The Effects of Drought on Amazonian Rain Forests

21 Pages·2009·0.73 MB·English

The Effects of Drought on Amazonian Rain Forests
P. Meir,1 P. M. Brando,2,3,4 D. Nepstad,5 S. Vasconcelos,6 A. C. L. Costa,7 E. Davidson,4
S. Almeida,8 R. A. Fisher,9 E. D. Sotta,10 D. Zarin,2 and G. Cardinot11
The functioning of Amazonian rain forest ecosystems during drought has become
a scientific focal point because of associated risks to forest integrity and climate.
We review current understanding of drought impacts on Amazon rain forests by
summarising the results from two throughfall exclusion (TFE) experiments in
old-growth rain forests at Caxiuanã and Tapajós National Forest Reserves, and
an irrigation experiment in secondary forest, near Castanhal, Brazil. Soil physical
properties strongly influenced drought impacts at each site. Over years 1 to 3 of
soil moisture reduction, leaf area index declined by 20–30% at the TFE sites. Leaf
physiology and tree mortality results suggested some species-based differences
in drought resistance. Mortality was initially resistant to drought but increased
after 3 years at Tapajós to 9%, followed by a decline. Transpiration and gross
primary production were reduced under TFE at Caxiuanã by 30–40% and 12–
13%, respectively, and the maximum fire risk at Tapajós increased from 0.27 to
0.47. Drought reduced soil CO emissions by more than 20% at Caxiuanã and
2
Castanhal but not at Tapajós, where N O and CH emissions declined. Overall, the
2 4
results indicate short-term resistance to drought with reduced productivity, but that
increased mortality is likely under substantial, multiyear, reductions in rainfall.
These data sets from field-scale experimental manipulations uniquely complement
existing observations from Amazonia and will become increasingly powerful if
the experiments are extended. Estimating the long-term (decadal-scale) impacts
of continued drought on Amazonian forests will also require integrated models to
couple changes in vegetation, climate, land management, and fire risk.
1School of Geosciences, University of Edinburgh, Edinburgh, 4Woods Hole Research Center, Falmouth, Massachusetts, USA.
UK. 5Gordon and Betty Moore Foundation, Palo Alto, California,
2Department of Botany, University of Florida, Gainesville, Flor- USA.
ida, USA. 6EMBRAPA-Amazônia Oriental, Belém, Brazil.
3Instituto de Pesquisa Ambiental da Amazônia, Belém, Brazil. 7Centro de Geociências, Universidade Federal do Pará, Belém,
Brazil.
8Museu Paraense Emilio Goeldi, Belém, Brazil.
Amazonia and Global Change 9Los Alamos National Laboratory, Los Alamos, New Mexico,
Geophysical Monograph Series 186 USA.
Copyright 2009 by the American Geophysical Union. 10EMBRAPA-Amapa, Macapa, Brazil.
10.1029/2009GM000882 11Instituto de Pesquisa Ambiental da Amazônia, Brazil.
429
430 EFFECTS OF DROUGHT ON AMAZONIAN RAIN FORESTS
1. INTRODUCTION drought events [Cox et al., 2008] and possibly also ENSO
events [Timmermann, 1999]. More generally with respect
Over the last decade, the possible impacts of drought have to climatic change over the twenty-first century, the multi-
become touchstone issues for environmental science and model data set (MMD) used in the IPCC Fourth Assessment
governance in Amazonia. The geographical size, biophysical Report projected an annual mean warming in Amazonia of
properties, and species diversity of Amazonian forests have 1.8°–5.1°C over this century, with rainfall reductions in parts
led to analysis of their role as providers of key environmen- of central and eastern Amazonia likely as a result, especially
tal services at all scales. Increased moisture limitation in the in the dry season [IPCC Working Group I, 2007]. In a recent
region is likely this century, and some of the services pro- analysis involving 23 MMD models, Malhi et al. [2008] re-
vided by forests, including the storage and sequestration of ported 20–70% agreement among models in the prediction
carbon, evapotranspiration, and the maintenance of species of substantial dry season reductions in precipitation across
diversity are potentially at risk. Human natural resource use Amazonia, with the greatest likelihood of drought in the east
intersects with these roles because of rapid land use change of the region.
