This article isThis article by protected copyright. All rightsreserved. 10.1111/nph.15838doi: differences to lead between the of thisversion c and Version Record.Please copyediting, paginationbeen throughthe andproofreadingtypesetting, process,may which This article acceptedhas been for publication andundergone fullpeer review buthasnot Accepted: Received: [email protected]: Tel: Author forcorrespondence: 5 76201 4 Chile. 3 Muñoz 396, 2 28040Madrid, Madrid, Spain. 1 Pintado Benavent Alberto mycorrhiza H : Article type (OrcidID:0000 GONZALEZ BENAVENT DR ALBERTO
Biological WaikatoBiological Sciences, University, Hamilton deInstituto y Ecología Parque EtnobotánicoOmora,Parque Williams, SedePuerto deMagallanes, Universidad Departamento de Biología Vegetal II, Facultad de Farmacia, Universidad Complutense de Complutense Universidad Farmacia, de Facultad II, Vegetal Biología de Departamento eatet f hlspy n Rlgo Studies, Religion and Philosophy of Department Accepted Articleigh (34)913941771
, USA n 1 , itrogen Ricardo Rozzi 29 August2018 28 2019 March
s . Chile.
drive
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Regular Manuscript Regular - contribution
González
an extraordinarily
2,3,4 Biodiversidad (IEB
, Alberto Benavent 1 T.G. Green Allan Js Raggio José ,
by
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and nitrogen transfer by by transfer nitrogen and f ot Txs Denton Texas, North of
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TX This article isThis article by protected copyright. All rightsreserved. Accepted discrimination,isotope Keywords: ArticleSummary Dr. Dr. Ricardo Rozzi GreenDr. Allan Dr ManuelJosé Blanquer Villagra Dr Johana Dr. Jos González Dr. Alberto Benavent ORCID: Ana Pintado Leopoldo G.Sancho
é Raggio shrub suggest results Our hostto the plant. mycorrhi su reported G of N a endosymbiotically δ N measured We zeronear to 1 place of front with centuries, take can development forest hemisphere, northern the In surfaces. bare about of rates information colonization provide glaciers retreating of forefront the at Chronosequences
15 unnera pr h rmwr of framework the pport N
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fixing and mycorrhizal fixing andmycorrhizal N symbionts in s n the in after only after with mycorrhi
the retreating Pia Glacier (Tierra del Fuego, Chile) Fuego, del (Tierra Glacier Pia retreating the
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This article isThis article by protected copyright. All rightsreserved. to stage successional each essential is succession al. et al. cryptogam 1994) stock C species vascular on by contribution impact their of but condition substrates harsh exposed initial barren the ameliorate to help certainly communities cryptogamic and increasing exponentially in importance paramount of are activity. photosynthetic therefore, association Chapin a establishment Arróniz ( stages symbiotic or al. 2006) forelands glacier processes increas limitation Yoshitake factors limiting common most the constrained generally Göransson 2007; habitats depleted nutrient are retreat glacier after soils exposed Recently Introduction ctinobacteria
, 2018) , C Accepted2012) , Article - fixation. Hwvr pooytei rts t lce frlns ae en oty evaluated mostly been have forelands glacier at rates photosynthetic However, . 2002) , and ing N Walker - Crespo t al. et
, and integrated approaches integrated and ,
(Vitousek & Farrington, 1997) Farrington, & (Vitousek possibly underestimated or often s the primary source primary the viaiiy iety mat piay rdciiy which productivity primary impacts directly availability system the in N of availability and quantity et al. et s
(Uchida (Uchida biological
ih aclr plants vascular with
Tu, mrvn or knowledge our improving Thus, . cyanobacteria (i.e. (i.e. 19; Kohls 1994; , et al et , 2007; Batterman 2007; , can occurs in early stages of stages early in occurs t al et with the with t al. et Frankia
. , et al. et
. , 2003; Schmidt 2003; introduce , (Tilman, 1990) (Tilman,
, 2014) not only not
N , 2011; Schulz Schulz 2011; , htsnhtc organisms Photosynthetic but also to obtain some level of understanding of understanding of level someobtain to also but - except , 2006; Yoshitake 2006; , fixation
with . s are classic classic are
ae i te succession the in Later of N of
t al. et ion of the of ion
to a to
Alnus Cokr Mjr 15; ates 19; Chapin 1992; Matthews, 1955; Major, & (Crocker
endosymbiotic in high (Vitousek (LeBauer & Treseder, 2008) Treseder, & (LeBauer et al. et in during primary succession succession primary during ccurately characterize the major source major the characterize ccurately et al et , with , 2003) ,
that also that these areas are areas these ) , 2013; Schmidt 2013; , . as more as t al. et diazotrophic . - A
colonization , latitude regions Himalayas (i.e. < 1 kg N ha N kg 1 < (i.e. Himalayas
2008; Menge Menge 2008; tmospheric deposition is small for most extensive most for small is deposition tmospheric nitrogen ( nitrogen et al. et et al. et .
2013) , includ Surprisingly, important , 2010; De los Ríos los De 2010; , , 1989, 2010; Vitousek & Howarth, 1991; Howarth, & Vitousek 2010; 1989, , along the succession succession the along α -
about e p
N release from the bedrock bedrock the from release N .
coming from coming N ,
roteobacteria organisms and
vascular E aclr ln clnzto ad tree and colonization plant vascular )
et al. et & cological cological the . and
is progressively is Hedin 2009; Raggio 2009; Hedin N is htsnhss uig primary during photosynthesis soil organic fraction. Microbial Microbial fraction. organic soil
, 2016; Castle 2016; , the the phosphorus ( phosphorus fixers fixers small .
species In the latter case f case latter the In is during N
deposition and deposition succession - seldom (Lawrence (Lawrence fixation - et al. et in (i.e. 1
, yr. are scarce are
in glacier forelands forelands glacier in possible compar n turn in
early early - (Yoshitake , 2011; Raggio 2011; , 1
P s
; mitigated by the the by mitigated Rhizobium
) et al. et
Dentener of organic C at C organic of measured
availability as availability y symbiotic by is successional et al. et et al et ison therefore, , (Houlton (Houlton
, limitations
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. , 1967; 1967; , , - to the the to
t al. et t al. et living
2012; 2012; et al. et or ) and, . N . on et et et , , ,
This article isThis article by protected copyright. All rightsreserved. succession ecological during nutrition plant in elements by acquisition delFuego.Tierra magellanica al. et r although in of role the studying when neglected surprisingly 20 Bergman, 1976; decades for attention scientific attracted ( taxon angiosperm present and Fuegian Crespo magellanica becom in early at succession be to reported height in m development 10 reaching trees with place in w levels abiotic of lack Glacier Pia receding the of front understanding 1996 Burt, & Alexander decades several al. Nostoc eight, DW eight, , 2009; Knelman 2009; ,
Accepted of estimates Article , at PiaGlacier,it , at , 2017) , ing increase L Plant and ) t al. et under glacierforelands tl is ittle
the ecent studies ecent ral distributed broadly ) after 34 yr 34 after ) on epiphytic and , ,
for
colonization of newly exposed soils in glacier forelands may forelands glacier in soils exposed newly of colonization
2014) , more effort more both
h unique the succession i Glacier Pia has been recently challenged by the the by challenged recently been has N
Nothofagus cuil suc i gair forelands glacier in source N crucial a
non
ilgcl N biological from known about about known biochemical cycles and ecosystem functioning functioning ecosystem and cycles biochemical
or inputs in this region (<0.7 kg N kg (<0.7 region this in inputs
- suggest vn udes f er (e.g. years of hundreds even nw t establish to known et al. et N
. 2 Brmn Obre 2002) Osborne, & Bergman 02; rapidly below the the below - unr magellanica Gunnera ies during fixers
suggest that the N fixing capacity of this species may be high be may species this of capacity fixing N the that suggest (Arróniz
, 2012) , suhr hmshr, Chile, hemisphere, southern ; (Henríquez & is .
(Fernández
nature of the the of nature
canopy forest spp. Free ht another that (Johnson still required still
- (Lambers herbaceous dominates the iain (Cleveland fixation both
mosses as
- in - but iig n smitc d symbiotic and living detection limit at initial initial at limit detection Crespo symbio Tierra del Fuego, Chile Fuego, del Tierra h ft o fxd N fixed of fate the forest development, forest primary - et et Martínez et al. et
Lusk, 2005; Troncoso Troncoso Lusk, 2005; (Sancho
al. N et al. et (Silvester & Smith, 1969; Silvester & McNamara, & Silvester 1969; Smith, & (Silvester a to endosymbio n 2016) , t , 2008; Dickie 2008; , yboi rltosi with relationship symbiotic ore psil booia N fixation N biological possibly source, better in s
i succession. succession. , 2014) , a aie N native a s (Sancho .
N
t al. et t al. et ha t al et oten hemisphere, northern h r The lichens -
understand rapid fixers in ecosystem succession, as well as well as succession, ecosystem in fixers - and 1
yr i ( sis when . Raggio 2011; , ; 2016) , , layer
- apid
1 have Chapin
99 Vitousek 1999; However, . t al. et aorpi microorganisms iazotrophic succession succession Pérez ;
if and M Dentener and son & ega, 2009) Bergman, & Osborne successional et al. et
(
climate allows tree growth, tree allows climate - a
Sancho
fixing herb herb fixing ycorrhiza along
soil
Nothofagus h mi ptwy diig N driving pathways main the been proposed proposed been
et al. et 2011) , the
in the the t al. et , 2013; Johnson 2013; , with t al. et
the Sub the
ecological relevance of relevance ecological enrichment N the succession succession the , 2013; Pérez , 2013;Pérez vascular vascular et al et et al et to a forest forest a to
2014) , . 1994) , ascain ae key are associations l hs eu hs been has genus this
cyanobacter t al. et
Gunnera Chapin Chapin stages . . ht is that t al et , , -
dominated forest is forest dominated
a 2011) antarctic region of region antarctic 2006) be 21; Arróniz 2012; , Hwvr this However, . cyanobacteri
, plant . rapid rapid
o be to
, pes up speeds
that occurs that to 2013). et al. et . Despite the Despite . t al. et
, total soil N soil total , common et al. et
is and is and .% (d 1.5% ia
(Sattin Gunnera h only the essential (usually
, 2016) , 1994; , , 2014) rapidly appear appear
(Pérez (Pérez
forest Thus take even
has um the
on G. ry in et s - . ,
This article isThis article by protected copyright. All rightsreserved. content P, N Piaat succession Glacier extraordinary fast N the foliar determined magellanica (photosynthetic fluxes species the of front in site the glacie an (Dentener ( Glacier Pia However, soil or plant multiple sources mycorrhizalplants autotrophic Hobbie 2003; reason 15 review) transfer ( concentrations external low at capacities uptake and host their to these transfer N of forms diffusible slowly and recalcitrant glacier in evaluated mycorrhi lack plants colonizing early many However, Arróniz δ N - 15 transferring N fix Acceptedmycorrhi Article almost - N enriched N enriched ing cryptogamic species cryptogamic ing ) - r.
