Parasitization by Edovum puttleri (Hymenoptera: Eulophidae) in relation to host density in the field

Abstract.

• 1 The relationship between parasitization by Edovum puttleri Grissell and density of eggs of the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae), was studied on two spatial scales (eggs mass and 6 m² cage).
• 2 For both scales, rates of parasitism were generally inversely related to host density for periods ranging from 2 to 8 days after parasitoid release. Thereafter, parasitism became independent of host density.
• 3 The initial inverse-density relationship and subsequent shift to density independence may result from several factors: (1) ambient temperatures, (2) the parasitoid's limited egg production, (3) differential times of exposure of egg masses to parasitoids, and/or (4) the parasitoid's patterns of host feeding and oviposition.
• 4 Although overall levels of parasitism were relatively low, total mortality of L.decemlineata eggs (including nonviable and cannibalized eggs, and those killed by parasitoid feeding) in parasitized egg masses was consistently high (?70–90%).

     

Response of the egg parasitoids of the pine processionary moth to host density and forest cover at the southern edge of the range

1. Thaumetopoea pityocampa is the most important pine defoliator in the Mediterranean basin. Despite being attacked by a number of natural enemies, populations occur frequently at high density in several areas.
2. Egg parasitism was studied in 27 pine and cedar forests in Algeria, in relation to the host density (tents per tree) and the proportion of forest cover in the landscape.
3. Egg parasitism varied from 2% to 25%, accounted by two parasitoid species, the specialist Baryscapus servadeii and the generalist Ooencyrtus pityocampae.
4. Tent density was negatively correlated with parasitism by B. servadeii but not with that of O. pityocampae. Conversely, parasitism by O. pityocampae increased with the proportion of forest and agricultural cover, but not in the case of B. servadeii.
5. Maximum summer temperature showed no correlation with parasitism rates. Still, temperature frequently exceeded 40 °C during the period of adult parasitoid activity.
6. The low performance of the egg parasitoids at the southern edge of the host range could be explained by the reduced fecundity of the host, climate effects, and phenological mismatching between the parasitoids and the egg development. These and other factors potentially involved the need to be further explored with a long-term study of population dynamics.

     

The spatial patterns of parasitism of eumenid wasps,Anterhynchium flavomarginatum andOrancistrocerus drewseni by the miltogrammine flyAmobia distorta

1. Spatial patterns of parasitism of eumenid wasps Anterhynchium flavomarginatum and Orancistrocerus drewseni by the miltogrammine fly Amobia distorta were studied in Kyoto, Japan during 1980–1984.
2. In generations of low (<5%) and medium (5–20%) parasitism, percent parasitism per shed (the habitat of the hosts) increased as a function of host density. Conversely, in generations of high (>20%) parasitism, percent parasitism was rather constant over different host densities.
3. The spatial distributions of adult miltogrammine flies among sheds were censused in generations of low and medium parasitism. The frequency of observations of adult miltogrammine flies was higher at sheds of higher host density (aggregative behavioral response), but on the other hand, the adult miltogrammine flies distributed in an underdispersed (or regular) manner in relation to other conspecifics.
4. The spatially density independent relationship between host density and percent parasitism in generations of high parasitism was explained in relation to parasitoid dispersal from patches of high parasitoid density.

     

Targeted sugar provision promotes parasitism of the cereal leaf beetle Oulema melanopus

• 1 Parasitoids may often lack access to sugar (e.g. floral nectar) in agricultural settings. Strategically timed spraying of host plants with sugar solution may provide one means of enhancing parasitism at the same time as minimizing nontarget effects (e.g. benefiting the pest itself).
• 2 Sucrose was sprayed in wheat fields of northern Utah (U.S.A.) to assess the effects on parasitism of the cereal leaf beetle Oulema melanopus by the larval parasitoid Tetrastichus julis.
• 3 Early‐season sugar provisioning, when larvae of the pest were first hatching and parasitoid adults were newly emerged, did not affect the numbers of cereal leaf beetle larvae that matured in treated plots but increased parasitism rates of beetle larvae by four‐fold in 2006 and by seven‐fold in 2007.
• 4 No net influx of adult parasitoids into plots was detected after the application of sugar. Locally‐emerging parasitoids may have spent less time searching for their own food needs versus hosts. A laboratory experiment also confirmed that access to sucrose significantly increased parasitoid longevity.
• 5 The field experimental results obtained demonstrate that applications of sugar, implemented to target a key time of the growing season when benefits are maximized for parasitoids and minimized for their hosts, can strongly promote parasitism of the cereal leaf beetle in wheat fields.

