Disentangling mite predator‐prey relationships by multiplex PCR

Gut content analysis using molecular techniques can help elucidate predator‐prey relationships in situations in which other methodologies are not feasible, such as in the case of trophic interactions between minute species such as mites. We designed species‐specific primers for a mite community occurring in Spanish citrus orchards comprising two herbivores, the Tetranychidae Tetranychus urticae and Panonychus citri, and six predatory mites belonging to the Phytoseiidae family; these predatory mites are considered to be these herbivores’ main biological control agents. These primers were successfully multiplexed in a single PCR to test the range of predators feeding on each of the two prey species. We estimated prey DNA detectability success over time (DS₅₀), which depended on the predator‐prey combination and ranged from 0.2 to 18 h. These values were further used to weight prey detection in field samples to disentangle the predatory role played by the most abundant predators (i.e. Euseius stipulatus and Phytoseiulus persimilis). The corrected predation value for E. stipulatus was significantly higher than for P. persimilis. However, because this 1.5‐fold difference was less than that observed regarding their sevenfold difference in abundance, we conclude that P. persimilis is the most effective predator in the system; it preyed on tetranychids almost five times more frequently than E. stipulatus did. The present results demonstrate that molecular tools are appropriate to unravel predator‐prey interactions in tiny species such as mites, which include important agricultural pests and their predators.     

Effect of cassava exudate and prey densities on the survival and reproduction of Typhlodromalus limonicus (Garman & McGregor) s.l. (Acari: Phytoseiidae), a predator of the cassava green mite,Mononychellus tanajoa (Bondar) (Acari: Tetranychidae)

The effects of cassava exudate and prey densities on reproduction and survival of the predatory mite, Typhlodromalus limonicus (Garman & McGregor) (Acari: Phytoseiidae), were investigated in the laboratory. Females were provided either cassava exudate ad lib. daily, low or high numbers of the cassava green mite prey, Mononychellus tanajoa (Bondar) (Acari: Tetranychidae) daily, or exudate for 5 or 10 days before switching to a low or high prey diet. Females fed only exudate laid no eggs. Females fed exudate before prey experienced a significant decrease (30%) in the number of eggs laid compared to females fed high numbers of prey daily. The reduction in fecundity was the result of prolonged preoviposition periods (2.0 days on prey daily vs 4.0 days on exudate before prey) and reduced number of eggs laid per female per day (1.7 eggs per female per day on prey daily vs 0.4 eggs per female per day on exudate before prey). Females fed only exudate had a greater survival rate and longevity than females fed prey daily or females fed exudate before a diet of prey. These results suggest that T. limonicus can survice for a limited period on cassava exudate during periods of low prey availability, but requires prey to complete oögenesis and propagate the population.     

Preceding crop affects soybean aphid abundance and predator–prey dynamics in soybean

Crop rotations alter the soil environment and physiology of the subsequent crop in ways that may affect the abundance of herbivores and their natural enemies. Soybean aphids are a consistent pest of soybean throughout North America, but little work has focused on how preceding crops may affect pest–predator dynamics. In a replicated experiment over three years, we examined how two preceding crops (spring wheat or an oat/pea mixture) affected seasonal soybean aphid pressure and the ratio of aphids to their predator community. Peak aphid populations were reduced by 40% and 75% in years 1 and 2 by planting spring wheat before soybeans (relative to the oat–pea mixture). Aphid densities were unaffected by preceding crop in the third year of study (aphids were at threshold in this year). Predators responded positively to aphid population increases and were unaffected by preceding crops. Additional research on how crop rotations can be used as a tool to manage soybean aphids warrants further attention.     

The role of resting spores in the survival of the mite-pathogenic fungus Neozygites floridana from Mononychellus tanajoa during dry periods in Brazil

Survival of pathogens during long periods of unfavorable conditions can be critical to their ecology and to their use in biological control. In northeastern Brazil, the mite pathogen Neozygites floridana must survive hot and dry conditions between wet seasons when it infects the cassava green mite Mononychellus tanajoa. We report on large numbers of mite cadavers bearing resting spores towards the end of epizootics in mid-1995. High within-leaf variability indicated that local factors may be important in determining resting spore formation. These spores remain in the host cadaver on a leaf until the cadaver breaks up, whereupon the spores fall freely to the soil, there to remain dormant. Laboratory simulation of field conditions led to ca. 25% of mycosed individuals bearing resting spores. Mummies (without resting spores) kept in hot and dry conditions showed little or no viability within 2 months, implying no role for survival over extended dry periods. It is proposed that resting spores form the principal means by which this pathogen survives the dry season in the study area. This has implications for its introduction to new areas in classical biological control.     