, fixing herb herb fixing of the available N sources, N available the of
W
. the the could be considered as considered be could provides the possibility to investigate to possibility the provides As a result a As of (e. of - Especially concomitant Crespo e
immediate disconnection of disconnection immediate et al. et g. h hs pat (3) plant; host the N δ measured zas receding
15
with
the exact δ exact the from mycorrhi from stpc signature isotopic N
t al. et , 2006) , play play
in the fungus the in
value in plants is an indicator of the occurrence of this process this of occurrence the of indicator an is plants in value et al et to non
other δ . magellanica G. , , creation of transfer compounds by mycorrhizal, creationofto compoundsfungiof byretention transfer leads 15 almost all almost
2005) , a N Pia . forelands. the , factors key role in N ac N in role key ,
2014) - foreland co and bedrock bedrock N
15 Glacier (Tierra del Fuego, Chile) Chile) Fuego, del (Tierra Glacier activity in situ in - - N of the latter latter the of N fixing plants. dominant (Näsholm
. nutrient zas
, atmospheric ,
can also can This
in the same area; (2) area; same the in and transfer of transfer and
N the photosynthetic photosynthetic the but a
N is at low levels low at is N Mycorrhi
to the to s unusual is substantial N in o ne N cycling N infer to
,
n respiration) and N - provid 15 normally fixing capacity fixing th
species present in the in present species contents of contents N fractionation fractionation N isotope discrimination is discrimination isotope is et al. et ir quisition quisition influence newly
glacier foreland glacier
host zas s h ag qatt of quantity large the es is , 2008, 2013) 2008, , N
and has
source of N of source , n ht nta si N otns r undetectable are contents N soil initial that in rarely known rarely
deposition it exposed surfaces from the melt water from the the from water melt the from surfaces exposed (see 15 are both sources of N and N of sources both
is u also but N
and, by the transfer process, transfer the by and, natural natural dominant species. species. dominant -
difficult to directly link plant link todirectly difficult
o only not depleted N to the plant symbiont. plant the to N depleted (Holloway & Dahlgren, 2002) Dahlgren, & (Holloway activity Hobbie & Högberg, & Hobbie
a considerably higher N higher a considerably of that
o opr te efrac of performance the compare to processes may alter the average the alter may uig transfer during zas the , in addition to their role in role their to addition in ,
probably isotopic in rate . Whilst t Whilst .
to
; and flowering
succession
of
in order order in this area. this Craine Craine take up organic compounds and and compounds organic up take be to able is one of the lowest in the world world the in lowest the of one is . magellanica G.
this symbiosis has been has symbiosis this also markedly changed by the by changed markedly also
(Craine
ratios
comes heir increased surface area surface increased heir rqie t spot the support to required N et al. et to determine to We hypothesize that: that: hypothesize We increase W plant al sequence al the role of mycorrhi of role the probably occurs in all all in occurs probably e also also e and ( , 2015) , t al. et 2012) from N from G - hinder fixation rate N . chang
measured
ln acs to access plant
magellanica 20, 2015) 2009, , il be will
discrimination δ for a detailed detailed a for . (Kohls - ,
15 . whether fixation In a In and there is there and Finally, w Finally, N to soil N soil toN
e the e the use of use the obtaining obtaining For this For ddition higher rarely et al. et the C the
δ
than and and this 15 zas (1)
G. in in N e , . ,
This article isThis article by protected copyright. All rightsreserved. 34 and 19 10, 7, 4, ages with marked were sites 5 transect, each On line. shore the to close oldest the to glacier the near surface youngest the from running apart m 10 established were transects common 2015. and 2009 visited was foreland Glacier Pia Sampling design aged 7 1 Oerst. (Mirb.) yr. Nothofagus surface all on patches dense with dominated of plants associations cyanobacterial establish which of most rapid. was of description) chronosequence detailed fast cross cor using dendrochronology 2006), and 2000 1990, from (images photographs aerial regression or granitic, moraine of temperature air annual mean with mm) Chile Fuego, del Tierra in Channel Beagle the (54º46 of side north the on Bay, Pia in Glacier study The descriptionSite andMaterials Methods endosymbiotic other to relative b
, S1 , Accepted) Article 4, 7, 10, 19 and 34 and 19 10, 7, 4, , -
growing lichen species lichen growing - a dense, 10 m high high m 10 dense, a sections of sections ). ´ yr.
S 69º40 S yr
ridges, consisting mainly ofmainly consisting ridges, The seral shrub shrub seral The
pce (al 1 aog h crnsqec i fot f h Pa Glacier. Pia the of front in chronosequence the along 1) (Table species G . At each of these sites, mature sites, these of each At . . The length of exposure (surface age) of individual moraines were determined by by determined were moraines individual of age) (surface exposure of length The . and older. The initial The site
unnera
seedlings (60 cm high) were already present after present already were high) cm (60 seedlings high )
cyanobacteria ´ with t with lies W). The climate of the area is dominated by high by dominated is area the of climate The W).
Nothofagus antarctica Nothofagus n h frt ii i visit first the On -
grade co
magellanica n h morain the in
heherbaceous -
stages of succession succession of stages curn non occurring yr
Gaultheria mucronata Gaultheria . eaopi materials, metamorphic
Nothofagus Vegetation colonization and development and colonization Vegetation Placopsis perrugrosa Placopsis .
Lam o ic n two different occasions during the Austral summers of of summers Austral the during occasions different two n layer
. gravels, stones and larger rocks composedof rocks larger and stones gravels, - field exposed after the retreat of two branches of Pia Pia of branches two of retreat the after exposed field .
20, ln mtra ws olce from collected was material plant 2009, n N
Sampling was carried out at five sites with surface ages ages surfacefive withat sites carried out Samplingwas
w oet a peet ( present was forest -
fixing present also ere (G. Forst.) Oerst. Forst.) (G. overwhelmingly dominated by dominatedoverwhelmingly
(< and s with s
c. 4 yr 4
sun
species 4.5ºC 4.5ºC (L.f.) Hook. & Arn. & Hook. (L.f.) .
) (
- Nyl.) Nyl. Nyl.) ages of 7 of ages exposed leav exposed were were (Arróniz (Sancho
u to due
Fg S1) (Fig. dominated by cryptogamic species, species, cryptogamic by dominated progressively trees, and lichenometry using the using lichenometry and trees, N. - yr. 7 Crespo
(see (see
antarctica t al. et yr.
es h drc N upy from supply N direct the and older (Fig.1). older and
annual .
and
Sancho were This
2011) , was present on all sites all on present was et al. et in ,
on the oldest site (34 site oldest the on
G the chronosequence the formed randomly latte precipitation (1600 precipitation .
and , 2014) , magellanica et al et The . r
N. betuloides betuloides N. species . ,
crystalline,
y glacier by (2011) but deposited h more the S collected collected cattered cattered young
T
s or es often (Fig. hree
for for
This article isThis article by protected copyright. All rightsreserved. developed C for used also was for described alpinum in present (only abundant locally were equipment). the of range measurement within (and camp base with cubes soil similar of possible N forest magellanica G. (10 cubes soil of consisting samples two plot, each At production). ( plants between independence ensure to separation m 10 ( clearings forest in areas rocks on growing cryptogams occasional and layer herbaceous the a within exposure) patagonica area) moraine front glacier the to close immediately 1: area 1): (Fig. front glacier the to parallel complete collected we this, do To fixation. Universidad sterile surface each at locations chosen randomly Green to couriered L 1). (Table obtained and from Fig. 1 Fig. -
Accepted fixation Article N. one or two plants two or one area (Fig. 1 (Fig. area ) O
t al et . Whirl
a effect Nothofagus In Laurer ex Funck ex Laurer n a second visit in 2015, we performed we 2015, in visit second a n ntarctica ; and area 2: area and ; tree growing tree growing thenear basecamp.
analysis (plants were processed differently, see description below). Contr below). description see differently, processed were (plants analysis both areas, six sampling pl sampling six areas, both Räsänen . Complutense , akt University Waikato
- G. magellanica G. Paks® s (2017)
of transplanting on plant photosynthetic plant on transplanting of plants (including roots), were collected and transported to our base camp in in camp base our to transported and collected were roots), (including plants moraine oiae b cytgmc pce (mainly species cryptogamic by dominated a , ). One sample was used for photosynthetic measurements and the other for other the and measurements photosynthetic for used was sample One ).
-
if
and mosses various fixation fixation . dominant
a smls ee lcd in placed were samples eaf o frhr description). further for surface age 40 age surface
present, They were then then were They
ee lo sampled: also were of the species the of area, used also for also used area, , . G. magellanica magellanica G.
Madrid Lichen thalli were collected with a similar spatial replication as as replication spatial similar a with collected were thalli Lichen analysis
and transported to base camp. The tree The camp. base to transported and forest forest ni a oa of total a until
(
(Spain) aitn Nw Zealand New Hamilton,
(hereafter forest area) forest (hereafter yr. with measurements made on exposed leaves of a well a of leaves exposed on made measurements with ots (0.5 x 0.5 m) were randomly selected with at least at with selected randomly were m) 0.5 x (0.5 ots G. magellanica, Gaultheria magellanica, G. )
(34 but with initial , (n = 5) = (n rzn meitl ad transported and immediately frozen age
for subsequent laboratory analysis.
N lcpi perrugosa Placopsis yr. G ) were collected were ) - . fixation fixation
in 2009), in magellanica ol ape (pe 1 cm 10 (upper samples Soil 6 in
naturally growing in growing naturally samples situ ae bags paper
measurements), and the the and measurements), measurements of the C fluxes and N and fluxes C the of measurements G. magellanica activity
c. G. magellanica G. , with , )
f ah plant each of 200 m distant from glacier front, glacier from distant m 200
o eeet determination element for plants from two moraine areas moraine two from plants
using sterile trowels, sterile using imdaey dried immediately ,
N were included and consisted and included were G. magellanica G.
