Density dependence and environmental factors affect population stability of an agricultural pest and its specialist parasitoid

Host–parasitoid dynamics are intrinsically unstable unless the risk of parasitism is sufficiently heterogeneous among hosts. Spatial aggregation of parasitoids can contribute to this heterogeneity, stabilising host–parasitoid population dynamics and thereby reducing pest outbreaks. We examined the spatial distribution of mango gall fly (Procontarinia matteiana, Kiefer and Cecconi), a non-native pest of South African mango orchards, which is controlled by a single parasitoid (Chrysonotomyia pulcherrima, Kerrich). We assessed whether spatial aggregation of parasitoids is associated with proximity to natural vegetation and/or to host density-dependent and host density-independent factors at three spatial scales. We found evidence for higher parasitism rates near natural vegetation at the field scale, and inverse host-density dependent and density-independent parasitoid aggregation at both the leaf scale and field scale. Therefore, we conclude that natural vegetation plays a role in promoting stabilising aggregation of parasitoids, possibly through provision of non-host resources (nectar, pollen), in this system.     

Winter host exploitation influences fitness traits in a parasitoid

Organisms can either evade winter's unfavourable conditions by migrating or diapausing, or endure them and maintain their activities. When it comes to foraging during winter, a period of scarce resources, there is strong selective pressure on resource exploitation strategy. Generalist parasitoids are particularly affected by this environmental constraint, as their fitness is deeply linked to the profitability of the available hosts. In this study, we considered a cereal aphid–parasitoid system and investigated (1) the host–parasitoid community structure, host availability, and parasitism rate in winter, (2) the influence of host quality in terms of species and instars on the fitness of the aphid parasitoid Aphidius rhopalosiphi De Stefani‐Perez (Hymenoptera: Braconidae: Aphidiinae), and (3) whether there is a detectable impact of host fidelity on parasitism success of this parasitoid species. Host density was low during winter and the aphid community consisted of the species Rhopalosiphum padi L. and Sitobion avenae Fabricius (both Hemiptera: Aphididae), both parasitized by A. rhopalosiphi at non‐negligible rates. Aphidius rhopalosiphi produced more offspring when parasitizing R. padi compared with S. avenae, whereas bigger offspring were produced when parasitizing S. avenae. Although aphid adults and old larvae were significantly larger hosts than young larvae, the latter resulted in higher emergence rates and larger parasitoids. No impact of host fidelity on emergence rates or offspring size was detected. This study provides some evidence that winter A. rhopalosiphi populations are able to take advantage of an array of host types that vary in profitability, indicating that host selectivity may drop under winter's unfavourable conditions.     

Differential effects of flower feeding in an insect host–parasitoid system

In many insect host–parasitoid systems, both the host and its parasitoids forage on shared floral resources. As a result of insect behaviour, morphology and physiology, flower species may act selectively at different levels of such systems, e.g., between the trophic levels of hosts and parasitoids, between species within a guild, between sexes or individuals within a species or between life history traits within an individual. We asked if effects of selectivity are consistent across levels in the horse chestnut leafminer, Cameraria ohridella, and its parasitoid complex. Insects were exposed singly in no-choice feeding trials to twelve common flower species and their survival and reproduction were recorded. Only one of twelve flower species (Ranunculus acris) tended to selectively favour the longevity of leafminers, but not of parasitoids. No flower species were found to favour parasitoids only. Both trophic levels profited from feeding on Anthriscus sylvestris, however, parasitoids benefited up to eight times more than their hosts. No differences were found among the species of the parasitoid guild, but females lived significantly longer than males, and single individuals within species were able to exploit generally unfavourable flower species. Out of the seven flower species that increased the longevity of leafminer females, only Chaerophyllum hirsutum significantly enhanced the number of eggs laid. Fecundity was generally positively correlated with longevity of leafminer females, but two flower species (C. hirsutum, Taraxacum officinale) had an additional positive effect on fecundity. In conclusion, we demonstrated that flowers act differently on life history traits in a host–parasitoid system at a multitude of biological levels and that these effects are not always consistent across levels. Selective plant-derived resources can therefore modify herbivore–natural enemy interactions in ways that are more complex than currently appreciated.     

