Functionally different predators break down antipredator defenses of spider mites

Prey that lives with functionally different predators may experience enhanced mortality risk, because of conflicts between the specific defenses against their predators. Because natural communities usually contain combinations of prey and functionally different predators, examining risk enhancement with multiple predators may help to understand prey population dynamics. It is also important in an applied context: risk enhancement with multiple biological control agents could lead to successful suppression of pests. We examined whether risk enhancement occurs in the spider mite Tetranychus kanzawai Kishida (Acari: Tetranychidae) when exposed to two predator species: a generalist ant, Pristomyrmex punctatus Mayr (Hymenoptera: Formicidae), and a specialist predatory mite, Neoseiulus womersleyi Schicha (Acari: Phytoseiidae). We replicated microcosms that consisted of spider mites, ants, and predatory mites. Spider mites avoided generalist ants by staying inside their webs on leaf surfaces. In contrast, spider mites avoided specialist predatory mites that intruded into their webs by exiting the web, which obviously conflicts with the defense against ants. In the presence of both predators, enhanced mortality of spider mites was observed. A conflict occurred between the spider mites’ defenses: they seemed to move out of their webs and be preyed upon by ants. This is the first study to suggest that risk enhancement occurs in web‐spinning spider mites that are exposed to both generalist and specialist predator species, and to provide evidence that ants can have remarkable synergistic effects on the biological control of spider mites using specialist predatory mites.     

Spatial distribution of predators and prey affect biological control of twospotted spider mites by Phytoseiulus persimilis in greenhouses

We evaluated the effects of predator release pattern and prey distribution on rate of suppression of the twospotted spider mite, Tetranychus urticae Koch (Acari, Tetranychidae) and visual damage to the ornamental plant, Impatiens wallerana Hook.f., in a greenhouse. Sixteen impatiens plants were arranged in a square and infested with the same total number of spider mites distributed either evenly (equal numbers on all plants) or clumped (divided equally among the 4 central plants), simulating a “hot spot.” The predatory mite, Phytoseiulus persimilis Athias-Henriot, was released at a 1:4 predator:prey ratio based on total spider mites in the experimental unit, but the pattern of release was either even or clumped, which simulated broadcast or point-release strategies, respectively. Nine days after predator release, spider mite populations were reduced in all treatments, but only in the clumped pest-clumped predator treatment were spider mites undetectable. Poorest pest suppression occurred in the clumped spider mite-even predator treatment. Eighteen days after predator release, spider mites were eliminated in all treatments, but a reduction in average plant damage occurred only in treatments in which the predator release pattern matched the spider mite distribution (i.e., even-even or clumped-clumped) with the greatest reduction in the even-even treatment. Results suggest that there is an advantage to releasing predators in “hot spots” provided that the recommended predator:prey ratio is maintained within infested patches. If more uniform predator releases are planned, overall predator numbers need to be kept sufficiently high so that the predator:prey ratio of 1:4 shown to prevent damage on impatiens is achieved in higher-density spider mite patches.     

Acaricides impair prey location in a predatory phytoseiid mite

The use of predatory mites as the sole management tactic in biological control programmes frequently does not fully and reliably prevents damage of phytophagous mites on plants. Therefore, as an alternative, the integration of predatory mites with acaricides can provide more effective control of phytophagous mites than that of the predators only. However, for such integration, acaricides minimal negative impacts on predatory mites are required. In this study, we evaluated the sublethal effects of three acaricides on the foraging behaviour of Neoseiulus baraki (Athias‐Henriot) (Acari: Phytoseiidae) in a coconut production system. The acaricides were assessed for interference with the location of prey habitat using a Y‐tube olfactometer and for interference with the location of the prey colony within the habitat using a video‐tracking system. In addition to the choice of odour source, the time required and the distance walked to make the choice were assessed. The acaricides tested were abamectin, azadirachtin and fenpyroximate. The predatory mite preferred coconuts infested with the coconut mite Aceria guerreronis Keifer (Acari: Eriophyidae) over uninfested coconuts when not exposed to acaricides. However, when exposed to acaricides, the predator did not distinguish between infested and uninfested fruits. When exposed to abamectin, N. baraki spent more time resting and walked greater distances before making the choice of an odour source. Thus, the acaricides impair the ability of the predatory mite N. baraki to locate a prey habitat and to locate a prey within that habitat. The acaricides differentially affected prey foraging by interfering with odour perception.     

