The contrasting effects of nutrient enrichment on

The contrasting effects of nutrient enrichment on growth, biomass allocation and decomposition of plant tissue in coastal wetlands Matthew A. Hayes, Amber Jesse, Basam Tabet, Ruth Reef, Joost A. Keuskamp & Catherine E. Lovelock Plant and Soil An International Journal on Plant-Soil Relationships ISSN 0032-079X Plant Soil DOI 10.1007/s11104-017-3206-0

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Author's personal copy Plant Soil DOI 10.1007/s11104-017-3206-0

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The contrasting effects of nutrient enrichment on growth, biomass allocation and decomposition of plant tissue in coastal wetlands Matthew A. Hayes & Amber Jesse & Basam Tabet & Ruth Reef & Joost A. Keuskamp & Catherine E. Lovelock Received: 23 August 2016 / Accepted: 14 February 2017 # Springer International Publishing Switzerland 2017

Abstract Aims Eutrophication of coastal waters can have consequences for the growth, function and soil processes of coastal wetlands. Our aims were to assess how nutrient enrichment affects growth, biomass allocation and decomposition of plant tissues of a common and widespread mangrove, Avicennia marina, and how eutrophication drives changes in below-ground carbon sequestration. Methods We assessed this through the measurement of above- and belowground growth and decomposition rates of plants and plant tissue in unenriched or nutrient enriched treatments. Responsible Editor: Jeffrey Walck . M. A. Hayes (*) Smithsonian Environmental Research Center, Smithsonian Institution, Edgewater, MD 21037, USA e-mail: [email protected]

Results Nutrient enrichment increased biomass allocation above-ground compared to below-ground in seedlings but not in fully developed, mature trees where we observed the opposite pattern. Experiments to assess root decomposition found that 40–50% of biomass was lost within six months with little change between 12 and 18 months, indicating a high potential for accumulation of organic matter over time. We estimate rootderived carbon sequestration rates of 53, 250 and 94 g C m−2 year−1 for unenriched control, N and P enriched treatments, respectively. Conclusions These results show coastal eutrophication can be beneficial and detrimental to ecosystem function of coastal plants. Eutrophication stimulates root growth in fully developed trees, increasing organic matter input to soils. Our data suggests that organic matter accumulation will increase in areas with high nutrient availability where root growth is increased and rates of decomposition are low.

A. Jesse : B. Tabet : C. E. Lovelock School of Biological Sciences, The University of Queensland, QLD, St. Lucia 4072, Australia

Keywords Carbon . Eutrophication . Growth . Mangrove . Nutrients

R. Reef School of Earth, Atmosphere and Environment, Monash University, Clayton, VIC 3800, Australia

Introduction

J. A. Keuskamp Ecology and Biodiversity, Department of Biology, Utrecht University, Utrecht, The Netherlands J. A. Keuskamp Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands

Nutrient enrichment, particularly from nitrogen (N) and phosphorus (P), is considered one of the most serious threats to coastal ecosystem health (Paerl 1997; Cloern 1999; Downing et al. 1999). Nutrient-rich pollutants discharged into coastal waterways, such as those from agricultural run-off and sewage treatment, often lead to

