Reproductive senescence and dynamic oviposition behaviour in insects

We explore the relationship between clutch size behaviour and the likelihood of egg limitation in insects with parasitoid-like life histories. We compare the incidence of egg limitation in insects that produce clutch sizes consistent with maximizing fitness per host (i.e. the single host maximum, or Lack clutch size) with insects exhibiting two types of dynamic behaviour. In the first case, insects produce clutch sizes according to a rule that specifies a negative relationship between egg complement and clutch size; in the second case, clutch size is determined by both egg complement and the host encounter rate using a dynamic state-variable model. The analyses are an extension of models presented by Rosenheim (1996), which predicted a strong positive relationship between the risk of egg limitation and the host encounter rate in the absence of dynamic oviposition behaviour. Our results are consistent with Rosenheim's, but they show that dynamic behaviour can greatly reduce th e risk of egg limitation and weaken the relationship between the host encounter rate and egg limitation.     

Mating or ovipositing? A crucial decision in the life history of the cabbage aphid parasitoid Diaeretiella rapae (M’Intosh)

1. The reproductive fitness of a parasitoid depends on its mating and ovipositing success. Virgin haplodiploid females can reproduce, but produce only males, and may diminish fitness by producing more male offspring than required. Therefore, females must decide on whether to mate or oviposit first. 2. This study was conducted to assess the mating versus ovipositing decision and its impact on the reproductive fitness of Diaeretiella rapae (Hymenoptera: Aphididae), an endoparasitoid of the cabbage aphid Brevicoryne brassicae (Hemiptera: Aphididae). 3. When newly emerged females were given a choice between mating and ovipositing, about 62% of D. rapae females preferred to mate before ovipositing. Those females who oviposited before mating parasitised only 10% of the available aphids. After mating, females superparasitised their hosts with fertilised eggs, which resulted in a highly female‐biased sex ratio in the offspring. 4. Mating success was very high (91%) in the presence of hosts (cabbage aphid nymphs) compared with that in the absence of aphids. However, mating success was not influenced by the quality (size) of the hosts present in the mating arena, despite a parasitoid preference for larger hosts during oviposition. The time between pairing and mating was also shorter in the presence of host aphids. The mean number of aphids parasitised and the parasitism rate were significantly greater after mating.     

Putting more eggs in the best basket: clutch-size regulation in the comma butterfly

Abstract.  1. Many studies have identified different factors influencing clutch-size regulation, primarily within various groups of insects. One prediction is that ovipositing females should increase clutch size with host quality. However, in many studies it is not clear whether ovipositing females are responding to host quality or quantity.
2. Females of the polyphagous comma butterfly, Polygonia c-album (L.), were allowed to oviposit on two hosts differing greatly in quality: the preferred host, stinging nettle ( Urtica dioica L.), and the low-ranked host, birch ( Betula pubescens Ehrh). Ovipositing females were observed visually and clutch sizes were recorded. The experiment was repeated in three different years; in total, 938 observations of oviposition events were made.
3. In all three years, females ovipositing on U. dioica laid larger clutches (median 1.6–1.85) compared with females ovipositing on B. pubescens (median 1.0–1.3) . The difference was significant in two out of three years and when all three years were pooled.
4. Thus, P. c-album females exhibit clutch-size regulation, with larger clutches on better hosts. It is suggested that the proximate mechanism is likely to be a response to the same stimuli used for female ranking of host plants in the preference hierarchy.     

