SEARCH

SEARCH BY CITATION

Keywords:

  • Avicennia germinans;
  • Belize;
  • fertilization;
  • Florida;
  • hydraulic conductivity;
  • leaf water potential;
  • photosynthesis

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  • • 
    Mangrove ecosystems can be either nitrogen (N) or phosphorus (P) limited and are therefore vulnerable to nutrient pollution. Nutrient enrichment with either N or P may have differing effects on ecosystems because of underlying differences in plant physiological responses to these nutrients in either N- or P-limited settings.
  • • 
    Using a common mangrove species, Avicennia germinans, in sites where growth was either N or P limited, we investigated differing physiological responses to N and P limitation and fertilization. We tested the hypothesis that water uptake and transport, and hydraulic architecture, were the main processes limiting productivity at the P-limited site, but that this was not the case at the N-limited site.
  • • 
    We found that plants at the P-deficient site had lower leaf water potential, stomatal conductance and photosynthetic carbon-assimilation rates, and less conductive xylem, than those at the N-limited site. These differences were greatly reduced with P fertilization at the P-limited site. By contrast, fertilization with N at the N-limited site had little effect on either photosynthetic or hydraulic traits.
  • • 
    We conclude that growth in N- and P-limited sites differentially affect the hydraulic pathways of mangroves. Plants experiencing P limitation appear to be water deficient and undergo more pronounced changes in structure and function with relief of nutrient deficiency than those in N-limited ecosystems.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Mangroves are intertidal forests that occur in the tropics and subtropics. They inhabit saline sediments, and their growth and stature generally declines with increasing sediment salinity (Clough et al., 1982) Recent studies have shown that nutrient limitations to growth are also common in mangrove environments (Feller, 1995; Koch, 1997; Feller et al., 2002, 2003; Lovelock et al., 2004). Although mangroves occur in environments that often have an ample supply of water, it is costly for plants to extract water of low ionic content from highly saline soils (Ball et al., 1988; Sobrado, 2000). Consequently, mangroves must limit water loss (i.e. transpiration), which occurs during photosynthetic CO2 uptake. Thus, mangroves have evolved in a setting where the rates of photosynthesis and growth, which are stimulated by high nutrient availability, are restricted by the capacity to maintain a favourable water balance with minimum salt uptake, resulting in trade-offs between nutrient resource utilization and salt tolerance (Ball et al., 1988; Ball, 1996; Lovelock & Feller, 2003). However, different nutrient limitations could have divergent effects on this trade-off.

In tropical intertidal mangrove forests, growth of trees can be limited by nitrogen (N) or phosphorous (P) (Boto & Wellington, 1983; Feller, 1995; Feller et al., 2002; Lovelock et al., 2004). Experimental studies in flooded dwarf Rhizophora mangle L. (red mangrove) forests in Belize (Cheeseman & Lovelock, 2004; Lovelock et al., 2006) and Panamá (Lovelock et al., 2004) suggested that enhancements in growth with P fertilization are associated with an increased capacity of plants to transport water. In other plant species, deficiencies in P are associated with reductions in water uptake (Carvajal et al., 1996), possibly because of the crucial role of phosphorylation in the function of water channels (aquaporins) in plant tissues (Johansson et al., 1998).

In contrast to our studies in Belize and Panamá, growth of dwarf Avicennia germinans (L.) Stearn (black mangrove) mangroves in Florida was N limited (Feller et al., 2003). When these N-limited trees were fertilized with N, growth enhancements were associated with higher photosynthetic capacity (Lovelock & Feller, 2003) and greater leaf area development (Feller et al., 2003). Other studies of the effects of N fertilization on the hydraulic function of trees in other ecosystems found that increases in leaf area were associated with proportional increases in hydraulic conductivity, indicating a high degree of co-ordination between photosynthesis and hydraulic conductivity with N enrichment (Hubbard et al., 2004). Because of the important role that P may have in water uptake (Carvajal et al., 1996; Johansson et al., 1998), and our previous observations of increases in hydraulic conductivity with relief of P limitation (Lovelock et al., 2004, 2006), we predict that where P limits growth, plants should exhibit symptoms of water deficiency [lower leaf water potential (ψleaf)] lower stomatal conductance and higher water-use efficiency (WUE)] that will be alleviated with the addition of P. By contrast, we predict that plant water relations will not be changed by the addition of N to N-limited plants. Rather, we expect N fertilization to stimulate sink strength or the number and activity of meristems, which instead limits photosynthesis and the growth of N-limited plants (Van der Werf & Nagel, 1996; Wilson, 2000). To test these hypotheses, we compared photosynthetic physiology, water relations and hydraulic architecture of fertilized dwarf trees of A. germinans in a P-limited setting in Belize and in an N-limited setting in Florida.

