Patterns of parasitism by insect parasitoids in patchy environments

Abstract. 1. This paper shows how the different spatial patterns of per cent parasitism in patches of different host density can be explained within a single model framework that takes into account the parasitoid's aggregative response, and the factors limiting the degree of host exploitation within patches.
2. Two contrasting laboratory examples are presented in which the distribution of searching parasitoids and the resulting levels of parasitism in different patches are both known for a range of parasitoid densities.
3. A model is described predicting the number of hosts parasitized per patch, in which the number of parasitoids searching is determined from a simple expression allowing different degrees of aggregation.
4. The model generates patterns of parasitism encompassing the two laboratory examples and a wide range of examples from the field.
5. The importance of density dependent spatial distributions of parasitism to population stability is briefly discussed.     

“Searching time aggregation” and density dependent parasitism in a laboratory host-parasitoid interaction

Summary Assuming random search by parasitoids within host-containing patches, and a constant search rate, current host-parasitoid models suggest that searching time aggregation by parasitoids in patches of high host density should tend to produce spatially density dependent parasitism at the patch level. It is not clear, however, that statistically significant searching time aggregation necessarily implies that significant density dependent parasitism will occur. In actual host-parasitoid systems the amounts of searching time allocated to patches of equal host density may vary a great deal from patch to patch. Such behavioral variability may be capable of obscuring an underlying density dependent trend, producing density independent parasitism at the patch level despite significant searching time aggregation in patches of high host density. This possibility is tested using data from an earlier laboratory study (Morrison and Lewis; Ent. exp. et appl. 30:31–39 [1981]) of the foraging behavior of Trichogramma pretiosum Riley, a generalist parasitoid of lepidopteran eggs. Searching time allocation is found to be highly variable among patches of equal host density, and significant density dependent parasitism does not occur despite significant searching time aggregation in patches of high host density. This suggests that in cases in which density independent or density vague patterns of parasitism are observed in field samples, direct field measurements of searching time allocation in patches of different host density may be necessary to demonstrate the presence or absence of significant searching time aggregation by foraging parasitoids.     

Optimal use of patches by parasitoids with a limited fecundity

1. a mathematical model is presented which predicts the expected optimal-patch-use strategy for solitary parasitoids with a limited fecundity.
2. The model predicts that the quality of the patches is determined by the proportion of unparasitized hosts and not by the density of those hosts, and that throughout the searching period the parasitoids should maintain the level of parasitism equal in all the patches irrespective of the host density per patch.
3. The spatial pattern of parasitism among field patches by a parasitoid with a low fecundity, Praestochrysis shanghaiensis, was in agreement with the prediction of the model, i.e., a similar level of parasitism in different patches was observed when the ratio of female parasitoids to hosts in the whole study area exceeded 0.07. When the ratio was less than 0.05, however, the level of parasitism per patch showed an inverse relation to the host density, and was positively correlated with the female parasitoid-host ratio.
4. The model assumes that the parasitoids move between patches without cost and have perfect information about patch quality. Consideration of the cost of moving and sampling bridges the gap between the observed and predicted rates of parasitism found when the female parasitoid-host ratio in the whole study area was low

     

Patterns of parasitism by Trybliographa rapae, a cynipid parasitoid of the cabbage root fly, under laboratory and field conditions

ABSTRACT.

• 1 The spatial patterns of parasitism of the cabbage root fly caused by the cynipid parasitoid Trybliographa rapae (Westw.) have been studied in a laboratory system, within field cages and in a natural situation.
• 2 Continuous observations during the laboratory experiments showed the parasitoids to spend proportionately more time on the patches of high host density. This resulted in the per cent parasitism per patch being directly density dependent.
• 3 Similar patterns of parasitism were found from the field cage system, and also from experiments using the natural parasitoid population and either manipulated or natural host densities.
• 4 While mutual interference was marked in the laboratory experiments, there was little or no sign of it within the larger field cages.

