Eur. J. Entomol. 100 (1): 1-10, 2003 | DOI: 10.14411/eje.2003.001
Searching and reproductive behaviour of female aphidophagous ladybirds (Coleoptera: Coccinellidae): a review
- Department of Biology, Utah State University, Logan, UT 84322-5305 USA; e-mail: ewevans@biology.usu.edu
In searching both for food to produce eggs and for suitable oviposition sites, females of aphidophagous ladybirds must be adapted to exploit prey that vary greatly in their occurrence and abundance over both space and time. A simple model of ladybird searching and oviposition behaviour emerged in the 1950s: adult ladybirds are highly mobile in traversing the landscape, but become less active and produce more eggs as their rate of aphid consumption increases. The net result is that most eggs tend to be laid at sites of high aphid density. Laboratory and field experiments and observations over the past several decades have generally supported this basic model, although the linkage between ladybird dispersal activity and local aphid density often appears to be relatively weak. Not all ladybird eggs are laid in patches of high aphid density. Females use resources from limited prey consumption to produce eggs in modest numbers. They may thus be prepared to lay some eggs quickly when they succeed in finding aphids in high numbers, but otherwise they may have little choice but to lay these eggs in suboptimal sites. Upon locating patches of high prey density, females are faced with the decision of how long to remain. The basic model raises the possibility that these females become passively trapped at such patches until local aphid density collapses. Recent studies, however, suggest that detection of oviposition-deterring pheromones may promote earlier departure from prey patches. Females may also have an innate tendency to disperse throughout their lives regardless of local conditions, as a bet-hedging strategy to spread their eggs widely over space. Additional studies are needed to evaluate further the degree to which females actively determine and vary the rhythms of dispersal and reproduction in response to the unpredictable and short-lived nature of populations of their aphid prey.
Keywords: Aphidophagy, bet-hedging, biological control, Coccinellidae, dispersal, foraging, oviposition, predation, reproductive strategy
Received: October 21, 2002; Revised: February 19, 2003; Accepted: February 19, 2003; Published: March 20, 2003 Show citation
References
- Acar E.B., Medina J.C., Lee M.L. & Booth G.M. 2001: Olfactory behavior of convergent lady beetles (Coleoptera: Coccinellidae) to alarm pheromone of green peach aphid (Hemiptera: Aphididae). Can. Entomol. 133: 389-397
Go to original source... - Agarwala B.K. & Dixon A.F.G. 1992: Laboratory study of cannibalism and interspecific predation in ladybirds. Ecol. Entomol. 17: 303-309
Go to original source... - Agarwala B.K. & Bardhanroy P. 1999: Numerical response of ladybird beetles (Col.: Coccinellidae) to aphid prey (Hom.: Aphididae) in a field bean in north-east India. J. Appl. Entomol. 123: 401-405
Go to original source... - Andow D.A. & Risch S.J. 1985: Predation in diversified agroecosystems: relations between a coccinellid predator Coleomegilla maculata and its food. J. Appl. Ecol. 22: 357-372
Go to original source... - Antolin M.F. & Strong D.R. 1987: Long-distance dispersal by a parasitoid (Anagrus delicatus, Mymaridae) and its host. Oecologia 73: 288-292
Go to original source... - Banks C.J. 1954: Random and non-random distributions of Coccinellidae. J. Soc. Brit. Entomol. 4: 211-215
- Banks C.J. 1955: An ecological study of Coccinellidae (Col.) associated with Aphis fabae Scop. on Vicia faba. Bull. Entomol. Res. 46: 561-587
Go to original source... - Banks C.J. 1956: The distribution of coccinellid egg batches and larvae in relation to numbers of Aphis fabae Scop. on Vicia faba. Bull. Entomol. Res. 47: 47-56
