tropical forests in a co2-rich world

TROPICAL FORESTS IN A CO 2-RICH WORLD

CHRISTIAN KORNERBotanisches Institut, Universitat Basel, Schonbeinstr. 6, 4056 Basel, Switzerland

Abstract. Tropical forests resemble, besides their enormous genetic diversity, the single largestbiomass carbon pool in the world. Only a ‘small’ annual increase of this pool could trap the currentsurplus of atmospheric CO2. The fact that this is not happening already today (after the world hasseen a 27% increase in atmospheric CO2 in only 150 years) sets the boundaries of the likely trendsto be expected in the future. In contrast to the possibly small overall responses of the tropical forestcarbon pool, individual plant responses to CO2 enrichment will be significant. Since species and theirgenotypes will not respond in identical ways, selective processes will be induced which will lead tonew community structures and alterations of numerous plant-plant, plant-animal and plant-microbeinteractions. Examples are provided for such subtile CO2 effects, measured both in the greenhouseand in the field. From what is known currently it is concluded that in closed humid tropical forestsleaf area index is unlikely to increase, mineral nutrient and water demand may (at least temporarily)become reduced, and leaf tissue quality plus associated consumer behavior will be altered. The bigunknown is the behavior of tropical soils and their microflora and fauna. There is a realistic possibilitythat carbon turnover will be increased in tropical forests in a CO2-enriched world, which would havesubstantial implications for nutrient cycling.

1. Introduction

Carbon dioxide is not only the leading indicator gas for atmospheric change, italso is a major determinant of the functioning of the biosphere. Here I will addressthese direct effects of CO2 enrichment on the world’s biota and the tropical ones inparticular. Together with other ‘greenhouse gases’ CO2 also influences the globalclimate system, and atmospheric CO2 enrichment is likely to create a warmerworld. This indirect effect of elevated CO2 on life will not be discussed.

During 3.2 billion years of evolution CO2 became the ‘master gas’ of higher lifeon earth. Wherever green plants grow on the globe they will (and do already) faceincreasing supplies of this key component for photosynthesis, and thus for biomassproduction. Based on the century-old observation that photosynthesis of mostplants (those using the C3 pathway of carbon fixation) responds immediately andpositively to increasing supplies of CO2, CO2 fertilization has become a standardprocedure in greenhouse horticulture (Wittwer, 1984). Doubling the concentrationof CO2 under otherwise optimal growth conditions has been found to stimulateseasonal biomass production by about one third (Cure, 1985; Kimball and Idso,1983). Numerous studies, mostly conducted within the last 20 years, have shownthat wild plants show similar positive responses to CO2 enrichment when grownunder fertile conditions and in isolation (e.g., Strain and Cure, 1985; Poorter, 1993).The problem is that 99% of the net primary production of biomass on the globeis achieved without fertilizer addition or watering, and plants in most ecosystems

[157]Climatic Change39: 297–315, 1998.c 1998Kluwer Academic Publishers. Printed in the Netherlands.

298 CHRISTIAN KORNER

of the world can not expand freely in any direction but are faced with competitionfor limiting resources and, in addition, have to cope with all sorts of disturbancesand stresses. Under such conditions the effects of elevated CO2 are very uncertain(Korner, 1993). Within the last 10 years a number of researchers have shown that(with the exception of a salt marsh) comparatively small or – in few cases – even nobiomass responses to CO2 enrichment may occur when more natural experimentalconditions are adopted (for reviews see e.g., Mooney et al., 1991; Bazzaz and Fajer,1992; Woodward et al., 1991; Eamus and Jarvis, 1989; Korner, 1996).

However, independently of whether overall ecosystem biomass responses toelevated CO2 were observed or not, differential responses of species (e.g., Reekieand Bazzaz, 1989; Williams et al., 1986; Owensby et al., 1993; Curtis et al., 1994;Amthor, 1995; Schappi and Korner, 1996) and changes in tissue composition (fortropical plants, see Korner and Arnone, 1992; for Mediterranean plants, see Kornerand Miglietta, 1994) were detected which could have far ranging consequences forecosystem functioning in the long term. Community structure, the food web anddecomposition of organic matter are most likely to be affected (Norby et al., 1995).

