REVIEWS 32 Arnqvist, G. (1992) The effects of operational sex ratio on the relative mating success of extreme mate phenotypes in the water strider Gerris odonfogaster @ett.) (Heteroptera;Gerridae), Anim. Behou. 43,681-683 33 Smith, C. and Wootton, R.J. (1995) The effect of brood cannibalism on the operational sex ratio in parental teleost fishes, Rev. Fish
39 Owens, I.P.F. et al. (1994) Extraordinary sex roles in the Eurasian
Biol. Fish. 5, 372-376
34 Berglund, A. and Rosenqvist, G. (1993) Selective males and ardent females in pipefishes, Behau. Ecot. Sociobiol. 32,
35 Forsgren, E. et al. (1996) Modes of sexual selection determined by resource abundance in two sand goby populations, Evolution 50, 646-654
36 Madsen, T. and Shine, R. (1993) Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes,Am. Not. 141,167-171 37 Hoglund, J. et a/. (1993) Costs and consequences of variation in the size of ruff leks, Behao. EcoL SociobioL 32,31-39 38 Summers, K. (1992) Dart-poison frogs and the control of sexual selection, Etho/ogy 91,89-107
dotterel: female mating arenas, female-female competition, and female mate choice, Am. Nat.144,76-100 Parker, G.A.(1983) Mate quality and mating decisions, in Mate Choice (Bateson, P., ed.), pp. 141-166, Cambridge University Press Berglund,A. (1994) The operational sex ratio influences choosiness in a pipefish, Behau. Ecol. 5,254-258 Souroukis, K. and Murray, A-M. (1995) Female mating behavior in the field cricket, GtyUus pennsyhnicus (Otthoptera: Gryllidae) at different operational sex ratios, J. Insect. Behau. 8,269-279 Grant, J.W.A.et al. (1995) Mate choice by Japanese medaka (f%ces, Oryziidae), Anim. Behau. 50,1425-1428 Cox, CR. and LeBoeuf, B.J. (1977) Female incitation of male competition: a mechanism in sexual selection, Am. Nat. 111, 317-335 Johnstone, R.A.et a[. Mutual mate choice and sex differences in choosiness, Euolution (in press) Crowley, P.H. et al. (1991) Mate density, predation risk, and the seasonal sequence of mate choices: a dynamic game, Am. Nat. 137, 567-596
Plant physiologicalecology of tropicalforest canopies Stephen S. Mulkey, Kaoru Kitajima and S. Joseph Wright
ver half of the global Mechanistic information about tropical ture, strong seasonality in rainfall annual net primary procanopy function is emerging at the leaf, and light is common in tropical tree, stand and landscape levels. With duction is estimated to forests. A high diversity of leaf occur in the tropics, with improved canopy access, comprehensive longevities and production stratmost of the production attributdata are accumulating about seasonal egies results in part from the conand spatial variation in light, temperature able to tropical forest’. The canopy trasting seasonality of water and is the business end of tropical for- and humidity, and corresponding variation light availability (the rainy season est, and plant physiologists have in leaf carbon gain and water loss. is typically cloudy while light is long had great interest in underAt the whole-plant level, simultaneous abundant during the dry season, standing the ecological and physiomeasurements at different spatial scales Fig. 1). Relative to temperate and logical determinants of canopy have revealed the role of boundary layer boreal forests, tropical forests exchange processes. Until recently, dynamics in regulating transpiration. have the highest solar radiation data have been sketchy, owing Emergent properties of canopy function and heat load per area due to to the difficulty of repeated, nonare being explored through models that higher solar declination. Accorddestructive, in situ measurements integrate leaf and landscape-level ingly, resource gradients within in the canopy. Over the past few exchange processes. Integration the canopy can be quite steep, years, there has been a surge of of exchange processes that include especially during the dry season3. functional diversity at different scales work facilitated by flexible canopy Thus, the central problem for the access systems, such as construchas the potential to validate regional study of the ecophysiology of tion (canopy) cranes and expanded estimates of gas exchange, which are tropical canopies is to characwalkwaysz, as well as by advances critical to our understanding of the role terize often extreme