poppy GM, Powell W, Pickett JA, Wadhams LJ, Woodcock CM (1998) Identification of semiochemicals, released during aphid feeding, that attract parasitoid Aphidius ervi. J Chem Ecol 24:1355–1368
Edwards JS (1966) Defence by smear: supercooling in the cornicle wax of aphids. Nature 211:73–74
Eisner T, Ziegler R, McCormick JL, Eisner M, Hoebeke ER, Meinwald J (1994) Defensive use of an acquired substance (carminic acid) by predaceous insect larvae. Experientia 50:610–615
Feeny P (1975) Biochemical coevolution between plants and their insect herbivores. In: Gilbert L, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Austin, pp 3–19
Francis F, Haubruge E, Gaspar Ch (2000) Influence of host plants on specialist/generalist aphids and on the development of Adalia bipunctata (Coloptera: Coccinellidae). Eur J Entomol 97:481–483
Francis F, Lognay G, Wathelet JP, Haubruge E (2001) Effects of allelochemicals from first (Brassicaceae) and second (Myzus persicae and Brevicoryne brassicae) trophic levels on Adalia bipunctata. J Chem Ecol 27:243–256
Francis F, Lognay G., Haubruge E (2004) Olfactory responses to aphid and host plant volatiles releases: (E)-β-farnesene an effective kairomone for the predator Adalia bipunctata. J Chem Ecol 30:741–755
Frechette B, Dixon AFG, Alauzet C, Hemptinne JL (2004) Age and experience influence patch assessment for oviposition by an insect predator. Ecol Entomol 29:578–583
Godeau J-F, Hemptinne J-L, Verhaeghe J-C (2003) Ant trail: a highway for Coccinella magnifica Redtenbacher (Coleoptera: Coccinellidae) In: Proceedings of 8th International Symposium Ecology Aphidophaga Arquipélago. Biology, ecology and behaviour of aphidophagous insects. Life Mar Sci Supplement 5:79–83
Han B, Chen Z (2002) Behavioral and electrophysiological responses of natural enemies from tea shoots and kairomones from tea aphids, Toxoptera aurantii. J Chem Ecol 28:2203–2219
Hemptinne J-L, Dixon AFG (1991) Why ladybirds have been generally so ineffective in biological control? In: Polgar L, Chambers RJ, Dixon AFG, Hodek I (eds) Behaviour and impact of aphidophaga. SP Academic, The Haghe
Hemptinne J-L, Dixon AFG (2000) Defence, oviposition and sex: semiochemical parsimony in two species of ladybird beetles (Coleoptera, Coccinellidae)? A short review. Eur J Entomol 97:443–447
Hemptinne J-L, Dixon AFG, Gauthier C (2000a) Nutritive cost of intraguild predation on eggs of Coccinella septempunctata and Adalia bipunctata (Coleoptera: Coccinellidae). Eur J Entomol 97:559–569
Hemptinne J-L, Gaudin M, Dixon AFG, Lognay G (2000b) Social feeding in ladybird beetles: adaptative significance and mechanism. Chemoecology 10:149–152
Hemptinne J-L, Lognay G, Gauthier C, Dixon AFG (2000c) Role of surface chemical signals in egg cannibalism and intraguild predation in ladybirds (Coleoptera: Coccinellidae). Chemoecology 10:123–128
Hemptinne J-L, Lognay G, Doumbia M, Dixon AFG (2001) Chemical nature and persistence of the oviposition deterring pheromone of the larvae of the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Chemoecology 11:43–47
Hodek I (1973) Biology of Coccinellidae. Academia, Prague
Hodek I, Honek A (1996) Ecology of Coccinellidae. Kluwer, Dordrecht
Iperti G (1965) Contribution à l’étude de la spécificité chez les principales coccinelles aphidiphages des Alpes-Maritimes et des Basses-Alpes. Entomophaga 10:159–178
