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Jeffrey A. Harvey - One of the best experts on this subject based on the ideXlab platform.

  • Honeydew composition and its effect on life-history parameters of Hyperparasitoids
    Ecological Entomology, 2019
    Co-Authors: Frank A. C. Van Neerbos, Jetske G. Boer, Lucia Salis, Ward Tollenaar, Martine Kos, Louise E. M. Vet, Jeffrey A. Harvey
    Abstract:

    1. Diets that maximise life span often differ from diets that maximise reproduction. Animals have therefore evolved advanced foraging strategies to acquire optimal nutrition and maximise their fitness. The free-living adult females of parasitoid wasps (Hymenoptera) need to balance their search for hosts to reproduce and for carbohydrate resources to feed. 2. Honeydew, excreted by phloem-feeding insects, presents a widely available carbohydrate source in nature that can benefit natural enemies of honeydew-producing insects. However, the effects of variation in honeydew on organisms in the fourth trophic level, such as Hyperparasitoids, are not yet understood. 3. This study examined how five different honeydew types influence longevity and fecundity of four hyperparasitoid taxa. Asaphes spp. (Pteromalidae) and Dendrocerus spp. (Megaspilidae) are secondary parasitoids of aphid parasitoids and are thus associated with honeydew-producing insects. Gelis agilis and Acrolyta nens (both Ichneumonidae) are secondary parasitoids of species that do not use honeydew-producing hosts. 4. Most honeydew types had a positive or neutral effect on life span and fecundity of Hyperparasitoids compared with controls without honeydew, although negative effects were also found for both aphid Hyperparasitoids. Honeydew produced by aphids feeding on sweet pepper plants was most beneficial for all hyperparasitoid taxa, which can partially be explained by the high amount of honeydew, but also by the composition of dietary sugars in these honeydew types. 5. The findings of this study underline the value of aphid honeydew as a carbohydrate resource for fourth-trophic-level organisms, not only those associated with honeydew-producing insects but also ?interlopers? without such a natural association.

  • Simulated heatwave conditions associated with global warming affect development and competition between Hyperparasitoids
    Oikos, 2019
    Co-Authors: Cong Chen, Rieta Gols, Arjen Biere, S. Helena Donner, Jeffrey A. Harvey
    Abstract:

    Anthropogenic global warming and attendant effects like heatwaves affect the biology and ecology of both individuals and species within and across different trophic levels. Here, we examined the effects of a simulated heatwave on development of and competition between two hyperparasitoid wasps, Lysibia nana and Acrolyta nens when attacking the same host, cocoons of the primary parasitoid, Cotesia glomerata. Parasitized hosts were exposed to three different day and night temperature regimes (low, medium and high) that reflect cool, normal and heatwave conditions in the Netherlands. We found that higher temperatures decreased survival to eclosion more strongly in the Hyperparasitoids than in their host. Heatwave conditions also shortened development time and led to the production of smaller adult wasps of both hyperparasitoid species in singly parasitized hosts. In multiparasitized hosts, L. nana won most of the contests when it oviposited first, irrespective of the time interval between the first and second parasitism, whereas A. nens only dominated when it had a 24 h head start or longer. Most importantly, our results show that L. nana in particular benefited in competition at higher temperatures, perhaps due to an increase in the metabolic rate and more rapid egg and/or larval development. This may potentially reduce opportunities for coexistence following heat waves. Our results suggest that heatwaves associated with global warming will enhance the rate of development, but negatively affect survival and other fitness-related traits in (hyper)parasitoids. Moreover, the outcome of larval competition may be determined via physiological responses that are species-specific and thus influence phenology.

  • Effects of temperature and food source on reproduction and longevity of aphid Hyperparasitoids of the genera Dendrocerus and Asaphes
    BioControl, 2019
    Co-Authors: Jetske G. Boer, Jeffrey A. Harvey, Lucia Salis, Ward Tollenaar, Martine Kos, Lisa J. M. Van Heumen, Thibault P. M. Costaz, Louise E. M. Vet
    Abstract:

    Hyperparasitoids of aphid parasitoids commonly occur in (sweet pepper) greenhouses, and can pose a threat to effective biological control of aphids. Here, we studied life history characteristics of laboratory colonies of Dendrocerus spp. Ratzeburg (Hymenoptera: Megaspilidae) and Asaphes spp. Walker (Pteromalidae) that originated from a commercial sweet pepper greenhouse. We aimed to clarify how these two hyperparasitoid taxa can coexist inside greenhouses. Hyperparasitoids of both taxa have a long lifespan that was extended significantly by food sources that are naturally available in a greenhouse environment, including aphid honeydew and sweet pepper flowers. Differences in sensitivity to decreased or increased temperatures did not appear to explain seasonal patterns in abundance of Dendrocerus spp. and Asaphes spp. in sweet pepper greenhouses. Instead, Dendrocerus spp. may have an advantage early in the season because it thrives on aphid honeydew, while Asaphes spp. may do better later in the season because of its long lifespan and extensive reproductive period.

