MARINE ECOLOGY PROGRESS SERIES 1 Published December 17 Mar Ecol Prog Ser

Relationship between conditions and Rhizophora apiculata seedling growth and nutrient status

Carlos M. ~uarte'l*,Ole Geertz-~ansen~,Udomluck ~hampanya~, Jorge ~errados',Miguel D. Fortes4, Lars amp-~ielsen~, Jens or urn^, Somsak ~oromthanarath~

'Centro de Estudios Avanzados de Blanes, CSIC, Cami de Santa Barbara, sln, E-17300 Blanes (Girona),Spain 'Freshwater Biological Laboratory,University of Copenhagen. Helsingersgade51, DK-3400 Hillered, Denmark %oastal Resources Institute. Prince of Songkla University. Hat Yai. Songkhla 90112. Thailand 4MarineScience Institute, University of The Philippines, Diliman,Ouezon City 1101. The Philippines

ABSTRACT: The growth rate and nutritional status of Rhizophora apiculata seedlings were analyzed across mangrove stands with different sediment composition in The Ph~lippinesand Southern Thai- land. Plant growth differed 10-fold and the production of new leaves, roots and branches varied between 50- and 100-fold across sites. Most (>60%)of the variance in mangrove growth rate across systems could be accounted for by differences in the nutrient concentrationof the leaves, which was in turn related to the interstitial nutrient concentration and the plus clay content of the . Nutrient-poor coarse sediments were characteristic of located in the mouths of rivers drain- ing small watersheds,while sediments at the mouths of large rivers had high silt, clay, and nutrient con- tents, thus allowing the development of nutrient-sufficient. fast-growing R. apiculata seedlings. The growth of R. apiculata seedlings increased significantly when the plants grew adjacent to rivers drain- ing areas >l0km2 The results provide evidence thatgrowth of R. apiculata seedlings at the edge of the progressing mangrove forests is often nutrient limited, and that the extent of nutrient limitation depends on the delivery of silt and nutrients from the rivers The coastal zones adlacent to small (

KEYWORDS: SE Asia . Mangrove growth . Nutrient status . Sediment nutrients . Watershed size

INTRODUCTION mangrove development, and mangrove forests cover large areas in the deltaic areas along the coasts of SE The developmentof large mangrove forests depends Asia (Mcnae 1968).Water hydrology is a major deter- on warm air temperatures, high (>0.75) values of minant of mangrove , and the highest pro- the mean annual rainfall/potential evapotranspiration ductivity values are usually reported in mangroves ratio (Blasco 19841, and the generation of vast inter- associated with rivers (Twilley et al. 1986).River flow tidal substrata by coastal geon~orphicprocesses (Thom and tides are powerful mechanisms for the transfer of 1984). The climate in Southeast (SE) Asia, which is matter between ecosystems and they cause a large characterized by high rainfall, and rivers with high silt fraction of mangrove production (on average 29.5%; loads (Milliman & Meade 1983, Milliman & Syvitski Duarte & Cebrian 1996) to be exported from the eco- 1992) combine to provide favourable conditions for system as leaf litter and propagules (e.g.Twilley et al. 1986, Hemminga et al. 1994,Panapitukkul et al. 1998). In addition, a substantial fraction of the mangrove pro- duction is buried in the sediments (10.4 % on average;

0 Inter-Research 1998 Resale of full article not permitted Mar Ecol Prog Ser 175: 277-283, 1998

increased ltkelihood of export losses and where nutnent availability In the sed~ment IS lower (Tam et a1 1995) These cons~der- atlons suggest that mangrove seedlings established at the edge of the mangrove forest may have reduced growth, whtch would represent an important bottleneck for the sustained expansion of the man- SauthChina Sea grove forest (e g Panap~tukkul et a1 1998) In order to test these hypotheses, we as- sessed the nutrient (C, N and P) status of mangrove seedlings growlng along the 95 100 105 110 115 l20 125 forest edge across a range of sites In SE LongitudeEast As~a The s~tesrecelve from nvers representing a grad~entof water- shed sizes, which vary from creeks in Bacuit Bay 5- pak-mg%ay small islands to large rivers (e.g. Pak (NorthPalawan) Phanang rlver, Nakhon Si Thamarath, Southern Thailand). In the present study we focused on the seedlings of Rhizophora apiculata, a common species throughout the region, and one that is particularly rel- evant because of its importance as the tar- get species in afforestation plans (Ak- sornkoae 1993). Growth of the seedlings was calculated from measurements of height and estimates of age derived from

