Rapid litter production and accumulation in Bornean mangrove forests

Rapid litter production and accumulation in Bornean mangrove forests SUKRISTIJONO SUKARDJO, 1 DANIEL M. ALONGI, 2, AND CECEP KUSMANA 3 1 The Centre for Oceanography, Indonesian Institute of Sciences, Jl Pasir Putih 1 Ancol Timur, P.O. Box 4801/JKTF, Jakarta 11048 Indonesia 2 Australian Institute of Marine Science, PMB3, Townsville MC, Queensland 4810 Australia 3 Faculty 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 forests ¼ 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 forests ¼ 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: Ó 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: d.alongi@aims.gov.au 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 production 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 assimilated 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, operationally 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 as linear regression analysis of litter fall and the increment growth of stems suggest that mangrove NPP increases with decreasing latitude (Saenger and Snedaker 1996, Alongi 2009). It is therefore very possible that some of the world s largest and most productive mangrove forests lying close to the equator have been excluded from analyses of global trends and patterns, having important consequences for the accuracy of global inventories of mangrove carbon sources and sinks. Some of the most extensive mangrove-lined coasts near the equator lie on the island of Borneo, especially along the east coast in East Kalimantan, Indonesia. Mangroves occupy 643,500 ha of the East Kalimantan coastline, providing a protective margin between land and sea and an extensive pool of resources for coastal inhabitants (Sukardjo and Alongi 2012). The East Kalimantan mangroves are among the most extensive in all of Southeast Asia (Spalding et al. 2010) and, while dwindling, remain an important coastal ecosystem along the entire coast of Borneo (MacKinnon et al. 1996). There is little information on litter production throughout the Indonesian archipelago (Sukardjo 1989, 1996, 2005, 2010, Sukardjo and Yamada 1992, Kusmana et al. 1997), but a pilot study (Sukardjo 1995) revealed high rates of litter production in East Kalimantan and preliminary reports (Murdiyarso et al. 2009, Donato et al. 2011) detailed carbon inventories of immense mangrove forests in Central Kalimantan. The aim of this paper is to provide a description of rapid rates of litter production and accumulation in five virgin mangrove forests in Apar- Adang Nature Reserve (ANR), East Kalimantan, Indonesia. We compare and contrast our results with those from other equatorial forests. METHODS Study area and sites The ANR is the most extensive mangrove area (109, 302 ha) in East Kalimantan, situated about 300 km southwest of the city of Balikpapan (1856.5 0 S, 116810.9 0 E). The reserve is bounded inland by extensive freshwater peat swamps. The area is equatorial with annual mean rainfall of 2,230 2,325 mm/yr. Tides are small (mean range ¼ 1.8 m) and diurnal, with salinity ranging from 33 44 and surface water temperature ranging from 298 348C. Mangrove forest metrics within the reserve were initially sampled in 2006 (BAPLAN MOF 2006). Replicate plots in five mangrove forests included in the 2006 study were used to measure litter dynamics. These five sites were chosen because they represent the major types of mangrove forest in East Kalimantan (Sukardjo1988, 1994, 1995). The forests were located perpendicular 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 the flat topography of the region. Forests IV and V receive sporadic freshwater inputs from adjacent freshwater swamps (Sukardjo 1994). All stands consisted 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 equal parts silt, clay, and sand (Sukardjo 1994). Forest site I, located at the sea edge, had a dense (basal area (BA) ¼ 34.38 m 2 / ha; tree density: 2,091 stems/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) content ¼ 4.1% and 0.38% DW; BAPLAN MOF 2006). Forest site II had a dense (BA ¼ 32.21 m 2 /ha; tree density: 3,088 stems/ha), tall canopy (MDH ¼ 21.5 m) dominated by R. apiculata and S. alba, inhabiting soils nearly identical to site I. Forest site III had a less dense (BA ¼ 23.42 m 2 /ha; tree density: 1,430 stems/ha) but tall canopy (MDH ¼ 21.5 m) dominated by R. apiculata and Bruguiera parviflora, inhabiting siltclay (OC and N content ¼ 5.0% and 0.93% DW) soils. Forest site IV was located further inland, with a less dense (BA ¼ 17.85 m 2 /ha; tree density: 1,430 stems/ha) tall canopy (MDH ¼ 21.5 m) dominated by Ceriops decandra, Exocoecaria agallocha, and B. sexangula, inhabiting clay-loam (OC and N content ¼ 11.6% and 0.97% DW) soils. Forest site V had a dense (BA ¼ 27.01 m 2 /ha; tree density: 2,200 stems/ha) tall canopy (MDH ¼ 22.9 m) dominated by B. parviflora and B. sexangula, inhabiting soils nearly identical to site IV. Litter measurements Within each forest type, a plot 10-m 3 150-m in size was marked out then further divided into 15 v www.esajournals.org 2 July 2013 v Volume 4(7) v Article 79

