Counterstrategy to Egg Dumping in a Coreid Bug: Recipient Individuals Discard Eggs from Their Backs

The golden egg bug, Phyllomorpha laciniata Vill. (Heteroptera: Coreidae), is the only terrestrial insect in which females oviposit on the backs of female and male conspecifics. Eggs do not survive unless carried by a bug. Herein, I report laboratory observations that egg-carrying individuals actively brush their backs against the host plant seemingly in an effort to rub off eggs. Egg scraping is more common among individuals carrying many eggs than among those carrying only a few eggs. The most recently received eggs were rubbed off first. Females did not avoid laying eggs on the backs of egg-loaded individuals, nor did bugs carrying several eggs resist oviposition attempts more often than unloaded ones. Some males were likely to have fertilized the eggs they scraped off their backs. Laboratory results of active egg removal correspond with egg loss in the field, suggesting that egg scraping may explain egg loss in nature. The data indicate a cost of egg carrying to an individual and an evolutionary arms race between oviposition and discarding behavior.     

Flexible oviposition behavior in the golden egg bug (Phyllomorpha laciniata) and its implications for offspring survival

Female golden egg bugs show unique flexibility in their oviposition behavior. Females can lay eggs on plants, where they are leftunattended, or on the back of conspecifics, where they remainuntil hatching. In this article we show that eggs have greatersurvival rates when carried by an adult than when laid on plants.The main causes of egg mortality are predators and a parasitoidwasp. Our results suggest that, although predation pressureis similar, fewer eggs are attacked by parasitoid wasps whencarried by an adult than when laid on plants. In addition,we show that, when given a choice, females prefer to lay eggson the backs of conspecifics than on plants. Thus, female ovipositionchoice is adaptive and minimizes individual offspring mortality.The factors that may maintain such behavioral variation in current populations are discussed.     

Kin recognition by the predatory mite Iphiseius degenerans: discrimination among own, conspecific, and heterospecific eggs

1. Kin recognition is important in many social insects, but has also been found in several nonsocial insects such as parasitoids, where it plays an important role in oviposition behaviour. In nonparasitic arthropods, however, the fitness of ovipositing females also depends on the oviposition behaviour of related and unrelated females, especially when eggs are oviposited in clusters by several females. 2. In this paper, kin recognition in a predatory mite, Iphiseius degenerans, is studied. Mothers are capable of determining offspring sex ratio, and cannibalism on juvenile stages is a common phenomenon. Therefore, kin recognition is expected to occur in this predator. 3. Oviposition behaviour of this species is particularly interesting because it alternates foraging bouts in flowers with deposition of a single egg at a time on a leaf, where predation risk is lower. The eggs are not scattered but are deposited in clusters. After feeding in a flower, females therefore have to locate clusters of eggs. 4. Experiments on two‐choice arenas showed that females prefer to oviposit close to conspecific eggs rather than close to heterospecific eggs. Females also showed a preference for ovipositing near closely related conspecific eggs rather than more distantly related eggs. 5. Females tended to displace eggs of heterospecifics more frequently than eggs of conspecifics. 6. These behavioural observations show that females can discriminate not only between conspecific and heterospecific eggs but also between eggs that vary in degree of relatedness. This enables females to oviposit in clusters containing related eggs and thus avoid cannibalism by non‐kin and/or produce adaptive sex ratios despite the fact that the adults commute between flowers and leaves.     

Effect of host deprivation on egg quality,egg load,and oviposition in a solitary parasitoid,Chetogena edwardsii (Diptera: Tachinidae)

Solitary parasitoids are limited to laying one egg per host because larvae compete within hosts. If host encounter rate is low, females should not increase the number of eggs/host in response. The tachinid fly, Chetogena edwardsii,was used to evaluate the effect of host deprivation on egg accumulation, oviposition behavior, and egg quality in a solitary parasitoid. Females deprived of hosts for 2– 7 days accumulate about 1 day's supply of eggs. Egg output of deprived females once hosts are restored does not differ from that of control females. Deprived females retain one egg in the uterus where it undergoes embryogenesis. Maggots emerging from retained eggs are more likely to survive in hosts molting in 40 h or less after receipt of an egg than are maggots emerging from eggs fertilized shortly before oviposition. Egg retention is a consequence of host deprivation that permits females to broaden the range of hosts they can exploit to include soon-to-molt hosts and possibly multiply parasitized hosts.     