  • Hyperparasitoids exploit herbivore induced plant volatiles during host location to assess host quality and non host identity
    Oecologia, 2019
    Co-Authors: Antonino Cusumano, Marcel Dicke, Jeffrey A. Harvey, Erik H. Poelman
    Abstract:

    Although consumers often rely on chemical information to optimize their foraging strategies, it is poorly understood how top carnivores above the third trophic level find resources in heterogeneous environments. Hyperparasitoids are a common group of organisms in the fourth trophic level that lay their eggs in or on the body of other parasitoid hosts. Such top carnivores use herbivore-induced plant volatiles (HIPVs) to find caterpillars containing parasitoid host larvae. Hyperparasitoids forage in complex environments where hosts of different quality may be present alongside non-host parasitoid species, each of which can develop in multiple herbivore species. Because both the identity of the herbivore species and its parasitization status can affect the composition of HIPV emission, Hyperparasitoids encounter considerable variation in HIPVs during host location. Here, we combined laboratory and field experiments to investigate the role of HIPVs in host selection of Hyperparasitoids that search for hosts in a multi-parasitoid multi-herbivore context. In a wild Brassica oleracea-based food web, the hyperparasitoid Lysibia nana preferred HIPVs emitted in response to caterpillars parasitized by the gregarious host Cotesia glomerata over the non-host Hyposoter ebeninus. However, no plant-mediated discrimination occurred between the solitary host C. rubecula and the non-host H. ebeninus. Under both laboratory and field conditions, hyperparasitoid responses were not affected by the herbivore species (Pieris brassicae or P. rapae) in which the three primary parasitoid species developed. Our study shows that HIPVs are an important source of information within multitrophic interaction networks allowing Hyperparasitoids to find their preferred hosts in heterogeneous environments.

  • Differential effects of climate warming on reproduction and functional responses on insects in the fourth trophic level
    Functional Ecology, 2019
    Co-Authors: Cong Chen, Rieta Gols, Arjen Biere, Jeffrey A. Harvey
    Abstract:

    Abstract Understanding the effects of anthropogenic global warming (AGW) on species interactions is essential for predicting community responses to climate change. However, while effects of AGW on resource?consumer interactions at the first and second trophic level have been well studied, little is known about effects on interactions at higher trophic levels at the terminal end of food chains (e.g. in the third and fourth trophic levels). Here, we examined the effects of temperature variability by simulating heatwaves on functional responses of two species at the fourth trophic level (Hyperparasitoids) that parasitize host species at the third trophic level (parasitoid cocoons). We found that host cocoons developed faster under simulated heatwave conditions, decreasing the temporal window of susceptibility of the host cocoons to parasitism by the two Hyperparasitoids, and consequently parasitism declined with temperature. However, the effects of a simulated heatwave markedly differed among the two hyperparasitoid species; temperature and host quality had a much stronger effect on early reproduction in the less fecund hyperparasitoid Gelis agilis, than in the more fecund species Acrolyta nens. Our results suggest that exposure to heatwaves, that are expected to increase in frequency, will affect the ability of species at higher trophic levels to exploit transient resources whose suitability is temperature-dependent. In turn, the observed effects of AGW on the functional responses of the Hyperparasitoids may disrupt trophic interactions and have profound impact on population dynamics and ecological processes. A plain language summary is available for this article.

Erik H. Poelman - One of the best experts on this subject based on the ideXlab platform.

  • Hyperparasitoids exploit herbivore induced plant volatiles during host location to assess host quality and non host identity
    Oecologia, 2019
    Co-Authors: Antonino Cusumano, Marcel Dicke, Jeffrey A. Harvey, Erik H. Poelman
    Abstract:

    Although consumers often rely on chemical information to optimize their foraging strategies, it is poorly understood how top carnivores above the third trophic level find resources in heterogeneous environments. Hyperparasitoids are a common group of organisms in the fourth trophic level that lay their eggs in or on the body of other parasitoid hosts. Such top carnivores use herbivore-induced plant volatiles (HIPVs) to find caterpillars containing parasitoid host larvae. Hyperparasitoids forage in complex environments where hosts of different quality may be present alongside non-host parasitoid species, each of which can develop in multiple herbivore species. Because both the identity of the herbivore species and its parasitization status can affect the composition of HIPV emission, Hyperparasitoids encounter considerable variation in HIPVs during host location. Here, we combined laboratory and field experiments to investigate the role of HIPVs in host selection of Hyperparasitoids that search for hosts in a multi-parasitoid multi-herbivore context. In a wild Brassica oleracea-based food web, the hyperparasitoid Lysibia nana preferred HIPVs emitted in response to caterpillars parasitized by the gregarious host Cotesia glomerata over the non-host Hyposoter ebeninus. However, no plant-mediated discrimination occurred between the solitary host C. rubecula and the non-host H. ebeninus. Under both laboratory and field conditions, hyperparasitoid responses were not affected by the herbivore species (Pieris brassicae or P. rapae) in which the three primary parasitoid species developed. Our study shows that HIPVs are an important source of information within multitrophic interaction networks allowing Hyperparasitoids to find their preferred hosts in heterogeneous environments.

  • Complexity of plant volatile-mediated interactions beyond the third trophic level
    Signaling and Communication in Plants, 2016
    Co-Authors: Erik H. Poelman
    Abstract:

    Food chains of plant-associated communities typically reach beyond three trophic levels. The predators and parasitoids in the third trophic level are under attack by top predators or parasitised by Hyperparasitoids. These higher trophic level organisms respond to plant volatiles in search of their prey or host. Thereby, plant volatiles affect community processes such as competition and intraguild predation among predators and parasitoids at the terminal end of the food chain. The response of fourth trophic level organisms to plant volatiles potentially reduces the benefit of these volatiles as indirect defence for the plant. In the application of parasitoids as biological control agents of herbivore pests, Hyperparasitoids may diminish the effectiveness of parasitoids. Detailed understanding of the use of plant odours by Hyperparasitoids may provide tools to further optimise biological control.