and tends to magnify the likelihoods of drought and forest Second, land use change is likely to exacerbate the effects
degradation through fire. of climatic warming. Widespread forest conversion to pas-
There is uncertainty with respect to all of these outcomes, ture and agriculture is expected to reduce rainfall in the re-
governed by two core questions: (1) How likely, widespread, gion through differential effects on latent and sensible heat
and severe is future drought? (2) What is the likely impact transfer [Werth and Avissar, 2002; Chagnon and Bras, 2005;
of drought on forest ecosystem properties? In this chapter, Costa et al., 2007; Nobre et al., 1991] and increased regional
we address the latter question considering alterations to the atmospheric aerosol loading could cause widespread reduc-
carbon balance, transpiration, tree mortality, species-based tions in precipitation [IPCC Working Group I, 2007]. Over-
differences in drought responses, and vulnerability to fire. all, these results imply an increased frequency of extreme
Evidence of the response by forests to drought is often based events at the seasonal and interannual timescale, and a secu-
on observation of forest processes during natural droughts. lar shift to drought at decadal timescales, the strength of any
However, unusually for any region, three large-scale soil shift strongly influenced by land use change.
moisture manipulation experiments have been implemented
in Amazonia during the Large-Scale Biosphere-Atmosphere 2.2. Modeling Drought Impacts
(LBA) Experiment in Amazonia. These experiments are pro-
viding new tests of the modeled response by rain forest eco- Estimates of the impact of drought on Amazonian forests
systems to levels of drought that are beyond the bounds of have historically been made with limited field data, and this
recent climatic variation, but in line with some future cli- has contributed to uncertainty in estimates of future global
mate scenarios. A comparison and analysis of the first re- atmospheric CO concentrations [Meir et al., 2006; IPCC
2
sults emerging from these experiments forms the core of this Working Group I, 2007; Huntingford et al., 2009]. Recent
chapter and is used to summarize a view of the risks to, and analysis of the bioclimatic distribution of current natural
responses by, Amazonian rain forests experiencing drought Amazonian vegetation and the predictive output from 19
during the twenty-first century. global circulation models (GCMs) suggests that twenty-first
century climate change is most likely to lead to drier condi-
2. BACkGROUND tions more appropriate for seasonal forest in eastern Ama-
zonia [Malhi et al., 2009], although edaphic conditions may
2.1. Future Drought? in reality favor a transition to degraded forest or savanna. In
contrast, smaller impacts are likely on vegetation in western
Two main lines of evidence suggest that Amazonian Amazonia [Malhi et al., 2009]. Driving a vegetation model
drought may become more frequent and more severe during with a variety of climate scenarios, Sampaio et al. [2007]
this century. First, episodic drought has been associated with predicted a similar but more extreme range of forest-to-sa-
the occurrence of the El Niño–Southern Oscillation (ENSO), vanna switches following climatic warming and drying. In
caused by the warming of the tropical eastern Pacific Ocean, both cases, these decadal-century timescale scenarios were
and more recently in 2005, with abnormal warming of the based on some form of “equilibrium” vegetation response
northern tropical Atlantic Ocean, relative to the south [Cox to drought. In reality, the actual vegetation response will
et al., 2008; Marengo et al., 2008]. Future increases in green- be determined (rapidly or gradually) by multiple ecologi-
house gas concentrations coupled with reductions in global cal and physical processes, as acknowledged by the same
aerosol emissions may increase the likelihood of 2005-like authors.
MEIR ET AL. 431
By contrast, process-based dynamic vegetation models previously [Cochrane, 2003], and the fragmentation effects
have the structure to capture the relevant ecology, enabling of deforestation tend to increase fire risk strongly [Uhl and
land surface-atmosphere interactions to be modeled on a Kauffman, 1990; Cochrane and Laurance, 2002]. Deforest-
continuous basis. However, they are computationally ex- ation has repeatedly been shown to affect regional climate,
pensive and ultimately require observation-based, ecologi- though the effects vary with scale [Werth and Avissar, 2002;
cal parameterization [Prentice and Lloyd, 1998; Meir et al., Chagnon and Bras, 2005]. At large scale, deforestation
2008]. The first predictions of substantial Amazonian die- scenarios result in modeled reductions in precipitation and
back in response to warming and drought emerged from a relative humidity, and increases in temperature [e.g., Hoff-
global dynamic vegetation model (DGVM) framework and mann et al., 2003; Costa et al., 2007]. Strong increases in
were made at the decadal-century timescale, with relatively fire risk (20–120%) have thus been associated with scenarios
simplistic representations of canopy structure, soil processes, of partial and complete deforestation [Cardoso et al., 2003].
