understory invasion by acacia longifolia alters the water ...€¦ · tem structure and function...

Understory Invasion by Acacialongifolia Alters the Water Balance

and Carbon Gain of a MediterraneanPine Forest

Katherine G. Rascher,1* Andre Große-Stoltenberg,2 Cristina Maguas,3

and Christiane Werner1

1Experimental and Systems Ecology, University of Bielefeld, Universitatstr. 25, 33615 Bielefeld, Germany; 2Institute of LandscapeEcology, University of Munster, Munster, Germany; 3Centre for Environmental Biology (CBA), University of Lisbon, Lisbon, Portugal

ABSTRACT

In water-limited ecosystems, where potential

evapotranspiration exceeds precipitation, it is of-

ten assumed that plant invasions will not increase

total ecosystem water use, because all available

water is evaporated or transpired regardless of

vegetation type. However, invasion by exotic

species, with high water use rates, may potentially

alter ecosystem water balance by reducing water

available to native species, which may in turn

impact carbon assimilation and productivity of co-

occurring species. Here, we document the impact

of invasion by an understory exotic woody species

(Acacia longifolia) in a semi-arid Mediterranean

dune pine forest. To quantify the effects of this

understory leguminous tree on the water use and

carbon fixation rates of Pinus pinaster we compare

an invaded and a non-invaded stand. A. longifolia

significantly altered forest structure by increasing

plant density and leaf area index in the mid-stratum

of the invaded forest. A. longifolia contributed sig-

nificantly to transpiration in the invaded forest (up

to 42%) resulting in a slight increase in stand tran-

spiration in the invaded relative to non-invaded

forest. More importantly, both water use and carbon

assimilation rates of P. pinaster were significantly

reduced in the invaded relative to non-invaded

stand. Therefore, this study shows that exotic plant

invasions can have significant impacts on hydro-

logical and carbon cycling even in water-limited

semi-arid ecosystems through a repartitioning of

water resources between the native and the invasive

species.

Key words: competition; delta 13-C; ecohydrol-

ogy; invasion ecology; Mediterranean; nitrogen;

Pinus pinaster; sap flux; transpiration; water cycle.

INTRODUCTION

Due to the interdependence between water cycling

and the structural and functional attributes of

biological communities, vegetation plays a major

role in shaping the terrestrial water balance (Vert-

essy and others 2001; Ewers and others 2002, 2005;

Moore and others 2004; Newman and others 2006;

Wilcox and Thurow 2006; Kagawa and others

Received 18 January 2011; accepted 11 May 2011

Author Contributions: KGR, CW, and CM conceived of and designed

the study. KGR and AGS performed research. KGR analyzed data. KGR

wrote the paper with assistance from CW.

*Corresponding author; e-mail: [email protected]

EcosystemsDOI: 10.1007/s10021-011-9453-7

� 2011 Springer Science+Business Media, LLC

2009). However, predicting the impact of vegeta-

tion change on the hydrologic cycle is not

straightforward, due to complex interactions and

feedbacks between the vegetation functioning (for

example, ecological strategy, water use efficiency,

phenology) and the abiotic characteristics of eco-

systems (for example, precipitation regime,

groundwater depth). Furthermore, in arid and

semi-arid ecosystems, vegetation cover often has

little impact on total evapotranspiration because

the available water is fully evaporated or transpired

regardless of vegetation type (Huxman and others

2005; Wilcox and others 2006; Brauman and oth-

ers 2007). Specifically, in Mediterranean climates,

the presence of woody shrubs in grasslands has

been shown to effect ecosystem water storage only

during winter when precipitation exceeds potential

evapotranspiration (Huxman and others 2005).

Woody invasive plants have the potential to

seriously disrupt water and nutrient cycling. Many

exotic woody invasives are fast-growing plants

with high transpiration rates which can lead to

decreased water storage (for example, streamflow,

groundwater recharge) in invaded communities

(Brauman and others 2007). Furthermore, in arid

ecosystems, native species are adapted to water-

limited conditions (either through dry season

senescence or efficient control of water loss, for

example, Werner and others 1999) whereas

invaders may lack those traits, thus leading to

greater water use in invaded relative to non-

invaded habitat (Fritzsche and others 2006; Brau-

man and others 2007). Phenology of invaders may

also be out of phase with the native species,

potentially resulting in the extraction of soil water

and nutrients at different times than native species

(Prater and DeLucia 2006).

Although there have been many studies of

woody exotic plant invasions in semi-arid riparian

zones (for example, Calder and Dye 2001; Shafroth

and others 2005; Cleverly and others 2006; Wilcox

and Thurow 2006) studies of woody exotic plant

invasions in non-riparian semi-arid systems are

lacking (but see Calder and Dye 2001). In addition,

the impact of plant invasions on water cycling has

typically been studied at the leaf-level and com-

parisons between invasive and native species at the

stand-level are scarce (Cavaleri and Sack 2010).

Invasive species do not always out-compete native

species to dominate ecosystems. In fact, they often

co-exist in the understory or as mixed stands

(Cleverly and others 2006; Rascher and others

2011). In fact, there is little evidence that plant

invasions have caused plant extinctions at the

population level (Sax and Gaines 2008); however,

invasion by species with novel life-forms like trees

in tree-less habitats can substantially alter ecosys-

tem structure and function (Jaeger and others

2009: Rascher and others 2011). To our knowledge,

the hydrologic impact of an understory invader in a

semi-arid Mediterranean forest has yet to be

examined. Furthermore, impacts of plant invasions

on the hydrologic cycle will also affect carbon

assimilation and wood production because water

availability determines growth rates, vegetation

structure, and light interception as well as playing a

role in determining photosynthetic efficiency

(Ryan and others 2010).

In this study, we investigated the impact of an

exotic understory invasive tree, Acacia longifolia, on

the ecosystem water balance and carbon fixation

rates of a Mediterranean dune Pinus pinaster forest.