spatial and in portable analytical equipment. of tropical forests in global atmospheric temporal variation in exchange Now, it is possible to examine rigcarbon balance. processes in a fashion that perorously variation in leaf exchange mits meaningful generalizations. rates of carbon (C) and water in Here, we review recent advances Stephen Mulkey is at the Dept of Biology, University tropical forest canopies at conat different spatial scales of obserof Missouri - St Louis, St Louis, MO 63121-4499, trasting spatial scales. The pervation, with particular emphasis USA; Kaoru Kitajima and Joseph Wright are at the spective provided by data from on the impact of the unique Smithsonian Tropical Research Institute, Unit 0948, different scales permits a compreecological variation of tropical APO AA, Miami, FL 34002-0948, USA. hensive assessment of functional forest on gas exchange in the diversity in the canopy, and its role canopy. in ecosystem exchange processes. The diversity of functional characters is high in tropical Canopy water relations forest because of the high diversity of life forms and speSeasonality of water availability and phenology ties, and their varied responses to environmental variation. Seasonal drought constrains the productivity of Although the growing season is not limited by low temperatropical plants whenever water deficits are sufficient to limit 408
2 22-g 0 20 -
‘5 18’ 2 16g
Month Fig. 1. Mean monthly rainfall (unfilled circles, dashed line) and mean monthly global radiation (filled circles, solid line) at a dry forest site (Parque Metropolitano) in Central Panama. Global radiation averaged 48% greater in the dry season (February and March) than in the cloudy wet season (June to November).
C assimilation4. Most tropical forests experience seasonal drought and are at least partially deciduous, and trees in these forests typically have a major leaf flush at the beginning of the rainy season. Although many species drop their leaves during the dry season, those with access to deep soil water typically produce leaves and flowers to coincide with the dry season when irradiance is high and herbivory is lows. Studies of stable hydrogen isotope concentrations of xylem sap suggest that tropical evergreen species may have access to more abundant soil water at a greater depth than neighboring deciduous [email protected]
Similarly, evergreen forests in Brazil require deep soil water to maintain green canopies during the dry season, with roots absorbing water from soil to depths of more than 8m (Ref. 7). Hydraulic architecture and water transport Despite almost two centuries of water-relations studies, how tall trees and lianas deliver water to the upper canopy is incompletely understood. Indeed, recently there has been serious debate as to whether the venerable cohesiontension theory, which states that water is pulled through a plant by tensile force, is sufficient to explain the ascent of sap in tall tree+10. A more complete description of the hydraulic architecture of trees requires knowledge of vulnerability to drought-induced cavitation (a common event in tropical species), the extent of hydrostatic pressures produced by roots (root pressure may refill cavitated vessels), leaf specific conductivity (which along with transpiration can predict pressure gradients throughout the plant) and water storage capacity (critical for surviving drought and regulating the duration of gas exchange during drought)11J2. Limited data suggest that tropical trees are more vulnerable to cavitation” than temperate trees, and that in the tropics, evergreen species are more efficient at supplying water to a given leaf area than are deciduous speciesi3. For example, the evergreen tropical tree Schefflera morototoni achieves high stem capacitance and high specific leaf conductivity at the cost of high vulnerability to cavitationi4. Ultimately, it should be possible to show that hydraulic architecture and associated dry-season water relations are functionally correlated with specific patterns of phenology. Canopy photosynthesis Complex spatial variation in light The canopy of tropical forest is a complex mosaic of sunlight intensity. Although irradiance generally decreases as one descends from the surface of a tropical canopy, there is TREE vol.
