Early social isolation disrupts adult personality expression in group-living mites.

Animal personalities are characterized by intra-individual consistency and consistent inter-individual variability in behaviour across time and contexts. Personalities abound in animals, ranging from sea anemones to insects, arachnids, birds, fish and primates, yet the pathways mediating personality formation and expression remain elusive. Social conditions during the early postnatal period are known determinants of mean behavioural trait expressions later in life, but their relevance in shaping personality trajectories is unknown. Here, we investigated the consequences of early social isolation on adult personality expression in plant-inhabiting predatory mites Phytoseiulus persimilis. These mites are adapted to live in groups. We hypothesized that transient experience of social isolation early in life, that is, deprivation of any social contact during a sensitive window in the post-hatching phase, has enduring adverse effects on adult personality expression. Newly hatched mites were transiently reared in isolation or in groups and tested as adults for repeatability of various within-group behaviours, such as movement patterns and mutual interactions including sociability, defined as the propensity to associate and interact benignly with conspecifics, and activity patterns when alone. Groups composed of individuals with the same or different early-life experiences were repeatedly videotaped and individual behaviours were automatically analysed using AnimalTA. Social experiences early in life had persistent effects on mean behavioural traits as well as adult personality expression, as measured by intraclass correlation coefficients (indicating repeatability). On average, isolation-reared females moved at higher speeds, meandered less, kept greater distances from others and had fewer immediate neighbours than group-reared females. Group-reared females were highly repeatable in inter-individual distance, moving speed, meandering and area explored, whereas isolation-reared females were repeatable only in the number of immediate neighbours. Activity, quantified as the proportion of time spent moving within groups, was only repeatable in group-reared females, whereas activity, quantified as the proportion of time spent moving when alone, was only repeatable in females reared in isolation. Strikingly, also the early-life experiences of male mates influenced personality expression of mated females, with isolation-reared males boosting the repeatability of behavioural traits of group-reared females. Overall, our study provides evidence that a transient phase of social isolation during a critical period early in life has lasting effects that extend into adulthood, impairing adult personality expression. These effects should cascade upward, changing the phenotypic composition and diversity within populations.

Balancing in- and out-breeding by the predatory mite Phytoseiulus persimilis.

In- and out-breeding depressions are commonly observed phenomena in sexually reproducing organisms with a patchy distribution pattern, and spatial segmentation and/or isolation of groups. At the genetic level, inbreeding depression is due to increased homozygosity, whereas outbreeding depression is due to inferior genetic compatibility of mates. Optimal outbreeding theory suggests that intermediate levels of mate relatedness should provide for the highest fitness gains. Here, we assessed the fitness consequences of genetic relatedness between mates in plant-inhabiting predatory mites Phytoseiulus persimilis, which are obligatory sexually reproducing but haplo-diploid. Both females and males arise from fertilized eggs but males lose the paternal chromosome set during embryogenesis, dubbed pseudo-arrhenotoky. Phytoseiulus persimilis are highly efficacious in reducing crop-damaging spider mite populations and widely used in biological control. Using iso-female lines of two populations, from Sicily and Greece, we assessed the fecundity of females, and sex ratio of their offspring, that mated with either a sibling, a male from the same population or a male from the other population. Additionally, we recorded mating latency and duration. Females mating with a male from the same population produced more eggs, with a lower female bias, over a longer time than females mating with a sibling or with a male from the other population. Mating latency was unaffected by mate relatedness; mating duration was disproportionally long in sibling couples, likely indicating female reluctance to mate and sub-optimal spermatophore transfer. Our study provides a rare example of in- and out-breeding depression in a haplo-diploid arthropod, supporting the optimal outbreeding theory.

Non-associative versus associative learning by foraging predatory mites.