Egg dispersion is more important than competition type for herbivores attacked by a parasitoid

Herbivore fitness can be altered by a combination of interacting organisms, such as its food plant, conspecifics, and predators/parasitoids. Here, we tested relative effects of plant species, herbivore intraspecific competition type, and spatial distribution of the herbivore among plant units on herbivore survival and whether parasitoids modified these effects. We used an endophagous bruchine seed predator Callosobruchus maculatus for the herbivore, and a braconid wasp Heterospilus prosopidis for the parasitoid. The survival rate of C. maculatus was measured for each of 16 combinations of two plants (bean species, Vigna unguiculata and V. radiata), two competition types of C. maculatus larvae (contest and scramble), two spatial distributions of hosts [sparse (1 C. maculatus larva per seed over 20 seeds) and dense (2 C. maculatus larvae per seed over ten seeds)], and with/without a parasitoid pair. In the absence of the parasitoid, C. maculatus survival rate was lower with V. radiata and in the contest type. With the parasitoid, the proportion parasitized hosts was independent of total host density. Neither the proportion of parasitized hosts nor host survival rate was affected by plant species or host strain, but they were affected by host spatial distribution. When host distribution was dense, a higher proportion of hosts were parasitized, and C. maculatus survival rate was lower. Here we discuss parasitoid potential as a selective agent for the sparse within-pod distribution of its hosts in the field.     

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.     

Autumn, winter and spring dynamics of aphid Sitobion avenae and parasitoid Aphidius rhopalosiphi interactions

The potential of parasitoids for aphid control during summer has been well documented. Few results are available on the impact of parasitoid populations on aphid hosts during autumn and winter and on the dynamics of their interactions during this period. The population development of Sitobion avenae, in Belgium, is analysed, from October to April, in the presence and absence of the parasitoid Aphidius rhopalosiphi. In the presence of parasitoids in winter, aphid populations decreased markedly and remained low at the beginning of spring. Induction of winter diapause in A. rhopalosiphi was observed during November at a mean temperature of 6.3°C and a decreasing photoperiod from 9.5–8.5 h of day light. A large range of A. rhopalosiphi mummy colourations, between dark and light, was noticed. This range of colouration did not allow a clear-cut distinction between diapausing and non-diapausing individuals of A. rhopalosiphi. The influence of seasonal weather and particularly temperature conditions on parasitoid mortality, strategy for overwintering and aphid population dynamics are discussed.     

Sex ratios in field populations of two parasitoids (Hymenoptera: Chalcidoidea) of Coccus hesperidum L. (Homoptera: Coccidae)

