Original f aper 135

Gradation in Nutrient Composition and Photosynthetic Pathways Across the Restinga Vegetation of Brazil

F. Reinert'.*. A. Roberts', J. M. Wilson'. L. de Ribas3. C. Cardinotz, and H. Criffiths' University of Newcastle upon Tyne. UK

Universidade Federal do Rio de Janeiro, Brazil Projeto Restinga - Jardim BotSnico do Rio de JaneirolFEEMA

Received: February 26,1996; Accepted: August 11,1996

Abstmct: The restingo comprises coastal vegetation formations which dominate the Atlantic seaboard of Brazil. Exposed sand ridges and associated lagoon systems have poorly developed soils subject to pronounced water deficits. Distinct vegetation zones support a high diversity of life forms, and a comparative study has been undertaken to investigate interactions between degree of exposure, nutrient supply and photosynthetic path- way (C,, or CAM) in selected species across the restinga. A num- ber of species occurring throughout the restinga were chosen as representative species of different life forms, comprising C, pioneer shrubs (Eugenia rotundifolio and Erythroxylurn ovalifo- lium). impounding (tank) terrestrial bromeliad (Neoregelia cruenta: CAM) and the atmospheric epiphyte (Tillandsia stricta: CAM). Comparisons of plant and soil nutrient composition, and airborne deposition were conducted for each zone. Soil nutrient content and organic matter were closely related, reaching a maximum in zone 4. the seaward face of the inner dune. Salt concentration in leaves was independent of atmospheric de- position for the terrestrial species, in contrast to the atmos- pheric epiphyte T. stricta. In the slack area, vegetation formed characteristic "islands" with the soil beneath enriched in nutri- ents, suggesting a complex interplay between plants and soil during the development of vegetation succession. Here, two additional trees were investigated, C, and CAM members of the Clusiaceae. respectively Clusia lanceolata and C. flurninensis. Stable isotope composition of nitrogen (815N) was generally more negative (depleted in 15N) in plants with low total nitro- gen content. This was exemplified by the atmospheric brome- liad. T. stricta. with an N content of 2.91 g/kg and 615N of -12.3 per mil. Stable isotopes of carbon (813C) were used to identify the distribution of photosynthetic pathways, and while the ma- jority of bromeliads and orchids were CAM. analysis of the soil organic matter suggested that C3 plants made the major contri- bution in each zone of the restinga. Since 613C of plant material also suggested that water supply was optimal in zone 4, we conclude that succession and high diversity in the restingo is de- pendent on exposure, edaphic factors, and perhaps a critical mass of vegetation required to stabilize nutrient relations of the system.

Key words: Nutrient composition, coastal vegetation, CAM, bromeliads. Clusia, vegetation zonation, stable isotopes.

Bot.Acta llO(1997) 135-142 0 Georg Thieme Verlag Stuttgart . New York

Introduction

Extensive sandy coastal plains known as restinga are com- monly found along much of the coastline of Brazil. These beach-ridge plains (Suguio and Tessler. 1984; Dominguez et al.. 1992) are relatively long (several km) and narrow (500 to 1000 m) bedforms running parallel to the shoreline, occasio- nally associated with river mouths, and may enclose coastal lagoons sometimes connected to the sea by tidal inlets. Of relatively recent origin, most Brazilian beach-ridge plains originate from Pleistocene and Holocene (120,000 and 5,000 years B.P., respectively), and similar formations extend throughout the South American Atlantic coast. One of the most evident aspects of the restinga vegetation is the zonation pattern from shoreline landward (Arafijo, 1992).

The chronological sequence of geological events from land to sea, the limited period to develop a soil profile, and the relatively uniform structure of restingas provide an excellent opportunity for determining the influences of water and nutrients on vegetation (Fensham, 1993). Previous studies on coastal communities have focused on vegetation zonation patterns, and the correlation between environmental parame- ters such as salt spray and soil nutrients (Barbour, 1978; Donnelly and Pammenter, 1983; Franco et al., 1984; Cutierrkz et al., 1993).

Coastal dune ecosystems are subjected to large inputs of salt in the form of salt spray, seasonal fluctuations in water table levels and also sporadic flooding from high tides and under- ground water table. Salt spray deposition strongly determines influx of minerals into coastal ecosystems (Art et al., 1974; Henriques et al., 1984; Henriques et al., 1986).