Dietary specialization in mutualistic acacia‐ants affects relative abundance but not identity of host‐associated bacteria

Acacia‐ant mutualists in the genus Pseudomyrmex nest obligately in acacia plants and, as we show through stable isotope analysis, feed at a remarkably low trophic level. Insects with diets such as these sometimes depend on bacterial symbionts for nutritional enrichment. We, therefore, examine the bacterial communities associated with acacia‐ants in order to determine whether they host bacterial partners likely to contribute to their nutrition. Despite large differences in trophic position, acacia‐ants and related species with generalized diets do not host distinct bacterial taxa. However, we find that a small number of previously undescribed bacterial taxa do differ in relative abundance between acacia‐ants and generalists, including several Acetobacteraceae and Nocardiaceae lineages related to common insect associates. Comparisons with an herbivorous generalist, a parasite that feeds on acacias and a mutualistic species with a generalized diet show that trophic level is likely responsible for these small differences in bacterial community structure. While we did not experimentally test for a nutritional benefit to hosts of these bacterial lineages, metagenomic analysis reveals a Bartonella relative with an intact nitrogen‐recycling pathway widespread across Pseudomyrmex mutualists and generalists. This taxon may be contributing to nitrogen enrichment of its ant hosts through urease activity and, concordant with an obligately host‐associated lifestyle, appears to be experiencing genomewide relaxed selection. The lack of distinctiveness in bacterial communities across trophic level in this group of ants shows a remarkable ability to adjust to varied diets, possibly with assistance from these diverse ant‐specific bacterial lineages.     

Cross‐resistance of chrysanthemum to western flower thrips,celery leafminer,and two‐spotted spider mite

Chrysanthemum [Chrysanthemum × morifolium Ramat. (Asteraceae)] is one of the economically most important greenhouse ornamentals worldwide. A major constraint in chrysanthemum production is adequate pest management, requiring the use of different tactics, such as improving host plant resistance, in the framework of an integrated pest management (IPM) approach. In this study, we investigated cross‐resistance of chrysanthemum to its three major pests: western flower thrips [Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae)], celery leafminer [Liriomyza trifolii (Burgess) (Diptera: Agromyzidae)], and two‐spotted spider mite [Tetranychus urticae Koch (Acari: Tetranychidae)]. We quantified resistance to each pest by performing greenhouse bioassays with a broad range of chrysanthemum types from commercial germplasm provided by Dutch breeding companies. Considerable variation was detected among the chrysanthemum cultivars in thrips silver damage and growth damage, leafminer damage, measured as number of mines and pupae, and spider mite numbers and damage. We observed significant positive correlations between thrips damage (both silver and growth damage) vs. leafminer numbers (both mines and pupae), and between leafminer numbers (both mines and pupae) vs. spider mite numbers. Our results indicate an overlap in resistance to all three herbivores. The important implications of this result for chrysanthemum breeding are discussed.     

Direct and indirect adverse effects of tomato on the predatory mite Neoseiulus californicus feeding on the spider mite Tetranychus evansi

Plants may defend themselves against herbivores via morphological traits, chemical traits, or a combination of both. Herbivores that overcome the defensive mechanisms of a plant tend to specialize on this plant due to enhanced protection from natural enemies. Well‐known examples of plants possessing a suite of defensive mechanisms are found in nightshades (Solanaceae), especially in the tomato genus Lycopersicon. The spider mite Tetranychus evansi Baker and Pritchard (Acari: Tetranychidae) is specialized on solanaceous plants and is an invasive pest of tomato in Europe and Africa. Biological control of T. evansi with currently available natural enemies, such as the predatory mites Phytoseiulus persimilis Athias‐Henriot and Neoseiulus californicus McGregor (both Acari: Phytoseiidae), is unsuccessful, with the underlying mechanisms only vaguely known. We hypothesized that T. evansi is a key pest of tomato because this host plant provides a two‐pronged protection from natural enemies. Direct adverse effects of tomato on predators may arise from morphological traits and/or trichome exudates, whereas indirect effects are prey‐mediated through the accumulation of toxic plant compounds. Using a 2 × 3 factorial design, we assessed and separated direct and indirect effects of tomato on the life history of N. californicus feeding on two strains of T. evansi (reared on bean or tomato) on three substrates (tomato leaf, bean leaf, and an artificial cage). Developmental time and oviposition rate of N. californicus were both directly and indirectly negatively affected by tomato whereas offspring sex ratio and survival of juveniles and adult females were unaffected. The direct and indirect, prey‐mediated adverse effects of tomato on N. californicus with T. evansi prey had similar magnitudes and were additive. We conclude that T. evansi per se is a suitable prey species for N. californicus and discuss the results with respect to the potential use of N. californicus as biological control agent of T. evansi on tomato and other host plants.     

