Density-dependent foraging behaviors in a parasitoid lead to density-dependent parasitism of its host

Empirical studies of spatial heterogeneity in parasitism by insect parasitoids have focused largely on patterns, while the many possible underlying mechanisms have been little studied in the field. We conducted experimental and observational studies on Tachinomyia similis (Diptera: Tachinidae) attacking western tussock moths (Orgyia vetusta; Lepidoptera: Lymantriidae) on lupine bushes at Bodega Bay, Calif., USA. We examined several foraging behaviors that have been hypothesized to create density-dependent variation in parasitism rates, including spatial aggregation of parasitoids to high host density, mutual interference among searching parasitoids and decelerating functional responses of the parasitoid. At the spatial scale of individual bushes, we detected both aggregation to a high density and a decelerating functional response. The resulting spatial pattern of parasitism was best fit by two models; one included an effect of parasitoid aggregation and the other included an effect of aggregation and a decelerating functional response. Most of the variation in parasitism was not correlated with density of O. vetusta.     

Response of insect parasitism to elevation depends on host and parasitoid life-history strategies

How global warming will affect insect parasitoids and their role as natural enemies of insect pests is difficult to assess within a short period of time. Considering that elevation gradients can be used as analogues for global warming, we carried out meta-analyses of 27 correlations between parasitoid richness and elevation and 140 correlations between parasitism rate and elevation in natural and semi-natural environments. We also explored various covariates that may explain the observed responses. Both parasitism rates and parasitoid species richness significantly decreased with increasing elevation. The decrease was greater for ectoparasitoids and parasitoids of ectophagous insects than for endoparasitoids and parasitoids of endophagous hosts, possibly because these latter are better protected from adverse and extreme climatic conditions occurring at higher elevations. Although our results suggest an increase of parasitism with increasing temperature, other factors regulating herbivorous insects have to be considered before concluding that climate warming will lead to a decrease in pest density.     

Nectar provisioning close to host patches increases parasitoid recruitment,retention and host parasitism

In the adult stage, many parasitoids require hosts for their offspring growth and plant-derived food for their survival and metabolic needs. In agricultural fields, nectar provisioning can enhance biological control by increasing the longevity and fecundity of many species of parasitoids. Provided in a host patch, nectar can also increase patch quality for parasitoids and affect their foraging decisions, patch time residence, patch preference or offspring allocation. The aim of this study was to investigate the impact of extrafloral nectar (EFN) provisioning close to hosts on parasitoid aggregation in patches. The aphid parasitoid Diaeretiella rapae (M’Intosh) was released inside or outside patches containing Brassica napus L. infested by Brevicoryne brassicae L. aphids and Vicia faba L. with or without EFN. When parasitoids were released outside patches, more parasitoids were observed in patches with EFN than in patches deprived of EFN. This higher recruitment could be linked to a higher attraction of a combination of host and food stimuli or a learning process. A release–recapture experiment of labeled parasitoids released within patches showed the higher retention of parasitoids in patches providing EFN and hosts, suggesting that food close to the host patch affects patch residence time. Both attractiveness and patch retention could be involved in the higher number of parasitoids foraging in host patches surrounded by nectar and for the higher parasitism recorded. Nectar provisioning in host patches also affected female offspring allocation inside the patch.     

Structure,organization, and response of a species-rich parasitoid community to host leafminer population dynamics

