Clutch Size Decisions Research Articles

Egg laying rather than host quality or host feeding experience drives habitat estimation in the parasitic wasp Nasonia vitripennis.

In variable environments, sampling information on habitat quality is essential for making adaptive foraging decisions. In insect parasitoids, females foraging for hosts have repeatedly been shown to employ behavioral strategies that are in line with predictions from optimal foraging models. Yet, which cues exactly are employed to sample information on habitat quality has rarely been investigated. Using the gregarious parasitoid Nasonia vitripennis (Walker; Hymenoptera: Pteromalidae), we provided females with different cues about hosts to elucidate, which of them would change a wasp's posterior behavior suggesting a change in information status. We employed posterior clutch size decisions on a host as proxy for a female's estimation of habitat quality. Taking into account changes in physiological state of the foraging parasitoid, we tested whether different host qualities encountered previously change the subsequent clutch size decision in females. Additionally, we investigated whether other kinds of positive experiences—such as ample time to investigate hosts, host feeding, or egg laying—would increase a wasp's estimated value of habitat quality. Contrary to our expectations, quality differences in previously encountered hosts did not affect clutch size decisions. However, we found that prior egg laying experience changes posterior egg allocation to a host, indicating a change in female information status. Host feeding and the time available for host inspection, though correlated with egg laying experience, did not seem to contribute to this change in information status.

Evolutionary constraints on polyembryony in parasitic wasps: a simulation model

Polyembryony involves the production of several genetically identical progeny from a single egg through clonal division. Although polyembryonic development allows highly efficient reproduction, especially in some parasitoid wasps, it is far less common than monoembryony (development of one embryo per egg). To understand what might constrain the evolutionary success of polyembryony in parasitoids, we developed Monte Carlo models that simulate the competition between polyembryonic females and their monoembryonic counterparts. We investigated which simulated life‐history traits of the females allow the monoembryonic mode of development to succeed. Published empirical studies were surveyed to explore whether these traits indeed differ between polyembryonic parasitoids and related monoembryonic species. The simulations predict an advantage to monoembryony in parasitoids whose reproduction is limited by host availability rather than by egg supply, and that parasitize small‐bodied hosts. Comparative data on the parasitoid families Encyrtidae and (to a lesser extent) Braconidae, but not the data from Platygastridae, circumstantially support these predictions. The model also predicts monoembryony to outcompete polyembryony when: 1) hosts vary considerably in quality, 2) polyembryonic development carries high physiological costs, and 3) monoembryonic females make optimal clutch size decisions upon attacking hosts. These multiple constraints may account for the rarity of polyembryony among parasitoid species.

Resource-Dependent Clutch Size Decisions and Size-Fitness Relationships in a Gregarious Ectoparasitoid Wasp, Bracon brevicornis

Gregarious parasitic wasps, which lay more than one egg into or onto a host arthropod’s body, are usually assumed to lay an optimal number of eggs per host. If females would lay too few eggs, some resources may be wasted, but if females lay too many eggs, offspring may develop into substantially smaller-sized adults or may not develop successfully and die. The availability of hosts can further influence a female’s clutch size decision, as more eggs should be laid when hosts are scarce. Here, we analyzed clutch size decisions and the fitness consequences thereof in the ectoparasitic wasp Bracon brevicornis (Hymenoptera: Braconidae), a potential biocontrol agent against pest moth species. For experiments, larvae of the Mediterranean flower moth, Ephestia kuehniella (Lepidoptera: Pyralidae) were used. Using artificially created as well as naturally laid clutches of eggs, the effects of clutch size on fitness of first (F1) and second (F2) generation offspring were investigated. Our results revealed that the fitness consequences of large clutches included both increased mortality and smaller adult sizes of the emerging offspring (F1). Smaller F1 females matured fewer eggs during their lifetime and their offspring (F2) had reduced egg-to-adult survival probability. Naturally laid clutches varied with host size up to a maximum, which probably reflects egg limitation. Clutches remained smaller than the calculated optimal (Lack) clutch size and females responded to high host availability with a decreased number of eggs laid. We thus conclude that large clutches may result in significantly smaller offspring with reduced fitness, and that host size as well as host availability influence the clutch size decision made by B. brevicornis females.

