ELSEVIER Journal of Experimental Marine Biology and Ecology,

202 (1996) 97-106

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

Evaluating seagrass leaf litter decomposition: an experimental comparison between litter-bag and oxygen-uptake methods

M.A. Mateo”, J. Romero

Departmnento de Ecologic, Universidad de Barcelonn, Diqpnal 64.5, 08028 , Burcrlonu, Spuirl

Received 21 December 1994; revised 2 January 1996; accepted 30 January 1996

Abstract

Comparison of the decay rates of leaves of the seagrass Posidonia oceunica (L.) Delile have

been performed under different experimental conditions (season, depth, and kind of material). using two methods: litter-bag incubation and oxygen uptake measurements. Weight loss in litter-bags was higher (i) in summer than in winter (ii) in shallow zones than in deep zones (iii) in senescent leaves still attached to the plant than in leaf litter fragments. Oxygen uptake rates were higher in summer and in senescent leaves, but no effect of the incubation depth was shown.

indicating that mechanical effects are relevant for weight loss inside bags but not for metabolic processes. When compared on the same basis (carbon loss), decay rates obtained from oxygen

uptake measurements were always lower than those obtained using litter bags. On average. only 40% of the weight loss observed in the litter bags is explained by respiratory consumption.

Keywords: Detritus; Litter bags; Oxygen uptake; Posidoniu oceunicu

1. Introduction

The evaluation of decay rates of seagrasses is of great interest, since detritus formation and processing represent one of the main carbon (and nutrient) fluxes in the

associated ecosystems (Peres, 1953; Odum and De la Cruz, 1967; Fenchel and Jorgensen, 1977; Mann, 1988; Francour, 1990; Pedersen and Borum, 1992). and the decay rate of seagrass-derived detritus has a strong influence on the recycled:exported

ratio of plant primary production (Romero et al., 1992). As in terrestrial vegetation (Falconer et al., 1933; Gustafson, 1943), a common

method to estimate decay rates of aquatic plant detritus is the assessment of weight loss

*Corresponding author. Fax: + 34-3-41 I 1438.

0022-0981/96/$ IS.00 0 1996 Elsevier Science B.V. All rights reserved

P/I SOO22-098 I (96)OOO 19-6

98 M.A. Mateo, J. Romero I J. Exp. Mar. Biol. Ecol. 202 (1996) 97-106

of plant material enclosed in mesh bags (litter-bags) and incubated in situ or in meso- or

microcosms (e.g., Pellikaan, 1984; Wetzel, 1984; Opsahl and Benner, 1993). The simplicity of the method has favoured the accumulation of a considerable amount of data (Harrison, 1989). However, weight loss within the mesh bags occurs not only due to metabolic consumption but also through biomechanical fragmentation of detritus, which is lost when particles become smaller than the mesh (Robertson and Mann, 1980; Nienhuis and Groenendijk, 1986; Whitefield, 1988). This makes the method unsuitable

for a series of relevant ecological purposes (e.g., carbon or nutrient budgets). Oxygen uptake measurements have been used as an alternative method (Odum and De

la Cruz, 1967; Fenchel and Riedl, 1970; Hat-grave, 1972; Wahbeh and Mahasneh, 1985; OlLh et al., 1987; Peduzzi and Herndl, 1991), giving results that are better estimates of the mineralization rates. However, the simultaneous use of both methods in the study of

detritus decay has been attempted only rarely (Ohih et al., 1987) and the comparison of the variability of the two kind of measurements has not, apparently, been attempted so far.

We present here a concurrent estimation of decay rates of seagrass leaves using both oxygen consumption and litter bag methods, with the final aim of comparing the estimates resulting from each one of them, and of evaluating the contribution of

metabolic processes to the overall decay observed. The work was performed using material from the Mediterranean seagrass Posidoniu

oceanica (L.) Delile, the beds of which exhibit large seasonal leaf litter accumulations

(Boudouresque and Meinesz, 1982), which in turn play a major role in matter and

energy fluxes in the associated ecosystem (Romero et al., 1992; Pergent et al., 1994).

