Patterns, mechanisms and spatial scale of aggregation in generalist and specialist predatory mites (Acari: Phytoseiidae)

Prey species often distribute themselves patchily in their habitats. In response to this spatial variation in prey density, some predator species aggregate in patches of higher prey density. This paper reviews a series of laboratory experiments to demonstrate the patterns of responses by phytoseiid predators (Phytoseiulus persimilis, Typhlodromus occidentalis and Amblyseius andersoni) to spatial variation in the density of their spider mite prey (Tetranychus urticae) and reveal the behavioural mechanisms underlying the observed patterns. In addition, patterns of aggregation were examined at a variety of spatial scales on plants in greenhouses. The patterns, mechanisms and spatial scale of aggregation in three predatory species are discussed in relation to their varying degrees of polyphagy. The results show that a specialist predator species (1) aggregates more strongly than generalist predators, (2) does so not because it finds prey patches of high density more easily but because it remains in these patches longer than generalist predators and (3) tends to aggregate more often at lower levels of spatial scale than generalist predators. It is suggested that these conclusions, based mainly on laboratory studies of a small sample of species, should be tested in the future on a wider selection of specialist and generalist species at different scales in the field. This revised version was published online in November 2006 with corrections to the Cover Date.     

Opportunistic predator prefers habitat complexity that exposes prey while reducing cannibalism and intraguild encounters

Structural features of habitat are known to affect the density of predators and prey, and it is generally accepted that complexity provides some protection from the environment and predators but may also reduce foraging success. A next step in understanding these interactions is to decouple the impacts of both spatial and trophic ingredients of complexity to explicitly explore the trade-offs between the habitat, its effects on foraging success, and the competition that ensues as predator densities increase. We quantified the accumulation of spiders and their prey in habitat islands with different habitat complexities created in the field using natural plants, plant debris and plastic plant mimics. Spiders were observed at higher densities in the complex habitat structure composed of both live plants and thatch. However, the numerically dominant predator in the system, the wolf spider Pardosa milvina, was observed at high densities in habitat islands containing plastic mimics of plants and thatch. In a laboratory experiment, we examined the interactive effects of conspecific density and habitat on the prey capture of P. milvina. Thatch, with or without vertical plant structure, reduced prey capture, but the plastic fiber did not. Pairwise interactions among spiders reduced prey capture, but this effect was moderated by thatch. Taken together, these experiments highlight the flexibility of one important predator in the food web, where multiple environmental cues intersect to explain the role of habitat complexity in determining generalist predator accumulation.     

Subsidy from the detrital food web, but not microhabitat complexity, affects the role of generalist predators in an aboveground herbivore food web

The activity and density of generalist predators, such as carabid beetles, rove beetles and spiders, may increase in response to: (1) increased availability of prey from the belowground subsystem and/or (2) enhanced complexity of aboveground vegetation. Organic farming practices support decomposer populations and enhance habitat complexity due to an increased weed density. A response by generalist predators to such below‐ or aboveground changes could affect predation rates on herbivores in the aboveground food web. We tested this hypothesis in a replicated field experiment conducted in a winter wheat field, where increased predator activity could lead to improved control of herbivorous pests. In a crossed design, we increased and lowered densities of decomposer prey, and manipulated vegetation complexity using artificial plants in order to examine the effect of structural complexity in isolation from effects of plant‐attracted additional prey. Isotomid Collembola exhibited lowest activity‐densities (AD) in plots treated with soil insecticide and had gradually increasing AD in untreated plots and plots receiving detrital subsidies. Carabid beetles and cursorial spiders did not respond to increased availability of isotomid prey, and they unexpectedly displayed higher AD in the structurally less‐complex plots. Aphid density mirrored the positive response of isotomids to detrital subsidies, suggesting that aphids benefited from reduced predation due to predators switching to abundant prey in the decomposer subsystem. The absence of a numerical response by surface‐active predators apparently strengthened this indirect effect of isotomids on aphids. Our results suggest that indirect predator‐mediated prey‐prey interactions can reduce beneficial effects of detrital subsidies on pest suppression. We further demonstrated that generalist predators may not per se benefit from structural complexity. Both results document the challenges associated with management practices that support generalist predators, as these measures may not necessarily improve herbivore suppression.     

