Disease, contagious cannibalism, and associated population crash in an omnivorous bug, Geocoris pallens.

Disease and cannibalism are two strongly density-dependent processes that can suppress predator populations. Here we show that California populations of the omnivorous predatory bug Geocoris pallens are subject to infection by a pathogen, as yet unidentified, that elicits elevated expression of cannibalism. Laboratory experiments showed that the pathogen is moderately virulent, causing flattened abdomens, elevated nymphal mortality, delayed development, and reduced body size of adult females. Infection furthermore increases the expression of cannibalism. Field populations of Geocoris spp. declined strongly in association with sharp increases in the expression of egg cannibalism by adult G. pallens. Increased cannibalism was accompanied by a strongly bimodal distribution of cannibalism expression, with some females (putatively uninfected) expressing little cannibalism and others (putatively infected) consuming most or all of the eggs present. Highly cannibalistic females did not increase their consumption of Ephestia cautella moth eggs, suggesting that the high cannibalism phenotype reflected a specific loss of restraint against eating conspecifics. Highly cannibalistic females also often exhibited reduced egg laying, consistent with a virulent pathogen; less frequently, more cannibalistic females exhibited elevated egg laying, suggesting that cannibalism might also facilitate recycling of nutrients in eggs. Elevated cannibalism was not correlated with reduced prey availability or elevated field densities of G. pallens. Geocoris pallens population crashes appear to reflect the combined consequences of direct virulence-adverse pathogen effects on the infected host's physiology-and indirect virulence-mortality of both infected and uninfected individuals due to elevated cannibalism expression by infected individuals.

Cannibalism amplifies the spread of vertically transmitted pathogens.

Cannibalism is a widespread behavior. Abundant empirical evidence demonstrates that cannibals incur a risk of contracting pathogenic infections when they consume infected conspecifics. However, current theory suggests that cannibalism generally impedes disease spread, because each victim is usually consumed by a single cannibal, such that cannibalism does not function as a spreading process. Consequently, cannibalism cannot be the only mode of transmission of most parasites. We develop simple, but general epidemiological models to analyze the interaction of cannibalism and vertical transmission. We show that cannibalism increases the prevalence of vertically transmitted pathogens whenever the host population density is not solely regulated by cannibalism. This mechanism, combined with additional, recently published, theoretical mechanisms, presents a strong case for the role of cannibalism in the spread of infectious diseases across a wide range of parasite-host systems.

The epidemiology and evolution of parasite transmission through cannibalism.

Cannibalism is a widespread behavior, and evidence is abundant for transmission from infected victims to susceptible cannibals in many parasite-host systems. Current theory suggests that cannibalism generally impedes disease spread, because each victim is usually consumed by a single cannibal. Thus, cannibalism merely transfers pathogens from one individual to another without spreading infections to additional hosts. This assumes that cannibalism is the only mode of transmission and that the host population is homogenous. However, host developmental stages are a key determinant of both cannibal-victim and host-pathogen interactions. We suggest that multiple modes of pathogen transmission can interact through host stage structure. We show theoretically that cannibalism can enhance disease spread by consistently transferring infections from low quality to high quality hosts that are more infectious via horizontal transmission. We review empirical evidence for the generality of key conditions required for this process, and analyze the implications for the evolution of transmission through cannibalism. More generally, our theory promotes the consideration of multiple transmission pathways when studying parasite-host systems, and advances a useful intuition for assessing whether or not such pathways may be mutually augmentative.

Intercohort size structure dynamics of fire salamander larvae in ephemeral habitats: a mesocosm experiment.

