This article was downloaded by: [University of Georgia]On: 18 December 2014, At: 04:19Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number: 1072954 Registeredoffice: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK

Click for updates

New Zealand Journal of BotanyPublication details, including instructions for authors andsubscription information:http://www.tandfonline.com/loi/tnzb20

Assessing the potential of Araucariaangustifolia (Araucariaceae) as a nurseplant in highland grasslands of southBrazilCL Korndörfera, LR Dillenburgb & LDS Duartec

a Departamento de Biologia, Universidade Estadual do Piauí, Piauí,Brazilb Departamento de Botânica, Universidade Federal do Rio Grandedo Sul, Porto Alegre, Brazilc Departamento de Ecologia, Universidade Federal do Rio Grandedo Sul, Porto Alegre, BrazilPublished online: 21 Nov 2014.

To cite this article: CL Korndörfer, LR Dillenburg & LDS Duarte (2014): Assessing the potential ofAraucaria angustifolia (Araucariaceae) as a nurse plant in highland grasslands of south Brazil, NewZealand Journal of Botany, DOI: 10.1080/0028825X.2014.979837

To link to this article: http://dx.doi.org/10.1080/0028825X.2014.979837

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the“Content”) contained in the publications on our platform. However, Taylor & Francis,our agents, and our licensors make no representations or warranties whatsoever as tothe accuracy, completeness, or suitability for any purpose of the Content. Any opinionsand views expressed in this publication are the opinions and views of the authors,and are not the views of or endorsed by Taylor & Francis. The accuracy of the Contentshould not be relied upon and should be independently verified with primary sourcesof information. Taylor and Francis shall not be liable for any losses, actions, claims,proceedings, demands, costs, expenses, damages, and other liabilities whatsoever orhowsoever caused arising directly or indirectly in connection with, in relation to or arisingout of the use of the Content.

This article may be used for research, teaching, and private study purposes. Anysubstantial or systematic reproduction, redistribution, reselling, loan, sub-licensing,systematic supply, or distribution in any form to anyone is expressly forbidden. Terms &

Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14

RESEARCH ARTICLE

Assessing the potential of Araucaria angustifolia (Araucariaceae) as a nurseplant in highland grasslands of south Brazil

CL Korndörfera, LR Dillenburgb* and LDS Duartec

aDepartamento de Biologia, Universidade Estadual do Piauí, Piauí, Brazil; bDepartamento de Botânica,Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil; cDepartamento de Ecologia, UniversidadeFederal do Rio Grande do Sul, Porto Alegre, Brazil

(Received 13 May 2014; accepted 17 October 2014)

The expansion of forests over natural grasslands is observed in many parts of the world. This study aimedto contribute to the investigation into the nursing effects promoted by Araucaria angustifolia during theprocess of forest expansion over grasslands in southern Brazil. Air temperature and humidity, and soilchemistry were evaluated beneath the canopy of isolated trees of A. angustifolia, and compared withvalues in adjacent grassland areas and under the canopy of the shrub Baccharis uncinella. Milder summertemperatures and vapour pressure deficits were measured under Araucaria and Baccharis compared withopen grassland. There were also ameliorating effects on soil chemistry under individuals of these twospecies, but these were more pronounced for Araucaria than for Baccharis. The results suggest that thelarge number of seedlings commonly found beneath the canopy of Araucaria is due not only to perching,but also to nursing, through the amelioration of environmental conditions.

Keywords: Araucaria forest; Baccharis uncinella; facilitation; microenvironment; nucleation; nursing

Introduction

The expansion of woody vegetation over naturalgrasslands is a natural phenomenon observed inmany parts of the world, but changes in grazing andfire regimes and global climate changes, such asincreasing atmospheric CO2, are accelerating thisprocess (Polley 1997; Bond et al. 2003; Müller et al.2012). The decrease in fire and grazing practices, forexample, is leading to dramatic landscape changes ingrasslands (Campos) from southern Brazil, by accel-erating the process of forest expansion (Oliveira &Pillar 2004; Overbeck et al. 2007)

Araucaria angustifolia (Bertol.) Ktze. (Arau-cariaceae) is a South American conifer that reachesup to 50m high and 2m in diameter at breast height.It is the dominant tree species in the upper canopy ofthe montane forests of the high-altitude plateaus ofsouthern Brazil (known as Araucaria forests). The

associated fauna broadly uses its starch-rich seeds,and its high-quality wood was exploited to thelimit during the first half of the twentieth century.Araucaria forests often form mosaics with theadjacent grasslands, and also appear as galleryforests along streams and as forest islands on hilltops (Reitz et al. 1988).

Palynological evidence, soil carbon isotope stud-ies and dendrochronological analyses have indi-cated that the montane Araucaria forests have beenexpanding over the adjacent grasslands in recentmillennia (Behling et al. 2004; Dümig et al. 2008;Silva et al. 2009; Silva & Anand 2011). Recentstudies have not only confirmed such expansion, buthave also demonstrated the importance of A. angu-stifolia as a forest nucleation species in the grasslandmatrix of the high-altitude plateaus of the southern-most state of Brazil, Rio Grande do Sul (Duarte et al.2006, 2007, 2010; Dos Santos et al. 2011).

