Parasitoid developmental mortality in the field: patterns, causes and consequences for sex ratio and virginity

1. Sex ratio theory predicts that developmental mortality can affect sex ratio optima under Local Mate Competition and also lead to ‘virgin’ broods containing only females with no sibling-mating opportunities on maturity. 2. Estimates of developmental mortality and its sex ratio effects have been laboratory based, and both models and laboratory studies have treated mortality as a phenomenon without identifying its biological causes. 3. We contribute a large set of field data on Metaphycus luteolus Timberlake (Hymenoptera: Encyrtidae), an endoparasitoid of soft scale insects (Hemiptera: Coccidae), which has sex allocation conditional on host quality and female-biased brood sex ratios. Developmental mortality within broods can be both assessed and attributed to distinct causes, including encapsulation by the host and larval–larval competition. 4. Thirty per cent of M. luteolus offspring die during development with 65% of this mortality because of encapsulation and 28% because of larval competition. The distributions of mortality overall and for each cause of mortality separately were overdispersed. 5. The probability of an individual being encapsulated increased with clutch size, while the probability of being killed by a brood mate declined with increasing clutch size and with increasing per capita availability of resources. 6. The sexual compositions of broods at emergence were influenced by both the degree and the type of mortality operating. At higher levels of mortality, single sex broods were more common and sex ratios were less precise. Overall, virginity was more prevalent than predicted and was more greatly affected by the occurrence of competition than by other sources of mortality, almost certainly because competition tended to eliminate males. 7. The reproductive and developmental biology of M. luteolus appears to be influenced by a complex interplay of maternal clutch size and sex allocation strategies, offspring–offspring developmental interactions, host defence mechanisms and postemergence mating behaviour. Despite the great sophistication of sex ratio theory, it has not yet evolved to the point where it is capable of considering all of these influences simultaneously

Detecting non-binomial sex allocation when developmental mortality operates

Optimal sex allocation theory is one of the most intricately developed areas of evolutionary ecology. Under a range of conditions, particularly under population sub-division, selection favours sex being allocated to offspring non-randomly, generating non-binomial variances of offspring group sex ratios. Detecting non-binomial sex allocation is complicated by stochastic developmental mortality, as offspring sex can often only be identified on maturity with the sex of non-maturing offspring remaining unknown. We show that current approaches for detecting non-binomiality have limited ability to detect non-binomial sex allocation when developmental mortality has occurred. We present a new procedure using an explicit model of sex allocation and mortality and develop a Bayesian model selection approach (available as an R package). We use the double and multiplicative binomial distributions to model over- and under-dispersed sex allocation and show how to calculate Bayes factors for comparing these alternative models to the null hypothesis of binomial sex allocation. The ability to detect non-binomial sex allocation is greatly increased, particularly in cases where mortality is common. The use of Bayesian methods allows for the quantification of the evidence in favour of each hypothesis, and our modelling approach provides an improved descriptive capability over existing approaches. We use a simulation study to situations where current methods fail, and we illustrate the approach in real scenarios using empirically obtained datasets on the sexual composition of groups of gregarious parasitoid wasps demonstrate substantial improvements in power for detecting non-binomial sex allocation in situations where current methods fail, and we illustrate the approach in real scenarios using empirically obtained datasets on the sexual composition of groups of gregarious parasitoid wasps

Reproductive efficiency of the bethylid wasp Cephalonomia tarsalis: the influences of spatial structure and host density

The parasitoid wasp Cephalonomia tarsalis (Ashmead) (Hymenoptera: Bethylidae) is commonly present in stored product facilities. While beneficial, it does not provide a high 24 degree of biological pest control against its host, the saw-toothed beetle Oryzaephilus surinamensis (L.) (Coleoptera: Silvanidae). A candidate explanation for poor host population suppression is that adult females interfere with each other’s foraging and reproductive behavior. We used simple laboratory microcosms to evaluate such mutual interference in terms of its overall effects on offspring production. We varied the density of the hosts and also the spatial structure of the environment, via the extent of population sub-division and the provision of different substrates. Production of C. tarsalis offspring was positively influenced by host density and by the isolation of females. With incomplete sub-division within microcosms offspring production was, in contrast, low and even zero. The provision of corrugated paper as a substrate enhanced offspring production and partially mitigated the effects of mutual interference. We recommend simple improvements to mass rearing practice and identify promising areas for further behavioral and chemical studies towards a better understanding of the mechanisms of mutual interference

Efficacy of entomopathogenic fungi against large pine weevil, Hylobius abietis, and their additive effects when combined with entomopathogenic nematodes

The large pine weevil Hylobius abietis is an important pest of reforestation in northern Europe. In field trials, we assessed the efficacy of entomopathogenic fungi (EPF) alone and in combination with entomopathogenic nematodes (EPN) against immature stages. We used commercial strains of Metarhizium brunneum and Beauveria bassiana and a strain of Beauveria caledonica isolated from the pest’s habitat. The EPN used were Steinernema carpocapsae and Heterorhabditis downesi. Efficacy was assessed by weevil infection in stumps and by numbers of adult weevils emerging in traps above the stumps. EPF infected up to 23% of pine weevils, at depths up to 25 cm below ground. Three EPF application methods were compared, but application method did not affect infection rates. When applied at half doses, EPF and EPN had additive effects: M. brunneum and S. carpocapsae caused a reduction in emergence of 58% relative to control, M. brunneum and H. downesi 93%, B. caledonica and H. downesi 86%. EPN alone offered good suppression of H. abietis populations and suppression by the mixture did not surpass suppression afforded by EPN alone. Our trials show B. caledonica is a promising species, rivalling the success of the other two species. Applied EPF, especially M. brunneum, can persist for at least 2 years in the forest setting. Additionally, different fungi can have differential action against weevils above versus below ground; therefore, EPF combinations may be beneficial. Based on our trials, further development of strains and application methods are required before EPF can be recommended for suppression of pine weevil. © 2018 Springer-Verlag GmbH Germany, part of Springer Natur