The size structure of a larval population facilitates interaction asymmetries that, in turn, influence the dynamics of size-structure. In species that exhibit conspicuous aggressive interactions, the competitive effects of the smaller individuals may be overlooked. We manipulated initial size differences between two larval cohorts and young-cohort density of Salamandra infraimmaculata in mesocosms to determine: (1) whether young individuals function primarily as prey or as competitors of older and larger individuals; (2) the resulting dynamics of size variation; and (3) recruitment to the postmetamorph population. Intercohort size differences generally remained constant over time at low young-cohort densities, but reduced over time at high densities due to retardation of the old-cohort growth rate. This suggests a competitive advantage to the young cohort that outweighs the interference advantage of older cohorts previously documented in this species. The increase in mortality from desiccation due to high young-cohort density was an order of magnitude greater in the old cohort than in the young-cohort, further indicating size-dependent vulnerability to competition. However, the conditions least favorable to most of the old-cohort larvae (large size difference and high young-cohort density) promoted cannibalism. Among cannibals, mortality and time to metamorphosis decreased and sizes at metamorphosis increased substantially. Thus, a balance between the competitive advantage to young cohorts, and the interference and cannibalism advantage to old cohorts shapes larval size-structure dynamics. Larval densities and individual expression of cannibalism can shift this balance in opposite directions and alter relative recruitment rates from different cohorts.

A Distinct Arabidopsis Latent Virus 1 Isolate Was Found in Wild Brassica hirta Plants and Bees, Suggesting the Potential Involvement of Pollinators in Virus Spread.

During our search for aphid-pathogenic viruses, a comovirus was isolated from wild asymptomatic Brassica hirta (white mustard) plants harboring a dense population of Brevicoryne brassicae aphids. The transmission-electron-microscopy visualization of purified virions revealed icosahedral particles. The virus was mechanically transmitted to plants belonging to Brassicaceae, Solanaceae, Amaranthaceae, and Fabaceae families, showing unique ringspot symptoms only on B. rapa var. perviridis plants. The complete viral genome, comprised of two RNA segments, was sequenced. RNA1 and RNA2 contained 5921 and 3457 nucleotides, respectively, excluding the 3' terminal poly-adenylated tails. RNA1 and RNA2 each had one open-reading frame encoding a polyprotein of 1850 and 1050 amino acids, respectively. The deduced amino acids at the Pro-Pol region, delineated between a conserved CG motif of 3C-like proteinase and a GDD motif of RNA-dependent RNA polymerase, shared a 96.5% and 90% identity with the newly identified Apis mellifera-associated comovirus and Arabidopsis latent virus 1 (ArLV1), respectively. Because ArLV1 was identified early in 2018, the B. hirta comovirus was designated as ArLV1-IL-Bh. A high-throughput-sequencing-analyses of the extracted RNA from managed honeybees and three abundant wild bee genera, mining bees, long-horned bees, and masked bees, sampled while co-foraging in a Mediterranean ecosystem, allowed the assembly of ArLV1-IL-Bh, suggesting pollinators' involvement in comovirus spread in weeds.

Analysis of apocarotenoid volatiles from lettuce (Lactuca sativa) induced by insect herbivores and characterization of carotenoid cleavage dioxygenase gene.

Plant apocarotenoids have been shown to have a diverse biological role in herbivore-plant interactions. Despite their importance, little is known about herbivores' effect on apocarotenoid emissions in Lactuca sativa. In this study, we examined changes in apocarotenoid emissions in lettuce leaves after infestation by two insects, viz., Spodoptera littoralis larvae and Myzus persicae aphids. We found that ß-ionone and ß-cyclocitral showed higher concentrations than the other apocarotenoids, with a significant increase as per the intensity of infestation of both herbivore species. Furthermore, we performed functional characterization of Lactuca sativa carotenoid cleavage dioxygenase 1 (LsCCD1) genes. Three LsCCD1 genes were overexpressed in E. coli strains, and recombinant proteins were assayed for cleavage activity on an array of carotenoid substrates. The LsCCD1 protein cleaved ß-carotene at the 9,10 (9',10') positions producing ß-ionone. The transcript analysis of LsCCD1 genes revealed differential expression patterns under varying levels of herbivores' infestation, but the results were inconsistent with the pattern of ß-ionone concentrations. Our results suggest that LsCCD1 is involved in the production of ß-ionone, but other regulatory factors might be involved in its induction in response to herbivory. These results provide new insights into apocarotenoid production in response to insect herbivory in lettuce. Supplementary Information: The online version contains supplementary material available at 10.1007/s13205-023-03511-4.

