Preference of Pentalonia nigronervosa for infected banana plants tends to reverse after Banana bunchy top virus acquisition.

Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae) is the vector of the Banana Bunchy Top Virus (BBTV), the most serious viral disease of banana (Musa spp.) in the world. Before acquiring the virus, the vector is more attracted to infected banana plants in response to the increased emissions of volatile organic compounds (VOCs). Here, we test the hypothesis that BBTV acquisition directly modifies the preference of P. nigronervosa for infected banana plants, and that the change in preference results from the alteration of the organs linked to the VOC detection or to the behaviour of the vector. We found that the preference of P. nigronervosa for infected banana plants reverses after virus acquisition in dessert banana, while it remains similar between healthy and infected banana plants before and after the acquisition of BBTV. At the same time, aphids reared on infected bananas had smaller forewing areas and hind tibia length than aphids reared on healthy bananas, although the number of secondary rhinaria on the antennae was lower on dessert banana-reared aphids than plantain-reared aphids, this was not affected by the infection status of the aphid. These results support the "vector manipulation hypothesis-VMH" of pathogens to promote their spread. They have implications for the BBTV management.

Deciphering the functional diversity of the gut microbiota of the black soldier fly (Hermetia illucens): recent advances and future challenges.

Bioconversion using insects is a promising strategy to convert organic waste (catering leftovers, harvest waste, food processing byproducts, etc.) into biomass that can be used for multiple applications, turned into high added-value products, and address environmental, societal and economic concerns. Due to its ability to feed on a tremendous variety of organic wastes, the black soldier fly (Hermetia illucens) has recently emerged as a promising insect for bioconversion of organic wastes on an industrial scale. A growing number of studies have highlighted the pivotal role of the gut microbiota in the performance and health of this insect species. This review aims to provide a critical overview of current knowledge regarding the functional diversity of the gut microbiota of H. illucens, highlighting its importance for bioconversion, food safety and the development of new biotechnological tools. After providing an overview of the different strategies that have been used to outline the microbial communities of H. illucens, we discuss the diversity of these gut microbes and the beneficial services they can provide to their insect host. Emphasis is placed on technical strategies and aspects of host biology that require special attention in the near future of research. We also argue that the singular digestive capabilities and complex gut microbiota of H. illucens make this insect species a valuable model for addressing fundamental questions regarding the interactions that insects have evolved with microorganisms. By proposing new avenues of research, this review aims to stimulate research on the microbiota of a promising insect to address the challenges of bioconversion, but also fundamental questions regarding bacterial symbiosis in insects.

The aphid Pentalonia nigronervosa (Hemiptera: Aphididae) takes advantage from the quality change in banana plant associated with Banana bunchy top virus infection.

Viral diseases can change plant metabolism, with potential impacts on the quality of the plant's food supply for insect pests, including virus vectors. The banana aphid, Pentalonia nigronervosa Coquerel, is the vector of the Banana bunchy top virus (BBTV), the causal agent of Banana bunchy top disease (BBTD), the most devastating viral disease of bananas in the world. The effect of BBTV on the life-history traits and population dynamics of P. nigronervosa remains poorly understood. We therefore studied the survival rate, longevity, daily fecundity per aphid, tibia length, population growth, and winged morph production of a P. nigronervosa clone grown on healthy or infected, dessert, or plantain banana plants. We found that daily fecundity was higher on infected banana than on healthy banana plants (plantain and dessert), and on plantain than on dessert banana plants (healthy and infected). Survival and longevity were lower on infected dessert bananas than on other types of bananas. In addition, virus infection resulted in a decrease in aphid hind tibia length on both plant genotypes. The survival and fecundity table revealed that the aphid net reproduction rate (Ro) was highest on plantains (especially infected plantain), and the intrinsic growth rate (r) was highest on infected plants. Finally, the increase of aphids and alate production was faster first on infected plantain, then on healthy plantain, and lower on dessert banana (infected and uninfected). Our results reinforce the idea of indirect and plant genotype-dependent manipulation of P. nigronervosa by the BBTV.

Combined light pollution and night warming as a novel threat to ecosystems.