Comparatively little is known for woody plants in general and whole forests inparticular. For obvious practical reasons research was done with small and handysystems, such as ruderal annual communities, perennial grass swards or smallassemblages of tree seedlings. Very rarely woody plants have been studied underelevated CO2 for more than a season (e.g., Norby et al., 1992; Idso and Kimball,1992; Murray et al., 1994; Arnone and Korner, 1995). This is clearly an insuffi-cient basis for making sound predictions for whole forests, and in particular forsuch complex ecosystems as tropical forests are. To my knowledge there exist 6published studies on the responses of humid tropical tree species grown underelevated CO2: a study with potted seedlings from Costa Rica in controlled envi-ronment chambers (Oberbauer et al., 1985), synchronous cultures of assemblagesof seedlings of tropical tree species in common containers in a greenhouse nearBoston (Reekie and Bazzaz, 1989), potted individual seedlings growing outdoorsunder a shade screen in Panama (Ziska et al., 1991; see also the review by Hoganet al., 1991), artificial tropical communities having 7 m2 of rather fertile groundin a greenhouse in Basel (Korner and Arnone, 1992), similar communities but onrather poor substrate (Arnone and Korner, 1995; Arnone et al., 1995), and twostoried monoculture canopies in the same facility but again under relatively fertileconditions (Arnone and Korner, 1993; see also review by Arnone, 1996). I am notaware of any work with tropical dry forest species.

This assessment will thus rely heavily also on results obtained in non-tropicalplants and on theoretical considerations. However, these will be supplemented bypreliminary results of ongoing CO2 enrichment experiments under field conditionsin the humid tropics of Panama.

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TROPICAL FORESTS IN A CO2-RICH WORLD 299

2. Carbon Storage in Tropical Forests

The term ‘tropical forests’ covers a wide variety of vegetation types ranging fromsavanna woodlands to equatorial moist lowland forests, and includes such extremesas thornbush and mangrove. Even the term ‘tropical rainforest’ is vaguely defined(Vareschi, 1980). Including all those types of tropical woody vegetation, a totalland area of about 1800 million ha may be considered as ‘tropical forests’ (Brownand Lugo, 1982). Biomass and soil carbon pools contained in these ecosystemshave repeatedly been revised within the last 25 years. While original IBP datacompiled by Whittaker and Likens (1975) who extrapolated mainly from matureexamples of vegetation, are possibly too high, those more recently compiled byBrown and Lugo (1982) and Olson et al. (1983) are possibly too low because recentstudies revealed that deep soil carbon pools have been underestimated (Brown andIverson, 1992; Nepstad et al., 1994). Since nobody really knows how much rootmass and soil organic matter is stored in deep soil horizons on a global scale (cf.Raich and Nadelhoffer, 1989; Nepstad et al., 1994), it seems appropriate as a bestguess to use the data by Brown and Lugo (rounded up by ca. +10%), and assumea current tropical biomass carbon pool of about 250 Gt C and a soil carbon poolof ca. 175 Gt C. Compared to global pools (again rounded up) of about 600 Gt Cfor biomass and 1650 Gt C for soil organic matter (based on Olson et al., 1983;Houghton et al., 1983; Bouwman, 1990) ‘tropical forests’ contain roughly 42%of the global biomass carbon and about 11% of the global organic soil carbon,together about one fifth of the total global organic C pool. These numbers clearlyunderline the fact that tropical forests resemble the single most important biomein terms of biomass carbon storage (cf. Soepadmo, 1993). Any marginal relativechange in tropical forest biomass would substantially alter the absolute amount ofbiomass carbon stored in the whole biosphere. Humid tropical forests also are aprime biome for potential carbon sequestration because of the large annual biomassproduction during the 12-month growing season which is twice as high as the annualproduction in northern temperate forests in 6 months (per month of active seasontheir productivity is approximately equal).

3. Tropical Carbon Sinks: What Size of Signal Are We Looking For?

CO2 fertilization effects are believed to be larger the warmer the climate (Long,1991). Hence, the biggest effects are expected for tropical ecosystems and thesmallest for boreal and polar ecosystems. Consequently, model predictions andestimates utilizing forest inventories indicate the possibility of substantial carbonsequestration in the tropics (Oikawa, 1986; Houghton, 1990; Taylor and Lloyd,1992; Melillo et al., 1993). The first available ecosystem-based carbon balance fora mature tropical forest (Grace et al., 1995) indicates that carbon sequestration mayalready be under way in the tropics, contrasting estimates from atmospheric chem-istry which suggest that the ‘missing carbon’ is to be found in the temperate zone

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(Tans et al., 1990). If the biosphere is to mitigate the current or future atmosphericCO2 enrichment, tropical ecosystems with their ca. 42% share of total global bio-mass carbon are likely to play a key role (cf. Lugo 1992; Lugo and Wisniewski,1992; Houghton, 1990).

