Metabolomic Evenness Underlies Intraspecific Differences Among Lineages of a Wetland Grass
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
LAB94095
U.S. Department of Agriculture
PubMed
37099216
DOI
10.1007/s10886-023-01425-2
PII: 10.1007/s10886-023-01425-2
Knihovny.cz E-zdroje
- Klíčová slova
- Common Reed, Ecological Omics, Invasion Ecology, Invasive Plant Species, Liquid Chromatography–Mass Spectrometry (LC–MS), Phytochemistry,
- MeSH
- fenotyp MeSH
- fytonutrienty MeSH
- lipnicovité * MeSH
- mokřady * MeSH
- rostliny MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- fytonutrienty MeSH
The metabolome represents an important functional trait likely important to plant invasion success, but we have a limited understanding of whether the entire metabolome or targeted groups of compounds confer an advantage to invasive as compared to native taxa. We conducted a lipidomic and metabolomic analysis of the cosmopolitan wetland grass Phragmites australis. We classified features into metabolic pathways, subclasses, and classes. Subsequently, we used Random Forests to identify informative features to differentiate five phylogeographic and ecologically distinct lineages: European native, North American invasive, North American native, Gulf, and Delta. We found that lineages had unique phytochemical fingerprints, although there was overlap between the North American invasive and North American native lineages. Furthermore, we found that divergence in phytochemical diversity was driven by compound evenness rather than metabolite richness. Interestingly, the North American invasive lineage had greater chemical evenness than the Delta and Gulf lineages but lower evenness than the North American native lineage. Our results suggest that metabolomic evenness may represent a critical functional trait within a plant species. Its role in invasion success, resistance to herbivory, and large-scale die-off events common to this and other plant species remain to be investigated.
Department of Ecology Faculty of Science Charles University Prague CZ 128 44 Czech Republic
Department of Entomology Louisiana State University Baton Rouge LA 70803 USA
Department of Integrative Biology University of Texas Austin TX 78712 USA
Department of Natural Resource Sciences University of Rhode Island Kingston RI 02881 USA
Smithsonian Tropical Research Institute Balboa Ancón Apartado 0843 03092 Republic of Panama
Zobrazit více v PubMed
Allen WJ, Meyerson LA, Cummings D, Anderson J, Bhattarai GP, Cronin JT (2017) Biogeography of a plant invasion: drivers of latitudinal variation in enemy release. Global Ecol Biogeogr 26:435–446 DOI
Allen WJ, Meyerson LA, Flick AJ, Cronin JT (2018) Intraspecific variation in indirect plant–soil feedbacks influences a wetland plant invasion. Ecology 99:1430–1440 PubMed DOI
Anaya AL, Cruz-Ortega R, Waller GR (2006) Metabolism and ecology of purine alkaloids. Fron Biosci 11(3):2354–2370 DOI
Barrett DP, Groenteman R, Fowler SV, Subbaraj AK, Clavijo-McCormick A (2021) Metabolomics analysis of host plant biochemistry could improve the effectiveness and safety of classical weed biocontrol. Biol Control 160:104663 DOI
Bhattarai GP, Meyerson LA, Anderson J, Cummings D, Allen WJ, Cronin JT (2017) Biogeography of a plant invasion: genetic variation and plasticity in latitudinal clines for traits related to herbivory. Ecol Monogr 87:57–75 DOI
Breiman L (2001) Random forests. Mach Learn 45:5–32 DOI