The parasitoid community dynamics of an agromyzid honeysuckle leafminer, Chromatomyia suikazurae (Agromyzidae, Diptera) were studied between 1981 and 1990 in a natural forest in Kyoto, Japan. The parasitoid fauna composed three koinobionts (all larval-pupal solitary parasitoids) and 22 idiodiont species (11 larval solitary, nine pupal solitary and one pupal gregarious). The parasitoid community was dominated by early-attacking oligophagous braconid koinobionts at early periods, but was gradually displaced by late-attacking polyphagous eulophid idiobionts. Accordingly, the diversity index of the parasitoid community peaked at an intermediate point in the intra-generational succession. The succeeding attack-in-waves by the late-attacking idiobionts greatly reduced not only the survival rates of early-attacking parasitoid larvae but also the survival rates of hosts. The density-dependence observed in the host pupal mortality was thought to result from density-dependent host-switching by a keystone polyphagous pupal idiobiont parasitoid, Chrysocharis pubens, whereas high host pupal mortality was potentially attained by an early-attacking koinobiont braconid. Supposed aggregation of polyphagous parasitoids at high host density resulted in intense within-host competition and in an increase of host-feeding attack, both of which contributed to low emergence rates of parasitoids at high host densities. Parasitoid emergence rates were also reduced at low host densities, probably by inter- and intra-specific hyperparasitism among oligophagous parasitoids for limited hosts. The regulation effects of the species-rich parasitoid community upon the host population dynamics are thought to derive from succeeding attack-in-waves by polyphagous late-attacking idiobionts, especially by the keystone species.     

Effects of urbanisation on the parasitoid community of a leafminer

Urbanisation may have detrimental effects on communities of parasitoids, affecting their species richness, abundance, and species dominance. Here we investigated the influence of the degree of urbanisation on parasitoid communities of Liriomyza commelinae (Frost) (Diptera: Agromyzidae), a leafminer of Commelina erecta L. (Commelinaceae), in the city of Córdoba, Argentina. To study changes in species richness, the specific composition of parasitic complexes and their degree of impact on the leafminer, 18 sampling sites from the centre to the outskirts of the city were selected and different variables indicative of urbanisation were quantified in each site. During January and February of 2005 and 2006, all mined leaves found in each plant patch were collected and the following variables were estimated: proportion of mined patches, abundance of the leafminer, total parasitoid species richness, total parasitism rates and parasitism due to the most abundant parasitoid species. The percentage of mined patches and leafminer abundance increased with urbanisation degree. Estimates of parasitoid species richness were not influenced by urbanisation degree but increased with species richness of mined plants. Changes in the specific composition of species along the urbanisation gradient were observed. Although parasitism by one of the species studied was higher in more urbanised sites of the city, the total parasitism rate of L. commelinae was not affected by urbanisation degree, species richness of mined plants or leafminer abundance. It appears that urbanisation benefits the herbivore species here studied but not through altering parasitoid activity. Changes in parasitoid community composition reflex dissimilar tolerance to environmental conditions displayed by different parasitoid species.     

Host location by a parasitoid using leafminer vibrations: characterizing the vibrational signals produced by the leafmining host

Abstract. The aim of this study was to characterize the vibrations produced by the apple tentiform leafminer Phyllonorycter malella (Ger.) (Lepidoptera, Gracillariidae). Host location using vibrations by one of its parasitoids Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae) was postulated by Casas (1989) on the basis of detailed quantitative behavioural observations and has also been suggested by other authors on similar systems. Both host and parasitoid send and may receive vibratory signals; consequently we first attempted to characterize and classify the signals, one of the first steps required in the design of an adequate vibrational biotest. In this respect, our approach differs fundamentally from the familiar setting of host location via semiochemicals and is best framed within the context of vibratory communication. Vibrational signals produced by a moving larva and pupa were measured on several spots on the leaf using a laser vibrometer. The emitted signals were characterized by their temporal patterns of change in amplitude and frequency spectra. The vibrational patterns released by a moving larva were different from those released by a wriggling larva and a wriggling pupa in the time as well as in the frequency domains. Wriggling larvae and wriggling pupae triggered vibrations that were similar in frequency, but differed in their temporal pattern. Frequencies up to 15 kHz could be identified. The amplitudes and frequencies of the signals both decreased significantly from the tip to the base of the leaf. A wriggling pupa and a wriggling larva produced stronger signals than a foraging larva. All calculated parameters (displacement, velocity, acceleration, and duration of the signal components) of the vibrational signals were found to be in a range comparable with others used for well-known arthropod communication systems. The vibrations produced by the host displayed distinct characteristics: they could usually be distinguished easily from background noise; could be perceived anywhere on the leaf; and were specific for a certain host stage and activity. Our findings support the hypothesis that vibration signals represent a reliable source of information to foraging parasitoids and, therefore, explain certain behavioural patterns observed in a population of S. sericeicornis females foraging in the field.     

