The role of tending ants in host plant selection and egg parasitism of two facultative myrmecophilous butterflies

Ovipositing adult females of myrmecophilous lycaenids are expected to select plants based on ant presence in order to maximize the survivorship of immature stages. Usually, larvae feed ants with honey-like solutions and, in turn, ants ward off parasitoids. Nonetheless, a rarely investigated approach is whether ant partners can also extend their protective behavior towards lycaenids eggs. Here, we investigated the ant-related oviposition pattern of Allosmaitia strophius and Rekoa marius; then, we compared egg parasitism according to the presence of ants. Lycaenid oviposition and egg parasitism (in percent) were experimentally compared in ant-present and ant-excluded treatments. The study plant, Heteropterys byrsonimifolia, is an extrafloral nectaried shrub which supports several ant species. We sampled 280 eggs, of which 39.65 % belonged to A. strophius and 60.35 % to R. marius. Both lycaenids eggs were significantly more abundant on branches with ants, especially those with Camponotus crassus and Camponotus blandus, two ant species known to attend to lycaenids. A. strophius and R. marius parasitism was 4.5- and 2.4-fold higher, respectively, in ant-present treatments, but the results were not statistically significant. Our study shows that ant-mediated host plant selection in lycaenids might be much more widespread than previously thought, and not restricted to obligate myrmecophilous species. Tending ants may be inefficient bodyguards of lycaenid eggs, because unlike larvae which release sugared liquids, eggs do not offer obvious rewards to ants. Ants can ward off parasitoids of larvae, as observed elsewhere, but our findings show that positive ant–lycaenid interactions are conditional and depend on immature ontogeny.     

Inaction levels for the red imported fire ant, Solenopsis invicta (hym.: formicidae): A predator of the boll weevil, Anthonomus grandis (col.: curculionidae)

The density of red imported fire ants, Solenopsis invicta Buren (Hymenoptera: Formicidae), necessary to limit boll weevil abundance, Anthonomus grandis Boheman (Coleoptera: Curculionidae), below the action level was determined. An inaction level of 0.4 fire ants per shake bucket sample (i.e., four ants per 10 plant terminals) will provide boll weevil control approximately 90% of the time. A dynamic inaction level is also provided. Total mortality of boll weevil developmental stages including eggs through teneral adults averaged 97.9%. Of 100 boll weevil eggs deposited in cotton squares (flower buds), an average of two adults survive of which about half are female. Thus, the net replacement rate per generation (R_o is 1.0 which, in this case, indicates a stable boll weevil population.     

The larval parasitoid <Emphasis Type="Italic">Microplitis croceipes</Emphasis> oviposits in conspecific adults

Microplitis croceipes (Hymenoptera: Braconidae) is a larval parasitoid of Helicoverpa/Heliothis spp. In the course of mass rearing of M. croceipes, we found that females oviposited in the conspecific adults in rearing cages. When 20 pairs of inexperienced females and males or of experienced females and males were reared in a cage, the males lived for 14–15 days and the females for 18–20 days on average. At their death, 37–42% of the males and 50–57% of the females contained conspecific eggs or first instar larvae in their abdominal cavity. When two of inexperienced females met on a host-infested leaf of soybean, they attempted to sting each other. Of the attacked females, 30% contained a conspecific egg laid in their abdomen. In abdominal cavity of the adults parasitized by a conspecific female, the majority of the parasitoid eggs laid disappeared within 1 day after oviposition. Only 10–30% of the parasitoid eggs laid in conspecific adults hatched 3–4 days after oviposition, but those larvae never molted to second instar. When the adults were stung by one or two conspecific females, their subsequent longevity was significantly shorter than that for the control adults. Oviposition in conspecific adults may be prevalent in other parasitic wasps that quickly oviposit without intensive host examination, and have cuticle and size of abdomen to be stung by conspeicifcs.     