     

Learning pays off: influence of experience on host finding and parasitism in Lariophagus distinguendus

Abstract. 1. The influence of experience on egg maturation, parasitism rate, and behaviour during host searching was investigated for Lariophagus distinguendus (Först.) (Hymenoptera: Pteromalidae) parasitizing larvae of the granary weevil Sitophilus granarius (L.) in grains of wheat Triticum aestivum L.
2. Dissection of female parasitoids and parasitism bioassays at high host density revealed that experience with hosts (e.g. by oviposition or by host feeding) is not required either for triggering oogenesis or for oviposition.
3. In parasitism experiments at low host density, when single host-infested grains were offered within a bulk of healthy grains, host finding and parasitism rate were increased by experience.
4. Behavioural observations revealed that searching time required for finding an infested grain was shorter for experienced parasitoids than for naive parasitoids, because travel time from grain to grain is shorter for experienced parasitoids, and because experienced parasitoids spend less time than naive parasitoids on non-infested grains.
5. In conclusion, experience due to host exposure increases parasitism and thereby the fitness of the parasitoids. It is discussed that this increase is more likely due to learning than to different egg load dynamics of experienced parasitoids.     

The effects of plant dispersion and prey density on parasitism rates in a naturally patchy habitat

Despite extensive research on parasitoid-prey interactions and especially the effects of heterogeneity in parasitism on stability, sources of heterogeneity other than prey density have been little investigated. This research examines parasitism rates by three parasitoid species in relationship to prey density and habitat spatial pattern. The herbivore Itame andersoni (Geometridae) inhabits a subdivided habitat created by patches of its host plant, Dryas drummondii, in the Wrangell Mountains of Alaska. Dryas colonizes glacial moraines and spreads clonally to form distinct patches. Habitat subdivision occurs both on the patch scale and on the larger spatial scale of sites due to patchy successional patterns. Itame is attacked by three parasitoids: an ichneumonid wasp (Campoletis sp.), a braconid wasp (Aleiodes n. sp.), and the tachinid fly (Phyrxe pecosensis). I performed a large survey study at five distinct sites and censused Itame density and parasitism rates in 206 plant patches for 1–3 years. Parasitism rates varied with both plant patch size and isolation and also between sites, and the highest rates of overall parasitism were in the smallest patches. However, the effects of both small- and large-scale heterogeneity on parasitism differed for the three parasitoid species. There was weak evidence that Itame density was positively correlated with parasitism for the braconid and tachinid at the patch scale, but density effects differed for different patch sizes, patch isolations, and sites. At the site scale, there was no evidence of positive, but some indication of negative density-dependent parasitism. These patterns do not appear to be driven by negative interactions between the three parasitoid species, but reflect, rather, individual differences in habitat use and response to prey density. Finally, there was no evidence that parasitism strongly impacted the population dynamics of Itame. These results demonstrate the importance of considering habitat pattern when examining spatial heterogeneity of parasitism and the impacts of parasitoids. Received: 3 June 1999 / Accepted: 4 October 1999     

Stochastic aggregative responses and spatial patterns of parasitism in patchy host-parasitoid interactions

