Factors controlling shrub encroachment in subtropical ...

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Received: 19 April 2017    Accepted: 8 January 2018 DOI: 10.1111/avsc.12366

Applied Vegetation Science

RESEARCH ARTICLE

Factors controlling shrub encroachment in subtropical montane systems Michele S. Dechoum1

 | Nivaldo Peroni2

1 Programa de pós graduação em Fungos, Algas e Plantas, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Trindade, Florianópolis, Brazil 2

Programa de pós graduação em Ecologia, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Florianópolis, Brazil 3

Estación Experimental de Zonas Áridas, Consejo Superior de Investigaciones Científicas (EEZA-CSIC), La Cañada, Almería, Spain Correspondence Michele S. Dechoum, Programa de pós graduação em Fungos, Algas e Plantas, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina, Trindade, Florianópolis, Brazil. Email: [email protected]

 | Francisco I. Pugnaire2,3

Abstract Aim: We aimed to assess the effects of temperature rise and neighbour removal on growth and performance of juvenile individuals of Baccharis uncinella shrubs in a montane grassland. We hypothesized that removal of neighbouring grasses and increased air temperature would enhance B. uncinella growth. Location: High-­elevation forest–grassland patches, southern Brazil. Methods: An experiment with factorial design was carried out from Aug 2014 to Sept 2015 using air temperature and neighbour removal as factors with two levels each. Air temperature was increased using acrylic open-­top chambers (OTC). For the neighbour removal treatment we removed neighbouring grasses from 30 cm around randomly selected B. uncinella juveniles. Survival, growth and plant physiological status were assessed at the end of the experiment. Results: Plants with OTCs grew more than plants without them. Neighbour removal did not have a significant effect on plant growth. These data suggest that an increase

Funding information Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Conselho Nacional de Desenvolvimento Científico e Tecnológico, Grant/Award Number: UFSC 114 A-2013

in temperature may enhance encroachment of B. uncinella in the studied grasslands,

Co-ordinating Editor: José Paruelo

wards grasslands, it is likely that montane grasslands in southern Brazil will be subject

and that neighbour grasses may act as facilitators for B. uncinella shrubs by improving water balance. Conclusions: Considering the capacity of B. uncinella to expand from forest edges toto B. uncinella encroachment within the next decades. The potential synergistic – negative – effects of global warming and habitat loss might jeopardize the high biodiversity of this ecosystem. Specific management actions and conservation public policies are needed to protect this already threatened montane system. KEYWORDS

Baccharis uncinella, climate change, community dynamics, facilitation, global warming, grassland, open-top chamber, soil moisture

1 |  INTRODUCTION

studies show that forest expansion over grasslands, savannas and prairies has occurred since the late Quaternary due to climatic factors

Woody encroachment in grasslands and other open-­canopy commu-

(rainfall and temperature) and, more recently, because of increased at-

nities has been reported throughout the world (e.g. van Auken, 2000;

mospheric CO2 and change in disturbance regimes (Bond & Midgley,

Cabral, De Miguel, Rescia, Schmitz, & Pineda, 2003; Duarte, dos

2000; Bowman, Cook, & Zoppi, 2004; Camill et al., 2003; Overbeck,

Santos, Hartz, & Pillar, 2006; Maestre et al., 2009; Roques, O’Connor,

Müller, Pillar, & Pfadenhauer, 2005). Encroachment is characterized by

& Watkinson, 2001). Paleontological data and soil carbon isotope

an increased density, cover and biomass of tree and/or shrub species

Appl Veg Sci. 2018;1–8.

wileyonlinelibrary.com/journal/avsc   © 2018 International Association for Vegetation |  1 Science

| Applied Vegetation Science

DECHOUM et al.