Disentangling mite predator‐prey relationships by multiplex PCR

Gut content analysis using molecular techniques can help elucidate predator‐prey relationships in situations in which other methodologies are not feasible, such as in the case of trophic interactions between minute species such as mites. We designed species‐specific primers for a mite community occurring in Spanish citrus orchards comprising two herbivores, the Tetranychidae Tetranychus urticae and Panonychus citri, and six predatory mites belonging to the Phytoseiidae family; these predatory mites are considered to be these herbivores’ main biological control agents. These primers were successfully multiplexed in a single PCR to test the range of predators feeding on each of the two prey species. We estimated prey DNA detectability success over time (DS₅₀), which depended on the predator‐prey combination and ranged from 0.2 to 18 h. These values were further used to weight prey detection in field samples to disentangle the predatory role played by the most abundant predators (i.e. Euseius stipulatus and Phytoseiulus persimilis). The corrected predation value for E. stipulatus was significantly higher than for P. persimilis. However, because this 1.5‐fold difference was less than that observed regarding their sevenfold difference in abundance, we conclude that P. persimilis is the most effective predator in the system; it preyed on tetranychids almost five times more frequently than E. stipulatus did. The present results demonstrate that molecular tools are appropriate to unravel predator‐prey interactions in tiny species such as mites, which include important agricultural pests and their predators.     

Prey selectivity of Piona exigua,a planktonic water mite

Summary Females, males and nymphs of Piona exigua were observed during prey capture and ingestion. The encounter radius of the mite was very small, allowing the escape of some crustaceans, such as the calanoid copepod Boeckella. Cladocerans, such as Bosmina or Chydorus, with little or no pre-contact escape response were the most vulnerable to mite predation. Preference values in size-selection experiments varied widely between individual mites. Adult mites presented with two sizes of Daphnia carinata generally preferred the smaller prey. When four sizes were presented simultaneously, however, the preferences of female mites for each size were not significantly different. Patterns of prey selection varied with predator age and sex; for example, female mites preferred Daphnia to Simocephalus, Ceriodaphnia and Chydorus, while nymphs showed a strong preference for Chydorus over Ceriodaphnia. When two prey types were present in equal proportions, differences in total prey density (range 5 or 10/1 – 30 or 50/1) did not alter preferences between the prey species. The preference of female mites for a particular prey type generally increased with increasing relative abundance of the prey type in each of three experiments (Daphnia: Ceriodaphnia, Ceriodaphnia: Chydorus, and Daphnia: Simocephalus). These results imply switching behaviour in these mites. Our results indicate the value of direct observation of predatory behaviour as an adjunct to prey selection experiments. It is also apparent that predatory behaviour in the presence of more than one prey type may not be predictable from that observed in single-prey situations. Predation rates on particular prey species were sometimes reduced in the presence of another species. The relative proportions of prey eaten when two species were present could not be predicted from the number of each species eaten when they were presented separately.     

A rapid technique for analysing diets of invertebrate predators by electrophoresis

A technique has been developed for the rapid determination of some species of prey consumed by mites and insects. The method detects prey enzymes within the gut of a predator by polyacrylamide gradient gel electrophoresis and subsequent staining for esterase activity. It is sufficiently sensitive to detect fruit tree red spider mite (Panonychus ulmi) esterases within the gut of a single predacious mite (Typhlodromus pyri) for at least 31 h after feeding. The method has been used to demonstrate feeding relationships among a range of insect and mite predator and prey species in the laboratory and in the field.     

Biological Control of the Bulb Mite, Rhizoglyphus robini , by the Predatory Mite, Hypoaspis aculeifer , on Lilies: Predator-Prey Dynamics in the Soil, under Greenhouse and Field Conditions