  • Development of a solitary koinobiont hyperparasitoid in different instars of its primary and secondary hosts
    Journal of insect physiology, 2016
    Co-Authors: Jeffrey A. Harvey, Erik H. Poelman, F. Zhu, Mark Lammers, Martine Kos, Minghui Fei, Robin Heinen, Rieta Gols
    Abstract:

    Parasitoid wasps are excellent organisms for studying the allocation of host resources to different fitness functions such as adult body mass and development time. Koinobiont parasitoids attack hosts that continue feeding and growing during parasitism, whereas idiobiont parasitoids attack non-growing host stages or paralyzed hosts. Many adult female koinobionts attack a broad range of host stages and are therefore faced with a different set of dynamic challenges compared with idiobionts, where host resources are largely static. Thus far studies on solitary koinobionts have been almost exclusively based on primary parasitoids, yet it is known that many of these are in turn attacked by both koinobiont and idiobiont Hyperparasitoids. Here we compare parasitism and development of a primary koinobiont hyperparasitoid, Mesochorus gemellus (Hymenoptera: Ichneumonidae) in larvae of the gregarious primary koinobiont parasitoid, Cotesia glomerata (Hymenoptera: Braconidae) developing in the secondary herbivore host, Pieris brassicae (Lepidoptera: Pieridae). As far as we know this is the first study to examine development of a solitary primary hyperparasitoid in different stages of its secondary herbivore host. Pieris brassicae caterpillars were parasitized as L1 by C. glomerata and then these parasitized caterpillars were presented in separate cohorts to M. gemellus as L3, L4 or L5 instar P. brassicae. Different instars of the secondary hosts were used as proxies for different developmental stages of the primary host, C. glomerata. Larvae of C. glomerata in L5 P. brassicae were significantly longer than those in L3 and L4 caterpillars. Irrespective of secondary host instar, every parasitoid cluster was hyperparasitized by M. gemellus but all only produced male progeny. Male development time decreased with host stage attacked, whereas adult male body mass did not, which shows that M. gemellus is able to optimally exploit older host larvae in terms of adult size despite their decreasing mass during the pupal stage. Across a range of cocoon masses, hyperparasitoid adult male body mass was approximately 84% as large as primary parasitoids, revealing that M. gemellus is almost as efficient at exploiting host resources as secondary (pupal) Hyperparasitoids.

  • Intrinsic competition between primary Hyperparasitoids of the solitary endoparasitoid Cotesia rubecula
    Ecological Entomology, 2016
    Co-Authors: F. Zhu, Jeffrey A. Harvey, Mark Lammers, Erik H. Poelman
    Abstract:

    1. In nature, competitive interactions occur when different species exploit similar niches. Parasitic wasps (parasitoids) often have narrow host ranges and need to cope with competitors that use the same host species for development of their offspring. When larvae of different parasitoid species develop in the same host, this leads to intrinsic and often contest com.petition. Thus far, m.ost studies on intrinsic competition have focused on primary parasitoids. However, competition among primary.Hyperparasitoids, parasitic wasps that use primary parasitoids as a host, has been little studied. 2. This study investigated intrinsic competition between two primary Hyperparasitoids, the gregarious Baryscapus galactopus and the solitary Mesochoru,s gemellu,s, which lay their eggs in primary parasitoid larvae of tesla rubecula, while those in turn are developing inside their herbivore host, Pieris rapae. The aims were to identify: (i) which hyperparasitoid is the superior competitor; and (ii) whether oviposition sequence affects the outcome of intrinsic competition. 3. The results show that B. galactopus won 70% of contests when the two Hyperparasitoids parasitised the host at the same time, and 90% when 13. galactopus oviposited first. When M. gemellus had a 48 h head start, the two Hyperparasitoids had an equal chance to win the competition. This suggests that M. galactopus is an intrinsically superior competitor to M. gemellu,s, Moreover, the outcome of competition is affected by time lags in oviposition events. 4. In contrast to what has been reported for primary parasitoids, we found that a. gregarious hyperparasitoid species had a competitive advantage over a solitary species.

  • Parasitism overrides herbivore identity allowing Hyperparasitoids to locate their parasitoid host using herbivore-induced plant volatiles
    Molecular ecology, 2015
    Co-Authors: F. Zhu, Marcel Dicke, Jeffrey A. Harvey, Berhane T. Weldegergis, Colette Broekgaarden, Ben Vosman, Erik H. Poelman
    Abstract:

    Foraging success of predators profoundly depends on reliable and detectable cues indicating the presence of their often inconspicuous prey. Carnivorous insects rely on chemical cues to optimize foraging efficiency. Hyperparasitoids that lay their eggs in the larvae or pupae of parasitic wasps may find their parasitoid hosts developing in different herbivores. They can use herbivore-induced plant volatiles (HIPVs) to locate parasitized caterpillars. Because different herbivore species induce different HIPV emission from plants, Hyperparasitoids may have to deal with large variation in volatile information that indicates host presence. In this study, we used an ecogenomics approach to first address whether parasitized caterpillars of two herbivore species (Pieris rapae and P. brassicae) induce similar transcriptional and metabolomic responses in wild Brassica oleracea plants and, second, whether Hyperparasitoids Lysibia nana are able to discriminate between these induced plant responses to locate their parasitoid host in different herbivores under both laboratory and field conditions. Our study revealed that both herbivore identity and parasitism affect plant transcriptional and metabolic responses to herbivory. We also found that Hyperparasitoids are able to respond to HIPVs released by wild B. oleracea under both laboratory and field conditions. In addition, we observed stronger attraction of Hyperparasitoids to HIPVs when plants were infested with parasitized caterpillars. However, Hyperparasitoids were equally attracted to plants infested by either herbivore species. Our results indicate that parasitism plays a major role in HIPV-mediated plant-hyperparasitoid interactions. Furthermore, these findings also indicate that plant trait-mediated indirect interaction networks play important roles in community-wide species interactions.