Given the ca. 250 Gt carbon stored in tropical forest biomass, this pool wouldhave to increase by ‘only’ 1.2% every year (3 Gt C) in order to stop currentatmospheric CO2 enrichment (an increase of ‘only’ +0.5% of the total biomasscarbon of the globe would do the same job). These numbers look small but, forinstance, applied to a forest with a 100 year rotation, and hence a mean annualincrement corresponding to 1% of the final C stock would mean roughly doublingnet primary production (NPP) if, for the sake of simplicity, we are disregardingnon-linearity of growth. However, such a faster carbon accumulation would mostlikely cause earlier maturation of trees and shorten their life span, possibly counter-balancing a CO2 fertilization effect on NPP by faster carbon biomass rotation, asPhillips and Gentry (1994) appear to have detected in wet tropical forests (see alsoCondit, 1998). If this were true, and C pools per unit land area would not go up,the theoretically required 1.2% increment in carbon stocks in tropical forests alonewould have to be achieved by a 1.2% annual increase in areal extent of mature(!) forests (or a combination of both effects). According to Brown et al. (1992) a2.5 Gt annual C-sequestration would theoretically be possible if human pressurecould completely be removed. Obviously these are unrealistic scenarios.

The fact that atmospheric CO2 currently increases by 3 Gt C per year (+1.4 ppm)suggests that such an additional carbon fixation is beyond the binding capacity ofterrestrial ecosystems. An increase of the biospheric net ecosystem productivity(NEP)� equivalent to a 5% higher annual NPP of terrestrial biota (the total assumedto be ca. 60 Gt Ca�1) would be required to continuously sequester this annualsurplus of atmospheric carbon.

The current carbon sequestration of the biosphere may serve as a guideline forestimating future trends. Every year about 1–2 Gt C from fossil carbon burningpresumably disappear in terrestrial biota (despite deforestation in the tropics andin the boreal zone). If a carbon sequestration of 2 Gt C were solely due to a CO2

fertilization effect (which is uncertain) the current ca. 29% CO2 enrichment ofthe atmosphere since preindustrial times would account for a ca. 0.3% increaseof global biomass C per year (assuming that preindustrial NEP was close to zero,for which we have no proof). Hence, applying the above optimistic estimates, the

� NEP, the net ecosystem carbon gain (or ‘production’) includes all carbon sequestered to biomassand soils and results from NPP (net primary production) minus all concomitant carbon losses. NPP isthe annual production of NEW biomass carbon, disregarding simultaneous decay or decompositionof biomass produced earlier. NEP has rarely been determined and is often assumed to be close to zerowhen large areas and long periods of time are considered. NPP has often been estimated by harvestingannual increments of biomass and litter, and adding losses to herbivores. However, numbers areusually quite inaccurate since annual production and turnover of these components below the groundare largely unknown. In seasonal climates and perennial vegetation it is further unknown how muchof annual ‘production’ above the ground is only allocated carbon from below-ground stores.

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global biomass response to a doubling of preindustrial atmospheric CO2 could,at the most, reach 1% (or an increase of annual non-recycled NPP by 10%). Ona global basis this is the maximum size of a signal we are looking for. Sincethe carbon cycle is tightly coupled to the mineral nutrient cycle (not included inthe above considerations; cf. Gifford, 1992) this approximation is likely to be anoverestimate. Yet, probably none of the currently practiced experimental ‘doublingCO2’ treatments in natural vegetation can detect biomass signals of less than 10%with statistical significance. Consequently, the most likely C pool signal derivedfrom CO2 enrichment experiments with natural vegetation is ‘no change’ – givenour commonly accepted criteria for statistical significance. This, however, does notmean that CO2 fertilization does not happen, it only means that the signal requiredto explain current and even doubling CO2 effects is below experimental resolution.An important caveat is that the above reasoning assumes that atmospheric CO2

concentrations would have stayed constant (e.g., at 280 ppm) if no anthropogenicCO2 production had occurred and that biospheric NEP remained zero.

Coming back to the question of tropical forest carbon sequestration, a recentexperiment conducted in Basel (Arnone and Korner, 1995) revealed some surprisingresults, in line with the above reasoning: After growing tropical plant communitiesfor 512 days under current ambient and ambient plus 300 ppm CO2 and verylow nutrient supply, NEP (true NEP!) increased by 4% compared to controls. Thisincrease was almost exclusively due to carbon sequestration to the soil C-pool whichaccounted for 80% of NEP, with surprisingly little variance between replicates butstill too much to acertain the 4% difference with statistical significance. Yet, thissmall 512-day response, if maintained in the long term, would be approximatelythree times as large as the one required to trap all human released CO2 in a ‘doubledCO2’ world on a global scale.

