Regeneration niches and functional traits of three common species in subtropical dune forest

Forest Ecology and Management 260 (2010) 1490–1497

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Regeneration niches and functional traits of three common species in subtropical dune forest R.M. Gunton a,1 , L.J. Boyes a , M.E. Griffiths a , M.J. Lawes b,∗ a b

School of Biological and Conservation Sciences, Forest Biodiversity Research Unit, University of KwaZulu-Natal, P/Bag X01, Pietermaritzburg 3209, South Africa School for Environmental Research, Charles Darwin University, Ellengowan Drive, Darwin, NT 0909, Australia

a r t i c l e

i n f o

Article history: Received 27 April 2010 Received in revised form 29 July 2010 Accepted 29 July 2010 Keywords: Disturbance Late-successional Nitrogen Pioneer Ruderal Shade-tolerance Acacia karroo Celtis africana Diospyros natalensis Isoglossa woodii

a b s t r a c t South African coastal dune forests are young, highly disturbed subtropical communities where conventional models of forest dynamics may be challenged. We tested predictions from the gap-phase regeneration model by comparing seedlings of three common species representing contrasting regeneration strategies: Acacia karroo as a ruderal, Celtis africana as a coloniser of forest gaps, and Diospyros natalensis as a late-successional species. We grew seedlings under contrasting light and nitrogen levels in a greenhouse and in the field for 1 year to compare their growth and survival rates, allocation and photosynthetic traits. Species’ growth rates generally followed the expected order: Acacia > Celtis > Diospyros, but Acacia responded strongly to light and Celtis responded strongly to nitrogen, leading to cross-overs in growth rates. The plasticity of allocation and photosynthesis did not clearly differentiate the strategies, although it was greater in the light-demanding species. Acacia and Celtis tended to survive better in Acacia stands than in forest plots. Leaf-level light compensation points (LCPs) were similar for the three species in most conditions, but auxiliary data suggest Diospyros has a lower whole-plant LCP than Acacia. Growth rates and LCPs were lower than most of those reported for primary-forest species in the literature, suggesting an unusual degree of shade-tolerance in this habitat. We discuss reasons why variation in shade-tolerance may be less important here than in the prevailing model for forest regeneration and suggest other biotic factors that may help differentiate regeneration niches. Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved.

1. Introduction In spite of the stochastic nature of seedling recruitment (Hubbell et al., 1999; Hubbell, 2005), forest regeneration opportunities are believed to provide a light–shade niche axis along which tree species may be ordinated, in tropical (Condit, 1996; Poorter and Arets, 2003), subtropical (Easdale et al., 2007) and temperate (Lusk and Reich, 2000; Portsmuth and Niinemets, 2007) forests. This gap-phase regeneration model is supported by a trade-off of lightresponsiveness vs. shade-tolerance (Kitajima, 1994; Barker et al., 1997; Lusk and Reich, 2000), reflecting species’ regeneration niches and driving succession from fast-growing pioneers towards shadetolerant, late-successional species. This continuum is not obscured by the functional classification of species into pioneers and latesuccessional species (Swaine and Whitmore, 1988). Indeed, other groups may be defined according to species’ plasticity and ability to exploit abrupt changes in the light environment. Denslow

∗ Corresponding author. Tel.: +61 08 89466527; fax: +61 08 89467720. E-mail address: [email protected] (M.J. Lawes). 1 Present address: Institute of Integrative and Comparative Biology, University of Leeds, Leeds, LS2 9JT, UK.