Bickford WA, Zak DR, Kowalski KP, Goldberg DE (2020) Differences in rhizosphere microbial communities between native and non-native Phragmites australis may depend on stand density. Ecol Evol 10:11739–11751 PubMed DOI PMC
Bowen JL, Kearns PJ, Byrnes JEK, Wigginton S, Allen WJ, Greenwood M, Tran K, Yu J, Cronin JT, Meyerson LA (2017) Lineage overwhelms environmental conditions in determining rhizosphere bacterial community structure in a cosmopolitan invasive plant. Nat Comm 8:433 DOI
Brix H (1999) The European research project on reed dieback and progression (EUREED). Limnologica 29:5–10 DOI
Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443 DOI
Cappuccino N, Arnason JT (2006) Novel chemistry of invasive exotic plants. Biol Lett 2:189–193 PubMed DOI PMC
Carson HL (1990) Increased genetic variance after a population bottleneck. Trends Ecol Evol 5:228–230 PubMed DOI
Cronin JT, Bhattarai GP, Allen WJ, Meyerson LA (2015) Biogeography of a plant invasion: plant–herbivore interactions. Ecol 96:1115–1127 DOI
Cronin JT, Johnston J, Diaz R (2020) Multiple potential stressors and dieback of Phragmites australis in the Mississippi River Delta, USA: implications for restoration. Wetlands 40:2247–2261 DOI
Croy JR, Allen WJ, Wigginton S, Meyerson LA, Cronin JT (2020) Lineage and latitudinal variation in Phragmites australis tolerance to herbivory: Implications for invasion success. Oikos 129:1341–1357 DOI
Čuda J, Skálová H, Meyerson LA, Pyšek P (2021) Regeneration of Phragmites australis from rhizome and culm fragments: an experimental test of environmental effects, population origin and invasion status. Preslia 93:237–254 DOI
Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431 PubMed DOI
de Mendiburu F, Yaseen M (2020) agricolae: Statistical Procedures for Agricultural Research. R Package Version 1:1–4
Di Castri F (1989) History of biological invasions with special emphasis on the Old World. Biological invasions: a global perspective, pp 1–30
Djoumbou Feunang Y, Eisner R, Knox C, Chepelev L, Hastings J, Owen G, Fahy E, Steinbeck C, Subramanian S, Bolton E, Greiner R (2016) ClassyFire: automated chemical classification with a comprehensive, computable taxonomy. J Cheminformatics 8:1–20 DOI
Dührkop K, Shen H, Meusel M, Rousu J, Böcker S (2015). Searching molecular structure databases with tandem mass spectra using CSI: FingerID. P Natl Acad Sci 112:12580-12585
Dührkop K, Fleischauer M, Ludwig M, Aksenov AA, Melnik AV, Meusel M, Dorrestein PC, Rousu J, Böcker S (2019) SIRIUS 4: a rapid tool for turning tandem mass spectra into metabolite structure information. Nat Methods 16:299–302 PubMed DOI
Dyer LA, Philbin CS, Ochsenrider KM, Richards LA, Massad TJ, Smilanich AM, Forister ML, Parchman TL, Galland LM, Hurtado PJ et al (2018) Modern approaches to study plant–insect interactions in chemical ecology. Nat Rev Chem 2:50–64 DOI
El-Mallakh RS, Brar KS, Yeruva RR (2019) Cardiac glycosides in human physiology and disease: update for entomologists. Insects 10(4):102 PubMed DOI PMC
Eller FJ, Sorrell BK, Lambertini C, Whigham DF, Hazelton ELG, Skalova H, Brix H, Cronin JT, Caplan JS, Kettenring KM et al (2017) The cosmopolitan model species Phragmites australis: Ecophysiology and responses to global change. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01833 PubMed DOI PMC
Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London DOI
