A N I M A L B E H A V I O R B U L L E T I N
Feature article from Volume 3, Number 2 (April 1998)
The Functional Response to Increases in Aphid Density in Female Two-spotted Lady Beetles, Adalia bipunctata
By John P. Roche
Figure: A lady beetle. Photo by Gilles San Martin from Namur, Belgium (Coccinella magnifica) [CC BY-SA 2.0 (http://creativecommons.org/licenses/by-sa/2.0)].
The foraging behavior of lady beetles (Family Coccinellidae), or what are often called "ladybird beetles" or "ladybugs," has been utilized by farmers throughout the world to reduce crop losses to plant pests such as aphids. Aphids are small insects that cause damage by sucking sap from crop plants. Aphids reproduce extremely rapidly (an estimated 600 billion aphids can be produced in nine generations), so their potential to reduce agricultural yields is prodigious. Lady beetles, however, are voracious predators on aphids and other pests such as scale insects and larval Colorado potato beetles. Their appetite for aphids, along with their ability to survive periods when aphids are not present by eating pollen and nectar, their ability to reproduce rapidly, and the fact that they themselves generally do not damage crops, make them extremely effective and economically-beneficial biological control agents. Lady beetles, of which there are more than 350 species in North America and approximately 4,000 species in the world, save U. S. farmers millions of dollars per year. No wonder they are said to bring good luck! What is it about their life cycle and foraging behavior that makes lady beetles so effective as biological control agents?
One factor that contributes to lady beetles ability to control aphid populations is that both larval and adult lady beetles consume prey (Ives et al. 1993; Hodek 1973). In the spring adult lady beetles mate and then adult females lay eggs. Each female can lay up to 1,000 eggs over the course of the spring. Larvae, which with their series of segmented plates look like tiny trilobites, begin eating right after hatching and may each eat up to 1,000 aphids in the several weeks before pupation. After molting through four larval instars, the larvae pupate into adults, which then begin again to consume aphids. As adults, each lady beetle may eat up to 4,000 or 5,000 aphids. With the onset of winter, adult lady beetles congregate in protected overwintering sites such as under leaf litter, under fallen trees, under rocks, or in buildings. Once spring returns, the adults mate and reinitiate the cycle.
Two other factors that allow lady beetles to control aphid populations are that the beetles display a "numerical response" to increases in aphid densities (Wright and Laing 1980), and a "functional response" to such increases (Hemptinne et al. 1996). A predator population is said to display a numerical response when the number of predators increases as a result of an increase in the number of its prey. A predator displays a functional response when each individual predator consumes more prey items per unit time when prey items are more abundant (Holling 1959). The lady beetles' high reproductive potential allows them to display a numerical response to increases in aphid densities; when more food is available more eggs can be laid and more larva and adults survive. That lady beetles can consume more prey items per predator at higher prey densities (i.e., display a functional response) is in part a result of the simple fact that with more prey items in the environment, it is easier for the beetles to find aphids. This functional response may be further magnified by the lady beetles' ability to adjust their searching behavior in response to localized differences in prey density; i.e., by their ability to exhibit facultatively what is called "area-restricted search" (see Tinbergen et al. 1967; Dawkins 1971; Timberlake 1990, 1991, 1993; Bell 1991).
When animals exhibit area-restricted search, they search localized areas of their environment exhaustively. Lady beetles, along with many species of invertebrates and vertebrates, switch into area-restricted search when they detect high prey densities, densities that often occur as concentrated clumps of prey or "prey patches." This ability to switch into area-restricted search in areas of high prey density tends to concentrate lady beetles in areas dense with aphids (Kareiva and Odell 1987). Area-restricted search also increases the beetles' efficiency at catching aphids. These patterns contribute to the observed functional response and in turn facilitate the survival of the beetles and the elimination of the aphids (see Hemptinne and Hough-Goldstein 1994).
Individual lady beetles eat tremendous numbers of aphids, lady beetles increase in number when aphid populations increase, and lady beetles increase their predation rate per beetle in response to increases in aphids. Do males and females contribute equally to this consumption and control of aphids? Females have higher energy demands placed on them because they produce eggs, which are energetically expensive. Therefore, females require, and consume, more aphids per day than males. For example, adult female convergent lady beetles ( Hippodamia convergens ) eat as many as 75 aphids per day, whereas the males eat a maximum of only 40. In addition, Hemptinne et al. (1996), in an experimental study of two-spotted lady beetles ( Adalia bipunctata ) predating on pea aphids ( Acyrthosiphon pisum ), found that at intermediate and high aphid densities, females ate more aphids per day than males. Hemptinne et al. also observed that the way in which increases in aphid density influence foraging behavior, and rate of aphid consumption, varies between males and females. They discovered that whereas males exhibited a weak functional response when aphid density was increased, females exhibited a pronounced functional response. For example, when the aphid density was one aphid/day/150cm 2, both males and females ate about one aphid per day. When the aphid density was 20 aphids/day/150cm 2, however, females ate around eight aphids per day but males ate approximately two.
If male two-spotted lady beetles show a much less pronounced functional response when faced with increases in aphid abundance than males, why is this? One reason may be that, as mentioned previously, males, which do not produce eggs, have lower energetic needs than females, and they require less food. A second reason is that with increases in aphid abundance, females devote a higher proportion of their search time to area-restricted search, whereas males do not increase their proportion of search time in area-restricted search at high prey densities (Hemptinne et al. 1996). Females increase their foraging efficiency at high prey densities by exhibiting more area-restricted search. Why don't we see such a pattern in male two-spotted lady beetles?
Although the energy needs of males are not as high as females, males might be expected to enjoy increased fitness by capturing their daily food requirement in less time (see Schoener 1971). The reason that males do not increase their area-restricted search for prey at high prey densities, and thus do not exhibit a pronounced functional response, appears to be that they are focusing on a currency with an even more powerful influence on fitness than food: mates. While females are working hard searching for aphids, males are working hard searching for females (Hemptinne et al. 1996). Whereas males do not increase the proportion of their search time spent in area-restricted search when aphid density increases, males do change their movement pattern in response to encounters with females; after detecting a female via a contact pheromone, males enter an area-restricted search state (Hemptinne and Dixon 1996).
The finding that female two-spotted lady beetles increase the number of aphids they eat per day at higher prey densities, while males do not, is a fascinating and important result. The beetles of Hemptinne et al. were reared and observed in a lab with a 16:8 Light:Dark cycle. Thus, we do not yet know the extent of male female differences in the functional response to increases in aphid concentrations in wild two-spotted lady beetles or how these patterns may change in the course of the crop-growing season. For example, once the beetles have mated, will the males spend more time foraging and perhaps display more of a functional response when aphid densities increase? Another important question that needs to be explored is the following: To what extent are the patterns observed in the two-spotted lady beetle in the study of Hemptinne et al. observed in other species of lady beetles?
The differences in foraging behavior observed between males and females in Hemptinne et al.'s study may also have implications for the design of integrated pest management programs that employ lady beetles for biological control. Hemptinne et al.'s findings show that female lady beetles of this species, and perhaps other species, are primarily responsible for the functional response to increases in aphid densities and that they therefore contribute more to the biological control of aphids than males. Thus, studies on the behavior and ecology of lady beetles need to take male-female differences into account to make accurate predictions about the effectiveness of specific lady beetle introduction or fostering programs accurately.
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(Reprinted from the Animal Behavior Bulletin, Center for the Integrative Study of Animal Behavior, Indiana University.)