     

A hierarchical multi‐scale analysis of the spatial relationship between parasitism and host density in urban habitats

Studies on spatial density dependence in parasitism have paid scarce attention to how changes in host density at different hierarchical scales could influence parasitism in an herbivore at a particular scale. Here, we evaluated if rates of parasitism per leaf (by the whole parasitic complex and by dominant species) of the specialist leaf miner Liriomyza commelinae (Diptera: Agromyzidae) respond to variations in host density at the leaf, plant patch and site levels in an urban setting. We used multi‐level Bayesian models that incorporate the spatial hierarchy occurring in this system, as well as habitat factors previously found to have an effect on the L. commelinae parasitoid community in an urban context (patch size, patch isolation and urbanization level). According to the fitted model, overall parasitism rates decreased with increasing number of mines per leaf, being independent of host‐density variations at patch and site level. Patch structure was found to have a strong effect on parasitism rates per leaf. The analysis of parasitism by parasitoid species separately showed consistent results with the response at community level. These results suggest that parasitism of the parasitoid community here studied would be sensitive to hierarchical cues related to the host at the leaf level and to the host habitat at the patch level.     

Factors influencing egg parasitism in sub‐social insects: insights from the treehopper Alchisme grossa (Hemiptera,Auchenorrhyncha, Membracidae)

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Responses of native egg parasitoids to the invasive seed bug Leptoglossus occidentalis

1. The Western conifer seed bug Leptoglossus occidentalis, a native insect of North America, was accidentally introduced in Europe in the late 1990s. Since then, it has spread rapidly. Biological control could provide an efficient management option but natural enemies of the pest have been poorly examined in Europe.
2. In this study, we exposed sentinel egg masses and collected naturally laid egg masses in southern France in 2016 and 2017, to identify the egg parasitoids of L. occidentalis and investigate their potentials.
3. Three egg parasitoids were detected: Anastatus bifasciatus, Ooencyrtus pityocampae and Ooencyrtus telenomicida. The overall parasitism was low compared to that observed in the native range with 6.4% of all eggs being parasitized, while 17.1% of egg masses carried at least one parasitized egg. The total number of parasitized egg masses was similar between parasitoid species, but the mean number of parasitized eggs per egg mass was highest for A. bifasciatus (5.57 vs. 1.25 for Ooencyrtus spp.).
4. Sentinel egg masses underestimated the parasitism compared to natural egg masses (respectively, 1.42% and 7.71%).
5. Our results suggested that the three generalist parasitoids detected can respond in a Leptoglossus egg density-dependent manner, but this requires further investigations.

     

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.

     

Spatio‐temporal variation in Helicoverpa egg parasitism by Trichogramma in a tropical Bt‐transgenic cotton landscape

• 1 Understanding the spatio‐temporal dynamics of insects in agroecosystems is crucial when developing effective management strategies that emphasize the biological control of pests.
• 2 Wild populations of Trichogramma Westwood egg parasitoids are utilized for the biological suppression of the potentially resistant pest species Helicoverpa armigera (Hübner) in Bt‐transgenic cotton Gossypium hirsutum L. crops in the Ord River Irrigation Area (ORIA), Western Australia, Australia.
• 3 Extensive, spatially‐stratified sampling during a season of relatively high Trichogramma abundance found that spatial patterns of pest egg parasitism in the ORIA tend toward heterogeneity, and do not necessarily coincide with host spatio‐temporal dynamics. Both patterns of host egg density and mean rates of parasitism are not good indicators of parasitoid spatio‐temporal dynamics in ORIA cotton crops.
• 4 Parasitism rates can be significantly higher within the middle strata of the cotton plant canopy before complete canopy closure, despite a similar number of host eggs being available elsewhere in the plant.
• 5 Spatial variation in egg parasitism by Trichogramma in Bt‐transgenic cotton is evident at the between‐field, within‐field and within‐plant scale, and is not solely driven by host spatial dynamics. These factors should be considered when estimating Trichogramma impact on pest species during biological control and spatio‐temporal studies of host‐parasitoid interactions in general.

