Genetic variability in the reactive distance inTrichogramma brassicae after automatic tracking of the walking path

Efficiency of hymenopterous parasitoids to control pests in a biological control release program probably increases with increasing searching ability of the females, which, in return, likely depends on the distance from which females perceive their hosts (i.e., reactive distance). In this study, we first analyse this hypothesis with the help of a stochastic model simulating the walking path of isolatedTrichogramma females during their searching behaviour. Then, this reactive distance is estimated using automatic recording and analysis of the walking path of female wasps. Finally, the genetic variability for this trait is analysed in aTrichogramma brassicae Bezdenko (Hym.; Trichogrammatidae) population. Three types of hosts were used: Eggs ofEphestia kuehniella Zeller (Lep.; Pyralidae), eggs ofMamestra brassicae L. (Lep.; Noctuidae) and 0.45 mm glass beads.M. brassicae eggs are perceived from 4.01±0.15 mm, which is a significantly longer perceptive distance than forE. kuehniella eggs (3.69±0.10 mm) and glass beads (3.67±0.10 mm). Moreover, whatever the host tested, a significant genetic variation is observed in this trait in the population studied. The ecological and evolutionary implications and the agronomical importance of these results are discussed.     

Ratio dependence in the functional response of insect parasitoids: evidence from Trichogramma minutum foraging for eggs in small host patches

Abstract.  1. Despite considerable recent debate on the suitability of ratio dependence as a more general form for the functional response in consumer–victim relationships, there have been few detailed studies to experimentally determine the response of insect parasitoids to host and parasitoid density at a local scale.
2. The experimental host, Ephestia kuehniella , was used to test for host dependence and ratio dependence in the functional response of the egg parasitoid, Trichogramma minutum , a species widely used in inundative biological control. The functional response was examined through four series of experiments in which either host density, parasitoid density, or the ratio of previously parasitised to healthy hosts was manipulated.
3. The response to host density was type I for both single and simultaneously foraging parasitoids, indicating a lack of host dependence in the functional response. The upper limit to the response was estimated as 39 hosts attacked in a 24-h period, with an estimated per capita search rate of 1.32 for individual females and 0.37 for three simultaneously searching females.
4. The response to parasitoid density provided an interference constant of unity, indicating an equal sharing of hosts and thus ratio dependence in the functional response. Female parasitoids responded to the presence of conspecifically parasitised eggs with a significant increase in search rate (1.75), but with no change to the form or upper limit of the response.
5. It is suggested that ratio dependence may be more common among insect parasitoids than previously supposed, and that a type I functional response, or the absence of host dependence, may be an emergent property of phylogenetic constraint within the monophyletic grouping of Cales , Eretmocerus , and Trichogramma .     

Is the parasitization capacity of Trichogramma cordubensis influenced by the age of the females?

We investigated the parasitization capacity of Trichogramma cordubensis Vargas & Cabello (Hymenoptera: Trichogrammatidae) females aged 24 h, 48 h, 72 h, 96 h, 120 h, and 144 h, using Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs as hosts. Wasps were held without hosts during the period of ageing, therefore being increasingly time-limited with respect to parasitization as they got older. The total number of parasitized hosts decreased as the age of the parasitoid increased. However, the proportion of lifetime parasitism carried out on the first day increased with wasp age, up to 120-h old females. These results show that the parasitization capacity of ageing T. cordubensis females changes as they become time-limited. The consequences of such changes for biological control programs are discussed.     

Genetic variation in the behavioural mechanisms involved in the response of the egg parasitoid Trissolcus brochymenae to contact chemical cues left by the pest Murgantia histrionica

1. The ability of parasitoid females to perceive chemical traces left by their hosts is of utmost importance in the host location process. The behaviours involved in such ability have thus most likely been promoted by natural selection in the course of the evolutionary time. For this to happen, however, there must be significant genetic variation in natural populations on which natural selection could act.
2. Using the isofemale line method and motion analysis, we detected significant intra‐population genetic variation for several walking behaviour traits of the egg parasitoid Trissolcus brochymenae (Hymenoptera: Scelionidae) females responding to chemical traces left by its host Murgantia histrionica (Heteroptera: Pentatomidae).
3. Besides opening new avenues of research on the reproductive strategies, behaviour, and biological control potential of parasitoid wasps, these results also have implications for understanding their life‐history evolution in general.

