A benefit-risk analysis for biological control introductions based on the protection of native biodiversity.

The release of biological control agents has been an important means of controlling invasive species for over 150 years. While these releases have led to the sustainable control of over 250 invasive pest and weed species worldwide, a minority have caused environmental harm. A growing recognition of the risks of biological control led to a focus on risk assessment beginning in the 1990s along with a precipitous decline in releases. While this new focus greatly improved the safety of biological control, it came at the cost of lost opportunities to solve environmental problems associated with invasive species. A framework that incorporates benefits and risks of biological control is thus needed to understand the net environmental effects of biological control releases. We introduce such a framework, using native biodiversity as the common currency for both benefits and risks. The model is based on interactions among four categories of organisms: (1) the biological control agent, (2) the invasive species (pest or weed) targeted by the agent, (3) one or more native species that stand to benefit from the control of the target species, and (4) one or more native species that are at risk of being harmed by the released biological control agent. Conservation values of the potentially benefited and harmed native species are incorporated as well, and they are weighted according to three axes: vulnerability to extinction, the ecosystem services provided, and cultural significance. Further, we incorporate the potential for indirect risks to native species, which we consider will result mainly from the ecological process of agent enrichment that may occur if the agent exploits but does not control the target pest or weed. We illustrate the use of this framework by retrospectively analyzing the release of the vedalia beetle, Novius (= Rodolia) cardinalis, to control the cottony cushion scale, Icerya purchasi, in the Galapagos Islands. While the framework is particularly adaptable to biological control releases in natural areas, it can also be used in managed settings, where biological control protects native species through the reduction of pesticide use.

Corrigendum: Acute imidacloprid exposure alters mitochondrial function in bumblebee flight muscle and brain.

[This corrects the article DOI: 10.3389/finsc.2021.765179.].

Protective Geometry and Reproductive Anatomy as Candidate Determinants of Clutch Size Variation in Pentatomid Bugs.

AbstractMany animals lay their eggs in clusters. Eggs on the periphery of clusters can be at higher risk of mortality. We asked whether the most commonly occurring clutch sizes in pentatomid bugs could result from geometrical arrangements that maximize the proportion of eggs in the cluster's interior. Although the most common clutch sizes do not correspond with geometric optimality, stink bugs do tend to lay clusters of eggs in shapes that protect increasing proportions of their offspring as clutch sizes increase. We also considered whether ovariole number, an aspect of reproductive anatomy that may be a fixed trait across many pentatomids, could explain observed distributions of clutch sizes. The most common clutch sizes across many species correspond with multiples of ovariole number. However, there are species with the same number of ovarioles that lay clutches of widely varying size, among which multiples of ovariole number are not overrepresented. In pentatomid bugs, reproductive anatomy appears to be more important than egg mass geometry in determining clutch size uniformity. In addition, our analysis demonstrates that groups of animals with little variation in ovariole number may nonetheless lay a broad range of clutch shapes and sizes.

Reproductive performance effects of rearing the quasi-social parasitoid, Sclerodermus brevicornis (Hymenoptera: Bethylidae), on a factitious host.

Wasps in the genus Sclerodermus are ectoparasitoids that typically attack the larvae of woodboring coleopterans. Interest in these species is increasing as they are used in programs to control longhorn beetle pests of economic importance in China and have invasive pest control potential in Europe. Wasps may be mass reared for field release, but using the target host species can be time consuming and physically demanding. There is thus a need for factitious hosts with lower production costs and that are easier to rear. The present research focuses on Sclerodermus brevicornis, which was found in Italy in association with the invasive longhorn beetle, Psacothea hilaris hilaris, and can be laboratory reared on this longhorn beetle and on a factitious lepidopteran host, Corcyra cephalonica. As it is known that the biology of natural enemies can be influenced by the host they emerge from and that the behavior of S. brevicornis is relatively complex due to its degree of sociality (multiple foundress females cooperate to paralyze the host and produce offspring communally), we explored whether, and how, performance and behavioral traits of adult females are influenced by the host species on which they were reared, both when no choice or a choice of current host species was offered. We evaluated the survival of foundresses and their movements between offered hosts and their tendency to form groups with other foundresses according to kinship and host characteristics. We also evaluated the production of offspring and the timing of their development. We found that S. brevicornis reared from C. cephalonica do have some disadvantages compared with those that have developed on P. h. hilaris but also that they recognize, prefer, and can reproduce on P. h. hilaris. We conclude that the use of the more convenient factitious host for mass-rearing is unlikely to greatly compromise the potential of S. brevicornis to suppress longhorn beetle pests in the field.