Erb M, Kliebenstein DJ (2020) Plant secondary metabolites as defenses, regulators, and primary metabolites: The blurred functional trichotomy. Plant Physiol 184:39–52 PubMed DOI PMC
Fernandez-Conradi P, Defossez E, Delavallade A, Descombes P, Pitteloud C, Glauser G, Pellissier L, Rasmann S (2022) The effect of community-wide phytochemical diversity on herbivory reverses from low to high elevation. J Ecol 110:46–56 DOI
Fortuna TM, Eckert S, Harvey JA, Vet LEM, Muller C, Gols R (2014) Variation in plant defences among populations of a range-expanding plant: consequences for trophic interactions. New Phyto 204:989–999 DOI
Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–362 PubMed DOI
Fridley JD, Craddock A (2015) Contrasting growth phenology of native and invasive forest shrubs mediated by genome size. New Phyto 207:659–668 DOI
Genuer R, Poggi JM, Tuleau-Malot C (2010) Variable selection using random forests. Pattern Recogn Lett 31:2225–2236 DOI
Glassmire AE, Philbin C, Richards LA, Jeffrey CS, Snook JS, Dyer LA (2019) Proximity to canopy mediates changes in the defensive chemistry and herbivore loads of an understory tropical shrub, Piper kelleyi. Ecol Lett 22:332–341 PubMed DOI
Glassmire AE, Zehr LN, Wetzel WC (2020) Disentangling dimensions of phytochemical diversity: alpha and beta have contrasting effects on an insect herbivore. Ecol 101:e03158 DOI
Guo R, Jiao D, Zhou J, Zhong X, Gu F, Liu Q (2019) Metabolic response and correlations between ions and metabolites in Phragmites communis under long-term salinity toxicity. Plant Physiol Bioch 139:651–659 DOI
Guo WY, Lambertini C, Pyšek P, Meyerson LA, Brix H (2018) Living in two worlds: Evolutionary mechanisms act differently in the native and introduced ranges of an invasive plant. Ecol Evol 8:2440–2452 PubMed DOI PMC
Harrison JG, Philbin CS, Gompert Z, Forister GW, Hernandez-Espinoza L, Sullivan BW, Wallace IS, Beltran L, Dodson CD, Francis JS et al (2018) Deconstruction of a plant-arthropod community reveals influential plant traits with nonlinear effects on arthropod assemblages. Funct Ecol 32:1317–1328 DOI
Hartmann T (2007) From waste products to ecochemicals: fifty years research of plant secondary metabolism. Phytochem 68(22–24):2831–2846 DOI
Hauber DP, Saltonstall K, White DA, Hood CS (2011) Genetic variation in the common reed, Phragmites australis, in the Mississippi River Delta marshes: evidence for multiple introductions. Estuar Coasts 34:851–862 DOI
Haug K, Cochrane K, Nainala VC, Williams M, Chang J, Jayaseelan KV, O’Donovan C (2020) MetaboLights: a resource evolving in response to the needs of its scientific community. Nucleic Acids Res 48:D440–D444 PubMed
Hughes AR, Stachowicz JJ, Williams SL (2009) Morphological and physiological variation among seagrass (Zostera marina) genotypes. Oecologia 159:725–733 PubMed DOI
Hunter MD (2016) The phytochemical landscape: linking trophic interactions and nutrient dynamics. Princeton University Press, Princeton, USA DOI
Jeschke JM (2014) General hypotheses in invasion ecology. Divers Distrib 20:1229–1234 DOI
Kaiser HF (1960) The application of electronic computers to factor analysis. Educ Psychol Meas 20:141–151 DOI
Kalske A, Luntamo N, Salminen JP, Ramula S (2022) Introduced populations of the garden lupine are adapted to local generalist snails but have lost alkaloid diversity. Biol Invasions 24:51–65 DOI
Kalu CM, Oduor Ogola HJ, Selvarajan R, Tekere M, Ntushelo K (2021) Fungal and metabolome diversity of the rhizosphere and endosphere of Phragmites australis in an AMD-polluted environment. Heliyon 7:e06399 PubMed DOI PMC