Modeling black cutworm—Parasitoid—Weed interactions in reduced tillage corn

Computer simulations were used to evaluate the impact of tillage upon black cutworm, Agrotis ipsilon (Hufnagel), damage to seedling corn through its effects on cutworm infestation, feeding and parasitism by Meteorus rubens (Nees von Esenbeck). Using 1982 conditions of Urbana, Illinois, simulated black cutworm infestations in no-till fields approached the economic threshold of two larvae per 100 corn seedlings. In disked and conventionally tilled fields, infestations were 30 and 75% less, respectively, because weeds for oviposition sites were less abundant before planting. Cutworm damage in notill equalled or exceeded the economic injury level of 3% yield reduction. In conventional tillage, damage was 75% less than in no-till due to decreased infestation. Although infestation in disked fields was more than double that in conventional fields, damage was similar because of preferential cutworm feeding on weeds. These simulated values for black cutworm infestation and damage were similar to field data obtained under comparable conditions of tillage and moth trap-captures. Predicted M. rubens density in no-till and conventional tillage ranged from ca. 4 to 22 per 100 corn seedlings, and black cutworm parasitism ranged from 26 to 75%. In disked fields, parasitoid density increased by 40% and parasitism increased slightly (33–80%) as a consequence of weed availability for floral nutrition after planting. Simulated values for parasitoid search efficiency were similar to those estimated from field data. The increased M. rubens density and parasitism in disked fields did not affect black cutworm damage substantially. Damage reduction due to parasitism ranged from 10 to 30% under all three tillage conditions. These simulations suggest that M. rubens—weed interactions are of minor importance compared to black cutworm—weed interactions in influencing cutworm damage. In addition, they indicate that preferential cutworm feeding on weeds can substantially offset preferential cutworm oviposition in weedy, reduced-tillage fields.     

Interactions of host-plant resistance in cotton with predators and parasites

Results from no-choice field and greenhouse studies established an inverse relationship between plant trichome density in cotton and the level of successful attacks on Heliothis zea (Boddie) eggs by the parasite, Trichogramma pretiosum (Riley) and the predator, Chrysopa rufilabris (Burmeister). Thus, plant damage from H. zea can be reduced on glabrous cotton phenotypes due to antixenosis and increased entomophage effectiveness compared to hirsute and pilose phenotypes. Studies by other scientists which demonstrate interactions of natural enemies with host-plant resistance in cotton are also discussed. Symbiotic relationships between the host-plant and its associated predator/parasitoid complex may significantly influence the expression of host-plant resistance in cotton. Scientists involved in programs for development of host-plant resistant cultivars are encouraged to utilize sources of resistance which increase effectiveness of key natural enemies of the major pest species.     

Impact of wildflower strips on biological control of cabbage lepidopterans

In a 2-year experiment we investigated whether wildflower strips can be used to enhance the control of cabbage moth, Mamestra brassicae L., and cabbage white butterfly, Pieris rapae L. At two sites, including six organically cultivated fields, M. brassicae egg parasitism and predation rates were determined along with an assessment of larval parasitism rates in M. brassicae and P. rapae using a DNA-based approach. Within each field, plots with and without wildflower strips were sampled and a grid design of 3 m × 3 m was used to analyze the spatial pattern of parasitism. The provision of wildflower strips provided an idiosyncratic effect on the control of lepidopterans: parasitism rates in M. brassicae eggs and larvae were not affected, whereas parasitism rates of larval P. rapae were significantly enhanced by the wildflower strips at one of the two sites. Moreover, at one site predation rates on M. brassicae eggs were significantly enhanced in the wildflower strip plots. Geostatistical analysis showed no distinct spatial patterns in parasitism rates. These results demonstrate that the provision of wildflower strips does not necessarily enhance biological control of lepidopteran cabbage pests and suggest that site-specific environmental factors strongly affect the impact of wildflower strips.     

