Host Handling Time Research Articles

Parasitism efficiency and progeny fitness of Peristenus spretus Chen et van Achterberg vary with nymphal instar of host, Apolygus lucorum (Meyer-Dür)

Peristenus spretus Chen et van Achterberg (Hymenoptera: Braconidae) is the dominant parasitoid of Apolygus lucorum (Meyer-Dür) nymphs (Hemiptera: Miridae) and exerts considerable control of the mirid’s populations in China. To understand developmental fitness of P. spretus in response to host stage selection, the development duration, parasitism efficiency, host handling time, survival rate, offspring size, and sex ratio of the parasitoid were determined when parasitoids were presented with five different instars of A. lucorum. The results showed that the developmental time of P. spretus individuals that parasitized 1st instar nymphs of A. lucorum was significantly longer than that of parasitoids developing in 2nd through 5th instars in no-choice parasitism tests. The sex ratio (as percent female) of P. spretus progeny was not significantly difference among host instars, and the regression between sex ratio (as percent female) and host instar was y = 9.80 ln (x) + 38.12. The best overall performance of P. spretus was observed when wasps parasitized 2nd, 3rd, or 4th instar hosts, because of shorter developmental duration, a higher parasitism rate, more offspring, a higher percent of female offspring, and a larger progeny size (measured as the length of the hind tibia). In choice parasitism test, fitness of P. spretus varied when it was reared in host stages ranging from 1st to 5th instars, and the parasitoid preferred to parasitize 2nd-4th instars. In addition, when parasitizing 3rd−5th instar hosts, parasitoids did not complete their development until their host had molted to an adult. Host body size significantly affected the time required for host capture and parasitization by P. spretus, and the parasitoid required the least time to parasitize medium-sized hosts. The longest handling times of P. spretus were observed for 1st and 5th instar nymphs, with values of 19.8 and 18.3 s, respectively, while the shortest handling time was 13.1 s, for 3rd instars. Our study has provided useful information for the mass rearing of this parasitoid in support of field releases of P. spretus.

Improving the efficiency of augmentative biological control with arthropod natural enemies: A modeling approach

A better understanding of the life-history traits of biocontrol agents and their effect on population dynamics is key to obtaining more efficient pest control and generating higher economic returns for biocontrol practitioners. To this end, we constructed an optimality simulation model based on principles of the behavioral ecology of natural enemies. This model allows for the identification of the most important life-history traits of natural enemies (e.g., fecundity, longevity, attack rate, competition and dispersal), taking into account the costs and benefits for biocontrol practitioners. The model was kept general and was designed in such a way that it can be adapted to different target species and their specific ecology (natural enemy-pest-plant combination). Results indicate strong interactions between the optimized life-history traits of the biocontrol agents. Two different optimized life-history strategies for the agents were found with higher potential economic returns. These strategies differ most significantly in the plant-leaving decision and host handling time of the biocontrol agent, but also in their respective fecundity, longevity and dispersal ability. The preferred strategy depends on the number of agents released and the growth rate of the plant. Information from these optimality models can help to determine which agents should be released and how they should be released in a specific agro-ecological situation.

Intraguild interactions between two biological control agents in citrus fruit: implications for biological control of medfly

AbstractThe parasitoid wasp Spalangia cameroni and the predatory beetle Pseudoophonus rufipes have long been studied for use as biological control agents against the Mediterranean fruit fly Ceratitis capitata, particularly in citrus fruit orchards. Nevertheless, these two species of natural enemies, when competing for a common resource, may experience intraguild predation (IGP) interactions. These possible interactions, affecting parasitism and predation, have been evaluated in the present work, under laboratory conditions, through potential changes in functional response. Regarding host/prey density, both natural enemies, when acting alone, showed a type II functional response. Nevertheless, due to IGP, S. cameroni, in the presence of P. rufipes, showed a higher fertility rate and a type III functional response. The parasitism behaviour of S. cameroni was affected by the presence of the predator, reducing the host handling time. Conversely, the parasitism rate of S. cameroni did not vary in the presence of P. rufipes but the degree of superparasitism decreased and led to an increased fertility rate and an increasingly female‐biased sex ratio. Meanwhile, the predatory efficiency of P. rufipes was not affected by the presence of S. cameroni but discrimination between parasitised and unparasitised pupae of C. capitata, with a preference for the latter, was reported for this predator species. Our results suggest that in biological control programmes, the use of only one of these species is recommended at low infestation levels, whilst at high densities of the pest, the combination of both natural enemies seems to be the most appropriate strategy.