great variation from point to pointls. Light at the canopysurface can exceed 2600ymol photons m-2s-1 (Ref. 16) and extinction can be as much as 94% over just 5m (Ref. 17). In Panama, we have routinely observed a drop of more than 90% directly below the uppermost canopy leaves. Most tropical trees place leaves throughout the canopy, not solely at its surface, and leaves in shaded canopy microhabitats exhibit the characteristic low gas exchange rates of shadeacclimated plants in the understoryl*. Managing strong irradiance in the canopy Work over the past decade shows that regulation of absorbed energy by the xanthophyll cycle is pervasive in terrestrial plants, and this mechanism of energy dissipation is especially important for canopy leaves under the strong irradiance of equatorial regionsigJ0. Tropical canopy species have the highest xanthophyll activity of all tropical forest plants studied, including those growing in treefall light gap+. These pigments shunt excess energy into a biochemical process that prevents free radical formation and damage to membranes and chlorophyll pigments, and the level of protection varies depending on the strength of irradiance during growth. In the canopy, xanthophyll protection is especially important during drought when leaves can be under strong irradiance at the same time that stomata limit gas exchange and the use of absorbed energy by photosynthesis. Trees growing at several levels in a dry forest produce young leaves that are better protected by the xanthophyll cycle than are mature leaves, which can more completely use absorbed energy through photosynthesiszl. One of the most tantalizing uses of this phenomenon is the possibility that the spectral shift in reflectance shown by leaves using xanthophyll cycle regulation can be used to indicate the regional potential for C gain through remote spectrophotometry22. Such a development could open up entire regions of inaccessible tropical forest for the study of productivity from airborne platforms. Seasonality of water and light In the tropics, where temperatures permit year-round growth, the timing of leaf production may be viewed as the result of selection for optimization of C gain with respect to the availability of light and water (Fig. l)sj*s.Evidence suggests that photosynthesis in the canopy is limited by cloudy conditions, especially for wet forests, where the radial growth of trees increases in years with higher irradiance (D.A.Clark, pers. commun.)*‘Q5.Most tree leaves are shaded by lianas, lateral shade from neighbors, and within-tree selfshadings, and cloud cover during the rainy season frequently reduces irradiance on exposed leaves below photosynthetic light saturation (>450-600 umol photons m-zs-1) (Refs 26-28). During the early dry season, water stress remains low, while clear skies provide increased irradiance. Thus, many tree species produce leaves just before and during the early dry season, and capitalize on this window of opportunity for C gain through higher assimilation capacity and water-use efficiency than leaves produced at the beginning of the rainy season*9JO.We are just beginning to document the diversity of leaf production strategies with respect to the seasonal opportunity for C gain. Drought limitation of photosynthesis can be especially acute in epiphytes and hemiepiphytes. In Panama, an epiphyte species with some CAM (Crassulacean acid metabolism) activity showed the highest water-use efficiency relative to two C, species31. CAM,which minimizes water loss during the day, is clearly an important adaptation among epiphytes, but the relative contribution of 409
REVIEWS gain for canopy leaves and streamline data collection for large-scale models of C exchange. It remains to be shown that this relationship holds for leaves in different canopy microhabitats.
rate of net COP assimilation
Fig. 2. Integrated daytime netcarbon (C) gain (unfilled circles; i?=O.92, PC 0.001) and integrated nocturnal C loss (filled circles; R2=0.43, P
CAM to the overall C budget of the forest canopy is unknown32. Correlates of assimilation capacity Interspecific variation in leaf photosynthetic capacities and leaf lifespan are linked to contrasting strategies of optimizing C gain over the lifetime of leaveS33-35. The highest photosynthetic rates are observed among tropical pioneers and early successions, which experience high irradiance throughout their lifetimes and produce short-lived leaveG36. Ecus insipida, a C, species that colonizes forest gaps throughout the neotropics, shows photosynthetic rates up to 33.1 pmol CO, m-2s-1,the highest rate of any tree species studied to dates?. Canopy leaves of most tropical species show maximum photosynthetic rates of 5-25 pmol m-Y (Refs 26-28,33,38), and interspecific differences in photosynthetic capacities per unit leaf area and leaf lifespan are associated with differences in a suite of functional characters, including leaf nitrogen (N) concentration and leaf mass per area18J9. Within a species, these characters are also determined by irradiance during growth, such that both photosynthetic capacity and N content generally decrease as one moves lower in the canopyJO.The observed range of leaf phenologies and functional characters correlated with photosynthetic capacity and leaf lifespan suggests that there are diverse solutions to the problem of resource allocation in tropical canopies. A strong relationship exists between instantaneous maximum assimilation and daytime C gain estimated from die1 carbon dioxide (CO,) exchange for exposed leaves of eight tropical species (Fig. 2)41.Such measures repeated several times a year could be used to predict the annual C budget for individual leaves41. Furthermore, because photosynthetic capacity is a strong correlate of leaf N content, it may be possible to estimate annual C income by periodic sampling of N contentsi. Periodic sampling is essential since leaf N content and photosynthetic rates concomitantly decline with leaf age. If the relationship among leaf N content, maximum assimilation and annual C gain can be generalized to most canopy species, it will permit rapid estimation of annual C 410