We tested the capacity of the soil-dwelling predatory mite, Hypoapsis aculeifer , to control mites attacking lily bulbs. Experiments in the greenhouse and in the field showed that in the absence of predatory mites populations of the bulb mite, Rhizoglyphus robini , on lily bulbs increased, whereas the release of predatory mites either slowed down the increase - as observed in the field - or caused the bulb mites populations to decrease - as observed in the greenhouse. In all cases the population of predatory mites increased as long as bulb mite densities were not too low. However, within the first week after predator release there was usually a sharp decline to 10-40% of the original number released. Greenhouse experiments on intact lily bulbs in pots, boxes and 1 m 2 plots with peat soil showed that when released in a ratio of 1 predator to 2 or 5 prey, the predatory mite, Hypoaspis aculeifer , suppressed populations of bulb mites to less than 10 individual per bulb within 6 weeks. Elimination of bulb mites was observed only when the predator-to-prey ratio at release was equal to 3:1. Field experiments in 2 m 2 plots with intact bulbs in rather compact sandy soil showed that when released in ratio of 1 predator to 1 or 2 prey, the predatory mite, H. aculeifer , did not cause the population of bulb mites to decrease, but it did reduce their population growth. The initial predator-to-prey ratios required to achieve suppression (ca 1:2) or elimination (3:1) in the soil environment are much higher than those required for bulb mite elimination when lily bulb scales were embedded in a medium of vermiculite (ca 1:20). Among the possible causes are: (1) the initial losses of predators in the greenhouse and even more so in the field due to mortality and/or emigration from the experimental plots; (2) the lower temperatures in the greenhouse and especially in the field, which slow down the growth and predation processes and thereby delay prey extinction; and (3) the spatial complexity of the soil environment which creates refuges for the bulb mites.     

Do Larval Damselflies make Adaptive Choices When Exposed to Both Parasites and Predators?

The importance of multiple enemies from different trophic levels on investment in defence by prey has, with some exceptions, received little attention. Some defences may make the victim more susceptible to other enemies; this latter situation applies to predators and parasites of larval damselflies. Baker and Smith [Oecologia 109 (1997) 622) showed that larval damselflies were as active in the presence of both mites and fish as they were when only mites were present, an apparently maladaptive behaviour that results in higher fish predation. In this paper, we further examine this maladaptive behavioural response to multiple enemies (fish predators and mite parasites) and test whether their defence responses are a result of the order in which they experience the parasite or predator, and/or if behavioural ‘personalities’ exist, such that some individuals show anti‐predator behaviours and other show anti‐parasite behaviours. Order of experience did not affect the four main behaviours (groom, crawl, turn and swim) exhibited when larval damselflies were simultaneously exposed to fish and mites. Grooming levels increased in response to mites, decreased in response to fish and when exposed to both mites and fish were similar to when they were exposed to mites alone. Duration of the other three behaviours was lower in the presence of both mites and fish. The crawling ‘personalities’ were evident. The apparently maladaptive response of high grooming levels in the presence of mites and fish is not a result of order of experience or ‘personalities’. It may be a result of relatively high encounter rates with mite parasites, compared with the encounter rates with fish. Lower encounter rates can result in diminishing investment in defence against an enemy.     

Behavioural responses of larval container mosquitoes to a size-selective predator

Abstract.  1. The hypothesis that size-selective predation and species-specific prey behaviours facilitate the coexistence between larvae of invasive Aedes albopictus (Skuse) and U.S.A.-native Ochlerotatus triseriatus (Say) was tested experimentally with the predator Corethrella appendiculata (Grabham).
2. Larval behaviours associated with a higher risk of predation were identified, and prey behavioural responses were tested in either the physical presence of predators or in water containing predation cues. Larvae that thrashed on container bottoms had a higher risk of being captured by fourth instar C. appendiculata than did larvae resting on the water surface. Ochlerotatus triseriatus , but not A. albopictus , adopted low-risk behaviours in response to water-borne cues to predation. Both prey species reduced risky behaviours in the physical presence of the predator, but O. triseriatus showed a stronger response.
3. The vulnerability of 2nd and 3rd instar prey to predation was compared, and behavioural responses were correlated with prey vulnerability. Second instars of both species were more vulnerable to predation by C. appendiculata than were 3rd instars, and the 3rd instar A. albopictus was more vulnerable than O. triseriatus of the same stage. All instars of O. triseriatus showed a similar reduction of risky behaviours in response to the presence of C. appendiculata despite 4th instar prey being relatively invulnerable to size-selective predation.
4. Weaker predator avoidance, coupled with superior competitive ability, of invasive A. albopictus is likely to contribute to its coexistence with O. triseriatus in containers of the south-eastern U.S.A., where C. appendiculata can be abundant.     