Linear functional response by two pupal Drosophila parasitoids foraging within single or multiple patch environments.

Functional response describes the number of prey or hosts attacked by a predator or parasitoid as a function of prey or host density. Using three different experimental designs, we found a linear functional response by two insect parasitoids (the pteromalid Pachycrepoideus vindemiae and the diapriid Trichopria drosophilae) to their hosts (the drosophilids Drosophila suzukii and D. melanogaster). A linear function response is considered unusual for insect parasitoids. The first design was a ‘fixed time within patch experiment’ where individual parasitoids were exposed to a range of host densities for 24 h; the second two designs were a ‘variable time functional response’ and a ‘selective functional response’ experiments where individual parasitoids were presented with a range of host patches and allowed to freely select and explore only one patch (variable time) or forage for 24 h (selective). In all experimental designs, the number of hosts parasitized increased linearly until reaching an upper limit. Under the laboratory conditions used, the functional response of P. vindemiae was limited by its egg supply and time (host handling time) whereas T. drosophilae was limited by time only. The linear functional response by both parasitoids likely resulted from a constant attack rate and an incremental foraging strategy where the parasitoids left a poor (low density) host patch or remained in a higher quality host patch when there was successful oviposition and adequate host density.

Functional response of Wolbachia-infected and uninfected Trichogramma dendrolimi Matsumura (Hymenoptera: Trichogrammatidae) to Asian corn borer, Ostrinia furnacalis Guenée (Lepidoptera: Pyralidae) eggs

Trichogramma dendrolimi Matsumura (Hymenoptera: Trichogrammatidae) are haplo-diploid egg parasitoid wasps widely used as biological control agents against the Asian corn borer, Ostrinia furnacalis Guenée (Lepidoptera: Pyralidae). Two reproductive modes have been found in this species. Typically, female wasps produce haploid male offspring from unfertilized eggs and diploid female offspring from fertilized eggs (bisexual). However, they can also produce only diploid females when they are infected with Wolbachia, though the eggs are unfertilized (thelytokokous). To investigate the potential of a thelytokous Wolbachia-infected (TdW+) and a bisexual uninfected (Td) T. dendrolimi strain as inundative biocontrol agents, the functional responses of both strains toward their natural enemy (Asian corn borer) were evaluated at three constant temperatures (20, 25 and 30°C). The results revealed two types of functional response for both strains: type II and III. TdW+strain displayed type II at 30°C (high temperature) and III at 20°C (low temperature) and 25°C, while Td strain displayed type II at 20°C and III at 25°C and 30°C. The comparison of functional response between two strains indicated TdW+ and Td strain had no significant difference at 20°C. However, the estimated host handling time of the TdW+ strain was significantly shorter than that of the Td strain at 25°C, and TdW+ strain had significantly higher instantaneous search rate and shorter handling time than Td strain at 30°C. Shorter host handling time and higher instantaneous search rate in thelytokous Wolbachia-infected T. dendrolimi showed that this strain might be more effective for controlling Asian corn borer.

Antagonistic Interactions between the African Weaver Ant Oecophylla longinoda and the Parasitoid Anagyrus pseudococci Potentially Limits Suppression of the Invasive Mealybug Rastrococcus iceryoides.

