Abstract
Large mammalian herbivores greatly influence the functioning of grassland ecosystems. Through plant consumption, excreta, and trampling, they modify biodiversity, nutrient cycling, and soil properties. Grazing mammals can also alter soil and rhizosphere bacterial communities, but their effect on the microbiome of other animals in the habitat (i.e., insects) is unknown. Using an experimental field approach and Illumina MiSeq 16S rRNA gene sequencing, we analyzed the influence of cattle grazing on the microbial community of spring webworm caterpillars, Ocnogyna loewii. Our experimental setup included replicated grazed and non-grazed paddocks from which caterpillars were collected twice (first-second and fourth-fifth instar). The caterpillars’ microbiome is composed mostly of Proteobacteria and Firmicutes, and contains a potential symbiont from the genus Carnobacterium (55% of reads). We found that grazing significantly altered the microbiome composition of late instar caterpillars, probably through changes in diet (plant) composition and availability. Furthermore, the microbiome composition of early instar caterpillars significantly differed from late instar caterpillars in 221 OTUs (58 genera). Pseudomonas and Acinetobacter were dominant in early instars, while Carnobacterium and Acinetobacter were dominant in late instars. This study provides new ecological perspectives on the cascading effects mammalian herbivores may have on the microbiome of other animals in their shared habitat.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Eisenhauer N, Schlaghamerský J, Reich PB, Frelich LE. The wave towards a new steady state: effects of earthworm invasion on soil microbial functions. Biol Invasions. 2011;13:2191–6.
Fukami T, Wardle DA, Bellingham PJ, Mulder CPH, Towns DR, Yeates GW, et al. Above- and below-ground impacts of introduced predators in seabird-dominated island ecosystems. Ecol Lett. 2006;9:1299–307.
McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci. 2013;110:3229–36.
Pechal JL, Benbow ME. Microbial ecology of the salmon necrobiome: evidence salmon carrion decomposition influences aquatic and terrestrial insect microbiomes. Environ Microbiol. 2016;18:1511–22.
Hammer TJ, Fierer N, Hardwick B, Simojoki A, Slade E, Taponen J, et al. Treating cattle with antibiotics affects greenhouse gas emissions, and microbiota in dung and dung beetles. Proc R Soc B. 2016;283:20160150.
Crawley MJ. Herbivory: the dynamics of animal-plant interactions. Oxford: Blackwell Scientific Publications; 1983.
McNaughton SJ, Oesterheld M, Frank DA, Williams KJ. Ecosystem-level patterns of primary productivity and herbivory in terrestrial habitats. Nature. 1989;341:142–4.
Harrison KA, Bardgett R. Impacts of grazing and browsing by large herbivores on soils and soil biological properties. In: Gordon IJ, Prins HHT, editors. The ecology of browsing and grazing. Springer; Berlin Heidelberg, 2008; p. 201–16.
Hamilton EW, Frank DA, Hinchey PM, Murray TR. Defoliation induces root exudation and triggers positive rhizospheric feedbacks in a temperate grassland. Soil Biol Biochem. 2008;40:2865–73.
Olsen YS, Dausse A, Garbutt A, Ford H, Thomas DN, Jones DL. Cattle grazing drives nitrogen and carbon cycling in a temperate salt marsh. Soil Biol Biochem. 2011;43:531–41.
Liu T, Nan Z, Hou F. Grazing intensity effects on soil nitrogen mineralization in semi-arid grassland on the Loess Plateau of northern China. Nutr Cycl Agroecosystems. 2011;91:67–75.
Shan Y, Chen D, Guan X, Zheng S, Chen H, Wang M, et al. Seasonally dependent impacts of grazing on soil nitrogen mineralization and linkages to ecosystem functioning in inner Mongolia grassland. Soil Biol Biochem. 2011;43:1943–54.
Zhou X, Wang J, Hao Y, Wang Y. Intermediate grazing intensities by sheep increase soil bacterial diversities in an inner Mongolian steppe. Biol Fertil Soils. 2010;46:817–24.
Gish M, Ben-Ari M, Inbar M. Direct consumptive interactions between mammalian herbivores and plant-dwelling invertebrates: prevalence, significance, and prospectus. Oecologia. 2017;183:1–6.
van Klink R, van der Plas F, van Noordwijk CGE, Wallisdevries MF, Olff H. Effects of large herbivores on grassland arthropod diversity. Biol Rev. 2015;90:347–66.