The effects of turbidity and an invasive species on foraging success of rosyside dace (Clinostomus funduloides)

1.  Habitat degradation and biological invasions are important threats to fish diversity worldwide. We experimentally examined the effects of turbidity, velocity and intra- and interspecific competition on prey capture location, reactive distance and prey capture success of native rosyside dace ( Clinostomus funduloides ) and invasive yellowfin shiners ( Notropis lutipinnis ) in Coweeta Creek, North Carolina, U.S.A.
2.  Increased turbidity and velocity produced significant decreases in the number of prey captured forward of the fish's location. It is possible that this represents an increase in the amount of energy expended per prey captured.
3.  We used Akaike's Information Criterion (AIC) to evaluate competing explanatory models for reactive distance (10 generalised linear models, GLM) and prey capture success (9 generalised linear mixed models, GLMM).
4.  Reactive distance decreased by 12% with an increase from 2 to 4 conspecifics, whereas a 10 NTU increase in turbidity reduced reactive distance by 9%. Capture success was affected by velocity, dominance and competition, and varied among species. A 6 cm s⁻¹ increase in velocity produced a 28% decline in capture probability; however, dominant fish were 3.2 times more likely to capture a prey item than non-dominant fish. Yellowfin shiners only were 0.62 times as likely to capture a prey item as rosyside dace. Both intra- and interspecific competition reduced capture probability, and fish in high density intraspecific or interspecific trials were 0.46 times and 0.44 times as likely to capture prey, respectively, as fish in two fish intraspecific trials.
5.  These results suggest behavioural variables are as important as physical factors in determining reactive distance and capture probability by these minnows.     

Stigmaeid-phytoseiid interactions and the impact of natural enemy complexes on plant-inhabiting mites

Interactions within the natural enemy complex of plant-inhabiting mites are of practical interest. There are frequently several predatory mite species present or available for introduction and it is difficult to tell whether a single species or combination of species should provide the most effective means of biological control. We used a simulation model to examine the interactions between predatory mites of two families, the Stigmaeidae and Phytoseiidae, representatives of which feed on phytophagous apple mites. To identify key differences in predatory behavior and life history, various stigmaeid parameters were substituted with those of phytoseiids, and changes in the efficacy of either stigmaeids alone or in combination with phytoseiids were evaluated graphically. At low prey densities stigmaeids held an advantage over phytoseiids in terms of efficacy because of their higher preference for prey eggs, higher oviposition relative to prey consumption and the ability to consume their own eggs, while at high prey densities the higher maximum predation rate of phytoseiids gave them a higher efficacy. Thus the weaker predator (the stigmaeid) is the more effective competitor at low prey densities. The model did not account for dispersal, but since stigmaeids are the weaker dispersers, the possibility of developing stability in this system is much greater than if phytoseiids were the better competitors. A combination of stigmaeids and phytoseiids was shown to have greater efficacy than either predator alone over a wide range of prey densities.     

Intraguild Interactions Between the Predatory Mites Neoseiulus californicus and Phytoseiulus persimilis

Species at the same trophic level may interact through competition for food, but can also interact through intraguild predation. Intraguild predation is widespread at the second and third trophic level and the effects may cascade down to the plant level. The effects of intraguild predation can be modified by antipredator behaviour in the intraguild prey. We studied intraguild predation and antipredator behaviour in two species of predatory mite, Neoseiulus californicus and Phytoseiulus persimilis, which are both used for control of the two-spotted spider mite in greenhouse and outdoor crops. Using a Y-tube olfactometer, we assessed in particular whether each of the two predators avoids odours emanating from prey patches occupied by the heterospecific predator. Furthermore, we measured the occurrence and rate of intraguild predation of different developmental stages of P. persimilis and N. californicus on bean leaves in absence or in presence of the shared prey. Neither of the two predator species avoided prey patches with the heterospecific competitor, both when inexperienced with the other predator and when experienced with prey patches occupied by the heterospecific predator. Intraguild experiments showed that N. californicus is a potential intraguild predator of P. persimilis. However, P. persimilis did not suffer much from intraguild predation as long as the shared prey was present. This is probably because N. californicus prefers to feed on two-spotted spider mites rather than on its intraguild prey.     

