Parasitoid Aggregation Research Articles

A STRONG ALLEE EFFECT AND PARASITOID AGGREGATION IN A DISCRETE HOST–PARASITOID SYSTEM

We study a discrete-time model of host–parasitoid interactions, where the host is subject to a strong Allee effect and the parasitoid is aggregated. The system may have multiple coexisting steady states and there are two host population thresholds. The hosts become extinct if it is below the Allee threshold. The other threshold depends on the Allee threshold beyond which the host also becomes extinct due to overcompensated density dependence. When the initial host population size is between the two thresholds, we derive a critical parasitoid population size above which both populations become extinct. The critical size depends on the degree of aggregation of parasitoids. It is shown that both populations are more likely to become extinct if parasitoid aggregation is increased. Numerical simulations reveal that a strong Allee effect on the host can stabilize the host–parasitoid interactions on one hand but may drive both populations to extinction on the other hand. Further, aggregation of the parasitoid can promote population persistence when the host is subject to a strong Allee effect with a large Allee threshold. However, a more aggregated parasitoid population is more vulnerable to extinction if the growth rate of hosts is large.

Foraging egg parasitoids, Trissolcus vassilievi (Hymenoptera: Platygastridae), respond to host density and conspecific competitors in a patchy laboratory environment.

The egg parasitoid Trissolcus vassilievi (Mayr) is a key natural enemy of sunn pest, Eurygaster integriceps Puton (Hemiptera: Scutelleridae). This laboratory study examined how the aggregation of parasitoids varied in response to host density and numbers of foraging conspecifics. Five host densities (1, 2, 4, 8, and 15 clutches of E. integriceps eggs), were offered simultaneously to 1, 2, 4, 8, or 16 female wasps in a standardized arena (30 cm diameter) and patch residence times were recorded. Patch residence time was strongly correlated with parasitism, and increased as the number of host clutches increased up to eight, but declined when more clutches were offered. Wasps displayed low mobility and tended to remain in the patch initially encountered, even when it contained few egg masses. At higher wasp densities, patches were occupied more quickly, host exploitation began sooner, and per capita handling time was reduced. However, total patch residence times were similar across all densities. Thus, females responded to conspecifics with increased movement, which increased dispersal and resulted in a more homogeneous distribution of wasps among patches. Pseudo-interference, resulting from wasps remaining in some patches and neglecting others, had greater impact on final levels of host exploitation than did actual interference (patch abandonment following conspecific encounters). These phenomena resulted in decreased parasitoid searching rates and a 2-fold increase in host survival at higher wasp densities.

Insight into the success of whitefly biological control using parasitoids: evidence from theEretmocerus warrae−Trialeurodes vaporariorumsystem

Mechanisms behind the success and failure of whitefly biological control using parasitoids are largely unknown. Here we use the Eretmocerus warrae-greenhouse whitefly system to investigate how the fluctuating density of the parasitoid and its host affects three key parasitoid fitness parameters, host searching, host feeding and parasitization, providing critical knowledge for evaluation and development of whitefly biological control programmes. This is the first such study in a parasitoid-whitefly system. Models used and developed here show that (1) both host feeding and parasitism fit a type II functional response; (2) overall parasitoid-caused whitefly mortality significantly increases with growing density of both organisms and the parasitoid density has a significantly more positive effect; (3) with a pro-synovigenic nature, E. warrae allocate significantly more resources to parasitization than to host feeding activity in low whitefly density and high parasitoid density; and (4) low mutual interference among searching parasitoids encourages parasitoid aggregation on host patches of high density. Regardless of greenhouse whitefly density, the pest can be effectively controlled by release of E. warrae. Our study provides insight into the success of whitefly biological control programmes using the parasitoid augmentation approach. Models used and developed here can also be employed to evaluate biological control programmes for other parasitoid-whitefly systems. © 2017 Society of Chemical Industry.

