rapid litter production and accumulation in bornean mangrove forests

Rapid litter production and accumulationin Bornean mangrove forests

SUKRISTIJONO SUKARDJO,1 DANIEL M. ALONGI,2,� AND CECEP KUSMANA3

1The Centre for Oceanography, Indonesian Institute of Sciences, Jl Pasir Putih 1 Ancol Timur,P.O. Box 4801/JKTF, Jakarta 11048 Indonesia

2Australian Institute of Marine Science, PMB3, Townsville MC, Queensland 4810 Australia3Faculty of Forestry, Bogor Agricultural University, Kampus Darmaga, Bogor, Indonesia

Citation: Sukardjo, S., D. M. Alongi, and C. Kusmana. 2013. Rapid litter production and accumulation in Bornean

mangrove forests. Ecosphere 4(7):79. http://dx.doi.org/10.1890/ES13-00145.1

Abstract. Litter fall and accumulation were measured weekly for one year (January–December 2007) at

five mangrove forests within the Apar-Adang Nature Reserve, East Kalimantan, Indonesia. Three forests

were located near the sea edge, each co-dominated by combinations of Sonnertia alba, Rhizophora apiculata,

and Bruguiera parviflora; two forests were co-dominated by Ceriops decandra, Exocoecaria agallocha, and

Bruguiera sexangula (site IV), and by B. parviflora and B. sexangula (site V) and located further inland but

subjected to intermittant freshwater inputs. Mean rates of annual litter production at forests I to V were

20.3, 19.7, 27.2, 24.2 and 27.6 Mg DW ha�1 yr�1 (mean of all forests¼ 23.7 Mg DW ha�1 yr�1) and rates of

litter accumulation were 44.4, 50.2, 45.9, 61.3 and 66.2 Mg DW ha�1 yr�1 (mean of all forests¼ 57.8 Mg DW

ha�1 yr�1), respectively, exhibiting peaks in the wet and dry seasons. Litter accumulation was greater than

litter fall due to tidal advection of litter from forests closer to the sea edge coupled with slow decay rates.

These rates of aboveground litter production and accumulation are the highest recorded for mangroves

and higher than rates measured in tropical humid evergreen forests, suggesting that large expanses of

equatorial mangrove forest, such as those on Borneo, may constitute an immense sink for coastal carbon.

Key words: Borneo, litter; litter accumulation; litter production; mangroves.

Received 18 April 2013; revised 5 June 2013; accepted 6 June 2013; published 3 July 2013. Corresponding Editor: Y. Pan.

Copyright: � 2013 Sukardjo et al. This is an open-access article distributed under the terms of the Creative Commons

Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the

original author and source are credited. http://creativecommons.org/licenses/by/3.0/

� E-mail: [email protected]

INTRODUCTION

Litter is one of the three components of net

forest primary production, especially so in

tropical forests where litter is rapidly produced

and recycled. On average, 34% of net primary

productivity (NPP) is allocated to litter produc-

tion in tropical humid evergreen forests (Mahli et

al. 2011). In mangrove forests, litter is equally

important both energetically and trophically,

accounting globally for 32% of forest NPP

(Alongi 2014). Mangrove litter is rapidly assim-

ilated into food webs and either eventually

buried in soil or exported by tides to adjacent

coastal waters (Alongi 2009). The magnitude and

fate of litter depends on multiple drivers such as

temperature, precipitation, canopy structure and

production, the degree and frequency of tidal

inundation, and the abundance of herbivorous

fauna (Kathiresan and Bingham 2001, Saenger

2002). Litter is thus a source of energy for forest

food webs, a recycled source of nutrients for new

plant growth, and a subsidy to support fisheries

(Alongi 2009).

A large database for mangrove litter fall exists

(Saenger and Snedaker 1996) but there are very

few measurements from equatorial forests, oper-

ationally defined here as forests located within 58

v www.esajournals.org 1 July 2013 v Volume 4(7) v Article 79

of the equator. Such lack of data is unfortunate aslinear regression analysis of litter fall and theincrement growth of stems suggest that man-grove NPP increases with decreasing latitude(Saenger and Snedaker 1996, Alongi 2009). It istherefore very possible that some of the world’slargest and most productive mangrove forestslying close to the equator have been excludedfrom analyses of global trends and patterns,having important consequences for the accuracyof global inventories of mangrove carbon sourcesand sinks.

