CENTENARY SYMPOSIUM SPECIAL FEATURE ESSAY REVIEW
The productivity,metabolism and carbon cycle of tropical forest vegetation
Yadvinder Malhi*
School of Geography and the Environment,University of Oxford,South Parks Road,Oxford OX13QY,UK
be cruel to be kindSummary
1.Tropical forests account for one-third of the total metabolic activity of the Earth’s land surface.Hence,understanding the controls on tropical forest photosynthesis and respiration,and the alloca-tion of the products of photosynthesis to canopy,woody tissue and rhizosphere,is important to understand global ecosystem functioning.
2.I review how studies in tropical ecosystem ecology have progresd since their inception in the 1960s towards developing a quantitative,mechanistic and global description of the carbon cycle of tropical vegetation.
3.I prent a synthesis of studies in tropical forest sites in the Americas and Asia for which gross primar
y productivity (GPP)has been reported,and a subt of the sites for which net primary pro-ductivity (NPP)and ecosystem carbon u efficiency (CUE)have been estimated.GPP ranges between 30and 40Mg C ha )1year )1in lowland moist tropical forests and declines with elevation.CUE in tropical forests is at the low end of the global range reported for forests.
4.A pathway and framework are prented to explain the link between photosynthesis and tropical forest biomass,and to explain differences in carbon cycling and biomass between forests.Variation in CUE and allocation of NPP can be as important as variation in GPP in explaining differences in tropical forest growth rates between sites.
5.Finally,I explore some of the key questions surrounding the functioning and future of tropical forests in the rapidly changing conditions of the early Anthropocene.
ohm6.Synthesis .There have been significant recent advances in quantifying the carbon cycle of tropical forests,but our understanding of caus of variation amongst forests is still poor.Moreover,we should expect all tropical forests in the 21st century,whether intact or disturbed,to be undergoing rapid change in function and composition;the key challenge for tropical ecosystem ecologists is to determine and understand the major and most fundamental aspects of this change.
Key-words:Anthropocene,carbon u efficiency,ecophysiology,ecosystem ecology,eddy covariance,global change,gross primary productivity,net primary productivity,photosynthesis,tropical ecology
Introduction
knockoverSince the days of earliest European scientific expeditions,scien-tists and naturalists have remarked on,and been inspired by,the productivity,diversity and abundance of the tropical forest regions.To Europeans arriving from the wintry climes of Europe in the Little Ice Age (16–19th Century),the wet tropics provided a vision of nature t free from the restrictions of cold and drought (Bates 1864).This impression of the bountiful tropics was later muted by the realization of an apparent
contradiction:that the high productivity and biodiversity of the tropics were often bad on very infertile soils.The soils are infertile due to their ancient status,not having undergone glacial weathering or benefitted from post-glacial deposition;and rapid leaching due to high rainfall and temperature.
Attempts to quantify the productivity of tropical forests began in the early 20th century,when colonial-era foresters first took an interest in managing timber yields from the for-ests (albeit with an inevita
speble focus on commercial species).The early studies focusd on wood productivity of commer-cial species as the most apparent and economically important aspect of tropical forest productivity.A more holistic and
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*Correspondence author.E-mail:yadvinder.ac.uk
Ó2012The Author.Journal of Ecology Ó2012British Ecological Society
Journal of Ecology 2012,100,65–75doi:
10.1111/j.1365-2745.2011.01916.x
ecology-focusd approach to carbon and nutrient cycling in forests began with the emergence of ecosystem ecology as a distinct branch of ecology,with the ecosystem as a primary focus of attention(Tansley1935;Hagen1992).Ecosystem ecology focuss on quantifying physicalflows of energy and matter(water,carbon and nutrients)through ecosystems,and on the role that physiological process play in the develop-ment and persistence of ecosystems.Challenging rearch in the tropics was boosted by the advent of the International Biological Programme(IBP),with a stated objective of deter-mining‘the biological basis of productivity and human wel-fare’.Tropical forest ecosystem ecology particularly advanced in the late1960s,when the pioneer of thisfield,Howard T.Odum,attempted thefirst detailed description of large-scale ecosystem process at the Luquillo Experimental Forest in Puerto Rico(Odum&Pigeon1970;Jordan1971),with the(in retrospect)rather unorthodox approach of killing an area of forest by dousing it with gamma rays(!).