BACKGROUND: Learning processes can be broadly categorized into associative and non-associative. Associative learning occurs through the pairing of two previously unrelated stimuli, whereas non-associative learning occurs in response to a single stimulus. How these two principal processes compare in the same learning task and how they contribute to the overall behavioural changes brought about by experience is poorly understood. We tackled this issue by scrutinizing associative and non-associative learning of prey, Western flower thrips Frankliniella occidentalis, by the predatory mite, Neoseiulus californicus. We compared the behaviour of thrips-experienced and -naïve predators, which, early in life, were exposed to either thrips with feeding (associative learning), thrips without feeding (non-associative learning), thrips traces on the surface (non-associative learning), spider mites with feeding (thrips-naïve) or spider mite traces on the surface (thrips-naïve). RESULTS: Thrips experience in early life, no matter whether associative or not, resulted in higher predation rates on thrips by adult females. In the no-choice experiment, associative thrips experience increased the predation rate on the first day, but shortened the longevity of food-stressed predators, a cost of learning. In the choice experiment, thrips experience, no matter whether associative or not, increased egg production, an adaptive benefit of learning. CONCLUSIONS: Our study shows that both non-associative and associative learning forms operate in foraging predatory mites, N. californicus. The non-rewarded thrips prey experience produced a slightly weaker, but less costly, learning effect than the rewarded experience. We argue that in foraging predatory mites non-associative learning is an inevitable component of associative learning, rather than a separate process.

Transgenerational loss and recovery of early learning ability in foraging predatory mites.

The ability to learn is ubiquitous in animals but highly variable within and between species, populations and individuals. Diet-related circumstances, such as diet quantity and quality can influence both long-term constitutive (genetic; by selection) and short-term operational (non-genetic; by the immediate circumstances) learning performance. Here, we scrutinized the causes of loss of learning ability, following multi-generational feeding on pollen, in a line of the predatory mite Amblyseius swirskii, which was previously well able to learn prey during early life, enhancing foraging later in life. We investigated whether, and, if so, how quickly, a transgenerational diet switch to live prey restores the early learning ability of foraging predatory mites. The first experiment shows that the early learning ability was restored after switching the diet of the pollen-fed predator line to live spider mites for two generations before conducting the behavioral assay. The second experiment reveals that offspring regained their learning ability if the diet of their mothers was switched from pollen to spider mites for 3 or 10 days before offspring production. Both experiments in concert suggest transgenerational, pollen-induced operational loss of learning ability in the predatory mite A. swirskii. Maternally-transmitted nutrient deficiency and/or maternally-induced epigenetic changes are the most plausible explanations for the pollen diet-induced loss of learning ability. Our study represents a key example for maternal diet-induced variation in learning ability.

Predation risk-mediated maternal effects in the two-spotted spider mite, Tetranychus urticae.

Predation risk is a strong selective force shaping prey morphology, physiology, life history and/or behavior. As a prime stressor, predation risk may even induce trans-generational alterations, called maternal effects. Accordingly, maternal predation risk during offspring production may influence offspring life history and anti-predator behavior. Here, we assessed whether different levels of predation risk, posed by the predatory mite Phytoseiulus persimilis, induce graded maternal effects in its prey, the herbivorous two-spotted spider mite Tetranychus urticae. First, we generated four types of predation risk-stressed spider mite mothers by exposing them to living predators, direct and indirect predator cue combinations or no predator cues, respectively. Then, we investigated the life history (offspring developmental time, sex) and anti-predator response (activity, position on the leaf) of their offspring on leaves with and without direct and indirect predator cues. Maternal stress, no matter of the predation risk level, prolonged the offspring developmental time, as compared to offspring from unstressed mothers. This pattern was more pronounced on leaves with than without predator cues. Offspring from stressed mothers resided more likely on the leaf blade than close to the leaf vein. Offspring sex ratio and activity were not influenced by maternal predation risk but activity was higher on leaves with than without predator cues. We argue that the prolonged developmental time is non-adaptive, yet the changed site preference is adaptive because reducing the encounter likelihood with predators. Our study represents a key example for predation risk-mediated maternal effects on developmental trajectories of offspring.

Systemic above- and belowground cross talk: hormone-based responses triggered by Heterodera schachtii and shoot herbivores in Arabidopsis thaliana.