The ant Oecophylla longinoda Latreille forms a trophobiotic relationship with the invasive mealybug Rastrococus iceryoides Green and promotes the latter’s infestations to unacceptable levels in the presence of their natural enemies. In this regard, the antagonistic interactions between the ant and the parasitoid Anagyrus pseudococci Girault were assessed under laboratory conditions. The percentage of parasitism of R. iceryoides by A. pseudococci was significantly higher on “ant-excluded” treatments (86.6% ± 1.27%) compared to “ant-tended” treatments (51.4% ± 4.13%). The low female-biased sex-ratio observed in the “ant-tended” treatment can be attributed to ants’ interference during the oviposition phase, which disrupted parasitoids’ ability to fertilize eggs. The mean foraging time, host handling time and number of successful oviposition in “ant-excluded” treatment were significantly higher compared to “ant-tended” treatments. When ant workers were allowed access to sterilized sand grains, mummified and unmummified R. iceryoides, they selectively removed the mummified mealybugs, indicating that they recognized the mummies as potential foods (1.2 ± 0.46 to 7.8 ± 1.17 mummies at 10 min intervals for 2 h). Percentage emergence from mummified R. iceryoides removed by the ants was significantly lower compared to emergence from mummies not exposed to ants. Although, host seeking parasitoids frequently evaded attacks, some were killed by the foraging ant workers (2.0 ± 0.38 to 6.0 ± 0.88 at 10 min intervals for 2 h). These results suggest for the first time that the presence of O. longinoda has a detrimental effect on the abundance, reproductive success and possibly oviposition strategy of female parasitoids, which might be a delimiting factor in field conditions if both natural enemies are to be recommended for use within the same agro-ecosystem.

The developmental strategies and related profitability of an idiobiont ectoparasitoid Sclerodermus pupariae vary with host size

Parasitoids can encounter patches of hosts of varying sizes. Trade‐offs may result in different developmental strategies and fitness characteristics in parasitoids. To explore developmental strategies and host suitability of a bethylid parasitoid, Sclerodermus pupariae, in relation to the size of oak long‐horned beetle larvae, Massicus raddei, effects of host size on parasitoid fitness parameters were tested under laboratory conditions. Maternal parasitoids obtained lower rates of parasitism when inoculating small or large hosts due to early host death and parasitoid injury, respectively, indicating significant fitness costs associated with paralysing those host sizes. Host size was shown to have highly variable effects on selected fitness parameters. For maternal females, increasing initial host size led to increasing host handling time, and fertility exhibited a parabolic relationship with host size. The highest fertility was exhibited when parasitoids oviposited on medium‐sized hosts. Host size effects were very apparent for parasitoid offspring, with the largest hosts producing later‐emerging but larger females. Parasitoid offspring sex ratios in all host size classes were significantly female‐biased, and exhibited a quadratic function with increasing host size. Assessment of host profitability revealed that medium‐sized hosts presented the best fitness return for the parasitoids. The findings suggest that this bethylid parasitoid can achieve a compromise in optimisation of the two most important fitness functions when encountering an abundance of different‐sized hosts.

Comparison of the host-handling behavior of Eretmocerus mundus on Bemisia tabaci B biotype, Q biotype and Trialeurodes vaporariorum

Host-handling behaviors of Eretmocerus mundus (Mercet) (Hymenoptera: Aphelinidae) toward first to fourth instar nymphs of the Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) B and Q biotypes and of Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae) were compared under laboratory conditions. The host acceptance rates differed among host stages but not among host species or biotypes. In all host species and biotypes, the parasitoids stopped their host-handling behavior before oviposition more often with older hosts. The total host-handling time was longer for the fourth instars than for younger instars, mainly due to the longer oviposition times and probing times. E. mundus showed marking behavior for the B. tabaci B and Q biotypes, but not for T. vaporariorum. In conclusion, E. mundus could parasitize all whitefly biotypes and species used in this study, but both B. tabaci biotypes were more suitable hosts than T. vaporariorum. The younger instars were good oviposition targets in all hosts.

A Comparative Study on the Functional Response ofWolbachia-Infected and Uninfected Forms of the Parasitoid WaspTrichogramma brassicae

Trichogramma species (Hymenoptera: Trichogrammatidae) are haplo-diploid egg parasitoids that are frequently used as biological control agents against lepidopteran pests. These wasps display two reproductive modes, including arrhenotoky (bisexuality) and thelytoky (unisexuality). Thelytokous forms are often associated with the presence of endosymbiotic Wolbachia bacteria. The use of thelytokous wasps has long been considered as a way to enhance the efficacy of biological control. The present study investigates the potential of a thelytokous Wolbachia-infected and an arrhenotokous uninfected Trichogramma brassicae Bezdenko strain as inundative biocontrol agents by evaluating their functional response towards different egg densities of the factitious host, the Angoumois grain moth, Sitotroga cerealella (Olivier) (Lepidoptera: Gelechiidae). The results revealed a type II functional response for both strains in which parasitism efficiency decreases with host egg density because of an increasing host handling time. A model with an indicator variable was used to compare the parameters of Holling's disc equation in different data sets. It was demonstrated that the two strains did not differ in host attack rate. However, the Wolbachia-infected strain did have an increased host handling time when compared to the bisexual strain. Some applied aspects of the findings are discussed.

