Tree Physiology 26, 1601–1606
© 2006 Heron Publishing—Victoria, Canada
Fine root respiration in the mangrove Rhizophora mangle over
variation in forest stature and nutrient availability
CATHERINE E. LOVELOCK,1,4 ROGER W. RUESS 2 and ILKA C. FELLER3
1
Centre for Marine Studies, University of Queensland, St. Lucia, QLD 4072, Australia
2
Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK 99775-0180, USA
3
Smithsonian Environmental Research Center, P.O. Box 28, Edgewater, MD 21037, USA
4
Corresponding author ([email protected])
Received October 6, 2005; accepted March 1, 2006; published online September 1, 2006
Summary Root respiration uses a significant proportion of
photosynthetically fixed carbon (C) and is a globally important
source of C liberated from soils. Mangroves, which are an important and productive forest resource in many tropical and
subtropical countries, sustain a high ratio of root to shoot biomass which may indicate that root respiration is a particularly
important component in mangrove forest carbon budgets.
Mangroves are often exposed to nutrient pollution from coastal
waters. Here we assessed the magnitude of fine root respiration
in mangrove forests in Belize and investigated how root respiration is influenced by nutrient additions.
Respiration rates of excised fine roots of the mangrove,
Rhizophora mangle L., were low (4.01 ± 0.16 nmol CO2 g – 1
s –1) compared to those measured in temperate tree species at
similar temperatures. In an experiment where trees where fertilized with nitrogen (N) or phosphorus (P) in low productivity
dwarf forests (1–2 m height) and more productive, taller (4–
7 m height) seaward fringing forests, respiration of fine roots
did not vary consistently with fertilization treatments or with
forest stature. Fine roots of taller fringe trees had higher concentrations of both N and P compared to dwarf trees. Fertilization with P enhanced fine root P concentrations in both dwarf
and fringe trees, but reduced root N concentrations compared
to controls. Fertilization with N had no effect on root N or
P concentrations. Unlike photosynthetic C gain and growth,
which is strongly limited by P availability in dwarf forests at
this site, fine root respiration (expressed on a mass basis) was
variable, but showed no significant enhancements with nutrient additions. Variation in fine root production and standing
biomass are, therefore, likely to be more important factors determining C efflux from mangrove sediments than variations
in fine root respiration per unit mass.
Keywords: Belize, fertilization, nitrogen, phosphorus.
Introduction
Root respiration uses a significant proportion of photosynthetically fixed carbon (C) (Boone et al. 1998), and is a globally important source of C liberated from forest soils (Raich
and Schlesinger 1992, Ruess et al. 2003). Mangrove forests
cover large areas of the coastal zone in the subtropics and tropics, where they may comprise significant components of regional C budgets (Alongi 2002). They are characterized by
conspicuous aboveground roots and, in many regions, by peat
substrates that are composed almost entirely of fine roots
(McKee 2001, Middleton and McKee 2001). Mangrove sediments are rich in C and have high rates of C accumulation per
unit area (mean value of 210 g C m – 2 year – 1; Chmura et al.
2003), much of which is derived from fine roots (McKee 2001,
Middleton and McKee 2001). The high biomass allocation to
aboveground- and coarse belowground roots with abundant
aerenchyma ensures an adequate supply of oxygen for fine
root metabolism in anaerobic sediments (McKee 1996),
whereas high C allocation to fine roots is thought to facilitate
nutrient uptake in nutrient limited settings (McKee 1996,
2001). Although aboveground C stocks and rate of C fixation
in mangrove forests are relatively well documented (Twilley et
al. 1992, Twilley 1995, Clough 1998), and estimated to be
globally significant (Ewel et al. 1998), belowground C stocks
and rates of C turnover are poorly known (e.g., Ong et al.
1995).
Respiration rates of fine roots in temperate ecosystems are
known to vary over sites and tree species, and are strongly influenced by root temperature and tissue nitrogen (N) concentration (Pregitzer et al. 1998, Reich et al. 1998, Burton et al.