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eutrophication of coastal waterways indicated by the presence of algal blooms, hypoxia, loss of species diversity and species mortality (Paerl 1997; Lovelock et al. 2009; Bala Krishna Prasad 2012). Additionally, eutrophication can modify the stoichiometric constraints on plants growing in a nutrient-enriched environment, changing growth rates, biomass allocation patterns and sediment organic matter accumulation (Gleeson and Tilman 1992; McKee 1995; James et al. 2005). Mangrove forests are important natural resources in the tropics and subtropics. They provide a range of ecosystem services, one of which is carbon sequestration in sediments that has led to suggestions that they have a role to play in mitigation of elevated CO2 in the atmosphere (McLeod et al. 2011). The potential for carbon sequestration in sediments of mangroves may be influenced by a wide range of factors. However, allocation of biomass to roots and decomposition of plant biomass are likely to be important components determining rates of carbon sequestration in mangrove forests (Alongi 2014). For example, Saintilan et al. (2013) found mangrove root material dominated soil organic carbon in mangrove forests in Australia. Both the allocation of biomass to roots and rates of decomposition of organic matter are sensitive to the availability of nutrients (McKee 1995; Feller et al. 1999; Huxham et al. 2010). Given the high level of exposure to nutrient enrichment in global coastal ecosystems (Paerl 1997; Smith 2003), there is the potential for nutrient enrichment to influence carbon sequestration in both biomass and sediments. In this study, we assessed the influence of nutrients on biomass allocation and rates of decomposition in mangrove forests with the aim of contributing to our understanding of how human activities in the coastal zone may influence carbon sequestration within these ecosystems. In order to maximize growth and other plant functions, plants have developed a range of strategies for acquisition, storage and allocation of resources (Chapin 1991). BBalanced growth^ describes the allocation of biomass in response to variation in resource availability. For example, under nutrient-limiting conditions, a greater proportion of biomass is allocated to the root systems of the plants, while under nutrient-replete conditions biomass allocation is increased to above-ground growth to increase photosynthetic carbon gain. Experiments with intertidal wetland plants of salt marsh and mangrove forests have indicated that while total biomass increases at higher nutrient availability, biomass

allocation to below-ground growth is increased when nutrient availability is limited (Clough 1992; Brewer et al. 1998; Sherman et al. 2003). In this paper, we assess the relative importance of increased biomass with nutrient additions and changes in biomass allocation in determining the level of organic matter contributed to mangrove sediments. Nutrient availability, in particular N, has also been shown to affect rates of organic matter decomposition in terrestrial forests (Janssens et al. 2010) and in mangroves (Romero et al. 2005; Huxham et al. 2010). Although N availability is important for enhancing microbial decomposition of plant detritus (Romero et al. 2005), nitrogen addition can also significantly reduce decomposition. Knorr et al. (2005) found decomposition of organic matter with high lignin concentrations was inhibited by high rates of N fertilization. Similarly, Hobbie et al. (2012) found over the long term, N addition slowed decomposition rates of slowly decomposing fractions of litter. An increase of N in areas where N is not limiting growth has also been shown to limit sediment organic matter decomposition, and in conjunction with increased plant productivity may lead to increased carbon accumulation within sediments (Janssens et al. 2010; Keuskamp et al. 2015). However, under conditions that are moderately enriched in N, availability of P may limit decomposition (Feller et al. 1999; Huxham et al. 2010; Keuskamp et al. 2015). Thus, we expect that in moderately N-rich settings additional N availability may decrease decomposition while enrichment with P may increase decomposition of root derived organic matter. The objectives of this investigation were to assess how nutrients (N + P) affect growth, biomass allocation and decomposition of tissues of Avicennia marina, the mangrove tree species commonly found in many of the mangrove forests in the Indo-Pacific region, particularly in subtropical and warm temperate regions (Duke et al. 1998). This investigation had two components; a controlled glasshouse experiment and a field fertilization experiment conducted within the coastal wetlands on the moderately eutrophic (Abal et al. 1998) western shores of Moreton Bay, Queensland, Australia. Previous studies in Moreton Bay have indicated mean sediment nutrient levels within mangrove forests on the western shores of Moreton Bay of 356 ± 51 μg cm−3 and 0.2 ± 0.03 g cm−3 for total P and N respectively (Lovelock et al. 2014). Unpublished values of nutrients delivered in sediments along the western shores of Moreton Bay indicate values of approximately 133 mg


kg−1 d−1 and 0.25%WT for total P and N respectively. For the controlled glasshouse experiment, we grew seedlings of A. marina under different nutrient concentrations, ranging from high nutrient availability that is representative of N-rich waterways to low nutrient availability that is typical to oligotrophic conditions. For the field experiment, we fertilized replicate mature A. marina trees within both the low intertidal fringing forests and high intertidal scrub forest zones. Nutrient availability varies over intertidal gradients, which may also influence root growth and decomposition (Feller et al. 1999; Middleton and McKee 2001), although salinity and oxygen availability also vary (Lugo and Snedaker 1974). In this experiment, we measured above- and below-ground growth and assessed rates of decomposition of root tissue. We tested the hypothesis that increasing nutrient availability (increased eutrophication) increases plant growth (total above and belowground production) but the ratio of root growth to shoot growth will decrease, such that nutrient enrichment does not increase the potential contribution of plant root organic matter to sediments. We also hypothesized that in this N-rich field site , increased soil N availability would reduce rates of decomposition of mangrove derived organic matter within mangrove sediments, but increased soil P availability would enhance decomposition.

