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Evaluation of rust pathogenicity (Phragmidium violaceum) as a biological control agent for the invasive plant Rubus ulmifolius on Robinson Crusoe Island, Chile

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Abstract

Rubus ulmifolius is a highly invasive species that negatively affects biodiversity, especially on Robinson Crusoe Island (RCI), one of the two global mini-hotspots of vascular plants. The rust Phragmidium violaceum has been used as a biological control agent for some Rubus species in mainland Chile, New Zealand and Australia. We aim to quantify P. violaceum pathogenicity over R. ulmifolius on RCI, under both field and laboratory conditions, to determine its potential as a biological control. In addition, in order to broaden our knowledge about the pathogenicity of P. violaceum from RCI, it was also tested on a highly susceptible Rubus species: R. cf. constrictus. We sampled four forest sites on RCI, measuring abiotic, micro-site, and vegetation variables that could be related with infection. In the laboratory, we inoculated P. violaceum into R. ulmifolius seedlings from RCI and R. cf. constrictus seedlings from mainland Chile. We found a low infection incidence in the field, where only 62 of 182 plots presented infected individuals. Applying a fitted generalized linear model, we predicted ten times more infection of P. violaceum on R. ulmifolius when located in southern aspect slopes and shallow soils (< 30 cm). In the laboratory we determined that rust from RCI infected R. ulmifolius individuals from the island in low density, and did not infect R. cf. constrictus; this low infection rate reinforces our field results. The low infection on R. cf. constrictus may mean that P. violaceum from RCI could originate from very impoverished genetic material. We recommend testing different rust genetic origins, mainly from the Old World, to increase their genetic diversity.

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References

  • Arroyo MK (1999) The archipelago of Juan Fernandez. In: Mittermeier R, Myers N, Robles P, Gil C, Mittermeier G (eds) Hotspots, 1st edn. Ediciones de Cemex, México, p 173

    Google Scholar 

  • Bernardello G, Anderson G, Stuessy TF, Crawford D (2006) The angiosperm flora of the archipelago Juan Fernandez (Chile): origin and dispersal. Can J Bot 84(8):1266–1281. https://doi.org/10.1139/b06-092

    Article  Google Scholar 

  • Borcean A, Colcea M, Nita S (2016) Blackberry leaf and fruit diseases in wild flora from south western part of Romania. Res J Agr Sci 48:21–26

    Google Scholar 

  • Bruckart WL III, Michael JL, Sochor M, Trávníček B (2017) Invasive blackberry species in Oregon: their identity and susceptibility to rust disease and the implications for biological control. Invas Plant Sci Mana 10:143–154

    Article  Google Scholar 

  • Bruzzese E, Hasan S (1986) Host specificity of the rust Phragmidium violaceurn, a potential biological control agent of European blackberry. Ann Appl Biol 108(3):585–596

    Article  Google Scholar 

  • Castillo J, Smith-Ramírez C (2018) Negative impact of invasive plant control on soil loss, Robinson Crusoe Island, Chile. Restor Ecol. https://doi.org/10.1111/rec.12700

  • Croarkin C, Tobias P, Filliben JJ, Hembree B, Guthrie W (2006) NIST/SEMATECH e-handbook of statistical methods. NIST/SEMATECH. http://www.itl.nist.gov/div898/handbook. Accessed 26 Jan 2018

  • Danton P, Perrier C (2006) Nouveau catalogue de la flore vasculaire de l’archipel Juan Fernández (Chili). Acta Bot Gallica 153:399–587. Oehrens https://doi.org/10.1080/12538078.2006.10515559

  • Diaz R (2013) Análisis y modelación de la evolución espacio-temporal de la invasión de Rubus ulmifolius, Aristotelia chilensis y Ugni molinae, en la Isla Robinson Crusoe. Undergaduate thesis. Universidad de Chile. Santiago

  • Dirección Meteorológica de Chile (1860-2016) Anuario del Servicio Meteorológico. https://climatologia.meteochile.gob.cl/application/index/anuarios. Accessed 27 Sept 2017

  • Dirnböck T, Greimler J, López P, Stuessy TF (2003) Predicting future threats to the native vegetation of Robinson Crusoe Island, Juan Fernández archipelago, Chile. Conserv Biol 17:1650–1659. https://doi.org/10.1111/j.1523-1739.2003.00173.x

    Article  Google Scholar 

  • Evans KJ, Bruzzese E (2003) Life history of Phragmidium violaceum in relation to its effectiveness as a biological control agent of European blackberry. Australas Plant Pathol 32:231–239

    Article  Google Scholar 

  • Evans KJ, Jones MK, Roush RT (2005) Susceptibility of invasive taxa of European blackberry to rust disease caused by the uredinial stage of Phragmidium violaceum under field conditions in Australia. Plant Pathol 54:275–286. https://doi.org/10.1111/j.1365-3059.2005.01183.x

    Article  Google Scholar 

  • Evans KJ, Gomez DR, Jones MK, Oakey H, Roush RT (2011) Pathogenicity of Phragmidium violaceum isolates on European blackberry clones and on leaves of different ages. Plant Pathol 60:532–544. https://doi.org/10.1111/j.1365-3059.2010.02396.x

