transitions from grassland to savanna under drought through passive facilitation by grasses

Journal of Vegetation Science && (2014)

Transitions from grassland to savanna under droughtthrough passive facilitation by grasses

V�ıctor Resco de Dios, Jake F. Weltzin, Wei Sun, Travis E. Huxman & David G. Williams

Keywords

Grass litter; Plant mortality; Precipitation shifts;

Seedling establishment; Tree–grass

interactions; Woody plant encroachment

Nomenclature

United States Department of Agriculture

PLANTS database

Received 27 July 2013

Accepted 4 January 2014

Co-ordinating Editor: Meelis P€artel

Resco de Dios, V. (corresponding author,

[email protected]), Sun,W.

([email protected]) &Williams, D.G.

([email protected]): Department of Ecosystem

Science and Management, University of

Wyoming, Laramie, WY, 82071, USA

Resco de Dios, V. : Hawkesbury Institute for

the Environment, University of Western

Sydney, Richmond, NSW, 2753, Australia

Weltzin, J.F. ([email protected]): Department

of Ecology and Evolutionary Biology, University

of Tennessee, Knoxville, TN, 37996, USA

Sun,W. : Institute of Grassland Science, Key

Laboratory of Vegetation Ecology, Ministry of

Education, Northeast Normal University,

Changchun, Jilin, 130024, China

Huxman, T.E. ([email protected]): Ecology and

Evolutionary Biology, University of California,

Irvine, CA, 92629, USA

Williams, D.G. : Department of Botany,

University of Wyoming, Laramie, WY, 82071,

USA

Weltzin, J.F.: Current address: USA National

Phenology Network, National Coordinating

Office, Tucson, AZ, 85721, USA

Abstract

Questions:Woody plant encroachment into former grasslands currently repre-

sents a major physiognomic shift globally. Seedling establishment is a critical

demographic bottleneck and is considered to be alleviated by increases in water

availability and negatively impacted by interactions with grasses, particularly

when water stress increases. However, interactions with grasses that are not

actively competing for resources (‘passive interactions’ when grasses are dead)

has seldom been considered. Could the transition from a live to a dead grass (lit-

ter) canopy favour recruitment of woody seedlings in a semi-arid grassland of

the American SW? How does the sign and intensity of grass–seedling interac-

tions change across drastically different summer precipitation regimes with and

without passive interactions?

Location: Sonoran Desert shrub savanna at the Santa Rita Experimental Range,

near Tucson, AZ, US.

Methods: Four cohorts of Prosopis velutina seeds were planted annually (2002–

2005) under rainout shelters that intercepted all incoming precipitation on a soil

with sandy loam texture. Summer precipitation was manipulated to simulate

either a 50% increase or decrease in the long-termmean, and cover was manip-

ulated to simulate a grassland dominated by the C4 bunchgrass Heteropogon con-

tortus or left unvegetated. Emergence and survival of P. velutina was monitored

and compared across cover types, along with monitoring of soil water content

and light interception.

Results: Strong active competition was observed with live grasses, under both

summer drought and also under ample summer water supply. However, the

pattern was reversed and strong passive facilitation of P. velutina was observed

over time when grass canopies died and remained in place. This passive facilita-

tion under dry summers was so strong that recruitment under dead grass condi-

tions was comparable to that observed when ample water supply removed the

effects of competition on unvegetated plots.

Conclusions: After significant mortality of standing grass canopies, which typi-

cally compete for limited soil moisture resources, rates of recruitment by shrubs

may increase even with significant seasonal drought. This work extends our

understanding of interactions among co-located organisms and their effects on

plant community dynamics, and introduces a new hypothesis on how grass litter

facilitates woody plant encroachment during seasonal droughts.