4. The Difficulty of Scaling from Fluxes to Pools

Before discussing the possible CO2 responses of tropical forests, an importanttrivial (though often overlooked) distinction needs to be recalled. Most scientistsstudy CO2 effects on plants by measuring growth, i.e., biomass increase of anindividual through time. Such growth responses are of great interest when plantproduction is considered, or when plants compete for space and resources, andbiodiversity effects are studied. However, such growth rates have little meaning ifcarbon sequestration (carbon storage) of an ecosystem is considered (cf. Korner,1995a). Pools and flux rates are not related! As in business, the flow of currency(carbon) is unrelated to capital (C stock). At peak season a crop of corn may fix fourtimes as much carbon than an adjacent forest, but once it is harvested and used, andremains are decomposed, the increment of the C pool is reduced to zero. Mature,late successional forests store the greatest amount of carbon but are growing veryslowly, whereas gap communities are growing fast but C stocks are small. Annual

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Figure 1. Idealistic life cycle of a forest tree community under ambient (a) and elevated (b, c)atmospheric CO2 concentrations. The diagram illustrates how two possible responses in the early lifephase may translate into dynamics of community maturation and life span of trees.

dry matter production of grasslands may exceed that of forests, but again C poolsin plant biomass are minute.

Such considerations are not restricted to ecosystems. At the level of an indi-vidual, the life time carbon acquisition does not necessarily increase with growthrate. Fast-growing species usually exhibit shorter life spans. If we account for thesefacts it becomes clear that it is impossible to predict the response of forest biomassfrom growth analysis data. Figure 1 illustrates a situation where young regrowthin a forest gap is assumed to be stimulated by elevated CO2 whereas old trees arenot. The gap will close faster, steady state leaf area index will be achieved earlier.Unless the contrary is proved, plausibility leads us to assume that CO2-stimulatedtrees would also mature earlier and possibly die earlier. The life time carbon acqui-sition thus may remain unchanged, and the net carbon gain per unit land area due toCO2 fertilization may become zero. Figure 2 illustrates three cases in which CO2

fertilization effects on developmental rates are considered to affect (a) none of thelife phases, (b) only the early life phase, (c) both life phases. Obviously, only incase (b) would carbon sequestration be increased. No data are available to supportcase (b), and I would suggest plausibility stands against it.

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Figure 2. CO2 effects on natural forests: Gap phase duration and tree life span largely control thebiomass C pool (a, b, c refer to the text).

5. Are Tropical Trees Currently Carbon Limited?

This question is not easy to answer. At present we have only one set of unpublisheddata for mature tropical trees that provides some rather indirect evidence, suggestingthat carbon supply may perhaps be close to saturation at current CO2 levels. Amongthe various theories explaining the accumulation of non-structural carbohydratesin leaves exposed to elevated CO2, ‘sink limitation’ is mentioned most often,although other mechanisms may be of even greater importance (Korner et al.,1995). A single leaf on a huge tree crown can be considered to be attached to aninfinitely large carbon sink, whatever the actual rate of carbon consumption by thetree may be. If sink activity were determining a leaf’s mobile carbohydrate poolunder elevated CO2, we should thus find no sustained carbohydrate increase whensupplying such a leaf or only part of it with increased concentrations of CO2. Theopposite was found when respiratory CO2 was pumped from the forest floor to topcanopy leaves in the tropical forest of Panama (Korner and Wurth, 1996; Wurth,Winter, and Korner, unpublished). Substantial carbohydrate accumulation acrossthe CO2-enriched vs. non-enriched leaf zone was also confirmed by carbon isotoperatios in the CO2-fertilized leaf sections, reflecting the13C depletion in forest floorderived CO2 (Korner and Wurth, 1996; see also Medina et al., 1991).

The analysis of the data of these experiments is now under way, but prelim-inary results either suggest a sink-independent stimulation of mobile C-pools inleaves or effective sink limitation already under current CO2 concentrations. Atleast at the leaf level, doubling CO2 supply appears to cause superfluent carbonassimilation. If persistent, this carbohydrate ‘overflow’ is likely to affect the foodweb depending on those leaves. It should be noted that this CO2-induced accu-mulation of non-structural carbohydrates observedin situ was only half as largeas the one found by Korner and Arnone (1992) in greenhouse experiments. This

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is best explained by the lower night temperatures prevailing in the latter experi-ment compared to the situation in the Panamanian forest (20 vs. 27�C). There isevidence that increasing temperature will increase sucrose synthesis and decreasecarbohydrate accumulation (Farrar and Williams, 1991).

