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Vertebrate faeces as sources of nodulating Frankia in Patagonia

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Abstract

Frankia strains nodulate the native actinorhizal plant Ochetophila trinervis (sin. Discaria trinervis), which grows in stream margins and nearby areas in northwest Patagonia (Argentina). Infective Frankia are found in soils with presence of host plants but also may be found in areas lacking them. This may be partly explained by water transport of Frankia propagules but there are other possible sources. The aim of this study was to discover whether the faeces of introduced mammalian herbivores, including cows (Bos taurus, adult and calf), horses (Equus caballus), sheep (Ovis aries), red and/or fallow deer (Cervus elaphus and Dama dama, respectively), wild boar (Sus scrofa), European hare (Lepus capensis), or the native upland goose (Chloephaga picta), could be a source of infective Frankia, and enhance its dispersal. Faecal material and soil samples were aseptically sampled in different plant communities, and tested via plant bioassays using O. trinervis. The faeces of all animals contained infective Frankia and led to an effective symbiosis with this plant. Faeces of large introduced herbivores gave rise to higher nodulation (number of nodulated plants with respect to the total number of inoculated plants) than faeces of hare and upland goose. Soils from the sites where the cow (two sites), sheep, wild boar and deer faeces were collected did not contain infective Frankia. This suggests that the animals may have ingested Frankia from plant material and that the Frankia propagules passed through the digestive tracts of the animals without losing its infectivity. We conclude that the faeces of large introduced herbivores contribute to the dispersal of infective Frankia in Northwest Patagonia.

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References

  • Arveby AS, Huss-Danell K (1988) Presence and dispersal of infective Frankia in peat and meadow soils in Sweeden. Biol Fertil Soils 6:39–44

    Article  Google Scholar 

  • Barrios-Garcia MN, Relva MA, Kitzberger T (2011) Patterns of use and damage by exotic deer on native plant communities in Northwestern Patagonia. Eur J Wildl Res. doi:10.1007/s10344-011-0554-6

  • Benson DR, Dawson JO (2007) Recent advances in the biogeography and genecology of symbiotic Frankia and its host plants. Physiol Plant 130:318–330

    Article  CAS  Google Scholar 

  • Benson DRB, Vanden Heuvel B, Potter D (2004) Actinorhizal symbioses: diversity and biogeography. In: Gillings M, Holmes A (eds) Plant microbiology. BIOS Scientific Publishers, Oxford, pp 97–127

    Google Scholar 

  • Bissett NS (2008) Avian dispersal of the Actinomycete Frankia across a barrier island landscape. Master of Science Thesis. Virginia Commonwealth University. Richmond, Virigina. http://amazon.evsc.virginia.edu/thesis/SPENCER_NATHANIEL_BISSETT2008.pdf Accessed 29/09/11

  • Blackhall M, Raffaele E, Veblen TT (2008) Cattle affect early post-fire regeneration in a Nothofagus dombeyi—Austrocedrus chilensis mixed forest in northern Patagonia, Argentina. Biol Conserv 141:2251–2261

    Article  Google Scholar 

  • Bond G (1976) The results of the IBP survey of root-nodule formation in non-leguminous angiosperms. In: Nutman PS (ed) Symbiotic nitrogen fixation in plants. Cambridge University Press, Cambridge, pp 443–474

    Google Scholar 

  • Burleigh SH, Dawson JO (1994a) Occurrence of Myrica-nodulating Frankia in Hawaiian volcanic soils. Plant Soil 164:283–289

    Article  CAS  Google Scholar 

  • Burleigh SH, Dawson JO (1994b) Desiccation tolerance and trehalose production in Frankia hyphae. Soil Biol Biochem 25:593–598

    Article  Google Scholar 

  • Burleigh HB, Dawson JO (1995) Spores of Frankia strain HFPCc13 nodulate Casuarina equisetifolia after passage through the digestive tracts of captive parakeets (Melopsittacus undulatus). Can J Bot 73:1527–1530

    Article  Google Scholar 

  • Cardoso BM, Chaia EE, Raffaele E (2010) Are Northwestern Patagonian “mallín” wetland meadows reservoirs of Ochetophila trinervis infective Frankia? Symbiosis 52:11–19

    Article  Google Scholar 

  • Chaia EE (1998) Isolation of an effective strain of Frankia from nodules of Discaria trinervis (Rhamnaceae). Plant Soil 205:99–102

    Article  CAS  Google Scholar 

  • Chaia E, Raffaele E (2000) Spatial patterns of root branching and actinorhizal nodulation in Discaria trinervis seedlings. Symbiosis 29:329–341

    Google Scholar 

  • Chaia EE, Ribeiro Guevara S, Rizzo A, Arribére M (2005) Occurrence of Discaria trinervis nodulating Frankia in dated sediments of glacial Andean lakes. Symbiosis 39:67–75