(1987) proposed a third functional group, “ruderal” tree species, which colonise open environments. Such trees, which may not be obligate forest species, have poorer survival than forest pioneers in low light, but they may be generalists in other respects. Other important axes of functional variation among forest species include nutrient requirements (Fownes and Harrington, 2004; Russo et al., 2008) and drought tolerance (Holmgren and Poorter, 2007). These are likely to be more important in types of forest where substrate conditions promote greater stress and disturbance. Coastal dune forests in southern Africa represent a young community (<6000 y, Eeley et al., 1999) generally comprising up to 100 tree species at any locality (Weisser, 1980). Forest patches are observed to arise from coastal grassland via bush encroachment (von Maltitz et al., 1996) and may have limited lifespans owing to landscape-scale vegetation shifts driven by fire, climate and human influences. Alongside the subtropical alternation of cool dry and warm wet seasons, there can be severe local disturbance from large herbivores (antelope, hippopotamus and elephant), exacerbated by the sloping terrain with its sandy, nutrient-poor substrate. The low canopy (<15 m) is dominated by broadleaved evergreen trees including Diospyros natalensis, D. inhacaensis and Teclea gerrardii (Nzunda et al., 2007). A dense subcanopy of the pervasive woody monocarpic herb Isoglossa woodii reduces light penetration to the

0378-1127/$ – see front matter. Crown Copyright © 2010 Published by Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2010.07.047

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ground, but its periodic die-back every 4–7 years (Van Steenis, 1978) may give regeneration opportunities for light-responsive species (Tsvuura et al., in press). At some sites these forests also contain clearings dominated by thickets of Acacia karroo. Often located in the dune slacks and largely anthropogenic in origin (Weisser, 1980), these thickets have persisted for at least 50 years and appear to be in a state of arrested succession (Boyes et al., in press). Although not exclusively a forest species, Acacia appears to maintain its dominance at the expense of pioneer species that typically colonise forest gaps, such as Celtis africana and Zizyphus mucronata. However, large dead Acacia stems found under the forest canopy in some places suggest a role for this species in primary succession at least. Plant adaptations may be defined as alternative ways of allocating resources to produce traits that maximise fitness. The mapping of allocation responses to environmental conditions constitutes a species’ strategy, so that the strategies of different species may be compared by measuring fitness under a range of conditions. In this paper we aim to elucidate the niche axes that may be important for subtropical dune forest dynamics by examining allocation and fitness components in the most abundant species of each of three regeneration niches, grown under contrasting light and nitrogen levels. We expect ruderals (represented by A. karroo) to have rapid growth but poor survival in shade. Pioneers (represented by C. africana) were expected to show higher plasticity in growth and physiological parameters in response to varying light levels, consistent with an opportunist strategy, whereas late-successional canopy species (represented by D. natalensis) were expected to have lower growth rates and plasticity at the morphological level (Portsmuth and Niinemets, 2007). At the same time, we hypothesized that more-plastic physiology would enable a positive carbon balance to be maintained in a wider range of conditions. 2. Materials and methods 2.1. Study species A. karroo (Fabaceae) is an evergreen heliophyte (Venter, 1976) associated with open habitats, forming thickets within dune forests but not found under a closed canopy (Boyes, 2007). Its leaves are thin, containing phenolics and high levels of tannins (Dube et al., 2001) and defended by paired thorns. Root nodules harbour nitrogen-fixing bacteria (Cramer et al., 2007). C. africana (Ulmaceae) is a common pioneer of coastal dune forests and other lowland forests in southern and eastern Africa (Kalema and Kasenene, 2007; Chapman et al., 2008); at our site it was the commonest pioneer (constituting 2% of trees; Z. Tsvuura, unpublished data) and one of the most common seedling bank components under a closed canopy (10% of seedlings, Boyes et al., in press), with young trees often found in canopy gaps and adults on forest edges. It has thin, deciduous leaves, and older trees develop a light, spreading canopy. D. natalensis (Ebenaceae) is the dominant species in coastal dune forest (Nzunda et al., 2007), constituting 20% of stems >2.5 cm dbh (Z. Tsvuura, unpublished data) and an evergreen. Its young leaves turn dark green, thick and waxy as they expand; they have low palatability and high longevity. 2.2. Field experiment Seedlings of Acacia, Celtis and Diospyros, approximately 10 cm tall, were planted in plots in coastal dune forest at Cape Vidal in the iSimangaliso Wetland Reserve, South Africa (28◦ 16 S, 32◦ 29 E). Five stations were established around each of three Acacia thickets. Each station consisted of a location in the Acacia thicket and a matched location 50 m into the adjacent forest, beneath

