Skip to main content Accessibility help
×
Hostname: page-component-848d4c4894-hfldf Total loading time: 0 Render date: 2024-05-01T21:51:49.277Z Has data issue: false hasContentIssue false

Chapter Twenty - Microbial mutualists and biodiversity in ecosystems

Published online by Cambridge University Press:  05 February 2013

Jennifer A. Rudgers
Affiliation:
Department of Biology, University of New Mexico
Keith Clay
Affiliation:
Department of Biology, Indiana University
Takayuki Ohgushi
Affiliation:
Kyoto University, Japan
Oswald Schmitz
Affiliation:
Yale University, Connecticut
Robert D. Holt
Affiliation:
University of Florida
Get access

Summary

Defining and detecting microbial trait-mediated indirect interactions

Microbial trait-mediated indirect interactions (TMIIs) occur when a microbe (species A) changes a trait of its host species (species B) that consequently affects another species in the community (species C, or the enemy of the host in a protection mutualism). This trait-mediated effect is distinguished from a density-mediated effect, in which the impact of the microbe would spread to other species exclusively through changes in the density of the host organism (e.g., via increased host mortality caused by a pathogen, density-mediated indirect interactions, DMII). Importantly, models reveal that TMIIs have different dynamical consequences than DMIIs (Chapter 1), thus it is important to distinguish between these effects.

Food web diagrams can bring clarity to the characterization of TMIIs. In contrast to typical predator–prey interactions, microbially-mediated protection mutualisms can involve a microbial partner at the same, or very similar, trophic level as the host organism (Fig. 20.1). Furthermore, symbioses involve the exchange of resources, for example photosynthetic carbon exchanged for soil nutrients in the symbiosis between plants and mycorrhizal fungi; this exchange is depicted explicitly in our diagrams, which include trait-mediated effects that are transmitted to a responding resource species (Fig. 20.1e) or to a consumer species (Fig. 20.1f).

Type
Chapter
Information
Trait-Mediated Indirect Interactions
Ecological and Evolutionary Perspectives
, pp. 391 - 413
Publisher: Cambridge University Press
Print publication year: 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arnold, A. E.Mejia, L. C.Kyllo, D. 2003 Fungal endophytes limit pathogen damage in a tropical treeProceedings of the National Academy of Sciences of the United States of America 100 15649CrossRefGoogle Scholar
Barton, E. S.White, D. W.Cathelyn, J. S. 2007 Herpes virus latency confers symbiotic protection from bacterial infectionNature 447 326CrossRefGoogle ScholarPubMed
Bertaux, J.Schmid, M.Hutzler, P. 2005 Occurrence and distribution of endobacteria in the plant-associated mycelium of the ectomycorrhizal fungus S238NEnvironmental Microbiology 7 1786CrossRefGoogle ScholarPubMed
Bertoni, M. D.Romero, N.Reddy, P. V.White, J. F. 1997 A hypocrealean epibiont on meristems of Mycologia 89 375CrossRefGoogle Scholar
Brundrett, M. C. 2002 Coevolution of roots and mycorrhizas of land plantsNew Phytologist 154 275CrossRefGoogle Scholar
Bush, L. P.Wilkinson, H. H.Schardl, C. L. 1997 Bioprotective alkaloids of grass–fungal endophyte symbiosesPlant Physiology 114 1CrossRefGoogle ScholarPubMed
Cahill, J. F.Elle, E.Smith, G. R.Shore, B. H. 2008 Disruption of a belowground mutualism alters interactions between plants and their floral visitorsEcology 89 1791CrossRefGoogle ScholarPubMed
Callaway, R. M.Ridenour, W. M. 2004 Novel weapons: invasive success and the evolution of increased competitive abilityFrontiers in Ecology and the Environment 2 436CrossRefGoogle Scholar
Clay, K. 1988 Fungal endophytes of grasses: a defensive mutualism between plants and fungiEcology 69 10CrossRefGoogle Scholar
Clay, K.Cheplick, G. P. 1989 Effect of ergot alkaloids from fungal endophyte-infected grasses on fall armyworm ()Journal of Chemical Ecology 15 169CrossRefGoogle Scholar