Plant life form determines the mode of water and nutrient uptake, and may be classed as either terrestrial, non-functio- nal root epiphytic, or water impounding rosette (tank). The respective nutrient sources for the different life forms are soil, airborne, and a combination of both, in addition to decompo- sition within the tank. One would expect foliar tissue nutrient contents to reflect those of the source at any particular point along the vegetation zonation. Nevertheless, only a small proportion of correlations between plant and soil nutrients have been found to be significant (Auclair, 1979; Hay and Lacerda. 1984; Henriques and Hay, 1992). This fact might be a result of the small amplitude of nutrient variation in the soil of the communities studied (Henriques and Hay, 1992).

136 Bot. A d a 110 (1997) F. Reinert, A. Roberts, J. M. Wilson, L. de Ribas, C. Cardinot, and H. Criffiths

The epiphytes which are completely independent of soil, must rely on epidermal absorption of nutrients and water (Martin et al., 1985, Reinert and Meirelles, 1993), although several nitrogen-fixing bacteria have been isolated from the leaf surface of Tillandsia species. These are believed to supply at least part of the plants requirement for nitrogen (Brighigna et al.. 1992; Puente and Bashan. 1994).

Carbon and nitrogen isotope composition (613C and 6'5N, respectively) of the foliar material and soil organic matter (excluding the sand particles) were measured in a mass spectrometer (Europa Automated Nitrogen Carbon Analysis- Solids/Liquids ANCA-SL System, Europa Ltd, Crewe. UK). 8 3 C and 615N values were obtained in parts per thousand (%.) according to the following equation:

This study was undertaken in order to explore the relation- ships between nutrient supply and photosynthetic pathway for a range of representative species of different life forms widely distributed in the restinga of Barra de Maricd. Two CAM bromeliads were selected; the tank root bromeliad Neoregelia cruenta (Graham) Smith (one of the dominant species, Lacerda and Hay, 1977) and Tillandsia stricta Soland, an atmospheric bromeliad which grows underneath the vegetation. Two C3 bushes Eugenia rotundifolia Casar (Myrta- ceae) and Erythroxylum ovalifolium Peyr. (Erythroxylaceae), were chosen as pioneer species, particularly in the formation of the vegetation islands found in the slack area (Ribas, 1992). In addition two trees, the full CAM Clusia fluminensis and the C3-CAM Clusia lanceolata. were included in the analysis of the slack area, where they predominantly occur.

Materials and Methods

Field work

Field work was conducted during the period of March to April of 1994 in the beach-ridge plains (restinga) of Barra de Marid (between 22" 535 and 22" 525 and 42" 52W and 42" 52W), Rio de Janeiro State, Brazil. The restinga extends over an area approximately 4 km long and between 500 and 1000 m wide. The two sandy ridges are separated by a flat depression, or slack, and delimited to the north by the ocean and to the south by a lagoon of marine origin. A north-south gradient across the restinga is established in terms of salt spray, wind action, and substrate mobility. The study site was defined as an area across the restinga (from the sea to the lagoon), 700 m long and 150 m wide, representing 6 contrasting vegetation zones (see Fig. 1 caption for zone definitions).

Nutrient analysis

Surface soil samples (from the first 10cm) were collected from underneath the vegetation across the restinga (zones 1 to 6) and also outside of the vegetation in the slack area (vegetation island formation: zone 3). Extractable calcium (Ca 2+). magnesium (Mg 2+), sodium (Na+). and potassium (K+) were extracted with 1 M ammonium nitrate. Soil phosphorus (P) was extracted at 20 f 1 "C with sodium bicarbonate (MAFF, 1986).

Foliar samples consisted of pooled leaves of each species for each zone across the restinga, except for Clusia species, which were collected only in the slack area. Leaf samples, dried to constant weight at 65°C were ground to pass a 1 mm sieve and dry combusted in a muffle furnace at 500°C overnight. The soluble mineral constituents in the ash were subsequent- ly dissolved in 36% (v/v) hydrochloric acid. The final aqueous solution was used for determination of Ca2+, Mg2+, Na+, K+, and P (MAFF, 1986).

