Daniela Hoffmann

Prey suitability of western flower thrips, Frankliniella occidentalis, and onion thrips, Thrips tabaci, for the predatory mite Amblyseius swirskii

Abstract Western flower thrips, Frankliniella occidentalis, and onion thrips, Thrips tabaci, are both important polyphagous pests of vegetables and ornamentals in greenhouses. Difficulties in biological control of these pests have prompted a search for new natural enemies. Most recently, the predatory mite Amblyseius swirskii has been commercialised as biological control agent of whiteflies and thrips. However, little is known about the suitability of thrips as prey for A. swirskii. We therefore assessed prey acceptance and life history of A. swirskii when feeding on F. occidentalis and T. tabaci at 25±1°C. Amblyseius swirskii juveniles preyed upon first larval instars of both F. occidentalis and T. tabaci but suffered from high mortality (67 and 78%). Developmental time (egg to adult) of A. swirskii was 7.8 days with either prey species. Adult A. swirskii females readily accepted first larval instars of both thrips species, which were attacked in <20 min on a leaf and <10 min in an artificial cage. Oviposition rates (0.92 and 0.99 eggs/female/day) and offspring sex ratios (63 and 70% females) were similar with F. occidentalis and T. tabaci as prey. Less than one-third of juveniles reaching adulthood and oviposition rates below one egg/female per day resulted in relatively low intrinsic rates of increase (r m) (0.056 and 0.024 per day with F. occidentalis and T. tabaci, respectively). Altogether, our study suggests that the recently reported superiority of A. swirskii to the widely used Neoseiulus cucumeris in suppression of thrips is due to other traits than its population growth capacity with thrips as prey.

Mycorrhiza-induced trophic cascade enhances fitness and population growth of an acarine predator

Research on trophic cascades in terrestrial ecosystems has only recently revealed that root-associated organisms interact with organisms living on aboveground plant parts. Arbuscular mycorrhizal (AM) symbiosis is a ubiquitous phenomenon, yet studies on its effect on aboveground natural enemies of herbivores are scarce and mainly deal with plant-mediated rather than herbivore-mediated interactions. Here, we studied herbivore-mediated effects of AM symbiosis on an acarine predator. We measured life history characteristics and population growth rates of Phytoseiulus persimilis preying on two-spotted spider mites, Tetranychus urticae, which were feeding on bean plants colonized or not colonized by the AM fungus Glomus mosseae. All major life history characteristics of P. persimilis, foremost oviposition rate, minimum prey requirements needed to reach adulthood, and developmental time, were positively affected by AM colonization of the host plant of their prey, together resulting in enhanced population growth rates of the predators. Hence, we hypothesize that a bottom-up trophic cascade may counteract the apparent negative effects of mycorrhizal symbiosis when promoting herbivory by promoting the predation of herbivores due to improved prey quality. We argue that this pathway may be involved in stabilizing plant–mycorrhizal symbiosis in ecosystems over time.

Arbuscular mycorrhizal symbiosis increases host plant acceptance and population growth rates of the two-spotted spider mite Tetranychus urticae

Most terrestrial plants live in symbiosis with arbuscular mycorrhizal (AM) fungi. Studies on the direct interaction between plants and mycorrhizal fungi are numerous whereas studies on the indirect interaction between such fungi and herbivores feeding on aboveground plant parts are scarce. We studied the impact of AM symbiosis on host plant choice and life history of an acarine surface piercing-sucking herbivore, the polyphagous two-spotted spider mite Tetranychus urticae. Experiments were performed on detached leaflets taken from common bean plants (Phaseolus vulgaris) colonized or not colonized by the AM fungus Glomus mosseae. T. urticae females were subjected to choice tests between leaves from mycorrhizal and non-mycorrhizal plants. Juvenile survival and development, adult female survival, oviposition rate and offspring sex ratio were measured in order to estimate the population growth parameters of T. urticae on either substrate. Moreover, we analyzed the macro- and micronutrient concentration of the aboveground plant parts. Adult T. urticae females preferentially resided and oviposited on mycorrhizal versus non-mycorrhizal leaflets. AM symbiosis significantly decreased embryonic development time and increased the overall oviposition rate as well as the proportion of female offspring produced during peak oviposition. Altogether, the improved life history parameters resulted in significant changes in net reproductive rate, intrinsic rate of increase, doubling time and finite rate of increase. Aboveground parts of colonized plants showed higher concentrations of P and K whereas Mn and Zn were both found at lower levels. This is the first study documenting the effect of AM symbiosis on the population growth rates of a herbivore, tracking the changes in life history characteristics throughout the life cycle. We discuss the AM-plant-herbivore interaction in relation to plant quality, herbivore feeding type and site and the evolutionary implications in a multi-trophic context.

Arbuscular mycorrhiza enhances preference of ovipositing predatory mites for direct prey-related cues

Most terrestrial plants are associated with arbuscular mycorrhizal fungi but research on the effects of arbuscular mycorrhizal symbiosis on aboveground plant‐associated organisms is scarcely expanded to tri‐trophic systems. The arbuscular mycorrhizal fungus Glomus mosseae Nicol. & Gerd. enhances fitness of the two‐spotted spider mite Tetranychus urticae Koch and its natural enemy, the predatory mite Phytoseiulus persimilis Athias‐Henriot, via changes in host plant and prey quality, respectively. In the present study, it is hypothesized that gravid P. persimilis are able to recognize arbuscular mycorrhiza‐enhanced prey quality and behave accordingly. In two experiments, on leaf arenas and in cages, P. persimilis is given a choice between prey patches deriving from mycorrhizal and non‐mycorrhizal bean plants (Phaseolus vulgaris L.) as feeding and oviposition sites. The use of cages allows the manipulation of distinct patch components acting as possible cues to guide predator foraging and oviposition behaviours, such as eggs produced and traces (webbing and faeces) left by the spider mite females. Both experiments show that P. persimilis preferentially resides close to prey fed on mycorrhizal plants. The cage experiment reveals that P. persimilis uses direct prey‐related cues, mainly derived from eggs, to discern prey quality and preferentially oviposits close to prey from mycorrhizal plants. This is the first study to document that predators recognize arbuscular mycorrhiza‐induced changes in herbivorous prey quality via direct prey‐related cues.