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 I II III IV V All forests 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 1.1 Annual 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 1.8 Annual 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 0.6 Annual 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 2.2 Daily 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 0.4 Daily 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 1.1 Daily 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 1.2 Daily 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 Forest individual 100 m 2 subplots. Within each subplot, three litter catchers (1 m 3 1m3 0.25 m; 1 mm nylon mesh) were randomly sited and suspended diagonally between trees by nylon rope. The catchers were at least 5 m apart and 2 m above the ground (English et al. 1994, Sukardjo 2010). Litter in each catcher was collected weekly from 1 January to 31 December 2007. Litter accumulating on the forest floor was also measured weekly from replicate 1 m 3 1 m quadrants within each subplot, at least 5 m from the nearest litter catcher (English et al. 1994). All litter was sorted, oven-dried at 658C for at least 5 d, and then weighed. Total amounts for each subplot were converted to monthly figures with no correction made for leaching or other losses. Statistical analysis One-way ANOVA was performed to determine differences in litter fall and accumulation between forest sites on untransformed data, if assumptions for the test were met. Pearson s correlation test was performed to determine the relationships of litter production with soil N content and soil C:N ratio (Sokal and Rohlf 2011). RESULTS The mean annual litter fall for all five forests was 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 total annual litter fall rates were significantly different among the five forests (one-way ANOVA; p, 0.011) with greatest production in forests III, IV and V, and lowest litter fall rates in the other forests (Table 1). The litter consisted of roughly equal amounts of leaves (37% of total), reproductive 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 wet and dry seasons, with monthly patterns similar among sites (Fig. 1). Total litter fall was significantly (one-way ANOVA; p, 0.054) greater in November-December (rainy months) than in the other months. Mean annual litter accumulation was 57.8 Mg DW ha 1 yr 1 (Table 2) with significantly greater (one-way ANOVA; p, 0.048) rates at forests IV and V than at the other three forests. Leaves were a higher proportion of total litter at forests IV (39%) and V (43%) than at the other sites (33 35%), but seasonal and monthly fluctuations were 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 forests varies globally from 3-18 Mg DW ha 1 yr 1 (Saenger and Snedakar 1996, Alongi 2014) and throughout Southeast Asia from 5-18 Mg DW ha 1 yr 1 (Christensen 1978, Sasekumar and Loi 1983, Sukardjo 1989, 2010, Ong 1993, Ong et al. 1995). By comparison, rainforest litter production usually ranges from 6-14 Mg DW ha 1 yr 1 (Mahli et al. 2011, Mahli 2012). Our mean litter fall of 23.7 Mg DW ha 1 yr 1 agrees well with values from an earlier pilot study by Sukardjo (1995) in adjacent mangroves. Thus, it is clear that mangrove forests along the coast of southeast Borneo have among the world s highest rates of litter fall, considerably greater than published rates from other equatorial mangrove forests v www.esajournals.org 3 July 2013 v Volume 4(7) v Article 79

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. (Table 3). Indeed, the mangroves of Borneo attain the most luxuriant growth known, as two recent studies confirmed their immense biomass and carbon storage potential in Central Kalimantan (Murdiyarso et al. 2009, Donato et al. 2011). As the island of Borneo has approximately 1.4 million hectares of mangrove forest (Spalding et al. 2010), our results and those of Murdiyarso et al. (2009) and Donato et al. (2011) imply an immense carbon reservoir in Bornean coastal forests. Some simple calculations give an idea of the magnitude of carbon fixation and storage. Using the global average that 33% of mangrove net primary production is litter (Alongi 2009) and multiplying this value by the total mangrove