Evolution of clutch size in insects. II. A test of static optimality models using the beetle Callosobruchus maculatus (Coleoptera: Bruchidae)

Wilson and Lessells (1993) analysed the effect of constraint assumptions on the predictions of static optimality models for insect clutch size. They concluded that the models could be reliably distinguished between (and hence the main constraints identified) only after precise quantitative predictions had been examined. The present paper describes a series of laboratory experiments, using the bruchid beetle Callosobruchus maculatus, that allow these quantitative predictions to be made and tested. Experiments in which female encounter rate with hosts was altered gave qualitative support for 3 out of 6 basic (single oviposition) models, but the quantitative fit of them all was poor. However, when the (a priori) condition was included in these models that several other females would oviposit on the same hosts (the multiple oviposition models), the time limiting multiple oviposition model alone produced quantitative predictions that were supported by observations. In other words, the results suggest that the main constraints on bruchid oviposition behaviour are the amount of time available for laying eggs and the number of other females ovipositing. However, additional qualitative predictions indicate that the number of eggs available to the female may also constrain clutch size evolutionarily. The usefulness of static optimality models for examining clutch size decisions in insects is discussed in the context of these results.     

Potential Costs of Selecting Good Sites For Offspring: Increased Risk of Drowning And Negative Effects on Egg Production

Many studies have shown the benefits of selecting suitable sites for offspring survival and growth. However, costs of selecting suitable sites have been little covered. If the female's costs associated with selecting suitable sites exceed the benefit from improvement of offspring performance, selecting such sites can have a negative effect on the ongoing reproductive success for ovipositing females. We investigate the potential costs of selecting suitable sites in the water strider Aquarius paludum insularis. Where there exists a risk of egg parasitism, the female A. paludum will submerge and select a deep site, more suitable for offspring survival, for oviposition. By forcing A. paludum underwater once a day for 10 d, we investigated the potential costs associated with oviposition at deep sites, firstly relating to the performance of submergence (latency to asphyxiation or proportion of buoyancy loss) and, secondly, in the number of eggs laid. Buoyancy became weaker and the latency to asphyxiation became shorter with the number of submergences. The number of eggs laid in the period of forced submergence was smaller than both before and after the period. Selecting deep sites can therefore increase the mortality risk of ovipositing females and also decrease the number of eggs laid in their lives. Selecting suitable sites in all the oviposition bouts can decrease ovipositing females' reproductive success. Costs, not only benefits, should be taken into consideration for understanding oviposition site selection during the lifespan of an ovipositing female.     

Factors influencing brood sex ratios in polyembryonic Hymenoptera

Copidosoma sp. is a polyembryonic encyrtid wasp which parasitizes isolated hosts. Most broods of this wasp are unisexual, but some contain both sexes and the secondary sex ratio of these is usually highly female biased. The overall population secondary sex ratio is female biased. Walter and Clarke (1992) argue that because the majority of individuals must mate outside the natal patch, the bias in the population secondary sex ratio contradicts predictions made by Hamilton's (1967) theory of local mate competition (LMC). We suggest that the primary sex ratio is unbiased and that Walter and Clarke's results do not cast doubt on LMC. Instead these results imply that ovipositing females make a combined clutch size and sex ratio decision influencing whether individuals developing from a particular brood will outbreed or largely inbreed; for each case the predictions of LMC theory are not violated. If this interpretation is correct, what is of interest is the basis on which this decision is made rather than the population secondary sex ratio. We show that host encounter rate influences the proportions of mixed and single sex broods laid by Copidosoma floridanum, a related polyembryonic parasitoid. Among single-sex broods the primary sex ratio is female biased, but our results are in agreement with LMC theory since offspring developing from these broods will probably mate with siblings from adjacent hosts. We consider the egg load of females to be of major influence on oviposition behaviour, and that the mating structure of parasitoid offspring, potentially differential costs of male and female broods and the natural distributions of hosts both at oviposition and eclosion, require further study.     