Go to original source... - Coderre D. 1999: L'utilisation des coccinelles aphidophages en lutte biologique. Ann. Soc. Entomol. Fr. (N.S.) 35 (Suppl.): 14-22
- Cottrell T.E. & Yeargan K.V. 1998a: Influence of a native weed, Acalypha ostryaefolia (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... - Curio E. 1976: The Ethology of Predation. Springer-Verlag, N.Y. Davidson W.M. 1924: Observations and experiments on the dispersion of the convergent lady-beetle (Hippodamia convergens Guerin) in California. Trans. Am. Entomol. Soc. 50: 163-175
- Delucchi V. 1954: Pullus impexus (Muls.) (Coleoptera: Coccinellidae), a predator of Adelges piceae (Ratz.) (Hemiptera: Adelgidae), with notes on its parasites. Bull. Entomol. Res. 45: 243-278
Go to original source... - Dingle H. 1972: Migration strategies of insects. Science 175: 1327-1335
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. 1970: Factors limiting the effectiveness of the coccinellid beetle, Adalia bipunctata (L.), as a predator of the sycamore aphid, Drepanosiphum platanoides (Schr.). J. Anim. Ecol. 39: 739-751
Go to original source... - Dixon A.F.G. 1997: Patch quality and fitness in predatory ladybirds. Ecological Studies: Analysis and Synthesis 130: 205-233
Go to original source... - Dixon A.F.G. 2000: Insect Predator-Prey Dynamics. Ladybird Beetles and Biological Control. Cambridge University Press, Cambridge, UK, 257 pp
- Dixon A.F.G. & Agarwala B.K. 1999: Ladybird-induced life-history changes in aphids. Proc. R. Soc. Lond. B 266: 1549-1553
Go to original source... - Dixon A.F.G. & Agarwala B.K. 2002: Triangular fecundity function and ageing in ladybird beetles. Ecol. Entomol. 27: 433-440
Go to original source... - 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... - Doutt R.L. 1964: Biological characteristics of entomophagous insects. In: DeBach P. (ed.): Biological Control of Insect Pests and Weeds. Reinhold Publishing, New York, pp. 145-167
- Duelli P. 1980: Adaptive dispersal and appetitive flight in the green lacewing, Chrysopa carnea. Ecol. Entomol. 5: 213-220
Go to original source... - Duelli P. 2001: Lacewings in field crops. In: McEwen P.K., New T.R. & Whittington A.E. (eds): Lacewings in the Crop Environments. Cambridge University Press, Cambridge, UK, pp. 158-171
Go to original source... - Elliott N.C., Kieckhefer R.W. & Beck D.A. 2000: Adult coccinellid activity and predation on aphids in spring cereals. Biol. Control 17: 218-226
Go to original source... - Evans E.W. 1982: Timing of reproduction by predatory stinkbugs (Hemiptera: Pentatomidae): patterns and consequences for a generalist and a specialist. Ecology 63: 147-158
Go to original source... - Evans E.W. 2000: Egg production in response to combined alternative foods by the predator Coccinella transversalis. Entomol. Exp. Appl. 94: 141-147
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... - Evans E.W., Stevenson A.T. & Richards D.R. 1999: Essential versus alternative foods of insect predators: benefits of a mixed diet. Oecologia 121: 107-112
Go to original source... - Evans E.W. & Youssef N.N. 1992: Numerical responses of aphid predators to varying prey density among Utah alfalfa fields. J. Kansas Entomol. Soc. 65: 30-38
- Ewert M.A. & Chiang H.C. 1966: Dispersal of three species of coccinellids in corn fields. Can. Entomol. 98: 999-1003
Go to original source... - Ferran A. & Dixon A.F.G. 1993: Foraging behaviour of ladybird larvae (Coleoptera: Coccinellidae). Eur. J. Entomol. 90: 383-402
- Frazer B.D. 1988: Coccinellidae. In: Minks A.K. & Harrewijn P. (eds): Aphids: their Biology, Natural Enemies and Control. Volume 2B. Elsevier, Amsterdam, pp. 231-247
- Frazer B.D. & Gilbert N. 1976: Coccinellids and aphids: a quantitative study of the impact of adult ladybirds (Coleoptera: Coccinellidae) preying on field populations of pea aphids (Homoptera: Aphididae). J. Entomol. Soc. Brit. Columbia 73: 33-56
