Altered feeding behavior and immune competence in paper wasps: A case of parasite manipulation?

Laura Beani; Marta Mariotti Lippi; Nadia Mulinacci; Fabio Manfredini; Lorenzo Cecchi; Claudia Giuliani; Corrado Tani; Niccolò Meriggi; Duccio Cavalieri; Federico Cappa

doi:10.1371/journal.pone.0242486

Altered feeding behavior and immune competence in paper wasps: A case of parasite manipulation?

Laura Beani^* (Corresponding Author), Marta Mariotti Lippi, Nadia Mulinacci, Fabio Manfredini, Lorenzo Cecchi, Claudia Giuliani, Corrado Tani, Niccolò Meriggi, Duccio Cavalieri^* (Corresponding Author), Federico Cappa

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

Research output: Contribution to journal › Article › peer-review

4 Citations (Scopus)

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Abstract

Paper wasps (Polistes dominula), parasitized by the strepsipteran Xenos vesparum, are castrated and desert the colony to gather on plants where the parasite mates and releases primary larvae, thus completing its lifecycle. One of these plants is the trumpet creeper Campsis radicans: in a previous study the majority of all wasps collected from this plant were parasitized and focused their foraging activity on C. radicans buds. The unexpected prevalence and unusual feeding strategy prompted us to investigate the influence of this plant on wasp behavior and physiology through a multidisciplinary approach. First, in a series of laboratory bioassays, we observed that parasitized wasps spent more time than non-parasitized ones on fresh C. radicans buds, rich of extra-floral nectaries (EFNs), while the same wasps ignored treated buds that lacked nectar drops. Then, we described the structure and ultra-structure of EFNs secreting cells, compatible with the synthesis of phenolic compounds. Subsequently, we analysed extracts from different bud tissues by HPLCDAD- MS and found that verbascoside was the most abundant bioactive molecule in those tissues rich in EFNs. Finally, we tested the immune-stimulant properties of verbascoside, as the biochemical nature of this compound indicates it might function as an antibacterial and antioxidant. We measured bacterial clearance in wasps, as a proxy for overall immune competence, and observed that it was enhanced after administration of verbascoside - even more so if the wasp was parasitized. We hypothesize that the parasite manipulates wasp behavior to preferentially feed on C. radicans EFNs, since the bioactive properties of verbascoside likely increase host survival and thus the parasite own fitness.

Original language	English
Article number	e0242486
Number of pages	16
Journal	PloS ONE
Volume	15
Issue number	12
Early online date	16 Dec 2020
DOIs	https://doi.org/10.1371/journal.pone.0242486
Publication status	Published - 16 Dec 2020

Bibliographical note

Acknowledgments
The authors are grateful to Rita Cervo, Stefano Turillazzi and the members of the Florence Group for the Study of Social Wasps, first of all to Irene Pepiciello, for their assistance during this study, both in the field and in the laboratory. The authors also thank two anonymous Reviewers for their helpful comments and suggestions.
Financial support to LB was provided by the University of Florence.

Data Availability Statement

Data are available at https://osf.io/jfvm2/quickfiles.

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Cite this

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title = "Altered feeding behavior and immune competence in paper wasps: A case of parasite manipulation?",

