Effects of Natural Habitat and Season on Cursorial Spider Assemblages in Mediterranean Vineyards.

Natural habitats adjacent to vineyards are presumed to have a positive effect on the diversity of natural enemies within the vineyards. However, these habitats differ in vegetation structure and seasonal phenology and in turn could affect the species composition of natural enemies. Here, we compared the species richness and diversity and the composition of spider assemblages in several locations within three commercial vineyards and the nearby natural habitats in a Mediterranean landscape in northern Israel. We sampled spiders by means of pitfall traps in early and in late summer. Both the time in the season and the habitat (natural versus vineyard) affected spider species richness and diversity. More species were found in early summer (47) than in late summer (33), and more occurred in the natural habitat (34 species) than in the vineyards (27-31 species). Fifteen species were found exclusively in the natural habitat, and only 11 species were shared by the vineyards and natural habitat, four of which were the most abundant and geographically widely distributed species in the samples. In late summer, spider diversity in the natural habitat was higher than within the vineyards: the spider assemblages in the vineyards became dominated by a few species late in the crop season, while those of the natural habitat remained stable. Overall, the natural habitat differed in assemblage composition from all within-vineyard locations, while the three locations within the vineyard did not differ significantly in assemblage composition. Season (early vs. late summer), however, significantly affected the spider assemblage composition. This study documents the large diversity of spiders in a local Mediterranean vineyard agroecosystem. Over 60% of the known spider families in the region occurred in our samples, highlighting the importance of this agroecosystem for spider diversity and the potential for conservation biocontrol, where natural habitats may be a source of natural enemies for nearby vineyards.

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.

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.

Can sociality facilitate learning of complex tasks? Lessons from bees and flowers.

The emergence of animal societies is a major evolutionary transition, but its implications for learning-dependent innovations are insufficiently understood. Bees, with lifestyles ranging from solitary to eusocial, are ideal models for exploring social evolution. Here, we ask how and why bees may acquire a new 'technology', foraging on morphologically complex flowers, and whether eusociality facilitates this technological shift. We consider 'complex' flowers that produce high food rewards but are difficult to access, versus 'simple' flowers offering easily accessible yet lower rewards. Complex flowers are less profitable than simple flowers to naive bees but become more rewarding after a learning period. We model how social bees optimally choose between simple and complex flowers over time, to maximize their colony's food balance. The model predicts no effect of colony size on the bees' flower choices. More foraging on complex flowers is predicted as colony longevity, its proportion of foragers, individual longevity and learning ability increase. Of these traits, only long-lived colonies and abundant foragers characterize eusocial bees. Thus, we predict that eusociality supports, but is not mandatory for, learning to exploit complex flowers. A re-analysis of a large published dataset of bee-flower interactions supports these conclusions. We discuss parallels between the evolution of insect sociality and other major transitions that provide scaffolds for learning innovations. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

Intraspecific Seasonal Variation of Flowering Synchronization in a Heterodichogamous Tree.

Heterodichogamous reproduction in plants involves two flowering morphs, reciprocal in their timing of male and female sexual functions. The degree of synchrony in floral sex phase, within and between individuals of each morph, determines the flowers' potential fertilization partners. Complete within-morph synchrony enables across-morph mating alone, whereas unsynchronized floral sex phases may allow fertilization within a plant individual (geitonogamy) or within a morph. We documented the disruption of flowering synchrony in the heterodichogamous Ziziphus spina-christi towards the end of its seven-month flowering season. This desert tree has self-incompatible, protandrous, short-lived (2-day) flowers that open before dawn ('Early' morph) or around noon ('Late' morph). We counted flowers in the male and female phase on flowering branches that were sampled monthly during the 2016-2018 flowering seasons. In 2018, we also tagged flowers and followed their sex-phase distributions over two days at the start, middle, and end of the season. The switch to the female phase was delayed at the end-season (November-December), and 74% of the flowers did not develop beyond their male phase. Differences in male-phase duration resulted in asynchrony among flowers within each tree and among trees of both flowering morphs. Consequently, fertilization between trees of the same morph becomes potentially possible during the end-season. In controlled hand-pollination assays, some within-morph fertilizations set fruit. The end-season breakdown of synchronous flowering generates variability within morphs and populations. We suggest that this variability may potentially enable new mating combinations in a population and enhance its genetic diversity.

Floral Complexity Traits as Predictors of Plant-Bee Interactions in a Mediterranean Pollination Web.