We tested several assumptions and predictions of host-quality-dependent sex allocation theory (Charnov et al. 1981) with data obtained for the parasitoid Metaphycus stanleyi Compere on its host, brown soft scale (Coccus hesperidum L.), in a California citrus grove and in the laboratory. Scales ceased growing after parasitization by M.?stanleyi. Thus, M. stanleyi may gauge host quality (=size) at oviposition. Host size positively influenced adult parasitoid size, and parasitoid size in turn influenced adult longevity of M. stanleyi. However, parasitoid fitness gains with host size and adult size were similar in males versus females. Sex allocation to individual hosts by M. stanleyi depended on host size; females consistently emerged from larger hosts than males. Host size was important in a relative sense; the mean host sizes of females versus males, and of solitary versus gregarious parasitoids varied with the available host size distribution. The offspring sex ratio of M. stanleyi reflected the available host size distribution; the sex ratio of emerging parasitoids varied with the available host size distribution. We did not detect a “critical host size” below which males emerged, and above which females emerged; rather, only females emerged from hosts in the upper size range, and a variable ratio of males and females emerged from hosts in the lower size range. We conclude that the sex ratio of field populations of M.?stanleyi is driven largely by the available size distribution of C. hesperidum. In addition, we tested predictions resulting from theoretical analyses of sex allocation in autoparasitoids with data obtained on Coccophagus semicircularis (Förster) parasitizing brown soft scale in the field. The sex ratio of C. semicircularis was consistently and strongly female biased (ca. 90% females). Based on available theoretical analyses, we suggest that this sex ratio pattern may have resulted from a very low encounter rate of secondary hosts coupled with a strong time limitation in C. semicircularis females. This explanation was the most plausible given constraints stemming from the detection of secondary hosts, their variable location within primary hosts, and their handling times. Finally, the size of hosts which yielded single versus multiple parasitoids, and the sizes of these parasitoids, were compared. These comparisons suggested that: (1) M. stanleyi females gauge host sizes precisely, and in terms of female offspring; thus a fitness penalty is not incurred by females which share a host, while males benefit from sharing a host, and; (2) instances where multiple C. semicircularis emerged from a single host were probably the result of parasitism by different females, or during different encounters by a single female.     

Mating and host density affect host feeding and parasitism in two species of whitefly parasitoids

Abstract The parasitoids in the genera of Encarsia and Eretmocerus (Hymenoptera: Aphelinidae) are important biological control agents of whiteflies, and some of them not only parasitize hosts but also kill them with strong host‐feeding capacity. Two whitefly parasitoid species, Encarsia sophia and Eretmocerus melanoscutus were examined to determine if mating and host density affected their host feeding and parasitism. The whitefly host, Bemisia tabaci, was presented to these two wasp species in densities of 10, 20, 30, 40, 50 and 60 third‐instar nymphs per clip cage. Mated whitefly parasitoid females fed on more hosts than unmated females under a range of host densities (under all six host densities for En. sophia; under the densities of 40 nymphs or more for Er. melanoscutus). Meanwhile, mated females parasitized more whitefly nymphs than unmated females under all host densities for both species. With increase of host density, mated or unmated Er. melanoscutus females killed more hosts by host feeding and parasitism. Mated En. sophia females killed more hosts by host feeding with increase of host density, whereas unmated females did not parasitze whitefly nymphs at all. Our results suggest that only mated female parasitoids with host‐feeding behavior should be released in crop systems to increase their bio‐control efficiency.     

Does sex-biased dispersal account for the lack of geographic and host-associated differentiation in introduced populations of an aphid parasitoid?

Host recognition and use in female parasitoids strongly relies on host fidelity, a plastic behavior which can significantly restrict the host preferences of parasitoids, thus reducing the gene flow between parasitoid populations attacking different insect hosts. However, the effect of migrant males on the genetic differentiation of populations has been frequently ignored in parasitoids, despite its known impact on gene flow between populations. Hence, we studied the extent of gene flow mediated by female and male parasitoids by assessing sibship relationships among parasitoids within and between populations, and its impact on geographic and host‐associated differentiation in the aphid parasitoid Aphidius ervi. We report evidences of a high gene flow among parasitoid populations on different aphid hosts and geographic locations. The high gene flow among parasitoid populations was found to be largely male mediated, suggested by significant differences in the distribution of full‐sib and paternal half‐sib dyads of parasitoid populations.     