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.

Metatranscriptome Analysis of Sympatric Bee Species Identifies Bee Virus Variants and a New Virus, Andrena-Associated Bee Virus-1.

Bees are important plant pollinators in agricultural and natural ecosystems. High average annual losses of honey bee (Apis mellifera) colonies in some parts of the world, and regional population declines of some mining bee species (Andrena spp.), are attributed to multiple factors including habitat loss, lack of quality forage, insecticide exposure, and pathogens, including viruses. While research has primarily focused on viruses in honey bees, many of these viruses have a broad host range. It is therefore important to apply a community level approach in studying the epidemiology of bee viruses. We utilized high-throughput sequencing to evaluate viral diversity and viral sharing in sympatric, co-foraging bees in the context of habitat type. Variants of four common viruses (i.e., black queen cell virus, deformed wing virus, Lake Sinai virus 2, and Lake Sinai virus NE) were identified in honey bee and mining bee samples, and the high degree of nucleotide identity in the virus consensus sequences obtained from both taxa indicates virus sharing. We discovered a unique bipartite + ssRNA Tombo-like virus, Andrena-associated bee virus-1 (AnBV-1). AnBV-1 infects mining bees, honey bees, and primary honey bee pupal cells maintained in culture. AnBV-1 prevalence and abundance was greater in mining bees than in honey bees. Statistical modeling that examined the roles of ecological factors, including floral diversity and abundance, indicated that AnBV-1 infection prevalence in honey bees was greater in habitats with low floral diversity and abundance, and that interspecific virus transmission is strongly modulated by the floral community in the habitat. These results suggest that land management strategies that aim to enhance floral diversity and abundance may reduce AnBV-1 spread between co-foraging bees.

Context-dependent reproductive habitat selection: the interactive roles of structural complexity and cannibalistic conspecifics.

Structural complexity generally reduces predation and cannibalism rates. Although the benefits from this effect vary among environmental contexts and through time, it has been the common explanation for high species abundance in complex habitats. We hypothesized that oviposition habitat selection for structural complexity depends on the expected trophic function of the progeny. In Salamandra infraimmaculata larvae, expected trophic function is dictated by their sequence of deposition. First cohorts cannibalize later-arriving cohorts, while all compete for shared prey resources. In a mesocosm experiment, we show that gravid salamanders facing conspecific-free pools preferred structurally simple habitats (no rocks), while females facing only pools with older conspecific larvae preferred complex habitats (with rocks). Context-dependent preference of habitat complexity for managing food/safety trade-offs may be extended from classic foraging patch decisions to breeding habitat selection. These trade-offs vary with dynamic larval processes such as priority effects and ontogenetic diet shifts, potentially leading to complex maternal parturition behaviours.

The effects of a windborne pollen-provisioning cover crop on the phytoseiid community in citrus orchards in Israel.