A. longifolia is native to relatively mesic habitats

with annual rainfall between 800 and 1600 mm

(Benson and McDougall 1996) in Australia and is a

typical tree in the understory of forests (Neave and

Norton 1998), especially in coastal sand dune eco-

systems (Ross and others 2004). Previous studies

have shown that A. longifolia is a strong competitor

with Portuguese dune species under a range of

water availabilities (Peperkorn and others 2005;

Werner and others 2010). On the other hand, the

atmospheric N2 fixed by A. longifolia is available to

and can have a facilitative effect on neighboring

native species (Hellmann and others 2011). Rec-

ognizing that interactions between abiotic site

attributes (for example, temperature and precipi-

tation regimes) and functional characteristics of the

vegetation (phenology, photosynthetic regulation,

water use efficiency) interact, our study encom-

passed all four seasons to determine the impact of

A. longifolia invasion on the hydrologic and carbon

cycles. We hypothesized that A. longifolia would

have a negative competitive effect on the water

status of co-occurring P. pinaster. However, we also

expected that the competitive strength of A. longi-

folia on P. pinaster would vary depending on

environmental conditions (for example, water

availability).

MATERIALS AND METHODS

Site Description

The study was conducted in a Pinus pinaster planta-

tion forest in Pinheiro da Cruz, Portugal (38�15¢ N,

8�46¢ W) approximately 70 km south of Lisbon. The

plantation forest contained approximately 35-year-

old P. pinaster trees growing in sandy soils (orthic

podzols) with an average height of 12.6 m ± 2.2

K. G. Rascher and others

(mean ± SD) and diameter at 1.4 m of 25.2 cm ±

5.8. The invasive A. longifolia forms a dense under-

story population (8706 individuals ha-1) with an

average tree height of 3.2 m ± 1.3 and diameter at

ground level of 3.1 cm ± 1.8. The study area

encompassed a 1000 m2 area (50 m 9 24 m) of the

plantation (half heavily invaded by A. longifolia and

half largely non-invaded—a 50 9 4 m2 wide fire-

break through the middle of the plot was excluded

from measurement). This ensured that the study

area was small enough to guarantee a uniform

site history (for example, disturbance from logging

and the same planting history) and homogenous

microclimate conditions. Furthermore, this fire-

break may have served to slow the progression of

A. longifolia population expansion; however, iso-

lated A. longifolia saplings were found in the ‘‘non-

invaded’’ forest indicating that the invasion is likely

to expand in the near future. For further site details

see Rascher and others (2010, 2011).

Climate

Microclimate parameters were measured either in

the forest or in an open area adjacent to the field

site. Microclimate data were collected from October

1, 2007 to August 15, 2008. Sensors were read

every 60 s and 15 or 60 min averages stored in data

loggers (CR1000, CR10X, Campbell Scientific,

Utah, USA). In the forest, air temperature and

relative humidity (CS-215, Campbell Scientific),

soil temperature (T107, Campbell Scientific) and

soil moisture were monitored. Soil moisture (vol-

umetric water content, VWC) was measured at 10–

20-, 20–30-, 30–40-, and 40–50-cm depths using

ECH2O EC-10 probes (Decagon, USA) with a cali-

bration equation specific to the site. VWC was

monitored in the invaded (2 sensors per depth),

non-invaded forest (2 sensors per depth), and open

sand (1 sensor per depth). Leaf to air vapor pressure

deficit (VPD) was calculated from temperature and

relative humidity data using the Goff-Gratch for-

mula. In an open area adjacent to the field site,

photosynthetic photon flux density (LI-190SB, LI-

COR, Nebraska, USA) and rainfall (ARG100 tipping

bucket rain gauge, Campbell Scientific) were

measured.

Sap Flow Measurements

Sap flow was monitored from October 1, 2007 to

July 31, 2008 in P. pinaster and A. longifolia trees

using Granier’s constant heat method (1985). Due

to power supply failure data are missing from

December 18 to 22, 2007 and January 5 to 11,

2008. Sensor pairs (UP-GmbH, Germany) were

installed at breast height in P. pinaster and between

0.3 and 1 m for A. longifolia (below the first live

branch). Sensors were read every 60 s and data

stored as 15-min means in a data logger (CR1000 &

AM16/32 multiplexers, Campbell Scientific). Five

invaded P. pinaster, five non-invaded P. pinaster,

and ten A. longifolia individuals were equipped for

sapflow. The diameter at breast height of P. pinaster

trees equipped for sapflow ranged from 18.3 to

26.4 cm in the non-invaded forest and 18.8 to

27.4 cm in the invaded forest. The A. longifolia used

for sapflow measurements ranged in diameter from

5.4 to 11.2 cm at sensor height. To avoid artifacts

introduced when individual sensors failed, data

were gap filled using linear relationships developed

when all sensors were functioning.

Sap flow terminology follows Edwards and others

(1997). Sap flux density, t (m3 m-2 15 min-1),

was calculated from the temperature difference

between the up- and the down-stream thermo-

couple every 15 min using the empirical relation-

ship developed by Granier (1985):

t ¼ 7:14k1:231 � 15

where

k ¼ dTMax

dT

� �� 1

and dTMax is the maximum daily temperature dif-

ference between the up- and the down-stream

thermocouples and dT is the current temperature

difference. Sapwood area-related sap flux density,

QS, is reported as daily values (m3 m-2 d-1) which

were calculated by summing t from 9:00 to 21:00.

To account for variation in sapflow with depth in

the xylem of P. pinaster three pairs of different

length sensors were installed covering 0–2-, 2–4-,

and 4–6-cm depths. For A. longifolia, sap flow was

measured in the outer 2 cm of xylem, and cir-

cumferential variability was accounted for by

installing two sensor pairs (in north and south

facing sides of the tree) and the mean of the two

sensor sets was used. All trees were insulated with

plastic bubble wrap and covered with a reflective

white plastic to minimize temperature gradients

caused by sunlight.

