Intrinsic and extrinsic competitive interactions between two larval parasitoids of Heliothis virescens

1. Competition between parasitoid species may be a key factor in the community dynamics of plant–herbivore-parasitoid systems and is an important consideration in the selection and management of effective biological control agents. 2. Interspecific competition can occur between adult parasitoids searching for hosts (extrinsic competition) and between multiple parasitoid larvae developing within a single host individual (intrinsic competition). A model system comprising the lepidopteran pest Heliothis virescens and two key hymenopteran endoparasitoids, Microplitis croceipes and Cardiochiles nigriceps, was employed to explore parasitoid host-location strategies and the consequences of intrinsic and extrinsic competitive interactions between parasitoid species. 3. The less specialised of the two parasitoids, M. croceipes, was found to have a shorter hatching time and to dominate intrinsic competition, except when its oviposition followed that of the more specialised parasitoid, C. nigriceps, by 16 h or more. This interval corresponded to the differential in hatching time between the two species. 4. Cardiochiles nigriceps, however, displayed superior host-searching efficiency that may compensate for its disadvantage in intrinsic competition. This parasitoid was more effective at detecting host infestation sites via airborne odours and at locating and attacking early instar host larvae than was M. croceipes.     

Differential electroantennogram response of females and males of two parasitoid species to host-related green leaf volatiles and inducible compounds

Parasitoids employ different types of host-related volatile signals for foraging and host-location. Host-related volatile signals can be plant-based, originate from the herbivore host or produced from an interaction between herbivores and their plant host. In order to investigate potential sex- and species-related differences in the antennal response of parasitoids to different host-related volatiles, we compared the electroantennogram (EAG) responses of both sexes of the specialist parasitoid, Microplitis croceipes (Cresson), and the generalist, Cotesia marginiventris (Cresson), to varying doses of selected plant-based host-related volatiles: two green leaf volatiles (cis-3-hexenol and hexanal) and three inducible compounds (cis-3-hexenyl acetate, linalool, and (E,E)-alpha-farnesene). Mating had no significant effect on EAG response. Females of both species showed significantly greater EAG responses than conspecific males to green leaf volatiles, which are released immediately after initiation of herbivore feeding damage. In contrast, males showed greater responses than conspecific females to inducible compounds released much later after initial damage. Cotesia marginiventris females and males showed greater EAG responses than counterpart M. croceipes to the tested compounds at various doses, suggesting that the generalist parasitoid shows greater antennal sensitivity than the specialist to the tested host-plant volatiles. These results are discussed in relation to the possible roles of green leaf volatiles and inducible compounds in the ecology of female and male parasitoids.     

Analyses of Two Parasitoids with Convergent Foraging Strategies

We compared the foraging strategies of two key braconid endoparasitoids of the tobacco budworm (Heliothis virescens Fab.), Cardiochiles nigriceps Vier. and Microplitis croceipes Cresson, that differ in host and habitat range but otherwise share comparable, overlapping niches. The most important host-location cues by far for both species were materials associated with damaged plants. Both species demonstrated a significant preference for volatiles released from plants damaged by H. virescens larvae over those released from undamaged tobacco and cotton plants. In choice experiments with damaged tobacco versus cotton, M. croceipes showed a significant preference for cotton plants. In contrast, C. nigriceps preferred damaged tobacco plants. Plant compounds provoked a strong response even when released from systemically induced plants (from which damaged leaves, host, and host by-products were removed). C. nigriceps appears to have a much keener ability to locate hosts over long distances than M. croceipes. This observation may be related to the highly specialized nature of this parasitoid. The possible adaptive significance of the foraging behaviors of these two parasitoids is discussed.     

The role of herbivore‐ and plant‐related experiences in intraspecific host preference of a relatively specialized parasitoid

Parasitoids use odor cues from infested plants and herbivore hosts to locate their hosts. Specialist parasitoids of generalist herbivores are predicted to rely more on herbivorederived cues than plant-derived cues. Microplitis croceipes (Cresson)(Hymenoptera: Braconidae) is a relatively specialized larval endoparasitoid of Heliothis virescens (F.)(Lepidoptera: Noctuidae), which is a generalist herbivore on several crops including cotton and soybean. Using M. croceipes/H. virescens as a model system, we tested the following predictions about specialist parasitoids of generalist herbivores:(i) naive parasitoids will show innate responses to herbivore-emitted kairomones, regardless of host plant identity and (ii) herbivore-related experience will have a greater influence on intraspecific oviposition preference than plant-related experience. Inexperienced (naive) female M. croceipes did not discriminate between cotton-fed and soybean-fed H. virescens in oviposition choice tests, supporting our first prediction. Oviposition experience alone with either host group influenced subsequent oviposition preference while experience with infested plants alone did not elicit preference in M. croceipes, supporting our second prediction. Furthermore, associative learning of oviposition with host-damaged plants facilitated host location. I terestingly, naive parasitoids attacked more soybeathan cotton-fed host larvae in two-choice tests when a background of host-infested cotton odor was supplied, and vice versa. This suggests that plant volatiles may have created an olfactory contrast effect. We discussed ecological significance of the results and concluded that both plant- and herbivore-related experiences play important role in parasitoid host foraging.     