Despite intensive research, predicting pairwise species associations in pollination networks remains a challenge. The morphological fit between flowers and pollinators acts as a filter that allows only some species within the network to interact. Previous studies emphasized the depth of floral tubes as a key shape trait that explains the composition of their animal visitors. Yet, additional shape-related parameters, related to the handling difficulty of flowers, may be important as well. We analyzed a dataset of 2288 visits by six bee genera to 53 flowering species in a Mediterranean plant community. We characterized the plant species by five discrete shape parameters, which potentially affect their accessibility to insects: floral shape class, tube depth, symmetry, corolla segmentation and type of reproductive unit. We then trained a random forest machine-learning model to predict visitor identities, based on the shape traits. The model's predictor variables also included the Julian date on which each bee visit was observed and the year of observation, as proxies for within- and between-season variation in flower and bee abundance. The model attained a classification accuracy of 0.86 (AUC = 0.96). Using only shape parameters as predictors reduced its classification accuracy to 0.76 (AUC = 0.86), while using only the date and year variables resulted in a prediction accuracy of 0.69 (AUC = 0.80). Among the shape-related variables considered, flower shape class was the most important predictor of visitor identity in a logistic regression model. Our study demonstrates the power of machine-learning algorithms for understanding pollination interactions in a species-rich plant community, based on multiple features of flower morphology.

Pollinator Behavior Drives Sexual Specializations in the Hermaphrodite Flowers of a Heterodichogamous Tree.

Dioecy, the specialization of individuals into either male-only or female-only sexual function, has multiple evolutionary origins in plants. One proposed ancestral mating system is heterodichogamy, two morphs of cross-fertilizing hermaphrodite flowers that differ in their timing of flowering. Previous research suggested that small specializations in these morphs' functional genders could facilitate their evolution into separate sexes. We tested the possible role of pollinators in driving such specializations. Ziziphus spina-christi is an insect-pollinated heterodichogamous tree with self-incompatible flowers and two sympatric flowering morphs. We compared the flower development patterns, floral food rewards, pollinator visits, and fruit production between the two morphs. Male-phase flowers of Z. spina-christi's "Early" and "Late" morphs open before dawn and around noon, respectively, and transition into female-phase 7-8 h later. Flowers of both morphs contain similar nectar and pollen rewards, and receive visits by flies (their ancestral pollinators) at similar rates, mostly during the morning. Consequently, the Early morph functions largely as pollen donor. The Late morph, functioning as female in the morning, produces more fruit. We developed an evolutionary probabilistic model, inspired by Z. spina-christi's reproductive system, to test whether pollinator visit patterns could potentially play a role in an evolutionary transition from heterodichogamy towards dioecy. The model predicts that reproductive incompatibility within flowering morphs promotes their evolution into different sexes. Furthermore, the pollinators' morning activity drives the Early and Late morphs' specialization into male and female functions, respectively. Thus, while not required for transitioning from heterodichogamy to dioecy, pollinator-mediated selection is expected to influence which sexual specialization evolves in each of the flowering morphs.

Evidence for trans-generational effects on egg maturation schedules in a syn-ovigenic parasitoid.

The lifetime reproductive success of a female parasitoid is limited by (1) host (or time) limitation - the number of hosts available for oviposition during its lifetime; and (2) egg limitation - its egg supply. Host limitation is expected to select for increased longevity and/or foraging efficiency, while increased fecundity is predicted to evolve under egg limitation. If the limiting factor varies, phenotypic plasticity in egg maturation schedules may be advantageous, i.e. adjusting investment in egg production to host availability. In the polyembryonic parasitoid Copidosoma koehleri, environmental conditions experienced during development indeed influence resource allocation to egg maturation. However, whether parasitoids' maternal environment also influences their daughters' egg production has hardly been studied. To address this knowledge gap, we tested whether exposure of C. koehleri females to previously parasitized hosts (signaling intraspecific exploitation competition and risk of host limitation) reduces their daughters' initial egg loads. We presented newly-emerged females with hosts that were either fresh or parasitized by conspecifics. The following day, we exposed both groups to additional fresh hosts, and reared out the daughters of these previously experienced, 24+ h old, individuals. The daughters' egg loads and body sizes were similar under both experimental conditions. Nevertheless, their egg loads were ~30% higher, and body sizes were ~10% lower, than in daughters of just-emerged parasitoids. We suggest that female experience or age, but not conditions associated with host exploitation, trigger maternal effects on the reproductive and developmental physiology of their daughters.

Lessons from the multitudes: insights from polyembryonic wasps for behavioral ecology.

Even for parasitic Hymenoptera, polyembryonic wasps are unusual creatures. Two features in particular, allow for novel exploration of major questions in behavioral ecology: the production of multiple offspring per egg and, in some species, the production of a soldier caste. Because final brood sizes of polyembryonic species are not constrained by trade-offs between current and future parental reproductive effort, we can clearly examine the selective forces at play that drive the balance between the number of offspring and their body size. Polyembryony also provides excellent opportunities to compare the performance of identical genotypes under different environmental conditions. Finally, polyembryonic species can provide unique tests of how genetic conflicts at multiple levels are resolved.