Trait-based approaches to predicting biological control success: challenges and prospects.

Identifying traits that are associated with success of introduced natural enemies in establishing and controlling pest insects has occupied researchers and biological control practitioners for decades. Unfortunately, consistent general relationships have been difficult to detect, preventing a priori ranking of candidate biological control agents based on their traits. We summarise previous efforts and propose a series of potential explanations for the lack of clear patterns. We argue that the quality of current datasets is insufficient to detect complex trait-efficacy relationships and suggest several measures by which current limitations may be overcome. We conclude that efforts to address this elusive issue have not yet been exhausted and that further explorations are likely to be worthwhile.

Individual- and group-level sex ratios under local mate competition: consequences of infanticide and reproductive dominance.

Extremely female-biased sex ratios of parasitoid wasps in multiple-foundress groups challenges evolutionary theory which predicts diminishing bias as foundress numbers increase. Recent theory based on foundress cooperation has achieved qualitative rather than quantitative success in explaining bias among parasitoids in the genus Sclerodermus. Here, we develop an explanation, expanding the theory of local mate competition, based on the observation that male production seems dominated by some foundresses within groups. Two sex ratio effects arise from such reproductive dominance: an immediate effect via suppression of male production, and a long-term evolutionary response to reproductive skew. We analyze the outcome of these effects at the individual and group level, the latter being more readily observable. Three model scenarios are analyzed: (1) random killing of developing sons in a group by all foundresses, without reproductive skew, (2) the development of reproductive dominance by some foundresses after sex allocation decisions by all foundresses have been implemented, and (3) reproductive dominance within foundress groups before sex allocation decisions are implemented. The 3 scenarios have subtly different implications for sex ratio evolution, with Models 2 and 3 being novel additions to theory, showing how reproductive dominance can alter the outcome of sex ratio evolution. All models match observations in their outcomes better than other recently proposed theory, but Models 2 and 3 are closest to observations in their underlying assumptions. Further, Model 2 shows that differential offspring mortality after parental investment can influence the primary sex ratio even when random with respect to parental and offspring characters, but targeted at entire clutches. The novel models are solved for both diploid and haplodiploid genetic systems, and confirmed with simulations. Overall, these models provide a feasible explanation for the extremely female-biased sex ratios produced by multi-foundress groups and expand the scope of local mate competition theory to consider reproductive dominance.

The evolutionarily stable strategy, animal contests, parasitoids, pest control and sociality.

The evolutionarily stable strategy, ESS, concept was first used in biology to understand sex ratio bias and, shortly afterwards, to explore the logic of contests over essential and indivisible resources. ESS models formed the basis of much subsequent research on animal behaviour and placed game-theoretic thinking firmly within the behavioural ecology approach. Among behavioural ecologists studying parasitoids, it was those asking questions about the evolution of sex ratios who first made extensive use of the game-theoretic approach. A later growth of interest in parasitoid host defence and fighting behaviour made use of these tractable study species to explore contests and their connections to further aspects of life-history evolution plus some pest control applications. Our aims are to (i) introduce the topic of contests, which are engaged in by a very wide array of animal taxa, and the importance, both historical and conceptual, of the game-theoretic approach to their study, and (ii) review recent studies of parasitoid contests, including those that have considered the context of social evolution and the performance of parasitoids as agents of biological control. We consider that game-theoretic models are eminently testable and applicable and will likely endure as valuable tools in studies of parasitoid biology. This article is part of the theme issue 'Half a century of evolutionary games: a synthesis of theory, application and future directions'.

Dynamic Economic Thresholds for Insecticide Applications Against Agricultural Pests: Importance of Pest and Natural Enemy Migration.

