Eur. J. Entomol. 109 (3): 363-371, 2012
Effect of presence and semiochemicals of conspecific stages on oviposition by ladybirds (Coleoptera: Coccinellidae)
- Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Lucknow-226007, India
Reduced oviposition by ladybirds in the presence of tracks of fourth instar larvae owing to the presence of oviposition deterring pheromones is well established across many genera. However, deterrence, if any, by other life stages has not been well investigated, in particular the effect of conspecific presence. The present study investigates the effects of conspecific presence and semiochemicals of conspecific life stages (eggs, fourth instar larvae, pupae, adult males and females) on oviposition by five ladybird (Coleoptera: Coccinellidae) species, viz. Coccinella septempunctata, Coccinella transversalis, Cheilomenes sexmaculata, Propylea dissecta and Anegleis cardoni. Results reveal that the presence of life stages inhibits oviposition and the inhibition is density-dependent, although the degree of inhibition is species-specific. Surface semiochemicals of eggs and larval and adult tracks also show density-dependent inhibitory effects. Moreover, the semiochemicals in tracks (oviposition deterring pheromones) and egg surface semiochemicals are not similar, indicating semiochemical parsimony. Of all species tested, C. transversalis and C. septempunctata were the most and the least responsive to both conspecific presence and semiochemicals, respectively.
Keywords: Oviposition deterring pheromone, interference, Coleoptera, conspecific, Coccinellidae
Received: December 20, 2011; Revised: March 27, 2012; Accepted: March 27, 2012; Published: July 2, 2012 Show citation
References
- AGARWALA B.K. & DIXON A.F.G. 1991: Cannibalism and interspecific predation in ladybirds. In Polgar L., Chambers R.J., Dixon A.F.G. & Hodek I. (eds): Behaviour and Impact of Aphidophaga. SPB Academic Publishing, The Hague, pp. 95-102
- AGARWALA B.K. & DIXON A.F.G. 1993: Kin recognition: egg and larval cannibalism in Adalia bipunctata. Eur. J. Entomol. 90: 45-50
- AGARWALA B.K., YASUDA H. & KAJITA Y. 2003: Effect of conspecific and heterospecific feces on foraging and oviposition of two predatory ladybirds: Role of fecal cues in predator avoidance. J. Chem. Ecol. 29: 357-376
Go to original source... - AL ABASSIS S., BIRKETT M.A., PETTERSON J., PICKETT J.A. & WOODCOCK C.M. 1998: Ladybird beetle odour identified and found to be responsible for attraction between adults. Cell. Mol. Life Sci. 54: 876-879
Go to original source... - ALHMEDI A., HAUBRUGE E. & FRANCIS F. 2010: Identification of limonene as a potential kairomone of the harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae). Eur. J. Entomol. 107: 541-548
Go to original source... - BANKS C.J. 1956: Observations on the behaviour and mortality in Coccinellidae before dispersal from the eggshells. Proc. R. Soc. Lond. (A) 31: 56-61
Go to original source... - BIRKETT M.A., CAMPBELL C.A.M., CHAMBERLAIN K., GUERRIERI E., HICK A.J., MARTIN J.L., MATTHES M., NAPIER J.A., PETTERSSON J., PICKETT J.A., POPPY G.M., POW E.M., PYE B.J., SMART L.E., WADHAMS G.H., WADHAMS L.J. & WOODCOCK C.M. 2000: New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc. Natl. Acad. Sci. USA 97: 9329-9334
Go to original source... - CHAN F.Y. 1995: Etude des alcaloides de Adalia bipunctata (L.) en relation avec le comportement de l'insecte. MSc thesis. Faculte des Sciences Agronomiques, Gembloux, 71 pp
