https://doi.org/10.1093/ee/nvae002
Journal: Environmental Entomology, 2024, №2, p.213-222
Publisher: Oxford University Press (OUP)
Authors: Robert K Straser, Kent M Daane, Judith M Stahl, Houston Wilson
Abstract
Abstract The diet of adult parasitoid wasps is vital for their survival and reproduction. However, the availability of food resources, such as plant nectar, can vary widely in cropping systems, potentially affecting parasitoid fitness and thereby biological control of pests. The egg parasitoid Hadronotus pennsylvanicus (Ashmead) (Hymenoptera: Scelionidae) is a potential biological control agent of the pistachio pest Leptoglossus zonatus (Dallas) (Heteroptera: Coreidae). While H. pennsylvanicus is known to attack L. zonatus eggs in California, USA, parasitism rates in orchards are highly variable. Floral resource provisioning has the potential to enhance parasitoid longevity and thus improve parasitism rates, leading to reduced pest densities. Here, a combination of field and laboratory studies was used to assess the influence of flowering groundcovers on the reproductive fitness of H. pennsylvanicus and the abundance of L. zonatus. Evaluated groundcovers included oat (Avena sativa L.), cowpea (Vigna unguiculata L.), white mustard (Sinapis alba L.), and buckwheat (fa*gopyrum esculentum Moench). Under laboratory conditions, buckwheat and mustard provided the greatest benefit to female H. pennsylvanicus longevity. However, females provided a buckwheat diet produced the greatest number of offspring over the course of their lifetime. In field trials, flowering groundcovers did not influence the abundance of H. pennsylvanicus nor parasitism rates on L. zonatus. While the availability of floral resources can improve the reproductive fitness of H. pennsylvanicus, the use of groundcovers in pistachio did not enhance biological control of L. zonatus.
Funders
- Western Sustainable Agriculture Research and Education Program
- Robert and Peggy van den Bosch Memorial Scholarship, the California Pistachio Research Board
- California Department of Food and Agriculture Specialty Crop Block Grant Program
- USDA NIFA Hatch Project
List of references
- Akotsen-Mensah, Evaluating potential trap crops for managing leaffooted bug (Hemiptera: Coreidae) and phytophagous stink bug (Hemiptera: Pentatomidae) species in peaches, Agric For Entomol, с. 332
- Bates, Fitting linear mixed-effects models using lme4, J Stat Softw, № 67, с. 1
https://doi.org/10.18637/jss.v067.i01
- Benelli, The impact of adult diet on parasitoid reproductive performance, J Pest Sci, с. 807
- Carmona, Influence of refuge habitats and cover crops on seasonal activity and density of ground beetles (Coleoptera: Carabidae) in field crops, Environ Entomol, с. 1145
- Chaplin-Kramer, A meta-analysis of crop pest and natural enemy response to landscape complexity, Ecol Lett, с. 922
- Colazza, Chemo-orientation responses in hymenopteran parasitoids induced by substrate-borne semiochemicals, BioControl, № 59, с. 1
https://doi.org/10.1007/s10526-013-9546-7
- Cornelius, Use of flowering plants to enhance parasitism and predation rates on two squash bug species Anasa tristis and Anasa armigera (Hemiptera: Coreidae), Insects, с. 318
- Cornelius, Impact of the egg parasitoid, Gryon pennsylvanicum (Hymenoptera: Scelionidae), on sentinel and wild egg masses of the squash bug (Hemiptera: Coreidae) in Maryland, Environ Entomol, с. 367
- Cornelius, Comparative study of egg parasitism by Gryon pennsylvanicum (Hymenoptera: Scelionidae) on two squash bug species Anasa tristis and Anasa armigera (Hemiptera: Coreidae), Environ Entomol, с. 1451
- Cornelius, Ovipositional behavior of the egg parasitoid Gryon pennsylvanicum (Hymenoptera: Scelionidae) on two squash bug species Anasa tristis (Hemiptera: Coreidae) and Anasa armigera: effects of parasitoid density, nutrition, and host egg chorion on parasitism rates, Environ Entomol, с. 1307
- Crowder, Relationships between biodiversity and biological control in agroecosystems: current status and future challenges, Biol Control, с. 8
- Daane, Large bugs damage pistachio nuts most severely during midseason, Calif Agric, № 59, с. 95
