Abstract
The high Andean forests of the genus Polylepis (Rosaceae) are threatened by extinction due to anthropogenic effects such as timber extraction, burning, and overgrazing. Some species are also affected by Tristerix chodatianus (Loranthaceae), a hemiparasitic plant which induces progressive host damage. To understand this hemiparasitic process, we evaluated the impact of T. chodatianus on growth and the wood anatomy of Polylepis flavipila using growth rings and digital image processing. We found that P. flavipila has a xeromorphic wood anatomy and that the ecological indices of mesomorphism and vulnerability decrease at higher elevations to avoid embolisms and vessel cavitation. Tristerix chodatianus causes anatomical changes in the host wood, mainly in the last 13 years measured. Alterations include a reduction in the vessel density, and an increase in the vessel diameter and Vulnerability Index, all of which are more evident in downstream sections of parasitized branches. These changes in the xylem tissues increase the vulnerability of the parasitized branches to embolisms and cavitation, thus leading to progressive death of the tree crown. Our study confirms that the analysis of the wood anatomy of parasitized branches can be used to determine the years of colonization of a tree branch by a hemiparasite and that it can be a useful tool to monitor the phytosanitary state of parasitized Polylepis trees.
Similar content being viewed by others
References
Amico G, Vidal-Russell R, Nickrent D (2007) Phylogenetic relationships and ecological speciation in the mistletoe Tristerix (Loranthaceae): The influence of pollinators, dispersers, and hosts. Am J Bot 94(4):558–567. https://doi.org/10.3732/ajb.94.4.558
Argollo J, Soliz C, Villalba R (2004) Potencialidad dendrocronológica de Polylepis tarapacana en los Andes Centrales de Bolivia. Ecol de Boliv 39(1):5–24
Arizapana M (2018) Estrutura populacional de florestas de Polylepis Ruiz & Pav. e o padrão de parasitismo por Tristerix um gradiente altitudinal nos andes centrais do Peru. Dissertation, Universidade Federal de Lavras.
Arroyo S (2015) Morfología y fisiología de tres especies de polylepis P. microphylla (Wedd.) Bitter, P. racemosa Ruiz & Pav. y P. subsericans J.F. Macbr. (Rosaceae) en tres niveles altitudinales, en yanacocha, urubamba – cusco. Dissertation, Universidad Nacional de San Antonio Abad del Cusco.
Atsatt P (1983) Host-parasite interactions in higher plants. In: Lange OL, Nobel PS (eds) Physiological plant ecology III: responses to the chemical and biological environment, vol 13. Springer, Berlin, pp 519–535
Baddeley A (2008) Analysing spatial point patterns in R. CSIRO, Canberra
Barão V (2015) Relações hídricas e anatomia da relação parasita-hospedeira entre Psittacanthus robustos e Vochysia thyrsoidea. Dissertation, Universidade de São Paulo.
Bartón K (2012) Package ‘MuMIn: Multi-model inference’. https://r-forge.r-project.org/R/?group_id=346
Bates D et al. (2015) Fitting Linear Mixed-Effects Models Using lme4. v. 67, n. 1, p. 48, 2015–10–07 2015. ISSN 1548–7660. https://www.jstatsoft.org/v067/i01
Beltrán L, Valencia G (2013) Anatomia de anillos de crecimiento de 80 especies arbóreas potenciales para estudios dendrocronológicos en la selva central, Perú. Rev de Biol Trop 61(3):1025–1037
Bolker B, Brooks M, Clark C, Geange S, Poulsen J, Stevens MH, White JS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24(3):127–135. https://doi.org/10.1016/j.tree.2008.10.008
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Camel V, Quispe-Melgar H, Ames-Martínez F, Navarro W, Segovia-Salcedo M, Kessler M (2019) Forest structure of three endemic species of the genus Polylepis (Rosaceae) in central Peru. Ecologia Austral
Carlquist S (1977) Ecological factors in wood evolution: a floristic approach. JSTOR 64(7):887–896. https://doi.org/10.2307/2442382
Chartier MP, Giantomasi MA, Renison D, Roig FA (2016) Exposed roots as indicators of geomorphic processes: A case-study from Polylepis mountain woodlands of Central Argentina. Dendrochronologia 37:57–63. https://doi.org/10.1016/j.dendro.2015.11.003
Clausen J (1963) Tree lines and germ plasm-a study in evolutionary limitations. Proc Natl Acad Sci USA 50:860–868
Fonti P, Von Arx G, García-González I, Eilmann B, Sass-Klaassen U, Gärtner H, Eckstein D (2010) Studying global change through investigation of the plastic responses of xylem anatomy in tree rings. New Phytol 185(1):42–53. https://doi.org/10.1111/j.1469-8137.2009.03030.x
Gil R, Villalba R (2005) Tree rings as a surrogate for economic stress – an example from the Puna of Jujuy, Argentina in the 19th century. Dendrochronologia 22:141–147. https://doi.org/10.1016/j.dendro.2005.06.002
Gonzáles W, Suárez LRM (2007) Outcrossing increases infection success in the holoparasitic mistletoe Tristerix aphyllus. Evol Ecol. https://doi.org/10.1007/s10682-006-0021-0
Glatzel G, Geils B (2009) Mistletoe ecophysiology: host-parasite interactions. Botany 87:10–15
Greenwell B, Schubert C (2014) investr: an R package for inverse estimation. R J 6(1):90–100
Grothendieck G (2013) Package “nls2”: non-linear regression with brute force.