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a closed canopy (under both I. woodii and tree cover). At each of these 30 locations (five stations × three Acacia thickets × two matched locations at each station), two 1 m × 1 m plots spaced at least 1.5 m apart were cleared of all vegetation and planted with five evenly spaced seedlings of each species. Seedlings that died within 2 weeks were replaced. One of the plots was selected at random for nitrogen enrichment by adding 20 g m−2 of limestone ammonium nitrate fertiliser in January prior to planting the seedlings; this is estimated to provide each seedling with an extra 0.4 g N, or 20% above the 2 g N estimated to be available in a rooting zone 50 cm deep (based on a background soil content of readily available N of 45 mg kg−1 ; Boyes et al., 2010). Levels of N may increase by just 10% from forest to Acacia thickets (Boyes et al., 2010). All plots were protected from large-mammal activity by covering with a weld-mesh wire cage (mesh size: 5 cm). The heights and stem diameters of surviving seedlings were monitored every 6–7 weeks for a year (February 2004–January 2005). Light levels in closed canopy and thicket areas were determined as proportional transmittance of photosynthetically active radiation (PAR) on cloudy days between 1000 h and 1400 h. At each plot, we calculated the ratio between readings of two PAR quantum sensors (SQ-110; Apogee Instruments, Logan, UT), one positioned in the plot at ground level and one located 4 m high in an open area nearby. The median transmittance under the canopy was 4.8% (interquartile interval: 2.7–7.1%), while the median transmittance in thickets was 42% (interquartile interval: 15–72%). 2.3. Greenhouse experiment Seedlings of the three species, approximately 14 cm tall, were collected from the Cape Vidal forest between November 2004 and January 2005. They were planted singly into 15-cm deep pots of cleaned river sand and grown in a shaded greenhouse at the University of KwaZulu-Natal, Pietermaritzburg. Twenty seedlings of each species were placed under shade-cloth, receiving 2% of ambient PAR, and another 20 were shaded only by the greenhouse roof, receiving 24% of PAR. These values of PAR are in proportion to and in the range of values corresponding to the forest and thicket sites in our field study; 20–50% transmission has also been shown to be the region where maximum growth rates occur for a range of forest species (Poorter, 1999). Every 3–5 days the seedlings were supplied with 100 ml (increased to 200 ml after 12 months) of a 50% strength Hoagland’s nutrient solution (Hewitt, 1966) containing either 1% nitrogen (low), or 10% nitrogen (high) (the lower level was based on soil samples from the field). The seedlings were provided with additional water to keep the substrate moist and the greenhouse temperature was maintained between 15 and 25 ◦ C according to the season, with relative humidity typically 50–60%. The stem height, stem diameter of the first internode and wet mass (after rinsing roots) were measured before planting. After 13 months the plants were harvested and remeasured. Each plant was divided into leaves (including petioles), stems and roots. The total leaf area of each plant was measured using a Li-3100 area meter (LiCor, Lincoln, NE). All the material was then oven-dried for 48 h at 70 ◦ C, and the dry masses of roots, stems and leaves were measured for each plant. We also estimated plant dry masses at the start of the experiment using another set of seedlings (12 of each species) harvested while they were small to derive calibration curves relating dry mass to wet mass for each species. Additional attributes were measured for the Acacia plants. The numbers of root nodules on each plant were counted at the beginning and end of the experiment. At the end of the experiment, the numbers of thorns on a 20-cm length of a terminal branch on each plant were counted and the lengths of a sample of five thorns were measured.

