J. Exp. Mar. Biol. &of.,
1988, Vol. 116, pp. 235-247
of mangrove leaf litter in tropical Australia A. I. Robertson
Australian Institute ofMarine Science. Townsville, Queens/and, Australia
(Received 19 August 1987; revision received 24 November 1987; accepted 19 December 1987) Abstract: Litter bag experi.ments were used to follow changes in mass and chemical constituents during decomposition of leaves from three mangrove species, Rhizophara sfyiosa Griff., Avicennia marina (Forsk.) Vierh. and Ceriops tagaf var. australis C.T. White. Losses of AFDW from leaves maintained in the subtidal were best described by double exponential models, which showed that the percentage of the initial AFDW which was relatively labile differed among species; Avicennia (61.5), Ceriops (45.4), Rhizophora (40.3). The times required for loss of half the initial AFDW (&) of submerged leaves were Avicennia 11 days, Ceriops 27 days and Rhizophora 39 days. The rates of loss of carbon were slightly slower, and were more readily fitted by single exponential models. Linear models were fitted to AFDW and carbon data for leaves left to decompose in intertidal forests. Leaves in the forest decomposed much more slowly than submerged leaves; I, 5 values for AFDW were Avicennia 90 days. Rhizophora 226 days, and Ceriops 228 days. For all species in both habitats, nitrogen was lost from leaves more slowly than carbon and AFDW, and at the end of the experiment, the percentage of the original mass of nitrogen in leaves was higher than the percentage of the original AFDW or carbon. In the subtidal habitat the concentration of nitrogen in leaves of all species increased during the first 70 days of the experiment, and levelled off or dropped thereafter. In the forest nitrogen concentrations in leaves showed a steady increase to Day 348 ofthe experiment. Bacterial densities initially increased rapidly in both habitats as tannins were lost from leaves. After Day 40 bacterial densities in the subtidal habitat fluctuated widely (Rhizophora, Ceriops) or declined (Avicennia), while in the forest, densities increased slowly (Ceriaps, Rhizophora) or declined (Avicennia). Bacterial nitrogen usually contributed less than one percent of the total leaf nitrogen concentration. Key words: Avicennia; Ceriops; Decomposition; Litter bag; Mangrove; Rhizophora
remove leaf litter has a number of potential fates, depending mainly on the degree and frequency of tidal inundation (Twifley, 1985; Twilley eb al., 1986) and the presence or absence of a leaf consuming fauna (Odum & Heald, 1975; Leh & Sasekumar, 1985; Robertson, 1986) within forests. Because of this in most regions of the world the dynamics of leaf litter breakdown will exhibit wide variation among sites and forest types. Such variation needs to be accounted for if robust food chain models for mangrove swamps are to be developed (e.g., Harris & Grifftths, 1987). In low- to mid-intertidal mangrove forests dominated by Rhizophora spp. in tropical northern Queensland, close to 30% of the annual leaf fall is taken underground and Contribution 4OP from Australian Institute of Marine Science. Correspondence address: A.I. Robertson, Australian Institute of Marine Science, P.M.B. No. 3, Townsville, MC, Queensland 4810, Australia. 0022-0981/8S~SO3.500 1988 Elsevier Science Publishers B.V. (Biomedical Division)
consumed by leaf eating crabs (Robertson, 1986). Most of the remaining leaf litter is exported to adjacent waterways (Boto 8c Bunt, 1982; Robertson, 1986), but some may accumulate in the higher levels of the forest, where after some decomposition, leaves are consumed by macroinvertebrates (e.g., Poovachiranon et al., 1986). In high-intertidal forests, flushed only by spring tides (e.g., those usually dominated by Ceriops spp., Bruguiera exaristata and Avicennia marina), there is some variation in the quantities of leaf litter removed by leaf eating crabs andfor decomposed by microbial action (pers. obs.). For instance in Ceriops forests most leaflitter is taken underwound and consumed by crabs, while in Avicennia forests most leaves are decomposed through microbial action (A. Robertson, unpubl. data). In order to develop a food chain model which gives an accurate picture of the variation