Gurau L, Timar MC, Porojan M, Ioras F (2013) Image processing method as a supporting tool for wood species identification. Wood Fiber Sci 45(3):303–313
Hadley W (2011) The split-apply-combine strategy for data analysis. J Stat Softw 40(1):1–29
Kessler M (2006) Bosques de Polylepis. Botánica Económica de los Andes Centrales. Universidad Mayorde San Andrés, La Paz
Kessler M, Schmidt-Lebuhn AN (2006) Taxonomical and distributional notes on Polylepis (Rosaceae). Org Divers Evol 6(1):67–69. https://doi.org/10.1016/j.ode.2005.04.001
Korner C, Paulsen J (2004) A world-wide study of high altitude treeline temperatures. J Biogeogr 31(5):713–732
Kuijt J (2016) Revision of Tristerix (Loranthaceae). JSTOR 19:1–61
Kuznetzova A, Bbrockhoff P (2015) Package ‘lmerTest’. https://github.com/runehaubo/lmerTestR
Legland D (2014) Statistical Mapping of Maize Bundle Intensity at the Stem Scale Using Spatial Normalisation of Replicated Images. PLoS ONE 9(3):1–10. https://doi.org/10.1371/journal.pone.0090673
Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol 190(3):709–723. https://doi.org/10.1111/j.1469-8137.2010.03518.x
Loepfe L, Martinez-Vilalta J, Piñol J, Mencuccini M (2007) The relevance of xylem network structure for plant hydraulic efficiency and safety. J Theor Biol 247(4):788–803. https://doi.org/10.1016/j.jtbi.2007.03.036
Mathiasen R, Nickrent D, Shaw D, Watson D (2008) Mistletoes: pathology, systematics, ecology, and management. Plant Dis 92(7):988–1006. https://doi.org/10.1094/PDIS-92-7-0988
Medel R, Botto-Mahan C, Smith-Ramírez C, Méndez MA, Ossa CG, Caputo L, Gonzáles WL (2002) Historia natural cuantitativa de una relación parásito-hospedero: El sistema Tristerix-cactáceas en Chile semiárido. Rev Chil de Hist Nat 75(1):127–140. https://doi.org/10.4067/S0716-078X2002000100012
Mencuccini M, Martinez-vilalta J, Pi J, Loepfe L, Burnat M, Alvarez X, Gil D (2010) A quantitative and statistically robust method for the determination of xylem conduit spatial distribution. Botany 97(8):1247–1259. https://doi.org/10.3732/ajb.0900289
Morales MS, Christie DA, Villalba R, Argollo J, Pacajes J, Silva JS, Llancabure JC (2012) Precipitation changes in the South American Altiplano since 1300 AD reconstructed by tree-rings. Clim Past. https://doi.org/10.5194/cp-8-653-2012
Moya J, Lara A (2011) Tree rings Chronologies of queñoa (Polylepis tarapacana) for the last 500 years in the Altiplano of Chile. Bosque 32(2):165–173. https://doi.org/10.4067/S0717-92002011000200007
Nickrent D (2002) Parasitic plants of the world. In: López-Sáez LA, Catalán P (eds) Parasitic plants of the Iberian Peninsula and Balearic Islands. Mundi-Prensa, Madrid, pp 7–27
Okubamichael D, Griffiths M, Ward D (2016) Host specificity in parasitic plants—perspectives from mistletoes. Environ Evol Plant Biol.. https://doi.org/10.1093/aobpla/plw069
Press C, Phoenix G (2005) Impacts of parasitic plants on natural communities. New Phytol 166(3):737–751. https://doi.org/10.1111/j.1469-8137.2005.01358.x
R Development core team (2015) R: a languague and enviroment for statistical computing. Vienna: R Foundation for Statistical Computing.