    Google Scholar 

  • Chaia EE, Fontenla S, Vobis G, Wall LG (2006) Infectivity of soilborne Frankia and micorrhizae in Discaria trinervis along a vegetation gradient in Patagonian soil. J Basic Microbiol 46:263–274

    Article  PubMed  Google Scholar 

  • Chaia EE, Wall LG, Huss-Danell K (2010) Life in soil by the actinorhizal root nodule endophyte Frankia. A review. Symbiosis 51:201–226

    Article  Google Scholar 

  • Dawson JO (2008) Ecology of actinorhizal plants. In: Pawloski K, Newton WE (eds) Nitrogen fixation: origins, applications, and researh progress, Vol 6, nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, pp 199–234

    Google Scholar 

  • del Valle H (1998) Patagonian soils: a regional synthesis. Ecol Austral 8:103–123

    Google Scholar 

  • Densmore RV (2005) Succession on subalpine glacier mine spoil: effects of revegetation with Alnus viridis, Alaska, U.S.A. Arctic Antarct Alpine Res 37:297–303

    Article  Google Scholar 

  • Gtari M, Dawson JO (2011) An overview of actinorhizal plants in Africa. Funct Plant Biol 38:653–661

    Article  Google Scholar 

  • Hahn D, Nickel A, Dawson J (1999) Assessing Frankia populations in plants and soil using molecular methods. FEMS Microbiol Ecol 29:215–227

    Article  CAS  Google Scholar 

  • Houwers A, Akkermans ADL (1981) Influence of inoculation on yield of Alnus glutinosa in the Netherlands. Plant Soil 61:189–202

    Article  Google Scholar 

  • Huss-Danell K (1978) Nitrogenase activity measurements in intact plants of Alnus incana. Physiol Plant 43:372–376

    Article  CAS  Google Scholar 

  • Huss-Danell K, Frej A (1986) Distribution of Frankia in soils from forests and afforestation sites in Northern Sweden. Plant Soil 90:407–418

    Article  Google Scholar 

  • Huss-Danell K, Uliassi D, Renberg I (1997) River and lake sediments as sources of infective Frankia (Alnus). Plant Soil 197:35–39

    Article  CAS  Google Scholar 

  • Huss-Danell K, Sverrisson H, Hahlin AS, Danell K (1999) Occurrence of Alnus-infective Frankia and Trifolium infective Rhizobium in circumpolar soils. Arctic Antarct Alpine Res 31:400–406

    Article  Google Scholar 

  • Kohls SJ, Van Kessel C, Baker DD, Grigal D, Lawrence DB (1994) Assessment of N2 fixation and N cycling by Dryas along a chronosequence within the forelands of the Athabasca glacier, Canada. Soil Biol Biochem 26:623–632

    Article  CAS  Google Scholar 

  • Laos F, Satti P, Walter I, Mazzarino MJ, Moyano S (2000) Nutrient availability of composted and noncomposted residues in a Patagonian Xeric Mollisol. Biol Fertil Soils 31:462–469

    Article  CAS  Google Scholar 

  • Manacorda M, Somlo M, Sbriller AP, Willems P (1996) Dieta de ovinos y bovinos en la región de los bosques de ñire (Nothofagus antartica) de Río Negro y Neuquén. RIA 26:137–146

    Google Scholar 

  • McCray Batzli J, Zimpfer JF, Huguet V, Smyth CA, Fernandez M, Dawson JO (2004) Distribution and abundance of infective, soilborne Frankia and host symbionts Shepherdia, Alnus and Myrica in a sand dune ecosystem. Can J Bot 82:700–709

    Article  Google Scholar 

  • Mirza BS, Welsh A, Hahn D (2007) Saprophytic growth of inoculated Frankia sp. in soil microcosms. FEMS Microbiol Ecol 62:280–289

    Article  CAS  PubMed  Google Scholar 

  • Mirza BS, Welsh A, Rieder JP, Paschke MW, Hahn D (2009) Diversity of frankiae in soils from five continents. Syst Appl Microbiol 32:558–570

    Article  CAS  PubMed  Google Scholar 

  • Nuñez MA, Bailey JK, Schweitzer JA (2009) Population, community and ecosystem effects of exotic herbivores: a growing global concern. Biol Invasions 12:297–301

    Article  Google Scholar 

  • Oremus PAI (1980) Occurrence and infective potential of the endophyte of Hippophae rhamnoides L. ssp. rhamnoides in coastal sand-dune areas. Plant Soil 56:123–139

    Article  CAS  Google Scholar 

  • Paruelo JM, Beltrán A, Jobbágy E, Sala OE, Golluscio RA (1998) The climate of Patagonia: general patterns and controls on biotic processes. Ecol Austral 8:85–101