and functional diversity among species [White et al., 1999; While we need to understand the responses to drought by
Cox et al., 2000]. Large differences in parameterization and Amazonian rain forest, the interactions between drought and
mathematical description of core ecosystem processes have increased fire risk must also be considered, as fire may well
since been identified among DGVMs [Dufresne et al., 2002; be the agent that, in the context of secular or episodic cli-
Meir et al., 2006; Friedlingstein et al., 2006; B. Poulter et matic drying, triggers the switch from a forest to a savanna
al., Managing uncertainty of tropical Amazon dieback, sub- [Hutyra et al., 2005; Aragão et al., 2007].
mitted to Global Change Ecology, 2009; D. Galbraith et al.,
Quantifying the contributions of different environmental 2.3. Basin-Wide Observations of the Forest Carbon
factors to predictions of Amazonian rain forest dieback in Balance During Drought
three dynamic global vegetation models (DGVMs), submit-
ted to Global Change Biology, 2009], emphasizing the need Inversion studies have provided the largest scale of obser-
for improvements using field-based measurements and ex- vation-based information on drought effects on Amazonia.
perimentation. Nondynamic, but process-based, vegetation Despite the limitations of this method [see Houghton et al.,
and biogeochemical models have also been used to advance this volume], a net emission of CO from the region of up
2
the representation of Amazonian forest functioning [Lloyd to 1.5 Pg C a−1 has been reported for dry and warm periods
et al., 1995; Williams et al., 1998; Potter et al., 2004], al- during strong ENSOs [Bousquet et al., 2000, Rödenbeck et
though differences in process description have been ap- al., 2003, Zeng et al., 2005, see also Houghton et al., this
parent [Tian et al., 1998; Prentice and Lloyd, 1998; Foley volume], although it is unclear if these higher emissions are
et al., 2002; Zeng et al., 2005; Meir et al., 2008]. Only re- principally the result of changes in ecosystem carbon cy-
cently have detailed validations been made of the modeled cling or increased fire occurrence [Langenfelds et al., 2002;
response to drought and with some success over seasonal Meir et al., 2008]. Results from biogeochemical modeling
to interannual timescales [Fisher et al., 2007; Baker et al., of the forest carbon cycle have been consistent with the ob-
2008]. servation of net regional CO emissions during ENSO [e.g.,
2
The validation of longer-term vegetation dynamics is Tian et al., 1998; Foley et al., 2002; Zeng et al., 2005], but
more difficult because it requires data sets at the scale of the mechanisms underpinning these modeled results have
years to decades, representing multiple ecological processes. tended to overemphasize the role of the temperature sensi-
The multiyear soil moisture manipulation experiments de- tivity of soil respiration during drought [Meir et al., 2008].
scribed here provide unique insight into some of the relevant Phillips et al. [2009] recently reported basin-wide long-term
physiological and ecological processes. Also, they indicate observations of Amazonian forest productivity, estimating
the potential first steps in quantifying natural lags in veg- an overall negative impact of 1.2–1.6 Pg C in old growth
etation change as a function of tree species’ drought resist- forests during the 2005 drought, which was driven by lower
ance and regeneration characteristics. However, vegetation growth and (spatially patchy) increases in tree mortality.
change under climatic drying is influenced strongly by fire This outcome is consistent with the notion that gross pri-
and deforestation. The area of burnt understory forest during mary production (GPP) declines under drought, but without
the ENSO of 1998 (2.9 × 106 ha) was more than 10 times measurements of concurrent soil processes (e.g., CO efflux
2
greater than during an average rainfall year and twice the from soil), it does not resolve the question of the short-term
area of annual deforestation [Nepstad et al., 1999; Alencar impact of the 2005 drought on net ecosystem productivity
et al., 2006], while a burnt area up to 2800 km2 was attrib- (NEP). [NEP is the difference between carbon that is photo-
uted to fire leakage alone in the 2005 drought [Aragão et synthesised and respired by an ecosystem. NEP = GPP −
al., 2007]. Fire is more probable in forest that has burned R , (R = total ecosystem respiration).]
eco eco
432 EFFECTS OF DROUGHT ON AMAZONIAN RAIN FORESTS
In summary, analysis of basin-wide atmospheric and tree ing of drought impacts on Amazonian rain forest, mostly in
growth data has highlighted the importance of understand- relation to the cycling of carbon and water, but also includ-
ing NEP at different timescales, and identified large changes ing the emission of other trace gases such as CH , NO, N O,
4 2
in possible ecosystem functioning during interannual-scale and isoprene. Where possible, we make a first comparison
drought, including reductions in aboveground productivity, of the still-emerging experimental results. We ask three
increases in mortality in response to drought, and differential questions: (1) What have we discovered about the impact
tree species’ survival [cf. Engelbrecht et al., 2007]. These of drought at seasonal to interannual timescales? (2) What
data will be invaluable to validate estimates of tree growth have we discovered about the impact of drought at multiyear
from DGVMs or finer-scale vegetation models, but alone, to decadal timescales? (3) How does the combined impact
they do not pinpoint the mechanisms determining large-scale of fire and drought influence the risk of widespread loss of
CO exchange observed during intermittent severe drought forest in favor of smaller-stature vegetation types, such as
2
[e.g., Rödenbeck et al., 2003]. In particular, CO emission savanna or degraded forest?