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To estimate light compensation points and photosynthetic rates, we used a Li6400 infra-red gas analyser (LiCor, Lincoln, NE). Four plants of each species per treatment were selected and photosynthesis was measured on one mature leaf of each. An initial photon flux density of 200 ␮mol m−2 s−1 was maintained until the leaf showed a steady rate of photosynthesis. The irradiance was then decreased to zero in 10 steps at intervals of 6 min, taking three readings of photosynthesis at each level. The CO2 level was held constant at 400 ppm, the leaf temperature at 20 ◦ C and the predicted vapour pressure deficit inside the leaf at 1.0 kPa (±0.03). 2.4. Data analysis For the field data, relative growth rates in height and stem diameter were calculated from median heights and diameters of the live plants in each plot, as the slope R in linear regression models of the form: log Wt = log W0 + Rt, where W0 is height or diameter at the start of the experiment and Wt is that after time t. Height:diameter ratios were calculated using the final measurements, as a measure of etiolation. Survival rates were calculated as the proportion of seedlings surviving in each plot after 12 months (when overall survival had fallen to 32%). Means were compared for each habitat and level of nitrogen, with light as a covariate, using multilevel (“mixed-effects”) models to account for spatial association in the data. Thus random intercepts were allowed for each site and each station nested within a site (using the R package lme4; Bates and Maechler, 2009). Since the survival rates were proportions, they were modelled using a generalised linear mixed model structure with log link function and binomial error distribution. Models contained all two- and three-way interactions between species, nitrogen treatment and light levels; habitat was allowed to interact with species and nitrogen but not light because of its strong relationship with light (t = 15.9, P < 0.001; 176 d.f.). For the greenhouse data, relative growth rates R were calculated from data at the start and end of the experiment using the formula R = (log Wt − log W0 )/t, for each of height (RH ), diameter (RD ), dry mass (RM ) and, for Acacia, number of root nodules (RN ). Specific leaf area (SLA) was calculated as the total leaf area divided by total leaf mass. Root, leaf and stem mass fractions (partitioning statistics) are the root, stem or leaf dry mass respectively, divided by the wholeplant dry mass. Since the greenhouse experiment had separate pots and homogeneous conditions, we considered it a fully randomised design and analysed data using Model 1 ANOVA. The photosynthesis data were fit to monomolecular curves of the form A = a(1 − exp(b − cI)), where A is rate of photosynthesis per unit leaf area, I is photon flux density and the other terms are fitted constants for a given plant. This equation (Norman Pammenter, personal communication) provided better fits to our data than the conventional rectangular hyperbola (see also Causton and Dale, 1990). From the fitted data we estimated the maximum rates of photosynthesis per unit leaf area (Amax ) and multiplied these by the SLA for each plant to obtain values on a leaf-mass basis. Using linear regression for light levels 0, 10 and 20 ␮mol m−2 s−1 , we determined the apparent quantum yield (from the initial slope), dark respiration rate (Rd , from the Yintercept) and light compensation point (LCP, from the X-intercept) for each individual. Only plants for which this regression yielded r2 > 0.9 were used. We quantified plasticity using differences between the maximum and minimum mean trait values among the four treatments, dividing these differences by the mean of the two selected values to standardise them. We did this for specific leaf area and root:shoot mass ratios (partitioning) as two measures of allocation patterns, and for physiological plasticity we used LCP and Amax per unit leaf mass. We also divided the Amax by the LCP for each plant to give a measure of responsiveness to varying light levels during

Table 1 Summary of analyses of variance for four response variables of plants grown in the field (2 -values for each term in multi-level linear models), with MacFadden R2 statistic for each model.

Species (Sp) Light (Lt) Nitrogen (Nt) Habitat (Hb) Sp:Lt Sp:Nt Lt:Nt Sp:Hb Nt:Hb Sp:Lt:Nt R2

RH

RD

E

S

d.f.

36.4*** 6.2 11.2 11.9* 2.6 6.0 2.6 5.5 0.2 1.5 0.09

41.4*** 24.5*** 21.3** 16.1** 14.7** 17.5** 10.8* 0.4 0.0 9.8** 0.15

39.5*** 8.7 11.1 17.2** 4.3 3.4 3.0 7.0* 0.1 2.2 0.36

23.1* 2.0 1.8 4.0 1.8 0.6 0.5 2.3 0.2 0.5 0.26

2 1 1 1 2 2 1 2 1 2

RH : relative growth rate (RGR) in height, RD : RGR in stem diameter, E: height: stemdiameter ratio, S: survival. d.f.: degrees of freedom for each variable. * P < 0.05. ** P < 0.01. *** P < 0.001.