Introduction

Savannas currently occupy about a third of the global land

surface (McPherson 1997), and are expanding through the

encroachment of woody plants into existing grasslands

(Bond 2008; Van Auken 2009). The traditional view of a

savanna is that of an intermediate ecosystem between a

grassland and a forest, where the degree of the main

resource limitation (e.g. water or nutrients) determines

potential woody plant cover (Walter 1979; Scholes &

Walker 1993). Indeed, potential woody cover in arid

and semi-arid savannas (i.e. where precipitation

1Journal of Vegetation ScienceDoi: 10.1111/jvs.12164© 2014 International Association for Vegetation Science

<650 mm�yr�1) has been found to increase linearly with

mean annual precipitation. The interaction between man-

agement, fire, herbivory and soil properties then reduce

the amount of potential woody cover to its actual values

(Scholes & Walker 1993; Higgins et al. 2000; Sankaran

et al. 2005; Hirota et al. 2011; Staver et al. 2011).

Seedling establishment (here defined as emergence and

survival) is the key demographic bottleneck influencing

the dynamics of woody plant encroachment, as the seed-

ling stage is the most vulnerable within the plant life cycle

(Bond 2008). At this demographic stage, the interaction

with a grass canopy is considered as a major driver of the

fate of emerging woody germinants (Scholes & Archer

1997; Van Auken 2009). Indeed, most experimental

manipulations of grass cover have observedminimal estab-

lishment of woody seedlings under a grass cover (Bush &

Van Auken 1995; Brown & Archer 1999; Nano & Clarke

2010; Grellier et al. 2012), although there are exceptions

(Brown &Archer 1999).

Whether competition, facilitation or neutral interactions

dominate depends on the spatial distribution and biomass

of below-ground and above-ground grass organs and how

they modify the availability of critical resources necessary

for seedling establishment. Under a dense live grass can-

opy, below-ground interactions mostly will be competi-

tive, because the intensive root system of grasses will

quickly utilize water or nutrients and water sources

between grasses and seedlings will, at least for some time,

overlap (Weltzin & McPherson 1997; Jurena & Archer

2003; Kulmatiski & Beard 2013). As the degree of water

scarcity increases, the intensity of competition also will

increase. Above-ground interactions with live grasses,

however, could be facilitative when shading protects

woody seedlings from excessive temperature and radia-

tion, but also competitive when woody seedlings

could otherwise benefit from high irradiance without

photoinhibition.

Another aspect of savanna dynamics that has received

considerable attention is how adult trees interact with

grasses (Dohn et al. 2013; Moustakas et al. 2013). How-

ever, a seldom-considered aspect is that of ‘passive interac-

tions’; i.e. the effect of the physical structure of grass

canopies when they are dead and, therefore, not actively

interacting with woody seedlings. The effects of plant litter

on seedling establishment in arid or semi-arid environ-

ments are currently being discussed. The traditional view

was that seedling emergence and survival could be pas-

sively facilitated by litter when soil water conditions are

improved (e.g. through reductions in evaporation or tran-

spiration), but hindered by mechanical impedance, shad-

ing and biochemical or allelopathic compounds (Facelli &

Pickett 1991; Xiong & Nilsson 1999). This discussion is

inevitably confounded by a lack of data. Indeed, a recent

meta-analysis observed that the positive effects of litter on

soil water availability enhance seedling emergence but

that ‘information (regarding seedling survival) for dry

grasslands is lacking’ (Loydi et al. 2013).

Here we studied how live and dead canopies of a C4

bunchgrass (Heteropogon contortus (L.) P. Bauv. Ex Roem. &

Schult.) affect the emergence, survival and recruitment of

the C3 woody leguminous shrub Prosopis velutina Woot.

(velvet mesquite) seedlings along an experimental rainfall

gradient. P. velutina is one of the most prominent

encroaching woody plant species within the American

Southwest (Van Auken 2000) and can grow a tap root

beyond 50 cm within the first 10 mo after germination

(Resco 2008). P. velutina shows a high light-use efficiency

and does not suffer from photoinhibition at high irradianc-

es, except when exposed to very strong drought stress

(Resco et al. 2008; Liu & Guan 2012).

