Ladybird Mothers Mitigate Offspring Starvation Risk by Laying Trophic Eggs

Behav Ecol Sociobiol (2005) 58: 578–586 DOI 10.1007/s00265-005-0947-1 ORIGINAL ARTICLE Jennifer C. Perry · Bernard D. Roitberg Ladybird mothers mitigate offspring starvation risk by laying trophic eggs Received: 5 October 2004 / Revised: 24 January 2005 / Accepted: 19 March 2005 / Published online: 1 June 2005 C Springer-Verlag 2005 Abstract A large proportion of ladybird beetle Keywords Coccinellidae . Harmonia axyridis . Hatching (Coleoptera: Coccinellidae) eggs are apparently infertile— synchrony . Sibling cannibalism . Trophic eggs they do not develop an embryo and are consumed by larvae hatching within the egg batch. The predicted benefits of egg consumption for larvae are empirically well supported. An important question, however, remains: are these eggs Introduction a maternal strategy to feed offspring (i.e., trophic eggs) or did egg eating evolve to exploit unavoidably infertile eggs? Parents in many species face the problem of high star- We investigated the adaptive value of infertile eggs in lab- vation risk for their offspring. Furthermore, some parents oratory experiments with multicoloured Asian ladybirds (e.g., most insects) do not interact with their offspring fol- (Harmonia axyridis). Female H. axyridis were assigned to lowing oviposition; hence mothers in this situation are lim- low and high resource environments for brief intervals; we ited to starvation-reduction behaviors that are expressed predicted that tactics to facilitate egg cannibalism, such as at the egg production or deposition stage. In the extreme infertile egg production and hatching asynchrony, would case, a mother’s best option might be to provide food be adopted in low food environments in which starvation for offspring in the form of eggs themselves (Alexander risk for offspring is greater. We conducted two experiments 1974; Mock and Forbes 1995). Mothers should sacrifice in this manner that provided females with information some offspring to others when they gain more offspring about resource levels through prey feeding or scent. We from the increased survival of the cannibals than they also observed female oviposition patterns and tested for lose as victims (Crespi 1992)—thus, when offspring star- infertile egg distributions that departed from random. vation risk is high and eating a sibling provides a large Females produced 56% more infertile eggs in the low vs. benefit. the high food treatment; however, hatching synchrony did One way for mothers to ensure that offspring have a not change. We consider a potential confound between sibling to eat is to produce ‘trophic’ offspring that serve information and nutrition state unlikely because ladybirds as a meal (Alexander 1974). This hypothesis provides a are well able to tolerate low food for 24 h, the duration of foundation for the study of trophic eggs—non-developing, trials, and because females were in good condition when ovariole-produced structures that are formed to feed trials began. Results suggest that ladybirds use information offspring (Crespi 1992). In studying hypothesized trophic from prey encounter to manipulate the proportion of eggs, then, it is necessary to ask the functional question: is trophic eggs in a manner consistent with the adaptive there an adaptive maternal strategy to feed offspring? The hypothesis, the first evidence of trophic egg plasticity in a alternative hypothesis is that some infertile eggs are un- non-eusocial insect. avoidably produced through some constraint (e.g., sperm limitation), and that offspring are adapted to consume Communicated by M. Elgar such eggs. In some taxa, the adaptive nature of trophic J. C. Perry () · B. D. Roitberg eggs seems clear; for example, when they have a unique Behavioural Ecology Research Group, Department of morphology, clearly different from viable eggs (e.g., Biological Sciences, Simon Fraser University, West and Alexander 1963; Henry 1972), or when parents Burnaby, British Columbia V5A 1S6, Canada actively feed them to offspring (e.g., Nakahira 1994; e-mail: [email protected] Heying 2001). In ladybird beetles, offspring consume J. C. Perry undifferentiated, apparently infertile eggs that occur within Department of Zoology, University of Toronto, their natal egg batch (e.g., Kawai 1978;Osawa1992). For Toronto, ON M5S 3G5, Canada ladybirds and similar taxa (e.g., Valerio 1977; Frechette 579 and Coderre 2000), the adaptive nature of trophic eggs optimize their contribution to sibling survival. Thus, we ex- must be empirically investigated. amined the spatial distribution and order of oviposition of A second way for mothers to sacrifice some offspring infertile eggs, suggesting that a uniform distribution indi- to others is to manipulate hatching synchrony (O’Connor cates adaptive production (e.g., if