the 1-h period over which measurements were taken (short-term acclimation). The uncertainty in all the plasticity and partitioning statistics was estimated by bootstrapping (Quinn and Keough, 2002). In each case we calculated means from 1000 re-samples from our data. For the partitioning data, we re-sampled individual plants to derive from each re-sample a triplet of mean partitioning values (leaf, stem and root mass fractions) that summed to unity. We then ordered these triplets according to their 3-dimensional Euclidean distances from the observed trivariate mean. After discarding the 5% that had the greatest distances, we used the minimum and maximum means for each component separately as upper and lower 95% confidence limits on the observed means. To test for differences among species and treatment groups, we used multivariate analysis of variance (MANOVA). Only two of the variables (leaf and stem mass fractions) were used since the third will always be dependent on the other two. Approximate F-statistics and P-values were derived from the Pillai trace (Quinn and Keough, 2002). All analyses were performed using the software R (R Development Core Team, 2009). 3. Results In the field experiment, relative growth rates were higher in the Acacia thickets than in the forest plots (Fig. 1, Table 1 [Table S1 – Supplementary information]). For Acacia, diameter growth rates also increased with light transmittance (by 0.11% day−1 per percentage point of PAR). Diameter growth rates varied more than height growth rates, and the greenhouse results (see below) suggest they are more closely linked to dry mass. In thickets, Acacia grew at 0.32% day−1 , Celtis at 0.19% day−1 and Diospyros at 0.22% day−1 ; adding nitrogen increased the growth rate of Celtis to 0.28% day−1 but had no significant effects on Acacia or Diospyros. The height:diameter ratios show greater etiolation in the forest and mostly suggest partitioning strategies changing with light availability. The exception is for Celtis in conditions of added nitrogen, where light increased growth rates without affecting etiolation. Survival rates, however, were lower for Celtis than the other two species (a median of zero in forest plots); there were also nonsignificant trends towards higher survival for Acacia and Celtis in the Acacia thickets and the converse for Diospyros, although the model fit did not deteriorate significantly even when habitat and light transmittance were both removed. In the greenhouse experiment, mortality was low (14 out of 120 plants) and almost entirely restricted to Celtis, where 33% of plants died. Mortality in this species was unaffected by either light or nitrogen (P > 0.1, N = 40, using logistic regression), but it is

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Fig. 1. Growth and survival of each species beneath a forest canopy and in Acacia thickets, with (solid lines) and without (dashed lines) nitrogen enrichment. For growth rates and height: diameter ratios, the lines connect means summarising the growth of all surviving plants in each of 15 quadrats; vertical bars show standard errors. For survival, the lines connect medians of the survival rates in the same 15 quadrats, with bars extending to the quartiles of the data.

possible that growth became impeded by the limited volume of the pots. Growth rates were faster than those of the field experiment [Table S2 – Supplementary information], in spite of the lower average light levels: on average 1.5 times faster in the high-light greenhouse treatments compared to in the thicket, and four times faster in the low-light treatments compared to the forest. The three species differed in their rates of growth (except in diameter), allocation and photosynthesis, and also in their growth and allocation responses to light levels, and in growth responses to nitrogen lev-

els (Table 2 [Table S2–Supplementary information]). For relative growth rate in mass (Fig. 2), Acacia grew twice as fast in high vs. low light, reaching 1.2% day−1 under high light and low nitrogen (but high nitrogen reduced the contrast). Conversely, Celtis roughly doubled its growth rate in high vs. low nitrogen, reaching 1.1% day−1 (shady conditions reduced this contrast), while Diospyros showed smaller but synergistic effects of light and nitrogen; its maximum growth rate was 0.9% day−1 [Table S2 – Supplementary information]. Relative growth rate in diameter was generally

Table 2 Summary of analyses of variance for 12 response variables of plants grown in the greenhouse: F-ratios for each term, with the R2 statistic for each model. RM Species (Sp) Light (Lt) Nitrogen (Nt) Sp:Lt Sp:Nt Lt:Nt Sp:Lt:Nt R2