Efficacy of entomopathogenic nematodes for control of large pine weevil, Hylobius abietis: effects of soil type, pest density and spatial distribution

The large pine weevil Hylobius abietis (L.), LPW, is a major pest of trees in replanted coniferous forests in northern Europe. The use of entomopathogenic nematodes (EPNs) applied against developing stages for population suppression is increasingly recognized as an effective alternative to plant protection using chemical pesticides. Here, we report results from a series of trials we conducted over 2 years using two species of EPN, Steinernema carpocapsae (Weiser) and Heterorhabitis downesi (Stock, Griffin, and Burnell) with different foraging strategies. Trials were conducted at lodgepole pine sites in Ireland on both mineral and peat soil type. EPN suspension was applied to the stumps of felled pine trees, and EPN efficacy was determined afterwards by directly assessing parasitism rates after debarking one quarter of the stumps and by collecting emerging adult weevils from traps erected over other treated and control stumps. Our results suggest that both species of EPN are equally effective in suppressing LPW populations to below the current, informal thresholds of economic damage. EPN were equally efficient in controlling LPW in peat and in mineral (lithosols/regosols and acid brown earth/brown podzolics) soils. Weevil density and distribution within pine stumps in peat versus mineral sites can explain patterns of LPW parasitism and suppression. Our results also suggest that infestation level (number of weevils per stump) can be an important factor in forecasting EPN application success as there is evidence of negative density-dependent parasitism when weevil densities were high. © 2016 Springer-Verlag Berlin Heidelber

Objective and subjective components of resource value in lethal fights between male entomopathogenic nematodes

Males sometimes engage in fights over contested resources such as access to mates; in this case, fighting behaviour may be adjusted based on the value they place on the females. Resource value (RV) can have two components. First, males can assess the quality of females, which constitutes an objective assessment of RV. Second, internal state such as previous mating experience can also influence motivation to fight thus constituting a subjective assessment of RV. If mating opportunities are scarce and available females have a major impact on the lifetime reproductive success of males, then fighting can be fatal; in this situation it is uncertain whether males would adjust fighting behaviour based on RV. We found that both female quality, that is, virginity (objective component of RV) and male mating status (subjective component of RV) influenced fighting intensity between males of the entomopathogenic nematode Steinernema longicaudum which engage in lethal fights. Male nematodes were more likely to engage in fighting and fought longer and more frequently in the presence of virgin (high-quality) females than in the presence of mated (lower-quality) females. Male mating status was also found to influence fighting behaviour: mated males were the winners in staged fights between mated and virgin males. Mated males may have superior fighting ability (greater resource-holding potential), but RV asymmetries between mated and virgin males cannot be excluded. Males were more likely to win when they were resident, but we did not find a significant interaction effect between male mating and residency status

Sustenance and performance: nutritional reserves, longevity and contest outcomes of fed and starved adult parasitoid wasps

Dyadic contests for possession of resources occur across a wide range of animal taxa, with contest outcome often being heavily influenced by the energetic reserves of the competitors. The majority of studied parasitoid wasps lack de novo lipogenesis, with adult lipid reserves being limited to those acquired throughout larval development. Carbohydrate- and lipid-rich adult diets can increase adult parasitoid lifespan and fecundity by potentially acting as a maintenance energy store. However, the effects of such diets on fat reserve compositions and some aspects of parasitoid behaviour contest outcome dynamics have not been examined. This study assesses the effect of a carbohydrate rich diet (honey) on the longevity, metabolic state and contest performance of Goniozus legneri, a bethylid wasp. The longevity of honey-fed diet adults was typically more than twice that of starved wasps. Compared to similarly-aged starved wasps, honey feeding increased concentrations of common haemolymph sugars and amino acids in a 3-day old and 7-day old wasps, and higher concentrations of stored lipid in7-day old wasps. However, nutritional status did not affect the outcome of dyadic contests over host possession when both contestants were either 3 days or 7 days old. While contest dynamics outcome may be unaffected by diet, it remains possible that an enhancing effect of feeding on contest ability is matched by an effect of higher value being placed on winning by starved wasps

Sex ratios, virginity, and local resource enhancement in a quasisocial parasitoid

Sclerodermus harmandi (Buysson) (Hymenoptera: Bethylidae) is an economically beneficial 2 species of parasitoid wasp that has an unusual level of sociality: groups of female foundresses 3 reproduce on a single host and exhibit cooperative post-ovipositional brood care. The 4 beneficial effects females have on each other’s reproductive success provide, via the theory 5 of local resource enhancement (LRE), an explanation for their female-biased progeny sex 6 ratios, which is part of the same framework for understanding sex-ratio evolution as the more 7 often invoked theory of local mate competition (LMC). Here we show that S. harmandi sex 8 ratios are over-dispersed, with high variance largely attributable to the common occurrence 9 (60%) of developmental mortality. Developmental mortality is also positively associated with 10 the proportion of broods which contain only females at emergence (virgin broods). Virginity 11 is more common when broods are produced by fewer foundresses. Virginity is expected to be 12 disadvantageous under LRE, as it is under LMC, but theory for LRE is less extensively 13 developed. We suggest approaches for the development of LRE theory, in particular using 14 models of ‘population elasticity’ in which the intensity of kin competition is reduced because 15 extra resources are available to local populations that are more cooperative. For S. harmandi, 16 such extra resources may include large hosts that can only be successfully utilized if multiple 17 foundresses cooperate