Egg and time limitation mediate an egg protection strategy

The number of mature eggs remaining in the ovaries and the time left for oviposition determine the reproductive decisions of the hyperdiverse guild of insects that require discrete and potentially limiting resources for oviposition (such as seeds, fruits or other insects). A female may run out of eggs before all available oviposition sites are used (egg limitation), or die before using all of her eggs (time limitation). Females are predicted to change clutch size depending on whether eggs or time is the limiting resource. We extend this framework and ask whether the same constraints influence a strategy in which females modify eggs into protective shields. In response to egg parasitism cues, female seed beetles (Mimosestes amicus) lay eggs in vertical groups of 2–4, modifying the top 1–3 eggs into shields in order to protect the bottom egg from attack by parasitoids. We made contrasting predictions of how egg and time limitation would influence egg size and the incidence and level of egg protection. By varying access to seed pods, we manipulated the number of remaining eggs a female had at the time she received a parasitism cue. Although egg size was not affected, our results confirm that egg‐limited females protected fewer eggs and time‐limited females protected more eggs. Female body size explained the number of eggs in a stack rather than host deprivation or the timing of parasitoid exposure. Our results clearly show that host availability relative to female age influences the incidence of egg protection in M. amicus. Furthermore, our study represents a novel use of life history theory to explain patterns in an unusual but compelling defensive behaviour.     

Stochasticity in reproductive opportunity and the evolution of egg limitation in insects

Is reproduction by adult female insects limited by the finite time available to locate hosts (time limitation) or by the finite supply of eggs (egg limitation)? An influential model predicted that stochasticity in reproductive opportunity favors elevated fecundity, rendering egg limitation sufficiently rare that its importance would be greatly diminished. Here, I use models to explore how stochasticity shapes fecundity, the likelihood of egg limitation, and the ecological importance of egg limitation. The models make three predictions. First, whereas spatially stochastic environments favor increased fecundity, temporally stochastic environments favor increases, decreases, or intermediate maxima in fecundity, depending on egg costs. Second, even when spatially or temporally stochastic environments favor life histories with less‐frequent egg limitation, stochasticity still increases the proportion of all eggs laid in the population that is laid by females destined to become egg limited. This counterintuitive result is explained by noting that stochasticity concentrates reproduction in the hands of a few females that are likely to become egg limited. Third, spatially or temporally stochastic environments amplify the constraints imposed by time and eggs on total reproduction by the population. I conclude that both egg and time constraints are fundamental in shaping insect reproductive behavior and population dynamics in stochastic environments.     

Egg maturation strategy and survival trade-offs in holometabolous insects: a comparative approach

One of the key predictions of general life-history theory is that reproduction incurs a survival cost. Although there is a convincing body of evidence to support this prediction at the intraspecific level in insects, evidence at the interspecific level is relatively scarce, as is the case for other animals. By employing two methods of phylogenetically controlled analysis, we demonstrate the existence of a negative correlation between life-span and early life investment in reproduction, across a wide diversity of Lepidoptera. The measure of initial reproductive effort used was the 'ovigeny index', defined as the proportion of the lifetime potential egg complement that is mature (ready to lay) upon female emergence. We present a graphical model for holometabolous insects, illustrating the trade-offs that are hypothesized to occur among capital resources (soma vs non-soma and initial eggs vs storage) in relation to variation in ovigeny index. These trade-offs, for which there is some empirical support, are postulated to underlie the life-span/ovigeny index relationship observed in the Lepidoptera and also in other insect orders.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 293–302.     

Egg resorption behaviour by the solitary egg parasitoid Anaphes nitens under natural conditions

