Lady beetles; Mating behavior; Sexual communication; Sex pheromone; Semiochemicals; Integrated Pest Management
Abstract :
[en] Chemical signals are involved in the courtship behavior of many invertebrate and vertebrate species. Lady beetles are no exception to this rule; a significant number of published reports highlight the role of cuticular chemicals involved in the reproduction of lady beetles, including gender recognition. Recent data have also demonstrated the presence of a volatile female sex pheromone that facilitates male attraction in some species. Here, we present a synthetic overview of the current knowledge about the sexual behavior of lady beetles and associated chemicals for which the function and identification have been provided. Because lady beetles are often reared as biological control agents, the chemical cues involved in their sexual behavior could be used as components in integrated management approaches against soft-bodied hemipterans. In conclusion, this review provides new perspectives and potential developments for sustainable insect management mainly based on the semiochemicals involved in the sexual behavior of lady beetles. A better understanding of these chemical signals would help maximize their presence in areas where their predatory behavior is requested, as a result of the application of formulations inducing behavioral manipulation.
Disciplines :
Entomology & pest control
Author, co-author :
Fassotte, Bérénice ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Entomologie fonctionnelle et évolutive
Francis, Frédéric ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Entomologie fonctionnelle et évolutive
Verheggen, François ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Entomologie fonctionnelle et évolutive
Language :
English
Title :
The scent of love: how important are semiochemicals in the sexual behavior of lady beetles?
Arn H, Louis F (1997) Mating disruption in European vineyards. In: Cardé RT, Minks AK (eds) Pheromone Research, new directions. Chapman and Hall, New York, pp 377–382
Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164. doi:10.1006/anbe.2000.1446
Baker TC, Obrycki JJ, Zhu J (2003) Attractants of beneficial insects. US Patent 6562332, issued 2003
Barbier R, Ferran A, Le Lannic J, Allo MR (1992) Morphology and ultrastructure of integumentary glands of Semiadalia undecimnotata Schn. (Coleoptera: Coccinellidae). Int J Insect Morphol Embryol 21:223–234. doi:10.1016/0020-7322(92)90018-I
Bayoumy MH, Michaud JP (2014) Female fertility in Hippodamia convergens (Coleoptera: Coccinellidae) is maximized by polyandry, but reduced by continued male presence. Eur J Entomol 111:513–520. doi:10.14411/eje.2014.067
Bind RB (2007) Reproductive behaviour of a generalist aphidophagous ladybird beetle Cheilomenes sexmaculata (Coleoptera: Coccinellidae). Int J Trop Insect Sci 27:78–84
Brakefield PM, Willmer PG (1985) The basis of thermal melanism in the ladybird Adalia bipunctata: differences in reflectance and thermal properties between the morphs. Heredity 54:9–14. doi:10.1038/hdy.1985.3
Cardé RT, Haynes KF (2004) Structure of the pheromone communication channel in moths. In: Cardé RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 283–332
Chi DF, Wang GL, Liu JW, Wu QY, Zhu YP (2009) Antennal morphology and sensilla of Asian multicolored ladybird beetles, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Entomol News 120:137–152. doi:10.3157/021.120.0203
De Jong PW, Verhoog MD, Brakefield PM (1993) Sperm competition and melanic polymorphism in the 2-spot ladybird, Adalia bipunctata (Coleoptera, Coccinellidae). Heredity 70:172–178. doi:10.1038/hdy.1993.26
De Jong PW, Brakefield PM, Geerinck BP (1998) The effect of female mating history on sperm precedence in the two-spot ladybird, Adalia bipunctata (Coleoptera, Coccinellidae). Behav Ecol 9:559–565