2
processes have been hard to pin down, first because respira-
tion terms are often poorly quantified [Meir et al., 2008], 3. SOIL MOISTURE MANIPULATION ExPERIMENTS
and second, because the increases in fire occurrence identi- AT CAxIUANã, TAPAjóS, AND CASTANHAL
fied during ENSO or the 2005 drought [Nepstad et al., 1999;
Aragão et al., 2007] are hard to quantify in terms of CO Species diversity is substantial (>150–200 species ha−1)
2
emissions [van der Werf et al., 2004]. in the old-growth rain forests at both Caxiuanã and Tapa-
jós, while only four tree species (=70% of stems) dominate
2.4. Observations at the Stand Scale the regrowth forest at Castanhal. Standing biomass is much
larger at the rain forest sites (approximately 300 t ha−1 at
Some of the first eddy covariance measurements in Ama- Caxiuanã, 240 t ha−1 at Tapajós, and 50 t ha−1 at Castanhal)
zonia, quantifying the forest water and carbon cycles at the [Baker et al., 2004; Vasconcelos et al., 2004; Brando et al.,
scale of a few square kilometers, suggested little seasonality 2008]. Rain forest canopy heights are similar at 30–40 m,
in rain forest carbon exchange capacity [Grace et al., 1995]. while the height of the secondary forest at Castanhal is ap-
However, although not universal, seasonal drought effects on proximately 5 m [Coelho et al., 2004]. The soils at Caxiuanã
NEP have since been observed at some sites, with observed and Tapajós are highly weathered Oxisols, and at Castan-
changes in gross photosynthesis, respiration, and transpira- hal, the soil is a dystrophic yellow Latosol. At Caxiuanã,
tion across sites differing in seasonality yielding new in- the soil composition is a sandy loam (70–83% sand) with
sights into the functional basis of the response [Malhi et al., the water table at 15–20 m depth; at Tapajós, the composi-
1998; Carswell et al., 2002; Saleska et al., 2003; Vourlitis tion is more clay-rich and the soil profile is much deeper
et al., 2005; see da Rocha et al., this volume; Saleska et al., (60–80% clay; >100 m in depth); and at Castanhal, the soil
this volume; da Rocha et al., 2009]. is shallow and concretionary, with a high sand content (20%
Uniquely, experimental field manipulation of soil moisture clay, 74% sand). Annual precipitation at Caxiuanã, Tapajós,
enables the separation of the effects of otherwise naturally and Castanhal is approximately 2300, 2000, and 2500 mm
covarying environmental drivers (i.e., edaphic and atmo- a−1, respectively. Further site descriptions are provided else-
spheric variables) of the processes determining NEP and has where [Davidson, 1992; Nepstad et al., 2002; Ruivo et al.,
the potential to provide powerful insight into process-level 2003; Fisher et al., 2007; Vasconcelos et al., 2004].
responses to short-term and extended drought. Three such The method of physically excluding rainfall that penetrates
field experiments have been performed within LBA, all in the canopy (“throughfall exclusion” (TFE)) was replicated
drought-threatened eastern Amazonia. Strong soil moisture at Caxiuanã and Tapajós using approximately six thousand
deficit has been imposed over 1 ha of old-growth forest 4.5 m2 plastic panels and guttering placed at 2 m above the
at two experimental sites, in the National Forest Reserves ground. The infrastructure removed approximately 50% of
of Caxiuanã (near Portel, State of Pará) and Tapajós (near incoming precipitation [Nepstad et al., 2002; Fisher et al.,
Santarém, State of Pará) [Nepstad et al., 2002; Fisher et 2007] (Table 1) and was installed at the beginning of 2000 at
al., 2007; Meir et al., 2008], and at a third site, dry-season Tapajós and 2002 at Caxiuanã. Each experiment comprised
moisture stress has been reduced though the irrigation of 1 ha of TFE forest and 1 ha of undisturbed (nonmanipulated)
replicated 0.04-ha plots in secondary regrowth forest near “control” forest. The large scale of the manipulation was nec-
Castanhal, State of Pará [Vasconcelos et al., 2004]. essary because of substantial lateral extension of the surface
The remainder of this chapter is concerned primarily with roots of large trees. Treatment replication at both sites was
how the results of these experiments inform our understand- limited by financial resources, but pretreatment calibration
MEIR ET AL. 433
Table 1. Total Incoming Precipitation for Each Year of the Drought Treatment by Dry (Panels Off)
and Wet Season (Panels On)a
Precipitation, mm
Panels On
Year Period of Exclusion Total Incoming Panels Off (Throughfall Excluded)
2000 1 Feb to 8 july 2517 830 1687 (844)
2001 1 jan to 31 july 1882 171 1711 (856)
2002 1 jan to 31 july 1958 292 1665 (833)
2003 21 jan to 14 Aug 1690 394 1295 (648)
Totals 8047 1687 6358 (3179)
aApproximately 50% of incoming precipitation was excluded when the panels were on; those
volumes are presented in parentheses.
