Environ. Res. Lett. 11 (2016) 125011 doi:10.1088/1748-9326/11/12/125011

LETTER

Mulga, amajor tropical dry open forest of Australia: recent insights tocarbon and water fluxes

DerekEamus1, AlfredoHuete, JamesCleverly, RachaelHNolan, XuanlongMa, TonantzinTarin andNadia S SantiniTerrestrial Ecohydrology ResearchGroup,University of Technology Sydney, Australia1 Author towhomany correspondence should be addressed.

E-mail: Derek.Eamus@uts.edu.au

Keywords:Acacia spp.,Mulga, ecohydrological niche separation, tropical dry forests, eddy covariance, hydraulic traits

AbstractMulga, comprised of a complex of closely relatedAcacia spp., grades from a low open forest to tallshrublands in tropical and sub-tropical arid and semi-arid regions of Australia and experiences warm-to-hot annual temperatures and a pronounced dry season. This short synthesis of current knowledgebriefly outlines the causes of the extreme variability in rainfall characteristic ofmuch of centralAustralia, and then discusses the patterns and drivers of variability in carbon andwaterfluxes of acentral Australian low openMulga forest. Variation in phenology and the impact of differences in theamount and timing of precipitation on vegetation function are then discussed.We use fieldobservations, with particular emphasis on eddy covariance data, coupledwithmodelling and remotesensing products to interpret inter-seasonal and inter-annual patterns in the behaviour of thisecosystem.We show thatMulga can vary between periods of near carbon neutrality to periods of beinga significant sink or source for carbon, depending on both the amount and timing of rainfall. Further,we demonstrate thatMulga contributed significantly to the 2011 global land sink anomaly, a resultascribed to the exceptional rainfall of 2010/2011. Finally, we compare and contrast the hydraulic traitsof three tree species growing close to theMulga and showhow each species uses differentcombinations of trait strategies (for example, sapwood density, xylem vessel implosion resistance,phenological guild, access to groundwater andHuber value) to co-exist in this semi-arid environment.Understanding the inter-annual variability in functional behaviour of this important arid-zone biomeandmechanisms underlying species co-existencewill increase our ability to predict trajectories ofcarbon andwater balances for future changing climates.

1. Introduction

Tropical dry forests (TDFs) are globally extensive andwidely threatened (Pulla et al 2015), representing thefirst frontier of anthropogenic land-use change (Por-tillo-Quintero and Sanchez-Azofeifa 2010). Globally,research and conservation efforts for rainforests andtropical moist forests greatly exceed that for TDFs(Pulla et al 2015), despite the fact that the loss of TDFsarising from human activities exceeds that for rain-forests and moist tropical forests (Miles et al 2006),probably because humanpopulation densities in TDFstend to be larger than those in rainforests and moisttropical forests.

Tropical forests represent significant sites of Cuptake and storage. In 2011 a global land sink anomalyoccurred (Le Quéré et al 2014, Poulter et al 2014) andthis was predominantly the result of increased pro-ductivity of southern hemisphere (especially Aus-tralian) semi-arid vegetation (Poulter et al 2014,Cleverly et al 2016a). Given the importance of Aus-tralian TDFs (including Mulga and riparian forests) toglobal atmospheric C dynamics and regional waterand C budgets it is timely to provide a synthesis ofrecent developments in our understanding of thestructure, function and behaviour of this biome and todiscuss the specifics of the behaviour of Mulga duringthe land sink anomaly.

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TDFs have two key climatic features: they experi-ence warm or hot temperatures all year (mean annualbiotemperature >18 °C), and they experience a pre-dictable dry season every year. The former attribute isthe same as that for lowland rainforests but distin-guishes them from tropical montane forests, whichexperience lower daytime temperatures because of theeffect of altitude on temperature (Eamus et al 2016).Unlike many TDFs globally, Australian TDFs, as withmost Australian woody ecosystems, are dominated byevergreen species.

In this short synthesis we summarise our currentunderstanding of the ecophysiology and ecohydrologyof a large (5500 km2) endorheic semi-arid tropical lowopen forest in central Australia. In particular weaddress the following key questions:

(1)What determines the climate of this region?

(2)How does climate influence phenology of thisregion?

(3)What are the principle drivers of daily, seasonaland inter-annual patterns of carbon (C) and waterfluxes?

(4)How did the Mulga forests contribute to the 2010/2011 global land sink anomaly?

(5)How do hydraulic traits of Mulga compare withthose of two co-occurring tree species and whichtraits may be associated with extreme droughtresilience?

1.1.Mulga: amajor dry open forest of tropicalAustraliaMulga are comprised of a complex of closely relatedAcacia spp., especially A. aneura and A. aptaneuera(Maslin and Reid 2012). Acacia dominated landscapesgrade from low open forests, through woodlands tolow shrub lands (Specht and Specht 1999) and cover20%–25% of the Australian continent (figure 1(a);Nicholas et al 2011). They are especially adapted tosemi-arid and arid tropical and sub-tropical regions.As with all Acacias, Mulga forms symbioses withnitrogen-fixing cyanobacteria. Across the continentforest density (trees per hectare), height and growthform of Mulga trees are highly variable, ranging fromrelatively short (<3 m) to relatively tall (>10 m) trees,and ranging from a very open tree canopy to arelatively closed canopy. Mulga occurs on flat terrainand requires significant water storage capacities in thesubstrate (e.g., clay-rich soils or the presence of ahardpan within several meters of the surface; Press-land 1976), with low rates of drainage past therelatively shallow roots. Mulga usually forms a non-overlapping mosaic with hummock (spinifex) grass-lands (figure 1(b); Nicholas et al 2011). The boundariesbetween Mulga and adjacent spinifex grasslands have

not moved in the past 1000 years (Bowman et al 2007),suggesting that they have persisted in roughly the samelocations over a possibly large diversity of climaticconditions.

In the Ti Tree basin in central Australia (approxi-mately 22° 14′ S, 133° 17′ E), the site of the studies dis-cussed here, the Mulga canopy is ca. 6.5 m tall with abasal area of 8 m2 ha−1 and a stem density of approxi-mately 3300 stems ha−1 (figure 1). Dominant unders-tory forbs and herbs include Psydrax latifolia,Eremophila gilesii, Eremophila latrobei ssp glabra, Sidaand Abutilon spp., and Solanum ellipticum. The domi-nant grasses form a nearly complete cover when con-ditions permit and include perennials Thyridolepismitchelliana and Eragrostis eriopoda, and annualEriachne pulchella ssp pulchella. The Ti Tree basinreceives the majority of its annual rainfall (long term(1987–2016) median of 299 mm) in the Austral sum-mer wet season (December to February; figure 2),although rainfall can occur in any month (figure 2).The low level of rainfall received in themonths June toSeptember inclusive (<20 mmmonth−1) is essentiallyineffective in wetting the soil profile to any significantdepth: almost all of this rain is intercepted by litter(and shallow roots) and evaporated rapidly back to theatmosphere. In the past 29 years annual rainfall hasvaried between 97.4 mm (1994) and 750.6 mm (2010).

1.2.What determines the climate of centralAustralia?The semi-arid climate of central Australia is old. Thedevelopment of a distinct dry season occurred asmuchas 35–50 Mya, preceding the separation of Australiaand South America from Antarctica which opened theSouthern Ocean and changed the world’s climate to acooler and drier regime (Crisp and Cook 2013). Themodern climate regime was established by the end ofthe Pliocene (2.6 Mya), since which time the climatehas dried by stages (Martin 2006) and was likely tohave become semi-arid ca. 0.5 Mya. By using the termdried by stages, Martin (2006)meant that, whilst glacialperiods have been drier than during inter-glacialperiods, successive glacial and inter-glacial periodshave been drier than those that occurred before. Thus,the longest and driest droughts in Australia spannedthemost recent glacial period.