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

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Histories of host shifts and cospeciation among free‐living parasitoids of Rhagoletis flies

Host shifts by specialist insects can lead to reproductive isolation between insect populations that use different hosts, promoting diversification. When both a phytophagous insect and its ancestrally associated parasitoid shift to the same novel host plant, they may cospeciate. However, because adult parasitoids are free living, they can also colonize novel host insects and diversify independent of their ancestral host insect. Although shifts of parasitoids to new insect hosts have been documented in ecological time, the long‐term importance of such shifts to parasitoid diversity has not been evaluated. We used a genus of flies with a history of speciation via host shifting (Rhagoletis [Diptera: Tephritidae]) and three associated hymenopteran parasitoid genera (Diachasma, Coptera and Utetes) to examine cophylogenetic relationships between parasitoids and their host insects. We inferred phylogenies of Rhagoletis, Diachasma, Coptera and Utetes and used distance‐based cophylogenetic methods (ParaFit and PACo) to assess congruence between fly and parasitoid trees. We used an event‐based method with a free‐living parasitoid cost model to reconstruct cophylogenetic histories of each parasitoid genus and Rhagoletis. We found that the current species diversity and host–parasitoid associations between the Rhagoletis flies and parasitoids are the primary result of ancient cospeciation events. Parasitoid shifts to ancestrally unrelated hosts primarily occur near the branch tips, suggesting that host shifts contribute to recent parasitoid species diversity but that these lineages may not persist over longer time periods. Our analyses also stress the importance of biologically informed cost models when investigating the coevolutionary histories of hosts and free‐living parasitoids.     

Tritrophic interactions between parasitoids and cereal aphids are mediated by nitrogen fertilizer

Host plant nutritional quality can directly and indirectly affect the third trophic levels. The aphid–parasitoid relationship provides an ideal system to investigate tritrophic interactions (as the parasitoids are completely dependent for their development upon their hosts) and assess the bottom up forces operating at different concentrations of nitrogen applications. The effects of varying nitrogen fertilizer on the performance of Aphidius colemani (V.) reared on Sitobion avenae (F.) and Aphidius rhopalosiphi (D.) reared on Rhopalosiphum padi (L.) were measured. Parasitism and percent emergence of parasitoids were positively affected by nitrogen fertilizer treatments while developmental duration (egg, larval, and pupal stages) was not affected by increasing nitrogen inputs. In males and females of both parasitoid species, adult longevity increased with the increasing nitrogen fertilizer. Hind tibia length and mummy weight of both parasitoid species increased with nitrogen fertilizer concentrations, as a result of larger aphids. This study showed that nitrogen application to the soil can have important consequences for aboveground multitrophic interactions.     

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

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

Strange limits of stability in host-parasitoid systems

The classical Nicholson-Bailey model for a two species host-parasitoid system with discrete generations assumes random distributions of both hosts and parasitoids, randomly searching parasitoids, and random encounters between the individuals of the two species. Although unstable, this model induced many investigations into more complex host-parasitoid systems. Local linearized stability analysis shows that equilibria of host parasitoid systems within the framework of a generalized Nicholson-Bailey model are generally unstable. Stability is only possible if host fertility does not exceede ⁴=54.5982 and if superparasitism is unsuccessful. This special situation has already been discovered by Hassell et al. (1983) in their study of the effects of variable sex ratios on host parasitoid dynamics. We discuss global behaviour of the Hassell-Waage-May model using KAM-theory and illustrate its sensitivity to small perturbations, which can give rise to radically different patterns of the population dynamics of interacting hosts and parasitoids.     

Parasitoids of the goldenrod gall moth: effects of scale on spatial density dependence

Summary A parasitoid assemblage consisting of four hymenopteran species caused larval and pupal mortality of the host Gnorimoschema gallaeosolidaginis. In the absence of discrete host patches, the relationship between densities of hosts and parasitized hosts was examined on scales of 0.25, 1, 4, 16 and 25 m² within a 400 m² plot and between ten 16 m² plots within a 1·3 km² area. Within the 400 m² plot, positive density dependence was observed on scales of 1, 4 and 16 m². Rates of parasitism were found to be density independent across the ten 16 m² plots. The nature of parasitoid and host spatial patterns were examined at the 400 m² plot by using Goodall's (1974) paired-quadrat variance function, and by fitting the observed distribution of galls and parasitized galls to the Poisson and negative binomial on three scales. Postive density dependence at the 400 m² plot occurred in the context of a host density gradient and may indicate aggregation of search time by parasitoids. However, significant responses on scales of 4 and 16 m² may only reflect the sum of parasitoid responses on lower scales because of this gradient. Predominance of significant responses on a 1 m² scale may be related to the high degree of variation in host density, and limits to active searching range of parasitoids.     