The next major location for tropical ecosystem ecology was Pasoh Forest in Peninsular Malaysia,where the IBP supported efforts at measuring tropical productivity by a predominantly Japane team(Kira1978).The work demonstrated that it was possible(and provided the detail required)to quantify produc-tivity through the measurement of the components of net primary product
ivity(NPP)and autotrophic respiration. The approaches for studying ecosystem carbonflows were ‘bottom-up’in that they required the measurement of individ-ual components of productivity,respiration and photosynthe-sis,often on individual plants.The key challenge,and one which still haunts current-day efforts,was one of scale:how to scale up from measurements of individual components on indi-vidual trees,to the properties of the forest stand?The attempts were also challenged by the technology of the1970s, when technology for the measurement of carbon dioxide in the field was in its infancy.
学美甲
The challenge of scale began to be tackled from a completely different direction,and by a rather different scientific commu-nity,in the1980s,with the development of micrometeorologi-cal approaches to measure theflow of carbon dioxide between the forest canopy and the atmosphere.Micrometeorological approaches to energy and water budgets had been around since the1960s,but the advent offield-portable fast-respon CO2analyrs and fast-respon sonic anemometers enabled the advent of eddy covariance techniques,where the turbulent transfer of energy,CO2and other trace gas could be directly measured.For thefirst time,the bulk ecosystemfluxes between the vegetation and the atmosphere could be quantified with a ‘top–down’approach.Such techniques measured the netflow of carbon between the forests and the atmos
phere,a combina-tion of plant photosynthesis,autotrophic(plant)respiration and heterotrophic(predominantly fungal and microbial)respi-ration.The netflow of carbon was termed the net ecosystem exchange(NEE)or net ecosystem productivity.Measurement of the NEE was the primary driver of the efforts,in an attempt to asss whether old-growth tropical forests were in equilibrium with the atmosphere or in diquilibrium becau of global atmospheric change or past disturbance.Such attempts at quantifying NEE have generally proved frustrating in the tropical forest environment,where there is a tendency for night-time respiration to be underestimated as cool,carbon dioxide-rich air tends to pool andflow laterally in the below-canopy air space(Finnigan et al.2003;Araujo et al.2008). This problem is particularly acute in tropical forest environ-ments becau the below-canopy space is large,nocturnal wind speeds tend to be low and bulk respirationfluxes are large (hence small proportional errors in respiration become large absolute errors in net carbon balance).However,theflux mea-surements also prove uful in quantifying the gross primary productivity(al canopy photosynthesis)of tropical forests.This can be achieved by estimating how the ecosystem respirationfluxes vary through the day bad on night-time respiration measurements and then subtracting the estimated ecosystem respiration from the NEE(Reichstein et al.2005).
Thefirst reported tropical forest eddy covariance study was a short campaign in the late1980s at the Ducke Forest near Manaus,Brazil(Fan et al.1990).Such studies proliferated and expanded in duration in the1990s and2000s,notably in Brazil-ian Amazonia(Grace et al.1995;Malhi et al.1998)followed by a major expansion under the Brazil-led Large-Scale Bio-sphere-Atmosphere Project in Amazonia(Araujo et al.2002; Carswell et al.2002;Miller et al.2004)and also in French Gui-ana(Bonal et al.2008)and Costa Rica(Loescher et al.2003). In the2000s,they also spread into tropical Asia,in Malaysia (Kosugi et al.2008),Thailand,Indonesia(Hirano et al.2007) and the southern tropical fringe of China(Tan et al.2010). Theflux-bad approaches have been able to give insights into how productivity and metabolism are affected by varia-tion in light,temperature and moisture availability,at scales ranging from minutes to years.On their own,however,they are unable to tea apart the internal components and mechan-ics of the forest carbon cycle.To do this,it is necessary to stay with the‘bottom-up’approach pioneered by Odum,Kira and others,but this time utilizing the more advanced andfield-ready gas exchange technology that is now available,and pos-sibly combining the approaches with new tools such as isoto-pic fractionation and DNA studies of soil microbial populations.Such an approach is able to provide a more com-prehensive picture of the carbon cycle and dynamics of tropical forests(Chambers et al.2004;Malhi et al.2009b;Tan et al. 2010)to answer some long-standing questions and po some new ones.An example of such a comprehensive pictu
re is given in Fig.1,for a site in Brazilian Amazonia.Currently I am coordinating a major effort to expand such work across the tropics,with sites in the wet and dry forests of Amazonia, along an elevation tranct in the Andes,in forests in West and Central Africa and in Borneo,with an explicit aim of collecting data from sufficient sites to tea apart the variation of tropical forest functioning along environmental gradients(rainfall,ele-vation,soil type)within the tropical forest zone.