     

The effect of temperature on progeny allocation and short interval timing in a parasitoid wasp

Abstract The parasitoid wasp Trichogramma dendrolimi Matsumura sets the number of progeny allocated to its insect egg hosts according to the duration of its initial transit walk across the host surface. Although cooling the wasp reduces its walking speed, reduced temperature does not affect progeny allocation. By locally heating and cooling the wasps, the initial transit can be thermally uncoupled from the subsequent oviposition. Using this technique we show that the timing of initial transit duration is temperature-dependent. These findings suggest that short interval timing by Trichogramma differs physiologically from the temperature compensated clocks that have been described for other insects.     

Oviposition and offspring survival within eggs of European corn borer: discrimination of the host embryo by female Trichogramma nubilale

Oviposition preference and offspring survival relative to the location of the host embryo was tested in the egg parasitoid Trichogramma nubilale on European corn borer host eggs. Females preferentially oviposited near to the embryo on hosts about 24 h old. Survival of Trichogramma was lower when females oviposited far from the embryo, and a higher proportion of host embryos hatched. Females did not show preferences for drilling or oviposition within very young hosts relative to where the embryo would develop, and these eggs did not produce wasps or host larvae. Female behavior was apparently adaptive in day-old hosts, not to very young hosts.     

Trichogramma pretiosum parasitism and dispersal capacity: a basis for developing biological control programs for soybean caterpillars

In order to succeed in biological control programs, not only is it crucial to understand the number of natural enemies to be released but also on how many sites per area this releasing must be performed. These variables might differ deeply among egg parasitoid species and crops worked. Therefore, these trials were carried out to evaluate the parasitism (%) in eggs of Anticarsia gemmatalis and Pseudoplusia includens after the release of different densities of the egg parasitoid Trichogramma pretiosum. Field dispersal was also studied, in order to determine appropriate recommendations for the release of this parasitoid in soybean fields. The regression analysis between parasitism (%) and densities of the parasitoid indicated a quadratic effect for both A. gemmatalis and P. includens. The maximum parasitism within 24 h after the release was reached with densities of 25.6 and 51.2 parasitoids per host egg, respectively, for the two pests. Parasitism of T. pretiosum in eggs of P. includens decreased linearly as the distance of the pest eggs from the parasitoid release sites increased. For P. includens, the mean radius of T. pretiosum action and the area of parasitoid dispersal in the soybean crop were 8.01 m and 85.18 m2, respectively. We conclude that for a successful biological control program of lepidopteran pests using T. pretiosum in soybean fields, a density of 25.6 parasitoids per host egg, divided into 117 sites per hectare, should be used.     

Genetic variability in the egg-laying behaviour ofTrichogramma maidis

SomeTrichogramma maidis females [Hymenoptera: Trichogrammatidae] aggregate their eggs in adjacent hosts whereas others scatter them amongst distant host eggs. The individual variability of aggregated-attack behaviour in matedTrichogramma maidis females was studied by isolating them with a uniform patch of about 500Ephestia kuehniella [Lepidoptera: Pyralidae] UV killed eggs. Genetic analysis demonstrated that similar behaviour exists between sisters and that the trait is transmissible and relatively stable over 2 successive generations. The ethological basis and the ecological significance of this variability are discussed.      