We investigated under outdoor conditions and inside a climate chamber: (i) whether Anaphes nitens Girault (Hymenoptera: Mymaridae), an egg parasitoid of the Eucalyptus snout beetle, Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae), experienced egg resorption, and (ii) how various treatments (location, food, and/or host supply) and body size influenced egg load, egg resorption, fecundity, and longevity. One‐day‐old females were mated and randomly assigned to five groups: (A) honey + hosts, (B) water + hosts, (C) only honey, (D) only water, and (E) control females killed at emergence. We compared the egg load of the newly emerged females, which represent the control group (egg load = ovarian eggs present at emergence), with the lifetime egg load (i.e., ovarian eggs + emerged offspring + not emerged offspring) of the females with various host and diet treatments, by dissection of the ovaries to find evidence of egg resorption. All groups reared outdoors had fewer eggs than the control, while indoors there was no significant difference. Outdoors, starved but host‐provided wasps (B) experienced the highest reduction of the lifetime egg load (51%). Groups without access to food (B + D) resorbed more eggs than groups provided with honey (A + C). Females with honey and hosts (A) had the highest lifetime fecundity, but those with water and hosts (B) showed a higher daily realized fecundity. Host‐deprived females with access to food (C) attained the longest lifespan. Our results suggest that under stress conditions, such as low temperature and food shortage, A. nitens females practice egg resorption, probably to save energy.     

Egg load dynamics and the risk of egg and time limitation experienced by an aphid parasitoid in the field

Insect parasitoids and herbivores must balance the risk of egg limitation and time limitation in order to maximize reproductive success. Egg and time limitation are mediated by oviposition and egg maturation rates as well as by starvation risk and other determinants of adult lifespan. Here, we assessed egg load and nutritional state in the soybean aphid parasitoid Binodoxys communis under field conditions to estimate its risk of becoming either egg‐ or time‐limited. The majority of female B. communis showed no signs of egg limitation. Experimental field manipulations of B. communis females suggested that an average of 4–8 eggs were matured per hour over the course of a day. Regardless, egg loads remained constant over the course of the day at approximately 80 eggs, suggesting that egg maturation compensates for oviposition. This is the first case of such “egg load buffering” documented for a parasitoid in the field. Despite this buffering, egg loads dropped slightly with increasing host (aphid) density. This suggests that egg limitation could occur at very high host densities as experienced in outbreak years in some locations in the Midwestern USA. Biochemical analyses of sugar profiles showed that parasitoids fed upon sugar in the field at a remarkably high rate. Time limitation through starvation thus seems to be very low and aphid honeydew is most likely a source of dietary sugar for these parasitoids. This latter supposition is supported by the fact that body sugar levels increase with host (aphid) density. Together, these results suggest that fecundity of B. communis benefits from both dynamic egg maturation strategies and sugar‐feeding.     

The timing of egg maturation in insects: ovigeny index and initial egg load as measures of fitness and of resource allocation

Both the ovigeny index (OI) – defined as the proportion of the potential lifetime complement of eggs that is mature upon female emergence, and egg load – defined as the number of mature eggs carried by a female at a given moment in her lifetime, have been identified as significant fitness variables in insects. In discussions of egg maturation strategies initial egg load (IEL) and OI are often considered together, and they have been assumed to be strongly correlated. The purpose of this review is: (i) to summarise what is known about variation in OI and IEL both in relation to one another and in relation to other fitness variables (notably life-span and body size), (ii) to assess the merits of OI and IEL as measures of resource allocation to reproduction, and (iii) to contrast knowledge of the mechanisms underlying cross-species variation in these two variables with what is known concerning the mechanisms underlying intraspecific variation. Our review concentrates upon parasitoid wasps because most information on OI and IEL has been obtained for these animals, but most of the issues we address are pertinent to other insects, at least holometabolous ones. We conclude that, despite certain limitations, OI is, for insect evolutionary ecology, more useful than IEL for two reasons: (i) OI is a true measure of the degree to which lifetime egg production is concentrated into the early phase of adult life, (ii) the observed intraspecific and interspecific declines in OI with increasing body size are consistent with theoretical predictions concerning body size-related changes in reproductive effort (when the proportional change in the allocation to reproduction is considered), whereas the intraspecific alteration in IEL is not (iii) OI is a measure of the relative extent of resource allocation between the juvenile and the adult stages of the female. Lastly, we discuss the possible application of OI to insect population dynamics and management.     

