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FEC534.fm Page 378 Friday, May 4, 2001 3:00 PM Functional Ecology 2001 15, 378 – 387 Leaf respiration in two tropical rainforests: constraints on physiology by phosphorus, nitrogen and temperature Blackwell Science, Ltd P. MEIR,*† J. GRACE* and A. C. MIRANDA‡ *Institute of Ecology and Resource Management, University of Edinburgh, The King’s Buildings, Mayfield Road, Edinburgh EH9 3JU, UK, and ‡Departamento de Ecologia, Universidade Nacional de Brasilia, 70910-900, Brasilia DF, Brazil Summary 1. Leaf respiration is a major component of the terrestrial carbon cycle, but is poorly quantified for tropical forests. We measured dark respiration, R, and nutrient concentration (nitrogen, N and phosphorus, P) of leaves within two forest canopies: in Reserva Jarú, south-west Brazil; and Mbalmayo Reserve, central Cameroon. The data, expressed on a leaf area basis (Ra, Na, Pa ) and a leaf mass basis (Rm, Nm, Pm ), were used to quantify the temperature sensitivity of R and to test the hypothesis that leaf metabolism is more strongly constrained by phosphorus than by nitrogen in these lowland rainforests. 2. Leaf respiration rate (Ra, at 25 °C) at Jarú was nearly half that at Mbalmayo (the range in Ra from near the ground to the upper canopy was 0·11–0·78 µmol m–2 s–1 at Jarú versus 0·22–1·19 µmol m–2 s–1 at Mbalmayo), and the mean Q10 for respiration at each site was 2·3 ± 0·9 (1 SD) and 2·0 ± 0·5 (1 SD), respectively. There were significant differences (P < 0·01) between sites in leaf phosphorus concentration, but not in leaf nitrogen concentration: Pm was very low at Jarú (0·2–0·7 mg g–1) but higher at Mbalmayo (0·5–2·4 mg g–1), whilst Nm was similar at both forests (10–45 mg g–1). 3. Rm was not significantly associated with canopy position or specific leaf area (SLA, m2 g–1) in either forest, but a significant relationship between SLA and Nm was found for both sites (P < 0·05), consistent with existing data. At Jarú, Rm was strongly related to Pm (P < 0·001) and less strongly related to Nm (P < 0·05), but at Mbalmayo, Rm was not significantly related to either Pm or Nm. 4. Ra was linearly related to Na and Pa at both sites (P < 0·01), principally because of changes in leaf mass per area (LMA, g m–2) associated with canopy position. At Mbalmayo, LMA explained 70% of the variation in Ra, but only 20% at Jarú. For Jarú, the strongest relationship with Ra was obtained by combining LMA with Pm in a multiple regression (r2 = 0·53); further inclusion of Nm did not improve the regression. At Mbalmayo neither Nm or Pm improved the regression of Ra on LMA. 5. These results indicate a strong influence of LMA on the relative rates of Ra within the vertical gradient of each canopy. They also suggest that at Jarú Pm constrains respiration more strongly than Nm, and further, that the very low Pm at Jarú may explain the lower absolute values of respiration there relative to Mbalmayo, where Pm was higher. The leaves at both sites are typical of lowland tropical rainforests in not having particularly low Nm, and consistent with this, Nm was a weaker predictor of respiration than Pm or LMA. Key-words: Leaf mass per area, leaf nitrogen, leaf phosphorus, nutrient constraints, Q10, temperature sensitivity Functional Ecology (2001) 15, 378 – 387 Introduction The dark respiration of leaves plays a key role in the carbon economy of plants, but is poorly understood © 2001 British Ecological Society †Author to whom correspondence should be addressed. E-mail: [email protected] in comparison to photosynthesis. Leaf respiration in forest canopies may consume 9–22% of gross primary production, and comprise 50–70% of above-ground (autotrophic) respiration (Linder 1985; Malhi et al. 1999; Yoda 1983). This large component of the carbon cycle is also sensitive to temperature and nutrient availability, and its consequent variation in response 378 FEC534.fm Page 379 Friday, May 4, 2001 3:00 PM 379 Leaf respiration in tropical forests to climate can be critical in determining the carbon balance of vegetation (Ryan 1991). The rates of dark respiration, R, and maximum photosynthesis, Amax, are strongly correlated in leaves on a mass and area