measurements were made in all plots to enable replication in all plots, and the relatively small stature of the vegetation
over time [Davidson et al., 2004], and the method follows allowed lower-canopy access for leaf water potential mea-
the design of other unreplicated large-scale ecosystem ma- surements [Fortini et al., 2003].
nipulation experiments [e.g., Likens et al., 1970], whose
strength is acknowledged, especially where large treatment 4. SEASONAL TO INTERANNUAL
effects are expected [Hurlbert, 2004]. The perimeter of the DROUGHT IMPACTS
TFE plots was trenched to 1–2 m depth to prevent the hori-
zontal ingress of water from adjacent normally watered soil, 4.1. Soil Moisture and Its Supply to Plants
and the control plot perimeters were also trenched to avoid
confounding treatment effects. Soil and plant measurements The change in soil moisture, in relation to adjacent un-
were made more than 20 m inside the perimeter of each plot disturbed (control) forest, was the main experimentally
to further eliminate confounding treatment effects. Manage- manipulated parameter in each experiment. The TFE infra-
ment of the experiments was similar, except that at Tapajós, structure at Caxiuanã and Tapajós resulted in reductions in
the panels were removed during the peak dry season, while plant available water (PAW) of 80–200 mm in the top 3 m
at Caxiuanã, this procedure was not followed because of the of soil (Table 1 and Figure 1a) [Fisher et al., 2007, 2008;
prevailing late dry season storm risk [Carswell et al., 2002]. Brando et al., 2008], while the irrigation at Castanhal nearly
Litterfall was manually returned to the soil, where it fell on completely removed the dry season moisture constraints
the TFE paneling. Full canopy access was provided using 40 [Vasconcelos et al., 2004]. A strong seasonality was evident
m towers in all plots, also enabling the installation of on-site in PAW at the TFE experiments, and the rate of soil moisture
automatic weather stations. Principal access to the soil was drawdown was larger over the first 1–3 years at Caxiuanã
provided by four soil shafts per plot, excavated to a maxi- than at Tapajós.
mum depth of 10 m at Caxiuanã and 14 m at Tapajós. The impact on PAW of manipulating precipitation input
The irrigation experiment at Castanhal was designed to to the soil was strongly modified by the soil properties at
remove dry season moisture stress and began in 1999 [Vas- each site. At Caxiuanã, the sandy-loam composition created
concelos et al., 2004]. Plot size was 20 m × 20 m (0.04 ha), a relatively high moisture holding capacity per unit volume
and four replicate plots were used to contrast irrigated and [Carswell et al., 2002; Fisher et al., 2008], while the deep
undisturbed vegetation; adjacent plots were placed 10 m or clay-rich soil at Tapajós potentially held substantial water
more apart and a nested 10 m × 10 m plot in each 0.04 ha reserves mainly because of its exceptional soil volume [Nep-
main plot was used for measurements. An additional treat- stad et al., 2002; Belk et al., 2007]. Detailed measurements
ment removing litter was also implemented at Castanhal, but of soil hydraulic properties [e.g., Tomasella and Hodnett,
is not discussed here. Ground-level irrigation was provided 1997] remain rare in Amazonia, but variation in the key soil
using perforated microtape installed at 2-m spacings; water parameters determining PAW, soil water potential, hydrau-
was applied at a rate of approximately 5 mm d−1 for 30 min lic conductivity, and moisture volume content, can cause
during the dry season. The amount of irrigation was selected large and basin-wide differences in the supply of water to
to approximately replace daily evapotranspiration estimated plants under moisture stress [Fisher et al., 2008]. Analo-
regionally (660–790 mm) [Jipp et al., 1998, Vasconcelos et gously, the shallow concretionary soil structure at Castanhal
al., 2004]. Surface soil moisture availability was measured likely contributes to moisture limitation of root and micro-
434 EFFECTS OF DROUGHT ON AMAZONIAN RAIN FORESTS
(a)
(b)
Figure 1. (a) Plant available water (PAW) over wet and dry seasons in the control (filled symbols) and throughfall ex-
clusion (TFE) plots (open symbols) for both experiments Tapajós (circles) and Caxiuanã (triangles). The experiment in
Caxiuanã began in 2001, and in Tapajós, it started in 1999 (pretreatment). PAW is the water available to plants between
field capacity and a soil moisture potential of −1500 kPa. The arrow shows when TFE infrastructure was installed at each
site. The data points are derived from 48 fortnightly measurements made per soil access shaft, four access shafts per plot
[Brando et al., 2008; Fisher et al., 2007]. (b) Monthly natural rainfall, soil water balance, and annual soil water deficit
at Caxiuanã, 1999–2004. Maximum PAW at Caxuiana is ~400 mm water (a) [Fisher et al., 2008]; under normal rainfall,
soil moisture supply is sufficient to support transpiration, but under strong drought, moisture limitation is likely.