Variation in clutch size in relation to nest size in birds.

Nests are structures built to support and protect eggs and/or offspring from predators, parasites, and adverse weather conditions. Nests are mainly constructed prior to egg laying, meaning that parent birds must make decisions about nest site choice and nest building behavior before the start of egg-laying. Parent birds should be selected to choose nest sites and to build optimally sized nests, yet our current understanding of clutch size-nest size relationships is limited to small-scale studies performed over short time periods. Here, we quantified the relationship between clutch size and nest size, using an exhaustive database of 116 slope estimates based on 17,472 nests of 21 species of hole and non-hole-nesting birds. There was a significant, positive relationship between clutch size and the base area of the nest box or the nest, and this relationship did not differ significantly between open nesting and hole-nesting species. The slope of the relationship showed significant intraspecific and interspecific heterogeneity among four species of secondary hole-nesting species, but also among all 116 slope estimates. The estimated relationship between clutch size and nest box base area in study sites with more than a single size of nest box was not significantly different from the relationship using studies with only a single size of nest box. The slope of the relationship between clutch size and nest base area in different species of birds was significantly negatively related to minimum base area, and less so to maximum base area in a given study. These findings are consistent with the hypothesis that bird species have a general reaction norm reflecting the relationship between nest size and clutch size. Further, they suggest that scientists may influence the clutch size decisions of hole-nesting birds through the provisioning of nest boxes of varying sizes.

Adaptive decision making or differential mortality: what causes offspring emergence in a gregarious parasitoid?

AbstractHosts represent a limited resource for the developing offspring of parasitic insects laying eggs in or on spatially discrete resources like fruits, seeds, or other insects. The quality of hosts differs with respect to the value and amount of resources they provide for the feeding larvae. Accordingly, the size of a clutch of eggs laid on a given host should be a function of host quality, because severe competition between developing larvae can lead to increased mortality and/or decreased size of the offspring, both causing a fitness loss for the offspring and the mother. Therefore, females should be selected for the ability to estimate host quality and to adjust their clutch size accordingly. Using the parasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) this study investigated the respective contribution of developmental mortality of offspring vs. the clutch size decision of the mother as a determinant of final offspring emergence per host. In addition, taking offspring size into account, the study examined the fitness consequences of female oviposition decisions. Developmental mortality was very low in all quality classes of hosts except previously frozen and thus dead host pupae. Females laid reduced clutch sizes on dead, previously parasitized, and smaller hosts. In contrast to offspring number, offspring size did not differ between host qualities. We conclude that females are able to sense the quality of a host and adjust the number of eggs they lay to mitigate larval competition.

Physiology vs. environment: what drives oviposition decisions in mango fruit flies (Bactrocera invadens and Ceratitis cosyra)?

AbstractIn frugivorous insects, the physiological state of the female (e.g. age, egg load) as well as environmental parameters like fruit availability and characteristics may affect oviposition decision, host choice and the resulting clutch size. We studied host acceptance and clutch size decision as a function of fly egg load as physiological state and mango variety and ripeness stage as the environmental parameter in two major mango pests in sub‐Saharan Africa, Bactrocera invadens and Ceratitis cosyra, under laboratory conditions. In addiction, egg maturation dynamics were investigated because for both species, egg production had never been explored before. Female egg load was the most important factor influencing host acceptance in both species. With respect to fruit characteristics, ripeness stage was significant for oviposition decisions only in C. cosyra. In particular, ripe and fully ripe fruits had more probability of oviposition than unripe ones. In contrast, fruit variety affected clutch size in B. invadens, with, respectively, the local variety Ngowe receiving the biggest clutches and the export Kent the smallest. Moreover, the invasive species showed a significantly higher egg production compared with the native species. Implications in terms of competitive displacement between the two species are also discussed.