Stomata/ limitation of C gain Stomata1 closure in response to vapor pressure deficit (VPD) in the air is one of the most commonly observed limits to C gain in tropical canopies. Regardless of the season, leaves of most tropical tree species show mild to extreme midday stomata1 closure whenever temperatures and radiation load in the canopy cause excessive evaporative demand28S38742. Midday reduction in conductance is particularly important in evergreen species during the dry season, but it may not be evident during the wet season, depending on the species and conditions, and it is not observed in some wet forest [email protected]
Indeed, species within the same forest often show contrasting stomata1 response to VPD. For example, canopy leaves of the evergreen Anacardium excelsum are exquisitely sensitive to VPD at the leaf surface, showing strong stomata1 limitation to C gain throughout the dry seaso+, while leaves of nearby Lueha seemannii show no reduction in photosynthesis below that in the wet season27. As detailed below, this diversity of functional response to humidity has important implications for large-scale models of canopy gas exchange. Scaling exchange processes from leaf to landscape Scaling of physiological processes from the leaf to the landscape level is a requirement for understanding the impact of tropical forest gas exchange on global CO, and climateds. A recent issue of Plant Cell and Enoironment40 reported that attempts at upscaling have met with some success in temperate systems, but only one group40,46has published results from tropical forest. This group has recently shown that old-growth tropical forest is probably a net C sink, challenging the conventional wisdom that this ecosystem is roughly in respiratory and photosynthetic balance46, an important result in the context of tropical deforestation and exponentially rising atmospheric CO,. Considering the global importance of this task, it is essential that this work be done in the tropics as widely and quickly as possible. Upscaling water vapor exchange from leaf to tree The first study to take simultaneous measures of flux at more than one spatial scale in a tropical canopy is that of Meinzer et ~1.4, in which the coupling coefficient (Q factor) was estimated for an emergent canopy tree, Anacardium excelsum, in the dry forest surrounding a crane in Panama (see ‘aggregation approach’ in Box 1). This species has the potential for a thick boundary layer because of its large, closely packed, ovate leaves that produce considerable within-branch self-shading. The boundary layer allows transpired water vapor to humidify the air near the leaf surface. Leaf-level measures of stomata1 conductance (in which the boundary layer is removed during measurement) resulted in a 10 to 100% overestimation of crown transpiration when compared to concurrent measures of sap flow using the heatbalance technique of monitoring stem sap velocities. The magnitude of this error increased sharply with increasing conductance, reflecting the decoupling effect of the boundary layer. Unfortunately, extrapolation of stomata1 control of CO, to larger scales is not simply analogous to that of water vapor because CO, uptake is not a linear function of the CO, gradient between the leaf and the air, and because light can change CO, uptake without affecting stomata. TREE vol.
Box 1. Approaches to upscaling As reviewed by Jarv+, there are three approaches to upscaling leaf data: summation, averaging and aggregation. Each of these approaches may compound errors of measurement at smaller scales, but in theory, these errors can be controlled through simultaneous measurements at multiple scales of observation”. The goal of the summation approach is to quantify and sum all individual fluxes in the system of interest. Gas exchange data from single leaves are collected to create a regression model that predicts the CO, and water-vapor exchange of leaves under a range of ambient conditions. The predicted values are summed over the scale of interest. The large number of simultaneous leaf chamber studies that are required to parameterize summation schemes make this impractical for stand and landscape studies, but data of this form are necessary to develop the other two approaches. The averagingscheme uses the range of leaf-level values of gas exchange to estimate a set of average parameters, such as stomata1 conductance, for a ‘big-leaf’ model of fluxes at the stand or higher level. This approach assumes that the gas exchange of all leaves can be treated collectively as a single surface. The average for the stand can then be extrapolated to the landscape. Critical to the success of this method is (1) stratified sampling of functional units in the region of interest, and (2) understanding the behavior of stomata1 and boundary layer conductances at larger scales. Accordingly, the aggregation approach, in which measures are made of stand or landscape fluxes, takes into account that there is large-scale feedback from the atmosphere to the plant that is dynamically mediated by boundary layer physics. High stomata1 conductance stabilizes transpiration by decoupling the saturation vapor deficit at the leaf surface from that in the ambient air. There is an analogous decoupling at the stand and landscape levels, in which high values of canopy conductance tend to reduce sensible heat flux through the convective boundary layer above the vegetation, and thus stabilize transpiration and CO, exchange with the atmosphere48.