Rieta Gols - One of the best experts on this subject based on the ideXlab platform.

  • Simulated heatwave conditions associated with global warming affect development and competition between Hyperparasitoids
    Oikos, 2019
    Co-Authors: Cong Chen, Rieta Gols, Arjen Biere, S. Helena Donner, Jeffrey A. Harvey
    Abstract:

    Anthropogenic global warming and attendant effects like heatwaves affect the biology and ecology of both individuals and species within and across different trophic levels. Here, we examined the effects of a simulated heatwave on development of and competition between two hyperparasitoid wasps, Lysibia nana and Acrolyta nens when attacking the same host, cocoons of the primary parasitoid, Cotesia glomerata. Parasitized hosts were exposed to three different day and night temperature regimes (low, medium and high) that reflect cool, normal and heatwave conditions in the Netherlands. We found that higher temperatures decreased survival to eclosion more strongly in the Hyperparasitoids than in their host. Heatwave conditions also shortened development time and led to the production of smaller adult wasps of both hyperparasitoid species in singly parasitized hosts. In multiparasitized hosts, L. nana won most of the contests when it oviposited first, irrespective of the time interval between the first and second parasitism, whereas A. nens only dominated when it had a 24 h head start or longer. Most importantly, our results show that L. nana in particular benefited in competition at higher temperatures, perhaps due to an increase in the metabolic rate and more rapid egg and/or larval development. This may potentially reduce opportunities for coexistence following heat waves. Our results suggest that heatwaves associated with global warming will enhance the rate of development, but negatively affect survival and other fitness-related traits in (hyper)parasitoids. Moreover, the outcome of larval competition may be determined via physiological responses that are species-specific and thus influence phenology.

  • Differential effects of climate warming on reproduction and functional responses on insects in the fourth trophic level
    Functional Ecology, 2019
    Co-Authors: Cong Chen, Rieta Gols, Arjen Biere, Jeffrey A. Harvey
    Abstract:

    Abstract Understanding the effects of anthropogenic global warming (AGW) on species interactions is essential for predicting community responses to climate change. However, while effects of AGW on resource?consumer interactions at the first and second trophic level have been well studied, little is known about effects on interactions at higher trophic levels at the terminal end of food chains (e.g. in the third and fourth trophic levels). Here, we examined the effects of temperature variability by simulating heatwaves on functional responses of two species at the fourth trophic level (Hyperparasitoids) that parasitize host species at the third trophic level (parasitoid cocoons). We found that host cocoons developed faster under simulated heatwave conditions, decreasing the temporal window of susceptibility of the host cocoons to parasitism by the two Hyperparasitoids, and consequently parasitism declined with temperature. However, the effects of a simulated heatwave markedly differed among the two hyperparasitoid species; temperature and host quality had a much stronger effect on early reproduction in the less fecund hyperparasitoid Gelis agilis, than in the more fecund species Acrolyta nens. Our results suggest that exposure to heatwaves, that are expected to increase in frequency, will affect the ability of species at higher trophic levels to exploit transient resources whose suitability is temperature-dependent. In turn, the observed effects of AGW on the functional responses of the Hyperparasitoids may disrupt trophic interactions and have profound impact on population dynamics and ecological processes. A plain language summary is available for this article.

  • Development of a solitary koinobiont hyperparasitoid in different instars of its primary and secondary hosts
    Journal of insect physiology, 2016
    Co-Authors: Jeffrey A. Harvey, Erik H. Poelman, F. Zhu, Mark Lammers, Martine Kos, Minghui Fei, Robin Heinen, Rieta Gols
    Abstract:

    Parasitoid wasps are excellent organisms for studying the allocation of host resources to different fitness functions such as adult body mass and development time. Koinobiont parasitoids attack hosts that continue feeding and growing during parasitism, whereas idiobiont parasitoids attack non-growing host stages or paralyzed hosts. Many adult female koinobionts attack a broad range of host stages and are therefore faced with a different set of dynamic challenges compared with idiobionts, where host resources are largely static. Thus far studies on solitary koinobionts have been almost exclusively based on primary parasitoids, yet it is known that many of these are in turn attacked by both koinobiont and idiobiont Hyperparasitoids. Here we compare parasitism and development of a primary koinobiont hyperparasitoid, Mesochorus gemellus (Hymenoptera: Ichneumonidae) in larvae of the gregarious primary koinobiont parasitoid, Cotesia glomerata (Hymenoptera: Braconidae) developing in the secondary herbivore host, Pieris brassicae (Lepidoptera: Pieridae). As far as we know this is the first study to examine development of a solitary primary hyperparasitoid in different stages of its secondary herbivore host. Pieris brassicae caterpillars were parasitized as L1 by C. glomerata and then these parasitized caterpillars were presented in separate cohorts to M. gemellus as L3, L4 or L5 instar P. brassicae. Different instars of the secondary hosts were used as proxies for different developmental stages of the primary host, C. glomerata. Larvae of C. glomerata in L5 P. brassicae were significantly longer than those in L3 and L4 caterpillars. Irrespective of secondary host instar, every parasitoid cluster was hyperparasitized by M. gemellus but all only produced male progeny. Male development time decreased with host stage attacked, whereas adult male body mass did not, which shows that M. gemellus is able to optimally exploit older host larvae in terms of adult size despite their decreasing mass during the pupal stage. Across a range of cocoon masses, hyperparasitoid adult male body mass was approximately 84% as large as primary parasitoids, revealing that M. gemellus is almost as efficient at exploiting host resources as secondary (pupal) Hyperparasitoids.