Placopsis -
and
iig ihn species lichen fixing mucronata, N. betuloides N. mucronata, x
10
the the P species
colonization x eltigera
10 cm) containing cm) 10 forest forest spreads species
spp., , 5 samples at at samples 5 ,
N. antarctica N. Stereocaulon Stereocaulon
close to the to close dominating patagonica
frozen
(hereafter by stolon stolon by a been had Peltigera placed in placed n then and
(c. 4 yr. (c. 4yr. ols for for ols
( that
see to - -
This article isThis article by protected copyright. All rightsreserved. by retention N with coupled tissue plant in mycorrhi When Mycorrhi (Arróniz nitrification (NH Ammonium K auto water and soil mass/volume 1:2.5 a as homogenized out carried were methods. analyses accredited internationally their using Zealand) New Hamilton, University, and (see Zealand New Hamilton, University, Waikato at Leaf Leaf were the because had lichens been hydrated byrain. measurements days, two remaining the On glacier. inactive manner measured were species) each for 5 = (n lichens of fluxes C day. each through as time same the at measured the of Leaves fluxes. C influence all can these as recorded were (rh) humidity relative and Tcuv) (ºC; cuvette measuring the inside temperature PAR), season. representative probably are which conditions and over made were Measurements conditions (CO fluxes Carbon Carbon fluxesmeasurements +
AcceptedPO , Article - over three full days full three over 15 nutrient analyz P N contents were measured by the the by measured were contents N
4
analysis was performed by ICP/MS (inductively coupled plasma mass spectrometry) mass plasma coupled (inductively ICP/MS by performed was analysis , During C flux measurement, incident photosynthetic active radiation (µmol radiation active photosynthetic incident measurement, flux C During 3 over over
- - so they so zas Crespo , SO , er system LECO CNS 2000I CNS LECO system er sn a otbe pn lw RA ytm GS 00 Wl, Germany). Walz, 3000, (GFS system IRGA flow open portable a using was determined was
, soil , soil and
he complete three 4 prior to prior δ 2 - zas 15 , and Cl and , were artificially wetted in the evening by spraying with water taken from the fromthe taken water with spraying by evening the in wettedartificially were et al.et 4 15 N can N + and )
N discrimination 2 are involved in transferring soil N to their host plants then large changes large then plants host their to N soil transferring in involved are
- was exchange , 2014; Green analysis. analysis. 15 - N discrimination analysisN discrimination result for lichens. The measuring period measuring The lichens. for
determined were
using the shaken soil shaken the using as h is a wsa r a, mea day, dry a was day first The days. . The transfer of transfer The . the the G. magellanica G.
analyz Soil pH was measured for all soil samples soil all for measured was pH Soil - four
htsnhss n rsiain wr measured were respiration) and photosynthesis fungi follows et al. et
- full colorimetrically suspension.
ed by ionic chromatography Metrohm chromatography ionic by ed theory ,
. leads to leads , 2017) days for for days . Soil nitrate (NO nitrate Soil
S akt Sal Iooe nt WI, Waikato (WSIU, Unit Isotope Stable Waikato
amples
(n = 5). All samples were measured at intervals intervals at measured were samples All 5). = (n
for 15
N depleted depleted N for further description.for further
15 Total s Total
the study area during the the during area study the G. magellanica G. slurry N -
Green (Arróniz depleted plant depleted ee air were
oil N oil
method 3 s - ),
et al et covered a wide range of climatic of range wide a covered compounds
made N. antarctica N. nitrite
- and C were C and Crespo - re, ivd 2 mm) (2 sieved dried,
. , (Belser & (Belser
and (
2017
ne ntrl conditions natural under s (NO
and ig ht ihn were lichens that ning N. antarctica antarctica N. et al. et
) from fungi to plants to fungi from 2
- for details). Leaf N Leaf details). for ) with a pH a with 15
,
measured with an with measured tree
Mays, 1980) Mays,
, 2014) , N summer Ca 761 compact IC. compact 761 - enriched fungi fungi enriched 2+
(n = (n
, Mg , in a similar a in ne field under . - P
samples,
growing meter in in meter 5) m 2+ otential otential , –
. 2 were Na
Soil See See and s – + 1 , , ,
This article isThis article by protected copyright. All rightsreserved. in area studied each for and species, ( photosynthesis outside and inside active ensure to light enough with but exposure, i attached removing 125 either alpinum field under magellanica ( measurements, assay reduction fluxes acetylene C the using to by parallel conditions, in estimated was activity Nitrogenase N two the to attached firmly is and 1.50i. version software ImageJ using patagonica cyanobacterium symbiotic apices rhizome of number as G estimates Biomass andapexdensity reportedand is tobe and fungus, With δ following equation Tr) ratio; transfer the (termed plants host to on passed then is that fungi mycorrhizal by up taken N of proportion the system, open an In 0.2‰). ± 5.0 ( mycorrhizal δ plants by formed association mycorrhizal of type the hos and ncubation 15 15
unnera fixation analysisfixation
Accepted ArticleN non order the in decreasing N t plants t plants
the S. alpinum S. h plant m
. the Tr between 0 and 1, f is the proportion of the N in the plant that comes from the the from comes that plant the in N the of proportion the is f 1, and 0 between Tr the in l
se
ih PTFE with =
one l one and stones stones and
magellanica magellanica 15 , the , δ , (Hobbie, 2005) 15 N patterns can provide insight into N partitioning between mycorrhizal fungi and and fungi mycorrhizal between partitioning N into insight provide can patterns N
P Δ samples (n = 5 for each sampled area) area) sampled each for 5 = (n samples N -
lacopsis f is the discrimination against discrimination the is f glass incubation bottles fitted with a rubber septum rubber a with fitted bottlesincubation glass 1.1 ± 0.1‰) > ectomycorrhizal ( ectomycorrhizal > 0.1‰) ± 1.1
available nitrogen nitrogen available bottles were placed under placed were bottles samples
the (Hobbie - with ae slcn spu. ro t incubation, to Prior septum. silicone faced ol n debris and soil 8
–
bottles plants spread by rhizomes so plant plant so rhizomes by spread plants perrugosa 10‰ by drying in an oven at 60ºC for 72 h., and for and h., 72 for 60ºC at oven an in drying by
rock) P ) . The extent of these changes in plant in ofthesechanges . Theextent
lacopsis - in each 10 each in et al.et
Δ (Hobbie &Hobbie, 2008) ,
was continuously monitored with iButton® (Fig. iButton® with monitored continuously was ( f x(1 , the apex the
by change in weight after burning the samples at 850ºC for 850ºC at samples the burning after weight in change by , 2000) and
- perrugosa – yoria (en S, . ± .‰ > 0.2‰) ± 0.9 SE, ± (mean mycorrhizal
T S. alpinum alpinum S. and
DW x
r the the : )
of the rhizome includes the apical bud apical the includes rhizome the of
10 cm sample. The projected area of the lichens the of area projected The sample. cm 10 x f Nothofagus
afterwards was obtained for obtained was ae of case
15 N during the creation of transfer compounds transfer of creation the during N thalli - 2.3 ± 0.2‰) > ericoid mycorrhizal plants ( plants mycorrhizal ericoid > 0.2‰) ± 2.3 samples was determined from photographs photographs from determined was samples ; n = 5 for each species each for 5 = n ; . magellanica G.
(Hobbie & Högberg, 2012) Högberg, & (Hobbie canopy to avoid warming by direct sun direct by warming avoid to canopy n l and . ARA,
et yrtd y spraying. by hydrated kept See
density (plants m (plants density ce smls ( samples ichen rationale in G. magellanica, P. patagonica P. magellanica, G. i Hardy s
14 determined according to the to according determined N: or ape wr peae by prepared were samples 15 one , wide t al et Fig. N ratio is influencedby is N ratio Methods Methods P. perrugosa P. -
mouth glass jars of jars glass mouth . S2 - , extra 2 . aaoia S. patagonica, P.
) 1968)
) were enclosed were ) . Temperature ). was determined determined was
S
and also the the also and S 2 ape was sample , with foliar with ,
). For each For ). 1 . arbuscular arbuscular .
Gunnera
During (lichen P. - ,
This article isThis article by protected copyright. All rightsreserved. photosynthetic on treatment photosynthetic more the a between followed of differences We respiration the factor. test species to the approach in complicated levels three with and habitat considering P Differences factors. random as treated habitat) within nested levels, (five replicate and levels) (seven time w matrix similarity a conducted the of differences sampling repeated by other each of independent analyses statistical For analysisStatistical continuous activity contribution area activity were concentration in volume incubation HP Agilent J&W a with equipped chromatograph gas 3300 Varian GC: by determination concentration 24 complete a Wani possible vials. and syringe gastight a using extracted acetylene with incubated were in stored produced production. ethylene basal detect to control a as acetylene without incubated
Acceptedlacopsis Article Method
then expressed as nmols C nmols as expressed then data et al. et After each sampling the i the sampling each After
rates per area unit area per rates long
1l n situ in s , 1983) , perrugosa o ec seis ( species each for
- between Tedlar® Gas Sampling Bags Sampling Gas Tedlar® PL by the the by S - s term effects on nitrogenase activity nitrogenase on effects term two
2 . magellanica G. assuming the the assuming T clm ad fae oiain detector. ionization flame a and column Q OT . -
h cycle. cycle. h y dig ae t clim carbide calcium to water adding by The . This . -
way PERMANOVA analysis analysis PERMANOVA way N and ethylene concentration ethylene and for all species; for allspecies; t hbtt to ees mrie n frs) rae a fxd atr and factor, fixed as treated forest) and moraine levels: (two habitat ith
-
species the fixation fixation of and we performed a repeated a performed we irgns activity nitrogenase p N the same individuals at specific intervals. To assess the significant the assess To intervals. specific at individuals same the rocess was repeated, for the same samples, at samples, same the for repeated, was rocess as - ( . alpinum S. Exetainer® Exetainer® fixation nmol C nmol
activity measurements of both of measurements ecosystem the to commonly ae of rates
see ncubation 2 at lns and plants H
k 4
0 vv and, v/v 10%
g N 2 g ecito in description rates of the three lichen species studied ( studied species lichen three the of rates
H - of 1 4
. magellanica G. ) were tested by a similar approach, but without without but approach, similar a by tested were ) DW
stored in 5.7 m 5.7 in stored ha cm
. magellanica G. v acc bottles ials were transported to Madrid for ethylene ethylene for Madrid to transported were ials - until until 1 -
2 h yr . antarctica N.
rates were then calculated from the ethylene ethylene the from calculated then were rates e - h 1 td C pted -
- 1 for each sample was determined as described as determined was sample each for 1 and µg N µg and - ) needed (i.e. needed ) was measure approach measure .
were aerated were were calculated using plant density/thallus plant using calculated were a
(Dart & Day, 1971; David & Fay, 1977; 1977; Fay, & David 1971; Day, & (Dart fter Adro, 2001) (Anderson, Method
N 2 estimated H -
fixation l 4 one plants between different habitats habitats different between plants
nie mdfe crie lamp carbide modified a inside :N ,
Exetainer® evacuated gas sampling gas evacuated Exetainer®
g as well as differences between between differences as well as - 2
1 re W asse te fet of effect the assessed We tree.
s
h incubation, a gas sample was was sample gas a incubation, h DW ovrin atr f 3:1. of factor conversion injected into each jar each into injected
S by opening the the opening by
and C fluxes were performed were fluxes C and 2 (
suig 0% oe and cover 100% assuming and ) d - because 1 After . In addition, In , based on Euclidean Euclidean on based ,
three potential each each samples were not were samples
h intervals h P. Acetylene was was Acetylene jars activ ARA, exact exact ARA, patagonica
nitrogenase
) to prevent to nul N annual .
