Growth Dynamics, Production, and Nutrient Status of the Seagrass Cymodocea nodosa in a Mediterranean Semi-Estuarine Environment

P.S.Z.N. I: Marine Ecology, 15 (1): 51-64 (1994) 0 1994 Blackwell Wissenschafts-Verlag, Berlin ISSN 0173-9565

Accepted: June 16,1993

Growth Dynamics, Production, and Nutrient Status of the Seagrass Cymodocea nodosa in a Mediterranean Semi-Estuarine Environment MARTA PBREZ & JAVIER ROMERO

Departament d’Ecologia, Facultat de Biologia, Universitat de Barcelona, Diagonal 645, E-08028 Barcelona, Spain.

With 8 figures and 2 tables

Key words: Primary production, seagrass, nutrients, phosphorus, Cymodocea nodosa, Mediterranean.

Abstract. Cymodocea nodosa is a relatively small seagrass species which is common in the Mediterranean. An intensive survey on its growth and production was carried out in a dense, monospecific stand located in a semi-estuarine embayment. Data on leaf appearance and growth, shoot recruitment and death, rhizome growth, above- and belowground biomass, and nutrient content in the different parts of the plant were obtained over 2 years. All these variables showed a clear seasonality. In general, maximum growth and production occurred in early summer (July), and maximum biomass was reached between July and September. Biomass, shoot density, growth and production showed clear minima in winter.

Problem

Estimation of primary production of seagrasses has been a routine part of littoral ecosystem research since the pioneering works of ZIEMAN (1974), and the literature is extensive (see reviews in PHILLIPS & McRou, 1980; HILLMAN et al., 1989; DUARTE, 1989). Similarly, great attention has been paid to evaluating the production of Mediterranean species. There are extensive data on the large species Posidonia oceanica (On, 1980; BEDHOMME et al., 1983; THBLIN & GIORGI, 1984; BAY, 1984; W ~ M A N N , 1984; ESTEBAN, 1989; ROMERO, 1989a; PERGENT et al., 1989; BUIA et al., 1992), but data on the production of Cymodocea nodosa, another common species in the Mediterranean (DEN HARTOG, 1970), are scarcer (GESSNER & HAMMER, 1960; DREW, 1978; PEDUZZI & VUKOVIC, 1990; VAN LENT et al., 1991; TERRADOS & Ros, 1992). Few studies include a survey of C. nodosa production over a yearly cycle.

Consequently, field research was carried out with the following objectives: (i) to evaluate the annual primary production of Cymodocea nodosa; (ii) to establish the seasonal pattern of production and the allocation of biomass to the

U. S. Copyright Clearance Center Code Statement: 0173-9565/94/1501-OOSl$lO.OO/O

52 P ~ R E Z & R O M L K ~

different parts of the plant: (iii) to estimate the amount of nutrients involved in this production.

Material and Methods

1. Study site

The stud) was performed in the Alfaques Bay. in the southern part of the Ebro Delta (Fig. 1) during the years I086 to 1988. This ha) has regular freshwater inputs and a permanent communication with the open sea. Its total area is about 50 km'. with a central basin having an average depth o f 4 m and shallon. ca. i m deep platforms surrounding it. The bathymctric range of C. nodosn is from 0.3 to 3 m. although the bulk of thc plant biomass and cover is between 0.5 and I m. More details on the hkdrograph) and other features of the bay can be found in CAMP & D~I .GADO (1987). CAMP ('I a/. (19c)I). and VIDAI ct ( I / . (1992).

A pcrniancnt sampling station was set up in the NE part of thc bay (see Fig. I ) . at a mean depth of 0.8 in. Lvhcre all the experiments and measurements described were performed. This part o f the 1x1). IS not directly affected by the freshnater inputs. as s h m n by the salinity data (see below).

Fig. 1 . Stud! site. located in the southern bay of the Ebro Delta (east of the Iberian Peninsula). Seagrass meadows: black areas; permanent station marked by an arrow.

Primary production in Cymodocea nodosa 53

2. Environmental parameters

Temperature, salinity, and nutrient concentration were measured at least monthly using standard methods (GRASSHOFF et al., 1983). Aerial irradiance was recorded continuously throughout the year (pyranometer Kipp & Zonen CM.5). These data were then converted to underwater quantum irradiance using an empirical factor, as described in PBREZ & ROMERO (1992).