More specifically, we tested the predictions that: (1)

active interactions with a live grass canopy will negatively

impact rates of P. velutina seedling recruitment, and that

the degree of the impact will increase as summer drought

increases; (2) passive interactions with a dead grass canopy

will facilitate seedling recruitment because of soil water

savings, particularly as summer drought increases, by

reducing evaporative water loss. Our project is novel

because we track rates of both seedling emergence and

subsequent survival to determine their relative contribu-

tion to seedling recruitment (i.e. number of surviving indi-

viduals after about 1 yr per number of seeds planted). In

addition, we combine both manipulative (i.e. seasonal irri-

gation under rainout shelters) and natural (i.e. grass can-

opy senescence and mortality) experiments across four

separate seed/seedling cohorts over 4 yrs to determine

interactive effects on seedling recruitment through time

under natural field conditions.

Methods

The study was performed at the Santa Rita Experimental

Range soil moisture manipulation facility in southern Ari-

zona, USA (English et al. 2005). Three rainout shelters

that intercepted all incoming precipitation were estab-

lished on a sandy loam surface in April 2001. The shelters

were divided into 24 1.5 9 1.8 m plots, the perimeters of

which were trenched and lined to ca. 1-m deep (English

et al. 2005). Each plot was randomly assigned to one of

two plant cover treatments crossed with one of two (until

November 2004) or one of four (after November 2004)

precipitation treatments (n = 6 until November 2004, and

n = 3 thereafter).

The experimental plant cover treatments were: (1)

stands of H. contortus; and (2) bare ground. H. contortus

plants established from seed in a greenhouse were

Journal of Vegetation Science2 Doi: 10.1111/jvs.12164© 2014 International Association for Vegetation Science

Passive facilitation drives seedling recruitment V. Resco de Dios et al.

transplanted to the field plots at a density of 20 individu-

als�m�2 in May 2001 and were well watered to ensure

establishment until July 2002, whereupon differential

watering treatments were established.

Grass density declined naturally, due to senescence and

mortality without replacement, from 18 to 15 individu-

als�m�2 in the first 2 yrs of the experiment (year 1: July

2002 to June 2003 and year 2: July 2003 to June 2004) to

0–0.3 individuals�m�2 (100–95% mortality, depending on

plot) in the last 2 yrs in all treatments and regardless of the

watering regime (year 3: July 2004 to June 2005 and year

4: July 2005/June 2006). An unknown driver of grass

mortality during the winter of 2004/2005, perhaps the

frosts in January/February 2005 (Scott et al. 2009) that

affected this subtropical species (Tothill 1966), contributed

to the relatively strong rates of mortality that winter,

althoughmortality causes were not determined.

Because watering treatments and seedling cohorts were

maintained throughout the experiment, we used the

decline in grass survivorship as a natural experiment to

contrast the effects of active interactions of live grasses vs

passive interactions of dead grasses on recruitment of

woody plants for the first 2 yrs and the last 2 yrs of the irri-

gation experiment, respectively. This approach differs from

other experiments that artificially remove or add senescent

plant material (i.e. litter) to plots (Loydi et al. 2013); the

advantage of our approach is that canopy architecture of

the senescent material is maintained, although this com-

plicates exact control over volume or mass of litter in

experimental plots. Litter accumulation in grasslands and

shrub savannas of the American southwest has been docu-

mented as ranging from 200 to 700 g�m�2 (Biggs 1997;

McGlone & Huenneke 2004), which is towards the higher

end of litter abundances documented in Loydi et al.

(2013).

Summer precipitation (July–September) was manipu-

lated throughout the experiment to simulate a 50%

increase or a 50% decrease in summer precipitation rela-

tive to the 30-yr seasonal mean (‘summer wet’ and ‘sum-

mer dry,’ respectively). All plots received equal amounts

of water between November and June (based on long-

term averages). Water was collected from a well nearby

and applied by hand. Winter precipitation (December–

February) was also manipulated between December 2004

until experiment termination in 2006, such that plots

within a given summer treatment were randomly

assigned a ‘winter wet’ or ‘winter dry’ treatment. That is,

for the latter 2 yrs, one plot of each cover type received

one of four possible combinations of 50% increases or

decreases in summer and winter precipitation. Mean

annual, summer and winter precipitation were 394, 220

and 138 mm, respectively. Full details of the shelter

superstructure, treatments and impact on the

microclimate have been presented elsewhere (English

et al. 2005; Resco et al. 2012).