Linking properties of an orb‐weaving spider's capture thread glycoprotein adhesive and flagelliform fiber components to prey retention time

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Altitude affects the distribution and abundance of two non‐native insect pests of the common walnut

The leaf miner Coptodisca lucifluella and the carpophagous Rhagoletis completa, of American origin, are two non‐native walnut (Juglans spp.) pests in Italy. For the Friuli Venezia Giulia region (FVG) (N‐E Italy), C. lucifluella is not yet listed, while R. completa has been present for over 25 years. During 2015, samples of leaves and fruits were collected from 219 single old common walnut trees (Juglans regia) placed at different altitudes (0–1,073 m a.s.l.) in FVG to detect the distribution and abundance of both pests. Samples of leaf miner larvae and their parasitoids were subjected to mitochondrial DNA analysis for identification. C. lucifluella has been found in 55 out of 219 sites. The species has been identified by typical leaf symptoms and by its DNA barcode. This is the first report of the species for FVG. The leaf miner distribution was negatively correlated with altitude. The species has not been observed at sites over 600 m a.s.l. Larvae were parasitized by native parasitoids identified as belonging to the genus Chrysocharis by morphological features and by DNA barcode. R. completa has been found in 89 out of 165 sites on walnut trees with fruits. The infestation level was very high in lowland localities. At sites over 700 m a.s.l., no infestation was found. Both species are widespread in the region, and their occurrence is significantly affected by altitude. Data suggest that walnut trees could be cultivated in some mountain areas without the need to control R. completa with insecticides.     

Phylogenetic conservatism in plant‐soil feedback and its implications for plant abundance

We examined whether plant‐soil feedback and plant‐field abundance were phylogenetically conserved. For 57 co‐occurring native and exotic plant species from an old field in Canada, we collected a data set on the effects of three soil biota treatments on plant growth: net whole‐soil feedback (combined effects of mutualists and antagonists), feedback with arbuscular mycorrhizal fungi (AMF) collected from soils of conspecific plants, and feedback with Glomus etunicatum, a dominant mycorrhizal fungus. We found phylogenetic signal in both net whole‐soil feedback and feedback with AMF of conspecifics; conservatism was especially strong among native plants but absent among exotics. The abundance of plants in the field was also conserved, a pattern underlain by shared plant responses to soil biota. We conclude that soil biota influence the abundance of close plant relatives in nature.     

Calcium concentration in leaf litter affects the abundance and survival of crustaceans in streams draining warm–temperate forests

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Stress‐induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid

Bacterial endosymbionts can drive evolutionary novelty by conferring adaptive benefits under adverse environmental conditions. Among aphid species there is growing evidence that symbionts influence tolerance to various forms of stress. However, the extent to which stress inflicted on the aphid host has cascading effects on symbiont community dynamics remains poorly understood. Here we simultaneously quantified the effect of host‐plant induced and xenobiotic stress on soybean aphid (Aphis glycines) fitness and relative abundance of its three bacterial symbionts. Exposure to soybean defensive stress (Rag1 gene) and a neurotoxic insecticide (thiamethoxam) substantially reduced aphid composite fitness (survival × reproduction) by 74 ± 10% and 92 ± 2%, respectively, which in turn induced distinctive changes in the endosymbiont microbiota. When challenged by host‐plant defenses a 1.4‐fold reduction in abundance of the obligate symbiont Buchnera was observed across four aphid clonal lines. Among facultative symbionts of Rag1‐stressed aphids, Wolbachia abundance increased twofold and Arsenophonus decreased 1.5‐fold. A similar pattern was observed under xenobiotic stress, with Buchnera and Arsenophonus titers decreasing (1.3‐fold) and Wolbachia increasing (1.5‐fold). Furthermore, variation in aphid virulence to Rag1 was positively correlated with changes in Arsenophonus titers, but not Wolbachia or Buchnera. A single Arsenophonus multi‐locus genotype was found among aphid clonal lines, indicating strain diversity is not primarily responsible for correlated host‐symbiont stress levels. Overall, our results demonstrate the nature of aphid symbioses can significantly affect the outcome of interactions under stress and suggests general changes in the microbiome can occur across multiple stress types.     