Artificial light at night (ALAN) and night-time warming (NW) are a combined threat altering the night-time environment and the behaviour and physiology of organisms. Impacts on fitness and the nocturnal niche have knock-on effects for ecosystem structure and function. Understanding the way both stressors interact is critical for making ecological predictions.

Still standing: The heat protection delivered by a facultative symbiont to its aphid host is resilient to repeated thermal stress.

Insects have evolved diverse strategies to resist extreme high temperatures (EHT). The adaptive value of such strategies has to be evaluated when organisms experience multiple EHT events during their lifetime, as predicted in a changing climate. This is particularly the case for associations with facultative microbial partners involved in insect heat tolerance, the resilience of which to repeated heat stress has never been studied. We compared two artificial lines of the pea aphid (Acyrthosiphon pisum) differing by the absence or presence of the heat-protective facultative bacterium Serratia symbiotica. We exposed insect nymphs to a varying number of EHT events (between 0 and 3), and recorded fitness parameters. Except survival traits, fitness estimates were affected by the interaction between aphid infection status (absence/presence of S. symbiotica) and thermal treatment (number of heat shocks applied). Costs of bacterial infection were detected in the absence of thermal stress: symbiont-hosting aphids incurred longer development, decreased fecundity and body size. However, symbiotic infection turned neutral, and even beneficial for some traits (development and body size), as the number of heat shocks increased, and compared to the aposymbiotic strain. Conversely, symbiotic infection mediated aphid response to heat shock(s): fitness decreased only in the uninfected group. These findings suggest that (i) the facultative symbiont may alternatively act as a pathogen, commensal or mutualist depending on thermal environment, and (ii) the heat protection it delivered to its host persists under frequent EHT. We discuss eco-evolutionary implications and the role of potentially confounding factors (stage-specific effects, genetic polymorphism displayed by the obligate symbiont).

Thermal tolerance of the rosy apple aphid Dysaphis plantaginea and its parasitoids: Effect of low temperatures on some fitness activities of Aphidius matricariae.

Understanding the thermal tolerance of insect herbivores and their natural enemies is crucial for biological control programs. The rosy apple aphid Dysaphis plantaginea is one of the most problematic pests of apple orchards, causing economic losses of up to 30% due to damage to fruits. Dysaphis plantaginea is highly adapted to low temperature, enabling it to appear early in the season. This study aimed at evaluating the critical thermal minimum of D. plantaginea and of two parasitoid species: Aphidius matricariae and Ephedrus cerasicola. For the generalist parasitoid A. matricariae we also evaluated the fitness traits of flight, walking, and oviposition, at four temperatures: 20, 15, 10 and 8 °C. We found that both males and females did not fly at the two lowest temperatures. Walking, parasitism rate and sex ratio (proportion of female progeny) were reduced at 8 °C. In addition, the parasitism rate was significantly lower at 8 and 10 °C compared to 15 and 20 °C. The progeny emerging from the oviposition experiment at 8 °C were significantly larger compared with other temperatures, possibly attributed to longer development time. The fact that the parasitoids were unable to fly at 8 and 10 °C, in combination with a more male-biased sex ratio, could reduce their efficiency at low temperature, even though they may still be able to walk and parasitize aphids.

Composition and structure of winter aphid-parasitoid food webs along a latitudinal gradient in Chile.

All species interact in complex antagonistic or mutualistic networks that may be driven by turnover in species composition due to spatiotemporal environmental filtering. Therefore, studying differences in insect communities along environmental gradients may improve our understanding of the abiotic and biotic factors that shape the structure of trophic networks. Parasitoids are interesting models to do so, due to their intimate eco-evolutionary relationship with their hosts. We explored the differences in cereal aphid-parasitoid food webs during the winter among nine localities in Chilean central-south valley, along a gradient of 1200 km from north (29° S) to south (40° S). We hypothesized that diapause incidence would increase in the coldest areas, resulting in a lower number of parasitoid species active during the winter. Consequently, network specialization, generality, and vulnerability indexes should increase with decreasing latitude, which implies fewer and more weakly connected links per parasitoid species through an increased fraction of basal host species. Based on the severity of winter, three areas along the explored gradient were distinguished, but clustering did not follow a clear north-south latitudinal gradient. Instead, few differences were observed in overwintering strategies, with very low levels of diapause in all localities, and no major differences in food-web composition. The major differences along the gradient were the relative abundances of the different aphid, parasitoid and hyperparasitoid species, with higher levels of spatial and temporal variation observed for the less abundant species. Our results provide a better understanding of the activity and abundance of aphid parasitoids during winter in relation to climatic conditions.