    Google Scholar 

  • Paschke MW (1993) Distribution and dispersal of Frankia. Ph.D. Thesis. University of Illinois at Urbana-Champaign. Illinois, USA, pp 83

  • Paschke MW, Dawson JO (1993) Avian dispersal of Frankia. Can J Bot 71:1128–1131

    Article  Google Scholar 

  • Pelliza A, Willems P, Nakamatsu V, Manero A (coordinadores) (1997) Atlas dietario de herbívoros patagónicos. In: Somlo R (ed) INTA Estación Experimental Agropecuaria Bariloche, pp. 109

  • Raffaele E, Veblen TT (2001) Effects of cattle grazing on early postfire regeneration of matorral in northwest Patagonia, Argentina. Nat Areas J 21:243–249

    Google Scholar 

  • Raffaele E, Veblen TT, Blackhall M, Tercero-Bucardo N (2011) Synergistic influences of introduced herbivores and fire on vegetation change in northern Patagonia, Argentina. J Veg Sci 22:59–71

    Article  Google Scholar 

  • Redell P, Spain AV (1991) Transmission of infective Frankia (actinomycetales) propagules in casts of the endogeic earth-worm Pontoscolex corethurus (Oligochaeta, Glossoscolecidae). Soil Biol Biochem 23:775–778

    Article  Google Scholar 

  • Relva MA, Caldiz MS (1998) Composición estacional de la dieta de ciervos exóticos en Isla Victoria, Parque Nacional Nahuel Huapi, Argentina. Gayana Zool 62:101–108

    Google Scholar 

  • Relva MA, Veblen TT (1998) Impact of introduced large herbivores on Austrocedrus chilensis forest in northern Patagonia, Argentina. For Ecol Manage 108:27–40

    Article  Google Scholar 

  • Reyes MF, Gobbi ME, Chaia EE (2011) Reproductive ecology of Ochetophila trinervis in northwest Patagonia. Funct Plant Biol 38:720–727

    Article  Google Scholar 

  • Roig C, Roig FA (2004) Consideraciones generales. In: Blanco DE, de la Balze VM (eds) Los Turbales de la Patagonia: Bases para su inventario y la conservación de su biodiversidad. Publicación No. 19. Wetlands International. Buenos Aires, Argentina, pp. 29

  • Rodriguez-Barrueco C (1968) The occurrence of the root-nodule endophyte of Alnus glutinosa and Myrica gale in soils. J Gen Microbiol 52:189–194

    Google Scholar 

  • Smolander A, Sundman V (1987) Frankia in acid soils devoid of actinorhizal plants. Physiol Plant 70:297–303

    Article  Google Scholar 

  • Van Dijk C (1984) Ecological aspects of spore formation in the Frankia-Alnus symbiosis. PhD Thesis, Leiden State University, The Netherlands, pp. 154

  • Vázquez DP (2002) Multiple effects of introduced mammalian herbivores in a temperate forest. Biol Invas 4:175–191

    Article  Google Scholar 

  • Warner NJ, Allen MF, Macmahon JA (1987) Dispersal agents of vesicular-arbuscular mycorrhizal fungi in a disturbed arid ecosystem. Mycologia 79:721–730

    Article  Google Scholar 

  • Young DR, Sande E, Peters G (1992) Spatial relationships of Frankia and Myrica cerifera on a Virginia, USA Barrier Island. Symbiosis 12:209–220

    Google Scholar 

  • Zimpfer JC, Smyth CA, Dawson JO (1997) The capacity of Jamaican mine spoils, agricultural and forest soils to nodulate Myrica cerifera, Leucaena leucocephala and Casuarina cunninghamiana. Physiol Plant 99:664–672

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Mark Paschke for early comments and suggestions for performing this study, to Andrea Relva and Gladys Galende for help in sampling and faeces identification and to David Richardson and three anonymous referees that contributed to improve the quality of the paper. This work was funded by Universidad Nacional del Comahue and Agencia Nacional de Promoción Científica y Tecnológica.

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Authors and Affiliations

  1. Centro Regional Universitario Bariloche, Universidad Nacional del Comahue / INIBIOMA, Quintral 1250, S.C. Bariloche, R8400 FRD, Argentina

    Eugenia E. Chaia

  2. Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, Quintral 1250, S.C. Bariloche, R8400 FRD, Argentina

    Maria C. Sosa

  3. Laboratorio Ecotono, Universidad Nacional del Comahue-INIBIOMA/CONICET, Quintral 1250, S.C. de Bariloche, R8400 FRD, Argentina

    Estela Raffaele

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  1. Eugenia E. Chaia
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Correspondence to Eugenia E. Chaia.

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Chaia, E.E., Sosa, M.C. & Raffaele, E. Vertebrate faeces as sources of nodulating Frankia in Patagonia. Symbiosis 56, 139–145 (2012). https://doi.org/10.1007/s13199-012-0169-z

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