Oecologia (2002) 131:333–342 DOI 10.1007/s00442-002-0888-6 ECOPHYSIOLOGY Elizabeth A. Newell · Stephen S. Mulkey S. Joseph Wright Seasonal patterns of carbohydrate storage in four tropical tree species Received: 3 July 2001 / Accepted: 3 January 2002 / Published online: 14 March 2002 © Springer-Verlag 2002 Abstract We examined the seasonal variation in total TNC concentrations occurred when canopies were at their non-structural carbohydrate (TNC) concentrations in fullest. In Cecro-pia, Urera, and Luehea, TNC concentra- branch, trunk, and root tissues of Anacardium excelsum, tions continued to increase even as canopies thinned in the Luehea seemannii, Cecropia longipes, and Urera caracas- early dry season. The greater photosynthetic capacity of ana growing in a seasonally dry forest in Panama. Our leaves produced at the beginning of the dry season and the main goals were: (1) to determine the main sites of carbo- potential for the export of carbohydrates from senescing hydrate storage, and (2) to determine if seasonal patterns leaves may explain this pattern. In all species, the phenol- of carbohydrate storage are related to seasonal asynchro- ogy of carbon gain was more important than the phenolo- nies in carbon supply and demand. We expected asynchro- gy of reproduction in influencing seasonal carbohydrate nies to be related to seasonal variation in water and light patterns. The combination of high TNC concentrations availability and to foliar and reproductive phenology. and the large biomass of branches, trunks, and roots indi- Cecropia and Urera are fully drought-deciduous and so cates these species are storing and moving large quantities we expected them to exhibit the most dramatic seasonal of carbohydrates. variation in TNC concentrations. We predicted that maxi- mum carbon supply would occur when canopies were at Keywords Total non-structural carbohydrates · their fullest and that maximum carbon demand would oc- Anacardium excelsum · Cecropia longipes · Luehea cur when leaves, flowers, and fruits were produced. The seemannii · Urera caracasana concentration of total non-structural carbohydrates was as- sessed monthly in wood tissue of roots and in wood and bark tissue of terminal branches. Trunk tissue was sam- Introduction pled bimonthly. All tissues sampled served as storage sites for carbohydrates. As predicted, TNC concentrations var- While temperatures in tropical forests are generally con- ied most dramatically in branches of Cecropia and Urera: ducive to plant growth year-round, seasonal variation in a 4-fold difference was observed between dry season max- the availability of water, light, and nutrients has the po- ima and wet season minima in branch wood tissue. Peak tential to limit plant productivity. For example, photo- concentrations exceeded 25% in Urera and 30% in Cecr- synthetic rates may be limited by low light intensities opia. Less dramatic but significant seasonal variation was during rainy seasons when water is plentiful or by observed in Anacardium and Luehea. In all species, mini- drought during dry seasons when light intensities are at mum branch TNC concentrations were measured during their highest (Wright and Van Schaik 1994; Mulkey et al. canopy rebuilding. In Anacardium, maximum branch 1996). The great variety of leaf longevity and patterns of leaf production observed in tropical trees may result in E.A. Newell (✉) part from this contrasting seasonality of water and light Department of Biology, Hobart and William Smith Colleges, availability (Wright 1996). Plants may also adapt to this Geneva, NY 14456, USA e-mail: [email protected] seasonal variation in resource availability at the level of Tel.: +1-315-7813590, Fax: +1-315-7813860 leaf morphology and physiology. There is evidence that some species produce seasonal leaf phenotypes with S.S. Mulkey Department of Botany, University of Florida, Gainesville, characteristics that optimize the allocation of resources FL 32611, USA for carbon gain during different seasons (Kitajima et al. S.J. Wright 1997). Another response to temporal variation in re- Smithsonian Tropical Research Institute, Apartado 2072, Balboa, source availability is to acquire a resource when it is Ancon, Panama plentiful and then store it until it is required. 334 Whenever species experience seasonal asynchronies nies in carbon supply and demand? Although the main in resource supply and demand, we should expect stored conducting cells in wood (secondary xylem) lack protop- reserves to play an important role in the plant’s resource lasts, living parenchyma cells intermingled with trache- budget (Chapin et al. 1990). Tropical deciduous species ids and vessel members do serve as sites of carbohydrate should be no different from temperate species in accu- storage (Kramer and Kozlowski 1979). We hypothesize mulating carbon when leaf canopies are full and drawing that the woody tissue of canopy branches will exhibit the from stored carbohydrates while leafless for respiratory greatest seasonal changes in carbohydrate concentration costs and for the flushing