Materials and Methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Site descriptions and experimental design

The study was conducted at Twin Cays, a 92-ha archipelago of mangrove islands located approx. 1.6 km inside the Belizean Barrier Reef Complex (16°50′N, 88°06′W, see Feller, 1995 and McKee, 1993 and references therein for a full site description) and in the Indian River Lagoon, North Hutchinson Island, Florida (27°33′N, 80°20′W, see Feller et al., 2003 for a full description). Briefly, both sites are microtidal, with tidal range of approx. 0.5 m. Mean minimum and maximum air temperatures are, respectively, 25.4 and 28.8°C at the site in Belize and 18.0 and 27.9°C at the site in Florida. Annual rainfall is approx. 2.5 m at Twin Cays, distributed relatively uniformly over the year, while in Florida annual rainfall is 1.37 m, falling mainly in the summer months. Twin Cays is 12 km from the mainland and does not receive terrigenous inputs of freshwater or sediments. The soil is composed of highly organic peat, comprising mainly red mangrove roots, and rests on the Pleistocene coral reef platform. The dwarf forests, where trees are less than 1.5 m tall, occur in the interior of the islands where tidal inundation is frequent and sediments are reduced (−30 mV, Feller et al., 2003). Within the Indian River Lagoon, our site in Florida is an abandoned mosquito impoundment (number 23) in which natural tidal flow and the mangrove forest was re-established in 1976. The mangrove soils are sandy with abundant shell fragments and are highly oxidized (+95 mV, Feller et al., 2003). Pore water salinity was hypersaline in both sites – mean 50 practical salinity units (PSU) – but these conditions are not likely to inhibit the growth of A. germinans to any great extent (see Cintrón et al., 1978). At Twin Cays, the dwarf forests are dominated by R. mangle, but dwarf A. germinans are also present. In Florida, dwarf forests are dominated by A. germinans with scattered Laguncularia racemosa (Feller et al., 2003).

At each site we fertilized eight to nine individual dwarf trees of A. germinans with N or P fertilizer, or designated them as controls (no fertilizer). In Belize, eight replicate trees were selected per treatment (24 total) and the treatments were 10 m apart. For the Florida site, we used nine replicate dwarf trees (27 total), previously described in Feller et al. (2003). The trees were each fertilized first in January 1997, and then at 6-month intervals until April 2001, with 300 g of N fertilizer as urea (45 : 0 : 0; PCS Sales, North Brook, IL, USA), or P fertilizer, as P2O5 (0 : 45 : 0, triple superphosphate; Diamond R Fertilizer Company, Winter Garden, FL, USA), or cored but not fertilized (controls) as described in Feller (1995). Briefly, fertilizer was encased in dialysis tubing (Spectropore; Spectrum, Gardena, CA, USA) and inserted in 30 cm deep × 7 cm wide holes, which were cored in the soil on either side of the tree at the dripline of the canopy. After inserting the fertilizer, the holes were then plugged with the extracted soil core. The same holes were used each time the fertilizer was applied.

Hydraulic conductivity and architecture

Hydraulic conductivity was measured on stem segments of each of the trees in December 2002 in Belize and in March 2004 in Florida. A branch from each experimental tree, cut at least 0.3 m from the target stem segment, was harvested in the morning (before 09:00 h) of measurement. All branches used were produced after the experimental fertilization had been imposed. Stems were transported to the laboratory and re-cut to approx. 7–10 cm length under water, before the measurement, and trimmed with a razor blade. Stems were inserted inline with a perfusion solution of 95% distilled water augmented with 5% seawater (collected locally) and allowed to equilibrate to steady state (approx. 5 min) before measurement. Native stem hydraulic conductivity (KH, kg m−1 s−1 MPa−1) was measured using a flow meter that measures the pressure drop across the stem segment relative to that across a capillary tube of known resistance (Brodribb & Feild, 2000). We used calibrated tubes of differing resistance (PEEKTM tubing; Upchurch Scientific, Oak Harbor, WA, USA) in order to match the resistance of the tube to that of the branch to minimize errors. The capillary tubing and stem segment were placed in series. The pressure applied to the stem was provided by an elevated reservoir, which varied between 2.2 and 2.7 kPa. After measurement, leaves were detached from the stem and their area measured using a Li-Cor leaf area meter (Li-Cor Corp., Lincoln, NE, USA). The KH was divided by the leaf area supported by the stem to give leaf area specific hydraulic conductivity (KL). The mean leaf area of stems sampled for measurements of hydraulic conductivity was 108 cm2 (standard error = 9 cm2).