Summary Assuming random search by parasitoids within host-containing patches, and a constant search rate, current host-parasitoid models suggest that positive searching time aggregation by parasitoids in patches of high host density should tend to produce spatially density dependent parasitism at the patch level. However, these models view the aggregative response as a deterministic process, ignoring variability in searching time (T _s) allocation among patches of equal host density, and it is not clear that stochastic analogues of these deterministic models would predict the same result.This question is examined by adding a stochastic aggregative response to the well-known random parasitoid equation, the deterministic equation on which most existing models have been based. Simulations, based on data collected in an earlier laboratory study, indicate that this stochastic model generates very different relationships between parasitoid searching behavior and spatial patterns of parasitism than are predicted using the deterministic approach. The stochastic model suggests that positive aggregative responses, in which patches of high host density receive larger allocations of searching time (on the average) than patches containing lower densities, may fail to produce spatially density dependent parasitism at the patch level if searching time allocation is also more variable at the higher densities. Similarly, a flat response, in which mean searching times do not vary among patches of different host density, may lead to density dependent, density independent, or inversely density dependent parasitism, depending on the variance of the searching time values among patches at different density levels. The different predictions generated by the deterministic and stochastic models can be explained on purely mathematical grounds.When models are written in units of total foraging time (T _TOT), different equations are usually required to describe the spatial features of host-parasitoid and predator-prey interactions. Because the model considered here is written in units of active searching time (T _s) it should, in cases in which the underlying assumptions hold, be capable of describing these different interactions in the framework of a single (unified) equation. This equation may also apply to some plant-herbivore systems and, to indicate its potential generality, might be referred to as a random forager equation.     

Coevolution of Contrary Choices in Host-Parasitoid Systems

We investigate patch selection strategies of hosts and parasitoids in heterogeneous environments. Previous theoretical work showed that when host traits vary among patches, coevolved populations of hosts and parasitoids make congruent choices (i.e., hosts and parasitoids preferentially select the same patches) and exhibit direct density dependence in the distribution of percent parasitism. However, host-parasitoid systems in the field show a range of patterns in percent parasitism, while behavioral studies indicate that hosts and parasitoids can exhibit contrary choices (i.e., hosts avoid patches favored by the parasitoid). We extend previous theory by permitting life-history traits of the parasitoid as well as the host to vary among patches. Our analysis implies that in coevolutionarily stable populations, hosts preferentially select patches that intrinsically support higher host equilibrium numbers (i.e., the equilibrium number achieved by hosts when both populations are confined to a single patch) and that parasitoids preferentially select patches that intrinsically support higher parasitoid equilibrium numbers (i.e., the equilibrium number achieved by the parasitoids when both populations are confined to a patch). Using this result, we show how variation in life-history traits among patches leads to contrary or congruent choices or leads to direct density dependence, inverse density dependence, or density independence in the distribution of percent parasitism. In addition, we determine when populations playing the coevolutionarily stable strategies are ecologically stable. Our analysis shows that heterogeneous environments containing patches where the intrinsic rate of growth of the host and the survivorship rate of the parasitoid are low result in the coevolved populations exhibiting contrary choices and, as a result, promote ecological stability.     

Consequences for a host–parasitoid interaction of host-plant aggregation, isolation, and phenology

Abstract.  1. Spatial habitat structure can influence the likelihood of patch colonisation by dispersing individuals, and this likelihood may differ according to trophic position, potentially leading to a refuge from parasitism for hosts.
2. Whether habitat patch size, isolation, and host-plant heterogeneity differentially affected host and parasitoid abundance, and parasitism rates was tested using a tri-trophic thistle–herbivore–parasitoid system.
3.  Cirsium palustre thistles ( n = 240) were transplanted in 24 blocks replicated in two sites, creating a range of habitat patch sizes at increasing distance from a pre-existing source population. Plant architecture and phenological stage were measured for each plant and the numbers of the herbivore Tephritis conura and parasitoid Pteromalus elevatus recorded.
4. Mean herbivore numbers per plant increased with host-plant density per patch, but parasitoid numbers and parasitism rates were unaffected. Patch distance from the source population did not influence insect abundance or parasitism rates. Parasitoid abundance was positively correlated with host insect number, and parasitism rates were negatively density dependent. Host-plant phenological stage was positively correlated with herbivore and parasitoid abundance, and parasitism rates at both patch and host-plant scales.
5. The differential response between herbivore and parasitoid to host-plant density did not lead to a spatial refuge but may have contributed to the observed parasitism rates being negatively density dependent. Heterogeneity in patch quality, mediated by variation in host-plant phenology, was more important than spatial habitat structure for both the herbivore and parasitoid populations, and for parasitism rates.     