Ohgushi T. Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst. 2005;36:81–105.
Stewart AJA. The impact of deer on lowland woodland invertebrates: a review of the evidence and priorities for future research. Forestry. 2001;74:259–70.
Dillon RJ, Dillon VM. The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol. 2004;49:71–92.
Pérez-Cobas AE, Maiques E, Angelova A, Carrasco P, Moya A, Latorre A. Diet shapes the gut microbiota of the omnivorous cockroach Blattella germanica. FEMS Microbiol Ecol. 2015;91:1–14.
Yun JH, Roh SW, Whon TW, Jung MJ, Kim MS, Park DS, et al. Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol. 2014;80:5254–64.
Broderick NA, Raffa KF, Goodman RM, Handelsman J. Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Appl Environ Microbiol. 2004;70:293–300.
Kikuchi Y, Hosokawa T, Fukatsu T. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl Environ Microbiol. 2007;73:4308–16.
Boucias DG, Cai Y, Sun Y, Lietze VU, Sen R, Raychoudhury R, et al. The hindgut lumen prokaryotic microbiota of the termite Reticulitermes flavipes and its responses to dietary lignocellulose composition. Mol Ecol. 2013;22:1836–53.
Minard G, Mavingui P, Moro CV. Diversity and function of bacterial microbiota in the mosquito holobiont. Parasit Vectors. 2013;6:146.
Engel P, Martinson VG, Moran NA. Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci USA. 2012;109:11002–7.
Köhler T, Dietrich C, Scheffrahn RH, Brune A. High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.). Appl Environ Microbiol. 2012;78:4691–701.
Poulsen M, Sapountzis P. Behind every great ant, there is a great gut. Mol Ecol. 2012;21:2054–7.
Mohr KI, Tebbe CC. Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environ Microbiol. 2006;8:258–72.
Xia X, Gurr GM, Vasseur L, Zheng D, Zhong H, Qin B, et al. Metagenomic sequencing of Diamondback moth gut microbiome unveils key holobiont adaptations for herbivory. Front Microbiol. 2017;8:1–12.
Chen B, Teh BS, Sun C, Hu S, Lu X, Boland W, et al. Biodiversity and activity of the gut microbiota across the life history of the insect herbivore Spodoptera littoralis. Sci Rep. 2016;6:29505.
Johnston PR, Rolff J. Host and symbiont jointly control gut microbiota during complete metamorphosis. PLoS Pathog. 2015;11:1–11.
Hammer TJ, McMillan WO, Fierer N. Metamorphosis of a butterfly-associated bacterial community. PLoS ONE. 2014;9:e86995.
Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J. Robustness of the bacterial community in the cabbage white butterfly larval midgut. Microb Ecol. 2010;59:199–211.
Dyson EA, Kamath MK, Hurst GDD. Wolbachia infection associated with all-female broods in Hypolimnas bolina (Lepidoptera: Nymphalidae): evidence for horizontal transmission of a butterfly male killer. Heredity (Edinb). 2002;88:166–71.
Hiroki M, Kato Y, Kamito T, Miura K. Feminization of genetic males by a symbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae). Naturwissenschaften. 2002;89:167–70.
Tagami Y, Miura K. Distribution and prevalence of Wolbachiain Japanese populations of Lepidoptera. Insect Mol Biol. 2004;13:359–64.
Swailem SM, Amin AH. On the biology of the spring webworm Ocnogyna loewii Z. (Arctiidae: Lepidoptera). Mesop J Agric. 1979;14:183–95.
Sternberg M, Gutman M, Perevolotsky A, Ungar ED, Kigel J. Vegetation response to grazing management in a Mediterranean herbaceous community: a functional group approach. J Appl Ecol. 2000;37:224–37.
Caporaso JG, Lauber CL, Walters WA, Berg-lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4.
Aizenberg-Gershtein Y, Izhaki I, Santhanam R, Kumar P, Baldwin IT, Halpern M. Pyridine-type alkaloid composition affects bacterial community composition of floral nectar. Sci Rep. 2015;5:11536.
Zhang J, Kobert K, Flouri T, Stamatakis A. PEAR: A fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics. 2014;30:614–20.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high- throughput community sequencing data. Nat Methods. 2010;7:335–6.