3. Biomass

Biomass was estimated by random sampling of three 1600cm2 quadrats each month. An iron frame was pushed into the sediment; first, all the leaves of the plant falling within the quadrat were cut off, and then the rhizomes were collected. Since most of the fragile roots were lost during this process, three additional samples were taken using a corer device, 16cm in diameter, pushed into the sediment to a depth of 30cm. The sediment cylinder obtained was then thoroughly rinsed and the root material separated from faunal or detritic components.

In the laboratory, the three fractions (rhizomes, roots, and leaves) were dried (llO"C, 24 h) and weighed.

4. Production

The biomass increase of the plant can be allocated to: (i) leaf elongation, (ii) new shoot appearance, and (iii) increase in the belowground biomass (roots and rhizomes). Each part was studied separately.

Leaf' elongation was measured using the classic punching method (PARKE, 1948; ZIEMAN, 1974; McRov & HELFFERICH, 1977; DENNISON, 1990). Thirty shoots were marked each time; all the leaves within a shoot were marked simultaneously using a thin needle at the level of the top of the leaf base of the outermost leaf. The marked shoots were collected after an interval of ca. 30 days. In the laboratory, the shoots were separated from their epiphytes by scraping, and then sorted into three fractions: leaf bases, new tissue (produced during the marking interval), and old tissue. Each part was dried and weighed separately. Other features of these shoots were also recorded (total number of leaves, new leaves, etc.).

In order to assess shoot recruitment and shoot death, three fixed quadrats of 30 X 30cm divided into 10 x lOcm subquadrats were established in the study area, and the number of shoots inside them was recorded monthly.

Rhiiome growth was measured using the finding of CAYE & MEINESZ (1985) that groups of long and short internodes alternate along the C. nodosa rhizomes. The short internodes correspond to winter growth, while a more active elongation during spring-summer leads to longer internodes. Thus, the portion of the axis produced in a given year can be determined from the apical meristem. Nevertheless, since most of the rhizome fragments within a random sample are not connected to their apical meristems, we used an alternative method for rhizome dating based on counting leaf scars on the vertical shoots. Our data showed the appearance of, on average, 13 leaves per year and shoot (see results), so the number of scars divided by 13 is an estimation of the shoot age in years. When possible, both methods were applied; they were in excellent agreement. The data of rhizome biomass distribution in annual cohorts showed a weight decline beginning in the first year of life (see results); thus, we estimated annual rhizome production as the biomass of the cohort of the actual year (September samples). Production in the form of roots was obtained from root biomass data, assuming an identical turnover time for roots and rhizomes. Since a very high variability was found in the monthly sampling of root and rhizomes, additional samples were taken (n = 10) in order to estimate their production; this was done at the moment of maximum development of belowground parts (late summer).

54 PBREZ & ROMERO

5. Chemical elementary composition

40

- 9 30 Y

; 5 20

; 0

10

0

Subsamples of roots. rhizomes. and leaves wcre dried at 70 'C, finely grounded, and then used for C-N-P content determination. The C-N content was determined by a Carlo-Erba autoanalyzer. The P content was detcrmined by ICP (induced coupling plasma) after an acid wet digestion in a microwave oven (see JACKSON. 1970. and modifications in MATEO & SABAIB, 1993).

b *

- /*--\,

/* \* i \*

/* ' 0

-

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1 ' 1 1 1 " 1 1 " '

Results

1. Environmental parameters

Environmental features of the study site are summarized in Figs.2 and 3 . Temperature variations are large due to the shallowness of the site, with minimum monthly average values of 10°C in winter (occasionally, 6°C was recorded) and maximum averages of 30°C in summer (up to 32°C). Total irradiance ranged between 400 W . m-? (June) and 100 W . m-2 (December), corresponding approximately to 2000 and 600 pmoles . m-2. s-I, respectively (PAR irradiance at the plant level). More details on the underwater light regime are given in PEREZ & ROMERO (1992).

r l a

Primary production in Cyrnodoceu nodusa 55

2 5

2 0

15 z Y

w '0 I z

5

0

1.0

0.8

- 0.6

0.4 5 Y

2 0.2

0.0

0 water column pore water

J F M A M J J A S O N D

0 water column 0 pore water

I I I I I I I I I I I I

J F M A M J J A S O N D

a

b

Fig. 3. Nutrient concentrations in both the water column and the pore water during a seasonal cycle (year 19%). a. Ammonium; b. Phosphate.