The second important feature of the Australian cli-mate is its inter-annual variability in rainfall. Amongstthe arid and semi-arid regions of the world, three ofthe four with the largest variability in rainfall occuralong the rim of the Indian Ocean (the Thar Desert inIndia, Somalia and Australia north of 27 °S; VanEtten 2009). In the Ti Tree basin over just the last 100years, for example, annual rainfall has been as low as25 mm yr−1 in 1928 and as high as 955 mm yr−1 in1974 (Cleverly et al 2016a, 2016b). Together, theancient and more recent climate histories underscoretwo critical features that impact the development of

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Figure 1. (a)The distrubution ofMulga in Australia. Thismap is generated based onAustralia’sNational Vegetation InformationSystem—MajorVegetationGroups (NVIS-MVGs). The original 26NVIS-MVGswere reclassified into severalmajor groups. TheMulga group includesAcacia-dominated forests, woodlands and shrubs, and the location of the Ti-Tree basin is indicated by the redtriangle in central Australia ; (b) theMulga viewed at ground level; (c) theMulga viewed from above the canopy.

Figure 2. Long-term (29 yr)meanmonthly rainfall for Ti Tree, demonstrating both seasonality and the large inter-annual variability.

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Australian TDFs: an exceptional amount of inter-annual variability in rainfall and a long-term dryingtrend.

Three climate drivers have the potential to have adirect influence on continental weather patterns inAustralia: El Niño-SouthernOscillation (ENSO) in theequatorial Pacific Ocean, the Indian Ocean dipole(IOD), and the southern annular mode (in the South-ernOcean, SAM). These climate modes have been indi-vidually related to the occurrence of rainfall, but not toamount (Pui et al 2012). However, ENSO, IOD andSAM periodically synchronise their effects on Aus-tralia’s weather patterns, resulting in extremes of rain-fall and drought (Cleverly et al 2016a). One suchperiod began in 1999, signalling an increase in extremeweather events like the Millennium Drought at thebeginning of the 21st century and widespread floodinginQueensland in 2011.

Our recent analysis (Cleverly et al 2016a) hasdemonstrated that when climate modes synchronise,the general amount of atmospheric moisture formedby ENSO (i.e., dry in Australia during El Niño, wetduring La Niña) combines with the strength of themonsoon depression driven by IOD and placement ofweather systems by SAM to enhance or prevent rainfallacross the continent (Cleverly et al 2016a). Facilitatedby Australia’s flat terrain, a strong monsoon depres-sion can interact with the continental low (which isindirectly influenced by SAM) to generate widespreadstorms with the intensity of summer rainfall but thelarge spatial and temporal extent of winter storms(Kong and Zhao 2010, Cleverly et al 2013). Alter-natively, dry conditions induced by each climatemodeindividually can combine to further reduce rainfallbeyond the effects of any single climate mode, leadingto more intense Australian heatwaves (Perkinset al 2015). However, these interactions were notapparent in the early part of the measurement record(1982–1998), suggesting that this interaction amongclimate modes is a periodic feature of regional climate.Thus, these three climate drivers interact in the IndianOcean region to generate the large degree of rainfallvariability observed across Australia.

2.Howdoes climate determinephenological patterns ofMulga lowopenforest?

Mulga has a highly variable phenology that is largelyrainfall-pulse driven. Key features of this phenologicalvariability include large fluctuations in the dates ofstart-of-growing season, growing season peak andend-of-growing season, along with season length andthe presence of a growing season in a given year(figure 3; Ma et al 2013). During very dry years, nodetectable growing season occurs (ie there is minimalseasonal variation in the enhanced vegetation indexEVI; Ma et al 2013), and minimal but non-negligible

amounts of photosynthetic production are restrictedto the winter dry season in Mulga (Cleverlyet al 2016c).

The phenology of Australia’s semi-arid ecosystemsis very sensitive to extremes of climate such that var-iance in total annual amount of rainfall alone explains80% of variation in the length of the growing season(Ma et al 2013, 2015). However, uneven distribution ofrainfall across the year can inhibit phenologicalresponses in Mulga of central Australia due to the jux-taposition of wet and dry months (Nano andClarke 2010). Thus, greenness in the vegetation of cen-tral Australia as determined from Moderate Resolu-tion Imaging Spectroradiometer (MODIS) EVI ismore highly correlated to the synchronised climatesignal amongst ENSO, IOD and SAM than to rainfall(Cleverly et al 2016a), implying that the suite ofmeteorological conditions associated with the state ofthe climate system (e.g., cool and wet or hot and dry)exerts a larger influence on the phenology of Mulgathan any individual environmental driver.

Seasonal and inter-annual phenological variationacross the landscape is large. Seasonal variations in leafarea index (LAI) and landscape-scale photosyntheticcapacity are primarily driven by seasonal variations inunderstory grasses and forbs (Eamus et al 2013a, Maet al 2013). Seasonal changes in LAI of the Acaciaoverstory, in contrast, are relatively minor (Eamuset al 2013a). In the understorey of Acacia Mulga,annual grasses (such as Aristida spp.) green up inresponse to summer rain (∼February) and set seed inautumn (Mott andMcComb1975). In contrast annualforbs, such as species of Helichrysum spp. and Helip-terum spp. germinate in response to rain in early win-ter (May–June) (Mott and McComb 1975), andperennial grasses green up into the summer monsoonperiods (Flora of Australia 2002). Collectively, thesedifferent phenological patterns of understorey in Aca-cia low open forests enable a long greening period(figure 3) at the community scale during the wet peri-ods and are observable by satellite sensors (Maet al 2013).

Despite the principal control of rainfall on phenol-ogy, the response of Mulga to rainfall can be inhibitedduring the summer wet season by canopy tempera-tures that exceed Acacia’s 38 °C thermal limit forgrowth (Nix and Austin 1973, Cleverly et al 2016b).Thus, growing-season phenology and canopy struc-ture of this low open forest are strongly related to itsphysiological phenology (e.g., the seasonal and annualcycle of ecosystem productivity and light use effi-ciency; Migliavacca et al 2015), which provides a basisfor the strong relationships amongst gross primaryproduction and EVI during the green-up phase andhysteresis during autumnal brown-down (figure 4;Maet al 2013, 2014). Hysteresis means that the relation-ships between GPP and EVI during greenup differsfrom that during browndown. In Mulga the lowerGPP for a given EVI during browndown presumably

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reflects a loss of photosynthetic potential in the canopyduring browndown.

Although direct empirical relationships betweenphotosynthetic activity, ecosystem productivity andMODIS vegetation indices have been observed in var-ious temperate and tropical ecosystems, MODIS vege-tation products have been less successful in capturingseasonality of productivity in many Australian ever-green forests and sclerophyll woodlands (Restrepo-Coupe et al 2016). This prompted a re-evaluation ofthe connection between satellite observations and var-ious flux productivity measures with the expectationthat satellite greenness products constituted a com-bined measurement of ecosystem structure (e.g. LAI)

and function (e.g. leaf level photosynthetic assimila-tion capacity), rather than productivity per se.Restrepo-Coupe et al (2016) showed the lowest corre-lations between MODIS vegetation products and pro-ductivity at locations where meteorological variables(drivers) and vegetation phenology were asynchro-nous, as in Mediterranean ecosystems (schelophyllforests). In contrast, the largest correlations wereobserved at locations where synchrony across meteor-ological variables and vegetation phenology wasapparent, as observed in the Mulga TDF. They con-cluded that remote sensing products would not followproductivity when: either phenology is asynchronouswith key meteorological drivers, and productivity is

Figure 3.There ismuch variability in the timing of the start, the end and the peak growing season forMulga lowopen forest in the TiTree basin. Some years (e.g. 2004–2005) have almost no seasonality in theMODIS enhanced vegetation index (EVI). SGS: start ofgreening season; PGS: peak of greening season; EGS: end of greening season. FromMa et al (2013). The date of the SGS is defined as thedate halfway between the date of theminimumEVI and date of the fastest rate of greenup (maximum slope in the EVI response in thegreenup). The date of the PGS is defined as the date when EVI ismaximum in each year. The EGS is defined as the date half-waybetween the fastest decline in EVI andminimumEVI.