Host discrimination modulates brood guarding behaviour and the adaptive superparasitism in the parasitoid wasp Trissolcus semistriatus (Hymenoptera: Scelionidae)

Because hosts utilized by parasitoids are vulnerable to further oviposition by conspecifics, host guarding benefits female wasps. The present study aims to test whether female adults regulate brood guarding behaviour by host discrimination in a solitary parasitoid Trissolcus semistriatus by presenting an intact or parasitized host egg mass to a female adult. Virgin females without oviposition experience have host discrimination ability, which enables them to adjust the number of eggs laid in the hosts. Mating experience increases superparasitism by female adults, whereas mated females achieve a higher discrimination ability as a result of oviposition experience and show a lower superparasitism rate. As expected, females exhibit brood guard after parasitizing an intact host egg mass, whereas those females visiting a previously parasitized host egg mass, do not. Because the survival of eggs in superparasitized hosts is relatively low, regulating brood guarding behaviour by host discrimination is adaptive for female wasps.     

Egg performance on an egg-carrying bug. Experiments in the field

Selection of oviposition sites has direct influence on female fitness. Differences in offspring survival among sites should favour females to select oviposition sites with the highest survival. Golden egg bug females ( Phyllomorpha laciniata; Coreidae, Heteroptera) use conspecifics as oviposition substrates. Most eggs are laid on the back of the bug but they can be found on all body parts. Females never carry their own eggs, and males commonly carry eggs received without copulation with the donor. We examined differences in egg survival relative to paternity to the egg, host sex and body size and attachment of an egg on a host's body in the field. We also studied which bugs received eggs. Egg loss was surprisingly common: 30–80% of recaptured individuals lost eggs during a six-day period. Unexpectedly, host's paternity to the eggs did not affect egg survival. Also, egg loss did not differ among hosts in respect to other parameters studied. Males received more eggs than females, but survival of the eggs was not better on a male's back than on a female's back. Since egg loss is common in the golden egg bug, we suggest that female oviposition strategy to lay eggs on conspecifics is not perfect. This is due to active behaviour of potential hosts (for example, rejected oviposition attempts) or lack of suitable oviposition substrates (conspecifics) in the field. Since eggs do not survive unless carried, females may be acting opportunistically, doing the best job possible by laying eggs on available conspecifics.     

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.     

Oviposition patterns of the pine weevil Hylobius abietis

Spatial and temporal distributions of eggs laid by the pine weevil Hylobius abietis (L.) (Coleoptera: Curculionidae) were studied by taking root and soil samples around pine stumps on a clear-cutting in central Sweden. In addition, first-instar larvae migrating in the soil were sampled using traps baited with host-odour. Eggs were found in the soil rather than in the bark of stump roots, which previously has been regarded as the usual oviposition site. Based on an oviposition experiment and additional field observations we conclude that eggs are laid in the bark of roots only when the surrounding material is likely to dry out. We suggest two explanations for why weevils oviposit mainly in the soil, although they are known to show stereotypic behaviour when inserting eggs in stump roots: (1) egg predation by other arthropods or by conspecifics is avoided, and (2) newly hatched pine weevil larvae are better than ovipositing females at locating suitable sites for larval feeding.     

Ability of ovipositing seed beetles to discriminate between seeds with differing egg loads

Abstract. 1. Previous work has shown that ovipositing females of Callosobruchus maculatus (F.) avoid seeds already bearing eggs, and thereby reduce competition among their larval progeny within seeds.
2. This study demonstrates that females also detect small differences in egg density, and prefer to oviposit on seeds with a lower-than-average number of eggs. A nearly uniform dispersion of eggs is thus maintained even after all seeds bear several eggs.
3. In addition, variation in egg load influences oviposition rate. Transfer of females from seeds with few eggs to seeds with many eggs inhibits oviposition; the reverse transfer stimulates it.
4. The upper surface of the egg chorion or egg 'cover' remains intact on the seed surface after the larva has entered the seed and continues to deter egg-laying for at least as long as the period required for larval development. 14-day-old egg covers provide as much deterrence as freshly laid eggs.     

