Organic Geochemistry 34 (2003) 1259–1275 www.elsevier.com/locate/orggeochem A taphonomic study of 13C and 15N values in Rhizophora mangle leaves for a multi-proxy approach to mangrove palaeoecology Matthew Woollera,*, Barbara Smallwoodb,1, Ursula Scharlerc, Myrna Jacobsonb, Marilyn Fogela aGeophysical Laboratory, Carnegie Institution of Washington, 5251 Broad Branch Road, NW Washington, DC 20015-1305, USA bUniversity of Southern California, 3616 Trousdale Parkway, Los Angeles, CA, 90089-0371, USA cSmithsonian Environmental Research Center, PO Box 28647 Contees Wharf Road, Edgewater, ML 21037, USA Received 21 October 2002; accepted 9 May 2003 (returned to author for revision 17 December 2002) Abstract The response of mangrove ecosystems to environmental change can be examined with stable isotopic tracers of C and N. The 13C and 15N of a taphonomic series of Rhizophora mangle L. (Red mangrove) leaves were analyzed from Twin Cays, Belize, to facilitate reconstruction of past mangrove ecosystems. On Twin Cays, fresh leaves of dwarf R. mangle trees (0.5 m high) were found to have more negative d15N values (mean=À10%) and more positive 13C values (mean=À25.3%) compared to tall R. mangle trees (mean d15N=0%, d13C=À28.3%). These isotopic differ- ences can be related to nitrogen and phosphorus availability [Ecology 83 (2002) 1065]. We investigated three tapho- nomic stages in the fossilization of R. mangle leaves into peat with the following: (1) senescent leaves; (2) fallen leaves on the surface of the peat; and (3) sub-fossil leaves found within mangrove peat. In addition, by examining natural leaf assemblages we established that 13C and 15NofR. mangle leaves were not altered during senescence, despite a sig- nificant (50%) decrease in the N%. Modern dwarf and tall trees could still be identified from 13C and 15N analyses of the leaf assemblages found directly below a tree. Dwarf and tall trees could also be identified from 13C analyses of leaves that had decomposed for four months. Although dwarf and tall trees could not be statistically separated after four months according to d15N analyses, leaves with very negative 15N(À7%) were only collected below dwarf trees. Leaf fragments were present in 50 cm long cores of peat from four sites on the island, and their isotopic compositions were determined. The ranges of 13C(À29 to À22%) and 15N(À11 to +2%) values from sub-fossil leaves were similar to the ranges from modern leaves (d13C=À29 to À23%, d15N=À11 to +1%). The sub-fossil leaf isotopic compositions were independent values, in comparison to the uniform values of the surrounding peat. Because of the stability and persistence of the stable isotopic signals, they could contribute significantly to a multi-proxy approach to mangrove palaeoenvironmental reconstruction. # 2003 Elsevier Ltd. All rights reserved. 1. Introduction *Corresponding author at current address: Current address: Alaska Stable Isotope Facility, Water and Environmental Research Center, University of Alaska Fairbanks, 441 Duck- Situated at the junction between terrestrial and marine ering Building, PO Box 755860, Fairbanks, AK 997, USA. ecosystems, mangrove habitats are particularly sensitive E-mail address: ff[email protected] (M. Wooller). to alterations of sea-level (e.g. Blasco et al., 1996). The 1 Current address: The Department of Oceanography, impact of future sea-level scenarios, related to O&M Building, Texas A & M University, TAMU 3146, Col- anthropogenic global warming, on mangrove ecosys- lege Station, TX 77843-3146, USA. tems continues to be debated (Woodroffe, 1988, 1990; 0146-6380/03/$ - see front matter # 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0146-6380(03)00116-5 1260 M. Wooller et al. / Organic Geochemistry 34 (2003) 1259–1275 Ellison and Stoddart, 1991; Parkinson et al., 1994; ammonia by microbial deamination of proteins (Wada, Swarzbach, 1999). Simulated sea-level changes pro- 1980; Fogel et al., 1989; Benner et al., 1991). 15N values foundly influence the anatomy and physiology of man- in plant remains can also be affected by nitrogen groves (Ellison and Farnsworth, 1997). One way to immobilization, which results from microbial incor- understand future outcomes has been to examine how poration of nitrogen from the pore water or by the reac- past mangrove ecosystems have reacted to environ- tion of nitrogen with humic substances (Rice,1982;Benner mental change (e.g. Suguio et al., 1988; Woodroffe, et al., 1991; Hoch et al., 1992; Fogel and Tuross, 1999). 