*Corresponding author. Email: lucia.dillenburg@ufrgs.br

New Zealand Journal of Botany, 2014http://dx.doi.org/10.1080/0028825X.2014.979837

© 2014 The Royal Society of New Zealand

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14

Woody vegetation may expand over naturalgrasslands from the forest edges or ‘in jumps’(Klein 1960; Oliveira & Pillar 2004). This secondprocess, called forest nucleation (sensu Yarranton& Morrison 1974), can include two mechanisms:perching, plants being used as perches by seed-dispersal birds; and/or nursing effects, ameliora-tion of the microenvironmental conditions. Whenthese two mechanisms act simultaneously, chancesof seedling recruitment and establishment beneathnucleation species are high (Flores & Jurado 2003;Pausas et al. 2006; Duarte et al. 2007). Araucariaforest expansion ‘in jumps’ may start by nucle-ation from rocks, trees and shrubs, but while allthese agents may act as perches, only rocks andtrees seem to also have a nursing effect (Duarteet al. 2006, 2010; Carlucci et al. 2011).

In a study conducted in the Araucaria forest/grassland mosaics in southern Brazil, a few tree andshrub species were found to grow as isolatedindividuals and to host forest seedlings under theircrowns. The pioneer shrub Baccharis uncinella DC(Asteraceae) was found to be particularly abundantamong these individuals, but had a very low densityof seedlings (height ≤ 50 cm) growing below them(< 0.05 individuals m−2). By contrast, the fewerisolated trees of A. angustifolia had a much higherdensity of seedlings under their crowns (c. 0.35individuals m−2) compared with all other species(Duarte et al. 2006). These results led the authorsto propose two mechanisms for the success ofA. angustifolia in promoting forest seedling recruit-ment and establishment: greater bird attraction(perching effect) and greater amelioration of abioticconditions (nursing effect) than other woody species.Although the strong perching effect of this coniferspecies was later confirmed by a seed rain study (DosSantos et al. 2011), its nursing effects and mechan-isms are yet to be explored (Duarte et al. 2010).

Nurse plants are those that ameliorate the micro-environmental conditions beneath their canopies,including reduction in air temperature, increase inwater and nutrient availability, shading and protectionfrom grazing and trampling (Franco & Nobel 1989;Tewksbury&Lloyd 2001; López et al. 2007; Gómez-Aparicio et al. 2008). This study aims to identify andexplore the nursing mechanisms promoted by A.

angustifolia, in order to explain its important role as anucleating species in the process of forest expansionin the highland forests of southern Brazil. In order toaccomplish that, we selected a representative forest/grassland mosaic in the southernmost state of Brazil,and compared some key aspects of the microenviron-ment under the canopy of A. angustifolia with thoseoperating on adjacent grassland areas, as well as withthose under the pioneer shrub, B. uncinella, whosenucleating effects were reported to be smaller thanthose of our target species.

Materials and methods

Study site

The study was conducted in the Pró-Mata Researchand Nature Conservation Centre (CPCN-Pró-Mata).The centre has 4500 ha and is located in SãoFrancisco de Paula, Rio Grande do Sul State, Brazil(29°28′52.04″S and 50°10′28.00″W). The regionalclimate is classified according to the Köppen systemas Cfb. The annualmean temperature is 14.5 °C, withnegative temperatures occurring from April toNovember, and high rainfall levels occurringthroughout the year, amounting to an annual meanof 2252 mm (Backes 1999). Soils are generallyacidic, with low base saturation and high levels ofexchangeable Al and organic matter (Streck et al.2008). Vegetation is characterised by tall grasslands(Campos), intermingled with Araucaria forests.Cattle grazing and burning practices were stoppedin 1993, allowing for increased regeneration of theforest and woody plant establishment in the grassland(Oliveira & Pillar 2004).

The study site was located in an area of c. 78 haof grassland, surrounded by Araucaria forests,where a significant colonisation of forest species inthe grassland matrix is observed. Individuals of thewoody species A. angustifolia, B. uncinella, Pinuselliottii and Myrceugenia euosma are commonlyfound in these grassland areas (Duarte et al. 2006).

Sampling methods

Isolated trees of A. angustifolia and shrubs ofB. uncinella (hereafter called Araucaria and Bac-charis) were randomly sampled in the grassland in

2 CL Korndörfer et al.

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14

January 2009. Starting from an arbitrarily definedinitial point, we walked towards one predeterminedcardinal point (N, S, E or W). The first isolatedindividual of Araucaria or Baccharis found wassampled. We considered an individual to be isolatedif it had no woody neighbour touching its crown,and if the distance separating it from another maturetree or shrub was at least 10 m (at the end, thisminimal distance turned out to be 15 m). For eachsampled Araucaria and Baccharis, a point wasmarked in the open field 10 m away from its mainstem and in the direction in which the least numberof other isolated woody plants could be seen. Thissampling procedure was repeated until we marked15 Araucaria, 15 Baccharis and 15 points in theopen, away from Araucaria, and 15 points in theopen, away from Baccharis. We completed the sam-pling procedure with 30 points in the open field(grassland), and 30 woody individuals (a total of 60sampling units).