- COTTRELL T.E. 2004: Suitability of exotic and native lady beetle eggs (Coleoptera: Coccinellidae) for development of lady beetle larvae. Biol. Control 31: 362-371
Go to original source... - COTTRELL T.E. & YEARGAN K.V. 1998a: Influence of a native weed, Acalypha ostryifolia (Euphorbiaceae), on Coleomegilla maculata (Coleoptera: Coccinellidae) population density, predation, and cannibalism in sweet corn. Environ. Entomol. 27: 1375-1385
Go to original source... - COTTRELL T.E. & YEARGAN K.V. 1998b: Effect of pollen on Coleomegilla maculata (Coleoptera: Coccinellidae) population density, predation, and cannibalism in sweet corn. Environ. Entomol. 27: 1402-1410
Go to original source... - DIXON A.F.G. 1959: An experimental study of the searching behaviour of the predatory coccinellid beetle Adalia decempunctata (L.). J. Anim. Ecol. 28: 259-281
Go to original source... - DIXON A.F.G. 1997: Patch quality and fitness in predatory ladybirds. In Dettner P. (eds): Vertical Food Web Interactions. Springer, Heidelberg, pp. 205-222
Go to original source... - DIXON A.F.G. 2000: Insect Predator-Prey Dynamics: Ladybird Beetles and Biological Control. Cambridge University Press, Cambridge, 257 pp
- DOUMBIA M., HEMPTINNE J.L. & DIXON A.F.G. 1998: Assessment of patch quality by ladybirds: role of larval tracks. Oecologia 113: 197-202
Go to original source... - EVANS E.W. & DIXON A.F.G. 1986: Cues for oviposition by ladybird beetles (Coccinellidae): response to aphids. J. Anim. Ecol. 55: 1027-1034
Go to original source... - FLOWERS R.W., SALOM S.M. & KOK L.T. 2005: Competitive interactions among two specialists predators and a generalist predator of hemlock woolly adelgid, Adelges tsugae (Homoptera: Adelgidae), in the laboratory. Environ. Entomol. 34: 664-675
Go to original source... - FRECHETTE B., DIXON A.F.G., ALAUZET C. & HEMPTINNE J.L. 2004: Age and experience influence patch assessment for oviposition by an insect predator. Ecol. Entomol. 29: 578-583
Go to original source... - FRECHETTE B., DIXON A.F.G., ALAUZET C., BOUGHENOU N. & HEMPTINNE J.L. 2006: Should aphidophagous ladybirds be reluctant to lay eggs in the presence of unsuitable prey? Entomol. Exp. Appl. 118: 121-127
Go to original source... - HATANO E., KUNERT G., MICHAUD J.P. & WEISSER W.W. 2008: Chemical cues mediating aphid location by natural enemies. Eur. J. Entomol. 105: 797-806
Go to original source... - HEMPTINNE J.L. & DIXON A.F.G. 1991: Why ladybirds have generally been so ineffective in biological control? In Polgar L., Chambers R.J., Dixon A.F.G. & Hodek I. (eds): Behaviour and Impact of Aphidophaga. SPB Academic Publishing, The Hague, pp. 149-157
- HEMPTINNE J.L. & DIXON A.F.G. 2000: Defence, oviposition and sex: semiochemical parsimony in two species of ladybird beetles (Coleoptera: Coccinellidae)? A short review. Eur. J. Entomol. 97: 443-447
Go to original source... - HEMPTINNE J.L., DIXON A.F.G. & COFFIN J. 1992: Attack strategy of ladybird beetles (Coccinellidae): factors shaping their numerical response. Oecologia 90: 238-245
Go to original source... - HEMPTINNE J.L., DIXON A.F.G., DOEUCET J.L. & PETERSEN J.E. 1993: Optimal foraging by hoverflies (Diptera: Syrphidae) and ladybirds (Coleoptera: Coccinellidae): mechanisms. Eur. J. Entomol. 90: 451-455
- HEMPTINNE J.L., DOUMBIA M. & DIXON A.F.G. 2000a: Assessment of patch quality by ladybirds: role of aphid and plant phenology. J. Insect Behav. 13: 353-359