In August of each year between 2002 and 2005, we

planted a set of 30 scarified P. velutina seeds collected on-

site into each plot, hereafter referred to as cohorts 1, 2, 3

and 4, respectively. The emergence and survival of individ-

ually marked seeds and seedlings in each cohort were

monitored every 2 d for the first week, every 4 d for the

following 2 wk, every 3 wk during the following 3 mo,

and every 4 or 5 wk thereafter.

After 10 mo (i.e. the following June), the surviving

seedlings from each cohort were manually removed with

minimal disturbance to the plots prior to the establishment

of the next cohort, with two exceptions. First, a subset of

the few seedlings from cohort 1 that had survived for

10 mo were retained for a total of 24 mo to determine

longer-term patterns of survivorship. Because there was

no significant difference in survival at month 10 vs 24 (Tu-

key’s HSD, P > 0.1), we assumed that the major bottleneck

to seedling survival was within the first year, so we

removed each subsequent cohort at 10 mo. Second, one

seedling per bare plot from cohort 1 was retained for

48 mo for physiological analysis; because seedlings

remained small (i.e. <ca. 20-cm tall), it is unlikely that

these seedlings affected later cohorts (Resco et al. 2008).

Our analyses for each 10-mo cohort were based on the

number of emerged seedlings, the survival of each

emerged seedling, and the number of live seedlings at the

end of the 10-mo period. We examined the sign and inten-

sity of the grass–seedling interactions on proportional

emergence (emerged seedlings/planted seeds), propor-

tional survival (live seedlings/emerged seedlings) and pro-

portional recruitment (live seedlings/planted seeds) with

the relative interaction index (RII; Armas et al. 2004):

RII ¼ RH � RB

RH þ RB

ð1Þ

where subscripts H and B indicate H. contortus and bare

plots, respectively, and R indicates proportional emer-

gence, survival or recruitment.

Soil volumetric water content (VWC) was measured

with custom-built, calibrated time-domain reflectometry

(TDR) probes connected to a time-domain reflectometer

(TDR100; Campbell Scientific, Logan, UT, US) and

installed horizontally at 15- and 35-cm deep in the side

wall of each plot during experiment set-up. VWCmeasure-

ments were taken regularly (i.e. biweekly to monthly)

throughout the experiment, except during 2004. Light

interception was measured in June of each year with a

line-integrating quantum sensor (LI-191; Li-Cor, Lincoln,

NE, US), and was calculated as the ratio between

the mean of three evenly spaced measurements of


V. Resco de Dios et al. Passive facilitation drives seedling recruitment

photosynthetically active radiation (PAR) at ground

level (under the grass canopy) and PAR just above the

canopy.

Additionally, to tested for overlaps in the source of water

used by grasses and mesquite; plots were irrigated in

August 2006, at the peak of the rainy summer season, with

water isotopically labelled by adding 99.9% D2O. We cal-

culated the percentage of the labelled water that had been

taken up by the plant by sampling branches (for P. veluti-

na) or crowns (for H. contortus). Water was extracted using

cryogenic vacuum distillation, and hydrogen isotope ratio

(d2H,&) of extracted water was analysed at the University

of Wyoming Stable Isotope Facility on a dual-inlet isotope

ratio mass spectrometer (Optima; Micromass UK Ltd.,

Manchester, UK) with a measurement precision of 0.8&.

The proportion of the pulse water present in the xylem

(PWU)was calculated as:

PWU ¼ 1� dDpw � dDx

dDpw � dDcon

� �� 100

where dDpw, dDx and dDcon indicate the stable isotope ratio

for hydrogen in the labelled irrigation water used during

the pulse, in the xylem and in the control (the well water

used for irrigation prior to the labelling), respectively. dDx

in P. velutina was corrected according to previous findings

of 9& offset between stem and source water (Ellsworth &

Williams 2007).