Cascading effects of belowground predators on plant communities are density‐dependent

Soil food webs comprise a multitude of trophic interactions that can affect the composition and productivity of plant communities. Belowground predators feeding on microbial grazers like Collembola could decelerate nutrient mineralization by reducing microbial turnover in the soil, which in turn could negatively influence plant growth. However, empirical evidences for the ecological significance of belowground predators on nutrient cycling and plant communities are scarce. Here, we manipulated predator density (Hypoaspis aculeifer: predatory mite) with equal densities of three Collembola species as a prey in four functionally dissimilar plant communities in experimental microcosms: grass monoculture (Poa pratensis), herb monoculture (Rumex acetosa), legume monoculture (Trifolium pratense), and all three species as a mixed plant community. Density manipulation of predators allowed us to test for density‐mediated effects of belowground predators on Collembola and lower trophic groups. We hypothesized that predator density will reduce Collembola population causing a decrease in nutrient mineralization and hence detrimentally affect plant growth. First, we found a density‐dependent population change in predators, that is, an increase in low‐density treatments, but a decrease in high‐density treatments. Second, prey suppression was lower at high predator density, which caused a shift in the soil microbial community by increasing the fungal: bacterial biomass ratio, and an increase of nitrification rates, particularly in legume monocultures. Despite the increase in nutrient mineralization, legume monocultures performed worse at high predator density. Further, individual grass shoot biomass decreased in monocultures, while it increased in mixed plant communities with increasing predator density, which coincided with elevated soil N uptake by grasses. As a consequence, high predator density significantly increased plant complementarity effects indicating a decrease in interspecific plant competition. These results highlight that belowground predators can relax interspecific plant competition by increasing nutrient mineralization through their density‐dependent cascading effects on detritivore and soil microbial communities.     

Sex-specific developmental plasticity of generalist and specialist predatory mites (Acari: Phytoseiidae) in response to food stress

We studied developmental plasticity under food stress in three female-biased size dimorphic predatory mite species, Phytoseiulus persimilis, Neoseiulus californicus, and Amblyseius andersoni. All three species prey on two-spotted spider mites but differ in the degree of adaptation to this prey. Phytoseiulus persimilis is a specialized spider mite predator, N. californicus is a generalist with a preference for spider mites, and A. andersoni is a broad generalist. Immature predators were offered prey patches of varying density and their survival chances, dispersal tendencies, age and size at maturity measured. Amblyseius andersoni dispersed earlier from and had lower survival chances in low density prey patches than N. californicus and P. persimilis. Age at maturity was not affected by prey density in the generalist A. andersoni, whereas both the specialist P. persimilis and the generalist N. californicus accelerated development at low prey densities. Species-specific plasticity in age at maturity reflects opposite survival strategies when confronted with limited prey: to prematurely leave and search for other food (A. andersoni) or to stay and accelerate development (P. persimilis, N. californicus). In all species, size at maturity was more plastic in females than males, indicating that males incur higher fitness costs from deviations from optimal body size.     