Figure 4.There is a strong correlation betweenGPP (derived from eddy covariance data) and theMODIS enhanced vegetation index(EVI) in the green-up and brown-down phases, with a distinct hysteresis observed between the two stages (Ma et al 2013, 2014).

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therefore driven by one or more meteorologic driversover different times of the year; or when phenology isrelatively aseasonal, and productivity is solely drivenbymeteorology (especially solar radiation, air temper-ature, soil water availability, VPD, or differentcombinations).

3.Drivers of seasonal and annual patternsof C andwaterflux

The environmental drivers associated with patterns ofC and water flux are closely related to those drivingphenology in Australia (Ma et al 2014). In this section,we will address how patterns of rainfall, soil moisturecontent and meteorological drivers affect dynamics inC and water fluxes during a drier-than-average year(hydrologic year 2012–2013) and two years withaverage amounts of rainfall (2013–2014 and2014–2015). Evaluation of drivers in this section willbegin with a comparison of rainfall, evapotranspira-tion (ET) and net ecosystem productivity (NEP)between a drier-than-average year (2012–2013) andthe subsequent year with average rainfall (2013–2014;Cleverly et al 2016c).

3.1. Comparing a drier-andwetter-thanaverage yearMulga shows a disproportionate response to extremelyhigh inputs of rainfall (e.g. during the global land sinkanomaly; Cleverly et al 2013, Eamus et al 2013a). Thisis driven by a tropical-extra-tropical connection in theGreat Australian Bight which creates a regular patternof storm-interstorm intervals (Berry et al 2011) andthereby provides periods of high light, soil moisturecontent and humidity during wetter-than-averageyears that are highly favourable for photosynthesis(Cleverely et al 2013). By contrast, inter-storm periodsduring dry-to-average years are hot and VPD is large,exceedingMulga’s thermal tolerance of 38°C (Cleverlyet al 2016b). In this section, we explore these issuesmore fully.

Rainfall in hydrologic years 2012–2013 (193 mm)and 2013–2014 (295 mm)was approximately 65% and99% of the long-term average (median 299 mm),respectively. As is typical of this site, rainfall pre-dominantly occurred in the summer wet season. Ratesof ET are extremely responsive to pulses of rain (Cle-verly et al 2016c). After rains have concluded, how-ever, ET declines rapidly (and exponentially) to zero(Eamus et al 2013a, Cleverly et al 2016c). Peak rates ofdaily ET in the wet season range between three andfour millimetres, whilst cumulative ET in the twoyears was 150 and 250 mm, or 50% and 84% of aver-age annual rainfall (figure 5).

Over these two years, the Mulga low open forestoscillated across the seasons between being a C sinkand C source (figure 6). During the winter and earlyspring, the Mulga was a small sink (positive values of

NEP ranged from 0.1 to 0.3 gC m−2 d−1). The largestsink activity during this two-year period (2012–2014)occurred in late summer/early autumn of 2014 whentemperatures, vapour pressure deficit and soil moist-ure content were optimal for NEP. Source activity inthe Mulga occurred in pulses during the summer/autumnof 2013 and the summer of 2014 (figure 6). Ona hydrological annual time-scale, the Mulga was asmall source in the drier-than-average hydrologic year(−26 gC m−2 d−1 in 2012–2013) and a small sink inthe average year (12 gCm−2 d−1 in 2013–2014). It wasnot until the wet summer of the second hydrologicyear that Mulga became a moderate-to-strong sink.Importantly, rainfall in the first hydrologic year(193 mm) was significantly less than in the secondhydrologic year (295 mm), thereby revealing theimportance of the amount of rainfall received as adeterminant of productivity of this semi-arid tropicalecosystem.

Different combinations of rainfall, temperature,solar radiation and vapour pressure deficit are theprinciple determinants of NEP and GPP (van Dijket al 2005, Baldocchi 2008, Kanniah et al 2010, Baldoc-chi and Ryu 2011, Zha et al 2013). It is apparent thatinter-annual differences in rainfall are the principlecauses of inter-annual differences in sink strength fortheMulga (table 1), in strong agreement with multipleother arid and semi-arid biomes (Huxman et al 2004,Flanagan and Adkinson 2011, Barron-Gaffordet al 2012, Ma et al 2012, Chen et al 2014) but inmarked contrast to boreal, tropical montane, tempe-rate mesic deciduous forests and tropical mesic savan-nas, where temperature, solar radiation and the lengthof the growing season are the principal drivers of varia-tion in NEP (Luyssaert et al 2007, Whitley et al 2011,Ma et al 2013, Zha et al 2013, Keenan et al 2014). How-ever, this does not mean that these other drivers arenot important for explaining inter-annual variation inNEP; instead, the environmental drivers are them-selves related to rainfall in a series of complexitieswhichwewill nowdiscuss.

3.2. The importance ofwet season rainfalldistribution in driving patterns ofNEPCleverly et al (2016b) compared NEP during two yearswith near-average annual rainfall (2013–2014 and2014–2015) but with different temporal patterns toevaluate the impact of differences in the distribution ofprecipitation within the wet season. Each wet seasonreceived about 280 mm, but it was distributed moreevenly across the wet season of 2013–2014 than that of2014–2015. In 2014–2015 most of the rainfall hadaccumulated by mid-January, and the site receivedvery little rainfall for months afterward (figure 7).These differences had significant effects on summerand autumn patterns of soil moisture content andhence the response of NEP across these two years. Inthe summer wet season 2013–2014, there was a

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Figure 5.Patterns of rainfall and evapotranspiration (ET, daily and cumulative), August 2012–July 2014. Redrawn fromCleverly et al(2016c).

Figure 6.Patterns of net ecosystemproductivity (NEP, daily and cumulative), August 2012–July 2014. Redrawn fromCleverly et al(2016c).

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substantial delay (six weeks) in the response of NEP tothe rainfall that began in late December 2013 and fellthrough February 2014. Sink activity was not recordeduntil late February, and this was maintained throughto the end of April 2014. The delayed stimulation ofNEP in early 2014 was the result of environmentalstress, in particular large temperatures andVPDs and alack of soil moisture in mid and late summer of 2014.This resulted in the Mulga canopy experiencingconditions that exceeded the thermal tolerance of thephyllodes. It was not until cooler temperatures, asmaller VPD and the positive impact of transpirationalcooling on canopy temperature (once soil moisturelevels were sufficient) were evident, that NEP becamepositive in late February and March 2014. In contrast,rain in December 2014–January 2015 produced apositive response in NEP almost immediately, and alarge C sink was maintained throughout January andFebruary of 2015. Cooler air temperatures and suffi-cient soil moisture above the hard pan to allowtranspirational canopy cooling resulted in positiveNEP inmid-January tomid-March 2015,much earlierthan during the previous year.

We will now demonstrate how differences in soilmoisture content were formed due to differences inthe weekly-to-monthly pattern of rainfall in theMulga TDF.

Soil moisture content measured at a pointapproximately 1 m below the ground surface is highlydependent upon the (i) amount, timing and intensityof rainfall and (ii) the presence of a subsurface hardpanat this site (Cleverly et al 2013, 2016b, 2016c). Thesiliceous hardpan is buried below the surface and pre-vents drainage of water to the regional water table,which is 49 m deep at this site (Cleverly et al 2016c).Soil moisture content in the hardpan is 0.05 m3 m−3

and has shown onlyminor fluctuations sincemeasure-ments began in 2010. Conversely, soil moisture con-tent in the unconsolidated loamy sand above thehardpan has fluctuated between ca. 0.08 m3 m−3 and0.35 m3 m−3 (saturated) since 2010 (Cleverlyet al 2013, 2016b). The fluctuations in soil moisturecontent in the unconsolidated soil above the hardpanrelate strongly to the amount and pattern of rainfall,hence providing a link for responses of NEP to rainfall(Cleverly et al 2016b).