Some of the most extensive mangrove-linedcoasts near the equator lie on the island ofBorneo, especially along the east coast in EastKalimantan, Indonesia. Mangroves occupy643,500 ha of the East Kalimantan coastline,providing a protective margin between land andsea and an extensive pool of resources for coastalinhabitants (Sukardjo and Alongi 2012). The EastKalimantan mangroves are among the mostextensive in all of Southeast Asia (Spalding etal. 2010) and, while dwindling, remain animportant coastal ecosystem along the entirecoast of Borneo (MacKinnon et al. 1996). Thereis little information on litter production through-out the Indonesian archipelago (Sukardjo 1989,1996, 2005, 2010, Sukardjo and Yamada 1992,Kusmana et al. 1997), but a pilot study (Sukardjo1995) revealed high rates of litter production inEast Kalimantan and preliminary reports (Mur-diyarso et al. 2009, Donato et al. 2011) detailedcarbon inventories of immense mangrove forestsin Central Kalimantan.

The aim of this paper is to provide a descriptionof rapid rates of litter production and accumula-tion in five virgin mangrove forests in Apar-Adang Nature Reserve (ANR), East Kalimantan,Indonesia. We compare and contrast our resultswith those from other equatorial forests.

METHODS

Study area and sitesThe ANR is the most extensive mangrove area

(109, 302 ha) in East Kalimantan, situated about300 km southwest of the city of Balikpapan(1856.50 S, 116810.90 E). The reserve is boundedinland by extensive freshwater peat swamps. Thearea is equatorial with annual mean rainfall of2,230–2,325 mm/yr. Tides are small (mean range

¼ 1.8 m) and diurnal, with salinity ranging from33–44 and surface water temperature rangingfrom 298–348C.

Mangrove forest metrics within the reservewere initially sampled in 2006 (BAPLAN MOF2006). Replicate plots in five mangrove forestsincluded in the 2006 study were used to measurelitter dynamics. These five sites were chosenbecause they represent the major types ofmangrove forest in East Kalimantan (Sukard-jo1988, 1994, 1995). The forests were locatedperpendicular to the coast ’50–100 m apart,from the seaward edge (site I) to furthest inland(site V), and were all inundated daily due to theflat topography of the region. Forests IV and Vreceive sporadic freshwater inputs from adjacentfreshwater swamps (Sukardjo 1994). All standsconsisted of tall, closed canopies (87.9–97.8%)inhabiting acidic (pH range: 3.9–5.3), saline(range: 30.2–33.8) soils consisting of nearly equalparts silt, clay, and sand (Sukardjo 1994). Forestsite I, located at the sea edge, had a dense (basalarea (BA) ¼ 34.38 m2/ ha; tree density: 2,091stems/ha), tall canopy (mean dominant height(MDH)¼ 19.35 m) dominated by Sonneratia alba,Rhizophora apiculata, and Bruguiera parviflora,inhabiting silt-clay soils (organic carbon (OC)and nitrogen (N) content¼ 4.1% and 0.38% DW;BAPLAN MOF 2006). Forest site II had a dense(BA ¼ 32.21 m2/ha; tree density: 3,088 stems/ha),tall canopy (MDH ¼ 21.5 m) dominated by R.apiculata and S. alba, inhabiting soils nearlyidentical to site I. Forest site III had a less dense(BA ¼ 23.42 m2/ha; tree density: 1,430 stems/ha)but tall canopy (MDH¼ 21.5 m) dominated by R.apiculata and Bruguiera parviflora, inhabiting silt-clay (OC and N content ¼ 5.0% and 0.93% DW)soils. Forest site IV was located further inland,with a less dense (BA¼ 17.85 m2/ha; tree density:1,430 stems/ha) tall canopy (MDH ¼ 21.5 m)dominated by Ceriops decandra, Exocoecaria agal-locha, and B. sexangula, inhabiting clay-loam (OCand N content ¼ 11.6% and 0.97% DW) soils.Forest site V had a dense (BA¼ 27.01 m2/ha; treedensity: 2,200 stems/ha) tall canopy (MDH¼ 22.9m) dominated by B. parviflora and B. sexangula,inhabiting soils nearly identical to site IV.