Sap Flow Scaling

Tree cores were taken at breast height in 21

P. pinaster trees growing just outside the study site.

Estimates of sapwood depth were made after the

cores were dried (heartwood distinguished by its

dark, reddish color: Delzon and others 2004; Pinto

Acacia Invasion Alters Ecosystem Functioning

and others 2004). The relationship between sap-

wood depth and tree radius at breast height was

determined and used to estimate depth of sapwood

and the sapwood area covered by each of the three

different length sap flow sensors. In cases in which

a tree had sapwood deeper than 6 cm the sap flux

density measured in the inner most xylem ring

(4–6 cm) was applied to all sapwood deeper than

6 cm.

Sapwood area per ground area was determined

by calculating tree radius from measurements of

circumference at breast height of all P. pinaster

individuals in the study site and applying the

relationship between sapwood depth and radius

to determine the sapwood area to ground area

ratio (AS:AG; m2 sapwood m-2 stand ground area)

separately for the invaded and the non-invaded

P. pinaster stands. For A. longifolia the diameter at

ground level was measured for all individuals in a

170 m2 subarea of the invaded forest and AS:AG

was calculated analogously assuming that sap-

wood was 2-cm deep for all Acacia trees. Studies

in other Acacia species have indicated a mean

sapwood depth of 25 mm (A. dealbata: Hunt and

Beadle 1998). Even if the true sapwood area

extended deeper than 2 cm only a small under-

estimate of stand level sap flux rates would occur

because 79% of the A. longifolia trees growing in

the stand had radii less than or equal to 2 cm.

Stand transpiration on a ground area basis

(m3 m-2 d-1) was calculated by multiplying daily

average QS by the corresponding AS:AG.

Determination of Vegetation Structure

The 1000 m2 study area was divided into 100

subplots (2 m 9 5 m = 10 m2) and vegetation

structure was characterized systematically in every

third subplot in fall 2007. Vegetation was subdi-

vided into two height strata: (1) adult plants taller

than 1.5 m, and (2) plants shorter than 1.5 m

(encompassing adult shrubs and juveniles of woody

species). Height to the nearest 0.5 m was measured

for plants taller than 1.5 m and plants shorter than

1.5 m were classified into height classes: 0–10, 11–

25, 26–50, 51–100, and 101–150 cm. Crown

diameter was calculated as the arithmetic mean of

the north–south and east–west diameters (mea-

sured to the nearest 5 cm). Canopy cover was then

calculated as the sum of the projected crown area

(calculated from crown diameter). More details

regarding vegetation structure can be found in

Rascher and others (2011).

Hemispherical Photographs and LeafArea Index Measurements

Hemispherical photographs (at three exposures:

-1.3, 0, and 1.3) were taken at dusk or dawn in the

center of each subplot used for vegetation structure

measurements using a Nikon Coolpix 950 camera

and a Nikon FC-E8 fish-eye lens. Photographs were

taken at the end of September 2007. Leaf area

index (LAI), transmitted gap light, and canopy

openness were calculated from the photograph

with the best contrast using Gap Light Analyzer 2.0

software (Frazer and others 1999).

Foliar Carbon, Nitrogen, and XylemWater Potential

Young, fully expanded, sun exposed foliage was

collected seasonally (fall: September 23, 2007;

winter: January 13, 2008; spring: May 7, 2008;

summer: August 7, 2008), oven-dried at 65�C for

48 h and ground into a fine powder with a ball mill

(Retsch, Haan, Germany) for analyses of nitrogen

content and carbon isotope ratios (d13C). Samples

(n = 3–5 non-invaded P. pinaster; n = 3–6 invaded

P. pinaster; n = 10 A. longifolia) were combusted in

an elemental analyzer (EuroEA, HEKAtech GmbH,

Wegberg, Germany) and analyzed in a continuous-

flow isotope ratio mass spectrometer (IRMS, Iso-

prime; GV, Manchester, UK) against IAEA-CH-4

and IAEA-CH-6 standards (International Atomic

Energy Agency, Vienna, Austria). Carbon isotope

ratios are reported in d-notation relative to Vienna

Pee Dee Belemnite (VPDB), and the precision of

repeated measurements was 0.1&. Predawn and

midday xylem water potential were measured

on sun-exposed foliage (n = 1–5 non-invaded

P. pinaster; n = 2–6 invaded P. pinaster; n = 3–10

A. longifolia) in winter (January 13, 2008), spring

(May 7, 2008), and summer (August 7, 2008).

Phloem Sap Sampling and Extraction

Phloem sap was collected from A. longifolia and

P. pinaster in the invaded and the non-invaded

stands on 12 days in May and 5 days in August

2008 (for sampling dates see Rascher and others

2010). Phloem sap was extracted using the bark

exudation technique (for example, Gessler and

others 2004) which has been demonstrated as a

sound method for determining d13C in numerous

species including P. pinaster (Devaux and others

2009). Pieces of bark (1 to 3 cm2) were removed

from trunks using a cork-borer or scalpel. Bark was

rinsed with double demineralized water and placed


in 6-ml vials (Exetainer, UK) containing 2-ml

double demineralized water, and left for 5 h at

room temperature after which time they were

frozen. After thawing to room temperature in the

lab, phloem exudates were transferred to tin cap-

sules, placed in an oven at 70�C to evaporate the

liquid (conducted in two steps of 250 ll for a total

of 500 ll), after which the tin capsules were cru-

shed and analyzed for d13C as described previously

for foliage.