Density‐dependent and ‐independent effects on the joint use of space by predators and prey in terrestrial arthropod food‐webs

The spatial distribution of predators and their prey is affected by their joint use of space. While the formation of such spatial patterns may be driven by density‐dependent and ‐independent factors our knowledge on the contribution of different land‐use activities on the formation of spatial patterns between predators and prey remains very limited. Agriculture is one of the most prevailing land‐use activities with strong effects on invertebrate densities and structural habitat conditions. Here, we used replicated conventionally and organically managed winter wheat fields to investigate the effects of agricultural land‐use on the spatial patterns of generalist predators and decomposer prey. We then identified the explanatory power of density‐dependent (prey and predator activity density) and density‐independent (vegetation structure) predictors for the observed spatial patterns. Generalist predators were regularly distributed only in conventionally managed fields and this pattern intensified with decreasing Collembola prey availability and increasing spider activity density. Segregation between carabid and spider predators was strongest in fields with lowest wheat plant height, suggesting more intense intraguild interactions in structurally less complex habitats. Collembola were aggregated independent of management and aggregation was strongest in fields with highest Collembola and carabid activity density. Spiders and Collembola prey were associated, but higher aphid densities under conventional management weakened or interrupted this spatial relationship. We conclude that active control of crop plant physiognomy by growth hormones and herbicides in conventionally managed fields promotes predator–predator segregation and that a high availability of aphid prey seems to decouple predator–Collembola prey associations. Our results emphasise the need for a more mechanistic understanding of the effects of land‐use on the formation of spatial patterns and species interactions, especially under scenarios of environmental change and an ongoing loss of biodiversity.     

Adjacent trophic-level effects on spatial density dependence in a herbivore—predator—parasitoid system

Abstract. 1. Spatial density dependence of enemy/victim relationships (predator/prey and host/parasitoid) were examined for the gall-making herbivore Eurosta solidaginis (Diptera: Tephritidae), its predator Mordellistena unicolor (Coleoptera: Mordellidae), and a parasitoid of Mordellistena, Schizoprymnus sp. (Hymenoptera: Braconidae), both before and after experimental perturbation of gall density.
2. Mordellistena predation did not depend on Eurosta density, nor did Schizoprymnus parasitism of Mordellistena depend on Mordellistena density.
3. Schizoprymnus parasitism of Mordellistena depended strongly on the density of Eurosta , the prey of its host.
4. The lack of density dependence in enemy/victim relationships may be explained by effects from adjacent trophic-levels. Ovipositing Schizoprymnus may search for high densities, not of its host Mordellistena , but of its host's prey ( Eurosta galls), and ovipositing Mordellistena may avoid patches of high gall density where the risk of being parasitized is greater.     

Temporal relationships between the generalist predator,Orius insidiosus,and its two major prey in soybean

The generalist predator, Orius insidiosus (Say) is an important early-season predator of the soybean aphid, Aphis glycines Matsumura, a newly invasive pest of major concern in soybean crop management. We conducted a 3 year, multiple field study to characterize the dynamic relationships between the predator, the pest, and alternative prey in soybean. Using field sampling data, we showed that thrips were the only alternative prey to be well-established in fields prior to O. insidiosus arrival and were likely to promote predator colonization of soybean fields prior to the arrival of soybean aphid. The predator displayed a reproductive numerical response to thrips in one of the 3 years and a primarily aggregative response in another year. The predator did not respond numerically to soybean aphid in the majority of fields. Experimental manipulations of thrips populations in field plots temporarily reduced thrips densities but had a minimal effect on O. insidiosus densities, suggesting that the predator is resilient against temporary reductions in a major resource. In the 2 years O. insidiosus populations were well-established in fields prior to soybean aphid arrival, soybean aphid remained at low levels throughout the season. In the year soybean aphid arrived early with respect to the growing season and before O. insidiosus populations were established, soybean aphid reached outbreak levels in all fields. Future research efforts on the factors determining soybean aphid population dynamics need to address the relative importance of early-season soybean aphid colonization and generalist predator population dynamics on the potential for soybean aphid population outbreaks.     