basis (Amthor 1989). These physiological parameters are also closely tied to leaf nutrient concentration (James 1953), and a strong correlation between Amax and leaf nitrogen concentration, N, has been found amongst different species and biomes, especially when expressed on a dry-mass basis (e.g. Field & Mooney 1986; Reich et al. 1997). More recently, a similar relationship has also been reported between N and R (Reich et al. 1998). However, a significant relationship between leaf physiological capacity (e.g. Amax ) and leaf phosphorus concentration, P, has rarely been observed in temperate, e.g. Pinus (Reich & Schoettle 1988) or tropical forests (e.g. Raaimakers et al. 1995). This may reflect either a lack of studies in appropriate regions, or the lack of a phosphorus constraint. A central role for nitrogen in determining R and Amax is well recognized (Kawahara et al. 1976; Reich et al. 1998; Ryan 1995), although a few studies have shown no correlation (e.g. Byrd et al. 1992). Respiratory and photosynthetic enzymes are nitrogen-rich and energetically expensive to maintain: 30–50% of leaf nitrogen is found in Rubisco (Lawlor 1993), and 50– 60% of maintenance respiration is used in protein turnover (Penning de Vries 1975). However, phosphorus also influences productivity (Smeck 1985) and may be the key limiting nutrient, in place of nitrogen, in lowland tropical rainforests where soils are highly weathered, phosphorus availability is very low, and nitrogen is relatively abundant (Tanner et al. 1998; Vitousek & Sanford 1986). In addition to its requirement in nucleic acid and protein structures, phosphorus is needed for the phosphorylation of ADP in respiration (Amthor 1989) and for the production of triose phosphate, the principal chloroplastic export product (Stitt 1990). Deficiencies in phosphorus can therefore be expected to influence physiological capacity, and do limit the rates of RuBP regeneration and CO2 assimilation (Jacob & Lawlor 1992; Kirschbaum & Tomkins 1990). For whole plants, true nutrient limitation is shown only if the rate of a (growth) process is increased by the addition of that nutrient (Chapin et al. 1986; Tanner et al. 1998). However, such fertilization experiments may not always be conclusive. Some early successional species in tropical rainforest respond more to phosphorus supplements than do late successional species, whilst others, apparently adapted to low phosphorus availability, may not be capable of responding to nutrient supplements, making nutrient limitation more difficult to identify (e.g. Huante et al. 1995; Veenendaal et al. 1996). In these latter circumstances a longer-term change in community composition may be a possible response to a change in nutrient availability (Berendse 1993). In the absence of clear experimental results, data on tissue nutrient concentration, physiological activity and minimal critical requirements can provide an indication of the relative constraints imposed by different nutrients in natural systems (e.g. Marschner 1995; Raaimakers et al. 1995). In this study we present data on dark respiration rates and the concentrations of nitrogen and phosphorus in leaves from the canopies of two tropical rainforests, in Brazil and Cameroon. In addition to measuring the temperature response in leaf respiration, we investigated the extent to which respiration is constrained by nitrogen or phosphorus, and tested the hypothesis that if phosphorus is more limiting than nitrogen, as has been suggested for many lowland rainforests (e.g. Martinelli et al. 1999; Tanner et al. 1998), then we should observe a stronger influence of leaf phosphorus concentration than nitrogen concentration on leaf respiration rate. Materials and methods The site characteristics for each forest are summarized in Table 1. The first site was at Jarú Biological Reserve, Rondonia State, south-west Brazil (10°05′ S, 61°55′ W) and is referred to here as ‘Jarú’. The forest is classed as undisturbed open forest grading to dense forest in places (IBGE 1993). The second site was at the Mbalmayo Reserve, Central Province of Cameroon (3°23′ N, 11°30′ W) and is referred to here as ‘Mbalmayo’. This is a secondary deciduous forest that