Effects of temporary host deprivation on the reproductive potential of Trichogramma brassicae

The effect of host deprivation on the reproductive potential and parasitization behaviour ofTrichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae) was investigated. Upon emergence, females were deprived of hosts for one to four days, and were subsequently provided with an unlimited number of hosts. Regardless of its duration, deprivation did not affect female longevity, overall rate of progeny emergence, or progeny sex-ratio. As deprivation time increased, however, the total number of parasitized host decreased from an average of 81.2 when hosts were provided at emergence, to an average of 34.0 when the waiting time was 4 days. This reduction was mainly due to the reduction in the parasitizations following the first laying peak, which was not affected when deprivation lasted fewer than 4 days.Trichogramma females are able to store ripe eggs (about 35) for 3 days without damage, but resorption occurs after four days of deprivation. Our results suggest that imaginal vitellogenesis occurs in this proovigenic wasp but that it is affected by host deprivation. The behaviour of females, as measured by the average distance between all parasitized hosts, was also modified by host deprivation. When deprivation exceeded one day, parasitizations were more scattered over the host patch. Moreover, increased deprivation times also appeared to delay the initiation of parasitization by a few hours. Host shortage is likely to occur in nature, reducing the efficiency ofTrichogramma as a biocontrol agent. The individual history of females must be taken into account in any study of the reproductive strategies of parasitoid females.     

Estimating parasitoid immature mortality by comparing oviposition and pupal development of Trichogramma galloi Zucchi and T. pretiosum Riley on natural and factitious hosts

Mortality during the immature development of T. galloi and T. pretiosum was estimated on UV-killed and live eggs of a factitious and a natural host, respectively. A staining technique was used to determine the actual parasitization of UV-treated eggs and was compared with the number of parasitoids that emerged per host egg (detectable parasitization). Effects of temperature as a factor of mortality during the immature development of both parasitoids on the factitious host was also assessed. The actual and detectable parasitization of live hosts was measured by recording both the parasitization behavior and the number of eggs where a parasitoid developed successfully. Our data show that mortality during immature development of both parasitoids may occur in live eggs of the natural host. No such mortality was observed when parasitoids developed on UV-killed eggs of the factitious host. Possible causes of parasitoid immature mortality and the effects of using UV-treated eggs of factitious hosts in estimating the parasitism capacity of Trichogramma in field conditions are discussed.     

Genetic variation in sex allocation in a parasitic wasp: variation in sex pattern within sequences of oviposition

In order to maximize their fitness under Local Mate Competition (LMC), arrhenotokous female wasps have to produce a precise sex ratio when encountering hosts. Recent progress in the theory of hymenopterous parasitoid reproduction suggest that they manage to do it by laying male and female eggs in a particular order and that such reproductive strategies are adaptive. Therefore, the determinism of such sequential patterns would be regulated by genetic control on which natural selection could act. To test this hypothesis, sequences of oviposition were recorded in a set ofTrichogramma brassicae Bezdenko (Hymenoptera; Trichogrammatidae) females and in their daughters by providing themEphestia kuehniella Zeller (Lepidoptera; Pyralidae) eggs. In order to describe accurately sex pattern within these oviposition sequences, I present a joined non-parametric and multivariate statistical method. It is shown thatT. brassicae females do not produce male and female eggs in random sequences. Moreover, the way they organize the sequence of the sexes in their progeny seems to be under a strong genetic control. The evolutionary consequences of such results are discussed.     

Patch time allocation in male parasitoids

Abstract 1. Patch time allocation has been mostly studied in female parasitoids exploiting patches of hosts. Different parameters such as oviposition, host encounters, patch quality, etc. have been repeatedly shown to modify the time females invest on hosts. 2. Male parasitoids are expected to maximise their lifetime fitness by maximising the number of females inseminated during their life. Because they can be sperm and/or time limited, they should optimise their time allocation on emergence patches. 3. Patch time allocation thus appears to be an important question for both male and female parasitoids. 4. In this study, we determined the parameters used by males of the egg parasitoid Trichogramma turkestanica to decide when to leave the emergence patch. Among the different patch‐leaving parameters tested, only contacts with parasitised hosts and presence of virgin females significantly influenced the patch‐leaving tendency. 5. Our results suggest that males express behaviours that could enable them to optimise their patch exploitation time, as females do, but using different strategies.     