King AG, Meinwald J (1966) Review of the defensive chemistry of coccinellids. Chem Rev 96:1105–1122
Laurent P, Braekman J-C, Daloze D, Pasteels JM (2003) Biosynthesis of defensive compounds from beetles and ants. Eur J Org Chem 15: 2733–2743. DOI: 10.1002/ejoc.200300008
Laurent P, Braekman J-C, Daloze D (2005) Insect chemical defense. Top Curr Chem 240: 167–229. DOI: 10.1007/b98317
Lebrun B, Braekman J-C, Daloze D, Kalushkov P, Pasteels JM (2001) Hyperaspine, a new 3-oxaquinolizidine alkaloid from Hyperaspis campestris (Coleoptera: Coccinellidae). Tetrahedron Lett 42:4621–4623
Leclercq S, Braekman JC, Daloze D, Pasteels JM (2000) The defensive chemistry of ants. In: Herz W, Falk H, Kirby GW, Moore RE (eds) Progress in the chemistry of organic natural products, 79. Springer, Wien, pp 239–249
Malcom SB (1990) Chemical defence in chewing and sucking insect herbivores: plant-derived cardenolides in the monarch butterfly and oleander aphid. Chemoecology 1:12–21
Marple NM, Braekfield PM, Cowie PG (1989) Differences between the 7-spot and 2-spot ladybird beetles (Coccinellidae) in their toxic effects on a bird predator. Ecol Entomol 14:79–84
Mendel Z, Blumberg D, Zehavi A, Weissenberg M (1992) Some polyphagous Homoptera gain protection from their natural enemies by feeding on the toxic plants Spartium junceum and Erythrina corallodendron (Leguminosae). Chemoecology 3:118–124
Merlin J, Lemaire O, Grégoire J-C (1996a) Oviposition in Cryptolaemus montrouzieri stimulated by wax filants of its prey. Entomol Exp Appl 79:141–146
Merlin J, Lemaire O, Grégoire J-C (1996b) Chemical cues produced by conspecific larvae deter oviposition by the coccidophagous ladybird beetle, Cryptolaemus montrouzieri. Entomol Exp Appl 79:147–151
Moore BP, Brown WV, Rothschild M (1990) Methylalkylpyrazines in aposematic insects, their host plants and mimics. Chemoecology 12:43–51
Nakashima Y, Birkett MA, Pye BJ, Pickett JA, Powell W (2004) The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata, by the aphid parasitoid, Aphidius ervi. J Chem Ecol 30:1103–1116
Ninkovic V, Abassi SA, Petterson J (2001) The influence of aphid-induced plant volatiles in ladybird beetle searching behavior. Biol Control 21:191–195
Obata S (1986) Mechanisms of prey finding in the aphidophagous ladybird beetle, Harmonia axyridis (Coleoptera: Coccinellidae). Entomophaga 31:303–311
Pasteels JM (1976) Evolutionary aspects in chemical ecology and chemical communication. In: White D (ed) Proceedings of the 15th international congress entomology. Entomological Society of America, Washington, pp 281–293
Pasteels JM (1978) Apterous and brachypterous coccinellids at the end of the food chain, Cionura erecta (Asclepiadaceae)-Aphis nerii. Entomol Exp Appl 24:379–384
Pasteels J M (1982) Is kairomone a valid and useful term? J Chem Ecol 8:1079–1081
Pasteels J M, Deroe C, Tursch B, Braekman J-C, Daloze D, Hootele C (1973) Distribution et activité des alcaloïdes des coccinelles. J Insect Physiol 19:1771–1784
Powell W, Pennachio F, Poppy GM, Tremblay E (1998) Strategies involved in the location of hosts by the parasitoid Aphidius ervi Haliday (Hymenoptera: Bracinidae: Aphidiinae). Biol Control 11:104–112
Rothschild M, von Euw J, Reichstein T (1970) Cardiac glycosides in the oleader aphid, Aphis nerii. J Insect Physiol 16:1141–1145
