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.

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.

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.

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) [...].

Learned predators enhance biological control via organizational upward and trophic top-down cascades.

Learning is a behavioural change based on memory of previous experiences and a ubiquitous phenomenon in animals. Learning effects are commonly life-stage- and age-specific. In many animals, early life experiences lead to pervasive and persistent behavioural changes.There is broad consensus that learning has far-reaching implications to biological control. Proximate and ultimate factors of individual learning by parasitoids and true predators are relatively well understood, yet the consequences of learning to higher organizational levels, populations and communities, and top-down trophic cascades are unexplored.We addressed this issue using a tri-trophic system consisting of predatory mites Amblyseius swirskii, Western flower thrips Frankliniella occidentalis and whole common bean plants, Phaseolus vulgaris. F. occidentalis are notorious horticultural pests that are difficult to control. Therefore, practitioners have much to gain by optimizing biological control of thrips.Previous studies have shown that early life experience of thrips by A. swirskii improves foraging on thrips later in life due to decreased prey recognition times and increased predation rates, together enhancing predator fecundity. Here, we hypothesized that early learning by A. swirskii enhances biological control of thrips via immediate and cascading effects. We predicted that release of thrips-experienced predators enhances predator population growth and thrips suppression and reduces plant damage as compared to release of thrips-naïve predators.The behavioural changes brought about by early learning cascaded up to the population and community levels. Thrips-experienced predators caused favourable immediate and cascading effects that could not be compensated for in populations founded by thrips-naïve predators. Populations founded by thrips-experienced predators grew faster, reached higher abundances, were more efficacious in suppressing an emerging thrips population and kept plant damage at lower levels than populations founded by thrips-naïve predators. Plant fecundity correlated negatively with thrips abundance and positively with predatory mite abundance. Improved biological control was mainly due to thrips-experienced founders providing for a head-start in predator population growth and thrips suppression. Synthesis and applications. Our study suggests that learned natural enemies have high potential to optimize augmentative biological control on a larger scale due to favourably modulating organizational upward and trophic top-down cascades.

Plant Growth-Promoting Rhizobacteria Enhance Defense of Strawberry Plants Against Spider Mites.

Plants mediate interactions between below- and above-ground microbial and animal communities. Microbial communities of the rhizosphere commonly include mutualistic symbionts such as mycorrhizal fungi, rhizobia and free-living plant growth-promoting rhizobacteria (PGPR) that may influence plant growth and/or its defense system against aboveground pathogens and herbivores. Here, we scrutinized the effects of three PGPR, Azotobacter chroococcum, Azospirillum brasilense, and Pseudomonas brassicacearum, on life history and population dynamics of two-spotted spider mites, Tetranychus urticae, feeding on aboveground tissue of strawberry plants, and examined associated plant growth and physiology parameters. Our experiments suggest that these three species of free-living rhizobacteria strengthen the constitutive, and/or induce the direct, anti-herbivore defense system of strawberry plants. All three bacterial species exerted adverse effects on life history and population dynamics of T. urticae and positive effects on flowering and physiology of whole strawberry plants. Spider mites, in each life stage and in total, needed longer time to develop on PGPR-treated plants and had lower immature survival rates than those fed on chemically fertilized and untreated plants. Reduced age-specific fecundity, longer developmental time and lower age-specific survival rates of mites feeding on rhizobacteria treated plants reduced their intrinsic rate of increase as compared to mites feeding on chemically fertilized and control plants. The mean abundance was lower in spider mite populations feeding on PGPR-treated strawberries than in those feeding on chemically fertilized and untreated plants. We argue that the three studied PGPR systemically strengthened and/or induced resistance in above-ground plant parts and enhanced the level of biochemical anti-herbivore defense. This was probably achieved by inducing or upregulating the production of secondary plant metabolites, such as phenolics, flavonoids and anthocyanins, which were previously shown to be involved in induced systemic resistance of strawberry plants. Overall, our study emphasizes that PGPR treatment can be a favorable strawberry plant cultivation measure because providing essential nutrients needed for proper plant growth and at the same time decreasing the life history performance and population growth of the notorious herbivorous pest T. urticae.

Kin-Mediated Male Choice and Alternative Reproductive Tactics in Spider Mites.

