Egg parasitoids of Thaumetopoea pityocampa (Den. & Schiff.) (Lep., Thaumetopoeidae) and their impact in SW Turkey

Abstract: Egg parasitoids (Hym., Chalcidoidea) and egg parasitism were studied in 132 egg batches of the pine processionary moth collected from stands of Pinus nigra Arnold and P. brutia Ten. in SW Turkey, at four places in heights of 800–1010 m a.s.l. in October 1998, beyond the caterpillars’ hatch. The egg batches deposited on P. nigra were high‐significantly smaller than those found on P. brutia. In this mountainous regions, Baryscapus servadeii (Dom.) and Ooencyrtus pityocampae (Mercet) were the most abundant egg parasitoids of Thaumetopoea pityocampa (Den. & Schiff.). Considering the different sampling places, Trichogramma sp. was found maximally in 3.1% of the parasitized eggs. Additionally, the hyper‐parasitoid Baryscapusransversalis Graham (mean infestation 1.8%) and Pediobius bruchicida (Rond.) (0.1%), both occurring in both sexes, and Anastatus bifasciatus (Fonsc.) (0.1%), only females, were established. The primary parasitoid O. pityocampae dominantly parasitized the eggs placed near the top of the batches, and B. servadeii was found mainly in eggs near the base. The rate of parasitism of the egg batches was very variable. The impact of egg parasitoids and predators varied from 24 to 35.9% depending on the sampling place. The hatching rate of the caterpillars was reduced to 50.7–65.6%. Under laboratory conditions, the emergence dynamics of the parasitoids showed a peak of B. tranversalis in December of the year, in which the host eggs were laid. Baryscapus servadeii emerged mainly in March–May of the following year, when the second part of O. pityocampae appeared. A large part of both parasitoids emerged before sampling of the batches. In O. pityocampae 1.65% and in B. servadeii 2.23% males developed under laboratory conditions. A rate of 15.7% of O. pityocampae and 7.9% of B. servadeii died in the eggs. The polyembryonic Trichogramma sp. (see also Tsankov et al., 1996a ) attacked 1.8% of the eggs. Up to 20 (mean 12) dead pupae were found in one egg. Minor parts of eggs were undeveloped (2.9%) and 0.6% totally empty.     

Honeydew feeding increased the longevity of two egg parasitoids of the pine processionary moth

The longevity of a generalist (Ooencyrtus pityocampae) and a specialist (Baryscapus servadeii) egg parasitoid of the pine processionary moth (Thau‐metopoea pityocampa) was compared under laboratory feeding conditions including water and honeydew from aphid species growing on maritime pine (Pinus pinaster) or pedunculate oak (Quercus robur). The longevity of both parasitoid species increased when specimens were fed with honeydew. This increase was larger for the generalist (3.7, 32.0 and 38.0 days) than for the specialist (3.0, 23.3 and 21.5 days) parasitoid species when fed with water, oak and pine aphid honeydew respectively. The phenology of the specialist species B. servadeii is well‐adapted with its host availability with or without food supply. The generalist species O. pityocampae could overlap its host emergence curve during 14.0–20.0 days when fed with oak and pine aphid honeydew respectively, vs. no overlap when no supplementary food was provided. Analysis of honeydew composition indicated that sugars and amino acids may have distinct effects on parasitoid longevity.     

Field studies on the behaviour of two egg parasitoids of the pine processionary mothThaumetopoea pityocampa

An investigation on the behaviour ofTetrastichus servadeii Domenichini (Hym.: Eulophidae) andOoencyrtus pityocampae Mercet (Hym.: Encyrtidae) was carried out in 2 stands ofPinus nigra Arnold in the Venitian Prealps (NE Italy) by quantitative observations in the field and by trapping with different baits. The results indicate that: 1)O.pityocampae is caught by traps baited with pityolure, the synthetic sex pheromone of the host, whileT. servadeii was never caught. 2) The host selection process ofT. servadeii seems to be associated with the host plant ofThaumetopoea pityocampa (Denis & Schiffermüller) and with the aggregative behaviour of the parasitoid females. 3) The frequency distribution ofT. servadeii on the egg masses follows the negative binomial distribution; the degree of aggregation decreases with the egg mass age. These results may be taken into account in the utilization of egg parasitoids for the biological control ofTh. pityocampa.      