was selectively logged in 1988 (Lawson 1995). Table 1. Site characteristics for Reserva Jarú, Brazil (undisturbed forest) and Mbalmayo Reserve, Cameroon (secondary forest). © 2001 British Ecological Society, Functional Ecology, 15, 378 – 387 Character Jarú, Brazil Mbalmayo, Cameroon Dominant tree families Mean canopy height (m) Leaf area index (m2 m–2) Total soil organic carbon (%) Total soil nitrogen (%) Total soil phosphorus (%) Rainfall (mm year–1) Above-ground biomass (t ha–1) Moraceae, Leguminoseae, Palmeae 35* 4·0* 1·18† 0·10† 0·011† 1900§ 220* Sterculiaceae, Ulmaceae, Leguminoseae 36* 4·4* 1·83‡ 0·16‡ 0·018‡ 1520‡ 90* Sources for data: *Meir, 1996; †Amaral Filho et al. (1978); ‡Ngeh (1989); §Culf et al. (1996). FEC534.fm Page 380 Friday, May 4, 2001 3:00 PM 380 P. Meir et al. Table 2. Species sampled at Jarú, Brazil and Mbalmayo, Cameroon Species Family Ra M H Jarú, Brazil Maximiliana maripa (Corre Serra) Drude Naucleopsis krunni (Standl) C.C. Berg Theobroma microcarpum Mart. Erythroxylum cf. macrophyllum Cav· Leonia glycicarpa Ruiz Leonia glycicarpa Ruiz Derris pterocarpa (DC) Killip Protium polybotrium (Turcz) Engl. Inga sp. Strychnos amazonicus Krukoff * Inga sp. Cedrela odorata L. Palmae Moraceae Sterculiaceae Erythroxylaceae Violaceae Violaceae Leguminoseae Burseraceae Leguminoseae Loganaceae Leguminoseae Meliaceae 0·11 (0·03) 0·13 (0·02) 0·24 (0·03) 0·22 (0·06) 0·24 (0·03) 0·23 (0·04) 0·37 (0·07) 0·39 (0·14) 0·43 (0·06) 0·78 (0·08) 0·57 (0·01) 0·55 (0·03) 2 1 1 2 2 2 1 2 1 2 1 1 1 1 1 3 10 16 20 20 26 30 32 36 Mbalmayo, Cameroon Hypsodelphis violacea (Ridl.) M-Redh Dichapetalum sp. Afromomum giganteum (Oliv. & Harb.) K. Schum. Trichilia sp. Musanga cecropioides R. Br. Haumania dankelmaniana M-Redh. Staudtia stipitata Warb. Celtis adolfi-friderici Engl. Celtis adolfi-friderici Engl. Musanga cecropioides R. Br. Musanga cecropioides R. Br. Amphimas pterocarpoides Harms. Amphimas pterocarpoides Harms. Marantaceae Dichapetalaceae Zingiberaceae Meliaceae Moraceae Marantaceae Myristicaceae Ulmaceae Ulmaceae Moraceae Moraceae Leguminoseae Leguminoseae 0·22 (0·09) 0·31 (0·11) 0·61 (0·06) 0·39 (0·04) 0·55 (0·08) 0·51 (0·10) 0·40 (0·11) 0·50 (0·02) 0·53 (0·01) 0·90 (0·02) 1·19 (0·02) 0·71 (0·03) 0·83 (0·04) 2 U 2 1 2 2 1 1 1 2 2 1 1 1 1 1 1 1 3 7 12 14 22 26 36 40 Ra (±1 SD; n = 2 – 4) is mean leaf respiration rate (µmol m–2 s–1), corrected to 25 °C as described in Materials and methods. M denotes likely arbuscular mycorrhizal associations for each species: 1 = known, 2 = probable, U = unknown; no likely nonor ectomycorrhizal species were identified (I. Alexander, personal communication); H, height (m); *denotes climber species. - © 2001 British Ecological Society, Functional Ecology, 15, 378 – 387 Measurements were made on fully expanded (but not senescing) leaves from throughout the vertical profile of each canopy. Access to the canopy was via a throughcanopy tower, and measurements were made at all available heights on adjacent leaves (n = 2–4) of each accessible species (Table 2). Gas-exchange measurements were made under similar climatic conditions (clear skies, low wind speeds) in Jarú, Brazil on the nights of 25 May and 4 June 1993, and in Mbalmayo, Cameroon, on 11 and 22 March 1994. Respiration measurements were made at ambient temperature and humidity by sealing attached leaves inside a chamber (Licor, Nebraska, USA) connected in a closed circuit to an infra-red gas analyser (Licor 6200); leaf temperature was measured using a calibrated leaf-chamber thermocouple. Where possible, measurements were made at 2 h intervals during the night. Measurements (three to six) were made during the night for a subset of leaves, and for these leaves (six species, two to four leaves per species; Table 3), the temperature response in respiration was also determined. Leaves were kept in the chamber for 60 s, during which the CO2 concentration rose to ≈50 times the sensitivity of the gas analyser (≈5·0 µmol mol–1; Licor 1990). The efflux rate of CO2 from the leaves was assumed to represent the rate of leaf respiration and was calculated on an area basis according to: Ra (µmol m–2 s–1) = ∆[CO2]Vch /(AchVT) eqn 1 where ∆[CO2] is the change in concentration