Methods Glasshouse experiment Propagules of Avicennia marina, were collected from Wynnum Esplanade along the western shore of Moreton Bay, Australia (27° 25′10.29″ S, 153° 10′12.59″ E). The collected propagules were carefully examined for signs of insect infestation such as boring holes or larvae. Propagules determined to be pest-free were transported to a greenhouse located at the University of Queensland, St Lucia Campus, Brisbane, Australia, where they were established in pots (175 mm dia, 175 mm height, 2.7 L volume) filled with a soil mix of 50% Canadian peat moss (Sun Gro Horticulture Distribution Inc. Agawam, MA, USA) and 50% sand. Plants were irrigated three times per week with 400 ml of a saline nutrient stock solution containing 0.42 mM NH4NO3, 1.2 mM KNO3, 0.69 mM Ca(NO3)2, 0.1 mM NaH2PO4, 0.05 mM FeEDTA, and 500 mM NaCl (seawater salinity) providing nutrient loading rates of 309 g N m2 yr.−1 and 20 g P

m2 yr.−1. After two months, any propagules that failed to establish were discarded along with seedlings that had failed to develop a single leaf pair or displayed signs of impaired development. The remaining 114 plants were irrigated with saline nutrient solution for a further period of four months, by which time the cotyledons had detached from the seedlings. Fifteen plants were then randomly selected and dried at 60 °C to a constant mass to calculate mean initial biomass. The 99 remaining plants were then randomly assigned to three nutrient treatments; High nutrient solution (double strength), Mid-nutrient solution (stock) and Low nutrient solution (8% concentration of nutrient stock solution). All nutrient solutions contained 500 mM NaCl, and all plants were watered three times per week with 400 ml of each respective solution. The soil remained moist, but not saturated, between watering treatments. Once a fortnight, the plants received a shower of fresh water (20 ml) from a spray bottle to simulate a rain event washing salt from their leaves. At three monthly intervals throughout the experiment, all treatments were supplied with 400 ml trace element solution containing 0.321 mM CaSO4, 0.003 mM B4Na2O7.10.0H2O, 0.025 mM CuSO 4 , 0.54 mM FeSO 4 , 0.297 mM MgCO 3 , 0.002 mM Na 2 MoO 4 , 0.257 mM MnO 4 S and 0.048 mM ZnSO4. These treatments were maintained in the glasshouse at a mean temperature of 20.5 °C ± 5.39 SD and a mean humidity of 62.5% ± 18.93 SD, for a period of 7 months (13 months since propagation) and harvested before the seedlings developed into saplings and became root bound. In August, 2012 eight seedlings from each nutrient treatment (24 in total) were randomly selected and leaf area was measured for each seedling. All seedlings from each of the three treatments were then separated into parts (leaf, stem and root), dried to a constant mass at 60 °C and weighed. The mean initial biomass calculations (pre-treatment) were then subtracted from the final root and shoot masses. Dry biomass weights from each of the respective plant components from each of the three plant treatments were then used to compare biomass allocation between plants growing in the different nutrient conditions.