in leaf litter dynamics among the major forest types in northern Queensland, and to assess the relative importance of processes supporting the very high sediment bacterial production (0.2-5.2 g C. me- 2 - day- ‘) in these forests (Alongi, 1988), I have begun a program to measure inputs to mangrove detrital pools from microbial decay of litter, turnover of litter by shredders (e.g., Robertson, 1986) and from another major source of detritus, the breakdown of wood biomass (see Robertson, 1987). In this paper I report the results of controlled field experiments on leaf litter decomposition used to obtain the decay rates of leaflitter due to leaching and bacterial action, both within the intertidal zone of mangrove forests and in subtidal waters adjacent to forests. Comparisons are made among the leaves of three important mangrove tree species in tropical Australia. In addition, I measured changes in carbon, nitrogen, hydrolyzable tannins and bacterial densities in decomposing leaves to obtain information on the relative nutritive quality for consumers of different types of leaf detritus. MATERIALS FIELD EXPERIMENTAL
All experiments were performed in mangrove forests at Chunda Bay (19” 17’ S : 147’ 03’E) near Townsville in northern Queensland. Experiments were performed on the leaves of the three tree species, Rhizophora stylosa Griff., Avicennia marina (Forsk.) Vierh., and Ceriops tagal var. australis C.T. White, which dominate the mangrove forests in this region (Smith, 1987). For the experiments, I used ageing yellow leaves that were still attached to branches, but were ready to abscise. After collection, several leaves of each species were placed in groups (Rh~zophora, n = 3 leaves; Avicennia, n = 12 leaves; Ceriops, n = 8 leaves), weighed (0.01 g) and sewn into numbered nylon mesh bags (mesh size, 2 mm’). The range of weights for all groups of leaves was 6.05-13.27 g. Collection and weighing of leaves was performed within 48 h and mesh bags were then set out in the field. Five leaf groups of each species were retained to derive fresh weight : dry weight : AFDW conversion factors for leaves placed in the field. The experiment commenced in November, towards the end of the main period of leaf fall for Avicennia, and the beginning of the leaf fall period of R~izophora and Ceriops (Duke, 1982).
DECOMPOSITION OF MANGROVE LEAF LI’M’ER
For each species, bags were placed in the field following a three factor experimental design, with habitat, site and time as factors. Leaves were left to decompose in two habitats; fully submerged in small creeks which did not drain completely at low tide ( = submerged), and within the mid-intertidal zone of forests dominated by Rhizophoru stylosa ( = forest). The mid-intertidal zone was chosen as a compromise, because leaves of all species are moved about the forests by tides, and the conditions in the midintertidal probably represent the average decomposition environment for most leaves. Enough bags were placed in each habitat to allow the experiment to run for 1 yr. Bags were placed in submerged and forest habitats at each of two sites separated by 1 km of mangrove forest. For each species, three bags were removed from each site and habitat on Days 14,40, 71, 112 and 156 of the experiment. After 156 days, leaves of all species in the submerged habitats, and Avicennia leaves in the forest habitats, were almost completely decomposed and collection of bags from these treatments was terminated. There was a final collection of leaves of Rhizophora and Ceriops from the forest habitats on Day 348 of the experiment. The use of litter bags for studies of decomposition has always been the subject of some criticism. Major drawbacks in the technique are that most small mesh litter bags deny access to macroinvertebrate shredders and thus retard the breakdown rate of litter, or if mesh size is large enough to allow entry of shredders, large fragments of detritus can be lost from bags (Newell et al., 1984). However such criticisms are not relevant to work described in the present paper, which aims to measure only microbial decomposition of leaves in the absence of shredders (see earlier). During the entire study only four amphipods were extracted from litter bags.