Short- and long-range cues used by ground-dwelling parasitoids to find their host

Parasitoids of phytophagous insects face a detectability–reliability dilemma when foraging for hosts. Plant-related cues are easily detectable, but do not guarantee the presence of the host. Host-related cues are very reliable, but much harder to detect from a distance. Little is known in particular about the way coleopteran parasitoid females use these cues when foraging for a suitable place to lay their eggs. The question is of interest because, unlike hymenopteran larvae, coleopteran parasitoid larvae are highly mobile and able to forage for hosts on their own. We assessed whether females of the parasitoid rove beetle Aleochara bipustulata (L.) (Coleoptera: Staphylinidae) are attracted to plant (Swede roots, Brassica napus) and host-related cues [pupae of the cabbage root fly Delia radicum (L.) (Diptera: Anthomyiidae)]. In the field, A. bipustulata adult females were captured in selective pitfall traps containing pieces of roots damaged by D. radicum larvae, but not in traps containing pieces of healthy roots or D. radicum pupae. However, in the laboratory, the odour of D. radicum pupae attracted A. bipustulata females to mini-pitfalls. Video monitoring in the laboratory showed that foraging A. bipustulata females preferred a zone containing D. radicum pupae and larval tracks rather than one containing an extract of D. radicum-infested roots. Our results suggest a behavioural sequence where A. bipustulata females use plant-related cues at a distance, but then switch their preference to host-related cues at a close range. This would be the first observation of this behaviour in coleopteran parasitoids.     

Effects of environmental parameters on the chestnut gall wasp and its complex of indigenous parasitoids

The chestnut gall wasp (CGW), Dryocosmus kuriphilus, an invasive pest native to China, has caused severe yield and economic losses to chestnut production in Europe since its arrival in 2002. In Southern Italy, the complex of indigenous parasitoids colonizing CGW was monitored between 2013 and 2015, with the aim of estimating the composition of the indigenous parasitoid complex, its ability to control CGW populations, and the interactions of both factors with several measured environmental parameters. We compared results among three differently managed field types. Results showed an increase in the rate of parasitism both when the host population density was lower and in unmanaged chestnut stands with more natural conditions. The percentage of parasitism in galls was related to morphological traits of the galls and to higher seasonal temperatures, which reduced the parasitism intensity because CGW develops earlier under such conditions. The host–parasitoid mortality inside galls varied among sites and was associated mostly with rot fungi during wet spring and summer months. Parasitoid species richness was similar among the study sites, but the proportion of parasitoid species differed between orchards and unmanaged coppice stands. The timing of attack by parasitoids followed a species-specific successional sequence throughout the larva-to-adult life cycle of the CGW. These interactions should be considered in future research on trophic relationships and when modeling invasive scenarios for new pest species.     

Effects of height and habitat type on egg parasitism by Trichogramma minutum and T. pretiosum (Hymenoptera: Trichogrammatidae)

Heliothis virescens (Fabricius) eggs were sampled to determine the effects of height and habitat type (soybean field vs. uncultivated vegetation) on rates of p arasitism by Trichogramma minutum Riley and T. pretiosum Riley. The potentially confounding effects of plant associations and host density and distribution were eliminated by sampling with laboratory-produced eggs deposited on cloths, rather than with eggs naturally deposited by endemic hosts.A 3-way contingency table analysis showed that parasitism (whether the egg cloths were parasitized or not) was significantly associated with height and habitat type in 1981, with higher rates of parasitism in the uncultivated habitat and at the greater height. Parasitism was independent of height and habitat in 1982. Rates of parasitism by the two Trichogramma species were not clearly associated with habitat type, but were associated with height. T. minutum consistently parasitized egg cloths positioned at greater heights than those parasitized by T. pretiosum. While the behavioral mechanisms responsible are unknown, this inter-specific difference could have important implications with regard to selecting the most suitable of these two Trichogramma species for a particular inundative release program.     

Evaluation of Steinernema feltiae and S. bibionis (Rhabditida: Steinernematidae) for suppression of Lymantria dispar (Lepidoptera: Lymantriidae) in Pennsylvania,U.S.A.