    Article  Google Scholar 

  • Frazer GW, Canham CD, Lertzman KP (1999) Gap Light Analyzer (GLA) Imaging software to extract canopy structure and gap light transmission indices from true-colour fisheye photographs, user’s manual and program documentation. Cary Institute of Ecosystem Studies, v2. http://www.caryinstitute.org/science-program/our-scientists/dr-charles-d-canham/gap-light-analyzer-gla. Accessed 27 Sept 2017

  • Gomez DR, Evans KJ, Baker J, Harvey PR, Scott ES (2008) Dynamics of introduced populations of Phragmidium violaceum and implications for biological control of European blackberry in Australia. Appl Environ Microbiol 74:5504–5510. https://doi.org/10.1128/AEM.02885-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greimler J, Lopez PS, Stuessy TF, Dirnböck T (2002) The vegetation of Robinson Crusoe Island (Isla Masatierra), Juan Fernández archipelago, Chile. Pac Sci 56:263–284. https://doi.org/10.1353/psc.2002.0022

    Article  Google Scholar 

  • Hahn IJ, Vergara PM, Römer U (2011) Habitat selection and population trends in terrestrial bird species of Robinson Crusoe Island: habitat generalists versus forest specialists. Biodivers Conserv 20:1–17. https://doi.org/10.1007/s10531-011-0109-x

    Article  Google Scholar 

  • Hejda M, Pyšek P, Jarošík V (2009) Impact of invasive plants on the species richness, diversity and composition of invaded communities. J Ecol 97:393–403. https://doi.org/10.1111/j.1365-2745.2009.01480.x

    Article  Google Scholar 

  • Knops JHM, Tilman D, Haddad NM, Naeem S, Mitchell CE, Haarstad J, Ritchie ME, Howe KM, Reich PB, Siemann E, Groth J (1999) Effects of plant species richness on invasion dynamics, disease outbreaks, insect abundances and diversity. Ecol Lett 2:286–293. https://doi.org/10.1046/j.1461-0248.1999.00083.x

    Article  Google Scholar 

  • Looser G (1927) La zarzamora (Rubus ulmifolius Schott) en Juan Fernández. Revista Chilena de Historia Natural n.d.:84–85

  • Mahr FA, Bruzzese E (1998) The effect of Phragmidium violaceum (Shultz) winter (Uredinales) on Rubus fruticosus L. agg. In South-Eastern Victoria. Plant Protection Quarterly 13:182–185

    Google Scholar 

  • Marzol MV, Cereceda P, Vide JM (2001) The annual regime and persistence of precipitation in Robinson Crusoe Island. Insula 10:53–59

    Google Scholar 

  • Matthei J, Marticorena C, Rodríguez R, Quezada M (1995) Manual de las malezas que crecen en Chile. Alfabeta impresores, Santiago

    Google Scholar 

  • Mazzolari AC, Comparatore VM, Bedmar F (2011) Control of elmleaf blackberry invasion in a natural reserve in Argentina. J Nat Conserv 19:185–191. https://doi.org/10.1016/j.jnc.2010.12.002

    Article  Google Scholar 

  • Mora JP, Smith-Ramírez C (2016) Are birds, wind and gravity legitimate dispersers of fleshy-fruited invasive plants on Robinson Crusoe Island, Chile? Flora-morphology, distribution. Functional Ecology of Plants 224:167–171. https://doi.org/10.1016/j.flora.2016.07.012

    Article  Google Scholar 

  • Morin L, Evans KJ, Sheppard AW (2006) Selection of pathogen agents in weed biological control: critical issues and peculiarities in relation to arthropod agents. Aust J Entomol 45:349–365. https://doi.org/10.1111/j.1440-6055.2006.00562.x

    Article  Google Scholar 

  • Morin L, Evans KJ, Jourdan M, Gomez DR, Scott JK (2011) Use of a trap garden to find additional genetically distinct isolates of the rust fungus Phragmidium violaceum to enhance biological control of European blackberry in Australia. Eur J Plant Pathol 131:289–303. https://doi.org/10.1007/s10658-011-9808-0

    Article  Google Scholar 

  • Morin L, Gomez DR, Evans KJ, Neill TM, Mahaffee WF, Linde CC (2013) Invaded range of the blackberry pathogen Phragmidium violaceum in the Pacific northwest of the USA and the search for its provenance. Biol Invasions 15:1847–1861. https://doi.org/10.1007/s10530-013-0413-3

    Article  Google Scholar 

  • Oehrens E, Garrido N (1986) Posibilidad del control biológico de la Zarzamora (Rubus spp.) en el Archipiélago Juan Fernández, Chile. Boletín de la Sociedad Argentina de Botánica 24:202

    Google Scholar 

  • Oehrens E, González S (1974) Introducción de Phragmidium violaceum (Schulz) winter como factor de control biológico de Zarzamora (Rubus constrictus Lef. et M. y R. ulmifolius Schott). Agro Sur 2:30–33