     

Heterogeneity and density dependence in a field study of a tephritid-parasitoid interaction

Abstract.

• 1 The spatial distributions of two tephritid flies (Urophora stylata (Fabricius) and Terellia serratulae L.) attacking thistle flower heads and the levels of parasitism from their associated parasitoid guilds were studied over a 7-year period.
• 2 Using these data it is possible to seek both temporal, density dependent relationships between average levels of parasitism and host density per generation, and also any spatial patterns of parasitism contributing to stability that may be operating within the same field system.
• 3 Parasitism by the two most important generalist parasitoids of T.serratulae is a direct function of average T.serratulae density per year. There is little evidence of any stabilizing heterogeneity arising from the spatial distribution of parasitism within generations.
• 4 Temporal density dependence of Urophora stylata cannot be confirmed from the 7 years of study but there is evidence of spatial heterogeneity which may have an important effect on the dynamics of the host population.

     

Biological control of cereal stem borers in Kenya: A cost benefit approach

Lepidopteran stem borers are the key pests of maize in Sub-Saharan Africa. In the lowland tropics, dry mid-altitude, dry transitional and the moist mid-altitude zones of Kenya, the invasive crambid Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) causes up to 73% yield loss. The International Centre of Insect Physiology and Ecology (ICIPE) started a biological control (BC) program in 1991 to control stem borers in subsistence agriculture in Africa with emphasis on classical BC of C. partellus. The project released the braconid larval parasitoid Cotesia flavipes Cameron (Hymenoptera: Braconidae) in 1993 in coastal Kenya, where it got established and spread to other regions. This study assesses the economic impact of the introduced parasitoid. Temporal data on percentage parasitism by the introduced parasitoid and on stem borer density were collected between 1995 and 2004. Socio-economic data was collected through administration of questionnaires to 300 farmers. Economic impact of the project was calculated as the value of the yield loss abated by the parasitoid based on a model of expected stem borer density and parasitism level. Average annual parasitism increased linearly from the time of introduction to reach 20% parasitism by 2004. The net reduction in total stem borer density over the last 10 years was 33.7%, thus abating 47.3% of yield loss. The region will accumulate a net present value of US $ 183 million in economic benefits in 20 years since release of the parasitoid. Introduction of other parasitoid species targeting the egg and pupal stages of the stem borer life cycle stages would be required for biological control to push yield loss by stem borers to an insignificant level.     

Direct and indirect effects of plant genetic variation on enemy impact

Abstract.

• 1 The Tritrophic and Enemy Impact concepts predict that natural enemy impact varies: (a) among plant genotypes and (b) may depend on the abundance of heterospecific herbivores, respectively. I tested these predictions using three herbivore species on potted, cloned genotypes of Salik sericea Marshall in a common garden experiment.
• 2 Densities of the leaf miner (Phyllonorycter salicifoliella (Chambers)) and two leaf galling sawflies (Phyllocolpa nigrita (Marlatt) and Phyllocolpa eleanorae Smith and Fritz) varied significantly among willow clones, indicating genetic variation in resistance.
• 3 Survival and natural enemy impact caused by egg and larval parasitoids and/or unknown predators differed significantly among willow clones for each of the three herbivore species, indicating genetic variation in survival and enemy impact.
• 4 Survival of Phyllonorycter was negatively density-dependent among clones.
• 5 Survival of Phyllonorycter and Phyllocolpa eleanorae were positively correlated with densities of heterospecific herbivores among clones and parasitism of these species were negatively correlated with densities of the same heterospecific herbivores among clones.
• 6 At least for Phyllonorycter this positive correlation may suggest either facilitation of survival between herbivore species, which do not share natural enemies, or an apparent interaction caused by host plant genetic variation.
• 7 Among clones, egg parasitism of Phyllocolpa eleanorae was weakly positively correlated with density of Phyllocolpa nigrita. Since these species share the same Trichogramma egg parasitoid, this interaction could support the hypothesis of apparent competition.

     

Are galling insects better protected against parasitoids than exposed feeders?: a test using tenthredinid sawflies

ABSTRACT.