With the hardpan acting as a barrier to drainage,rainfall that delivers water in excess of that which isrequired by the vegetation can be stored and carried-over to other seasons or years. The importance ofinter-seasonal and inter-annual carry-over of rainfallto sustaining NEP is well documented in arid andsemi-arid ecosystems globally (Flanagan and Adkin-son 2011). Even during a drier-than-average year(2011–2012, 184 mm of rainfall), drawdown of thestorage reservoir in the unconsolidated soil above thehardpan (from0.10 m3m−3 to 0.08 m3m−3)was asso-ciated with maintenance of gross primary productionat low but non-negligible levels (Cleverly et al 2013).The reservoir was then rapidly re-filled and main-tained soil moisture content of ca. 0.10 m3 m−3 acrossthe following autumn-winter (Cleverly et al 2013). Wehave found that Mulga trees have a small but sig-nificant proliferation of roots near the top of the hard-pan where this soil moisture reservoir accumulates(Cleverly et al 2016b), and these roots are likely toremain active during all seasons because of the con-sistent elevation of soil moisture content in the reser-voir relative to the hardpan (Cleverly et al 2013,2016b). Whereas carry-over of soil moisture appearedto be an important feature of the site water budget ina drier-than-average year, it wasn’t until the firstyear with average rainfall in the study (2014–2015)when soil moisture content increased substantially(>0.2 m3 m−3) such that delayed increases in NEPwere associated with carry-over of that soil moisture(figure 7).

In comparing the summer wet season during twoyears with average rainfall (2013–2014 versus2014–2015), it became apparent that the pattern ofrainfall distribution affected the degree to which soilmoisture storage filled to capacity in the unconsoli-dated soil above the hardpan (Cleverly et al 2016b).During the summer-autumn of 2013–2014, soilmoisture content increased to 0.26 m3 m−3 followingseveral weeks of rainfall (150 mm of rainfall by mid-January, figure 8), including one storm which deliv-ered 105 mm of rainfall over six days (Cleverlyet al 2016b). By contrast, in the summer-autumn of2014–2015, rainfall was 250 mm by mid-January with145 mm delivered over 12 days; soil moisture contentincreased to saturation (which is 0.35 m3 m−3 in thissoil) immediately thereafter; and NEP respondedimmediately and was positive by mid-January 2015.Saturation of the upper soil profile (top 1 m) in Jan-uary 2015 resulted in the formation of a perched,ephemeral water table located in the unconsolidatedsoil above the hardpan (figure 8). These results areconsistent with the threshold-delay model of Ogle andReynolds (2004)whereby a pulse of rain that is insuffi-cient to fill the ‘bucket’ (i.e., the soil moisture storagereservoir containing roots) causes a delay in theresponse of NEP, whereas sufficient rain to fill thebucket induces a rapid response in NEP (i.e., inhibi-tion of the delay).

Table 1.Annual rainfall, net ecosystemproductivity (NEP) andevapotranspiration (ET) in theMulga lowopen forest across themeasurement period.

Year

Rainfall

(mmy−1)NEP (gCm−2 yr−1)

ET

(mmyr−1)

2010–2011 565 259 (sink) 518

2011–2012 184 −4 (source) 204

2012–2013 193 −25 (source) 151

2013–2014 295 12 (sink) 248

2014–2015 302 34 (sink) 245

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When stomatal conductance is large, transpirationand transpirational cooling proceed at rates thatexceed those observed when conductance is low.When the bucket was not filled during summer of2013–2014 and NEP was delayed, transpiration wouldhave beenminimised; therefore, incoming solar radia-tion would have been partitioned into sensible heatflux instead of latent heat flux, thereby minimisingtranspirational cooling (Cleverly et al 2016b). In con-trast, in the summer of 2014–2015 when NEP waspositive and large rates of transpiration were occur-ring, less partitioning to sensible heat flux would beexpected. In agreement with this is the observationthat sensible heat flux in January–February 2014 was307.1Wm−2 but in the same period in 2015, sensibleheat flux was smaller (270.4Wm−2). Using imageryobtained from an unmanned drone with a thermalcamera inMarch 2014 (i.e., during the autumn follow-ing the delay in NEP), it was revealed that a large frac-tion of the Mulga canopy still exceeded the 38 °Cthermal optimum for this species (Cleverlyet al 2016b), further suggesting that a soil moisturereservoir that is not full is insufficient to provide the

resources for transpirational cooling until the heat ofthe summer has passed.

3.3. Interactions of soilmoisture contentwithtemperature andVPDas drivers of variation inNEPHaving established the importance of the timing ofrainfall as a determinant of the response of NEP, weextend this analysis to examine in detail the interac-tions among soil moisture content, VPD and solarradiation as determinants of NEP. Thus we evaluatemeteorological drivers and NEP across a wide range ofsoil moisture contents during a very wet year(2010–2011) and the subsequent drier-than-averageyear (2011–2012). The effects of air and soil temper-ature, VPD and solar radiation on NEP were closelyrelated to variations in soil moisture content as aconsequence of correlations between these drivers andrainfall (Cleverly et al 2013). For example, the temper-ature at which peak NEP occurred and the reductionof NEP at high temperature were dependent upon soilmoisture content (figure 9). Similarly, the VPD atwhich NEP was maximised depended upon soilmoisture, as was the response of NEP to light intensity.

Figure 7.A comparison of the pattern ofNEP for summer–autumnof 2013–2014 and 2014–2015. Redrawn fromCleverly et al(2016b).

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The thermal responses ofNEP to soilmoisture contentin Mulga were not dissimilar to those of Eucalyptusleaves as a function of [CO2], although NEP in Mulgaappears to bemore limited at low temperature than forleaf photosynthesis in Eucalyptus (Eamus et al 1995).Furthermore, the responses of NEP to VPD in Mulgaimply a close link to ET via canopy conductance (asassimilation is linked to transpiration via stomatalconductance in leaves; Duursma et al 2014). Thus inMulga, ecosystem inherent water-use efficiency(IWUE, the ratio of [NEP×VPD] to ET) is highlydependent upon soil moisture content during wet anddry seasons (Eamus et al 2013a), illustrating thecoordinated control of NEP and ET by soil moisture,VPD and temperature.

4. The global land sink anomaly andMulga

Having established general relationships among rain-fall (timing and amount), temperature, VPD and NEPwe now discuss the specific case of the 2010/2011global land sink anomaly andMulga.

Le Quéré et al (2014) identified the 2011 globalland sink anomaly whereby global rates of C uptakeincreased from a decadal average of 2.8 GtC yr−1

(2003–2012) to 4.0 GtC yr−1. Poulter et al (2014)used a combination of remote sensing and biogeo-chemical modelling to establish that this global landsink anomaly was driven by an upsurge in growth ofvegetation in semi-arid regions. In particular theyidentified the Southern Hemisphere as being themain location of this enhancement in growth, with60% of the enhancement occurring in Australia. Thecause of this C sink anomaly was a strong monsoondepression (negative IOD), deep continental low(negative SAM) and the strongest sustained La Niñasince 1917 (Cleverly et al 2016a). The massiveincrease in rainfall resulted in a drop in global meansea level of about 5 mm, and remote sensing estab-lished a dramatic greening of eastern and centralAustralia (figure 10). The Gravity Recovery and Cli-mate Experiment satellites also recorded significantincreases in the mass of water stored across Australiain 2011 (Boening et al 2012, Xie et al 2016). Further-more, Fasullo et al (2013) demonstrated that

Figure 8.A comparison of the pattern of soilmoisture content in hardpan and unconsolidated soil above the hardpan for summer-autumn of 2013–2014 and 2014–2015.Onemoisture sensor was located at approximately 1 mdepth in unconsolidated soil; a secondsensor was located at the same depth butwithin the hardpan. Redrawn fromCleverly et al (2016b).