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.     

Avoidance of the host immune response by a generalist parasitoid, Compsilura concinnata Meigen

Abstract.  1. Ecological interactions between parasitoids and their hosts are extremely strong as parasitoid offspring rely entirely on an individual host to complete development. The ability of a parasitoid to use a host is influenced directly by the degree to which the parasitoid can overcome host defences and grow within the host.
2. Hymenopteran parasitoids have evolved different host-specific strategies to defeat the host immune system, such as the use of venom, endosymbiont virus, or mimicking the host tissue. Dipteran parasitoids from the Tachinidae family do not use these subterfuges and rely mainly on avoiding the host immune system by hiding in specific tissues.
3. Little is known of the effect of this strategy on the host immune system, the absorption of nutrients by the parasitoid larvae, or the implications for parasitoid host range.
4. In this study, the impact of a polyphagous tachinid parasitoid Compsilura concinnata Meigen on a pest lepidopteran Trichoplusia ni Hübner are assessed. Phenoloxidase levels and haemolymph proteins were measured in parasitised T. ni as a function of host immune response.
5. Haemolymph phenoloxidase in the host did not vary with parasitisation but was triggered when a piece of monofilament was implanted in the haemocoel. Haemolymph proteins were depleted in heavily parasitised T. ni .
6. These results indicate that C. concinnata has a strategy that avoids the host immune system, and accesses the necessary nutrients for larval growth. This strategy could explain the success of this tachinid and its wide host range.     

Age-dependent clutch size in a koinobiont parasitoid

Abstract.  1. The Lack clutch size theory predicts how many eggs a female should lay to maximise her fitness gain per clutch. However, for parasitoids that lay multiple clutches it can overestimate optimal clutch size because it does not take into account the future reproductive success of the parasitoid.
2. From egg-limitation and time-limitation models, it is theoretically expected that (i) clutch size decreases with age if host encounter rate is constant, and (ii) clutch size should increase with host deprivation and hence with age in host-deprived individuals.
3. Clutch sizes produced by ageing females of the koinobiont gregarious parasitoid Microplitis tristis Nees (Hymenoptera: Braconidae) that were provided daily with hosts, and of females ageing with different periods of host deprivation were measured.
4. Contrary to expectations, during the first 2 weeks, clutch size did not change with the age of the female parasitoid, neither with nor without increasing host-deprivation time.
5. After the age of 2 weeks, clutch size decreased for parasitoids that parasitised hosts daily. The decrease was accompanied by a strong decrease in available eggs. However, a similar decrease occurred in host-deprived parasitoids that did not experience egg depletion, suggesting that egg limitation was not the only factor causing the decrease in clutch size.
6. For koinobiont parasitoids like M. tristis that have low natural host encounter rates and short oviposition times, the costs of reproduction due to egg limitation, time limitation, or other factors are relatively small, if the natural lifespan is relatively short.
7. Koinobiont parasitoid species that in natural situations experience little variation in host density and host quality might not have strongly evolved the ability to adjust clutch size.     

Learning and the role of host-specific volatiles during in-flight host-finding in the specialist parasitoid Microplitis croceipes

Abstract The effect of antennal contact with host-related stimuli on the subsequent flight response to host-specific volatiles was examined in the specialist parasitoid, Microplitis croceipes (Cresson) (Hymenoptera: Braconidae). In a choice test between two species of caterpillars feeding on cowpea, free-flying female M.croceipes lacking prior contact with host cues landed more often on sources of odour from its host, Heliothis tea (Boddie), than from non-host Spodoptera frugiperda (Smith). After female parasitoids contacted host cues with their antennae, more landings on sources containing hosts were observed only when caterpillars used in the pre-flight treatment and in the odour sources fed on the same plant species. The degree to which host-experienced wasps landed more often on hosts as compared with non-hosts varied with host-instar and plant species. The role of learning in host finding in specialist parasitoids is discussed.     