Seasonal history,plant interactions and egg parasitism of the variegated caper bug Stenozygum coloratum Klug (Heteroptera: Pentatomidae)

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Egg mortality in the cedar processionary moth,Thaumetopoea bonjeani (Lepidoptera: Notodontidae), in an outbreak area of Algeria

The cedar processionary moth, Thaumetopoea bonjeani (Lepidoptera: Notodontidae), is one of the most serious pests of Cedrus atlantica in north-western Africa (Algeria and Morocco). We report on T. bonjeani egg mortality and the diversity and abundance of parasitoids associated with its eggs in the area of Djurdjura Mountain (Tala-Guilef, Algeria). For this goal, 223 egg batches were collected from C. atlantica over two cohorts (2012 and 2013). The average number of eggs per egg batch increased from 143 in 2012 to 171 in 2013, while the egg mortality decreased from 47.4% and 23.9%, respectively, possibly because of a dilution effect. The most important factors of egg mortality were parasitoids and predators, with hymenopteran egg parasitoids killing from 12.1% to 34.9%, and predators from 5.2% to 7.4% of the eggs. The pattern of egg parasitism was driven largely by Ooencyrtus pityocampae, accounting for about 94% of the total parasitoids, followed by Baryscapus servadeii and Trichogramma embryophagum. An hyperparasitoid Chartocerus sp. was collected for the first time from eggs of Thaumetopoea species. As the two major egg parasitoids are shared with the pine processionary moth Thaumetopoea pityocampa in the same area, it is likely that parasitoid abundance may depend on the occurrence of both hosts.     

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.

     

Influence of egg load and host size on host-feeding behaviour of the parasitoid Aphytis lingnanensis

Abstract.

• 1 Direct behavioural assays were used to investigate the influences of host size and parasitoid egg load on the decision to host feed versus oviposit made by the parasitoid Aphytis lingnanensis Compere. Egg load was manipulated without concurrent influences on the history of host contact by exploiting size-related variation in fecundity and by holding parasitoids at different temperatures to vary the rate of oocyte maturation.
• 2 Host feeding comprised a series of feeding bouts, separated by renewed probing of the scale insect body. Successive feeding bouts were progressively shorter, suggesting that hosts represent ‘patches’ yielding resources at a decelerating rate.
• 3 Parasitoids were significantly more likely to host feed on smaller hosts and oviposit on larger hosts.
• 4 Neither egg load nor the treatment variables (parasitoid size and holding temperature) exerted significant influences on the decision to host feed versus oviposit on second instar (low quality) hosts.
• 5 The failure to observe an effect of egg load on host-feeding decisions was not simply a reflection of the parasitoids being entirely insensitive to egg load; significant effects of egg load on parasitoid search intensity and clutch size decisions were observed.
• 6 Parasitoids developing on second instar (low quality) hosts experienced high levels of mortality late during development and yielded very small adults.
• 7 The discord between these experimental results and predictions regarding the importance of egg load underscores the need for additional work on the proximate basis for host-feeding decisions and the nutritional ecology of insect parasitoids.

     

Optimal biological parameters for rearing Ooencyrtus pityocampae on the new laboratory host Philosamia ricini