= Rsample - Rstandard 1000 Rstandard

where Rsample is the molar ratio of 13C: 12C or 15N: I4N in the sample and Rstandard refers to the international standards (Pee Dee Belemnite for carbon; atmospheric N, for nitrogen) with the instrument calibrated against a secondary standard.

Total soil organic matter (OM) was measured as C02 using an infra-red carbon/sulfur analyzer, CS-125 (LECO Corporation, St Joseph, Michigan, USA). Conductivity and pH were measured for a 1 : 2.5 (w/v) ratio of soil to de-ionized water.

Salt spray collection

Ten salt traps were placed along the gradient from the sea to the lagoon, two in each zone, one underneath the vegetation and one outside. Salt traps were composed of a wooden pole 1 m long placed vertically in the ground with a loose filter paper at the top, so that salt spray was collected irrespective of wind direction. The filter papers were exposed to the atmosphere for 5 h on two different days. Salt spray gathered on filter papers was released overnight into deionized water. The aqueous solution was used to determine conductivity, cations (Ca2+. Mg2+, Na+, K+) and P were measured using an Inductively Coupled Plasma Optical Emission Spectrophoto- meter (ICP-OES: UNICAM 701, Cambridge, UK). CI- was measured using ion chromatography (DX100-Dionex. UK).

Plant 83C survey

A survey for the presence of the crassulacean acid metabolism (CAM) in the restinga vegetation was performed among potential CAM species. Plants were classified as potential CAM if they possessed succulent leaves or if CAM had been reported in at least one species in the family. The presence of CAM was determined using the 613C technique as described above. 8 3 C values for CAM plants range from - 12 to - 20%,, C3 plants from - 20 to - 34%. and C4 from - 10 to - 18%,.

Statistics

The data were analyzed using Minitab (Statistical Software- Minitab Inc., USA). Significant differences between the means were determined by one-way ANOVA.

Results

Soil nutrients

The vegetation zones in the restinga of Barra de Maricd, as defined and described in Fig. 1. were sampled so as to determine edaphic and vegetational influences on soil nu- trients. The soil chemistry data across the vegetation zones are given in Fig. 2. It is evident from results across the six zones that macronutrient content and organic matter were

Nutrient Composition and Photosynthetic Pathways in Restingo Vegetation Bot. Ada 110 (1997) 137

N+S

t Sea

Fig.1 Figure 1 shows the study site defined a t Barra de Maricd across the restinga (from the sea to the lagoon) [After Silva and Sonner, 19841. The study site was divided into six zones for the purposes of this study, as follows: Zone 1) Seaward outer ridge: outer (or secondary) sandy ridge, facing seaward occasionally subjected to inundation by seawater during high tides and storms; Zone 2) Landward outer ridge: Shrub vegetation on the outer sandy ridge facing the slack area: Zone 3) Slack valley between the two sandy ridges. In the slack area four distinct vegetational types can be clearly distinguished. From west to east, there is a progression between 1) wet slack or swamp, 2) dry slack, a creeping vegetation dominated by grasses with sparse shrubs of Myrtaceae and Cada- ceae, 3) "clump" or "island" formation surrounded by sparse creeping

1 2 3 4 5 6 1 2 3 4 5 6

4

'c I a 0 5 .1/111 C m 0 5 'c

F 0 0 E

00 1 2 3 4 5 6 1 2 3 4 5 6 00

Lagoon vegetation dominated by Leguminosae and Gramineae. Both Clusia species are mainly found sympatrically in the islands together with N. cruento and T. stricto. 4) fields of Melastomataceae; Zone 4) Seaward inner ridge: inner (or primary) sandy ridge facing the slack, charac- terized by closed Myrtaceae formation; Zone 5) Landward inner ridge: inner sandy ridge facing the lagoon characterized by restingo forest where canopy reaches from 4 to 8 m; Zone 6) Grassland area of disturbed vegetation from a road following the base of inner ridge, this zone between the base of the inner ridge and swamp is dominated by grasses and sparse shrubs. The margins of the lagoon are occupied by the sedge swamp community. The two shrub species used in this work are found up to the landward inner ridge, although more frequently a t the seaward inner ridge (Aralijo, 1992)

invariably higher in zone 4 (the seaward inner ridge) and to a lesser extent in zone 3 (slack area). The correlation coeffi- cients between mean soil macronutrients and organic matter for the six zones were all significant at p < 0.001 (data not shown). Results show that soil development resulting from increasing nutrient input, organic matter level and nutrient retention were closely related to the development of a denser vegetation, typified by zone 4. Ca*+ had the highest concen- tration in the surface soil across the restinga compared to the other macronutrients. except in zone 1 (nearest to the sea) where Na+ was higher. High levels of salt deposition and high tide inundation in this zone probably account for the results.