Parasitic wasps learn and report diverse chemicals with unique conditionable behaviors

Parasitoids exploit numerous chemical cues to locate hosts and food. Whether they detect and learn chemicals foreign to their natural history has not been explored. We show that the parasitoid Microplitis croceipes can associate, with food or hosts, widely different chemicals outside their natural foraging encounters. When learned chemicals are subsequently detected, this parasitoid manifests distinct behaviors characteristic with expectations of food or host, commensurate with prior training. This flexibility of parasitoids to rapidly link diverse chemicals to resource needs and subsequently report them with recognizable behaviors offers new insights into their foraging adaptability, and provides a model for further dissection of olfactory learning related processes.     

Does mother really know best? Oviposition preference reduces reproductive performance in the generalist parasitoid Aphidius ervi

The reproductive success of female parasitoids is dependent on their ability to accurately assess the suitability of a host for larval development. For generalist parasitoids, which utilize a broad range of species and instars as hosts, a set of assessment criteria determines whether a host is accepted or rejected. The suitability of a host, however, can only be imperfectly assessed by the female parasitoid, which can result in the selection of lesser quality hosts for oviposition. In this study we explored the disparity between host quality and host preference using the generalist koinobiotic parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae) and the host Aulacorthum solani (Harris) (Homoptera: Aphididae), the foxglove aphid. The second instar hosts produced the highest level of reproductive success, while third and fourth instars resulted in a substantially reduced reproductive performance. When given a choice of host instars, parasitoids preferred the older hosts for oviposition disregarding their reduced suitability for larval development. Results are discussed in context of mechanisms involved in A. ervi host selection and biases in the criteria used to assess hosts that may arise when parasitoids transfer host species between generations.     

Host age and fitness-related traits in a koinobiont aphid parasitoid

Abstract.  1. Trade-offs play a key role in species evolution and should be found in host–parasitoid interactions where the host quality may differ between host age categories.
2. The braconid wasp, Aphidius ervi , is a solitary endoparasitoid that allows its aphid hosts to continue to feed and grow after parasitisation. The hypotheses that host age influences their quality and that female parasitoids exploit their hosts based on that quality were tested under laboratory conditions using no-choice tests.
3.  Aphidius ervi females accepted the aphid Myzus persicae for oviposition and their progeny developed successfully in all host ages. The fitness-related traits of parasitoids did not increase linearly with the host age in which they developed. Host quality was found to be optimal at intermediate host ages and the females preferred to parasitise these hosts. The shortest progeny development time and a more female-biased sex ratio were observed in hosts of intermediate age.
4. This study suggests the existence of multiple interactive trade-offs occurring during host–parasitoid interactions according to host age related quality.     

Choosy egg parasitoids: Specificity of oviposition-induced pine volatiles exploited by an egg parasitoid of pine sawflies

Generalist parasitoids are well‐known to be able to cope with the high genotypic and phenotypic plasticity of plant volatiles by learning odours during their host encounters. In contrast, specialised parasitoids often respond innately to host‐specific cues. Previous studies have shown that females of the specialised egg parasitoid Chrysonotomyia ruforum Krausse (Hymenoptera: Eulophidae) are attracted to volatiles from Pinus sylvestris L. induced by the egg deposition of its host Diprion pini L. (Hymenoptera: Diprionidae), when they have previously experienced pine twigs with host eggs. In this study we investigated by olfactometer bioassays how specifically C. ruforum responded to oviposition‐induced plant volatiles. Furthermore, we studied whether parasitoids show an innate response to oviposition‐induced pine volatiles. Naïve parasitoids were not attracted to oviposition‐induced pine volatiles. The attractiveness of volatiles from pines carrying eggs was shown to be specific for the pine and herbivore species, respectively (species specificity). We also tested whether not only oviposition, but also larval feeding, induces attractive volatiles (developmental stage specificity). The feeding of D. pini larvae did not induce the emission of P. sylvestris volatiles attractive to the egg parasitoid. Our results show that a specialist egg parasitoid does not innately show a positive response to oviposition‐induced plant volatiles, but needs to learn them. Furthermore, the results show that C. ruforum as a specialist does not learn a wide range of volatiles as some generalists do, but instead learns only a very specific oviposition‐induced plant volatile pattern, i.e., a pattern induced by the most preferred host species laying eggs on the most preferred food plant.     

Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size

Abstract.  1. Many studies examining the relationship between host size, an index of host quality, and parasitoid fitness use development time and/or adult parasitoid size as currencies of fitness, while ignoring pre-adult mortality. Because the physiological suitability of the host may vary in different stages, sizes, or ages of hosts, a misleading picture of host quality may therefore be obtained in cases where fitness is based on only one or two developmental traits.
2. The development of the solitary koinobiont endoparasitoid Microplitis demolitor is examined in different larval age-classes of its host the soybean looper Pseudoplusia includens . Hosts were parasitised on days 1–8 after hatching from the egg, and development time, adult body size, and mortality of the parasitoid were compared.
3. A comparison of larval growth trajectories (using dry body mass) of M. demolitor revealed that parasitoid larvae attained over twice as much body mass in old hosts than in younger hosts. Similarly, adult parasitoid size at eclosion generally increased with host size, although parasitoids developing in smaller hosts lost a much lower proportion of mass between pupation and eclosion.
4. Overall egg-to-adult development was most rapid in intermediate-aged hosts, and longer in hosts at opposite ends of the age continuum. Moreover, parasitoid mortality varied non-linearly with host stage, and was generally higher in very young and older hosts.
5. Based on these results and other empirical data for koinobionts, it is argued that fitness functions in this group of parasitoids are not simply a positive function of host size or age, but instead may be distinctly dome-shaped, both patterns reflecting the degree of physiological and nutritional compatibility between the two organisms.     

Combining pheromone-baited and food-baited traps for insect pest control: Effects of additional control by parasitoids

Two age-structured population dynamic models are analyzed in which pheromone-baited trapping and food-baited trapping are used simultaneously to eradicate an insect pest. The pest species is assumed to be under partial control by a host-specific parasitoid species. The two models assume that density-dependent population regulation is accomplished either by host larval competition or by means of oviposition interference among the parasitoids. The two trap types interact in a positive synergistic manner and this combination appears to be very promising as a useful combination of pest control methods. Several features of the system are examined; the feature which appears to cause the greatest problem is the possibility of the parasitoids being attracted to the pheromone or the food traps. In either case, the degree of attraction does not have to be very great to undermine the control effort. It is seen that food trapping becomes indispensible if host pheromone is used by the parasitoids as a host-locating kairomone. If odor in the food traps is used by the parasitoids as kairomone, then the situation appears more optimistic, as the reduction in efficiency of the food traps appears much less than with the pheromone traps when pheromone acts as kairomone.     

Discrimination of previously searched,host-free sites byMicroplitis croceipes (Hymenoptera: Braconidae)

The ability of free- ranging parasitoids to discriminate between previously visited and unvisited sites containing host kairomone (caterpillar frass) but not hosts was tested. Females of Microplitis croceipes,a host specialist and plant generalist larval parasitoid of Helicoverpa (Heliothis) zea,were allowed to fly freely in a simulated plant patch in a flight chamber. Wasps spent less time searching frass sites previously searched by themselves or by conspecifics than unsearched frass sites. In addition to chemical marking, spatial memory of visual cues was implicated as a mechanism for discriminating against self-visited, host-free sites.     

Interaction of a solitary larval endoparasitoid, Microplitis mediator, with its host, Mamestra brassicae: host acceptance and host suitability

Abstract:  Microplitis mediator (Haliday) (Hym., Braconidae) is an important parasitoid of early instar larvae of the European cabbage moth, Mamestra brassicae L. (Lep., Noctuidae). In the laboratory, we examined attack responses of female M. mediator to the first three larval instars of M. brassicae . Females were presented with M. brassicae larvae either one individual at a time in a no-choice experiment, or three individuals, one from each instar, simultaneously in a choice experiment. Whether or not there was choice, naïve female parasitoids attacked a high proportion of larvae and did not discriminate among instars. In the no-choice experiment, attacked larvae were reared, and parasitoid cocoons were produced from about 76% of larvae attacked as first and second instars, but from only 19% of larvae attacked as third instars. Dissections of attacked larvae from the choice experiment showed that about 79% of attacks on first and second instars resulted in oviposition compared with only 49% for third instars. When given choice, frequency and number of attacks on first instar larvae increased with increasing parasitoid experience. Our results suggest that first and second instar larvae of M. brassicae are suitable hosts for M. mediator , but that third instar larvae are suboptimal both because oviposition attempts were frequently unsuccessful and because immature parasitoids failed to complete development. Nevertheless, naïve attacking parasitoids exhibited minimal discrimination among instars, although experienced parasitoids most frequently attacked first instar larvae. The host selection behaviour of M. mediator is discussed in the context of optimal foraging theory and implications for biological control.     