Dixon AFG (2000) Basic Biology and Structure. In: Dixon AFG (ed) Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, New York, pp 6–35
Durieux D, Verheggen FJ, Vandereycken A, Joie E, Haubruge E (2010) Synthèse bibliographique: l’écologie chimique des coccinelles. Biotechnol Agron Soc Environ 14:351–367
Durieux D, Fischer C, Brostaux Y, Sloggett JJ, Deneubourg J-L, Vandereycken A, Joie E, Wathelet J-P, Lognay G, Haubruge E, Verheggen FJ (2012) Role of long-chain hydrocarbons in the aggregation behaviour of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). J Insect Physiol 58:801–807. doi:10.1016/j.jinsphys.2012.03.006
Durieux D, Fassotte B, Vanderplanck M, Deneubourg J-L, Fischer C, Lognay G, Haubruge E, Verheggen FJ (2013) Substrate marking by an invasive ladybeetle: seasonal changes in hydrocarbon composition and behavioral responses. Plos One 8:e61124. doi:10.1371/journal.pone.0061124
Fassotte B, Fischer C, Durieux D, Lognay G, Haubruge E, Francis F, Verheggen FJ (2014) First evidence of a volatile sex pheromone in lady beetles. Plos One 9:e115011. doi:10.1371/journal.pone.0115011
Fisher T (1959) Occurrence of spermatophore in certain species of Chilocorus. Pan-Pac Entomol 35:205–208
Ginzel M, Hanks L (2003) Contact pheromones as mate recognition cues of four species of longhorned beetles (Coleoptera: Cerambycidae). J Insect Behav 16:181–187. doi:10.1023/A:1023911701159
Haddrill PR, Shuker DM, Mayes S, Majerus ME (2007) Temporal effects of multiple mating on components of fitness in the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Eur J Entomol 104:393–398. doi:10.14411/eje.2007.058
Haddrill PR, Shuker DM, Amos W, Majerus MEN, Mayes S (2008) Female multiple mating in wild and laboratory populations of the two-spot ladybird, Adalia bipunctata. Mol Ecol 17:3189–3197. doi:10.1111/j.1365-294X.2008.03812.x
Harmon JP, Hayden A, Andow DA (2008) Absence makes the heart grow fonder: isolation enhances the frequency of mating in Coleomegilla maculata (Coleoptera: Coccinellidae). J Insect Behav 21:495–504. doi:10.1007/s10905-008-9145-0
Hemptinne J-L, Dixon AFG, Lognay G (1996) Searching behaviour and mate recognition by males of the two-spot ladybird beetle, Adalia bipunctata. Ecol Entomol 21:165–170. doi:10.1111/j.1365-2311.1996.tb01183.x
Hemptinne J-L, Lognay G, Dixon AFG (1998) Mate recognition in the two-spot ladybird beetle, Adalia bipunctata: role of chemical and behavioural cues. J Insect Physiol 44:1163–1171. doi:10.1016/S0022-1910(98)00081-X
Hemptinne J-L, Dixon A, Adam B (2001a) Do males and females of the two-spot ladybird, Adalia bipunctata (L.), differ in when they mature sexually? J Insect Behav 14:411–419
Hemptinne J-L, Lognay G, Doumbia M, Dixon AFG (2001b) 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 11:43–47. doi:10.1007/PL00001831
Heuskin S, Verheggen FJ, Haubruge E, Wathelet J-P, Lognay G (2011) The use of semiochemical slow-release devices in integrated pest management strategies. Biotechnol Agron Soc Environ 15:459–470
Hodek I (2012) Diapause/Dormancy. In: Hodek I, van Emdem HF, Honěk A (eds) Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). Blackwell Publishing Ltd, Chichester, pp 275–342
Hodek I, Ceryngier P (2000) Sexual activity in Coccinellidae (Coleoptera): a review. Eur J Entomol 97:449–456. doi:10.14411/eje.2000.069
Hodek I, Landa V (1971) Anatomical and histological changes during dormancy in two Coccinellidae. Entomophaga 16:239–251
Honěk A, Martinková Z, Pekár S (2005) Temporal stability of morph frequency in central European populations of Adalia bipunctata and A. decempunctata (Coleoptera: Coccinellidae). Eur J Entomol 102:437–442. doi:10.14411/eje.2005.062
Howard RW (1993) Cuticular hydrocarbons and chemical communication. In: Stanley-Samuelson DW, Nelson DR (eds) Insect lipids: chemistry, biochemistry and biology. University of Nebraska Press, Lincoln, pp 179–226
Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393. doi:10.1146/annurev.ento.50.071803.130359
Howard RW, Pérez-Lachaud G, Lachaud JP (2001) Cuticular hydrocarbons of Kapala sulcifacies (Hymenoptera: Eucharitidae) and its host, the ponerine ant Ectatomma ruidum (Hymenoptera: Formicidae). Ann Entomol Soc Am 94:707–716
Ioriatti C, Lucchi A, Bagnoli B (2008) Grape areawide pest management in Italy. In: Koul O, Cuperus G, Elliott G (eds) Areawide pest managements: theory and implementation. CAB International, Wallingford, pp 208–225
Jourdan H, Barbier R, Bernard J, Ferran A (1995) Antennal sensilla and sexual dimorphism of the adult ladybird beetle Semiadalia undecimnotata Schn. (Coleoptera: Coccinellidae). Int J Insect Morphol Embryol 24:307–322. doi:10.1016/0020-7322(95)98584-Z
Kumar M, Chakraborty N (1997) Biology of Scymnus nubilus Mulsant (Coleoptera: Coccinellidae), a native predator of pink mealy bug, Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae). J Entomol Res 21:329–334
Magro A, Ducamp C, Ramon-Portugal F, Lecompte E, Crouau-Roy B, Dixon A, Hemptinne J-L (2010) Oviposition deterring infochemicals in ladybirds: the role of phylogeny. Evol Ecol 24:251–271. doi:10.1007/s10682-009-9304-6
Maisin N, Hassan S, Hussein M, Sajap A (1997) Mating behaviour of Menochilus sexmaculatus Fabr. (Coleoptera: Coccinellidae). Malays Appl Biol 26:57–62
Majerus MEN (1994a) Female promiscuity maintains high fertility in ladybirds (Col., Coccinellidae). Entomol Mon Mag 130:205–209
Majerus MEN (1994b) Ladybirds. Harper Collins Publishers, London
Majerus MEN (1999) Spotting the darker side of ladybirds. Biologist 46:109–114
Majerus M, O’Donald P, Weir J (1982) Evidence for preferential mating in Adalia bipunctata. Heredity 49:37–49. doi:10.1038/hdy.1982.63
Michaud JP, Bista M, Mishra G, Omkar (2013) Sexual activity diminishes male virility in two Coccinella species: consequences for female fertility and progeny development. Bull Entomol Res 103:570–577. doi:10.1017/S0007485313000199
Muggleton J (1979) Non-random mating in wild populations of polymorphic Adalia bipunctata. Heredity 42:57–65. doi:10.1038/hdy.1979.6
Nakashima Y, Birkett MA, Pye BJ, Powell W (2006) Chemically mediated intraguild predator avoidance by aphid parasitoids: interspecific variability in sensitivity to semiochemical trails of ladybird predators. J Chem Ecol 32:1989–1998. doi:10.1007/s10886-006-9123-y
Nedvěd O, Honěk A (2012) Life history and development. In: Hodek I, van Emdem HF, Honěk A (eds) Ecology and Behaviour of the Ladybird Beetles (Coccinellidae). Blackwell Publishing Ltd, Chichester UK, pp 54–109
Nelson DR, Carlson DA (1986) Cuticular hydrocarbons of the tsetse flies Glossina morsitans morsitans, G. austeni and G. pallidipes. Insect Biochem 16:403–416. doi:10.1016/0020-1790(86)90054-5
Obata S (1987) Mating behavior and sperm transfer in the ladybird beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Appl Entomol Zool 22:434–442
Obata S (1988) Mating refusal and its significance in females of the ladybird beetle, Harmonia axyridis. Physiol Entomol 13:193–199
Obata S (1997) The influence of aphids on the behaviour of adults of the ladybird beetle, Harmonia axyridis (Col.: Coccinellidae). Entomophaga 42:103–106. doi:10.1007/bf02769885
Obata S, Hidaka T (1987) Ejection and ingestion of the spermatophore by the female ladybird beetle, Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Can Entomol 119:603–604
Obata S, Johki Y (1991) Comparative study on copulatory behaviour in four species of aphidophagous ladybirds. In: Proceedings of the 4th meeting of the IOBC WG ecology of aphidophaga, pp 207–212
O’Donald P, Muggleton J (1979) Melanic polymorphism in ladybirds maintained by sexual selection. Heredity 143–148
Omkar, Srivastava S (2002) The reproductive behaviour of an aphidophagous ladybeetle, Coccinella septempunctata (Coleoptera: Coccinellidae). Eur J Entomol 99:465–470. doi:10.14411/eje.2002.060