2      

in open-­ canopy ecosystems (van Auken, 2000). Woody encroach-

considering that climatic (rainfall) and soil conditions would not limit

ment modifies the structure and functioning of open-­canopy ecosys-

forest development in the region (Blanco et al., 2014). Vegetation dy-

tems (Eldridge et al., 2011), which may lead to irreversible ecosystem

namics are determined by the history of disturbance regimes, with

changes and jeopardize provision of ecosystem services (van Auken,

fire and grazing being the main factors favouring grassland vegetation

2009; Jackson, Banner, Jobbagy, Pockman, & Wall, 2002; Scheffer,

(Overbeck et al., 2007). In the absence of fire and grazing, grasslands

Carpenter, Foley, Folke, & Walker, 2001).

may be subject to shrub encroachment and, when in the vicinity of

The temperature increase over the last three decades has made the Earth’s surface warmer than in any preceding decade since 1850

forest, to forest expansion (Müller, Overbeck, Pfadenhauer, & Pillar, 2007; Oliveira & Pillar, 2004).

(IPCC 2013). Regionally, increasing trends in annual rainfall and warm-

Over the last decades, management actions implemented by the

ing have been recorded in southeastern South America since 1950.

local farmers aim for a reduction in grazing intensity, through cattle

By the end of the century, a mean increase of 4°C and about 15–20%

exclusion, and for fire suppression. Such interventions have reduced

increase in rainfall are forecast for this region (Magrin et al., 2014). On

the levels of disturbance and stress in these grasslands, causing

a local scale, the multiple effects of climate change will not only affect

changes in the interaction dynamics between grasses and woody spe-

communities through increased temperature, changes in water avail-

cies. Baccharis uncinella DC (Asteraceae) is a widespread and abundant

ability and increased incidence of extreme events (IPCC 2013) but also

shrub in these systems that may act as a nurse, triggering the conver-

indirectly through changes in species interactions (Adler, Dalgleish, &

sion of grasslands into forest (Blanco et al., 2014; Duarte et al., 2006;

Ellner, 2012; Anthelme, Cavieres, & Dangles, 2014; Brooker et al.,

Guido et al., 2017). B. uncinella encroachment had a significant effect

2008). Studies on how changes in biotic interactions driven by climate

on grassland communities, reducing native plant species richness, and

shifts influence the response of plants are much needed to anticipate

particularly the number of forbs (Guido et al., 2017).

its effects and implement mitigation strategies; particularly important

In this context, we aimed to assess the effects of temperature

considering the current knowledge gaps (Adler et al., 2012; Brooker

and neighbours on growth and performance of juvenile individuals of

et al., 2008).

B. uncinella shrubs in a montane grassland in southern Brazil. We hy-

In the face of climate change, the distribution range of many plant

pothesized that removal of neighbour grasses and increased air tem-

species is expected to change. Montane forest species, for instance,

perature would enhance B. uncinella growth. To our knowledge, this is

are expected to migrate up-­slope and expand their range into mon-

the first study in which the combined effects of climate change and

tane grasslands (Rehm & Feeley, 2015), increasing woody encroach-

neighbouring plant removal were assessed in tropical montane grass-

ment of these areas. However, the grassland matrix is a harsher

lands. Since B. uncinella plays an important role in vegetation dynamics

environment compared to neighbouring forests in terms of solar radi-

in the region, its responses to changes in abiotic and biotic conditions

ation and microclimate, with high frequency of frost events that limit

may provide valuable information to forecast how these systems will

establishment of woody species above the tree line (Rehm & Feeley,

be affected by climate change.

2015). Therefore, forest expansion over grasslands has been occurring gradually from the edges, sometimes facilitated by other plant species (Blanco et al., 2014; Duarte et al., 2006; Guido, Salenque, & Dresseno, 2017). Over the last two decades an increasing number of studies have

2 | METHODS 2.1 | Study system

assessed the combined effects of changes in climate (especially tem-

Our field site was in the São Joaquim National Park, a 49,300 ha pro-

perature and precipitation) and neighbours on species performance

tected area in Santa Catarina state, southern Brazil. The mountain-

in temperate grasslands and alpine plant communities (Jentsch et al.,

ous relief is undulating, at 350–1,822 m a.s.l. (Souza, 2004). Climate is

2011; Klanderud & Totland, 2005; Mariotte, Vandenberghe, Kardol,

oceanic (Cfb according to Köppen–Geiger) with precipitation ranging

Hagedorn, & Buttler, 2013; Okano & Bret-­Harte, 2015; Olsen, Töpper,

from 1,500 to 2,000 mm without a marked dry season, and mean an-

Skarpaas, Vandvik, & Klanderud, 2016; White, Carlyle, Fraser, & Cahill,

nual temperature of 16–22°C except at the highest elevations where

2012). The main interest in most of these studies was to assess the ef-

it may be as low as 10°C (Nimer, 1990). While summers (Dec–Mar)

fect of competitors on neighbours. Although grasslands are responsive

are warm, frosts can occur in winter (Jun–Sept), especially at higher

to climate change in general, there is uncertainty regarding the mag-

elevations.