area on Borneo and by our average rate of litter production (further assuming a carbon content of 44%; Alongi 2009), the total amount of mangrove carbon fixation on the island is 43 Tg C yr 1 which is equivalent to 20% of the world s mangrove carbon fixation (Alongi 2014). As for carbon storage, if we assume that 15% of litter (as C) is buried and that 42% of mangrove C buried in soil is derived from litter (Alongi 2014),then the total amount of mangrove carbon stored on Borneo is 5 Tg C yr 1 which equates to 21% of carbon sequestered by the world s mangroves (Alongi 2014). Both of these values are overestimates as most forests on Borneo are not pristine, but they do suggest both the magnitude and the importance of Borneo s mangrove forests as a source and sink for carbon. Caution must be applied, of course, when comparing litter production among different studies, as three critical problems are: (1) variation in methodology which affects the reliability of results, viz. litter catchers (size, shape, and mesh size); (2) proper replication and canopy placement of traps; and (3) duration and frequency of collection (English et al. 1994). In our study, litter production was seasonally variable, attributable mainly to the effects of high temperature and low rainfall in the dry season and high rainfall and high humidity during the monsoon season. Many Asian litter fall studies have been for,1 year, so either maximum litter fall in the rainy season or minimum production in the dry season were missed, giving unrepresentative results. Annual variation in biological (e.g., flowering and fruiting) and physical (e.g., rainfall) factors play v www.esajournals.org 4 July 2013 v Volume 4(7) v Article 79

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. Litter accumulation Forest 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 4.5 II 54.3 6 3.1 18.1 6 1.5 15.9 6 1.7 12.5 6 2.7 7.8 6 4.4 III 50.0 6 3.6 17.3 6 0.7 13.9 6 1.4 14.2 6 3.6 4.6 6 11.0 IV 65.6 6 7.5 25.9 6 2.4 14.4 6 1.5 19.1 6 5.3 6.2 6 7.2 V 70.4 6 8.1 30.3 6 3.2 16.7 6 1.7 17.9 6 2.6 5.5 6 0.7 Mean 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 principal roles in litter dynamics that must be incorporated into studies of litter production (Sukardjo 1996, 2010). The seasonal peaks of litter fall in the wet and dry season are very similar to those described elsewhere in Southeast Asia (Kusmana et al. 1997), and although close to the equator, Borneo s climate is determined by two main monsoons expressed as distinct northwest wet and southeast dry seasons (MacKinnon et al. 1996). The most obvious reason for high litter fall rates in southeastern Borneo is the humid equatorial climate. Also, these forests are pristine and mature with luxuriant canopies; by comparison, few virgin forests remain in East Kalimantan or throughout Southeast Asia (MacKinnon et al. 1996, Spalding et al. 2010). The mangroves of the ANR are diurnally flooded, implying that tides provide not only silt and clay, but replenish nutrients and provide sufficient aeration for optimal growth. Mangrove forest productivity varies in relation not only to disturbance regime (or a lack thereof ) and equitable climate, but also to soil fertility and optimal physical properties, such as tidal hydrodynamics (Sukardjo 1988, 1994, Alongi 2009). A simple correlation analysis of our litter data with soil N content from these forests (measured during an earlier pilot study, Sukardjo 1995) found a significant (P, 0.05) correlation of litter production with soil nitrogen (Pearson s r ¼þ0.933) and the soil C:N ratio (Pearson s r ¼þ0.897). Forests III, IV, and V also received freshwater runoff during the year, which likely enhanced their high productivity. At all five forests, litter accumulation rates were rapid (48.8 70.4 Mg DW ha 1 yr 1 ) compared with measurements made in other mangrove forests (Conacher et al. 1996, Schories et al. 2003, Roy 2011, Abib and Appadoo 2012), and no other mangrove studies have measured rates of accumulation several times greater than litter fall as crabs and other detritivorous fauna ordinarily consume large amounts of litter (Cannicci et al. 2008). The large standing stocks and accumulation rates of litter in the forest floor reflect not only high litter production but low detritivore numbers and also the fact that we have observed input of litter tidally advected from forests closer to the sea edge and piled as tidal lines within our plots. Also, a large portion of mangrove litter carried by a particular tide is likely to return on the subsequent tide as the ANR covers large expanses of freshwater, estuarine, and marine intertidal habitat area. Modelling of litter dynamics in the pilot study (Sukardjo 1995) indicated low rates (mean litter decay constant, 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 1995 2.5 Avicennia, Rhizophora, Lagunculata 6.5 10.6 Ecuador Twilley et al. 1997 3 Avicennia, Sonneratia, Rhizophora 14.0 15.8 Malaysia Sasekumar and Loi 1983 3 Mixed species 13.8 Colombia Mullen and Hernandez 1978 4 Bruguiera 11.0 12.7 Sumatra Kusmana et al. 1997 4.5 Ceriops, Rhizophora 3.8 9.2 Kenya Slim et al. 1996 5 Mixed species 7.6 12.0 Malaysia Ong 1993, Ong et al. 1995, Gong et al.1984 v www.esajournals.org 5 July 2013 v Volume 4(7) v Article 79