Density dependence and environmental factors affect population stability of an agricultural pest and its specialist parasitoid

Host–parasitoid dynamics are intrinsically unstable unless the risk of parasitism is sufficiently heterogeneous among hosts. Spatial aggregation of parasitoids can contribute to this heterogeneity, stabilising host–parasitoid population dynamics and thereby reducing pest outbreaks. We examined the spatial distribution of mango gall fly (Procontarinia matteiana, Kiefer and Cecconi), a non-native pest of South African mango orchards, which is controlled by a single parasitoid (Chrysonotomyia pulcherrima, Kerrich). We assessed whether spatial aggregation of parasitoids is associated with proximity to natural vegetation and/or to host density-dependent and host density-independent factors at three spatial scales. We found evidence for higher parasitism rates near natural vegetation at the field scale, and inverse host-density dependent and density-independent parasitoid aggregation at both the leaf scale and field scale. Therefore, we conclude that natural vegetation plays a role in promoting stabilising aggregation of parasitoids, possibly through provision of non-host resources (nectar, pollen), in this system.

Parasitoid aggregation and interference in host-parasitoid dynamics

1. Parasitoids do not distribute themselves evenly among available patches, which has an important bearing on the dynamics of host–parasitoid interactions. This study examined the density-dependent nature of aggregation of the parasitoid Dirhinus giffardii Silvestri on the oriental fruit fly host, Bactrocera dorsalis (Hendel) distributed among discrete patches. 2. Four artificial patches were created in a cage, and the number of hosts in each patch was manipulated. Parasitoids were released into the cage, and whether parasitoid density and host density influence the degree of parasitoid aggregation was examined. 3. Parasitoid aggregation became stronger (e.g. uneven distribution among patches) as the parasitoid density decreased and also as the host density increased. The index of parasitoid aggregation was not influenced by the distribution of hosts among patches. 4. The empirically characterised aggregation pattern was incorporated in a host–parasitoid model that consists of one host and one parasitoid species. The analysis of the model shows that an unstable system (i.e. the coexistence of the host and parasitoid is impossible) can be stabilised (i.e. coexistence is possible) when the parasitoid aggregates in a way that is consistent with the pattern found in the experiment.

Effects of habitat type and spatial scale on density dependent parasitism in Anagrus parasitoids of leafhopper eggs

The ability of parasitoids to maintain a high rate of parasitism under varying conditions is considered crucial to their ability to control the populations of their hosts. Here, I tested parasitism rate by Anagrus parasitoids and its dependency on the density of Erythroneura leafhopper eggs at two spatial scales (leaf and field) and two habitat types (natural vs. agricultural). The rate of parasitism differed among field sites, increased across the season, and was similar in natural and agricultural sites. At the leaf scale, the rate of parasitism was density-independent or inversely density-dependent, consistent with a weak aggregation of parasitoids on leaves with high host densities and with limited oviposition-rate or egg supply. At the field scale, in contrast, parasitism rate was positively dependent on host density, which may be explained by demographic processes, such as higher recruitment and higher fecundities of females in host-rich field sites. Overall, the results demonstrate that parasitism patterns are highly dynamic in time and space and depend on the scale of observation.

Neochrysocharis okazakii(Hymenoptera: Eulophidae) as a Major Parasitoid Wasp of Stone Leek Leaf MinerLiriomyza chinensis(Diptera: Agromyzidae) in Central Vietnam

Liriomyza chinensisis a major pest of Welsh onionAllium fistulosumin Asia but little is known about the abundance of its natural enemies. A field survey was made to explore the major parasitoids ofL. chinensisleaf miner in central Vietnam. An eulophid parasitoid,Neochrysocharis okazakii,comprised more than 95% of parasitoids reared from leaf miner larvae collected in the onion field and 98.3% of leaf miner parasitoids found during searches of onion plants. The mean number of femaleN. okazakiion plants was greater in onion fields with a higher density ofL. chinensis, and, during searches, a greater proportion ofN. okazakiiwas found on onion with moreL. chinensismines, suggesting density-dependent parasitoid aggregation. Melanized dead larvae ofL. chinensiswere more frequently found in onion fields with more parasitoids, demonstrating that melanized leaf miners are a good indicator of parasitoid activity. Mean instant rate of host encounter byN. okazakiiin the field was estimated at 0.077, and the likelihood of a parasitoid finding a host increased with host density. Taken together, these results show thatN. okazakiiis the major parasitoid ofL. chinensis. Usefulness of this parasitoid in stone leek leaf miner management is discussed.