After measuring the hydraulic conductivity of the stem segment, xylem vessels were stained using basic fuschin red dye drawn into the stem segment by attaching the segment to a 50-ml syringe. Hand-cut sections where mounted in glycerol, then photographed at ×100 magnification (Nikon Coolpix 995; Nikon Corp., Tokyo, Japan). Variation in xylem structure of stem segments was assessed by measuring diameters of 50–100 xylem vessels at ×100 magnification on a randomly selected section from each stem segment using the program scion image (Scion Corp., Frederick, MD, USA). Xylem diameters were weighted to reflect the enhanced flow rates possible with larger-diameter xylem vessels. Hydraulically weighted xylem diameter was calculated as (Σ r5)/(Σ r4), where r is the xylem vessel radius (Sperry et al., 1994). We estimated the magnitude of hydraulic conductivity of the whole hydraulic system, KS–L, using the Soil–Plant continuum model and Cohesion–Tension theory (Tyree & Ewers, 1996; Sperry, 2000), as follows:

E (transpiration or flux per unit leaf area) = KS−L × (ψsoil − ψleaf).

Water potential of leaves and porewater

The ψleaf values were measured in January 2004 in Belize, and in March 2004 in Florida. We measured mid-morning ψleaf values on bright sunny days when photosynthetic rates are at a maximum. One fully expanded leaf, exposed to full sunlight, was measured for each experimental plant. The leaves of A. germinans have salt-excreting glands. To remove salt from the leaf surface, the leaves were washed with distilled water, carefully blotted dry with paper tissues, allowed to air-dry for approx. 15 min and then visually checked for any remaining moisture before sampling. The ψleaf values were measured on leaf punches (5.6 mm diameter) using Peltier-type leaf-cutter psychrometers (Merrill Instruments, Logan, UT, USA) and an automated multichannel microvoltmeter (Model CR7; Campbell Scientific, Logan, UT, USA). Psychrometers were calibrated with NaCl solutions and were capable of measurements down to at least −7.5 MPa. The psychrometers were temperature equilibrated in an insulated water bath for 3–4 h before measurements. Measurements were taken after applying a 2.5 mV excitation voltage for 45 s.

Pore water was extracted from the base of each experimental tree at each site at approx. 30 cm depth using a 50-ml syringe attached to rigid tubing (McKee, 1993). Porewater salinity was measured with a handheld refractometer. The ψ of porewater was measured using leaf-cutter psychrometers (Merrill Instruments; see above) by placing filter papers, thoroughly soaked with porewater, into the chambers.

Photosynthetic gas exchange

Rates of photosynthetic gas exchange were measured with a Li-Cor 6400 photosynthesis measuring system (Li-Cor Corp.) in February 2001 in Belize, and in March 2004 in Florida. Photosynthesis was measured on sunny days with little or no cloud cover, using sunlight under ambient conditions of CO2, air temperature and humidity. The quantum flux density of photosynthetically active radiation was generally saturating for photosynthesis (> 800 µmol m−2 s−1), and thus photosynthetic rates were assumed to be close to maximal. Measurements were made on three young, fully expanded leaves per tree, which were then averaged to obtain one value for each experimental tree. Instantaneous WUE was calculated as CO2 assimilation/transpiration.

After each measurement was completed (usually in approx. 1 min), the leaf was harvested. Leaf area was measured using a Li-Cor leaf area meter (Li-Cor Corp.). Leaves were then dried in an oven at 60°C and then weighed. Dried leaf material was ground to a fine powder in a small mill. The nitrogen concentration within the leaves was analyzed in a CHN analyzer (Perkin Elmer, Norwalk, CT, USA) using a small subsample of the ground leaf tissue. Leaf P concentrations were determined using Inductively Coupled Plasma Mass Spectrometer analysis at the Agricultural Testing Laboratory of Pennsylvania State University (PA, USA). Integrated measures of WUE of leaves were obtained by measuring the leaf carbon isotope discrimination ratio (δ13C), using an Isotope Ratio Mass Spectrometer at the UC Davis Stable Isotope Facility of the Department of Plant Sciences, University of California, Davis (CA, USA).

