Functional response of Telenomus remus (Hymenoptera: Scelionidae) to different egg densities of Spodoptera frugiperda (Lepidoptera: Noctuidae)

The behaviour of searching parasites and predators in relation to varying populations of their hosts or prey is unlikely to be simple. Early theorists sought to describe the relationship by a single constant (Lotka 1925; Volterra 1931; Thompson 1930; Nicholson 1933; Nicholson & Bailey 1935). Solomon (1949) first suggested the terms functional and numerical for more complex responses of parasites and predators to their hosts and prey. These terms have since been used by several authors, not always as they were originally defined. They are suitable for describing the effects of the host or prey density on the behaviour and reproduction of the parasite or predator concerned, but not to describe the effects of the parasitism or predation on the host or prey population. The purpose of this paper is to review some of the uses of this terminology in the literature and to introduce a new and more precise system of classifying parasite or predator responses to host or prey density. It should be added, however, that it is almost an impossible task to find any system for classifying responses of this kind that caters for all cases, and there will certainly be instances in which the proposed system of terms is unsuitable. Solomon (1949) stated that '. . . to be density dependent, the enemy must respond to changes in the numbers of host (cf. Nicholson 1933; Varley 1947). The nature of this response is commonly twofold. First, there must be a FUNCTIONAL response to (say) an increase in the host density, because of the increased availability of victims: as host density rises, each enemy will attack more host individuals, or it will attack a fixed number more rapidly. A frequent, but not invariable result of this is an increase in the numbers of the enemy (a NUMERICAL influence) due to an increased rate of survival or reproduction, or of both; this may or may not be sufficient to produce an increase in the PROPORTION of enemies to the increasing hosts'. It is important to realize that a weak functional response may be insufficient to result in density-dependent mortality, for which there must be an increase in the proportion of hosts taken by each enemy as host density increases. Likewise, a numerical response in the enemy may not produce delayed density-dependency for which a proportionate increase in the numbers of enemy compared with those of the host or prey is necessary. Holling (1959a) elaborated these terms in his study of the predation of cocoons of Neodiprion sertifer (Geoff.) by small mammals in Canada. The functional response was defined in terms of changes in the number of prey consumed by each predator, and the numerical response as changes in the predator density at different prey densities. Holling divided the functional response into three basic types and expressed them graphically by plotting the numbers of prey taken per predator per unit time as the dependent variable against the prey density (Fig. la). Similarly, the numerical response was subdivided into three types (direct, none and inverse) and expressed as the numbers of predators per unit area against prey density (Fig. 2, A, B and C). Varley & Gradwell (1963a) used these terms in a different sense and implied that functional and numerical responses resulted in density-dependent and delayed density-dependent mortalities of the host or prey. A functional response was defined as occurring when '. . . local concentrations of prey are

This work aims to evaluate the interspecific interaction between Trichogramma pretiosum and Telenomus remus, two biological control agents of fall armyworm (Spodoptera frugiperda) eggs. Eggs of Spodoptera frugiperda previously parasitized by Telenomus remus were offered to Trichogramma pretiosum, and those parasitized by Trichogramma pretiosum were offered to Telenomus remus. The previously parasitized eggs were tested at different embryonic development stages for each parasitoid. In addition, to evaluate the competition between species, Spodoptera frugiperda eggs were offered to the parasitoids simultaneously. The behavior of the insects was recorded under a stereomicroscope. When Spodoptera frugiperda eggs were previously exposed to either parasitoid, there was no emergence of the other parasitoid. When the Telenomus remus and Trichogramma pretiosum females were placed together with Spodoptera frugiperda eggs, Telenomus remus had a greater parasitism rate. Except searching time, all Trichogramma pretiosum behaviors took a longer time than Telenomus remus behaviors. Thus, despite belonging to different families, each of these parasitoids is able to recognize host eggs previously parasitized by the other. So, this suggests that the recognition mechanism involved is not exclusively specific.

Functional response of Telenomus remus Nixon (Hymenoptera, Scelionidae) to Spodoptera frugiperda (J. E. Smith) (Lepidoptera, Noctuidae) eggs: effect of female age. Functional response of 24-h and 48-h-old Telenomus remus adults was studied on Spodoptera frugiperda eggs. The study was carried out in climatic chamber regulated at 25 ± 1°C, 70 ± 10% RH and 12:12h (L: D). Females of T. remus were honey fed and individualized in glass vials along with 25, 50, 75, 100, 150, 200, 250 or 300 eggs of S. frugiperda for 24 h. Complete randomized design with ten replications was adopted. The parameters evaluated to construct the functional response curve were daily average parasitism, searching rate and oviposition time. It was observed that the higher the egg density, the higher the parasitism for 24-h and 48-h-old females although there was a tendency of parasitism stabilization at 150-egg density. The results showed a type II functional response curve for both 24-h and 48-h-old female.