2002). Nitrogen concentrations of fine roots are correlated
with N uptake rates and assimilation (Pregitzer et al. 1998,
Reich et al. 1998). Mangroves forests are subject to nutrient
enrichment due to agricultural and urban pollution of estuaries
(Valiela et al. 2001), which is likely to affect nutrient uptake,
fine root nutrient content and, hence, fine root respiration. Effects of nutrient enrichment on fine root respiration may, in
turn, affect C cycling and ecosystem function (Rivera-Monroy
et al. 2004).
In aboveground tissues, enhanced growth rates (e.g., Onuf et
al. 1977, Feller 1995, Lovelock et al. 2004) and rates of
photosynthetic C gain have been observed in mangroves fertilized with both N and phosphorus (P) (Lovelock and Feller
2003, Lovelock et al. 2006), but less is known about responses
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LOVELOCK, RUESS AND FELLER
of belowground tissues to nutrient enrichment.
In the mangrove forested islands in Belize, where our experiment was conducted, there is a marked gradient in tree height
from taller (4–7 m) more productive fringing forests of Rhizophora mangle L. on the seaward side of the islands to less productive inland stands of dwarf trees, 1–2 m in height. The soils
in the fringing forest are flooded by the tide daily, whereas the
inland dwarf forest is perennially flooded except during unusually low tides. By means of a fertilization experiment, it
was established that aboveground growth of trees in the taller
fringing forests is N limited whereas growth of dwarf trees is
strongly P limited (Feller et al. 2002). In this study, we aimed
to test whether fine root respiration of R. mangle was sensitive
to nutrient additions. We, therefore, assessed fine root respiration across the natural tree-height gradient and in settings
where aboveground growth was limited by either N or P or
both.
Based on the existence of correlations among plants traits
(Chapin 1980), in particular between above- and belowground
traits (e.g., Comas et al. 2002, Tjoelker et al. 2005), and reports linking tissue nutrient concentration and respiration rate
over a range of species (Reich et al. 1998), we expected root
respiration of R. mangle to reflect aboveground growth, with
taller fringe trees having a higher fine root respiration rate than
dwarf trees. We also anticipated that tall N-limited trees of the
fringing forest would exhibit enhanced fine root respiration in
response to N fertilization, whereas P-limited dwarf trees
would exhibit enhanced fine root respiration rates in response
to P fertilization.
Materials and methods
Site description and experimental design
The study was conducted at Twin Cays (16°50′ N, 88°6′ W), a
92-ha archipelago of mangrove islands located approximately
1.6 km inside the Belizean Barrier Reef Complex (see Feller et
al. 2002, McKee et al. 2002 and references therein for a full
site description). The islands are composed of peat that rests
on the Pleistocene coral reef platform. They are situated approximately 12 km from the mainland and receive no terrigenous inputs of freshwater or sediments. Twin Cays is dominated by Rhizophora mangle (red mangrove) and Avicennia
germinans (L.) Stearn. (black mangrove) with scattered Laguncularia racemosa (L.) Gaertn. f. (white mangrove).
There is a distinctive tree-height gradient, from a narrow
(5–10 m wide) fringe zone of uniformly tall trees (4–7 m) that
occur within the low intertidal zone around the margins of the
islands to a zone of dwarf trees, 1–2 m in height, in the island
interior. Soil surface elevation varies along this height gradient, with the transition zone, or zone intermediate between
fringe and dwarf, having the highest elevation and the dwarf
zone having the lowest (McKee et al. 2002). Flooding follows
the variation in elevation: the fringe zone is flooded and
drained > 700 times per year, while the dwarf zone is perennially flooded, except during unusually low tides. Both fringe
and dwarf zones are dominated by R. mangle.
Experimental sites were established on the two largest islands of Twin Cays. There were two sites on the eastern island,
one near Boa Flats to the south and the other on the Lair Channel to the north, and there was one site on the western island,
near the boat dock (see Feller et al. 2002 and McKee et al.
2002 for a full site description). The dwarf trees at Boa Flats
and the boat dock, but not at the Lair Channel site, were adjacent to inland ponds. Trees at the Lair Channel site were
flooded less often than at the other sites.