Foraging behaviour of a leafminer parasitoid in the field

Abstract. 1. The searching behaviour of the parasitoid Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae) is analysed under field conditions.
2. Females were tracked when flying around the canopy of apple trees infested with the tentiform leafminer Phyllonorycter cydoniella (D. & S.)(Lepidoptera, Gracillariidae) and their behaviour studied at the level of a single mine and at the level of several mines on the same leaf (patch level).
3. The presence of mines is detected during flight. The foraging behaviour at the patch level is efficient: the female is able to distinguish the suitable from the unsuitable hosts and handle the suitable hosts first. Not all mines are visited before departure from the leaf and those left unvisited are exclusively mines without suitable hosts. The patch leaving rule is discussed.
4. An ethogram of the behaviour on the mine is constructed. Selected behavioural categories are analysed for different combinations of mine content and outcome of the visit to the mine. The assessment of the mine content is done in a differential way, quickly and without mistakes.
5. The results are discussed in the context of two environmental factors, wind speed and temperature, which reduce the available time for searching. They are also related to the growing percentage of unsuitable hosts during each host generation. Tentiform mines remain attractive for a long period of time, even after parasitism or emergence of the adult, and their examination reduces the rate of host discovery.     

Active defence of herbivorous hosts against parasitism: Adult parasitoid mortality risk involved in attacking a concealed stemboring host

Phytophagous insects have several defence strategies to defend themselves against attack by parasitic wasps. Larval lepidopteran hosts can defend themselves actively to prevent oviposition by the parasitoid. Among the aggressive kinds of behaviour exhibited by hosts against parasitoids are violent wriggling, biting and spitting. The behaviour of the braconid parasitoid Cotesia sesamiae attacking stemboring larvae inside their feeding tunnel in the plant stem was investigated in maize and sugarcane stem pieces and transparent artificial tunnels. Attacking a defending stemborer host inside the confined space of a tunnel was shown to be risky for the female parasitoid. A considerable proportion (25%) of female wasps were killed in their attempt to attack the spitting and biting host. No difference was found in the behaviour of C. sesamiae attacking the suitable host Sesamia calamistis or the unsuitable host Eldana saccharina. The consequences of this high mortality risk involved in each host attack is discussed in relation to the ecology of the parasitoid.     

Analysis of searching movements of a leafminer parasitoid in a structured environment

ABSTRACT. Pnigalio soemius (Hymenoptera, Eulophidae) is a polyphagous ectoparasitoid of the apple leafminer Phyllonorycter cydo-niella (Lepidoptera, Gracillaridae). The tracks of females searching on the unmined leaf lamina and on the mine were segmented into 2 mm steps and analysed for angle distributions and correlations between successive steps. The movements on the mine are characterized by a higher mean and higher variance of turn angles compared to the turn angles on the leaf (kinesis-reaction family). Both klinokinesis and schemakinesis, for which a more precise definition is proposed, are present. Varying the step length has a great influence on the result and can be used to identify different orientation reactions within one track. The insect turns sharply once the mine border has been reached, a behaviour shown to be a crude taxis. An ecologically related species, Sympiesis sericeicornis (Hymenoptera, Eulophidae), moves in the same way. For this species a taxis towards the host could also be observed. A complex mixture of these orientation behaviours allows the parasitoid to remain on the mine and to localise the host.     