Time limitation, egg limitation, the cost of oviposition, and lifetime reproduction by an insect in nature

For more than 80 years, ecologists have debated whether reproduction by female insect herbivores and parasitoids is constrained by the time needed to find hosts (time limitation) or by the finite supply of mature eggs (egg limitation). Here we present the first direct measures of permanent time limitation and egg limitation and their influences on the cost of oviposition and lifetime reproduction for an insect in nature. We studied the gall midge Rhopalomyia californica, which neither matures nor resorbs eggs during the adult stage. By sampling females soon after their death and correcting for predation effects, we demonstrate that females lay a large proportion of their total complement of eggs (multiyear mean: 82.9%). The egg supplies of 17.1% of females were completely exhausted, with the remaining 82.9% of females being time limited. As predicted by theory, we estimate that even though egg limitation is a minority condition within the population, egg costs make a substantial contribution (57% of the total) to the cost of oviposition. We conclude that insect life histories evolve to produce a balanced risk of time and egg limitation and, therefore, that both of these constraining factors have important influences on insect oviposition behavior and population dynamics.     

Distention-mediated egg maturation in the mosquito,Aedes aegypti

Abdominal distention accelerates the release of a factor from the head of blood-fed Aedes aegypti mosquitoes. The critical period during which the head is required for oögenesis following blood ingestion is approx 6 h with a 5 μl meal, but small blood meals of 1 μl require the head to be present for significantly longer. Increasing the abdominal distention by supplementing the 1 μl meal with saline results in a critical period similar to that with 5 μl of blood. The information from the distended abdomen appears to travel via the ventral nerve cord. Transection of the ventral nerve cord prevents oögenesis from occurring after small blood meals, but not with larger blood volumes. Topical application of 100 pg of juvenile hormone III can substitute for the distention message.     

Periodicity, persistence, and collapse in host-parasitoid systems with egg limitation

There is an emerging consensus that parasitoids are limited by the number of eggs which they can lay as well as the amount of time they can search for their hosts. Since egg limitation tends to destabilize host-parasitoid dynamics, successful control of insect pests by parasitoids requires additional stabilizing mechanisms such as heterogeneity in the distribution of parasitoid attacks and host density-dependence. To better understand how egg limitation, search limitation, heterogeneity in parasitoid attacks, and host density-dependence influence host-parasitoid dynamics, discrete time models accounting for these factors are analyzed. When parasitoids are purely egg-limited, a complete anaylsis of the host-parasitoid dynamics are possible. The analysis implies that the parasitoid can invade the host system only if the parasitoid's intrinsic fitness exceeds the host's intrinsic fitness. When the parasitoid can invade, there is a critical threshold, CV*>1, of the coefficient of variation (CV) of the distribution of parasitoid attacks that determines that outcome of the invasion. If parasitoid attacks sufficiently aggregated (i.e., CV>CV*), then the host and parasitoid coexist. Typically (in a topological sense), this coexistence is shown to occur about a periodic attractor or a stable equilibrium. If the parasitoid attacks are sufficiently random (i.e. CV1. When CV<1, the parasitoid exhibits highly oscillatory dynamics. Alternatively, when parasitoid attacks are sufficiently aggregated but not overly aggregated (i.e. CV>1 but close to 1), the host and parasitoid coexist about a stable equilibrium with low host densities. The implications of these results for classical biological control are discussed.     

Egg components, egg size, and hatchling size in leatherback turtles

Relationships between egg size, egg components, and neonate size have been investigated across a wide range of oviparous taxa. Differences in egg traits among taxa reflect not only phylogenetic differences, but also interactions between biotic (i.e., maternal resource allocation) and abiotic (i.e. nest environment conditions) factors. We examined relationships between egg mass, egg composition, and hatchling size in leatherback turtles (Dermochelys coriacea) because of the unique egg and reproductive characteristics of this species and of sea turtles in general. Albumen comprised 63.0%+/-2.8% (mean+/-S.D.) of egg mass and explained most of the variation in egg mass, whereas yolk comprised only 33.0%+/-2.7%. Additionally, leatherback albumen dry mass was approximately 16% of albumen wet mass. Whereas hatchling mass increased significantly with egg mass (n = 218 clutches), hatchling mass increased by only approximately 2 g for each 10 g increase in egg mass and was approximately 10-20 g greater than yolk mass. Taken together, our results indicate that albumen might play a particularly significant role in leatherback embryonic development, and that leatherback eggs are both capable of water uptake from the nest substrate and also possess a large reservoir of water in the albumen. Relationships between egg mass and egg components, such as variation in egg mass being largely explained by variation in albumen mass and egg mass containing a relatively high proportion of albumen solids, are more similar to bird eggs than to eggs of other non-avian reptiles. However, hatchling mass correlates more with yolk mass than with albumen mass, unlike patterns observed in bird eggs of similar composition.     