Today,tropical ecosystem ecology(and ecosystem ecology in general)forms a bridge between the realm it has traditionally occupied,that of being a branch of ecology focusd on understanding the detailed functioning and
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interactions of particular systems,and the relatively new realms of Earth System science and global change ecology, where tropical forests have been recognized as a major influence on global biogeochemical cycles and atmospheric function.The new disciplines take the philosophical per-spective of ecosystem ecology up further in scale,treating whole biomes or the global biosphere as the primary unit of study.The modus operandi of ecosystem ecology has been site-specific studies,of
ten involving laborious data collection in sometimes challenging locations.In contrast,the core toolkit of the terrestrial aspects of Earth system science is increasingly centred around terrestrial ecosystem model sim-ulation,coupled with satellite remote nsing data and eddy covarianceflux tower data,but needing to be grounded with field data(and ideally networks offield sites)where possible. One of the key challenges is to work out how much detail is needed to accurately reprent the function and nsitivity of tropical forests in the Earth’s system.Do details in the process of carbon production,allocation and turnover matter?Are there important biogeographical differences in ecosystem function between,for example,the legume-rich forests of Amazonia and the dipterocarp-dominated forests of SE Asia that affect their ecosystem-level properties?Is it sufficient to treat a tropical canopy as a homogenous single tropical‘species’,or better to divide it into functional groups,trait spectra,or collections of species?How much biological detail is appropriate before it becomes unwieldy and unhelpful?Through its focus on quantitativeflows of carbon,water and nutrients,the currency of Earth system science,ecosystem ecology is well-placed to act as an inter-face between ecology-focusdfield studies and Earth Sys-tem science.
In this study,I review and explore what the last few decades of rearch have revealed about the productivity,carbon cycling and metabolism of tropical forest vegetation,drawing on primary productiv
ity,forest inventory and eddy covariance studies.There are many other equally important aspects of tropical ecosystem decomposition,soil ecosystem process,soil carbon turnover,remineralization and recycling of nutrients)but the are worthy of a parate review and
derek andersonnot
Carbon cycle of tropical forests67Ó2012The Author.Journal of EcologyÓ2012British Ecological Society,Journal of Ecology,100,65–75
covered here.Part of this work is a synthesis of recent litera-ture,and part prents new data emerging from our recent work across Amazonia.In the limited space of this article,I do not dwell on methodological issues and limitations;the are substantial but are covered elwhere in the literature(Clark et al.2001;Malhi et al.2009b;Metcalfe et al.2010).Rather I focus on what insights are revealed and questions opened up by the recent availability of data.
There are many aspects of forest carbon cycling that can be considered;to limit scope,I focus on the relationship between photosynthesis,productivity and biomass,the latter two being two of the most apparent aspects of tropical forests and amongst the aspects most frequently noted by early scientist–explorers.I prent a framework for this analysis in Fig.2, which prents a causal chain linking GPP to biomass.The tropical ecological and natural history literature is replete with assumptions that productivity is somehow related to biomass, that tall,majestic forests must somehow be more productive than shorter forests.As we shall e below,this is rarely the ca,as th
ere are a number of intermediate steps linking pho-tosynthesis to biomass.I consider each item in the chain of influence in Fig.2in turn.