Patch residence time and patch preference of the predatory mite <Emphasis Type="Italic">Amblyseius swirskii</Emphasis> in relation to prey diversity

Patch-related behaviour of a generalist predator may be influenced by patch prey diversity and result in more time being spent in patches with more than one prey species to increase the benefits of mixed diet. To examine if generalist predators are able to discern differences in prey diversity in and among patches, we examined the patch-related behaviour of the predatory mite Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae). Three lab experiments using clean, single-prey or mixed-prey patches were conducted, using whiteflies and spider mites as prey. The experiments were: (1) patch leaving tendency and residence time in absence and (2) presence of another patch, (3) patch preference. A. swirskii recognized prey-inhabited patches from a distance and showed a preference for mixed-prey patches over single-prey patches. The patch-related behaviour of A. swirskii, which seems tuned to exploiting the fitness gains of a mixed diet, is influenced by both local and distant cues.     

Predation of the cereal aphid Sitobion avenae by polyphagous predators on the ground

Abstract. 1. Polyphagous predator densities were manipulated in a wheat crop using polythene exclusion barriers.
2. The rates at which aphids fell to the ground and subsequently climbed and returned to the crop canopy were measured.
3. Peak aphid density was highest when polyphagous predator density was lowest.
4. Similar rates of aphid fall-off were measured in each plot, but aphid climbing rate was highest when predator densities were lowest.
5. It was concluded that ground-zone predators reduced the rate at which aphids return to the crop canopy.     

Herbivore response to vegetational diversity: spatial interaction of resources and natural enemies

Vegetational diversity in agricultural systems is predicted to reduce herbivore populations, but we observed the opposite effect: higher nymph population densities of a functionally monophagous herbivore, the squash bug, Anasa tristis (Hemiptera: Coreidae) in a vegetationally diverse squash-bean-corn polyculture than in a squash monoculture. We examined spatial and temporal aspects of squash bug and predator populations in relation to vegetational diversity. Average colonization, oviposition, and mortality rates for the herbivore were similar in monocultures and polycultures. In the polyculture, however, we found that squash bugs eggs were highly aggregated on plants on the outer edges of plots. Predation was also lower on plants near the edges, allowing the large aggregations of eggs found in the polyculture to escape predation and ultimately produce more squash bugs. Spatial interactions between herbivores and natural enemies may underlie some of the general effects of vegetational diversity on herbivores.     

Monoclonal antibodies reveal changes in predator efficiency with prey spatial pattern

Spatially explicit predator–prey interactions can alter the predatory potential of natural enemies augmented through conservation biological control. To test hypotheses regarding such interactions and predatory efficiency, we used a combination of molecular techniques and mark–release–recapture to study the foraging behaviour of a generalist carabid predator, Poecilus cupreus , in response to spatial patterns of its cereal aphid prey ( Metapolophium dirhodum and Sitobion avenae ). Beetle and aphid numbers were measured across two grids of sampling locations, within which aphid spatial pattern had been manipulated to generate patchy and more homogenous distributions. Aphid consumption was measured by enzyme-linked immunosorbent assays (ELISA) of beetle gut contents, using an aphid-specific monoclonal antibody. Movement and distribution patterns suggest that P. cupreus does not aggregate at, nor instigate prey-taxis within, aphid patches. However, more than two-thirds of the 2169 P. cupreus tested by ELISA had consumed aphids and the proportion of beetles containing aphid proteins was positively related to aphid density. Against expectation, the proportion of predators feeding on aphids was greatest where prey were homogenously distributed, and this was attributed to the loss of partial refuges for prey in aphid patches. The functional value of this type of uniform foraging strategy is ideally suited to early colonization of the crop habitat, when aphid numbers are low, before populations build up and form strong spatial patterns.     