Impact of heat stress on the fitness outcomes of symbiotic infection in aphids: a meta-analysis.

Beneficial microorganisms shape the evolutionary trajectories of their hosts, facilitating or constraining the colonization of new ecological niches. One convincing example entails the responses of insect-microbe associations to rising temperatures. Indeed, insect resilience to stressful high temperatures depends on the genetic identity of the obligate symbiont and the presence of heat-protective facultative symbionts. As extensively studied organisms, aphids and their endosymbiotic bacteria represent valuable models to address eco-evolutionary questions about the thermal ecology of insect-microbe partnerships, with broad relevance to various biological systems and insect models. This meta-analysis aims to quantify the context-dependent impacts of symbionts on host phenotype in benign or stressful heat conditions, across fitness traits, types of heat stress and symbiont species. We found that warming lowered the benefits (resistance to parasitoids) and costs (development, fecundity) of infection by facultative symbionts, which was overall mostly beneficial to the hosts under short-term heat stress (heat shock) rather than extended warming. Heat-tolerant genotypes of the obligate symbiont Buchnera aphidicola and some facultative symbionts (Rickettsia sp., Serratia symbiotica) improved or maintained aphid fitness under heat stress. We discuss the implications of these findings for the general understanding of the cost-benefit balance of insect-microbe associations across multiple traits and their eco-evolutionary dynamics faced with climate change.

Multi-scale approach to biodiversity proxies of biological control service in European farmlands.

Intensive agriculture has profoundly altered biodiversity and trophic relationships in agricultural landscapes, leading to the deterioration of many ecosystem services such as pollination or biological control. Information on which spatio-temporal factors are simultaneously affecting crop pests and their natural enemies is required to improve conservation biological control practices. We conducted a study in 80 winter wheat crop fields distributed in three regions of North-western Europe (Brittany, Hauts-de-France and Wallonia), along intra-regional gradients of landscape complexity. Five taxa of major crop pests (aphids and slugs) and natural enemies (spiders, carabids, and parasitoids) were sampled three times a year, for two consecutive years. We analysed the influence of regional (meteorology), landscape (structure in both the years n and n-1) and local factors (hedge or grass strip field boundaries, and distance to boundary) on the abundance and species richness of crop-dwelling organisms, as proxies of the service/disservice they provide. Firstly, there was higher biocontrol potential in areas with mild winter climatic conditions. Secondly, natural enemy communities were less diverse and had lower abundances in landscapes with high crop and wooded continuities (sum of interconnected crop or wood surfaces), contrary to slugs and aphids. Finally, field boundaries with grass strips were more favourable to spiders and carabids than boundaries formed by hedges, while the opposite was found for crop pests, with the latter being less abundant towards the centre of the fields. We also revealed temporal modulation-and sometimes reversion-of the impact of local elements on crop biodiversity. To some extent, these results cause controversy because they show that hedgerows and woodlots should not be the unique cornerstones of agro-ecological landscape design strategies. We point out that combining woody and grassy habitats to take full advantage of the features and ecosystem services they both provide (biological pest control, windbreak effect, soil stabilization) may promote sustainable agricultural ecosystems. It may be possible to both reduce pest pressure and promote natural enemies by accounting for taxa-specific antagonistic responses to multi-scale environmental characteristics.

Homeostasis theory: What can we learn from dormancy and symbiotic associations?

In this letter, I discuss the notion of dormancy that De Luca Jr. relies on to criticize the theory of homeostasis. In particular, I try to qualify the issues related to the fact that dormancy is not always a free behavior but is in most situations under the influence of environmental factors. To this end, I discuss diapause in arthropods, which can be obligatory (under the influence of endogenous commands) but which is in most cases facultative (under external command). I emphasize that the notion of stability of a dormant organism must be taken with caution. I briefly mention what the study of sleep in animals can contribute to the notion of homeostasis. Finally, I focus on the role of microbial symbionts and the notion of holobiont. Through this, I question the future of the notions of internal environment and homeostasis and I propose to revisit them in the context of the effects of species interactions on the physiology of organisms.