Data analysis

We used a generalized linear model with site and nutrient treatment as fixed effects in the model. Where a significant main effect or interaction between site and nutrient treatment occurred, we used Fisher's Least Significant Difference post hoc hypothesis test to examine pairwise differences within and among the treatment levels. To analyse for heteroscedasticity, probability plots of all variables and residual plots were examined. For heterogeneous variances, we transformed continuous data using logarithms.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Photosynthesis and stomatal conductance

In control plants, photosynthetic rates and stomatal conductance were lower in the P-limited Belize plants than in the N-limited Florida plants (Fig. 1, main effect of site F1,43 = 42.03, P < 0.0001). In Belize, P-fertilized plants had photosynthetic rates that were similar to those of the controls in Florida (Fig. 1, site × treatment interaction, F2,43 = 12.27, P < 0.0001). In both sites, photosynthetic carbon (C) gain was linearly correlated with stomatal conductance, with both sites showing a similar slope of the relationship between stomatal conductance and photosynthetic C gain (Fig. 2a, R2 = 0.78). Rates of photosynthetic C gain were not correlated with leaf N concentration at either site (leaf N ranged from 0.97 to 2.88%, data not shown), but were correlated with leaf P concentrations at the P-limited site (Fig. 2b, R2 = 0.40). On a dry weight basis, leaf P ranged from 0.028 to 0.21%. The leaf to air vapour pressure difference was variable (range 1.9–2.8 kPa) but did not vary significantly over the sites (data not shown).

image

Figure 1. Photosynthetic CO2 fixation (a) and stomatal conductance (b) in Avicennia germinans trees fertilized with nitrogen (N) and phosphorus (P), or unfertilized controls (C), in Belize where growth is limited by P (dark bars) and in Florida where growth of trees is limited by N (light bars). Values are the mean and standard errors of eight to nine trees per treatment.

Download figure to PowerPoint

image

Figure 2. Variation in photosynthetic CO2 fixation with stomatal conductance (a), and leaf phosphorus concentrations (b) in Avicennia germinans trees fertilized with either nitrogen (N) or phosphorus (P), and in unfertilized controls (C), in Belize where growth is limited by P (open symbols) and in Florida where growth of trees is limited by N (closed symbols). Lines in plots are lines of best fit of the form y = 3.06 + 50.2x, R2 = 0.78 (a, for both sites), y = 3.72 + 3.27x, R2 = 0.40 (b, open symbols, P-limited Belize) and y = 9.58 + 0.18x, R2 = 0.01 (b, closed symbols, N-limited Florida).

Download figure to PowerPoint

Hydraulic conductivity and xylem architecture

The native hydraulic conductivity of stems was similar in the P- and N-limited sites (KH, Fig. 3a, P > 0.05), although in the P-limited site, P-fertilized trees had a significantly higher KH (site × treatment interaction F2,43 = 4.00, P  = 0.025). When conductivity was adjusted for leaf area, no significant differences were found among sites or treatments (KL, Fig. 3b, P > 0.05). Data were variable, particularly in control stems in the N-limited site. Calculation of hydraulic conductivity of the whole soil to leaf pathway, KS–L, found that total pathway hydraulic conductivity was lower in the P-limited compared with the N-limited site (Table 1, main effect of site F1,39 = 17.41, P = 0.002). Although the main effect of treatment was not significant (P > 0.05), fertilization treatments tended to have differing effects at different sites (site × treatment interaction F2,39 = 3.16, P = 0.052). In the P-limited site, fertilization with P tended to increase KS–L, while N fertilization had little effect on KS–L at either site. Fertilization with P at the N-limited site tended to reduce KS–L.

image

Figure 3. Native hydraulic conductivity of stems (KH) (a), and hydraulic conductivity per unit leaf area (KL) (b) for Avicennia germinans trees fertilized with either nitrogen (N) or phosphorus (P), and for unfertilized controls (C), in Belize where growth of trees is limited by P (dark bars) and in Florida where growth of trees is limited by N (light bars). Values are the mean and standard errors of eight to nine trees per treatment.

Download figure to PowerPoint

Table 1.  Total hydraulic conductivity of the soil–leaf pathway, KS–L, in a phosphorus (P)-limited (Belize) and a nitrogen (N)-limited (Florida) site with fertilization with N and P, or left as controls (C)
SiteTreatmentTranspiration (mmol m−2 s−1)ψsoil (MPa)ψleaf (MPa)KS–L (mmol m−2 s−1 MPa−1)
  1. Calculated from: Flux per unit leaf area (i.e. transpiration) = KS–L × (ψsoil–ψleaf). ψleaf, leaf water potential; ψsoil, soil water potential. The ψsoil is estimated from the relationship between porewater soil salinity, measured with a handheld refractometer, and ψsoil measured by psychrometry [ψsoil = −0.073–0.08 × salinity in practical salinity units (PSU), R2 = 0.52].