    Article  Google Scholar 

  • Oehrens E, González S (1977) Dispersión, ciclo biológico y daños causados por Phragmidium violaceum (Schulz) winter en Zarzamora (Rubus constrictus Lef. et M. y R. ulmifolius Schott.) en las zonas Centro Sur y Sur de Chile. Agro Sur 5:73–85

    Google Scholar 

  • R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 27 Sept 2017

  • Rejmánek M (2015) Invasion of Rubus praecox (Rosaceae) is promoted by the native tree Aristotelia chilensis (Elaeocarpaceae) due to seed dispersal facilitation. Gayana Bot 72:27–33

    Article  Google Scholar 

  • Salas C, Stage AR, Robinson AP (2008) Modeling effects of overstory density and competing vegetation on tree height growth. For Sci 54(1):107–122

    Google Scholar 

  • Saunders A, Glen A, Campbell K, Atkinson R, Sawyer J, Hagen E, Torres H (2011) Estudio sobre la factibilidad del manejo de especies invasoras en el archipiélago de Juan Fernández. Chile: Invasive Species International (Informe). Research Gate Web. https://www.researchgate.net/publication/281321190_Estudio_sobre_la_factibilidad_del_manejo_de_especies_invasoras_en_el_Archipielago_de_Juan_Fernandez_Chile/. Accesed 27 Sept 2017

  • Schlatter J, Grez R, Gerding V (2015) Manual Para el reconocimiento de suelos. Universidad Austral de Chile, Valdivia

    Google Scholar 

  • Skottsberg CJF (1953) The vegetation of the Juan Fernández islands. Nat Hist Juan Fernandez and Easter Islands 2:793–960

    Google Scholar 

  • Smith-Ramírez C, Arellano G, Hagen E, Vargas GR, Castillo J, Miranda AA (2013) El rol de Turdus falcklandii (Aves: Passeriforme) Como dispersor de plantas invasoras en el archipiélago de Juan Fernández. Rev Chil Hist Nat 86:33–48. https://doi.org/10.4067/S0716-078X2013000100004

    Article  Google Scholar 

  • Smith-Ramírez C, Vargas R, Castillo J, Mora JP, Arellano-Cataldo G (2017) Woody plant invasions and restoration in forests of island ecosystems: lessons from Robinson Crusoe Island, Chile. Biodivers Conserv 7:1–18. https://doi.org/10.1007/s10531-017-1317-9

    Article  Google Scholar 

  • Stuessy T, Foland KA, Sutter JF, Sanders RW, Silva M (1984) Botanical and geological significance of potassium-argon dates from the Juan Fernandez Islands. Science 225:49–51. https://doi.org/10.1126/science.225.4657.49

    Article  CAS  PubMed  Google Scholar 

  • Thorp JR, Lynch R (2000) The determination of weeds of national significance. http://smtp.auricht.com/dewnr/data/Full_The%20Determination%20of%20Weeds%20of%20National%20Significance.pdf/. Accessed 11 Sept 2017

  • Tykhonenko Y (2007) Geographical distribution of the genus Phragmidium Link. http://dspace.nbuv.gov.ua/handle/123456789/3988. Accessed 11 Sept 2017

  • Vargas R, Gärtner S, Alvarez M, Hagen E, Reif A (2013) Does restoration help the conservation of the threatened forest of Robinson Crusoe Island? The impact of forest gap attributes on endemic plant species richness and exotic invasions. Biodivers Conserv 6–7:1283–1300. https://doi.org/10.1007/s10531-013-0461-0

    Article  Google Scholar 

  • Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 7:702–708. https://doi.org/10.1111/j.1461-0248.2011.01628.x

    Article  Google Scholar 

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Acknowledgments

We are grateful to I. Leiva, (Juan Fernandez National Park administrator 2004-2017) for help in collecting and sending samples to the mainland; to Ana Abarzúa (Universidad Austral de Chile) for collaborating with seedling collection, and Diego Pennekamp who contributed to the field methods. Additionally, we thank Marcia Barrientos and Carla Manríquez (Universidad de La Frontera) who collaborated with formatting matters. Our thanks to Dr. Michael Sohor for performing the ploidy analysis of seeds and to ElSharif Ramires for helping us with the pictures to confirm the identification of R. constrictus. We also acknowledge the collaboration of Susan Angus in the English edition of the manuscript. We especially thank the two anonymous reviewers who significantly improved this document. RVG thanks FONDECYT 11170987 and the Vicerrectoría de Investigación y Postgrado, Universidad de La Frontera (UFRO) for funding this study. CSR thanks the IEB (Instituto de Ecología y Biodiversidad-Chile) projects PF-23, 05-002 and CONICYT AFB 170008 for their financial support.

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Vargas-Gaete, R., Doussoulin, H., Smith-Ramírez, C. et al. Evaluation of rust pathogenicity (Phragmidium violaceum) as a biological control agent for the invasive plant Rubus ulmifolius on Robinson Crusoe Island, Chile. Australasian Plant Pathol. 48, 201–208 (2019). https://doi.org/10.1007/s13313-019-0615-y

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