Biological control programmes involving Ooencyrtus pityocampae Mercet (Hymenoptera: Encyrtidae) have proved effective at reducing the damage caused by the pine processionary Thaumetopoea pityocampa Denis & Schiffermüller (Lepidoptera: Thaumatopoeidae). In this study, the biological variables that influence the parasitism of O. pityocampae on the new laboratory host Philosamia ricini Danovan (Lepidoptera: Saturniidae) have been investigated. Laboratory experiments were conducted under the conditions of 25 ± 1°C, 65 ± 5% R.H (relative humidity) and a photoperiod of 16 : 8 h (L : D = light : dark). The host egg age and parasitoid age are often regarded as being key factors influencing the emergence rate of O. pityocampae. The optimal age of host eggs for parasitization was 1–2 days, and the emergence rate was highest with 5‐day‐old female parasitoids. Thus, our results define the optimal conditions for the effective and economic rearing of parasitoids as follows: one 5‐day‐old female parasitoid per 50 (1–2)‐day‐old host eggs. The development time of O. pityocampae ranged between 19.5 and 22.6 days. Parasitoids that were exposed to bio‐honey survived 10.5 times longer than those that did not receive supplemental food. O. pityocampae was reared for more than nine generations on the eggs of P. ricini. Consequently, P. ricini has been found as a suitable new laboratory host for the mass rearing of O. pityocampae for the use of biological control programmes against T. pityocampa in future.     

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.

     

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%).

     

The effect of host developmental stage at parasitism on sex‐related size differentiation in a larval endoparasitoid

• 1 For their larval development, parasitoids depend on the quality and quantity of resources provided by a single host. Therefore, a close relationship is predicted between the size of the host at parasitism and the size of the emerging adult wasp. This relationship is less clear for koinobiont than for idiobiont parasitoids.
• 2 As size differentiation in host species exhibiting sexual size dimorphism (SSD) is likely to occur already during larval development, in koinobiont larval endoparasitoids the size of the emerging adult may also be constrained based on the sex of the host caterpillar.
• 3 Sex‐specific growth trajectories were compared in unparasitised Plutella xylostella caterpillars and in second and fourth instar hosts that were parasitised by the solitary larval koinobiont endoparasitoid Diadegma semiclausum. Both species exhibit SSD, where females are significantly larger than males.
• 4 Healthy female P. xylostella caterpillars developed significantly faster than their male conspecifics. Host regulation induced by D. semiclausum parasitism depended on the instar attacked. Parasitism in second‐instar caterpillars reduced growth compared to healthy unparasitised caterpillars, whereas parasitism in fourth‐instar caterpillars arrested development. The reduction in growth was most pronounced in hosts producing male D. semiclausum.
• 5 Parasitism itself had the largest impact on host growth. SSD in the parasitoid is mainly the result of differences in growth rate of the parasitoid–host complex producing male and female wasps and differences in exploitation of the host resources. Female wasps converted host biomass more efficiently into adult biomass than males.

     

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.

     

Interactions between the egg and larval parasitoids of a gall-forming midge and their impact on the host

1. The gall‐forming midge Rhopalomyia californica was exposed experimentally to parasitism and predation during only the egg stage, during only the larval stage, during neither stage, or during both stages. 2. The combined action of natural enemies that attack during both the egg stage and the larval stage led to the lowest number of midges and total insects (midges + parasitoids) in the next generation, and the highest percentage parasitism. 3. The larval parasitoid killed a large fraction of hosts without producing new parasitoid offspring, while there is some indication that the egg parasitoid on its own tended to produce the most parasitoid offspring. The contrasting implications of host mortality versus parasitoid production for biological control are discussed. 4. Exposure to larval parasitoids resulted in a reduction in the number of egg parasitoid offspring produced, but exposure to the egg parasitoid did not affect the number of larval parasitoid offspring produced significantly.     

Exploration for native parasitoids of Asian longhorned beetle in China as prospective biological control agents