The gross primary productivity of tropical forests
The GPP is the rate offixation of CO2by photosynthesis in the forest canopy,and as such is the primary measure of carbon supply and metabolic activity in the canopy.A large amount of empirical and theoretical tropical ecosystem rearch has focusd on determining the GPP of tropical forests,and how it is constrained by water supply,light and nutrients.Table1 lists a number of intact tropical forest sites where GPP has been directly estimated,either‘top–down’through eddy covariance studies or‘bottom–up’through biometric studies. The list is probably not exhaustive but reprents a range of forests from the Neotropics and Asia.To date(to my knowl-edge),there has been no substantive study published for Afri-can tropical forests,although my rearch team is currently investing efforts in veral sites in Central and West
matin
Africa.
Table1.Values of gross primary productivity(GPP),net primary productivity(NPP)and carbon u efficiency(CUE)for mature tropical forest sites where GPP has been measured,at given latitude(lat.)a
nd longitude(long.).Units of GPP and NPP are Mg C ha)1year)1.Elevation is in m a.s.l.Top-down GPP(GPPtd)is calculated from eddy covariance measurements,and bottom-up GPP(GPPbu)is calculated from summing components of NPP and autotrophic respiration.Estimates of GPP and CUE from the Andes are from an unpublished study by Y.Malhi et al. (unpublished data)
Site Lat.Long.Elevation GPP td GPP bu NPP CUE Sources
Mae Klong14.5898.8516032.3Hirata et al.(2008)
Sakaerat14.48101.9253538.1Gamo et al.(2005)
Pasoh* 2.97102.3075–15031.212.80.41Takanashi et al.(2005b),Kosugi
et al.(2008),Kira(1978) Palangkaraya)2.35114.033033.0Hirano et al.(2007) Xishuangbanna21.93101.2725.926.08.80.34Tan et al.(2010)
Caxiuana˜1531.231.410.00.32Malhi et al.2009b
Tapajo´s20031.429.314.40.46Malhi et al.2009b
or是什么意思奥运会
Manaus9030.429.910.10.33Malhi et al.2009b
Caxiuana˜drought control)1.72)51.461531.233.09.50.30Metcalfe et al.2010
Caxiuana˜drought)1.72)51.461527.07.40.27Metcalfe et al.2010
Tono100024.97.30.29Malhi et al.,unpublished
San Pedro150026.910.80.40Malhi et al.,unpublished Wayqecha302519.68.40.43Malhi et al.,unpublished
La Selva10.43)80.0280–15029.5Loescher et al.2003
Paracou 5.28)52.9110–4037.3Bonal et al.(2008)
*The values shown for Pasoh incorporate estimates of NPP and GPPbu from the1970s,and values of GPPtd from the2000s,three dec-ades later.Given ongoing and rapid atmospheric change,the data from the two periods may not be strictly comparable.
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At sites where there are both independent top–down and bottom–up estimates of GPP,there tends to be a fair degree of consistency in measurements,suggest that the most significant aspects of the carbon cycle are being captured by both approaches (or,less parsimoniously,that both approaches have a systematic bias).In all moist lowland forests,the GPP appears to range between 30and 40Mg C ha )1year )1.There are hints that the higher values are found on more fertile soils,but without a consistent soils data t it is difficult to draw a definitive conclusion on this.GPP appears to be reduced at the drier or more asonal sites,as would be expected as the length of the growing ason is reduced,although the Mae Klong site in Thailand (Hirata et al.2008)appears to break from this pat-tern.GPP also appears reduced in tropical montane systems,which may be a direct effect of lower temperatures on leaf photosynthetic parameters,an indirect effect of nutrient avail-ability,or reduction in light availability in the cloud forest.An insight that has been established from the eddy covari-ance studies is that,per unit of light,tropical forests are no more productive than temperate broadleaf forests in their peak growing ason (e.g.Hirata et al.2008).The high productivity of wet tropical forests appears almost entirely derived from the abnce of a dormant period (winter or dry ason),rather than an intrinsic high productivity associated with,for exam-ple high diversity or high temperatures.Flux studies have shown that many moist tropical forests can have some form of dry ason moisture limitation (e.g.in Amazonia:(Malhi et al.1998;Bonal et al.2008)and can be light-limite
d in the wet a-son,but overall many moderately asonal tropical forests exhibit fairly constant GPP over the annual cycle.