The reproductive strategy of the gregarious parasitoid,Pteromalus puparum (Hymenoptera: Pteromalidae)

Summary Pteromalus puparum is a gregarious parasitoid of many butterfly pupae. Adult size, mortality, and sex ratio of P. puparum, as a parasitoid of Papilio xuthus, were unit weight of the host. Effects of female size on fecundity, wing load, and longevity were also examined.The highest total weight of progeny from the host was attained when the number of eggs per gram of the host was approximately 150. Positive correlations were observed between the size of the females and their fecundity and wing load. The maximum longevity of the female kept with honey but without hosts was attained when the initial number of parasitoids per g of the host was 150.Considering the total fecundity of all female progeny, the reproductively most efficient number of eggs to be deposited per g of the host was estimated to be approximately 300. However, as shortage of food for the adult females strongly affects their fecundity, the reproductively most efficient number of eggs to be deposited per g of the host was about 70 when the adult female progeny was not provided with food.The optimal number of eggs to be deposited when the emale oviposits in the host under field conditions is discussed.     

Using parthenogenesis‐inducing Wolbachia for the selection of optimal lines of the egg parasitoid Trichogramma pretiosum for use in biocontrol

Trichogramma wasps (Hymenoptera: Trichogrammatidae) are egg parasitoids commonly employed in augmentative biological control releases against a variety of mainly lepidopteran pests. By exploiting the mechanism by which the endosymbiotic bacterium Wolbachia induces parthenogenesis in this genus, we created a set of completely homozygous Wolbachia‐infected recombinant isofemale lines (RILs), each consisting of a different combination of the genome of two well‐characterized lines of Trichogramma pretiosum Riley. We subsequently use 16 of these RILs to investigate the effect of genetic variation on various measures associated with offspring production under laboratory conditions. Unsurprisingly, substantial differences were found between the RILs in their propensity to parasitize hosts, the number of hosts they parasitize, and the levels of mortality in their offspring. Such measures can be used to choose an optimal line for biological control purposes. A method was also developed to characterize the 16 RILs using their allelic state at five loci. Essentially, this binary system uses high‐resolution melt analysis to resolve identity at each locus, with alleles originating from either the grandmaternal or grandpaternal line, and is such that each RIL can be distinguished from each other RIL by their allelic state at one or more loci. The method facilitates the easy diagnosis of line origin when two or more lines are competing with each other in competition assays, allowing for the design of more complicated tests of parasitoid quality. Future field experiments will determine which genetic line performs best under more realistic biological control conditions. The fact that these lines are infected with parthenogenesis‐inducing Wolbachia will allow for prolonged rearing without appreciable change in their genetic makeup, which should lead to a predictable biological control performance.     

Foraging Behavior of the Parasitoid Encarsia formosa on Gerbera jamesonii Leaves

Insight into the foraging behavior of the parasitoid Encarsia formosa Gahan for whitefly hosts was gained by continuous observation of individual parasitoids on leaves of the ornamental plant Gerbera jamesonii, until females left the leaf. Comparison of the parasitoid behavior on three cultivars gave similar results. Mean searching time on uninfested G. jamesonii leaves of three cultivars was 1 h 30 min and the mean percentage of walking activity of the total observation time on those cultivars was 61%. Both parameters were not influenced by different leaf structures of Gerbera cultivars. Encounters with hosts arrested the parasitoids on the leaves. The walking activity and the percentage of host encounters that resulted in an oviposition decreased with decreasing egg load of the parasitoid. In comparison with tomato, where biological control of whiteflies is successful, only minor differences in the foraging behavior occur, except for the residence time of females, which was about three to four times longer on G. jamesonii leaves, but these leaves are about seven times larger than tomato leaves. The facts that (1) the foraging behavior of E. formosa on G. jamesonii is independant of the cultivar and (2) the foraging behavior is, in many aspects, similar to that on tomato suggest that biological control of whitefly on this ornamental plant is a potential option.     