A comparison of the soil chemistry underneath and outside "island" vegetation formation found in the slack area (zone 3) is shown in Table 1. Mineral nutrients and organic matter were 5 to 7 times more concentrated underneath the vegeta- tion islands than in the open areas. Electrical conductivity, and hence ion content, was also higher underneath the vegetated areas, whereas pH values were similar.

Airborne nutrients

Figure 3 represents salt deposition in both the open areas (Fig. 3 A) and under the vegetation clumps (Fig. 3 B). From the open areas it is clear that topography plays an important role in the airborne deposition across the restinga. with the back of the outer ridge receiving considerably less salt than the

4 Fig. 2 Surface soil nutrients and organic matter content across the restingo of Barra de Maricd (n = 3). Errors bars indicate standard errors. zones zones

138 Bot. Acta 110 (1997) F. Reinert, A. Roberts, J. M. Wilson, L. de Ribas. G. Cardinot. and H. Griffiths

Table 1 pH, all figures are significantly different at p < 0.001, mean f SD. OM: organic matter; EC: electrical conductivity.

Soil chemistry underneath and outside clump vegetation of the slack area of the restingo of Barra de Maric6. With the exception of

Outside 163.7f0.37 28.0f0.06 19.250.09 12.8f0.31 0.489f0.008 2.32f0.10 4.57f0.02 0.659f0.009 0.086f0.005 Underneath 974.9f0.44 204.6f0.09 118.1 f0.43 71.7f0.17 2.252+0.008 10.79f0.30 4.29f0.00 1.244k0.017 0.326f0.005

-

Fig. 3 Mean values of airborne conduc- tivity, and Na+ and CI- concentration in the salt spray deposition outside (A) and underneath (B) the vegetation across the restinga.

Zones

subsequent two zones (zones 3 and 4). On the other hand, airborne deposition under the vegetation canopy decreases exponentially with distance from the sea, irrespective of topography (Fig. 3 B). There were no significant correlations between element concentrations in the soil and in the airborne deposition (data not shown). Salt spray deposition under the vegetation across the resfinga was highly correlated with the foliar nutrient content in Tillandsia sfricta but not in the terrestrial vegetation (data not shown). K+ and P collected in the salt traps were at concentrations below the equipment sensitivity.

Plant nutrients

Leaf macronutrients were generally similar in the two C3 bushes and different from the bromeliads (Table 2). In the present work all nutrients measured in the foliar material were in the range reported for the beach community species

(Henriques and Hay, 1992). Only K+ content in Eryfhroxylum ovalifolium showed a significant correlation with K+ levels in surface soil across the resfinga (data not shown). These results indicate that the variation in nutrient content shown by the terrestrial species did not reflect that of the soil. However, leaves were not rinsed before analysis, such that results would reflect both surface deposition and internal leaf content. Ca2+ was about 140-220 times and Na+ approxima- tely 320-400 times more concentrated in the two terrestrial shrubs, Eugenia rotundifolia and E. ovalifoliurn, compared to the surface soil. K+ was generally high in plant material, 900- 1300 times more concentrated in the terrestrial species than in the surface soil.

Average nutrient values solely in the slack area for six species, including the two Clusia are shown in Table 3. Ca2+ was highest in C.lanceolafa, whereas Na+ was lowest in C.pu- minensis. Nitrogen content was significantly higher in the terrestrial species. Figure 4 shows Na+, Ca2+ and Mg2+ concentrations in salt spray (top) and in leaf material of Tsm'cta (bottom). The pattern of ion deposition in the salt traps was positively correlated with the ion content in the leaves of Tsfricta. Ion contents in the other species showed no significant correlation.