  • Host preference and offspring performance are linked in three congeneric hyperparasitoid species
    Ecological Entomology, 2014
    Co-Authors: Jeffrey A. Harvey, Rieta Gols, Helen Snaas, Miriama Malcicka, Bertanne Visser
    Abstract:

    1. The optimisation theory predicts that insect mothers should oviposit on resources on which they attain the highest exclusive fitness. The development of parasitoid wasps is dependent on limited host resources that are often not much larger than the adult parasitoid. 2. In the present study preference and development in three congeneric species of secondary Hyperparasitoids attacking cocoons of two congeneric primary parasitoids that differ significantly in size were compared. Gelis agilis (Fabricius) and G. acarorum (L.) are wingless Hyperparasitoids that forage in grassy habitats, whereas G. areator (Panzer) is fully winged and forages higher in the canopy of forbs. 3. The three species were reared on cocoons containing pupae of a small gregarious endoparasitoid, Cotesia glomerata (L.), and a larger solitary species, C. rubecula (Marshall), both of which develop in the caterpillars of pierid butterflies. 4. Adult mass was correlated with initial cocoon mass in all three species, whereas development time was unaffected. Wasps were larger when developing in C. rubecula. However, for a given host mass, wasps were larger when developing on the smaller host, C. glomerata. This suggests that there is a physiological limit to hyperparasitoid size that was exceeded when C. rubecula served as host. 5. All three Hyperparasitoids strongly preferred to attack cocoons of the larger species, C. rubecula, often avoiding cocoons of C. glomerata entirely. 6. Preference and performance are correlated in the three Gelis species. However, owing to variation in the distribution and thus abundance of their hosts, it is argued that cumulative fitness may be still higher in the smaller host species.

  • Development of a hyperparasitoid wasp in different stages of its primary parasitoid and secondary herbivore hosts.
    Journal of insect physiology, 2012
    Co-Authors: Jeffrey A. Harvey, Rieta Gols, Louise E. M. Vet, H. Marjolein Kruidhof
    Abstract:

    Parasitoid wasps are model organisms for exploring constraints on life history and development strategies in arthropods. Koinobiont parasitoids attack hosts that may vary considerably in size at parasitation. Thus far, studies exploring koinobiont development in hosts of different size have been exclusively done with primary parasitoids attacking insect herbivores. However, the larvae of primary koinobiont parasitoids may in turn be attacked by koinobiont Hyperparasitoids. We examined development of the gregarious hyperparasitoid Baryscapus galactopus in different stages of its primary parasitoid host, Cotesia glomerata, itself developing in different stages of caterpillars of the cabbage butterfly, Pieris brassicae. This is the first study exploring hyperparasitoid development in different stages of a primary and secondary host. Second instar (L2) larvae of P. brassicae were parasitized by C. glomerata, and separate cohorts of L3 to L5 P. brassicae containing different stages of C. glomerata were then presented to B. galactopus females. B. galactopus was able to parasitize tiny larvae of C. glomerata in L3 caterpillars of P. brassicae, but hyperparasitism efficiency increased in later instars of both C. glomerata and P. brassicae. Development time of B. galactopus was extended in younger C. glomerata/P. brassicae hosts, whereas adult mass was largest when C. glomerata was attacked in L3 through early L5 P. brassicae. Our results show that B. galactopus adjusts its development rate in accordance with the size of both its primary and secondary hosts, in order to ensure survival. Adaptive responses to phylogenetic constraints on the development of primary Hyperparasitoids are discussed.

Marcel Dicke - One of the best experts on this subject based on the ideXlab platform.

  • Hyperparasitoids exploit herbivore induced plant volatiles during host location to assess host quality and non host identity
    Oecologia, 2019
    Co-Authors: Antonino Cusumano, Marcel Dicke, Jeffrey A. Harvey, Erik H. Poelman
    Abstract:

    Although consumers often rely on chemical information to optimize their foraging strategies, it is poorly understood how top carnivores above the third trophic level find resources in heterogeneous environments. Hyperparasitoids are a common group of organisms in the fourth trophic level that lay their eggs in or on the body of other parasitoid hosts. Such top carnivores use herbivore-induced plant volatiles (HIPVs) to find caterpillars containing parasitoid host larvae. Hyperparasitoids forage in complex environments where hosts of different quality may be present alongside non-host parasitoid species, each of which can develop in multiple herbivore species. Because both the identity of the herbivore species and its parasitization status can affect the composition of HIPV emission, Hyperparasitoids encounter considerable variation in HIPVs during host location. Here, we combined laboratory and field experiments to investigate the role of HIPVs in host selection of Hyperparasitoids that search for hosts in a multi-parasitoid multi-herbivore context. In a wild Brassica oleracea-based food web, the hyperparasitoid Lysibia nana preferred HIPVs emitted in response to caterpillars parasitized by the gregarious host Cotesia glomerata over the non-host Hyposoter ebeninus. However, no plant-mediated discrimination occurred between the solitary host C. rubecula and the non-host H. ebeninus. Under both laboratory and field conditions, hyperparasitoid responses were not affected by the herbivore species (Pieris brassicae or P. rapae) in which the three primary parasitoid species developed. Our study shows that HIPVs are an important source of information within multitrophic interaction networks allowing Hyperparasitoids to find their preferred hosts in heterogeneous environments.

