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Reproductive phenology of the Mediterranean seagrasses Posidonia oceanica (L.) Delile, Cymodocea nodosa (Ucria) Aschers., and Zostera noltii Hornem.
Aquatic Botany, 40 ( 1991 ) 343-362 Elsevier Science Publishers B.V., Amsterdam
343
Reproductive phenology of the Mediterranean seagrasses Posidonia oceanica (L.) Delile, Cymodocea nodosa ( Ucria ) Aschers., and Zostera noltii Hornem. M.C. Buia and L. Mazzella Laboratorio di Ecologia del Benthos della Stazione Zoologica "A. Dohrn "' di Napoli, 80077 lschia, Italy (Accepted for publication 14 February 1991 )
ABSTRACT Buia, M.C. and Mazzella, L., 1991. Reproductive phenology of the Mediterranean seagrasses Posidonia oceanica (L.) Delile, Cymodocea nodosa ( Ucria ) Aschers., and Zostera noltii Hornem. Aquat. Bot., 40: 343-362. Investigations on the sexual reproduction of Posidonia oceanica (L.) Delile, Cymodocea nodosa (Ucria) Aschers. and Zostera noltii Hornem. were conducted in situ from 1979 to 1988 in beds around the island of Ischia. Seed germination and phenological features of seedlings of P. oceanica and C. nodosa were observed in situ and in the laboratory. The reproductive cycles showed, for each species, different timing of start and duration of flowering, fruiting and germination. Posidonia oceanica flowers always appeared in September in shallow stands and in November in stands deeper than 15 m. This time delay seems to be related to the different maximum summer temperatures found at those depths. This species did not show dormancy. Cymodocea nodosa flowering was always recorded after the mini mum winter temperature (April-May); germination of the seeds followed after 8-10 months of dormancy. Zostera noltii flowers were always recorded in July, with fruiting in August. The life cycles of these species seem to be related to the annual temperature range rather than to other environmental parameters. The different reproductive strategies adopted by each species are discussed.
INTRODUCTION
The most common seagrasses in the Mediterranean Sea are Posidonia oceanica (L.) Delile, Cymodocea nodosa (Ucria) Aschers., and, in restricted shallow areas, Zostera noltii Hornem. Zostera marina L., unlike the situation along the Atlantic and Pacific coasts, is confined to brackish waters such as deltas or the north Adriatic Sea. Posidonia oceanica forms the largest and the most widespread beds, representing one of the most productive mediterranean ecosystems (Boudouresque et al., 1984, 1989). Meadows of C. nodosa are the second largest in 0304-3770/91/$03.50
© 1991 - - Elsevier Science Publishers B.V.
344
M.C. BUIA AND L. MAZZELLA
extent (Simonetti, 1972-73; Buia et al., 1985d). Zostera noltii, which colonizes the tidal zones on the Atlantic European coasts (Jacobs, 1982 ), reaches a depth of 5 m in the Mediterranean. It rarely forms monospecific meadows and mixes mainly with C. nodosa, which represents the dominant taxon and is the first species to colonize the substratum (Buia et al., 1985e). Mixed meadows, consisting of the two species and the green alga Caulerpa prolifera (Forssk.) Lamouroux, also occur frequently (Meinesz and Verlaque, 1979; Meinesz and Simonian, 1983; Pirc et al., 1983 ). The three species differ in morphological and phenological features, and hence their systems differ in structure and dynamics. Cymodocea nodosa is considered the pioneer species of Posidonia oceanica beds, the latter species forming the 'climax' stage. When P. oceanica beds regress, C. nodosa often replaces them (Molinier and Picard, 1952; den Hartog, 1977); as a result, P. oceanica, C. nodosa, and Z. noltii do not form mixed persistent stands. A large amount of data has been accumulated about the Posidonia ecosystem (for a review, see Boudouresque et al., 1984, 1989). Much less is known about the ecology and sexual reproduction of C. nodosa and Z. noltii (Caye and Meinesz, 1985a; L. Mazzella, G.F. Russo and M.C. Buia, unpublished data, 1985 ). The reproduction phenomena of P. oceanica have been observed in both the northern and southern parts of the Mediterranean and are related to the different latitudes (Giraud, 1977; Cooper, 1979; Giraud et al., 1979; Giaccone and Calvo, 1980; Cinelli and Salghetti-Drioli, 1983; Caye and Meinesz, 1984a; Gambi et al., 1984; Mazzella et al., 1984; Thelin and Boudouresque, 1985; Thelin et al., 1985). The first study on the sexual reproduction of C. nodosa with a description of flowers, seeds and seedlings was conducted by Bornet in 1864, but only recently has the reproductive cycle of this species been studied in relation to the structure of the meadow and to several environmental factors (Mazzella et al., 1983-84; Caye and Meinesz, 1985a; Buia et al., 1985c; Pirc et al., 1986 ). Little information on the flowering of Z. noltii is available for the Mediterranean Sea; data have been reported for the north Adriatic, the Island of PortCros (Gulf of Hybres ) and the Island of Ischia ( Gulf of Naples ) ( Benacchio, 1938; Simonetti, 1972-73; Caye and Meinesz, 1984b; Buia et al., 1985b). The morphology and life histories of these three species are related to environmental factors (e.g. light regime, hydrodynamic force, temperature) of the habitat where they form beds. Sexual reproduction is crucial not only in maintaining genetic diversity, but as a species dispersal mechanism. The aim of the present study was to characterize the features of the sexual reproduction of these plants and to clarify their life cycle. Pluriannual investigations on the sexual reproduction of the three species were conducted in situ from 1979 to 1988 in beds around the Island of Ischia. Germination and the phenological features of seedlings ofP. oceanica and C. nodosa, were stud-
REPRODUCTIVE PHENOLOGYOF MEDITERRANEANSEAGRASSES
345
ied in situ and in the laboratory. The reproductive cycles of the three plants are described and an attempt is made to identify the strategies adopted by each of them in relation to environmental parameters. STUDY AREAS A N D M E T H O D S
Study areas The areas studied around the Island of Ischia are shown in Fig. I. Posidonia oceanica forms the most extensive beds surrounding the island from a depth of 1 to about 38 m (Colantoni et al., 1982). Cymodocea nodosa is found mainly along the coasts exposed to the north, where it forms separate meadows down to a depth of 6 m and from 10 to 21 m (Buia et al., 1985d). Zostera noltii occurs down to a depth of 5 m, always mixed with C. nodosa, mainly in meadows adjacent to ports. The sexual reproductive cycle of P. oceanica was observed in three beds: Lacco Ameno, San Pancrazio and La Nave (Fig. 1 ). At Lacco Ameno, the beds face north-northeast and extend from a depth of 1 m down to 35 m over a distance of 600 m (Mazzella et al., 1986). From 1 to 20 m the plants occur on a 'matte' (a terrace formed by P. oceanica roots and rhizomes and en1 P. V i c e 2 Lacco Ameno 3 Fungo 4 S. P F e t r o
5 Castello
Aragonese
6 P. S. P a n c r a z l o
7 La N a v e 8 S. M o n t a n e
,,--;,---8 ,.-f :I
,. ",
7'
0
,
"J
',,
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10 K m
.
~ "",.--,..
[ ] P. o c e a n i c a [ ] C. nodosa [ ] Z. n o l t i i
,,--?
~ "". . . . . . "! ,sq. ,,' ','-:"'"" "'"?-',,
-,:,:
,/'f ,.
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-:
PLES
....
Fig. 1. Distribution of Posidonia oceanica, Cymodocea nodosa and Zostera noltii around the Island of Ischia (Gulf of Naples, insert) and location of the sampling sites.