nitude and direction of such responses, which can be highly variable

The park is in the Atlantic Forest biome (IBGE 2012), and the land-

depending on treatment, site and species identity (White et al., 2012).

scape is composed of a mosaic of remnants of mixed ombrophilous

In high-­elevation systems of south and southeast Brazil the land-

forest (Araucaria forest), subtropical cloud forest and montane grass-

scape is composed of a forest–grassland mosaic (Garcia, Longhi-­

lands. Our study site (27°52′S, 49°19′W, 1,600 m a.s.l.) is a grassland

Wagner, Pirani, & Meirelles, 2009; Overbeck et al., 2007). Montane

on the forest–grassland boundary, with the shrubby layer dominated

grasslands, known as ‘campos de altitude’, are considered relicts of

by B. uncinella.

drier and colder, post-­glacial climates that preceded present-­day sys-

Baccharis uncinella is a woody, perennial shrub that occurs in for-

tems (Behling, 2002; Behling, Pillar, Orlóci, & Bauermann, 2004). Both

est edges and secondary Araucaria forests in the highlands of south

vegetation types can be considered as alternative vegetation states,

and southeastern Brazil (Barroso & Bueno, 2002). It is a pioneer

      3 Applied Vegetation Science |

DECHOUM et al.

species that can reach up to 4 m, with sessile leaves, 6–15-­mm

branch were selected and individually weighed, then placed in paper

long and 4–6-­mm wide (Barroso & Bueno, 2002). It dominates areas

bags and dried at 72°C for 48 hr to obtain leaf dry mass. LDMC of each

known locally as “vassourais” (dense groups of shrubs and small

plant was calculated as dry mass divided by fresh mass. Three extra

trees) and grasslands near forests, and tends to occupy grasslands,

leaves were removed from each branch, scanned at 300 dpi, and the

enabling the expansion of forests (Duarte et al., 2006; Oliveira &

projected area of each leaf was measured to calculate leaf area using

Pillar, 2004).

the software Midebmp v 4.2 (EEZA, Almeria, Spain). Each leaf was then weighed after drying at 72°C for 48 hr. SLA was computed as the ratio

2.2 | Experimental design and data collection A factorial experiment was carried out between Aug 2014 and Sept 2015. Forty young plants of B. uncinella (25–50 cm in height) occur-

between leaf area and leaf dry mass for each individual plant.

2.3 | Data analysis

ring in a grassland, up to 100 m from a forest edge, were selected as

Air temperature, and soil moisture and temperature, were compared

targets. Half of them were randomly assigned to be enclosed in acrylic

among treatments separately through two-­way ANOVA, with OTC

open-­top chambers (OTCs), which can increase air temperature by

(presence or absence), neighbour (presence or removal) and the inter-

2–5°C when properly set in open systems (Owensby, Auen, & Coyne,

action between them considered as fixed effects. Tukey’s test was ap-

1994). The OTCs were 34 cm in height, 58 cm in bottom diameter

plied a posteriori (95% CI) when the interaction between temperature

and 23 cm at the top, and were positioned 10 cm above the ground

and neighbour was significant to verify which treatments were differ-

to avoid overheating. These two groups will be called ambient tem-

ent. Welch’s t-test was used to compare mean values of PAR with and

perature (T−) and elevated temperature (T+). Furthermore, ten plants

without OTC. Growth, BLI, Fv/Fm, LDMC and SLA were analysed with

in each group were assigned to neighbour removal (C−), in which all

two-­way ANOVA followed by Tukey tests. Model validations were

shoots of neighbouring grasses in a 30-­cm radius around each plant

based on graphical analysis of residuals (for normality and homogeneity

were clipped at ground level; neighbour grasses of the remaining

of variances). Normality distribution and homogeneity of variances for

plants were left intact (C+). Neighbour grasses were removed once at

the parametric correlation tests were tested prior to analysis. Survival

the beginning of the experiment.