Hsieh TC, Ma KH, Chao A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol. 2016;7:1451–6.
Hammer Ø, Harper DAT, Ryan PD. Paleontological statistics software: Package for education and data analysis. Palaeontol Electron. 2001;4:1–9.
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, et al. vegan: community ecology package. R package version 2.0-10; 2015. R Packag ver 24–3; 2013. Retrieved from: http://vegan.r-forge.r-project.org.
Lin XL, Kang ZW, Pan QJ, Liu TX. Evaluation of five antibiotics on larval gut bacterial diversity of Plutella xylostella (Lepidoptera: Plutellidae). Insect Sci. 2015;22:619–28.
Milchunas DG, Lauenroth WK. Quantitative effects of grazing on vegetation and soils over a global range of environmnents. Ecol Monogr. 1993;63:327–66.
Gish M, Dafni A, Inbar M. Mammalian herbivore breath alerts aphids to flee host plant. Curr Biol. 2010;20:628–9.
Berman TS, Ben-Ari M, Glasser TA, Gish M, Inbar M. How goats avoid ingesting noxious insects while feeding. Sci Rep. 2017;7:1–10.
Yathom S. Distribution and flight period of two Ocnogyna species in Israel (Lepidoptera: Arctiidae). Isr J Entomol. 1984;18:63–6.
Engel P, Moran NA. The gut microbiota of insects - diversity in structure and function. FEMS Microbiol Rev. 2013;37:699–735.
Skarpe C, Hester AJ. Plant traits, browsing and grazing herbivores, and vegetation dynamics. In: Gordon I, Prins HHT, editors. The ecology of browsing and grazing. Berlin: Springer; 2008; p. 217–47.
Sternberg M, Golodets C, Gutman M, Perevolotsky A, Ungar ED, Kigel J, et al. Testing the limits of resistance: a 19-year study of Mediterranean grassland response to grazing regimes. Glob Chang Biol. 2015;21:1939–50.
Henkin Z, Ungar ED, Dvash L, Perevolotsky A, Yehuda Y, Sternberg M, et al. Effects of cattle grazing on herbage quality in a herbaceous Mediterranean rangeland. Grass Forage Sci. 2011;66:516–25.
Colman DR, Toolson EC, Takacs-Vesbach CD. Do diet and taxonomy influence insect gut bacterial communities? Mol Ecol. 2012;21:5124–37.
Tang X, Freitak D, Vogel H, Ping L, Shao Y, Cordero EA, et al. Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS ONE. 2012;7:e36978.
Priya NG, Ojha A, Kajla MK, Raj A, Rajagopal R. Host plant induced variation in gut bacteria of Helicoverpa armigera. PLoS ONE. 2012;7:e30768.
Beylich A, Oberholzer HR, Schrader S, Höper H, Wilke BM. Evaluation of soil compaction effects on soil biota and soil biological processes in soils. Soil Tillage Res. 2010;109:133–43.
Adler P, Raff D, Lauenroth W. The effect of grazing on the spatial heterogeneity of vegetation. Oecologia. 2001;128:465–79.
Belovsky GE, Slade JB, Stockhoff BA. Susceptibility to predation for different grasshoppers: an experimental study. Ecology. 1990;71:624–34.
Brinkmann N, Martens R, Tebbe CC. Origin and diversity of metabolically active gut bacteria from laboratory-bred larvae of Manduca sexta (Sphingidae, Lepidoptera, Insecta). Appl Environ Microbiol. 2008;74:7189–96.
Vallet-Gely I, Lemaitre B, Boccard F. Bacterial strategies to overcome insect defences. Nat Rev Microbiol. 2008;6:302–13.
Ceja-Navarro JA, Nguyen NH, Karaoz U, Gross SR, Herman DJ, Andersen GL, et al. Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut of Odontotaenius disjunctus. ISME J. 2014;8:6–18.
Jones RT, Sanchez LG, Fierer N. A cross-taxon analysis of insect-associated bacterial diversity. PLoS ONE. 2013;8:e61218.
Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, et al. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature. 2007;450:560–5.
Xia X, Zheng D, Zhong H, Qin B, Gurr GM, Vasseur L, et al. DNA sequencing reveals the midgut microbiota of Diamondback moth, Plutella xylostella (L.) and a possible relationship with insecticide resistance. PLoS ONE. 2013;8:e68852.