Statistical analyses

For each seedling cohort, we tested for facilitation or com-

petition by comparing whether RII was significantly differ-

ent from zero using a linear mixed model, with block as a

random factor, and irrigation as a fixed factor. In addition,

we analysed differences in emergence, survival and

recruitment across plant cover types and irrigation treat-

ments. To avoid confounding associated with different

winter watering regimes among years, the analyses were

performed independently for each year. We used linear

mixed models with cover and irrigation as fixed variables

and block (shelter) as a random variable. Temporal

changes in VWC were also analysed using linear mixed

models that considered the interaction between cover and

irrigation and that included block and day of measurement

as random factors. Because VWC was not monitored in

2004, we analysed VWC separately for the period 2002–

2004 (i.e. for cohorts 1 and 2) and the period 2005–2006

(i.e. for cohorts 3 and 4). Differences in light interception

among irrigation treatments were analysed separately for

each year using ANOVA after testing for homoscedasticity

of variance and normal distribution. Statistical analyses

were implemented in R (v 3.0.2; R Foundation for

Statistical Computing, Vienna, AT, US), using the package

‘nlme’ for mixedmodels.

Results

The effect of irrigation on interactions between grasses and

seedlings differed depending on whether the grass canopy

was live or dead, and the life-cycle stage of P. velutina (i.e.

seeds vs seedlings). In the first two cohorts, emergence of

seedlings was actively facilitated by the live grass canopy in

wet summers (Fig. 1; with RII significantly higher than

zero, P < 0.05), but was not affected by the grass canopy

during dry summers (RII not different from zero,

P > 0.05). In cohorts 3 and 4, however, RII for emergence

of seedlings was significantly positive (P < 0.01) in all dry

summer treatments (regardless of winter precipitation)

except in the dry summer/wet winter of cohort 4, where it

was not significantly different from zero (P = 0.28). More-

over, RII for emergence was not significantly different

from zero in all wet summer treatments of cohorts 3 and 4

(P > 0.15) except in the wet summer/dry winter of cohort

3, where it was significantly positive (P = 0.005).

The effect of the irrigation treatments on survival of

seedlings in the different grass treatments through time

also shifted depending on whether the interactions with

the grass canopy were active or passive (Fig. 1). Strong

competition always occurred in cohorts 1 and 2, regardless

of irrigation level (RII significantly negative, P < 0.0001).

However, in cohort 3, the grass canopy facilitated seedling

survival during dry summers (RII significantly positive,

P < 0.05), while a neutral effect was observed during wet

summers (RII not significant from zero, P > 0.05). Effects

on survival in cohort 4 were neutral (RII not different than

zero).

The effects of the grass canopy on recruitment of P. velu-

tina showed the same trends as those observed for survival

in cohorts 1, 2 and 3 (Fig. 1). That is, RII was significantly

negative in the first two cohorts and for both precipitation

treatments (P < 0.001), significantly positive in the dry

summers of cohort 3 (P < 0.05), and not significantly dif-

ferent from zero in the wet summers of cohort 3

(P > 0.35). In cohort 4, however, RII was significantly

positive (P < 0.05) in the dry summer/dry winter treat-

ment, similar to the response observed for emergence.

Linear mixed models testing for significant differences

across treatments in the level of recruitment generally led

to the same results as the analysis on RII (Table 1). That is,

significantly higher or lower recruitment under grasses,

relative to bare plots, was usually accompanied by RII

being significantly higher or lower than zero, respectively.

Similar results were also obtained when comparing differ-

ences in the levels of emergence or survival with the

results on RII (data not shown). It is noteworthy that



during the dry summers in cohorts 3 and 4 on bare ground,

recruitment was 0%and 1.1–4.4%, respectively. However,

on the dead grass plots, recruitment was 4.44–13.33% in

cohort 3 and 10.00–16.67% in cohort 4 (Table 1) also dur-

ing the summer dry treatment. This high recruitment

under dead grass in dry summers was comparable with

that observed during wet summers on bare ground (4.44–

25.56%) or during wet summers under a dead grass can-

opy (4.44–12.22% in cohort 3 and 16.67–21.11% in

cohort 4).