0 counts of internodes as described by Duke - & Pinzon (1992) for Rhizophora mangle and modified by Duarte et al. (unpubl.) for Flg. 1. Study sltes and locat~ons(e) of the R. aplculata. The nutnent status of the sampling statrons plants was described from the C, N and P content In their leaves (Chapin 19801, while the nutrient availability at the study Duarte & Cebrian 1996), so that the production avail- sites was represented by the nutnent concentrations able for recycling wlthtn the ecosystem is reduced within the sediments. (50% on average, Duarte & Cebrian 1996) Accord- inylv, a larqr fract~onof the rn~lngroveproduct~on is lost frvm the ecosystem (Boto & Bunt 1981, Tcvilley et METHODS a1 1986), leading to an associated high loss of nutn- ents Mangrove ecosystems tend to be, therefore, auto- Study sites. The study was conducted under the trophic cornmun~ties(Duarte & Cebl~an1996, Gateuso fran~m~zrorkof a large, interdisclpl~naryproject aimed et a1 1998) whose primarl product~onshould, tht re- at elur~dat~nqeffects of siltat~onon SE Asian coastal fore, depend on contlnuous nutrient supply from land ecosystems (CERDS project, funded by the European or sea Commiss~on)The study extended across sltes In The The contlnuous export of nutrients from mangrove Phil~pplnes(Bacu~t Bay, Palawan) and Thailand (Trang ecosystems led us to hypothesize that the growth of coast, adjacent to KO Talibong island, and Pak mangrove trees may often be nutnent limited, as al- Phanang ), encompassing a broad range of con- ready shown by some nutrient addit~onexpenments d~tions(Flg 1) Bacuit Bay is a large, open bay w~th (Boto & Wellington 1983 Feller 1995),and that the ex- numerous islands of different slzes, which receives tent of nutrient limitation should depend on the input of freshwater discharges from a couple of medium-slzed nutrients from land Moreoi rr, we suggest that nutrient nvers that support s~gn~ficantmangrove forests at their limltat~onmay be most pronounced at the edge of the mouths Although the Bay is st~lllargelv surrounded by mangrove forest, where the higher exposure leads to an forldsts the watershc ds of the larger rivers are now Duarte et al.: h4angrove seedlin ~ggrowth and nutrient status 279