Host Handling Time in a Polyembryonic Wasp is Affected both by Previous Experience and by Host State (Parasitized or Not)

Foraging behavior for hosts in parasitoids resembles that of predators with respect to finding, evaluating and manipulating of the prey. Host handling time may depend on the life history of the parasitoid and can be affected by oviposition experience. Additionally, handling time can be affected by host aggregation, species, size and state (parasitized or not). We studied handling times in the egg-larval parasitoid wasp Copidosoma koehleri. We allowed naive female wasps to oviposit into three consecutive unparasitized hosts, and measured time until oviposition, and the duration of ovipositor insertion. We recorded the same data for naive females ovipositing into already parasitized hosts. We found that both previous experience by females and previous parasitism of hosts reduced handling time. The results suggest that host handling durations reflect the interplay between host state and parasitoid internal state.

The biology of Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae), a parasitoid of the red gum lerp psyllid (Hemiptera: Psylloidea)

Abstract The red gum lerp psyllid, Glycaspis brimblecombei Moore (Hemiptera: Psylloidea), is native to Australia, where it feeds upon Eucalyptus species. It first appeared near Los Angeles, California, in 1998, and soon spread throughout the state. A biological control program directed against the psyllid was initiated and Psyllaephagus bliteus Riek (Hymenoptera: Encyrtidae) was imported from Australia and released in California. During quarantine screening, the taxonomic status of Psyllaephagus quadricyclus Riek was assessed by one of us (RLZ) and is proposed here as a new junior synonym for P. bliteus . The experiments discussed herein provide basic biological information on P. bliteus to supplement and improve the control program. We found that P. bliteus can oviposit into psyllid nymphs of any age but prefers third and fourth instars. Observations of host-handling behavior suggest that the large lerps of fifth instar psyllids increase host-handling time, thereby impeding oviposition and providing some protection from parasitism. Female P. bliteus were observed host-feeding on all psyllid nymphal development stages. Adults are relatively long-lived and, at constant temperatures of 17, 21, 23, 26, and 32 °C, longevity is a negative linear function of temperature. Females lived significantly longer than males. Adult females can live for several months, provided with hosts and held under glasshouse conditions (22 ± 3 °C), however, maximum egg deposition occurred within 22 days after adult emergence. Studies of larval development show that P. bliteus is a koinobiont and larval development is not initiated until the host reaches the late fourth or early fifth instar.

Playing the hare or the tortoise in parasitoids: could different oviposition strategies have an influence in host partitioning in two Aphidius species?

In this paper, we compare the host selection behaviours of two parasitoids, Aphidius rhopalosiphi and Aphidius picipes, in order to analyse whether behavioural adaptations to the defensive behaviour of their host (the grain aphid Sitobion avenae) could, in part, be responsible for the simultaneous presence of both species in cereal fields. The oviposition behaviour of A. picipes differed from that of A. rhopalosiphi by including a number of ‘fluttering wings’ sequences followed by immobility. It resulted in a 44 times longer host-handling time for A. picipes than for A. rhopalosiphi. Hosts attacked by A. picipes exhibited fewer defensive behaviours than hosts attacked by A. rhopalosiphi. A. picipes and A. rhopalosiphi rejected respectively 0% and 53% of unparasitized hosts presenting cornicle secretions, one of the defensive means of aphids. Furthermore, A. picipes females rejected 100% of the hosts that were already parasitized, whereas A. rhopalosiphi was previously described to reject only 20 to 40% of such hosts. Such differences could be explained by the way the two species deal with the aphid defensive behaviour. Field analyses, showed that A. rhopalosiphi was already present in wheat fields in early April whereas A. picipes appeared later and only achieved a low level of parasitism. However, when both species were present simultaneously, they shared the same resource.