Optimal outbreeding and kin selection theories state that the degree of kinship is a fundamental determinant in any mating system. However, the role of kinship in male choice and alternative reproductive tactics (ARTs) is poorly known. We assessed the influence of kinship on male choice and expression of ARTs in two populations of two-spotted spider mites Tetranychus urticae. Male spider mites guard premature females, which is an indicator of mate choice, and may conditionally adopt fighting or sneaking tactics to secure access to females. Males competing with kin or non-kin were offered one kin or non-kin female (experiment 1) and single males were presented a choice of kin and non-kin females (experiment 2). Under kin competition, males of both populations were more prone to guard non-kin than kin females at a 3:1 fighter:sneaker ratio. Under non-kin competition, all males were fighters. Under no-choice, males used novelty as indicator of genetic dissimilarity, serving as absolute decision rule for outbreeding. Under choice, comparative evaluation allowed males to preferentially guard females with higher reproductive potential. Overall, our study suggests that male spider mites can assess kinship of rivals and prospective mates. Kin discrimination allows adaptive, context-specific non-random mating preference and adjustment of ARTs.

Plastic female choice to optimally balance (k)in- and out-breeding in a predatory mite.

Both close inbreeding and extreme outbreeding may negatively affect direct fitness. Optimal outbreeding theory suggests that females should preferentially mate with distantly related males. (K)in breeding theory suggests that, at similar direct fitness costs of close inbreeding and extreme outbreeding, females should prefer close kin to non-kin. Empirical evidence of plastic female choice for an optimal balance between close inbreeding and extreme outbreeding remains elusive. We tested the combined predictions of optimal outbreeding and (k)in breeding theories in predatory mites Phytoseiulus persimilis from two origins, Sicily and Greece, which suffer from both close inbreeding and extreme outbreeding depression. In three separate experiments, virgin females were presented binary choices between familiar and unfamiliar brothers, and between familiar/unfamiliar brothers and distant kin or non-kin. Females of Greece but not Sicily preferred unfamiliar to familiar brothers. Females of both origins preferred distant kin to unfamiliar and familiar brothers but preferred unfamiliar brothers to non-kin. Females of Sicily but not Greece preferred familiar brothers to non-kin. The suggested kin recognition mechanisms are phenotype matching and direct familiarity, with finer-tuned recognition abilities of Greece females. Overall, our experiments suggest that flexible mate choice by P. persimilis females allows optimally balancing inclusive fitness trade-offs.

Spider mite mothers adjust reproduction and sons' alternative reproductive tactics to immigrating alien conspecifics.

Maternal effects on environmentally induced alternative reproductive tactics (ARTs) are poorly understood but likely to be selected for if mothers can reliably predict offspring environments. We assessed maternal effects in two populations (Y and G) of herbivorous arrhenotokous spider mites Tetranychus urticae, where males conditionally express fighting and sneaking tactics in male-male combat and pre-copulatory guarding behaviour. We hypothesized that resident mothers should adjust their reproduction and sons' ARTs to immigrating alien conspecifics in dependence of alien conspecifics posing a fitness threat or advantage. To induce maternal effects, females were exposed to own or alien socio-environments and mated to own or alien males. Across maternal and sons' reproductive traits, the maternal socio-environment induced stronger effects than the maternal mate, and G-mothers responded more strongly to Y-influence than vice versa. G-socio-environments and Y-mates enhanced maternal egg production in both populations. Maternal exposure to G-socio-environments demoted, yet maternal Y-mates promoted, guarding occurrence and timing by sons. Sneakers guarded earlier than fighters in Y-environments, whereas the opposite happened in G-environments. The endosymbiont Cardinium, present in G, did not exert any classical effect but may have played a role via the shared plant. Our study highlights interpopulation variation in immediate and anticipatory maternal responses to immigrants.

Founder effects on trans-generational dynamics of closed inbreeding lineages of the predatory mite Phytoseiulus persimilis.

Both close inbreeding and distant outbreeding may reduce fitness below the level of individuals with intermediate parental relatedness. In the haplodiploid plant-inhabiting predatory mite Phytoseiulus persimilis, which is patchily distributed within and among host plants, fitness is indeed reduced in the short term, i.e. by a single generation of inbreeding. However, in the medium to long term (multiple generations), distant out-breeding should provide for favorable demographic founder effects in isolated populations. We tested this prediction in isolated experimental lineages founded by females mated to a sibling (close inbreeding), a male from the same population (intermediate relatedness) or a male from another population (distant outbreeding) and monitored lineage growth and persistence over four generations. Cross-generationally, lineages founded by distantly outbred females performed the best, i.e. produced the most descendants. However, this was solely due to superior performance from the F2 generation onwards, whereas in the F1 generation, lineages founded by females mated to males from their own population (intermediate relatedness) performed the best, as predicted from short-term in- and out-breeding depression effects. At the genetic level, this result was most likely due to distantly outbred founders introducing higher allelic variability and lower homozygosity levels, counterbalancing inbreeding depression, which inevitably occurs in isolated lineages, from the F2 generation onwards.