A simple method to estimate percentage parasitism when the host and parasitoid phenologies are unknown: A statistical approach

When host and parasitoid phenologies areunknown the estimation of the generationalpercentage parasitism poses severalmethodological problems. We developed a simplemethod, based on a statistical approach, tosolve that problem. An unbiased estimator wasfound, named _CR, of thegenerational percentage parasitism, and itsperformance was tested through the analysis ofdata from two host-parasitoid systems: Phyllonorycter crataegella (Clemens)(Lepidoptera: Gracillariidae) and Sympiesis marylandensis (Girault)(Hymenoptera: Eulophidae), and Pierisrapae L. (Lepidoptera: Pieridae) and Cotesia (Apanteles) glomerata (L)(Hymenoptera: Braconidae). The _CR estimator proved to be a goodapproximation of the generational percentageparasitism, but its 95% confidence intervalwas very wide. The performance of the _CR estimator was improved and the95% confidence interval was smaller when someinformation on host and parasitoid phenologieswas added. The results suggested that thesmaller interval _CR ± onestandard deviation would contain with a greatprobability the generational percentageparasitism.     

Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness

1. The study reported here examined growth and developmental interactions between the gregarious larval koinobiont endoparasitoid Cotesia glomerata (Hymenoptera: Braconidae) and two of its hosts that vary considerably in growth potential: Pieris rapae and the larger P. brassicae (Lepidoptera: Pieridae). At pupation, healthy larvae of P. brassicae are over twice as large, in terms of fresh body mass, as those of P. rapae. 2. Clutch size of C. glomerata was manipulated artificially, and the relationship between parasitoid burden and the maximum weight of the parasitised host (= host–parasitoid complex) was measured. In both hosts, the maximum complex weight was correlated positively with parasitoid burden. Compared with unparasitised hosts, however, the growth of P. rapae was increased at significantly lower parasitoid burdens than in P. brassicae. Emerging wasp size was correlated negatively with parasitoid burden in both host species, whereas development time was less affected. 3. After larval parasitoid egress, the weight of the host carcass increased slightly, but not significantly, with parasitoid burden, although there was a strong correlation between the proportion of host mass consumed by C. glomerata larvae during development and parasitoid burden. 4. Clutch size was generally correlated positively with instar parasitised in both hosts, and greater in P. brassicae than in P. rapae. Sex ratios were much more female biased in L1 and L2 P. rapae than in all other host classes. Adult parasitoid size was correlated inversely with host instar at parasitism, and wasps emerging from P. brassicae were larger, and completed development faster, than conspecifics emerging from P. rapae. 5. The data reveal that parasitism by C. glomerata has profound species‐specific effects on the growth of both host species. Consequently, optimality models in which host quality is often based on host size at parasitism or unparasitised growth potential may have little utility in describing the development of gregarious koinobiont endoparasitoids. The results of this investigation are discussed in relation to the potential effectiveness of gregarious koinobionts in biological control programmes.     

Effects of seasonal variation in host quality and availability on parasitism by the egg parasitoid Telenomus coloradensis

Hemlock looper, Lambdina fiscellaria (Guenée) (Lepidoptera: Geometridae), is one of the most important defoliator in North American forests. The common egg parasitoid Telenomus coloradensis Crawford (Hymenoptera: Platygastridae) plays a significant role as a natural control agent, with parasitism levels in spring typically higher than in fall. The objectives of this study were to quantify changes in host acceptance and reproductive performance of the parasitoid in relation to (1) host egg fertilization in fall, (2) host diapause status, (3) host embryonic development in spring, and (4) host deprivation during summer. Our results indicate that T. coloradensis do not have the capacity to develop in unfertilized host eggs, whereas early‐diapausing eggs are more suitable for the parasitoid than post‐diapausing eggs. Furthermore, the host physiological suitability decreases with embryonic development in spring. Finally, a host deprivation period during the summer tends to negatively affect the parasitic activity of T. coloradensis. These laboratory results confirm previous hypotheses concerning T. coloradensis seasonal ecology and contribute to a better understanding of the effect of hemlock looper egg physiology and availability on the reproductive potential of T. coloradensis.     