experiencing and increased erosion uum directly into 20 m1 vials and preserved with 100 yl resulting from road construction and slash and burn of concentrated sulfuric acid until later analysis. After practices, which have led to increased silt loading neutralization with sodium hydroxide, the samples (Hodgson 1989). In contrast, the islands present in the were analyzed for dissolved reactive phosphate, am- bay are still almost fully covered by vegetation, and monium and nitrate on an Alpkem RAF autoanalyzer pockets of mangroves grow near the mouth of the following standard methods (Parsons et al. 1984). The small streams and creeks draining the islands. silt plus clay content of sediments was analyzed by The coastal areas in Pak Phanang and Trang in Thai- weighing the fraction of a subsample of sediment ma- land both receive the discharge of large rivers (15 to terial dried at 105°C for 24 h which passed through a 120 and 2.5 to 51.5 m3 S-', respectively), and mangrove 63 pm screen in a sieve-shaker. forests develop in the proximity of these river mouths Seedling growth determinations. Seedling age was (Fig. 1). The watersheds of both rivers have suffered estimated from counts of the number of internodes and major changes in land use over the past century, knowledge of the number of internodes produced an- including a recent proliferation of shrimp , which nually. Duke & Pinzon (2992) reported that seedling have led to a major increase in the silt loads of these age of the mangrove Rhizophora mangle can be deter- rivers (CORIN 1991). The Pak Phanang river dis- mined from the presence of distinct seasonal changes in charges into a semi-enclosed Bay, where a thick man- the length of the internodes, which was also recently grove forest (92 km2; CORIN 1991) progresses at rates confirmed for SE Asian mangrove species, including of about 40 to 50 m yr-' along the mud flat formed by R,apiculata (Duarte et al. unpubl.). In essence, the se- river deposits (cf. Panapitukkul et al. 1998). Additional quence of the internodal length is first filtered to re- details on the sites can be found in Panapitukkul et al. move short (l2 watersheds of the different rivers was obtained from annual cycles per sampling site, and seedling age was national geographic databases and reports. Whenever determined as the ratio between the number of inter- these estimates were unavailable, the watershed of the nodes produced over the life span of the seedling and rivers was delineated on a topographic map and digi- the average number produced annually. tized to estimate the size of the riverine watershed The rate of seedling growth was subsequently calcu- associated with the mangrove stands sampled. lated from linear regression between the height of the At each sampling site, the height of 30 to 40 Rhi- seedlings, the number of roots, branches and standing zophora apiculata seedlings, spanning the broadest leaves, and their estimated age. The slope of the possible range in size (

Table 1.Mean (*SE) and range of the variables measured or derived in this study

Mean + SE

Leaf C (% DW) 41.16 + 0.59 Leaf N (%, DW) 1.05 + 0.05 Leaf P (% DW) 0.075 + 0.004 Growth (cm d-') 0.059 + 0.010 Internode production (internodes yr-l) 7.3 r 0.2 Net leaf production (].eavesseedling-' d-') 0.062 r 0.026 Branch production (branches d-l) 0 004 r 0.001 Root production (roots d.') 0.004 i 0.001 Allometric coefficient of growth in height 0.38 * 0.04 ALlometric coefficient of leaf production 0.99 * 0.13 Watershed size (km2) 21.85(median)

RESULTS

The number of internodes produced per year did not vary much among mangrove stands and averaged 7.3 k 0.2 (mean k SE) internodes yr-' (Table 1). Inter- node production was independent of sediment condi- tions and nutrient status of the plants (Pearson linear correlation coefficient, p > 0.05), suggesting that the number of internodes produced per seedling per year is a rather conservative feature of Rhizophora apicu- lata. In contrast, the growth rates varied 10-fold among sites (Table l), with the fastest growth (0.15 cm d-l) recorded for seedlings from the mud flat of the Pak Phanang River and the slowest growth (0.015 cm d-l) for seedlings growing on the shores of the smaller islands in Bacuit Bay. The relationship between seedling height and age was nonlinear and best described by an allometric relationship. The slope of the allometric relationship averaged 0.38 + 0.04, indi- cating seedling height to increase as the third power of age (Table 1). The seedlings produced, on average, 1 new stilt root and a new branch every 250 d but with considerable differences among stands (Table 1). The canopy of the seedlings increased with age, with the plants gaining a new leaf every 2 wk, on average. The canopy of seedlings growing on the shores of small islands only gained a new leaf every 200 d, because of high leaf loss rate, while that of seedlings growing on the rich mud flat of the Pak Phanang gained a new leaf every other day (Table l), as a result of extensive branching and longer leaf life spans. The nitrogen content of Rhizophora apiculata leaves varied from 0.78 to 1.66% of dry weight (DW)(Table 1).

