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High Nitrogen Contribution by Gunnera Magellanica and Nitro- Gen Transfer by Mycorrhizas Drive an Extraordinarily Fast Primary Succession in Sub-Antarctic Chile

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High Nitrogen Contribution by Gunnera Magellanica and Nitro- Gen Transfer by Mycorrhizas Drive an Extraordinarily Fast Primary Succession in Sub-Antarctic Chile Research High nitrogen contribution by Gunnera magellanica and nitro- gen transfer by mycorrhizas drive an extraordinarily fast primary succession in sub-Antarctic Chile Alberto Benavent-Gonzalez1 , Jose Raggio1 , Johana Villagra1, Jose Manuel Blanquer1, Ana Pintado1 , Ricardo Rozzi2,3,4 , T. G. Allan Green1,5 and Leopoldo G. Sancho1 1Departamento de Biologıa Vegetal II, Facultad de Farmacia, Universidad Complutense de Madrid, 28040, Madrid, Spain; 2Parque Etnobotanico Omora, Sede Puerto Williams, Universidad de Magallanes, Teniente Munoz~ 396, Punta Arenas, Chile; 3Instituto de Ecologıa y Biodiversidad (IEB-Chile), Teniente Munoz~ 396, Puerto Williams, Chile; 4Department of Philosophy and Religion Studies, University of North Texas, Denton, TX76201,USA; 5Biological Sciences, Waikato University, Hamilton3240, New Zealand Summary Author for correspondence: Chronosequences at the forefront of retreating glaciers provide information about coloniza- Alberto Benavent-Gonzalez tion rates of bare surfaces. In the northern hemisphere, forest development can take cen- Tel: +34 913941771 turies, with rates often limited by low nutrient availability. By contrast, in front of the Email: [email protected] retreating Pia Glacier (Tierra del Fuego, Chile), a Nothofagus forest is in place after only 34 yr Received: 29 August 2018 of development, while total soil nitrogen (N) increased from near zero to 1.5%, suggesting a Accepted: 28 March 2019 strong input of this nutrient. We measured N-fixation rates, carbon fluxes, leaf N and phosphorus contents and leaf d15N New Phytologist (2019) 223: 661–674 in the dominant plants, including the herb Gunnera magellanica, which is endosymbiotically doi: 10.1111/nph.15838 associated with a cyanobacterium, in order to investigate the role of N-fixing and mycorrhizal symbionts in N-budgets during successional transition. Key words: cyanobacteria, Gunnera G. magellanica presented some of the highest nitrogenase activities yet reported (potential À1 À1 15 magellanica, mycorrhizas, nitrogen fixation, maximal contribution of 300 kg N ha yr ). Foliar d N results support the framework of a nitrogen isotope discrimination, photosyn- highly efficient N-uptake and transfer system based on mycorrhizas, with c. 80% of N taken thesis, primary succession, Tierra del Fuego. up by the mycorrhizas potentially transferred to the host plant. Our results suggest the symbiosis of G. magellanica with cyanobacteria, and trees and shrubs with mycorrhizas, to be the key processes driving this rapid succession. 2008; Menge & Hedin, 2009; Raggio et al., 2012; Arroniz-Cre- Introduction spo et al., 2014). Later in the succession, vascular plant coloniza- Recently exposed soils after glacier retreat are nutrient-depleted tion and tree establishment can introduce endosymbiotic a- habitats (Yoshitake et al., 2007; Goransson€ et al., 2011; Schulz proteobacteria (i.e. Rhizobium) or actinobacteria (i.e. Frankia et al., 2013). Ecological succession is therefore generally con- with Alnus) as more important N fixers (Lawrence et al., 1967; strained (Tilman, 1990), with nitrogen (N) and phosphorus (P) Chapin et al., 1994; Kohls et al., 2003). Surprisingly, the N-fixa- availability as the most common limiting factors (Vitousek et al., tion by symbiotic associations with vascular plants during pri- 1989, 2010; Vitousek & Howarth, 1991; Yoshitake et al., 2007; mary succession is seldom measured and is therefore possibly Batterman et al., 2013; Schmidt et al., 2016; Castle et al., 2017). underestimated in high-latitude regions. N limitation often occurs in early stages of colonization and is N availability directly impacts primary productivity which, in progressively mitigated by the increasing quantity and availability turn, rests on photosynthetic activity. Photosynthetic organisms of N in the system coming from deposition and biological pro- along the succession in glacier forelands are of paramount impor- cesses (Vitousek & Farrington, 1997). Atmospheric deposition is tance in exponentially increasing the soil organic fraction. Micro- small for most extensive glacier forelands with the exception of bial and cryptogamic communities certainly help to ameliorate À À the Himalayas (i.e. < 1kgNha 1 yr 1; Dentener et al., 2006) the initial harsh conditions of barren exposed substrates, but their and the primary sources of N in these areas are N release from impact on C stock is small in comparison with the contribution the bedrock (Houlton et al., 2018) or biological N-fixation by vascular species (Crocker & Major, 1955; Matthews, 1992; (LeBauer & Treseder, 