abstract = "Paper wasps (Polistes dominula), parasitized by the strepsipteran Xenos vesparum, are castrated and desert the colony to gather on plants where the parasite mates and releases primary larvae, thus completing its lifecycle. One of these plants is the trumpet creeper Campsis radicans: in a previous study the majority of all wasps collected from this plant were parasitized and focused their foraging activity on C. radicans buds. The unexpected prevalence and unusual feeding strategy prompted us to investigate the influence of this plant on wasp behavior and physiology through a multidisciplinary approach. First, in a series of laboratory bioassays, we observed that parasitized wasps spent more time than non-parasitized ones on fresh C. radicans buds, rich of extra-floral nectaries (EFNs), while the same wasps ignored treated buds that lacked nectar drops. Then, we described the structure and ultra-structure of EFNs secreting cells, compatible with the synthesis of phenolic compounds. Subsequently, we analysed extracts from different bud tissues by HPLCDAD- MS and found that verbascoside was the most abundant bioactive molecule in those tissues rich in EFNs. Finally, we tested the immune-stimulant properties of verbascoside, as the biochemical nature of this compound indicates it might function as an antibacterial and antioxidant. We measured bacterial clearance in wasps, as a proxy for overall immune competence, and observed that it was enhanced after administration of verbascoside - even more so if the wasp was parasitized. We hypothesize that the parasite manipulates wasp behavior to preferentially feed on C. radicans EFNs, since the bioactive properties of verbascoside likely increase host survival and thus the parasite own fitness.",

author = "Laura Beani and Lippi, {Marta Mariotti} and Nadia Mulinacci and Fabio Manfredini and Lorenzo Cecchi and Claudia Giuliani and Corrado Tani and Niccol{\`o} Meriggi and Duccio Cavalieri and Federico Cappa",

note = "Acknowledgments The authors are grateful to Rita Cervo, Stefano Turillazzi and the members of the Florence Group for the Study of Social Wasps, first of all to Irene Pepiciello, for their assistance during this study, both in the field and in the laboratory. The authors also thank two anonymous Reviewers for their helpful comments and suggestions. Financial support to LB was provided by the University of Florence.",

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AU - Beani, Laura

AU - Lippi, Marta Mariotti

AU - Mulinacci, Nadia

AU - Manfredini, Fabio

AU - Cecchi, Lorenzo

AU - Giuliani, Claudia

AU - Tani, Corrado

AU - Meriggi, Niccolò

AU - Cavalieri, Duccio

AU - Cappa, Federico

N1 - Acknowledgments The authors are grateful to Rita Cervo, Stefano Turillazzi and the members of the Florence Group for the Study of Social Wasps, first of all to Irene Pepiciello, for their assistance during this study, both in the field and in the laboratory. The authors also thank two anonymous Reviewers for their helpful comments and suggestions. Financial support to LB was provided by the University of Florence.

PY - 2020/12/16

Y1 - 2020/12/16

N2 - Paper wasps (Polistes dominula), parasitized by the strepsipteran Xenos vesparum, are castrated and desert the colony to gather on plants where the parasite mates and releases primary larvae, thus completing its lifecycle. One of these plants is the trumpet creeper Campsis radicans: in a previous study the majority of all wasps collected from this plant were parasitized and focused their foraging activity on C. radicans buds. The unexpected prevalence and unusual feeding strategy prompted us to investigate the influence of this plant on wasp behavior and physiology through a multidisciplinary approach. First, in a series of laboratory bioassays, we observed that parasitized wasps spent more time than non-parasitized ones on fresh C. radicans buds, rich of extra-floral nectaries (EFNs), while the same wasps ignored treated buds that lacked nectar drops. Then, we described the structure and ultra-structure of EFNs secreting cells, compatible with the synthesis of phenolic compounds. Subsequently, we analysed extracts from different bud tissues by HPLCDAD- MS and found that verbascoside was the most abundant bioactive molecule in those tissues rich in EFNs. Finally, we tested the immune-stimulant properties of verbascoside, as the biochemical nature of this compound indicates it might function as an antibacterial and antioxidant. We measured bacterial clearance in wasps, as a proxy for overall immune competence, and observed that it was enhanced after administration of verbascoside - even more so if the wasp was parasitized. We hypothesize that the parasite manipulates wasp behavior to preferentially feed on C. radicans EFNs, since the bioactive properties of verbascoside likely increase host survival and thus the parasite own fitness.

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Altered feeding behavior and immune competence in paper wasps: A case of parasite manipulation?

Abstract

Bibliographical note

Data Availability Statement

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