Samples ity , Rates
over and and and we we G. G. ,
This article isThis article by protected copyright. All rightsreserved. on an species lichen All 0.05). than lower significantly was lichen The 2). DW species lichen 2) Table 2, values mean highest the had forest ( sunrise before (12 midday around values highest the with species, studied activity Nitrogenase N Results waslocalities investigated using in PERMANOVA tests hoc post pairwise using by tested were assessments) respiration and photosynthesis (in betwe Differences UK). (PRIMER package statistical v6 PRIMER for PERMANOVA+ the with data) raw of (permutation permutations 9999 using developed factors replicatelevels, andtime (five factor, and nested species) levels) treatedas (11 within random w species low the of because measurements fluxes measurement. res conditions measuring the in differences photosynthetic the test to approach similar for a followed then We samples. between account to photosynthesis of covariates as (five replicate and levels) wit (12 nested levels, time and factors, fixed as species) within nested moraine, transplanted and forest transplanted control, levels: (three treatment and levels) (two species magellanica
fixation rates fixation
Accepted Article( lichens two the of piration
basis ( basis
area basis( area
on morphology of influence the Finally,
and ue a two a used e P but
A, cv n r icue a cvrae. EMNV aaye were analyses PERMANOVA covariates. as included rh and Tcuv PAR, = 0.561; Table S1), Table 0.561; = and P. patagonica P. troaln alpinum Stereocaulon S. alpinum S.
the sites the 0 P 4 hin treatment) treated as random factors. PAR, Tcuv and rh were included were rh and Tcuv PAR, factors. random as treated treatment) hin . antarctica N. .00
< 0.05; S1), Table with ,
- ae on based 0
- 5 en habitats (in case of case (in habitats en differed significantly differed way PERMANOVA analysis, with species (two levels) as a fixed fixed a as levels) (two species with analysis, PERMANOVA way .00 differed
had the lowest nitrogenase activity, on a on activity, nitrogenase lowest the had
that of that h and Fg 2). Fig. ; P. patagonica P. ,
one ARA with rates with y odcig four a conducting by P from for lacopsis P. patagonica P. - way ANOVA.
, nitrogenase activity nitrogenase a initially was
one another one showed similar, and marked, diel variation for all all for variation diel marked, and similar, showed unr magellanica Gunnera
P. patagonica
-
close to those obtained for obtained those to close rates measured for this species. species. this for measured rates Ld Pyot Mrn Lbrtr, Ivybridge, Laboratory, Marine Plymouth Ltd, E perrugosa
and only N - N fixation -
P
and fixation rates of rates fixation on a on
lacopsis when nitrogenase activity was expressed was activity nitrogenase when included
P had similar nitrogenase activities on a on activities nitrogenase similar had DW - lacopsis ), and between treatment and species and treatment between and ), a PRAOA nlss with analysis, PERMANOVA way
having highest the rate (Table 2). on
perrugosa basis ( basis .00
both u fnly icre fo C from discarded finally but
plants from the moraine and and moraine the from plants -
perrugosa 15 P a G. magellanica G. 0 h .00
DW DW = 0.041; Table S1). The S1). Table 0.041; = ) used during C fluxes fluxes C during used ) G. magellanica G.
ad oet values lowest and )
and area basis (Fig. basis area and and area basis, and basis, area and
(Table 2, S1, 2, (Table o te l the For activity
fro m both both m (Table ichen ichen
P and
<
This article isThis article by protected copyright. All rightsreserved. thenlowest, in difference specific for (except sites all leaf for similar 2.2 around contents shrub seral betuloides N. species shrub the than N more times a,b). 4 Fig. 3; (Table species plant analyzed magellanica G. Leaf NandPcontents were less clear. for patterns the to close very peak the with whereas However, of response N. antarctica P and species that between nor forest significant no were 3) Fig. 0.005; herb the for higher significantly for higher photosynthetic on effect significant magellanica statistically no had Transplanting Comparison carbonfluxes of between locations andspecies 100% they as caution with treated be to need and for Table 0.996; forest and moraine between difference
Acceptedlacopsis Article P. patagonica P. . alpinum S. cover Maximal
perrugosa G. magellanica G.
. mucronata G. ( N.
plants (Table S2). Net photosynthe Net S2). (Table plants 2
NP Methods
but a similar similar but a and 30% higher than the the than higher 30% and but ,
betuloides S P
4.1 n 2.4 g ha N kg 27.84 and (48.41 1 leaves
estimated
o eprtr (Fig temperature to content with P contents contents P with content (151.8 NP for NP ). For the lichen species, estimated N contribution was significantly higher significantly was contribution N estimated species, lichen the For ).
G. magellanica G. differences in respiration respiration in differences N. betuloides N. -
.% and 3.0% had much lower net photosynthetic rates than both than rates photosynthetic net lower much had
P S
2
consistently otn wt te ae ak re a fr N for as order rank same the with content
kg N ha N kg ) , both species both .
NP in the forest ( forest the in N. antarctica
a te oet cnet, c. contents, N lowest the had annual annual
response to response . betuloides N. -
1 at early stage early at . magellanica G.
yr had a had cnrbto of contribution N N. antarctica N. - 1 G a hge N n P otn cmae t the to compared content P and N higher had . ; was
aultheria P are
deciduous def wt otmm temperature optimum with d,e,f) 3 sites n P and
< 0.005) than the observed for observed the than 0.005) <
incident optimum around 15ºC, around optimum remaining almost constant constant almost remaining = 0.005; Table S2). Net photosynthetic rates were rates photosynthetic Net S2). Table 0.005; = saturated at saturated based on daily estimates, daily on based - 1 G
N. antarctica N.
rates
26 n 37 g ha N kg 327 and (276 yr unnera a much lower lower much a , 7 , G -
1 tic rates tic unnera mucronata
,
yr lichens The S2). (Table
between between light (Fig. 3 c). All species showed (Fig.light similar Allspecies 3c). tree tree oprd o the to compared respectively). . ; Fig. 4b). However, there were species were there However, 4b). Fig. ;
magellanica . magellanica G. similar light similar N. antarctica N.
magellanica ( , NP,
G. magellanica G. the 1%, whilst whilst 1%, , twice that of the the of that twice , c. area basis) w basis) area optima for the for optima .% Te eut ae very are results The 1.5%. The following
highest).
levels
tree - se 1 continuous (Table 3 (Table otn ( content for leaves
yr
hwd o statistical no showed . antarctica N. nul contributions annual P
G. magellanica G. - each species across species each . antarctica N. 1
lacopsis
P (Fig from
respectively a Gaussian curve Gaussian a .
ere
s otie three contained patagonica activity
, Fig. 4a). The 4a). Fig. , evergreen . . mucronata G. lichen species species lichen around 15ºC. 15ºC. around
3 a 3
significantly moraine and moraine activity and activity
perrugosa , b). There There b).
a N had of ; other (
P P tree and and and
G. G.
= = - ilgcl fxto, e on ltl eiec o ehne pooytei rts in isThis article by protected copyright. All rightsreserved. rates photosynthetic enhanced of evidence little found we mycorrhi fixation, via N biological vegetation tree and shrub by acquired surfa with sites high intrinsic its of because herb forest rapid an with and inputs N N coupled efficient fixed biologically N for role of important an lack indicates strongly early establishment The succession. vegetation underpinning a it make that research Our Discussion slow decline. Cl and 10 around forest S3 chronosequence the along undetectable soils the of feature impressive An analysesSoil species (Tr between0.6 values rather had contents betuloides to decline similar very and steady mucronata G. 10 at negative least be chronosequence the along betuloides substrate the of age increasing with change little and zero to chronosequence the along plants Foliar isotopevaluesLeaf stable
Accepted mature a when site oldest the at reached only are levels high Relatively ). Article
a more negative more a G δ - osset aus o al tde species studied all for values consistent . )
15
magellanica remain almost constant or show a slow rise over the first 19 first the over rise slow a show or constant almost remain and N results indicated that indicated results N
-
and and transfer system. Answering our in our Answering system. transfer
, levels of key nutrients such as such nutrients key of levels ,
mycorrhizal types (Table 1). All species present on surfaces younger than 10 than younger surfaces on present species All 1). (Table types mycorrhizal Potential demonstrates respectively). , unique G . mucronata G. e gs f 7 of ages ce
m in height has established. Other elements Other established. has height in m aultheria
δ appears to be the most important N important most the be to appears
15
location for location yr n N including N itrification .