Shifts in the effects of active vs passive interactions with

grass canopy on P. velutina seedlings across irrigation treat-

ments were accompanied by temporal changes in VWC

(Fig. 2, Table 2). For the first 2 yrs (i.e. when grasses were

alive and cohorts 1 and 2 were in place), VWC was higher

under bare ground than under the grass canopy (Fig. 2a;

linear mixed effect analyses, F = 13.24, P = 0.0003). Irri-

gation and the interaction between cover and irrigation

were also significant (linear mixed effect analyses,

F = 96.36 and P < 0.0001, F = 7.46 and P = 0.0064,

respectively).

However, for the next 2 yrs, when the grasses were

senescent or dead and cohorts 3 and 4 were in place, VWC

was higher under the grass canopy than under the bare soil

(Fig. 2b; linear mixed effect analyses, F = 36.34,

P < 0.0001). VWC was influenced significantly by interac-

tions between irrigation and cover (linear mixed effect

analyses, F = 12.44, P < 0.0001). VWC at 15 and 35 cm

soil depth changed across treatments and time similarly, so

data for the deeper depth are not shown.

The proportion of pulse water used by grasses

(80.8 � 14.2%, mean � SE) did not differ from that used

by woody seedlings (72.1 � 15.2%; ANOVA, F = 0.318,

P = 0.58).

Light interception by the extant grass canopywas gener-

ally higher during the last 2 yrs (when cohorts 3 and 4

were in place) than during the first 2 yrs (when cohorts 1

and 2 were in place; Fig. 3). However, irrigation treatment

Fig. 1. Relative interaction index (RII, eq. 1) for the effects of grass cover on seedling emergence, survival and recruitment and for each cohort. RII varies

from �1 to 1, with negative values indicating competition and positive values indicating facilitation. The dotted line indicates neutral interactions. Ws, Ds,

Ww and Dw denote a wet summer (50% above long-term average), dry summer (50% below long-term average), wet winter and dry winter, respectively.

Active interactions with a live grass cover occurred in the first two cohorts, but transformed into passive interactions with a dead grass canopy in the last

two cohorts. Error bars are SE and asterisks indicate values significantly different from 0 (P < 0.05). Small error bars may be hidden. Each value represents

the results in six (for cohorts 1 and 2) or three (for cohorts 3 and 4) plots. Each column represents a different cohort and, from left to right, they are Cohort

1, 2, 3 and 4.



did not affect light interception in years 1, 2 or 4 (Table 3).

In year 3, we observed significant differences in light inter-

ception across irrigation treatments (ANOVA, F = 4.41,

P = 0.04): post-hoc analyses (Tukey HSD) revealed that sig-

nificantly lower light interception in the wet summer/dry

winter treatment occurred relative to the dry summer/wet

winter treatment (Fig. 3).

Discussion

Dead grass canopies passively facilitated seedling recruit-

ment by increasing soil moisture content when irrigation

simulated a 50% reduction in mean seasonal (summer)

precipitation. However, the effect of a dead grass canopy

on seedling recruitment was neutral with precipitation

50% above the long-term average, likely because water

was not limiting recruitment under that irrigation treat-

ment. These results were independent of winter precipita-

tion and led to comparable levels of seedling recruitment

under a dead grass canopy during a summer drought as

during a summer with a 50% increase in irrigation,

relative to the long-term mean. Drought often has a posi-

tive effect on woody plant recruitment by killing compet-

ing grasses before rains return (Scholes & Archer 1997).

Our findings suggest the ‘mulching’ effect of grass litter

can counteract negative effects of drought, even while the

drought is still occurring. That is, a lagged response of

woody plant recruitment to grass mortality is generally

expected as later wet periods are often thought necessary

to positively affect woody plant recruitment. However, our

results show that immediate strong effects of grass mortal-

ity on woody plant recruitment may be observed provided

a seed source is available.