After removal from the field, leaves from each bag were rinsed under freshwater over a OS-mm sieve to remove sediment, and a small subsample of leaf tissue to be used for enumeration of bacterial densities was removed. The remaining leaf material was oven dried (5 days at 60 “C), weighed and then ground to a powder. Subsamples of the powdered sample were used to determine percent ash (muffle furnace, 24 h at 500 “C), percent carbon and nitrogen (Leco 600 C-H-N analyser; precision, carbon 0.3:/,, nitrogen 3.0%) and percent soluble tannins (Folin-Denis method; Allen et al., 1974). Leaf tissue for bacterial counts was preserved in 2.5% formaldehyde in filtered seawater, and all counts were made within 14 days of sampling. Leaf tissue was blended for 5 min in a Sorval tissue homogenizer and bacteria were stained and prepared for counting by epifluorescence microscopy following the method of Hobbie et al. (1977). After removal of the small quantity of solution required for bacterial counts, the remaining homogenized leaf tissue was trapped on a preweighed filter, dried and weighed. Bacteria were counted at x 1200 magnification and dilutions were such that between 20 and 200 cells were counted per field. Bacterial densities ( . g - ’ dry wt leaf material) were converted to biomass in terms of nitrogen by assuming that there is
A. I. ROBERTSON
1.7 x lo- l4 g C * bacterial cell- ’ (Alongi, 1988) and that the C : N ratio of bacteria is six (Nagata, 1986). Changes in leaf chemistry during decomposition are expressed in two ways in the present study. For instance, nitrogen concentration is g N *g- ’ dry wt leaf material x 100, and percent of original nitrogen remaining is nitrogen concentration multiplied by residual dry weight normalized to nitrogen mass at Day 0. DATA
Four-way analyses of variance (ANOVAs) with species (three levels), time (five levels), site (two levels) and habitat (two levels) as fixed factors were used to compare means of weight loss (AFDW, carbon and nitrogen) among all treatments during the first 156 days of the experiment (only forest samples continued to Day 348). Raw percentage data were used in each analysis. Data could not be arcsine p-transformed because percentages > 100 were common in the data set. Several models were used to describe weight loss (AFDW, carbon) from leaf litter. AFDW data for submerged leaves of each species were fitted to a double exponential model, X,/X, = AePKlt + (1 - A)ePKZ’, where X,/X, is the proportion of initial material remaining at time t, K, and K, are decay constants, A is the relatively labile proportion of initial material and (1-A) is the more refractory portion of initial material (Wieder & Lang, 1982). Best tit models for carbon data for submerged leaves of Rhizophora and Ceriops were provided by single exponentials, X,/X, = eBKl. Decomposition data for leaves retained in forests were much more variable than that for submerged leaves, and simple linear models gave the best tit to the data for AFDW and carbon. Wieder & Lang (1982) have pointed out that although the assumptions of the linear model (i.e., constant absolute decay rate, and increasing rate of relative decomposition with time) may be diflicult to justify biologically, they may be useful in obtaining estimates of decay rates to be used in subsequent modelling of leaf litter dynamics, subject to the proviso that in the fitted linear model all of the initial litter is present at t = 0. All linear regressions in the present study were forced through (0,100).
LOSS OF AFDW,
There was no significant difference in the mean percentage of the original AFDW, carbon or nitrogen in leaves at the two sites for all species, habitats and times (no
OF MANGROVE LEAF LITTER
Summary of four-way ANOVAs for loss of AFDW, carbon and nitrogen from leaves. *** = P i 0.001: ** = P < 0.05; NS = not significant. Source of variance
Species (Sp.) Time (T.) Site (52.) Habitat (H.) Sp. x T. Sp. x Si. Sp. x H. T. x Si. T. x H. Si. x H. Sp. x T. x Si. Sp. x T. x H. Sp. x Si. x H. T. x Si. x H. Sp. x T. x Si. x H.
NS *** NS
Fig. 1. Changes which occurred during the decomposition of Rhizophora stylosa leaves, Data are means ( & 1 SE,n = 6) of variates for submerged (0) and forest (0) habitats. Figures in parentheses on the graph of nitrogen concentration are the estimated percentage contributions of bacterial nitrogen to the total concentration of nitrogen in leaf samples. Equations for fitted lines are given in Table 11.
A. I. ROBERTSON
signiftcant site main effect or interaction involving site in ANOVAs, Table I), and data from the two sites were pooled in all further analyses (e.g., Figs. 1-3). The pattern of weight loss (AFDW, carbon and nitrogen) varied amongst habitat and times for each species (significant habitat x time x species interactions in ANOVAs, Percent
Percent original carbon
Percent original nitrogen
\ *-----ii 80
tl.th~f~~e6$--+--~ / C,&7p&) (1.0)
Fig. 2. Changes which occurred during the decomposition of Avicenniu marim Fig. 1.