346
M.C. BUIA A N D L. MAZZELLA
trapped sediment, as defined by Molinier and Picard, 1952), and, at greater depths, on sand. At San Pancrazio, the bed is exposed to the south; it is found between 10 and 35 m and grows on a 'matte' throughout its length (Colantoni et al., 1982). At La Nave, P. oceanica occurs between 15 and 30 m with a patchy distribution, growing on rocky substrate throughout (Mazzella et al., 1984). The C. nodosa meadows studied were mostly in shallow waters, within a depth of 6 m (Castello Aragonese, San Pietro, Lacco Ameno and Fungo ); the San Montano m e a d o w occurs at 15 m (Fig. 1 ). The Castello meadow, formed only by C. nodosa, occurs on a sandy substratum. It is relatively protected from water movement, and grows in a channel within a P. oceanica bed (see Fig. 1 ) that is implanted on a 1 m high 'matte'. The Fungo and Lacco Ameno meadows occur at a depth o f 2 m (Fig. 1 ). The former is near the small barbout, and the latter lies behind a m a n - m a d e cliff that separates the harbour from the open sea. Both meadows are mixed with Z. noltii and both occur on a m u d d y sediment. The San M o n t a n o m e a d o w grows on a coarse sandy sediment, between the upper limit of a deep P. oceanica bed and the rocky shore, and has a very low shoot density (Fig. 1 ). The m e a d o w of San Pietro occurs between depths of 1.5 and 4 m in an area protected by artificial cliffs. It mainly grows on 'turf' (a terrace formed by C. nodosa and Z. noltii roots and rhizomes and entrapped sediment, as defined by Buia et al., 1985e) with a m u d d y - s a n d y sediment (L. Mazzella, G.F. Russo and M.C. Buia, unpublished data, 1985 ) and partially on sandy substratum (Fig. 2 ). In this meadow, C. nodosa is mixed with Z. noltii, which shows a patchy distribution and is not present in the shallowest part of the m e a d o w (Buia et al., 1985e). 4.0 m
Fig. 2. Map of the San Pietro meadow and location of the four study sites (A,B,C,D).
REPRODUCTIVE PHENOLOGY OF MEDITERRANEAN SEAGRASSES
347
Methods The reproductive phenology ofP. oceanica was studied from 1979 to 1988. During these years, flowering and fruiting in the above-mentioned beds were recorded. In the beds of Lacco Ameno and San Pancrazio, stations were established along depth transects in relation to the appearance of flowering shoots, and the frequency of flowers per square metre (five replicates for each stand) was calculated. Germination experiments were conducted with mature P. oceanica seeds collected at the end of May 1987 on the shoreline of the Amalfi coast (Gulf of Salerno). They were kept in aquaria with running sea water at ambient temperature and light conditions. Growth and phenological parameters of seedlings (mean number of leaves and roots per shoot, length and width of leaves of different classes, length of roots) were recorded bimonthly from germination (May 1987 ) until January 1988. The reproductive phenology of C. nodosa was studied from 1982 to 1988. The appearance of flowers, fruits and seeds in the different meadows during these years was recorded. Methods to determine flower, fruit and seed density, and the microdistribution of male and female flowers, have been described previously (Mazzella et al., 1986). In the San Pietro meadow, four stations were established along a depth transect between 1.5 and 4 m (Buia et al., 1985d) (Fig. 2). The density of C. nodosa and Z. noltii was measured at each station. Germination of C. nodosa seeds, collected in 1985 in meadows at different latitudes (Castello, San Pietro, Lacco Ameno for the south Meditteranean and Antibes for the north Meditteranean), was also studied in the laboratory at ambient light and temperature conditions, and the phenological features of seedlings were measured (e.g. number of leaves per shoot, length and width of leaves, number of roots per shoot, length of roots). Differences in leaf phenology of the seedlings and in the length and width of seeds were statistically tested (ANOVA). The occurrence in situ of flowers and fruits of Z. noltii was recorded from 1984 to 1988 in the San Pietro meadow (Fig. 2). In 1984 and 1985, the density and the microdistribution of the inflorescences were measured in situ using the methods described above for C. nodosa. RESULTS
Reproduction ofPosidonia oceanica Posidonia oceanica flowering (Fig. 3) has occurred every year since 1979 (Mazzella et al., 1982; Mazzella et al., 1983; Mazzella et al., 1984). However, the intensity of flowering varied year by year and along depth transects in the shallow and deep stands of the same beds (Table 1 ). Flowering shoots have a patchy distribution (data not presented) and stands at the same depth never
348
M.C. BUIA AND L. MAZZELLA
Fig. 3. Early developmentalstage of the Posidonia inflorescence(size bar, 0.3 cm ). appeared to flower in successive years. Many dead inflorescences at an initial fruiting stage were often found (Table 1 ). In shallow stands (down to 15 m ) a low frequency ofinflorescences was followed by 2 years of high density (Table 1 ). In deep beds, fruiting showed alternate yearly maxima and minima. A high abundance of flowers in one area often corresponded with a high abundance in other Mediterranean areas (French coast and south Italy) (Frad~ Orestano et al., 1989; G. Pergent, personal communication, 1988 ). Between shallow (down to 15 m) and deep stands (from 15 to 28 m ) , Posidonia oceanica showed a persistent phase-difference, whereby there was a flowering delay of about 2 months in the deep meadows (Fig. 4 ). In the shallow meadows the first flower buds, borne by a short stalk, were usually recorded in September, and on rare occasions at the beginning of October. In the deep meadows this stage was observed in November or at the beginning of December. Anthesis occurred in October in the shallow waters and in December in the deep stands. Fruits developed from December to March-April in the shallow stands, and from February to May-June, sometimes to July, in the deep stands (Fig. 4). At both depths, flowering was recorded a month after the m a x i m u m water temperature, measured in August for the shallow waters (25°C, as the average of 3 years) and in October at a depth of 20 m ( 22.5 ° C ) below the s u m m e r thermocline (Fig. 4 ). Germination in the laboratory under ambient light and temperature levels,
REPRODUCTIVE PHENOLOGY OF MEDITERRANEAN SEAGRASSES
349
TABLE1 M i n i m u m a n d m a x i m u m values of d e n s i t i e s of flowers (flowers per square m e t r e ) a n d fruits (fruits per square raetre) ofPosidonia oceanica from 1981 to 1988 in shallow a n d deep s t a nds of three beds: Lacco Ameno, San Pan crazio, a n d La N a v e Lacco A m e n o Shallow
San P a n c r a z i o Deep
La Nave
Shallow
Deep Deep
1981-1982 Flowers Frmts
-
0-3
-
0-2
3-28
-
1-25
0-5
-
1-18
1982-1983 Flowers Fr uits
9-15 -
10-30
•
•
-
-
1983-1984 Flowers Fruits
0-13 0-4
0-2 .
0-7 .
.
.
1984-1985 Flowers Fruits
0-2 - -
*
-
-
-
,
~
_
_
1985-1986 Flowers Fr uits
0-94
0-25
-
0-1
0-1
0-40 0-2
0-2 0-2
-
0-3 -
0-69 -
0-38 0-2
0-41 0-1
, ,
, -
, -
1986-1987 Flowers Fruits
1987-1988 Flowers Fr uits
*Only occurrences of flowers a n d fruits.
occurred a few days after the seeds were collected (end of May). This finding excludes dormancy. Of the total of 57 seeds, 40 (70%) germinated, and from these only 11 (28%) survived to the end of the experiment (January). The m a x i m u m mean number of leaves per shoot (seven) was reached in summer. The leaf length per leaf class increased during the experiment with the maxim u m occurring in January (Fig. 5 ). The mean width varied between 0.2 and 0.35 cm in August, and between 0.46 and 0.53 cm in January. The m a x i m u m length and width was reached by the youngest leaves, which indicates a differential growth for leaves of different ages. In particular, in June and August the second leaf was the longest ( 3.52 + 0.51-7.11 _+0.95 ), and in November and January, the third leaf was the longest ( 11.68 + 2.74-13.48 + 3.34 ). The number and length of roots showed the same increasing pattern from June to January, in accordance with the seedlings age (Fig. 5 ).