Plant structural complexity and host-finding by a parasitoid

Summary There are three major components to plant structure relevant to searching parasitoids: 1) plant size or surface area, 2) the variation among plant parts (structural heterogeneity), such as seed heads, flowers and nectaries, and heterogeneous surfaces (e.g. glabrous, hirsute), and 3) the connectivity of parts or plant form (structural complexity). We examined the effect of structural complexity, while controlling for size and structural heterogeneity, on searching behaviors of Trichogramma nubilale in controlled environments. Females were presented with a structurally simple surface and a structurally complex one. Parasitism rates were 2.9 times higher on simple surfaces than on complex ones. Unexpectedly, when no hosts were present, searching time on simple surfaces was 1.2 times higher than on complex surfaces. This implies that structural complexity per se can affect the giving-up-time of a searching parasitoid. Searching efficiency, however, was the dominant process, and females found hosts on simple surfaces 2.4 times faster than on complex surfaces. Structural complexity can have a dramatic effect on the success of parasitoid search.     

Male reproductive strategy in Trichogramma evanescens: sperm production and allocation to females

Abstract.  The production and allocation of sperm among successive mates during a male's life largely determine its fitness. The sperm production pattern and sperm allocation to females is studied in Trichogramma evanescens , a short-lived egg parasitoid of several lepidopteran species. At emergence, virgin males have an average of 1607 ± 249 sperm stored in the seminal vesicles and no further production occurs during adult life. These males are able to mate with at least 20 females in rapid succession. During the first 10 matings, the males transfer approximately 100 sperm each time and then transfer fewer and fewer sperm per mating. The number of sperm stored in spermathecae of successively mated females remains relatively constant for the first 10 females, and decreases slowly for the subsequent females. The relationship between male reproductive strategy and some life-history traits are discussed.     

Adaptiveness of sex ratio control by the pupal parasitoid Itoplectis naranyae (Hymenoptera: Ichneumonidae) in response to host size

Adaptiveness of sex ratio control by the solitary parasitoid wasp Itoplectis naranyae (Hymenoptera: Ichneumonidae) in response to host size was studied, by examining whether differential effects of host size on the fitness of resulting wasps are to be found between males and females. The offspring sex ratio (male ratio) decreased with increasing host size. Larger hosts yielded larger wasps. Male larvae were less efficient in consuming larger hosts than female larvae. No significant interaction in development time was found between parasitoid sex and host size. Larger female wasps lived longer than smaller females, while longevity of male wasps did not increase with increasing wasp size. Smaller males were able to mate either with small or with large females, while larger males failed to mate with small females. Larger female wasps had a greater number of ovarioles and mature eggs at any one time than smaller females, although the number of eggs produced per host-feeding was not influenced by female wasps. Thus, the differential effect of host size on the fitness of males and females exists in I. naranyae. The basic assumption of the host-size model was therefore satisfied, demonstrating that sex ratio control by I. naranyae in response to host size is adaptive.     

Intrinsic, inter-specific competition between egg, egg–larval, and larval parasitoids of plusiine loopers

Abstract.  1. Intrinsic, inter-specific competition between parasitoid wasp species is a key factor in ecological community dynamics and is particularly important for application in biological control. Here three parasitoid wasp species with overlapping host ranges and differing life history strategies were chosen to examine parasitoid–parasitoid interactions: the egg parasitoid Trichogramma pretiosum, the egg–larval, polyembryonic parasitoid wasp Copidosoma floridanum, and the gregarious larval parasitoid Glyptapanteles pallipes , with the plusiine loopers Acanthoplusia agnata and Trichoplusia ni as hosts.
2.  Copidosoma floridanum has been shown to be an intrinsically superior competitor against larval parasitoids because of their production and increased investment in a soldier larval caste during development, but little is known of their interactions with egg parasitoid species. Trichogramma pretiosum completely dominated intrinsic competition with C. floridanum regardless of oviposition order or sex of the C. floridanum egg.
3. Competition between C. floridanum and G. pallipes , however, depended on the host stage at which parasitism occurred, the sex of the C. floridanum egg, and parasitoid development time. Copidosoma floridanum outcompeted G. pallipes overall, despite the fact that G. pallipes injects a polyDNA virus into the host.
4. The sex of the C. floridanum egg was a significant factor in its ability to shift caste ratios to produce more soldiers in response to G. pallipes competition.
5. Only developing female C. floridanum responded to competition with G. pallipes by increasing the ratio of soldier to reproductive larvae, and this happened only when multiparasitism occurred in the host's 1st and 2nd instar.