Omkar (2004) Reproductive behaviour of two aphidophagous ladybeetles, Cheilomenes sexmaculata and Coccinella transversalis. Entomol Sin 11:113–124
Omkar, James BE (2005) Reproductive behaviour of an aphidophagous ladybeetle Coccinella transversalis (Coleoptera: Coccinellidae). Int J Trop Insect Sci 25:96–102
Omkar, Mishra G (2005a) Evolutionary significance of promiscuity in an aphidophagous ladybird, Propylea dissecta (Coleoptera: Coccinellidae). Bull Entomol Res 95:527–533. doi:10.1079/BER2005386
Omkar, Mishra G (2005b) Mating in aphidophagous ladybirds: costs and benefits. J Appl Entomol 129:432–436. doi:10.1111/j.1439-0418.2005.00996.x
Omkar, Pervez A (2005) Mating behavior of an aphidophagous ladybird beetle, Propylea dissecta (Mulsant). Insect Sci 12:37–44. doi:10.1111/j.1744-7917.2005.00006.x
Omkar, Sahu J, Kumar G (2013) Age specific mating incidence and reproductive behavior of the ladybird beetle, Anegleis cardoni (Weise) (Coleoptera: Coccinellidae). J Asia Pac Entomol 16:263–268. doi:10.1016/j.aspen.2013.03.003
Omkar, Singh SK, Pervez A (2006) Influence of mating duration on fecundity and fertility in two aphidophagous ladybirds. J Appl Entomol 130:103–107. doi:10.1111/j.1439-0418.2005.01029.x
Omkar, Singh SK, Mishra G (2010) Multiple matings affect the reproductive performance of the aphidophagous ladybird beetle, Coelophora saucia (Coleoptera: Coccinellidae). Eur J Entomol 107:177–182. doi:10.14411/eje.2010.023
Osawa N (1994) The occurrence of multiple mating in a wild population of the ladybird beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae). J Ethol 12:63–66. doi:10.1007/BF02350081
Osawa N, Nishida T (1992) Seasonal variation in elytral colour polymorphism in Harmonia axyridis (the ladybird beetle): the role of non-random mating. Heredity 69:297–307
Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567. doi:10.1111/j.1469-185X.1970.tb01176.x
Pattanayak R, Mishra G, Omkar, Chanotiya CS, Rout PK, Mohanty CS (2014) Does the volatile hydrocarbon profile differ between the sexes: a case study on five aphidophagous ladybirds. Arch Insect Biochem Physiol 87:105–125. doi:10.1002/arch.21184
Perry JC, Rowe L (2008) Neither mating rate nor spermatophore feeding influences longevity in a ladybird beetle. Ethology 114:504–511. doi:10.1111/j.1439-0310.2008.01499.x
Perry JC, Tse CT (2013) Extreme costs of mating for male two-spot ladybird beetles. Plos One 8:e81934. doi:10.1371/journal.pone.0081934
Perry JC, Sharpe DMT, Rowe L (2009) Condition-dependent female remating resistance generates sexual selection on male size in a ladybird beetle. Anim Behav 77:743–748. doi:10.1016/j.anbehav.2008.12.013
Pervez A, Maurice N (2011) Mate choice and polyandry benefit reproduction and progeny fitness in the ladybird Hippodamia variegata (Goeze). Eur J Environ Sci 1:19–23
Pervez A, Omkar, Richmond AS (2004) The influence of age on reproductive performance of the predatory ladybird beetle, Propylea dissecta. J Insect Sci 4:22–29. doi:10.1093/jis/4.1.22
Pervez A, Omkar (2011) Ecology of aphidophagous ladybird Propylea species: a review. J Asia Pac Entomol 14:357–365. doi:10.1016/j.aspen.2011.01.001
Pervez A, Singh SK (2013) Mating patterns in the aphidophagous ladybird, Hippodamia variegata, depend on body size. Eur J Environ Sci 3:109–112
Pettersson J (2012) Coccinellids and Semiochemicals. In: Hodek I, van Emdem HF, Honek A (eds) Ecology and behaviour of the ladybird beetles (Coccinellidae). Blackwell Publishing Ltd, Chichester, pp 444–464
Putman WL (1955) Bionomics of Stethorus punctillum Weise (Coleoptera: Coccinellidae) in Ontario. Can Entomol 87:9–33
Rawat R, Modi B (1969) Studies on Nephus regularis (Coleoptera: Coccinellidae) as a predator of the striped mealybug in Madhya Pradesh (India). Ann Entomol Soc Am 62:953–956. doi:10.1093/aesa/62.5.953