BACKGROUND: Several phytoseiid species can potentially control the citrus rust mite (CRM). Their effectiveness varies, however, as do their intraguild interactions. Under laboratory conditions, Euseius stipulatus, E. scutalis and Iphiseius degenerans preyed effectively on CRM, whereas Amblyseius swirskii and Typhlodromus athiasae had no effect on CRM. In combination with A. swirskii, Euseius numbers were reduced due to intraguild predation, and consequently CRM suppression was less effective. In the field, predatory mite species can be variably provisioned by windborne pollen released from cover crops such as Rhodes grass (RG). We aimed to determine the effects of RG on the phytoseiid community in two field experiments, on different cultivars (pomelo and Shamouti orange). We also tested these communities for negative interspecific abundance relationships that are expected if their respective laboratory-observed intraguild interactions are manifested in the field. RESULTS: Overall, on pomelo, we observed a dominance of A. swirskii, relatively low E. stipulatus and high CRM abundances. Amblyseius swirskii and E. stipulatus abundances were both elevated near RG, despite apparent intraguild predation by A. swirskii. Conversely, T. athiasae abundances were lower near RG, likely due to predation by A. swirskii. On Shamouti, E. stipulatus abundances were much higher than on pomelo and were not negatively related to A. swirskii abundances. There, RG increased E. stipulatus abundance, and CRM was reduced. CONCLUSION: RG cover cropping can enhance CRM control, depending on variation in intraguild interactions among phytoseiids, particularly between A. swirskii and E. stipulatus. These may be modulated by climatic and/or cultivar effects. © 2018 Society of Chemical Industry.

A Pyrus communis gene for p-hydroxystyrene biosynthesis, has a role in defense against the pear psylla Cacopsylla biden.

Styrene analogs are known to be naturally synthesized in the leaves of pears and in other plant species, including several trees in the Styracaceae family. Styrene analogs are potential contributors to the aroma of wine, perfumes, pharmaceuticals, and other fermented foods and beverages. In addition, styrene analogs perform important ecological functions such as insecticidal and antifeedant activities against insects. We showed here that exogenous applications of styrene and p-hydroxystyrene caused a dramatic reduction the number of eggs laid by psylla and of subsequent nymph survival. Despite their importance specific reactions that lead to the biosynthesis of the styrene analogs in pear are unknown. To identify genes involved in the synthesis of these metabolites, existing genome databases of the Rosaceae were screened for pear genes with significant sequence similarity to bacterial phenolic acid decarboxylase. Herein described are the isolation and characterization of a pear phenolic acid decarboxylase, designated PyPAD1, which catalyzed the decarboxylation of p-coumaric acid and ferulic acid to p-hydroxystyrene and 3-methoxy-4-hydroxystyrene respectively. Its apparent Km values for p-coumaric acid and ferulic acid were 34.42 and 84.64 µM, respectively. The PyPAD1 preferred p-coumaric acid to ferulic acid as a substrate by a factor of 2.4 when comparing catalytic efficiencies in vitro. Expression analysis of PyPAD1 showed that the gene was transcribed in all five pear genotypes examined. However, transcript abundance was increased in correlation with the presence of p-hydroxystyrene in resistant cultivars Py-701 and Py-760 and in the sensitive cultivar Spadona when grafted on these resistant cultivars. Thus, PyPAD1 appears to be responsible for the decarboxylation of the p-coumaric acid, and for the production of metabolites that are active against pear psylla.

Compensatory development and costs of plasticity: larval responses to desiccated conspecifics.

Understanding constraints on phenotypic plasticity is central to explaining its evolution and the evolution of phenotypes in general, yet there is an ongoing debate on the classification and relationships among types of constraints. Since plasticity is often a developmental process, studies that consider the ontogeny of traits and their developmental mechanisms are beneficial. We manipulated the timing and reliability of cues perceived by fire salamander larvae for the future desiccation of their ephemeral pools to determine whether flexibility in developmental rates is constrained to early ontogeny. We hypothesized that higher rates of development, and particularly compensation for contradictory cues, would incur greater endogenous costs. We found that larvae respond early in ontogeny to dried conspecifics as a cue for future desiccation, but can fully compensate for this response in case more reliable but contradictory cues are later perceived. Patterns of mortality suggested that endogenous costs may depend on instantaneous rates of development, and revealed asymmetrical costs of compensatory development between false positive and false negative early information. Based on the results, we suggest a simple model of costs of development that implies a tradeoff between production costs of plasticity and phenotype-environment mismatch costs, which may potentially underlie the phenomenon of ontogenetic windows constraining plasticity.