Shao Y, Arias-Cordero E, Guo H, Bartram S, Boland W. In vivo Pyro-SIP assessing active gut microbiota of the cotton leafworm, Spodoptera littoralis. PLoS ONE. 2014;9:e85948.
Douglas AE. Lessons from studying insect symbioses. Cell Host Microbe. 2011;10:359–67.
WenHong L, Jin D, Li F, Jin J, Ying C. Phenotypic fingerprints of bacterium Erwinia persicina from larval gut of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Acta Entomol Sin. 2016;59:456–63.
Hernández-Flores L, Llanderal-Cázares C, Guzmán-Franco AW, Aranda-Ocampo S. Bacteria present in Comadia redtenbacheri larvae (Lepidoptera: Cossidae). J Med Entomol. 2015;52:1150–8.
Frankenhuyzen K, van, Liu Y, Tonon A. Interactions between Bacillus thuringiensis subsp. kurstaki HD-1 and midgut bacteria in larvae of gypsy moth and spruce budworm. J Invertebr Pathol. 2010;103:124–31.
Douglas AE. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol. 1998;43:17–37.
Inbar M, Doostdar H, Mayer RT. Effects of sessile whitefly nymphs (Homoptera: Aleyrodidae) on leaf-chewing larvae (Lepidoptera: Noctuidae). Environ Entomol. 1999;28:353–7.
Hammes WP, Hertel C. The genera Lactobacillus and Carnobacterium. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E, editors. The prokaryotes. New York: Springer; 2006. p. 320–403.
Schmid RB, Lehman RM, Brözel VS, Lundgren JG. An indigenous gut bacterium, Enterococcus faecalis (Lactobacillales: Enterococcaceae), increases seed consumption by Harpalus pensylvanicus (Coleoptera: Carabidae). Fla Entomol. 2014;97:575–84.
Vásquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, Szekely L, et al. Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS ONE. 2012;7:e33188.
Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F. Lactobacillus plantarum promotes drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab. 2011;14:403–14.
Acknowledgements
We thank the staff of ‘Karei Deshe’ for their valuable support. We thank Amir Viner, Daniel Schlesinger, Natalie Amar and Achiad Sade for their technical assistance. We also thank Dr. Assaf Malik from the Bioinformatics Unit at the University of Haifa for his help. We thank the two anonymous reviewers for their helpful comments. Finally, we would like to thank Dr. Elah Pick and Dr. Einat Zchori-Fein for fruitful discussions.
Funding:
This research was supported by The Israel Science Foundation (ISF, grant No. 248/17) and by the German Research Foundation (DFG, the Deutsche Forschungsgemeinschaft) grant No. GZ: HO 930/5-2.
Author contributions:
Conceived and designed the experiments: TSB, MH, and MI. Performed the experiments: TSB with technical advice from SL-S. Analyzed the data and prepared the figures: TSB, SL-S, and ML. Wrote the paper: TSB, MH, and MI. Reviewed and commented on the paper: ML. Contributed reagents/materials: MH and MI. All authors read and approved the chapter.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Berman, T.S., Laviad-Shitrit, S., Lalzar, M. et al. Cascading effects on bacterial communities: cattle grazing causes a shift in the microbiome of a herbivorous caterpillar. ISME J 12, 1952–1963 (2018). https://doi.org/10.1038/s41396-018-0102-4
Received:
Revised:
Accepted:
Published:
Version of record:
Issue date:
DOI: https://doi.org/10.1038/s41396-018-0102-4
This article is cited by
-
Genome assembly of the grassland caterpillar Gynaephora qinghaiensis
Scientific Data (2025)
-
Herbivore Dung inputs mainly drive copiotrophic bacterial contributions to soil nutrient pool turnover in alpine grasslands
Biology and Fertility of Soils (2025)
-
Grazing-to-fencing increases alpine soil phosphorus availability by promoting phosphatase activity and regulating the phoD-harboring bacterial communities
Journal of Soils and Sediments (2024)
-
Impact of gut microbiota composition on black cutworm, Agrotis ipsilon (hufnagel) metabolic indices and pesticide degradation
Animal Microbiome (2023)
-
Trophic level drives the host microbiome of soil invertebrates at a continental scale
Microbiome (2021)