Age-dependent clutch size in a koinobiont parasitoid

Abstract.  1. The Lack clutch size theory predicts how many eggs a female should lay to maximise her fitness gain per clutch. However, for parasitoids that lay multiple clutches it can overestimate optimal clutch size because it does not take into account the future reproductive success of the parasitoid.
2. From egg-limitation and time-limitation models, it is theoretically expected that (i) clutch size decreases with age if host encounter rate is constant, and (ii) clutch size should increase with host deprivation and hence with age in host-deprived individuals.
3. Clutch sizes produced by ageing females of the koinobiont gregarious parasitoid Microplitis tristis Nees (Hymenoptera: Braconidae) that were provided daily with hosts, and of females ageing with different periods of host deprivation were measured.
4. Contrary to expectations, during the first 2 weeks, clutch size did not change with the age of the female parasitoid, neither with nor without increasing host-deprivation time.
5. After the age of 2 weeks, clutch size decreased for parasitoids that parasitised hosts daily. The decrease was accompanied by a strong decrease in available eggs. However, a similar decrease occurred in host-deprived parasitoids that did not experience egg depletion, suggesting that egg limitation was not the only factor causing the decrease in clutch size.
6. For koinobiont parasitoids like M. tristis that have low natural host encounter rates and short oviposition times, the costs of reproduction due to egg limitation, time limitation, or other factors are relatively small, if the natural lifespan is relatively short.
7. Koinobiont parasitoid species that in natural situations experience little variation in host density and host quality might not have strongly evolved the ability to adjust clutch size.     

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.     

Intraspecific variability in host plant quality and ovipositionaI preferences in Eucheira socialis (Lepidoptera: Pieridae)

Abstract.

• 1 This study investigates interactions between Eucheira socialis (Pieridae: Lepidoptera), a strict monophagous herbivore, on Arbutus xalapensis (Ericaceae), a host plant with few herbivores. This tight association of insect on plant has many attributes conducive to reciprocal rather than diffuse evolution.
• 2 An indirect way of testing plant–insect coevolutionary theories is to test for the necessary conditions for reciprocal evolution in ecological time. Two conditions for coevolution were studied: (1) host plants vary in their suitability for larval growth and development, and (2) ovipositing insects discriminate among these plants based on their relative suitability.
• 3 Large differences in host plant suitability were found and relative differences were consistent from year to year.
• 4 There was no evidence that female insects based their ovipositional decisions on relative tree quality, which implies that factors other than host plant quality are involved in the maintenance and evolution of oviposition behaviour in Eucheira.
• 5 Of seven factors known to influence ovipositional preferences of insects among plants independent of potential larval success, the most likely causal factor in this system is the ability of females to balance a time/energy budget for finding potential oviposition sites, discriminating among them, and actually ovipositing.

     

Diel patterns of reproductive activities in the tomato fruit fly, Neoceratitis cyanescens

We describe the diurnal temporal and spatial patterns of reproductive activities (mating and ovipositing) of adult tomato fruit flies, Neoceratitis cyanescens (Bezzi) (Diptera: Tephritidae), under laboratory, field‐cage and field conditions. The distribution pattern of flies in the different habitats (host and non‐host plants) showed temporal, physiological and sexual differences. Mature females were observed to frequent host plants preferentially, particularly in the late afternoon. By contrast, immature females preferred to rest on non‐host plants throughout the day. Males frequented mainly non‐host plants but some were observed on host fruits in the morning. Mating activity took place preferentially on non‐host plants, in the morning. In laboratory cages, females showed a strong daily propensity to engage in mating behaviour; the mean percentage of mating females was 88 ± 5%. Time allotted to this activity (4 h 52 min ± 1 h 23 min in laboratory cages and at least 3 h for the mating pairs observed in the field) appeared considerable compared to the time required to satisfy feeding or oviposition activities. Except for a few ovipositing females observed in the morning, oviposition activities occurred mainly in the late afternoon.     