Aggregation of parasitism risk in an aphid-parasitoid system: Effects of plant patch size and aphid density

Few studies have linked density dependence of parasitism and the tritrophic environment within which a parasitoid forages. In the non-crop plant-aphid, Centaurea nigra–Uroleucon jaceae system, mixed patterns of density-dependent parasitism by the parasitoids Aphidius funebris and Trioxys centaureae were observed in a survey of a natural population. Breakdown of density-dependent parasitism revealed that density dependence was inverse in smaller colonies but direct in larger colonies (>20 aphids), suggesting there is a threshold effect in parasitoid response to aphid density. The CV² of searching parasitoids was estimated from parasitism data using a hierarchical generalized linear model, and CV²>1 for A. funebris between plant patches, while for T. centaureae CV²>1 within plant patches. In both cases, density independent heterogeneity was more important than density-dependent heterogeneity in parasitism. Parasitism by T. centaureae increased with increasing plant patch size. Manipulation of aphid colony size and plant patch size revealed that parasitism by A. funebris was directly density dependent at the range of colony sizes tested (50–200 initial aphids), and had a strong positive relationship with plant patch size. The effects of plant patch size detected for both species indicate that the tritrophic environment provides a source of host density independent heterogeneity in parasitism, and can modify density-dependent responses.     

Spatial patterns of Trybliographa rapae parasitism of Delia radicum larvae in oilseed rape and cauliflower

Trybliographa rapae (Westwood) is an important parasitoid of Delia radicum (L.). Parasitism of D. radicum larvae by T. rapae in relation to host density on canola (oilseed rape) and cauliflower roots was examined at 10 field sites in Germany and Switzerland. For roots with host larvae, the proportion of roots with one or more parasitized hosts increased with increasing host density. However, for these infested roots, the parasitism of individual larvae was not consistently related to host density. When considering only roots on which there were parasitized larvae and the opportunity for multiple attacks, the proportion of larvae that were parasitized decreased with increasing host density in the field locations, and in a cage study under controlled conditions. A model of patch‐finding and number of attacks by female parasitoids suggests that patch‐finding is density‐dependent, but that low attack rate and interference effects limit numbers of attacks to three or less per visit to a host patch; the reduced number of attacks per visit leads to the inverse relationship of larval parasitism with host density in the host patches visited. The interplay of the density‐dependent and inversely density‐dependent processes appears to be responsible for the inconsistency of density dependence of overall larval parasitism in this and previous studies. In the laboratory, adult female T. rapae parasitized hosts at ≤4 cm deep in soil, but not at 6 cm deep. From the depth distribution of larval feeding sites in the field, we infer that between 4% and 20% of Delia larvae may be in a physical refuge from T. rapae parasitism, which may have a stabilizing influence on the host–parasitoid interaction.     

Host–parasitoid dynamics in a fragmented landscape: Holly trees,holly leaf miners and their parasitoids

Many species inhabit fragmented landscapes, where units of resource have a patchy spatial distribution. While numerous studies have investigated how the incidence and dynamics of individual species are affected by the spatial configuration and landscape context of habitat patches, fewer studies have investigated the dynamics of multiple interacting resource and consumer species in patchy landscapes. We describe a model system for investigating host–parasitoid dynamics in a patchy landscape: a network of 166 holly trees, a specialised herbivore of holly (the leaf miner, Phytomyza ilicis (Curtis, 1948)), and its suite of parasitoids. We documented patch occupancy by P. ilicis, its density within patches, and levels of parasitism over a 6-year period, and manipulated patch occupancy by creating artificially vacant habitat patches. Essentially all patches were occupied by the herbivore in each year, suggesting that metapopulation dynamics are unlikely to occur in this system. The main determinants of densities for P. ilicis and its parasitoids were resource availability (patch size and host density, respectively). While P. ilicis is apparently not restricted by the spatial distribution of resources, densities of its parasitoids showed a weaker positive relationship with host density in more isolated patches. In patches where local extinctions were generated experimentally, P. ilicis densities and levels of parasitism recovered to pre-manipulation levels within a single generation. Furthermore, patch isolation did not significantly affect re-colonisation by hosts or parasitoids. Analysing the data at a variety of spatial scales indicates that the balance between local demography and dispersal may vary depending on the scale at which patches are defined. Taken together, our results suggest that the host and its parasitoids have dispersal abilities that exceed typical inter-patch distances. Patch dynamics are thus largely governed by dispersal rather than within-patch demography, although the role of demography is higher in larger patches.     