Wurth, Winter and Korner have recently completed the firstin situCO2 enrich-ment study in the understory of a tropical forest (Barro Colorado Island). Theirunpublished data suggest a significant CO2 stimulation of both shrub and treeseedlings in deep shade, supporting predictions that relative responses to elevat-ed CO2 should be pronounced in low light environments (e.g., Long, 1991). Inessence, these results are in line with observations in conifer forest understoryplants (Hattenschwiler and Korner, 1996a) and suggest faster tree recruitment andimproved light utilization under very low light. These data also indicate that CO2

is currently limiting plant growth underneath dense tropical forest canopies. Sincetropical forest regeneration usually requires gap formation (cf. Kursar, 1998) thesebeneficial effects in the first place may support only seedling survival rather thanregeneration as such. It is important to note that vines may profit from CO2 fer-tilization in extremely low light as well, which could cause their presence in thecanopy to become increased – a negative consequence for trees. Indeed, Phillipsand Gentry (1994) and Phillips (1996) have observed enhanced vine frequency inrecent decades which they considered as a possible alternative or additional expla-nation for the increased tree turnover they found. In the light of the above reasoning,recent CO2 enrichment may be the ultimate cause also for this development.

6. Tropical Biodiversity under Elevated CO2

Among the many uncertainties about plant CO2 responses one aspect is certain:plants differ in their responses (cf. Bazzaz, 1998; Bazzaz and McConnaughay, 1992;Bazzaz et al., 1993; Korner et al., 1996). These differences may find expressionin overall growth response or in less obvious responses such as changes in tissuecomposition, stress resistance or rhizospheric interactions. In the long term thesedifferent responses will change the competitive situation in mixed communitiesand affect biodiversity (Korner, 1995b).

Furthermore, it is unlikely that all individuals of a given population of a specieswill respond identically to CO2 enrichment. Small genotypic response differencesmay translate into new genotype abundance patterns, and over several generationswill cause evolutionary selection. These selective processes will occur, no matterhow ecosystem properties such as productivity, biomass or resource turnover areaffected by elevated CO2. However, selection by CO2 responsiveness is only oneof many selective forces to which species and all their individuals are permanentlyexposed. Potential ‘CO2 selection’ may get drowned by other overriding selectivedrivers, or may itself overrule other selective processes. The ultimate outcomeof these adaptive processes is unpredictable, but the one-sided shift in supply of

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the key resource for photosynthesis is unlikely to remain completely uneffective.Hence, genetic responses are progammed both at the population as well as at thecommunity level (cf. Korner and Bazzaz, 1996).

6.1. DIFFERENTIAL RESPONSES BETWEEN PLANT SPECIES

What evidence do we have for CO2 effects on biodiversity? Whether the abovetrends will become visible during an experiment will depend on experimentalduration and on the vigor of growth (Korner, 1995a). The best document of differ-ential species responses in tropical plants is the study with fast growing seedlingassemblages by Reekie and Bazzaz (1989). Even though these species were care-fully nursed to reach equal starting height at the onset of CO2 treatment, it tookless than 100 days to clearly identify winners and losers due to CO2 enrichment.The most remarkable result of this competition experiment was the overridingimportance of morphology. One may argue that this is an artificial competitivesituation, unlikely to occur in nature. But this is not the point here. We certainlycan not mimic the real world under controlled conditions. However, this screeningtest convincingly documented that, even under optimum growth conditions andsynchronous development, species differ enormously in their CO2 responsiveness.How much might they differ if starting conditions were not equal?

Older and larger plants may not exhibit responses that fast. Korner and Arnone(1992) grew dense thickets of artificial communities of tropical plants from acanopy height of about 1 m to a height exceeding 2 m over three months. Thoughgrowth was vigorous and the mix of species included almost all life forms foundin a tropical forest, no significant shifts in the contribution of individual species tototal biomass or leaf area were detected which does not mean that such differentialresponses did not occur, but they were below resolution level. In a much longerexperiment and with much less fertile soil, CO2 did, however, affect biodiversity inmodel communities of tropical plants in a remarkable manner (Arnone and Korner,1995). CO2 enrichment changed the speed of succession. The fast growing pioneerCecropia peltatatook off first, but got slowed down by below-ground competi-tion of vigorously developing mats of monocotyledonous species (e.g.,Eletariacardamomum, Zingiberaceae) which in turn was in favour of the later succession-al speciesFicus benjaminawhich could raise its leaf canopy into and above theCecropiacanopy, and thus made its way to become the dominant species. Theseresponses are rather subtile and slow but faster under elevated CO2. Statisticallythese trends were only significant when tested for the whole community rather thanfor each individual species alone, and mechanisms are unclear (Arnone, 1996).

The above mentionedin situCO2 enrichment with understory plants in the deepshade of the tropical forest of Panama (Wurth, Winter, and Korner, unpublished)also revealed that CO2 did not affect all species equally.Piper cordulatumandPsychotria limonensiswere stimulated most whereasPharus latifolius, a typicalshade-tolerant grass, profited less.