The mean ± SEM height and crown area of theselected Araucaria individuals were 6.46 ± 0.34 mand 48.80 ± 5.97 m2, respectively, and, for Bac-charis, 2.05 ± 0.07 m and 6.39 ± 0.67 m2, respect-ively. The two species also differed on the amount ofvertical space available below their crows: c. 5 m forAraucaria and < 1 m for Baccharis. These threemicroenvironments (Araucaria, Baccharis and openfield) were organised into three blocks, separatedfrom each other by c. 500 m. Each block includedfive Araucaria, five Baccharis, five points in theopen near Araucaria and five points in the open nearBaccharis (20 samples per block).

Microclimate and canopy openness

The microclimate (temperature and air humidity)associated with the sampling points was evaluatedusing 20 data loggers LOGBOX-RHT (NOVUS,Ltda, Porto Alegre, Brazil). Temperature and airhumidity were used to calculate the vapour pressuredeficit (VPD) of the air. Data loggers were placed 80cm from the ground, standing above the grassyvegetation in the open sites. Under the canopies,data loggers were placed 70 cm away from thetrunk. Data for each block were recorded everyhour, for five consecutive days, in the summer of

2009. Measurements were made on 8–12 March2009, 22–27 February 2009 and 1–5March 2009, inblocks 1, 2 and 3, respectively. Daily means formean, minimum and maximum air temperatures,humidity and VPD were based on all hourlymeasurements taken over five consecutive days.Mean values for each hour of the day were based onall measurements taken at a given hour over the fivedays. A fewwinter measurements were also taken inthe same year, and because the results followed thesame pattern as the summer measurements, only thesummer results are shown.

The percentage of open canopy beneath Arau-caria and Baccharis was assessed with hemispher-ical photographs. Pictures were taken with a NikonCoolpix 8700 camera, coupled with a fisheye lensFC-E9 (Raynox DCR-CF 185° – Pro Fisheyecircular) in June 2010, 30 cm above the groundunder the shrubs and 1.65 m above the ground underthe trees. The images were analysed using theprogram Gap Light Analyzer 2.0 (Frazer et al. 1999).

Soil characteristics

Soil chemistry was analysed in all 60 sampling unitsin January 2009 (summer) and in August 2010(winter). Five hundred grams of soil (composed offour subsamples) were taken from the upper 20 cm ofsoil below the canopies and in the open field, using ashovel. Soil samples were placed in plastic bags andtransported to the Analyses Laboratory of the SoilDepartment of the Federal University of Rio Grandedo Sul. Soil variables were determined as follows:pH measured in water solution (1 : 1; v/v), P (mgdm−3) and K (mg dm−3) based on the Mehlich Imethod; organic matter (OM%) obtained by sulfo-cromic solution oxidation with external heat,exchangeable Ca (cmolc dm−3), Mg (cmolc dm−3)and Al (cmolc dm

−3) extracted with KCl 1 mol L−1;cation-exchange capacity (CEC, cmolc dm−3) at pH7, and N determined by TKN–Kjeldahl/0.01%method. After extraction, exchangeable cations weredetermined in an inductively coupled plasma spec-trometer (Optima 7300DV ICO-OES, PerkinElmer,Inc., USA). In addition to absolute values, we alsoreport the difference between the value recordedbelow the canopy of Araucaria or Baccharis and

Araucaria angustifolia as a nurse plant 3

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14

that recorded in the adjacent open field, in order tocompare the soil chemical changes induced by thepresence of the two woody species.

Soil samples for textural analysis were collectedfollowing the same procedures used for chemicalanalyses, in October 2010. However, only 27samples were taken (nine Araucaria, nine Baccharisand nine open field, all randomly sampled). Soilmoisture was estimated by gravimetric water content.Forty-five samples (15 Araucaria, 15 Baccharis and15 open field) of 250 g soil (composed of foursubsamples) were taken following the same proce-dures previously described for chemical and texturalanalyses, in March 2010. Immediately after collec-tion, samples were weighed to obtain the fresh mass(FM) and placed in plastic bags. Back in the lab, theywere dried at 60 °C for 24 h to obtain the dry mass(DM). The gravimetric water content (GWC) wasthen calculated as (FM – DM)/DM.