Functional response and progeny production of the Madeira mealybug parasitoid, Anagyrus sp. nov. nr. sinope: The effects of host and parasitoid densities

The possibility of imperfect coincidence between the appropriate stages of Neodiprion sertifer (Geoff.) and two of its important parasites was demonstrated. One of the parasites, the indigenous ichneumonid Exenterus canadensis Prov., which attacks late-stage larvae, has good spatial coincidence; but some members of each generation suffer from imperfect temporal coincidence, or asynchrony, caused by the interaction of temperature influence on parasite development rate and temperature variability between development sites in the litter. The second parasite, Pleolophus basizonus (Grav.), is an introduced, multivoltine ichneumonid cocoon parasite. It may be imperfectly synchronized in its first generation each year and may show imperfect spatial coincidence in all generations through its inability to attack host cocoons beneath approximately 1 in. or more of litter.The intricate relations between parasite and host density, time, attack, and coincidence were investigated using the basic functional response submodel developed by Holling, a submodel that describes changes in oviposition behaviour with time, and a submodel that predicts the number of hosts attacked, given the number of eggs laid and data on the distribution of eggs among hosts. In the two species studied, the effect of asynchrony in one generation cannot be considered without considering the influence of superparasitism. At low host densities, superparasitism largely buffers the effects of decreased synchrony. This buffering effect decreases as host density increases until when each parasite is attacking all the hosts it can, it is almost eliminated. Imperfect spatial coincidence in one generation merely lowers the usable host density. Thus its effect can be seen in the functional response of the parasite to host density. When host–parasite interactions over 25 to 35 host generations were simulated, using initial conditions resembling those ensuing when small numbers of both host and parasite invade a previously unattacked stand, populations became stable after passing through one or more oscillations. Decreasing temporal or spatial coincidence increased host and parasite densities at the peaks of oscillations and increased the ultimate steady density of host and parasite, until coincidence was reduced to nearly half. At this level, the host escaped the regulating ability of both species of parasites.

The functional and numerical responses, reproductive characteristics, and viability of Campoletis flavicincta (Hymenoptera: Ichneumonidae) as well as the mortality after parasitism of the host Spodoptera frugiperda (Lepidoptera: Noctuidae) were analyzed in the laboratory. Campoletis flavicincta pairs were maintained until female death with 10, 20, 30, 40, or 50 caterpillars day-1 of the host S. frugiperda. A type III functional response curve was fitted to the average number of caterpillars supplied per day during the female wasp lifespan, as the explanatory variable. The handling time was 0.5940 ± 0.0875h, and the instantaneous search 0.0047 ± 0.0020 h-1. The functional response for each of the first five days of the host was a type III. The longevity at the five host densities and the parasitism rate showed a significant linear decrease with the host density. The offspring production showed an increasing quadratic variation with increased host density. The production of females by C. flavicincta, the offspring sex ratio, the viability of the parasitoid pupae and the percentage of mortality of S. frugiperda caterpillars were not affected by host density. The functional and numerical responses of C. flavicincta indicate that this parasitoid could be a candidate for biological control of S. frugiperda.

Parasitism of the glassy-winged sharpshooter, Homalodisca coagulata (Homoptera: Cicadellidae): Functional response and superparasitism by Gonatocerus ashmeadi (Hymenoptera: Mymaridae)

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 ofCales,Eretmocerus, andTrichogramma.

Abstract: Release of egg parasitoids for biological control of pests is a promising technique in integrated pest management (IPM). However, there is a lack of information on the performance of parasitoid females of different ages, and specifically on the behavior of the parasitoid Telenomus remus towards pest eggs at different stages of embryonic development. Thus, the relationships between host age, parasitoid age, and parasitism by T. remus on Spodoptera frugiperda eggs were evaluated. Three separate bioassays were performed, each in a completely randomized design. In the first bioassay, T. remus females grouped by age in days (ranging from 1 to 10 days old) were offered 100 ± 20 eggs of S. frugiperda for 24 hours. In the second bioassay, 100 ± 20 eggs of S. frugiperda (24, 48 or 72 hours old) were offered to females of T. remus for 24 hours. In the third bioassay, 24, 48- and 72-hour-old host eggs of S. frugiperda were offered to T. remus females in a choice test. The variables evaluated were: number of parasitized eggs, parasitoid emergence (%), and sex ratio of progeny in bioassays 1 and 2, and the number of eggs parasitized in bioassay 3. The age of T. remus females did not affect the number of S. frugiperda eggs parasitized or emergence of the progeny. However, the sex ratio was more male-biased in the progeny of 1- and 2-day-old females compared to older wasps. In bioassay 2, the highest parasitism was observed in 24- and 48-hour-old eggs. Percentage emergence and sex ratios were not influenced by the ages of the eggs tested. Telenomus remus preferred to parasitize 24-hour-old eggs in bioassays 3. Overall, the age of T. remus females tested did not affect the parasitism of S. frugiperda eggs, but the number of eggs parasitized decreased with increasing host age.