Optimal foraging shapes host preference of a polyphagous leafminer

Abstract.  1. Most research on host selection by arthropods is based on optimal oviposition theory. This theory, also called the oviposition preference–offspring performance hypothesis, predicts that a female will choose those hosts for oviposition on which larvae perform best. Recent studies suggested, however, that optimal foraging by adults, or the quality of the host for adult performance, might also influence host choice.
2. This study investigated whether host preference of the polyphagous leafminer Liriomyza trifolii is determined by optimal foraging and/or optimal oviposition.
3. Female realised fecundity correlated nearly perfectly with feeding and oviposition preference of L. trifolii . The relationships between host preference and the offspring performance measures were always weaker. Hosts optimal for adult nutrition were also optimal for offspring performance but not vice versa . Hence, it was concluded that optimal foraging shapes feeding and oviposition preference of L. trifolii as this is the best strategy in order to maximise female fitness.     

菜蛾盘绒茧蜂主要寄生因子导致的寄主小菜蛾幼虫脂肪体结构的变化

在不同的寄生状态下,菜蛾盘绒茧蜂Cotesia plutellae不同的寄生因子可引起寄主小菜蛾Plutella xylostella幼虫脂肪体结构发生相应的改变。显微和亚显微形态结构显示： 假寄生后多分DNA病毒和毒液对脂肪体结构的完整性没有显著影响,但细胞内脂质体变得小而密集,线粒体和内质网丰富,并有糖原积累; 正常寄生后,脂肪体结构被破坏,多数线粒体内嵴紊乱,脂质体也变得不规则,特别是当幼蜂完成在寄主体内发育时,寄主体内几乎无完整脂肪体存在。与此同时,同批未被寄生的小菜蛾幼虫发育到4龄末期时,体内脂肪体细胞发育正常,已开始向蛹期细胞形态转化,细胞内脂质体很大,细胞器数量较多、糖原积累丰富, 而且部分细胞已成为游离态细胞。由此证明,寄生蜂携带的寄生因子,如多分DNA病毒、毒液、畸形细胞和幼蜂等,均对寄主脂肪体结构的改变产生影响,但程度明显不同。     

Shiny Cowbird parasitism of a low quality host: effect of host traits on a parasite's reproductive success

ABSTRACT.   The reproductive success of parasitic cowbirds ( Molothrus spp.) varies among host species and is influenced by the degree of synchronization in timing of egg laying, the duration of parasite and host incubation periods, and the ability of hosts to incubate and rear parasite young. We studied the reproductive success of Shiny Cowbirds ( Molothrus bonariensis ) that parasitized the nests of Creamy-bellied Thrushes ( Turdus amaurochalinus ) in the Monte desert region of Argentina. Shiny Cowbirds frequently parasitized Creamy-bellied Thrush nests (60%), and most cowbirds synchronized egg laying with that of thrushes (79%). Most parasitic eggs (80%) hatched within 1 d of the hatching of the first host egg, and more than 91% of the eggs survived until the end of the incubation. However, only 60% of the cowbird eggs hatched and 52% of young survived. The proportion of Shiny Cowbirds eggs laid in Creamy-bellied Thrush nests that resulted in fledged young was 0.03, including eggs and young lost due to predation or desertion. Despite this low reproductive success, Creamy-bellied Thrushes were heavily parasitized by Shiny Cowbirds in our study area. Shiny Cowbirds may continue to parasitize these thrushes because of diffuse selection or because Shiny Cowbird chicks are more likely to fledge from Creamy-bellied Thrush nests in years or areas with greater food availability when brood reduction does not occur.     