Modeling Canopy Carbon AssimilationRate

We modeled canopy carbon assimilation rate (Acan)

for A. longifolia and P. pinaster in the invaded and

the non-invaded forest. Full details of the modeling

approach can be found in Rascher and others

(2010). d13C signatures of phloem sap collected in

the trunk integrate carbon fixed in the entire can-

opy and can therefore be used as an integrative

proxy for changing canopy carbon isotope dis-

crimination (D13C). D13C recorded in the phloem

sap in May and August 2008 (spanning the wettest

and driest time periods) was related to changes in

VPD and soil VWC using linear models. Models

combining 4-day lagged VPD with same day soil

VWC had the best predictive power (see Rascher

and others 2010 for modeling details). These

models (Table 1) were then used to simulate D13C

on a daily basis from changes in VPD and soil VWC

throughout the entire study. Finally, canopy car-

bon assimilation rates (Acan) were estimated by

applying Fick’s law to combine canopy stomatal

conductance (GS), determined from QS using a

modified Penman–Monteith equation (Oren and

others 2001), with the ratio of leaf internal to

external CO2 concentration (ci/ca), determined

from the simulated D13C using the Farquhar two-

stage discrimination model for C3 species (Farquhar

and others 1982).

Statistical Analyses

Comparisons of leaf area index, canopy openness,

and transmitted light between the invaded and the

non-invaded stands were made using t tests. One-

way ANOVA followed by Tukey’s HSD test was

used to test for seasonal differences in foliar d13C,

N-content and leaf water potential within a species

and stand. Repeated measures ANOVA using linear

mixed effects models (package nlme in R) was used

to compare sapflow on a sapwood area basis (QS)

for invaded and non-invaded P. pinaster stands on

clear days (legend of Table 3 details which days

were removed). The five trees in each stand were

treated as replicates and the effects of day of study

(DOS), invasion status, season, and the invasion

status * season interaction were tested. Within

each season, one-way ANOVA was used to test for

differences in stand transpiration and canopy car-

bon assimilation rates (Acan) between the two

P. pinaster stands on clear days. Two-way ANOVA

(season and invasion status) was used to compare

total stand transpiration between the invaded for-

est (P. pinaster + A. longifolia) and the non-invaded

forest over the entire study. All analyses were

conducted in R v. 2.6.2 (R Development Core

Team 2008).

RESULTS

Climate

The site has a typical Mediterranean climate with

cool, wet winters and hot, dry summers (Figure 1).

VPD varied throughout the study with moderate

values in winter (<1.5 kPa) and maximum midday

values (up to 4 kPa) during the fall, spring, and

summer (Figure 1B). Due to the poor water

retention capacity of the highly porous sandy soils,

and the variability in frequency and magnitude of

precipitation events (Figure 1E), soil volumetric

water content (VWC) was highly variable with

peaks after rainfall events quickly diminishing to

relatively low levels (<5% in fall, spring, and

summer and <10% in winter) (Figure 1D).

A. longifolia Alterations to ForestStructure

Presence of A. longifolia altered the forest structure

predominantly by increasing plant density in the

Table 1. Model Parameters Used to EstimateCanopy D13C from 4-Day Lagged VPD and SameDay VWC from October 2007 to July 2008

Non-invaded Invaded

P. pinaster P. pinaster A. longifolia

b1 18.92 20.62 20.65

b2 -1.12 -1.67 -2.44

b3 0.001 -0.27 -0.18

b4 0.15 0.23 0.20

RMSEP 0.39 0.42 0.64

Models are of the form: D13C = b1 + b2 * VPD + b3 * VWC + b4 * VPD *VWC. Also given are estimates of model error, the root mean squared error ofprediction, RMSEP, calculated using the PRESS procedure (Kutner and others2004).


lower and mid-canopy (Figure 2). A. longifolia

contributed significantly to canopy cover in the

invaded forest (Figure 3A), resulting in signifi-

cantly greater leaf area index (LAI) (P < 0.01),

lower canopy openness (P < 0.01), and decreased

transmitted light (P < 0.01) in the invaded com-

pared to the non-invaded forest (Table 2; Figure 3).

Structure of the herbaceous understory was similar

between the invaded and the non-invaded stands

and P. pinaster dominated the upper canopy of both

stands, reaching 18 m in the non-invaded and

15 m in the invaded forest (Figure 2). P. pinaster

tree height and diameter at breast height (DBH)

tended to be greater in the non-invaded than the

invaded stand but the difference was only signifi-

cant for height (t34: P < 0.001 for height, P = 0.11

for DBH; Table 2). Accordingly, the basal area to

ground area ratio (AB:AG) of Pinus was greater in

the non-invaded than the invaded stand (Table 2).

Functional Differences Betweenthe Native and Invasive Species

P. pinaster and A. longifolia differed not only struc-

turally but also functionally. Significant seasonal

changes in foliar carbon isotope signatures were

found in A. longifolia, highlighting that the invader

was more plastic in responding to changes in envi-

ronmental conditions than P. pinaster (Figure 4A).

For A. longifolia, high carbon isotope discrimination

against 13C occurred during winter when water was

abundant (Figure 1) and xylem water potentials

(WPREDAWN and WMIDDAY) were highest (Figure 4C,

D). Discrimination against 13C was lowest during

the dry summer (Figure 1) when WPREDAWN

and WMIDDAY were also significantly reduced

(Figure 4C, D). In comparison, P. pinaster foliar d13C

did not vary by season (Figure 4A) although

WPREDAWN and WMIDDAY did decrease significantly

Figure 1. Microclimate at

Pinheiro da Cruz,

Portugal from October 1,

2007 to August 15, 2008.

A average midday air and

soil temperatures, B

average midday leaf to air

vapor pressure deficit, C

average midday

photosynthetic photon

flux density, D daily

average soil volumetric

water content from 10- to

50-cm depth for the non-

invaded forest, the

invaded forest, and the

open sand, and E rainfall.

Midday averages are

computed from data

collected between 10:00

and 14:00. Arrows in

panel D indicate time

periods of detailed soil dry

down analyses (see

Figure 5).


during the summer drought period (Figure 4C, D).