• 1 Data mostly from the published literature were used to assess the effect of galling on the number of parasitoid species per host species in the phylogeny of nematine sawflies from free external feeders (colonial and solitary) to leaf gallers and shoot gallers.
• 2 The strongest effects of galling were the total elimination of the species-rich cocoon-attacking guild of parasitoids, and eonymphal parasitoids, from the parasitoid community on shoot gallers, all of which are in the genus Euura.
• 3 All tachinid larval parasitoids were also eliminated by the galling habit.
• 4 The cumulative effects of these exclusions resulted in a decline in mean number of parasitoid species per host species from almost sixteen species on external colonial feeders to 4.0 species on shoot gallers.
• 5 General patterns in per cent parasitism by non-tachinid and tachinid larval parasitoids, eonymphal and cocoon parasitoids, on exposed feeders to shoot gallers, showed declines in non-tachinid attack and elimination of tachinid, eonymphal and cocoon parasitoids. But leaf gallers tended to be attacked more than exposed feeders by non-tachinid larval parasitoids.
• 6 The galling habit had a long-term impact by reducing the number of parasitoid species attacking nematine sawfly gallers and per cent mortality inflicted, so that natural enemies may have been important as a selective factor in the evolution of galling nematine sawflies.

     

Superparasitism and mutual interference in the egg parasitoid Anagrus delicatus (Hymenoptera: Mymaridae)

Abstract.

• 1 In nature, interference among Anagrus delicatus (Hymenoptera: Mymaridae) parasitoids reduced the per-capita number of hosts parasitized. Interference increased with parasitoid density.
• 2 Anagrus delicatus did not avoid parasitizing hosts that had recently been parasitized by conspecific wasps. Evidence indicated that this superparasitism was largely a random process, increasing with the ratio of parasitized to unparasitized hosts.
• 3 Individual parasitoid efficiency, the number of hosts killed per wasp per unit time, decreased with increasing wasp density. This occurred whether wasps searched the patch together (simultaneously) or one by one (sequentially), and was the result of an increase in time spent superparasitizing hosts at higher wasp density. This is known as indirect mutual interference.
• 4 Increasing numbers of parasitoids together on the same patch caused a significant decline in the rate and per-capita number of hosts parasitized. However, there was not a correspondent decline in searching efficiency with increasing wasp density (i.e. no direct mutual interference).
• 5 These forms of parasitoid density dependence should contribute to the stability of the host—parasitoid interaction.

     

Parasitism of cotton leafworm Alabama argillacea eggs by Trichogramma pretiosum in commercial cotton fields

Release of natural enemies in commercial fields is challenging and has been inconsistent in the results achieved. This work discusses the augmentative releases of Trichogramma pretiosum to control the cotton leafworm (CLW) Alabama argillacea and also examines the parasitoid–host interaction under grower field conditions. The treatments consisted of fields with and without releases of T. pretiosum set up in Primavera do Leste and Campo Verde Counties, MT, Brazil, during three different seasons (2003 and 2004 dry and 2004 regular summer seasons). Trichogramma wasps were weekly released in the treated fields throughout the entire sampling period (14–15 week period) at a rate of 100 000 wasps per hectare. One‐way repeated measures analysis of variance was performed for the number of parasitized eggs, followed by a meta‐analysis procedure to determine the contribution of T. pretiosum release on overall parasitism. In addition, regression analysis was conducted with each season’s data sets to study the relationship of the host density and parasitism response by T. pretiosum. The overall results of Trichogramma augmentative releases did not result in significant increase of CLW egg parasitism beyond the natural parasitism in the areas studied. However, based on Cohen’s d effect sizes from the meta‐analysis, the parasitism rate was greater in fields under T. pretiosum releases during four out of 15 weeks surveyed. The parasitism of CLW eggs by T. pretiosum exhibited host density‐dependence only in one out of three seasons surveyed. These findings are encouraging as they are evidence that T. pretiosum is able to maintain a considerable level of parasitism under commercial field conditions, highlighting their potential value in large‐scale commercial areas of cotton as previously found at the small and diverse farming scale. Future studies should address the potential of early‐season, low density releases of the parasitoid.     