Kaneta M, Sugiyama N (1972) The Constituents of Arthraxon hispidus Makino, Miscanthus tinctorius Hackel, Miscanthus sinensis Anderss, and Phragmites communis Trinius. B Chem Soc Jpn 45(2):528–531 DOI
Kessler A, Kalske A (2018) Plant secondary metabolite diversity and species interactions. Annu Rev Ecol Evol S 49:115–138 DOI
Kim HW, Wang M, Leber CA, Nothias LF, Reher R, Kang KB, Van Der Hooft JJ, Dorrestein PC, Gerwick WH, Cottrell GW (2021) NPClassifier: a deep neural network-based structural classification tool for natural products. J Nat Prod 84:2795–2807 PubMed DOI PMC
Knight IA, Cronin JT, Gill M, Nyman JA, Wilson BE, Diaz R (2020) The role of plant phenotype, salinity, and infestation by the Roseau Cane Scale in the dieback of Phragmites australis in the Mississippi River Delta, Louisiana, USA. Wetlands 40:1327–1337 DOI
Knight IA, Wilson BE, Gill M, Aviles L, Cronin JT, Nyman JA, Schneider SA, Diaz R (2018) Invasion of Nipponaclerda biwakoensis (Hemiptera: Aclerdidae) and Phragmites australis dieback in southern Louisiana, USA. Biol Invasions 20:2739–2744 DOI
Lambert AM, Casagrande RA (2007) Susceptibility of native and non-native common reed to the non-native mealy plum aphid (Homoptera: Aphididae) in North America. Environ Entomol 36:451–457 PubMed DOI
Lambertini C, Mendelssohn IA, Gustafsson MHG, Olesen B, Riis T, Sorrell BK, Brix H (2012) Tracing the origin of Gulf Coast Phragmites (Poaceae): a story of long-distance dispersal and hybridization. Am J Bot 99:538–551 PubMed DOI
Lavorel S, Díaz S, Cornelissen JHC, Garnier E, Harrison SP, McIntyre S, Pausas JG, Pérez-Harguindeguy N, Roumet C, Urcelay C (2007) Plant functional types: are we getting any closer to the Holy Grail?. Terrestrial ecosystems in a changing world, pp 149–164.
Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280 PubMed DOI
Levin DA (2002) The role of chromosomal change in plant evolution. Oxford University Press, New York, NY
Liaw A, Wiener M (2002) Classification and regression by randomForest. R News 2:18–22
Macel M, de Vos RCH, Jansen JJ, van der Putten WH, van Dam NM (2014) Novel chemistry of invasive plants: exotic species have more unique metabolomic profiles than native congeners. Ecol Evol 4:2777–2786 PubMed DOI PMC
Macel M, van Dam NM, Keurentjes JJB (2010) Metabolomics: the chemistry between ecology and genetics. Mol Ecol Resour 10:583–593 PubMed DOI
Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373 DOI
Maynard LD, Slinn HL, Glassmire AE, Matarrita-Carranza B, Dodson CD, Nguyen TT, Burroughs MJ, Dyer LA, Jeffrey CS, Whitehead SR (2020) Secondary metabolites in a neotropical shrub: spatiotemporal allocation and role in fruit defense and dispersal. Ecology 101:e03192 PubMed DOI
Meadows RE, Saltonstall K (2007) Distribution of native and introduced Phragmites australis in freshwater and oligohaline tidal marshes of the Delmarva peninsula and southern New Jersey. J Torrey Bot Soc 134:99–107 DOI
Meyerson LA, Mooney HA (2007) Invasive alien species in an era of globalization. Front Ecol Environ 5:199–208 DOI
Meyerson LA, Viola DV, Brown RN (2010) Hybridization of invasive Phragmites australis with a native subspecies in North America. Biol Invasions 12:103–111 DOI
Meyerson LA, Lambertini C, McCormick M, Whigham DF (2012) Hybridization of common reed in North America? The answer is blowing in the wind. AoB Plants pls022. https://doi.org/10.1093/aobpla/pls1022 .