Dynamic virulence in a parasitoid wasp: the influence of clutch size and sequential oviposition on egg encapsulation

We examined factors affecting the virulence of Metaphycus flavus (Hymenoptera: Encyrtidae), a facultatively gregarious endoparasitoid of Coccus hesperidum (Hemiptera: Coccidae). Clutch size significantly negatively influenced encapsulation rates of the parasitoid’s eggs by the host (in some cases encapsulation rates increased two-fold in incomplete clutches of eggs). Clutches were smaller when individuals sequentially parasitized two hosts in a patch. This resulted in increased egg encapsulation rates in the second parasitized host. Our results suggest that increased encapsulation rates in second hosts are due not entirely to clutch size, but also possibly to the depletion of chemicals with immunosuppressive properties that individual wasps inject inside hosts during oviposition. This hypothesis is also supported by the fact that 4 h after the first oviposition experience wasp virulence decreased, whereas 48 h after oviposition experience virulence was regained. Our results suggest that parasitoid virulence is dynamic because it is directly linked with clutch size decisions. However, clutch size in synovigenic, egg-limited parasitoids such as M. flavus is influenced by several parameters such as egg load, experience, host availability and physiological state. This study has implications for understanding how constraints on the evolution of solitary to gregarious larval development have been overcome: the allocation of multiple eggs to suppress host immune defences could serve as the first step in the transition from solitary to gregarious development. We also discuss how larval immobility within a host and other life history characteristics of this species further facilitate this transition.

Females increase current reproductive effort when future access to males is uncertain

Trade-offs between current and future reproduction shape life histories of organisms, e.g. increased mortality selects for earlier reproductive effort, and mate limitation has been shown to shape male life histories. Here, we show that female life histories respond adaptively to mate limitation. Female common gobies (Pomatoschistus microps) respond to a female-biased operational sex ratio by strongly increasing the size of their first clutch. The plastic response is predicted by a model that assumes that females use the current competitive situation to predict future difficulties of securing a mating. Because female clutch size decisions are much more closely linked to population dynamics than male life-history traits, plastic responses to mate-finding limitations may be an underappreciated force in population dynamics.

How two different host species influence the performance of a gregarious parasitoid: host size is not equal to host quality

1. Hyssopus pallidus Askew (Hymenoptera, Eulophidae) is a gregarious ectoparasitoid of the two tortricid moths species Cydia molesta Busck and C. pomonella L. (Lepidoptera, Tortricidae). It paralyses and parasitizes different larval instars of both species inside the apple fruit, which leads to the death of the caterpillar. 2. We assessed the influence of host species characteristics and host food on the performance of the parasitoid female in terms of clutch size decisions and fitness of the F(1) generation. 3. A comparison of clutch size revealed that female parasitoids deposited similar numbers of eggs on the comparatively smaller C. molesta hosts as on the larger C. pomonella hosts. The number of parasitoid offspring produced per weight unit of host larva was significantly higher in C. molesta than in C. pomonella, which is contrary to the general prediction that smaller hosts yield less parasitoid offspring. However, the sex ratio was not influenced by host species that differed considerably in size. 4. Despite the fact that less host resources were available per parasitoid larva feeding on C. molesta caterpillars, the mean weight of emerging female wasps was higher in the parasitoids reared on C. molesta. Furthermore, longevity of these female wasps was neither influenced by host species nor by the food their host had consumed. In addition we did not find a positive relationship between adult female weight and longevity. 5. Parasitoid females proved to be able to assess accurately the nutritional quality of an encountered host and adjust clutch size accordingly. These findings indicate that host size is not equal to host quality. Thus host size is not the only parameter to explain the nutritional quality of a given host and to predict fitness gain in the subsequent generation.