Plant and soil 6'5N

Nitrogen isotope composition (615N) of the soil was extremely variable within each zone across the resfinga (-11.9 to +3.9%o, data not shown). B5N results in the plant material exclusively in the slack area showed that all six species discriminated against the heavier isotope, with the atmo- spheric Tsm'cfa some 8 to 11%, more depleted in 15N ( 8 5 N is more negative). However when 615N data across the resfinga were averaged (Table 4) the two terrestrial species showed positive 6'5N values contrasting with the other two life forms, tank and atmospheric bromeliad, which showed negative values indicating a fractionation effect against the heavier nitrogen isotope. All four species showed significantly diffe- rent N contents. Tillandsia sfricfa had the lowest nitrogen content and showed the lowest 6'5N values (Table 4).

Table 2 Average leaf nutrient content (g/ Mg 2+ Na+ K+ P kg) across the restingo. for four species. SPECIES Ca 2+

Different lower case letters indicate signifi- Eugenio rotundifolio 5.2 f 1.4a 3.7 f 1 .ZA 5.3 f 1 .2a 8.0f 1 .6a 0.083 f 0.01 3a cant differences among species at < Erythroxylurn ovalifoliurn 8.2 f 2.Ob 3.0 f O.gA 4.4 f O.ga 5.5 f 0.6a 0.089+ 0.014a 0.001. Different upper letters indicate Neoregelio cruento 2.5 f 1 .2' 2.2 k0.7' 11.7 f 1 .4b 12.6k 5.5b 0.076f0.014a significant differences among species at < Tillandsia strict0 1 .9fO.gc 2.3f0.6' 7.6f3.6' 4.3 f 1 .ga 0.024f0.007b 0.05 (n =6): mean f SD.

Nutrient Composition and Photosynthetic Pathways in Restinga Vegetation

Table 3 Average leaf nutrient content (g/kg) and foliar nitrogen isotope composition for six species in the slack. Different upper case letters indicate significant differences among species at p < 0.05 (n = 3); mean values f SD.

SPECIES Ca 2+ Mg 2+ Na+ K+ P N 6’5N(%)

Bot. Acta 110 (1997) 139

Eugenia rotundifolia 4.59f0.6Oa 2.88f0.31a 6.72f0.72a 9.97f0.68a 0.067f0.008a 9.67f l.Olab -3.1 f0.85a Erythroxylum ovalifolium 9.55f0.91’ 2.55f0.07’ 3.6550.14’ 5.83f0.67’ 0.082f0.004b 18.52f 1.1 1c -0.750.39’

Tillandsia stricta 2.18f0.21‘ 2.45f0.35ab 5.06f0.19‘ 4.52fO.Wd 0.029f0.00W 2.91 fO.OOe -12.3f 1.33c Clusia flurninensis 11.13f0.23d 11.08f 1.OZc 2.12+0.28e 6.15f0.64’ 0.059f0.004a 8.76f0.46a -3.6f0.25a Clusia lanceolata 22.93 f 1 .34e 3.67 f 0.04d 4.20 f 0.47’ 4.20 f 0.07d 0.082 f 0.008’ 1 1.29 f 1.06’ -2.9 f 0.2Od

Neoregelia cruenta 2.49 f 0.2W 2.80 f 0.21a 1 1 .OO f 0.99‘ 17.06f 0.94‘ 0.068 f O.OOZa 5.59 f 0.46‘ -4.4 f 0.52a

Na+ Ca2+

..-.. B 1

1 2 3 4 5

3

2

1

1 0 1 2 3 4 5

Zones Zones

SPECIES 6’5N (%)

Eugenia rotundifolio 0.3 f 2.0Sa Erythroxylum ovalifoliurn 1.3 f 2.12a Neoregelia cruenta -2.7 f 1.76’ Tillandsia stricta -1 1.2f 1.31‘

0.30

0.25

0.20

0.15

0.1c

0.05

Z.!

2.(

1 .f

1 .(

O.!

Mg2+ Fig. 4 Mean values of (A) Na+, (B) Ca2+, and (C) Mg2+ concen- tration in the salt spray (top) and in the leaf material of Til- landsia strict0 (bottom). Num- bers on the top right indicate Pearson correlation coefficient between each of the above macronutrients in the airborne deposition and in the leaf mate- rial of Tillandsia stricta. * * p <0.01. p <0.05.