2. Methods

Decay experiments using litter bags were performed in a Posidonia oceanica meadow near Medas Islands (NE Spain) extending from 5 m to 15 m depth (see Ros et al., 1984). Weight loss and oxygen uptake were measured under different field conditions (seasonality: approximately summer and winter seasons of two consecutive years; depth:

5 m and 13 m, near the shallow and deep limits, respectively, of the plant distribution in the study site), and using different kinds of material (senescent leaves from 5 and 13 m,

and standing leaf litter). In autumn 1990, the oldest, outermost leaf of a number of bundles was collected by hand at both 5 and 13 m; litter was collected from large accumulations found at around 9 m depth. This material was immediately frozen

(-20°C); suitable amounts were defrosted for each experiment. For each experiment, mesh bags (1 mm mesh) containing ca. 10 g of dry weight

(DW) of leaves or leaf litter were placed under the leaf canopy of P. oceunicu at 5 and 13 m depth. Four mesh bags were used for each combination of time, material and depth. The bags were collected after 64- 117 days of incubation; three of them were used to assess weight loss, and the fourth to evaluate oxygen uptake.

The remaining material from three litter bags was dried (70°C) until constant weight and weighed separately, and subsamples were kept for elemental analysis. Decay rates were estimated as:

M.A. Muteo, J. Romrro I J. Exp. Mar. Bid. Ed. 202 (1996) 97-106 99

k = In(w,,w,) * ( 1 lt)

where k is the decay rate, and w0 and w, the initial dry weight and the dry weight at time

t of bag content respectively. Since the incubation period differed slightly between

experiments, taking into account that decay rates can decrease with time (Godshalk and Wetzel, 1978b), it was assumed that:

k, = k -h’.A

r+Jr .e (2)

where k, is the decay rate at a reference time t and kr+d, is the decay rate observed at

time t’ (with dt=r- t’). k’, i.e., the rate of variation of k (see Eq. (l)), was estimated

from data obtained in an experiment of leaf decay using litter bags lasting for 1 year,

performed at the same site (Mateo, 1995). Using Eq. (2), we computed a normalized decay rate for t=85 days (k,,).

Oxygen uptake measures were made on the material prior to field incubation, and on

the content of the fourth mesh bag, which was transported to the laboratory at around 4°C and always processed within 4 h of sampling. Oxygen uptake was measured by incubating the leaf material in stoppered 25 ml serum vials. About 5-6 pieces of

seawater-rinsed blade tissue of ca. 2 cm* each (around 100 mg dry weight) were placed in the vials. This size-selection was applied to avoid differences in oxygen uptake due to differences in the surface-to-volume ratio of the detritus. Then, 10 ml of filtered (0.2 ,um Nucleopore) seawater was added, leaving about 15 ml of head-space. The vials were

incubated in the dark at 15°C or 30°C for 48 h. Oxygen depletion in the head-space after the incubation period was then measured using gas chromatography following Kaplan et

al. ( 1979) as modified by L6pez ( 1993). A test of linearity of oxygen evolution during incubation was performed showing that linearity was conserved until 4 days after the

beginning of the experiment. For each sampling event, for each depth and for each type of material, three vials were incubated at each temperature.

To assess whether random differences between the four mesh bags would add a significant amount of variability to the results, a preliminary experiment was performed, in which four mesh bags were incubated as described, and after ca. 2 months, oxygen uptake was measured on four subsamples from each one.

To assess the effect of freezing on oxygen uptake rates, additional senescent leaves were sampled, and divided into two groups: one was frozen and oxygen uptake in the

other was measured immediately. After one week, oxygen uptake was measured in defrosted material. Five replicates were used in this experiment.

Results from weight loss and oxygen uptake were compared in terms of carbon loss rates as follows:

( 1) Carbon loss rate within litter bags (k,, in days ’ ) was computed as

k, = ( I lt) . ln(c,, /c,)

where c,, an c, are the initial weight and weight at time t inside the bags, expressed on a carbon basis.