of CO2 in chamber (µmol mol–1 s–1), Vch and Ach are chamber volume (m3) and enclosed leaf area (m2), respectively, and VT is the volume of one mole of gas at ambient temperature and pressure. Fresh leaf area was measured using a precalibrated Delta-T leaf-area meter (Delta-T Devices Ltd, Cambridge, UK). A leaf corer was used to obtain 10–30 discs (diameter = 16 mm) from each fresh sample, and the leaf material was oven-dried at 70 °C to constant mass. Specific leaf area (SLA, m2 g–1) determinations were made using a precision balance (Sauter Re1614, Albstadt, Switzerland; maximum sensitivity = 0·1 mg). Leaf nitrogen and phosphorus concentrations for the leaves from Mbalmayo were determined using an acid digestion followed by colorimetric analysis (Grimshaw et al. 1989), and for those from Jarú using a Carlo –Erba elemental analyser and an ammonium molybdate FEC534.fm Page 381 Friday, May 4, 2001 3:00 PM 381 Leaf respiration in tropical forests Table 3. Temperature responses for night-time leaf respiration at Jarú and Mbalmayo Species Q10 r2 Jarú, Brazil Maximiliana maripa Theobroma microcarpum Naucleopsis krunnii Inga sp. Leonia glycicarpa Derris pterocarpa Mean 1·5 (0·5) 2·1 (0·2) 2·9 (0·8) 1·7 (0·7) 1·9 (0·3) 4·1 (1·8) 2·3 (0·9) 0·66 (0·23) 0·56 (0·14) 0·64 (0·24) 0·70 (0·15) 0·84 (0·20) 0·47 (0·31) 0·65 (0·11) Mbalmayo, Cameroon Amphimas ptercarpoides Musanga cecropoides Afromomum giganteum Staudtia stipitata Hypsodelphis violacea Celtis adolphi-friderici Mean 1·8 (0·2) 1·6 (0·3) 2·1 (0·5) 3·1 (0·4) 1·7 (1·1) 1·9 (0·6) 2·0 (0·5) 0·87 (0·10) 0·65 (0·23) 0·58 (0·16) 0·54 (0·18) 0·57 (0·42) 0·41 (0·35) 0·60 (0·14) Q10 is the multiple by which Ra (µmol m–2 s–1) increases in response to a 10 °C increase in temperature, obtained by fitting Equation 2 (see Materials and methods); r 2 is the coefficient of determination of the fitted model. Values are means from temperature responses of two to four leaves per species (±1 SD). method (Allen et al. 1974). SLA was used to convert mass-based nutrient concentrations (Nm, Pm; mg g–1) to an area basis (Na, Pa; g m–2) and to calculate the massbased respiration rate (Rm, nmol m–2 s–1) from Ra. An exponential model was fitted to the temperature response data. This type of model is frequently used to represent the temperature response in respiration (e.g. Amthor 1989; Bolstad et al. 1999; Landsberg 1986), and was chosen to facilitate comparison with other studies, although the relationship is almost linear over small temperature ranges. The model used was: Ra = R0 ekT eqn 2 where T is temperature in °C, R0 is Ra at 0 °C and k is the temperature sensitivity in Ra. The relative rate at which Ra increases with an increase in temperature of 10 °C is termed the Q10 (Q10 = e10k ). Respiration, leaf-nutrient concentration and SLA values were compared using single and multiple linear regression analyses. To make an appropriate comparison with area-based leaf nutrient concentrations, SLA (cm2 g–1) was converted into its reciprocal, leaf mass per area (LMA; g m–2). As an area-based description of leaf nutrient content (g m–2) comprises LMA and the massbased value of that nutrient concentration (g g–1), multiple linear regression analysis (using a stepwise procedure) was restricted to the combination of LMA and mass-based nutrient concentrations. Differences between sites or species were tested using t-tests. Statistical analyses were done using SPSS v.6. Results Ten species in each canopy were sampled (Table 2), including individuals from the dominant families of each forest. The list includes species with suspected arbuscular mycorrhizal associations, but none with ectomycorrhizal associations. Leaf temperatures during dark respiration measurement ranged from 21–25 °C at Jarú and 19–24 °C at Mbalmayo, dropping during the night by up to 4 °C at the top of the canopy and by up to 2 °C near the ground. The fitted exponential model explained 47 – 87% of the variance in Ra with temperature, and yielded Q10 values between 1·5 and 4·1 for individual species, with a mean for each forest close to 2 (Table 3). Ra was corrected to 25 °C using the individual species temperature-response functions where available, or by applying the mean Q10 for each forest for species where a temperature-response function was not available. All measured respiration rates, whether Ra or Rm, are reported here corrected to 25 °C. © 2001 British Ecological Society, Fig. 1. Changes in leaf respiration (Ra or Rm at 25 °C) and SLA with height, at Jarú (d) and Mbalmayo (s). Error bars are ±1 SD for all leaves measured per level, one to four species Functional Ecology, per level, n per species = 2 – 4. (a) Ra, µmol m–2 s–1; (b) Rm, nmol g–1 s–1; (c) SLA, cm2 g–1. 