Nectar provisioning close to host patches increases parasitoid recruitment, retention and host parasitism

In the adult stage, many parasitoids require hosts for their offspring growth and plant-derived food for their survival and metabolic needs. In agricultural fields, nectar provisioning can enhance biological control by increasing the longevity and fecundity of many species of parasitoids. Provided in a host patch, nectar can also increase patch quality for parasitoids and affect their foraging decisions, patch time residence, patch preference or offspring allocation. The aim of this study was to investigate the impact of extrafloral nectar (EFN) provisioning close to hosts on parasitoid aggregation in patches. The aphid parasitoid Diaeretiella rapae (M’Intosh) was released inside or outside patches containing Brassica napus L. infested by Brevicoryne brassicae L. aphids and Vicia faba L. with or without EFN. When parasitoids were released outside patches, more parasitoids were observed in patches with EFN than in patches deprived of EFN. This higher recruitment could be linked to a higher attraction of a combination of host and food stimuli or a learning process. A release–recapture experiment of labeled parasitoids released within patches showed the higher retention of parasitoids in patches providing EFN and hosts, suggesting that food close to the host patch affects patch residence time. Both attractiveness and patch retention could be involved in the higher number of parasitoids foraging in host patches surrounded by nectar and for the higher parasitism recorded. Nectar provisioning in host patches also affected female offspring allocation inside the patch.

Parasitism of a pollinator fig wasp: mortalities are higher in figs with more pollinators, but are not related to local densities of figs

Fig trees (Ficus) and their species‐specific pollinators (Agaonidae) represent a remarkable example of a coevolved mutualism. A number of non‐pollinating fig wasps (gallers and parasitoids,NPFW) are also an integral part of the mutualism, but have a negative impact on the reproductive success of the mutualists. MostNPFWbelong to subfamilies only associated with figs and clearly have a long association with the plants and their pollinators.In the present study, the costs imposed by an undescribed parasitoidSycoscaptersp. on its host pollinatorKradibia (=Liporrhopalum) tentacularisof a dioecious fig treeFicus montanamaintained under glasshouse conditions are described.It was asked whether pollinator numbers and sex ratios are changed by the presence or absence of parasitoids within individual figs. The effect of fig densities on parasitism rates at two spatial scales and within the general glasshouse population was also recorded. Parasitoid aggregation in relation to pollinator densities inside figs was also examined.Sycoscaptersp. significantly reduced the numbers of pollinators emerging from the figs, but host sex ratios were not distorted. The parasitoid showed host density independence at both spatial scales of fig densities, but targeted individual figs that contained higher initial densities of pollinators.

Spatial Patterns of Parasitism of the Solitary ParasitoidPseudapanteles dignus(Hymenoptera: Braconidae) onTuta absoluta(Lepidoptera: Gelechiidae)

We examined the interaction between the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), a key pest of tomato crops in South America, and its main solitary larval parasitoid, Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae). The pattern of parasitism of T. absoluta by the parasitoid was studied at three scales on tomato crops: plant, leaf, and leaflet. Host density, spatial distributions of both host and parasitoid, percentages of parasitism, variation in the probability and risk of parasitism in relation to host density, and the spatial density dependence were assessed in a horticultural region in Argentina. The spatial distribution of T. absoluta was clumped at all sites and scales, whereas that of P. dignus was much more variable, fitting to negative, positive binomial distributions and to Poisson series. Percentages of parasitism were as follows: site 1, 17.06%; site 2, 27.53%; site 3, 26.47%; site 4, 45.95%. Parasitoid aggregation in relation to host density was found at leaf and leaflet scales. However, the proportion of parasitized hosts was independent of host density. The variability of parasitism rates exhibited at the three spatial scales seems to result in partial refuges for the host, which might contribute to the persistence of the interaction between host and parasitoid. We discuss our field observations in relation to ecological theory and its potential application to the biological control of T. absoluta on tomato.