Intra‐ and interspecific interactions between aphidophagous ladybirds: the role of prey in predator coexistence

Cannibalism (CANN) and intraguild predation (IGP) may provide energy and nutrients to individuals and eliminate potential competitors. These negative competitive interactions could also affect the coexistence of predatory species. The co‐occurrence of aphidophagous ladybird species in crops creates opportunities for CANN and IGP, especially when aphids become scarce. The Lotka–Volterra model predicts the coexistence of two species if intraspecific competition is stronger than interspecific interference interactions. Cycloneda sanguinea L. and Eriopis connexa (Germar) (both Coleoptera: Coccinellidae) coexist in sweet pepper crops in La Plata (Argentina) consuming mainly Myzus persicae (Sulzer) (Hemiptera: Aphididae). The present study used laboratory experiments to estimate levels of CANN and IGP by adults and larvae on eggs, and by adults on larvae, in both the presence and absence of prey (i.e., M. persicae), to explain the effect of prey on coexistence of these two predators. Levels of CANN by C. sanguinea and E. connexa were high in the absence of aphids, and decreased when prey was present. Intraguild predation was bidirectional and asymmetric. Adults and larvae of E. connexa were more voracious IG predators of C. sanguinea than vice versa, the former being the stronger IG predator and interference competitor. Eriopis connexa always won when larvae of the same instar were compared, whereas the larger larva always won when larvae were of different instars, regardless of species. In the presence of prey, CANN by both species decreased, but IGP by E. connexa on C. sanguinea remained high, suggesting that E. connexa could displace C. sanguinea via interspecific interference competition. Other factors potentially affecting the coexistence of C. sanguinea and E. connexa in sweet pepper crops are discussed.     

Age‐ and temperature‐dependent oviposition model of Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) with Tetranychus urticae as prey

In this study, we developed an oviposition model of Neoseiulus californicus (McGregor) with Tetranychus urticae Koch as prey. To obtain data for the model, we investigated the longevity, fecundity and survivorship of adult female N. californicus at six constant temperatures (16, 20, 24, 28, 32 and 36°C), 60–70% RH and a photoperiod of 16 : 8 (L : D) h. Longevity (average ± SE) decreased as temperature increased and was longest at 16°C (46.7 ± 5.25 days) and shortest at 36°C (12.8 ± 0.75 days). Adult developmental rate (1/average longevity) was described by the Lactin 1 model (r² = 0.95). The oviposition period (average±SE) was also longest at 16°C (29.8 ± 2.93 days) and shortest at 36°C (6.7 ± 0.54 days). Fecundity (average±SE) was greatest at 24°C (43.8 ± 3.23 eggs) and lowest at 36°C (15.9 ± 1.50 eggs). The oviposition model comprised temperature‐dependent fecundity, age‐specific cumulative oviposition rate and age‐specific survival rate functions. The temperature‐dependent fecundity was best described by an exponential equation (r² = 0.81). The age‐specific cumulative oviposition rate was best described by the three‐parameter Weibull function (r² = 0.96). The age‐specific survival rate was best described by a reverse sigmoid function (r² = 0.85).     