Clutch size decisions of a gregarious parasitoid under laboratory and field conditions

Under field conditions, insect parasitoids probably experience lower rates of host encounter and life expectancy than under optimal conditions in laboratory studies. We examined the clutch size response of Mastrus ridibundus, a gregarious idiobiont parasitoid of codling moth, Cydia pomonella, cocoons, to variation in both host encounter rate and life expectancy as possible explanatory variables in a comparison of brood size in the field and laboratory. Under laboratory conditions, mean clutch size (number of eggs laid) declined from 5.8 to 3.4 as host encounter rate increased from one to eight cocoons per day. In contrast, when we reduced life expectancy by withholding honey as a food source, females did not adjust clutch size. Mean brood size (number of progeny surviving to pupation) of females foraging in walnut orchards (3.9) was significantly greater than that under laboratory conditions with excess hosts (3.1). Brood size also increased with host size in the field, but not under laboratory conditions. Brood size fitness curves were derived using both host-finding ability in the field and lifetime fecundity under laboratory conditions as indices of female fitness. Host-finding ability increased exponentially with body size, generating an estimated Lack brood size of 4.3, but lifetime fecundity increased linearly with body size, giving a Lack brood size estimate of 5.5. Under field conditions, female M.ridibundus produced brood sizes that closely approximated the Lack brood size estimated from host-finding ability, but that were significantly smaller than that estimated from lifetime fecundity. These observations suggest that, in contrast to lifetime fecundity measures from the laboratory, host-finding ability in the field provides a more accurate estimate of lifetime reproductive success for parasitoids with a low expectation of future reproduction. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Egg recognition and counting reduce costs of avian conspecific brood parasitism.

Birds parasitized by interspecific brood parasites often adopt defences based on egg recognition but such behaviours are puzzlingly rare in species parasitized by members of the same species. Here I show that conspecific egg recognition is frequent, accurate and used in three defences that reduce the high costs of conspecific brood parasitism in American coots. Hosts recognized and rejected many parasitic eggs, reducing the fitness costs of parasitism by half. Recognition without rejection also occurred and some hosts banished parasitic eggs to inferior outer incubation positions. Clutch size comparisons revealed that females combine egg recognition and counting to make clutch size decisions--by counting their own eggs, while ignoring distinctive parasitic eggs, females avoid a maladaptive clutch size reduction. This is clear evidence that female birds use visual rather than tactile cues to regulate their clutch sizes, and provides a rare example of the ecological and evolutionary context of counting in animals.

Vive la variance: a functional oviposition theory for insect herbivores

AbstractWe developed state‐dependent life‐history theory to explain the variance in clutch size decisions made by insect herbivores under a variety of ecological scenarios. An important aspect of our theory is explicit representation of the distribution of host quality and frequency of occurrence. Examination of the theory suggests that clutch size decisions can be highly non‐linear with respect to host quality and variability. We then use our theory to explore the potential for bet‐hedging strategies to evolve as a function of unpredictable catastrophic events that decimate entire clutches. Our analysis suggests that the benefits to employing such a strategy will frequently be outweighed by costs brought on by delayed oviposition.

Effects of parental survival on clutch size decisions in fluctuating environments

Whereas in constant environments parental survival has no effect on optimal clutch size in the absence of trade-offs between juvenile and parental survival, the situation is drastically different in fluctuating environments. We consider a model in which, with respect to reproduction, parents and offspring are equivalent at the start of the next breeding season. When generations are non-overlapping, the clutch size maximizing geometric mean surviving number of offspring is optimal among all pure clutch size strategies. We prove that, as parental survival increases relative to that of the offspring, the optimal clutch size converges to the arithmetic mean maximizing clutch size (the so-called ‘Lack clutch size’). We also give a numerical procedure for calculating optimal mixed strategies and we show that, as environmental variance increases and/or parental survival decreases, mixed rather than pure strategies become optimal. Furthermore, we explain how to estimate fitness from empirical data under the assumptions of our model.

