Inter-trophic Interaction of Gut Microbiota in a Tripartite System
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HOST MICROBE INTERACTIONS
Inter-trophic Interaction of Gut Microbiota in a Tripartite System Xianfeng Yi 1 & Jiawei Guo 1 & Minghui Wang 1 & Chao Xue 1 & Mengyao Ju 1 Received: 29 June 2020 / Accepted: 5 November 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020
Abstract Gut microbiota can be transmitted either environmentally or socially and vertically at intraspecific level; however, whether gut microbiota interact along trophic levels has been largely overlooked. Here, we characterized the gut bacterial communities of weevil larvae of Curculio arakawai that infest acorns of Mongolian oak (Quercus mongolica) as well as acorn-eating mammals, Siberian chipmunk (Tamias sibiricus), to test whether consumption of seed-borne larvae remodels the gut bacterial communities of T. sibiricus. Ingestion of weevil larvae of C. arakawai significantly altered the gut bacterial communities of T. sibiricus. Consequently, T. sibiricus fed larvae of C. arakawai showed higher capability to counter the negative effects of tannins, in terms of body weight maintenance, acorn consumption, N content in feces, urine pH, and blood ALT activity. Our results may first show that seed-borne insects as hidden players have a potential to alter the gut microbiota of seed predators in the tripartite system. Keywords Seed predator . Weevil larvae . Gut microbe . Microbial transmission . Tannin-degrading bacteria . Tripartite interaction
Introduction Larvae of many insect groups, relying on seeds for their early development, appear to be the most prominent cohort of predispersal seed predators of numerous plant species [12, 13, 111]. Many oak species throughout the world bear acorns with high nutrition and therefore suffer a high level of predation by several guilds of invertebrate animals [13, 16, 20, 24, 53, 69, 90, 109]. Previous observations have identified three major insect groups in oak acorns: weevils (Coleoptera: Curculionidae), moths (Lepidoptera: Tortricidae), and gall wasps (Hymenoptera: Cynipidae) [25, 38, 73]. Weevils, particularly in the genus Curculio, are generally considered the major guild of obligate acorn feeders [34, 35, 44, 47, 111]. Although weevil infestation usually causes severe damage to acorns of various oak species, weevil-damaged acorns can serve as important resource supplies for food-hoarding animals [46, 70, 73, 90]. An increasing body of literature has shown that weevil infestation is one critical factor influencing
* Xianfeng Yi [email protected] 1
College of Life Sciences, Qufu Normal University, Qufu 273165, China
the foraging and caching decisions of these animals [21, 90, 109, 110]. Although several studies have shown that mammalian and avian seed consumers avoid selecting the infested acorns [27, 60, 88, 98], other literatures provide evidence that small mammals are unable to distinguish between sound seeds and those infested by insect larvae [14, 21, 80, 101]. Moreover, recent studies evidenced that food-hoarding animals selectively consume both the weevil larvae and the undamaged
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