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Together, these experiments underline that CO2 can, and most likely will affectcompetition and succession in tropical forests. There do not seem to exist obvious‘markers’ which permit ranking of species as potential winners and losers, inparticular, since below-ground processes are so unpredictable, and since above theground architectural plasticity may overrule all physiological responses (cf. Reekieand Bazzaz, 1989). It also seems unlikely that legumes will generally respond fasterthan non-legumes because most often nitrogen is not the most limiting mineralresource in tropical forests, and their understories in particular (Vitousek, 1984;Grubb, 1989; Walker, 1994). Furthermore, nitrogen demand of tropical plantsis likely to remain unchanged or rather decrease than increase under elevatedCO2 (Korner and Arnone, 1992; Arnone, 1996). Also mineral nutrients other thannitrogen are not necessarily limiting, as suggested by fertilizer experiments withPiper and Miconia in small forest gaps in premontane rain forests of Costa Rica(Denslow et al., 1990). However, in Jamaican montane forests both nitrogen andphosphate fertilizer stimulated the growth of tall trees (Tanner et al., 1990).

6.2. TROPICAL PLANT – ANIMAL INTERACTIONS UNDER ELEVATED CO2

Pollination, diaspore distribution and herbivory are major drivers of biodiversity,particularly in the tropics. Experimental evidence for CO2 effects on such interac-tions is almost non-existent but the few studies that have been made suggest thatchanges in plant quality are likely to translate into changes in plant and animalabundance (see also Coley, 1998). CO2 fertilization has been shown to either speedup or slow down flowering and seed production (Garbutt et al., 1990; Woodin etal., 1992; Bazzaz et al., 1992; Reekie and Bazzaz, 1991), or to alter seed quality(or size). As part of an ongoing study on the effects of elevated CO2 on biodiver-sity in highly diverse calcareous grasslands, Rusterholz and Erhardt (1997) foundstatistically significant increases in the number of flowers inLotus corniculatus, asignificant reduction inTrifolium pratenseand a significantly earlier flowering inCentaurea jacea.

There is now also evidence from the same experiment that elevated CO2 doesaffect the amount and quality of nectar in a rather specific and unpredictable manner.For instance, inScabiosa columbariaandCentaurea jaceathe nectar volume perflower was reduced. At the same time, the sucrose content was increased inScabiosabut not inCentaurea. The concentration of amino acids remained unaffected, but thecomposition was significantly changed inLotus corniculatuswhen growing underelevated CO2, and butterflies have been shown by these researchers to exhibit clearpreferences for certain nectar compositions. Such changes may be more importantin the tropics where plant pollinator systems are often obligate (Kodric-Brown andBrown, 1979; Erhardt, 1992).

Herbivory can be affected by CO2-induced changes of tissue quality, i.e., animalseating greater quantities of the protein-depleted food (cf. Lincoln et al., 1993; Coley,1998). However, these results need to be treated with great caution. Herbivores were

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not given a choice of food plant species in those experiments, and plant tissue wasproduced while plants received ample fertilizer. Arnone et al. (1995) who presentedthe first and so far only data set for herbivory on tropical plants did not findsuch effects. They created an ‘outbreak’ ofSpodopteralarvae (army budworm, ageneralist herbivore) in a multispecies, artificial tropical plant community that grewunder elevated CO2 and very low mineral nutrient supply. Under these conditionsleaf tissue quality did not change, and leaf consumption also did not change underelevated CO2. However, much more subtile interactions became apparent. Larvaeshowed very clear food preference. They climbed through the understory thicket,following a long leaf-less stem to reach their preferred food,Cecropialeaves. SinceCecropiawas suffering from below-ground competiton (see above) and had lessleaf area under elevated CO2, similar herbivory in both treatments accelerated theCO2-induced decline ofCecropia.

Such interactions obviously would not be detected in a single-plant pot experi-ment or in a petri-dish feeding experiment, requiring a much more complex exper-iment to become visible. I do not see how such interactions could be predicted byany currently available theory, providing a strong argument for more realistic CO2

experiments (Korner, 1995a). Until more studies of this kind become abvailable wecan only conclude that plant-animal interactions are most likely to be influencedby increasing CO2, and it remains uncertain whether genotype selection can trackthe speed of change before it affects species abundance.

There are many other plant products released in order to attract consumers. InCecropiafor instance, some species produce segmented trichomes at the leaf basewhich are rich in glycogen (‘Muller bodies’) and which are harvested by certainant species which in turn, ‘defend’ their host against leaf cutting ants. It had beenshown previously that the dry mass of Muller bodies increases when photosynthesisis stimulated by higher light intensities (Folgarait and Davidson, 1994). We haveinvestigated whether elevated CO2 influences the rate of Muller body production inCecropia peltata(Korner and Pelaez-Riedl, unpublished). While the concentrationof non-structural carbohydrates in leaf blades was increased rapidly under elevatedCO2, the rate of Muller body production remained completely unaffected and thesize of each ‘body’ also was not changed.