(2) To convert oxygen uptake rates into carbon loss units, first (2a) a field oxygen uptake value was estimated by correcting the laboratory value for field temperature,

100 M.A. Mateo, J. Romero I J. Exp. Mar. Biol. Ecol. 202 (1996) 97-106

using the following expressions (Jorgensen and Sorensen, 1985; Vallespinos and Mallo, 1991):

R r=ln 15 . ( ) 1

R 30 (30 - 15)

R, = R,, . $WT)l

where R, is the oxygen uptake at temperature T, R,, and R,, are the oxygen uptake at 15 and 30°C respectively, and r is the rate of variation of oxygen uptake with

temperature. In these formulae we used the averaged values between oxygen uptake rates before and after field incubation.

Afterwards, (2b) oxygen values were transformed into carbon units using a 1: 1 molar ratio (Elliot and Davison, 1975), and then referred to initial carbon weight (k,, in days-‘)

Elemental composition was determined on subsamples from the litter bags and from the original material. Total carbon and nitrogen concentration were determined using a Carlo-Erba NA1500 autoanalyzer. Phosphorus was analyzed by ICP-AES after acid digestion, as described in Mateo and SabatC (1993).

One-way ANOVA was used to analyze data of variability among mesh bags and

differences following freezing of the plant tissues. Decay rates (kxs), final C, N and P content of the detritus, and oxygen consumption, were analyzed using a three-way

ANOVA. k, and k, were compared by linear regression analysis; residuals were computed and their variability was analyzed using three-way ANOVA.

3. Results and discussion

The variability in oxygen uptake rates among the four replicated mesh bags was of the same order as the variability within each mesh bag, i.e., no significant differences among

bags were found compared to within-bags differences (one-way ANOVA, P =0.456). This implies that random variability in oxygen uptake rates is caused mainly by the

heterogeneity of the incubated material (differences in the bacterial colonization, in the

quality of the material, etc.). Oxygen uptake rates did not differ significantly between freshly collected and frozen

material, as demonstrated by one-way ANOVA (P = 0.542). This is probably due to the

kind of material used, in which the first phases of decomposition (i.e., leaching and, partially, bacterial degradation: see Valiela, 1984) had been completed.

Results of field and laboratory experiments are summarized in Table 1, Table 2 and Fig. 1. The effects of incubation depth (5 and 13 m), season (summer and winter) and kind of material (senescent leaves from 5 and 13 m, and leaf litter) on k,, and oxygen uptake values were tested. A significant effect of season and kind of material was found for both dependent variables, while the incubation depth affected only the k,, rates (Table 3). Since the Tukey post-hoc test showed no significant differences either in oxygen uptake or in decay rates between senescent leaves from 5 and 13 m, for the rest

M.A. Mateo, J. Romero / J. Exp. Mar. Bid. Ed. 202 (1996) 97-106 IO1

Table I Main results and field experimental conditions

Experiment Period Depth Number Mean T k,,?SE

(m) of days (“C) (day ‘) OL uptaketSE

(mgO;g ‘DW.d ‘)