Dynamics of a host–parasitoid model with Allee effect for the host and parasitoid aggregation

In this paper, a discrete-time host–parasitoid model is investigated. Two biological phenomena, the Allee effect of the host population and the aggregation of the parasitism, are considered in our mathematical model. Through extensive numerical simulations, we gain some interesting findings related to Allee effect from this research. Firstly, the ranges of parameter, in which the population dynamics is chaos, are compressed when Allee effect is added. Secondly, the sensitivity to initial conditions of the host–parasitoid system decreased after adding Allee effect. Thirdly, without Allee effect, we observed two complicated dynamics, intermittent chaos and supertransients. However, when Allee effect is included, these two phenomena are replaced by another kind of phenomenon-period alternation, where chaos is eliminated. From above three novel findings, it can be concluded that dynamic complexities are alleviated by Allee effect. This conclusion is crucial in resolving the discrepancy between real population dynamics and theoretical predictions. Furthermore, the importance of this research is to help us understand the mechanisms inducing the irregular fluctuations of the natural populations.

Effects of flower attractiveness and nectar availability in field margins on biological control by parasitoids

Flowering plants have been shown to differ with regard to their attractiveness to parasitoids and nectar accessibility. These floral traits are likely to affect the foraging performance of parasitoids in agricultural landscapes. Using a spatially explicit simulation model we explore how the attractiveness and nectar availability of flowering field margins affects their impact on parasitoids and ultimately on pest populations in crops. The model simulates the movement, nectar feeding and parasitism of parasitoids in an agroecosystem composed of a crop and adjacent flower margin. The perception of olfactory cues emitted by flowers and host-infested plants drives the movement of the parasitoid. Its preference for floral nectar or hosts is described as a function of its internal energy status. Model validation reveals that simulations and measurements of the spatial distribution and energy status of parasitoids are generally in good agreement. Model simulations suggest that aggregation of parasitoids at flower strips are caused by a prolonged longevity of parasitoids feeding on floral nectar as well as by attraction of parasitoids from the surrounding area. We found no indication for depletion of parasitoids in the field interior as a result of migration towards flower strips. Simulations further suggest that the attractiveness of flowers is an important characteristic that should be taken into account for the selection of flowering plants. This study implies that tailoring nectar supply to the requirements of parasitoids holds potential to increase their effectiveness as biological control agents.

Foraging Behavior of Field Populations of Diadegma Spp. (Hymenoptera: lchneumonidae):Testing for Density-Dependence at Two Spatial Scales

The foraging behavior of populations of Diadegma spp. (Hymenoptera: Ichneumonidae) attacking the diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), was studied in the field. The effect of host density on percentage parasitism was investigated at two spatial scales: that of the individual plant, as well as a “cluster of plants” at low, medium and high densities. Using binoculars, parasitoid searching was observed on host plants at different host densities over an 8-h period. Behavior was compared to that predicted under the Patch Selection Theory. Percentage parasitism was independent of host density at both spatial scales. However, the behavioral studies showed parasitoid aggregation behavior at higher host densities. The population displayed an imperfect preference for higher host densities in the first 4 h of foraging. In the second 4-h period, no preference was observed.

Density-dependent foraging behaviors in a parasitoid lead to density-dependent parasitism of its host.