Rothschild M, von Euw J, Reichstein T (1973) Cardiac glycosides in a scale insect (Aspidiotus), a ladybird (Coccinella) and a lacewing (Chrysopa). J Entomol A 48:89–90
Ruzicka Z (1997a) Persistence of the oviposition-deterring pheromone in Chrysopa oculata (Neur.: Chrysopidae). Entomophaga 42:107–112
Ruzicka Z (1997b) Recognition of oviposition-deterring allomones by aphidophagous predators (Neuroptera: Chrysopidae, Coleoptera : Coccinellidae). Eur J Entomol 94:431–434
Schröder FC, Farmer JJ, Attygalle A, Smedley SC, Eisner T, Meinwald J (1998) Combinatorial chemistry in insects: a library of defensive macrocyclic polyamines. Science 281:428–431
Sloggett JJ, Wood RA, Majerus MEN (1998) Adaptation of Coccinella magnifica Redtenbacher, a myrmecophiloous coccinellid, to aggression by wood ants (Formica rufa group). I. Adult behavioural adaptation, its ecological context and evolution. J Insect Behav 6:889–904
Souissi R, Le Rü B (1999) Behavioural responses of the endoparasitoid Apoanagyrus lopezi to odours of the host and host’s cassava plants. Entomol Exp Appl 90:215–220
Souissi R, Nénon JP, Le Rü B (1998) Olfactory responses of parasitoid Apoanagyrus lopezi to odor of plants, mealybugs, and plant-mealybug complexes. J Chem Ecol 24:37–48
Stadler B, Dixon AFG (1999) Ant attendance in aphids: why different degrees of myrmecophily? Ecol Entomol 24:363–369
Turlings TCJ, Wäckers F (2004) Recruitment of predators and parasitoids by hebivore–injured plants. In: Cardé RT, Millar JC (eds) Advances in chemical ecology. Cambridge University Press, Cambrige, pp 21–75
Turlings TCJ, Bernasconi M, Bertossa R (1998) The induction of volatiles in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biol Control 11:122–129
Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 371:141–172
Way MJ (1963) Mutualism between ants and honeydew-producing Homoptera. Annu Rev Entomol 8:307–344
Wink M, Römer P (1986) Acquired toxicity-the advantages of specializing on alkaloid-rich lupins to Macrosiphon albifrons (Aphididae). Naturwissenschaften 73:210–212
Wink M, Witte L (1991) Storage of quinolizidine alkaloids in Macrosiphum albifrons and Aphis genistae (Homoptera: Aphididae). Entomol Gener 15:237–254
Wink M, Hartmann T, Witte L, Rheinheimer J (1982) Interrelationship between quinolizidine alkaloid producing legumes and infesting insects: Exploitation of the alkaloid-containing phloem sap of Cytisus scoparius by the Broom aphid (Aphis cytisorum). Z Naturforsch 37c:1081–1086
Witte L, Ehmke A, Hartmann T (1990) Interspecific flow of pyrrolizidine alkaloids. Naturwissenschaten 77:540–543
Zhu J, Cossé AA, Obrycki JJ, Boo KS, Baker TC (1999) Olfactory reactions of the twelve-spotted lady beetle, Coleomegilla maculata and the green lacewing, Chrysoperla carnea to semiochemicals released from their prey and host plant: electroantennogram and behavioural responses. J Chem Ecol 25:1163–1177
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Many thanks are due to H.J. Jacobson for correcting the English and for helpful discussion. J.L. Hemptinne and D. Daloze made valuable comments on the manuscript.
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Pasteels, J.M. Chemical defence, offence and alliance in ants–aphids–ladybirds relationships. Popul Ecol 49, 5–14 (2007). https://doi.org/10.1007/s10144-006-0023-3
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DOI: https://doi.org/10.1007/s10144-006-0023-3