Comparison of Host-Searching and Ovipositional Behavior of Cardiochiles nigriceps Viereck (Hymenoptera: Braconidae), a Parasitoid of Heliothis virescens (Fabricius) (Lepidoptera: Noctuidae), in Tobacco and Cotton

To compare host-searching and ovipositional behavior of Cardiochiles nigriceps Viereck (CN) in tobacco and cotton, behavior of CN females was observed on Hellothis virescens (Febricius)-infested plants and recorded using a Psion Organizer II with Observer software. Hover, search, oviposit, preen, rest, walk, agony-search, drop-search, and miss-search were the nine behaviors observed for each plant species. Agony-search was a searching behavior exhibited when CN females were prevented from ovipositing in a host because they were unable to reach the host. Drop-search and miss-search were the searching behaviors that occurred by CN females after a host dropped from the plant and when CN females missed ovipositing in a host, respectively. Hovering, searching, oviposition, miss-search, resting, and walking were equally common for CN on tobacco and cotton. Agony-search was exhibited more on tobacco than cotton, while drop-search and preening occurred more on cotton than tobacco. Female CN spent more time hovering in tobacco than in cotton, indicating that these females preferred tobacco to cotton. Female parasitoids also spent more time in the main ovipositional sequence, hover–search–oviposit, in tobacco than in cotton, mainly because females hovered more in tobacco than in cotton. Frequency and time of behavioral sequences associated with experiencing frustration in ovipositing due to difficulty in reaching or finding a host and subsequent level of success in ovipositing in a new host were determined. Overall, the rate of successful oviposition by CN females was significantly higher in tobacco (87.7%) than in cotton (79.5%). For cotton and tobacco, the rate of successful oviposition by CN females was significantly reduced (ca. 40.0%) when they experienced frustration in ovipositing compared to the rate of ovipositional success (100%) for CN females when hosts were present and easily accessible. Encountering ovipositional frustration also increased the duration of time for successful oviposition in comparison to the time spent for problem-free oviposition in cotton and tobacco. Interestingly, with successful oviposition, the amount of time spent in a behavioral sequence was not significantly different for tobacco and cotton regardless of whether females experienced ovipositional frustration or not. However, female CN invested more time in tobacco than in cotton when they were unsuccessful in ovipositing due to the inaccessibility or disappearance of hosts. CN females' preference for tobacco over cotton probably gave them more motivation to continue searching for hosts, especially those not easily attained, on tobacco than on cotton. Nevertheless, CN females readily searched in cotton for HV even in the presence of host-infested tabacco. CN females possibly could be successful in maintaining levels of HV below an economic threshold when using a tobacco trap crop to protect cotton as the main crop.     

Wasp sex ratios when females on a patch are related

Optimality theory of sex allocation in structured populations has proved remarkably successful in explaining patterns of facultative sex ratio behaviour in numerous species. Extensions to the basic theory have included more specific aspects of species biology, including the relatedness of interacting individuals. We considered the sex ratio decisions made by female Nasonia vitripennis wasps when they were ovipositing on a patch with either relatives or nonrelatives. Theory predicts that females should produce more female-biased sex ratios when ovipositing with relatives, for example sisters, than with unrelated females. This is because related females should limit the level of local mate competition between their sons for female partners. Contrary to theory, two experiments showed that female sex ratio behaviour was unaffected by the relatedness of their oviposition partner, and was also unrelated to an environmental cue that could signal relatedness, i.e. whether females responded differently to sisters emerging from the same or a different host. Instead, in both experiments, we found that only wasp strain significantly influenced sex ratio. A meta-analysis of studies conducted on a range of species on the effects of the relatedness of oviposition partners on sex ratio failed to show the predicted pattern. We discuss why females appear to behave in a maladaptive way when allocating sex under these conditions, and suggest that weak selection and/or conflict between females over optimal sex ratios may influence the evolution of kin discrimination.     