Foliar N was seasonally variable in P. pinaster,

whereas A. longifolia had relatively constant and

comparatively high (>2.0 %) foliar N throughout

the study (Figure 4B). Foliar nitrogen content for

P. pinaster tended to be greater during winter and

spring compared to fall and summer (Figure 4C, D).

Comparing the two stands of P. pinaster, there was a

tendency for greater foliar N, more depleted d13C

signatures and lower WPREDAWN and WMIDDAY in the

invaded stand although the differences were non-

significant, which may be at least partially due

to small sample sizes (P > 0.05 in every season;

Figure 4). Nevertheless, this trend may indicate a

small facilitative effect of A. longifolia N2-fixation on

co-occurring P. pinaster.

A. longifolia Effects on Soil MoistureDynamics

A. longifolia invasion induced changes in vegetation

structure were also related to altered soil infiltration

and dry down dynamics (Figures 1D, 5). The

invaded forest exhibited the largest peaks in soil vol-

umetric water content (15–20% VWC) followed by

the non-invaded forest (7–15%) and the open sand

(4–15%). Although the presence of A. longifolia was

associated with increased precipitation interception

and higher VWC immediately following rainfall

events, soil dried out more rapidly in the invaded

compared to non-invaded stand (Figure 5B–D),

although at the beginning of fall, dry down was

similar between the two plots (Figure 5A).

Invasion Impacts on SapwoodArea-Based Transpiration (QS)

The faster use of soil water in the invaded stand

(Figure 5) corresponded with a higher sap flow rate

per sapwood area (QS) of the invasive A. longifolia

compared to the native P. pinaster (Figure 6A). In

both species, the seasonal trend in water availability

(Figure 1D) was also reflected in QS (Figure 6A).

The highest water flux occurred during spring when

Figure 2. Distribution of

plant height in the A

non-invaded and B

invaded stand. Shown are

the distributions for

P. pinaster, A. longifolia

and the herbaceous

understory. Herbaceous

species include: Calluna

vulgaris, Corema album,

Daphne gnidium, Erica

australis, Erica scoparia,

Erica umbellata, Halimium

commutatum, Juniperus

navicularis, Lithodora

prostrata, Osyris

quadripartita, Rosmarinus

officinalis, Santolina

impressa, Thymus sp., Ulex

jussiaei.


Figure 3. Depiction of how the presence of A. longifolia affects forest structure and light climate within the 1000 m2 study

area (50 m 9 24 m including a 4-m wide firebreak between the invaded and non-invaded stands). A A. longifolia canopy

cover (%), B transmitted gap light (%), C canopy openness (%), and D leaf area index (LAI). Panels B–D are calculated

from hemispherical photographs. Measurements of A. longifolia canopy cover and hemispherical photographs were taken

at 34 locations on a systematic grid within the forest (see Rascher and others 2011 for more details on sampling design).

For depiction, data were interpolated between measurement points using the linear interpolation algorithm within the

contour plot function of SigmaPlot v.10.0.

Table 2. Stand Characteristics at Pinheiro da Cruz, Portugal (38�15¢ N, 8�46¢ W)

Non-invaded Invaded

P. pinaster P. pinaster A. longifolia

Tree height (m) 13.7 ± 1.8 11.4 ± 1.9 3.2 ± 1.3

Trunk diameter* (cm) 26.7 ± 5.5 23.5 ± 5.9 3.1 ± 1.8

Basal area/ground area (AB:AG) (cm2 m-2) 27.67 26.08 6.86

Sapwood/basal area (AS:AB) (cm2 cm-2) 0.85 0.85 0.91

Sapwood/ground area (AS:AG) (cm2 m-2) 23.55 22.17 6.21

Non-invaded Invaded

Leaf area index 0.86 ± 0.04a 1.13 ± 0.08b

Canopy openness (%) 40.32 ± 1.07a 32.94 ± 1.84b

Transmitted light (%) 53.34 ± 2.49a 42.93 ± 2.53b

Data are means ± SD for the tree height and diameter. Data are means ± SE (n = 17) for the leaf area index, canopy openness, and transmitted light (calculated using GLA2.0 from hemispherical photographs). Different letters within rows indicate a significant difference between the invaded and non-invaded forest (Student’s t test; P < 0.05).* P. pinaster diameter at breast height, A. longifolia diameter at ground level.


conditions were favorable for photosynthesis and

the lowest rates occurred during winter when both

low PPFD and temperature presumably limited

photosynthetic activity (Figure 1). Over the course

of the study, QS differed significantly depending on

day of study (DOS) and season (Table 3a).

Furthermore, the difference in transpiration rate

between P. pinaster growing alone and in competi-

tion with A. longifolia varied depending on season

(significant invasion status * season interaction;

Table 3a).

Within each season QS varied significantly by

DOS, highlighting that transpiration rates faithfully

tracked the day to day variability in abiotic condi-

tions (for example, PPFD, VPD, temperature). Fur-

thermore, in fall (P < 0.05), winter (P < 0.1), and

summer (P < 0.05) there was a significant interac-

tion between DOS and invasion status reflecting that

Figure 4. A Foliar

d13C, B foliar nitrogen

concentration, C

predawn xylem water

potential (WPREDAWN),

and D midday xylem

water potential

(WMIDDAY) for

A. longifolia and

P. pinaster in the

invaded and non-

invaded forest.

Different letters indicate

significant difference

between the seasons

within a species and

invasion status.

Sampling dates: fall:

September 23, 2007;

winter: January 13,

2008; spring: May 7,

2008; and summer:

August 7, 2008.