Factors affecting the rate of attack by Cotesia rubecula (Hymenoptera: Braconidae)

Abstract. 1. The relationship between responses of the insect parasitoid Cotesia rubecula (Marshall) to kairomones produced by the feeding activities of its host, Pieris rapae (L.), and patterns of parasitism were investigated under field conditions.
2. Parasitoid adults aggregated in patches with the highest densities of host larvae but there was no commensurate increase in the rate of attack in these patches.
3. The rate of attack was not limited by the availability of eggs.
4. The rate of parasitoid attack was highest where feeding damage by the host was highest, irrespective of current host density.
5. The rate of parasitoid attack was further influenced by host age distribution. Late instar larvae were less susceptible to parasitism than were early instar larvae. The rate of attack on early instar larvae occupying the same plants as late instar larvae was reduced. This reduction in rate of attack was due to limitations on parasitoid search time imposed by the increased feeding damage associated with large host larvae and by the increased time the parasitoid required to recover from an attack on these large host larvae.     

Spatial density‐dependent parasitism and specificity in the robber fly Mallophora ruficauda (Diptera: Asilidae)

The density‐dependence in parasitism by the robber fly Mallophora ruficauda (Diptera: Asilidae) on scarab beetle larvae (Coleoptera: Scarabaeidae) populations was studied in the present research. Mallophora ruficauda is a pestiferous species common in the open grasslands of the Pampas region of South America. Adults are predators of insects and larvae are solitary parasitoids of third instar larvae of several species of scarab beetle (Coleoptera: Scarabaeidae). In contrast with most studied host‐parasitoid interactions, host searching by M. ruficauda is carried out by both larvae and adults. Typically, robber fly females lay eggs on tall grasses from where larvae drop to the ground, and attack hosts which are buried in the soil. We carried out our study at two spatial scales close to 14 apiaries located in the provinces of Buenos Aires and Entre Ríos (Argentina). We found that parasitism is density‐independent at the larger spatial scale and inversely density‐dependent at the smaller one. We also found that M. ruficauda selects Cyclocephala signaticollis among several scarab beetle species. Specificity is observed both at large and small spatial scales. We discuss the implications of both host specificity and host searching behaviour on the observed parasitism patterns.     

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.     

Emergence of global behaviour in a host–parasitoid model with density-dependent dispersal in a chain of patches

We present a time discrete spatial host–parasitoid model. The environment is a chain of patches connected by dispersal events. Dispersal of parasitoids is host-density dependent. When the host density is small (resp. high), the proportion of migrant parasitoids is close to unity (resp. to zero). We assume fast patch to patch dispersal with respect to local interactions. Local host–parasitoid interactions are described by the classical Nicholson–Bailey model. By using time scales separation methods (or aggregation methods), we obtain a reduced model that governs the total host and parasitoid densities (obtained by addition over all patches). The aggregated model describes the time evolution of the total number of hosts and parasitoids of the system of patches. This global model is useful to make predictions of emerging behaviour regarding the dynamics of the complete system. We study the effects of number of patches and host density-dependent parasitoid dispersal on the overall stability of the host–parasitoid system. We finally compare our stability results with the CV² > 1 rule.     