1. Native to China and the Korean Peninsula, the Asian longhorned beetle (ALB) Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae) is a high-risk invasive pest of hardwood trees.
2. To explore the potential of biological control of ALB in the United States, we conducted surveys of ALB parasitoids using sentinel logs in five geographical regions (Beijing, Gansu, Guizhou, Shanghai, and Yunnan) in China from 2019 to 2022.
3. Seven hymenopteran larval parasitoid species, Bracon planitibiae Yang, Eurytoma chinensis Yang, Heydenia sp., Oxysychus glabripennis Yang, Sclerodermus guani Xiao et Wu, Spathius anoplophorae Yang, and Zolotarewskya anoplophorae Yang, were collected in Beijing. Four, three and two of these species were also found in Shanghai, Guizhou, and Yunnan, respectively. No parasitoid was found in Gansu.
4. Mean parasitism rates by all parasitoid species were 3.6%–15.8% in Beijing, 1.4%–16.4% in Guizhou, 1.6%–7.1% in Shanghai, and 5.8% in Yunnan.
5. Spathius anoplophorae and O. glabripennis were the two most dominant parasitoids collected consistently in the four different regions and may be considered as prospective agents for biological control introduction against ALB in the United States.
6. We discuss some underlying ecological mechanisms that might contribute to the rarity of egg parasitoids and future opportunities and challenges for biological control of ALB.

     

Seasonal phenology and stage-specific parasitism of the apple ermine moth, Yponomeuta malinellus Zeller, in Korea

The apple ermine moth, Yponomeuta malinellus Zeller (Lepidoptera: Yponomeutidae), is a tent caterpillar that feeds on Malus spp. in Korea. Populations of the moth in native areas appeared to be regulated by the assemblage of parasitoids. Phenological associations between host stages and parasitoids, susceptible stage(s) of the host for each parasitoid, and stage‐specific parasitism were studied. The egg larval parasitoid Ageniaspis fuscicollis (Dalman) had highest parasitism of first instar larvae (24%), with 14% parasitism of other larval stages. Dolichogenidea delecta (Haliday) was recovered from all larval instars with the highest parasitism rate of second instar larvae (20.1%), followed by 19.9% parasitism of mid‐larval hosts. Herpestomus brunicornis Gravenhorst was reared from second instar larvae through to pupal collection, and had the highest parasitism rate (29.9%) at the pupal stage. The larval pupal parasitoid Zenillia dolosa (Meigen) was recovered from mid‐larval to pupal stages with the highest parasitism rate (5.5%) occurring in third to fourth instar larvae. The host stages for developing A. fuscicollis completely overlap with those of D. delecta, and with those of H. brunicornis to some degree. A statistically significant negative correlation exists between A. fuscicollis and these dominant parasitoids, indicating competitive interaction within the host.     

Host tissue identification for cryptic hymenopteran parasitoids associated with Sirex noctilio

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

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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.

     

Multitrophic influences on egg distribution in a specialized leaf beetle at multiple spatial scales

Egg distribution in herbivorous beetles can be affected by bottom-up (host plant), and by top-down factors (parasitoids and predators), as well as by other habitat parameters. The importance of bottom-up and top-down effects may change with spatial scale.

In this study, we investigated the influence of host plant factors and habitat structure on egg distribution in the leaf beetle Cassida canaliculata Laich. (Coleoptera: Chrysomelidae), a monophagous herbivore on Salvia pratensis L. (Lamiales: Lamiaceae), on four spatial scales: individual host plant, microhabitat, macrohabitat, and landscape. At the individual host plant scale we studied the correlation between egg clutch incidence and plant size and quality. On all other scales we analyzed the relationship between the egg clutch incidence of C. canaliculata and host plant percentage cover, host plant density, and the surrounding vegetation structure. Vegetation structure was examined as herbivores might escape egg parasitism by depositing their eggs on sites with vegetation factors unfavorable for host searching parasitoids.

The probability that egg clutches of C. canaliculata were present increased with an increasing size, percentage cover, and density of the host plant on three of the four spatial scales: individual host plant, microhabitat, and macrohabitat. There was no correlation between vegetation structure and egg clutch occurrence or parasitism on any spatial scale. A high percentage of egg clutches (38–56%) was parasitized by Foersterella reptans Nees (Hymenoptera: Tetracampidae), the only egg parasitoid, but there was no relationship between egg parasitism and the spatial distribution of egg clutches of C. canaliculata on any of the spatial scales investigated. However, we also discuss results from a further study, which revealed top-down effects on the larval stage.