BelizeC1.63 ± 0.15−4.00 ± 0.19−4.97 ± 0.141.91 ± 0.42
N1.67 ± 0.16−4.06 ± 0.17−4.88 ± 0.222.05 ± 1.18
P2.28 ± 0.16−4.23 ± 0.24−4.80 ± 0.193.19 ± 1.31
FloridaC2.78 ± 0.15−3.82 ± 0.06−4.36 ± 0.149.77 ± 4.27
N3.36 ± 0.16−4.31 ± 0.07−4.47 ± 0.128.28 ± 2.50
P2.93 ± 0.25−3.80 ± 0.05−4.46 ± 0.164.08 ± 0.97

Mean xylem diameters, and hydraulically weighted vessel diameters, were smaller at the N-limited than at the P-limited site (main effect of site F1,43 = 17.35, P < 0.0001). Xylem diameter was not significantly greater in N-fertilized trees at the N-limited site, but was much larger in P- and N-fertilized trees than in control trees at the P-limited site (Table 2, treatment F2,43 = 3.93, P = 0.027). The cross-sectional area of xylem that is vessel lumen was higher in the N-limited site than in the P-limited site (main effect of site F1,43 = 5.48, P = 0.024). Fertilization enhanced the proportion of xylem lumen in P-fertilized plants in the P-limited Belize site and in N- and P-fertilized trees in the N-limited Florida site (treatment F2,43 = 3.17, P = 0.052). The cross-sectional area of the stem that was xylem tissue was higher in P-fertilized plants than in control and N-fertilized trees in the P-limited Belize site (Table 2). For this parameter, comparative data were not available for the Florida site.

Table 2.  Xylem characteristics of Avicennia germinans in a phosphorus (P)-limited (Belize) and a nitrogen (N)-limited (Florida) site with fertilization with N and P, or left as controls (C)
SiteTreatmentMean vessel diameter (µm)Hydraulically weighted vessel diameter (µm)Percentage of the xylem in vesselsProportion of the stem that is xylem
  1. Values are means ± standard error of seven to nine plants. Different letters after the mean values in each column indicate that the means are different at P < 0.05.

BelizeC17.8 ± 1.4a24.8 ± 1.6a 7.5 ± 0.3a27.3 ± 3.1
N21.8 ± 0.9b31.6 ± 0.9b 7.5 ± 0.9a37.5 ± 4.6
P23.0 ± 2.4b33.1 ± 3.5b 9.7 ± 1.3ab48.5 ± 7.1
FloridaC15.6 ± 0.7a21.2 ± 0.8a 8.5 ± 0.9a
N17.3 ± 0.2a22.7 ± 0.8a10.5 ± 0.6b
P16.6 ± 1.0a20.1 ± 1.3a11.0 ± 1.1b

Water potential and water use efficiency

The ψ values were approx. 0.5 MPa lower in the P-limited than in the N-limited site (Fig. 4a, main effect of site F1,43 = 11.39, P = 0.0015), despite no significant differences in substrate salinity between sites or among treatments (Fig. 4b). Instantaneous WUE was higher in the P-limited site than the N-limited site (Site F1,43 = 9.32, P = 0.0039). However, δ13C, which gives a time-integrated indication of WUE, was lower (indicating lower WUE) in the P-limited site than in the N-limited site (Fig. 5, Site F1,43 = 21.27, P < 0.0001). Fertilization had no significant effects on ψleaf or WUE at either site, but δ13C was higher in P-fertilized compared with control plants at the P-limited site (P= 0.0037).

image

Figure 4. Leaf water potential (ψleaf) (a), and soil porewater salinity in practical salinity units (PSU) (b) in Avicennia germinans trees fertilized with either nitrogen (N) or phosphorus (P), and in unfertilized controls (C), in Belize where growth is limited by P (dark bars) and in Florida where growth of trees is limited by N (light bars). Values are the mean and standard errors of eight to nine trees per treatment.