The Influence of Competition between Foragers on Clutch Size Decisions in Insect Parasitoids

The effect of competition between ovipositing females on their clutch size decisions is studied in parasitoid insects. The effect of this competition depends on whether the competition between parasitoid larvae within a host is contest (solitary parasitoids) or scramble competition (gregarious parasitoids). For gregarious parasitoids, a decreasing clutch size with increasing competition between females is predicted while for solitary parasitoids an increase is predicted. These predictions mere tested using the gregarious parasitoid Aphaereta minuta (M. E. Visser, 1996, Behav. Ecol. 7, 109-114) and the solitary parasitoid Comperiella bifasciata (J. A. Rosenheim and D. Hongkham, 1996, Anim. Behav. 51, 841-852). Parasitoids were either kept alone or in groups before the experiments, in which they were introduced singly into a patch containing unparasitized hosts. In the experiment with A. minuta, females kept together before the experiment laid smaller clutches than females kept alone. In C. bifasciata, the clutch size laid by females kept together was larger than that of females kept alone. Thus, both predictions were supported. [KEYWORDS: parasitoids; clutch size; competition; Aphaereta minuta; Comperiella bifasciata Hymenoptera; superparasitism; patch; oviposition; braconidae; allocation; females; wasp]

When should a female avoid adding eggs to the clutch of another female? A simultaneous oviposition and sex allocation game

Avoidance of double oviposition (ADO) is the strategy not to oviposit on food patches where another female has oviposited before. If two females oviposit on the same patch, competitive and mating interactions within and between broods may lead to both a clutch size game and a sex allocation game between the two visitors. Though the two games interact, they are usually considered separately. Here, the ESS conditions for ADO are investigated in an analysis that combines the two games into one. The analysis strengthens the notion that it is really ADO that needs to be explained, because role-dependent net pay-off from an additional egg is most likely to favour double oviposition (DO). To a first female, the net payoff includes the effect on the eggs already present, whereas to a second female only the egg's gross pay-off matters. ADO is the evolutionary stable strategy (ESS) if there are enough patches still without eggs and either (1) the fitness of an additional egg is so low that the first female would not lay it even in the absence of detrimental effects on earlier offspring, so neither would a second female, or (2) differences in either the survival probability of the offspring or their reproductive success are sufficient to counterbalance the differential interest in the eggs already present. The first condition requires that eggs are relatively large, because then the decrease in pay-off between two successive eggs can be large. The second condition may be met when there is a time interval between ovipositions of subsequent females. The resulting developmental lag of the second clutch will (1) diminish its ability to compete for food and (2) lower its reproductive success when there is local mate competition and sons are too late to mate with daughters of the first female. If sons of first and second females compete on equal terms, however, ADO is unlikely. Male migration between patches reduces the influence of sex allocation strategies on clutch size decisions; the same holds for small clutch sizes. To illustrate the importance of considering sex allocation and clutch size decisions in an integrated way, oviposition strategies of plant-inhabiting predatory mites (Acari: Phytoseiidae) are discussed.

The influence of competition between foragers on clutch size decisions in an insect parasitoid with scramble larval competition

The effect of competition between ovipositing females on their clutch size decisions is studied in animals that lay their eggs in discrete units of larval food (hosts). In such species the effect of competition depends on the form of the larval competition within such units. In insect parasitoids, there might either be contest (solitary parasitoids) or scramble competition (gregarious parasitoids) between larvae within a host For gregarious parasitoids, a decreasing clutch size with increasing competition between foragers is predicted. This prediction is tested in experiments using the parasitoid Aphaertta minuta. Parasitoids were either kept alone or in groups of four before the experiment, in which they were introduced singly in a patch containing unparasitized hosts. Animals kept together laid on average clutches of 0.74 eggs smaller than females kept alone (average clutch is 5.3), thereby confirming the prediction. Clutch size decreased with encounter number, which might be due to the adjustment of the female's estimate of the encounter rate with hosts. Finally, the results are compared with those reported for solitary parasitoids (that have scramble larval competition), for which it is predicted that the clutch size will increase with increasing levels of competition between females.

Pre-incubation feeding activities and energy budgets of Snow Geese: can food on the breeding grounds influence fecundity?