Morphological Complexity as a Floral Signal: From Perception by Insect Pollinators to Co-Evolutionary Implications.

Morphologically complex flowers are characterized by bilateral symmetry, tube-like shapes, deep corolla tubes, fused petals, and/or poricidal anthers, all of which constrain the access of insect visitors to floral nectar and pollen rewards. Only a subset of potential pollinators, mainly large bees, learn to successfully forage on such flowers. Thus, complexity may comprise a morphological filter that restricts the range of visitors and thereby increases food intake for successful foragers. Such pollinator specialization, in turn, promotes flower constancy and reduces cross-species pollen transfer, providing fitness benefits to plants with complex flowers. Since visual signals associated with floral morphological complexity are generally honest (i.e., indicate food rewards), pollinators need to perceive and process them. Physiological studies show that bees detect distant flowers through long-wavelength sensitive photoreceptors. Bees effectively perceive complex shapes and learn the positions of contours based on their spatial frequencies. Complex flowers require long handling times by naive visitors, and become highly profitable only for experienced foragers. To explore possible pathways towards the evolution of floral complexity, we discuss cognitive mechanisms that potentially allow insects to persist on complex flowers despite low initial foraging gains, suggest experiments to test these mechanisms, and speculate on their adaptive value.

Phenotypic plasticity of pre-adult egg maturation in a parasitoid: Effects of host-starvation and brood size.

Larvae of parasitoid wasps develop on a single arthropod host, and often face resource limitation that induces a tradeoff between egg maturation and somatic growth. Part of the variation in the growth-reproduction allocation was shown to be heritable, but how the larval developmental environment affects this allocation is not well-known. Detection of life history tradeoffs is often facilitated under stress conditions. We therefore exposed developing female larvae of the polyembryonic parasitoid Copidosoma koehleri (Hymenoptera: Encyrtidae) to laboratory manipulations aimed to restrict host resources (either host-starvation or high larval density). We compared the females' body sizes and egg loads shortly after adult emergence (<24 h) to those of closely related control females, which developed at a lower larval density within non-starved hosts. Host-starvation reduced the females' body sizes but not their initial egg loads. Females that experienced high larval density produced more eggs but were similar in body size to the low-density controls. Thus, the relative allocation to reproduction increased in response to both manipulations of host condition. Developmental duration and longevity were similar in all treatments. The negative correlation between body size and reproductive allocation, observed in the host-starvation treatment, is compatible with previous evidence from other parasitoids. In the high larval density treatment, however, reproductive allocation increased while body size was maintained, suggesting that the higher density increased rather than limited host resources per developing parasitoid female. The additional host resources that were diverted into egg production possibly resulted from increased feeding and body mass gain by hosts parasitized by large broods of wasps. Our results demonstrate phenotypic plasticity in resource allocation between growth and reproduction in a developing parasitoid. This plasticity may contribute to an adaptive balance between longevity and mobility vs. fecundity during the adult stage.

Does mating disruption of Planococcus ficus and Lobesia botrana affect the diversity, abundance and composition of natural enemies in Israeli vineyards?

BACKGROUND: Mating disruption (MD) employs high doses of a pest's synthetic sex pheromone in agricultural plots, to interfere with its reproduction. MD is assumed to have few behavioral effects on non-target arthropods, because sex pheromones are highly species-specific and non-toxic. Nevertheless, some natural enemies use their host's sex pheromones as foraging cues, and thus may be attracted to MD plots. To investigate this hypothesis, we compared parasitoid and spider assemblages in paired plots in five Israeli vineyards during 2015. One plot was MD-treated against two key pests, Lobesia botrana (Denis & Schiffermüller) and Planococcus ficus (Signoret). Both plots were insecticide-treated as needed. Natural enemies were suction-sampled and collected from pheromone-baited monitoring traps. RESULTS: The total abundance, species diversity and species composition of most natural enemies were unaffected by MD. An important exception involved P. ficus' main parasitoid, Anagyrus sp. nr. pseudococci (Girault). Anagyrus sp. nr. pseudococci females were mainly captured in control plots, while male captures were low and not influenced by MD. Parasitized P. ficus occurred only in MD plots. CONCLUSION: Non-target effects of MD involved mostly A. sp. nr. pseudococci females and hardly affected other natural enemies. These findings support the use of MD as an environmentally friendly pest management strategy. © 2018 Society of Chemical Industry.

Genome methylation patterns across castes and generations in a parasitoid wasp.

