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Azorella Compacta: Survival Champions in Extreme, High-Elevation Environments 1, 1 1 FRANCISCO I

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Azorella Compacta: Survival Champions in Extreme, High-Elevation Environments 1, � 1 1 FRANCISCO I ECOSPHERE NATURALIST Azorella compacta: survival champions in extreme, high-elevation environments 1, 1 1 FRANCISCO I. PUGNAIRE , JOSE A. MORILLO , CRISTINA ARMAS , 2 3,4,5 SUSANA RODRIGUEZ-ECHEVERRIA , AND AURORA GAXIOLA 1Laboratorio Internacional de Cambio Global, Estacion Experimental de Zonas Aridas, Consejo Superior de Investigaciones Cientıficas (EEZA-CSIC), Carretera de Sacramento s/n, 04120 La Canada~ de San Urbano, Almerıa, Spain 2Centro de Ecologia Funcional, Departamento de Ci^encias da Vida, Faculdade de Ci^encias e Tecnologia, Universidade de Coimbra, Apartado 3046, 3001-401 Coimbra, Portugal 3Departamento de Ecologıa, Facultad de Ciencias Biologicas, Pontificia Universidad Catolica de Chile, Alameda 340, Santiago, Chile 4Laboratorio Internacional de Cambio Global, Facultad de Ciencias Biologicas, Pontificia Universidad Catolica de Chile, Alameda 340, Santiago, Chile 5Instituto de Ecologıa and Biodiversidad (IEB), Casilla 653, Santiago, Chile Citation: Pugnaire, F. I., J. A. Morillo, C. Armas, S. Rodrıguez-Echeverrıa, and A. Gaxiola. 2020. Azorella compacta: survival champions in extreme, high-elevation environments. Ecosphere 11(2):e03031. 10.1002/ecs2.3031 Abstract. Cushion plants are life forms with a hemispherical or mat-like, prostrate canopy well adapted to the extreme conditions of cold regions that have appealed to scientists for their ability to cope with extreme environments in most mountains, arctic, and subantarctic regions of the world. They can buffer the effects of low temperature and drought and improve soil conditions, which makes them notable facili- tator species. Living at the edge in the Atacama Desert is one such species, Azorella compacta (yareta or llar- eta), in the Apiaceae family that can reach much over 6 m (~20 ft) in diameter with a mat-like shape that tends to hemispherical growth form. Azorella compacta can be found in the dry Puna system, which spreads from northern Chile and Argentina to southern Peru and western Bolivia, between 3800 and 5200 m eleva- tion, making it one of the woody plant species occurring at highest elevations in the world. In this deserted edge of the Atacama, nutrient limitation adds to other stressors such as water scarcity and high UV radia- tion. A compact canopy and the fact that they are embedded in resin prevent beneficiary species from growing within the cushion and condition how senesced leaves decompose inside the canopy. They can reach 3000 yr old and have to deal with episodic disturbance and herbivory events. Plants in such environ- ments may potentially act as microbial refuges, and it could be expected that bacterial endophytes and mycorrhizal fungi have a main role in the functioning of these survival champions. Key words: cushion plants; high-elevation ecosystems; long-lived plants; plant-microbe interactions; Puna. Received 19 November 2019; accepted 25 November 2019. Corresponding Editor: Uffe Nielsen. Copyright: © 2020 The Authors. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail: fi[email protected] Cushion plants are life forms with a hemi- world (Aubert et al. 2014). Their compact habit spherical or mat-like, prostrate canopy well allows cushions to decouple microclimate inside adapted to the extreme conditions of cold regions the canopy from the surrounding environment. that have appealed to scientists for their ability to They can buffer the effects of low temperature cope with extreme environments in most moun- and drought and improve soil conditions tains, arctic, and subantarctic regions of the (Cavieres and Badano 2009). This feature makes ❖ www.esajournals.org 1 February 2020 ❖ Volume 11(2) ❖ Article e03031 ECOSPHERE NATURALIST PUGNAIRE ET AL. them notable facilitator species that enhance sur- western Bolivia, between 3800 and 5200 m eleva- vival of other plant functional groups living tion, making it one of the woody plant species inside the cushion (Reid et al. 2010, Cavieres occurring at highest elevations in the world et al. 2014). The cushion habit is relatively wide- (Kleier et al. 2015). spread, as there have been identified 1309 cush- We came first across this species in 2016, work- ion-forming species distributed in 272 genera ing in Northern Chile to test the effects of cush- and 63 families of angiosperms (Aubert et al. ion plants on soil microbial communities and 2014). their facilitation effect along environmental gra- Since the 1990s, their appeal has increased dients. Work on cushion plants has been exten- among ecologists and, as a consequence, knowl- sive in the Andes since the 1980s (e.g., Villagran edge about their growth form, functional vari- et al. 1978, Armesto et al. 1980, Alliende and ability, ecosystem role, and evolutionary origin Hoffmann 1983), and their facilitation effects (Reid et al. 2010, Boucher et al. 2016) has accrued have been widely documented (e.g., Cavieres