Figure 5. Curves illustrating the drying of the upper soil (10–50-cm depth) in the invaded and non-invaded forest after a

representative rainfall event in each season. Data were normalized by dividing by the maximum VWC occurring on the

day of the rainfall. Rainfall events: A fall: September 30, 2007; B winter: February 4, 2008; C early spring: March 19, 2008;

D late spring: May 29, 2008. The rainfall on May 29, 2008 was the last rainfall before the summer drought began.


the difference in transpiration between the

two P. pinaster stands varied substantially within

most seasons (Table 3b). This interaction occurred

because immediately after rainfall, when water was

abundant, the difference between the two P. pinaster

stands was large but as water availability decreased

the differences in QS between the two stands also

diminished (Figure 6A). In contrast, in spring when

rainfall events were frequent (Figure 1E) and water

was relatively abundant there was no significant

difference in water use between the two pine stands

on a sapwood area basis.

Figure 6. A Sapwood area-related sap flow (QS: m3 m-2 sapwood d-1) and B stand transpiration on a ground area basis

(mm d-1) for the non-invaded and the invaded P. pinaster stands and the A. longifolia understory from October 1, 2007 to

July 31, 2008. Error bars for QS represent 1 SE (n = 5 for Pine and 10 for Acacia) and are shown every fifth day for clarity.

Data are missing due to power supply failure from December 18 to 22, 2007 and January 5 to 11, 2008. Seasons are as

follows: fall: October 1, 2007 to November 17, 2007; winter: November 18, 2007 to February 29, 2008; spring: March 1,

2008 to May 31, 2008; summer: June 1, 2008 to July 31, 2008.


Invasion Impacts on Stand LevelTranspiration

However, when the differences in stand structure

(for example, AB:AG and AS:AG) between the two

pine stands were taken into account, an even

stronger negative effect of competition with

A. longifolia was seen (Figures 6B, 7). In fall, win-

ter, and spring stand transpiration was significantly

greater in the non-invaded compared to the

invaded P. pinaster stand (P < 0.001). In summer,

the difference between the P. pinaster stands was

marginally significant (P = 0.05) reflecting that by

July, when soil water was severely limiting (Fig-

ure 1D), there were very similar rates between

both P. pinaster stands and the presence of A. lon-

gifolia had little effect on P. pinaster water use.

Averaged over the entire study, P. pinaster tran-

spiration was 0.70 mm d-1 in the invaded and

0.93 mm d-1 in the non-invaded stand, a reduc-

tion of 25%. This substantial difference between

the two stands results from the fact that stand

transpiration combines QS, which tended to be

greater in the non-invaded P. pinaster forest

(Figure 6A), and stand basal area which was also

greater for the non-invaded P. pinaster forest

(Table 2). Furthermore, the largest difference in

stand transpiration between the P. pinaster stands

corresponded with the time periods where the

largest differences in QS were seen (the beginning

of the fall and summer seasons; Figure 6A). Dif-

ferences between the two P. pinaster stands in

winter were smallest (average over the winter

season in invaded vs. non-invaded: 0.74 vs.

0.58 mm d-1, a difference of 21%) corresponding

to the period when A. longifolia stand transpiration

was at its minimum (average 0.23 mm d-1) and

rainfall was substantially greater than transpiration

indicating a water surplus (Figure 7A). In this wa-

ter-limited Mediterranean system, tree transpira-

tion balances out (fall, spring) or exceeds (summer)

the amount of incoming precipitation during most

of the year (Figure 7A) indicating very little surplus

Table 3. Repeated Measures ANOVA ResultsComparing Sapwood Area-Related Sap Flux (QS)Between P. pinaster in the Invaded and the Non-invaded Stand

df F P

(a)

DOS 1, 2750 945.6 <0.0001

Invasion status 1, 8 1.4 0.2681

Season 3, 2750 138.0 <0.0001

Invasion status * season 3, 2750 4.2 0.0054

(b)

Fall

DOS 1, 461 1262.8 <0.0001

Invasion status 1,8 1.3 0.292

DOS * invasion status 1, 461 23.1 <0.0001

Winter

DOS 1, 812 539.0 <0.0001


DOS * invasion status 1, 812 3.0 0.0834

Spring

DOS 1, 848 93.7 <0.0001


DOS * invasion status 1, 848 0.1 0.7305

Summer

DOS 1, 598 4077.0 <0.0001


DOS * invasion status 1, 598 20.4.0 <0.0001

Only data from clear days were used (midday average PPFD > 1000 lmolm-2 s-1; Figure 1C). (a) Result across the entire study and (b) results of withinseason tests. Dates removed before analysis: November 19, 2007; November 20,2007; December 5, 2007; December 6, 2007; December 7, 2007; December 9, 2007;February 17, 2008; February 18, 2008; February 23, 2008; March 11, 2008;March 19, 2008; April 9, 2008; May 11, 2008; May 15, 2008; May 24, 2008.* DOS—day of study.

Figure 7. A Seasonal summed rainfall and stand transpiration for P. pinaster and A. longifolia in the invaded stand and

pine in the non-invaded stand, B total rainfall and transpiration during the entire study from October 1, 2007 to July 31,

2008. Seasons are as in Figure 6. Significant differences between the invaded and the non-invaded stand are indicated

with stars: *P < 0.05, **P < 0.01, ***P < 0.001.


water. Regardless, A. longifolia presence was asso-

ciated with decreased water use of competing

P. pinaster in all seasons (Figures 6B, 7A). A. longi-

folia not only markedly restricted water available to

P. pinaster; but also led to slightly increased total

stand transpiration in the invaded forest through-

out the study (Figure 7).