Lymantria dispar L. larvae exposed to the entomogenous nematodes Steinernema feltiae Filipjev and S. bibionis (Bovien) for ⩾ 16 h in laboratory petri dish tests averaged 93 and 91% mortality, respectively. Nylon pack cloth bands, lined with Pellon fleece or terry cloth, placed around oak tree boles were treated with nematode suspensions in central Pennsylvania. Fifth and 6th stage host larvae collected from beneath these bands after nematode treatment averaged 28% mortality.     

Spatial distribution of different stages of mango stone weevil, Sternochetus mangiferae (fabricius) (coleoptera: Curculionidae)

Studies were conducted on the spatial distribution of different stages of the mango stone weevil, Sternochetus mangiferae (Fabr.) at Hessaraghatta farm of the Indian Institute of Horticultural Research, Bangalore, during 1983. The values of various parameters of distribution showed that the eggs are distributed as a negative binomial (contagious) distribution, whereas larvae and adults follow a positive binomial (random) distribution. It is suggested that the change in distribution may be due to the lower population densities in larval and adult stages.     

Phenology and control of the onion maggot (Diptera: Anthomyiidae) in Michigan onion production

The phenology and control of the onion maggot, Delia antiqua (Meigen) (Diptera: Anthomyiidae), were investigated in commercial onion fields in Michigan from 1978 to 1980. First-generation emergence of adults occurred at 399 Dδ (degree-days) (4.4°C base). Second- and third-generation emergence occurred at 1142 and 1840 D°. Adult flight activity was correlated with time of damage to onion plants by 1st and 2nd generation larvae. Third-generation larvae were only observed on unharvested mature onions. Phenologies of the various life-stages are compared to development rates determined in the laboratory. Application of foliar insecticide sprays for adult control did not provide additional protection from root maggot damage where granular insecticides had been applied at planting. Recommendations for onion maggot control are discussed.     

Integrated pest management of Liriomyza trifolii: Influence of avermectin,cyromazine, and methomyl on leafminer ecology in celery

The impact of weekly applications of avermectin, cyromazine and methomyl on Lyriomyza trifolii (Burgess) and an associated complex of six parasite species was evaluated in celery, Apium graveolens L. Avermectin suppressed leafminer populations, but did not adversely affect (1) seasonal per cent parasitism, (2) adult parasite mortality, or (3) survival and emergence of immature parasites from treated foliage. Although cyromazine use also reduced L. trifolii density, significant reductionsin survival and emergence of immature parasites greatly diminished the potential for biological control by lowering the seasonal per cent parasitism and increasing the L. trifolii: parasite ratio. Methomyl application for control of lepidopterous larvae increased leafminer density and reduced the seasonal percent parasitism by reducing survival of adult parasites.Species composition of the parasite complex was least affected by avermectin and methomyl. Cyromazine significantly reduced the relative abundance of some key parasite species. Major parasite species included species in the family Eulophidae: Diglyphus intermedius (Girault), D. begini (Ashmead), Chrysonotomyia (Achrysocharella) punctiventris (Crawford), Chrysocharis parksi Crawford and C. ainsliei Crawford, and the family Pteromalidae: Halticoptera circulus (Walker). The potential for incorporation of these compounds into an integrated pest management program for celery and tomatoes, Lycopersicon esculentum Mill., is discussed.     

Mortality of pollen beetle (Meligethes spp.) larvae due to predators and parasitoids in rape fields and the effect of conservation strips