1 2 3 4 5 Zones

Table 4 Average 615N (%) va- N (pg/mg) 615N vs N lues, N content (pg/mg), and

the Pearson correlation coeffici- 10.95 f 1 .432a ent between 615N and N con- 18.77 f 1.927’ 0.63 tent for the foliar material

across the restinga of Barra de 6.13 f 0.707‘ Marica. Different lower case let- 2.91 + 0.416d 0.1 3 ters indicate significant diffe-

0.1 9

0.96”

Plant 83C survey

Carbon isotope composition (613C) for the potential CAM plants is presented in Table 5. Among the halophytes sampled there was only one C4 species (Philoxerus porfulacoides). CAM is well represented among Bromeliaceae. Cactaceae. and Orchidaceae. Only one bromeliad (Vriesea procera) was C3.

Table 6 shows 613C values in the surface soil and in the foliar material of the four species which occur across zones 1 to 5. 6*3C of Eugenia rofundifolia and Erythroxylum ovalifolium was around -30%o in zone 4 which suggests lower water use efficiency ( W E ) in these plants. Additionally, B3C of Neo- regelia cruenfa and Tillandsia sfticfa was more negative in this zone, indicating a greater contribution of the C3 pathway. These results also suggest higher water availability in zone 4. N. cruenfa and T. stn‘cfa showed less negative 613C in zone 1, implying a higher contribution of CAM in the plants within this area. The 613C of the surface soil of around - 12% in zone 6 suggested that the organic matter present was derived

rences among species a t p < 0.001, * * p < 0.01 (n = 3); mean f SD.

mainly from C4 grasses. In the other 5 zones, soil 6l3C lay within the range of C3 plants, and did not differ significantly between zones (Table 6).

Discussion

With respect to the two bromeliad species investigated in this study, the tank-forming Neoregelia cruenfa. displayed signifi- cantly higher levels of Na+ as compared to the atmospheric Tillandsia stricta (Table 2). It might have been expected that Tsm’cfa, with long narrow leaves, would trap more salt per unit area than the broad-leaved N. cruenfa (Edwards and Claxton, 1964; Clayton, 1972). Even if the ratio of leaf fresh weight to leaf area (0.131 :T. sm’cfa and 0.101 :N. cruenfa) is taken into account when comparing Na+ content in the two bromeliads, Na+ content in N. cruenfa is still higher (data not shown). This would suggest that results reflect higher Na+ storage in N.cruenfa than expected. T.srn’cfa had foliar K+ contents of the same order of magnitude as the terrestrial species studied, even though K+ concentration in the salt

140 Bot. A d a 110 (1997) F. Reinert. A. Roberts, J. M. Wilson, L. de Ribas. G. Cardinot, and H. Griffiths

Table 5 8 3 C (%) values for potential CAM plants in the restinga of Barra de Marica. (H): halophytes.

SPECIES FAMILY 6’3C (%)

Alternonthera moritima (H) Blutaparon portulocoides (H) Achmea nudicaulis Bilbergia amoena Brornelio othiacanto Neoregelia cruenta Tillandsia stricta T. usneoides Vriesea procera Opuntia sp. Maytenus obtusifolio Clusia fluminensis (exposed) C. fluminensis (shaded) C. lanceolata (exposed) Nymphoides humboldtiona Mollugo verticilata Polypodiurn brasiliensis P. voccinifolium Pteridium aquilinum Epidendrum denticulatum E. huebneri Cyrtopodium sp. Vanilla chamissonis Borreia capitato 6. verticillata Hedyotis thesiifolia

Amaranthaceae Amaranthaceae Bromeliaceae Bromeliaceae Bromeliaceae Bromeliaceae Bromeliaceae Bromeliaceae Bromeliaceae Cactaceae Celastraceae Clusiaceae Clusiaceae Clusiaceae Menyanthaceae Mollugiaceae Polypodiaceae Polypodiaceae Polypodiaceae Orchidaceae Orchidaceae Orchidaceae Orchidaceae Rubiaceae Rubiaceae Rubiaceae

-25.21 -13.23 -1 4.06 -16.01 -1 3.07 -1 3.95 to -1 4.73 -12.89 to -13.71 -15.10 -24.62 -1 6.79 -24.93 -1 6.24 -1 5.76 -21.72 -26.45 -27.39 -24.45 -24.33 -24.61 -14.72 -1 6.47 -27.98 -16.32 -30.32 -27.1 0 -27.80

spray was below the limits of detection. Cells have active transport mechanisms to exclude Na+ and accumulate K+ against an eletrochemical gradient and this general mecha- nism probably accounts for the higher accumulation of K+ than Na+ in the leaf material.