Do reproductive activities compromise immunological competence as measured by phenoloxidase activity? Field and experimental manipulation in females of two damselfly species

Recent studies of female insects indicate that reproductive activities, such as mating and oviposition, can impair immune ability. Using the two tropical damselfly species Argia anceps Garrison and Hetaerina americana (Fabricius), egg production and phenoloxidase (PO) activity, a key enzyme in insect immunity, are measured in mating, ovipositing and perching females in December and March. Perching females of both species have fewer eggs compared with mating and ovipositing females, which suggests that perching females are not engaged in reproduction. There is seasonal variation in egg number for the three categories in H. americana but not in A. anceps, which can be interpreted in terms of adaptive changes in egg production depending on female–male interactions in the former species but not in the latter species. There is no difference in PO activity among mating, ovipositing or perching females within either species, although measurements in December and March indicate distinct seasonal changes. Juvenile Hormone (JH) is known to reduce the effectiveness of the immune system by favouring the use of resources for reproduction. A possible role for JH is examined in H. americana, using the JH analogue methoprene to manipulate hormone activity, revealing that PO activity is reduced in methoprene‐treated H. americana females. Thus, although the results of the present study are indicative of possible hormone‐driven changes in PO, there is not necessarily a down‐regulation of immune function (as determined by PO activity) during mating or oviposition. The results complement some recent studies countering the idea that reproductive activities reduce the immune ability in insects.     

Behavior and Activity Pattern of Cephalonomia stephanoderis (Hymenoptera: Bethylidae) Attacking the Coffee Berry Borer,Hypothenemus hampei (Coleoptera: Scolytidae)

We describe behavioral sequences and daily activities of pre-ovipositing and ovipositing females of Cephalonomia stephanoderis (Hymenoptera: Bethylidae), an ectoparasitoid of the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). Noticeable behavioral differences among preovipositing and ovipositing females include host examination, host stinging—probing, host feeding, and the oviposition per se. The female of C. stephanoderis feeds primarily on host eggs, but pupae are also exploited, mainly by pre-ovipositing females. After the onset of the oviposition period, C. stephanoderis examines the pupae repeatedly, stings them at frequent intervals, and spends more time feeding than during the pre-oviposition period. Host paralysis is linked both to host feeding and oviposition. It induces irreversible developmental arrest, which presumably allows preservation of the host until subsequent utilization, and contributes to successful offspring development, particularly by reducing host motility. Oviposition consists in a host selection process, a prolonged period of preparation of the potential host, and the egg-laying phase itself. Under our experimental conditions, pre-ovipositing and ovipositing females are active 17% and 36% of the day, respectively. Host handling time averages 6% and 23% in pre-ovipositing and ovipositing females, respectively. All coffee berry borer developmental stages are exploited by C. stephanoderis females, either for host feeding and/or oviposition activities. Such flexible behavior is advantageous given that host availability is limited inside the coffee berries.     

Does mother really know best? Oviposition preference reduces reproductive performance in the generalist parasitoid Aphidius ervi

The reproductive success of female parasitoids is dependent on their ability to accurately assess the suitability of a host for larval development. For generalist parasitoids, which utilize a broad range of species and instars as hosts, a set of assessment criteria determines whether a host is accepted or rejected. The suitability of a host, however, can only be imperfectly assessed by the female parasitoid, which can result in the selection of lesser quality hosts for oviposition. In this study we explored the disparity between host quality and host preference using the generalist koinobiotic parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae) and the host Aulacorthum solani (Harris) (Homoptera: Aphididae), the foxglove aphid. The second instar hosts produced the highest level of reproductive success, while third and fourth instars resulted in a substantially reduced reproductive performance. When given a choice of host instars, parasitoids preferred the older hosts for oviposition disregarding their reduced suitability for larval development. Results are discussed in context of mechanisms involved in A. ervi host selection and biases in the criteria used to assess hosts that may arise when parasitoids transfer host species between generations.     

Unpredictable offspring survivorship in the damselfly, Megaloprepus coerulatus, shapes parental behavior, constrains sexual selection, and challenges traditional fitness estimates

Evolutionary biologists typically assume that the number of eggs fertilized or developing embryos produced is correlated with an individual's fitness. Using microsatellite markers, we document for the first time estimates of realized fitness quantified as the number of offspring surviving to adulthood in an insect under field conditions. In a territorial damselfly whose males defend tree hole oviposition sites, patterns of offspring survivorship could not be anticipated by adults. Fewer than half of the parents contributing eggs to a larval habitat realized any reproductive success from their investment. The best fitness correlate was the span over which eggs in a clutch hatched. Among parents, female fecundity and male fertilization success were poor predictors of realized fitness. Although body size was correlated with female clutch size and male mating success, larger parents did not realize greater fitness than smaller ones. The uncoupling of traditional fitness surrogates from realized fitness provides strong empirical evidence that selection at the larval stage constrains selection on mated adults.     