Effect of developmental temperatures on Aphidius colemani host-foraging behavior at high temperature.

Temperatures experienced by insects during their adult life often differ from developmental temperatures. Yet, developmental thermal acclimation can play an important role in shaping physiological, morphological, and behavioral traits at the adult stage. We explored how three rearing temperatures (10, 20, and 28 °C) affected host-foraging behaviors and associated traits under warm conditions in the parasitoid Aphidius colemani, a key model in behavioral ecology and an important natural enemy of aphids. Developmental time was longer at lower temperatures, resulting in bigger emerging parasitoids, with higher egg-loads. Parasitism rates, emergence rates, and parasitoid survival (once placed at high temperature) were the highest for parasitoids developed at 20 °C. When exposed to 28 °C, the expression of all behavioral items (time spent walking searching for hosts, number of antennal and ovipositor contacts with hosts) was higher for parasitoids reared at 20 °C, followed by those reared at 10 °C, then those reared at 28 °C. Finally, we showed that parasitoid residence time on aphid patches was determined by both developmental temperatures and the number of host encounter without oviposition, representative of the resource quality. We revealed that developing at 28 °C did not lead to increased adult performance at this temperature, probably because of complex interactions and trade-offs between developmental costs at high temperature and optimal foraging behaviors (e.g., parasitoid size and host-handling capacities). Our results strengthen the idea that thermal developmental plasticity may play an important role in insect behavioral responses to varying temperatures, and is important to consider in the context of climate change.

A perspective on insect-microbe holobionts facing thermal fluctuations in a climate-change context.

Temperature influences the ecology and evolution of insects and their symbionts by impacting each partner independently and their interactions, considering the holobiont as a primary unit of selection. There are sound data about the responses of these partnerships to constant temperatures and sporadic thermal stress (mostly heat shock). However, the current understanding of the thermal ecology of insect-microbe holobionts remains patchy because the complex thermal fluctuations (at different spatial and temporal scales) experienced by these organisms in nature have often been overlooked experimentally. This may drastically constrain our ability to predict the fate of mutualistic interactions under climate change, which will alter both mean temperatures and thermal variability. Here, we tackle down these issues by focusing on the effects of temperature fluctuations on the evolutionary ecology of insect-microbe holobionts. We propose potentially worth-investigating research avenues to (i) evaluate the relevance of theoretical concepts used to predict the biological impacts of temperature fluctuations when applied to holobionts; (ii) acknowledge the plastic (behavioural thermoregulation, physiological acclimation) and genetic responses (evolution) expressed by holobionts in fluctuating thermal environments; and (iii) explore the potential impacts of previously unconsidered patterns of temperature fluctuations on the outcomes and the dynamic of these insect-microbe associations.

Cascading effects of caffeine intake by primary consumers to the upper trophic level.

Secondary metabolites are central to understanding the evolution of plant-animal interactions. Direct effects on phytophagous animals are well-known, but how secondary consumers adjust their behavioural and physiological responses to the herbivore's diet remains more scarcely explored for some metabolites. Caffeine is a neuroactive compound that affects both the behaviour and physiology of several animal species, from humans to insects. It is an alkaloid present in nectar, leaves and even sap of numerous species of plants where it plays a role in chemical defences against herbivores and pathogens. Caffeine effects have been overlooked in generalist herbivores that are not specialized in coffee or tea plants. Using a host-parasitoid system, we show that caffeine intake at a relatively low dose affects longevity and fecundity of the primary consumer, but also indirectly of the secondary one, suggesting that this alkaloid and/or its effects can be transmitted through trophic levels and persist in the food chain. Parasitism success was lowered by ≈16% on hosts fed with caffeine, and parasitoids of the next generation that have developed in hosts fed on caffeine showed a reduced longevity, but no differences in mass and size were found. This study helps at better understanding how plant secondary metabolites, such as caffeine involved in plant-animal interactions, could affect primary consumers, could have knock-on effects on upper trophic levels over generations, and could modify interspecific interactions in multitrophic systems.

Developmental Temperature Affects Life-History Traits and Heat Tolerance in the Aphid Parasitoid Aphidius colemani.