https://doi.org/10.3733/ca.v059n02p95
- Daane, Stink bugs and leaffooted bugs, Pistachio production manual, с. 225
- Duyck, Addition of a new resource in agroecosystems: do cover crops alter the trophic positions of generalist predators, Basic Appl Ecol, с. 47
- Ellers, Discriminating between energetic content and dietary composition as an explanation for dietary restriction effects, J Insect Physiol, с. 1670
- Fair, Assessment of habitat modification and varied planting dates to enhance potential natural enemies of Anasa tristis (Hemiptera: Coreidae) in squash, Environ Entomol, № 46, с. 291
https://doi.org/10.1093/ee/nvx043
- Fiedler, Maximizing ecosystem services from conservation biological control: the role of habitat management, Biol Control, с. 254
- Foresti, Economic injury levels and economic thresholds for Leptoglossus zonatus (Dallas) (Hemiptera: Coreidae) infesting seed maize, Pest Manag Sci, № 74, с. 149
https://doi.org/10.1002/ps.4671
- Gillespie, Beyond nectar provision: the other resource requirements of parasitoid biological control agents, Entomol Exp Appl, с. 207
- Gurr, Habitat management to suppress pest populations: progress and prospects, Annu Rev Entomol, с. 91
- Haviland, Pistachios: insects and mites, University of California IPM Pest Management Guidelines, с. 3461
- Hothorn, Simultaneous inference in general parametric models, Biom J, с. 346
- Jervis, Resource acquisition, allocation, and utilization in parasitoid reproductive strategies, Annu Rev Entomol, с. 361
- Jones, Sentinel eggs underestimate rates of parasitism of the exotic brown marmorated stink bug, Halyomorpha halys, Biol Control, с. 61
- Joyce, Assessing feeding damage from two leaffooted bugs, Leptoglossus clypealis Heidemann and Leptoglossus zonatus (Dallas) (Hemiptera: Coreidae), on four almond varieties, Insects, с. 333
- Kishinevsky, Sugar feeding of parasitoids in an agroecosystem: effects of community composition, habitat and vegetation, Insect Conserv Divers, с. 50
- Landis, Habitat management to conserve natural enemies of arthropod pests in agriculture, Annu Rev Entomol, с. 175
- Maltese, Parasitoids of Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) recovered in western North America and first record of its egg parasitoid Gryon pennsylvanicum (Ashmead) (Hymenoptera: Platygastridae) in California, Pan-Pacific Entomol, с. 347
- Marchiori, Natural enemies of Leptoglossus zonatus (Dallas, 1852) (Hemiptera: Coreidae) on maize in Itumbiara, Goias, Biotemas, № 15, с. 69
- Masner, A revision of Gryon Haliday in North America (Hymenoptera: Proctotrupoidea: Scelionidae), Can Entomol, с. 123
- Michailides, The ‘Achilles heel’ of pistachio fruit, Calif Agric, № 43, с. 10
- Mitchell, Parasitism and predation of leaffooted bug (Hemiptera: Heteroptera: Coreidae) eggs, Ann Entomol Soc Am, с. 854
- Mitchell, Natural mortality of leaf footed bug (Hemiptera: Heteroptera: Coreidae) eggs in cowpea, J Agric Urban Entomol, № 16, с. 25
- Nechols, Comparative ecological studies of indigenous egg parasitoids (Hymenoptera: Scelionidae: Encyrtidae) of the squash bug, Anasa tristis (Hemiptera: Coreidae), J Kans Entomol Soc, с. 177
- Nielsen, Identifying a potential trap crop for a novel insect pest, Halyomorpha halys (Hemiptera: Pentatomidae), in organic farms, Environ Entomol, с. 472
- Nilsson, Ignoring ecosystem service cascades undermines policy for multifunctional agricultural landscapes, Front Ecol Evol, № 5, с. 109
https://doi.org/10.3389/fevo.2017.00109
- Olson, Effects of squash leaf trichome exudates and honey on adult feeding, survival, and fecundity of the squash bug (Heteroptera: Coreidae) egg parasitoid Gryon pennsylvanicum (Hymenoptera: Scelionidae), Environ Entomol, с. 454
- R Core Team, R: a language and environment for statistical computing
- Rivero, Species, seasonal occurrence, and natural enemies of stink bugs and leaffooted bugs (Hemiptera: Pentatomidae, Coreidae, Largidae) in pecans, Southwest Entomol, № 34, с. 305
https://doi.org/10.3958/059.034.0311
- Roversi, Pre-release risk assessment of the egg parasitoid Gryon pennsylvanicum for classical biological control of Leptoglossus occidentalis, J Appl Entomol, с. 27