- Frazer B.D., Gilbert N., Nealis V. & Raworth D.A. 1981: Control of aphid density by a complex of predators. Can. Entomol. 113: 1035-1041
Go to original source... - Frazer B.D. & Gill B. 1981: Hunger, movement, and predation of Coccinella californica on pea aphids in the laboratory and in the field. Can. Entomol. 113: 1025-1033
Go to original source... - Frazer B.D. & Raworth D.A. 1985: Sampling for adult coccinellids and their numerical response to strawberry aphids (Coleoptera: Coccinellidae; Homoptera: Aphididae). Can. Entomol. 117: 153-161
Go to original source... - Gordon R.D. 1985: The Coccinellidae (Coleoptera) of America north of Mexico. J. N.Y. Entomol. Soc. 93: 1-912
- Hagen K.S. 1962: Biology and ecology of predaceous Coccinellidae. Annu. Rev. Entomol. 7: 289-326
Go to original source... - Hagen K.S. 1987: Nutritional ecology of terrestrial insect predators. In: Slansky F. & Rodriquez J.G. (eds): Nutritional Ecology of Insects, Mites, Spiders and Related Invertebrates. John Wiley, N.Y., pp. 533-577
- Hazzard R.V. & Ferro D.N. 1991: Feeding responses of adult Coleomegilla maculata (Coleoptera: Coccinellidae) to eggs of the Colorado potato beetle (Coleoptera: Chrysomelidae) and green peach aphids (Homoptera: Aphididae). Envir. Entomol. 20: 644-651
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. & Lognay G. 1996: Searching behaviour and mate recognition by males of the two-spot ladybird beetle, Adalia bipunctata. Ecol. Entomol. 21: 165-170
Go to original source... - Hemptinne J.-L., Lognay G. & Dixon A.F.G. 1998: Mate recognition in the two-spot ladybird beetle, Adalia bipunctata: role of chemical and behavioural cues. J. Insect Physiol. 44: 1163-1171
Go to original source... - Hemptinne J.-L., Doumbia M. & Dixon A.F.G. 2000: Assessment of patch quality by ladybirds: role of aphid and plant phenology. J. Insect Behav. 13: 353-359
Go to original source... - Hodek I. 1973: Biology of Coccinellidae. Czechoslovak Academy of Science, Prague, 260 pp
Go to original source... - Hodek I. 1993: Habitat and food specificity in aphidophagous predators. Biocontrol Sci. Techn. 3: 91-100
Go to original source... - Hodek I. & Honek A. 1988: Sampling, rearing and handling of aphid predators. In: Minks A.K. & Harrewijn P. (eds): Aphids: their Biology, Natural Enemies and Control. Volume 2B. Elsevier, Amsterdam, pp. 311-321
- Hodek I. & Honek A. 1996: Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, The Netherlands, 464 pp
Go to original source... - Hodek I., Iperti G. & Hodkova M. 1993: Long-distance flights in Coccinellidae (Coleoptera). Eur. J. Entomol. 90: 403-414
- Honek A. 1978: Trophic regulation of postdiapause ovariole maturation in Coccinella septempunctata (Col.: Coccinellidae). Entomophaga 23: 213-216
Go to original source... - Honek A. 1980: Population density of aphids at the time of settling and ovariole maturation in Coccinella septempunctata (Col.: Coccinellidae). Entomophaga 25: 427-430
Go to original source... - Honek A. 1985: Activity and predation of Coccinella septempunctata adults in the field (Col.: Coccinellidae). Z. Ang. Entomol. 100: 399-409
Go to original source... - Honek A. 1990: Seasonal changes in flight activity of Coccinella septempunctata L. (Coleoptera: Coccinellidae). Acta Entomol. Bohemoslov. 87: 336-341
- Ives A.R., Kareiva P. & Perry R. 1993: Response of a predator to variation in prey density at three hierarchical scales: lady beetles feeding on aphids. Ecology 74: 1929-1938
Go to original source... - Ives P.M. 1981a: Estimation of coccinellid numbers and movement in the field. Can. Entomol. 113: 981-997
Go to original source... - Ives P.M. 1981b: Feeding and egg production of two species of coccinellids in the laboratory. Can. Entomol. 113: 999-1005