At each site, three transects, 10 m apart, were established
perpendicular to the shoreline and traversing the tree-height
gradient from shoreline to island interior. Transects were subdivided into three zones based on tree height (fringe: 4–7 m;
dwarf: 1–2 m; and transition: 2–4 m) , and three experimental
trees were selected within each zone for a total of nine trees
across each transect and a total of 81 trees overall. Rhizophora
mangle trees selected were each fertilized first in January
1995, and then at 6-month intervals with 300 g of N fertilizer
as urea (N,P,K, 45,0,0) or P fertilizer as P2O5 (N,P,K, 0,45,0),
as described in Feller (1995). Only trees from the fringing and
dwarf zones were studied (54 trees, 18 each of N and P fertilized and 18 control trees). Over the 9 years between establishment of the experiment and measurement of fine root
respiration in February 2004, each tree received approximately 5.5 kg of fertilizer.
Root respiration
Fine roots were harvested from the top 5 cm of sediment at the
base of each experimental tree in February 2004. Roots were
harvested during the mornings (between 0900 and 1100 h local time). The harvested roots were washed in seawater and a
sample with roots of less than 2 mm diameter selected. The
fine root sample (between 0.05 and 0.4 g dry mass) was
loosely wrapped in a tissue paper moistened with sea water
and placed immediately in an aluminum cuvette (5.4 cm diameter × 15 cm in length) coupled to an LI-6400 photosynthesis
system (Li-Cor, Lincoln, NE) configured as an “open” system.
The cuvette was immersed in sea water to keep the chamber at
ambient temperature (28 °C). Humidified air (> 90% RH) was
drawn through both the sample and reference cuvette of the
LI-6400. Roots were allowed to equilibrate with ambient air
with a CO2 concentration of approximately 370 ppm for 5 min,
in which time a constant CO2 exchange rate was achieved.
Subsequently, CO2 exchange was logged every 30 s for
7.5 min. Respiration rate for each sample was calculated as the
mean of the 15 values.
Because the moistened tissue paper was found to de-gas
CO2 over the course of the root respiration measurement, tissue paper controls, without fine roots, were run and the control
values subtracted from root respiration values.
After the respiration measurement, the root samples were
oven-dried at 60 °C. Nitrogen concentrations of the dried tissue were determined by near infrared spectrometry (NIRS,
Model 5000, Foss NIRS Systems, Silver Springs, MD), the
instrument being calibrated against R. mangle tissue by analysis with a CHN Analyzer (Perkin-Elmer 2400, Perkin Elmer,
TREE PHYSIOLOGY VOLUME 26, 2006
FINE ROOT RESPIRATION IN MANGROVES
Norwalk, CT) at the Smithsonian Environmental Research
Center, Edgewater, MD. Tissue phosphorus concentrations
were determined by inductively coupled plasma spectrophotometry (ICP) by Analytical Services, Pennsylvania State University, State College, PA.
Data analysis
Effects on fine root respiration, and N and P concentrations
were evaluated by a 3 × 2 factorial (nutrient treatment × zone)
analysis of variance (ANOVA), blocked by site. Where significant main effects or interactions were identified, Fisher’s Least
Significant Difference post hoc hypothesis test was used to assess pairwise differences within and among the treatments. To
analyze for heteroscedasticity, probability plots of all variables
and residual plots were examined.
Results
Fine root respiration was low in all treatments. The overall
mean value of 4.01 ± 0.16 nmol CO2 g –1 s –1 (Figure 1) was not
significantly (P < 0.05) affected by site, zone or fertilization
(Table 1), although respiration tended to be higher in fertilized
than in control trees (particularly in the dwarf trees) and in
fringe trees than dwarf trees (Figure 1). There were highly significant site × zone, site × treatment and site × zone × treatment interactions on fine root respiration (Table 1), which
were largely caused by the low respiration of control dwarf
trees at the Boa Flats site (data not shown).