15, 378 – 387 Overall Ra (µmol m–2 s–1) was significantly smaller at Jarú than at Mbalmayo (t56 = 5·3, P < 0·001; Fig. 1a), and Ra was significantly larger in the upper canopy (above 25 m) than near the ground (below 5 m) in both forests (t6 = –5·4, P < 0·01 at Jaru; t6 = –3·1, P < 0·01 at Mbalmayo; Table 2). Ra by species and height (Table 2) ranged from 0·78 (upper canopy) to 0·11 µmol m–2 s–1 (1 m) at Jarú; at Mbalmayo Ra ranged from 1·19 (upper canopy) to 0·22 µmol m–2 s–1 (1 m). Mass-based respiration, Rm (nmol g–1 s–1), did not vary with height in either FEC534.fm Page 382 Friday, May 4, 2001 3:00 PM non-palms at the same height (t5 = – 2·0, P > 0·05). Although SLA was slightly larger at Jarú, it decreased with height in both forests from ≈200 cm2 g–1 at 1 m to ≈90 cm2 g–1 at the top of the canopy (Fig. 1c). 382 P. Meir et al. , , Fig. 2. Specific leaf area (SLA), leaf mass per unit area (LMA), nutrient concentrations and respiration rate: Jarú (d) and Mbalmayo (s). (a–c) Variation in Na (g m–2), Pa (g m–2) and Ra at 25 °C (µmol m–2 s–1) with LMA (g m–2); (d–f ) variation in Nm (mg g–1), Pm (mg g–1) and Rm at 25 °C (nmol g–1 s–1) with SLA (cm2 g–1). Also plotted in (d) are data from Reich et al. (1998) for a rainforest in Venezuela (crosses) and a relationship (solid line) reported by Schulze et al. (1994), where Nm = 0·157 SLA. Also plotted in (f ) (solid line) is an Rm–SLA relationship reported by Reich et al. (1998). Values for p and r 2 in each graph refer to regression results for each data set. forest (Fig. 1b), though Rm was also smaller at Jarú (t56 = 6·41, P < 0·001). Differences among species were mostly confounded by position in the canopy, though a climber, Strychnos amazonicus, had a significantly higher rate relative to nearby tree species (t2 = 4·8, P < 0·05; Table 2); and a palm, Maximilliana maripa, had a (non-significantly) lower respiration rate than For Mbalmayo, significant regressions (P < 0·001) were obtained for Na and Pa on LMA, and for Nm and Pm on SLA (Fig. 2). At Jarú the same relationships were either non-significant (Na on LMA; P = 0·26) or less significant than at Mbalmayo (P < 0·05 for all other regressions; Fig. 2). Pa and Pm were significantly smaller at Jarú than at Mbalmayo (Pa: t56 = 12·1; P < 0·001; Pm: t56 = 9·6; P < 0·001; mean Pm was 0·44 mg g–1 at Jarú and 0·71 mg g–1 at Mbalmayo), but leaf nitrogen concentrations, on the other hand, were similar at both sites, with Na between 0·9 and 3·0 g m–2 and Nm between 10 and 40 mg g–1 (Fig. 2). Respiration (Ra ) was significantly associated with LMA at both forests (P < 0·05 for Jarú, P < 0·01 for Mbalmayo; Fig. 2c; Table 4), but the slopes of the regressions were not significantly different from each other [slopes: Jarú = 0·004 (±0·002 SE), Mbalmayo = 0·008 (±0·002 SE)]. In contrast, Rm was not related to SLA at either site (P > 0·2; Fig. 2f). Significant regressions for Ra on Na and Pa were obtained for both sites (P < 0·01; Fig. 3a,b). For Rm (Fig. 3c,d) there was no significant relationship with Nm or Pm at Mbalmayo, but at Jarú there was, with Pm explaining more of the variance in Rm than Nm (Fig. 3c,d). LMA alone explained 20% of the variance in Ra for the leaves at Jarú (Table 4). In a stepwise multiple regression for the Jarú data, incorporating LMA, Nm and Pm as variables, Nm was less significant than Pm in combination with LMA alone, and became nonsignificant when combined with LMA and Pm (Table 4). For Mbalmayo, LMA explained 70% the variance in Table 4. Regression results for stepwise multiple linear regressions of Ra (µmol m–2 s–1) on LMA, Pm and Nm for Jarú (J) and Mbalmayo (M), where Ra = a + bLMA + cNm + dPm © 2001 British