Meyerson LA, Cronin JT, Bhattarai GP, Brix H, Lambertini C, Lucanova M, Rinehart S, Suda J, Pyšek P (2016a) Do ploidy level and nuclear genome size and latitude of origin modify the expression of Phragmites australis traits and interactions with herbivores. Biol Invasions 18:2531–2549 DOI
Meyerson LA, Cronin JT, Pyšek P (2016b) Phragmites as a model organism for studying plant invasions. Biol Invasions 18:2421–2431 DOI
Meyerson LA, Pyšek P, Lučanová M, Wigginton S, Tran CT, Cronin JT (2020) Plant genome size influences stress tolerance of invasive and native plants via plasticity. Ecosphere 11:e03145 DOI
Mozdzer TJ, Brisson J, Hazelton EL (2013) Physiological ecology and functional traits of North American native and Eurasian introduced Phragmites australis lineages. AoB Plants 5:plt048 DOI PMC
Nothias LF, Petras D, Schmid R, Dührkop K, Rainer J, Sarvepalli A, Protsyuk I, Ernst M, Tsugawa H, Fleischauer M, Aicheler F (2020) Feature-based molecular networking in the GNPS analysis environment. Nat Methods 17:905–908 PubMed DOI PMC
Ohlrogge J, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957 PubMed PMC
Ohmoto T (1969) riterpenoids and the related compounds from graminaceous plants. Yakugaku Zasshi 89:1682–1687 DOI
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H et al. (2019). Package ‘vegan’. Community ecology package, version 2:1-295
Packer JG, Meyerson LA, Richardson DM, Brundu G, Allen WJ, Bhattarai GP, Brix H, Canavan S, Castiglioni S, Cicatelli A et al (2017) Global networks for invasion science: benefits, challenges and guidelines. Biol Invasions 19:1081–1096 DOI
Pan S, Zhang J, Pan H, Li K, Wu J (2021) Herbivore identity and intensity interact to influence plant metabolic response to herbivory. Arthropod-Plant Inte 15:285–298 DOI
Philbin CS, Dyer LA, Jeffrey CS, Glassmire AE, Richards LA (2022) Structural and compositional dimensions of phytochemical diversity in the genus Piper reflect distinct ecological modes of action. J Ecol 110:57–67 DOI
Pluskal T, Castillo S, Villar-Briones A, Orešič M (2010) MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics 11:1–11 DOI
Pyšek P, Richardson DM (2006) The biogeography of naturalization in alien plants. J Biogeogr 33:2040–2050 DOI
Pyšek P, Skálová H, Čuda J, Guo WY, Suda J, Doležal J, Kauzál O, Lambertini C, Lučanová M, Mandáková T et al (2018) Small genome separates native and invasive populations in an ecologically important cosmopolitan grass. Ecology 99:79–90 PubMed DOI
Pyšek P, Skálová H, Čuda J, Guo WY, Doležal J, Kauzál O, Lambertini C, Pyšková K, Brix H, Meyerson LA (2019) Physiology of a plant invasion: biomass production, growth and tissue chemistry of invasive and native Phragmites australis populations. Preslia 91:51–75 DOI
Pyšek P, Hulme PE, Simberloff D, Bacher S, Blackburn TM, Carlton JT, Dawson W, Essl F, Foxcroft LC, Genovesi P et al (2020a) Scientists’ warning on invasive alien species. Biol Rev 95:1511–1534 PubMed DOI
Pyšek P, Čuda J, Šmilauer P, Skálová H, Chumová Z, Lambertini C, Lučanová M, Ryšavá H, Trávníček P, Šemberová K et al (2020b) Competition among native and invasive Phragmites australis populations: An experimental test of the effects of invasion status, genome size, and ploidy level. Ecol Evol 10:1106–1118 PubMed DOI PMC
Quinn PJ, Williams WP (1979) Plant lipids and their role in membrane function. Prog Biophys Mol Biol 34:109–173 DOI
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rejmánek M, Richardson D (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661 DOI
Reusch TB, Hughes AR (2006) The emerging role of genetic diversity for ecosystem functioning: estuarine macrophytes as models. Estuar Coast 29:159–164 DOI
Richards LA, Dyer LA, Forister ML, Smilanich AM, Dodson CD, Leonard MD, Jeffrey CS (2015) Phytochemical diversity drives plant–insect community diversity. P Natl Acad Sci 112:10973–10978 DOI
Ripley B, Venables B, Bates DM, Hornik K, Gebhardt A, Firth D, Ripley MB (2013) Package ‘mass’. Cran r 538: 113-120