Above- and belowground plant parts are simultaneously attacked by different pests and pathogens. The host mediates these interactions and physiologically reacts, e.g. with local and systemic alterations of endogenous hormone levels coupled with coordinated transcriptional changes. This in turn affects attractiveness and susceptibility of the plant to subsequent attackers. Here, the model plant Arabidopsis thaliana is used to study stress hormone-based systemic responses triggered by simultaneous root parasitism by the cyst nematode Heterodera schachtii and shoot herbivory by the thrips Frankliniella occidentalis and the spider mite Tetranychus urticae. First, HPLC/MS and quantitative reverse transcriptase PCR are used to show that nematode parasitism strongly affects stress hormone levels and expression of hormone marker genes in shoots. Previous nematode infection is then demonstrated to affect the behavioural and life history performance of both arthropods. While thrips explicitly avoid nematode-infected plants, spider mites prefer them. In addition, the life history performance of T. urticae is significantly enhanced by nematode infection. Finally, systemic changes triggered by shoot-feeding F. occidentalis but not T. urticae are shown to make the roots more attractive for H. schachtii. This work emphasises the importance of above- and belowground signalling and contributes to a better understanding of plant systemic defence mechanisms against plant-parasitic nematodes.

Food stress causes sex-specific maternal effects in mites.

Life history theory predicts that females should produce few large eggs under food stress and many small eggs when food is abundant. We tested this prediction in three female-biased size-dimorphic predatory mites feeding on herbivorous spider mite prey: Phytoseiulus persimilis, a specialized spider mite predator; Neoseiulus californicus, a generalist preferring spider mites; Amblyseius andersoni, a broad diet generalist. Irrespective of predator species and offspring sex, most females laid only one small egg under severe food stress. Irrespective of predator species, the number of female but not male eggs decreased with increasing maternal food stress. This sex-specific effect was probably due to the higher production costs of large female than small male eggs. The complexity of the response to the varying availability of spider mite prey correlated with the predators' degree of adaptation to this prey. Most A. andersoni females did not oviposit under severe food stress, whereas N. californicus and P. persimilis did oviposit. Under moderate food stress, only P. persimilis increased its investment per offspring, at the expense of egg number, and produced few large female eggs. When prey was abundant, P. persimilis decreased the female egg sizes at the expense of increased egg numbers, resulting in a sex-specific egg size/number trade-off. Maternal effects manifested only in N. californicus and P. persimilis. Small egg size correlated with the body size of daughters but not sons. Overall, our study provides a key example of sex-specific maternal effects, i.e. food stress during egg production more strongly affects the sex of the large than the small offspring.

Spider mites adaptively learn recognizing mycorrhiza-induced changes in host plant volatiles.

Symbiotic root micro-organisms such as arbuscular mycorrhizal fungi commonly change morphological, physiological and biochemical traits of their host plants and may thus influence the interaction of aboveground plant parts with herbivores and their natural enemies. While quite a few studies tested the effects of mycorrhiza on life history traits, such as growth, development and reproduction, of aboveground herbivores, information on possible effects of mycorrhiza on host plant choice of herbivores via constitutive and/or induced plant volatiles is lacking. Here we assessed whether symbiosis of the mycorrhizal fungus Glomus mosseae with common bean plants Phaseolus vulgaris influences the response of the two-spotted spider mite Tetranychus urticae to volatiles of plants that were clean or infested with spider mites. Mycorrhiza-naïve and -experienced spider mites, reared on mycorrhizal or non-mycorrhizal bean plants for several days before the experiments, were subjected to Y-tube olfactometer choice tests. Experienced but not naïve spider mites distinguished between constitutive volatiles of clean non-mycorrhizal and mycorrhizal plants, preferring the latter. Neither naïve nor experienced spider mites distinguished between spider mite-induced volatiles of mycorrhizal and non-mycorrhizal plants. Learning the odor of clean mycorrhizal plants, resulting in a subsequent preference for these odors, is adaptive because mycorrhizal plants are more favorable host plants for fitness of the spider mites than are non-mycorrhizal plants.