Periodicity,persistence, and collapse in host–parasitoid systems with egg limitation

There is an emerging consensus that parasitoids are limited by the number of eggs which they can lay as well as the amount of time they can search for their hosts. Since egg limitation tends to destabilize host–parasitoid dynamics, successful control of insect pests by parasitoids requires additional stabilizing mechanisms such as heterogeneity in the distribution of parasitoid attacks and host density-dependence. To better understand how egg limitation, search limitation, heterogeneity in parasitoid attacks, and host density-dependence influence host–parasitoid dynamics, discrete time models accounting for these factors are analyzed. When parasitoids are purely egg-limited, a complete anaylsis of the host–parasitoid dynamics are possible. The analysis implies that the parasitoid can invade the host system only if the parasitoid’s intrinsic fitness exceeds the host’s intrinsic fitness. When the parasitoid can invade, there is a critical threshold, CV ^*>1, of the coefficient of variation (CV) of the distribution of parasitoid attacks that determines that outcome of the invasion. If parasitoid attacks sufficiently aggregated (i.e., CV>CV ^*), then the host and parasitoid coexist. Typically (in a topological sense), this coexistence is shown to occur about a periodic attractor or a stable equilibrium. If the parasitoid attacks are sufficiently random (i.e. CV<CV ^*), then the parasitoid drives the host to extinction. When parasitoids are weakly search-limited as well as egg-limited, coexistence about a global attractor occurs even if CV<CV ^*. However, numerical simulations suggest that the nature of this attractor depends critically on whether CV<1 or CV>1. When CV<1, the parasitoid exhibits highly oscillatory dynamics. Alternatively, when parasitoid attacks are sufficiently aggregated but not overly aggregated (i.e. CV>1 but close to 1), the host and parasitoid coexist about a stable equilibrium with low host densities. The implications of these results for classical biological control are discussed.     

Pre‐Patch Experience Affects the Egg Distribution Pattern in a Polyembryonic Parasitoid of Moth Egg Batches

According to foraging theory, female parasitoids should alter their host choice in response to cues that indicate a limitation of resources. We tested whether females of the polyembryonic parasitoid Ageniaspis fuscicollis (Hymenoptera: Encyrtidae), which attack egg batches of small ermine moths (Lepidoptera: Yponomeutidae), would alter their host acceptance pattern in response to different pre‐patch experience. We kept females of the parasitoid prior to a patch visit under different conditions, which should indicate different levels of competition for hosts. With increased competition as pre‐patch experience, females laid more eggs per host egg and self‐superparasitized more often, and the resultant egg distributions showed a trend from more regular distributions to increasingly Poisson and aggregated distributions. Consequently, females with a pre‐patch experience that would indicate low competition for hosts had the most even egg distributions. We conclude that pre‐patch experience of competitors may lead to a significant change of mutual interference patterns in egg‐laying A. fuscicollis wasps.     

Host discrimination of a larval parasitoid: the quick movement of Microplitis demolitor