Clay, K.Holah, J. 1999 Fungal endophyte symbiosis and plant diversity in successional fieldsScience 285 1742CrossRefGoogle ScholarPubMed
Clay, K.Schardl, C. 2002 Evolutionary origins and ecological consequences of endophyte symbiosis with grassesAmerican Naturalist 160 S99CrossRefGoogle ScholarPubMed
Clay, K.Hardy, T. N.Hammond, A. M. 1985 Fungal endophytes of and their effect on an insect herbivoreAmerican Journal of Botany 72 1284CrossRefGoogle Scholar
Clay, K.Holah, J.Rudgers, J. A. 2005 Herbivores cause a rapid increase in hereditary symbiosis and alter plant community compositionProceedings of the National Academy of Sciences of the United States of America 102 12465CrossRefGoogle Scholar
Cook, D.Gardner, D. R.Ralphs, M. H. 2009 Swainsoninine concentrations and endophyte amounts of in different plant parts of Journal of Chemical Ecology 35 1272CrossRefGoogle Scholar
Crawford, K. M.Land, J. M.Rudgers, J. A. 2010 Fungal endophytes of native grasses decrease insect herbivore preference and performanceOecologia 164 431CrossRefGoogle ScholarPubMed
Currie, C. R.Bot, A. N. M.Boomsma, J. J. 2003 Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasitesOikos 101 91CrossRefGoogle Scholar
Currie, C. R.Mueller, U. G.Malloch, D. 1999 The agricultural pathology of ant fungus gardensProceedings of the National Academy of Sciences of the United States of America 96 7998CrossRefGoogle ScholarPubMed
Currie, C. R.Scott, J. A.Summerbell, R. C.Malloch, D. 1999 Fungus-growing ants use antibiotic-producing bacteria to control garden parasitesNature 398 701CrossRefGoogle Scholar
Damiani, C. C. 2005 Integrating direct effects and trait-mediated indirect effects using a projection matrix modelEcology 86 2068CrossRefGoogle Scholar
Davidson, S. K.Allen, S. W.Lim, G. E.Anderson, C. M.Haygood, M. G. 2001 Evidence for the biosynthesis of bryostatins by the bacterial symbiont ‘Candidatus ’ of the bryozoan Applied and Environmental Microbiology 67 4531CrossRefGoogle Scholar
Dean, J. M.Mescher, M. C.Moraes, C. M. 2009 Plant–rhizobia mutualism influences aphid abundance on soybeanPlant and Soil 323 187CrossRefGoogle Scholar
Dillon, R. J.Charnley, A. K. 1988 Inhibition of by the gut bacterial flora of the desert locust: characterization of antifungal toxinsCanadian Journal of Microbiology 34 1075CrossRefGoogle Scholar
Dillon, R. J.Vennard, C. T.Buckling, A.Charnley, A. K. 2005 Diversity of locust gut bacteria protects against pathogen invasionEcology Letters 8 1291CrossRefGoogle Scholar
Dong, Y. M.Manfredini, F.Dimopoulos, G. 2009 Implication of the mosquito midgut microbiota in the defense against malaria parasitesPLoS Pathogens 5CrossRefGoogle ScholarPubMed
Folgarait, P. J. 1998 Ant biodiversity and its relationship to ecosystem functioning: a reviewBiodiversity and Conservation 7 1221CrossRefGoogle Scholar
Garrido, J. M. G. 2009 Arbuscular mycorrhizae as defense against pathogensWhite, Jr. J. F.Torres, M. S.Defensive Mutualism in Microbial SymbiosisBoca Raton, FLCRC Press183Google Scholar
Gerardo, N. M.Altincicek, B.Anselme, C. 2010 Immunity and other defenses in pea aphids, Genome Biology 11CrossRefGoogle Scholar
Gil-Turnes, M. S.Fenical, W. 1992 Embryos of are protected by epibiotic bacteriaBiological Bulletin 182 105CrossRefGoogle ScholarPubMed
Gil-Turnes, M. S.Hay, M. E.Fenical, W. 1989 Symbiotic marine bacteria chemically defend crustacean embryos from a pathogenic fungusScience 246 116CrossRefGoogle ScholarPubMed
Glaser, R. L.Meola, M. A. 2010 The native endosymbionts of and increase host resistance to West Nile virus infectionPLoS ONE 5 e11977CrossRefGoogle ScholarPubMed
Görtz, H.Rosati, G.Schweikert, M.Schrallhammer, M.Omura, G.Suzaki, T. 2009 Microbial symbionts for defense and competition among ciliate hostsWhite, Jr. J. F.Torres, M. S.Defensive Mutualism in Microbial SymbiosisBoca Raton, FLCRC PressGoogle Scholar