Regional‐scale dominance of non‐framework building corals on Caribbean reefs affects carbonate production and future reef growth

Coral cover on Caribbean reefs has declined rapidly since the early 1980's. Diseases have been a major driver, decimating communities of framework building Acropora and Orbicella coral species, and reportedly leading to the emergence of novel coral assemblages often dominated by domed and plating species of the genera Agaricia, Porites and Siderastrea. These corals were not historically important Caribbean framework builders, and typically have much smaller stature and lower calcification rates, fuelling concerns over reef carbonate production and growth potential. Using data from 75 reefs from across the Caribbean we quantify: (i) the magnitude of non‐framework building coral dominance throughout the region and (ii) the contribution of these corals to contemporary carbonate production. Our data show that live coral cover averages 18.2% across our sites and coral carbonate production 4.1 kg CaCO₃ m^?2 yr^?1. However, non‐framework building coral species dominate and are major carbonate producers at a high proportion of sites; they are more abundant than Acropora and Orbicella at 73% of sites; contribute an average 68% of the carbonate produced; and produce more than half the carbonate at 79% of sites. Coral cover and carbonate production rate are strongly correlated but, as relative abundance of non‐framework building corals increases, average carbonate production rates decline. Consequently, the use of coral cover as a predictor of carbonate budget status, without species level production rate data, needs to be treated with caution. Our findings provide compelling evidence for the Caribbean‐wide dominance of non‐framework building coral taxa, and that these species are now major regional carbonate producers. However, because these species typically have lower calcification rates, continued transitions to states dominated by non‐framework building coral species will further reduce carbonate production rates below ‘predecline’ levels, resulting in shifts towards negative carbonate budget states and reducing reef growth potential.     

Identification of chloroplast genome loci suitable for high‐resolution phylogeographic studies of Colocasia esculenta (L.) Schott (Araceae) and closely related taxa

Recently, we reported the chloroplast genome‐wide association of oligonucleotide repeats, indels and nucleotide substitutions in aroid chloroplast genomes. We hypothesized that the distribution of oligonucleotide repeat sequences in a single representative genome can be used to identify mutational hotspots and loci suitable for population genetic, phylogenetic and phylogeographic studies. Using information on the location of oligonucleotide repeats in the chloroplast genome of taro (Colocasia esculenta), we designed 30 primer pairs to amplify and sequence polymorphic loci. The primers have been tested in a range of intra‐specific to intergeneric comparisons, including ten taro samples (Colocasia esculenta) from diverse geographical locations, four other Colocasia species (C. affinis, C. fallax, C. formosana, C. gigantea) and three other aroid genera (represented by Remusatia vivipara, Alocasia brisbanensis and Amorphophallus konjac). Multiple sequence alignments for the intra‐specific comparison revealed nucleotide substitutions (point mutations) at all 30 loci and microsatellite polymorphisms at 14 loci. The primer pairs reported here reveal levels of genetic variation suitable for high‐resolution phylogeographic and evolutionary studies of taro and other closely related aroids. Our results confirm that information on repeat distribution can be used to identify loci suitable for such studies, and we expect that this approach can be used in other plant groups.     

Genetic control of α‐farnesene production in apple fruit and its role in fungal pathogenesis

Terpenes are important compounds in plant trophic interactions. A meta‐analysis of GC‐MS data from a diverse range of apple (Malus × domestica) genotypes revealed that apple fruit produces a range of terpene volatiles, with the predominant terpene being the acyclic branched sesquiterpene (E,E)‐α‐farnesene. Four quantitative trait loci (QTLs) for α‐farnesene production in ripe fruit were identified in a segregating ‘Royal Gala’ (RG) × ‘Granny Smith’ (GS) population with one major QTL on linkage group 10 co‐locating with the MdAFS1 (α‐farnesene synthase‐1) gene. Three of the four QTLs were derived from the GS parent, which was consistent with GC‐MS analysis of headspace and solvent‐extracted terpenes showing that cold‐treated GS apples produced higher levels of (E,E)‐α‐farnesene than RG. Transgenic RG fruit downregulated for MdAFS1 expression produced significantly lower levels of (E,E)‐α‐farnesene. To evaluate the role of (E,E)‐α‐farnesene in fungal pathogenesis, MdAFS1 RNA interference transgenic fruit and RG controls were inoculated with three important apple post‐harvest pathogens [Colletotrichum acutatum, Penicillium expansum and Neofabraea alba (synonym Phlyctema vagabunda)]. From results obtained over four seasons, we demonstrate that reduced (E,E)‐α‐farnesene is associated with decreased disease initiation rates of all three pathogens. In each case, the infection rate was significantly reduced 7 days post‐inoculation, although the size of successful lesions was comparable with infections on control fruit. These results indicate that (E,E)‐α‐farnesene production is likely to be an important factor involved in fungal pathogenesis in apple fruit.