Data analyses

Microclimate and soil parameters were compared inrelation to block and microenvironment effectsusing analysis of variance (ANOVA) with permu-tation test (Pillar & Orlóci 1996). For this, aEuclidean distance matrix between the observationswas computed, and the sum of squared distancesbetween groups of observations, defined by twofactors (block and microenvironment), was used astest criterion (Qb statistics, see also Pillar 2013). Theprobability of the observed Qb for factor environ-ment being lower than null Qb values was obtainedby permuting the observations within blocks andthen recomputing Qb for microenvironment. Theprocedure was repeated 10,000 times, and thenumber of times the observed Qb value was lowerthan null Qb values defined that probability. Formicroclimate and soil parameters, ANOVA withpermutation tests included the three microenviron-ments (Araucaria, Baccharis and open field). Datafrom each season were analysed separately in thecase of soil data. When comparing the differencesbetween each species and the open field for the soilparameters, the ANOVA only included two levels ofmicroenvironment (Araucaria and Baccharis). Inall cases, when microenvironment effect was found

to be significant, the differences between the levelsof the factor microenvironment were comparedusing orthogonal contrasts with permutation test,in a similar way as the overall effect ANOVA (Pillar& Orlóci 1996). The MULTIV v. 2.67 statisticalsoftware (V. Pillar, available at http://ecoqua.ecologia.ufrgs.br/ecoqua/MULTIV.html) was used forthese analyses.

Results

Microclimate and canopy openness

Mean and maximum daily temperatures were sig-nificantly higher in the open field than underAraucaria andBaccharis, but did not differ betweenthese two species (Table 1). There were no differ-ences in mean and maximum air humidity amongthe three microenvironments. Minimum air humid-ity was higher in Baccharis than in Araucaria andlower in the open field than in Araucaria. Mean andmaximum values of VPD were greater in the openfield than under the woody individuals. Diurnalvariations in these meteorological parametersrevealed that maximum temperatures and VPDs atmidday were not only higher in the open field, butalso higher under Araucaria than under Baccharis(Fig. 1). The percentage of canopy openness wasalso significantly higher under the former thanunder the latter species (Table 1).

Soil conditions

Textural analyses showed that the soil in the areahas higher percentages of silt (c. 50%) and clay(c. 30%) than of sand, with no significant dif‐ferences among the three microenvironments (datanot shown). There were also no differences ingravimetric soil water content (measured in thesummer) among them (Table 1).

The soil in all three environments and bothseasons was characterised by a low pH and highlevels of organic matter. Although the CEC did notvary among the environments, the base saturationwas greater under the trees and shrubs than in theopen field. The Al saturation showed an oppositepattern. Soil concentrations of N, P and K were, ingeneral, greater under Araucaria and Baccharis

4 CL Korndörfer et al.

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14

than in the open field, but these differences weremore consistent for the former species. In theparticular case of P in the summer and K in thewinter, soil concentration under Araucariawas alsogreater than under Baccharis. The availability of Caand Mg in the three different soil environmentschanged markedly from summer to winter. The Caand Mg availabilities were higher in the open fieldin the summer, followed by Baccharis and Arau-caria. In the winter, the availability of thesenutrients reduced substantially in the open field,such that soil under both Araucaria and Baccharishad greater concentrations than the soil in the open(Table 2).

Araucaria had a greater positive effect on theconcentrations of N, K, P and Mg (measured bythe difference from the open field) than Baccharis(Fig. 2A, 2B, 2D–2F). With respect to Al satura-tion of CEC (Fig. 2C), the reduction effect wasalso higher for Araucaria than for Baccharis.Deviations of soil parameters not presented inFigure 2 were not significantly different betweenthe two species.

Discussion

Changes in microclimate

Mean and maximum temperatures and VPDsduring the summer were lower under Araucariaand Baccharis than in the open field, indicatingmilder and more favourable conditions for seed-ling establishment under individuals of thesespecies than in the more open grassy environment.Most studies with nurse plants recognise theimportance of tree canopies in reducing thetemperature and VPD in open areas (Ludwig et al.2004; Gómez-Aparicio et al. 2008). Our study wasconducted in a montane, cool and very humidenvironment and, as expected, maximum tempera-tures and VPDs registered in the study area weremuch smaller than those reported in other studies,which were mostly conducted in open, but warmerand drier environments (Holl 1999; Gómez-Apar-icio et al. 2005; Munguía-Rosas & Sosa 2008).However, we believe that the reported reductionsin temperature and VPD promoted by the twoT

able

1Microclim

atic

characteristicsun

derthecano

pies

ofAraucaria

andBaccharisandin

theop

enfield.