Growth analysis Biomass weight ratios were calculated by dividing the biomass of the specific plant component with the total


plant biomass. Root: shoot ratios (RSR) were calculated by dividing the root biomass by the biomass of the above-ground plant components. Leaf area was measured using an LI-3100C Area Meter (LI-COR, Lincoln, Nebraska, U.S.A.). Leaf area ratio (LAR) was determined by dividing the leaf area (cm2) by the total seedling biomass (g), whilst the specific leaf area (SLA) was calculated by dividing the plant leaf area (cm2) by the leaf biomass. Net assimilation rate (NAR; grams of dry weight per m 2 of leaf area per day (g m −2 day−1)) was determined by dividing the total dried plant weight (g) by the length of the experimental period (days) multiplied by the leaf area (m2). Relative growth rate (RGR; g g−1 day−1) over the experimental period was calculated as: RGR = (lnW2 − ln W1)/(T2 − T1) where W1 and W2 are the seedling dry mass at the beginning and end of the experimental period, T2 - T1 (McGraw and Garbutt 1990).

then plugged with the extracted sediment core. The same extraction and replacement of the core (but no fertilizer added) was carried out for the control trees.

Above-ground growth To assess above-ground growth of A. marina trees from each fertilized plot, stainless steel dendrometer bands were installed on each tree (Krauss et al. 2007). Cumulative changes in circumference of each tree were then measured every 6 months to the nearest 0.25 mm with a digital vernier calliper for a period of 22 months. Cumulative changes in circumference over the 22 months were then converted to basal area growth rate (cm2 month−1).

Root growth Field experiment A field experiment was established at the Tinchi Tamba Wetland Reserve (Brisbane City Council) wetland, on the western shore of Moreton Bay, Queensland where a long-term fertilization experiment has been established since 2005. 54 plants in total were included in the experiment, with 27 mature tall trees (>5 m) located along a low intertidal creek bank (designated as Fringing mangroves) and 27 mature, stunted trees ( 0.05; Fig. 2b).

Field experiment

Table 1 Biomass partitioning and leaf measurements (± SE) in A. marina seedlings grown on Low, Mid and High nutrient treatments. Leaf, stem, and root mass ratios (LWR, SWR & RWR

respectively) and leaf area ratio (LAR) indicate the proportion of total plant biomass partitioned to those components. Specific leaf area (SLA) indicate the ratio of individual leaf area to biomass

Basal area growth rate differed significantly between the forest zones (F 1,28 = 6.3, P < 0.05) with

Plant component Nutrient treatment

Total leaf area (cm2)

Total leaf number

Leaf area ratio (cm2 g−1)

Specific leaf area (cm2 g−1)

Leaf mass ratio

Shoot m ass ratio

Root mass ratio

High

790.4 ± 92.5

35.5 ± 3.4

22.3 ± 1.6

51 ± 3.6

0.44 ± 0.01

0.24 ± 0.01

0.32 ± 0.01

Mid

644 ± 73.6

30.1 ± 3.4

17.6 ± 0.7

40.7 ± 1.1

0.43 ± 0.01

0.25 ± 0.01

0.3 ± 0.01

Low

522.2 ± 54.1

26.9 ± 4.2

15.1 ± 0.9

50.7 ± 1.9

0.30 ± 0.01

0.22 ± 0.01

0.48 ± 0.01

ANOVA

F 2,21 = 3.2 P = 0.06

F 2,21 = 1.4 P = 0.27

F 2,21 = 10.9 P < 0.001

F 2,21 = 5.92 P < 0.001

F 2,21 = 47.0 P < 0.001

F 2,21 = 3.4 P = 0.05

F 2,21 = 48.5 P < 0.001


Fig. 2 The relationship between relative growth rate and net assimilation rate (a) and leaf area ratio (b). Symbols indicate High (triangle), Mid (diamond) and Low (square) nutrient treatments.

The trend line describes the relationship between RGR and NAR and is of the form Y = 70.77× + 3.23 (R2 = 0.79, P < 0.001)

Fringing trees growing in basal area at a faster rate (0.12 ± 0.03 cm 2 month − 1 ) than Scrub trees (0.03 ± 0.01 cm2 month−1; P < 0.05). Growth rates tended to be highest in trees fertilized with N and lowest for control trees although the difference among nutrient treatments was not significant over the whole research area (F 2,28 = 1.63, P = 0.21; Fig. 3a). There were significant differences in root growth rates (g m−2 month−1) among nutrient treatments with N treated trees having higher growth rates than P-treated or control

trees within each of the forest zones (F 2, 41 = 34.29, P < 0.05; Fig. 3b). There was no difference in root growth between P-treated and control trees in either Fringe or Scrub zones (P > 0.05). There was no significant difference in root growth rate (g m−2 month−1) between Fringe and Scrub locations (F 1, 41 = 0.82, P = 0.37) although growth rates tended to be higher for plants growing in the Fringe zone (56.9 ± 10.2 g m−2 month−1) than in the Scrub zone (49.6 ± 7.9 g m−2 month−1). Decomposition rate (k1) did not differ significantly across Scrub and Fringe locations without the addition of