2008). In the latter case free-living or sym- Chapin et al., 1994). However, photosynthetic rates at glacier biotic cyanobacteria are classic diazotrophic organisms during forelands have been mostly evaluated on cryptogams (Uchida early successional stages (Walker et al., 2003; Schmidt et al., et al., 2006; Yoshitake et al., 2010; De los Rıos et al., 2011; Ó 2019 The Authors New Phytologist (2019) 223: 661–674 661 New Phytologist Ó 2019 New Phytologist Trust www.newphytologist.com New 662 Research Phytologist Raggio et al., 2012), and integrated approaches that also include forms of N but also to take up organic compounds and transfer vascular species are scarce (Muraoka et al., 2002). Thus, improv- these to their host (N€asholm et al., 2008, 2013). Whilst their ing our knowledge of photosynthesis during primary succession increased surface area and uptake capacities at low external con- is essential, not only to accurately characterize the major sources centrations may alter the average N discrimination (d15N) of the of organic C at each successional stage, but also to obtain some available N sources, N isotope discrimination is also markedly level of understanding of possible limitations to C-fixation. changed by the transfer of N from mycorrhizas to their host (for Plant colonization of newly exposed soils in glacier forelands a detailed review see Hobbie & H€ogberg, 2012). In particular, may be rapid (Sattin et al., 2009; Knelman et al., 2012) but forest creation of transfer compounds by mycorrhizal fungi leads to development, if climate allows tree growth, takes several decades retention of 15N-enriched N in the fungus and transfer of 15N- or even hundreds of years (e.g. northern hemisphere: Chapin depleted N to the plant symbiont. For this reason, the d15N value et al., 1994; Alexander & Burt, 1996; southern hemisphere, in plants is an indicator of the occurrence of this process (Kohls Chile: Perez et al., 2014). However, this understanding has been et al., 2003; Hobbie et al., 2005). This 15N fractionation during recently challenged by the rapid succession to a forest that occurs transfer probably occurs in all autotrophic mycorrhizal plants in front of the receding Pia Glacier in Tierra del Fuego, Chile but, normally, it is difficult to directly link plant d15N to soil N (Sancho et al., 2011). Despite the lack of abiotic N inputs in this sources (e.g. the exact d15N of the latter is rarely known; Craine À À region (< 0.7 kg N ha 1 yr 1; Dentener et al., 2006), total soil N et al., 2015). In addition, multiple concomitant factors can also levels increase from below the detection limit at initial succes- influence natural isotopic ratios and hinder the use of plant or sional stages to 1.5% (DW) after 34 yr (Arroniz-Crespo et al., soil isotopic signature to infer N cycling processes (Craine et al., 2014) when a Nothofagus-dominated forest is in place with trees 2009, 2015). However, Pia Glacier foreland is unusual in that reaching 10 m in height. The rapid soil N enrichment and forest initial soil N contents are undetectable (Arroniz-Crespo et al., development both suggest that another N source, possibly biolog- 2014), atmospheric N deposition rate is one of the lowest in the ical N fixation (usually reported to be a crucial N source in glacier world (Dentener et al., 2006), bedrock N is at low levels (Hol- forelands; Chapin et al., 1994), speeds up the succession at Pia loway & Dahlgren, 2002), and there is an almost immediate dis- Glacier. Free-living and symbiotic diazotrophic microorganisms connection of newly exposed surfaces from the meltwater from appear early in the succession (Fernandez-Martınez et al., 2016) the glacier. As a result, almost all N in this glacier foreland proba- with cyanobacteria rapidly becoming broadly distributed as sym- bly comes from N-fixation and the site provides the possibility to bionts in lichens and the vascular plant Gunnera magellanica, and investigate both sources of N and the role of mycorrhizas in epiphytic on mosses (Sancho et al., 2011; Raggio et al., 2012; transferring N to non-N-fixing plants. Arroniz-Crespo et al., 2014). G. magellanica is a native N-fixing We measured the in situ N-fixing capacity of the flowering herb that is common on Fuegian glacier forelands (Henrıquez & plant G. magellanica in front of the receding Pia Glacier to deter- Lusk, 2005; Troncoso et al., 2013; Perez et al., 2014) and, at Pia mine whether this species could be considered as a substantial Glacier, it rapidly dominates the herbaceous layer along the suc- source of N in this area. We also measured the C fluxes (photo- cession and is even present under Nothofagus spp. forest canopy synthetic activity and respiration) to compare the performance of (Sancho et al., 2011). Gunnera is the only angiosperm taxon G. magellanica with other codominant species present in the suc- known to establish a symbiotic relationship with a cyanobac- cessional sequence. Finally, we determined
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