14*** 65*** 12*** 23*** 14*** 0.2 4.9** 0.67

RD 2.7 123*** 13*** 25*** 12*** 0.2 4.3* 0.71

RH

E

42*** 0.0 20*** 3.3* 7.7*** 9.8** 5.4** 0.61

72.5*** 92.6*** 12.8*** 3.0 1.5 7.8** 3.3* 0.72

L-S-R 40*** 88*** 2.9 7.3*** 0.5 0.2 1.6 –

SLA

Amax

Amax[m]

LCP

149*** 137*** 0.7 8.7*** 0.9 0.6 0.0 0.83

52*** 19*** 0.1 1.1 0.3 1.9 2.0 0.80

57*** 0.4 0.1 0.9 0.1 2.0 1.7 0.78

7.1** Acacia: 53*** 39*** 2.1 4.5* 3.4* 0.7 9.4** 0.0 1.6 0.73 0.56

RN

LT

DT

Acacia: Acacia: 154*** 4.0 0.9 0.0

1.4

0.1

0.82

0.11

d.f. 2 1 1 2 2 1 2

RM : relative growth rate (RGR) in dry mass, RH : RGR in height, RD : RGR in stem diameter, E: height: stem-diameter ratio, L-S-R: partitioning among leaf, stem and root mass fractions (approximate F-statistics and P-values from MANOVA), SLA: specific leaf area, Amax : maximum unit leaf rate, Amax[m] : maximum unit leaf-mass rate, LCP: light compensation point (the last three were log-transformed). Also, for Acacia only: RN : RGR in number of nodules, LT : length of thorns, DT : density of thorns. d.f.: degrees of freedom for each variable in the univariate ANOVAs. * P < 0.05. ** P < 0.01. *** P < 0.001.

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Fig. 2. Growth rates in mass (RM ), height (RH ) and diameter (RD ), ratio of plant height: stem diameter at harvest and specific leaf areas (SLA), comparing shady (2% transmission) and bright (24% transmission) conditions in the greenhouse experiment. Dashed lines indicate low nitrogen supply, solid lines high nitrogen. The vertical bars show standard errors of the means, based on the 39 Acacia, 27 Celtis and 40 Diospyros plants that survived.

proportional to that in mass, but growth in height behaved differently (Fig. 2). Celtis had the highest vertical growth rate that we observed (0.5% day−1 ) under high light and high nitrogen, yet with reduced nitrogen its vertical growth was the slowest of all (0.15% day−1 ), giving plants a stunted appearance. Diospyros required high nitrogen to increase its vertical growth under high light (to 0.3% day−1 ); Acacia grew vertically at around 0.4% day−1 under all conditions. The median height at harvest of plants in the different treatments ranged from 18 to 30 cm for Diospyros, from 33 to 115 cm for Celtis and from 73 to 90 cm for Acacia. Partitioning between leaves, stems and roots clearly distinguishes the three species (Fig. 3). Acacia invested predominantly in stem and leaf mass under low light but more in root mass under high light. Celtis allocated biomass less to roots and more to leaves under low light, its limited etiolation responses notwithstanding. Diospyros allocated the greatest proportion to leaves of any species, especially in low light. Its response to nitrogen level was minimal

except for reducing allocation to roots slightly [Table S2 – Supplementary information]. Specific leaf area (SLA) decreased in the order Celtis > Acacia > Diospyros; it was also reduced by on average 35% in high-light conditions but not affected by nitrogen availability (Fig. 2). For Diospyros our values for SLA at high light and nitrogen are similar to those reported from forests in the same area by Midgley et al. (1995), but for Celtis and Acacia they are 50% higher. Maximum rates of photosynthesis, on the basis of both leaf area and leaf mass, were 2–3 times faster for Acacia than for the other species (Fig. 4) [Table S3–Supplementary information]. The maximum rate for Celtis was in turn twice as high as that of Diospyros on the basis of leaf area, but on a leaf-mass basis these two species were similar. Light compensation points (LCPs) for shade-grown plants, at around 3–5 ␮mol photons m−2 s−1 , were similar among all three species regardless of the nitrogen level. LCPs were higher for plants grown in high light, especially for Acacia and Celtis, and for plants grown under low nitrogen [Table S3 – Supplementary Information].