J
:
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:
M
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~
-
A
~
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M
-
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°
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A
-
-
~
S
0
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-
o
Fig. 4. Diagramatic representation of the reproductive cycles of Posidonia oceanica, Cymodocea nodosa and Zostera noltii in the south Mediterranean area and mean annual variations in water temperature (as average of 1984-1986 records at the surface and at 20 m depth).
i,i
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R E P R O D U C T I V E P H E N O L O G Y OF M E D I T E R R A N E A N SEAGRASSES
o Z
15_
15
10
10 "~
i' 0 JANJ
.J=
Z NJAN
U,I
~
!Innn JANJ
1234567891011
Z
Leaf
o
Month
Fig. 5. Leaf and root growing trends of Posidonia oceanica seedlings kept in the laboratory at ambient temperature and light conditions (mean _+confidence limits); (the youngest leaf is indicated as 1 ).
Reproduction ofCymodocea nodosa In the meadows under study (in shallow waters ), the first flower buds were recorded at the end of April, when the water temperature started to rise after the annual minimum (Fig. 4 ). In April the flowers were mainly hypogean and sheathed. In May, both male and female flowers were easily recognizable in situ, the stamens being on the stalk that at this time was elongated, and the pistils showing the filamentous stigmata rising from the leaf sheath (Fig. 6 ). The first mature fruits, still attached to the mother plant, were found at the end of July or beginning of August (Mazzella et al., 1983-1984). The seeds were dormant, buried in the sediment until germination started in April, coinciding with a rise in water temperature after the winter minimum (Fig. 4 ). The maximum germination rate was recorded in June (present study) or in July (Pirc et al., 1986). Since the start of our study in 1982, Cyrnodoceahas had a high fecundity. Staminate and pistillate flowers, fruits and seedlings were collected in each of 7 years in some of the meadows studied. Table 2 shows the vegetative and reproductive shoot density recorded in four stations of the San Pietro meadow in June and July 1984. The highest total flower density usually coincided with the maximum shoot density; however, male and female flowers differed in density in the same station. In June, the total amount of flowering shoots was higher in the deeper stations and decreased towards the coastline. A similar
352
M.C. BUIA AND L. MAZZELLA
F i g . 6. M a l e ( o n t h e l e f t ) a n d f e m a l e
(on the right; arrow indicates the stigmata)
flowers of
Cymodocea nodosa ( s i z e b a r , 1.8 c m ) .
TABLE 2 D e n s i t y ( n u m b e r s p e r s q u a r e m e t r e ) o f Cymodocea nodosa a n d Zostera ers, f r u i t s , s e e d s a n d s e e d l i n g s in t h e S a n P i e t r o m e a d o w in 1 9 8 4
noltii v e g e t a t i v e s h o o t s , f l o w -
Zostera noltii
Cymodocea nodosa Vegetative shoots
Female flowers
991 1176
99 -
1062 722
Male flowers
Fruits
Seeds
Seedlings
Vegetative shoots
Flowers
-
113
127 340
71
1020 991
-
85 -
85 -
142
340 227
14 28
821 1119
-
623 510
42 -
. -
-
-
1232 1076
57
864 1331
3 -
. -
-
-
Station A June July
Station B June July
Station C June July
.
. 14
.
Station D June July
.
. 28
. 14
. 14
.
353
REPRODUCTIVE PHENOLOGY OF MEDITERRANEAN SEAGRASSES JUNE ST.
1984 ST.
C d' o'
d' d' 4' ~/{ d' o, ~l o' ~' d' d' (¢ o' a' ~ c¢ J d'
d d' ~ 9 9 ? g c~ ?
B
o" o' o'
~/~. c¢c¢'
o'eA ~o,o, o' o' o'
9 g
o'~o,
Fig. 7. Microdistribution of male and female flowers of Cymodocea nodosa w i t h i n a 1 m 2 q u a d rat, divided into units of 12.5 c m × 12.5 c m at Stations B and C in June 1984.
TABLE 3
Germination rate of Cymodocea nodosa seeds collected from different sites Ischia
Antibes
Castello
San Pietro
Lacco Ameno
49
32
31
25
37 (76%)
26 (81%)
27 (87%)
13 (52%)
43 (88%)
29 (91%)
27 (87%)
15 (60%)
13/1/1986 No. seeds
collected
12/5/1986 No. seedlings
germinated
5/6/1986 No. seedlings
germinated
pattern was found for fruits and seedlings in July, and for free seeds, collected in the sediment, originating from the previous reproductive season. Investigations on the microdistribution of flowers (Fig. 7 ), showed patches of male flowers separated from female flowers in stands where flower density was low (Station C). In stations where the flower density was higher (Station B ), patches formed by both male and female flowers were recorded together (Fig. 7). In both stations, the flowers showed a contagious distribution. In fact, the Z 2 values were highly significant (Station B: Z2 total, 59.7; male, 24.9; female, 100; P > 0,5%; Station C: Z2 total, 15.8; male, 21.7; female, 226; P>0.5%). Germination occurred in April-May and reached a maximum in June, in all Ischia meadows. However, comparing the germination of seeds from meadows at different latitudes (Ischia, Gulf of Naples and Antibes, France ),
354
M . C . B U I A A N D L. M A Z Z E L L A
6
I~J Z
10
il nnn ,~25 E o 20 0 .=
,. 15
>. .-I ~
~
,-j
5
o 0
,,- 300
Z
"J 25
23456
2O
6[
10 1511
CSLA
C
i1
S
L
i
I< A
Fig. 8. Leaf growing trends of Cymodocea nodosa seedlings, kept in the laboratory at ambient light and temperature conditions (mean _+confidence limits); (the youngest leaf is indicated as 1).
differences were found in the rates of germination, being lower for Antibes (Table 3 ). Seedling growth patterns are shown in Fig. 8. The mean leaf number per shoot reached a m a x i m u m in July. The mean leaf length for each leaf class showed a constant pattern in each month. Leaf decay began in August. At the end of the experiment, the mean number of leaf scars on the rhizomes was 6 + 1 plus 2 leaves for Castello, 7 _+0.5 plus 3 leaves for San Pietro, 5 + 1 plus 1 leaf for Lacco Ameno and 5 + 0.5 plus 1 leaf for Antibes. Therefore, the mean leaf production of seedlings was again highest for seedlings from the San Pietro meadow and lowest for Antibes. The number of roots on the seedlings increased for each meadow from June to August (Fig. 9), and the Antibes seedlings gave the highest values (4.0 + 1 ). The mean length increased only for seedlings from the Castello and San Pietro meadows, while seedlings from Lacco Ameno and Antibes showed a decreasing trend (Fig. 9 ). Significant differences were also found in the length and
REPRODUCTIVE PHENOLOGY OF MEDITERRANEAN SEAGRASSES
355
6
6
uJ Z 0 tu~
6
.c
6
0
.A
m 0 0 L.
Z
0
0
°f
4
O <
o CSLA
CSLA Meadows
Fig. 9. Growing trends of roots of Cymodocea nodosa seedlings kept in the laboratory at ambient light and temperature conditions (mean +_confidence limits).