Fine root nutrient concentrations were significantly influenced by forest zone and by the P fertilization treatment (Table 1). Dwarf forests had lower fine-root N and P concentrations than fringe forest trees (Figure 2). Fertilization with P
enhanced P concentrations in fine roots in the dwarf and fringe
forest trees, and resulted in significant reductions in fine root
N concentrations. Within treatments, N and P were correlated
Figure 1. Fine root respiration of Rhizophora mangle trees of the seaward fringe (Fringe) and landward dwarf (Dwarf) stands either unfertilized (C) or fertilized with nitrogen (N) or phosphorus (P). Values
are means ± standard errors.
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(Figure 3). Regressions of N and P concentrations of fine roots
for the three treatments had similar slopes (unfertilized control
(C) = 0.049, N = 0.054, P = 0.057), but fine roots of P fertilized
plants had higher P concentrations at the same N concentration
(i.e., different intercepts). Despite large variation in fine root N
and P (from 1–6 mg g – 1 N and 0.15–0.5 mg g – 1 P) there was
no correlation between fine root respiration and fine root N or
P concentration (data not shown; r 2 = 0.04 and 0.05, respectively).
Discussion
In this study we observed fine root respiration rates in R. mangle of 0.5–6 nmol CO2 g – 1 s – 1, which are comparable to rates
reported for R. mangle in hydroponic culture (3–6 nmol CO2
g – 1 s – 1 at 25 °C; McKee 1996). These rates are low compared
with the reported range (3–55 nmol CO2 or O2 g – 1 s – 1) for
other angiosperm trees species (Reich et al. 1998, Burton et al.
2002, Comas et al. 2002, Tjoelker et al. 2005). Only in junipers
and pines in arid, high-elevation sites in New Mexico have
such low fine root respiration rates been reported (Burton et
al. 2002).
Fine root N concentrations on a mass basis were low in
R. mangle (range 1–6 g kg – 1) compared to fine roots of a range
Table 1. Summary of three-way ANOVAs performed on fine root respiration, and nitrogen and phosphorus concentrations of Rhizophora
mangle trees at Twin Cays, Belize, with three nutrient treatments
(control; nitrogen; and phosphorus) in two zones (fringe and dwarf)
blocked by site (two on the eastern island (Boa Flats and Lair Channel) and one on the western island).
Source
df
F ratio
P
Fine root respiration
Site
Zone
Treatment
Site × Zone
Site × Treatment
Zone × Treatment
Site × Zone × Treatment
2
1
2
2
4
2
4
0.99
0.30
1.48
5.22
6.12
0.42
6.39
0.3811
0.6394
0.3302
0.0105
0.0008
0.6856
0.0006
Fine root nitrogen
Site
Zone
Treatment
Site × Zone
Site × Treatment
Zone × Treatment
Site × Zone × Treatment
2
1
2
2
4
2
4
1.57
138
10.5
0.266
0.437
5.18
0.106
0.2221
0.0072
0.0256
0.7674
0.7810
0.0776
0.9796
Fine root phosphorus
Site
Zone
Treatment
Site × Zone
Site × Treatment
Zone × Treatment
Site × Zone × Treatment
2
1
2
2
4
2
4
4.04
54.7
12.9
0.670
2.09
1.57
0.880
0.0261
0.0178
0.0180
0.5176
0.1021
0.3144
0.4853
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LOVELOCK, RUESS AND FELLER
Figure 3. Relationship between fine root nitrogen (N) and phosphorus
(P) concentration in Rhizophora mangle trees fertilized with nitrogen
(䊊), phosphorus (䉲) or unfertilized (䊉). A linear regression was fit to
each treatment: control: y = 0.138 + 0.049x, r 2 = 0.435; nitrogen fertilized: y = 0.108 + 0.054x, R 2 = 0.346; and phosphorus fertilized: y =
0.263 + 0.057x, r 2 = 0.467.