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Australia maintained a positive water mass anomalyin 2012, meaning that a significant fraction of theextra water received in 2011 in Australia remained

detectable after the conclusion of the global land sinkanomaly and suggesting that increased C uptake inarid Australia may have persisted beyond the 2010/

Figure 9.Envelope analysis showing the functional responses forNEP versus temperature, vapour pressure deficit and solar irradianceas a function of soilmoisture content (θ). Redrawn fromCleverly et al (2013).

Figure 10.Differences in greenness between a very dry year (2008–2009) and a verywet year (2010–2011). FromCleverly et al (2016a).

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2011 global sink anomaly. We now address the ques-tion: was there an observed response in C uptake forthe Mulga during the 2010/2011 global land sinkanomaly?

During the hydrologic year 2010–2011 rainfall inthe Ti Tree basin was 565 mm, or 75% larger than thelong-term average. Furthermore, a large fraction ofthis rainfall was received in the dry season of 2010, as isreflected in the repeated recharge of soil moisture inSeptember–November 2010 (figure 11). Indeed thewet season for this hydrologic year was eight monthslong (figure 12) rather than the usual three or fourmonths (Ma et al 2013).

The response of ET and NEE to this unusual pat-tern and amount of rainfall is shown in figure 13.Large rates of ET were maintained for the unseason-ably wet dry season of 2010 through to the earlyautumn of 2011. By the winter of 2011, however, ET

had declined to zero except for a brief increase inresponse to rain in June 2011. Across the 372-daystudy, total ET was 430.6 mm (76% of rainfall). Theexponential decline in ET following rainfall exhib-ited a half-time of decay of 5.2 days, whilst a thresh-old amount of rainfall had to be exceeded (3.0 mm)for transpiration to increase. This half-time is simi-lar to that observed in semi-arid grasslands andshrublands of central New Mexico (half-timeapproximately 2 days; Kurc and Small 2004) butshorter than the range in half-times observed across15 sites of North America, Europe, Afric and NewZealand (15–35 days) by Teuling et al (2006). Inter-estingly, despite large differences across sites, therewere no significant differences within sites acrossmultiple years, and longer half-times were observedat sites experiencing seasonal droughts or at siteswith woody vegetation. Ourmuch shorter half-times

Figure 11. Soilmoisture content beneathMulga as an average of the top 10 cmdepth, September 2010–September 2011.

Figure 12.Monthly rainfall, January 2010–December 2011.

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may reflect the sandy soils, the impact of the veryshallow roots of Mulga and Mulga’s rapid phenolo-gical response to precipitation when conditions arefavourable (Cleverly et al 2016b).

The large rates of ET in the winter of 2010 and thelate summer and autumn of 2011 were mirrored bylarge rates of C uptake (figure 13). The half-time of thedecay in C uptake following rain was 7.2 days (Eamuset al 2013a). Unlike ET, which increased immediatelyfollowing rain, C uptake showed a 1–3 day delay.

The large rates of C uptake sustained from Sep-tember 2010 through to June 2011 are in markedcontrast to the short duration of C uptake in figure 7and in contrast to the annual totals for years2011–2015 (table 1), and reflect the impact of largeand sustained increase in soil moisture content dur-ing the 2010/2011 La Niña event. If we assume thatall Australia’s Mulga behave the same as theMulga inthe Ti Tree and all received similar increases in rain-fall, it is possible to estimate the contribution of Aus-tralia’s Mulga to the NEE anomaly quantified inPoulter et al (2014). Mulga covers approximately33% of the 70% of Australia that is semi-arid. Theanomalous increase in C uptake by the Ti TreeMulgawas 247 gC m−2 yr−1 (the difference between uptakein 2010–2011 and uptake in a 2013–2014 when rain-fall was average). This represents 0.435 Pg C yr−1 forthe entire Mulga estate, which accounts for about50%–70% of the anomaly identified by Poulter et al(2014) as originating in Australia (0.6–0.9 Pg Cyr−1). However, tree density of Mulga in the Ti Treeis larger than that of most Mulga in Australia and thecontribution of all Mulga is therefore likely to rangefrom 30% to 40%of the total anomaly.

5. EcosystemCandwater budgets: anecosystem services perspective

Ecosystem services are the goods and services providedby ecosystems that are of benefit to humans (Eamuset al 2005). Examples of ecosystem services includeerosion control, regulation of local and regionalclimate, C sequestration and the regulation of waterflows (surface, sub-surface and groundwaterrecharge). For terrestrial ecosystems, the provision ofecosystem services is dependent on neutral or positiveC and water budgets. A neutral or positive C budgetmeans no net loss or an accumulation of C within thecatchment. A neutral or positive water budget meansthat there is not a net export of water from thecatchment; for example, by over-extraction of ground-water (by human extraction). This raises the question:over what timeframe should C and water budgets bedetermined? It is clear that seasonally, Mulga canoscillate between being a net sink or a net source of C.Similarly, at an annual time-scale, Mulga can be a netsink or source of C. Mulga in the Ti Tree basin hasundoubtedly persisted for more than 50 yr, andprobably for considerably longer. Table 1 shows howwidely NEP and ET can vary across just four years ofstudy. Interestingly, a regression of NEP versus rainfallusing data in table 1 shows that when annual rainfallexceeded a threshold of 233 mm (R2=0.95), Mulgawas a sink but when rainfall is<233 mmMulga was asource. This is smaller than the thresholds of275–350 mm identified for several semi-arid ecosys-tems in south-western USA (Scott et al 2015), but, isconsistent with the approximately 100 mm differencebetween the threshold rainfall and the long-termaverage rainfall observed by Scott et al (2015). We

Figure 13.Daily ET (positive values) and daily carbon flux ( Fc, equal to−NEP), September 2010–August 2011. Redrawn fromEamuset al (2013a).

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estimate that this offset of 100 mm ensures that apositiveCbalancewill bemaintained in approximately70% of years (because only about 30% of years haverainfall less than this threshold).

In a recent analysis of the Ti TreeMulga, Chen et al(2014) concluded that annual vegetation water usevaried between 64 and 601 mm for the period1981–2012.Most importantly (from an ecosystem ser-vices perspective), groundwater recharge (noting thatthe Ti Tree basin may become a significant source ofpotable groundwater for industrial, irrigation anddomestic uses in central Australia) varied between 0and 48 mm yr−1 but significant rates of recharge werevery rare events, highlighting the need to extractgroundwater at sustainable rates for the long-termpreservation of this important resource.

It is clear that short-term (<5 years) studies of Cbalances for TDFs are unlikely to be adequate to pro-vide sufficient information to determinewhether part-icular locations are in a negative, neutral or positive Cbalance. This is because TDFs tend to have much lar-ger variability in the timing, intensity and amount ofrainfall than tropical rainforests and other mesicbiomes. This large degree of variability is reflected inthe large fluctuations between sink and sourcestrength. Furthermore, large inter-annual variabilityin rainfall and hence ET impacts on the provision ofwater resources (surface and groundwater), and thisshould inform management decisions on the timingand volume of water resource extraction. The size andmagnitude of changes in C storage pools (above-ground and below ground, biotic and abiotic) and therole of disturbance (for example fire and prolongeddrought) in C and water balances remain poorly docu-mented for much of the arid and semi-arid regions ofAustralia.

6.Mulga traits versus traits of co-occurringtree species

The Ti Tree basin contains three major ecosystems.The first is Mulga, dominated by Acacia spp., thesecond is riparian forest that follows the ephemeralrivers. The riparian forest is dominated by largeEucalyptus camaldulensis trees. Whilst the majority oftree species across the basin are evergreen (includingMulga and Eucalyptus camaldulensis), patches of thedeciduous Erythrina vespertilio occur in paleochannels(a remnant of an inactive river or stream that has beensubsequently infilled by younger sediment; Shanafieldet al 2015) and along ephemeral rivers. Ecohydrologi-cal niche separation theory (Silvertown et al 2015)predicts that co-occurring species should partitionwater resources through variation in traits related tothe uptake and transport of water. Table 2 summarisessome hydraulic traits of these three contrastingspecies. Comparisons of traits amongst these speciescontribute to our understanding of niche separation

and also to our understanding of how some species insemi-arid regions, such as Mulga, are so resilient. Thethird ecosystem in the Ti Tree is a sparse Corymbiasavannawhichwe do not discuss further.