Go to original source... - HEMPTINNE J.L., DIXON A.F.G. & GAUTHIER C. 2000b: Nutritive cost of intraguild predation on eggs of Coccinella septempunctata and Adalia bipunctata (Coleoptera: Coccinellidae). Eur. J. Entomol. 97: 559-562
Go to original source... - HEMPTINNE J.L., LOGNAY G., GAUTHIER C. & DIXON A.F.G. 2000c: Role of surface chemical signals in egg cannibalism and intraguild predation in ladybirds (Coleoptera: Coccinellidae). Chemoecology 10: 123-128
Go to original source... - HEMPTINNE J.L., LOGNAY G., DOUMBIA M. & DIXON A.F.G. 2001: Chemical nature and persistence of the oviposition deterring pheromone in the tracks of the two spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Chemoecology 11: 43-47
Go to original source... - HILKER M. & MEINERS T. 2002: Chemoecology of Insect Eggs and Egg Deposition. Blackwell, Berlin, 410 pp
Go to original source... - HOLMES H.B. 1972: Genetic evidence for fewer progeny and higher percent males when Nasonia vitripennis oviposits in previously parasitized hosts. Entomophaga 17: 79-88
Go to original source... - JACKSON D.J. 1966: Observations on the biology of Craphractus cinctus Walker (Hymenoptera: Mymaridae), a parasitoid of the eggs of Dytiscidae (Coleoptera). Trans. R. Entomol. Soc. Lond. 118: 23-49
Go to original source... - KAJITA Y., YASUDA H. & EVANS E.W. 2006: Effects of native ladybirds on oviposition of the exotic species, Adalia bipunctata (Coleoptera: Coccinellidae), in Japan. Appl. Entomol. Zool. 41: 57-61
Go to original source... - KAN E. 1988a: Assessment of aphid colonies by hoverflies. I. Maple aphids and Episyrphus balteatus (De Geer) (Diptera: Syrphidae). J. Ethol. 6: 39-48
Go to original source... - KAN E. 1988b: Assessment of aphid colonies by hoverflies. II. Pea aphids and 3 syrphid species: Betasyrphus serarius (Wiedeman), Metasyrphus frequens Matsumara and Syrphus vitripennis (Meigen). J. Ethol. 6: 135-142
Go to original source... - KAN E. & SASAKAWA M. 1986: Assessment of the maple aphid colony by the hoverfly, Episyrphus balteatus (De Geer) (Diptera: Syrphidae). J. Ethol. 4: 121-127
Go to original source... - KAZANA E.T., POPE W., TIBBLES L., BRIDGES M., PICKETT J.A., BONES A.M., POWELL G. & ROSSITER J.T. 2007: The cabbage aphid: a walking mustard oil bomb. Proc. R. Soc. Lond. (B) 274: 2271-2277
Go to original source... - KINDLMANN P. & DIXON A.F.G. 1993: Optimal foraging in ladybird beetles (Coleoptera: Coccinellidae) and its consequences for their use in biological control. Eur. J. Entomol. 90: 443-450
- KLEWER N., RUzICKA Z. & SCHULZ S. 2007: (Z)-Pentacos-12-ene, an oviposition deterring pheromone of Cheilomenes sexmaculata. J. Chem. Ecol. 33: 2167-2170
Go to original source... - KOSAKI A. & YAMAOKA R. 1996: Chemical composition of footprints and cuticular lipids of three species of lady beetles. Jpn. J. Appl. Entomol. Zool. 40: 47-53
Go to original source... - LAUBERTIE E., MARTINI X., CADENA C., TREILHOU M., DIXON A.F.G. & HEMPTINNE J.L. 2006: The immediate source of the oviposition-deterring pheromone produced by larvae of Adalia bipunctata (L.) (Coleoptera: Coccinellidae). J. Insect Behav. 19: 231-240
Go to original source... - MAGRO A., TENE J.N., BASTIN N., DIXON A.F.G. & HEMPTINNE J.L. 2007: Assessment of patch quality by ladybirds: relative response to conspecific and heterospecific larval tracks a consequence of habitat similarity? Chemoecology 17: 37-45
Go to original source... - MAGRO A., DUCAMP C., RAMON-PORTUGAL F., LECOMPTE E., CROUAU-ROY B., DIXON A.F.G. & HEMPTINNE J.L. 2010: Oviposition deterring infochemicals in ladybirds: the role of phylogeny. Evol. Ecol. 24: 251-271