Araucaria

Baccharis

Openfield

Clim

atevariable

Minim

umMean

Maxim

umMinim

umMean

Maxim

umMinim

umMean

Maxim

um

Airtemperature

(°C)

16.4

a19

.8b

26.6

b16

.6a

19.9

b25

.8b

16.3

a20

.6a

29.2

a(0.24)

(0.46)

(0.97)

(0.20)

(0.43)

(0.82)

(0.19)

(0.46)

(0.91)

Relativehu

midity

(%)

56.2

b89

.1a

100.00

a59

.2a

89.5

a10

0.0a

50.4

c87

.8a

100.0a

(2.46)

(0.49)

(0.66)

(2.99)

(1.16)

(0.82)

(2.00)

(0.72)

(0.61)

VPD

(kPa)

0.04

a0.26

b2.12

b0.05

a0.25

b1.77

b0.04

a0.30

a2.56

a(0.27)

(0.02)

(0.03)

(0.02)

(0.03)

(0.19)

(0.01)

(0.03)

(0.30)

Canop

yop

enness

(%)

–61

.2a

––

51.2

b–

––

–(2.52)

(2.56)

SoilGWC

(ggsoil−1)

–0.78

a–

–0.83

a–

–0.75

a–

(0.08)

(0.08)

(0.07)

GWC,gravim

etricwater

content;VPD,vapo

urpressure

deficit.

Dataaregivenas

means

±SEM.P

-valuesweregeneratedfrom

ANOVAthroug

han

aleatorisatio

ntestwith

10,000

perm

utations.D

ifferent

lower

case

lettersindicatesign

ificant

differencesbetweenenvironm

entsforagivenparameter

(P<0.05).Airtemperature

andrelativ

ehumidity

weremonito

redforfive

consecutivedays

insummer

2009.For

air

temperature,relativ

ehu

midity

andVPD,n=12

(Araucaria),n=13

(Baccharis)andn=18

(openfield).For

cano

pyop

enness

andsoilGWC,n=15

.

Araucaria angustifolia as a nurse plant 5

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14

woody species are of ecological significance fortheir nursing effects during the summer. Middaymaximum temperature and VPD registered duringthe summer in the open areas reached c. 40 °C and4 kPa, respectively. The cooling effect of thecanopies amounted to at least 5 °C and caused areduction of at least 1 kPa in VPD.

Despite striking differences in plant height,crown morphology and canopy openness betweenthe two species, the summer microclimate undertheir canopies was not very distinct, except for thehigher VPDs and maximum temperatures meas-ured under Araucaria during the warmest hours ofthe day. Because of the much denser and more

Figure 1 Daily variation in minimum (A), mean (B) and maximum (C) air temperature (black) and relativehumidity (grey) and minimum (D), mean (E) and maximum (F) vapour pressure deficit under the canopy ofAraucaria angustifolia (•, n = 12), Baccharis uncinella (▴, n = 13) and in the open field (▪, n = 18). Data are givenas means ± SEM, and represent the hourly records during five consecutive days in summer 2009.

6 CL Korndörfer et al.

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14

closed canopy of Baccharis, lower temperaturesand VPDs under their crowns than under those ofthe conifer species were expected. However, theconcentration of branches up high in the tall crownsof Araucaria may have allowed for a greater aircirculation than in the dense and bushy crowns ofBaccharis, attenuating the expected differences.

Shading

Although this study has not directly assessed theavailability of light in the different environments,it did show that the canopies of Araucaria imposeless shade than the canopies of Baccharis.

Light attenuation might be an important facil-itation effect in seedling establishment, by redu-cing the risks of photoinhibition, which are morelikely to occur under suboptimal conditions suchas those generated by low temperatures (Longet al. 1994). However, less light may also meanless photosynthesis and growth. Thus, it is pos-sible that the lesser shade imposed by the canopyof Araucaria improves the establishment of treeseedlings by limiting the occurrence of photoinhi-bition, particularly during cold periods, withoutlimiting light availability for seedling growth.However, a better understanding of this possiblefacilitation mechanism requires measurements ofirradiance beneath the canopy of the two speciesand in the open field, as well as the photosyntheticresponses to light of individuals that are recruitedinto these different environments.

Changes in soil moisture and nutrients

Water content in the soil under the target speciesdid not differ from that under the grassy vegeta-tion. This similarity in water content does notcome as a great surprise, considering the largeamounts of rainfall in the region (Backes 1999).However, the presence of mature individuals ofeither Araucaria or Baccharis in the grasslandresulted in an overall improvement of soil fertilityand this effect was more pronounced for theconifer than for the shrub species.

Nurse plants can improve soil chemical condi-tions by litter deposition, leaching of atmosphericT

able

2Chemical

characteristicsof

thesoilun

derAraucaria

(n=15

),Baccharis(n

=15

),andin

theop

enfield(n

=30

).