Effects of starvation and oviposition activity on the reproductive physiology of the sweet potato whitefly, Bemisia tabaci

Abstract. We examined the effects of starvation and oviposition on the reproductive physiology of the sweet potato whitefly, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae). In a first set of experiments, females were starved as well as denied the opportunity to oviposit. The combined amounts of vitellogenin and vitellin per female increased by 69% when they were removed from plants for 24 h, egg load increased two-fold in approximately 4.5 h. The lipid content, on the other hand, decreased significantly over an 8 h perod. Thus, vitellogenin synthesis and the formation of mature eggs do not seem to be limited by the lack of nutrient intake or the ability to oviposit. In a second set of experiments, females were restricted to either young leaves of melon plants (Cumis melo), that are preferred oviposition sites, or to old melon leaves, that are non-preferred oviposition sites. At the end of the experiment, females on the old leaves contained significantly higher amounts of vitellogenins and vitellins than females confined to young leaves. These comparisons were made relative to body weight. The data also indicate that females accumulated both vitellogenins and lipids when confined to old leaves, but did not do so on young leaves. These results are consistent with the hypothesis that females of B. tabaci explicitly discriminate against older leaves for oviposition. We argue that examinations of changes in egg load or the combined vitellogenin and vitellin content that accompany oviposition can provide better insights into the oviposition behaviour of B. tabaci.     

Host-feeding and oviposition by parasitoids on hosts of different fitness value: Influences of egg load and encounter rate

A dynamic optimization model is presented for the decision to host feed or oviposit on hosts by female parasitoids. Optimal host utilization decisions are compared between two host types with different fitness payoffs for oviposition. The model predicts that hosts of higher fitness value should always be used for oviposition unless the egg load approaches zero. This general prediction is not influenced by levels of host availability or metabolic reserves, the age of the parasitoid, or the magnitude of the fitness difference. An egg-load threshold is predicted above which lower value hosts should be used for oviposition and below which they are used for host feeding. The position of this egg-load threshold is higher when the difference in fitness between host types is larger. The threshold is also higher when overall host availability is high or metabolic reserves for the production of new eggs are low. The threshold for oviposition on low-value hosts decreases to zero near the end of the parasitoid’s life. Under conditions where high-value hosts are rarely encountered compared to low-value hosts, the model predicts that lower value hosts should be accepted for oviposition at a lower egg-load threshold.     

Oviposition Sites of the Cypress Seed Bug <Emphasis Type="Italic">Orsillus maculatus</Emphasis> and Response of the Egg Parasitoid <Emphasis Type="Italic">Telenomus</Emphasis> gr. <Emphasis Type="Italic">Floridanus</Emphasis>

Phytophagous insects have many strategies to escape parasitoids, for example by hiding eggs into plant tissues, but oviposition in holes made by another insect is rather scarce. The cypress seed bug Orsillus maculatus Fieber (Heteroptera: Lygaeidae) is strictly dependent on the availability of cones of Cupressus sempervirens L. to oviposit. Females lay eggs either in exit holes cut through the cone scale by emerging adults of the cypress seed chalcid, Megastigmus wachtli Seitner (Hymenoptera: Torymidae), or on the inner side of scales of partly open cones. A recently discovered egg parasitoid belonging to the genus Telenomus has been shown to attack bug eggs in both oviposition sites. In this paper we investigated the parasitoid performance according to oviposition sites. Field samplings were conducted in two evergreen cypress orchards located in the south of France. The distribution and condition of the egg patches were compared between the two locations and oviposition sites. Seed bugs preferred to oviposit in emergence holes of M. wachtli, and parasitoid performance was higher in eggs laid on cone scales. The chalcid emergence holes seemed to ensure bug eggs with enemy-free space. Oviposition site selection could be an adaptive strategy to escape parasitoid attack.     

Conspecifics enhance egg production in an egg-carrying bug

Variation in host availability and quality is likely to affectfemale decision making on when to lay eggs in arthropods. Inthe present study, we show a case in which female reproductionis limited by the availability of conspecifics in a speciesin which females preferably oviposit on conspecific bodies.Female golden egg bugs (Phyllomorpha laciniata; Heteroptera,Coreidae) deposit eggs mainly on the bodies of both male andfemale conspecifics. Bugs other than parents carry most eggs.Egg carrying is costly for individuals. A few eggs are laidon the bug's food plant, but in most habitats, those eggs donot survive owing to intensive ant predation. We explored ifconspecific presence affects female egg production (eggs laidand eggs in reproductive tract) in the field. In our experiment,conspecific presence (two females enclosed with food plant)increased female egg-laying rate and egg production comparedwith that of females that were alone with the food plant. Innature, gaining a conspecific host is difficult, and the encounterrate of conspecifics (i.e., operational host density) is likelyto be important for female reproduction. There are opposinginterests between an egg-laying female and the recipient (maleor female) because most eggs are dumped on individuals thatare not the parent of the eggs.     