In Integrated Pest Management programs, insecticides are applied to agricultural crops when pest densities exceed a predetermined economic threshold. Under conditions of high natural enemy density, however, the economic threshold can be increased, allowing for fewer insecticide applications. These adjustments, called 'dynamic thresholds', allow farmers to exploit existing biological control interactions without economic loss. Further, the ability of natural enemies to disperse from, and subsequently immigrate into, insecticide-sprayed areas can affect their biological control potential. We develop a theoretical approach to incorporate both pest and natural enemy movement across field borders into dynamic thresholds and explore how these affect insecticide applications and farmer incomes. Our model follows a pest and its specialist natural enemy over one growing season. An insecticide that targets the pest also induces mortality of the natural enemy, both via direct toxicity and reduced resource pest densities. Pest and natural enemy populations recover after spraying through within-field reproduction and by immigration from neighboring unsprayed areas. The number of insecticide applications and per-season farmer revenues are calculated for economic thresholds that are either fixed (ignoring natural enemy densities) or dynamic (incorporating them). The model predicts that using dynamic thresholds always leads to reduced insecticide application. The benefit of dynamic thresholds in reducing insecticide use is highest when natural enemies rapidly recolonize sprayed areas, and when insecticide efficacy is low. We discuss real-life situations in which monitoring of natural enemies would substantially reduce insecticide use and other scenarios where the presence of beneficial organisms may lead to threshold modifications.

Escaping the evolutionary trap: Can size-related contest advantage compensate for juvenile mortality disadvantage when parasitoids develop in unnatural invasive hosts?

The quality of hosts for a parasitoid wasp may be influenced by attributes such as host size or species, with high quality for successful development usually coincident with high quality for larger offspring. This is not always the case: for the Scelionid wasp Trissolcus basalis, oviposition in eggs of the Brown Marmorated Stink Bug, Halyomorpha halys, rather than of the normal host, the Southern Green Stink Bug, Nezara viridula, leads to lower offspring survival, but survivors can be unusually large. Adult female T. basalis engage in contests for host access. As larger contestants are typically favoured in contests between parasitoids, the larger size of surviving offspring may compensate for the mortality of others. We construct a general game-theoretic model to explore whether size advantage can sustain a maternal preference to utilize a more deadly host species. We find that size advantage alone is unlikely to sustain a shift in host preference, yet such an outcome is possible when size asymmetries act simultaneously with advantages in host possession (ownership effect). Halyomorpha halys is an invasive pest of major agro-economic importance in Europe and the Americas, and use of its eggs as hosts by native parasitoids such as T. basalis has been seen as an evolutionary trap due to their high developmental mortality. Our model suggests that the recently discovered effect of host choice on offspring size may provide an escape from the trap via effects on contest biology of T. basalis which could foster a more stable association with H. halys. An evolutionary shift in the reproductive value of H. halys could increase the efficiency of T. basalis as a biological control agent of this invasive stink bug pest.

Thiamethoxam exposure deregulates short ORF gene expression in the honey bee and compromises immune response to bacteria.

Maximizing crop yields relies on the use of agrochemicals to control insect pests. One of the most widely used classes of insecticides are neonicotinoids that interfere with signalling of the neurotransmitter acetylcholine, but these can also disrupt crop-pollination services provided by bees. Here, we analysed whether chronic low dose long-term exposure to the neonicotinoid thiamethoxam alters gene expression and alternative splicing in brains of Africanized honey bees, Apis mellifera, as adaptation to altered neuronal signalling. We find differentially regulated genes that show concentration-dependent responses to thiamethoxam, but no changes in alternative splicing. Most differentially expressed genes have no annotated function but encode short Open Reading Frames, a characteristic feature of anti-microbial peptides. As this suggested that immune responses may be compromised by thiamethoxam exposure, we tested the impact of thiamethoxam on bee immunity by injecting bacteria. We show that intrinsically sub-lethal thiamethoxam exposure makes bees more vulnerable to normally non-pathogenic bacteria. Our findings imply a synergistic mechanism for the observed bee population declines that concern agriculturists, conservation ecologists and the public.