  • Symbiotic polydnavirus and venom reveal parasitoid to its Hyperparasitoids.
    Proceedings of the National Academy of Sciences of the United States of America, 2018
    Co-Authors: F. Zhu, Antonino Cusumano, Marcel Dicke, Jeffrey A. Harvey, Berhane T. Weldegergis, Janneke Bloem, Nina E. Fatouros, J.j.a. Van Loon, Alexandre Villela, Heiko Vogel
    Abstract:

    Symbiotic relationships may provide organisms with key innovations that aid in the establishment of new niches. For example, during oviposition, some species of parasitoid wasps, whose larvae develop inside the bodies of other insects, inject polydnaviruses into their hosts. These symbiotic viruses disrupt host immune responses, allowing the parasitoid’s progeny to survive. Here we show that symbiotic polydnaviruses also have a downside to the parasitoid’s progeny by initiating a multitrophic chain of interactions that reveals the parasitoid larvae to their enemies. These enemies are Hyperparasitoids that use the parasitoid progeny as host for their own offspring. We found that the virus and venom injected by the parasitoid during oviposition, but not the parasitoid progeny itself, affected hyperparasitoid attraction toward plant volatiles induced by feeding of parasitized caterpillars. We identified activity of virus-related genes in the caterpillar salivary gland. Moreover, the virus affected the activity of elicitors of salivary origin that induce plant responses to caterpillar feeding. The changes in caterpillar saliva were critical in inducing plant volatiles that are used by Hyperparasitoids to locate parasitized caterpillars. Our results show that symbiotic organisms may be key drivers of multitrophic ecological interactions. We anticipate that this phenomenon is widespread in nature, because of the abundance of symbiotic microorganisms across trophic levels in ecological communities. Their role should be more prominently integrated in community ecology to understand organization of natural and managed ecosystems, as well as adaptations of individual organisms that are part of these communities.

  • Data from: Symbiotic polydnavirus and venom reveal parasitoid to its Hyperparasitoids
    2018
    Co-Authors: F. Zhu, Antonino Cusumano, Marcel Dicke, Jeffrey A. Harvey, Berhane T. Weldegergis, Janneke Bloem, A. Nunes Villela, Nina E. Fatouros, J.j.a. Van Loon, Heiko Vogel
    Abstract:

    Symbiotic relationships may provide organisms with key innovations that aid in the establishment of new niches. For example, during oviposition, some species of parasitoid wasps, whose larvae develop inside the bodies of other insects, inject polydnaviruses into their hosts. These symbiotic viruses disrupt host immune responses, allowing the parasitoid’s progeny to survive. Here, we show that symbiotic polydnaviruses also have a downside to the parasitoid’s progeny by initiating a multi-trophic chain of interactions that reveals the parasitoid larvae to their enemies. These enemies are Hyperparasitoids that use the parasitoid progeny as host for their own offspring. We found that the virus and venom injected by the parasitoid during oviposition, but not the parasitoid progeny itself, affected hyperparasitoid attraction towards plant volatiles induced by feeding of parasitized caterpillars We identified activity of virus-related genes in the caterpillar salivary gland. Moreover, the virus affected the activity of elicitors of salivary origin that induce plant responses to caterpillar feeding. The changes in caterpillar saliva were critical in inducing plant volatiles that are used by hyperparsitoids to locate parasitized caterpillars. Our results show that symbiotic organisms may be key drivers of multi-trophic ecological interactions. We anticipate that this phenomenon is widespread in nature, because of the abundance of symbiotic microorganisms across trophic levels in ecological communities. Their role should be more prominently integrated in community ecology to understand organization of natural and managed ecosystems as well as adaptations of individual organisms that are part of these communities.

  • Parasitism overrides herbivore identity allowing Hyperparasitoids to locate their parasitoid host using herbivore-induced plant volatiles
    Molecular ecology, 2015
    Co-Authors: F. Zhu, Marcel Dicke, Jeffrey A. Harvey, Berhane T. Weldegergis, Colette Broekgaarden, Ben Vosman, Erik H. Poelman
    Abstract:

    Foraging success of predators profoundly depends on reliable and detectable cues indicating the presence of their often inconspicuous prey. Carnivorous insects rely on chemical cues to optimize foraging efficiency. Hyperparasitoids that lay their eggs in the larvae or pupae of parasitic wasps may find their parasitoid hosts developing in different herbivores. They can use herbivore-induced plant volatiles (HIPVs) to locate parasitized caterpillars. Because different herbivore species induce different HIPV emission from plants, Hyperparasitoids may have to deal with large variation in volatile information that indicates host presence. In this study, we used an ecogenomics approach to first address whether parasitized caterpillars of two herbivore species (Pieris rapae and P. brassicae) induce similar transcriptional and metabolomic responses in wild Brassica oleracea plants and, second, whether Hyperparasitoids Lysibia nana are able to discriminate between these induced plant responses to locate their parasitoid host in different herbivores under both laboratory and field conditions. Our study revealed that both herbivore identity and parasitism affect plant transcriptional and metabolic responses to herbivory. We also found that Hyperparasitoids are able to respond to HIPVs released by wild B. oleracea under both laboratory and field conditions. In addition, we observed stronger attraction of Hyperparasitoids to HIPVs when plants were infested with parasitized caterpillars. However, Hyperparasitoids were equally attracted to plants infested by either herbivore species. Our results indicate that parasitism plays a major role in HIPV-mediated plant-hyperparasitoid interactions. Furthermore, these findings also indicate that plant trait-mediated indirect interaction networks play important roles in community-wide species interactions.