. (
For the For - mucronata that the the that 2.06‰, nitrogenase activity nitrogenase
δ yr - ha 0.8) insoilsyounger 19 than 15
G. magellanica G. te bcm icesnl ngtv a odr ie wt a with sites older at negative increasingly became then N d n older and (Fig. 4c) (Fig.
latter investigating and investigating rates ey similar very G. magellanica G. Pia Glacier Pia -
2.51‰, and 2.51‰, around around
always had negative negative had always
three w . ere (2) . While itial hypothesis, we found that: (1) the perennial the (1) that: found we hypothesis, itial NH
below species, - ‰ fe 34 after 6‰
foreland r consistently h δ The δ 4 ate (Fig. 4d), with higher differences between between differences higher with 4d), (Fig. - + 15 3.38‰ G. magellanica G. ,
N at the older sites, despite despite sites, older the at N s but also because of its high its of because also but s (Fig. 4c). (Fig. PO detection limit understanding the role of symbioses in in symbioses of role the understanding δ 15 4 15 3
zas N values values N
- ( N was initially low and then rose to rose then and low initially was N
- for Southern Chile Southern and fixing species in the area not area the in species fixing . (3) (3) . yr
δ N. antarctica, N. differed from the rest of studied of rest the from differed Finally, Tr calculations showed showed calculations Tr Finally, yr . , 15 ( Mg soil total soil
the species the . N
Nothofagus Despite N acquisition acquisition N Despite 2+
values wa showed suggest
at all at sites.
in the first 10 first the in s yr
h vr lw often low, very the C, Ca C, . )
n these and whilst pH shows a a shows pH whilst
has characteristics has
δ that N is rapidly rapidly is N that N. betuloides N. N. antarctica, N. 15
N 2+ antarctica,
, Na ,
values presence on presence Nothofagus different yr
+ changed changed . , SO ,
(Table close only
and
4
yr by G. N. N. N. 2 N - , .
This article isThis article by protected copyright. All rightsreserved. chronosequence the in Raggio rates fixation N attain mossthe (i.e. mosses on epiphytic cyanobacteria fixing 10 around at maximum as al. et soils exposed recently at communities bacterial by nitrification low forests surrounding water at negative very also is contents P and N highest their have Glacier. Pía at species all in content P higher a also and forest, to longer times (Pérez 2004) trees for expected range evergreen; or deciduous, herbaceous, (e.g. biotypes plant different the for expected are that levels relative at and 4ab) (Fig. chronosequence the However tissues plant in levels P 10 by soil the around S3; (Table nutrients essential of inputs nutrient The species potentially combining by foreland Glacier explain helps that framework a provide and Fuego del Tierra in magellanica -
. fixing lichens (i.e. (i.e. lichens fixing
Acceptedthe by indicated Article 11 their high their
δ , 2016) ,
. 15 to 12. to from instantaneous rates of 283.4 nmol C nmol 283.4 of rates instantaneous
et al. et . h NP ais r lwr hn hs rpre fo aohr lce frln nearby foreland glacier another from reported those than lower are ratios N:P The
N 7 to 10 to 7 et al et (Table S3) (Table
, , for each individual species, individual each for Fig. allochthonous 9 fiin ptwy fr uret acquisition nutrient for pathways efficient . . , 2014) , ., 2012) .,
0 There There
Our results Our growth rates growth n an on
for all species all for yr S3 .
) . However, the plants show plants the However, . until
:
. then then above the glacier front, glacier the above 15 . but this may be a result of the the of result a be may this but recently exposed substrates at Pia Glacier foreland Glacier Pia at substrates exposed recently
hs s upre by supported is This ra ai (al 2) (Table basis area Following its early appearance after 4 after appearance early its Following N discrimination values values discrimination N P
s h hge plant higher the is . nutrient stocks nutrient (Flückiger & Braun, 2003) Braun, & (Flückiger these appears to be to appears
yr highlight
patagonica detrit and markedly .
Fg 4) Ti sit s ams crany iiily rvn y N by driven initially certainly, almost is, shift This 4c). (Fig. . This is impressive when one considers that the absolute N and N absolute the that considers one when impressive is This . , initial stages. This suggests that N is initially sourced initially is N that suggests This stages. initial
also by foliar N:P ratio that ratio N:P foliar by also us h etariaiy ih N high extraordinarily the
Arróniz the deposited on ifrd betwee differed levels of both N and P remained almost constant along constant almost remained P and N both of levels
relevance and a the young the
(i.e. soil total C, total soil (i.e. shift from detrital N supply to products of N of products to supply N detrital from shift
-
Crespo 2 or P which would be expected to have high leaf N and and N leaf high have to expected be would which ih potential high H . magellanica G. lacopsis on the glacier the on 4 lcpi contortuplicata Placopsis which
g few
of - er 1
DW
t al et
G. magellanica G.
surfaces, up to 7 to up surfaces, but lower than those for herbs herbs for those than lower but much slower succession at the latter the at succession slower much sign Larcher, 1995) Larcher,
become less negative less become seis y fco o u t three to up of factor a by species n perrugosa
Ditrichum cylindricarpum Ditrichum h , 2014) ., s
- PO
1
of nutrient nutrient of ; Arróniz ; i mycorrhi via rai plmr degradation polymer organic
- wt is nsa cyanobacterial unusual its with , surface remains almost constant between between constant almost remains 4 fixation yr 3 -
. and , t , ( This . 1
ih iia hg diy N daily high similar with he main provider of N of provider main he th -
7 .
for ecosystem functioning ecosystem for
NH - e ( The N:P The Crespo yr e.g. debris coming from from coming debris e.g. yr
of deficiency rapid . .
4 condition ; (Fig. 4) (Fig. + hs species this zas
have
) Fernández and start to start
and succession et al et n non in ratios are in the in are ratios very low levels low very P
. , as indicated as , and
reac
., 2014) ., stenophylla Plant persists for for persists , which can which , increase (Güsewell, (Güsewell, -
- hed Martínez leaf - N with fixation in melt in
- leaves leaves in Pia in fixing
δ their their , later later
and and 15 ten the
in N - - ; .
This article isThis article by protected copyright. All rightsreserved. mucronata involved be to reported leaf appears to process high have all latter the as the plants to fixing N fixed the moves that mechanism transfer efficient highly a be must there Mycorrhi 2001; Persson&Näsholm, 2001) plants 4 about older on especially mosses of and coverage contrast, lichens in whilst, of surfaces coverage reduced in result exposure rock of (Fig. N individual on dependent < lichens < mosses on epiphytic cyanobacteria been has (Osborne as requirements, N its for symbiosis the magellanica & periods incubation long (e.g. approaches methodological different possibly magellanica 2017) in inhibition strong Rennie 1988; Casuarina ( species phanerogamic nodulated from reported highest the among is Glacier Pia at 8 at arenaria Methods ha kg 300 cm around nmol 74 are rates reduction acetylene mean overall Instantaneous symbiosis.
Accepted ArticleWani 1977; Fay -
tissues 10ºC, daylight hours daylight 10ºC, S . both depend on both depend 1 Our results contrast with previous attempts to provide tentative N tentative provide to attempts previous with contrast results Our W )
yr
. The loss of open soil surfaces as the herbaceous the as surfaces soil open of loss The . xlie b a by explained (72 kg N ha N kg (72 zas S e can rate the rate can e n mycorrhi in et et al. , . However, the fate of fixed N a N fixed of fate the However, .
2 , establish
), o ), Acacia
as found here found as as in Tierra del Fuego del Tierra in n ter rnfr role transfer their and et al. et , 1992) mycorrhizal ur results ur being -
1 be viamycorrhibe
et al et
, 1988; Binkley 1988; , N and
yr in the succession the in
- - 1 largely reliant on fixed N, suggesting an almost obligate dependency on dependency obligate almostan suggesting N, fixed on reliant largely .
zas -
differentpathways fixation is expected during expected is fixation
1 yr
. , Table 2 Table , relevance as N as relevance , Glycine
- 1983) would eaie fet of effect negative only 1 omto bcm more become formation , - ; , fixation rates but on the extent of the organisms in the community the in organisms the of extent the on but rates fixation but
Silvester including ; , . Becking
; also exceed those reported for other for reported those exceed Finally, ARA Finally, ).
. (
Troncoso elr Glmn 17; ivse, 93 George 1983; Silvester, 1979; Goldman, & Kellar zas Although these Although , et al. et T ahee h rpd oet ucsin n i Glacier Pia in succession forest rapid the achieve To :
&
a because not only do they only notbecause (Fernández ll the dominant plants on the Pia Glacier foreland are are foreland Glacier Pia the on plants dominant the ll
G. magellanica G.
, contributors
Smith 1969) Smith
N
1976) that remainthat . magellanica G. , 1994; Vaishampayan 1994; , - c
nd its transfer from N from transfer its nd et al. et ontents ln manipulation plant rates rates . The N The . . magellanica G. , 2013; Pérez 2013; , - less favorable, colder favorable, less
Martínez values should be taken with caution ( caution with taken be should values bnat when abundant and , or , and growth rates rates growth and foreland Glacier Pia the in
largely unexplored largely
fixation rate fixation rpsd for proposed (Table 1). (Table leaf leaf G. macrophylla G.