Ecological Society, Functional Ecology, 15, 378 – 387 Site Intercept a LMA b J J J J M M M M J+M J+M J+M J+M 0·074 – 0·479* – 0·413** – 0·496** 0·031 0·043 – 0·014 0·017 – 0·002 – 0·523** – 0·355*** – 0·526 0·004* 0·006*** 0·006*** 0·006*** 0·008*** 0·008*** 0·008*** 0·008*** 0·007*** 0·009*** 0·008*** 0·009*** Nm c Pm d 0·014** 0·004 0·773*** 0·629* – 0·0004 – 0·001 0·026 0·036 0·014** 0·007 0·324*** 0·292*** n r2 P (overall regression) 30 30 30 30 28 28 28 28 58 58 58 58 0·20 0·42 0·53 0·52 0·70 0·68 0·68 0·67 0·35 0·42 0·60 0·60 0·01 <0·0001 <0·0001 <0·0001 <0·0001 <0·0001 <0·0001 <0·0001 <0·0001 <0·0001 <0·0001 <0·0001 LMA (g m–2 ), Pm (mg g–1) and Nm (mg g–1) are regression variables; *, ** and *** indicate significance of variable where P < 0·05, 0·01 and 0·001, respectively; n is the number of leaves measured; r 2 is adjusted for multiple regressions. FEC534.fm Page 383 Friday, May 4, 2001 3:00 PM may reflect true species differences, as similar variation in k has been found elsewhere in temperate forest and grassland species (Amthor 1989; Bolstad et al. 1999; Ryan 1991). It is also possible that the measurements included an unquantified component of respiration in addition to the true ‘maintenance’ value, such as that required for biochemical export processes, although this is unlikely because non-senescing leaves were selected (McCree 1970; Thornley & Cannell 2000). Consistent with this view, our data are exceeded by maintenance respiration rates reported for the leaves of crops and grasses (2–16 versus 7–30 nmol g–1 s–1 at 25 °C; Amthor 1989), but with the exception of the slowest rates they are similar to those found for temperate hardwood trees (4–13 nmol g–1 s–1 at 25 °C; Mitchell et al. 1999). 383 Leaf respiration in tropical forests Fig. 3. Leaf nutrient concentration and respiration: Jarú (d) and Mbalmayo (s). (a,b) Ra (µmol m–2 s–1), Na (g m–2) and Pa (g m–2); (c,d) Rm (nmol g–1 s–1), Nm (mg g–1) and Pm (mg g–1). Also plotted in (c) (solid line) is an Rm–Nm relationship from Reich et al. (1998). Regression equations for each data set are specified in each graph. Ra, but the addition of Nm and Pm into the regression did not improve the fit: Nm and Pm were non-significant variables in all formulations (Table 4). Overall, respiration was best predicted on an area basis (Ra ), using LMA alone at Mbalmayo (r 2 = 0·70) and LMA and Pm together at Jarú (r 2 = 0·53), and also for the combined data set of both forests (r 2 = 0·60; Table 4). Discussion © 2001 British Ecological Society, Functional Ecology, 15, 378 – 387 Few published data exist for dark respiration of leaves in tropical forests, although Reich et al. (1998) reported values for a terra firme rainforest in Venezuela of 0·7–1·2 µmol m–2 s–1 (at 25 °C), a narrower range than presented here (0·1–1·2 µmol m–2 s–1), with a higher minimum. The mean Q10 for respiration was close to 2 at Jarú and Mbalmayo, although interspecific variation was noticeable (Table 3). This variation may have resulted from uncertainty in fitting the temperature-response parameter (k) over a small temperature range, but it Nitrogen concentration and respiration (Nm and Ra ) were significantly related to the changes in SLA and LMA accompanying the light gradient within both canopies (Fig. 2). Although the high species diversity at each site made it difficult to determine how representative each sample was of the canopies as a whole, the outcome is strongly consistent with other studies of N and Amax in other temperate and tropical broadleaf canopies (e.g. Carswell et al. 2000; Ellsworth & Reich 1993). Unlike Ra, Rm did not scale with SLA at either forest, and was significantly related to Nm only at Jarú (Fig. 3). These results contrast with a global data set (Reich et al. 1998) where Rm was strongly correlated with Nm. However, Reich et al. (1998) reported on sun leaves only, and where a vertical canopy profile has been sampled elsewhere, only a weak Rm–Nm relationship has been observed (Mitchell et al. 1999). Some Rm : Nm ratios from (canopy-top) sun leaves at Jarú and Mbalmayo are close to those predicted by Reich et al. (1998), but lower in the vertical profile, large variation in SLA disrupts any relationship