Acute Imidacloprid Exposure Alters Mitochondrial Function in Bumblebee Flight Muscle and Brain.

Mitochondria are intracellular organelles responsible for cellular respiration with one of their major roles in the production of energy in the form of ATP. Activities with increased energetic demand are especially dependent on efficient ATP production, hence sufficient mitochondrial function is fundamental. In bees, flight muscle and the brain have particularly high densities of mitochondria to facilitate the substantial ATP production required for flight activity and neuronal signalling. Neonicotinoids are systemic synthetic insecticides that are widely utilised against crop herbivores but have been reported to cause, by unknown mechanisms, mitochondrial dysfunction, decreasing cognitive function and flight activity among pollinating bees. Here we explore, using high-resolution respirometry, how the neonicotinoid imidacloprid may affect oxidative phosphorylation in the brain and flight muscle of the buff-tailed bumblebee, Bombus terrestris. We find that acute exposure increases routine oxygen consumption in the flight muscle of worker bees. This provides a candidate explanation for prior reports of early declines in flight activity following acute exposure. We further find that imidacloprid increases the maximum electron transport capacity in the brain, with a trend towards increased overall oxygen consumption. However, intra-individual variability is high, limiting the extent to which apparent effects of imidacloprid on brain mitochondria are shown conclusively. Overall, our results highlight the necessity to examine tissue-specific effects of imidacloprid on respiration and energy production.

Adjustment of sex allocation to co-foundress number and kinship under local mate competition: An inclusive-fitness analysis.

Hamilton's theory of local mate competition (LMC) describes how competition between male relatives for mating opportunities favours a female-biased parental investment. LMC theory has been extended in many ways to explore a range of genetic and life-history influences on sex allocation strategies, including showing that increasing genetic homogeneity within mating groups should favour greater female bias. However, there has been no quantitative theoretical prediction as to how females should facultatively adjust their sex allocation in response to co-foundress number and kinship. This shortfall has been highlighted recently by the finding that sex ratios produced by sub-social parasitoid wasps in the family Bethylidae are affected by the number of co-foundresses and by whether these are sisters or unrelated females. Here we close this gap in LMC theory by taking an inclusive-fitness approach to derive explicit theoretical predictions for this scenario. We find that, in line with the recent empirical results, females should adopt a more female-biased sex allocation when their co-foundresses are less numerous and are their sisters. Our model appears to predict somewhat more female bias than is observed empirically; we discuss a number of possible model extensions that would improve realism and that would be expected to result in a closer quantitative fit with experimental data.

Factors Affecting the Reproduction and Mass-Rearing of Sclerodermus brevicornis (Hymenoptera: Bethylidae), a Natural Enemy of Exotic Flat-Faced Longhorn Beetles (Coleoptera: Cerambycidae: Lamiinae).

Many species of long-horned beetles are invasive pests causing significant economic damage in agro-forestry systems. They spend the majority of their life-cycle concealed inside natural wood or wooden packaging materials and are largely protected from adverse environmental conditions and pesticide sprays. Biological control via parasitoid natural enemies including members of the bethylid genus Sclerodermus, has proven effective against some long-horned beetles that are invasive in China. In Europe, the biocontrol potential of native Sclerodermus species is being evaluated with a view to developing efficient mass-rearing techniques and then actively deploying them against invasive Asian beetles. Here, we continue evaluations of S. brevicornis by establishing that groups of females that have already reared offspring to emergence are capable of reproducing subsequent hosts and by evaluating the lifetime reproductive capacity of individual females provided with successive hosts. Additionally, we assess the laboratory shelf-life of adult females stored for different times at different temperatures including cold storage, and then assess the post-storage reproductive performance of groups of females provided with a single host. We found that adult female longevity declines with increasing storage temperature and that most aspects of subsequent performance are negatively affected by high temperatures. The adaptability to low temperature storage enhances the suitability of S. brevicornis to mass-rearing programs and thus biocontrol deployment.

Co-foundress confinement elicits kinship effects in a naturally sub-social parasitoid.