Mulga is shallow rooted (<2 m), evergreen andlocated above a shallow hard pan (Cleverlyet al 2016b). Consequently it experiences very lowphyllode water potentials, both pre-dawn and midday(the limit of our pressure chamber was 10MPa, hencewe can only state that midday water potentials werelower than −10MPa). Several predictions can bemade about the traits that should be associated withsuch low water potentials. A key prediction is thatMulga should exhibit a high resistance to xylem embo-lism to avoid catastrophic loss of the ability to trans-port water to the canopy (Sperry and Tyree 1988). Ahigh resistance to embolism requires thick walledxylem conduits, which in turn results in a large wooddensity, coupledwith a small sapwood conductive areaand a concomitant small sapwood hydraulic con-ductivity. Similarly, wewould predict a large resistanceto vessel implosion (Hacke et al 2001). Finally, wewould predict a large water-use-efficiency, as indi-cated by an enrichment (closer to zero) of δ13C ofleaves. It is clear that Mulga does possess this suite oftraits (table 2), and this contributes to the ability of thisspecies to persist through multi-year periods of lowannual rainfall and the dry season that occurs eachyear. These traits also confer a low rate of tree water-use, as has been previously observed (O’Gradyet al 2009). Low rates of tree water use are also theresult of the large Huber values (Hv, ratio of sapwoodarea to leaf area; Eamus and Prior 2001) exhibited inMulga (table 2). For every m2 of sapwood, only about880 m2 of phyllode area is supported. This is muchsmaller than the 1800–2000 m2 of leaf area supportedby 1 m2 of sapwood in Eucalyptus camaldulensis andErythrina vespertilio. Changes in Hv in response tochanges in soil water availability are a common adap-tive strategy to differences in water availability (Toga-shi et al 2015, Zolfaghar et al 2015).

A high resistance to xylem embolism and the verylow leaf potentials experienced byMulga are also asso-ciated with the lowest water potential at zero turgor ofthe three species discussed herein. Lowwater potentialat zero turgor in Mulga is indicative of the accumula-tion of chemically inert compounds that confer pro-tection from water stress, and these osmoprotectivecompounds are known to occur in Mulga as nitrogen-rich compounds such as proline and glycine betaine(Erskine et al 1996). This is an important trait for shal-low rooted evergreen species in semi-arid regionsgrowing without access to groundwater. The main-tenance of positive turgor is required to drive cellgrowth and maintain open stomata, thereby allowingphotosynthesis to occur during periods of low soilmoisture availability.

By contrast, Eucalyptus camaldulensis and Ery-thrina vespertilio exhibit markedly different strategies

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from Mulga for persistence in this semi-arid environ-ment. Eucalyptus camaldulensis has access to ground-water and thus does not experience the very low pre-dawn and midday water potentials that occur inMulga. Eucalyptus camaldulensis is highly ground-water dependent and occurs predominantly as ripar-ian forest above shallow unconfined groundwater(<6 m depth). Because it is less reliant on rainfall, withyearlong access to groundwater, this species does notexperience low leaf water potentials, and thus does notrequire thick xylem cell walls to resists xylem embo-lism. Consequently the sapwood density and vesselimplosion resistance (Hacke et al 2001) are smaller inEucalyptus camaldulensis than in Mulga (table 2). Thiseasy access to groundwater and large conductive sap-wood area support much larger rates of transpirationthan observed in Mulga, despite high canopy waterpotential (relative to Mulga; O’Grady et al 2009). Tomaintain a large rate of transpiration and high canopywater potential requires a large sapwood hydraulicconductivity, as is observed (table 2). Furthermore,Eucalyptus camaldulensis has a larger (closer to zero)water potential at zero turgor than Mulga because itexperiences much larger canopy water potentials thanMulga. Finally, the δ13C of its leaves are much largerthan those of Mulga, reflecting its relatively lowWUE:the value recorded is close to that observed for leavesof Eucalypts growing in regions receiving >1500 mmrain per year. However, it does possess the capacity fora reduction in leaf area as a mechanism for adjustingwater use during prolonged dry periods (O’Gradyet al 2009), and mortality can occur in small trees dur-ing extended dry periods (Horner et al 2009).

Erythrina vespertilio has a similar strategy to Euca-lyptus camaldulensis for surviving semi-arid condi-tions, but with one important difference. LikeEucalyptus camaldulensis,Erythrina vespertilio does notexperience low canopy water potentials and therefore

has a low wood density, narrow fibre walls and a verylow vessel implosion resistance. It also possesses largecross-sectional areas of parenchyma, indicative of alarge capacity for water storage. Similarly, it has a largetheoretical hydraulic conductivity (table 2). However,it has ephemeral access to groundwater, occurring inpaleochannels which are sites of small amounts of run-on from precipitation and which contain perchedshallow water tables for short periods of time. Conse-quently the δ13C of leaves of Erythrina vespertilio (andhence WUE) is intermediate between Mulga andEucalyptus camaldulensis, and its Hv is also inter-mediate between these two species. However, the keytrait exhibited by this species is its deciduous habit. Bybeing an obligate deciduous species its canopy entirelyavoids periods of low soil and atmospheric water con-tent. Consequently it never experiences low canopywater potential and therefore its water potential at zeroturgor is very high (close to zero)—a trait that is asso-ciatedwith deciduous andmesic species.

7. Conclusions and future directions

TDFs experience warm/hot temperatures and a pre-dictable dry season. However, as we have shown forour Mulga site in central Australia and in agreementwith most other semi-arid and arid ecosystems, rain-fall is extremely variable in terms of the amount andtiming of precipitation. This has major impacts onphenological behaviour and concomitant productivityof such ecosystems. Mulga in this climate zone canoscillate repeatedly between being approximately Cneutral to being large C sinks and large C sources.Contrary to widely held expectations the behaviour ofsemi-arid ecosystems can impact significantly onglobal C and water cycles. An important feature of aridand semi-arid regions is the importance of

Table 2.Trait comparisons of three contrasting tree species in the Ti Tree basin. FromSantini et al (2016).

Trait

Acacia aneura

(Mulga)Eucalyptus camaldulensis

(River RedGum) Erythrina vespertilio

Phenology Evergreen Evergreen Deciduous

Groundwater dependent or not Not Highly Confined to paleochannels which act as sites

of run-on and possible short-lived perched

shallowwater table

Pre-dawn/midday leaf water

potentialMarch/April

2014 (MPa)

−7.2/<−10.0 −1.0/−2.4 −0.5/−0.9

Branch sapwood density (g cm−3) 0.95 0.65 0.4

Fibrewall thickness (μm) 4.01 3.31 2.80

Vessel implosion resistance (t/b)2 0.059 0.0237 0.0096

Conductive area (mm2mm−2) 0.098 0.258 0.249

Theoretical hydraulic con-

ductivity (kgmm−1

MPa−1 s−1)

0.109 0.328 0.383

Huber value 0.001696 0.00049 0.000554

Water potential at turgor loss −2.51 −1.13 −1.02

δ13C of leaves/WUE −26.96/82.38 −29.89/47.89 −27.45/75.26

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groundwater and associated terrestrial groundwaterdependent ecosystems both to human well-being andthe health and functioning of these landscapes. Thissynthesis has reiterated the importance of field eco-physiology, remote sensing and modelling to thegeneration of an in-depth understanding of thebehaviour and functioning of these regions (Eamuset al 2016).