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Fig. 3. Mean leaf, root and stem mass fractions for the three species (shaded regions indicate 95% confidence regions from bootstrapping). The mass-partitioning patterns for each species are shown for low light (circles) and high light (crosses) with low nitrogen (pale shading) and high nitrogen (dark shading).

Dark respiration rates (per unit leaf mass) increased in sun-grown plants, and in Diospyros they were generally less than half the rates of the other species. Quantum yields were highest for Acacia and generally lowest for Celtis. Plasticity varied among the species for both root:shoot ratio and LCP (P < 0.05), with Acacia having the greatest plasticity and Diospyros the least [Fig. S1 –Supplementary information]. Most plasticity

was due to light responses. There were no significant species plasticity differences with respect to SLA, Amax or for light-response acclimation. For Acacia plants, high light increased the proliferation of root nodules and high nitrogen reduced it as expected; the length of thorns was also increased by high light (Table 2). There were no significant effects on thorn density.

Fig. 4. Photosynthetic parameters of each species, comparing low-light and high-light conditions. Dashed lines indicate low nitrogen supply, solid lines indicate high nitrogen. The vertical bars show standard errors of the means, based on 4 plants of each species in each treatment.

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4. Discussion Our results show clear differences between allocation and fitness parameters of the three species in several respects. We first explore how these may explain the species’ observed strategies, and then note some contrasts between our results and findings from other systems, to place this community in the context of tropical and temperate forests. Our three species fitted the expectations for the strategies of ruderal, pioneer and late-successional species in most but not all respects. The rapid growth of Acacia karroo under high light levels and its greater allocation to stems under low light indicate a shade-avoidance strategy. In the sandy thickets where it predominates, Acacia grows quickly from seed, obtaining nitrogen via its nodules and defending captured resources from large herbivores by means of its thorns; the shorter thorn-length in shade may reflect resource limitation but it could also be adaptive to greater herbivore pressure in open habitats (Grubb, 1992). By contrast, the dependence of Celtis africana on elevated nitrogen for rapid growth may be more suited to a forest pioneer that pre-empts space when nutrients are released by disturbance events such as tree-falls. This, together with its deciduous habit, make it unlikely to colonise poor soils. Indeed, Celtis and other dune-forest pioneers such as Ziziphus mucronata often attain large sizes in the forest but regenerate only locally; they are also reported to have high leaf nitrogen concentrations (Midgley et al., 1995). Diospyros natalensis behaves as a shade-tolerant late-successional species, maintaining similar allocation and photosynthetic parameters across contrasting environments and investing resources in durable leaves. However, Diospyros had the lowest plasticity for photosynthetic parameters as well as for partitioning, contrary to our hypothesis. Overall plasticity was greater for the more light-demanding species, as generally reported (Portsmuth and Niinemets, 2007), but the success of slow-growing late-successional species in deep shade seems to require explanation in terms of carbon storage and tissue protection (e.g. leaf longevity and herbivore resistance) rather than plasticity (Walters and Reich, 1999). Relative fitness among our three species is clearly affected by light and nitrogen levels. Light-responsiveness, as indicated by maximum growth rates and photosynthetic capacity, follows the order Acacia > Celtis > Diospyros (i.e. ruderal > pioneer > latesuccessional), but suboptimal combinations of light and nitrogen levels can change the ranking. For example, with low light and high nitrogen in the greenhouse, Celtis had the highest growth rate, followed by Acacia, whereas the opposite combination put Acacia first, followed by Diospyros. Such changes in performance rankings are commonly reported (Sack and Grubb, 2001; Baltzer and Thomas, 2007) and may facilitate stable coexistence by resource partitioning (Tilman, 1982). The tendency for Diospyros to have the highest survival in the shaded field sites, and for Celtis to grow fast in optimal conditions in spite of low survival rates, also accord with tradeoffs often found between growth rates in high light and survival rates in shade (Kitajima, 1994; Kobe, 1999). Soil nitrogen availability appears to be an important niche axis alongside light (Grubb, 1996), since even the marginal rate of N enrichment in the field experiment produced a benefit for Celtis in bright conditions, while the minimal response of Acacia accords with its nitrogen-fixing ability. We expect water availability to be less important, in view of the deep, free-draining substrate of the sand dunes. Differences between the regeneration niches of forest pioneers and ruderals may explain the arrested succession of the Acacia thickets (Boyes et al., in press). The similarity of leaf-level LCPs among our three species when grown in low light need not imply similar levels of shade-tolerance, because whole-plant LCPs depend not only on leaf light-response curves but also on the ratio of leaf area to plant mass and the respira-