Dynamics of a host–parasitoid model with Allee effect for the host and parasitoid aggregation

In this paper, a discrete-time host–parasitoid model is investigated. Two biological phenomena, the Allee effect of the host population and the aggregation of the parasitism, are considered in our mathematical model. Through extensive numerical simulations, we gain some interesting findings related to Allee effect from this research. Firstly, the ranges of parameter, in which the population dynamics is chaos, are compressed when Allee effect is added. Secondly, the sensitivity to initial conditions of the host–parasitoid system decreased after adding Allee effect. Thirdly, without Allee effect, we observed two complicated dynamics, intermittent chaos and supertransients. However, when Allee effect is included, these two phenomena are replaced by another kind of phenomenon-period alternation, where chaos is eliminated. From above three novel findings, it can be concluded that dynamic complexities are alleviated by Allee effect. This conclusion is crucial in resolving the discrepancy between real population dynamics and theoretical predictions. Furthermore, the importance of this research is to help us understand the mechanisms inducing the irregular fluctuations of the natural populations.     

Relationships between parasitoid host range and host defence: a comparative study of egg encapsulation in two related parasitoid species

Abstract. Parasitoid host range may proceed from traits affecting host suitability, traits affecting parasitoid foraging behaviour, or both. We tested the hypothesis that encapsulation can be used as a reliable indicator of parasitoid host range in two closely related larval endoparasitoids of Lepidoptera. Cotesia glomerata (L.) (Hymenoptera: Braconidae) is gregarious and a generalist on several species of Pieridae, whereas C. rubecula (Marshall) is solitary and specific to Pieris rapae (L.). We determined the effects of host species ( Pieris brassicae (L.), P. napi (L.) and P. rapae ) (Lepidoptera: Pieridae) and host developmental stage (early first, second and third instar) on encapsulation of parasitoid eggs. Host species and parasitoid species, as well as the resulting interaction between these two factors had significant effects on encapsulation of Cotesia eggs. Encapsulation in Pieris hosts was much lower for C. glomerata (<34%, except for second and third instar of P. rapae ) than for C. rubecula (>32%), even when the latter was parasitizing P. rapae. Encapsulation increased with the age of the larvae, although the only significant difference was for C. glomerata. Overall, P. rapae showed a stronger encapsulation reaction than P. brassicae and P. napi. Encapsulation levels of C. glomerata corresponded well to patterns of female host species and host age preference for oviposition and parasitoid larval performance. In contrast, percentages of encapsulation of C. rubecula were not consistent with host preference and host suitability. We argue that encapsulation alone is unlikely to provide a sufficient explanation for C. glomerata and C. rubecula host range.     

Behavioral responses of a parasitoid fly to rapidly evolving host signals

Animals eavesdrop on signals and cues generated by prey, predators, hosts, parasites, competing species, and conspecifics, and the conspicuousness of sexual signals makes them particularly susceptible. Yet, when sexual signals evolve, most attention is paid to impacts on intended receivers (potential mates) rather than fitness consequences for eavesdroppers. Using the rapidly evolving interaction between the Pacific field cricket, Teleogryllus oceanicus, and the parasitoid fly, Ormia ochracea, we asked how parasitoids initially respond to novel changes in host signals. We recently discovered a novel sexual signal, purring song, in Hawaiian populations of T. oceanicus that appears to have evolved because it protects the cricket from the parasitoid while still allowing males to attract female crickets for mating. In Hawaii, there are no known alternative hosts for the parasitoid, so we would expect flies to be under selection to detect and attend to the new purring song. We used complementary field and laboratory phonotaxis experiments to test fly responses to purring songs that varied in many dimensions, as well as to ancestral song. We found that flies strongly prefer ancestral song over purring songs in both the field and the lab, but we caught more flies to purring songs in the field than reported in previous work, indicating that flies may be exerting some selective pressure on the novel song. When played at realistic amplitudes, we found no preferences–flies responded equally to all purrs that varied in frequency, broadbandedness, and temporal measures. However, our lab experiment did reveal the first evidence of preference for purring song amplitude, as flies were more attracted to purrs played at amplitudes greater than naturally occurring purring songs. As purring becomes more common throughout Hawaii, flies that can use purring song to locate hosts should be favored by selection and increase in frequency.