  • Body odors of parasitized caterpillars give away the presence of parasitoid larvae to their primary hyperparasitoid enemies.
    Journal of chemical ecology, 2014
    Co-Authors: F. Zhu, Marcel Dicke, Jeffrey A. Harvey, Berhane T. Weldegergis, Boris Lhie, Erik H. Poelman
    Abstract:

    Foraging success of parasitoids depends on the utilization of reliable information on the presence of their often, inconspicuous hosts. These parasitic wasps use herbivore-induced plant volatiles (HIPVs) that provide reliable cues on host presence. However, host searching of Hyperparasitoids, a group of parasitoids that parasitize the larvae and pupae of other parasitoids, is more constrained. Their hosts do not feed on plants, and often are even concealed inside the body of the herbivore host. Hyperparasitoids recently have been found to use HIPVs of plants damaged by herbivore hosts in which the parasitoid larvae develop. However, Hyperparasitoids that search for these parasitoid larvae may be confronted with healthy and parasitized caterpillars on the same plant, further complicating their host location. In this study, we addressed whether the primary hyperparasitoid Baryscapus galactopus uses caterpillar body odors to discriminate between unparasitized herbivores and herbivores carrying larvae of parasitoid hosts. We show that the Hyperparasitoids made faster first contact and spent a longer mounting time with parasitized caterpillars. Moreover, although the three parasitoid hosts conferred different fitness values for the development of B. galactopus, the Hyperparasitoids showed similar behavioral responses to caterpillar hosts carrying different primary parasitoid hosts. In addition, a two-chamber olfactometer assay revealed that volatiles emitted by parasitized caterpillars were more attractive to the Hyperparasitoids than those emitted by unparasitized caterpillars. Analysis of volatiles revealed that body odors of parasitized caterpillars differ from unparasitized caterpillars, allowing the Hyperparasitoids to detect their parasitoid host.

Louise E. M. Vet - One of the best experts on this subject based on the ideXlab platform.

  • Honeydew composition and its effect on life-history parameters of Hyperparasitoids
    Ecological Entomology, 2019
    Co-Authors: Frank A. C. Van Neerbos, Jetske G. Boer, Lucia Salis, Ward Tollenaar, Martine Kos, Louise E. M. Vet, Jeffrey A. Harvey
    Abstract:

    1. Diets that maximise life span often differ from diets that maximise reproduction. Animals have therefore evolved advanced foraging strategies to acquire optimal nutrition and maximise their fitness. The free-living adult females of parasitoid wasps (Hymenoptera) need to balance their search for hosts to reproduce and for carbohydrate resources to feed. 2. Honeydew, excreted by phloem-feeding insects, presents a widely available carbohydrate source in nature that can benefit natural enemies of honeydew-producing insects. However, the effects of variation in honeydew on organisms in the fourth trophic level, such as Hyperparasitoids, are not yet understood. 3. This study examined how five different honeydew types influence longevity and fecundity of four hyperparasitoid taxa. Asaphes spp. (Pteromalidae) and Dendrocerus spp. (Megaspilidae) are secondary parasitoids of aphid parasitoids and are thus associated with honeydew-producing insects. Gelis agilis and Acrolyta nens (both Ichneumonidae) are secondary parasitoids of species that do not use honeydew-producing hosts. 4. Most honeydew types had a positive or neutral effect on life span and fecundity of Hyperparasitoids compared with controls without honeydew, although negative effects were also found for both aphid Hyperparasitoids. Honeydew produced by aphids feeding on sweet pepper plants was most beneficial for all hyperparasitoid taxa, which can partially be explained by the high amount of honeydew, but also by the composition of dietary sugars in these honeydew types. 5. The findings of this study underline the value of aphid honeydew as a carbohydrate resource for fourth-trophic-level organisms, not only those associated with honeydew-producing insects but also ?interlopers? without such a natural association.

  • Effects of temperature and food source on reproduction and longevity of aphid Hyperparasitoids of the genera Dendrocerus and Asaphes
    BioControl, 2019
    Co-Authors: Jetske G. Boer, Jeffrey A. Harvey, Lucia Salis, Ward Tollenaar, Martine Kos, Lisa J. M. Van Heumen, Thibault P. M. Costaz, Louise E. M. Vet
    Abstract:

    Hyperparasitoids of aphid parasitoids commonly occur in (sweet pepper) greenhouses, and can pose a threat to effective biological control of aphids. Here, we studied life history characteristics of laboratory colonies of Dendrocerus spp. Ratzeburg (Hymenoptera: Megaspilidae) and Asaphes spp. Walker (Pteromalidae) that originated from a commercial sweet pepper greenhouse. We aimed to clarify how these two hyperparasitoid taxa can coexist inside greenhouses. Hyperparasitoids of both taxa have a long lifespan that was extended significantly by food sources that are naturally available in a greenhouse environment, including aphid honeydew and sweet pepper flowers. Differences in sensitivity to decreased or increased temperatures did not appear to explain seasonal patterns in abundance of Dendrocerus spp. and Asaphes spp. in sweet pepper greenhouses. Instead, Dendrocerus spp. may have an advantage early in the season because it thrives on aphid honeydew, while Asaphes spp. may do better later in the season because of its long lifespan and extensive reproductive period.