Herbivore-Associated Bacteria as Potential Mediators and Modifiers of Induced Plant Defense Against Spider Mites and Thrips.

Induced plant defense, comprising contact with exogenous stimuli, production of endogenous signals alerting the plant, associated biochemical cascades, and local and/or systemic expression of the defense mechanisms, critically depends on the nature of the inducing agents. At large, bio-trophic pathogenic microorganisms and viruses usually trigger the salicylate (SA)-mediated pathway, whereas necro-trophic pathogens and herbivores usually trigger the jasmonate (JA)-mediated pathway in plants. The SA- and JA-mediated pathways do not operate independently but commonly interfere with each other. Several recent studies revealed abnormal plant responses upon herbivore attack in diverse plant-herbivore systems. Observed abnormalities range from suppression of the common JA-pathway, induction of the SA-pathway to no response, yet the underlying proximate causes and ultimate consequences of these variations are elusive. Strikingly, some studies provide compelling evidence that anti-herbivore plant responses may decisively depend on bacteria associated with the herbivore attacking the plant (HAB for herbivore-associated bacteria). HAB may influence herbivore recognition by the plant and alter the biochemical cascades inside plants. Here, I report cases in point of HAB manipulating induced anti-herbivore plant responses, suggest spatial and temporal categorization of HAB, and point at proximate and ultimate aspects of plant defense manipulation by HAB. Following, I overview the diversity of HAB of spider mites and herbivorous thrips, argue that, considering recently reported phenomena of abnormal plant responses upon spider mite attack, some of these HAB could represent important, but hitherto largely neglected, mediators/modifiers of induced plant defense against spider mites and thrips, and conclude with suggestions for future research.

Categorizing experience-based foraging plasticity in mites: age dependency, primacy effects and memory persistence.

Behavioural plasticity can be categorized into activational (also termed contextual) and developmental plasticity. Activational plasticity allows immediate contextual behavioural changes, whereas developmental plasticity is characterized by time-lagged changes based on memory of previous experiences (learning). Behavioural plasticity tends to decline with age but whether this holds true for both plasticity categories and the effects of first-in-life experiences is poorly understood. We tackled this issue by assessing the foraging plasticity of plant-inhabiting predatory mites, Amblyseius swirskii, on thrips and spider mites following age-dependent prey experience, i.e. after hatching or after reaching maturity. Juvenile and young adult predator females were alternately presented thrips and spider mites, for establishing 1st and 2nd prey-in-life experiences, and tested, as gravid females, for their foraging plasticity when offered both prey species. Prey experience by juvenile predators resulted in clear learning effects, which were evident in likelier and earlier attacks on familiar prey, and higher proportional inclusion of familiar prey in total diet. First prey-in-life experience by juvenile but not adult predators resulted in primacy effects regarding attack latency. Prey experience by adult predators resulted mainly in prey-unspecific physiological changes, with easy-to-grasp spider mites providing higher net energy gains than difficult-to-grasp thrips. Prey experience by juvenile, but not adult, predators was adaptive, which was evident in a negative correlation between attack latencies and egg production. Overall, our study provides key evidence that similar experiences by juvenile and adult predators, including first-in-life experiences, may be associated with different types of behavioural plasticity, i.e. developmental and activational plasticity.

Corrigendum: Benefit-cost Trade-offs of Early Learning in Foraging Predatory Mites Amblyseius Swirskii.

This corrects the article DOI: 10.1038/srep23571.

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.

Low level of polyandry constrains phenotypic plasticity of male body size in mites.