is extensive at all sites older than than older sites all at extensive is layer develops and the low amount low the and develops layer et al. et δ 15 et al. et N produce Gunnera Ti odr s o s much so not is order This . (Söderbäck
et al. et , 2017) , values near values ; - In addition, In
fixing organisms to other other to organisms fixing found for found Dart , 2014, 2017) 2014, ,
Nothofagus other (Fig. 4a). (Fig. , 2001) ,
seasons seasons negative δ negative (12 (Lipson & Näsholm, & (Lipson . & -
fixation rates of rates fixation species, such as such species, Many studies have studies Many
Day 1971; David 1971; Day - Gunnera 21 kg N ha N kg 21 t al. et zero G. magellanica G. . fung Nevertheless,
in this order: this in (Pérez The transfer The p. and spp. , a ,
15 1990) , support al groups groups al nd this is this nd N in N - 2
species species non h Alnus t al. et et al. et - - 1 1 host host
yr - see
(or (or N G. G. G. G. G. G. G. or - - 1 , , ,
This article isThis article by protected copyright. All rightsreserved. bacteria soil by released compoundsN utilize fungi the that assumed been basis interesting an provide would topics and reasonable fungus the by supplied N plant of proportion include might it the and Pia at process dominant be might transfer mycorrhizal that suggests equation theoretical the with fit of level The plants the all for identical & Hobbie 2008; Hobbie, it probably highproportion is a about that produce magellanica G. δ N systems transformations root plant by acquisition N direct during fractionation significant limit to known is availability N soil low addition, In atlow be to is expected succession glacier, the foreland Glacier Pia however, to hindrance N isotopic atmospheric N on exclusively plants by formed association 2012) Högberg, in host enriched its to fungus fungus the from compounds N of process transfer by driven plants boreal or alpine Arctic, in regions plants mycorrhizal ericoid and ectomycorrhizal that reported 15 - is also highly energetically efficient in terms of carbon supplied by the host host the by supplied carbon of terms in efficient energetically highly also is iain n N and fixation
Acceptedδ plant and N Article (Schulze
s even hne i te rprin f eyld n nwy fixed newly and recycled of proportion the in changes are
a 75
relatively
spl is supply N
infcnl dpee in depleted significantly interpreting foliar δ foliar interpreting % of N taken up by the by up taken N of % be the only(Table process the be ,
. The . declines as recycling increases recycling as declines considering 15 (e.g. nitrification) nitrification) (e.g. et al. et - N to the chronosequence chronosequence the to N - rnfr i mycorrhi via transfer iain r uuly 0 (s cus for occurs (as ~0‰ usually are fixation 15 constant transfer constant , 1994; Michelsen 1994; , N and the supplied plant, depleted depleted plant, supplied the and N magnitude
values values
potentially Högberg, 2012) Högberg, although
the the reflect (Hobbie & Högberg, 2012) Högberg, & (Hobbie (Handley & Scrimgeour, 1997; Hobbie 1997; Scrimgeour, & (Handley is unusual in unusual is end 15
undetect of these changes is influenced by the type of mycorrhizal of type the by influenced is changes these of N is that multiple N sources can distort isotopic signatures; signatures; isotopic distort can sources N multiple that is N on young
ing
result (i.e. a constant transferratio) a result (i.e. the quantities moved to moved quantities the niey rm N from entirely
mycorrhi soil soil ratio (Craine (Craine
15 the large N of large quantities the zas S rltv t co to relative N et al. et
. It is also interesting that the transfer ratio is almost almost is ratio transfer the that interesting also is It . able
for 3 successional stages (i.e. c. stages(i.e. successional δ
). assume . (Tr) at around 0. around at (Tr) 15
that The h apiain f h frua ikn source linking formula the of application The future research future
N nitrification potential of the soils the of potential nitrification , 1996; Hobbi 1996; , zas
later in the chronosequence the in later t al. et is presumably low compared to the effect of of effect the to compared low presumably is ( , following the removal of any supply from supply any of removal the following , Methods Methods
assumptions madeassumptions is s that s
transferred to the mycorrhizal host. This host. mycorrhizal the to transferred - fixation. 2015) ,
the proportion of the N coming from from coming N the of proportion the
. The δ The . - S curn absua mycorrhizal arbuscular occurring (Hobbie 1 75 . e
) Although, t Although, G. magellanica G.
. W . et al. et
Furthermore, (Fig. 4d). This 4d). (Fig. 15 stored Thus, . magellanica G. N values of plants that rely that plants of values N e feel the values used are are used values the feel e , 2005) , N - in the above calculations above the in t al. et 1
‰ in leaf litter, and the the and litter, leaf in , we suggest that these these we that suggest , in et al. et the the
o date it has usually has it date o ; N (Wu, 2011) (Wu, , 2005; Hobbie & & Hobbie 2005; , Pérez . The depletion is depletion The .
( fixers fixers which Methods Methods , 2005) , influence soil
must be small. be must would indicate would
also et al. , reflecting ), δ detritus detritus Hbi & (Hobbie 15 leav . A major A .
N suggests suggests S , 2014) ,
but 1 e n the in f N of ) s
and and but the the the the .
This article isThis article by protected copyright. All rightsreserved. during content these initial Glacier Pia in colonization primary of stages th conditions optimum under cryptogams for 1995) reported commonly been has this as surprising not was species leaves all N different system, the N between al. et in species expected wa content N higher from derived advantage photosynthetic the Farquhar 1999; Niinemets, capacity photosynthetic higher species tree the for species photo Plant than mycorrhi for role greater much a of possibility the opens This shown). not (data plants the all in levels adequate at constant but soils original the in absent is which includes this and nutrients their all with supplied adequately are plants the that suggests vegetation the of successionrapid the conte P foliar normal have Glacier Pia at plants the all that therefore, surprise, function this for symbionts mycorrhizal many of understanding our previouslymight than thought be higher by contribution the that suggest here presented results
Acceptedeir Article
has , 2008; Albert Albert 2008; , low photosynthetic capacity photosynthetic low Peiu lbrtr analysis laboratory Previous . ) y . The lower photosynthetic lower The Involvement
ea G. magellanica G. , with rates with , so far r polar or temperate regions temperate or polar - s
fixers and non and fixers
which would minimize the physiological advantage of N of advantage physiological the minimize would which ytei status synthetic that they are also efficient P suppliers and that plants are dependent on their their on dependent are plants that and suppliers P efficient also are they that been cto srtge (e.g. strategies ocation N.
et al. et considered. of mycorrhi of similar to those previously reported from reported previously those to similar their a ntarctica. were similar in range in similar were , 2011) , -
N function successional (De los Ríos los (De Bt pooytei atvt ad eprto o te herbaceous the of respiration and activity photosynthetic Both : et al. et - fixers might be a consequence of the absence of N of absence the of consequence a be might fixers
, zas . , 2002; Wright 2002; , as suggested by suggested as
The , We in rates
cryptogams
(Näsholm in the N supply to plants is a more recent development in in development recent more a is plants to supply N the in
. magellanica G. indicate initially hypothesized initially (Larcher, 1995; Martínez Pastur Martínez 1995; (Larcher, lack of evident differences in photosynthetic activities photosynthetic in differences evident of lack
of the studied lichens studied the of . stages es allocated less
et al. et (Jansa
, 2011; Raggio 2011; , et al. et to ht u fed esrmns ee performed were measurements field our that (Arróniz , ,
, but significantly higher significantly but , which are the dominant organisms at initial at organisms dominant the are which al. et a epan h sih iceet n ol C soil in increment slight the explain may t al. et (Zhang , 2008, 2013) 2008, , , 2004; Shipley Shipley 2004; ,
21; Johnson 2011; , - Eas 18; Reich 1989; (Evans, N Crespo
et al. et iet novmn of involvement direct o UIC in RUBISCO to
that et al. et other other , 2015) , in comparison in et al. et s much weaker than initially than weaker much s higher N higher . It has been well known for known well been has It . , 2012) , Nothofagus , 2014) - fixers in this habitat this in fixers et al. et ,
supplying magnesium supplying et al. et t al. et zas
supply than .
, 2005) , in nutrient uptake nutrient in However, . Muraoka 2007; , 2016) ,
. magellanica G. to the vascular vascular the to , that observed that , nts. However, nts. t al. et -
deficiency deficiency spp. or spp.
mycorrhi would drive would .
However, . It is no no is It . (Larcher, (Larcher, 1997; , despite other other , or , zas in
This article isThis article by protected copyright. All rightsreserved. excludedphotobonts are Antarctica from continental Accepted2004) N for just not temperatures 1980) Harper, & Schweitzer 1980; Raguse, & shown). not data rates; ha example, for leaves, of (removal light in changes than rather sites other at and here found impacted year a months 5 for zero below minima mean and year each months 3 for zero below are temperatures monthly mean 1.3 is (lowest degrees masses. land extensive more the to hemispherethedue northern in severe aremore muchrespectively),winters thePia and latitudes similar at although particular, In sites. glacier hemisphere open layer herbaceous the in 1990) Dale, & succession the impact Article2003) Alnus sites hemisphere but hemisphere north the is difference obvious most The hemispheres. Hodkinson (Chapin other of hundreds northerninhemisphere sitescover takes succession treevegetation to general, from reported after situation the 34 in Glacier Pia with at strongly mature a contrasts Whilst hemisphere. northern the in chronosequences foreland Glacier Pia comparison hemisphere Northern/southern
hr i a ao cnrs i te ye n N and type the in contrast major a is there c and
Sm hraeu o daf shr dwarf or herbaceous Some . Lw eprtrs r sgetd o e h rao wy ihn wt cyanobacterial with lichens why reason the be to suggested are temperatures Low . . 80 . pce with species n diin tee s mre dfeec i ciae ewe suhr ad northern and southern between climate in difference marked a is there addition, In et al. et
forest environments.forest by low temperatures temperatures low by - 120 et al. et , 1994; Sigler & Zeyer, 2004; Jones & Del Moral, 2005; Schmidt 2005; Moral, Del & Jones 2004; Zeyer, & Sigler 1994; , .
yr G
, 2009) , . unnera (
(Crocker & Major, 1955; Chapin 1955; Major, & (Crocker i.e. yr Frankia . N .
. but th but o lce Bay Glacier , a Pet Wlim, nab catl tow coastal nearby a Williams, Puerto at C
This has also been also has This , in , thus it is interesting to consider what is different is what consider to interesting is it thus ,
- magellanica
fixing plants occur at both northern and southern hemisphere sites hemisphere southern and northern both at occur plants fixing exclu (https://wrcc.dri.edu/). Alaska eir
- show symbionts which occur later in the succession succession the in later occur which symbionts iain u as fr photosynthesis for also but fixation
ding (Cleveland M low be to seem rates fixation
onthly mean temperatures at Pia are always above zero zero above always are Pia at temperatures mean onthly in ed
r ednal Glacier, Mendenhall or most other species, and versatile so that it that so versatile and species, other most
site
a nighttime depression depression nighttime a not only establishes early in succession but is dominant is but succession in early establishes only not u s N b
that shown et al. et Te xrodnrl fs piay ucsin at succession primary fast extraordinarily The : - th . Cyanobacteria are poor performers at subzero subzero at performers poor are Cyanobacteria . ies sc as such fixers, are at t at , 1999; Reed 1999; ,
Biological N Biological
-
for other N other for also at sea level, a spruce forest establishes forest spruce a level, sea at also fixing ability of these plants. At northern northern At plants. these of ability fixing here is no equivalent no is here et al. et (Green (Green
, 1994; Alexander & Burt, 1996) Burt, & Alexander 1994; ,
et al. et Alaska) (Lawrence (Lawrence that - et al. et - fixing symbiotic plants symbiotic fixing ra drummondii Dryas fixation is strongly strongly is fixation Nothofagus d , 2011) wa
no effect on the the on effect no , 2011) ,
( ) hlt t lce Bay Glacier at whilst n) s due to low temperature low to due s te ao N major the , 59 (Lange, 1965; Antoine, Antoine, 1965; (Lange, °
et al. et . and 55 and to
. The daily pattern pattern daily The .
G. magellanica G. forest is achieved achieved is forest between , 1967; Blundon Blundon 1967; , ° (Kohls , Glacier Bay Glacier , is present in present is et al. et apa to appear , - N negatively ies are fixers -
fixation the two the (Eckart , 2008; , t al. et . In In . yr
in , , .