Empirical studies of spatial heterogeneity in parasitism by insect parasitoids have focused largely on patterns, while the many possible underlying mechanisms have been little studied in the field. We conducted experimental and observational studies on Tachinomyia similis (Diptera: Tachinidae) attacking western tussock moths (Orgyia vetusta; Lepidoptera: Lymantriidae) on lupine bushes at Bodega Bay, Calif., USA. We examined several foraging behaviors that have been hypothesized to create density-dependent variation in parasitism rates, including spatial aggregation of parasitoids to high host density, mutual interference among searching parasitoids and decelerating functional responses of the parasitoid. At the spatial scale of individual bushes, we detected both aggregation to a high density and a decelerating functional response. The resulting spatial pattern of parasitism was best fit by two models; one included an effect of parasitoid aggregation and the other included an effect of aggregation and a decelerating functional response. Most of the variation in parasitism was not correlated with density of O. vetusta.

PATCH STRUCTURE, OVIPOSITION BEHAVIOR, AND THE DISTRIBUTION OF PARASITISM RISK

To date, almost no experimental field studies have attempted to assess the factors that generate heterogeneity in the distribution of parasitism risk, a putative indicator of host–parasitoid stability. In this study, I examined the interaction between a planthopper Prokelisia crocea and its egg parasitoid Anagrus columbi among discrete patches of prairie cordgrass, Spartina pectinata. In particular, I examined how patch geography and host distribution within a patch influenced the distribution of adult parasitoids, parasitoid oviposition behavior, the proportion of hosts parasitized, and the aggregation of parasitism (cv2) and adult parasitoids. Based on six generations of census data, the distribution of parasitism was strongly aggregated within (cv2 = 3.58), but not among (cv2 = 0.58) cordgrass patches. Parasitism was also spatially and temporally density independent. To determine what influences the distribution of parasitism risk, I selected 26 discrete cordgrass patches, removed all sources of A. columbi, and then quantified the immigration and subsequent oviposition behavior of A. columbi colonists. I found that the number of immigrants significantly increased with patch size and decreased with patch isolation. Patch size had no influence on the per capita hosts parasitized per leaf, but there was a significant twofold increase in per capita attacks from the least to the most isolated patches. The isolation effect was likely due to an optimal oviposition response to dispersal distance by A. columbi. For these experimental patches, substantial within-patch aggregation of parasitism (cv2 = 1.63) did not translate into strong among-patch aggregation (cv2 = 0.13). Searching adult parasitoids were randomly distributed within and among patches and thus did not explain the high cv2 within patches. Interestingly, the aggregation of parasitism risk within a patch was significantly negatively correlated with patch size and positively correlated with patch isolation. The distribution of parasitism risk could be divided into two general components. The within-parasitoid component was attributable to individuals engaging in multiple ovipositions within a leaf and the distance-dependent oviposition response. The latter response was likely the cause for the variation in cv2 with respect to patch size and isolation. Within-parasitoid aggregation has no effect on host–parasitoid stability. The among-parasitoid component of aggregation appears to have been due to heterogeneity in the vulnerability of hosts and an edge effect (parasitism risk is 60% more heterogeneous at the edge than interior of a patch) and is in theory stabilizing. Consequently, a change in landscape structure that leads to an increase in cordgrass edge habitat may promote a more stable host–parasitoid interaction. Corresponding Editor: R. F. Denno.

Dispersal of the exotic parasitoid Cotesia flavipes in a new ecosystem

AbstractA study on the dispersal of the exotic larval endoparasitoid, Cotesia flavipes Cameron (Hymenoptera: Braconidae), was conducted in a maize field in the northern Kilifi District in the coastal area of Kenya. Because C. flavipes did not previously occur in the release area, it was possible to use a unique indirect method to estimate dispersal by examining the distribution of parasitised hosts. Parasitoids released in the centre of the field moved as far as 64 meters during their life span, and dispersal was dependent on wind direction. The level of parasitism was influenced by the location of hosts in plants. The majority of parasitised stemborers (88.4%) were found inside the plant (stems and tassel stems), where 74.3% of the suitable hosts were found, which indicates that female parasitoids were not searching randomly for hosts. Aggregation of parasitoids in response to plants with different host densities was not detected. Implications of the release of C. flavipes on stemborers population in the agroecosystem of East Africa are discussed.