Density dependence of Anaphes sordidatus (Hymenoptera: Mymaridae) parasitism on eggs of Listronotus oregonensis (Coleoptera: Curculionidae)

Listronotus oregonensis (LeConte) (Coleoptera: Curculionidae) oviposits in carrot leaves and the larvae feed in carrot roots. Its eggs are parasitized by Anaphes sordidatus (Girault) (Hymenoptera: Mymaridae) throughout its oviposition period. This parasitoid is the major biotic mortality factor for L. oregonensis. Parasitism by A. sordidatus was studied for three years in sequentially sown plots of carrots, Daucus carota var. sativa. Over the scason, significantly fewer L. oregonensis eggs were oviposited in later sown carrots than in earlier sown carrots because oviposition started later in late sown plots of carrots. A positive temporal density-dependent relationship was observed each year between parasitism rates and host densities. This positive density dependence occurred in early and mid-summer for earlysown carrots where host density reached 1–2 host eggs per plant but disappeared in late summer when host density decreased while parasitism remained high. Latesown carrots had low host egg density (0.2 host egg per plant) and contributed little to the total number of eggs. In these late sown plots, parasitism increased rapidly to over 80% but no density dependence was observed. Spatially, few statistically significant regressions were found but all indicated a positive spatial density-dependence. Most non-significant regressions occurred because the range of egg density was too small between plots for a given date.     

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

     

The relationship between variable host grouping and functional responses among parasitoids of Antispila nysaefoliella (Lepidoptera: Heliozelidae)

Our study investigated the importance of variability in the parasitoid community as a source of selection on host group size using a field population of the tupelo leafminer, Antispila nysaefoliella Clemens, which specializes on tupelo, Nyssa sylvatica Marsh. Larvae were collected from leaves with variable numbers of larvae and screened for parasitism using polymerase chain reaction of mitochondrial cytochrome oxidase I using markers designed specifically for amplifying parasitoid DNA while excluding host DNA. This method of selective PCR was effective for detecting the presence and identifying species of immature stages of three hymenopteran superfamilies: Chalcidoidea, Ichneumonoidea and Platygastroidea, which represented 83.4%, 16.0% and 0.6% of the total detectable parasitism, respectively. Our resulting sequences were then calibrated with sequences from identified adult parasitoids that had been either reared or field‐captured. A cluster analysis revealed 10 distinct clades that showed differences in attack patterns with respect to host traits and season. Total parasitism followed an inverse density‐dependent or density‐independent pattern with respect to host density (number per leaf). However, when parasitoid taxa were considered separately, one clade, which could be a cryptic species of Pnigalio maculipes Crawford (Chalcidoidea: Eulophidae), was found to increase its per leaf attack rate with host density. Our results suggest that parasitoid community composition and differences among species in their attack strategies can play a large role in determining the adaptive advantage of host grouping.     

The effect of multi‐species host density on superparasitism and sex ratio in a gregarious parasitoid

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Recruitment of native parasitoids by an exotic leaf miner, Cameraria ohridella: host-parasitoid synchronization and influence of the environment

Abstract

• 1 The horse‐chestnut leaf miner, Cameraria ohridella, is a moth of unknown origin that has recently invaded Europe and severely defoliates the European horse‐chestnut, an important ornamental tree.
• 2 Several indigenous parasitoids have colonized this new host, but parasitism remains low. One of the hypotheses suggested to explain the low parasitism is that candidate parasitoids emerge too early in spring to attack the first host generation and, thus, need early‐occurring leaf miners as alternate hosts. This hypothesis was tested by observing the synchronization between the phenology of the moth and that of its main parasitoids, and by comparing parasitism rates and parasitoid richness in different environments with various levels of biological diversity.
• 3 In spring, the bulk of the parasitoids emerge at least 5 weeks before the occurrence of the first suitable larvae of C. ohridella whereas most parasitoid adults reared outdoors die within 5 weeks after emergence.
• 4 Parasitism rates and parasitoid richness do not increase with biological diversity, suggesting that most parasitoids attacking the first generation of C. ohridella do not come from alternate hosts. Parasitism does not increase later in the year in the subsequent generations, when host‐parasitoid synchronization becomes less critical.
• 5 We conclude that, although the spring emergence of parasitoids is not synchronized with the phenology of C. ohridella, the parasitoids attacking the first generation are probably old or late‐emerging adults of the overwintering generation. The lack of synchronization is probably not the only reason for the poor recruitment of native parasitoids by C. ohridella.