Developmental temperature plays important roles in the expression of insect traits through thermal developmental plasticity. We exposed the aphid parasitoid Aphidius colemani to different temperature regimes (10, 20, or 28 °C) throughout larval development and studied the expression of morphological and physiological traits indicator of fitness and heat tolerance in the adult. We showed that the mass decreased and the surface to volume ratio of parasitoids increased with the development temperature. Water content was not affected by rearing temperature, but parasitoids accumulated more lipids when reared at 20 °C. Egg content was not affected by developmental temperature, but adult survival was better for parasitoids reared at 20 °C. Finally, parasitoids developed at 20 °C showed the highest heat stupor threshold, whereas parasitoids developed at 28 °C showed the highest heat coma threshold (better heat tolerance CTmax1 and CTmax2, respectively), therefore only partly supporting the beneficial acclimation hypothesis. From a fundamental point of view, our study highlights the role of thermal plasticity (adaptive or not) on the expression of different life history traits in insects and the possible correlations that exist between these traits. From an applied perspective, these results are important in the context of biological control through mass release techniques of parasitoids in hot environments.

Effects of Constant versus Fluctuating Temperatures on Fitness Indicators of the Aphid Dysaphis plantaginea and the Parasitoid Aphidius matricariae.

Testing fluctuating rather than constant temperatures is likely to produce more realistic datasets, as they are ecologically more similar to what arthropods experience in nature. In this study, we evaluated the impact of three constant thermal regimes (7, 12, and 17 °C) and one fluctuating thermal regime (7-17 °C with a mean of 12 °C) on fitness indicators in the rosy apple aphid Dysaphis plantaginea, a major pest of apple orchards, and the parasitoid Aphidius matricariae, one of its natural enemies used in mass release biological control strategies. For some-but not all-traits, the fluctuating 7-17 °C regime was beneficial to insects compared to the constant 12 °C regime. Both aphid and parasitoid development times were shortened under the fluctuating regime, and there was a clear trend towards an increased longevity under the fluctuating regime. The fecundity, mass, and size were affected by the mean temperature, but only the mass of aphids was higher at 7-17 °C than at a constant 12 °C. Parasitism rates, but not emergence rates, were higher under the fluctuating regime than under the constant 12 °C regime. Results are discussed within the framework of insect thermal ecology and Jensen's inequality. We conclude that incorporating thermal fluctuations in ecological studies could allow for the more accurate consideration of how temperature affects host-parasitoid interactions and insect responses to temperature change over time.

Banana Tree Infected with Banana Bunchy Top Virus Attracts Pentalonia nigronervosa Aphids Through Increased Volatile Organic Compounds Emission.

Banana plants are affected by various viral diseases, among which the most devastating is the "bunchy top", caused by the Banana bunchy top virus (BBTV) and transmitted by the aphid Pentalonia nigronervosa Coquerel. The effect of BBTV on attraction mechanisms of dessert and plantain banana plants on the vector remains far from elucidated. For that, attractiveness tests were carried out using a two columns olfactometer for apterous aphids, and a flight cage experiment for alate aphids. Volatile Organic Compounds (VOCs) emitted by either healthy or BBTV-infected banana plants were identified using a dynamic extraction system and gas-chromatography mass-spectrometry (GC-MS) analysis. Behavioral results revealed a stronger attraction of aphids towards infected banana plants (independently from the variety), and towards the plantain variety (independently from the infection status). GC-MS results revealed that infected banana plants produced VOCs of the same mixture as healthy banana plants but in much higher quantities. In addition, VOCs produced by dessert and plantain banana plants were different in nature, and plantains produced higher quantities than dessert banana trees. This work opens interesting opportunities for biological control of P. nigronervosa, for example by luring away the aphid from banana plants through manipulation of olfactory cues.

Ecology and biology of the parasitoid Trechnites insidiosus and its potential for biological control of pear psyllids.