Sum

mer

Winter

Param

eter

Araucaria

Baccharis

Openfield

Araucaria

Baccharis

Openfield

pH(inH2O)

4.41

±0.05

a4.46

±0.04

a4.43

±0.05

a4.81

±0.05

a4.85

±0.04

a4.81

±0.02

aP(m

gdm

−3)

8.03

±0.83

a5.51

±0.48

b4.55

±0.39

b5.79

±0.88

a5.24

±0.80

ab3.70

±0.52

bK

(mgdm

−3)

142.87

±12

.14a

123.27

±8.74

a79

.73±5.18

b12

8.60

±15

.84a

71.80±8.39

b57

.10±4.10

bCEC(cmol

cdm

−3)

42.20±2.35

a36

.41±2.24

a37

.13±2.25

a23

.15±1.93

a23

.77±1.57

a23

.37±1.04

aBasesaturatio

n(%

)3.80

±0.46

a3.00

±0.45

a2.13

±0.22

b9.07

±1.03

a6.93

±0.68

ab5.20

±0.53

bAlsaturatio

n(%

)81

.96±1.63

c87

.01±1.18

b90

.04±0.74

a74

.33±2.65

b76

.56±1.92

b83

.18±1.16

aN

(%)

0.94

±0.07

a0.88

±0.04

a0.78

±0.04

b0.70

±0.03

a0.63

±0.04

ab0.59

±0.03

bAl(cmol

cdm

−3)

6.88

±0.29

a6.87

±0.32

a2.89

±0.26

b5.71

±0.34

a5.27

±0.35

a5.58

±0.18

aCa(cmol

cdm

−3)

0.71

±0.08

b0.45

±0.04

c2.09

±0.12

a1.05

±0.12

a1.07

±0.10

a0.74

±0.07

bMg(cmol

c.dm

−3)

0.42

±0.05

b0.22

±0.03

c0.84

±0.08

a0.54

±0.05

a0.35

±0.05

b0.25

±0.02

cOM

(%)

>10

>10

>10

7.51

±0.10

a7.07

±0.17

a7.24

±0.14

a

CEC,catio

nexchange

capacity;OM,organicmatter.

Dataaregivenas

means

±SEM.Different

lower

case

letters

indicate

sign

ificantdifferencesbetweenenvironm

entsin

thesummer

andwinter(P

≤0.05).

Araucaria angustifolia as a nurse plant 7

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14

nutrients intercepted by their crowns, mycorrhizalassociations and droppings from grazing, perchingand hiding animals (Kellman 1979; Callaway et al.1991; Gea-Izquierdo et al. 2009). The results do notallow us to identify the mechanisms involved in theameliorating conditions of soil fertility. However,Silva & Anand (2011), working in the same area,also reported a progressive increase in soil fertility(particularly N) and microbial biomass across thevegetation gradient (grasslands < isolated trees <forest patches < forests). By evaluating δ15N in theA. angustifolia leaves, these authors suggested an

increasing importance of biological interactions forthe N nutrition of plants when moving along thissame gradient.

Araucaria angustifolia was found to be highlydependent on mycorrhiza (Moreira-Souza et al.2003; Zandavalli et al. 2004). Its presence in thegrass matrix might then increase the availability ofnutrients in the soil, as a result of this strongbiological interaction. Mycorrhizal associations ofB. uncinella have not yet been investigated, butZimmer et al. (2010) reported negative competit-ive effects (resource competition and mechanicalinterference) of this species on the colonisationof Podocarpus lambertii in a restoration area.Taking into account the fast growth of this short-lived pioneer shrub species, intense competitionfor soil resources with the surrounding vegeta-tion is to be expected, and might help explain itsless-pronounced amelioration of soil chemicalconditions.

One could argue that, in the process of grass-land colonisation by Araucaria trees, these wouldbe preferentially established in those spots that arericher than average to begin with, such that wecould not be certain that isolated trees causechanges in soil properties or if their distribution issimply a reflection of pre-existing heterogeneity. Ina previous study conducted in the same area,Garbin et al. (2006) analysed and compared soilpatchiness for inorganic nitrogen in mature Arau-caria forest and in an adjacent grassland area.Despite patchiness, there was no overall relation-ship between the position of mature trees andyoung individuals of A. angustifolia and patchlocation in the forest, indicating that the successfulestablishment of new trees may not depend onwhether they find a richer spot of soil or not. Thesefindings further support our suggestion that thisconifer species ameliorate soil conditions.

Conclusions

Our results have shown that, under the canopies ofAraucaria and Baccharis, seedlings and saplingsexperience lower summer temperatures and VPDs,as well as overall greater soil fertility, than whengrowing in the open field. However, when comparing

Figure 2 Chemical characteristics of the soil under thecanopy of Araucaria angustifolia (n = 15) and Bac-charis uncinella (n = 15). Data are given as means ±SEM and represent the differences, for a given para-meter, between the value under the canopy and that inthe adjacent open space. The P-values correspond to thecomparisons of the mean differences.

8 CL Korndörfer et al.

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14

these two pioneer species, Araucaria individualswere found to impose less shade and to promotegreater amelioration of soil chemical conditions undertheir canopies than Baccharis individuals.