Surface soil nutrient content did not correlate significantly with nutrient content in the plant material of the terrestrial species (data not shown). Similar results were found else- where (Auclair, 1979; Abrahamson and Caswell, 1982). How- ever, the significant positive correlation of soil organic matter (OM) with soil macronutrients (Fig. 2) suggests that plant availability of these elements is primarily controlled by biotic processes. While there is a background contribution of K+, P, Na+. Ca2+, and Mg2+ from abiotic sources (precipitation, salt spray and mineral weathering), the relatively high OM content in the upper layer of the soil helps to conserve these elements and increase their availability to plants (Silver et al.. 1994). Average nutrient content across the restinga was

generally similar for the terrestrial bush species and different from those of the two bromeliads. suggesting distinct utiliza- tion of the restinga resources among the different life forms (Table 1).

It would be expected that relatively wetter sites would have a higher soil nutrient content due to higher decomposition rates than in the drier, water limited areas (Vitousek et al., 1992). Data for the present work suggest that this relationship between water and nutrient levels in the soil holds for the restinga. Zone 4, or the seaward inner ridge, invariably showed higher OM and macronutrients. No direct measure- ment of the soil water status across the sand ridge system was performed. However, lower water use efficiency values inferred from more negative 613C values for the C3 plants within zone 4, and less CAM-like values for the bromeliad species also implied by more negative 613C. suggest higher water availability in this site.

Within the slack area or zone 3, no pattern was evident in relation to resource utilization among the different life forms. The sympatric Clusia species, which differ markedly in photo- synthetic pathway both in the short-term and seasonally (Roberts et al., 1996) appeared to show no clear pattern of nutrient utilization which could be related to the CAM or C, pathway of photosynthesis. It is important to note that members of the genus Clusia are often found growing (hemi) epiphytically in coastal or rain forest formations. The occur- rence of both C3 and CAM forms in the nutrient limited slack area is significant for the development and sustainability of the characteristic “island” or “clumps” of vegetation which they help to form (Roberts et al.. 1996).

In this study we have found excellent agreement between the three methodologies used to analyze airborne Na+, CI- and conductivity (see Materials and Methods). Airborne deposi- tion patterns differed under the vegetation and in the open areas (Fig. 3). In the open areas the profile of the dunes represents the main barrier against salt spray deposition (Fig. 3A). The first ridge inland from the sea (outer ridge) acts as an obstacle to salt deposition in zone 2.111 the slack area airborne deposition increases relative to that in zone 2. Un- derneath the vegetation salt spray deposition decreased exponentially with distance from the sea (Fig. 3 B). This is the result of the height of vegetation in zone 2 being level with the crest of the ridge, thereby attenuating the topographic effect. Henriques and Hay (1992) showed that airborne deposition decreases with distance within the beach line in the restinga of Barra de Maricd. A detailed study of the patterns of salt spray deposition carried out in a dune scrub community in the beach zone showed that airborne deposi-

Table 6 Average 613C (%) values for foliar material and surface soil across the restinga of Barra de Marica. Different lower case letters indicate significant differences among zones in each species a t p < 0.001. Different upper case letters indicate significant differences among zones in each species at p < 0.05 (n = 6); mean f SD.

SPECIES ZONE 1 ZONE 2 ZONE 3 ZONE 4 ZONE 5 ~ ~~~~~~ ~~ ~~~~~~ . ~ -

Eugenia rotundifolio -28.90 f 0.247a -28.59 f 0.580a -27.74 f 0.057a -30.24f 0.071‘ -28.37 f 0.226a Erythroxylum ovalifoliurn -27.77 f 0.092a -27.41 f 0.042a -27.80 f 0.290a -30.43 f 0.219’ -27.38 f 0.474a Neoregelia cruenta -13.95 f 0.021A -14.55 f 0.269”’ -14.32 f 0.085A’ -14.73 f 0.198’ -14.37 f 0.04gAB Tillondsia stricta -12.89f0.177A -12.97f0.191A -13.39f0.269”’ -13.71 f0.071’ -13.21 f0.028AB 613C (%) of surface soil -23.79 f 1.94 -25.71 f 0.28 -28.54 f 0.93 -27.86 f 0.78 -28.1 7 f 0.43

Nutrient Composition and Photosynthetic Pathways in Restingo Veqetation Bot. Acta 110 (1997) 141

tion decreases with distance from the sea within the beach line (Barbour, 1978), and that further inland topography plays an important role in airborne deposition (Holton and Johnson, 1979; Donnelly and Pammenter, 1983). Na+, Ca2+. and Mg2+ in the airborne deposition were highly correlated with these elements in the atmospheric bromeliad Tillandsia stricta (Fig. 4) but not in the tank bromeliad Neoregelia cruenta or the terrestrial species (data not shown).