The nutrient concentration in the water column showed no clear seasonal trends and was in general higher than in adjacent Mediterranean coastal waters, but lower than in other estuarine areas (CARRADA et al., 1980; KENNISH, 1986). The nutrient concentration in the pore water was higher than in the water column, and a depletion appeared at the end of the summer, possibly due to the very high plant growth during previous months.

Salinity (not represented) remained fairly constant throughout the year, with an average value around 35 "/w and departures from the mean of less than 2 %o.

2. Seasonal pattern: shoot features

All shoot features showed a well-defined seasonal pattern, indicating, in gen- eral, a high degree of activity in late springlearly summer and an almost quiescent phase during winter. The number of leaves increased from 2 (winter) to 4 (summer; average values), and the rate of leaf formation was higher in summer (Fig.4). During winter, no new leaves appeared in the shoot; leaf appearance began in spring, with a maximum in summer and a decline in autumn. This indicates that the life span of winter leaves was high (ca. 200

56 PBREZ & ROMERO

days), while it shortened towards summer ( 3 M 0 d ) and increased again in autumn (80d). An average shoot produced a total of 13 leaves per year, which gives an average plastochrone interval (sensu PATRIQUIN, 1973) of 28 days (see Fig. 4).

1 9 8 7 1988

M A M J J A S O N D J F M A M J J A I

I L

F i g . 4 Life span of individual leavcs on an average C. nodoscz shoot. Each leaf is rcprescntcd by a horizontal line. beginning un the date of leaf appearance and ending on the date of leaf fall.

The individual weight of shoots also peaked in summer, resulting both from leaf number and from leaf length increase (Fig. 5a) .

Leaf growth reached its maximum in June-July (Fig. 5 b), with values up to 1.4mg DW.shoot - I .d - ' , and decreased in late summer and autumn to a minimum value in winter (0.2 mg DW * shoot-' . d-l). A similar seasonal pattern uas found in turnover rates (production to biomass ratio or biomass-specific growth rates: see Fig. 5 c).

3. Biomass and production: stand features

The seasonal pattern of standing leaf biomass resulted from both the shoot biomass change and the increase or decrease in the meadow density. The minimum number of shoots (about loo0 shootsem-') was found in winter (Fig. 6 a), as a result of autumn shoot mortality, and the maximum was reached i n summer (about 2000 shoots. m-?) following the recruitment of new shoots during late sprindearly summer. Leaf standing biomass varied from very low winter values (20-50 g DW . m- ?: see Fig. 6 b) to 150-200 g DW . m -* in July/ August (depending on the year). Although less pronounced, the same trend was found in belowground biomass, revealing an active rhizome growth and branch- ing (reflected in the larger internodes) during spring. Root biomass was very high throughout the year, and a maximum value was reached in summer.

Primary production in Cyrnodocea nodosa 57

2o 0

b

C

1986 1987 1988 Fig. 5. Some features of individual shoots during the seasonal cycle. a. Shoot weight; b. Absolute shoot growth rates; c. Biomass-specific shoot growth rates. Vertical bars are standard errors.

Summer values for both rhizome and root biomass were 248 f 15 g DW . m-2 and 148 k 13 g DW . m-*, respectively (standard error of the mean, n = lo).

Shoot growth (as weight of new parts) is correlated with shoot size (as total dry weight; correlation coefficients between shoot growth and shoot weight were significantly different from zero at the 5 % level in 20 out of 22 cases). Consequently, in order to estimate leaf production of the plant, the PA3 ratio was computed at each sampling interval for the marked shoots, and then multiplied by the biomass obtained in the quadrats of the same sampling event; this approach is similar to the method of VAN LENT et al. (1991). When

3000 I

2500 - 2000 - 1500 - 1000 -

500 0 & 300

250 1

A M J J A S O N O J F M A M J J A S O N D J F M A M J J A S

0

b

1986 1 9 8 7 1988 Fig. 6 . Some featurcs of thc c'. nodow stand during the seasonal cycle. a. Shoot density; b. Leaf biomass: c. leaf production. Vertical bars are standard errors.

appropriate (spring-summer), the biomass of the new shoots was added, but this quantity rarely exceeded 10% of the total. An alternative procedure, consisting of computing the average production per shoot and multiplying it by shoot density, was also considered but rejected since (i) the underwater count- ing of shoot density was subject to large errors and (ii) P/B and biomass data showed much lower variance than production per shoot and shoot density. Results obtained are shown in Fig. 6 c and follow the basic pattern described above: during winter, production was very low, rising slowly in early spring and increasing dramatically in May-June; from August to October, production decreased again.