The potential contribution of early spring feeding conditions in the Arctic to clutch size variation was examined in a population of Lesser Snow Geese Anser caerulescens caerulescens. Behavioural observations were combined with energetic analyses of food material to derive an estimate of the energy budgets of pre-laying and laying females. Food intake of females between arrival on the breeding grounds and incubation was considerable; estimated energy gains in this period were in the same magnitude as the cost of one or several eggs. The pre-laying period spent on the breeding grounds can thus be energetically beneficial rather than costly. Accumulation of resources for reproduction in Snow Geese is a continual process including the breeding grounds, and nutrient limitation after arrival in the Arctic cannot sufficiently explain the environmental component of clutch size variation. The timing of migration and follicle development is such that clutch size decisions are sometimes made during the late stages of migration and some-times after arrival. In the latter case food conditions on the breeding grounds may greatly influence clutch size; in the former case they may still influence readjustments of clutch size after the initial decision. The universal negative correlation between clutch size and laying date in Snow Geese can be explained by negative fitness consequences of late hatching, which outweigh the benefits of delayed laying and further nutrient accumulation. Food shortage on the breeding grounds may sometimes be a secondary factor contributing to seasonal clutch size decline.

Clutch Size in a Larval-Pupal Endoparasitoid: Consequences for Fitness

1. Aphaereta minuta (Hymenoptera: Braconidae) is a gregarious larval-pupal endoparasitoid of many Diptera species. Several larval instars can be parasitized and the size differences between host species can be considerable. After parasitization, however, the host larva continues to grow and the parasitoid's eggs hatch after the host pupates. We question whether this delay between the moment of oviposition and that of resource availability for offspring development hampered the ovipositing female in making optimal clutch size decisions. 2. Using an optimality approach we analysed the relationship between clutch size (number of eggs) and fitness in different instars of the host Delia antiqua in the laboratory. 3. Clutch size was artificially manipulated, and the relationship between clutch size and fitness was quantified using the following parameters: offspring egg to adult survival, sex ratio of emerging adults and size of emerging daughters (since size and number of eggs are positively correlated, size is a measure of fecundity). 4. Survival to adult stage was slightly positively correlated with clutch size in first instar host larvae and negatively correlated with clutch size in second instar host larvae. Sex ratio (proportion daughters) increased with increasing clutch size. The size of both males and females on emergence was negatively related to clutch size, and more strongly to the number of emerging adults. 5. The calculated Lack clutch size (whereby fitness is maximized per clutch) increased with larval host stage, as did the observed clutch size. 6. For each instar the observed clutch size was lower than the calculated Lack clutch size. We argue that under natural conditions females are selected to lay a clutch lower than the Lack clutch size.

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

AbstractWilson 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.

Clutch size in a larval-pupal endoparasitoid : 1. Variation across and within host species.

Clutch size decisions by Aphaereta minuta (Nees) (Hymenoptera: Braconidae), a polyphagous, gregarious, larval-pupal endoparasitoid, were studied under laboratory conditions. This parasitoid attacks larvae of Diptera inhabiting ephemeral microhabitats such as decaying plant and animal material. Females oviposit in young larval stages, but the eventual size of the host pupa determines host food availability for competing offspring. The size of the pupa can differ greatly between host species. We questioned how A. minuta females deal with this delay between the moment of oviposition and eventual host food availability, and whether they make clutch size decisions that benefit their fitness. It was shown that females indeed vary their clutch size considerably and in an adaptive way: (1) females lay larger clutches in larvae of host species that produce larger pupae, even when the larvae are the same size at the moment of oviposition, and (2) females lay larger clutches in larger larvae than in smaller larvae of the same host species. The latter seems functional as larvae parasitized at an older stage indeed developed into larger pupae compared to larvae parasitized at a younger stage. Furthermore, mortality of parasitized young host larvae was greater than that of both unparasitized larvae and parasitized older larvae. Under field conditions the risk of mortality of young host larvae is expected to be even higher due to the limited period of microhabitat (host food) availability, strong scramble type competition between the host larvae, and the longer period of being exposed to predation.