Go to original source... - Johnson C.G. 1969: Migration and Dispersal of Insects by Flight. Methuen, London, 763 pp
- 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 (Wiedemann), Metasyrphus frequens Matsumura and Syrphus vitripennis (Meigen) (Diptera: Syrphidae). J. Ethol. 6: 135-142
Go to original source... - Kan E. & Sasakawa M. 1986: Assessment of the maple aphid colony by the hover fly, Episyrphus balteatus (de Geer) (Diptera: Syrphidae) I. J. Ethol. 4: 121-127
Go to original source... - Kareiva P. 1987: Habitat fragmentation and the stability of predator-prey interactions. Nature 326: 388-390
Go to original source... - Kareiva P. & Odell G. 1987: Swarms of predators exhibit "preytaxis" if individual predators use area-restricted search. Am. Nat. 130: 233-270
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
- Kring T.J., Gilstrap F.E. & Michels G.J. Jr. 1985: Role of indigenous coccinellids in regulating greenbugs (Homoptera: Aphididae) on Texas grain sorghum. J. Econ. Entomol. 78: 269-273
Go to original source... - Lorenzetti F., Arnason J.T., Philogene B.J.R. & Hamilton R.L. 1997: Evidence for spatial niche partitioning in predaceous aphidophaga: use of plant colour as a cue. Entomophaga 42: 49-56
Go to original source... - Mills N.J. 1981: Some aspects of the rate of increase of a coccinellid. Ecol. Entomol. 6: 293-299
Go to original source... - Mills N.J. 1982: Voracity, cannibalism and coccinellid predation. Ann. Appl. Biol. 101: 144-148
- Minoretti N. & Weisser W.W. 2000: The impact of individual ladybirds (Coccinella septempunctata, Coleoptera: Coccinellidae) on aphid colonies. Eur. J. Entomol. 97: 475-479
Go to original source... - Mondor E.B. & Roitberg B.D. 2000: Has the attraction of predatory coccinellids to cornicle droplets constrained aphid alarm signaling behavior? J. Insect Behavior 13: 321-329
Go to original source... - Munyaneza J. & Obrycki J.J. 1997: Reproductive response of Coleomegilla maculata (Coleoptera: Coccinellidae) to Colorado potato beetle (Coleoptera: Chrysomelidae) eggs. Envir. Entomol. 26: 1270-1275
Go to original source... - Nakamuta K. 1982: Switchover in searching behavior of Coccinella septempunctata L. (Coleoptera: Coccinellidae) caused by prey consumption. Appl. Entomol. Zool. 17: 501-506
Go to original source... - Nakamuta K. 1987: Diel rhythmicity of prey-search activity and its predominance over starvation in the lady beetle, Coccinella septempunctata bruckii. Physiol. Entomol. 12: 91-98
Go to original source... - Nakamuta K. 1991: Aphid alarm pheromone component, (E)-B-farnesene, and local search by a predatory lady beetle, Coccinella septempunctata bruckii Mulsant (Coleoptera: Coccinellidae). Appl. Entomol. Zool. 26: 1-7
Go to original source... - Nedved O., Ceryngier P., Hodkova M. & Hodek I. 2001: Flight potential and oxygen uptake during early dormancy in Coccinella septempunctata. Entomol. Exp. Appl. 99: 371-380
Go to original source... - Obata S. 1986: Mechanisms of prey finding in the aphidophagous ladybird beetle, Harmonia axyridis (Col.: Coccinellidae). Entomophaga 31: 303-311
Go to original source... - Obrycki J.J. & Kring T.J. 1998: Predaceous Coccinellidae in biological control. Annu. Rev. Entomol. 43: 295-321
Go to original source... - Okuda T., Hodkova M. & Hodek I. 1986: Flight tendency in Coccinella spetempunctata in relation to changes in flight muscles, ovaries and corpus allatum. In: Hodek I. (ed.): Ecology of Aphidophaga, Proceedings of a Symposium held at Zvikovske Podhradi, September 2-8, 1984. Czechoslovak Academy of Sciences, Academia, Praha, pp. 217-223
- Osawa N. 1989: Sibling and non-sibling cannibalism by larvae of a lady beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in the field. Res. Popul. Ecol. 31: 153-160
Go to original source... - Osawa N. 2000: Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. Popul. Ecol. 42: 115-127