Host-handling behaviours in parasitoids of the black scale: a case for ant-mediated evolution

Summary 1 We hypothesize that differences in host-handling times among three closely related encyrtid parasitoids (Metaphycus anneckei Guerrieri & Noyes, Metaphycus hageni Daane & Caltagirone and Metaphycus lounsburyi[Howard]) are influenced by the defences of their host, black scale (Saissetia oleae[Olivier]). Two forms of host defence were examined: (i) the scale’s possession of a hard integument, and (ii) the effect of ants tending S. oleae. 2 Duration of host assessment, host rejection, drilling/oviposition and the presence or absence of host feeding were measured for M. anneckei, M. hageni and M. lounsburyi. Results show that M. anneckei oviposits through the soft ventral integument while M. hageni and M. lounsburyi oviposit through the harder dorsal integument. M. anneckei was never observed to host feed while both M. hageni and M. lounsburyi use hosts for either oviposition or host feeding. The ventral drilling location and absence of non-concurrent host feeding significantly reduced the overall host-handling time of M. anneckei, relative to M. lounsburyi and M. hageni. 3 Oviposition success of M. anneckei and M. hageni in the presence of ants was compared. An observation arena was established with the numbers of Argentine ants, Linepithema humile (Mayr) and S. oleae manipulated on potted oleanders. M. hageni and M. anneckei were placed, individually, onto the observation arena and their interaction with ants and S. oleae recorded. While 55·3% of M. anneckei successfully oviposited, M. hageni was unable to oviposit or host feed in the presence of foraging ants. 4 Field tests were conducted using potted oleander plants, infested with S. oleae, to determine the effect of L. humile on scale density, parasitism levels and parasitoid species composition. Ant-tended plants had significantly more scale, lower scale parasitism and lower levels of host feeding (as indicated by unknown scale mortality levels). There were also significant differences in parasitoid species composition between ant-tended and ant-excluded treatments, with the relative frequency of parasitoid species with faster host-handling times more common in the ant-tended treatment.

Factors influencing the evolution of clutch size in a gregarious insect parasitoid

Summary 1. In this study we examined the clutch size of Hyssopus pallidus (Askew) (Hymenoptera, Eulophidae), a gregarious ectoparasitoid of codling moth (Lepidoptera, Tortricidae) larvae that is characterized by a host handling time of 2 days approximately. 2. Clutch size increased asymptotically with host larval size (fresh weight) to a maximum of 32 eggs. A single male developed from each clutch, brood survival was 83% and pupal size of female offspring was 0·45 mg, all independent of clutch size. 3. A comparison of the response of both experienced and naïve adult parasitoids to varying host larval size, indicated that experience was not necessary for H. pallidus to be able to accurately estimate host size. 4. Clutch size increased by 50% for medium size host larvae (30–40 mg) and 83% for large host larvae (60–76 mg) when the encounter rate was reduced from one host every second day to one every seventh day. A significantly lower clutch size was produced on the last day at the highest encounter rate for large host larvae, suggesting exhaustion of the egg supply for H. pallidus. 5. Manipulation of parasitoid clutch size on constant size host larvae did not influence sex ratio (single male) or brood survival (93%), but produced a linear trade‐off between clutch size and the size (fresh weight) of female pupae. Longevity, lifetime fecundity, total number of hosts attacked, and clutch size all increased linearly with the adult size (female pupal weight). 6. The observed clutch size in newly emerged H. pallidus is consistent with a strategy of maximizing lifetime fitness gain rather than the gain from individual hosts (Lack clutch size) despite a significant investment in the time required to attack each host.

Influence of experience on the sequential and temporal organization of host-acceptance behavior inBrachymeria intermedia (Chalcididae), an endoparasitoid of gypsy moth

Experienced Brachymeria intermediafemales are almost twice as likely to accept a Lymantria disparpupa as inexperienced parasitoids. The sequence of parasitoid behaviors that leads to host acceptance is highly canalized. Experienced parasitoids, however, have a higher probability of initiating host investigation and making a transition from drumming to grasping, which in turn almost invariably leads to ovipositor insertion. Experienced females found the host more quickly than inexperienced females. Host-handling time did not change with experience but was longer in females that accepted rather than rejected the host. Females exposed to gypsy moth odor but not contacting pupae behaved similarly to females that never experienced host-related stimuli.