Gribben, P. E.Byers, J. E.Clements, M.McKenzie, L. A.Steinberg, P. D.Wright, J. T. 2009 Behavioural interactions between ecosystem engineers control community species richnessEcology Letters 12 1127CrossRefGoogle ScholarPubMed
Guerrieri, E.Lingua, G.Digilio, M. C.Massa, N.Berta, G. 2004 Do interactions between plant roots and the rhizosphere affect parasitoid behaviourEcological Entomology 29 753CrossRefGoogle Scholar
Guimaraes, P. R.Rico-Gray, V.Oliveira, P. S. 2007 Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networksCurrent Biology 17 1797CrossRefGoogle ScholarPubMed
Haine, E. R.Boucansaud, K.Rigaud, T. 2005 Conflict between parasites with different transmission strategies infecting an amphipod hostProceedings of the Royal Society of London, Series B 272 2505CrossRefGoogle ScholarPubMed
Hartley, S. E.Gange, A. C. 2009 Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic contextAnnual Review of Entomology 54 323CrossRefGoogle Scholar
Haygood, M. G.Distel, D. L. 1993 Bioluminescent symbionts of flashlight fishes and deep sea anglerfishes form unique lineages related to the genus Nature 363 154CrossRefGoogle ScholarPubMed
Hoeksema, J. D.Chaudhary, V. B.Gehring, C. A. 2010 A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungiEcology Letters 13 394CrossRefGoogle ScholarPubMed
Jaenike, J.Unckless, R.Cockburn, S. N.Boelio, L. M.Perlman, S. J. 2010 Adaptation via symbiosis: recent spread of a defensive symbiontScience 329 212CrossRefGoogle ScholarPubMed
Kaltenpoth, M.Gottler, W.Herzner, G.Strohm, E. 2005 Symbiotic bacteria protect wasp larvae from fungal infestationCurrent Biology 15 475CrossRefGoogle ScholarPubMed
Kaltenpoth, M.Schmitt, T.Polidori, C.Koedam, D.Strohm, E. 2010 Symbiotic streptomycetes in antennal glands of the South American digger wasp genus (Hymenoptera, Crabronidae)Physiological Entomology 35 196CrossRefGoogle Scholar
Kellner, R. L. L.Dettner, K. 1996 Differential efficacy of toxic pederin in deterring potential arthropod predators of (Coleoptera: Staphylinidae) offspringOecologia 107 293CrossRefGoogle ScholarPubMed
Kempel, A.Brandl, R.Schadler, M. 2009 Symbiotic soil microorganisms as players in aboveground plant–herbivore interactions: the role of rhizobiaOikos 118 634CrossRefGoogle Scholar
Koh, S.Hik, D. S. 2007 Herbivory mediates grass–endophyte relationshipsEcology 88 2752CrossRefGoogle ScholarPubMed
Koppenhofer, H. S.Gaugler, R. 2009 Entomopathogenic nematode and bacterial mutualismWhite, Jr. J. F.Torres, M. S.Defensive Mutualism in Microbial SymbiosisBoca Raton, FLCRC PressGoogle Scholar
Koricheva, J.Gange, A. C.Jones, T. 2009 Effects of mycorrhizal fungi on insect herbivores: a meta-analysisEcology 90 2088CrossRefGoogle ScholarPubMed
Laird, R. A.Addicott, J. F. 2007 Arbuscular mycorrhizal fungi reduce the construction of extrafloral nectaries in Oecologia 152 541CrossRefGoogle Scholar
Lemons, A.Clay, K.Rudgers, J. A. 2005 Connecting plant-microbial interactions above and belowground: a fungal endophyte affects decompositionOecologia 145 595CrossRefGoogle ScholarPubMed
Lindquist, N.Hay, M. E. 1996 Palatability and chemical defense of marine invertebrate larvaeEcological Monographs 66 431CrossRefGoogle Scholar
Lindquist, N.Barber, P. H.Weisz, J. B. 2005 Episymbiotic microbes as food and defence for marine isopods: unique symbioses in a hostile environmentProceedings of the Royal Society of London, Series B 272 1209CrossRefGoogle Scholar
Lopanik, N.Lindquist, N.Targett, N. 2004 Potent cytotoxins produced by a microbial symbiont protect host larvae from predationOecologia 139 131CrossRefGoogle ScholarPubMed
Maherali, H.Klironomos, J. N. 2007 Influence of phylogeny on fungal community assembly and ecosystem functioningScience 316 1746CrossRefGoogle ScholarPubMed
Mazmanian, S. K.Round, J. L.Kasper, D. L. 2008 A microbial symbiosis factor prevents intestinal inflammatory diseaseNature 453 620CrossRefGoogle ScholarPubMed