Consistent with many other studies, seedling recruit-

ment was strongly inhibited by the presence of a live grass

cover (Walter 1971; Scholes & Archer 1997; Weltzin &

McPherson 1997; Wiegand et al. 2006; Bond 2008; Kam-

batuku et al. 2011; Pillay & Ward 2014). We observed a

similar proportion of pulse water taken up by both grass

and woody plant seedlings, indicating overlap in water

sources. Moreover, VWCwas significantly lower under the

live grass canopy than on bare ground. The active effect of

the live grass canopy, with relatively high water demand,

that takes up moisture from the same soil depths exploited

by woody plant seedlings accounts for the strong negative

effect on recruitment.

Increases in light interception during dry summers

under a dead grass canopy are also likely to have played

a role in the facilitation of woody seedling recruitment.

P. velutina is a light-demanding species, and any reduc-

tions in light availability likely reduced its carbon assimi-

lation rate (Resco et al. 2008; Liu & Guan 2012).

However, increased shading by dead plant material

likely reduced soil and surface temperature, which can

exceed 40 °C in this system. The temperature optimum

for P. velutina photosynthesis occurs at ca. 30 °C, and

carbon assimilation decreases with further increases in

temperature (Barron-Gafford et al. 2012). Moreover,

excessive temperatures can denature proteins and dam-

age the stem of young seedlings. The positive effect of

increased light interception is thus likely driven by a

reduction in thermal stress.

The equal likelihood of woody plant recruitment during

prolonged dry spells and episodic wet events may only

apply to the seedling stage. Our experimental methods

Table 1. Mean (�SE) recruitment of P. velutina (in %, relative to 30 seeds

planted in each 1.5 9 1.8-m plot) for each cohort, cover type and irriga-

tion regime.

Irrigation Cohort Bare plots H. contortus Plots RII

Ws 1 25.56 (8.24)a 4.44 (1.11)b �Ds 1 25.00 (8.38)a 0.00 (0.00)b �Ws 2 4.44 (1.11)a 0.56 (0.56) b �Ds 2 0.56 (0.56)b 0.00 (0.00)b �WsWw 3 6.67 (1.92)ab 4.44 (2.94)ab 0

WsDw 3 7.78 (4.01)ab 12.22 (4.44)a 0

DsWw 3 0.00 (0.00)b 4.44 (2.94)ab +

DsDw 3 0.00 (0.00)b 13.33 (6.67)a +

WsWw 4 7.78 (2.94)abc 21.11 (10.60)a 0

WsDw 4 12.22 (6.75)abc 16.67 (6.67)ab 0

DsWw 4 4.44 (2.93)abc 10.00 (8.38)abc 0

DsDw 4 1.11 (1.11)c 16.67 (7.70)ab +

Different letters indicate significant differences within a cohort (linear

mixed models, P < 0.05). Ws, Ds, Ww and Dw denote a wet summer (50%

above long-term average), dry summer (50% below long-term average),

wet winter and dry winter, respectively. Symbols under RII denote whether

values were significantly negative (‘�’, indicating competition), significantly

positive (‘+’, indicating facilitation), or not different from zero (‘0’, indicating

neutral interations).

Table 2. Results of linear mixed effect analyses on the effects of cover, irrigation and day of measurement on soil volumetric water content.

Dependent Variable Independent Variables Cohorts 1 and 2 Cohorts 3 and 4

df F P df F P

Volumetric Water Content Cover 1, 816 13.24 0.0003 1, 256 36.34 <0.0001

Irrigation 1, 816 96.36 <0.0001 3, 256 5.22 0.0016

Cover 9 Irrigation 1, 816 7.46 0.0064 3, 256 12.44 <0.0001



included thinning of seedlings after 10 mo (based on our

observations of a virtually stable population of seedlings

between months 10 and 24). However, as seedlings

develop and their water demands increase, continued

reductions in summer precipitation relative to longer-term

averages will likely be detrimental to already established

saplings or evenmature trees (McDowell et al. 2008; Resco

et al. 2009).