Pear cultivation accounts for a large proportion of worldwide orchards, but its sustainability is controversial because it relies on intensive use of pesticides. It is therefore crucial and timely to find alternative methods to chemical control in pear orchards. The psyllids Cacopsylla pyri and Cacopsylla pyricola are the most important pests of pear trees in Europe and North America, respectively, because they infest all commercial varieties, causing damage directly through sap consumption or indirectly through the spread of diseases. A set of natural enemies exists, ranging from generalist predators to specialist parasitoids. Trechnites insidiosus (Crawford) is undoubtedly the most abundant specialist parasitoid of psyllids. In our literature review, we highlight the potential of this encyrtid species as a biological control agent of psyllid pests by first reviewing its biology and ecology, and then considering its potential at regulating psyllids. We show that the parasitoid can express fairly high parasitism rates in orchards, and almost perfectly matches the phenology of its host and is present early in the host infestation season, which is an advantage for controlling immature stages of psyllids. We propose new research directions and innovative approaches that would improve the use of T. insidiosus in integrated pest management strategies in the future, regarding both augmentative and conservation biocontrol. We conclude that T. insidiosus has many advantages and should be included as part of integrated biological control strategies of pear psyllids, along with predators, in-field habitat conservation, and the rational use of compatible chemicals. © 2021 Society of Chemical Industry.

Impact of the COVID-19 pandemic on apple orchards in Europe.

CONTEXT: The COVID-19 pandemic, caused by the SARS-CoV-2 virus, has affected global agricultural chains and intensified the issue of food insecurity worldwide. OBJECTIVE: We propose a short retrospective of the reported effects of the COVID-19 pandemic from its beginning in March 2020 in Europe, on orchard management and harvest, sales and agricultural chains, monitoring and research in orchards, and we expose some of the solutions undertaken to tackle down these issues. RESULTS AND CONCLUSION: In Europe, the fruit and vegetable sector has been affected by the pandemic in terms of production, distribution, and disturbance in market performance. Concerning apple, the most harvested and exported fruit in Europe, national governments, European institutions, the industry and producers have undertaken actions to ensure production and supply demand. Yet, stakeholders have faced several difficulties and additional costs for growth and harvest, sales, but also monitoring and research. However, European Union demand for fresh apples has increased during the pandemic. In addition, apple harvest has started a couple of months after the end of the first lockdown in most countries, and European apple orchards are usually in more flexible smallholder or family farms. Finally, the fruit itself has relatively long shelf-life comparatively to other fruits. For these main reasons, we argue that the apple sector might be more resilient than other fruit sectors or other cultures, despite the negative effects of seasonal workforce shortage and unstable market. The apple sector may suffer more from side-effects such as increasing labor, distribution, and packaging costs, than from actual stock and production issues. SIGNIFICANCE: The pandemic could be an opportunity to reconsider production modes and to innovate for the future of food production in different crop systems in Europe, including apple orchards.

Transgenerational phenotypic plasticity of diapause induction and related fitness cost in a commercial strain of the parasitoid Aphidius ervi Haliday.

Diapause is an adaptation that insects have evolved to synchronize their life cycle with that of seasonal climatic changes and resources availability. However, cues for its induction are not always clear and, in some cases, a maternal effect may be involved. At the population level, just a part of the individuals may exhibit diapause with important consequences in terms of winter survival. Moreover, clear indicators of diapause state are difficult to identify. Diapause induction was thus investigated in the aphid parasitoid species Aphidius ervi Haliday (Hymenoptera: Braconidae) developing in the aphid Sitobion avenae (Hemiptera: Aphididae) at four crossed photothermal regimes (16 °C and 8 °C, 16:8 h L:D and 8:16 h L:D), and during 2 successive generations. We analyzed the reliability of changes in mummy color to assess for the diapausing state compared to dissections, and we measured parasitoid morphological and physiological traits. We observed that the proportion of dark brown mummies increased after one generation under low photothermal regime compared to other regimes. No diapause was recorded at 16 °C, 16:8 h L:D, while we observed 16.2% and 67.5% diapause incidence at 8 °C, 8:16 h L:D, at 1st and 2nd generation, respectively. Diapause induction is thus increased by short day-length conditions and low temperatures as well as by maternal effects. All parasitoid life-history traits (weight, size, fat content, water content, egg-load, and longevity) were affected by the photothermal regime and/or the generation. These results raise new questions on the environmental thresholds needed to induce diapause and on survival and adaptation potential of commercially available parasitoid strains in different environments.