Go to original source... - MAJERUS M.E.N. 1994: Ladybirds. Harper Collins, London, 367 pp
- MARPLES N.M., BRAKEFIELD P.M. & COWIE R.J. 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
Go to original source... - MARTINI X., HACCOU P., OLIVIERI I. & HEMPTINNE J.L. 2009: Evolution of cannibalism and female's response to ovipositiondeterring pheromone in aphidophagous predators. J. Anim. Ecol. 78: 964-972
Go to original source... - MEISNER M.H., HARMON J.P. & ANTHONY R.I. 2011: Response of coccinellid larvae to conspecific and heterospecific larval tracks: a mechanism that reduces cannibalism and intraguild predation. Environ. Entomol. 40: 103-110
Go to original source... - MICHAUD J.P. & JYOTI J.L. 2007: Repellency of conspecific and heterospecific larval residues to Hippodamia convergens (Coleoptera: Coccinellidae) ovipositing on sorghum plants. Eur. J. Entomol. 104: 399-405
Go to original source... - MICHAUD J.P. & MACKAUER M. 1995: The oviposition behavior of Monoctonus paulensis (Ashmead) (Hymenoptera: Aphidiidae): Factors influencing reproductive allocation to hosts and host patches. Ann. Entomol. Soc. Am. 88: 220-226
Go to original source... - MILLS N.J. 1982: Voracity, cannibalism and coccinellid predation. Ann. Appl. Biol. 10: 144-148
- MISHRA G. & OMKAR 2006: Conspecific interference by adults in an aphidophagous ladybird Propylea dissecta (Coleoptera: Coccinellidae): effect on reproduction. Bull. Entomol. Res. 96: 407-412
Go to original source... - MOSER S.E., HAYNES K.F. & OBRYCKI J.J. 2010: Behavioral response to larval tracks and the influence of tracks on intraguild scavenging by coccinellid larvae. J. Insect Behav. 23: 45-58
Go to original source... - NAKASHIMA Y., BIRKETT M.A., PYE B.J., PICKETT J.A. & 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
Go to original source... - OLIVER T.H., TIMMS J.E.L., TAYLOR A. & LEATHER S.R. 2006: Oviposition responses to patch quality in the larch ladybird Aphidecta obliterata (Coleoptera: Coccinellidae): effects of aphid density, and con- and heterospecific tracks. Bull. Entomol. Res. 96: 25-34
Go to original source... - OMKAR, PERVEZ A. & GUPTA A.K. 2004: Role of surface chemicals in egg cannibalism and intraguild predation by neonates of two co-occurring aphidophagous ladybirds, Propylea dissecta and Coccinella transversalis. J. Appl. Entomol Zool. 128: 691-695
Go to original source... - PASTEELS J.M., DALOZE D. & ROWELL-RAHIER M. 1986: Chemical defense in chrysomelid eggs and neonate larvae. Physiol. Entomol. 11: 29-37
Go to original source... - PASTEELS J.M., DEROE C., TRUSCH B., BRECKMAN J.C., DALOZE D. & HOOTELE C. 1973: Distribution des alcaloides defensifs des Coccinellidae. J. Insect Physiol. 19: 1771-1784
Go to original source... - PETTERSSON J.A., QUIROZ A., STEPHANSSON D. & NIEMEYER H. 1995: Odour communication of Rhopalosiphum padi on grasses. Entomol. Exp. Appl. 76: 325-328
Go to original source... - PETTERSSON J., NINKOVIC V., GLINWOOD R., BIRKETT M.A. & PICKETT J.A. 2005: Foraging in a complex environment - semiochemicals support searching behaviour of the seven spot ladybird. Eur. J. Entomol 102: 365-370
Go to original source... - PETTERSSON J., NINKOVIC V., GLINWOOD R., AL ABASSI S., BIRKETT M.A., PICKETT J.A. & WADHAMS L. 2008: Chemical stimuli supporting foraging behaviour of Coccinella septempunctata L. (Coleoptera: Coccinellidae): volatiles and allelobiosis. Appl. Entomol. Zool. 43: 315-321.