Metapopulation dynamics for spatially extended predator–prey interactions

Traditional metapopulation theory classifies a metapopulation as a spatially homogeneous population that persists on neighboring habitat patches. The fate of each population on a habitat patch is a function of a balance between births and deaths via establishment of new populations through migration to neighboring patches. In this study, we expand upon traditional metapopulation models by incorporating spatial heterogeneity into a previously studied two-patch nonlinear ordinary differential equation metapopulation model, in which the growth of a general prey species is logistic and growth of a general predator species displays a Holling type II functional response. The model described in this work assumes that migration by generalist predator and prey populations between habitat patches occurs via a migratory corridor. Thus, persistence of species is a function of local population dynamics and migration between spatially heterogeneous habitat patches. Numerical results generated by our model demonstrate that population densities exhibit periodic plane-wave phenomena, which appear to be functions of differences in migration rates between generalist predator and prey populations. We compare results generated from our model to results generated by similar, but less ecologically realistic work, and to observed population dynamics in natural metapopulations.     

Spatial and temporal variation in the diet of a predaceous stonefly (Plecoptera: Perlodidae)

SUMMARY. 1. Spatial and temporal variation in the diet of the univoltine predatory stonefly, Kogotus nonus , was studied over 3 years in a small Alberta stream to determine whether the relative abundance of prey types in the diet of Kogotus reflected relative prey densities in the stream and whether the variation in absolute feeding rate was related to either prey or predator density.
2. The seasonal shift from sole utilization of Orthocladiinae to inclusion of Baetis in the diet could not be attributed to seasonal changes in prey density, but was probably related to predator size and ability to handle very active prey. Most of the spatial variation in diet could be related to differences in background prey densities, but very high densities of Baetis caused the predator to specialize on this prey.
3. Feeding rate on Baetis . as assessed by per capita gut contents, showed a seasonal shift from a positive correlation with Baetis density in winter to a negative relationship with predator density in spring. This suggested that feeding by small Kogotus is a function of prey density. while feeding by later instars is influenced by between predator interactions such as interference.     

The effect of prey species and environmental complexity on the functional response of Franklinothrips orizabensis: a test of the fractal foraging model

Abstract. 1. The hypothesis proposed by the fractal foraging model, that prey procurement by predators declines as habitat complexity increases, was tested. To evaluate this hypothesis, the effect of two prey species, second-instar larvae of Scirtothrips perseae Nakahara and Heliothrips haemorrhoidalis (Bouché) (both Thysanoptera: Thripidae), and environmental complexity on the functional response of the predatory thrips Franklinothrips orizabensis Johansen (Thysanoptera: Aeolothripidae) was examined.
2. The Koch curve, a well-studied fractal, was used to generate the shapes of experimental arenas to test the effect of environmental complexity on the functional response of F. orizabensis. Complexity was defined in terms of the number of acute vertices in which prey thrips could seek refuge and the length of the perimeter that had to be searched by the predator. Four shapes were tested: a circle (zero acute vertices, circumference = 186.61 mm), equilateral triangle (three acute vertices, perimeter = 240 mm), star (six acute vertices, perimeter = 277.13 mm), and snowflake (18 acute vertices, perimeter = 333.65 mm). All shapes were scaled so that the area of each arena was 2771 mm².
3.  Franklinothrips orizabensis exhibited a Type II functional response for both prey species and all four experimental arenas tested. Significantly fewer S. perseae larvae were killed in the most complex arena (i.e. the snowflake) when prey densities exceeded 16. For H. haemorrhoidalis , significant differences in mortality were observed only when prey densities equalled four. These results demonstrated that the fractal foraging model was supported when certain prey densities coincided with particular levels of environmental complexity.
4. Subtle changes in environmental complexity and different prey species of varying density can affect prey–predator interactions significantly.     