All symbols as in
Table I). During the early phase of the experiment the rate of loss of AFDW and carbon for all species was much greater from leaves that were continually submerged than those in the mid-intertidal zone of the forest (Figs. l-3). Double exponential equations describing weight loss from submerged leaves indicate that the percentage of relatively labile material in leaves (the A values, Table II) increases in the order Rhizophoru (40.3),
OF MANGROVE LEAF LITTER
Ceriops (45.4), Avicennia (61.5), and the time taken for loss of half the original AFDW or carbon increases in the order; Avicennia, Ceriops, Rhizophora. The time courses of AFDW and carbon loss from leaves maintained in the forest were much more variable than for submerged leaves, and linear models (implying constant
Fig. 3. Changes which occurred during the decomposition of Ceriops tugal leaves. All symbols as in Fig. 1. TABLE II
The gradients (a) for the linear models describing decomposition in the forest and single (K,) or double exponential decay parameters (A, X,, R,) describing decomposition of leaves when submerged. &,, values indicate the time in which half of the original AFDW or carbon was lost from leaves of each species under each condition. Units for each parameter and value are given in brackets. -
Forest c (day- i) ro.5(day) Submerged A (%) K, (day-‘) K, (day-‘) rc.s (day)
- 0.221 226
- 0.213 235
- 0.558 90
- 0.219 228
- 0.157 318
61.5 0.128 0.010 11
40.3 0.047 0.008 39
* Single exponential model.
51.6 0.102 0.009 15
45.4 0.109 0.005 27
0.009* 17 -
A. I. ROBERTSON
rates of decomposition) provided the best fits to the data (Figs. l-3, Table II). Although there were great differences in the initial rates of weight loss between forest and submerged leaves of Rh~zop~oraand Ceriops, once the more labile fractions of submerged leaves had decomposed, rates of loss in the two habitats were fairly similar (Figs. 1,3). The decay constant for Avicenniu leaves maintained in the forest was much more negative than for Ceriops and Rhizophoru (Figs. l-3), and after 156 days there was no significant difference in AFDW or carbon remaining in A vicenniu leaves from submerged and forest habitats (Fig. 2). Changes in the percentage of the original mass of nitrogen remaining in leaves of all species did not follow the same time courses as changes in AFDW or carbon. For Rhizophora and Ceriops in both habitats the amount of leaf nitrogen either remained near 100% of the original value, or increased, during the first 40-7 1 days of the experiment (Figs. 1,3). Thereafter the amount of nitrogen decreased fairly rapidly in the submerged leaves. However, even after 156 days in water, the amount of nitrogen was still z 60 % of the original value in Ceriops, but ~40% for Rhizophora. Leaves of Ceriops and Rhizophora maintained in the forest also lost nitrogen after 40-7 1 days of the experiment, but at a much slower rate, so that at Day 348 of the experiment w 80% of the original mass of nitrogen was present. Of the three species, the time course of nitrogen loss for Av~ce~n~ufollowed most closely the loss of carbon and AFDW (Fig. 2). Leaves ofAvicennia in both habitats lost nitrogen throughout the experiment (but initially at a slower rate in the forest). However, as with leaves of Ceriops and Rhizophoru, a greater proportion of the original amount of nitrogen than AFDW or carbon remained in Avicenniu leaf detritus in both habitats at the end of the experiment (Figs. 1-3). CHANGES
IN LEAF CHEMISTRY
In both habitats the concentration of nitrogen in leaf tissue of all species showed rapid initial increases followed by a flattening off or slight drop towards the end of the experiment (Figs. l-3). For all species nitrogen concentration was greater in submerged leaves until at least Day 112 of the experiment (Rhizophora, Avicenniu) or longer (Ceriops). By Day 156 the nitrogen concentration in Avicenniu was greatest for leaves maintained within the forest. The mean C : N ratios of leaves of all species were high at the beginning of experiment, but dropped steadily with time in both habitats (Figs. 1-3). Decreases in C : N ratios were initially more rapid in submerged leaves, but ratios were similar for both habitats after 156 days. C : N ratios of leaves of Rhizophoru and Ceriops maintained in forests did not change between Days 156 and 348 of the experiment. After 156 days ratios were lowest in Avicenniu (E 25) and greatest in Ceriops (w 40). Both Ceriops and R~izop~oru had very high concen~ations of hydrolyzable tannins at the beginning of the experiment, but tannins were lost rapidly from the leaf detritus in both habitats, so that after 70 days concentrations were generally < 3% by weight
(Figs. l-3). Between Days 156 and 348 there were small, but significant increases in the concentration of tannins in leaves of Rhizophoru and Ceriops in the forest habitat. The initial concentration of tannins in Avicenniu leaves was much less than for the other species, and mean concentrations dropped to below 3 y0 after 14 days in both habitats. During the rest of the experiment concentrations of tannins in Avicennia leaves remained low, although they were significantly higher in the forest habitat. Bacterial densities increased rapidly during the first 40 days of the experiment (Figs. l-3), and densities were two to three times greater in the submerged habitat for all species. For Avicennia, bacterial densities declined during the remainder of the experiment, while they fluctuated markedly on leaves of Ceri0p.s and Rhjzophora. At Day 348, densities on leaves of Ceriops and Rh~zophoruin the forest habitat were as great or greater than at any time during the experiment. Overall the contribution of bacterial nitrogen to total nitrogen concentrations in decomposing litter was very small in all species, at most contributing 1.7% of the measured leaf nitrogen (Figs. l-3).