MEIR ET AL. 435
bial activity during the natural dry season [Vasconcelos et Table 2. Minimum Leaf Water Potential (Min ψ) Measurements
l
al., 2004]. More soil hydraulics data from across the region for Tree Species at the Caxiuanã and Tapajós TFE Experiments
are required to make satisfactory PAW calculations for the and the Castanhal Irrigation Experimenta
modeling of vegetation activity. Site Species Min ψb, MPa
l
The supply of moisture from soil to leaf is also affected
T Aparisthmium cordatum −1.5
by site differences in rooting properties. Rooting depth can T Astrocaryum gynacanthum −1.5
be substantial, enabling increased access to soil water: roots T Coussarea racemosa −2.7
have been detected at depths >14 m at Tapajós and at Cax- T Poecilanthe effusa −2.4
iuanã, to the approximate maximum depth of excavation, C Licaria ameniaca −2.2
9 m [Nepstad et al., 2004; Fisher et al., 2007]. As well as C Hirtela bicornis −2.1
enabling fuller exploration of the soil profile, deep rooting C Lecythis confertiflora −2.9
C Swartzia racemosa −3.2
can also facilitate hydraulic redistribution, thus further help-
Cs Miconia ciliate −3.0
ing to maintain rhizosphere moisture availability and plant
function under reduced rainfall, as observed at Tapajós in aAbbreviations are C, Caxiuanã; T, Tapajós; Cs, Castanhal.
some instances [Oliveira et al., 2005]. Initial data have not bValues for T and C are taken from trees in the TFE plots, and
values for Cs are from an understorey species (data from Fisher et
identified major changes in root dynamics at Tapajós in the
al. [2006], Fortini et al. [2003], and G. Cardinot et al., manuscript
TFE treatment [Brando et al., 2008]. However, responses
in review, 2009).
in the modes of root growth at Caxiuanã are partially con-
sistent with theory [Joslin et al., 2000; Schymanski et al.,
2008]. As the drought progressed at Caxiuanã, surface roots tional evidence of direct uptake of dew in two species at the
(0–30 cm) tended to increase in length per unit mass, thus Tapajós experiment (G. Cardinot et al., manuscript in re-
increasing the explored soil volume [Metcalfe et al., 2008], view, 2009) suggest likely differences in survivorship under
but it is less clear how plastic root growth responses were to drought at multiyear or decadal time scales.