Fig. 10. Inflorescence of Zostera noltii (arrow indicates the erect style and stigmata) (size bar, 0.3 cm). width of seeds among the Ischia meadows (Castello, San Pietro, Fungo, Lacco Ameno, San Montano ). Compared two by two, seeds from Castello and Fungo were significantly different from each other and from the other stations for both parameters. Seeds from San Pietro and Lacco Ameno did not show significant differences.
356
M.C. BUIA AND L. MAZZELLA
JULY ST.
1985
B
[] o
----'1
[]
4 7
3
6 9
i Fig. 11. Microdistribution of rhipidia (class density) of Zostera noltii within a 1 rn 2 quadrat, divided into units of 12.5 c m X 12.5 cm at Station B.
Reproduction ofZostera noltii
In the Ischia meadows, Zostera noltii flowers have been observed every year since the first report in 1984, at the end of June (Buia et al., 1985b) (Fig. 10). The stigmata emerge in July from the spatha. Later, the anthers of the same inflorescences release the pollen, thus preventing self-pollination. Flowering spathes can still be found in August, but these are usually smaller. Fruits were usually found in August (Fig. 4). Seeds were never found in the sediment, but seedlings were observed in July. Flowering shoots were present in the central part of the San Pietro meadow (Station C), notwithstanding the high density of vegetative shoots in other stations (Table 2). In July 1985, the flowering shoots in the San Pietro meadow showed a high density, with a contagious distribution, similar to the flowering shoots of C. nodosa (Fig. 11 ). DISCUSSION
The most striking finding of this study is that the reproductive cycles are phased differently in the three Mediterranean seagrasses. In P. oceanica there is an interval of about 8 months between flowering and germination, including 3 months for anthesis and 5 months for the fruit to mature. In C. nodosa the reproductive cycle lasts 12 months, with about 2 months for anthesis and 2 months for fruit development, followed by a period of seed dormancy of 8 months. Therefore, in April both flowers and seedlings are found in the C. nodosa meadow. The complete life history of Z. noltii cannot be constructed from the data available at present. However, seedlings were found in July together with flowering shoots, which suggests the existence of seed dormancy. Our studies in leaf production and biomass (Buia et al., 1985e) demonstrated that, in the Ischia meadows, Z. noltii is perennial, as reported from other areas (Hootsmans et al., 1987).
REPRODUCTIVE PHENOLOGY OF MEDITERRANEAN SEAGRASSES
3 57
This study also shows a difference in the length of the post-fertilization development period between P. oceanica and C. nodosa, with a longer fruit development in the former and dormancy in the latter. Thus, in P. oceanica, a lower vegetative growth in winter (Buia et al., 1991 ), coincides with higher energy costs that last until fruit maturation. Moreover, sexual reproduction can depress leaf growth and production in this season (Panayotidis, 1986 ). Another important difference between P. oceanica and C. nodosa is the success of fruit maturation. Posidonia oceanica usually bore two, or very rarely, four fruits, as against six to eight flowers per inflorescence (Caye and Meinesz, 1984a). In C. nodosa, the two ovaries per flowering unit usually became mature fruits, the latter being always found in couples at the bases of the leaf shoots. Posidonia oceanica and C. nodosa use different strategies for seed dispersal. Our results indicate that C. nodosa seeds remain buried in the sediment for a dormant period of 8-10 months. In P. oceanica, characterized by a very slow vegetative growth (Pirc, 1983; Caye and Rossignol, 1983), the buoyant period of the fruits seems to ensure species dispersion, and avoids competition with the parent plants. By contrast, in C. nodosa sexual reproduction seems to ensure the maintenance of meadow stability: it increases the density, which can vary greatly from year to year, as a result of uprooting in winter and fast rhizome growth and production in spring (Caye and Meinesz, 1985b; L. Mazzella, G.F. Russo and M.C. Buia, unpublished data, 1985). Posidonea oceanica can be germinated with some degree of success in controlled experiments both in situ (Cooper, 1979 ) and in the laboratory (Caye and Meinesz, 1984a; present paper) despite the few records of seedlings in situ (Pergent, 1987; Buia and Piraino, 1989 ). This apparent discrepancy could be due to the mechanism of seed dissemination that results in a high loss of fruits on the shoreline and to the difficulty of finding seedlings in very dense stands. However, the frequent findings of fruits and seedlings in south Italy (mainly along the Sicilian coasts) (Giaccone and Sortino, 1974; Buia et al., 1985a; Frad~t Orestano et al., 1989; M.C. Gambi, personal observation, 1987; S. Piraino, personal observation, 1986; our observations) seem to support the hypothesis that sexual reproduction might influence the species variability and distribution more in this part of the Mediterranean than at other latitudes. The reproductive success of C. nodosa seems also to differ at different latitudes. In fact, we found for Ischia that germination occurred every year, while germination seems to be occasional along the French coast, notwithstanding frequent flowering (Caye and Meinesz, 1985a). Moreover, seed size and seedling features differed between Ischia and Antibes. This morphological variability, already observed by den Hartog (1977) could correspond to different genotypes, as two karyotypes seem to be found in different Mediterranean regions (den Hartog et al., 1987 ). Environmental factors such as salinity, temperature and nutrient supply in the sediment also influence
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M.C. BUIA AND L. MAZZELLA
germination (Caye and Meinesz, 1986). To clarify the life history of C. nodosa, further studies are required both on the species variability and on the factors influencing germination, in particular on the influence of sediment features, which can vary greatly in C. nodosa meadows. In C. nodosa and P. oceanica, flower abundance seems to be related to the structure of the meadow, while the occurrence of flowering seems to be regulated by environmental factors. In particular, in the three species studied here, the m a x i m u m flower density was usually found in the densest stands, as reported for other seagrasses (Durako and Moffler, 1987). This appears to enhance the success of pollination among flowering shoots that probably belong to the same parent plant (Mazzella et al., 1984). Temperature changes over the year seem to play an important role in regulating the reproductive cycle ofP. oceanica and C. nodosa. In P. oceanica, the time delay observed for the deep beds can be related to the summer thermocline, which also influences leaf growth and production (Pirc, 1984; Mazzella and Ott, 1984 ). The different response to the annual temperature range could be related to the origin and geographical distribution of these plants. In P. oceanica, which belongs to a temperate genus, the reproductive process takes place in the colder months, whereas in C. nodosa whose genus is typical of tropical waters (den Hartog, 1970), it occurs in the warmer months, unlike the congeneric tropical species which have an almost continuous germination over the year (McMillan, 1980, 1982). In relation to the theory of r- and K-selection (Pianka, 1970), for the Mediterranean seagrasses, taking into account a continuum from the two strategies, we can classify P. oceanica as a K-selected species, Z. noltii as an r-selected species and C. nodosa as having a strategy more similar to that of the latter. In fact, as a K-selected plant, P. oceanica, which lives in a more constant and predictable environment, has a long lifespan (it is perennial) and a low growth rate. Moreover, P. oceanica, which has the largest size among Mediterranean phanerogams, has a shoot density and a leaf canopy fairly constant in time, and the maintenance of the bed via rhizomes and roots is ensured by the use of a large portion of its resources. In contrast, Z. noltii, which lives in a highly variable environment, has a short lifespan (it is perennial, but can also be annual) and grows rapidly during spring; however, the population size is greatly reduced when the temperature drops. Cymodocea nodosa, whose size is intermediate, lives in a less predictable environment than P. oceanica. It has a long lifespan (it is perennial) but a rapid development, although slower than Z. noltii, with higher rhizome and leaf growth than P. oceanica and a clear seasonality in meadow structure (e.g. shoot density). Maintenance of the meadow is ensured by many offspring via sexual reproduction. Following Pianka's (1970) classification, various schemes of life strategies of terrestrial and aquatic plants have been postulated (Grime, 1974; Jacobs 1982; Kautsky, 1988). Present knowledge about the life histories and
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physiological requirements suggests that P. oceanica is a "competitive" plant or "biomass storer", Z. noltii a "ruderal" and C. nodosa seems to be a ruderal or a competitive plant. However, more studies, aimed at clarifying the adaptive processes that allowed the evolution of these plants and the ability to live in Mediterranean areas, are required. ACKNOWLEDGEMENTS
We are indebted to colleagues of the Oceanographic Laboratory of the Stazione Zoologica for the temperature data. Thanks are due to Maurizio Lorenti for his collaboration during the SCUBA diving observations, and Antonio Rando for his assistance in field activities. The authors gratefully acknowledge Dr. Gilberte Caye and Dr. Alexander Meinesz for providing C. nodosa seeds from Antibes (France).