1990; Martin and Suguio, 1992; Parkinson et al., 1994; Fogel and Tuross (1999) suggested that the significant Angulo and Suguio, 1995; Blasco et al., 1996; Angulo et alteration of 15N in organic material during decomposi- al., 1999). Despite concerns over the turbation of pollen tion preclude the use of 15N values when reconstructing assemblages by tidal fluctuations, past mangrove palaeoenvironments. Nitrogen immobilization can reflect dynamics can be reconstructed using palynological the sources of nitrogen that were immobilized during techniques (e.g. Spackman et al., 1966; Grindrod, 1985; decomposition (Benner et al., 1991). However, in anoxic or Behling et al., 2001; Behling and Costa, 2001). tannin rich depositional environments, such as mangrove In many palaeoecological investigations, stable iso- peat, decomposition rates are diminished (Gonzalez-Far- tope data have successfully supplemented pollen data to ias and Mee, 1988) and nitrogen can remain preserved resolve the reconstruction of past ecosystems (e.g. Cer- (Bohlolli et al., 1977). The 15N of sub-fossil material can ling et al., 1997; Ficken et al., 2002; Wooller et al., therefore be used to illustrate variations in the source of 2003). We investigate the potential of using the stable nitrogen into sedimentary environments (e.g. Finney, isotopes of carbon and nitrogen in sub-fossil mangrove 1998). Decomposition rates of organic material are highly leaves as proxies of past mangrove eco-physiology. dependent on the type of plant species, the plant organ Stable isotope data derived from the measurement of (e.g. roots or leaves) and chemical composition (Benner et sub-fossil mangrove leaves in addition to pollen data al., 1987, 1991; Fogel and Tuross, 1999). could provide a multi-proxy approach towards past We investigated the potential of using carbon and mangrove environmental reconstruction. Sub-fossil nitrogen stable isotopic signatures in sub-fossil leaves of leaves are preserved as a small fraction of mangrove R. mangle as indicators of past mangrove stand struc- peat (McKee and Faulkner, 2000). The leaves of mod- ture and nutrient dynamics. Our approach was to study ern tall and dwarf Rhizophora mangle L. (Red man- several stages during the taphonomy of R. mangle leaves grove) often have distinctly different carbon and in a natural setting (Fig. 1) and the influence of these nitrogen stable isotopic characteristics, which are rela- stages on the stable isotopic composition of leaves. ted to the nutrient status and salinity of the environment Three requirements were investigated: (e.g. Alongi et al., 1992, 1993; Lin and Sternberg, 1992a,b; McKee et al., 2002). Dwarf R. mangle trees 1. The senescence of mangrove leaves on a tree. If have been noted as having more negative 15N values the stable isotopic signatures (13C and 15N) of (À5.38%) and more positive 13C values (À26.5%) R. mangle leaves are to be used in palaeoecologi- compared with tall R. mangle trees (15N=0.1% and cal investigations, then the signatures should 13C=À28.4%) (see McKee et al., 2002, for a compre- remain unaltered by senescence or fractiona- hensive review of the range of isotopic variation tion should be systematic. demonstrated for R. mangle). Dwarf trees are associated 2. Fallen leaves on the surface of mangrove peat. If with sites that are often in the interior of mangrove R. mangle leaves preserved in sediments are to be islands in Central America, while tall trees are more used to illustrate the past stand structure of often, but not exclusively, found around the edge of mangrove ecosystems, then assemblages of leaves islands. The morphological differences are generally directly below modern dwarf and tall trees should associated with phosphorus and nitrogen limitation, possess dwarf and tall stable isotopic signatures, where the dwarf trees are phosphorus limited and the respectively. tall trees are nitrogen limited (McKee et al., 2002). 3. Preservation of leaf tissue and chemistry within Compared with stable carbon isotopes, 15N measure- mangrove peat. If mangrove leaves are present ments are not as commonly used as palaeoecological in peat they need to retain sufficient carbon and proxies, because nitrogen in leaves can be turned over by nitrogen to measure both 13C and 15N microbes and invertebrates during the degradation of respectively. Variations in both d13C and d15N primary biomass. The 13C values, on the other hand, from mangrove leaves from older sediments alter very little during decomposition (Fogel et al., 1989; should be in accordance with the range of var- Fogel and Tuross, 1999). The direction of 15N changes iation seen in modern mangrove leaves, rather can also vary during decomposition (Fogel and Tuross, than the surrounding peat that is composed 1999), although generally 15N values become more primarily of fine roots and not likely to be positive due to the preferential loss of 15N-depleted contemporaneous with the leaves. M. Wooller et al. / Organic Geochemistry 34 (2003) 1259–1275 1261 Fig. 1. A model of the taphonomic stages in the production of sub-fossil R. mangle leaves. 2. Study site fallen leaves were collected from the peat surface. These specimens were dried at 50 C under N2 at the Smith- Fieldwork was conducted in Belize, Central America sonian Marine Station, Carrie Bow Cay, Belize. Samples at Twin Cays (16500N, 88060W) (Fig. 2), a peat based, were then packaged and transported to the Geophysical 92-ha archipelago of mangrove islands inside the crest Laboratory, Carnegie Institution of Washington (GL, of a barrier reef 12 km off the shore of Belize.