Download figure to PowerPoint

image

Figure 5. The leaf carbon isotope discrimination ratio (δ13C) (a), and instantaneous water use efficiency (WUE) (b) in Avicennia germinans trees fertilized with either nitrogen (N) or phosphorus (P), or in unfertilized control trees (C), in Belize where tree growth is limited by P (dark bars) and in Florida where tree growth is limited by N (light bars). Values are the mean and standard errors of eight to nine trees per treatment.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

Because of the important role that P can have for water uptake and transport in plants (Caravajal et al., 1996; Clarkson et al., 2000), we hypothesized that P-deficient mangroves would be effectively water deficient, while this would not be the case at our N-limited site. At the P-limited site we found that the plants had lower ψleaf values, lower stomatal conductance and lower CO2-assimilation rates, but higher instantaneous WUE, compared with those at the N-limited site, characteristics that are consistent with water deficiency. Contrary to enhanced instantaneous WUE, δ13C was lower at the P-limited site than at the N-limited site, suggesting that long-term WUE was lower at the P-limited site (Farquhar et al., 1989). It is possible that this contrary pattern, of higher instantaneous WUE and lower δ13C observed at the P-limited site compared with the N-limited site, indicates that instantaneous values obtained when photosynthetic rates are at a maximum do not reflect longer-term patterns (Martin & Thorstenson, 1988). Rates of photosynthetic C fixation show marked daily depressions at the P-limited site (Cheeseman & Lovelock, 2004) and in other mangrove systems (Cheeseman, 1994), and therefore WUE may be lower than we recorded for much of the day. Lower δ13C values have also been observed in other nutrient-deficient trees compared with nutrient-replete treatments, indicating there may be a loss of stomatal efficiency with severe nutrient deficiency (Guehl et al., 1995).

Additional support for our hypothesis, that P-deficient mangroves are water deficient, is that fertilization with P at the P-limited site significantly increased stomatal conductance, δ13C, mean xylem diameter, abundance of conductive tissue and KH, and tended to enhance KS–L. Enhancements in KH were tightly coupled with increased leaf area, such that KL was not significantly affected by fertilization treatments. Similar co-ordination of hydraulic conductivity, CO2 assimilation and allocation to leaf area has previously been observed in other species (see review Hubbard et al., 1999, 2001, 2004; Sperry, 2000; Brodribb et al., 2002, 2003; Meinzer et al., 2004).

In our N-limited site, fertilization with N slightly increased xylem diameter and the proportion of the xylem that was vessel lumen, but did not significantly enhance stomatal conductance, KH, KL or KS–L. Apparently, relief from N deficiency in these plants is not tightly linked to improving water-transport processes, but is caused by other processes, such as enhanced meristem activity and associated increase in the strength of C sinks, as the addition of new tissues demands more C for their function (Wilson, 2000, I. C. Feller, unpublished). Fertilization with N in the P-limited site, and with P in the N-limited site, had significant effects on xylem anatomy in some cases, with N significantly increasing vessel size in P-limited plants in Belize, and fertilization with P enhancing the proportion of the vessel lumen in N-limited plants in Florida. The addition of nonlimiting macronutrients therefore does exert some influence on tissue structure and, possibly, function. Changes in vulnerability to mid-day embolism have been observed to occur with fertilization in other species (Harvey & van der Driessche, 1997; Ewers et al., 2000). However, plant hydraulic function was only influenced by the addition of limiting nutrients in the P-limited site in this study.

Unlike stomatal conductance and KH, the lower values of ψleaf at the P-limited site were not ameliorated by fertilization with P. These results suggest that some factor, in addition to P limitation, contributes to the lower ψleaf at the P-limited Belize site. This other factor is unlikely to be salinity, as soil salinity and ψ of porewater in both sites were similar. In Belize – the P-limited site – sediments are reduced more than those in the N-limited Florida site because of consistent inundation (Feller et al., 2002, 2003; McKee et al., 2002). Low-sediment oxygen concentrations inhibit root function, including water uptake (Greenway & Gibbs, 2003), and can alter xylem anatomy (Yanez-Espinosa et al., 2001). Therefore, differences in the ψ across sites could be partially associated with low oxygen concentrations in soils at the P-limited site. Flooded plants have also been observed to transport solutes from roots to shoots, decreasing the ψleaf by 0.08 MPa and providing important signals that give rise to altered physiology and allocation patterns (Jackson et al., 1996). The functional consequences of lower ψleaf and KH in the P-limited compared with the N-limited site may be an increased sensitivity of stomata, and thus transpiration and photosynthesis, to variation in environmental conditions (e.g. leaf temperature, humidity, salinity and redox potential), which would promote survival during unfavourable conditions (Sperry, 2000).

Although our hypothesis that P-limited plants would be water deficient because of the important role of P in water uptake in roots through aquaporins (Caravajal et al., 1996; Clarkson et al., 2000), hydraulic limitations at P-limited sites may also be relieved with P fertilization because P fertilization increases the root surface per unit leaf area of plants (i.e. thinner, longer roots). In addition to increasing root surface area, enhanced allocation to roots in P-fertilized tree of the mangrove, R. mangle, has been observed to contribute to vertical accretion (i.e. soil elevation), thereby reducing inundation and enhancing oxygenation of the root zone (McKee et al., 2002; K. L. McKee, unpublished). Understanding the mechanisms underlying P limitation of hydraulic conductivity requires more detailed study of allocation to roots and root function at both N- and P-limited sites.