Upscaling CO, exchange to the landscape Work in Amazonia has shown that big-leaf models of gas exchange (which treat the photosynthetic surface of the canopy as a homogeneous entity; described in Box 1) can be calibrated against eddy covariance measurements of CO,, water vapor and sensible heat flux to predict yearly C gain40. The eddy covariance technique requires direct measurement of these fluxes for periods of weeks or months over a uniform stand of vegetation with a generally smooth canopy surface. The big-leaf model was developed from water vapor and CO, fluxes that were measured above a dry canopy, and which were used to parameterize an empirical model of stomata1 conductance and a biochemical model of leaf assimilation. This calibrated model was used to estimate gross primary productivity and to predict the effects of increasing atmospheric CO, on ecosystem productivity. This study used a relatively homogeneous palm-rich forest without the high diversity of patches and edges typical of tropical forest. Because of the sensitivity of the eddy covariance technique to such environmental heterogeneity, it may not be possible to extrapolate these results to all old-growth tropical forests. Regardless, this study remains a robust demonstration of the ability to unify measures taken at the landscape level with flux models based on leaf biochemistry and empirical stomata1 responses. The next decade Three areas will be developed as the promise of tropical canopy ecophysiology unfolds: energy capture in leaves, whole-plant patterns of resource allocation and water relations, and refinement of upscaling models to include the functional diversity found in tropical forest canopies. We have only scratched the surface with regard to understanding the role of photoinhibition and photoprotection in the C budgets of tropical plants20. Studies of leaf-level TREE
no. 10 October
physiology should focus on how leaves process the characteristic high energy load under clear tropical skies, beginning with detailed studies of seasonal and die1 variation in energy availability and leaf energy transfer. For example, under extreme evaporative demand at midday, leaves of many species close their stomata and allow mesophyll temperatures to rise. What are the biochemical dynamics of energy dissipation under such extreme conditions with the Calvin cycle shut down? What are the C costs of overnight repair of tissue damage? Dry season leaves should have significantly different strategies for energy management than wet season leaves, and this feature will be central to defining the array of functional leaf types in tropical canopies. Studies of temporal and spatial variation in C and nutrient allocation and water relations should be expanded from the leaf level to intermediate scales, such as branches, and ultimately to the whole plant in order to develop an organismal view of resource regulation. Improved canopy access permits experimental manipulation of the opportunity for C gain, for example, through strategic artificial shading or defoliation of branches. Similarly, flexible canopy access provides an unparalleled opportunity to follow seasonal and diurnal variation in carbohydrate pools throughout the plant with respect to variation in C acquisition by the canopy47. Simultaneous measurements of water potentials and resistances throughout tall trees and lianas will provide critical tests of existing models of water movement. Lianas, which in such high diversity characterize tropical forests, will be an especially profitable group for study because of their potential for acclimation to habitats throughout the canopy, and their ability to maintain water flow to leaves over great distances during drought. Incorporating the functional diversity found in tropical forest is the central challenge for implementing upscaling models (Box 1). Realism could be added to the models by identifying functional units, or patches, and developing sub units that express the unique effect of the functional units on the overall behavior of the model. For example, different tree species with contrasting access to soil water may show large differences in stomata1 conductance. When conspecifics occur as a patch of several adjacent individuals in the landscape, their aggregate effect on the atmosphere and consequent feedback on leaf physiology must be considered42. Cranes and mobile towers can be used to acquire the leaf-level data for such functional units across a heterogeneous landscape. Edges present a similar complication, and their inclusion in upscaling models requires that spatial variation in exchange processes across an edge be measured. The ultimate goal of quantifying and predicting the dynamics of atmospheric and ecosystem C fluxes cannot be realized without first quantifying the diverse effects of the functional units found in tropical canopies. Acknowledgements We thank the National Science Foundation (IBN-9220759 to S.S.M. and S.J.W.; BIR-9419994 to S.S.M.), the Smithsonian Scholarly Studies Program (awards to S.J.W. and S.S.M.), and the Andrew W. Mellon Foundation (award to K.K.) for support.
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