changes in the vertical distribution of soil moisture availabil-
ity within the soil profile, and answering this question will 4.2. Canopy Structure and Productivity
have implications for modeling resilience to drought. Spe-
cies variation in these root properties differentially affects Although some savanna tree species have a deciduous or
water acquisition among species and between sites, and vari- brevi-deciduous phenology [Furley et al., 1992], this strat-
ation in resistance to drought was also observed in the foli- egy is relatively unusual in rain forests, where leaf area index
age. Leaves generally experience maximum daily moisture (LAI, m2 leaf area per m2 unit ground area) is maintained un-
limitation at high atmospheric moisture deficit, soon after der normal climatic variation. There is some ground-based
midday. Early afternoon measurements of the minimum leaf evidence for dry-season increases in LAI [Carswell et al.,
water potential tolerated by tree species at Caxiuanã, Tapa- 2002] and albedo [Culf et al., 1995], but irrespective of how
jós, and Castanhal demonstrated differences among species this may affect forest functioning, it seems that PAW can
(Table 2), although the minimum value measured in both often be maintained by forest trees through extensive and
TFE plots was similar (−3.2 and −2.7 MPa, respectively), sometimes exceptionally deep rooting systems [Nepstad
indicating a possible maximum tolerance to moisture limita- et al., 1994; Bruno et al., 2006]. However, under moisture
tion in eastern Amazonian rain forest trees. Stem hydraulic constraints in excess of normal climatic variation, we have
conductance did not appear to be the major constraint to leaf limited understanding of the limits to moisture access by for-
water supply at low soil PAW, but species-based differences est trees. The TFE experiments thus provide a direct way of
in this parameter were also observed at Caxiuanã [Fisher et determining the thresholds in PAW that may lead to changes
al., 2006] potentially further influencing species-based dif- in canopy productivity, LAI, and fire vulnerability.
ferences in resistance to soil moisture limitation [cf. Franks The LAI at both sites was resistant to strong artificial
et al., 2007]. soil moisture deficit for about a year following installation
In summary, substantial differences in soil properties at of the TFE infrastructure, remaining at 5–6 m2 m−2. After
each experimental site strongly influenced the storage of wa- 12 months, and a reduction in PAW of about 150–200 mm,
ter in soil and its supply to plant roots under drought. The LAI declined to 70–80% of the control (and original) values
TFE results from Tapajós and Caxiuanã also highlighted at each site (Figure 2), and this reduction was maintained
mechanisms conferring tolerance to drought in terms of subsequently following three more years of TFE (Brando
root, stem, and leaf hydraulic properties. Variation among et al., 2008, D. B. Metcalfe et al., Impacts of experimen-
tree species in these responses to drought, including addi- tally imposed drought on leaf respiration and morphology
436 EFFECTS OF DROUGHT ON AMAZONIAN RAIN FORESTS
Figure 2. Variation in leaf area index (LAI) during the TFE experiments at Caxiuanã and Tapajós. LAI is expressed as
the quotient of (TFE plot LAI) / (Control plot LAI). LAI in undisturbed forest at both sites is 5–6 m2 m−2. The arrow
denotes when the TFE infrastructure was installed at each site. (LAI was measured using a Li2000 (Licor, USA) at fixed
100 points [Brando et al., 2008; Fisher et al., 2007; Metcalfe et al., submitted manuscript, 2009]).
in an Amazon rain forest, submitted to Functional Ecology, In summary, initial resistance to change in LAI during the
2009). However, litter production patterns differed among first 12 months of soil drought at both TFE experiments was
sites, perhaps partially reflecting differences in tree commu- followed by substantial reductions in LAI of 20–30% over
nity responses to moisture limitation. At Caxiuanã, litterfall the following 2 years, and this was maintained subsequently.
in the TFE plot declined within the first 12 months following Dry season litterfall declined at Caxiuanã relative to undis-
installation of the TFE and remained lower than undisturbed turbed forest, but artificial droughting and irrigation had only
forest over the following dry seasons. At Tapajós in the small effects on litterfall at Tapajós and Castanhal. Drought
TFE plot, and at Castanhal under irrigation, litterfall did not impacts on forest canopy physiology and structure have also
change significantly and tracked the control forest litter flux been examined using remote sensing data products [Asner
rates closely in the first 2–3 years of rainfall manipulation et al., 2004; Saleska et al., 2007; Huete et al., 2008, see
(Figure 3). The reduction in LAI and subsequent litterfall at also Saleska et al., this volume]. It remains unclear if these
Caxiuanã is consistent with reduced leaf regrowth, while the data can be used to reliably quantify changes in productivity
maintenance of litterfall at Tapajós and Castanhal suggests a during drought, but the TFE experiments provide a way of
stronger limitation on leaf replacement. However, observed specifying models to test such estimates. The consequences
increases in leaf mass per unit area during experimental of reduced LAI for alterations in gas exchange capacity and
drought also contributed substantially to changes in LAI at fire vulnerability are considered below.