Fig. 3 Biomass partitioning across low intertidal Fringe trees and high intertidal Scrub trees showing (a) basal area growth (cm2 month−1) and (b) root growth (g m2 month−1)


nutrients. In the N and P treatments of the Scrub zone, k could not be estimated reliably, as most of the labile material had been lost within the first 180 days, prior to our first sampling period. Although the rapid weight loss made it impossible to estimate significance, decomposition rate was higher in both nutrient treatments as compared to the control. In the Fringe vegetation, there was no effect of nutrient treatments on decomposition rate. Labile fraction (a) was estimated to be 20% lower in the Scrub as compared to the Fringe vegetation (z = −4.5, p < 0.05; Table 2), indicating that in the Scrub vegetation more litter material is sequestered over longer periods of time. Nutrient amendments did not significantly affect the limit value in either vegetation zone, although P amendment marginally increased the labile fraction (a) in the Fringe by an estimated 7% (z = 1.65, p < 0.1; Table 2). Fitted estimates of decomposition rates (kl) and labile fraction (a) (Table 2) were used to construct decomposition curves (Fig. 4a, b).

Discussion Monitoring growth of A. marina seedlings at different nutrient treatments in the glasshouse and mature individuals in the field found that this species varied allocation of biomass between above-ground and belowground compartments depending on nutrient availability. Consistent with theoretical predictions (Chapin et al. 1991), the biomass allocated to above- or below-ground growth in the glasshouse experiment was dependent on nutrient availability with increased biomass allocation to below-ground components at lower nutrient availability. The root: shoot ratio observed in the glasshouse study (between 0.5 and 2) were similar to those observed in

other pot experiments. In a study of A. marina biomass allocation Naidoo (1987) found low N availability increased biomass allocation to below-ground components and McKee (1995) found increasing nutrient availability decreased biomass allocation to the roots of Laguncularia racemosa and Avicennia germinans from a root: shoot ratio of approximately 1.5 and 0.5, respectively, to 0.5 for L. racemosa and 0.25 for A. germinans. The results of the field experiment did not follow the same pattern as identified in the controlled glasshouse experiment, where we could not identify a biomass allocation response to nutrients in fringe or scrub trees. According to the functional equilibrium model, plants respond to a decrease in below- ground resources with increased allocation to roots (Poorter and Nagel 2000). Although this was a clear response to nutrients identified in the controlled experiment, there may have been other factors resulting in high variation among individual stems or other factors limiting growth in the field experiment trees. These factors may include unfavorable soil conditions such as salinity and pH, or biological factors, including competition or shading (Ball 2002; Krauss et al. 2007; Bompy et al. 2014; Santini et al. 2015). Comparisons between field and controlled growth experiments are difficult, particularly when comparing plants from different life-cycle stages. Our combined field and controlled experimental findings suggest organic matter inputs to sediments are higher with increasing nutrient availability in large fully developed trees, whilst in seedlings there is a distinct biomass allocation to the above-ground components of the plant. While differences in biomass allocation were clearly developed in the seedlings, no significant differences in total plant biomass were observed among the nutrient

Table 2 Mean (±SE) decomposition rate (kl) and labile fraction (a) for organic matter in sediments at nitrogen, phosphorus and control nutrient treatments in low intertidal Fringe trees and high intertidal Scrub trees Decomposition rate (kl (g g−1 d−1))

labile fraction (a (g g−1))