Richards AM (1980) Sexual selection, guarding and sexual conflict in a species of Coccinellidae (Coleoptera). Aust J Entomol 19:26. doi:10.1111/j.1440-6055.1980.tb00956.x
Ridley M (1989) The incidence of sperm displacement in insects: four conjectures, one corroboration. Biol J Linn Soc 38:349–367. doi:10.1111/j.1095-8312.1989.tb01582.x
Rodstein J, McElfresh JS, Barbour J, Ray A, Hanks L, Millar J (2009) Identification and synthesis of a female-produced sex pheromone for the Cerambycid beetle Prionus Californicus. J Chem Ecol 35:590–600. doi:10.1007/s10886-009-9623-7
Schaller M, Nentwig W (2000) Olfactory orientation of the seven-spot ladybird beetle, Coccinella septempunctata (Coleoptera: Coccinellidae): attraction of adults to plants and conspecific females. Eur J Entomol 97:155–160. doi:10.14411/eje.2000.029
Sengonca C, Liu B (1994) Responses of the different instar predator, Coccinella septempunctata L. (Coleoptera: Coccinellidae), to the kairomones produced by the prey and non-prey insects as well as the predator itself. Z Pflanzenkr Pflanzenschutz 101:173–177
Seo MJ, Kim GH, Youn YN (2008) Differences in biological and behavioural characteristics of Harmonia axyridis (Coleoptera: Coccinellidae) according to colour patterns of elytra. J Appl Entomol 132:239–247. doi:10.1111/j.1439-0418.2007.01241.x
Shuker DM (2014) Sexual selection theory. In: Shuker DM, Simmons LW (eds) The evolution of insect mating systems. Oxford University Press, New York, pp 20–41
Sloggett JJ, Magro A, Verheggen FJ, Hemptinne J-L, Hutchison WD, Riddick EW (2011) The chemical ecology of Harmonia axyridis. Biocontrol 56:643–661. doi:10.1007/s10526-011-9376-4
Smart LE, Aradottir GI, Bruce TJA (2014) Role of semiochemicals in integrated pest management. In: Abrol DP (ed) Integrated pest management, current concepts and ecological perspectives. Academic Press, San Diego, pp 93–109
Srivastava S, Omkar (2005) Mate choice and reproductive success of two morphs of the seven spotted ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae). Eur J Entomol 102:189–194. doi:10.14411/eje.2005.030
Stewart LA, Dixon AFG (1989) Why big species of ladybird beetles are not melanic. Funct Ecol 3:165–171. doi:10.2307/2389297
Susset E, Ramon-Portugal F, Hemptinne J-L, Dewhirst S, Birkett M, Magro A (2013) The role of semiochemicals in short-range location of aggregation sites in Adalia bipunctata (Coleoptera, Coccinellidae). J Chem Ecol 39:591–601. doi:10.1007/s10886-013-0285-0
True JR (2003) Insect melanism: the molecules matter. Trends Ecol Evol 18:640–647. doi:10.1016/j.tree.2003.09.006
Ueno H (1996) Estimate of multiple insemination in a natural population of Harmonia axyridis. Appl Entomol Zool 31:621–623. doi:10.1303/aez.31.621
Ueno H, Sato Y, Tsuchida K (1998) Colour-associated mating success in a polymorphic ladybird beetle, Harmonia axyridis. Funct Ecol 12:757–761. doi:10.1046/j.1365-2435.1998.00245.x
Varner M, Lucin R, Mattedi L, Forno F (2001) Experience with mating disruption technique to control grape berry moth, Lobesia botrana, in Trentino. IOBC WPRS Bull 24:81–88
Waldner W (1997) Three years of large-scale control of codling moth by mating disruption in the South Tyrol, Italy. IOBC WPRS Bull 20:35–44
Wang S, Michaud JP, Zhang R, Zhang F, Liu S (2009) Seasonal cycles of assortative mating and reproductive behaviour in polymorphic populations of Harmonia axyridis in China. Ecol Entomol 34:483–494. doi:10.1111/j.1365-2311.2008.01075.x
Wheeler C, Cardé R (2014) Following in their footprints: cuticular hydrocarbons as overwintering aggregation site markers in Hippodamia convergens. J Chem Ecol 40:418–428. doi:10.1007/s10886-014-0409-1
Witzgall P, Kirsch P, Cork A (2010) Sex pheromones and their impact on pest management. J Chem Ecol 36:80–100. doi:10.1007/s10886-009-9737-y
Zhu J, Cossé A, Obrycki J, Boo K, Baker T (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 behavioral responses. J Chem Ecol 25:1163–1177. doi:10.1023/a:1020846212465