REFERENCES Benacchio, N., 1938. Osservazioni sistematiche e biologiche sulle Zosteraceae dell'alto Adriarico. Thalassia, 3 (3): 2-41. Bornet, E., 1864. Recherches sur le Phucagrostis major Cavol. Ann. Sci. Nat. Ser. Bot., 1: 5-51. Boudouresque, C.F., Jeudy De Grissac, A. and Olivier, J., 1984. International Workshop on Posidonia Beds. G.I.S. Posidonie, Oceanica, 1. 454 pp. Boudouresque, C.F., Meinesz, A., Fresi, E. and Gravez, V., 1989.2nd International Workshop on Posidonia oceanica Beds. G.I.S. Posidonie, Oceanica, 2, 322 pp. Buia, M.C. and Piraino, S., 1989. Record of a Posidonia oceanica (L.) Delile seedling in the Egadi Island (Sicily, Italy ). Posidonia Newsl., 2 (2): 19-22. Buia, M.C., Cormaci, M. Furnari, G. and Mazzella, L., 1985a. Osservazioni sulla struttura delle praterie di Posidonia oceanica (L.) Delile di Capo Passero (Siracusa) e studio della macroflora epifita delle foglie. Boll. Accad. Gioenia Sci. Nat., 18: 463-484. Buia, M.C., Mazzella, L., Pirc, H. and Russo, G.F., 1985b. Fioritura di Zostera noltii Hornem. a Ischia (Golfo di Napoli). Oebalia, 11, N.S.: 861-862. Buia, M.C., Mazzella, L. and Russo, G.F., 1985c. Fenomeni riproduttivi della Cymodocea nodosa (Ucria) Aschers. in rapporto alia struttura della prateria. Oebalia, 11, N.S. :377. Buia, M.C., Mazzella, L., Russo, G.F. and Scipione, M.B., 1985d. Observations on the distribution of Cymodocea nodosa (Ucria) Aschers. prairies around the Island of Ischia (Gulf of Naples). Rapp. Comm. Int. Mer M6dit., 29 (6): 205-208. Buia, M.C., Russo, G.F. and Mazzella, L., 1985e. Interrelazioni tra Cymodocea nodosa (Ucria) Aschers. e Zostera noltii Hornem. in un prato misto superficiale dell'isola di Ischia. Nova Thalassia, 7: 406-408. Buia, M.C., Zupo, V. and Mazzella, L., 1991. Primary production and growth dynamics in Posidonia oceanica. P.S.Z.N.I. Mar. Ecol., in press. Caye, G. and Meinesz, A., 1984a. Observations sur la floraison et la fructification de Posidonia oceanica dans la baie de Villefrance et en Corse du Sud. In: C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), International Workshop on Posidonia oceanica Beds, GIS Posidonie, Marseille, pp. 193-201. Caye, G. and Meinesz, A., 1984b. Floraison et fructification des phan6rogames marines
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Cymodocea nodosa (Ucria) Ascherson et Zostera noltii Hornemann ~ Port-Cros (France). Trav. Sci. Parc nation. Port-Cros, Notes br6ves, 10:153-156. Caye, G. and Meinesz, A., 1985a. Observations on the vegetative development, flowering and seeding of Cymodocea nodosa (Ucria) Ascherson on the Mediterranean coasts of France. Aquat. Bot., 22: 277-289. Caye, G. and Meinesz, A., 1985b. Evaluation de la longevit6 des rhizomes de Cymodocea nodosa d'apres les variations cycliques de la longeur des entre-noeuds. Rapp. Comm. Int. Met Mddit., 29: 187-188. Caye, G. and Meinesz, A., 1986. Experimental study of seed germination in the seagrass Cvmodocea nodosa. Aquat. Bot., 26: 79-87. Caye, G. and Rossignol, M., 1983. Etude des variations saisonni6res de la croissance des feuilles et des racines de Posidonia oceanica. Mar. Biol., 75: 79-88. Cinelli, F. and Salghetti-Drioli, U., 1983. Observations en plongde sur les peuplements a Penicillus capitatus et sur la floraison de Posidonia oceanica de l'Ile d'Elbe (Mdditerrande Occidentale). Rapp. Comm. Int. Mer Mddit., 28(8): 169-170. Colantoni, P., Gallignani, P., Fresi, E. and Cinelli, F., 1982. Patterns ofPosidonia oceanica (L.) Delile beds around the Island of Ischia (Gulf of Naples) and in adjacent waters. P.S.Z.N.I. Mar. Ecol., 3: 53-74. Cooper, G., 1979. Posidonia oceanica: un arbre. Jardinier de la Mer, 3: 1-65. Den Hartog, C., 1970. The Seagrasses of the World. North-Holland, Amsterdam, 275 pp. Den Hartog, C., 1977. Structure, function, and classification in seagrass communities. In: C.P. McRoy and C. Helfferich (Editors), Seagrass Ecosystems: a Scientific Perspective. Marcel Dekker, New York, pp. 89-121. Den Hartog, C., Hennen, J., Noten, Th.M.P.A. and van Wijk, R.J., 1987. Chromosome numbers of the European seagrasses. Plant Syst. Evol., 156: 55-59. Durako, M.J. and Moffier, M.D., 1987. Factors affecting the reproductive ecology of Thalassia testudinum (Hydrocharitaceae). Aquat. Bot., 27: 79-95. Frad~ Orestano, C., Calvo, S., Abbadessa, P. and Aric6, S., 1989. Fioritura e fruttificazione di Posidonia oceanica nella Baia di San Nicola (Palermo). Oebalia, 15, N.S. :137-144. Gambi, M.C., Russo, G.F. and Chessa, L.A., 1984. Fioritura de Posidonia oceanica (L.) Delile in una prateria superficiale della rada di Porto Conte (Sardegna Nord-Occidentale). Rend. Sem. Fac. Sci. Univ. Cagliari, 54 (Suppl.): 189-196. Giaccone, G. and Calvo, S., 1980. Restaurazione del manto vegetale mediante trapianto di Posidonia oceanica (Linneo) Delile. Risultati preliminari. Mere. Biol. Marine e Oceanogr., Suppl. 10:207-211. Giaccone, G. and Sortino, M., 1974. Zonazione della vegetazione marina delle Isole Egadi (Canale di Sicilia). Lav. 1st. Bot. Giardino Colon Palermo, 25:165-183. Giraud, G., 1977. Contribution ~ la description et/l la phdnologie quantitative des herbiers de Posidonia oceanica (L.) Delile. Th6se, Universit6 d'Aix-Marseille. Giraud, G., Boudouresque, C.F., Cinelli, F., Fresi, E. and Mazzella, L., 1979. Observations sur l'herbier de Posidonia oceanica (L.) Delile autour de l'Ile d'Ischia (Italie). G. Bot. ltal., 113: 261-274. Grime, J.P., 1974. Vegetation classification by reference to strategies. Nature, 250:26-31. Hootsmans, M.J.M., Vermaat, J.E. and van Vierssen, W., 1987. Seed-bank development, germination and early seedling survival of two seagrass species of The Netherlands: Zostera marina L. and Zostera noltii Hornem. Aquat. Bot., 28: 275-285. Jacobs, R.P.W.M., 1982. Reproductive strategies of two seagrass species (Zostera marina and Z. Noltii) along west European Coasts. In: J.J. Symoens; S.S. Hooper and P. Comp6re (Editors), Studies on Aquatic Vascular Plants. Royal Botanical Society of Belgium, Brussels, pp. 150-155. Kautsky, L., 1988. Life strategies of aquatic soft bottom macrophytes. Oikos, 53:126-135. Mazzella, L. and Ott, J., 1984. Seasonal changes in some features of Posidonia oceanica (L.)
