Why do predators attack parasitized prey? Insights from a probabilistic model and a literature survey.

Predators and parasitoids often encounter parasitized prey or hosts during foraging. While the outcomes of such encounters have been extensively studied for insect parasitoids, the consequences of a predator encountering parasitized prey have received less attention. One extreme example involves the potter wasp Delta dimidiatipenne that frequently provision their nest with parasitized caterpillars, despite the low suitability of this prey for consumption by their offspring. This raises two main questions: (1) why do female potter wasps continue collecting parasitized caterpillars? and (2) is this an exceptional example, or do predatory insects often suffer from fitness costs due to encounters with parasitized prey? We addressed the first question using a probabilistic mathematical model predicting the value of discrimination between parasitized and unparasitized prey for the potter wasp, and the second question by surveying the literature for examples in which the parasitism status of prey affected prey susceptibility, suitability, or prey choice by a predator. The model demonstrates that only under certain conditions is discrimination against parasitized prey beneficial in terms of the potter wasp's lifetime reproductive success. The literature survey suggests that the occurrence of encounters and consumption of parasitized prey is common, but the overall consequences of such interactions have rarely been quantified. We conclude that the profitability and ability of a predator to discriminate against parasitized prey under natural conditions may be limited and call for additional studies quantifying the outcome of such interactions.

Invasive brown widow spiders avoid parasitism despite high densities.

Invasive species are sometimes less susceptible to natural enemies compared to native species, but the mechanism is often unclear. Here we tested two potential mechanisms for lower parasitism of invasive species: density-dependent parasitism and preference for human-dominated habitats. We investigated how variation in host density and habitat type affect egg sac parasitism in two widow spider species (family Theridiidae). We compared parasitism on the egg sac of the brown widow, Latrodectus geometricus, an urban invasive species, and the white widow, Latrodectus pallidus, a species native to Israel. To investigate variation in host and parasitoid density, we measured nearest-neighbor distance between spider webs and parasitism rates in 16 sites, and in a single site monthly throughout a year. In L. pallidus, denser sites were more heavily parasitized (up to 55%) and parasitism rate increased with population density throughout the season. Extremely dense L. geometricus populations, however, had very low rates of parasitism (0-5%). We then conducted an egg sac transplant experiment in human-dominated and natural habitats. We found no parasitism of either species in the human-dominated habitat, compared to 30% parasitism of both species in the natural habitat. In addition, we found evidence for higher predation of L. pallidus than of L. geometricus egg sacs, particularly in the natural habitat. These combined results suggest that the human-dominated habitats inhabited by L. geometricus have a lower abundance of predators and parasites. We conclude that lower parasitism and predation in human-dominated habitats could contribute to the invasion success of L. geometricus.

The Impact of Terrestrial Oil Pollution on Parasitoid Wasps Associated With Vachellia (Fabales: Fabaceae) Trees in a Desert Ecosystem, Israel.

Oil is a major pollutant of the environment, and terrestrial oil spills frequently occur in desert areas. Although arthropods account for a large share of animal diversity, the effect of oil pollution on this group is rarely documented. We evaluated the effects of oil pollution on parasitoid wasps associated with Vachellia (formerly Acacia) tortilis (Forssk.) and Vachellia raddiana (Savi) trees in a hyper-arid desert that was affected by two major oil spills (in 1975 and 2014). We sampled the parasitoid populations between 2016 and 2018 in three sampling sites and compared their abundance, diversity, and community composition between oil-polluted and unpolluted trees. Parasitoid abundance in oil-polluted trees was lower in one of the sites affected by the recent oil spill, but not in the site affected by the 1975 oil spill. Oil-polluted trees supported lower parasitoid diversity than unpolluted trees in some sampling site/year combinations; however, such negative effects were inconsistent and pollution explained a small proportion of the variation in parasitoid community composition. Our results indicate that oil pollution may negatively affect parasitoid abundances and diversity, although the magnitude of the effect depends on the tree species, sampling site, and the time since the oil spill.

Parasitoid Abundance and Community Composition in Desert Vineyards and Their Adjacent Natural Habitats.

Parasitoids are important natural enemies of many agricultural pests. Preserving natural habitats around agricultural fields may support parasitoid populations. However, the success of such an approach depends on the ability of parasitoids to utilize both crop and natural habitats. While these aspects have been studied extensively in temperate regions, very little is known about parasitoid communities in desert agroecosystems. We took one step in this direction by sampling parasitoids in six vineyards and their surrounding natural desert habitat in a hyper-arid region of the Negev Desert Highlands, Israel. We predicted that due to the high contrast in environmental conditions, parasitoid abundance and community composition would differ greatly between the crop and the natural desert habitats. We found that parasitoid abundance differed between the habitats; however, the exact distribution pattern depended on the time of year-with higher numbers of parasitoids in the natural habitat at the beginning of the vine growth season and higher numbers in the vineyard at the middle and end of the season. Although parasitoid community composition significantly differed between the vineyard and desert habitats, this only accounted for ~4% of the total variation. Overall, our results do not strongly support the notion of distinct parasitoid communities in the crop vs. the desert environment, suggesting that despite environmental contrasts, parasitoids may move between and utilize resources in both habitats.