The impact of patch encounter rate on patch residence time of female parasitoids increases with patch quality

Abstract.  1. For animal species that forage on patchily distributed resources, patch time allocation is of prime importance to their reproductive success. According to Charnov's marginal value theorem (MVT), the rate of patch encounter should influence negatively the patch residence time: as the rate of patch encounter decreases, the patch residence time increases. Moreover, the MVT predicts that animals should stay longer in high quality patches.
2. Using the aphid parasitoid Aphidius rhopalosiphi (Hymenoptera: Aphidiinae), the effects of these two factors (patch encounter rate and host density) were combined in order to test if the increment in patch residence time for a given decrease in patch encounter rate was larger for high quality patches than for low quality patches.
3. The results show a significant effect of the interaction between the two factors. In high host density patches, parasitoids spent more time if they experienced a low patch encounter rate, while in low host density patches, patch encounter rate had no significant effect on the patch residence time. This suggests that the response of A. rhopalosiphi females to patch encounter rate varied with host density in the patch. Moreover, the same interaction effect was observed for the number of ovipositor contacts on aphids.
4. Parasitoid females can use patch encounter rate to estimate patch density in the habitat but the effect of this estimate on their patch residence time is modulated by patch quality. Staying longer in a patch when patches are rare is more advantageous when the fitness gained by doing so is large. In low quality patches, the expected fitness gain is small and the female may gain more by leaving and taking her chance at finding another patch.     

Effects of patch scale on density-dependence and species-dependence in two host-parasitoid systems

Summary Data from two host-parasitoid communities were analyzed to ascertain whether patch scale affected the kinds of correlations existing between 1) spatial differences in host density and the intensity of parasitism (density-dependence) and 2) number of species of parasitoids and the intensity of parasitism (species-dependence). We concluded that parasitization rates are usually independent of both host density and number of parasitoid species present regardless of patch scale. Therefore, the responses of parasitoids to host density and the addition of parasitoid species to a community are equally unpredictable in outcome.     

The response of aphid secondary parasitoids to different patch densities of their host

Aphids are attacked by a large guild of natural enemies including many primary parasitoids which mummify their hosts. These mummies are themselves attacked by a guild of mummy parasitoids which are potentially important in regulating primary parasitoids at densities below which they can exert biological control. The response of mummy parasitoids to mummy densities was investigated in an experiment in which mummy densities of the pea aphid (Acyrthosiphon pisum) attacked by the parasitoid Aphidius ervi were manipulated across host plant patches. Overall, the risk of parasitism was density independent, though with very high inter-patch variability which may allow probabilistic refuges from secondary parasitism. Six species of four genera of mummy parasitoids were recorded. Of the responses of the individual genera, Coruna were reared most frequently from patches of high host density while amongst patches from which Syrphophagus was reared parasitism was inversely density dependent.     

Host refuges and spatial patterns of parasitism in an endophytic host–parasitoid system

Abstract. 1. Larvae of Tephritis conura Loew (Diptera: Tephritidae) live gregariously in flower heads of Cirsium heterophyllum (L.) Hill (Cardueae). They are attacked by the endoparasitic wasps Eurytoma sp. near tibialis Boheman (Hymenoptera: Eurytomidae) and Pteromalus caudiger (Graham) (Hymenoptera: Pteromalidae).
2. The responses of the parasitoids to different host patch sizes were investigated from the analysis of field samples. At the host population level, overall probabilities of parasitism were independent of host numbers per flower head or showed a tendency to inverse density-dependence for both parasitoid species.
3. Measurements of ovipositor length in Eurytoma and P.caudiger indicated that parts of the flower head constitute a structural refuge from parasitism.
4. The accessibility of hosts in a flower head was found to differ markedly, depending on larval locations and flower head characters. In spite of this high variability, similar average percentages of larvae were accessible to the parasitoids in each patch size class.
5. High variability of oviposition success in laboratory experiments can be explained by random locations of hosts in the flower heads.