Figure 2. Tissue concentrations of nitrogen (N) and phosphorus (P) in
fine roots of Rhizophora mangle trees of the seaward fringe (Fringe)
and landward dwarf (Dwarf) stands. Values are means ± standard errors. Abbreviation: C = unfertilized control.
of temperate forest tree species (Burton et al. 2002; range
8–20 g kg –1 ), and were within or beyond the low end of the
range (2–28 g kg –1 ) reported for coniferous forest tree species
(Gordon and Jackson 2000). Low fine root N and fine root respiration rates in R. mangle compared to other tree species may
be related to the dominance of ammonium as a source of N in
mangrove soils (Alongi 1996, McKee et al. 2002). Because
ammonium is energetically inexpensive to assimilate, its use
limits the the respiratory costs of N uptake and assimilation.
On a unit N basis, fine root respiration of R. mangle averaged 20 µmol mol –1 N s –1 at 28 °C, corresponding to a rate of
7 µmol mol –1 N s –1 at 15 °C, assuming a Q10 of 2.0. This is
considerably higher than rates (2.1–2.60 µmol mol – 1 N s – 1)
reported for Pinus pinaster L. and other species after standardization to 15 °C (Vose and Ryan 2002).
We found no significant correlation between root nutrient
concentration and fine root respiration despite a large range of
N concentrations, which contrasts with results of interspecific
comparisons (Burton et al. 2002, Tjoelker et al. 2005) and a
study of variation within Pinus radiata L. (Ryan et al. 1996).
Our result are consistent, however, with findings for Pinus
strobus L. (Vose and Ryan 2002).
One possible reason for the absence of a correlation be-
tween fine root respiration and tissue N content is that root N
is, in part, stored in metabolically inactive compounds when N
availability is high (Chapin 1991). This interpretation is consistent with the reduction in N concentration of roots of trees
fertilized with P (Figure 2). Growth at our experimental site is
strongly P limited, particularly in dwarf trees. Thus, fertilization with P reduces N concentrations of both fine roots (Figure 3) and leaves (Feller et al. 2002, Lovelock et al. 2004),
presumably because limiting P stimulated growth, allowing
deployment of excess N to growing tissues.
Fine root respiration rates have been found to correlate with
aboveground growth and other traits in tree seedlings over a
range of species (Reich et al. 1998, Comas et al. 2002). However, in our study, although growth rates varied more than
10-fold between fertilized and control trees, we found no significant correlation between rates of fine root respiration and
aboveground growth (data not shown). A similar absence of
correlation was reported by Comas and Eissenstat (2004) in a
study of mature individuals of 11 temperate tree species. Furthermore, within a single species (Pinus strobus), the strength
of correlations between growth and respiration in different tissues was found to depend on the tissues considered, shoot
growth, for example, being correlated with stem respiration,
but not with branch or coarse root respiration (Vose and Ryan
2002).
In our study, growth of trees in the fringing forest at the island margins was enhanced by N fertilization, but photosynthetic C gain expressed on a per unit leaf area basis was not;
whereas in dwarf trees in the island interior, growth and photosynthetic C gain were both strongly enhanced by additions of
P (Feller et al. 2003, Cheeseman and Lovelock 2004, Lovelock
et al. 2006). In another fertilization experiment in Bocas del
Toro, Panama, both N and P additions stimulated shoot growth
of R. mangle, but not photosynthetic rate (Lovelock et al.
TREE PHYSIOLOGY VOLUME 26, 2006
FINE ROOT RESPIRATION IN MANGROVES
2004).
Comparison of trait plasticity in R. mangle for aboveground
processes showed that leaf-level physiological processes are
less plastic than architectural and biomass allocation traits
(Lovelock et al. 2006). Similar trends may be evident below
ground, with the biomass allocation to fine roots being more
variable than the physiological processes of roots themselves.
Meta-analysis of variation in the strength of physiological responses to nutrient availability over a range of terrestrial species found the strength of responses to nutrient additions
depended on differences in allocation to plant organs and to
variation in availability of other resources and abiotic stresses
(Poorter and Nagal 2000).
Acknowledgments
This study was supported by the National Science Foundation under
Grant DEB-9981535. The work also received support from the Smithsonian’s Marine Science Network, and logistic support from the Caribbean Coral Reef Ecosystems Program (Contribution No. 749). We
thank the staff of Carrie Bow Cay Research Station and Pelican Beach
Resort, Belize.
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