Litter measurementsWithin each forest type, a plot 10-m3 150-m in

size was marked out then further divided into 15


SUKARDJO ET AL.

individual 100 m2 subplots. Within each subplot,three litter catchers (1 m 3 1 m 3 0.25 m; 1 mmnylon mesh) were randomly sited and suspendeddiagonally between trees by nylon rope. Thecatchers were at least 5 m apart and 2 m abovethe ground (English et al. 1994, Sukardjo 2010).Litter in each catcher was collected weekly from 1January to 31 December 2007. Litter accumulat-ing on the forest floor was also measured weeklyfrom replicate 1 m 3 1 m quadrants within eachsubplot, at least 5 m from the nearest littercatcher (English et al. 1994). All litter was sorted,oven-dried at 658C for at least 5 d, and thenweighed. Total amounts for each subplot wereconverted to monthly figures with no correctionmade for leaching or other losses.

Statistical analysisOne-way ANOVA was performed to deter-

mine differences in litter fall and accumulationbetween forest sites on untransformed data, ifassumptions for the test were met. Pearson’scorrelation test was performed to determine therelationships of litter production with soil Ncontent and soil C:N ratio (Sokal and Rohlf 2011).

RESULTS

The mean annual litter fall for all five forestswas 23.7 Mg DW ha�1 yr�1 (Table 1). Total daily(mean ¼ 6.8 g DW m�2 d�1; Table 1) and totalannual litter fall rates were significantly differentamong the five forests (one-way ANOVA; p ,

0.011) with greatest production in forests III, IVand V, and lowest litter fall rates in the otherforests (Table 1). The litter consisted of roughlyequal amounts of leaves (37% of total), repro-ductive parts (34%), and twigs (29%). These

proportions were consistent among the sites,varying slightly, but not significantly (ANOVA; p. 0.046).

Litter production exhibited peaks in the wetand dry seasons, with monthly patterns similaramong sites (Fig. 1). Total litter fall was signif-icantly (one-way ANOVA; p , 0.054) greater inNovember-December (rainy months) than in theother months.

Mean annual litter accumulation was 57.8 MgDW ha�1 yr�1 (Table 2) with significantly greater(one-way ANOVA; p , 0.048) rates at forests IVand V than at the other three forests. Leaves werea higher proportion of total litter at forests IV(39%) and V (43%) than at the other sites (33–35%), but seasonal and monthly fluctuationswere similar among forests (data not shown).Total litter mass was significantly (p , 0.05)greater in the dry season that in the wet season.

DISCUSSION

Litter production in tropical mangrove forestsvaries globally from 3-18 Mg DW ha�1 yr�1

(Saenger and Snedakar 1996, Alongi 2014) andthroughout Southeast Asia from 5-18 Mg DWha�1 yr�1 (Christensen 1978, Sasekumar and Loi1983, Sukardjo 1989, 2010, Ong 1993, Ong et al.1995). By comparison, rainforest litter productionusually ranges from 6-14 Mg DW ha�1 yr�1

(Mahli et al. 2011, Mahli 2012). Our mean litterfall of 23.7 Mg DW ha�1 yr�1 agrees well withvalues from an earlier pilot study by Sukardjo(1995) in adjacent mangroves. Thus, it is clearthat mangrove forests along the coast of south-east Borneo have among the world’s highest ratesof litter fall, considerably greater than publishedrates from other equatorial mangrove forests

Table 1. Annual (Mg DW ha�1 yr�1) and daily (g DW m�2 d�1) rates (mean 6 1 SD) of litter fall at the five

mangrove forests, East Kalimantan, Indonesia.