7. Ecosystem Effects to Elevated CO2

As outlined above, species composition or species abundance is likely to changedue to differential CO2 responses, but land area related processes may respondindependently of such changes in community structure, unless substantial alter-ations in species composition take place. In the following I will discuss the likelyeffect of elevated CO2 on important ecosystem properties.

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7.1. BIOMASS RESPONSES

Though we do not have strong experimental evidence, a slight stimulation of netprimary production of tropical forests by elevated CO2 appears plausible. Themagnitude of such a response most likely is below resolution of experimentaltests, if natural growth conditions are applied. In none of the four experiments inwhich whole canopies of tropical plants were allowed to grow under elevated CO2

until and beyond canopy closure, growth rate and final biomass were significantlystimulated by CO2 enrichment. Remarkably this was even true when rather youngplants, receiving ample fertilizer, were exposed to elevated CO2 (like in Reekie andBazzaz’s, 1989, experiment and in the work withRicinusby Arnone and Korner,1993).

However, such experiments, as mentioned above, cannot account for life historyeffects, and thus do not permit any conclusion with respect to biomass carbon poolsper unit land area in the long term (as long as closed stands are considered). Carbonmay still be sequestered at greater rates under elevated CO2 when soil carbon isincluded. Whenever photosynthetic responses in plants growing under elevatedCO2 were studied, rates were found to be persistently increased far beyond whatwould be required to explain a significant growth stimulation (Korner, 1996). Thelikely fate of this extra carbon taken up but not accreted in biomass is to end upin the soil humus or being recycled as respiratory CO2 (Korner and Arnone, 1992)and volatile C-compounds such as isopren (Turner et al., 1991; Sharkey et al.,1991). Arnone and Korner (1995) showed that during their 512-day CO2 treatmentof tropical model communities 80% of all carbon taken up ended in the soil,underlining the fact that this is a major pathway of ecosystem carbon accretion (seeparagraph three). Since mineral nutrients are co-sequestered with carbon, negativefeedbacks on biomass need to be considered in the long term.

7.2. LEAF AREA INDEX

None of the available experimental data on natural plant communities growingunder elevated CO2and none of the studies with artificial tropical plant communitieshas shown a stimulation of leaf area index as might be predicted from physiologicaltheory (Korner, 1996). In fact, steady state LAI in the tropical model communitiestended to exhibit slightly smaller LAI under high CO2, accompanied by slightlyenhanced leaf turnover (Korner and Arnone, 1992; Arnone and Korner, 1993,1995). These data are clearly not in support of trends predicted by models assuminga CO2-induced shift in the light compensation point of photosynthesis to increaseLAI (Oikawa, 1986), but are in line with a number of observations in studies withisolated tree seedlings which showed reduced leaf area ratio under elevated CO2

(Norby and O’Neil, 1991; Mousseau and Enoch, 1989; Wong et al., 1992), andwith results in CO2-enriched model ecosystems of conifers (Hattenschwiler andKorner, 1996b).

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The situation may be rather different in drought limited ecosystems when leafarea development is moisture controlled. In addition, increasing water use efficiencyof gas exchangeunder elevated CO2 as documented for isolated tree seedlings couldfacilitate denser leaf canopies in drought deciduous tropical forests. This certainlyis an area that requires both experimental tests as well as modelling (see alsoparagraph 7.5).

7.3. MINERAL NUTRIENT DEMAND

Under elevated CO2 less photosynthetic machinery is required to maintain or evenincrease CO2 fixation, hence nitrogen demand is reduced. Except when plants aregrown under severe nutrient limitation leaf nitrogen content was always found todecrease under elevated CO2 (many references, cf. Korner and Miglietta, 1994;Korner, 1996). Since leaf area index in closed canopies was not found to increaseunder elevated CO2, either no change or reduced above-ground biomass nitrogenwas found (Korner and Arnone, 1992; Arnone and Korner, 1995). The situationwith phosphate is different. Conroy et al. (1990) showed that phosphate demandcan be increased in plants exposed to elevated CO2, and higher leaf phosphateconcentrations in a tropical plant community exposed to elevated CO2 were indeedobserved (Korner and Arnone, 1992). In view of the fact that tropical forestsare often phosphate rather than nitrogen limited (Grubb, 1989; McGill and Cole,1991), and P availability is strongly mycorrhiza dependent (Alexander, 1989),CO2 fertilization can induce a transitory shortage of this key element until a newequilibrium, perhaps at lower growth rates, is achieved.