In 1996–1999, different mortality factors of pollen beetle larvae were investigated in twenty six rape fields in the northern part of Switzerland which had either a wild flower strip or an extensively managed meadow adjacent to the long side of the field. At 3 and 30 m into the crop from the conservation strip, total mortality, mortality from predators, parasitoids and unspecified factors were measured. Total pollen beetle larval mortality was 66–96%. Mortality caused by predators was 16–27% and there was no significant difference between mortality at 3 m and that 30 m from the extensively managed meadows. However, in fields with wild flower strips adjacent to them, the percentage mortality from predators was significantly greater at 30 m than at 3 m. The range of parasitism of pollen beetle larvae was 0–54% and was on average greater at 3 m than at 30 m. In fields with wild flower strips, the percentage parasitism with Tersilochus heterocerus was significantly higher than in fields with extensively managed meadows. However, mortality from all parasitoids was only 1–2% and there was no significant difference between 3 and 30 m. The effect of parasitoids on pollen beetle mortality was masked by the high unspecified mortality and the mortality from predators. The unspecified mortality was 46–72% and was significantly greater in 1998 and 1999 than in 1996 and 1997. These differences are probably because of meteorological factors (wet in 1999 and dry in 1998). The possible influences of the two types of conservation strips on pollen beetle larval density were investigated. The results show that in fields with adjacent wild flower strips, the pollen beetle larvae were more evenly distributed (but not significantly so) than in fields with extensively managed meadows where larval density decreases faster from the edge into the rape field.     

Temperature and parasitism by <Emphasis Type="BoldItalic">Asobara tabida</Emphasis> (Hymenoptera: Braconidae) influence larval pupation behaviour in two <Emphasis Type="BoldItalic">Drosophila</Emphasis> species

In holometabolous insects, pupation site selection behaviour has large consequences for survival. Here, we investigated the combined effects of temperature and parasitism by the parasitoid Asobara tabida on larval pupation behaviour in two of its main Drosophila sp. hosts differing in their climate origin. We found that larvae of Drosophila melanogaster—a species with a (sub)tropical origin—placed at 25°C pupated higher in rearing jars than those placed at 15°C. The opposite pattern was observed for Drosophila subobscura larvae—a species from temperate regions—which pupated lower, i.e. on or near the substrate at 25°C, than those placed at 15°C. When placed at 25°C, parasitized larvae of both species pupated closer to the substrate than unparasitized ones. Moreover, the Drosophila larvae that had been exposed and probably stung by A. tabida, but were not parasitized, pupated lower than the control unparasitized larvae. These results provide new insights of host behaviour manipulation by A. tabida larvae.     

Pre-pupation behaviour of the aphid parasitoid <Emphasis Type="Italic">Aphidius ervi</Emphasis> (Haliday) and its consequences for pre-imaginal learning

Olfactory learning may occur at different stages of insect ontogeny. In parasitoid wasps, it has been mostly shown at adult emergence, whilst it remains controversial at pre-imaginal stages. We followed larval growth of the parasitoid wasp, Aphidius ervi Haliday, inside the host aphid, Acyrthosiphom pisum Harris, and characterised in detail the behaviour of third instar larvae. We found that just before cocoon spinning begins, the third instar larva bites a hole through the ventral side of the mummified aphid exoskeleton. We then evaluated whether this period of exposure to the external environment represented a sensitive stage for olfactory learning. In our first experiment, the third instar larvae were allowed to spin their cocoon on the host plant (Vicia faba L.) surface or on a plastic plate covering the portion of the host plant exposed to the ventral opening. Recently emerged adults of the first group showed a preference for plant volatiles in a glass Y-olfactometer, whereas no preference was found in adults of the second group. In a second experiment, during the period in which the aphid carcass remains open or is being sealed by cocoon spinning, third instar larvae were exposed for 24 h to either vanilla odours or water vapours as control. In this experiment, half of the parasitoid larvae were later excised from the mummy to avoid further exposure to vanilla. Adult parasitoids exposed to vanilla during the larval ventral opening of the mummy showed a significant preference for vanilla odours in the olfactometer, regardless of excision from the mummy. The larval behaviour described and the results of the manipulations performed are discussed as evidences for the acquisition of olfactory memory during the larval stage and its persistence through metamorphosis.     