In nature the observed net fractionation of 15N/'4N is small, generally no more than - 10 to + 20%, in any one system, with meaningful differences often within 1%, (Handley et al., 1991 ; Handley and Raven, 1992). The two terrestrial species had a similar range of 15N across the restinga. As can be seen from the standard deviation of the mean, values had a relatively high scatter (-3.11 to +2.12%, in Eugenia rotundifolia and - 0.71 to + 4.85%, in Erythroxylum ovalifoliurn). Several au- thors have reported a wide range of 6I5N for the same species grown in different sites or under different N regimes (Vitou- sek et al., 1989; Schulze et al., 1994). The atmospheric Tillandsia stricta showed the lowest values of 6I5N values. Stewart et al. (1995) also reported lower 615N values for epiphytes (some of them bromeliads) in comparison to host trees and suggest that epiphytes with more negative 615N values utilize nitrogen derived from l5N depleted deposition.

The nutritional requirements of Neoregelia cruenta are mostly fulfilled by products of decomposition that takes place within the tank, whereas in Tillandsia shicta the majority of nutrients are derived from atmospheric deposition. Brighigna et al. (1992) found several types of N2-fixing bacteria on the leaf surfaces of epiphytic bromeliads (tank and atmospheric). It is possible that T. stricta and N. cruenta rely on N,-fixing bacteria for nitrogen supply. On the other hand the two terrestrial species rely solely on the soil for nutrition. There seems to be a positive correlation between N concentration and 615N in the foliar material (Vitousek et al., 1989; Wendy Robe, University of Newcastle, UK , unpublished data), however this relationship does not always hold. Only N. cruenta showed a significant correlation coefficient (Table 4). The relationship between N concentration and 615N in the foliar material is not fully understood. Results suggested that 6l5N can be further used as a tool to differentiate between nitrogen sources in the restinga environment, and to clarify nutritional processes in epiphytes, provided that sources and sinks are carefully evaluated.

As expected, CAM was not present among halophytes (Winter, 1979). The presence of a more significant biomass of CAM plants inland, such as in Bromeliaceae and Cactaceae was not, however reflected in the 8 3 C of the soil. One possible ex- planation for this fact is that the CAM species in the restinga are slow growing, long-lived plants and do not contribute significantly to soil organic matter.

In conclusion development of complex vegetation represents a tradeoff between exposure and availability of nutrients and water within the restinga. Primary production is largely dependent on meteorological inputs acquired over a period of time through precipitation, and airborne deposition. Reten- tion of nutrients in the ecosystem is almost solely a function of their accumulation in living biomass and soil organic matter, where a greater biomass leads to a greater ability to trap and retain nutrients (Art et al, 1974). It is not surprising

therefore, that life forms represented on the restinga are so diverse. While we may not identify the specific causes of increase/decline in particular vegetation types we note, for example, that atmospheric and tank bromeliads reflect the optimization of different modes of nutrient acquisition and drought tolerance, whilst C3 and CAM trees of the genus Clusia exhibit plasticity at a more physiological level (Roberts et al.. 1996).

Acknowledgements

This work was funded by the Brazilian Government via CNPq. The authors are grateful to the Departamento de Ecologia, UFRJ. in particular to Andre Taouil. Joyce Rocha, Claudio Ferreira, Elazaro. lsabella Reinert and Lucia Ferreira for assistance with field work and to Phil Green, AES Newcastle, for all his technical assistance.

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H. Criffiths Department of Agricultural and Environmental Science. Ridley Building University of Newcastle upon Tyne Newcastle upon Tyne NEI 7RU UK E-mail Howard.Griffiths@ncl.ac.uk

Section Editor: M. Riederer