Although there have been a number of studies of mangrove litter decomposition in the New World (e.g., Heald, 1971; Fell et al., 1975, 1980; Cundell et al., 1979; Fell & Masters, 1980; Newell et al,, 1984; Flares-Verdugo et d., 1987), work on litter decay in mangroves of the Indo-West Pacific tropics is rare (e.g., Poovachiranon & Chansang, 1982; Boonruang, 1984). This work is the first of its kind in Australian tropical forests, although decomposition rates are available for Avicennia in temperate Australian forests (Goulter & Allaway, 1979; Van de Valk & Attiwill, 1984). In this study leaves of Avicennia, with their high initial nitrogen concentration, low C : N ratio and low hydrolyzable tannin concentration, had the most rapid decomposition rates. By contrast, leaves of Ceriops and Rhizophora with low initial nitrogen concentrations, high C : N ratios and very high tannin concentrations decayed much more slowly. Initial chemical status of litter, in particular C : N ratios and tannin or lignin concen~ations also have a controlling inthrence on decay rates of litter in grassland and terrestrial forest systems (Hunt, 1977; MelilIo et al., 1982; Wieder et al., 1983). In addition, submerged leaves of all species generally decayed more rapidly, and with less variability (at the replicate level) than leaves in the intertidal zone of the forest. Submerged conditions provide a more stable, predictable environment for small heterotrophs involved in the decomposition process, and this was reflected in the generally greater densities of bacteria on submerged vs. forest leaves for each species. The more variable decomposition environment of the intertidal zone, with major fluctuation in temperature and degree of water cover, probably led to the slower development of a bacterial flora, and slower decay rates. As indicated by the double exponential equations fitted to the AFDW data for submerged leaves, the percentage of AFDW which was relatively labile decreased in the
A. I. ROBERTSON
order Avicennia (6 1.5 %), Ceriops (45.4%), Rhizop~o~Q(40.3 %). Studies on leaching of dissolved organic matter (DOM) from leaves of Avicenniu marina and Rh~z~pho~u mangle have shown that 13 and 40% of the original AFDW may be released by leaching in the first 3-9 days of decomposition, respectively (Van der Valk & Attiwill, 1984; Camilleri & Ribi, 1986). This implies that only 21% of the relatively labile portion of Avicenniu leaves is lost by leaching, the remainder (79%) must have been present as nonleachable, but easily decomposed organic matter. By contrast (if data for R. stylosa and R. mangle is combined), nearly 100% of the relatively labile portion of Rhizophora leaves would have been lost by leaching in the present study. Comparison with other litter bag studies on submerged mangrove leaves in the tropics reveals that the mean number of days taken for a 50% reduction in weight for Rhizophora styrosa (39 days) is very similar to that for R. upiculata in Thailand (40 days) (Boonruang, 1984). By contrast Avicennia leaves lost 50% of their weight in 11 days in this study, approximately half the time taken in two studies in Thailand (28 and 20 days) (Poovachiranon & Chansang, 1982; Boonruang, 1984). The rapid (14-40 days) loss of tannins from leaves of all three species coincided with rapid increases in the densities of bacteria on leaves, as has been observed in a previous study on mangrove leaves (Cundell ef al., 1979). However, despite the high densities of bacteria (x lO’*-10” . g- ’ leaf tissue), bacterial nitrogen usually contributed only z 1y0 of the nitrogen concentration of decomposing leaves. Work with other aquatic vascular plants detritus has revealed that the number of bacteria on detrital particles usually accounts for < 5 y0 of the particulate nitrogen (Christian & Wetzel, 1978; Marsh & Odum, 1979; Rice & Hanson, 1984). While fungi are also abund~t on decomposing mangrove litter (Fell et al., 1975, 1980; Fell & Masters, 1980) it appears unlikely that they contribute any more to total detrital nitrogen than do bacteria (Rice & Hanson, 1984). Recent work suggests that much of the observed increase