Kinship among interacting individuals is often associated with sociality and also with sex ratio effects. Parasitoids in the bethylid genus Goniozus are sub-social, with single foundress females exhibiting post-ovipositional maternal care via short-term aggressive host and brood defence against conspecific females. Due to local mate competition (LMC) and broods normally being produced by a single foundress, sex ratios are female-biased. Contests between adult females are, however, not normally fatal, and aggression is reduced when competing females are kin, raising the possibility of multi-foundress reproduction on some hosts. Here, we screen for further life-history effects of kinship by varying the numbers and relatedness of foundresses confined together with a host resource and also by varying the size of host. We confined groups of 1-8 Goniozus nephantidis females together with a host for 5+ days. Multi-foundress groups were either all siblings or all nonsiblings. Our chief expectations included that competition for resources would be more intense among larger foundress groups but diminished by both larger host size and closer foundress relatedness, affecting both foundress mortality and reproductive output. From classical LMC theory, we expected that offspring group sex ratios would be less female-biased when there were more foundresses, and from extended LMC theory, we expected that sex ratios would be more female-biased when foundresses were close kin. We found that confinement led to the death of some females (11% overall) but only when host resources were most limiting. Mortality of foundresses was less common when foundresses were siblings. Developmental mortality among offspring was considerably higher in multi-foundress clutches but was unaffected by foundress relatedness. Groups of sibling foundresses collectively produced similar numbers of offspring to nonsibling groups. There was little advantage for individual females to reproduce in multi-foundress groups: single foundresses suppressed even the largest hosts presented and had the highest per capita production of adult offspring. Despite single foundress reproduction being the norm, G. nephantidis females in multi-foundress groups appear to attune sex allocation according to both foundress number and foundress relatedness: broods produced by sibling foundresses had sex ratios similar to broods produced by single foundresses (ca. 11% males), whereas the sex ratios of broods produced by nonsibling females were approximately 20% higher and broadly increased with foundress number. We conclude that relatedness and host size may combine to reduce selection against communal reproduction on hosts and that, unlike other studied parasitoids, G. nephantidis sex ratios conform to predictions of both classical and extended LMC theories.

Field evaluation of synthetic and neem-derived alternative insecticides in developing action thresholds against cauliflower pests.

Synthetic chemical pesticides can enhance crop yields but also have undesired effects. Alternative 'botanical insecticides' may also have non-target effects on pollinators and biocontrol services. Employing action thresholds (ATs) can reduce pesticide (whether synthetic or botanical) use compared to fixed-interval applications. Here the azadirachtin-based botanical formulation NeemAzal and a neem seed extract (NSE) were evaluated in field spraying trials alongside commonly-used synthetics (Voliam Flexi [chlorentraniliprole plus thiamethoxam] and imidacloprid) in developing ATs for the regular and cosmopolitan cauliflower pests Brevicoryne brassicae, Plutella xylostella and Spodoptera litura. We considered the size of the S. litura larvae infesting the crop in order to derive ATs. ATs per plant were higher for NeemAzal (0.55 larvae for P. xylostella and 3 larvae for large-sized S. litura) than for Voliam Flexi (0.30 larvae for P. xylostella and 0.80 larvae for S. litura) but were similar for B. brassicae (50 individuals). Higher ATs when using azadirachtin were associated with the diverse modes of action of botanicals, for instance NeemAzal and NSE deterred oviposition of S. litura. Although the exact values of ATs are likely to have regional limits, our approach can be applied for determining ATs against common lepidopteran and aphid pests in many other vegetable crop agro-ecosystems.

Direct and indirect influences of intercrops on the coconut defoliator Opisina arenosella.