Based on these results, we propose that A. angu-stifolia does act as an effective nucleating species, notonly by acting as a perch for seed dispersers (Duarteet al. 2006; Dos Santos et al. 2011), but by also bynursing the seedlings afterwards. The nursingmechanisms do seem to include the attenuation ofextreme temperatures and VPDs during the summer,the imposition of moderate shading and an increasein the availability of soil nutrients. Although indivi-duals of B. uncinella also create a more suitablemicroclimate under their canopies during the sum-mer, they offer a more closed canopy than individualsof this species, and the reduced canopy openness,associated with the dense and low crown of thisshrub, might impose light and space limitations to thecolonising seedlings. Also, their ameliorating effectsof the soil conditions are less pronounced than thoseof A. angustifolia.

Although we have made a significant contribu-tion to identifying nursing effects and mechanismsof A. angustifolia in the process of forest expansionover grasslands, future studies that compare theability of selected forest species to survive andgrow under the canopy of this and other speciesare needed. Also, a more in-depth investigationof changes in irradiance and soil chemical andbiological conditions promoted by the presence ofA. angustifoliawill greatly add to our knowledge ofthe nursing mechanisms of this conifer species.

Acknowledgements

This study is part of the doctoral thesis of the firstauthor, developed in the Post-Graduate Program inBotany of the Federal University of Rio Grande doSul. We thank the Inter-American Institute for GlobalChange Research (IAI), Fernanda Alabarce, PaulaFagundes and Luciano da Silva Figueiredo for fieldassistance, and the Coordination for Improvement ofHigher Education Personnel (CAPES/Brazil) and theBrazilian Council for Scientific and TechnologicalDevelopment (CNPq/Brazil) for fellowships awarded tothe first and second author, respectively.

References

Backes A 1999. Condicionamento climático e distribui-ção geográfica de Araucaria angustifolia (Bertol.)Kuntze no Brasil. Pesquisas (Série Botânica) 49:31–51.

Behling H, Pillar VD, Orlóci L, Bauermann SG 2004.Late Quaternary Araucaria forest, grassland (Cam-pos), fire and climate dynamics, studied by high-resolution pollen, charcoal and multivariate analysisof the Cambará do Sul core in southern Brazil.Palaeogeography, Palaeoclimatology, Palaeoecol-ogy 203: 277–297.

Bond WJ, Midgley GF, Woodward FI 2003. The import-ance of low atmospheric CO2 and fire in promotingthe spread of grasslands and savannas. GlobalChange Biology 9: 973–982.

Callaway RM, Nadkarni NM, Mahall BE 1991. Facilita-tion and interference of Quercus Douglasii onunderstory productivity in central California. Eco-logy 72: 1484–1499.

Carlucci MB, Teixeira FZ, Brum FT, Duarte LDS 2011.Edge expansion of Araucaria forest over southernBrazilian grasslands relies on nurse plant effect.Community Ecology 12: 196–201.

Dos Santos MMG, Oliveira JM, Müller SC, Pillar VD2011. Chuva de sementes de espécies lenhosasflorestais em mosaicos de floresta com Araucária ecampos no sul do Brasil. Acta Botanica Brasilica25: 160–167.

Duarte LDS, Carlucci MB, Hartz SM, Pillar VD 2007.Plant dispersal strategies and the colonization ofAraucaria forest patches in a grassland-forestmosaic. Journal of Vegetation Science 18: 847–858.

Duarte LDS, Dos-Santos MMG, Hartz SM, Pillar VD2006. Role of nurse plants in Araucaria Forestexpansion over grassland in south Brazil. AustralEcology 31: 520–528.

Duarte LDS, Hofmann GS, Dos Santos MMG, Hartz SM,Pillar VD 2010. Testing for the influence of nicheand neutral factors on sapling community assemblybeneath isolated woody plants in grasslands. Journalof Vegetation Science 21: 462–471.

Dümig A, Schad P, Rumpel C, DignacMF, Kögel-KnabnerI 2008.Araucaria forest expansion on grassland in thesouthern Brazilian highlands as revealed by 14C andδ13C studies. Geoderma 145: 143–157.

Flores J, Jurado E 2003. Are nurse-protégé interactionsmore common among plants from arid environ-ments? Journal of Vegetation Science 14: 911–916.

Franco AC, Nobel PS 1989. Effect of nurse plants onthe microhabitat and growth of cacti. Journal ofEcology 77: 870–886.

Frazer GW, Canham CD, Lertzman KP 1999. Gap lightanalyzer (GLA): imaging software to extract can-opy structure and gap light transmission indices

Araucaria angustifolia as a nurse plant 9

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14

from true-colour fisheye photographs, user manualand program documentation, version 2.0. Mill-brook, NY, Institute of Ecosystem Studies.

Garbin ML, Zandavalli, RB, Dillenburg, LR 2006. Soilpatches of inorganic nitrogen in subtropical Bra-zilian plant communities with Araucaria angustifo-lia. Plant and Soil 286: 323–337.

Gea-Izquierdo G, Monteiro G, Cañellas I 2009. Changesin limiting resources determine spatio-temporalvariability in tree–grass interactions. AgroforestrySystems 76: 375–387.