Egg size, egg composition and reproductive success in the Oystercatcher Haematopus ostralegus

We investigated the relationship between egg size and composition and their subsequent effects on hatching and fledging success in Eurasian Oystercatchers Haematopus ostralegus on the island of Schiermonnikoog (53̀30'N, 06̀10'E) in the Dutch Wadden Sea between 1986 and 1990. Egg size variation was considerable. The ratio in egg volume of the largest over the smallest egg was more than 1.5 in each of five years. Differences between females accounted for, on average, 61% of the total variance of egg volume. Individual females produced similarly sized eggs from one year to another. Nevertheless, average egg volume per clutch declined by 0.2 cm³ per year as females aged, but this explains little of the observed variation. Female size and food supplementation had no significant effect on egg volume. In absolute terms, large eggs contain more lean dry matter and lipid than small eggs, but the proportion of both constituents decreases with egg size. Consequently, the combustible energy content of eggs increases less than proportionally with egg size. Hatchability averaged 87% and was not correlated with egg volume. Hatchling weight increased with egg size, averaging 65% of fresh egg weight. Chick survival until fledging did not increase with egg volume. Consequently, within the size range observed, large and small eggs are of comparable quality. Since both the costs and benefits of large eggs compared with small eggs seem small at best, we propose that, within the size range encountered in this population, egg size can be considered an evolutionarily neutral trait.     

The dynamics of egg production, oviposition and resorption in a parasitoid wasp

1. The extent to which parasitoid wasps are limited by their egg supply is very important in understanding their reproductive strategies. Egg reserves are dynamic, with most wasps maturing new eggs throughout their life (synovigeny) and many species resorbing eggs that are not used in oviposition. We investigated the extent to which a parasitoid modulates its egg reserves in the light of its experience in finding hosts.
2. The egg dynamics of the Encyrtid Wasp Leptomastix dactylopii , a solitary parasitoid of mealybugs, were studied in the laboratory. This species is synovigenic and practises egg resorption.
3. We allowed newly emerged wasps to experience one of four environments of increasing value in terms of reproductive opportunities. We proposed that wasps that experienced good quality environments would maintain more mature eggs ready for oviposition. Dissection of wasps subject to different periods of host deprivation after the experimental treatment failed to confirm the hypothesis: egg load was independent of experience.
4. We also proposed that any adjustment of egg supply to make up for eggs oviposited would be effected through a reduction in egg resorption. Instead, we found that the wasp quickly made up for eggs oviposited by increased egg production.     

Effects of time limitation and egg limitation on lifetime reproductive success of a parasitoid in the field

We used field observations of freely foraging Aphytis aonidiae parasitoids in conjunction with results of laboratory studies of A. aonidiae and other Aphytis species to simulate lifetime patterns of behavior and reproduction. Field observations provided estimates of encounter rates with three classes of hosts, the mortality rate from predation on adult parasitoids, and host-handling times for oviposition and host feeding by adult wasps. A series of physiological parameters, including the egg maturation rate and the value of host-feeding meals, were estimated from previously published studies. Plasticity in parasitoid behavior was incorporated in two ways. For one set of simulations we used a behavioral rule derived empirically from observations of parasitoids made in the field, and for another we used a dynamic state-variable model to generate a set of behavioral rules that maximize lifetime reproductive success. As was expected, the empirically derived rule led to better matches with field observations than did simulations using the output of the dynamic model. Projections of lifetime reproductive success in the field ranged between three and 37 eggs within the 95% confidence intervals of the mortality rate and host encounter rate and depending on which behavioral rule was used. Lifetime reproductive success from the simulation with central estimates of the mortality and host encounter rates that incorporated the empirical rule was 6.25 eggs. Using the empirical versus the theoretical rule in the simulations led to a 10%-30% decline in projections of lifetime reproductive success, depending on mortality and host encounter rates. Regardless of the behavioral rule, the simulations underscored the observation that the host encounter rate was greater than the egg maturation rate. The overall oviposition rate was sufficiently high to lead to daily episodes of temporary egg limitation during which parasitoids must mature an egg before being able to oviposit.     