tion rates of roots and stems (Givnish, 1988; Craine and Reich, 2005; Baltzer and Thomas, 2007). Acacia had a lower leaf area ratio when grown in shade [Table S2 – Supplementary information] compared to the other species, and this would give it a higher whole-plant LCP compared to the other species, assuming its specific root and stem respiration rates are similar to the other species. In fact, Acacia tended to have higher leaf dark respiration rates than the other species [Table S2 – Supplementary information], and Reich et al. (1998) found that root respiration correlated with leaf dark respiration rates among nine temperate forest tree species, although a study of 13 tropical species found no relationship between growth rates and leaf gas-exchange characteristics (Kitajima, 1994). There is also evidence that differences in shade-tolerance may increase towards the sapling and adult stages (Lusk et al., 2008). We conclude that although leaf-level shade-tolerance at the seedling stage does not differentiate the regeneration niches of our representative dune-forest species, whole-plant carbon balance may well do so. The growth rates we observed are low compared to most other studies. In the greenhouse, Acacia reached 1.1% day−1 , but only 0.3% day−1 in the field; for Diospyros this was 0.9 and 0.2% day−1 , respectively. In the field, seedlings were protected from large herbivores and herbivory was not severe. One comparison of 15 tropical species including both pioneer and shade-tolerant species found that growth rates at 25% full sun ranged from 0.3 to 3.2% day−1 (Poorter, 1999), and a comparison of nine temperate pioneer species at 11% irradiance revealed growth rates between 0.8 and 4.2% day−1 (Grubb et al., 1996); both these studies used seedlings in protected outdoor conditions. A comparison of ten Amazonian species using saplings in situ below the canopy found growth rates for height ranging from 2 to 6% day−1 (Coomes and Grubb, 1998). It may be that the high levels of herbivory and disturbance of the dune-forest habitat select for slower growth and greater investment in defence. The leaf-level light compensation points (LCP) of all three species when grown in low light (3.0–4.9 ␮mol photon m−2 s−1 ) are also rather low in the context of seedling leaf LCPs reported in the literature: values as low as 1.5 ␮mol m−2 s−1 are reported but the majority, for temperate as well as tropical species, are around 5–9 ␮mol m−2 s−1 (reviewed in Tsvuura et al., in press). The potential shade-tolerance of our species is likely related to the dense subcanopy of I. woodii that shades the forest floor. I. woodii typically covers 65–95% of established forest for periods of 4–7 years at a time, reducing light transmittance to <1% of ambient PAR (Griffiths et al., 2007). Our study shows how the regeneration niches for A. karroo (as a ruderal) and C. africana (as a forest pioneer) may be distinguished by nitrogen responses, while the importance of light distinguishes them from D. natalensis. However, our three common representative species of the coastal dune forest community all appear slow-growing and shade-tolerant by contrast with other communities and these findings should be validated by testing other species. The possible absence of fast-growing pioneers warrants further investigation, particularly in the context of the infertile substrate, herbivore pressure and the suppressive effect of I. woodii.

Acknowledgments This work was supported by the Andrew W. Mellon Foundation and the National Research Foundation of South Africa (Focus area: Conservation and Management of Ecosystems and Biodiversity [GUN: 2069339]). We thank Peter Franks and Norman Pammenter for advice on light-response curves, Zivanai Tsvuura and Hylton Adie for fieldwork, the iSimangaliso Wetland Park Authority for hosting our research at Cape Vidal, Ezemvelo KwaZulu-Natal

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