Attribute

Forest

All forestsI II III IV V

Annual leaf 7.5 6 0.8 7.3 6 1.2 10.0 6 2.1 8.9 6 0.4 10.2 6 2.0 8.8 6 1.1Annual flower, fruit þ bud 7.0 6 0.8 6.8 6 1.2 9.4 6 6.5 8.3 6 2.5 8.5 6 1.1 8.0 6 1.8Annual twig 5.2 6 0.7 5.7 6 1.1 7.8 6 4.2 7.0 6 2.2 8.9 6 4.5 6.9 6 0.6Annual total 19.7 6 0.8 19.8 6 1.2 27.2 6 4.8 24.2 6 2.5 27.6 6 3.5 23.7 6 2.2Daily leaf 2.1 6 0.9 2.1 6 0.3 2.9 6 0.3 2.6 6 0.4 2.9 6 0.3 2.5 6 0.4Daily flowers, fruits þ buds 2.0 6 0.6 2.0 6 0.4 2.7 6 0.8 2.4 6 0.6 2.5 6 0.7 2.3 6 1.1Daily twig 1.7 6 0.4 1.6 6 1.0 2.3 6 1.4 2.0 6 0.3 2.6 6 0.9 2.0 6 1.2Daily total 5.8 6 0.7 5.7 6 0.7 7.9 6 0.6 7.0 6 0.4 8.0 6 1.2 6.8 6 0.8


SUKARDJO ET AL.

(Table 3). Indeed, the mangroves of Borneo attainthe most luxuriant growth known, as two recentstudies confirmed their immense biomass andcarbon storage potential in Central Kalimantan(Murdiyarso et al. 2009, Donato et al. 2011).

As the island of Borneo has approximately 1.4million hectares of mangrove forest (Spalding etal. 2010), our results and those of Murdiyarso etal. (2009) and Donato et al. (2011) imply animmense carbon reservoir in Bornean coastalforests. Some simple calculations give an idea ofthe magnitude of carbon fixation and storage.Using the global average that 33% of mangrovenet primary production is litter (Alongi 2009) andmultiplying this value by the total mangrove areaon Borneo and by our average rate of litterproduction (further assuming a carbon content of44%; Alongi 2009), the total amount of mangrovecarbon fixation on the island is 43 Tg C yr�1

which is equivalent to 20% of the world’smangrove carbon fixation (Alongi 2014). As forcarbon storage, if we assume that 15% of litter (asC) is buried and that 42% of mangrove C buriedin soil is derived from litter (Alongi 2014),thenthe total amount of mangrove carbon stored onBorneo is 5 Tg C yr�1 which equates to 21% ofcarbon sequestered by the world’s mangroves(Alongi 2014). Both of these values are overesti-mates as most forests on Borneo are not pristine,but they do suggest both the magnitude and theimportance of Borneo’s mangrove forests as asource and sink for carbon.

Caution must be applied, of course, whencomparing litter production among differentstudies, as three critical problems are: (1)variation in methodology which affects thereliability of results, viz. litter catchers (size,shape, and mesh size); (2) proper replication andcanopy placement of traps; and (3) duration andfrequency of collection (English et al. 1994). Inour study, litter production was seasonallyvariable, attributable mainly to the effects ofhigh temperature and low rainfall in the dryseason and high rainfall and high humidityduring the monsoon season. Many Asian litterfall studies have been for ,1 year, so eithermaximum litter fall in the rainy season orminimum production in the dry season weremissed, giving unrepresentative results. Annualvariation in biological (e.g., flowering and fruit-ing) and physical (e.g., rainfall) factors play

Fig. 1. Patterns of mean monthly litter fall rates (Mg

DW ha�1) measured at the five forests (sites I–V from

top to bottom panel) over the study period, January–

December 2007.


SUKARDJO ET AL.

principal roles in litter dynamics that must beincorporated into studies of litter production(Sukardjo 1996, 2010). The seasonal peaks of litterfall in the wet and dry season are very similar tothose described elsewhere in Southeast Asia(Kusmana et al. 1997), and although close tothe equator, Borneo’s climate is determined bytwo main monsoons expressed as distinct north-west wet and southeast dry seasons (MacKinnonet al. 1996).