Host selection by Homalodisca vitripennis: the interplay between feeding, egg maturation, egg load, and oviposition

For some phytophagous insects, egg maturation may be dependent on adult feeding. Accordingly, rates of egg maturation may be dependent on the quality and quantity of available food sources. In turn, oviposition behavior could be affected by diet quality via changes in egg load (number of mature eggs carried by a female). Experiments were conducted to determine whether adult feeding may affect oviposition behavior of the glassy-winged sharpshooter, Homalodisca vitripennis. No-choice tests demonstrated that eggs accumulated in glassy-winged sharpshooter abdomens as time since last oviposition increased largely as a function of feeding plant species. In choice tests, glassy-winged sharpshooter females were observed most frequently on the plant species that imparted the greatest egg maturation rate in no-choice tests. Direct tests of the effects of egg load on glassy-winged sharpshooter oviposition behavior found that females were more likely to deposit eggs as egg load increased. Similarly, acceptance of a low-ranked oviposition plant species by female glassy-winged sharpshooters increased with egg load and time since last oviposition. The results indicate that adult feeding affected glassy-winged sharpshooter egg maturation, plant species varied in quality for providing nutrients for egg maturation, and egg load affected oviposition behavior. Thus, the quantity and quality of available feeding plant species may affect glassy-winged sharpshooter egg maturation rates, which in turn may affect the plant species female glassy-winged sharpshooters select for oviposition.     

Hormonal control of egg maturation in the corn earworm, Heliothis zea

At eclosion, the ovaries of female Corn earworm Heliothis zea do not contain mature eggs. Virgin-unfed females produced approximately 400 mature eggs in 8 days; mating or feeding doubled this number, and mating plus feeding more than tripled it. Females allatectomized or decapitated at day O matured few eggs. Egg production was restored by implantation of active corpora allata (CA) or by treatment with the juvenile hormone (JH) analogue methoprene at day 0. 20-Hydroxyecdysone, on the other hand, had no effect. Females in which the CA had been denervated or in which the median neurosecretory cells of the brain had been ablated at day O produced fewer eggs than sham-operated animals. These results indicate that egg maturation is controlled by JH and that continuous input from the brain is required for sustained CA activity for maintaining a high rates of egg maturation.The rate of JH biosynthesis by CA in vitro was determined with a radiochemical assay. The major hormones produced were JH-II and JH-III with small quantities of JH-I. The rates of JH synthesis were similar in all experimental groups which may indicate that the in vitro rate of JH synthesis does not reflect the actual state of CA activity in the female.     

Egg limitation in host-parasitoid dynamics: an individual-based perspective

Theoretical models of parasitoid-host dynamics predict that egg limitation in parasitoids destabilizes community dynamics. However, although egg limitation is experienced by individual parasitoids with variable success of encountering hosts, such details were neglected in previous models. This study developed an individual-based parasitoid-host model that explicitly incorporates egg limitation and host encounters of individual parasitoids. The model indicates that the combination of egg limitation and variation in the success of encountering hosts stabilizes parasitoid-host dynamics. The stabilizing mechanism emerges from Jensen’s inequality because egg limitation makes the number of offspring inherently concave down in the number of encountered hosts. Reasons for the inconsistent predictions of the effect of egg limitation between the current model and previous models are discussed.     

Egg chorion architecture in stick insects (Phasmatodea)

Comparative analysis of egg chorion architecture by scanning and transmission electron microscopy is reported in about 50 species of stick insects (Phasmatodea). Particular attention has been paid to: (1) synthesis and structure of egg shell layers; (2) egg shape; (3) morphology of the external chorionic surface; (4) position and structure of the micropylar plate and its cup; (5) morphology and details of the operculum, including capitulum or pseudocapitulum; and (6) posterior pole differentiation (the so-called polar mound), The taxonomic value of the various characters is discussed: some are clearly species-specific, while others (such as general egg shape and micropylar plate) appear to reflect phylogenetic relationships of higher rank. Intraspecific features, such as the fine chorionic and opercular patterns of Bacillus and Clonopsis, have been recognized.In natural hybrids, egg chorion architectures were related to that of the parent species, resembling one of the parents in some cases and being intermediate between the 2. The study of the Phasmatodea egg can provide much taxonomic information that is useful in the definition of natural groups.