Nitrogen

0.009 ± 0.001***

0.56 ± 0.02***

Phosphorous

0.010 ± 0.001***

0.60 ± 0.02 ***

Location

Treatment

Fringe

Scrub

Control

0.010 ± 0.002***

0.55 ± 0.02***

Nitrogen

n.d

0.40 ± 0.02***

Phosphorous

n.d

0.42 ± 0.01***

Control

0.015 ± 0.006*

0.43 ± 0.02***

n.d. indicates where decomposition was too fast to obtain a reliable estimation (>0.05) *indicate reliability of fits for each value


Fig. 4 Decomposition of low intertidal Fringe trees and high intertidal Scrub trees. Symbols indicate measured mass loss with standard errors. Thick lines represent best fit to a two-pool

Mt decomposition model M ¼ ae−k l t þ 1−a, with 95% confidence 0 interval delineated by thin lines

treatments in the glasshouse experiment. In contrast to the glasshouse, above-ground growth and root growth were both enhanced in the field experiment when trees were fertilized with N, with no significant indication of a change in biomass allocation patterns. Reconciling this result with the glasshouse experiment is difficult where we observed a clear difference in biomass allocation patterns among nutrient treatments. The lack of a change in total seedling biomass in the glasshouse experiment may indicate that a factor other than nutrient availability, such as irradiance (Ball 2002), limited the growth in high-nutrient seedlings, where large above-ground growth and leaf areas were recorded. Changes in RGR were highly correlated with NAR of glasshouse grown plants, although the relationship between LAR and RGR was variable. These results are consistent with those of Ball and Pidsley (1995) who found NAR accounted for most of the change in RGR in Sonneratia alba and Sonneratia lanceolata with increasing salinity. Likewise, Ball (1988) found decreases in RGR of A. marina and Aegiceras corniculatum with increasing salinity levels was directly related to a decrease in NAR. These findings suggest that variation in NAR may be the primary determinant of changes in growth rates of A. marina when these plants are growing across gradients in nutrient availability. The decomposition rates observed in this study (0.01 g g−1 d−1 and 0.017 g g−1 d−1 for Fringe and Scrub zones, respectively) were comparable to those reported in other studies using the two stage decomposition model such as Romero et al. (2005) who found decomposition rates in closely related Avicennia germinans of 0.011 (g g−1 d−1). The root decomposition rates (kl)

across the research site varied depending on the forest zone, with decomposition rates being lower for the Scrub compared to the Fringe zones. The labile fraction (a) was 20% lower in the Scrub zone than the Fringe zone, indicating a higher recalcitrant fraction which would take longer to decompose and lower the mass loss at the higher intertidal zone. These observations were similar to those observed by Huxham et al. (2010) who also found lower mass loss within higher intertidal zones where elevated salinity and reduced tidal inundation reduced decomposition rates. Conversely, others have observed slower decomposition at lower intertidal zones (Feller et al. 1999; McKee and Faulkner 2000; Poret et al. 2007; Keuskamp et al. 2015) where reduced decomposition rates were associated with saturated sediments and low redox potentials. The decomposition response to nutrient enrichment is also often mediated by litter characteristics where some material, such as root tissue used in this study, contain more recalcitrant components and take longer to decompose than more labile plant components such as leaf tissue (Middleton and McKee 2001; Knorr et al. 2005). In addition to gradients in salinity and redox potential, variation in rates of decomposition have also been attributed to higher levels of nutrient availability. While increasing N availability is often associated with enhanced decomposition (Huxham et al. 2010), under moderately eutrophied settings such as the western shore of Moreton Bay, we predicted that N fertilization should be associated with decreased rates of decomposition (after Janssens et al. 2010) and P fertilization would result in increased rates of decomposition (Feller et al. 1999; Keuskamp et al. 2015). In our study,