Go to original source... - QUIROZ A., PETTERSSON J., PICKETT J.A., WADHAMS L. & NIEMEYER H.M. 1997: Key compounds in a spacing pheromone in the bird cherry-oat aphid, Rhopalosiphum padi (L.) (Hemiptera, Aphididae). J. Chem. Ecol. 23: 2599-2607
Go to original source... - RUzICKA Z. 1997: Recognition of oviposition-deterring allomones by aphidophagous predators (Neuroptera: Chrysopidae, Coleoptera: Coccinellidae). Eur. J. Entomol. 94: 431-434
- RUzICKA Z. 2001a: Oviposition responses of aphidophagous coccinellids to tracks of ladybird (Coleoptera: Coccinellidae) and lacewing (Neuroptera: Chrysopidae) larvae. Eur. J. Entomol. 98: 183-188
Go to original source... - RUzICKA Z. 2001b: Response of chrysopids (Neuroptera) to larval tracks of aphidophagous coccinellids (Coleoptera). Eur. J. Entomol. 98: 283-285
Go to original source... - RUzICKA Z. 2002: Persistance of deterrent larval tracks in Coccinella septempunctata, Cycloneda limbifer and Semiadalia undecimnotata (Coleoptera: Coccinellidae). Eur. J. Entomol. 99: 471-475
Go to original source... - RUzICKA Z. 2003: Perception of oviposition-deterring larval tracks in aphidophagous coccinellids Cycloneda limbifer and Ceratomegilla undecimnotata (Coleoptera: Coccinellidae). Eur. J. Entomol. 100: 345-350
Go to original source... - RUzICKA Z. 2006: Oviposition-deterring effects of conspecific and heterospecific larval tracks on Cheilomenes sexmaculata (Coleoptera: Coccinellidae). Eur. J. Entomol. 103: 757-763
Go to original source... - 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: 155-159
Go to original source... - SEAGRAVES M.P. 2009: Lady beetle oviposition behavior in response to the trophic environment. Biol. Control 51: 313-322
Go to original source... - SOARES A.O. & SERPA A. 2006: Interference competition between ladybird beetle adults (Coleoptera: Coccinellidae): effects on growth and reproductive capacity. Popul. Ecol. 49: 37-43
Go to original source... - VIKTOROV G.A. 1968: The influence of the population density upon the sex ratio in Trissolcus grandis Thoms. (Hymenoptera: Scelionidae). Zool. Zh. 47: 1035-1039
- WIEDEMANN R., WOODRING J., VOLKL W. & HOFFMANN K.H. 2004: Amino acid composition of honeydew from aphid species feeding on tansy, Tanacetum vulgare. Mitt. Dt. Ges. Allgem. Angew. Entomol. 14: 459-462
- YASUDA H., TAKAGI T. & KOGI K. 2000: Effects of conspecific and heterospecific larval tracks on the oviposition behaviour of the predatory ladybird, Harmonia axyridis (Coleoptera: Coccinellidae). Eur. J. Entomol. 97: 551-553
Go to original source... - ZHU J., COSSE A.A., OBRYCKI J.J., BOO K.S. & BAKER T.C. 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
Go to original source... - ZHU J. & PARK K.C. 2005: Methyl salicylate, a soybean aphidinduced plant volatile attractive to the predator Coccinella septempunctata. J. Chem. Ecol. 31: 1733-1746
Go to original source...
This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.