The fairly consistent results emerging from tropical eddy covariance sites enable attempts to scale to a global level.How significant are tropical forests in the global carbon cycle?Beer et al.(2010)ud data-driven scaling approaches to scale up from the eddy covariance measurements to the globe (Fig.3).They estimated total global terrestrial GPP to be 122Pg C year )1,of which tropical forests contribute about 41Pg C year )1,34%of the global total.Tropical savannas and grass-lands contribute a further 26%,while covering an area twice as
large as the tropical forests.Hence,in total,tropical biomes account for about 60%of the total terrestrial land surface metabolism.In comparison,boreal and temperate forests account for 8and 10Pg C year )1,respectively.In terms of ter-restrial metabolism,we live on a predominantly tropical planet.
Carbon u efficiency
The carbon u efficiency (CUE),is defined as the ratio of NPP to GPP.NPP is the rate of production of biomass and organic compounds by the plant or ecosystem,which can be in the form of woody str
uctures,leaf and reproductive tissues,or less obvi-ously as root exudates,carbon transfers to mycorrhizal associa-tions or nitrogen fixers,as volatile organic compound emissions from the canopy,or as storage as non-structural carbohydrates.The remainder of GPP is utilized for the internal metabolism autotrophic respiration of the plants within the ecosystem.
There has been debate as to the degree to which the CUE is invariant with a value of CUE c.0.5(Dewar,Medlyn &McMurtrie 1998;Waring,Landsberg &Williams 1998).The key question is to what extent is autotrophic respiration tightly coupled to GPP and hence limited by carbohydrate supply,or to what extent is it more related to biomass maintenance costs (Reich et al.2006),nsitive to environmental factors such as temperature,or optimal allocation decisions within a plant.It has been suggested that old-growth forests tend to have lower CUE than younger and condary forest (Litton,Raich &Ryan 2007).However,the literature report a wide range of CUE values,ranging from c.0.2to c.0.8(Litton,Raich &Ryan 2007),although theoretical calculation of growth effi-ciency and respiratory costs associated with maintenance,nutrient acquisition and transport suggest it should be con-strained between 0.2and 0.65(Amthor 2000).There are very few estimates for tropical forests;the estimates that we are aware of for mature systems are prented in Table 1.For the site at Pasoh,Malaysia,we have combined Kira’s classic 1978study of NPP components mentioned abov
e with a recent value of GPP derived from eddy covariance (Hirano et al.2007).This approach assumes no net change in fluxes between the 1970s and the 2000s,which may be unlikely (e below).The few tropical sites that have reported CUE tend to pro-duce estimates within the range 0.30–0.40,both in Amazonia and in Asia (Table 1).This also ems to apply to tropical montane forest sites,which have a cooler mean temperature.It may be that old-growth systems have higher biomass mainte-nance and defensive costs that rai respiration rates (De Lucia et al.2007).Part of the difference may simply be related to variation in CUE with life stage.It is likely that young trees allocate more carbon to NPP as they compete spatially for light and nutrients,but older trees invest more in maintenance of their large existing biomass,and perhaps also give greater priority to maintenance of chemical defence of existing bio-mass relative to acquisition of new biomass.The demography of forest stands recovering from disturbance,or in the more productive and high turnover steady state found on more fer-tile sites,would tend towards younger,faster growing trees and hence towards higher CUE.Another possibility that has
been
Fig.3.The average gross primary productivity (GPP)of the land sur-face,over the period 1998–2005(from Beer et al.2010).The analysis is bad on a world-wide network of eddy covariance flux measure-ments,extrapolated to the globe using five data-driven approaches that incorporate climate and remote nsing information.The figure shows the median of the five outputs.Units of GPP here are g m )2.100g m )2=1Mg ha )1.
Carbon cycle of tropical forests 69
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