Primary production in Cymodocea nodosa 59

The results of rhizome dating (Fig. 7) suggest mortality and rhizome loss from the first year of life; the annual rhizome production was 118 g DW * m-*. ax1. Root production, as derived from rhizome P/B (0.48 ax1), gives an estimate of 71 g DW - m-2 * ax1.

T - - - - -

120

100

80

60

40

20

0

Fig. 7. Age distribution of rhizome weight. Samples were collected in August. Horizontal axis is expressed in time before collection. Vertical bars are standard errors.

Selected meadow features are presented in Table 1, their seasonal changes in Figs. 5 and 6. The seasonal growth pattern and phenology of Cymodocea nodosa clearly has two contrasting phases. Winter is an almost quiescent phase, since both dynamic descriptors (rhizome growth, shoot recruitment, leaf elongation, and leaf formation rate) and static descriptors (shoot density, biomass, number of leaves per shoot) are at their minima. Summer is the moment of maximum plant activity, when active leaf and rhizome growth (and, in consequence, shoot recruitment) leads to very high biomass values.

Table 1. Summary of features of C. nodosa growth, production, and leaf area index.

max. production P/B biomass

g DW.m-2 g DW.m-2.a-1 ax1

leaves

rhizomes roots

~

1986 197 456 2.3 1987 156 368 2.5 1988 208 438 2.2 1988 248 118 0.48 1988 148 71 (0.48)

LA1 1986 4.7 -

1987 3.1 - 1988 4.5 -

60 PBKEZ & ROMERO

4. Nutrient content of plant tissues

50

40

30

$ 2 0

C

f 0

10

0

The C, N, and P content of leaves, rhizomes, and roots are shown in Fig. 8. A seasonal pattern appears for both N and P, with lower values in summer than in winter. while the C content remains more or less constant. Nitrogen and phosphorus values are higher in the leaves than in the belowground parts.

- A/A

O.L,L:+g - \. '.-,#.-. - leaves

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1 1 1 1 1 1 1 1 1 1 1 1

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.'.I .I0\ -.--/ .'. - :=-\...-. /'=, /I7

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./ A.~-A-A-A '. I I 1 1 1 I I I

Primary production in Cymodocea nodosa 61

Discussion

Although high growth plasticity has been reported for this species (PEREZ et al., in press), our results are consistent with those reported in previous works (CAYE & MEINESZ, 1985; PEDUZZI & VUKOVIC, 1990; TERRADOS, 1991; VAN LENT et al., 1991), i. e., with regard to month of maximudminimum growth, number of leaves produced, seasonality of shoot density, etc. This suggests a certain geographic uniformity in the general growth dynamics of this species, which can be attributed either to a robust internal growth programme or to the depend- ence of this rhythm on factors that do not vary on a regional scale (i. e . , within the Western Mediterranean). A seasonality close to that described in this paper has also been found in other temperate species (i. e. , Zostera marina: SAND- JENSEN, 1975; STEVENSON, 1988), and is a relatively common feature in most seagrass species according to DUARTE (1989). The peak biomass (and frequently peak growth) during July-August seems to be a consequence of a growth cycle mainly controlled by light/temperature, as we demonstrated for C. nodosa in our study site (PBREZ & ROMERO, 1992).

Comparing our data to those of tropical Cyrnodocea species (BROUNS, 1987) reveals a similar seasonal pattern, though with some differences. The tropical species show: (i) maxima shifted towards autumn due to different environmen- tal constraints, such as the monsoon; (ii) less marked seasonality (for example: the ratio minimudmaximum leaf biomass is 0.6 for tropical species, while in this paper we report values around 0.25); (iii) higher values of primary produc- tion, leaf appearance rate, etc., probably due to a longer growing season. This confirms the importance of latitudinal constraints on the control of certain features of seagrass growth (DUARTE, 1989).