Moran, N. A.Degnan, P. H.Santos, S. R.Dunbar, H. EOchman, H. 2005 The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genesProceedings of the National Academy of Sciences of the United States of America 102 16919CrossRefGoogle Scholar
Oliver, K. M.Moran, N. A. 2009 Defensive symbionts in aphids and other insectsWhite, Jr. J. F.Torres, M. S.Defensive Mutualism in Microbial SymbiosisBoca Raton, FLCRC Press129Google Scholar
Oliver, K. M.Moran, N. A.Hunter, M. S 2006 Costs and benefits of a superinfection of facultative symbionts in aphidsProceedings of the Royal Society of London, Series B 273 1273CrossRefGoogle ScholarPubMed
Oliver, K. M.Russell, J. A.Moran, N. A.Hunter, M. S. 2003 Facultative bacterial symbionts in aphids confer resistance to parasitic waspsProceedings of the National Academy of Sciences of the United States of America 100 1803CrossRefGoogle ScholarPubMed
Omacini, M.Eggers, T.Bonkowski, M.Gange, A. C.Jones, T. H. 2006 Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plantsFunctional Ecology 20 226CrossRefGoogle Scholar
Osborne, S. E.Leong, Y. S.O’Neill, S. L.Johnson, K. N. 2009 Variation in antiviral protection mediated by different strains in PLoS Pathogens 5CrossRefGoogle Scholar
Partida-Martinez, L. P.de Looss, C. F.Ishida, K. 2007 Rhizonin, the first mycotoxin isolated from the Zygomycota, is not a fungal metabolite but is produced by bacterial endosymbiontsApplied and Environmental Microbiology 73 793CrossRefGoogle Scholar
Pena, J. A.Rogers, A. B.Ge, Z. M. 2005 Probiotic spp. diminish induced inflammatory bowel disease in interleukin-10-deficient miceInfection and Immunity 73 912CrossRefGoogle ScholarPubMed
Piel, J. 2002 A polyketide synthase-peptide synthetase gene cluster from an uncultured bacterial symbiont of beetlesProceedings of the National Academy of Sciences of the United States of America 99 14002CrossRefGoogle ScholarPubMed
Piel, J. 2004 Metabolites from symbiotic bacteriaNatural Product Reports 21 519CrossRefGoogle ScholarPubMed
Poulsen, M.Cafaro, M. J.Erhardt, D. P. 2010 Variation in antibiotic defence helps govern parasite-induced morbidity in leaf-cutting antsEnvironmental Microbiology Reports 2 534CrossRefGoogle ScholarPubMed
Ralphs, M. H.Creamer, R.Baucom, D. 2008 Relationship between the endophyte spp. and the toxic alkaloid swainsonine in major locoweed species ( and )Journal of Chemical Ecology 34 32CrossRefGoogle Scholar
Reshef, L.Koren, O.Loya, Y.Zilber-Rosenberg, I.Rosenberg, E. 2006 The coral probiotic hypothesisEnvironmental Microbiology 8 2068CrossRefGoogle ScholarPubMed
Ritchie, K. B. 2006 Regulation of microbial populations by coral surface mucus and mucus-associated bacteriaMarine Ecology-Progress Series 322 1CrossRefGoogle Scholar
Rodriguez, R. J.White, J. F.Arnold, A. E.Redman, R. S. 2009 Fungal endophytes: diversity and functional rolesNew Phytologist 182 314CrossRefGoogle ScholarPubMed
Rosenberg, E.Koren, O.Reshef, L.Efrony, R.Zilber-Rosenberg, I. 2007 The role of microorganisms in coral health, disease and evolutionNature Reviews Microbiology 5 355CrossRefGoogle ScholarPubMed
Rosso, M. L.Maier, M. S.Bertoni, M. D. 2000 Macrocyclic trichothecene production by the fungus epibiont of Molecules 5 345CrossRefGoogle Scholar
Ruby, E. G. 1996 Lessons from a cooperative, bacterial–animal association: the light organ symbiosisAnnual Review of Microbiology 50 591CrossRefGoogle ScholarPubMed
Rudgers, J. A.Clay, K. 2005 Fungal endophytes in terrestrial communities and ecosystemsDighton, E. J.Oudemans, P.White, J. F. J.The Fungal CommunityNew YorkM. Dekker423Google Scholar
Rudgers, J. A.Clay, K. 2007 Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystemsFungal Biology Reviews 21 107CrossRefGoogle Scholar
Rudgers, J. A.Clay, K. 2008 An invasive plant–fungal mutualism reduces arthropod diversityEcology Letters 11 831CrossRefGoogle ScholarPubMed