Many parasitoids discriminate previously parasitised hosts from unparasitised ones to avoid mortality of offspring. Parasitoids that parasitise aggressive hosts such as lepidopteran larvae are known to attack hosts very quickly to avoid being attacked. However, little is known about host discrimination of such quick attacking parasitoids. We investigated host discrimination of Microplitis demolitor (Wilkinson) (Hymenoptera: Braconidae) a quick attacking parasitoid of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Results showed that ratios of female wasps that rejected the hosts after antennal examination did not differ between parasitised and unparasitised hosts, indicating that M. demolitor did not discriminate hosts by antennal examination. However, 95% of females that inserted ovipositor into unparasitised hosts actually laid eggs, whereas it was only 31% for parasitised hosts, indicating that females discriminated hosts by oviposition insertion. Analyzing video recordings revealed that the ovipositor exploration of the host took 0.3 s. Female wasps that had experienced high-host density of unparasitised hosts readily rejected parasitised hosts, while wasps with experience of low host availability of parasitised hosts tended to accept parasitised hosts. This suggests that host discrimination behaviour of M. demolitor is affected by previous experience of different host availability and host quality.

     

Distribution and colonisation ability of three parasitoids and their herbivorous host in a fragmented landscape

Habitat fragmentation can disrupt communities of interacting species even if only some of the species are directly affected by fragmentation. For instance, if parasitoids disperse less well than their herbivorous hosts, habitat fragmentation may lead to higher herbivory in isolated plant patches due to the absence of the third trophic level. Community-level studies suggest that parasitoids tend to have limited dispersal abilities, on the order of tens of metres, much smaller than that of their hosts, while species-oriented studies document dispersal by parasitoids on the scale of kilometres. In this study the distribution patterns of three parasitoid species with different life histories and their moth host, Hadena bicruris, a specialist herbivore of Silene latifolia, were compared in a large-scale network of natural fragmented plant patches along the rivers Rhine and Waal in the Netherlands. We examined how patch size and isolation affect the presence of each species. Additionally, experimental plots were used to study the colonisation abilities of the species at different distances from source populations.In the natural plant patches the presence of the herbivore and two of the parasitoids, the gregarious specialist Microplitis tristis and the gregarious generalist Bracon variator were not affected by patch isolation at the scale of the study, while the solitary specialist Eurylabus tristis was. In contrast to the herbivore, the presence of all parasitoid species declined with plant patch size. The colonisation experiment confirmed that the herbivore and M. tristis are good dispersers, able to travel at least 2 km within a season. B. variator showed intermediate colonisation ability and E. tristis showed very limited colonisation ability at this spatial scale. Characteristics of parasitoid species that may contribute to differences in their dispersal abilities are discussed.     

Effects of plant diversity and structural complexity on parasitoid behaviour in a field experiment

1. In natural ecosystems, plants containing hosts for parasitoids are often embedded within heterogeneous plant communities. These plant communities surrounding host‐infested plants may influence the host‐finding ability of parasitoids. 2. A release‐recapture‐approach was used to examine whether the diversity and structural complexity of the community surrounding a host‐infested plant influences the aggregation behaviour of the leaf‐miner parasitoid Dacnusa sibirica Telenga and naturally occurring local leaf‐miner parasitoids. Released and locally present parasitoids were collected on potted Jacobaea vulgaris Gaertn.plants infested with the generalist leaf‐miner Chromatomyia syngenesiae Hardy. The plants were placed in experimentally established plant communities differing in plant diversity (1–9 species) and habitat complexity (bare ground, mown vegetation, and tall vegetation). Additionally, parasitoids were reared out from host mines on the trap plants. 3. Plant diversity did not influence the mean number of recaptured D. sibirica or captures of other locally present parasitoids but the number of recaptured parasitoids was influenced by habitat complexity. No D. sibirica parasitoids were recaptured in the bare ground plots or plots with mown vegetation. The mean number of recaptured D. sibirica generally increased with increasing complexity of the plant community, whereas locally present parasitoids were captured more frequently in communities with more bare ground. There was a unimodal relationship between the number of reared out parasitoids and diversity of the surrounding vegetation with the highest density of emerged parasitoids at intermediate diversity levels. 4. The present study adds to the thus far limited body of literature examining the aggregation behaviour of parasitoids in the field and suggests that the preference of parasitoids to aggregate in complex versus simple vegetation is association specific and thus depends on the parasitoid species as well as the identity of the plant community.