remarkably. Some of the biggest among all cush- and Badano 2009 and references therein), as well ion plants are found in the Andes, where species as their changes with elevation (Alliende and in the Azorella or Bolax genera can reach out- Hoffmann 1983, Badano and Cavieres 2006, standing size (Badano and Cavieres 2006). Living Anthelme et al. 2017). But in the Lauca National at the edge in the Atacama Desert is one such Park and Atacama highlands (Puna), Chile, we monster plant, Azorella compacta (yareta or llar- found that A. compacta barely hosted any benefi- eta), a species in the Apiaceae family that can ciary species (Table 1), in sharp contrast to coex- reach much over 6 m (~20 ft) in diameter with a isting Pycnophyllum cushions (Anthelme et al. mat-like shape that tends to hemispherical 2017) and Azorella species elsewhere (Badano growth form (Fig. 1). It catches the eye by its lux- and Cavieres 2006). As other cushion plants, uriant light green amid the pale colors of desert. A. compacta branches are tightly packed and Yareta cushions are generally on a north-facing make a thick canopy with a smooth, continuous aspect and at an angle of about 20° from the hori- surface that has important microclimate effects. zontal to maximize catching solar radiation (Kle- Senesced leaves are kept in contact with the ier et al. 2015). Azorella compacta can be found in branch as it grows, producing a characteristic the dry Puna system, which spreads from north- brown and white pattern if sectioned. In this ern Chile and Argentina to southern Peru and deserted edge of the Atacama, nutrient limitation Fig. 1. A large individual of Azorella compacta at 4600-m elevation in the Puna region at the edge of the Atacama Desert near the Chile-Bolivia border. ❖ www.esajournals.org 2 February 2020 ❖ Volume 11(2) ❖ Article e03031 ECOSPHERE NATURALIST PUGNAIRE ET AL. Table 1. Relative interaction index (RII; Armas et al. cushion and condition how senesced leaves 2004, Ecology 85: 2682–2686) of Azorella compacta and decompose inside the canopy. Most likely the Pycnophyllum sp in the Lauca and Sajama National process is similar to peat formation, that is, an Parks (Chile and Bolivia, respectively). anaerobic process in which organic matter only decomposes in part, making this species a signifi- Lauca National Sajama National Park (Chile)† Park (Bolivia)‡ cant carbon sink. Species RII RII Azorella compacta Phill. can reach 3000 yr old Azorella compacta À0.8 À1.00 (Ralph 1978) although the typical age is around Pycnophyllum sp 0.7 0.59 850 yr; being such long-lived species means it has to deal with episodic stress and herbivory Notes: RII ranges À1to+1, with positive values showing facilitation and negative values showing competition. In both events. And so it does! Loads of resin protect cases, A. compacta appears as a strong competitor which does yaretas against herbivores, and especially, some not allow other (beneficiary) species to grow into its canopy, in clear contrast to co-occurring cushion species like Pycno- chemical compounds called terpenes that make phyllum sp or other Azorella species. up an important fraction of its dry mass and can † Unpublished. ‡ from Anthelme et al. (2017). be seen as droplets on the canopy and in the soil around the cushion. They are serious deterrent adds to other stressors such as water scarcity and for herbivores, to the point that A. compacta is high UV radiation. Plants in such environments virtually free of them (Ralph 1978). Terpenes pro- may potentially act as microbial refuges (Roy duced by A. compacta have high antimicrobial et al. 2013), and in the dry Puna A. compacta activity (Donoso et al. 2015) and contribute to cushions could play a main role as unique protect the plant against pathogenic bacteria. microorganisms shelters. The compact canopy Resin might also affect, thus, the structure and and the fact that they are embedded in resin pre- function of soil microbial communities around vent beneficiary species from growing within the the cushion. This high chemical protection has Thousand-year old meristems likely Microorganisms in the canopy to undergo somac mutaons surface exposed to UV radiaon Endosymbionts and microbial communies buffered from extreme environment Leaf lier embedded in resin undergoing decomposion in a rather unusual environment Soil microbial communies thriving in the root system Fig. 2. Sketch of the structure of a cushion plant and points where research could provide important clues concerning the longevity and adaptation of these species to extreme environments. ❖ www.esajournals.org 3 February 2020 ❖ Volume 11(2) ❖ Article e03031 ECOSPHERE NATURALIST PUGNAIRE ET AL. drawbacks, however, as resin burns easily and efficiently purged by intraorganismal selection thunderstorms lightning often set afire and kill (Pineda-Krch and Fagerstrom€ 1999) but there are the cushion. Nevertheless, and because of its beneficial mutations that are important sources compact structure, protected buds can restore of adaptive fitness (Pineda-Krch and Fagerstrom€ back the canopy after burning in a process easily 1999).
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