Conversely, C. nodosa seasonality differs greatly from that described in Posidonia oceanica, in that maximum production occurs in early spring or even in winter (Om, 1980; ROMERO, 1989 a; BUIA et al., 1992). The factors that govern Posidonia seasonality are not known although an internal rhythm has been described (On, 1979). This suggests a certain independence from external factors in Posidonia; the growth rhythm of C. nodosa, in contrast, is subject to tighter environmental control. Thus, factors others than latitudinal situation, such as evolutionary history, may control the general growth pattern of sea- grasses.

The primary production of C. nodosa is relatively low compared with other seagrass species (HILLMAN et al., 1989). This is also true for the P/B ratio, and these values seem to be a local characteristic of our C. nodosa stand. TERRADOS & Ros (1992) found similar low values in a coastal lagoon, while P/B ratios reported from other areas (PEDUZZI & VUKOVIC, 1990; VAN LENT et al., 1991) are higher. This suggests an additional limiting factor (nutrients). There is indirect evidence of growth limitation by phosphorus in our stand: low P concentration in leaves, especially at the period of maximum growth (see Fig. S), well below the values considered critical by DUARTE (1990); phosphate depletion in pore water during peak summer growth (see Fig. 3) ; and unusually high C : P and N : P ratios (see Fig. 8). This limitation has also been demon- strated experimentally (PEREZ et al., 1991). A similar nutrient limitation (involv- ing both nitrogen and phosphorus) has also been reported by TERRADOS (1991),

62 P6RF7 & ROMERO

while the data of PEDUZZI & VUKOVIC (1990) and VAN LENT et al. (1991) indicate a less severe nutrient limitation.

The ratio of belowground biomass : aboveground biomass is high in our stand, with values of 2.2 in the summer months and up to 8 in winter. The value of this ratio has been linked to the degree of hydrodynamism (PEDUZZI & VUKOVIC:, 1990) and to the nature of the sediment or its nutritional capacity (ZIEMAN & WFTZEL, 1980). In our case, the very high root biomass should be attributed to a maximization of root nutrient absorption, since in the northern shore of the bay (see Fig. 1) where phosphorus levels are high, root biomass is extremely low, and roots are mainly unbranched; in contrast, roots in our study site are densely branched (see P ~ R E Z et id., in press).

Finally. a comparison of the present data with that of other key Mediterra- nean seagrass species (Posidonia oceanica) reveals great differences (see Table 2). In general, C . rzodosa has growth features of “opportunistic” species,

Table 2. Comparative data on growth and production of Posidonia oceanica and Cymodocea nocfosa. Data for C. nodosa are exclusively from this paper. Data for P. oceunica are mainly from KohrFRo (I989 a and b) and include results from other studies quoted in the introduction.

Cymodocea notiosa Posidonia ocaanica

leaf biomass turnover (a-I) 2.2-2.5 rhizome biomass turnover (a-I) 0.40 max. shoot weight (mg’shoot-I) 80-100 leaves per growth cycle 13 plastochrone interval (days) 28 leaf life span (days) 30-200 shoot longevity (years) 6 ( 8 )

1.5-1.9 0.074.1 I 670-850

7-8 40-50

140-340 >30 (?)

while P. oceanica shows characteristics of “late successional” species (following the criteria of LITTLER & LITTLER, 1980, for macroalgae). This conclusion is consistent with the known autoecology of these seagrasses (DEN HARTOG, 1970) and with the successional relations among them (P~REs, 1982).

Summary

Data on growth rhythm, primary production, and nutrient content in the different parts of the plant from a Cymodocea rzodosa stand are presented. A clear seasonality is evidenced, with maximum values of biomass, growth, production, rhizome growth, and shoot recruitment during summer months. The range of values found for selected variables are: leaf standing crop: 20-208 g DW . m-?; total net primary production: 0.2-3.8 g DW . mP2. d-’; shoot density: 1000-2000 shoots. m-?; daily P/B: 0.0054.02. The stand studied is subject to limitation of growth by phosphorus, which explains relatively low P/B values and other plant features, such as the high ratio belowground biomass/above- ground biomass. Comparison of the general features of the Cymodocea nodosa seasonal growth pattern with other species (mainly Posidonia oceanica) seems

Primary production in Cymodocea nodosa 63

to confirm the pioneering-colonizing role of this species in Mediterranean shallow benthic ecosystems.

Acknowledgements

The support and advice of JORDI CAMP throughout the field work and in later stages has been of invaluable help. The work was funded by CICYT grant no CE89-0017.

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