The effect of molecular structure on olfactory discrimination by the parasitoid Microplitis croceipes

Flight chamber experiments were conducted to examine the capacity of the larval parasitoid Microplitis croceipes (Hymenoptera: Braconidae) to learn to distinguish between structurally related aliphatic alcohols differing in the carbon chain-length and the position of the functional group, and between an alcohol and the respective aldehyde. The parasitoid's ability to discriminate between the components depended on the chain-length of the alcohol to which they had been conditioned. Discrimination improved with increasing difference in carbon chain-length, e.g. the parasitoids made clear distinction between 1-hexanol and 1-octanol. Microplitis croceipes could also distinguish different isomers of six-carbon alcohols on the basis of the position of the alcoholic group as well as between 1-hexanol and 1-hexanal. The learning abilities of M. croceipes correspond to the specificity of antennal odour receptors towards aliphatic alcohols and aldehydes in previous electrophysiological studies of M. croceipes and other insects. Differences in perception or processing of single compounds might reflect differences of their ecological relevance.     

Coexistence of multiple parasitoids on a single host due to differences in parasitoid phenology

There are many well-documented cases in which multiple parasitoids can coexist on a single host species. We examine a theoretical framework to assess whether parasitoid coexistence can be explained through differences in timing of parasitoid oviposition and parasitoid emergence. This study explicitly includes the phenology of host and parasitoid development and explores how this mechanism affects the population dynamics. Coexistence of the host with two parasitoids requires a balance between parasitoid fecundity and survival and occurs most readily if one parasitoid attacks earlier but emerges later than the other parasitoid. The host density can either be decreased or increased when a second coexisting parasitoid is introduced into the system. However, there always exists a single parasitoid type that is most effective at depressing the host density, although this type may not be successful due to parasitoid competition. The coexistence of multiple parasitoids also affects the population dynamics. For instance, population oscillations can be removed by the introduction of a second parasitoid. In general, subtle differences in parasitoid phenology can give rise to different outcomes in a host–multi-parasitoid system, and this may offer some insight into why establishing criteria for the ‘ideal’ biological control agent has been so challenging.     

Heterospecific ovicide influences the outcome of competition between two endoparasitoids, Encarsia formosa and Encarsia luteola

Abstract.  1. Studies of inter-specific competition in parasitoids have largely focused on the outcome of within-host competition and the behavioural mechanisms by which female parasitoids prevent competition. Another, less well studied, possibility is oviposition preceded by 'heterospecific ovicide', the destruction of the other species' egg. Heterospecific ovicide essentially eliminates within-host competition.
2. This study investigated the mechanisms and outcome of within-host competition in Encarsia formosa and Encarsia luteola , solitary endoparasitoids of whitefly pests. These species are known to commit ovicide of conspecific eggs.
3. Competition experiments indicated that the offspring of second-ovipositing females had an apparent advantage in competition, regardless of whether the second female was E. formosa or E. luteola .
4. Observations of ovipositor movement through the cuticle of host whitefly nymphs showed that both species often committed heterospecific ovicide and then oviposited or host-fed. Multiparasitism and heterospecific host discrimination were less common and absent respectively.
5. Heterospecific ovicide appears to explain the second-female advantage in competition between these species. Second-female advantage is contrary to the paradigmatic view of multiparasitism, where the first-ovipositing female has an advantage in competition or one of the species consistently prevails in competition.     

Temporal variation and the evolution of a parasitoid foraging cue

This work details theory in which selection favors generalists in a more variable environment. Specifically, in a two-host-one-parasitoid model, temporal variation in host abundances alters the optimal searching strategy and leads to the evolution of more generalist parasitoid strategies. Consistent with empirical observations, parasitoids learn host/plant odors, and use them as a cue to search for oviposition sites. The amount of unsuccessful search time required before a parasitoid alters its searching cues (the "giving-up time") is modeled in order to understand the evolutionarily optimal giving-up times under a variety of conditions. When host abundances vary across time, a generalist parasitoid strategy evolves with short giving-up times as it is likely that the host initially favored by a parasitoid will now have a low abundance. In contrast, when populations reach stable dynamics across time, giving-up times typically evolve to longer times, i.e. parasitoids remain specialized longer. The effect of temporal fluctuations is consistent across variation caused by endogenous population interactions and, to some degree, by environmental stochasticity. The conclusions are robust in that there is a strong degree of concordance between the results of a stochastic, individual-based model and a deterministic, numerical model. As an extension, spatial variation in hosts that leads to unequal tradeoffs between generalist parasitoids and specialist parasitoids may also result in the evolution of reduced giving-up times.