Gómez-Aparicio L, Gómez JM, Zamora R, Boettinger JL2005. Canopy vs. soil effects of shrubs facilitatingtree seedlings in Mediterranean montane ecosys-tems. Journal of Vegetation Science 16: 191–198.

Gómez-Aparicio L, Zamora R, Castro J, Hódar JA 2008.Facilitation of tree saplings nurse plants: microha-bitat amelioration or protection against herbivores?Journal of Vegetation Science 19: 161–172.

Holl KD 1999. Factors limiting tropical rain forestregeneration in abandoned pasture: seed rain, seedgermination, microclimate, and soil. Biotropica 31:229–242.

Kellman M 1979. Soil enrichment by neotropical savannatrees. Journal of Ecology 67: 565–577.

Klein RM 1960. O aspecto dinâmico do pinheirobrasileiro. Sellowia 12: 17–44.

Long SP, Humphries S, Falkowski, PG 1994. Photoinhi-bition of photosynthesis in nature. Annual Review ofPlant Physiology and Plant Molecular Biology 45:633–662.

López RP, Valdivia S, Sanjinés N, Quintana D 2007.The role of nurse plants in the establishment ofshrubs seedlings in the semi-arid subtropical An-des. Oecologia 152: 779–790.

Ludwig F, Kroon H, Berendse F, Prins HHT 2004. Theinfluence of savanna trees on nutrients, water andlight availability and the understory vegetation.Plant Ecology 170: 93–105.

Moreira-Souza M, Trufem SFB, Gomes-da-Costa SM,Cardoso EJBN 2003. Arbuscular mycorrhizal fungiassociated with Araucaria angustifolia (Bert.) O.Ktze. Mycorrhiza 13: 211–215.

Müller SC, Overbeck GE, Pfadenhauer J, Pillar VD2012. Woody species patterns at forest-grasslandboundaries in southern Brazil. Flora 207: 586–598.

Munguía-Rosas MA, Sosa VJ 2008. Nurse plants vs.nurse objects: effects of woody plants and rockycavities on the recruitment of the Pilosocereusleucocephalus columnar cactus. Annals of Botany101: 175–185.

Oliveira JM, Pillar VD 2004. Vegetation dynamics onmosaics of Campos and Araucaria forest between1974 and 1999 in Southern Brazil. CommunityEcology 5: 197–202.

Overbeck GE, Müller SC, Fidelis A, Pfadenhauer J, PillarVD, Blanco CC 2007. Brazil’s neglected biome: theSouth Brazilian Campos. Perspectives in Plant Eco-logy, Evolution and Systematics 9: 101–116.

Pausas JG, Bonet A, Maestre FT, Climent A 2006. Therole of the perch effect on the nucleation process inMediterranean semi-arid oldfields. Acta Oecolo-gica 29: 346–352.

Pillar VD 2013. How accurate and powerful are rando-mization tests in multivariate analysis of variance?Community Ecology 14: 153–163.

Pillar VD, Orlóci L 1996. On randomization testing invegetation science: multifactor comparisons ofrelevé groups. Journal of Vegetation Science 7:585–592.

Polley HW 1997. Implications of rising atmosphericcarbon dioxide concentration for rangelands. Jour-nal of Range Management 50: 561–577.

Reitz R, Klein RM, Reis A 1988. Projeto Madeira doRio Grande do Sul. Porto Alegre, Herbário Bar-bosa Rodrigues. 525 p.

Silva LCR, Anand M 2011. Mechanisms of Araucaria(Atlantic) Forest Expansion into Southern BrazilianGrassland. Ecosystems 14: 1354–1371.

Silva LCR, Anand M, Oliveira JM, Pillar VD 2009. Pastcentury changes in Araucaria angustifolia (Bertol.)Kuntze water use efficiency and growth in forest andgrassland ecosystems of southern Brazil: implica-tions for forest expansion. Global Change Biology15: 2387–2396.

Streck EV, Kampf N, Dalmolin RSD, Klamt E,Nascimento PC, Schneider P et al. 2008. Solosdo Rio Grande do Sul. 2 edition. Porto Alegre,EMATER. 222 p.

Tewksbury JJ, Lloyd JD 2001. Positive interactions undernurse-plants: spatial scale, stress gradients andbenefactor size. Oecologia 127: 425–434.

Yarranton GA, Morrison RG 1974. Spatial dynamics of aprimary succession: nucleation. Journal of Ecology62: 417–428.

Zandavalli RB, Dillenburg LR, Souza PVD 2004. Growthresponses of Araucaria angustifolia (Araucariaceae)to inoculation with mycorrhizal fungus Glomusclarum. Applied Soil Ecology 25: 245–255.

Zimmer GO, Paz CP, Ganade G 2010. Effects of differentpioneer species on the colonization of Podocarpuslambertii in a restoration area. Neotropical Biologyand Conservation 5: 160–166.

10 CL Korndörfer et al.

Dow

nloa

ded

by [

Uni

vers

ity o

f G

eorg

ia]

at 0

4:19

18

Dec

embe

r 20

14