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Delile leaves and epiphytes at different depths. In: C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), International Workshop on Posidonia Oceanica Beds, GIS Posidonie, Marseille, pp. 119-127. Mazzella, L., Russo, G.F. and Gambi, M.C., 1982. Fioritura di praterie profonde di Posidonia oceanica (L.) Delile intorno all'isola d'Ischia. Boll. Mus. Ist. Biol. Univ. Genova, 50 (Suppl.):388. Mazzella, L., Gambi, M.C., Russo, G.F. and Wittmann, K., 1983. Flowering in Posidonia oceanica (L.) Delile prairies around the Island of Ischia (Gulf of Naples). Rapp. Comm. Int. Met M6dit., 28(3): 117-119. Mazzella, L., Buia, M.C. and Russo, G.F., 1983-84. Osservazioni "in situ" sul ciclo riproduttivo della Cymodocea nodosa (Ucria) Aschers. Nova Thalassia, 6 (Suppl.): 719. Mazzella, L., Gambi, M.C., Russo, G.F. and Buia, M.C., 1984. Deep flowering and fruiting of Posidonia oceanica beds around the Island of Ischia (Gulf of Naples, Italy). In: C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), International Workshop on Posidonia oceanica Beds, GIS Posidonie, Marseille, pp. 203-209. Mazzella, L., Scipione, M.B., Buia, M.C. and Russo, G.F., 1986. In situ measurements and sampling techniques on Cyrnodocea nodosa (Ucria) Aschers. prairie. Rapp. Comm. Int. Mer M6dit., 30: 265. McMillan, C., 1980. Reproductive physiology in the seagrass Syringodium filiforme from the Gulf of Mexico and the Caribbean. Am. J. Bot., 67:104-110. McMillan, C., 1982. Reproductive physiology of tropical seagrasses. Aquat. Bot., 14: 245-258. Meinesz, A. and Simonian, M., 1983. Cartes de la v6g6tation sous-marine des Alpes Maritimes (C6tes Fran~aises de la M6diterran6e) II. La v6g6tation mixte ~ Cymodocea nodosa-Zostera noltii-Caulerpa prohfera et la limite sup6rieure de l'herbier de Posidonia oceanica entre Juanles-Pins et Golf Juan. Ann. Inst. Oceanogr., (Paris), 59: 21-35. Meinesz, A. and Verlaque, M., 1979. Note pr61iminaire concernant quelques exp6riences de repiquage de Caulerpa et de Zostera noltii dans la zone de reject de l'effiuent thermique de la centrale 61ectrique de Martigues-Pontea (Golfe de Fos--France). Rapp. Comm. Int. Mer M6dit., 25/26: 209-212. Molinier, R. and Picard, J., 1952. Recherches sur les herbiers de phan6rogames marines du littoral m6diterran6en franqais. Ann. Inst. Oceanogr., Paris, 28:157-234. Panayotidis, P., 1986. Influence de la floraison sur le cycle de renouvellement des feuilles de Posidonia oceanica (L.) Delile, dans le Golf Saronikos (Mer Eg6e, Grece). Rapp. Comm. Int. Mer M6dit., 30: 6. Pergent, G., 1987. Recherches lepidochronologiques chez Posidonia oceanica (Potamogetonaceae): fluctuations des parametres anatomiques et morphologiques des 6cailles des rhizomes. Thesis, Universit6 Aix-Marseille II, 368 pp. Pianka, E., 1970. On r and K selection. Am. Nat., 104: 592-597. Pirc, H., 1983. Belowground biomass of Posidonia oceanica (L.) Delile and its importance to the growth dynamics. Proceedings of an International Symposium on Aquatic Macrophytes, Nijmegen, pp. 177-181. Pirc, H., 1984. Depth adaptation in Posidonia oceanica (L.) Delile. In: C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), International Workshop on Posidoni Oceanica Beds, GIS Posidonie, Marseilles, pp. 227-234. Pirc, H., Mazzella, L. and Russo, G.F., 1983. Record of Cymodocea nodosa (Ucria) Aschers. fruiting in a prairie of the island of Ischia (Gulf of Naples). Rapp. Comm. Int. Mer M6dit., 28: 121-122. Pirc, H., Buia, M.C. and Mazzella, L., 1986. Germination and seedling development of Cymodocea nodosa (Ucria) Ascherson under laboratory conditions and in situ. Aquat. Bot. 26: 181-188. Simonetti, G., 1972-73. I consorzi a fanerogame nel Golfo di Trieste. Atti. Ist. Veneto Sci., Lett. Articl. Sci. Mat. Nat., 131: 459-502.
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Thelin, I. and Boudouresque, C.F., 1985. Posidonia oceanica flowering and fruiting: recent data from an international inquiry. Posidonia Newsl., 1 ( 1 ): 5-14. Thelin, I., Mosse, R.A., Boudouresque, C.F. and Lion, R., 1985. Le benthos littoral d'El Dabaa (M6diterran6e, Egypte). II. L'herbier ~ Posidonia oceanica. Rapp. Comm. Int. Mer M6dit., 29(5): 247-248.
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Reproductive phenology of the Mediterranean seagrasses Posidonia oceanica (L.) Delile, Cymodocea nodosa ( Ucria ) Aschers., and Zostera noltii Hornem. M.C. Buia and L. Mazzella Laboratorio di Ecologia del Benthos della Stazione Zoologica "A. Dohrn "' di Napoli, 80077 lschia, Italy (Accepted for publication 14 February 1991 )
ABSTRACT Buia, M.C. and Mazzella, L., 1991. Reproductive phenology of the Mediterranean seagrasses Posidonia oceanica (L.) Delile, Cymodocea nodosa ( Ucria ) Aschers., and Zostera noltii Hornem. Aquat. Bot., 40: 343-362. Investigations on the sexual reproduction of Posidonia oceanica (L.) Delile, Cymodocea nodosa (Ucria) Aschers. and Zostera noltii Hornem. were conducted in situ from 1979 to 1988 in beds around the island of Ischia. Seed germination and phenological features of seedlings of P. oceanica and C. nodosa were observed in situ and in the laboratory. The reproductive cycles showed, for each species, different timing of start and duration of flowering, fruiting and germination. Posidonia oceanica flowers always appeared in September in shallow stands and in November in stands deeper than 15 m. This time delay seems to be related to the different maximum summer temperatures found at those depths. This species did not show dormancy. Cymodocea nodosa flowering was always recorded after the mini mum winter temperature (April-May); germination of the seeds followed after 8-10 months of dormancy. Zostera noltii flowers were always recorded in July, with fruiting in August. The life cycles of these species seem to be related to the annual temperature range rather than to other environmental parameters. The different reproductive strategies adopted by each species are discussed.