Different uses of plant semiochemicals in host location strategies of the two tachinid parasitoids

Some members of the family Tachinidae (Insecta: Diptera) deposit numerous very small eggs, termed “microtype” eggs, on the food plants of their caterpillar hosts. Parasitization is successful only when the hosts ingest these eggs. To increase the chance of hosts encountering the eggs, microtype tachinid parasitoids have to choose a suitable plant that harbors hosts and lay their eggs near the hosts. In their host location process, semiochemicals emitted by host-infested plants offer the tachinids a reliable cue. We investigated the behavioral responses of two microtype tachinid parasitoids, Pales pavida and Zenillia dolosa, to maize plants infested with their caterpillar host, Mythimna separata, in a wind tunnel. P. pavida females showed a significantly higher rate of landing on caterpillar-infested plants than on mechanically wounded or intact plants, whereas Z. dolosa landed on both the caterpillar-infested and mechanically wounded plants at significantly higher rates than on intact plants. We also examined which part of a caterpillar-infested maize leaf induces oviposition. P. pavida deposited eggs on the margin of the leaf, whereas Z. dolosa preferentially laid eggs around a caterpillar-infested area or a mechanically wounded spot. P. pavida eggs retained their parasitization ability for more than 15?days after they were deposited, whereas the eggs of Z. dolosa could not survive more than 5?days after oviposition. Our results suggest that each tachinid parasitoid employs a different host location strategy to exploit semiochemicals coming from plant–herbivore interaction as cues in order to increase their parasitization success.     

Postembryonic development of the bone-eating worm Osedax japonicus

Bone-eating worms of the genus Osedax exclusively inhabit sunken vertebrate bones on the seafloor. The unique lifestyle and morphology of Osedax spp. have received much scientific attention, but the whole process of their development has not been observed. We herein report the postembryonic development and settlement of Osedax japonicus Fujikura et al. (Zool Sci 23:733–740, 2006). Fertilised eggs were spawned into the mucus of a female, and the larvae swam out from the mucus at the trochophore stage. Larvae survived for 10 days under laboratory conditions. The larvae settled on bones, elongated their bodies and crawled around on the bones. Then they secreted mucus to create a tube and the palps started to develop. The palps of O. japonicus arose from the prostomium, whereas the anterior appendages of other siboglinids arose from the peristomium. The recruitment of dwarf males was induced by rearing larvae with adult females. Females started to spawn eggs 6 weeks after settlement.     

Mass releases of Aphidius rhopalosiphi (Hymenoptera: Aphidiinae), and strip management to control of wheat aphids

Biological control of cereal aphids was attempted during two years, using two approaches: (1) mass-release of Aphidius rhopalosiphi (21,000 individuals/ha) in May and (2) use of a clover-ryegrass strip as a parasitoid reservoir. Two aphid species (Metopolophium festucae and Acyrtosiphon pisum) considered as alternative hosts for cereal aphid parasitoids occurred in the grassy strips. Three fields for each of the mass release or strip management were compared in 2000 with two control fields where no aphid control was done. Aphid population growth was significantly reduced under both mass release and management compared to controls. There was no significant difference between the two treatments. Yet, the parasitism rates were significantly higher under mass release and strip management than in the controls. In 2001, three fields per treatment were compared with three controls. Aphid numbers were very low in all fields, strip management being the only treatment to slow down aphid population growth.     

Host genotype and age have no effect on rejection of parasitic eggs

Egg rejection belongs to a widely used host tactic to prevent the costs incurred by avian brood parasitism. However, the genetic basis of this behaviour and the effect of host age on the probability of rejecting the parasitic egg remain largely unknown. Here, we used a set of 15 polymorphic microsatellite loci, including a previously detected candidate locus (Ase64), to link genotypes of female great reed warblers (Acrocephalus arundinaceus), a known rejecter, with their egg rejection responses in two host populations. We also tested whether host female age, as a measure of the experience with own eggs, plays a role in rejection of common cuckoo (Cuculus canorus) eggs. We failed to find any consistent association of egg rejection responses with host female genotypes or age. It seems that host decisions on egg rejection show high levels of phenotypic plasticity and are likely to depend on the spatiotemporal variation in the parasitism pressure. Future studies exploring the repeatability of host responses towards parasitic eggs and the role of host individual experience with parasitic eggs would greatly improve our understanding of the variations in host behaviours considering the persistence of brood parasitism in host populations with rejecter phenotypes.