we did not observe a difference in organic matter loss across nutrient treatments. This may suggest the microbial community in these habitats may have been limited by nutrients other than N and P. Although clearly above and below ground tree growth was limited by N availability, the microbial community may also be limited by other nutrients (Hartman and Richardson 2013). The lower decomposition rates in N fertilized sites may also be due to limitation of the microbial community by P availability. Although an increase in sediment acidity with N additions was proposed to limit microbial decomposition (Janssens et al. 2010), limitations by other components required for microbial metabolism is also possible (Hartman and Richardson 2013). Additionally, Keuskamp et al. (2015) found that in some cases P suppresses phenol oxidase, and hence suppresses decomposition of recalcitrant organic matter suggesting the effect of P on organic matter decomposition may be site specific. The amount of organic matter accumulated over time in mangroves is largely dependent on autochthonous biomass production and decomposition rates and, to a lesser extent, on allochthonous organic matter input, i.e. from upstream or from the sea during tidal flow (Saintilan et al. 2013). Autochthonous matter in mangrove sediments is largely comprised of root material (McKee 2011; Saintilan et al. 2013) although leaf litter and woody biomass may form an important component in some forests (Twilley et al. 1997). Where tidal regimes are relatively high as it is in Moreton Bay, export of leaf litter is high (Adame and Lovelock 2011). Thus, leaf contribution to mangrove sediments are likely to be low. A forest that has high root biomass inputs and low rates of decomposition is likely to be a well-developed carbon sink, increasing organic matter accumulation over time. Conversely, an area experiencing lower root biomass inputs and has high decomposition rates is likely to accrete sediment organic matter slowly or experience a net loss of sediment organic matter over time. Across both forest zones in our study, 43% of the root material was lost in the first six months, with only a small increase in total organic matter loss thereafter. Similar results were observed by Middleton and McKee (2001) who also found more than half of the buried root material was lost after 300 days with very little of the original mass lost at longer incubations. The large initial organic matter loss is likely due to the initial loss or labile components, with more recalcitrant

components taking longer to decompose. These findings indicate a high potential for accumulation of organic matter over time in sediments of Moreton Bay. At Tinchi Tamba wetland, we observed root annual growth rates of 267, 1234 and 491 g m−2 year−1 across both forests types for control, N and P treated trees, whilst the annual organic matter mass loss were 49%, 48% and 51% across both forest types for control, N and P treatments, respectively. Based on our values of root production and decomposition, we estimate organic matter accumulation of 136, 641 and 240 g m−2 year−1, or 53, 250 and 94 g C m−2 year−1 (assuming organic matter is 39% C; Kauffman and Donato 2012) for control, N and P treatments, respectively. These C sequestration rates indicate an increase in C sequestration of 371% and 77% above unenriched control treatments for N and P nutrient treatments, respectively. The C sequestration rates observed in this study are comparable with those by Lovelock et al. (2014) who estimated C sequestration based on measurements of vertical accretion (~75 g Corg m−2 year−1) and those by Saintilan et al. (2013) who estimated C sequestration using accretion rates obtained from dating of sediment cores (256 and 207 g Corg m−2 year−1) for mangrove and salt marsh habitats, respectively). Carbon sequestration is an important service offered by mangroves that is dependent on plant productivity, biomass allocation to roots, decomposition and sediment accretion. In large, fully developed trees, our research has shown that nutrient enrichment increases below-ground growth in mangroves, which has the potential to increase organic matter accumulation in mangrove sediments. In seedlings, there is the potential for increasing nutrient pollution to affect biomass allocation of mangrove trees by reducing biomass allocation to root systems, which could, in turn, negatively affect sediment C storage. However, nutrients may also affect the chemical characteristics of plant tissues, which has the potential to influence changes in organic matter decomposition rates (Romero et al. 2005; Ferreira et al. 2015). Where biomass allocation to the root system is not reduced, as was observed at our field site, organic matter accumulation in sediments is high, in particular in areas where decomposition is slower than organic matter input. Our data suggests that organic matter accumulation will increase in areas with high nutrient availability where root growth is increased and rates of decomposition are low.

Author's personal copy Plant Soil Acknowledgements This work was partially supported by the CSIRO Marine and Coastal Carbon Biogeochemistry Cluster (Coastal Carbon Cluster) and The National Center for Groundwater Research and Training. Author contributions MH and CEL conceived and designed the experiments. MH, AJ, BT, and RR performed the experiments. MH, JK and CEL analysed the data. MH wrote the manuscript; with other authors providing editorial advice.

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