Environmental influences shape phenotypes within and across generations, often through DNA methylations that modify gene expression. Methylations were proposed to mediate caste and task allocation in some eusocial insects, but how an insect's environment affects DNA methylation in its offspring is yet unknown. We characterized parental effects on methylation profiles in the polyembryonic parasitoid wasp Copidosoma koehleri, as well as methylation patterns associated with its simple caste system. We used methylation-sensitive amplified fragment length polymorphism (MS-AFLP) to compare methylation patterns, among (1) reproductive and soldier larvae; and (2) offspring (larvae, pupae, and adults) of wasps that were reared at either high or low larval density and mated in the four possible combinations. Methylation frequencies were similar across castes, but the profiles of methylated fragments differed significantly. Parental rearing density did not affect methylation frequencies in the offspring at any developmental stage. Principal coordinate analysis indicated no significant differences in methylation profiles among the four crossbreeding groups and the three developmental stages. Nevertheless, a clustering analysis, performed on a subset of the fragments, revealed similar methylation patterns in larvae, pupae, and adults in two of the four parental crosses. Nine fragments were methylated at two cytosine sites in all larvae, and five others were methylated at two sites in all adults. Thus, DNA methylations correlate with within-generation phenotypic plasticity due to caste. However, their association with developmental stage and with transgenerational epigenetic effects is not clearly supported.

Sex allocation in a polyembryonic parasitoid with female soldiers: an evolutionary simulation and an experimental test.

Parasitoid wasps are convenient subjects for testing sex allocation theory. However, their intricate life histories are often insufficiently captured in simple analytical models. In the polyembryonic wasp Copidosoma koehleri, a clone of genetically identical offspring develops from each egg. Male clones contain fewer individuals than female clones. Some female larvae develop into soldiers that kill within-host competitors, while males do not form soldiers. These features complicate the prediction of Copidosoma's sex allocation. We developed an individual-based simulation model, where numerous random starting strategies compete and recombine until a single stable sex allocation evolves. Life-history parameter values (e.g., fecundity, clone-sizes, larval survival) are estimated from experimental data. The model predicts a male-biased sex allocation, which becomes more extreme as the probability of superparasitism (hosts parasitized more than once) increases. To test this prediction, we reared adult parasitoids at either low or high density, mated them, and presented them with unlimited hosts. As predicted, wasps produced more sons than daughters in all treatments. Males reared at high density (a potential cue for superparasitism) produced a higher male bias in their offspring than low-density males. Unexpectedly, female density did not affect offspring sex ratios. We discuss possible mechanisms for paternal control over offspring sex.

Developmental patterns in the polyembryonic parasitoid wasp Copidosoma koehleri.

Polyembryony is a unique mode of development in which multiple genetically identical embryos develop from a single egg. In some polyembryonic species a proportion of the embryos develop into soldier larvae, which attack competitors in the host. We studied the development of the polyembryonic wasp Copidosoma koehleri in its host Phthorimaea opercullela. We dissected hosts parasitized by either virgin or mated female wasps at 2day intervals from hatching to the final instars. We documented host mass and head width, the number and size of developing wasps and the presence of a soldier larva. Additionally, we kept a sample of parasitized hosts until emergence of wasps and measured the head width of emerging adults. We characterized wasp development in relation to host development. One half of the broods produced by mated wasps contained one soldier larva throughout development. This suggests that in C. koehleri each female brood produces a single soldier larva, and that the soldier probably survives and grows gradually during host development. Additionally, we found that female broods were larger than male broods during development and also upon emergence. Accordingly, body size was larger for males during development as well as upon emergence. These findings may extend the existing knowledge on polyembryonic development in general, and serve as a baseline for further experiments.

Spatial and temporal dynamics of potato tuberworm (Lepidoptera: Gelechiidae) infestation in field-stored potatoes.

The potato tuberworm, Phthorimaea operculella (Zeller), is a major pest of potatoes in fields and traditional storage. A common method of nonrefrigerated storage is to pile potatoes in straw-covered heaps in the field. Tubers may be stored up to 3-4 mo in this manner, until the next harvest. We studied the dynamics of potato tuber moth infestation associated with such field storage in a 12-wk experiment in Israel. We set up six potato heaps, and sampled them for potato tuber moth at different locations at weekly intervals. Potato tuber moth infestation was significantly higher at the perimeter of the heaps than at their center, but it did not differ between bottom, mid-height, and top of the heaps. The proportion of potato tuber moth-infested potato tubers increased from 10 to 65% over the course of the experiment, and the mean number of potato tuber moth larvae per tuber increased from 0.25 to 2.50. Potato tuberworm populations increased sharply after 3, 6, and 9 wk of study, possibly corresponding to successive generations that developed within the heaps. This interpretation is supported by calculations of potato tuberworm generation length based on temperature data. Catches in pheromone traps that were placed near the heaps were not correlated (spatially and temporally) with potato tuberworm densities within heaps, hinting that migration among heaps did not considerably affect within-heap population dynamics. Potato tuberworm levels were not correlated with ambient temperatures, perhaps because of the warm, humid, and constant microclimate within the heaps. We discuss the significance of our findings for control efforts of the potato tuberworm.