Conclusions

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

This study shows that in the mangrove species A. germinans, over N- and P-limited sites, physiological characteristics conform to similar relationships (e.g. Fig. 2), but physiological processes which result in enhancements in growth with relief of nutrient limitation differ between N- and P-limited mangrove ecosystems. In our P-limited site, hydraulic conductivity appeared to be a key process limiting photosynthetic C gain and thus growth. By contrast, in the N-limited site, hydraulic conductivity was not improved by fertilization with limiting N. Instead allocation to leaf area, by increasing the number of branching modules, is implicated in improving the performance of N-fertilized trees (Feller et al., 2003, I. C. Feller, unpublished). At the P-limited site, plants had lower ψ, lower KH and lower δ13C than at the N-limited site. With P fertilization, the δ13C approached that of the N-limited site, together with improved hydraulic conductivity, greater xylem vessel diameter and rates of photosynthetic C gain, suggesting that relief from P deficiency improved plant water uptake and transport.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References

This study was supported by the National Science Foundation under Grant DEB 9981535, awards from the Smithsonian Marine Station at Fort Pierce (contribution no. 656), and a Mellon Foundation award to M. C. Ball. The work also received support from the Smithsonian's Marine Science Network, and logistic support from the Caribbean Coral Reef Ecosystems Program (contribution no. 755). We thank the staff of Carrie Bow Cay Research Station and Pelican Beach Resort, Belize, and those of the Smithsonian Marine Station in Fort Pierce.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  • Ball MC. 1996. Comparative ecophysiology of mangrove forest and tropical lowland moist forest. In: Mulkey SS, Chazdon RL, Smith AP, eds. Tropical forest plant ecophysiology. New York, USA: Chapman and Hall, 461496.
  • Ball MC, Cowan IR, Farquhar GD. 1988. Maintenance of leaf temperature and the optimisation of carbon gain in relation to water loss in a tropical mangrove forest. Australian Journal of Plant Physiology 15: 263276.
  • Boto KG, Wellington JT. 1983. Phosphorus and nitrogen nutritional status of a northern Australian mangrove forest. Marine Ecology Progress Series 11: 6369.
  • Brodribb TJ, Feild TS. 2000. Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforest. Plant, Cell & Environment 23: 13811388.
  • Brodribb TJ, Holbrook NM, Edwards EJ, Gutiérrez MV. 2003. Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant, Cell & Environment 26: 443450.
  • Brodribb TJ, Holbrook NM, Gutierrez MV. 2002. Hydraulic and photosynthetic co-ordination in seasonally dry tropical forest trees. Plant, Cell & Environment 25: 14351444.
  • Carvajal M, Cooke DT, Clarkson DT. 1996. Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function. Planta 199: 372381.
  • Cheeseman JM. 1994. Depressions of photosynthesis in mangrove canopies. In: BakerNR, BowyerJR, eds. Photoinhibition of photosynthesis: from molecular mechanisms to the field. Oxford, UK: Bios Scientific Publishers, 377389.
  • Cheeseman JC, Lovelock CE. 2004. Photosynthetic characteristics of dwarf and fringe Rhizophora mangle in a Belizean mangrove. Plant Cell & Environment 27: 768780.
  • Cintrón G, Lugo AE, Pool DJ, Morris G. 1978. Mangroves of arid environments in Puerto Rico and adjacent islands. Biotropica 10: 110121.
  • Clarkson DT, Carvajal M, Henzler T, Waterhouse RN, Smyth AJ, Cooke DT, Steudle E. 2000. Root hydraulic conductance: diurnal aquaporin expression and the effects of nutrient stress. Journal of Experimental Botany 51: 6170.
  • Clough BF, Andrews TJ, Cowan JR. 1982. Physiological processes in mangroves. In: CloughBF, ed. Mangrove ecosystems in Australia: structure, function and management. Canberra, ACT, Australia: Australian National University Press, 194210.
  • Ewers BE, Oren R, Sperry JS. 2000. Influence of nutrient versus water supply on hydraulic architecture and water balance in Pinus taeda. Plant, Cell & Environment 23: 10551066.
  • Farquhar GD, Ehleringer JR, Hubick KT. 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40: 503537.