Rudgers, J. A.Davitt, A. J.Clay, K.Gundel, P.Omacini, M. 2010 Searching for evidence against the mutualistic nature of hereditary symbiosis: a comment on Faeth (2009)American Naturalist 76 99CrossRefGoogle Scholar
Rudgers, J. A.Fischer, S.Clay, K. 2010 Managing plant symbiosis: fungal endophyte genotype alters plant community compositionJournal of Applied Ecology 47 468CrossRefGoogle Scholar
Rudgers, J. A.Holah, J.Orr, S. P.Clay, K. 2007 Forest succession suppressed by an introduced plant-fungal symbiosisEcology 88 18CrossRefGoogle ScholarPubMed
Rudgers, J. A.Mattingly, W. B.Koslow, J. M. 2005 Mutualistic fungus promotes plant invasion into diverse communitiesOecologia 144 463CrossRefGoogle ScholarPubMed
Saikkonen, K.Lehtonen, P.Helander, M.Koricheva, J.Faeth, S. H. 2006 Model systems in ecology: dissecting the endophyte-grass literatureTrends in Plant Science 11 428CrossRefGoogle ScholarPubMed
Scarborough, C. L.Ferrari, J.Godfray, H. C. J. 2005 Aphid protected from pathogen by endosymbiontScience 310 1781CrossRefGoogle ScholarPubMed
Schmitt, S.Wehrl, M.Bayer, K.Siegl, A.Hentschel, U. 2007 Marine sponges as models for commensal microbe-host interactionsSymbiosis 44 43Google Scholar
Sicard, M.Hinsinger, J.Le Brun, N. 2006 Interspecific competition between entomopathogenic nematodes () is modified by their bacterial symbionts ()BMC Evolutionary Biology 6 68CrossRefGoogle Scholar
Sikes, B. A.Cottenie, K.Klironomos, J. N. 2009 Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizasJournal of Ecology 97 1274CrossRefGoogle Scholar
Sonnenburg, J. L.Chen, C. T. L.Gordon, J. I. 2006 Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and hostPLoS Biology 4 2213CrossRefGoogle Scholar
Stabb, E. V.Millikan, D. S. 2009 Is the symbiosis a defensive mutualismWhite, Jr. J. F.Torres, M. S.Defensive Mutualism in Microbial SymbiosisBoca Raton, FLCRC Press85Google Scholar
Steiner, U.Ahimsa-Muller, M. A.Markert, A. 2006 Molecular characterization of a seed transmitted clavicipitaceous fungus occurring on dicotyledonous plants (Convolvulaceae)Planta 224 533CrossRefGoogle Scholar
Stovall, M.Clay, K. 1991 Fungitoxic effects of (Clavicipitaceae)Mycologia 83 288CrossRefGoogle Scholar
Tinh, N. T. N.Dierckens, K.Sorgeloos, P.Bossier, P. 2008 A review of the functionality of probiotics in the larviculture food chainMarine Biotechnology 10 1CrossRefGoogle ScholarPubMed
Tsuchida, T.Koga, R.Horikawa, M. 2010 Symbiotic bacterium modifies aphid body colorScience 330 1102CrossRefGoogle ScholarPubMed
Turnbaugh, P. J.Ley, R. E.Hamady, M. 2007 The Human Microbiome ProjectNature 449 804CrossRefGoogle ScholarPubMed
van der Heijden, M. G. A.Klironomos, J. N.Ursic, M 1998 Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivityNature 396 69CrossRefGoogle Scholar
Vannette, R. L.Hunter, M. D. 2009 Mycorrhizal fungi as mediators of defence against insect pests in agricultural systemsAgricultural and Forest Entomology 11 351CrossRefGoogle Scholar
Verschuere, L.Heang, H.Criel, G.Sorgeloos, P.Verstraete, W. 2000 Selected bacterial strains protect spp. from the pathogenic effects of CW8T2Applied and Environmental Microbiology 66 1139CrossRefGoogle ScholarPubMed
Werner, E. E.Peacor, S. D. 2003 A review of trait-mediated indirect interactions in ecological communitiesEcology 84 1083CrossRefGoogle Scholar
Xie, J. L.Vilchez, I.Mateos, M. 2010 bacteria enhance survival of attacked by the parasitic wasp PLoS ONE 5 e12149CrossRefGoogle ScholarPubMed
Yoder, J. A.Benoit, J. B.Denlinger, D. L.Tank, J. L.Zettler, L. W. 2008 An endosymbiotic conidial fungus, , protects the American dog tick, , from desiccation imposed by an entomopathogenic fungusJournal of Invertebrate Pathology 97 119CrossRefGoogle ScholarPubMed
Zytynska, S. E.Fleming, S.Tetard-Jones, C.Kertesz, M. A.Preziosi, R. F. 2010 Community genetic interactions mediate indirect ecological effects between a parasitoid wasp and rhizobacteriaEcology 91 1563CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×