it maximizes the chance 1978; Forbes et al. 2002). If cannibalism is directed to- that cannibals attack an infertile egg first rather than a viable wards siblings still in the defenceless egg stage, as in many offspring). insects (e.g., Branquart et al. 1997;Via1999; Sigsgaard et al. 2002), then mothers can decrease hatching synchrony in low-food environments to allow early-hatching offspring Methods to cannibalize (otherwise viable) siblings. For example, mothers might alter hatching synchrony by staggering the Study system and experimental animals rate of egg development or by creating eggs that vary in mass (and, hence, development time). Mothers in some Harmonia axyridis is an aphidophagous ladybird beetle, insect [e.g., lacewings (Frechette and Coderre 2000)] native to Asia. It was introduced to parts of North America and bird [e.g., American kestrels (Wiebe and Bortolotti for the biological control of aphid pests, and is now the 1994)] species appear to manipulate hatching synchrony dominant coccinellid in many areas (Koch 2003). After to facilitate sibling cannibalism. overwintering, females emerge in the spring and lay One way to investigate whether mothers adaptively use clusters of eggs on plants infested with prey (aphids or these two provisioning strategies—trophic eggs and hatch similar phloem-feeding insects, Koch 2003). Females synchrony adjustment—is to test whether they are adjusted produce a clutch of 10–50 eggs every 1–2 days for their to offspring starvation risk (Frechette and Coderre 2000), adult lives of 1–3 months. Larvae progress through four which determines the benefit of sibling cannibalism from a instars in 3–5 weeks. Several generations per summer are mother’s perspective. The multicolored Asian lady beetle usually possible (Koch 2003). Harmonia axyridis is a good candidate species for examin- Harmonia axyridis and other ladybirds produce three ing flexible use of the behaviors for several reasons. First, types of eggs: apparently infertile eggs, viable eggs, and females produce many apparently infertile eggs (15.2%, ‘inviable’ eggs where a larva develops but does not emerge Kawai 1978; 24.5%, Osawa 1992) that are consumed by from the egg capsule (Ng 1986). In this study, we investi- larvae hatching in the same egg batch. Second, first instar gate the trophic function of infertile eggs, excluding in- larvae face a high starvation risk due to oviposition sites viable eggs because some embryo development occurs. that are some distance from aphid prey (Majerus 1994) and Larvae are soft-bodied upon emergence. After a period their poor predatory abilities (Hodek and Honek 1996). Fur- of quiescence (mean: 141 min; 95% CI: 126–155; N=76; thermore, egg cannibalism dramatically reduces the risk of unpublished data) following hatching, they are sclerotized starvation in H. axyridis (up to 226%, Osawa 1992, see also enough to consume any unhatched eggs in the natal clutch. Kawai 1978) and other ladybirds (reviewed by Hodek and Egg-eating larvae apparently do not discriminate between Honek 1996). Finally, female ladybirds frequently disperse viable and infertile or inviable eggs (Banks 1956;Brown to new sites between bouts of egg laying (Evans 2003) 1972;Osawa1992). Other unhatched eggs are normally and are thus likely to deposit offspring at sites that vary in hatched or consumed by the time a cannibal is ready to resource availability. Therefore, female ladybirds should eat a second egg. Larvae remain at the egg batch for about be selected to use plastic strategies to mitigate offspring 24 h, then disperse in search of aphid prey (Osawa 1989). starvation risk. Newly eclosed adult H. axyridis were obtained from Two possibilities, then, are that the infertile eggs of H. Applied Bionomics (Victoria, British Columbia, Canada). axyridis are trophic offspring adaptively designed to be Females were maintained individually in petri dishes and eaten (Osawa 2003); or that sibling cannibalism behav- supplied daily with an excess of pea aphids (Acyrthosiphon ior takes advantage of an available food source. We also pisum reared on broad bean, Vicia faba) and a water source. looked for evidence that females use hatching synchrony They were mated to males from laboratory colonies every to alter the opportunity for sibling cannibalism among off- 10 days. spring. We hypothesized that if the behaviors are plastic, female ladybirds would lay clutches with fewer trophic eggs and more synchronous hatching when food resources Resource level experiments for offspring were high, and more trophic eggs and less synchronous hatching in low food environments. We con- The goal of these experiments was to test the hypothesis ducted two experiments to test the hypotheses that differed that ladybirds would increase trophic egg production

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