Invasion Impacts on Carbon Assimilation

Clearly, A. longifolia invasion had a significant

impact on the water use of co-occurring P. pinaster

trees, which led to the question: to what extent

does invasion by A. longifolia impact stand-level

carbon assimilation rates? To address this we esti-

mated canopy carbon assimilation rates (Acan) on a

daily basis for A. longifolia and P. pinaster in the

invaded and the non-invaded stand. Acan was

determined by combining canopy stomatal con-

ductance (GS) with changes in canopy carbon dis-

crimination (D13C) modeled from the relationship

between phloem sap d13C signatures and changes

in VPD and soil VWC (see ‘‘Material and methods’’

and Rascher and others 2010 for details). Acan

varied seasonally with a general increase from fall

through spring and then a decrease during the

summer drought period (Figure 8). Day-to-day

variability in photosynthetic rate was greatest in

winter and spring when climate conditions (for

example, rainfall and VPD) were also most variable

(Figure 1). The ranking of Acan between the species

was: non-invaded P. pinaster > invaded P. pinaster >

A. longifolia (Figure 8). We found that on clear days

across all seasons P. pinaster in the invaded forest

had significantly lower canopy carbon assimilation

rates compared to P. pinaster in the non-invaded

stand (Figure 8).

DISCUSSION

Here, we have demonstrated the substantial impact

that the understory exotic woody invasive,

A. longifolia, had on water and carbon dynamics in a

Mediterranean dune pine forest. These results

complement previous work detailing significant

alterations in Portuguese dune ecosystems after

invasion by A. longifolia. A. longifolia presence

decreases native plant diversity (Marchante and

others 2003; Rascher and others 2011), significantly

Figure 8. Canopy carbon

assimilation rate: A Daily

average canopy carbon

assimilation rate for

A. longifolia and P. pinaster

in the invaded and the

non-invaded stand, B

seasonal average carbon

assimilation rate for

A. longifolia and P. pinaster

in the invaded and the

non-invaded stand. Error

bars indicate standard

deviation. Seasons are as

in Figure 6. Significant

differences between

P. pinaster in the invaded

and the non-invaded

forest are indicated with

stars: *P < 0.1,

***P < 0.001.


alters soil properties (for example, Marchante and

others 2008a, b, 2009) and alters nitrogen cycling

(Hellmann and others 2011). In this study, we

found that A. longifolia had a strong competitive

effect on P. pinaster, decreasing water use and car-

bon fixation rates whereas there was little facilita-

tive effect from introduced nitrogen. This is in

contrast to Australian studies examining the impact

of Acacia sp. on co-occurring Eucalyptus sp. in mixed

plantations (Bristow and others 2006; Forrester and

others 2006a, b) in its relatively wet, native habitat

(annual rainfall � 1000 mm). Those studies found

little competition for water and enhanced growth

and wood production in mixed stands, which was

attributed to the facilitative effect of introduced

nitrogen allowing for increased aboveground car-

bon allocation (Forrester and others 2006a, 2010;

Kelty 2006). Comparing the two stands of P. pinaster

in our study we found a tendency for greater foliar

N, more depleted d13C signatures and lower WPRE-

DAWN and WMIDDAY in the invaded relative to the

non-invaded stand although the differences were

non-significant, which may be partly due to small

sample sizes (P > 0.05 in every season; Figure 4).

Nevertheless, this trend may indicate a small

facilitative effect of A. longifolia N2-fixation on

co-occurring P. pinaster. This contrast highlights the

dominant role that the interdependence between

abiotic site conditions and vegetation characeteris-

tics has in controlling the hydrologic cycle. In mesic

habitats, with little to no competition for water, the

facilitative effect of an additional nitrogen source

may dominate interspecies interactions (Bristow

and others 2006; Forrester and others 2006a).

At our semi-arid site (<400-mm rainfall over

10 months), competition for water dominated the

interaction between A. longifolia and P. pinaster and

overrode any positive effect of increased N2.

We have shown that A. longifolia induced major

changes in P. pinaster forests through the intro-

duction of novel structural and functional traits.

A. longifolia invasion led to a dramatic increase in

vegetation density in the mid-stratum of the

invaded forest, a niche that was empty in the non-

invaded stand (Figure 2). Regarding solely the

structure of the invaded P. pinaster forest, one could

theorize that A. longifolia and P. pinaster would

occupy different niches (for example, understory

vs. overstory, drought semi-deciduous vs. ever-

green, shallow rooted vs. deep rooted) to an extent

that the species would not be in direct competition

for resources (for example, Forrester and others

2005). Applying the theory of complementary

resource use (Forrester and others 2005, 2006b;

Kelty 2006) we could further hypothesize that

invaded forest may more efficiently capture

resources than non-invaded forest. When combin-

ing A. longifolia and P. pinaster we indeed found 9%

greater total stand transpiration (Figure 7) and an

increase in total carbon fixation (Figure 8) in the

invaded forest compared to the non-invaded forest.

Even though A. longifolia filled an empty above-

ground stratum in the forest, its resource use still

impacted the overstory P. pinaster trees indicating

that there was substantial niche overlap in terms of

water sources between the invader and the native

pines.

Furthermore, the changes in aboveground forest

structure after invasion by A. longifolia (Figures 2,

3) were also associated with substantial differences

in soil moisture dynamics (Figures 1D, 5) and

water use rates (Figures 6, 7) between invaded and

non-invaded P. pinaster stands. Immediately after

rain events, soil moisture was typically greater in

the invaded stand than the non-invaded stand

(Figure 1D). Other studies in semi-arid and

savannah ecosystems have similarly found higher

soil moisture underneath canopies of woody shrubs

and trees (Bhark and Small 2003; Segoli and others

2008; Potts and others 2010) which has been

attributed to increased infiltration as a result of

both stemflow (Pressland 1976) and roots of woody

shrubs increasing soil macroporosity which in turn

increases soil water-holding capacity (Segoli and

others 2008). Furthermore, soil organic matter

(OM) content is greater underneath A. longifolia

canopies compared to more open areas (Hellmann

and others 2011) and higher OM decreases soil

bulk density in turn increasing soil water holding

capacity (Segoli and others 2008). A. longifolia also

has smooth bark which has been shown to facili-

tate stem flow (Iida and others 2005). However,

although presence of A. longifolia increased soil

water content directly after rain events (Figure 1D),

the soils in the invaded stand dried out more rapidly

than soils in the non-invaded stand (Figure 5)

indicating that any benefit from this increased soil

water was short-lived and compensated for by the

high transpiration rates of the invader (Figure 6A).