Early-life intraguild predation risk produces adaptive personalities in predatory mites.

Animal personalities are defined by within-individual consistency, and consistent among-individual variation, in behavior across time and/or contexts. Here we hypothesized that brief early-life experience of intraguild predation (IGP) risk has enduring phenotypic effects on personality expression in boldness and aggressiveness in later life. We tested our hypothesis in predatory mites Phytoseiulus persimilis, which are IG predators with ontogenetic role reversals, i.e., they are potential IG prey during early life but IG predators as adults. Adult P. persimilis females, which had experienced IGP risk early in life or not, were subjected to three tests each for boldness and aggressiveness. IGP-experienced individuals were on average bolder and more aggressive. Boldness was moderately repeatable, aggressiveness was weakly repeatable. Strikingly, early-life IGP experience shifted the within-group personality composition toward consistently bold and aggressive personalities. Phenotypic adjustment of personality expression was adaptive, as indicated by the positive correlation between personality scores and egg production.

From repulsion to attraction: species- and spatial context-dependent threat sensitive response of the spider mite Tetranychus urticae to predatory mite cues.

Prey perceiving predation risk commonly change their behavior to avoid predation. However, antipredator strategies are costly. Therefore, according to the threat-sensitive predator avoidance hypothesis, prey should match the intensity of their antipredator behaviors to the degree of threat, which may depend on the predator species and the spatial context. We assessed threat sensitivity of the two-spotted spider mite, Tetranychus urticae, to the cues of three predatory mites, Phytoseiulus persimilis, Neoseiulus californicus, and Amblyseius andersoni, posing different degrees of risk in two spatial contexts. We first conducted a no-choice test measuring oviposition and activity of T. urticae exposed to chemical traces of predators or traces plus predator eggs. Then, we tested the site preference of T. urticae in choice tests, using artificial cages and leaves. In the no-choice test, T. urticae deposited their first egg later in the presence of cues of P. persimilis than of the other two predators and cue absence, indicating interspecific threat-sensitivity. T. urticae laid also fewer eggs in the presence of cues of P. persimilis and A. andersoni than of N. californicus and cue absence. In the artificial cage test, the spider mites preferred the site with predator traces, whereas in the leaf test, they preferentially resided on leaves without traces. We argue that in a nonplant environment, chemical predator traces do not indicate a risk for T. urticae, and instead, these traces function as indirect habitat cues. The spider mites were attracted to these cues because they associated them with the existence of a nearby host plant.

Phenotypic plasticity in anti-intraguild predator strategies: mite larvae adjust their behaviours according to vulnerability and predation risk.

Interspecific threat-sensitivity allows prey to maximize the net benefit of antipredator strategies by adjusting the type and intensity of their response to the level of predation risk. This is well documented for classical prey-predator interactions but less so for intraguild predation (IGP). We examined threat-sensitivity in antipredator behaviour of larvae in a predatory mite guild sharing spider mites as prey. The guild consisted of the highly vulnerable intraguild (IG) prey and weak IG predator Phytoseiulus persimilis, the moderately vulnerable IG prey and moderate IG predator Neoseiulus californicus and the little vulnerable IG prey and strong IG predator Amblyseius andersoni. We videotaped the behaviour of the IG prey larvae of the three species in presence of either a low- or a high-risk IG predator female or predator absence and analysed time, distance, path shape and interaction parameters of predators and prey. The least vulnerable IG prey A. andersoni was insensitive to differing IGP risks but the moderately vulnerable IG prey N. californicus and the highly vulnerable IG prey P. persimilis responded in a threat-sensitive manner. Predator presence triggered threat-sensitive behavioural changes in one out of ten measured traits in N. californicus larvae but in four traits in P. persimilis larvae. Low-risk IG predator presence induced a typical escape response in P. persimilis larvae, whereas they reduced their activity in the high-risk IG predator presence. We argue that interspecific threat-sensitivity may promote co-existence of IG predators and IG prey and should be common in predator guilds with long co-evolutionary history.

Spider mite males undress females to secure the first mating.