The most obvious reason for high litter fallrates in southeastern Borneo is the humidequatorial climate. Also, these forests are pristineand mature with luxuriant canopies; by compar-ison, few virgin forests remain in East Kaliman-tan or throughout Southeast Asia (MacKinnon etal. 1996, Spalding et al. 2010). The mangroves ofthe ANR are diurnally flooded, implying thattides provide not only silt and clay, but replenishnutrients and provide sufficient aeration foroptimal growth. Mangrove forest productivityvaries in relation not only to disturbance regime(or a lack thereof ) and equitable climate, but alsoto soil fertility and optimal physical properties,such as tidal hydrodynamics (Sukardjo 1988,1994, Alongi 2009). A simple correlation analysisof our litter data with soil N content from theseforests (measured during an earlier pilot study,

Sukardjo 1995) found a significant (P , 0.05)correlation of litter production with soil nitrogen(Pearson’s r ¼ þ0.933) and the soil C:N ratio(Pearson’s r ¼þ0.897). Forests III, IV, and V alsoreceived freshwater runoff during the year,which likely enhanced their high productivity.

At all five forests, litter accumulation rateswere rapid (48.8–70.4 Mg DW ha�1 yr�1) com-pared with measurements made in other man-grove forests (Conacher et al. 1996, Schories et al.2003, Roy 2011, Abib and Appadoo 2012), and noother mangrove studies have measured rates ofaccumulation several times greater than litter fallas crabs and other detritivorous fauna ordinarilyconsume large amounts of litter (Cannicci et al.2008). The large standing stocks and accumula-tion rates of litter in the forest floor reflect notonly high litter production but low detritivorenumbers and also the fact that we have observedinput of litter tidally advected from forests closerto the sea edge and piled as tidal lines within ourplots. Also, a large portion of mangrove littercarried by a particular tide is likely to return onthe subsequent tide as the ANR covers largeexpanses of freshwater, estuarine, and marineintertidal habitat area. Modelling of litter dy-namics in the pilot study (Sukardjo 1995)indicated low rates (mean litter decay constant,

Table 2. Annual (Mg DW ha�1 yr�1) rates (mean 6 1 SD) of litter accumulation at the five Apar-Adang mangrove

forests, East Kalimantan, Indonesia.

Forest

Litter accumulation

Total Leaves Twigs Flowers þ Fruits þ Buds Other

I 48.8 6 4.5 16.1 6 2.1 13.9 6 1.6 12.4 6 2.9 6.4 6 4.5II 54.3 6 3.1 18.1 6 1.5 15.9 6 1.7 12.5 6 2.7 7.8 6 4.4III 50.0 6 3.6 17.3 6 0.7 13.9 6 1.4 14.2 6 3.6 4.6 6 11.0IV 65.6 6 7.5 25.9 6 2.4 14.4 6 1.5 19.1 6 5.3 6.2 6 7.2V 70.4 6 8.1 30.3 6 3.2 16.7 6 1.7 17.9 6 2.6 5.5 6 0.7Mean 57.8 6 5.4 21.5 6 2.3 15.0 6 1.2 15.2 6 4.2 6.1 6 5.2

Table 3. Mean litter fall rates (Mg DW ha�1 yr�1) in equatorial mangrove forests worldwide.

Latitude (8) Dominant species Litter fall Location Reference

2 Ceriops, Bruguiera, Rhizophora, Sonneratia 19.7–27.6 Apar Bay,East Kalimantan

This study

2 Avicennia, Ceriops, Rhizophora 21.0–26.1 Indonesia Sukardjo 19952.5 Avicennia, Rhizophora, Lagunculata 6.5–10.6 Ecuador Twilley et al. 19973 Avicennia, Sonneratia, Rhizophora 14.0–15.8 Malaysia Sasekumar and Loi 19833 Mixed species 13.8 Colombia Mullen and Hernandez 19784 Bruguiera 11.0–12.7 Sumatra Kusmana et al. 19974.5 Ceriops, Rhizophora 3.8–9.2 Kenya Slim et al. 19965 Mixed species 7.6–12.0 Malaysia Ong 1993, Ong et al. 1995, Gong et al.1984


SUKARDJO ET AL.

k ¼ 0.44) of litter turnover in these forests. Thesmall tidal range (1.8 m) is also likely to facilitatehigh retention of litter thus constituting anotherpositive feedback mechanism to maintain highlitter accumulation.

Using the global average of 33% of net primaryproductivity vested in mangrove litter produc-tion (Alongi 2014), we derive NPP estimates forthese five forests of between 62 and 86 Mg DWha�1 yr�1. This calculation, if correct, implies thatthese mangrove stands are five to eight timesmore productive than the global average formangrove forests (Alongi 2009). These resultsunderscore the fact that the luxuriant growth oftropical vegetation on the island of Borneoextends to coastal mangroves.