Anastrepha fraterculus (Wiedemann) (Diptera: Tephritidae) is a significant fruit pest of economic and quarantine importance in South America. Biological control using augmentative releases of parasitoids or conservation strategies for these natural enemies are handy tools in integrated fruit fly management programs. The functional response describes the natural enemy consumption rate with increasing resource density. Such information may be relevant for selecting the parasitoid species that is potentially most suitable to serve as a biocontrol agent of A. fraterculus. Furthermore, the number of discarded hosts determined from functional response analysis might be used to estimate suitable host densities, avoiding wastage of larvae/puparia associated with host overproduction. Therefore, the current study aimed to evaluate the functional response of four Neotropical-native parasitoid species commonly associated with species of the Anastrepha genus in the Americas, such as the pupal parasitoid Coptera haywardi (Ogloblin) (Hymenoptera: Diapriidae) and the larval parasitoids Ganaspis pelleranoi (Brèthes) (Hymenoptera: Figitidae), Doryctobracon crawfordi (Viereck), and Opius bellus Gahan (Hymenoptera: Braconidae). The package "frair" from R software was used to determine the functional response type and parameter estimation, enabling selection, fitting, and comparison among standard functional response models and integral parameters. Four relevant conclusions can be highlighted: (a) G. pelleranoi showed a flexible functional response, with a statistically significant deviation to a Type III rather than a Type II response found among the three other parasitoid species; (b) G. pelleranoi had a handling time significantly lower than the other tested parasitoid species; (c) the number of attacked hosts varied among all four parasitoid species, with C. haywardi and G. pelleranoi exhibiting the highest proportion of attacks at low and high host densities, respectively; and (d) the percentage of discarded hosts was significantly low at 1-5 and 1-20 hosts per parasitoid in C. haywardi and G. pelleranoi, respectively, whereas in both D. crawfordi and O. bellus, it was high at any offered host density. Results provide helpful comparative information about the possible performance of these species as biocontrol agents against A. fraterculus populations within augmentative and/or conservative biological control programs.

Effect of host density and location on the percentage parasitism, fertility and induced mortality of Aganaspis daci (Hymenoptera: Figitidae), a parasitoid of Ceratitis capitata (Diptera: Tephritidae)

Telenomus remus (Nixon) (Hymenoptera: Scelionidae), is an endoparasitoid on eggs of Spodoptera frugiperda (J. E. Smith). T. remus information as a natural enemy of S. frugiperda is limited. The research objective was to determine some biological aspects of T. remus, i.e., longevity, fecundity, and life table variables. The demographic statistics used the jackknife method. The parasitoids were obtained from the eggs of S. frugiperda from a maize plantation in the field. The released parasitoids were identified in the laboratory. Parasitoid identified as T. remus used to biological observations, life tables, sex ratios, and parasitization rate. The immature stage of T. remus reached 8.13 days, the longevity of the male was 10.07 days, while a female was 10.29 days with a fecundity of 75 eggs, and a sex ratio of male and female was 1:2.03. The life table parameters of T. remus, i.e., gross reproduction rate (GRR) was 74.987 individuals/generation, net reproduction rate (R0) was 67.485 females/female/generation, with generation period (T) was 8.541 days, and intrinsic growth rate (r) was 0.493 females/female/day. The Parasitization rate of T. remus reaches 91%. This research showed that T. remus has the potential natural enemy to control S. frugiperda.

The fecundity, reproductive rate, and survival of Lysiphlebia mirzai parasitising third instar nymphs of the cereal aphid Rhopalosiphum maidis were measured at six different host densities under constant laboratory conditions. The survival rate (lx) of the female parasitoids was unaffected by host density, with an average adult life‐span of 5–6 days at all densities. The age‐specific fecundity rate (mx) was host density‐dependent. The value of mx decreased rapidly from the first day of parasitisation. The number of hosts available determined the maximum possible number of mummies. At 200 hosts available per day, the average fecundity was 184.6 mummies/female; the maximum number of mummies yielded by any female was 200. The relationship between host density and the number of aphids parasitised per female was linear at ≤50 aphids/cage/day, but at higher host densities (≥100 aphids/cage/day) a significant curvilinear regression was observed. The intrinsic rate of natural increase (rm) increased with increasing host density. Maximum value of rm (0.262) was obtained at a host density of 200. The response of rm to changes in host density and parasitoid sex ratio is shown. A typical type II functional response was observed for L. mirzai. The curve was described by a logistic curve, Np = 200/[1 + exp(5.65 − 1.60 ln No)]. The search rate of the parasitoid was inverse host density‐dependent. No significant variation in the sex ratio of F1 offspring was observed at different initial host densities. Sex ratio values exceeded 0.5 at all host densities. The results evaluated the reproductive potential of L. mirzai as a promising biological control agent.

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.

Summary The functional response to, and preference for, the host density in a parasite were examined experimentally using an icheumon wasp, Exidechthis canescens, and its host Cadra cautella under controlled conditions. Wasps were more active in host‐searching at higher than lower host densities. Percent parasitism increased rapidly with initial increments in host density and then tended to increase more slowly at higher host densities. A sigmoid functional response curve is indicated, which implies that the parasite is able to control its host even at low densities. Wasps actively selected areas of high host density in which to concentrate host‐searching behavior. Host‐searching by E. canescens is stimulated by the odor of the host when present, and by food in which hosts have developed but have been removed. Both the functional response and the host‐density preference of the parasite are mediated by its host‐searching behavior. This relationship is discussed in the context of population regulation.