INTRODUCTION
The most common seagrasses in the Mediterranean Sea are Posidonia oceanica (L.) Delile, Cymodocea nodosa (Ucria) Aschers., and, in restricted shallow areas, Zostera noltii Hornem. Zostera marina L., unlike the situation along the Atlantic and Pacific coasts, is confined to brackish waters such as deltas or the north Adriatic Sea. Posidonia oceanica forms the largest and the most widespread beds, representing one of the most productive mediterranean ecosystems (Boudouresque et al., 1984, 1989). Meadows of C. nodosa are the second largest in 0304-3770/91/$03.50
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extent (Simonetti, 1972-73; Buia et al., 1985d). Zostera noltii, which colonizes the tidal zones on the Atlantic European coasts (Jacobs, 1982 ), reaches a depth of 5 m in the Mediterranean. It rarely forms monospecific meadows and mixes mainly with C. nodosa, which represents the dominant taxon and is the first species to colonize the substratum (Buia et al., 1985e). Mixed meadows, consisting of the two species and the green alga Caulerpa prolifera (Forssk.) Lamouroux, also occur frequently (Meinesz and Verlaque, 1979; Meinesz and Simonian, 1983; Pirc et al., 1983 ). The three species differ in morphological and phenological features, and hence their systems differ in structure and dynamics. Cymodocea nodosa is considered the pioneer species of Posidonia oceanica beds, the latter species forming the 'climax' stage. When P. oceanica beds regress, C. nodosa often replaces them (Molinier and Picard, 1952; den Hartog, 1977); as a result, P. oceanica, C. nodosa, and Z. noltii do not form mixed persistent stands. A large amount of data has been accumulated about the Posidonia ecosystem (for a review, see Boudouresque et al., 1984, 1989). Much less is known about the ecology and sexual reproduction of C. nodosa and Z. noltii (Caye and Meinesz, 1985a; L. Mazzella, G.F. Russo and M.C. Buia, unpublished data, 1985 ). The reproduction phenomena of P. oceanica have been observed in both the northern and southern parts of the Mediterranean and are related to the different latitudes (Giraud, 1977; Cooper, 1979; Giraud et al., 1979; Giaccone and Calvo, 1980; Cinelli and Salghetti-Drioli, 1983; Caye and Meinesz, 1984a; Gambi et al., 1984; Mazzella et al., 1984; Thelin and Boudouresque, 1985; Thelin et al., 1985). The first study on the sexual reproduction of C. nodosa with a description of flowers, seeds and seedlings was conducted by Bornet in 1864, but only recently has the reproductive cycle of this species been studied in relation to the structure of the meadow and to several environmental factors (Mazzella et al., 1983-84; Caye and Meinesz, 1985a; Buia et al., 1985c; Pirc et al., 1986 ). Little information on the flowering of Z. noltii is available for the Mediterranean Sea; data have been reported for the north Adriatic, the Island of PortCros (Gulf of Hybres ) and the Island of Ischia ( Gulf of Naples ) ( Benacchio, 1938; Simonetti, 1972-73; Caye and Meinesz, 1984b; Buia et al., 1985b). The morphology and life histories of these three species are related to environmental factors (e.g. light regime, hydrodynamic force, temperature) of the habitat where they form beds. Sexual reproduction is crucial not only in maintaining genetic diversity, but as a species dispersal mechanism. The aim of the present study was to characterize the features of the sexual reproduction of these plants and to clarify their life cycle. Pluriannual investigations on the sexual reproduction of the three species were conducted in situ from 1979 to 1988 in beds around the Island of Ischia. Germination and the phenological features of seedlings ofP. oceanica and C. nodosa, were stud-
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ied in situ and in the laboratory. The reproductive cycles of the three plants are described and an attempt is made to identify the strategies adopted by each of them in relation to environmental parameters. STUDY AREAS A N D M E T H O D S
Study areas The areas studied around the Island of Ischia are shown in Fig. I. Posidonia oceanica forms the most extensive beds surrounding the island from a depth of 1 to about 38 m (Colantoni et al., 1982). Cymodocea nodosa is found mainly along the coasts exposed to the north, where it forms separate meadows down to a depth of 6 m and from 10 to 21 m (Buia et al., 1985d). Zostera noltii occurs down to a depth of 5 m, always mixed with C. nodosa, mainly in meadows adjacent to ports. The sexual reproductive cycle of P. oceanica was observed in three beds: Lacco Ameno, San Pancrazio and La Nave (Fig. 1 ). At Lacco Ameno, the beds face north-northeast and extend from a depth of 1 m down to 35 m over a distance of 600 m (Mazzella et al., 1986). From 1 to 20 m the plants occur on a 'matte' (a terrace formed by P. oceanica roots and rhizomes and en1 P. V i c e 2 Lacco Ameno 3 Fungo 4 S. P F e t r o
5 Castello
Aragonese
6 P. S. P a n c r a z l o
7 La N a v e 8 S. M o n t a n e
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,
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.
~ "",.--,..
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Fig. 1. Distribution of Posidonia oceanica, Cymodocea nodosa and Zostera noltii around the Island of Ischia (Gulf of Naples, insert) and location of the sampling sites.
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M.C. BUIA A N D L. MAZZELLA
trapped sediment, as defined by Molinier and Picard, 1952), and, at greater depths, on sand. At San Pancrazio, the bed is exposed to the south; it is found between 10 and 35 m and grows on a 'matte' throughout its length (Colantoni et al., 1982). At La Nave, P. oceanica occurs between 15 and 30 m with a patchy distribution, growing on rocky substrate throughout (Mazzella et al., 1984). The C. nodosa meadows studied were mostly in shallow waters, within a depth of 6 m (Castello Aragonese, San Pietro, Lacco Ameno and Fungo ); the San Montano m e a d o w occurs at 15 m (Fig. 1 ). The Castello meadow, formed only by C. nodosa, occurs on a sandy substratum. It is relatively protected from water movement, and grows in a channel within a P. oceanica bed (see Fig. 1 ) that is implanted on a 1 m high 'matte'. The Fungo and Lacco Ameno meadows occur at a depth o f 2 m (Fig. 1 ). The former is near the small barbout, and the latter lies behind a m a n - m a d e cliff that separates the harbour from the open sea. Both meadows are mixed with Z. noltii and both occur on a m u d d y sediment. The San M o n t a n o m e a d o w grows on a coarse sandy sediment, between the upper limit of a deep P. oceanica bed and the rocky shore, and has a very low shoot density (Fig. 1 ). The m e a d o w of San Pietro occurs between depths of 1.5 and 4 m in an area protected by artificial cliffs. It mainly grows on 'turf' (a terrace formed by C. nodosa and Z. noltii roots and rhizomes and entrapped sediment, as defined by Buia et al., 1985e) with a m u d d y - s a n d y sediment (L. Mazzella, G.F. Russo and M.C. Buia, unpublished data, 1985 ) and partially on sandy substratum (Fig. 2 ). In this meadow, C. nodosa is mixed with Z. noltii, which shows a patchy distribution and is not present in the shallowest part of the m e a d o w (Buia et al., 1985e). 4.0 m
Fig. 2. Map of the San Pietro meadow and location of the four study sites (A,B,C,D).
