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      Parasitoid-induced changes in metabolic rate and feeding activity of the emerald ash borer (Coleoptera: Buprestidae): implications for biological control

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      Scientific Reports
      Nature Publishing Group UK
      Ecology, Physiology

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          Abstract

          Parasitoid-host interactions form the foundation of biological control strategies against many agriculture and forest insect pests. The emerald ash borer (EAB), Agrilus planipennis (Coleoptera: Buprestidae), is a serious invasive pest of ash ( Fraxinus spp.) trees in North America. Tetrastichus planipennisi (Hymenoptera: Eulophidae) is a gregarious, koinobiont endoparasitoid, attacking late (3rd to 4th) instars of EAB larvae, which feed in the live phloem of ash trunks or branches, making serpentine-like galleries filled with larval frass. In the present study, we tested the hypothesis that T. planipennisi regulates the host metabolism and feeding activity to optimize its offspring development and fitness. We first compared the respiration rate of parasitized and unparasitized host larvae at different times after parasitism, and then measured feeding activity of both parasitized and unparasitized host larvae inside their feeding galleries. Although parasitized host larvae increased metabolic rate and feeding activity in the first few days of parasitism, T. planipennisi parasitism induced an overall reduction of the metabolic rate and decrease in feeding activity of parasitized host larvae over their development period. In addition, there was a negative relationship between feeding activity of parasitized hosts and brood sizes of the parasitoid progeny—i.e., the more parasitoid progeny a host larva received, the less feeding activity the host had. These findings suggest that T. planipennisi has limited ability to optimize its offspring development and fitness through regulations of the host metabolism and feeding activity and its parasitism reduces feeding damage of parasitized EAB larvae to infested ash trees.

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          Most cited references36

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          Manipulation of host behavior by parasitic insects and insect parasites.

          Parasites often alter the behavior of their hosts in ways that are ultimately beneficial to the parasite or its offspring. Although the alteration of host behavior by parasites is a widespread phenomenon, the underlying neuronal mechanisms are only beginning to be understood. Here, we focus on recent advances in the study of behavioral manipulation via modulation of the host central nervous system. We elaborate on a few case studies, in which recently published data provide explanations for the neuronal basis of parasite-induced alteration of host behavior. Among these, we describe how a worm may influence the nervous system of its cricket host and manipulate the cricket into committing suicide by jumping into water. We then focus on Ampulex compressa, which uses an Alien-like strategy for the sake of its offspring. Unlike most venomous hunters, this wasp injects venom directly into specific cerebral regions of its cockroach prey. As a result of the sting, the cockroach remains alive but immobile, but not paralyzed, and serves to nourish the developing wasp larva.
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            Host Regulation by Insect Parasitoids

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              Flexibility in basal metabolic rate and evaporative water loss among hoopoe larks exposed to different environmental temperatures.

              The 'energy demand' hypothesis for short-term adjustments in basal metabolic rate (BMR) posits that birds adjust the size of their internal organs relative to food intake, a correlate of energy demand. We tested this hypothesis on hoopoe larks (Alaemon alaudipes), inhabitants of the Arabian desert, by acclimating birds for 3 weeks at 15 degrees C and at 36 degrees C, then measuring their BMR and total evaporative water loss (TEWL). Thereafter, we determined the dry masses of their brain, heart, liver, kidney, stomach, intestine and muscles of the pectoral region. Although mean body mass did not differ initially between the two groups, after 3 weeks, birds in the 15 degrees C group had gained mass (44.1+/-6.5 g), whereas larks in the 36 degrees C group had maintained a constant mass (36.6+/-3.6 g; means +/- s.d., N=6). Birds in the 15 degrees C group had a mean BMR of 46.8+/-6.9 kJ day(-1), whereas birds in the 36 degrees C group had a BMR of 32.9+/-6.3 kJ day(-1), values that were significantly different when we controlled for differences in body mass. When measured at 35 degrees C, larks in the cold-exposure group had a TEWL of 3.55+/-0.60 g H(2)O day(-)(1), whereas TEWL for birds in the 36 degrees C group averaged 2.23+/-0.28 g H(2)O day(-1), a difference of 59.2%. Mass-independent TEWL differed significantly between groups. Larks in the 15 degrees C group had a significantly larger liver, kidney and intestine than larks in the 36 degrees C group. The total increase in organ mass contributed 14.3% towards the total mass increment in the cold exposure group. Increased food intake among larks in the cold group apparently resulted in enlargement of some of the internal organs, and the increase in mass of these organs required a higher rate of oxygen uptake to support them. As oxygen demands increased, larks apparently lost more evaporative water, but the relationship between increases in BMR and TEWL remains unresolved.
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                Author and article information

                Contributors
                jian.duan@usda.gov
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                19 December 2023
                19 December 2023
                2023
                : 13
                : 22663
                Affiliations
                [1 ]Agriculture Research Service, Beneficial Insects Introduction Research Unit, U.S. Department of Agriculture, ( https://ror.org/02d2m2044) Newark, DE 19713 USA
                [2 ]Ecology and Nature Conservation Institute, Chinese Academy of Forestry, ( https://ror.org/0360dkv71) Beijing, 100091 China
                [3 ]Agriculture Research Service, Invasive Insect Biocontrol and Behavior Laboratory, U.S. Department of Agriculture, ( https://ror.org/02d2m2044) Beltsville, MD 20705 USA
                Article
                50147
                10.1038/s41598-023-50147-8
                10730522
                38114572
                b4087636-8662-4bcf-9ce8-f1dd10e820fe
                © This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 2 November 2023
                : 15 December 2023
                Funding
                Funded by: U.S. Department of Agriculture
                Award ID: CRIS 8010-22000-031D
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                © Springer Nature Limited 2023

                Uncategorized
                ecology,physiology
                Uncategorized
                ecology, physiology

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