Ws02

810

04

62

46

810

Ds

01/02 04/02 07/02 10/02 01/03 04/03 07/03 10/03 01/04

Bare groundH. contortus

Vol

umet

ric w

ater

con

tent

(%)

Mo/Yr

Ws Dw Ws Ww02

46

810

120

24

68

1012

Ds Dw Ds Ww

01/05 05/05 09/05 01/06 01/05 05/05 09/05 01/06

Vol

umet

ric w

ater

con

tent

(%)

Mo/Yr

(a)

(b)

Fig. 2. Temporal changes in volumetric water content (VWC) at 15 cm soil depth for years 2002–2003 (when seedling cohorts 1 and 2 were in place) (a)

and 2005 (when seedlings from cohorts 3, until June, and 4, after August, were in place) (b). VWC was not collected in 2004. Ws, Ds, Ww and Dw denote a

wet summer (50% above long-term average), a dry summer (50% below long-term average), a wet winter and a dry winter, respectively. There was a

significant effect of cover on both sets of cohorts, but opposite in sign: VWC was significantly lower under the grass canopy than on bare ground while

grasses were live (a), but significantly higher when grasses died and passively influence soil water dynamics (b). Error bars indicate SE. Each value

represents the results in six (for cohorts 1 and 2) or three (for cohorts 3 and 4) plots.



Under a live grass canopy, patterns of recruitment were

more often driven by seedling survival than by seedling

emergence. Although emergence of seedlings was

facilitated by conditions in a number of treatment combi-

nations in this experiment, survival of seedlings presented

a strong demographic bottleneck to recruitment, particu-

larly under intact grass canopies (i.e. cohorts 1 and 2)

because of soil moisture consumption by grasses. However,

under a passive grass canopy, even during dry summers,

we observed facilitation of both seedling emergence and

survival. Considering all life-history stages in woody plant

demography is important, as there is a potential for compe-

tition to override facilitation at early life stages (Grubb

1977;Weltzin &McPherson 1999, 2000).

The divergence in the sign of grass–seedling interactions

during emergence and survival under a live grass canopy

indicates an ontogenetic differentiation of the realized

niche in P. velutina. The strong competitive effect observed

on survival, as previously discussed, can be ascribed to

effects of water extraction by grasses. However, the

observed facilitation of emergence by the live grass canopy

during wet summers is surprising, as it is unlikely that

decreases in water availability enhance germination, and

there was no clear difference in light interception across

water treatments.

An increasing number of observations indicate wide-

spread plant mortality under drought, and efforts are being

made towards elucidating the underlying mechanisms

(Allen et al. 2010; Anderegg et al. 2012). However, physi-

ognomic shifts triggered by the presence of a senesced or

dead grass canopy have received less attention. Additional

research is needed to understand the spatial and temporal

nature of complex feedbacks between drought and passive

interactions – and how drivers such as fire, herbivory and

variation in soil properties – influence patterns of woody

plant recruitment in semi-arid grasslands.

Acknowledgements

This project was funded by NSF (DEB-0417228). Invalu-

able field assistance was provided by L. Thomas, N. Eng-

lish, M. Mason, N. Pierce and many others. We remain

Cohort 1

Ws Ds Ws Ds

Cohort 2

Ligh

t int

erce

ptio

n (%

)

Cohort 3

a ab

abb Cohort 4

020

4060

8010

0

020

4060

8010

0Ws Ws Ds Ds

020

4060

8010

0

Dw Ww Dw WwWs Ws Ds Ds

020

4060

8010

0Dw Ww Dw Ww

Fig. 3. Temporal changes in light interception for each cohort. Different letters, when present, indicate significant differences across water treatments

within a cohort. Error bars are SE. Each value represents the results in six (for cohorts 1 and 2) or three (for cohorts 3 and 4) plots. Ws, Ds, Ww and Dw

denote a wet summer (50% above long-term average), dry summer (50% below long-term average), wet winter and dry winter, respectively.

Table 3. Results of ANOVA on the effects of irrigation on light intercep-

tion for each cohort.

Dependent Variable Independent

Variable

Cohort df F P

Light Interception Irrigation 1 1, 10 0.001 0.978

2 1, 10 0.641 0.447

3 3, 8 4.414 0.041

4 3, 8 2.525 0.131



grateful to J. G Alday, D. Ward and three anonymous

reviewers for their insightful comments.

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transitions from grassland to savanna under drought through passive facilitation by grasses

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