This article isThis article by protected copyright. All rightsreserved. T.G.A.G. contributedAll authors to drafts the and gave J.M.B J.R., by performed A.B. by performed were analysis fixation Nitrogen methodology. A.B. Authors’ contributions y Competitividad. (BES FPI by supported was ABG (CTM2015 Competitividad y Economía analysis. soil with help their for Madrid) de Complutense Universidad Farmacia, de (Facultad Edafología de board, on hospitality kind their for and channels southern demanding highly the of navigation the thank We Acknowledgements limit performance the of P magellanica rare often and herbs small mainly are of species 10 also are There mountains. forested through run Zeala New is which
Accepted Articlelimitation - G., as well as for their logistic support during field sampling. field during support logistic their for as well as location hemisphere southern equivalent an in situation the comparing worth is It J.R., J.R., Captain Ezio Firmani and Firmani Ezio Captain
characteristic of characteristic either in size or in ability to dominate the herbaceous the dominate to ability in or size in either Soil and plant material sampling were materialsampling plant and Soil .. R.R. A.P.,
hs eerh a spotd y rns rm h Saih Ministe Spanish the from grants by supported was research This nd.
Some g Some Gunnera
, .
New Zealand Zealand New T.G.A.G. n JV Te aucit a witn y A.B. by written was manuscript The J.V. and
laciers laciers
- spp 2013 the crew of the vessel “Oveja Negra” for their skillful in skillful their for Negra” “Oveja vessel the of crew the . i
(WCSP, 2018) (WCSP,
n the South Islands South the n although thisalthough speculative the is at moment. - and 062945) grant from Spanish Ministerio de Economía de Ministerio Spanish from grant 062945) soils -
64728 L.G.S.
(Richardson - C2
conducted by conducted . There seems to be no equivalent to equivalent no be to seems There . eind h suy n experimental and study the designed - - 1 G. final approval forfinal approval publication. - ad CTM2012 and R
also abn lx measurements flux Carbon Gunnera et al. et
terminate at low elevation andelevation low at terminate
We thank the Departamento the thank We , 2004) , L.G.S., A.P. and T.G.A.G. T.G.A.G. and A.P. L.G.S., layer
in New Zealand which which Zealand New in .
P is severe enough to enough severe is ossibl - 38222 - G. y
, the , J.R. , - CO2
strong rio de de rio
were - 01). 01). and and G.
Nothofagus betuloides Nothofagus antarctica Nothofagus mucronata Gaultheria magellanica Gunnera Species
This article isThis article by protected copyright. All rightsreserved. Accepted Article Ectomycorrhiza. Crespo in are provided site agedetermination of details and the chronosquence along distribution from were obtained types Mycorrhizal chronosequence. the presencein and mycorrhizal association, of type ( isotopic and element leaf for selected species Plant 1: Table Tables
et al
. ,
(2014)
. VAM,
Vesicular Tree (evergreen)Tree (deciduous)Tree Shrub Herb Form
–
Fontenla Fontenla Arbuscular Mycorrhiza; Eric., Ericoid mycorrhiza; Ecto., Ericoid Eric., Mycorrhiza; Arbuscular
et al. Ecto. Ecto. Eric. VAM type Mycorrhizal , (
2001
) ; &Zak, Becerra 15
N) content, indicating the life the indicating content, N)
+ 4
Presence (siteyears)Presence agein ( + + + 7 2011)
. + + + + 10 Species
Arróniz - form and and form + + + + 19
- + + + + 34
Estimated rates Estimated C nmol 1 nmols C r Measured kg Nha kg N m g µg Ng This article isThis article by protected copyright. All rightsreserved. ( nitrogenase activity continuous assuming speciesand selected of cover 100% calculated assuming For assay reduction acetylene Table Accepted Article Gunnera magellanica Gunnera - 2: 2 - 1
2
- yr H
2 1 DW Nitrogen fixation rates (average rates fixation Nitrogen H
yr 4 - 1
4 cm
ates - g 1
d
- 1 - -
2 1 DW
h - 1
h - . 373.32 373.32 , average estimates using all data from both sample sets are provided as sample areprovided sets from both alldata , averageusing estimates
41.86 41.86 275.58 275.58 27.56 (±3.8) 27.56 67.41 Moraine (±5.62) (±50.18)
(±9.3) (±38)
d
) Gunnera magellanica Gunnera for evaluated species from both sampling locations locations sampling both from species evaluated for 327.33 327.33 292.39 32.73 (±4.11) 32.73 32.75 (±10.05) 80.1 Forest (±41.08) (±4.44) (±39.68)
341.76 (±15.82) 341.76 303. 30.31 (±2.33) 30.31 (±1.77) 38.28 74. 15 (±5.7) 15 74. Overall 11 (±23.3) 11
Peltigera patagonica Peltigera 151.8 290.28 1 32.51 (±10.6) 37.13 5.18 5.18 Moraine
(±43.32) obtained from da from obtained (± (±9.25)
(±6.72) 4.33 overall poikilohydric poikilohydric
)
. Data are means ± SE (n = ± SE(n means are Data
Pacopsis perrugosa Pacopsis il 359.61 organisms y cycles of nitrogenase activity measured by measured activity nitrogenase of cycles y 40.28 4 4.84 (±2.4) 11.84 8.41 Moraine
(± (± (±34.06)
(±9.8) 0.97 8.17 will be inactive at dry periods atdry inactive will be
) )
5) . Stereocaulon alpinum Stereocaulon Estimated rates were were Estimated rates 27.84 22.74 2.78 2.78 2. (±1.65) 6.81 55 Forest
(± (± (±6.72) (±2.48)
0.67 0.63
) )
).
This article isThis article by protected copyright. All rightsreserved. c) (ppm); content P Leaf b) DW); chronosequencethe infront ofthe 4. Figure temperature. where Pe magellanica Gunnera of conditions natural field under positive) photosynthesis net values, negative (respiration exchange Gas 3. Figure secondary axis the on right. cases. all for patagonica Petigera considered: Fig 1) (area Glacier front and initial the of colonization stages of cover dense with 2) (area forest respectively) Area Chile). Fuego, 1. Figure Figure captions means± Data are species value Averaged 3: Table Nothofagus antarctica antarctica Nothofagus betuloides Nothofagus mucronata Gaultheria magellanica Gunnera Species
Acceptedl Article tigera patagonica tigera ure
five for all sampled all for . Nitrogen 2. Leaf elemental and isotopic analysis in selected plant species plant selected in analysis isotopic and elemental Leaf (a)
evs f ae niiul ee sd PAR used. were individual same of leaves
unr magellanica Gunnera
Note that that Note n te ro idcts h lcto o te il camp. field the of location the indicates arrow the and ceai dsrpin f lce frln i fot f P of front in foreland glacier of description Schematic SE
.
;
iain ae udr il ntrl odtos for conditions natural field under rates fixation (n = 2
; sites of Pia Glacier foreland (Tierra del Fuego, Chile). Chile). delFuego, (Tierra foreland Glacier Pia of sites s light (a, light (n = (n = 2 (n = Placopsisperrugosa
s of foliar N (%), P ( P N(%), foliar s of
Placopsis perrugosa Placopsis (a Stereocaulon alpinum Stereocaulon ad 2 and 1 ,
16 18 8 d), 0 )
) ) )
b, ohfgs antarctica Nothofagus 2. ±0. 1.390 1.0 3.25
c) and temperature (d, temperature and c) 4
Pia are δ 19 54 15 3 (a, N N patterns N unr magellanica Gunnera ±0. ±0.03 ±0.0
Glacier, Tierra delFuegoGlacier, Tierra (Chile
h smln locations sampling the b 119 051 , % 5 ; 5 3 d ) and δ ) and
). c ande c
ad fxn lces ( lichens fixing N and )
n (c 0.191 ±0.00 0.191 0.1 0.0 0.29 ; d) estimated values for Tr (transfer ratio for ratio (transfer Tr for values estimated d) ; = 5 for all cases except for except cases all for 5 = ,
15 90 90 e) and e) N ). 3
P ±0.03 ±0.0 ±0.02 Values are mean(n Values are (‰)
(b
e, , , 12
Placopsis perrugosa Placopsis
obtained from the evaluated plant plant evaluated fromobtained the
5 5 4 htsnhtc cie radiation active photosynthetic G. magellanica ) n N iig ihn ( ad f: and (c lichens fixing N and e) f) for different species considered: species different for f)
t h hraeu lyr () Pia (c) layer. herbaceous the at 12. 10. 1 12.
2. mrie n forest and (moraine 901 107 76 68 N:P 5
±
± ± ±0. 1 troaln alpinum Stereocaulon ) 0.687 1
. . i
024 .
Gair Ter del (Tierra Glacier a
the 107 82 a) (% N Leaf content (b) (b) = 5 = . (see Table 1) along along 1) Table (see
5
) different species species different Nothofagus Nothofagus ±
(e) refer to the the to refer (e) standard error standard - - - - 3. 4.03 4. 0.31 958 683 δ 3 4 15
±0. ±0.410 ±0. ±0.0 N areas
tree, tree, 434 454 spp. ; 5
T 5
; , ,
This article isThis article by protected copyright. All rightsreserved. nitrogenPS, ed.Symbiotic fixation in Edinburgh: plants. Cambridge UniversityPress, 539 Accepted JHBecking biotechnology of ectomycorrhiza morphology, colonization,anddivers ZakBecerra AG, MR 224 ofsymbiotic dinitrogenrole fixa J,CravenDJ, JS Batterman M,Ransijn SA, HedinLO,VanBreugel Hall delof Tierra Fuego (Chile). Bryophyte Casermeiro MÁ,DeCruz D, La Pintado A,Palacios MT, Rozzi R, Arróniz Lobaria oregana Antoine ME EcologyAustral Anderson MJ Alaska.southeast 1.The and morphology.moraines soil Alexander EB,Burt R Botany andExperimental Environmental reduces PSII B radiation performance photosynthesis andnet in highArctic Article KR, Albert Mikkelsen TN, Ro References: mean only estimates are used values The glacier. the from water melt the from mainly to 34 at 30% and 90% as calculated air the from assumptions) of follow calculated host) to fungus from N Gunnera – 227.
( ed these ed n
- = 5) Crespo M,Pérez
- cyanobacteria associations primary deglaciatedareas during succession inrecently
.
magellanica . and has been set at 0.1. at set been has and ± standard ± standard error 1976 200 .
yr assumptions 2001 : F is set at 0.7 for all plants except plants all for 0.7 at set is F :
26 . .