that may exist between Nm and Rm (Figs 2f, 3c). Strong Rm–Nm correlations have been found among subalpine and boreal trees and shrubs (e.g. Ryan 1995), and an additional explanation for the difference in outcomes may be that such multistand studies incorporate a wider range of species groupings (conifer, broadleaf, etc.), and hence of LMA and Nm, than is usually found in a single canopy (Mitchell et al. 1999). The use of a simple Rm–Nm (or an Amax–Nm ) relationship based only on measurements of sun leaves may therefore overestimate respiration (or photosynthesis) in the middle and lower canopy of a forest. The significant relationship at Jarú and Mbalmayo between SLA and Nm (Fig. 2d) agrees closely with a global correlation reported by Schulze et al. (1994), and with data from the Venezuelan rainforest reported by Reich et al. (1998). The conservation of this relationship among canopies and widely differing species contrasts with the weaker Rm–Nm relationships described above, FEC534.fm Page 384 Friday, May 4, 2001 3:00 PM 384 P. Meir et al. Fig. 4. The mass- and area-based relationships between photosynthetic capacity, Amax, from McWilliam et al. (1996) and Meir (1996), and mean respiration rate. Data points from both sites are mean values for individual species at the same height; Jarú (d) and Mbalmayo (s). Values for P and r 2 in each graph refer to regression results for combined-site data sets. Table 5. Mean leaf nitrogen (Nm, mg g–1) and phosphorus (Pm, mg g–1) concentrations from different individual rainforest sites (*) and the range in Nm and Pm for three classes of rainforest, grouped by soil type (†) Individual forest site* or forest class†, grouped by soil type Nm Pm Reference *SW Amazon *Central Cameroon *Central Amazon *Central Amazon *Central Amazon 25·0 25·7 27·9 18·0 15 0·44 1·15 0·7 0·54 0·51 *Venezuela *Venezuela *Venezuela †‘Moderately fertile’ †‘Infertile’ (oxisol /ultisol) †‘Very infertile’ (podsol /psamment) 14·5 11·6 12·7 24·5–25·4 12·7–19·3 7·4 –1·11 0·7 0·73 0·60 1·2–1·5 0·5 – 0·6 0·4 –1·2 This study This study Carswell et al. (2000) Furch et al. (1989) Ferraz et al. (personal communication) Reich et al. (1994) Medina & Cuevas (1989) Medina & Cuevas (1989) Vitousek & Sanford (1986) Vitousek & Sanford (1986) Vitousek & Sanford (1986) Vegetation was classified as ‘tall’ in the original references, with the exception of the ‘very infertile’ group of sites given by Vitousek & Sandford (1986), which was classified as ‘low’. © 2001 British Ecological Society, Functional Ecology, 15, 378 – 387 and indicates a general structural requirement for nitrogen. In some stands nitrogen may be allocated to structural compounds such as lignin in response to differential within-canopy water stress (Niinements & Kull 1988). However, leaves with larger SLA also had a larger Nm (Fig. 2d); investment in epidermal thickening of canopytop leaves may increase leaf mass per unit area at a small nitrogen cost. Alternatively, high nitrogen investment at low respiratory cost may reflect the presence of nonstructural nitrogen stored in those leaves with large Nm and SLA values. This has been proposed for some species (e.g. Cromer et al. 1993; Field & Mooney 1986), and possible storage sites include defence compounds and Rubisco (Amthor 1989; Millard 1988; Stitt & Schuze 1994). The two forests differed in the variables that best predicted leaf respiration. Although Na and Pa were significantly related to Ra (Fig. 3), the discussion is restricted here to the components of these variables, LMA, Nm and Pm. At Mbalmayo, LMA explained 70% of the variation in Ra, with nutrient concentration contributing no additional predictive power to the regression. In contrast, at Jarú Pm was most strongly related to respiration, explaining the most variation in Ra (33%); LMA improved the coefficient of determination by a further 20%, but Nm was non-significant (Table 4). The small Pm at Jarú may explain the lower Ra values at that site: Pm significantly below 0·7– 1·0 mg g–1, as found at Jarú but not at Mbalmayo, limits leaf photosynthesis and respiration in tropical trees and herbs (Cromer et al. 1993; Marschner 1995, Zech & Drechsel 1992). Small Pm or Ra at