Senescent

I Feb l99l-May 1991

I’ Feb l99l-May 1991

3 Jul 1991-Sep 1991

2’ Jul 1991-Sep 1991

3 Nov l99l-Jan 1992

3’ Nov 1991-Jan 1992

4 Jun l992-Ott 1992

4’ Jun 1992-Ott 1992

Litter

I Feb l99l-May 1991

I’ Feb l99l-May 1991

2 Jul l99l-Sep 1991

2’ Jul l99l-Sep 1991

3 Nov 1991-Jan 1992

3’ Nov l99l-Jan 1992

4 Jun l992-Ott 1992

4’ Jun 1992-Ott 1992

5 80 13.5

13 80 13.5

5 64 20.0

I3 64 19.5

5 78 15.0

13 78 IS.0

5 I I7 21.0

I3 II7 20.5

5 80 13.5

I3 80 13.5

5 64 20.0

I3 64 19.5

5 78 IS.0

I3 78 IS.0

5 II7 21.0

I3 II7 20.5

0.0052’-0.0006

0.0044 ? 0.0004

O.CKJ96~0.0012

0.0058+0.0014

O.O06Ot-0.0007

o.o053t-0.0003

0.0136~0.0016

0.0075 zo.00 I8

0.0042-c0.0027

0.0029-t0.0004

O.OO89-tO.OOlO

O.OO6O-cO.OOO5

0.0037-+0.0006

0.0040-t0.0006

0.0133-+0.0079

O.OOS2~0.0006

0.08 to.009

0.0820.0037

0.15+0.0051

0.12+0.0104

0.09~0.0105

0.10-+0.0070

0. I3 ~0.0070

0.18t0.0035

0.06-tO.Ol2S

0.06?0.0128

0. I 1 to.0 I24

0. I I -to.0044

0.07 +-0.0032

0.0710.0045

0.1210.0046

0.09~0.003.5

Respiration values are corrected for field temperature

of the discussion and for the sake of clarity, we have pooled data from these two kinds

of material into a single class (senescent leaves). Elemental composition of the different kinds of detritus did not change significantly

following incubation (Table 2), except for nitrogen, which increased in summer (three

way ANOVA, P<O.OOl). Seasonality explained most of the variability of both decay and oxygen uptake rates

(Table 3). However, the extent of the seasonal control differed among them: while the decay rate (k,,) increased 90% from winter to summer, oxygen uptake showed only a 30% increase for the same time interval (Table 1). Since laboratory experiments were

Table 2

Senesent leave\ and leaf litter carbon, nitrogen and phosphorus content, before and after the field incubation

period

Leaf material Season Initial (96) Final (%)

C N P C N P

Summer 3 I .S(O.2) I .3 I(O.02) 0.0.53(0.01 I ) Senescent 32.9(0.4) I, 13(0.02) 0.072(0.04)

Winter 34.3( 0.96) 0.95( 0.03) 0.06X0.042 1

Summer 31.8(0.93) 0.95(0.08) 0.063(0.010)

Litter 30..5(0.4) 0.85(0.02) 0.060(0.001 ) Winter 3 I .4(0.26) 0.73(0.02) 0.078(0.010)

Standard error of the mean in parentheses.

102 M.A. Mateo, J. Romero I .I. Exp. Mar. Biol. Ecoi. 202 (1996) 97-106

Litter Senescent

T------ r----l

Experiment

Fig. 1. Remaining dry weight in the litter bags after field incubations. Error bars are the standard error of the

mean with n = 3 for leaf litter and n = 6 for senescent leaves (after pooling of data, see text). Experiment No.

on the x-axis (see Table 1).

performed under the same conditions throughout the year, the summer increase in

oxygen uptake may be the result of increased bacterial biomass, which is also indicated by the nitrogen increase in detritus after the field incubation (Table 2). Other factors linked to summer temperature increase can explain the seasonal differences observed,

such as the stimulation of bacterial (and other micro-organism) activity (Jorgensen, 1977; Godshalk and Wetzel, 1978~; Jorgensen and Sorensen, 1985; Hall et al., 1989; Vallespinos and Mallo, 1991; this study: Q,,= 1.58 after laboratory leaf material 0,

uptake at 15 and 3O”C), the increase in cell autolysis (Godshalk and Wetzel, 1978a) and the meiofaunal abundance (Harrison and Mann, 1975; Robertson and Mann, 1980;

Gunnarsson et al., 1988; Menendez et al., 1989); most of these factors operate in the

Table 3

Variance analysis results

Litter bags (k,,) Oxygen uptake (k,)

% V.E. P % V.E. P

Season

Depth

Material Error

Interactions

30 <O.OOl 43 <O.ool

II <O.OOl _ n.s.

5 0.022 18 <O.OOl 48 _ 31 _

6 CO.05 2 CO.05

(1 X2) (1X2) (I X2X3)

YE., variance explained.

M.A. Mateo, .I. Romero I J. Exp. Mar. Biol. Ecol. 202 (1996) 97-106 103

field, and may thus explain the differential response to seasonality between field

measurements of weight loss and laboratory measurements of oxygen uptake.