Do Golden Egg Bugs (Phyllomorpha laciniata: Heteroptera, Coreidae) Require Conspecifics for Oviposition?

Golden egg bug (Phyllomorpha laciniata) females lay eggs on the bodies of conspecifics of both sexes. We investigated to what extent reproduction depended on the availability of conspecifics as oviposition substrate and the acceptability of the host plant as an alternative oviposition substrate in the absence of conspecifics. Mated females were placed in experimental enclosures each containing a sprig of fresh host plant. Each experimental female was subjected to one of three treatments: isolated from conspecifics (solitary), paired with another female, or paired with a male. Solitary females laid a few eggs on the host plant but then stopped laying eggs, and solitary females laid significantly fewer eggs than those enclosed with another female or a male. Females enclosed with a male laid no more eggs than those enclosed with a female. When two previously isolated females were later enclosed together, they soon renewed oviposition. Females in nature contained significantly more oviducal eggs than did females that were enclosed with other females for a short period. Thus the availability of suitable conspecifics as oviposition substrate stimulates the deposition of mature eggs, and reproduction depends on the presence of conspecifics of either sex as oviposition substrate.     

豚草生育期和被利用状态对广聚萤叶甲产卵选择的影响

【背景】植食性昆虫对产卵场所的选择行为受多种因素的影响,其中寄主植物的发育阶段和被同种其他个体利用程度是影响其产卵选择的重要因素之一。【方法】采用野外罩笼的选择性试验,观察了广聚萤叶甲成虫对不同生长发育阶段、不同被取食程度、不同落卵量的豚草植株的产卵选择行为,分析产卵选择频次,用Cox比例风险模型拟合识别期以估计产卵选择偏好性。【结果】开花期豚草被选择产卵的风险(瞬间概率)仅为生长期的16.5%,苗期豚草被选择产卵的风险为生长期的34.1%;成虫对3种被食程度豚草的产卵选择频次之间存在显著差异(n=20,P<0.01),在3级被食程度豚草上产卵次数最多(12次),而在5级被食豚草上产卵次数最少(2次),表明成虫明显偏好将卵产于已被中等程度取食的植株上;成虫对不同落卵量植株(0、4、8个.株-1)未表现出显著的产卵偏好,对不同密度(高、低)斑块的豚草的产卵选择亦无显著差异。【结论与意义】豚草生育期和被取食程度影响广聚萤叶甲雌虫的产卵选择,而植株上的落卵量和豚草密度对产卵选择没有影响。     

Egg-dumping lace bugs preferentially oviposit with kin

Egg dumping, or abandoning eggs and young to the care of other conspecifics, results in an extreme form of alloparental care. It is unclear, however, if egg dumpers discriminate among kin and nonkin egg recipients. In the lace bug Gargaphia solani (Heteroptera: Tingidae), some females with eggs (guards) also accept and defend eggs of conspecifics. Other females (egg dumpers) abandon their offspring after oviposition, leaving a single guard as the caregiver. We asked if egg dumpers preferentially dump their eggs among unguarded eggs of kin or nonkin. When given a choice between dumping among eggs of full siblings and eggs of nonsiblings, most eggs (67%) were dumped with full siblings' eggs. Furthermore, egg dumpers were just as likely to oviposit among eggs of kin with whom they had interacted on a shared host plant during juvenile development as they were to oviposit with kin reared on different host plants. Thus, egg dumpers discriminate kin by using cues associated with eggs, and such cues are not likely to be acquired through interaction on a common host plant environment. Copyright 2000 The Association for the Study of Animal Behaviour.     

Do Egg Carrying and Protracted Copulation Affect Mobility in the Golden Egg Bug?

Golden egg bug Phyllomorpha laciniata (Heteroptera, Coreidae) females oviposit on male and female conspecifics that carry ova until they hatch. Embryos benefit from being carried because of diminished risks of predation. Female carriers are never the parents of carried eggs, and males are only rarely the fathers of any carried eggs. Eggs develop and hatch without being carried in the laboratory. Egg carriers may be viewed as victims, exploited by females that encumber them with eggs. The intensity of selection favouring resistance to egg carrying should be proportional to the costs of this behaviour. One possible cost could be a reduction in mobility caused by carried eggs. We compare movement rates among encumbered and unencumbered golden egg bugs of both sexes. Protracted copulations (often exceeding 20 h) typical of this species and mating may also cause reduction in bugs mobility. Therefore, we also evaluate rates of movement of coupled pairs of bugs. Our results indicate that egg loads do not affect the mobility and speed of either males or females. However, copulating pairs are significantly slowed as compared to single bugs. Thus protracted copulations have a clear cost in rates of movement and possibly risks of predation, but there are no apparent mobility costs for egg carrying.     