in total detrital nitrogen during the decomposition of marine macrophytes occurs through the production of mucopolysaccharide exudates by bacteria (Hobbie & Lee, 1980) and that such exudates may be incorporated in humic macromolecules in the detritus (Rice & Hanson, 1984). Changes in le~chemis~ which occur during the decomposition of leaves, often have important implications for detritus consumption by macroinve~ebrates in northern Queensland mangrove forests. For instance, during the fust 2 wk of decomposition in the forest habitat the concentration of tannins in Ceriops leaves dropped by 50%) while there was no significant change in the concentration of nitrogen or the C : N ratio of leaves. This helps to explain why the major leaf-consuming crab in Ceriops forests, ~eo~~~rnati~rnsmithii, prefers to feed on leaves that have aged for at least two weeks (Giddins et al., 1986). Simil~ly the ~phipod P~rhyffle ha~uie~i~, which is abundant amongst Ieaf litter accumulations at the high tide mark of Rh~zopho~a~ty~o~aforests, exhibits maximum feeding rates on leaves that have lost most of their soluble tannins and have a higher leaf nitrogen content (Poovachiranon etal., 1986). Althougb Poovachiranon et al. (1986) did not know the age of the Rhizophora detritus preferred by P. hawaiensis (their type ‘D’ detritus), it had nitrogen and tannin concentrations of
0.79 and 2.34x, respectively, which occurred after 71 days for Rh~~~phoraleaves in the present study. However, not all cons~ers of leaf detritus in northern Queensl~d mangrove forests require that leaves ‘age’ before they are palatable. The grapsid crab Sesarma messa (Campbell) consumes leaves of Rhizophora spp. that have just fallen from trees (Robertson, 1986), that is with tannin concentration of z 17%. This indicates that individuals of S. messa possess enzymes capable of overcoming the normal proteinbinding effects of tannins. It remains questionable whether increases in the concentration of nitrogen, and decreases in the C : N ratios during the decomposition of mangrove leaf detritus reflect increases in the nutritional status of detritus for higher consumers. Rice (1982) showed that there were increases in nitrogen concentration and the absolute mass of nitrogen during a 150-day microcosm experiment using detritus derived from leaves of Rhizophoru mangle. In his experiment there existed a significant positive relationship between nitrogen accumulation and the production of humic substances formed from the complexing of phenolics and amino acids. He concluded that the biological availability of humic nitrogen probably depends on the extent to which protein subunits are retained in humic macromolecules (Rice, 1980). In my field experiments the percentage of the original mass of nitrogen (Rice’s absolute mass of nitrogen) remaining in Rhizophora and Ceriops detritus remained constant or increased slightly for the fust 70-100 days and then declined. The mass of nitrogen in Avicennia detritus dropped initially, remained constant for a further 70 days, and then declined. Such step-like patterns of nitrogen dynamics fit the cyclic model of detrital nitrogen immobilization and mineralization proposed recently by Mel~lo et al. (1984). In this model miner~ization occurs when microbial exoenzymes depolymerize the detrital substratum, producing (among other compounds) reactive carbohydrates and phenolics. During this phase there is some loss of nitrogen. During the next phase (immobilization) the reactive compounds condense with components of the detrital nitrogen pool to produce nitrogen-rich compounds. Such cycles continue throughout the period of decomposition, with most of the increase in the concentration of nitrogen ( y0N) being accounted for by build up of nitrogen in humic compounds which are probably unav~lable to higher consumers.
C. Payn performed all of the chemical analyses and K. Boto, B. Clough and M. Pichon made useful comments on an earlier draft of this paper.
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PARKINSON & C. QIJARMBY, 1974. Chemical analysis of ecological
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