k ¼ 0.44) of litter turnover in these forests. The small tidal range (1.8 m) is also likely to facilitate high retention of litter thus constituting another positive feedback mechanism to maintain high litter accumulation. Using the global average of 33% of net primary productivity vested in mangrove litter production (Alongi 2014), we derive NPP estimates for these five forests of between 62 and 86 Mg DW ha 1 yr 1. This calculation, if correct, implies that these mangrove stands are five to eight times more productive than the global average for mangrove forests (Alongi 2009). These results underscore the fact that the luxuriant growth of tropical vegetation on the island of Borneo extends to coastal mangroves. ACKNOWLEDGMENTS S. Sukardjo thanks BAPLAN MOF for the invitation to join an integrated team to evaluate the Apar Adang Nature Reserve, especially the team leader, Mr. Kustanto. Many thanks go to Pasir District officers, especially Mr. Romif and Mr. Sanusi Onieh, and the local people for welcoming and helping us conduct research on their property within the reserve. LITERATURE CITED Abib, S., and C. Appadoo. 2012. A pilot study for the estimation of above ground biomass and litter production in Rhizophora mucronata dominated mangrove ecosystems in the island of Mauritius. Journal of Coastal Development 16:40 49. Alongi, D. M. 2009. The energetics of mangrove forests. Springer, Dordrecht, The Netherlands. Alongi, D. M. 2014. Carbon cycling and storage in mangrove forests. Annual Review in Marine Science 6 in press. BAPLAN MOF. 2006. Laporan Tim Teknis Kondisi Hutan Mangrove Cagar Alam Teluk Adang Teluk Apar, 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. Faunal impact on vegetation structure and ecosystem function in mangrove forests: a review. Aquatic Botany 89:186 200. Christensen, B. 1978. Biomass and primary production of Rhizophora apiculata Bl. in mangroves in northern Thailand. Aquatic Botany 4:43 52. Conacher, C. A., C. O Brian, J. L. Horrocks, and R. K. Kenyon. 1996. Litter production and accumulation in 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 in the tropics. Nature Geoscience 4:293 297. English, S., C. Wilkinson, and V. Baker. 1994. Survey manual for tropical marine resources. Australian Institute of Marine Science, Townsville, Queensland, Australia. Gong, W.-K., J.-E. Ong, C. H. Wong, and G. Dhanarajan. 1984. Productivity of mangrove trees and its significance in a managed mangrove ecosystem in Malaysia. Pages 216 225 in E. Soepadmo, A. N. Rao, and D. J. Macintosh, editors. Proceedings of the Asian symposium on mangrove environment, research and development. Perctakan Ardyas Sdn Bhd, Kuala Lumpur, Malaysia. Kathiresan, K., and B. L. Bingham. 2001. Biology of mangroves and mangrove ecosystems. Advances in Marine Biology 40:91 251. Kusmana, C., S. S. Takeda, and H. Watanabe. 1997. Litterfall production of a mangrove forest in East Sumatra, Indonesia. Indonesian Journal of Agriculture 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. The allocation of ecosystem net primary productivity in tropical forests. Philosophical Transactions of the Royal Society B 366:3225 3245. Mahli, Y. 2012. The productivity, metabolism and carbon cycle of tropical forest vegetation. Journal of Ecology 100:65 75. Mullen, K., and A. Hernandez. 1978. Productivdad primaria neta en un manglar del Pacifico Colombiano. Pages 663 685 in M. V. Velez and R. R. Beltran, editors. Memorias seminaro sobre el Oceano Pacifico Sudamerica. Universidad del Valle, Cali, Colombia. Murdiyarso, S., D. Donato, J. B. Kauffman, S. Kurnianto, M. Stidham, and M. Kanninen. 2009. Carbon storage in mangrove and peatland ecosystems: a preliminary account from plots in Indonesia. 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 stand of Rhizophora apiculata Bl. mangrove forest. Journal of Biogeography 22:417 424. Roy, S. 2011. Seasonally and spatially coordinated strategy of detritus conservation and use in the world s largest mangrove ecosystem. Proceedings v www.esajournals.org 6 July 2013 v Volume 4(7) v Article 79

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