functions were estimated for each treatment using the Kaplan–Meyer

Soil moisture and temperature were characterized in one repli-

method for censored data, and the Mantel–Haenszel test was used

cate of each of the four treatments using sensors (5TM Soil Moisture

to test for differences in survival between treatments. Pearson

and Temperature Sensor) attached to EM50 data loggers (Decagon

correlation tests were performed between growth, BLI, Fv/Fm,

Devices, Pullman, WA, USA), from 15 Jul to 3 Aug 2015. Sensors were

LDMC and SLA and the environmental variables (mean day and night

installed 10–15 cm below the ground. Photosynthetic active radiation

air temperature; mean day and night soil moisture; mean day and night

was recorded with QSO-­S sensors (Skye Instruments, Llandrindod

soil temperature) and between the environmental variables. All statis-

Wells, UK) inside and outside one randomly selected OTC. Air tem-

tical analyses and figures were done with R v 3.0.3 (R Foundation for

perature was recorded with iButton data loggers (Maxim Integrated,

Statistical Computing, Vienna, Austria), using the survival’ package for

San Jose, CA, USA), each placed next to a B. uncinella plant, from

survival analysis and the ‘sciplot’ package for figures.

10 Jun to 6 Aug 2015. iButtons were installed 25–30 cm above the ground. Growth was estimated in each B. uncinella individual by height dif-

3 | RESULTS

ference between the start and end of the experiment, 400 days later. The initial average heights (± SD) of plants measured were 41.3 ± 7.6

Both factors tested (OTC and neighbour), as well as the interac-

(T− C+), 41.0 ± 6.6 (T− C−), 41.2 ± 6.3 (T+ C+) and 40.3 ± 4.7 cm

tion between them, were relevant for soil moisture and tempera-

(T+ C−). Branch length increment (BLI) over the last growth season

ture, and for air temperature (Table 1). Soil moisture was higher in

(i.e. summer, Dec–Mar) was estimated for each plant by measuring

the control treatment (T−C+) and lower when neighbour grasses

with calipers the length of the distal part of four randomly selected

were removed (T−C−; Figure 1a). However, OTC must have com-

branches, which were whitish and more hairy than older branch parts

pensated for the effect of neighbour removal on the reduction of

(‘new growth’). Branch length was averaged to assess mean annual in-

soil moisture, considering that soil moisture did not differ between

crement per plant.

treatments T+C+ and T+C− (Figure 1a). Soil temperature was lower

Plant physiological status was assessed at the end of the experiment by measuring the photochemical efficiency of photosystem II

in control (T−C+) and did not differ among the other three treatments (Figure 1b).

(Fv/Fm), specific leaf area (SLA) and leaf dry matter content (LDMC).

There was a considerable variation in mean temperature, which

Fv/Fm was measured in the morning on one young, fully developed,

was as high as 31.8 ± 0.6°C during the day and as low as −5.6 ± 0.11°C

healthy leaf per plant after 20 min dark adaptation using a PEA flu-

at night. As expected, OTCs (T+C− and T+C+) increased mean air tem-

orimeter (Hansatec, King’s Lynn, UK). For LDMC calculations, one

perature by about 8% (Figure 1c). The highest air temperatures were

branch was collected per plant, wrapped in aluminium foil, kept in a

recorded when OTCs were present and neighbours had not been

dark, cool box and taken to the lab. Six intact, fresh leaves from each

removed (treatment T+C+; Figure 1c). When OTCs were absent, air

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DECHOUM et al.

4      

T A B L E   1   Results of two-­way ANOVA for soil moisture, soil temperature and air temperature in four experimental conditions at the study area in the São Joaquim National Park, Santa Catarina, Brazil. The factors included in each model were: air temperature (Temp), neighbour grasses (Neigh) and the interaction between them (Temp x Neigh). Significant values of p are in bold Soil moisture Fixed effects

F

Soil temperature p

F

Air temperature p

F

p

144.8