Parasitoid‐mediated effects: apparent competition and the persistence of host–parasitoid assemblages

AbstractIndirect effects such as apparent competition (in which two hosts that do not compete for resources interact via a shared natural enemy) are increasingly being shown to be prevalent in the structure and function of ecological assemblages. Here, we review the empirical and theoretical evidence for these enemy‐mediated effects in host–parasitoid assemblages. We first address questions about the design of experiments to test for apparent competition. Second, we consider factors likely to affect the coexistence of host species that share a parasitoid and are involved in apparent competition. We show that parasitoid aggregation, and the switching effect that this can generate when hosts occur in separate patches, not only promotes persistence but is also strongly stabilizing. The broader consequences of these effects are discussed.

Aggregation and the Coexistence of Competing Parasitoid Species

In nature, many insect species are attacked by more than one specialized species of parasitoid. We examine whether parasitoid aggregation among patches containing hosts can promote the coexistence of specialized parasitoids on the same host species. We construct models to analyze the effects of three types of parasitoid aggregation: direct density-dependent, inverse density-dependent, and density-independent aggregation. All three types of aggregation may facilitate coexistence, provided the parasitoid species show behavioral differences that produce different patterns of aggregation. By deriving general conditions of coexistence of parasitoids, we show that all three types of aggregation act to facilitate coexistence in the same way—by increasing the covariance between the distributions of susceptible hosts and the least common parasitoid. Although they act in the same way, in general the effect of density-independent aggregation in facilitating coexistence is greater than either direct or inverse density-dependent aggregation. This suggests that density-independent aggregation may have the greatest potential to facilitate the coexistence of specialize parasitoids using the same host.

Host―parasitoid metapopulations : the consequences of parasitoid aggregation on spatial dynamics and searching efficiency

Recent studies of host-parasitoid metapopulations have shown how uniform dispersal, from a patch to its neighbouring patches, can result in the persistence of an otherwise non-persistent interaction. Here these models are extended to include density-dependent parasitoid aggregation. The fraction of dispersing hosts colonize the neighbouring patches equally, whereas parasitoid dispersal is related to the relative density of healthy hosts in each surrounding patch. Interestingly, this shows that the degree of parasitoid aggregation is associated with the self-organization of spatial structures and, in particular, spiral waves. Regions where spirals are most pronounced correspond to minimal variance in population densities. It is demonstrated, however, that parasitoid searching efficiency is highest (and mean host densities lowest) for levels of aggregation where the spatial dynamics consist of an even mixture of spirals and disordered patterns. Using an algorithmic complexity measure, it is verified that spatial transitions are also reflected in the temporal dynamics. Finally, it is demonstrated that multiple episodes of parasitoid dispersal, within a host generation, can inhibit persistence, particularly for large parasitoid movement rates.

Parasitoid Aggregation and the Stabilization of a Salt Marsh Host‐Parasitoid System

We examine a salt marsh host—parasitoid system, consisting of the planthopper Prokelisia marginata and its egg parasitoid Anagrus delicatus, for evidence of stabilizing parasitoid behavior. We first determine if there is sufficient parasitoid aggregation to potentially stabilize the Prokelisia—Anagrus interaction, using methods that infer parasitoid behavior from the spatial pattern of parasitism. We then test a basic assumption implicit in theory, that the degree of parasitoid aggregation is invariant with respect to changes in overall host and parasitoid density, and through time. Our results suggest that Anagrus behavior should, in theory, exert a consistent stabilizing effect on Prokelisia—Anagrus dynamics. Using field experiments, and direct sampling of the spatial distribution of parasitoids, we then try to determine if parasitoid aggregation is in fact responsible for the heterogeneous pattern of parasitism observed in the field. The results of these studies indicate that there is insufficient parasitoid aggregation to account for this heterogeneity. Instead, factors such as the degree of tidal inundation, or the age of host eggs, may cause host patches to differ in their vulnerability to parasitoid attack.