4 Bryologist
( . Nitrogen fixation . Nitrogen fixation in some ecosystems In: natural Nutman inIndonesia. sourced : 32 . An ecophysiological . An approach quantifying to by nitrogen fixation mean . A new method. Anew for non – . . 46. 2011 1996
δ a be ajse i te al years early the in adjusted been has 15
-
from
Ortega S,Ortega DeLosRíos A,Green TGA,Ochoa PLoS ONE N = N (see Supp (see
107 . Th . . Soil development. Soil moraines on Glacier, ofMendenhall
- tion secondarytion in tropical forest succession. Poulsen H, Arndal H, A Poulsen MF,Michelsen - : 82 e. Gunnera e ectomycorrhizal e ectomycorrhizal symbiosi 0.74, Springer o ec seis ln te chronosequence the along species each for – ity. In:Rai ity. M, Varma eds.Divers A, 87. Non orting Information orting
- 9 0.96,
: 15 73
- magellanica N - : 10 - Verlag Berlin Verlag Heidelberg Press, 19 – - parametric multivariate ofvariance.analysis fixing - 17. 1.92 and 1.92 – 18.
plan Gunnera
at 7 at - Geoderma
4.39‰, respectively). 4.39‰, t
data for a more detailed explanation detailed more a for data s receive N from their their from N receive s yr s in South s inSouth America: .
, 70% at 10 at 70% , magellanica o elc ta i i coming is it that reflect to
72 : 1 et al. et . 2011 – ity and ity 17.
- yr
Salix arcticaSalix 2014 Nature Hueso R,Hueso which gets its gets which
. Ambient UV . . , 50% at 19 at 50% ,
δ 2013 – Estimations . 15 41. . mycorrhi . N available N Values are Values
502 . Key : . – zas yr - N .
This article isThis article by protected copyright. All rightsreserved. of legumenitrogenase activity nodules. root Dart PJ,DayJM Glacier Bay,Alaska. RL,Crocker MajorJ concentrations, andnitrogen availability. andisotopes relationships their with cliamte, mycorrhizalfungi, nutrient foliar K, Kendra Michelsen A, Nardoto GB, AJ,AidarMPM,DawsonTE Craine JM,Elmore soils. Wang L MD,HasselquistNJ,KobaK, ENJ,Craine JM,Brookshire Marin Cramer 6 nitrogenbiological (N SS, Latty EF, VonFischer JC,ElseroadA, DS, CC, AR,FisherH, Cleveland Howarth Townsend Schimel LO, RW,Hedin Perakis 175. followingdeglacisuccession Chapin LR,CL,SharmanWalker FS,Fastie LC ecosystem development. CC SC,Sullivan BW,KnelmanCastle J,HoodE,Nemergut DR, SK,Cleveland Schmidt Mount near Robson, BritishColumbia, Canada. Blundon DaleM D, alder Hibbs and controls. In: DE, DeBell DS, Tarrant RF, eds.The D Binkley Royal ofthe Proceedings Academy Irish Bergman B,OsborneB eds. Cyanobacteria in Bergman B 505 and insoils nitrification sedimentsassessing LW, Belser Mays EL 550. Accepted23 Article . – –
2017 645. 510. . Michigan: Press, Oregon University State 57 Plant and Soil .
. Nutrient limitation of. soilmicrobial a 2015 , Cromack K, Backer DD . 2002 . Ecological interpretations. Ecological nitrogen of isotope ofterrestrialratios plants and . . The 1971
. 396 Journal ofEcology 1990 2 s . . ) fixation in natural) fixationin ecosystems. ymbiosis. Springer Dordrecht: Netherlands, 207 1980 1955 Nostoc . Effects temperature ofincubation and oxygen tensionon : 1 . Oecologia 2002 . Dinitroge – 26. . ation ation at Glacier Bay,Alaska. . Soi
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Gunnera l development to inrelation surface vegetation at age ific inhibition of oxidati nitrite
185 Gunnera . n fixation n fixation (acetylene reduction) primary in succession 1994 : 513
et al. et 102 43 s New Phytologist ymbiosis : 427 . Nitrogen fixation . Nitrogen alder: byred . Plant andSoil : 35 – Applied andEnvironmental Applied Microbiology -
et al. et 524. 2009 Nostoc Arct. Alp.Res.Arct. – ctivity duringctivity earliest of the stages – 39. 448.
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1994
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. Mec 183
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22 hanismsprimary of on by Biology and Environment: : 255 – – 184. 992.
– – chlorate andits in use 263. 232.
b
iology, rates, iology, rates, - Spiotta E,
64 : 149
13
39 : : – This article isThis article by protected copyright. All rightsreserved. TGA,Green S,Arróniz SanchoLG,Pintado A, SacoMartín D, 1333 limitation along achronosequence from forefield. aglacier Göransson VenterinkH, Olde 80 f T,SingletonGeorge PW, BohloolBBen stepp J, JA Fontenla S,Puntieri Ocampo SwissBerne: Environment, Agencyforthe ForestsandLandscape (SAEFL), 273 trees Flückiger W, Braun S 19 communities alongaglacierforefield del inTierra Fuego(Chile). TG, RozziR, SanchoLG,delosR Fernández forefield chronosequencesTierra Fuego(Chile). in del Rozzi LG, R,Sancho delos Fernández nitrogen and area content. Farquhar GD,MillerTN, JM Buckley 78 Evans JR a JF, Eckart ecosystem development. Richardson SJ IA, Martínez Dickie GB4003. andregional scales:Amultimodelevaluation. global Horowitz M,UC, Krol Kulshrestha LW, B,FioreAM,Hauglustaine J,LamarqueJF,BeyI,Eickhout D, Dentener F,Drevet microorganisms. David KAV,FayP ixation ixation cetylene
Accepted: 563. : 161 Article:
9
– – e, Argentina. -
1340. 19. a comment. BA, Empirical In: RB,eds. critical loads for nitrogen –
by 173.
r . eduction - - 1989 s
Raguse CA Martínez MA,PointingSB, Pérez Martínez MA,Pérez oybean
. . Photosynthesis and relationships. Photosynthesis nitrogen ofC3 in leaves plants. 2013 Applied andEnvironmApplied Plant and Soil . a from ctivity ctivity 1977 - . Mycorrhizas and mycorrhizal fungal. Mycorrhizasandmycorrhizal communities throughout García LB,García Koele N,Grelet GA,Tylianakis JM, Peltzer DA, . . 2003 Plant andSoilPlant 1980 f . Effects long of Silva Fennica our of Ríos A . Critical limits concentrations. Critical fornutrient and forforest ratios . Effects of m s ubterranean aturity aturity H, Bååth E
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g ental Microbiologyental 367
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. Optimal relation stomatal control in to leaf g – . - rown – . Yield, . Yield,
Ortega S,Arróniz Ortega 39. Functional ecology of Functional microbial ecology soil 2006 v 637. . . Soil bacterial. Soil growthandnutrient ariation ariation Agronomy Journal
Global at at
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Soil Biology and Biochemistry 34 Biogeochemical Cycles n l e itrogen itrogen : 640 ight ight levations International Microbiology and - – - Crespo M, Casermeiro Crespo M,Casermeiro 646. Crespo M,AllanGreen
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43
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This article isThis article by protected copyright. All rightsreserved. BZ, Houlton Morford implications. Holloway JM,DahlgrenRA west. chronosequence SJ,WebbNR,Hodkinson ID, Coulson CoulsonJ concentrations may plant indicate EA,Hobbie Mack analytical models. development andnitrogen ofmycorrhizae primary supply during succession: Testing EA,Hobbie JumpponenA, J Trappe dynamicnitrogen EA,Hobbie P Högberg 815 canestimatetundra nitrogen cyclingmycorrhizalthrough fungi: Areview. EA,Hobbie HobbieJE 383 Heidelberg, Biology, vol3.Springer, Berlin, F,eds.VarmaA, Buscot Microorg EA Hobbie EcologyAustral prostrate shrub by the Henríquez CH JM, Lusk for N RWF,Hardy Hol oldScottisch field. t LL,Handley CM Scrimgeour Phytologist Güsewell S 1656. on terrestrial in forced vegetation Antarctica byglobalwarming. TGA,Green SanchoLG,Pintado A, SchroeterB withcyanobacterialglycophyte plants symbionts. MA, Caravaca de MT Accepted Article he present limits for tointerpretation systemsorigional uncultivated from with data a – 830. 2
Society
fixation: laboratory fieldevaluation. and
. . 164 2004
2005 Global Biogeochemical Cycles 91 : 243 s com : 651 30 s. . N:P ratios in terrestrial plants: interrestrial . N:Pratios andfunctional variarion significance. . Assessing . Assessing sten RD, EK,RC Jackson Burns Oecologia o SA, M Williams : 877 Advances inecological research New Phytologist New – – munity in highthe Arctic : vegetation and development soil innorth 266. Empetrum rubrum 663.
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s 16 . Foliarfungal 15N:14 and reflectN ratios – oils m 382. : 65 Plant physiologyPlant . Convergent evidence for Convergentevidence . widespread rock Nothofagus antarctica icrobes icrobes – : AoB PLANTS 402. . r
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This article isThis article by protected copyright. All rightsreserved. Accepted infront chronosequence of PiaGlacier(TierradelFuego, the Chile). Table S3 Article respiration and ratesfor photosynthesis speciesobtained and studied localities. Table S2 activity rates obtained forstudied speciesand Table S1 S2 Methods S1 Methods frontandforest.glacier Fig. S4 Fig. S3 Fig. S2 Fuego, Chile)showing colonization vegetation sequence. Fig. S1 Supporting Information Biomass production of andapex andpathwaysProposed nitrogen uptake transfer atPia Glacier foreland. Temperature ofDescription the sampled infront chronosequence of PiaGlacier(Tierradel the Soil variablesSoil measured from collectedatdifferent soils ofexposurealongages ofPERMANOVA postResults pairwise ofPERMANOVA postResults pairwise Calculation Calculation of headspaces forARA differentbottle measurement. Cal culations nitrogen about transfers andsources control inside andoutside incubation bottles.
Gunnera magellanica Gunnera localities. - - hoc comparisons between net hoc comparisons between nitrogenase
in the in the two sampled locations:
the the This article isThis article by protected copyright. All rightsreserved. Accepted Article
This article isThis article by protected copyright. All rightsreserved. Accepted Article
This article isThis article by protected copyright. All rightsreserved. Accepted Article