of new leaves. Three species simply because canopy branches are closest to the car- from Neotropical forests were found to follow this pat- bon supply provided by sun leaves and the carbon de- tern, whether they were leafless during the dry season mand of distal reproductive structures. Roots and trunks (Jacaratia mexicana, Spondias purpurea; Bullock 1992) are also expected to store carbohydrates, but with less or during the rainy season (Jacquinia pungens; Janzen extreme seasonal variation. We also hypothesize that: (1) and Wilson 1974). While seasonal variation in carbon greatest seasonal fluctuations in total non-structural car- gain may be less common for evergreen species in tropi- bohydrate (TNC) concentrations will occur in deciduous cal forests than in temperate forests, there still may be species, with maximum and minimum concentrations periods when demand for carbon does not match supply. when canopies are full and rebuilding, respectively, and For example, in three understory Psychotria shrub spe- (2) TNC concentrations will drop during reproduction, cies, the costs of leaf production are paid in part by non- especially if reproduction occurs when current photo- structural carbohydrates stored in shoot tissues (Tissue synthate is unlikely to meet the demands of flower or and Wright 1995). In Piper arieianum, an understory fruit production. These hypotheses were tested by mea- shrub of wet tropical forests, the costs of reproduction suring TNC concentrations monthly in roots and termi- require the use of stored reserves in addition to current nal branch tissues and bimonthly in trunk tissues of four photosynthate (Marquis et al. 1997). common species growing in a seasonally dry forest in The importance of carbohydrate storage in temperate Panama. The species differed in leaf phenology, repro- trees has been well-documented (Kramer and Kozlowski ductive phenology, and successional status. 1979), but we know little about its role in the productivi- This study of the seasonality of carbohydrate storage ty and reproduction of tropical trees. Most studies on the in four tropical tree species is unique for three reasons. seasonal patterns of carbohydrate storage in tropical First, we examine carbohydrates in canopy branch, trees have measured carbohydrate concentrations in one trunk, and root tissues. Secondly, we assess these carbo- organ or another (e.g. canopy branches: Bhatt and hydrates on a monthly basis, allowing for a more de- Appukuttan 1986; trunk tissue: Olofinboba 1969; Newell tailed picture of the seasonality of carbohydrate storage 1994), but rarely has storage been examined in multiple than possible in most other studies. Thirdly, detailed da- organs simultaneously. When branch and trunk tissues ta from previous and concurrent studies on canopy leaf have been sampled together (e.g. Bullock 1992), a limit- physiology and reproductive and vegetative phenology ed number of sampling dates made a detailed description for the same four tree species (Kitajima et al. 1997) are of annual patterns difficult. combined with information on carbohydrate storage to This study addresses the following questions for trop- produce a comprehensive picture of the role carbohy- ical trees: (1) What are the main sites of carbohydrate drate storage plays in the carbon budget of tropical storage? and (2) Are seasonal patterns in carbohydrate trees. concentrations related to predictable seasonal asynchro- Table 1 General information on the species studied. Nomencla- ter at breast height (DBH, mean with range) is for trees from ture follows D’Arcy (1987) and mature height and successional which canopy branch tissues were sampled (n=5) and from which status are based on Croat (1978) and personal observation. Diame- root and trunk tissues were sampled (n=5) Species Cecropia Urera caracasana Anacardium excelsum Luehea seemannii longipes Pitt. (Jacq.) Griseb. (Bert. & Balb.) Skeels Tr. & Pl. General information Family Moraceae Urticaceae Anacardiaceae Tiliaceae Mature height (m) 10–15 5–10 20–40 15–30 Successional status Pioneer Pioneer Early-Late Early-Late Leafless period February–March January–March December/January (<1 week) April/June (4–10 weeks) Leaf production April–December April–November December–June June–December Reproduction May–November April–May January–May January–May DBH (cm) of trees sampled Branch samples 27.2 (23.5–31.5) 16.8 (12.0–22.0) 85.2 (65.0–103.0) 47.9 (34.5–47.6) Trunk and root samples 18.3 (14.5–22.0) 16.8 (12.0–22.0) 76.6 (36.5–133.0) 62.3 (40.0–110.0) 335 Materials and methods Site and canopy approach The study was conducted in a seasonally dry forest in the Parque Natural Metropolitana near Panama City, Panama. Annual rainfall averages 1,740 mm with most precipitation occurring between May and December. The forest is a stand of 75- to 150-year-old second growth, with tree heights up to 40 m. We used a 42-m-tall tower crane with a 51-m jib to reach the upper canopy (Parker et al. 1992). Species The four focal species varied in stature, successional status, and phenology (Table 1, Fig.