Maternal manipulation of hatching asynchrony limits sibling cannibalism in the predatory mite Phytoseiulus persimilis

1. Sibling cannibalism is a common phenomenon in the animal kingdom but entails a high risk of direct and inclusive fitness loss for the mother and her offspring. Therefore, mechanisms limiting sibling cannibalism are expected to be selected for. One way of maternal manipulation of sibling cannibalism is to influence hatching asynchrony between nearby laid eggs. This has rarely been tested experimentally. 2. We examined the ability of ovipositing females of the cannibalistic predatory mite Phytoseiulus persimilis to influence the occurrence of sibling cannibalism among offspring by manipulating hatching asynchrony of nearby laid eggs. 3. In the first experiment, we assessed the occurrence of sibling cannibalism in relation to the hatching interval (24 h and 48 h) between nearby laid eggs. In the second experiment, we tested whether ovipositing females discriminate sites containing young (24-h old) and old (48-h old) eggs, fresh and old traces (metabolic waste products and possibly pheromones) left by the same female (24 h and 48 h ago), or young eggs plus fresh female traces and old eggs plus old female traces. Both experiments were conducted with and without prey. 4. Without prey, siblings were more likely to cannibalize each other if the hatching interval between nearby laid eggs was short (24 h). Cannibalism occurred less often when senior siblings (protonymphs) experienced a delay in the opportunity to cannibalize junior siblings (larvae). 5. Independent of prey availability, females preferentially added new eggs to sites containing old eggs plus old female traces but did neither distinguish between young and old eggs presented without own traces nor between fresh and old traces presented without eggs. 6. We discuss cue perception and use by P. persimilis females and contrast the outcome of our experiments and theoretical predictions of sibling cannibalism. We conclude that P. persimilis mothers increase hatching asynchrony of nearby laid eggs to prevent sibling cannibalism on the last produced offspring. Such a behaviour may be considered a simple form of maternal care increasing the survival prospects of offspring.

Mycorrhiza modulates aboveground tri-trophic interactions to the fitness benefit of its host plant

1. Arbuscular mycorrhiza (AM), the association of AM fungi and plant roots, may alter morphological and physiological attributes of aboveground plant parts and thereby influence plant‐associated organisms such as herbivores and their natural enemies, predators and parasitoids.

Effects of Euseius stipulatus on establishment and efficacy in spider mite suppression of Neoseiulus californicus and Phytoseiulus persimilis in clementine.

The two-spotted spider mite, Tetranychus urticae, is one of the most problematic phytophagous pests in Spanish clementine orchards. The most abundant predatory mites in this ecosystem are Euseius stipulatus, Phytoseiulus persimilis and Neoseiulus californicus. Euseius stipulatus is dominant but poorly adapted to utilize T. urticae as prey. It mainly persists on pollen and citrus red mite, Panonychus citri. A recent study suggested that the more efficacious T. urticae predators P. persimilis and N. californicus are negatively affected by lethal and non-lethal intraguild interactions with E. stipulatus. Here, we investigated the potential of N. californicus and P. persimilis to colonize and thrive on young clementine trees infested by T. urticae in presence and absence of E. stipulatus. Presence of E. stipulatus interfered with establishment and abundance of P. persimilis and negatively affected the efficacy of N. californicus in T. urticae suppression. In contrast, the abundance of E. stipulatus was not affected by introduction of a second predator. Trait-mediated effects of E. stipulatus changing P. persimilis and N. californicus behavior and/or life history were the most likely explanations for these outcomes. We conclude that superiority of E. stipulatus in intraguild interactions may indeed contribute to the currently observed predator species composition and abundance, rendering natural control of T. urticae in Spanish clementine orchards unsatisfactory. Nonetheless, stronger reduction of T. urticae and/or plant damage in the predator combination treatments as compared to E. stipulatus alone indicates the possibility to improve T. urticae control via repeated releases of N. californicus and/or P. persimilis.

Food imprinting revisited: early learning in foraging predatory mites.

Learning is a ubiquitous phenomenon in foraging animals, allowing behavioural optimisation in variable environments. Food imprinting is a specific form of learning restricted to the early stages of life and with long lasting consequences. However, since coining of the term four decades ago, the uniqueness of food imprinting has been largely questioned due to a putative mechanistic similarity with associative learning. Here, we demonstrate food imprinting in the predatory mite Neoseiulus californicus , which primarily feeds on spider mites but may use thrips as alternative prey. Brief (24 h) exposure to thrips (contact without feeding) early in life resulted in shorter attack latencies and consistently higher predation rates on thrips during adulthood. Predation and oviposition rates were positively correlated but oviposition did not differ between naive and experienced females. Our results suggest that food imprinting is indeed special because, unlike associative learning, it occurred without reinforcement, was restricted to a sensitive phase and persisted into adulthood. Food imprinting seems particularly advantageous when prey species availability varies little within generations and a given prey is difficult to ingest for young small but not older larger life stages. Food imprintability could be used to improve the efficacy of biocontrol agents such as N. californicus .