  • Honeydew composition and its effect on life‐history parameters of Hyperparasitoids
    'Wiley', 2019
    Co-Authors: Van Neerbos, Frank Antonie Cornelus, Louise E. M. Vet, De Boer, Jetske G, Salis Lucia, Tollenaar Ward, Kos Martine, Harvey, Jeffrey A.
    Abstract:

    1. Diets that maximise life span often differ from diets that maximise reproduction. Animals have therefore evolved advanced foraging strategies to acquire optimal nutrition and maximise their fitness. The free‐living adult females of parasitoid wasps (Hymenoptera) need to balance their search for hosts to reproduce and for carbohydrate resources to feed. 2. Honeydew, excreted by phloem‐feeding insects, presents a widely available carbohydrate source in nature that can benefit natural enemies of honeydew‐producing insects. However, the effects of variation in honeydew on organisms in the fourth trophic level, such as Hyperparasitoids, are not yet understood. 3. This study examined how five different honeydew types influence longevity and fecundity of four hyperparasitoid taxa. Asaphes spp. (Pteromalidae) and Dendrocerus spp. (Megaspilidae) are secondary parasitoids of aphid parasitoids and are thus associated with honeydew‐producing insects. Gelis agilis and Acrolyta nens (both Ichneumonidae) are secondary parasitoids of species that do not use honeydew‐producing hosts. 4. Most honeydew types had a positive or neutral effect on life span and fecundity of Hyperparasitoids compared with controls without honeydew, although negative effects were also found for both aphid Hyperparasitoids. Honeydew produced by aphids feeding on sweet pepper plants was most beneficial for all hyperparasitoid taxa, which can partially be explained by the high amount of honeydew, but also by the composition of dietary sugars in these honeydew types. 5. The findings of this study underline the value of aphid honeydew as a carbohydrate resource for fourth‐trophic‐level organisms, not only those associated with honeydew‐producing insects but also ‘interlopers’ without such a natural association.status: Published onlin

  • Comparing and contrasting life history variation in four aphid Hyperparasitoids
    Ecological Entomology, 2017
    Co-Authors: R. Buitenhuis, Jeffrey A. Harvey, Louise E. M. Vet, Guy Boivin, Jacques Brodeur
    Abstract:

    1. In primary parasitoids, significant differences in life history and reproductive traits are observed among parasitoids attacking different stages of the same host species. Much less is known about Hyperparasitoids, which attack different stages of primary parasitoids. 2. Parasitoids exploit hosts in two different ways. Koinobionts attack hosts that continue feeding and growing during parasitism, whereas idiobionts paralyse hosts before oviposition or attack non-growing host stages, e.g. eggs or pupae. 3. Koino-/idiobiosis in primary parasitoids are often associated with different expression of life history trade-offs, e.g. endo- versus ectoparasitism, high versus low fecundity and short versus long life span. 4. In the present study, life history parameters of two koinobiont endoparasitic species (Alloxysta victrix; Syrphophagus aphidivorus), and two idiobiont ectoparasitic species (Asaphes suspensus; Dendrocerus carpenteri) of aphid Hyperparasitoids were compared. These Hyperparasitoids attack either the parasitoid larva in the aphid before it is killed and mummified by the primary parasitoid or the parasitoid prepupa or pupa in the dead aphid mummy. 5. There was considerable variation in reproductive success and longevity in the four species. The idiobiont A. suspensus produced the most progeny by far and had the longest lifespan. In contrast, the koinobiont A. victrix had the lowest fecundity. Other developments and life history parameters in the different species were variable. 6. The present results reveal that there was significant overlap in life history and reproductive traits among hyperparasitoid koinobionts and idiobionts, even when attacking the same host species, suggesting that selection for expression of these traits is largely association specific.

  • Development of a hyperparasitoid wasp in different stages of its primary parasitoid and secondary herbivore hosts.
    Journal of insect physiology, 2012
    Co-Authors: Jeffrey A. Harvey, Rieta Gols, Louise E. M. Vet, H. Marjolein Kruidhof
    Abstract:

    Parasitoid wasps are model organisms for exploring constraints on life history and development strategies in arthropods. Koinobiont parasitoids attack hosts that may vary considerably in size at parasitation. Thus far, studies exploring koinobiont development in hosts of different size have been exclusively done with primary parasitoids attacking insect herbivores. However, the larvae of primary koinobiont parasitoids may in turn be attacked by koinobiont Hyperparasitoids. We examined development of the gregarious hyperparasitoid Baryscapus galactopus in different stages of its primary parasitoid host, Cotesia glomerata, itself developing in different stages of caterpillars of the cabbage butterfly, Pieris brassicae. This is the first study exploring hyperparasitoid development in different stages of a primary and secondary host. Second instar (L2) larvae of P. brassicae were parasitized by C. glomerata, and separate cohorts of L3 to L5 P. brassicae containing different stages of C. glomerata were then presented to B. galactopus females. B. galactopus was able to parasitize tiny larvae of C. glomerata in L3 caterpillars of P. brassicae, but hyperparasitism efficiency increased in later instars of both C. glomerata and P. brassicae. Development time of B. galactopus was extended in younger C. glomerata/P. brassicae hosts, whereas adult mass was largest when C. glomerata was attacked in L3 through early L5 P. brassicae. Our results show that B. galactopus adjusts its development rate in accordance with the size of both its primary and secondary hosts, in order to ensure survival. Adaptive responses to phylogenetic constraints on the development of primary Hyperparasitoids are discussed.