Intense mate competition favors the evolution of extraordinary mating strategies such as the ability of males to identify premature females that are close to becoming mature and associate with them until they are sexually receptive (dubbed precopulatory mate guarding). Owing to possible take-overs by rival males, precopulatory guarding is a high-risk, time- and energy-intensive strategy. Here, we provide experimental evidence that guarding spider mite males undress females by actively removing the exuvia during ecdysis to adult; females undressed by guarding males eclose faster than unguarded females. Such behavior is adaptive because it maximizes the guard's chances of being the first mate.

Correction: Jafari et al. Modeling Thermal Developmental Trajectories and Thermal Requirements of the Ladybird Stethorus gilvifrons. Insects 2023, 14, 11.

Following the publication of [...].

Thermal Oviposition Performance of the Ladybird Stethorus gilvifrons Preying on Two-Spotted Spider Mites.

The ladybird, Stethorus gilvifrons (Mulsant) (Coleoptera: Coccinellidae), is an important predator of two-spotted spider mites, Tetranychus urticae Koch (Acari: Tetranychidae), in southeastern Europe and western and southwestern Asia, such as Iran, India, and Turkey. To enhance forecasting the occurrence and performance of this predator in natural control and improve its usage in biological control, we evaluated and compared four non-linear oviposition models, i.e., Enkegaard, Analytis, Bieri-1, and Bieri-2. The models were validated by using data of age-specific fecundity of female S. gilvifrons at six constant temperatures (15, 20, 25, 27, 30, and 34 °C). All four models provided good fit quality to age-dependent oviposition at 15 to 30 °C (R2 0.67 to 0.94; R2adj 0.63 to 0.94) but had a poor fit at 34 °C (R2 0.33 to 0.40; R2adj 0.17 to 0.34). Within temperatures, the best performing models were Bieri-1 (R2), Bieri-2 (R2adj), and Analytis (RSS) at 15 °C, Bieri-1 at 27 °C, and Analytis at 20, 25, and 30 °C. Analytis was the best suited model across the wide temperature range tested (from 15 to 30 °C). The models presented here allow for prediction of the population dynamics of S. gilvifrons in field and greenhouse crops in temperate and subtropical climates.

Social familiarity modulates group living and foraging behaviour of juvenile predatory mites.

Environmental stressors during early life may have persistent consequences for phenotypic development and fitness. In group-living species, an important stressor during juvenile development is the presence and familiarity status of conspecific individuals. To alleviate intraspecific conflicts during juvenile development, many animals evolved the ability to discriminate familiar and unfamiliar individuals based on prior association and use this ability to preferentially associate with familiar individuals. Assuming that familiar neighbours require less attention than unfamiliar ones, as predicted by limited attention theory, assorting with familiar individuals should increase the efficiency in other tasks. We assessed the influence of social familiarity on within-group association behaviour, development and foraging of juvenile life stages of the group-living, plant-inhabiting predatory mite Phytoseiulus persimilis. The observed groups consisted either of mixed-age familiar and unfamiliar juvenile mites or of age-synchronized familiar or unfamiliar juvenile mites or of pairs of familiar or unfamiliar larvae. Overall, familiar mites preferentially grouped together and foraged more efficiently, i.e. needed less prey at similar developmental speed and body size at maturity, than unfamiliar mites. Preferential association of familiar mites was also apparent in the inter-exuviae distances. Social familiarity was established by imprinting in the larval stage, was not cancelled or overridden by later conspecific contacts and persisted into adulthood. Life stage had an effect on grouping with larvae being closer together than nymphal stages. Ultimately, optimized foraging during the developmental phase may relax within-group competition, enhance current and future food supply needed for optimal development and optimize patch exploitation and leaving under limited food.

Intraguild predation and cannibalism between the predatory mites Neoseiulus neobaraki and N. paspalivorus, natural enemies of the coconut mite Aceria guerreronis.