Go to original source... - Phoofolo M.W. & Obrycki J.J. 1997: Comparative prey suitability of Ostrinia nubilalis eggs and Acyrthosiphon pisum for Coleomegilla maculata. Biol. Contr. 9: 167-172
Go to original source... - Putman W.L. 1955: Bionomics of Stethorus punctillum Weise (Coleoptera: Coccinellidae) in Ontario. Can. Entomol. 87: 9-33
Go to original source... - Racioppi J.V., Burton R.L. & Eikenbary R. 1981: The effects of various oligidic synthetic diets on the growth of Hippodamia convergens. Entomol. Exp. Appl. 30: 68-72
Go to original source... - Rankin M.A. & Rankin S. 1980: Some factors affecting presumed migratory flight activity of the convergent ladybeetle, Hippodamia convergens (Coccinellidae: Coleoptera). Biol. Bull. 158: 356-369
Go to original source... - Richards D.R. & Evans E.W. 1998: Reproductive responses of aphidophagous lady beetles (Coleoptera: Coccinellidae) to non-aphid diets: an example from alfalfa. Ann. Entomol. Soc. Am. 91: 632-640
Go to original source... - Ruzicka Z. 1994: Oviposition-deterring pheromone in Chrysopa oculata (Neuroptera: Chrysopidae). Eur. J. Entomol. 91: 361-370
- Ruzicka Z. 1997: Recognition of oviposition-deterring allomones by aphidophagous predators (Neuroptera: Chrysopidae; Coleoptera: Coccinellidae). Eur. J. Entomol. 94: 431-434
- Ruzicka Z. 2001: 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. & Havelka J. 1998: Effects of oviposition-deterring pheromone and allomones on Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Eur. J. Entomol. 95: 211-216
- Sakuratani Y. & Nakamura Y. 1997: Oviposition strategies of Coccinella septempunctata (Col.: Coccinellidae). Entomophaga 42: 33-40
Go to original source... - Schanderl H., Ferran A. & Garcia V. 1988: L'elevage de deux coccinelles Harmonia axyridis et Semiadalia undecimnotata a l'aide d'oeufs d'Anagasta kuehniella tues aux rayons ultraviolets. Entomol. Exp. Appl. 49: 235-244
Go to original source... - Schellhorn N.A. & Andow D.A. 1999: Cannibalism and interspecific predation: role of oviposition behavior. Ecol. Appl. 9: 418-428
Go to original source... - Sloggett J.J. & Majerus M.E.N. 2000: Habitat preferences and diet in the predatory Coccinellidae (Coleoptera): an evolutionary perspective. Biol. J. Linn. Soc. 70: 63-88
Go to original source... - Takahashi K. 1989: Intra- and inter-specific predations of lady beetles in spring alfalfa fields. Jpn. J. Entomol. 57: 199-203
- Takahashi K. 1993: Daily behavior of adult Coccinella septempunctata brucki (Coleoptera: Coccinellidae). Jpn. J. Entomol. 61: 839-845
- van der Werf W., Evans E.W. & Powell J. 2000: Measuring and modelling the dispersal of Coccinella septempunctata (Coleoptera: Coccinellidae) in alfalfa fields. Eur. J. Entomol. 97: 487-493
Go to original source... - Weisser W.W., Braendle C. & Minoretti N. 1999: Predator-induced morphological shift in the pea aphid. Proc. R. Soc. Lond. B 266: 1173-1181
Go to original source... - Wetzler R.E. & Risch S.J. 1984: Experimental studies of beetle diffusion in simple and complex crop habitats. J. Anim. Ecol. 53: 1-19
Go to original source... - White C. & Eigenbrode S.D. 2000: Leaf surface waxbloom in Pisum sativum influences predation and intra-guild interactions involving two predator species. Oecologia 124: 252-259
Go to original source... - Wratten S.D. 1973: The effectiveness of the coccinellid beetle, Adalia bipunctata (L.), as a predator of the lime aphid, Eucallipterus tiliae L. J. Anim. Ecol. 42: 785-802
Go to original source... - Wright E.J. & Laing J.D. 1980: Numerical response of coccinellids to aphids in corn in southern Ontario. Can. Entomol. 112: 977-988
Go to original source... - Yasuda H. & Shinya K. 1997: Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Entomophaga 42: 153-163
Go to original source... - 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...
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.