There was competition for water, with stand

transpiration matching or exceeding incoming

precipitation in both the invaded and the non-

invaded stands during most of the year (Figure 7).

Areas with severe water limitation are often

hydrologically insensitive to changes in woody

plant cover, because regardless of vegetation type

all water is evaporated or transpired (for example,

Huxman and others 2005; Wilcox and others

2006). However, in our study we did find a small,

but significant (9%), increase in total transpiration


in the invaded compared to the non-invaded stand

(293 mm vs. 269 mm, respectively: Figure 7). The

only time there was not a significant difference

between total transpiration in the invaded and

non-invaded stand was during the summer

drought when water scarcity alone led to signifi-

cant decreases in water use rates of all species

(Figure 7A). More importantly, because Acacia

contributed significantly to stand transpiration in

the invaded stand in all seasons (between 27 and

42%; Figures 6B, 7), the competing P. pinaster trees

experienced a clear water restriction, transpiring

between 21 and 33% less water than P. pinaster

growing in the non-invaded stand (Figures 6, 7).

Similarly, detrimental effects of understory vege-

tation on water use of canopy trees have been

documented for Betula emanii growing with a dwarf

bamboo understory in Japan (Ishii and others

2008); and, in New Zealand stands of Pinus radiata

with a vegetated understory had lower transpira-

tion rates than stands with a bare understory

(Miller and others 1998). Furthermore, decreased

carbon assimilation and stomatal conductance rates

and increased leaf d13C in unmanaged Pinus densi-

flora stands relative to managed stands (where the

understory was clear-cut yearly) have also been

attributed to water restriction in the unmanaged

stand due to presence of understory vegetation

(Kume and others 2003).

Because Acacia invasion substantially decreased

the water available to the co-occurring P. pinaster

trees (Figures 6, 7) and reduced canopy carbon

assimilation rates (Figure 8) in the invaded forest, it

is feasible that P. pinaster growth rates and biomass

production were also affected. Indeed, the largest

difference in stand transpiration (Figure 7) and

carbon assimilation (Figure 8) between the invaded

and the non-invaded stands of P. pinaster occurred

in spring, the season characterized by highest pro-

ductivity, growth, and biomass production. Our

study lacks pre-invasion stand characteristics so we

cannot definitively ascertain if Pinus in the invaded

stand were always smaller or if Acacia invasion

resulted in decreased growth rates and depressed

biomass production. However, the study was con-

ducted in an even-aged plantation forest with the

stands only being separated by a 4-m wide fire-

break making it unlikely that other site character-

istics were responsible for the decreased tree sizes in

the invaded stand (Table 2; Figure 2). This is similar

to results from controlled studies where A. longifolia

was found to out-compete Pinus pinea (also native

to Portuguese dune ecosystems) under a range of

water availabilities, with the pine exhibiting rela-

tively low plasticity (Peperkorn and others 2005;

Werner and others 2010). In general, competition

experiments have shown that A. longifolia has a

consistently high nitrogen uptake efficiency and

higher relative growth rate than native competitors

under a range of water (Werner and others 2010),

light (Peperkorn and others 2005) and nutrient

(Peperkorn and others 2005) levels indicating that

the N2 fixed by A. longifolia in the field may have a

predominantly self-facilitating effect and not be

readily available to native species.

Acacia longifolia may have additionally limited

P. pinaster growth through nutrient limitation. It

has been documented that most N2-fixing species

require significant amounts of phosphorus (Rothe

and Binkley 2001) and aboveground biomass

production of P. pinaster has been linked with

phosphorus availability (Trichet and others 2008).

Therefore, although A. longifolia may enrich the

system with atmospheric N2 it may also limit

phosphorus availability to P. pinaster which could

have contributed to the reduced size of the

P. pinaster growing in competition with A. longifolia

(Table 2; Figure 2).

CONCLUSIONS

In conclusion, we have demonstrated that woody

plant invasions can significantly alter hydrological

cycles in water-limited ecosystems even when the

invader co-exists with native species in the

understory. Even though A. longifolia is in many

ways functionally unique compared to native spe-

cies (N2-fixer in an N limited system, small tree

where all other understory species are small shrubs

or herbaceous, Figure 2), it nevertheless had a

substantial impact on the native vegetation. Fur-

thermore, we demonstrated that changes in

hydrologic dynamics brought about by A. longifolia

invasion were also associated with decreased car-

bon fixation rates of the overstory P. pinaster trees.

To develop a more complete picture of the overall

impact of A. longifolia invasion, future studies

should examine differences in carbon cycling

between invaded versus non-invaded stands in

more detail (for example, soil C dynamics, fine root

turnover, ecosystem respiration).

ACKNOWLEDGMENTS

Funding for this project was provided by the

Deutsche Forschungsgemeinschaft, (TRANSDUNE

Project: # WE 2681/3-1). KGR gratefully acknowl-

edges additional funding from the PEO Scholar

Award. We also thank the Estabelecimento Pri-

sional de Pinheiro da Cruz for logistical support and


allowing the establishment of our field site. We are

also grateful to Ana Julia Pereira, Tine Hellmann

and Rabea Sutter for their assistance in the field

and Babsi Teichner for isotope analyses.

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http://dx.doi.org/10.1029/2005WR004141

http://dx.doi.org/10.1029/2005WR004141

http://dx.doi.org/10.1093/treephys/tpq036

http://dx.doi.org/10.1007/s10530-011-9949-2

http://dx.doi.org/10.1007/s10530-011-9949-2

understory invasion by acacia longifolia alters the water ...€¦ · tem structure and function...

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