- Russell, A meta-analysis of physiological and behavioral responses of parasitoid wasps to flowers of individual plant species, Biol Control, с. 96
- Sabbatini Peverieri, Host egg age of Leptoglossus occidentalis (Heteroptera: Coreidae) and parasitism by Gryon pennsylvanicum (Hymenoptera: Platygastridae), J Econ Entomol, № 106, с. 633
https://doi.org/10.1603/EC12344
- Sabbatini Peverieri, Long-term storage of eggs of Leptoglossus occidentalis for the mass-rearing of its parasitoid Gryon pennsylvanicum, BioControl, с. 293
- Sabbatini Peverieri, Laboratory evaluation of Gryon pennsylvanicum (Ashmead) (Hymenoptera: Platygastridae) as a biological control agent of Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae), Biol Control, с. 104
- Segoli, Spatial and temporal variation in sugar availability for insect parasitoids in agricultural fields and consequences for reproductive success, Biol Control, с. 163
- Stahl, Comparing the feeding damage of the invasive brown marmorated stink bug to a native stink bug and leaffooted bug on California pistachios, Insects, с. 688
- Stahl, Irrigated trap crops impact key hemipteran pests in organic pistachio orchard, Arthropod Plant Interact, с. 949
- Straser, Evaluation of egg parasitoid Hadronotus pennsylvanicus as a prospective biocontrol agent of the leaffooted bug Leptoglossus zonatus, BioControl, с. 123
- Straser, Food deprivation alters reproductive performance of biocontrol agent Hadronotus pennsylvanicus, Sci Rep, с. 7129
- Straser, Diet quality influences nutrient retention and reproductive fitness of biocontrol agent Hadronotus pennsylvanicus (Hymenoptera: Scelionidae), J Insect Physiol, с. 104522
- Talamas, A maximalist approach to the systematics of a biological control agent: Gryon aetherium Talamas, sp nov (Hymenoptera, Scelionidae), J Hymenopt Res, № 23, с. 323
https://doi.org/10.3897/jhr.87.72842
- Tena, Sugar provisioning maximizes the biocontrol service of parasitoids, J Appl Ecol, с. 795
- Tscharntke, Conservation biological control and enemy diversity on a landscape scale, Biol Control, № 45, с. 238
https://doi.org/10.1016/S1049-9644(08)00082-0
- Tscharntke, When natural habitat fails to enhance biological pest control—five hypotheses, Biol Conserv, с. 449
- Tscharntke, Landscape perspectives on agricultural intensification and biodiversity on ecosystem service management, Ecol Lett, № 8, с. 857
https://doi.org/10.1111/j.1461-0248.2005.00782.x
- Wäckers, Food for protection: an introduction, Plant-provided food for carnivorous insects, с. 1
https://doi.org/10.1017/CBO9780511542220.002
- Wade, Excised or intact inflorescences? Methodological effects on parasitoid wasp longevity, Biol Control, с. 347
- Wan, Ecological engineering of trap cropping promotes biocontrol services in peach orchard ecosystems, Ecol Eng, с. 427
- Wilson, Landscape diversity and crop vigor out weight influence of local diversification on biological control of a vineyard pest, Ecosphere, № 8, с. e01736
https://doi.org/10.1002/ecs2.1736
- Xiao, Evaluation of damage to satsuma mandarin (Citrus unshiu) by the leaffooted bug, Leptoglossus zonatus (Hemiptera: Coreidae), J Appl Entomol, с. 694
- Zalom, Almonds: insects and mites, University of California IPM Pest Management Guidelines, Publication 3431 ed
- Zhu, Relevance of the ecological traits of parasitoid wasps and nectariferous plants for conservation biological control: a hybrid meta-analysis, Pest Manag Sci, с. 1881
Publications that cite this publication
Flourishing with sugars - following the fate of parasitoids in the field
Jana C Lee
Transcriptomic Insights into Host Metabolism and Immunity Changes after Parasitization by Leptopilina myrica
Junwei Zhang, Jieyu Shan, Wenqi Shi, Ting Feng, Yifeng Sheng, Zixuan Xu, Zhi Dong, Jianhua Huang, Jiani Chen
https://doi.org/10.3390/insects15050352 ·
2024, Insects, №5, p.352
Scopus
WoS
Crossref citations:0
Find all citations of the publication
About this publication
Number of citations | 1 |
Number of works in the list of references | 62 |
Journal indexed in Scopus | Yes |
Journal indexed in Web of Science | Yes |