Future work is required to examine the above-andbelow groundC storage pools and how these change atannual and decadal time-scales and to determine theresilience, sensitivities and and tipping-points ofMulga in the face of a changing climate. Since 1940,mean annual temperature in Alice Springs (200 kmsouth) has increased by approximately 1.5 °C, withassociated increases in VPD during all except the wet-test years. Since increased VPD and temperatureincrease the likelihood of forest mortality, (Eamuset al 2013b), the probability of mortality of Mulga islikely to also increase, thereby exerting a significantimpact on regional C and water budgets and globalproductivity (Poulter et al 2014), especially duringdroughts in the SouthernHemisphere. Althoughmor-tality and drought are not unusual for Mulga, whichwas found to experience up to 40% mortality duringthe 1964–1966 drought (Cunningham andWalker 1973), thus far, Mulga has shown resilience todrought and high temperatures, therebymaintaining aneutral carbon balance through drier-than-averageyears. Determining the climate thresholds that inducemortality (and recruitment; Mulga is a masting spe-cies, producing large seed crops only after exception-ally high rainfall years) and determining how theseeventsmight change in the future remains a significantresearch challenge.

Recent studies have found semi-arid ecosystems(including Mulga) to be particularly sensitive tohydroclimatic variability and are thus vulnerable tofuture climatic extremes (Ma et al 2015). Such sensitiv-ity suggests that maintaining ecosystem services andfunctioning of Mulga may be threatened in the future.Further studies are needed to examine the impact ofclimatic extremes on Mulga ecosystems to betterunderstand climate thresholds of this important Aus-tralian TDF. Finally, further investigations of themechanisms underpinning ecohydrological nicheseparation within these biomes is required to informland surface models and global dynamic vegetationmodels, which are increasingly used in ecological andecohydrological studies of TDFs.

Acknowledgments

This work was partially supported by an AustralianResearch Council grant and NCRIS grants awarded toDE. Tarin T, would like to thanks to the ConsejoNacional de Ciencia y Tecnologia (CONACyT) inMexico for a graduate fellowship (232184).

References

BaldocchiD 2008 Breathing of the terrestrial biosphere: lessonslearned from a global network of carbon dioxide fluxmeasurement systemsAust. J. Bot. 56 1–26

BaldocchiDD2011A synthesis of forest evaporation fluxes—fromdays to years—asmeasuredwith eddy covariance ForestHydrology and Biogeochemistry: Synthesis of Past Research andFutureDirections edDFLevia et al (Dordrecht: Springer)pp 101–16

Barron-GaffordGA, Scott R L, Jenerette GD,Hamerlynck E P andHuxmanTE 2012Temperature and precipitation controlsover leaf- and ecosystem-level CO2flux along awoody plantencroachment gradientGlob. Change Biol. 18 1389–400

BerryG, ReederM J and JakobC 2011 Physicalmechanismsregulating summertime rainfall over northwesternAustraliaJ. Clim. 24 3705–17

BoeningC,Willis J K, Landerer FW,NeremRS and Fasullo J 2012The 2011 LaNiña: so strong, the oceans fellGeophys. Res. Lett.39 L19602

BowmanD, BoggsG S, Prior LD andKrull E S 2007Dynamics ofAcacia aneura-Triodia boundaries using carbon (14C andδ13C) and nitrogen (δ15N) signatures in soil organicmatter incentral AustraliaHolocene 17 311–8

ChenC, EamusD,Cleverly J, BoulainN,Cook P, Zhang L,Cheng L andYuQ2014Modelling vegetationwater-use andgroundwater recharge as affected by climate variability in anarid-zoneAcacia savannawoodland J. Hydrol. 519 1084–96

Cleverly J, BoulainN,Villalobos-Vega R, GrantN, FauxR,WoodC,Cook PG, YuQ, Leigh A and EamusD2013Dynamics ofcomponent carbon fluxes in a semi-aridAcaciawoodland,central Australia J. Geophys. Res. 118 1168–85

Cleverly J, EamusD, LuoQ, RestrepoCoupeN,KljunN,MaX,EwenzC, Li L, YuQ andHuete A 2016a The importance ofinteracting climatemodes onAustralia’s contribution toglobal carbon cycle extremes Sci. Rep. 6 23113

Cleverly J et al 2016b Soilmoisture controls on phenology andproductivity in a semi-arid critical zone Sci. Total Environ.568 1227–37

Cleverly J et al 2016c Productivity and evapotranspiration of twocontrasting semiarid ecosystems following the 2011 globalcarbon land sink anomalyAgric. ForestMeteorol. 220 151–9

CrispMDandCook LG2013Howwas theAustralian floraassembled over the last 65million years? Amolecularphylogenetic perspectiveAnnu. Rev. Ecol. Evol. Syst. 44303–24

CunninghamGMandWalker P J 1973Growth and survival ofmulga (Acacia aneura F.Muell. ex Benth.) inwesternNewSouthWalesTropical Grasslands 7 69–77

DuursmaRA, BartonCVM, Lin Y S,Medlyn BE, EamusD,TissueDT, EllsworthDS andMcMurtrie R E 2014Thepeaked response of transpiration rate to vapour pressuredeficit infield conditions can be explained by the temperatureoptimumof photosynthesisAgric. ForestMeteorol. 189 2–10

EamusD, BoulainN,Cleverly J and BreshearsDD2013bGlobalchange-type drought-induced treemortality: vapor pressuredeficit ismore important than temperature per se in causingdecline in tree healthEcol. Evol. 3 2711–29

EamusD,Cleverly J, BoulainN,GrantN, FauxR andVillalobos-Vega R 2013aCarbon andwaterfluxes in an arid-zoneAcacia savannawoodland: An analyses of seasonalpatterns and responses to rainfall eventsAgric. ForestMeteorol. 182–183 225–38

EamusD,Duff GA andBerrymanCA1995 Photosyntheticresponses to temperature, lightflux density, CO2

concenrtation and vapour pressure deficit inEucalyptustetrodonta under CO2 enrichment Environ. Pollut. 90 41–9

EamusD,Huete A andYuQ2016VegetationDynamics: A Synthesisof Plant Ecophysiology, Remote Sensing andModelling (NewYork: CambridgeUniversity Press) 518pp

EamusD,Macinnis-NgCMO,HoseGC, ZeppelM J B,TaylorDT andMurray BR 2005 Ecosystem services: anecophysiological examinationAust. J. Bot. 53 1–19

16

Environ. Res. Lett. 11 (2016) 125011

EamusD andPrior L 2001 Ecophysiology of trees of the seasonallydry tropics: comparisons among phenologiesAdv. Ecol.Res.31 113–97

Erskine PD, Stewart GR, Schmidt S, TurnbullMH,UnkovichMandPate J S 1996Water availability—aphysiological constraint on nitrate utilization in plants ofAustralian semi-aridmulgawoodlands Plant Cell Environ. 191149–59

Fasullo J T, BoeningC, Landerer FWandNeremRS 2013Australia’s unique influence on global sea level in 2010–2011Geophys. Res. Lett. 40 4368–73

Flanagan LB andAdkinsonAC2011 Interacting controls onproductivity in a northernGreat Plains grassland andimplications for response to ENSO eventsGlob. Change Biol.17 3293–311

Flora of Australia 2002 vol 43 (Canberra: CSIROPublishing andAustralian Biological Resources Study)p 172&p 216

HackeUG, Sperry J S, PockmanWT,Davis SD andMcCullohKA2001Trends inwood density and structure are linked toprevention of xylem implosion by negative pressureOecologia126 457–61

HornerG J, Baker P J,MacNally R, CunninghamSC,Thomson J R andHamilton F 2009Mortality of developingfloodplain forests subjected to a drying climate andwaterextractionGlob. Change Biol. 15 2176–86

HuxmanTE, Snyder KA, TissueD, Leffler A J, Ogle K,PockmanWT, Sandquist DR, Potts D L and Schwinning S2004 Precipitation pulses and carbon fluxes in semiarid andarid ecosystemsOecologia 141 254–68

KanniahKD, Beringer J andHutley LB 2010The comparative roleof key environmental factors in determining savannaproductivity and carbon fluxes: a review, with specialreference toNorthern Australia Prog. Phys. Geogr. 34 459–90