ACKNOWLEDGMENTS

S. Sukardjo thanks BAPLAN MOF for the invitationto join an integrated team to evaluate the Apar AdangNature Reserve, especially the team leader, Mr.Kustanto. Many thanks go to Pasir District officers,especially Mr. Romif and Mr. Sanusi Onieh, and thelocal people for welcoming and helping us conductresearch on their property within the reserve.

LITERATURE CITED

Abib, S., and C. Appadoo. 2012. A pilot study for theestimation of above ground biomass and litterproduction in Rhizophora mucronata dominatedmangrove ecosystems in the island of Mauritius.Journal of Coastal Development 16:40–49.

Alongi, D. M. 2009. The energetics of mangroveforests. Springer, Dordrecht, The Netherlands.

Alongi, D. M. 2014. Carbon cycling and storage inmangrove forests. Annual Review in MarineScience 6 in press.

BAPLAN MOF. 2006. Laporan Tim Teknis KondisiHutan Mangrove Cagar Alam Teluk Adang TelukApar, Kabupaten Pasir, Kalimantan Timur. BA-PLAN MOF Intern Report 1, Ministry of Fisheries,Jakarta, Indonesia. [In Indonesian.]

Cannicci, S., D. Burrows, S. Fratini, T. J. Smith III, J.Offenberg, and F. Dahbouh-Guebas. 2008. Faunalimpact on vegetation structure and ecosystemfunction in mangrove forests: a review. AquaticBotany 89:186–200.

Christensen, B. 1978. Biomass and primary productionof Rhizophora apiculata Bl. in mangroves in northernThailand. Aquatic Botany 4:43–52.

Conacher, C. A., C. O’Brian, J. L. Horrocks, and R. K.Kenyon. 1996. Litter production and accumulationin stressed mangrove communities in the Embley

River Estuary, North-eastern Gulf of Carpentaria,Australia. Marine and Freshwater Research 47:737–743.

Donato, D. C., J. B. Kauffman, D. Murdiyarso, S.Kurnianto, M. Stidham, and M. Kanninen. 2011.Mangroves among the most carbon-rich forests inthe tropics. Nature Geoscience 4:293–297.

English, S., C. Wilkinson, and V. Baker. 1994. Surveymanual for tropical marine resources. AustralianInstitute of Marine Science, Townsville, Queens-land, Australia.

Gong, W.-K., J.-E. Ong, C. H. Wong, and G. Dhanar-ajan. 1984. Productivity of mangrove trees and itssignificance in a managed mangrove ecosystem inMalaysia. Pages 216–225 in E. Soepadmo, A. N.Rao, and D. J. Macintosh, editors. Proceedings ofthe Asian symposium on mangrove environment,research and development. Perctakan Ardyas SdnBhd, Kuala Lumpur, Malaysia.

Kathiresan, K., and B. L. Bingham. 2001. Biology ofmangroves and mangrove ecosystems. Advancesin Marine Biology 40:91–251.

Kusmana, C., S. S. Takeda, and H. Watanabe. 1997.Litterfall production of a mangrove forest in EastSumatra, Indonesia. Indonesian Journal of Agricul-ture 9:52–59.

MacKinnon, K., G. Hatta, H. Halim, and A. Mangalik.1996. The ecology of Kalimantan. Periplus Editions,Singapore.

Mahli, Y., C. Doughtry, and D. Galbraith. 2011. Theallocation of ecosystem net primary productivity intropical forests. Philosophical Transactions of theRoyal Society B 366:3225–3245.

Mahli, Y. 2012. The productivity, metabolism andcarbon cycle of tropical forest vegetation. Journalof Ecology 100:65–75.

Mullen, K., and A. Hernandez. 1978. Productivdadprimaria neta en un manglar del Pacifico Colom-biano. Pages 663–685 in M. V. Velez and R. R.Beltran, editors. Memorias seminaro sobre elOceano Pacifico Sudamerica. Universidad delValle, Cali, Colombia.