The combined impacts of wheat spatial position and phenology on cereal aphid abundance.

BACKGROUND: Wheat is a staple crop that suffers from massive yield losses caused by cereal aphids. Many factors can determine the abundance of cereal aphids and the damage they cause to plants; among them are the plant's genetic background, as well as environmental conditions such as spatial position within the plot, the composition and the distance from neighboring vegetation. Although the effects of these factors have been under scrutiny for many years, the combined effect of both factors on aphid populations is not fully understood. The goal of this study was to examine the collective impact of genotype and environment on wheat phenology (developmental stages), chemical diversity (metabolites), and insect susceptibility, as manifested by cereal aphid abundance. METHODS: To determine the influence of plant genotype on the metrics mentioned above, we measured the phenology, chemical profile, and aphid abundance of four wheat genotypes, including the tetraploid wild emmer (Triticum turgidum ssp. dicoccoides cv. Zavitan), tetraploid durum (Triticum turgidum ssp. durum cv. Svevo), and two hexaploid spring bread (Triticum aestivum), 'Rotem' and 'Chinese Spring'. These genotypes are referred to as "focal" plants. To evaluate the impact of the environment, we scored the distance of each focal plant (spatial position) from two neighboring vegetation types: (i) natural resource and (ii) monoculture wheat resource. RESULTS: The results demonstrated that the wild emmer wheat was the most aphid-resistant, while the bread wheat Rotem was most aphid-susceptible. Aphids were more abundant in plants that matured early. The spatial position analysis demonstrated that aphids were more abundant in focal plants located closer to the margin monoculture wheat resource rather than to the natural resource, suggesting a resource concentration effect. The analysis of metabolic diversity showed that the levels of three specialized metabolites from the flavonoid class, differed between the wheat genotypes and some minor changes in central metabolites were shown as well. Altogether, these results demonstrate a combined effect of genetic background and spatial position on wheat phenology and aphid abundance on plants. This exposes the potential role of the marginal vegetation environment in shaping the insect population of desirable crops. These findings highlight the importance of maintaining plant intra-specific variation in the agriculture system because of its potential applications in reducing pest density.

Frequency and consequences of the collection of already parasitized caterpillars by a potter wasp.

Maladaptive behaviors reflecting a "bad" choice of habitat or resource have been widely documented; however, their persistence is often difficult to interpret. The potter wasp Delta dimidiatipenne constructs mud cells, in each of which it lays a single egg and places several caterpillars to feed its offspring. Preliminary observations indicated that a portion of these caterpillars were already parasitized and contained the offspring of the gregarious parasitoid Copidosoma primulum. As a result, the offspring of the potter wasp often failed to develop. To characterize the distribution, frequency and consequences of this intriguing phenomenon, we surveyed potter wasp nests throughout the Negev Desert. Evidence for parasitized caterpillars (mummies) was found in ~85% of the sampled sites, in ~20% of previous years' nest cells and in ~70-80% of the same year's cells. The survival and pupal mass of the potter wasp offspring were negatively associated with the presence and number of parasitized caterpillars inside the cells. We concluded that the collection of parasitized caterpillars by D. dimidiantipenne is frequent and costly. The persistence of this behavior may result from limited discrimination ability against parasitized prey by female potter wasps, or by their limited ability to exhibit choosiness under field conditions.

Control of the Tomato Leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), in Open-Field Tomatoes by Indigenous Natural Enemies Occurring in Israel.

The tomato leafminer, Tuta absoluta (Meyrick), had established in Israel by 2010, attacking both open-field tomatoes and greenhouse crops.We searched for its natural enemies in open-field tomatoes, and tried to determine their potential for controlling this pest. We surveyed the local natural enemies in open tomato fields and measured their impact on pest populations in an unsprayed field. We assessed the suppressive ability of the dominant hemipteran predator, Nesidiocoris tenuis Reuter, against T. absoluta under controlled laboratory conditions and evaluated the impact of its augmentation on T. absoluta control in open-field tomatoes. We found five natural enemy species:the predator, N. tenuis, two braconids, and two eulophids. Predation accounted for 64.5±9.2% (mean ± SE) of T. absoluta larval mortality, whereas parasitism accounted for 20.96±7.5%. Together, they eliminated the pest population at tomato harvest time. Under controlled conditions, predation by N. tenuis rose from 58 to 72% with increased density of T. absoluta, suggesting positive density dependence. The reduction of T. absoluta (83%) by N. tenuis was higher than that of Bemisia tabaci (32%), suggesting a preference of N. tenuis for T. absoluta. Augmentation of N.tenuis was as effective as conventional treatment insecticide treatment, and plant damage was low and did not seem to affect yield. Results indicate that reduced pesticide use enables indigenous natural enemies, particularly N.tenuis, to successfully control T. absoluta and prevent crop damage in open-field tomatoes.