Diet‐dependent intraguild predation between the predatory mites Neoseiulus californicus and Neoseiulus cucumeris

Based on the hypothesis that matching diets of intraguild (IG) predator and prey indicate strong food competition and thus intensify intraguild predation (IGP) as compared to non‐matching diets, we scrutinized diet‐dependent mutual IGP between the predatory mites Neoseiulus cucumeris and N. californicus. Both are natural enemies of herbivorous mites and insects and used in biological control of spider mites and thrips in various agricultural crops. Both are generalist predators that may also feed on plant‐derived substances such as pollen. Irrespective of diet (pollen or spider mites), N. cucumeris females had higher predation and oviposition rates and shorter attack latencies on IG prey than N. californicus. Predation rates on larvae were unaffected by diet but larvae from pollen‐fed mothers were a more profitable prey than those from spider‐mite fed mothers resulting in higher oviposition rates of IG predator females. Pollen‐fed protonymphs were earlier attacked by IG predator females than spider‐mite fed protonymphs. Spider mite‐fed N. californicus females attacked protonymphs earlier than did pollen‐fed N. californicus females. Overall, our study suggests that predator and prey diet may exert subtle influences on mutual IGP between bio‐control agents. Matching diets did not intensify IGP between N. californicus and N. cucumeris but predator and prey diets proximately influenced IGP through changes in behaviour and/or stoichiometry.     

Prey preference,intraguild predation and population dynamics of an arthropod food web on plants

The theory of intraguild predation (IGP) largely studies effects on equilibrium densities of predators and prey, while experiments mostly concern transient dynamics. We studied the effects of an intraguild (IG) predator, the bug Orius laevigatus, on the population dynamics of IG-prey, the predatory mite Phytoseiulus persimilis, and a shared prey, the phytophagous two-spotted spider mite Tetranychus urticae, as well as on the performance of cucumber plants in a greenhouse. The interaction of the predatory mite and the spider mite is highly unstable, and ends either by herbivores overexploiting the plant or predators exterminating the herbivores. We studied the effect of IGP on the transient dynamics of this system, and compared the dynamics with that predicted by a simple population-dynamical model with IGP added. Behavioural studies showed that the predatory bug and the predatory mite were both attracted to plants infested by spider mites and that the two predators did not avoid plants occupied by the other predator. Observations on foraging behaviour of the predatory bug showed that it attacks and kills large numbers of predatory mites and spider mites. The model predicts strong effects of predation and prey preference by the predatory bugs on the dynamics of predatory mites and spider mites. However, experiments in which the predatory bug was added to populations of predatory mites and spider mites had little or no effect on numbers of both mite species, and cucumber plant and fruit weight.     

The Effects of Timing and Rates of Release of Phytoseiulus persimilis against Two-spotted Spider Mite Tetranychus urticae on Dwarf Hops

Single inoculative releases of the phytoseiid mite Phytoseiulus persimilis were made against the two-spotted spider mite, Tetranychus urticae, on two varieties of dwarf hops in 1996 and 1997 at means of 20, 10, 5, 2.5 and nil per plant, and at up to three timings. The numbers of spider mites recorded on leaves after the predators were released were related inversely to the rates of release. The earliest releases of the predator maintained spider mites at lower population densities than did those made later in the year. In all treatments the numbers of spider mites decreased when the prey:predator ratio reached approximately 10:1.     

Potential of the predatory mite Phytoseius finitimus (Acari: Phytoseiidae) to feed and reproduce on greenhouse pests

Phytoseiid mites of the genus Phytoseius are natural enemies of tetranychid and eriophyid herbivorous mites mostly found on hairy plants where they feed on prey, as well as on pollen. Nevertheless, the nutritional ecology and the role of these predators in biological pest control are only rarely addressed. In the present study, we evaluated the potential of Phytoseius finitimus to feed and reproduce on three major greenhouse pests, the two-spotted spider mite, the greenhouse whitefly and the western flower thrips. Additionally, we estimated the effect of cattail pollen when provided to the predator alone or in mixed diets with prey. Contrary to thrips larvae, both spider mite larvae and whitefly crawlers sustained the development of P. finitimus. In addition, females consumed more spider mite eggs and larvae, as well as whitefly crawlers than thrips larvae, but laid eggs when feeding on all prey. When provided alone, cattail pollen sustained the development and reproduction of the predator. The addition of pollen in mixed diets with prey reduced prey consumption, though it increased the predator’s egg production. We discuss the implications of our findings for biological pest control.     