Neoseiulus neobaraki and N. paspalivorus are amongst the most common phytoseiid predators of coconut mite, Aceria guerreronis, found in the spatial niche beneath coconut fruit bracts. Both predators may occur on the same coconut palms in Benin and Tanzania and are therefore likely to interact with each other. Here, we assessed cannibalism and intraguild predation (IGP) of the two predators in the absence and presence of their primary prey A. guerreronis. In the absence of the shared extraguild prey, A. guerreronis, N. neobaraki killed 19 larvae of N. paspalivorus per day and produced 0.36 eggs/female/day, while the latter species killed only 7 larvae of the former and produced 0.35 eggs/female/day. Presence of A. guerreronis only slightly decreased IGP by N. neobaraki but strongly decreased IGP by N. paspalivorus, which consumed 4-7 times less IG prey than N. neobaraki. Resulting predator offspring to IG prey ratios were, however, 4-5 times higher in N. paspalivorus than N. neobaraki. Overall, provision of A. guerreronis increased oviposition in both species. In the cannibalism tests, in the absence of A. guerreronis, N. neobaraki and N. paspalivorus consumed 1.8 and 1.2 conspecific larvae and produced almost no eggs. In the presence of abundant herbivorous prey, cannibalism dramatically decreased but oviposition increased in both N. neobaraki and N. paspalivorus. In summary, we conclude that (1) N. neobaraki is a much stronger intraguild predator than N. paspalivorus, (2) cannibalism is very limited in both species, and (3) both IGP and cannibalism are reduced in the presence of the common herbivorous prey with the exception of IGP by N. neobaraki, which remained at high levels despite presence of herbivorous prey. We discuss the implications of cannibalism and IGP on the population dynamics of A. guerreronis and the predators in view of their geographic and within-palm distribution patterns.

Transgenerational effects of grandparental and parental diets combine with early-life learning to shape adaptive foraging phenotypes in Amblyseius swirskii.

Transgenerational effects abound in animals. While a great deal of research has been dedicated to the effects of maternal stressors such as diet deficiency, social deprivation or predation risk on offspring phenotypes, we have a poor understanding of the adaptive value of transgenerational effects spanning across multiple generations under benign conditions and the relative weight of multigenerational effects. Here we show that grandparental and parental diet experiences combine with personal early-life learning to form adaptive foraging phenotypes in adult plant-inhabiting predatory mites Amblyseius swirskii. Our findings provide insights into transgenerational plasticity caused by persistent versus varying conditions in multiple ancestral generations and show that transgenerational effects may be adaptive in non-matching ancestor and offspring environments.

Modeling Thermal Developmental Trajectories and Thermal Requirements of the Ladybird Stethorus gilvifrons.

The development rate of the predatory ladybird, Stethorus gilvifrons (Mulsant), fed on Tetranychus urticae Koch, was determined at 15, 20, 25, 27, 30, 34, and 38 °C. The total development time from egg to adult emergence for females was estimated to be 61.4, 31.6, 14.4, 13.3, 12.5, and 11.7 days, respectively. The development time decreased with increasing temperature from 15 to 34 °C, but all eggs failed to hatch at 38 °C. The lower temperature threshold (T0) for the entire development period and the thermal constant (K) for female S. gilvifrons were estimated to be 11.64 °C and 194.50 degree-days (DD) using the common linear model, and 11.96 °C and 187.87 DD using the Ikemoto and Takai model, respectively. Data were fitted to 20 non-linear development rate models and the thermal thresholds (Tmin and Tmax) and optimal temperature (Topt) were estimated. Among non-linear models, the Briere-2 and Ikemoto and Takai linear model provided adequate descriptions of the temperature-dependent development of S. gilvifrons. The upper-temperature threshold was estimated to be about 44 °C using the Logan-10 non-linear model. The estimated thermal development characteristics can be used to predict the occurrence and the population dynamics, as well as to improve the mass rearing and release, of S. gilvifrons for the biological control of T. urticae.

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.

Not Seeing the Mites for the Hairs. Comment on Möth et al. Unexpected Effects of Local Management and Landscape Composition on Predatory Mites and Their Food Resources in Vineyards. Insects 2021, 12, 180.

Möth et al. (2021) [...].