Leaf N (5%DW) Leaf P (5%DW) The phosphorus concentration in ].eaves ranged from 0.057 to 0.1 17 % of DW and was significantly correlated Fig. 2. Rhizophora apiculata. Relationship between the growth to foliar nitrogen content (r = 0.93, p < 0.001). In gen- rate of mangrove seedlings and the nitrogen and phosphorus concentrations of their leaves (as % DW).Solid lines represent eral, R. aplculata seedlings had rather balanced N:P ra- the fitted regression equations, and r is the corresponding tios (31.2 * 0.6 atomic ratio). The ratio of total inorganic linear correlation coefficient. "p < 0.01, "'p < 0.001 nitrogen (TIN) to phosphate in the sediment porewaters Duarte et al.: Mangrove seedling growth and nutrient status 281

Total ~norganicnitrogen Dissolved reactive phosphorus % (DW) Silt plus clay Watershed sue (km2) in porewater ( PM) inporewater ( PM) in the sediment

Fig. 3. Rhizophora apiculata. Relationship between the Fig. 4. Rhizophora apiculata Relationship between the growth rate of mangrove seedlings and the total inorganic growth rate of mangrove seedlings and the silt plus clay con- nitrogen and dissolved reactive phosphorus concentrations in tent of the sediments, and the area drained by adjacent rivers the sediment porewaters. Solid lines represent the fitted or streams. Solid lines represent the fitted regression equa- regression equations, and r is the corresponding linear corre- tions, and r is the linear correlation coefficient. "p < 0.01, lation coefficient. 'p c 0.05, "p < 0.01, "'p < 0.001 "'p < 0.001

was relatively low (molar N:P ratio = 7.2 + 1.3), sug- and r = 0.88 for N and P, respectively, p < 0.005). As a re- gesting a deficit in nitrogen availability relative to that sult, there were strong, significant positive correlations of phosphorus in the sediment porewaters. between seedling growth and nutrient concentrations in The hypothesis that Rhizophora apiculatagrowth may the sediment porewaters (r > 0.74 and r t 0.86 for total in- be nutnent hmted in the area was supported by the find- organic nitrogen and phosphorus, respectively, p < 0.005; ing of strong positive correlations between seedling Fig. 3). elongation rate, leaf, root and branch formation and leaf Leaf nitrogen and phosphorus concentrations were N concentrations (r t 0.72, p > 0.005; Fig. 2). Seedling positively (p 0.01) correlated with the percent of silt growth was also positively correlated with leaf P con- plus clay in the sediment (r = 0.89 and r = 0.82, respec- centrations (r > 0.64, p > 0.005; Fig. 2). Nutrient concen- tively), and seedling growth was also positively corre- trations in the leaves were, in turn, associated with the lated with the percent of silt plus clay in the sediment porewater inorganic nutrient concentrations (r = 0.72 (Fig. 4, r > 0.85, p < 0.01). The sediments with low Mar Ecol Prog Ser 175: 277-283. 1998

nutrient concentrations and low contents of silt and mangroves (0.7 to 2.5% of DW; Onuf et al. 1977, Boto & clay occurred in association with rivers draining small Wellington 1983, Twilley et al. 1986, Rao et al. 1994, (

al. 1998). Our results show that increased siltation will herbivory of dwarf red mangrove (Rhizophora mangle). enhance seedling growth, which likely helps the seed- Ecol Monogr 65477-505 lings to outbalance the high mortality rates en- Gattuso JP. Frankignoulle M, Wollast R (1998) Carbon and carbonate metabolism in coastal aquatic ecosystems. countered by newly established unprotected seedlings Annu Rev Ecol Syst 29:405-433 (Clarke & Myerscough 1993). In order to promote man- Hemminga MA. Slim FJ, Kazungu J, Ganssen GM, Nieuwen- grove progression and compensate for earlier losses of huize J, Kruyt NM (1994) Carbon outwelling from a man- forest area, various programmes have been initiated to grove forest with adjacent beds and coral reefs (Gazi Bay, Kenya). Mar Ecol Prog Ser 106:291-301 protect expanding mangrove fringes and afforestation Hodgson G (1989) The effects of sedlmentatlon on Indo- programmes have also been conducted. The nonlinear Pacific reef . 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Ed~torialresponsibility: Otto Kjnne (Ed~tor), Submitted: May 13, 1998; Accepted: August 12, 1998 Oldendorf/Luhe, Germany Proofs received from author(s): November 19, 1998