Predatory role of Neoseiulus fallacis (Acari: Phytoseiidae): spatial and temporal dynamics in Washington red raspberry fields

The seasonal abundance of spider mites and their predator Neoseiulus fallacis (Garman) (Acari: Phytoseiidae) was determined during three consecutive years in Washington State red raspberry fields. Tetranychus urticae Koch (Acari: Tetranychidae), Eotetranychus carpini borealis (Ewing) (Acari: Tetranychidae), and N. fallacis were commonly found in Skagit and Whatcom Counties. E. carpini borealis colonized the fruiting canes earlier in the season than T. urticae. The two phytophages overlapped in midseason, but T. urticae entered diapause earlier than E. carpini borealis and N. fallacis. Densities of N. fallacis increased with increase in spider mite densities. However, the numerical response of the predator was more evident for T. urticae than for E. carpini borealis. Nevertheless, the predator was spatially associated with the two prey species. The spatial and seasonal distribution of N. fallacis in relationship to host plant phenology and prey distribution may influence the effectiveness of this predator as a biological control agent against spider mites in red raspberry. Densities of the predator increased too late to prevent spider mite damage. The predatory role of N. fallacis could be enhanced by introducing or conserving predators that are more tolerant to climatic factors that prevail in and around the cane canopy in the beginning of the season.     

Satiation and the functional response: a test of a new model

Abstract. 1. A model of the functional response to prey density is derived to include the reduction in time available for search, T_s , resulting from predator satiation.
2. For larger prey items predator satiation occurs at each prey capture and T_s is reduced by the attack time and digestive pause of a series of attack cycles. For small prey items predator foraging is continuous at low densities with T_s reduced solely by attack time. At higher densities predator satiation occurs after the capture of several small prey items and T_s is reduced by the attack time and digestive pause of a series of foraging cycles.
3. A comparison of the predicted asymptotic level of prey capture using experimentally estimated parameter values, with the maximum consumption of aphids by larval and adult coccinellids provides a test of the satiation model.
4. The limitation of prey capture by predator satiation is discussed with reference to handling time and the success of coccinellids in biological control.     

Predatory mites avoid ovipositing near counterattacking prey

Attacking prey is not without risk; predators may endure counterattackby the prey. Here, we study the oviposition behaviour of a predatory mite(Iphiseius degenerans) in relation to its prey, thewesternflower thrips (Frankliniella occidentalis). This thrips iscapable of killing the eggs of the predator. Thrips and predatory mites - apartfrom feeding on each other - can also feed and reproduce on a diet of pollen.Because thrips may aggregate at pollen patches, such patches may be risky foroviposition by the predatory mites. We found that, in absence of thrips,predatory mites lay their eggs close to pollen, but further away when thripsarepresent. Predatory mite eggs near pollen were killed more frequently by thripsthan when they were deposited further away. The oviposition behaviour of thepredatory mite was also studied in absence of thrips, but in presence of thealarm pheromone of thrips. This pheromone is normally secreted upon contactwithpredators or competitors. When applied close to the pollen, predatory mitesoviposited significantly further away from it. When the alarm pheromone wasapplied away from the food source, most eggs were found near the pollen. Theseresults indicate that female predatory mites show flexible ovipositionbehaviourin response to the presence of their counterattacking prey.     

The evolution of rates of successful and unsuccessful predation

Summary The question, how will evolutionary change in a predator or in its prey change the ratio of the rate of successful captures to the rate of unsuccessful capture attempts is addressed. I argue that this ratio is not a good index of the predator's adaptation to prey capture, because decreased costs of capture attempts or increased assimilation efficiency (both favored by natural selection in the predator) will usually reduce the ratio. In addition, the evolution of increased ability to capture prey may lead to a reduction in the success/failure ratio. Analysis of several simple models suggests that this result is robust. The presence of unsuccessful predation does have an important influence on the evolution of predator traits that increase its rate of encounter with the prey; the presence of unsuccessful predation may cause the predator to increase its adaptations for prey detection in response to an increase in the prey's ability to avoid detection.