KeenanTF et al 2014Net carbon uptake has increased throughwarming-induced changes in temperate forest phenologyNat. Clim. Change 4 598–604

KongQ andZhao S 2010Heavy rainfall caused by interactionsbetweenmonsoon depression andmiddle-latitude systems inAustralia: a case studyMeteorol. Atmos. Phys. 106 205–26

Kurc SA and Small E 2004Dynamics of evapotranspiration in semi-arid grassland and shrubland ecosystems during the summermonsoon season, centralNewMexicoWater Resour. Res. 40W09305

LeQuéré C et al 2014Global carbon budget 2013Earth Syst. Sci.Data 6 235–63

Luyssaert S et al 2007CO2 balance of boreal, temperate, and tropicalforests derived from a global databaseGlob. Change Biol. 132509–37

MaX,Huete A,Moran S, Ponce-CamposG and EamusD 2015Abrupt shifts in phenology and vegetation productivity underclimate extremes J. Geophys. Res. 120 2036–52

MaX,Huete A, YuQ, Restrepo-CoupeN, Beringer J, Hutley L B,KanniahKD,Cleverly J and EamusD 2014 Parameterizationof an ecosystem light-use-efficiencymodel for predictingsavannaGPPusingMODIS EVIRemote Sens. Environ. 154253–71

Ma J, Zheng X J and Li Y 2012The response of CO2flux to rainpulses at a saline desertHydrol. Process. 26 4029–37

MaX et al 2013 Spatial patterns and temporal dynamics in savannavegetation phenology across theNorth Australian TropicalTransectRemote Sens. Environ. 139 97–115

MartinHA2006Cenozoic climatic change and the development ofthe arid vegetation inAustralia J. Arid Environ. 66 533–63

Maslin BR andReid J B 2012A taxanomic revision ofMulga (Acaciaaneura and its close relatives: Fabaceae) inWesternAustraliaNuytsia 22 129–267

MigliavaccaM et al 2015 Influence of physiological phenology onthe seasonal pattern of ecosystem respiration in deciduousforestsGlob. Change Biol. 21 363–76

Miles L et al 2006A global overview of the conservation status oftropical dry forests J. Biogeogr. 33 491–505

Mott J J andMcCombA J 1975The role of photoperiod andtemperature in controlling the phenology of three annual

species from an arid region ofWesternAustralia J Ecol. 63633–41

Nano C EM andClarke P J 2010Woody-grass ratios in a grassyarid system are limited bymulti-causal interactions ofabiotic constraint, competition and fireOecologia 162719–32

Nicholas AMM, FranklinDC andBowmanDMJ S 2011 Floristicuniformity across abrupt boundaries betweenTriodiahummock grassland andAcacia shrubland on anAustraliandesert sandplain J. Arid Environ. 75 1090–6

NixHA andAustinMP1973Mulga: a bioclimatic analysisTropicalGrasslands 7 9–20

O’GradyAP, Cook PG, EamusD,DuguidA,Wischusen JDH,Fass T andWorldegeD2009Convergence of treewater usewithin an arid-zonewoodlandOecologia 160 643–55

Ogle K andReynolds J F 2004 Plant responses to precipitation indesert ecosystems: integrating functional types, pulses,thresholds, and delaysOecologia 141 282–94

Perkins S E, ArguesoD andWhiteC J 2015Relationships betweenclimate variability, soilmoisture, andAustralian heatwavesJ. Geophys. Res.: Atmos. 120 8144–64

Portillo-Quintero CA and Sanchez-Azofeifa GA 2010 xtent andconservation of tropical dry forests in theAmericasBiol.Conserv. 143 144–55

Poulter B et al 2014Contribution of semi-arid ecosystems tointerannual variability of the global carbon cycleNature 509600–3

PresslandA J 1976Effect of stand density onwater-use ofmulga(Acacia aneura F.Muell)woodlands in southwesternQueenslandAust. J. Bot. 24 177–91

Pui A, SharmaA, Santoso A andWestra S 2012 Impact of the ElNino-southern oscillation, IndianOcean dipole, andsouthern annularmode on daily to subdaily rainfallcharacteristics in East AustraliaMon.Weather Rev. 1401665–82

Pulla S, RamaswamiG,MondalN, Chitra-Tarak R, SureshHS,DattarajaH S, Vivek P, ParthasarathyN, RameshBR andSukumarR 2015Assessing the resilience of global seasonallydry tropical forests Int. Forestry Rev. 17 91–113

Restrepo-CoupeN,Huete A,Davies K, Cleverly J, Beringer J,EamusD, vanGorsel E,Hutley LB andMeyerWS 2016MODIS vegetation products as proxies of photosyntheticpotential: a look acrossmeteorological and biologic drivenecosystemproductivityBiogeosciences 13 5587–608

SantiniN S, Cleverly J, FauxR, LestrangeC, RummanR andEamusD 2016Xylem traits andwater-use efficiency of woodyspecies co-occurring in the Ti Tree basin arid zoneTrees 30295–303

Scott R L, Biederman J A,Hamerlynck E P andBarron-GaffordGA2015The carbon balance pivot point of southwesternU.S.semiarid ecosystems: insights from the 21st century droughtJ. Geophys. Res.: Biogeosci. 120 2612–24

ShanafieldM,Cook PG,Gutierrez-JuradoHA, FauxR,Cleverly J andEamusD2015 Field comparison ofmethodsfor estimating groundwater discharge by evaporation andevapotranspiration in an arid-zone playa J. Hydrol. 5271073–83

Silvertown J, Araya Y andGowingD2015Hydrological niches interrestrial plant communities: a review J. Ecol. 103 93–108

Specht RA and Specht A 1999Australian plant communities(Melbourne: OxfordUniversity Press) pp 492

Sperry J S andTyreeMT1988Mechanisms towater stress-inducedxylem embolism Plant Physiol. 88 581–7

TeulingA JM, Seniviratne S I,WilliamsC andTroch PA2006Observed time-scales of evapotranspiration response to soilmoistureGeophys. Res. Lett. 33 L23403

TogashiHF, Prentice I C, Evans B J, ForresterD I, Drake P,FeikemaP, BrooksbankK, EamusD andTaylorD 2015Morphological andmoisture availability controls of the leafarea-to-sapwood area ratio: analysis ofmeasurements onAustralian treesEcol. Evol. 5 1263–70

vanDijk A,DolmanA J and Schulze ED 2005Radiation,temperature, and leaf area explain ecosystem carbon fluxes in

17

Environ. Res. Lett. 11 (2016) 125011

boreal and temperate European forestsGlob. Biogeochem.Cycles 19GB2029

VanEtten E J B 2009 Inter-annual rainfall variability of aridAustralia: greater than elsewhere?Aust. Geogr. 40 109–20

Whitley R J,Macinnis-NgCMO,Hutley L B, Beringer J, ZeppelM,WilliamsM, TaylorD and EamusD2011 Is productivity ofmesic savannas light limited orwater limited? Results of asimulation studyGlob. Change Biol. 17 3130–49

Xie Z,Huete A, Restrepo-CoupeN,MaX,Devadas R andCaprarelli G 2016 Spatial partitioning and temporal

evolution of Australia’s total water storage under extremehydroclimatic impactsRemote Sens. Environ. 183 43–52

ZhaT S, Li CY, Kellomaki S, PeltolaH,WangKY andZhangYQ2013Controls of evapotranspiration andCO2fluxes fromScots pine by surface conductance and abiotic factors PloSOne 8 e69027

Zolfaghar S, Villalobos-Vega R, ZeppelM and Eamus D 2015 Thehydraulic architecture of Eucalyptus trees growing across agradient of depth to groundwater Funct. Plant Biol. 42888–98

18

Environ. Res. Lett. 11 (2016) 125011

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Mulga, a major tropical dry open forest of Australia: recent insights to carbon and water fluxes

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