Coconut palm (Cocos nucifera) infestation by Opisina arenosella (Lepidoptera: Oecophoridae) in the Indian subcontinent may occur in November to May each year in the same or adjoining areas of plantations. Parasitoids of O. arenosella may also be consistently present at these times. During other periods, pests and/or parasitoids could be maintained on intercrops that are commonly grown throughout the year. Field surveys of 54 intercrop species in Kerala, India, found that O. arenosella attacks banana, but not others, while laboratory screening showed that O. arenosella can mature on jack fruit, cashew and oil palm. Larvae of 20 lepidopteran species found on intercrops were screened for use by Goniozus nephantidis (Hymenoptera: Bethylidae), a larval parasitoid of O. arenosella, which oviposited on two species but its offspring failed to mature. Thirteen intercrop herbivore species were screened for use by Brachymeria nosatoi (Hymenoptera: Chalcididae), a pupal parasitoid of O. arenosella, which completed development on the pyralids Herculia nigrivita, Syllepte derogata and Psara basalis. Further, connectance trophic webs were compiled using prior field records of coconut, 33 species of intercrops, 58 species of lepidopteran herbivores and 29 species of primary parasitoids. Both laboratory and literature evidence suggests that populations of O. arenosella are unlikely to be maintained by feeding on intercrops or strongly influenced by direct competition with other lepidopterans but are likely to be affected by sharing parasitoids. Intercrop herbivores have clear potential for maintaining parasitoids of O. arenosella, and we recommend thirteen plant species as intercrops that should aid in conservation biocontrol.

Volatile Chemical Emission as a Weapon of Rearguard Action: A Game-Theoretic Model of Contest Behavior.

We use a game-theoretic model to explore whether volatile chemical (spiroacetal) emissions can serve as a weapon of rearguard action. Our basic model explores whether such emissions serve as a means of temporary withdrawal, preventing the winner of the current round of a contest from translating its victory into permanent possession of a contested resource. A variant of this model explores an alternative possibility, namely, that such emissions serve as a means of permanent retreat, attempting to prevent a winner from inflicting costs on a fleeing loser. Our results confirm that the underlying logic of either interpretation of weapons of rearguard action is sound; however, empirical observations on parasitoid wasp contests suggest that the more likely function of chemical weapons is to serve as a means of temporary withdrawal. While our work is centered around the particular biology of contest behavior in parasitoid wasps, it also provides the first contest model to explicitly consider self-inflicted damage costs and thus responds to a recent call by empiricists for theory in this area.

The impact of competition on elephant musth strategies: A game-theoretic model.

Mature male African Savannah elephants are known to periodically enter a temporary state of heightened aggression called "musth", often linked with increased androgens, particularly testosterone. Sexually mature males are capable of entering musth at any time of year, and will often travel long distances to find estrous females. When two musth bulls or two non-musth bulls encounter one another, the agonistic interaction is usually won by the larger male. However, when a smaller musth bull encounters a larger non-musth bull, the smaller musth male can win. The relative mating success of musth males is due partly to this fighting advantage, and partly to estrous females' general preference for musth males. Though musth behavior has long been observed and documented, the evolutionary advantages of musth remain poorly understood. Here we develop a game-theoretic model of male musth behavior which assumes musth duration as a parameter, and distributions of small, medium and large musth males are predicted in both time and space. The predicted results are similar to the musth timing behavior observed in the Amboseli National Park elephant population, and further results are generated with relevance to Samburu National Park. We discuss small male musth behavior, the effects of estrous female spatial heterogeneity on musth timing, conservation applications, and the assumptions underpinning the model.

PARTIALLY CONSTRAINED SEX ALLOCATION AND THE INDIRECT EFFECTS OF ASSISTED REPRODUCTIVE TECHNOLOGIES ON THE HUMAN SEX RATIO.

Infertility affects around 15% of human couples and in many countries approximately 1-4% of babies are born following Assisted Reproductive Technologies (ART). Several ART techniques are used and these differentially affect the sex ratio of offspring successfully produced. These direct effects on sex ratio also have the potential to influence, indirectly, the sex ratios of offspring born to untreated couples. This is of concern because human sex ratio bias may adversely affect public health. Here the extent of indirect effects of ART that could operate, via Fisherian frequency-dependent natural selection, on the progeny sex ratio of unassisted members of a population is heuristically modelled. Given the degrees to which ART techniques bias sex ratios directly, it is predicted that well over 20% of couples would have to reproduce via ART for there to be any discernible effect on the sex ratios produced, in response, by the remainder of the population. This value is greater than the estimated prevalence of infertility problems among human couples. It is concluded that providing ART to couples with fertility problems does not currently generate significant ethical issues or public health concern in terms of indirect effects on the offspring sex ratios of untreated couples.