7.4. SOIL RESPONSES

Soil and rhizosphere are the most complex and most unknown ecosystem com-partments, and their responses to canopy CO2 fertilization is largely speculative(cf. Norby et al., 1995; Wullschleger et al., 1995). At present, both increasedcarbon accumulation in soils of tropical model ecosystems (Arnone and Korner,1995) as well as increased carbon release (Korner and Arnone, 1992) are possibleconsequences. The more nutrient-limited a system is, the more likely carbon isto accumulate in the soil carbon pool, which will lock up more nutrients in soilorganic matter. In contrast, in nutrient-rich ecosystems, breakdown of humus maybe primed by low molecular weight plant exudates. Whichever direction a systemmoves, the change is likely to be extremely slow and may even cease after transitoryadjustment because of many negative feedbacks. For instance, increased microbialbiomass, as it was found in short term experiments (Diaz et al., 1993), is unlikelyto persist since the soil food web will also adjust (Protozoa, Nematoda, Acaridaetc.) and may only cause faster carbon cycling. Indirect evidence for the latter inthe form of increased soil CO2 evolution was clearly found in the nutrient-richtropical model community studied by Korner and Arnone (1992), was not seen

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in the follow up study with poor nutrition (Arnone and Korner, 1995), was againclearly evident in the third year of an ongoing experiment with spruce mesocosmsin natural soil in the Basel phytotron (Hattenschwiler and Korner, 1996b) and wasalso observed in mediterranean grassland under elevated CO2 (Navas et al., 1995).

Soil responses to CO2 enrichment clearly deserve top priority in future research,not only because soils represent the biggest biological carbon reserves on the globebut also because the soil carbon pool (in contrast to the biomass carbon pool) inprinciple can be expanded substantially without increasing vegetated land area (seealso Silver, 1998). However, temperate and boreal ecosystems as well as grasslandecosystems with their larger soil carbon pools and slower turnover may be moreimportant in this respect than tropical forests.

7.5. WATER RELATIONS OF TROPICAL FORESTS IN A CO2-RICH WORLD

Changing plant water relations could become the most important of all CO2 effectson tropical forests. Except for swamp forests water is always a selective driver ofplant growth, even in the heart of the humid tropical forests. Periodic moistureshortage, the length of dry spells in an otherwise humid climate are among the keydeterminants of the species structure of communities (see also Condit, 1998). Sincereduced water consumption is one of the most often observed effects of atmosphericCO2 enrichment on plants (cf. Hogan et al., 1991 for tropical plants; Kursar, 1998),soil moisture depletion can be expected to be slower under high CO2 (but otherwisesimilar climate). However, the data shown by Korner and Wurth (1996) for CO2

responses of stomata in mature tropical trees in Panama, suggest great caution inthe use of any seedling responses for predicting such canopy responses. InCecropiathey found no reduction in leaf diffusive conductancein situ, but more tree speciesneed to be studied before more general conclusions can be made.

Unless one assumes that all plant species will respond in a similar way, thebalance between ‘water savers’ and ‘water wasters’ will be altered and will causecommunity structure to change, no matter what the CO2 effects on growth anddevelopment will be. Root responses to elevated CO2, in particular rooting depthand rates of soil exploration would have to be known. Ongoing experiments inthe Basel phytotron indicate a substantial initial stimulation of root growth inseedlings of Panamanian forest plants by elevated CO2. Sound evidence for CO2�drought interactions in intact plant communities is generally scarce, but for grass-land reduced water consumption under elevated CO2 has been found (e.g., Jacksonet al., 1994, for Mediterranean grassland; Owensby et al., 1996, for prairie).

8. Conclusions

Elevated atmospheric CO2 is likely to exert a number of direct effects on tropicalplant life and ecosystem functioning. Since species and their genotypes are unlikely

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to respond identically, this will (and probably does already) cause changes in speciesstructure of diverse tropical forest communities. Besides differential responsesof growth to CO2 fertilization, the most important indirect effect appears to bereduced consumption/demand of water and altered tissue composition. While thefirst may improve the water balance and reduce drought stress – but perhaps, onlyduring a transitory phase – the latter will persistently influence the tropical foodweb and other more subtile plant-animal and plant-microbe interactions. Currentlyavailable data do not suggest a significant increase of tropical forest biomassdue to increasing CO2 concentrations. However, accelerated carbon turnover, inparticular a stimulation during the early life phase of a plant, is a likely consequenceof continued atmospheric CO2 enrichment.

Acknowledgements

Part of the work referred to in this paper was funded by the A. Mellon Founda-tion (Washington) and supported by the Smithsonian Tropical Research Institute(Panama). We thank Joe Wright (Panama) and a number of participants of theWWF-organized workshop in Puerto Rico in April 1995 for references and valu-able comments.

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(Received 8 August 1995; in revised form 18 July 1997)

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tropical forests in a co2-rich world

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