Polyandry, i.e. females mating with multiple males, is more common than previously anticipated and potentially provides both direct and indirect fitness benefits to females. The level of polyandry (defined by the lifetime number of male mates of a female) is an important determinant of the occurrence and intensity of sexual selection acting on male phenotypes. While the forces of sexual selection acting on phenotypic male traits such as body size are relatively well understood, sexual selection acting on phenotypic plasticity of these traits is unexplored. We tackled this issue by scrutinizing the link between polyandry and phenotypic plasticity of male body size in two sympatric plant-inhabiting predatory mite species, Phytoseiulus persimilis and Neoseiulus californicus. These two species are similar in life history, ecological niche requirements, mating behavior, polygyny and female body size plasticity but strikingly differ in the level of both polyandry and phenotypic plasticity of male body size (both lower in P. persimilis). We hypothesized that deviations from standard body size, i.e. the size achieved under favorable conditions, incur higher costs for males in the less polyandrous P. persimilis. To test our hypotheses, we conducted two experiments on (i) the effects of male body size on spermatophore transfer in singly mating females and (ii) the effects of mate sequence (switching the order of standard-sized and small males) on mating behavior and paternity success in doubly mating females. In P. persimilis but not N. californicus, small males transferred fewer but larger spermatophores to the females; in both species, females re-mated more likely with standard-sized following small than small following standard-sized males; in P. persimilis, first standard-sized males sired a higher proportion of offspring produced after re-mating by the female than first small males, whereas in N. californicus the paternity success of small and standard-sized males was independent of the mating sequence. Based on our results and pertinent previous studies, which showed that females of P. persimilis, but not N. californicus, prefer mating with standard-sized over small males and allow them fertilizing more eggs, the lack of interspecific difference in female body size plasticity, and the absence of any clue pointing at a role of natural selection, we suggest that the interspecific difference in male body size plasticity is sexually selected. Our study provides an indication of sexual selection constraining plasticity of male phenotypes, suggesting that the level of polyandry may be an important co-determinant of the level of phenotypic plasticity of male body size.

Interference in early dual-task learning by predatory mites.

Animals are commonly exposed to multiple environmental stimuli, but whether, and under which circumstances, they can attend to multiple stimuli in multitask learning challenges is elusive. Here, we assessed whether simultaneously occurring chemosensory stimuli interfere with each other in a dual-task learning challenge. We exposed predatory mites Neoseiulus californicus early in life to either only conspecifics (kin) or simultaneously conspecifics (kin) and food (thrips or pollen), to determine whether presence of food interferes with social familiarization and, vice versa, whether presence of conspecifics interferes with learning the cues of thrips. We found that N. californicus can become familiar with kin early in life and use kin recognition later in life to avoid kin cannibalism. However, when the juvenile predators were challenged by multiple stimuli associated with two different learning tasks, that is, when they grew up with conspecifics in the presence of food, they were no longer capable of social familiarization. In contrast, the presence of conspecifics did not compromise the predators' ability to learn the cues of thrips. Memory of experience with thrips allowed shorter attack latencies on thrips and increased oviposition by adult N. californicus. Proximately, the stimuli for learning the features of thrips were apparently more salient than those for learning to recognize kin. We argue that, ultimately, learning the cues of thrips at the expense of impeded social familiarization pays off because of negligible cannibalism risk in the presence of abundant food. Our study suggests that stimulus-driven prioritization of learning tasks is in line with the predictions of selective and limited attention theories, and provides a key example of interference in dual-task learning by an arthropod.

Adaptive aggregation by spider mites under predation risk.

Grouping together is a commonly observed anti-predator strategy. Possible anti-predator benefits of aggregation include the encounter/avoidance effect for visually hunting predators and the dilution effect, together dubbed attack abatement. Possible costs opposing the dilution effect are easier detection of aggregated than scattered individuals. The benefits of attack abatement, and opposing costs after group detection, are poorly understood for chemosensory predator-prey interactions. We tackled this issue by assessing the aggregation behavior of spider mites Tetranychus urticae under predation risk emanating from predatory mites Phytoseiulus persimilis. We examined whether adult spider mite females aggregate more tightly when perceiving predator cues (traces left and eggs), representing graded risk levels, and whether grouping enhances survival in physical predator presence. The spider mites aggregated more tightly and were more active in presence than absence of predator cues. Grouped spider mites were less likely and later detected and attacked than scattered spider mites. Moreover, encounter and attack of one group member did not increase the risk of other members to be attacked, as compared to scattered spider mites. To the best of our knowledge, our study is the first rigorous documentation of the adaptive benefit of tightened prey aggregation towards a purely chemosensorily hunting predator.