Jarú was not, however, associated with low SLA or LMA, relative to Mbalmayo (Fig. 2). Consequently, whilst Pm may have acted as a key constraint on the absolute respiration rate at Jarú, the relative distribution of Ra within the vertical canopy profile in both forests was most strongly influenced by LMA. It is likely that the low Ra at Jarú also reflected a smaller photosynthetic capacity (Amthor 1989). Mean Amax values from McWilliam et al. (1996) and Meir (1996) show significant linear relationships between Amax and R for individual species at Mbalmayo and Jarú (Fig. 4). Respiration was 8–10% of Amax, and the data imply a range in the ratio of Amax : leaf phosphorus between 2 and 5 mmol CO2 mol–1 P s–1. This phosphorususe efficiency exceeds that for Pinus (Reich & Shoettle 1988), but is not exceptionally high in comparison with other tropical species (3–8 mmol CO2 mol–1 P s–1; Raaimakers et al. 1995). The corresponding nitrogen-use efficiency is relatively low for both sites (20–70 µmol CO2 mol–1 N s–1), in keeping with the notion that nitrogen is relatively abundant in tropical forests in comparison with temperate forests (Martinelli et al. 1999). Although nitrogen-fixing species were present in both forests (the Leguminoseae is a dominant family at both sites), ectomycorrhizal species were not found amongst the sampled species, perhaps also indicating a relative abundance of nitrogen (Buscot et al. 2000). Leaf phosphorus and nitrogen stoichiometry therefore appear to be relatively well conserved at both sites, even where Pm is low. However, why Pm should be higher at Mbalmayo is unclear, as both sites have low soil phosphorus concentrations and a similar number of species considered to host arbuscular mycorrhizal (AM) associations (Table 2). Although the presence of AM species may imply adaptation to low phosphorus availability (Moyersoen et al. 1998), those species with AM did not have significantly larger Ra or Pm (paired t-test for AM species at the same height at both sites Ra: t3 = –0·60, P = 0·59; Pm: t3 = 0·03, P = 0·97). On the other hand, the slightly larger soil phosphorus concentration at Mbalmayo (Table 1) conceivably reflects higher phosphorus availability, as the previous disturbances at Mbalmayo (Lawson 1995) could have led to a slow release of available nutrients through the decomposition of organic matter (cf. Lloyd et al. 2001). FEC534.fm Page 385 Friday, May 4, 2001 3:00 PM 385 Leaf respiration in tropical forests Compared with other tropical forests in the Amazon region and elsewhere, the Pm values at Jarú appear to be especially small, particularly for high forest (Table 5). Whether or not those species at Jarú with small respiration rates and small Pm are capable of responding to higher phosphorus availability is unclear (Veenendaal et al. 1996), but with mean Pm < 0·5 mg g–1, the leaves are probably close to being critically low in phosphorus (Cromer et al. 1993; Zech & Drechsel 1992) and may represent an extreme point on the spectrum of leaf metabolic capacity in tall lowland rainforests. Conclusions Changes in LMA associated with the vertical radiation gradient in both forest canopies strongly influenced the relative response in leaf respiration rate to changes in leaf nutrient concentration. Leaf stoichiometry and respiratory metabolism at both sites were fairly well conserved in terms of phosphorus-use efficiency or temperature response in comparison to other studies. However, exceptionally low Pm at Jarú appeared to constrain respiration more strongly than Nm, and is probably responsible for the low absolute rates of respiration at Jarú relative to Mbalmayo, where Pm was higher. Nitrogen was relatively abundant in leaves at both sites and was not the best predictor of respiration for either canopy. Acknowledgements We are grateful to two research programmes for financial and infrastructural support in Brazil and Cameroon: the Brazil–UK ABRACOS project, supported by the UK Overseas Development Administration (now DFID)/ Agencia Brasileira Cooperação, and the UK NERC programme ‘Terrestrial Initiative for Global Environment Research’, TIGER (grant no. GST/02/065). 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