  • Feller IC. 1995. Effects of nutient enrichment on growth and herbivory of dwarf red mangrove (Rhizophora mangle). Ecological Monographs 65: 477505.
  • Feller IC, Whigham DF, McKee KM, O’Neill JP. 2002. Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62: 145175.
  • Feller IC, Whigham DF, McKee KL, Lovelock CE. 2003. Nitrogen limitation of growth and nutrient dynamics in a mangrove forest, Indian River Lagoon, Florida. Oecologia 134: 405414.
  • Greenway H, Gibbs J. 2003. Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes. Functional Plant Biology 30: 9991036.
  • Guehl JM, Fort C, Ferhi A. 1995. Differential response of leaf conductance, carbon isotope discrimination and water-use efficiency to nitrogen deficiency in maritime pine and pedunculate oak plants. New Phytologist 131: 149157.
  • Harvey HP, Van der Driessche R. 1997. Nutrition, xylem cavitation and drought resistance in hybrid poplar. Tree Physiology 17: 647654.
  • Hubbard RM, Yoder BJ, Ryan MG. 1999. Evidence that hydraulic conductance limits photosynthesis in old ponderosa pine trees. Tree Physiology 19: 165172.
  • Hubbard RM, Stiller V, Ryan MG, Sperry JS. 2001. Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant, Cell & Environment 24: 113121.
  • Hubbard RM, Ryan MG, Giardina CP, Banard H. 2004. The effect of fertilization on sap flux and canopy conductance in a eucalyptus saligna experimental forest. Global Change Biology 10: 427436.
  • Jackson MB, Davies WJ, Else MA. 1996. Pressure flow relationships, xylem solutes and root hydraulic conductance in flooded tomato plants. Annals of Botany 77: 1724.
  • Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P. 1998. Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10: 451460.
  • Koch MS. 1997. Rhizophora mangle L. seedling development into the sapling stage across resource and stress gradients in subtropical Florida. Biotropica 29: 427439.
  • Lovelock CE, Feller IC. 2003. Photosynthetic performance and resource utilization of two mangrove species coexisting in hypersaline scrub forest. Oecologia 134: 455462.
  • Lovelock CE, Feller IC, McKee KL, Engelbrecht BMJ, Ball MC. 2004. The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panama. Functional Ecology 18: 2533.
  • Lovelock CE, Ball MC, Choat B, Engelbrecht BMJ, Holbrook NM, Feller IC. 2006. Linking physiological processes with mangrove forest structure: phosphorus deficiency limits canopy development, hydraulic conductivity and photosynthetic carbon gain in dwarf Rhizophora mangle. Plant, Cell & Environment 29: 793802.
  • Martin B, Thorstenson YR. 1988. Stable carbon isotope composition (δ13C), water use efficiency, and biomass productivity of Lycopersicon esculentum, Lycopersicon pennellii, and the F1 hybrid. Plant Physiology 88: 213217.
  • McKee KL. 1993. Soil physicochemical patterns and mangrove species distribution – reciprocal effects? Journal of Ecology 81: 477487.
  • McKee KL, Feller IC, Popp M, Wanek W. 2002. Mangrove isotopic fractionation (δ15N and δ13C) across a nitrogen versus phosphorus limitation gradient. Ecology 83: 10651075.
  • Meinzer FC, Woodruff DR, Shaw DC. 2004. Integrated responses of hydraulic architecture, water and carbon relations of western hemlock to dwarf mistletoe infection. Plant, Cell & Environment 27: 937946.
  • Sobrado MA. 2000. Relation of water transport to leaf gas exchange properties in three mangrove species. Trees: Structure and Function 14: 258262.
  • Sperry JS. 2000. Hydraulic constraints on plant gas exchange. Agricultural and Forest Meteorology 104: 1323.
  • Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE. 1994. Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75: 17361752.
  • Tyree MT, Ewers FW. 1996. Hydraulic architecture of trees and other woody plants. In: MulkeySS, ChazdonRL, SmithAP, eds. Tropical Forest Plant Ecophysiology. New York, NY, USA: Chapman & Hall, 217243.
  • Van der Werf A, Nagel OW. 1996. Carbon allocation to shoots and roots in relation to nitrogen supply is mediated by cytokinins and sucrose. Opinions in Plant Soil 185: 2132.
  • Wilson BF. 2000. Apical control of branch growth and angle in woody plants. American Journal of Botany 87: 601607.
  • Yanez-Espinosa L, Terrazas T, Lopez-Mata L. 2001. Effects of flooding on wood and bark anatomy of four species in a mangrove forest community. Trees: Structure and Function 15: 9197.