Rudrappa T, Bonsall J, Gallagher JL, Seliskar DM, Bais HP (2007) Root-secreted allelochemical in the noxious weed Phragmites australis deploys a reactive oxygen species response and microtubule assembly disruption to execute rhizotoxicity. J Chem Ecol 33:1898–1918 PubMed DOI
Salazar D, Lokvam J, Mesones I, Pilco MV, Zuñiga JMA, de Valpine P, Fine PV (2018) Origin and maintenance of chemical diversity in a species-rich tropical tree lineage. Nat Ecol Evol 2:983–990 PubMed DOI
Saltonstall K (2002). Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. P Natl Acad Sci 99:2445-2449
Sedio BE (2017) Recent breakthroughs in metabolomics promise to reveal the cryptic chemical traits that mediate plant community composition, character evolution and lineage diversification. New Phytol 214:952–958 PubMed DOI
Sedio BE, Devaney JL, Pullen J, Parker GG, Wright SJ, Parker JD (2020) Chemical novelty facilitates herbivore resistance and biological invasions in some introduced plant species. Ecol Evol 10:8770–8792 PubMed DOI PMC
Sedio BE, Spasojevic MJ, Myers JA, Wright SJ, Person MD, Chandrasekaran H, Dwenger JH, Prechi ML, Lopez CA, Allen DN, Anderson-Teixeira KJ (2021) Chemical similarity of co-occurring trees decreases with precipitation and temperature in North American forests. Front Ecol Evol 9:679638
Seebens H, Blackburn TM, Dyer EE, Genovesi P, Hulme PE, Jeschke JM, Pagad S, Pyšek P, Winter M, Arianoutsou M et al (2017) No saturation in the accumulation of alien species worldwide. Nat Comm 8:1–9 DOI
Seigler DS (1983). Role of lipids in plant resistance to insects. In: PA Hedin, ed. Plant Resistance to Insects. ACS Symposium Series, Vol. 208. Washington, USA: American Chemical Society, 303–327
Skubel SA, Su X, Poulev A, Foxcroft LC, Dushenkov V, Raskin I (2020) Metabolomic differences between invasive alien plants from native and invaded habitats. Sci Rep 10:9749 PubMed DOI PMC
Suda J, Meyerson LA, Leitch IJ, Pyšek P (2015) The hidden side of plant invasions: the role of genome size. New Phytol 205:994–1007 PubMed DOI
Tewksbury L, Casagrande R, Blossey B, Hafliger P, Schwarzlander M (2002) Potential for biological control of Phragmites australis in North America. Biol Control 23:191–212 DOI
Uddin MN, Caridi D, Robinson RW (2012) Phytotoxic evaluation of Phragmites australis: an investigation of aqueous extracts of different organs. Mar Freshwater Res 63(9):777–787 DOI
van der Putten W (1997) Die-back of Phragmites australis in European wetlands: An overview of the European research programme on reed dieback and progression (1993–1994). Aquat Bot 59:263–275 DOI
van Kleunen M, Dawson W, Schlaepfer D, Jeschke JM, Fischer M (2010) Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol Lett 13:947–958 PubMed DOI
Wahman R, Sauvêtre A, Schröder P, Moser S, Letzel T (2020) Untargeted metabolomics studies on drug-incubated Phragmites australis profiles. Metabolites 11:2 PubMed DOI PMC
Walker TW, Alexander JM, Allard PM, Baines O, Baldy V, Bardgett RD, Capdevila P, Coley PD, David B, Defossez E et al (2022) Functional Traits 2.0: The power of the metabolome for ecology. J Ecol 110:4–20 DOI
Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, Nguyen DD, Watrous J, Kapono CA, Luzzatto-Knaan T, Porto C (2016) Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat Biotechnol 34:828–837 PubMed DOI PMC
Wetzel WC, Whitehead SR (2020) The many dimensions of phytochemical diversity: linking theory to practice. Ecol Lett 23:16–32 PubMed DOI
Whitehead SR, Bass E, Corrigan A, Kessler A, Poveda K (2021) Interaction diversity explains the maintenance of phytochemical diversity. Ecol Lett 24:1205–1214 PubMed DOI
Williams JR (1954) The biological control of weeds. In: Report of the Sixth Commonwealth Entomological Congress. London, UK, 95–98
Zhang X, Dong J, Raftery D (2020) Five Easy Metrics of Data Quality for LC–MS-Based Global Metabolomics. Anal Chem 92:12925–12933 PubMed DOI PMC