浙江舟山五种卵生游蛇科动物个体大小、窝卵数和卵大小之间的关系

阐明五种游蛇科动物雌体大小、窝卵数和卵大小之间的关系和雌性繁殖特征的种间差异。５种蛇均产单窝卵,产卵高峰期为６月下旬至７月,窝卵数与雌体大小（ＳＶＬ）呈显著的正相关,相对窝卵重与雌体ＳＶＬ无关,卵理与窝卵数无关。灰鼠蛇卵重与雌体ＳＶＬ呈正相关,赤链蛇、王锦蛇、黑眉锦蛇和乌梢蛇的卵重与雌体ＳＶＬ无关,黑眉锦蛇卵长径与窝卵娄呈负相关,其余４种蛇卵长径与窝卵数无关。５种蛇卵长径与短径无关。黑眉锦蛇卵短径     

Induction of egg maturation and oviposition in the tick Ornithodoros parkeri (Acari: Argasidae)

Hemocoelic injection and vaginal insertion of selected male reproductive and non-reproductive tissue homogenates into fed-virgin female Ornithodoros parkeri stimulated varying degrees of ovum maturation and/or oviposition during 14 and 30 day observation periods, respectively. Mean times for oviposition and mean numbers of eggs laid per ovipositing female receiving hemocoelic injections of male reproductive tissue homogenates did not differ significantly from fed-mated controls. In addition, hemocoelic injection of male salivary glandular homogenate induced oviposition, yet synganglial homogenate did not. Although vaginal insertion induced both ovum maturation and oviposition, the effect was not as pronounced as when similar doses were administered by hemocoelic injection. These results indicate that a complex interrelated series of precopulatory and copulatory stimuli are necessary for oviposition to occur in fed O. parkeri.     

Influence of Conspecific Presence, Experience, and Host Quality on Oviposition Behavior and Clutch Size Determination in Anastrepha ludens (Diptera: Tephritidae)

Females of some insect species adjust the number of ovipositions and clutch size adaptively depending on conspecific density and probably experience. In a series of three experiments, we examined the effect of the presence of conspecifics, host quality, and oviposition experience on oviposition behavior and clutch size determination by females of the polyphagous fruit fly Anastrepha ludens (Diptera: Tephritidae). In the first experiment, we determined that grouped (eight females per cage) A. ludens females tended to visit and oviposit in more hosts than did solitary females probably as a result of stimulation by the presence of conspecifics. We also determined that females with previous oviposition experience visited and oviposited in more hosts than inexperienced ones. Importantly, when females were grouped, we observed significantly more landings on unoccupied hosts (i.e., devoid of flies) than on occupied ones (i.e., with at least one fly on it). However, oviposition experience, and not female density, was the most important factor affecting clutch size. Naive females deposited larger egg clutches than experienced ones. In the second experiment, we found that oviposition experience and host quality (i.e., clean fruit or fruit covered with a host marking pheromone [HMP] extract), influenced clutch size and the decision of females to defend or not defend the host. Clutch size and number of fights were greater on clean than on HMP-marked hosts. In the third experiment, we observed that host quality (i.e., size) played a significant role with regard to the number of female fights, host marking behavior, and clutch size. Specifically, females fought and dragged their aculeus longer on small- and medium-sized hosts than on large ones. But this behavior varied according to whether females were kept alone or grouped. Clutch size was greatest in the largest hosts. Considering all the above, we believe that the observed increase in ovipositional activity by grouped A. ludens females can be attributed to competition through mutual interference and not social facilitation as has been reported in other tephritid species.