Rowntree JK, Cameron DD, Preziosi RF, Sheffield S (2011) Genetic variation changes the interactions between the parasitic plant-ecosystem engineer Rhinanthus and its hosts. R Soc 366(1569):1380–1388. https://doi.org/10.1098/rstb.2010.0320
Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET, Eliceiri KW (2017) Image J2: ImageJ for the next generation of scientific image data. BMC Bioinform 18(1):1–26. https://doi.org/10.1186/s12859-017-1934-z
Rundel PW, Gibson AC, Midgley GS, Wand SJE, Palma B, Kleier C (2003) Ecological and ecophysiological patterns in a pre-altiplano shrubland of the Andean Cordillera in northern Chile. Plant Ecol 169:179–193. https://doi.org/10.1023/A:102607572
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675. https://doi.org/10.1038/nmeth.2089
Scholz A, Klepsch M, Karimi Z, Jansen S (2013) How to quantify conduits in wood? Front Plant Sci 4:56. https://doi.org/10.3389/fpls.2013.00056
Sylvester SP, Sylvester MDPV, Kessler M (2014) The world’s highest vascular epiphytes found in the Peruvian Andes. Alp Bot 124(2):179–185. https://doi.org/10.1007/s00035-014-0130-2
Sylvester SP, Heitkamp F, Sylvester MDPV, Jungkunst HF, Sipman HJM, Toivonen JM, Kessler M (2017) Relict high-Andean ecosystems challenge our concepts of naturalness and human impact. Sci Rep 7(1):1–13. https://doi.org/10.1038/s41598-017-03500-7
Teixeira-Costa GC (2015) Embolism increase and anatomical modifications caused by a parasitic plant: Phoradendron crassifolium (Santalaceae) on Tapirira guianensis (Anacardiaceae). IAWA J. https://doi.org/10.1163/22941932-00000091
Trinidad H, Cano A (2016) Composición florística de los bosques de Polylepis Yauyinazo y Chaqsii-Chaqsii, Reserva Paisajística Nor Yauyos-Cochas, Lima. Rev Peru de Biol, 23(3), 271–286.
Winston RR (2002) Historia de los pueblos de Yauyos. R&R Ediciones, Lima
Wickham H (2016) ggplot2: ggplot2: elegant graphics for data analysis. Springer, New York
Zotz G (2005) Vascular epiphytes in the temperate zones–a review. Plant Ecol 176(2):173–183. https://doi.org/10.1007/s11258-004-0066-5
Zutta BR, Rundel PW (2017) Modeled shifts in polylepis species ranges in the Andes from the last glacial maximum to the present. Forests 8(7):232. https://doi.org/10.3390/f8070232
Zutta B, Rundel P, Saatchi S (2012) Prediciendo la distribución de Polylepis: bosques Andinos vulnerables y cada vez más importantes. Rev Peru de Biol 19: 205–212
Acknowledgements
We thank the “Servicio Nacional de Áreas Naturales Protegidas por el Estado” for providing authorizations for research under the R.D. 009–2018-SERNANP-JEF. We are also grateful to the District Municipality of Laraos. Thanks are also due to Edith Orellana, Julio Alvares, Italo Castañeda, Joel Sulca, Henry Pariona, David Huayta, Mirla and Antoni Guerra for supporting the fieldwork.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
The manuscript described above is in compliance with Ethical Standards.
Additional information
Communicated by Joy Nystrom Mast.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Camel, V., Arizapana-Almonacid, M., Pyles, M. et al. Using dendrochronology to trace the impact of the hemiparasite Tristerix chodatianus on Andean Polylepis trees. Plant Ecol 220, 873–886 (2019). https://doi.org/10.1007/s11258-019-00961-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-019-00961-w