Caxiuanã and Tapajós [cf. Wright et al., 2006; Metcalfe et
al., submitted manuscript, 2009; Tohver et al., unpublished 4.3. Trace Gas Emissions From Soil
data, 2007]. Finally, changes in leaf turnover rates, and the
temporary impacts of mortality events after three years or The flux of CO from soil (“soil respiration,” R), com-
2 s
more (data not shown) may help explain litterfall patterns prises the largest single respiratory flux in the terrestrial
over the longer term at Tapajós and Castanhal [Brando et al., carbon cycle and derives from the combined respiration
2008; Vasconcelos et al., 2008]. of heterotrophic (microbial, faunal) and autotrophic (root)
MEIR ET AL. 437
Figure 3. Seasonal litterfall (±SE) at Caxiuanã, Tapajós, and Castanhal from 1999 to 2004. The arrows denote when
the TFE or irrigation treatments were installed. The data are derived from 20 litter traps (1 m2) per plot; litterfall was
collected fortnightly or monthly at each site [Brando et al., 2008; Vasconcelos et al., 2008; Meir et al., manuscript in
preparation, 2009].
components of the soil biological community [Trumbore, significant [Sotta et al., 2007]. After 3–4 years, dry season
2006; see also Trumbore and de Camargo, this volume]. R R in the Caxiuanã TFE plot remained lower than for soil
s s
has been reported for all three experiments, and additional in undroughted forest, although overall between-plot dif-
measurements of NO, N O, and CH have also been made at ferences in R were smaller, perhaps because of increased
2 4 s
Tapajós and Castanhal. wet-season root respiration rates in the TFE plot [Metcalfe
Consistent with biophysical expectation [Howard, 1979; et al., 2007]. At Castanhal, the difference in R between ir-
s
Meir et al., 2008], seasonal declines in R under reduced rigated and undisturbed soil reached maxima during the dry
s
soil moisture have been observed widely in Latin American seasons, and annual R in irrigated plots was 13–27% larger
s
rain forests [Davidson et al., 2000; Schwendenmann et al., than on undisturbed (drier) plots [Vasconcelos et al., 2004].
2003]. While the experimental manipulation of soil moisture In contrast, at Tapajós, although the gross fluxes were not
lowered R strongly during the first 2 years at Caxiuanã (by unusual in magnitude, R was similar between the TFE and
s s
>20%, equivalent to >2 t C ha−1 a−1; Figure 4) [Sotta et al., control plots throughout the experiment, even after 5 years
2007], the response of R to temperature was small and non- of TFE treatment [Davidson et al., 2008]. This outcome was
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438 EFFECTS OF DROUGHT ON AMAZONIAN RAIN FORESTS
Figure 4. Soil respiration (CO efflux from soil, R) at Caxiuanã, Tapajós, and Castanhal. TFE or irrigated plots (gray
2 s
triangles) are plotted against control plots (black filled circles) at each site. Measurements were made by infrared gas
analysis, using permanently installed collars. Data are presented as monthly means ±SE (n = 20 at Caxiuanã and Tapajós,
n = 12 at Castanhal), with the experimental soil moisture manipulations beginning at month 0. Inset: the relationship
between soil moisture potential and R from Caxiuanã. Data are from Vasconcelos et al. [2004], Sotta et al. [2007], and
s
Davidson et al. [2008]. Inset from Sotta et al. [2007], reprinted with permission from Wiley-Blackwell.
surprising given the seasonal variation in PAW at Tapajós, but was not detected using the time domain reflectometry
and the close tracking of R with seasonal PAW in the TFE instruments installed there [Nepstad et al., 2002; Oliveira
s
plot at Caxiuanã (Figures 1 and 4). The similarity in R be- et al., 2005], then autotrophic and heterotrophic respiration
s
tween TFE and control plots at Tapajós is consistent with may have continued in the roots and rhizosphere, respec-
the similarity in total litterfall and the radiocarbon-derived tively, maintaining relatively high R even at the low PAW
s
ages of respired carbon from both plots. This has led to the measured in the TFE plot, although how (or if) R and GPP
s
suggestion that the unusually large soil and rooting depths at were differentially affected by such levels of rhizosphere
Tapajós explains the unexpected maintenance of normal R moisture availability remains unexplored at Tapajós.
s
fluxes under drought, although increased root mortality and Emissions of NO, N O, and CH were also measured at
2 4
decomposition in the TFE plot may also have been responsi- Tapajós and Castanhal. Moisture limitation effects on each
ble [Brando et al., 2008; Davidson et al., 2008]. An additional followed biophysical expectation [Forster et al., 2007], al-
possible explanation is that the role of hydraulic redistribu- though NO emissions were more resistant to change than
tion has been underestimated. For example, if nighttime re- expected. At the Tapajós TFE experiment, N O emissions
2
covery of rhizosphere moisture content occurred at Tapajós, declined, and CH consumption increased at low soil mois-
4