Control of aphids on wheat by generalist predators: effects of predator density and the presence of alternative prey

There is evidence for both positive and negative effects of generalist predators on pest populations and the various reasons for these contrasting observations are under debate. We studied the influence of a generalist predator, Pardosa lugubris (Walckenaer) (Araneae: Lycosidae), on an aphid pest species, Rhopalosiphum padi (L.) (Hemiptera: Aphididae; low food quality for the spider), and its host plant wheat, Triticum spec. (Poaceae). We focused on the role of spider density and the availability of alternative prey, Drosophila melanogaster Meigen (Diptera: Drosophilidae; high food quality). The presence of spiders significantly affected plant performance and aphid biomass. Alternative prey and spider density strongly interacted in affecting aphids and plants. High spider density significantly improved plant performance but also at low spider density plants benefited from spiders especially in the presence of alternative prey. The results suggest that generalist arthropod predators may successfully reduce plant damage by herbivores. However, their ability to control prey populations varies with predator nutrition, the control of low-quality prey being enhanced if alternative higher-quality prey is available.     

Effect of predator density dependent dispersal of prey on stability of a predator-prey system

This work presents a predator-prey Lotka-Volterra model in a two patch environment. The model is a set of four ordinary differential equations that govern the prey and predator population densities on each patch. Predators disperse with constant migration rates, while prey dispersal is predator density-dependent. When the predator density is large, the dispersal of prey is more likely to occur. We assume that prey and predator dispersal is faster than the local predator-prey interaction on each patch. Thus, we take advantage of two time scales in order to reduce the complete model to a system of two equations governing the total prey and predator densities. The stability analysis of the aggregated model shows that a unique strictly positive equilibrium exists. This equilibrium may be stable or unstable. A Hopf bifurcation may occur, leading the equilibrium to be a centre. If the two patches are similar, the predator density dependent dispersal of prey has a stabilizing effect on the predator-prey system.     

Life-history trade-off in two predator species sharing the same prey: a study on cassava-inhabiting mites

In cassava fields, two species of predatory mites, Typhlodromalus aripo and T. manihoti, co-occur at the plant level and feed on Mononychellus tanajoa , a herbivorous mite. The two predator species are spatially segregated within the plant: T. manihoti dwells on the middle leaves, while T. aripo occurs in the apices of the plant during the day and moves to the first leaves below the apex at night.
To monitor the prey densities experienced by the two predator species in their micro-environment, we assessed prey and predator populations in apices and on the leaves of cassava plants in the field. Prey densities peaked from November to January and reached the lowest levels in July. They were higher on leaves than in the apices. To test whether the life histories of the two predator species are tuned to the prey density they experience, we measured age-specific fecundity and survival of the two predators under three prey density regimes (1 prey female/72 h, 1 prey female/24 h and above the predators level of satiation). T. manihoti had a higher growth rate than T. aripo at high prey densities, mainly due to its higher fecundity. T. aripo had a higher growth rate at low prey density regimes, due to its late fecundity and survival. Thus, each of the two species perform better under the prey density that characterizes their micro-habitat within the plant.     

Deconstructing insect herbivore trivial movement in a monoculture and triculture: Limitations of emigration

Significantly higher population densities of a squash pest beetle, Acalymma vittatum, were observed in a squash monoculture than a triculture of squash, maize, and beans. One hypothesis for such differences is that non-host plants in the triculture cause the herbivore to move more frequently resulting in higher emigration rates from the tricultures. Plant to plant movement of the beetle was studied in vegetative winter squash to evaluate if differences in components of trivial movement would generate a higher emigration rate from the triculture. Tenure times were shorter on plants in the triculture than on plants in the squash monoculture, there was no movement directionality, movement distances were greater in squash monocultures than in tricultures and were greater during July than August. In the tricultures, plant-to-plant transitions were primarily to maize from non-host plants and to beans or squash from host plants during July, but during August, movement from any plant was primarily to maize. We integrated the values of the movement components from vegetative winter squash into a simple Markov model, and found that during July, emigration was estimated to be faster from the triculture than the monoculture, supporting the hypothesis. However, in August, emigration was estimated to be slower from the triculture. In August, maize plants were tall and, by acting like a fence, greatly reduced the movement distance of beetles. The effect of the differences in emigration rate on beetle population density was greatest for small patches, indicating that emigration may be important only in small-scale production systems.     

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.