Egg maturation, egg resorption and the costliness of transient egg limitation in insects

Although there is widespread agreement that the cost of oviposition underlies selective oviposition in insects, there is no consensus regarding which factors mediate the cost of oviposition. Models have suggested that egg costs are often paramount in those insects that do not continue to mature eggs during the adult stage (pro-ovigenic insects). Here we address the hypothesis that egg costs are generally less significant in synovigenic insects, which can replenish oocyte supplies through continuous egg maturation. A dynamic optimization model based on the biology of a highly synovigenic parasitoid, Aphytis aonidiae, suggests that the maximum rate of egg maturation is insufficient to balance the depletion of eggs when opportunities to oviposit are abundant. Transient egg limitation therefore occurs, which imposes opportunity costs on reproducing females. Thus, whereas the most fundamental constraint acting on the lifetime reproductive success of pro-ovigenic species is the fixed total number of eggs that they carry at eclosion, the most fundamental constraint acting on a synovigenic species is the maximum rate of oocyte maturation. Furthermore, the ability of synovigenic species to reverse the flow of nutrients from the soma to oocytes (i.e. egg resorption) has a dramatic influence on the cost of oviposition. Whereas females in hostrich environments may experience oviposition-mediated egg limitation, females in host-poor environments may experience oosorption-mediated egg limitation. Both forms of egg limitation are costly. Contrary to initial expectations, the flexibility of resource allocation that typifies synovigenic reproduction actually appears to broaden the range of conditions under which costly egg limitation occurs. Egg costs appear to be fundamental in mediating the trade-off between current and future reproduction, and therefore are an important factor favouring selective insect oviposition.     

Measuring the discrepancy between fecundity and lifetime reproductive success in a pollinating fig wasp

Lifetime reproductive success in female insects is often egg‐ or time‐limited. For instance in pro‐ovigenic species, when oviposition sites are abundant, females may quickly become devoid of eggs. Conversely, in the absence of suitable oviposition sites, females may die before laying all of their eggs. In pollinating fig wasps (Hymenoptera: Agaonidae), each species has an obligate mutualism with its host fig tree species [Ficus spp. (Moraceae)]. These pro‐ovigenic wasps oviposit in individual ovaries within the inflorescences of monoecious Ficus (syconia, or ‘figs’), which contain many flowers. Each female flower can thus become a seed or be converted into a wasp gall. The mystery is that the wasps never oviposit in all fig ovaries, even when a fig contains enough wasp females with enough eggs to do so. The failure of all wasps to translate all of their eggs into offspring clearly contributes to mutualism persistence, but the underlying causal mechanisms are unclear. We found in an undescribed Brazilian Pegoscapus wasp population that the lifetime reproductive success of lone foundresses was relatively unaffected by constraints on oviposition. The number of offspring produced by lone foundresses experimentally introduced into receptive figs was generally lower than the numbers of eggs carried, despite the fact that the wasps were able to lay all or most of their eggs. Because we excluded any effects of intraspecific competitors and parasitic non‐pollinating wasps, our data suggest that some pollinators produce few offspring because some of their eggs or larvae are unviable or are victims of plant defences.     

The use of volatile cues in recognition of kin eggs by predatory mites

1. Several animal species are known to distinguish between their own eggs and eggs of unrelated conspecifics. However, the cues involved in this discrimination are often unknown. These cues were studied using the predatory mite Gynaeseius liturivorus Ehara.
2. Adult females of these predatory mites oviposit in clusters and avoid oviposition close to eggs laid by other females, resulting in reduced cannibalism between offspring. Because predatory mites are blind, it was tested whether volatiles of eggs were used as a cue for egg recognition.
3. Adult female predatory mites were offered volatile cues of their own eggs and of unrelated conspecific eggs, and females were prevented from contacting the eggs. Predatory mites oviposited closer to their own eggs than to unrelated eggs. This preference was observed even when one own and one unrelated egg were offered as a volatile source.
4. These results suggest that adult female predatory mites can determine kinship using volatiles released from the eggs.