The quality of the material has been mentioned as a control on the overall

decomposition process (Harrison and Mann, 1975; Godshalk and Wetzel, 1978a; Rietsma et al., 1988; Taylor et al., 1989; Buchsbaum et al., 1991). On average, senescent leaves decayed 15% faster than leaf litter, and oxygen uptake was 23% higher (Table 1). The first phases of decomposition (leaching of soluble compounds; bacterial attack on the more labile components: see for example Godshalk and Wetzel, 1978a; Brock et al.,

1985; Valiela et al., 1985) occur within a few days after leaf abcision, or even when the old leaves are still attached to the shoot, and thus the leaf litter (with a mean residence

time of the order of months: see Romero et al., 1992) is enriched in refractory materials.

More specifically, nitrogen concentration was higher in senescent leaves than in leaf litter (Table 2). If we assume a C:N ratio for bacteria close to the Redfield ratio (C:N = 6.25 by atoms), it is clear that growth using senescent leaves as substratum (C:N

ratio: 17-25) can proceed faster than using leaf litter (C:N ratio: 35-40), and thus our results can be explained, at least partially, in the light of a potential N-limitation (Lopez

et al., 1995). Decay rates are 57% higher in the shallower station (similar to results found in other

meadows; Romero et al., 1992), while oxygen uptake was depth-independent (Table 1 and Table 3). This suggests the importance of water movement, which quickly decreases with depth (see Gambi et al., 1989) as a factor acting mostly on mechanical losses

(fragmentation, particle losses through bag shaking, enhancement of sand abrasion, etc.).

There may also be an interaction between mechanical fragmentation and oxygen uptake, since reduction in particle size increases decomposer metabolism (Hargrave, 1972;

Godshalk and Wetzel, 1978b; Robertson and Mann, 1980; Harrison, 1989; Gunnarsson et al., 1988). However, this effect is not shown by our data, as the particle size

composition of the material selected for incubation was constant (see Section 2). Rates of carbon loss (k,) and oxygen consumption (k,) showed the same trends, but,

as expected, oxygen consumption rates were always lower (see Table 1). Both rates (k, and k,) are highly correlated (Fig. 2), and about 40% of the variability in decay rates (as observed in the litter-bags) is explained by the variability in the metabolic consumption

of this detritus (r* =0.397, see Fig. 2). Since the intercept of the regression line is not significantly different from zero, we can assume that the reverse of the slope is an

estimate of the average contribution of the respiration process to the decay observed in

situ (about 40%). Residuals of this regression model, which represent the part of decay rates k, that is not explained by respiratory activity k,, were analyzed using a three way ANOVA for the effects of seasonality, kind of material and incubation depth. The only

factor explaining a significant, although small (15%) part of the residual’s variance was the depth of incubation. The residuals were lower (negative) in the deep station, and positive in the shallow one, indicating a major role of fragmentation processes near the

sea surface due to higher hydrodynamism. The lack of seasonal trend in this analysis may be attributed to the fact that fragmentation is influenced by both hydrodynamic forcing and biological consumption by meiofauna and microfauna, which, in temperate, shallow marine environments, follow opposite seasonal trends (Gambi et al., 1989, Gambi et al., 1992).

104 M.A. Mateo, J. Romero I .I. Exp. Mar. Biol. Ecol. 202 (1996) 97-106

0.000 ’ , I I I

0.0018 0.0027 0.0036 0.0045 0.0054

Fig. 2. Comparison of litter-bag vs. oxygen uptake methods in terms of decay rates (k, and kr, respectively).

Rates are in day-‘. Fitting parameters: intercept = - 0.0006; slope = 2.46; r = 0.63; P <0.0001 (see text for

details).

In summary, the litter-bag method to assess the decay rates includes metabolic activity

(and thus reproduces its variability: seasonal trends and response to material quality) but is by no means equivalent to oxygen-uptake method (i.e., mechanical factors affect

litter-bag estimations but not, or to a lesser extent, oxygen uptake). Litter-bag estimates are inadequate for carbon budgets, as shown, and at least in the system under study,

around 40% of the decay rates derived from litter bag incubations corresponds to metabolic consumption, while the rest are losses in the form of fine organic debris (less than 1 mm) which can, in turn, be mineralized, exported or stored in the sediment.

Acknowledgments

This work was supported by the Grant STEP-0063-C of the EU. We thank N. Lopez and F. Vallespinos for assessment.

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