Murdiyarso, S., D. Donato, J. B. Kauffman, S. Kur-nianto, M. Stidham, and M. Kanninen. 2009.Carbon storage in mangrove and peatland ecosys-tems: a preliminary account from plots in Indone-sia. CIFOR Working paper No. 48. http://www.cifor.org.nc/omline-library/browse/view

Ong, J.-E. 1993. Mangroves- a carbon source and sink.Chemosphere 27:1097–1107.

Ong, J.-E., W.-K. Gong, and B. F. Clough. 1995.Structure and productivity of a 20-year-old standof Rhizophora apiculata Bl. mangrove forest. Journalof Biogeography 22:417–424.

Roy, S. 2011. Seasonally and spatially coordinatedstrategy of detritus conservation and use in theworld’s largest mangrove ecosystem. Proceedings


SUKARDJO ET AL.

of the Zoological Society 64:63–71.Saenger, P. 2002. Mangrove ecology, silviculture and

conservation. Kluwer Academic, Dordrecht, TheNetherlands.

Saenger, P., and S. C. Snedaker. 1996. Pantropicaltrends in mangrove above-ground biomass andannual litterfall. Oecologia 96:293–299.

Sasekumar, A., and J. J. Loi. 1983. Litter production inthree mangrove forest zones in the Malay Penin-sula. Aquatic Botany 17:283–290.

Schories, D., A. Barletta-Bergan, M. Barletta, U.Krumme, U. Mehlig, and V. Rademaker. 2003.The keystone role of leaf-removing crabs inmangrove forests of North Brazil. Wetlands Ecol-ogy & Management 11:243–255.

Slim, F. J., P. M. Gwada, M. Kodjo, and M. A.Hemminga. 1996. Biomass and litterfall of Ceriopstagal and Rhizophora mucronata in the mangroveforests of Gazi Bay, Kenya. Marine and FreshwaterResearch 47:999–1007.

Sokal, R. R., and F. J. Rohlf. 2011. Biometry. Fourthedition. W.H. Freeman, New York, New York,USA.

Spalding, M., M. Kainuma, and L. Collins. 2010. Worldatlas of mangroves. Earthscan Publications, Lon-don, UK.

Sukardjo, S. 1988. The biological resources of themangrove forest in the Apar deltaic system, TanahGrogot, East Kalimantan, Indonesia. Pages 18–24 inD. Parish and C. Prentice, editors. Wetland andwaterfowl conservation in Asia. Asian WetlandBureau/IWRB, Kuala Lumpur, Malaysia.

Sukardjo, S. 1989. Litterfall production and turnover in

the mangrove forests in Muara Angke, Kapuk,Jakarta. Biotrop Special Publication 37:129–144.

Sukardjo, S. 1994. Soils in the mangrove forests of theApar Nature Reserve, Tanah Grogot, East Kali-mantan Indonesia. Southeast Asian Studies 32:385–398.

Sukardjo, S. 1995. Structure, litterfall, and net primaryproduction in the mangrove forests in East Kali-mantan. Pages 585–611 in E. O. Box, R. K. Peet, T.Masuzawa, I. Yamada, K. Fujiwara, and P. F.Maycock, editors. Vegetation science in forestry.Kluwer Academic, Dordrecht, The Netherlands.

Sukardjo, S. 1996. The relationship of litterfall to basalarea and climatic variables in a Rhizophora mucro-nata L. plantation at Tritih, Central Java, Indonesia.Southeast Asian Studies 34:424–432.

Sukardjo, S. 2010. Litterfall production of the man-grove forests in Tiris, Indramayu, West Java,Indonesia. Marine Research in Indonesia 35:21–33.

Sukardjo, S. and D. M. Alongi. 2012. Mangroves of theSouth China Sea: ecology and human impacts onIndonesia’s forests. Nova Science, New York, NewYork, USA.

Sukardjo, S., and I. Yamada. 1992. Biomass andproductivity of a Rhizophora mucronata L. plantationin Tritih Cilacap, Central Java, Indonesia. ForestEcology and Management 49:195–209.

Twilley, R. R., M. Pozo, V. H. Garcia, V. H. Rivera-Monroy, R. Zambrano, and A. Bodero. 1997. Litterdynamics in riverine mangrove forests in theGuayas River estuary, Ecuador. Oecologia111:109–122.


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rapid litter production and accumulation in bornean mangrove forests

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