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Methods The reproductive phenology ofP. oceanica was studied from 1979 to 1988. During these years, flowering and fruiting in the above-mentioned beds were recorded. In the beds of Lacco Ameno and San Pancrazio, stations were established along depth transects in relation to the appearance of flowering shoots, and the frequency of flowers per square metre (five replicates for each stand) was calculated. Germination experiments were conducted with mature P. oceanica seeds collected at the end of May 1987 on the shoreline of the Amalfi coast (Gulf of Salerno). They were kept in aquaria with running sea water at ambient temperature and light conditions. Growth and phenological parameters of seedlings (mean number of leaves and roots per shoot, length and width of leaves of different classes, length of roots) were recorded bimonthly from germination (May 1987 ) until January 1988. The reproductive phenology of C. nodosa was studied from 1982 to 1988. The appearance of flowers, fruits and seeds in the different meadows during these years was recorded. Methods to determine flower, fruit and seed density, and the microdistribution of male and female flowers, have been described previously (Mazzella et al., 1986). In the San Pietro meadow, four stations were established along a depth transect between 1.5 and 4 m (Buia et al., 1985d) (Fig. 2). The density of C. nodosa and Z. noltii was measured at each station. Germination of C. nodosa seeds, collected in 1985 in meadows at different latitudes (Castello, San Pietro, Lacco Ameno for the south Meditteranean and Antibes for the north Meditteranean), was also studied in the laboratory at ambient light and temperature conditions, and the phenological features of seedlings were measured (e.g. number of leaves per shoot, length and width of leaves, number of roots per shoot, length of roots). Differences in leaf phenology of the seedlings and in the length and width of seeds were statistically tested (ANOVA). The occurrence in situ of flowers and fruits of Z. noltii was recorded from 1984 to 1988 in the San Pietro meadow (Fig. 2). In 1984 and 1985, the density and the microdistribution of the inflorescences were measured in situ using the methods described above for C. nodosa. RESULTS
Reproduction ofPosidonia oceanica Posidonia oceanica flowering (Fig. 3) has occurred every year since 1979 (Mazzella et al., 1982; Mazzella et al., 1983; Mazzella et al., 1984). However, the intensity of flowering varied year by year and along depth transects in the shallow and deep stands of the same beds (Table 1 ). Flowering shoots have a patchy distribution (data not presented) and stands at the same depth never
348
M.C. BUIA AND L. MAZZELLA
Fig. 3. Early developmentalstage of the Posidonia inflorescence(size bar, 0.3 cm ). appeared to flower in successive years. Many dead inflorescences at an initial fruiting stage were often found (Table 1 ). In shallow stands (down to 15 m ) a low frequency ofinflorescences was followed by 2 years of high density (Table 1 ). In deep beds, fruiting showed alternate yearly maxima and minima. A high abundance of flowers in one area often corresponded with a high abundance in other Mediterranean areas (French coast and south Italy) (Frad~ Orestano et al., 1989; G. Pergent, personal communication, 1988 ). Between shallow (down to 15 m) and deep stands (from 15 to 28 m ) , Posidonia oceanica showed a persistent phase-difference, whereby there was a flowering delay of about 2 months in the deep meadows (Fig. 4 ). In the shallow meadows the first flower buds, borne by a short stalk, were usually recorded in September, and on rare occasions at the beginning of October. In the deep meadows this stage was observed in November or at the beginning of December. Anthesis occurred in October in the shallow waters and in December in the deep stands. Fruits developed from December to March-April in the shallow stands, and from February to May-June, sometimes to July, in the deep stands (Fig. 4). At both depths, flowering was recorded a month after the m a x i m u m water temperature, measured in August for the shallow waters (25°C, as the average of 3 years) and in October at a depth of 20 m ( 22.5 ° C ) below the s u m m e r thermocline (Fig. 4 ). Germination in the laboratory under ambient light and temperature levels,
REPRODUCTIVE PHENOLOGY OF MEDITERRANEAN SEAGRASSES
349
TABLE1 M i n i m u m a n d m a x i m u m values of d e n s i t i e s of flowers (flowers per square m e t r e ) a n d fruits (fruits per square raetre) ofPosidonia oceanica from 1981 to 1988 in shallow a n d deep s t a nds of three beds: Lacco Ameno, San Pan crazio, a n d La N a v e Lacco A m e n o Shallow
San P a n c r a z i o Deep
La Nave
Shallow
Deep Deep
1981-1982 Flowers Frmts
-
0-3
-
0-2
3-28
-
1-25
0-5
-
1-18
1982-1983 Flowers Fr uits
9-15 -
10-30
•
•
-
-
1983-1984 Flowers Fruits
0-13 0-4
0-2 .
0-7 .
.
.
1984-1985 Flowers Fruits
0-2 - -
*
-
-
-
,
~
_
_
1985-1986 Flowers Fr uits
0-94
0-25
-
0-1
0-1
0-40 0-2
0-2 0-2
-
0-3 -
0-69 -
0-38 0-2
0-41 0-1
, ,
, -
, -
1986-1987 Flowers Fruits
1987-1988 Flowers Fr uits
*Only occurrences of flowers a n d fruits.
occurred a few days after the seeds were collected (end of May). This finding excludes dormancy. Of the total of 57 seeds, 40 (70%) germinated, and from these only 11 (28%) survived to the end of the experiment (January). The m a x i m u m mean number of leaves per shoot (seven) was reached in summer. The leaf length per leaf class increased during the experiment with the maxim u m occurring in January (Fig. 5 ). The mean width varied between 0.2 and 0.35 cm in August, and between 0.46 and 0.53 cm in January. The m a x i m u m length and width was reached by the youngest leaves, which indicates a differential growth for leaves of different ages. In particular, in June and August the second leaf was the longest ( 3.52 + 0.51-7.11 _+0.95 ), and in November and January, the third leaf was the longest ( 11.68 + 2.74-13.48 + 3.34 ). The number and length of roots showed the same increasing pattern from June to January, in accordance with the seedlings age (Fig. 5 ).
J
:
F
o---0
:
M
shallow deep
~
-
A
~
-
M
-
~
J
°
~
J
-
~
A
-
-
~
S
0
~
N
D
.?-
-
o
Fig. 4. Diagramatic representation of the reproductive cycles of Posidonia oceanica, Cymodocea nodosa and Zostera noltii in the south Mediterranean area and mean annual variations in water temperature (as average of 1984-1986 records at the surface and at 20 m depth).
i,i
o
:=
o
o
U)
o o
m
¢:
m u
m
o
k.
I-
,30
II
N N
z
©
0
351
R E P R O D U C T I V E P H E N O L O G Y OF M E D I T E R R A N E A N SEAGRASSES
o Z
15_
15
10
10 "~
i' 0 JANJ
.J=
Z NJAN
U,I
~
!Innn JANJ
1234567891011
Z
Leaf
o
Month
Fig. 5. Leaf and root growing trends of Posidonia oceanica seedlings kept in the laboratory at ambient temperature and light conditions (mean _+confidence limits); (the youngest leaf is indicated as 1 ).
Reproduction ofCymodocea nodosa In the meadows under study (in shallow waters ), the first flower buds were recorded at the end of April, when the water temperature started to rise after the annual minimum (Fig. 4 ). In April the flowers were mainly hypogean and sheathed. In May, both male and female flowers were easily recognizable in situ, the stamens being on the stalk that at this time was elongated, and the pistils showing the filamentous stigmata rising from the leaf sheath (Fig. 6 ). The first mature fruits, still attached to the mother plant, were found at the end of July or beginning of August (Mazzella et al., 1983-1984). The seeds were dormant, buried in the sediment until germination started in April, coinciding with a rise in water temperature after the winter minimum (Fig. 4 ). The maximum germination rate was recorded in June (present study) or in July (Pirc et al., 1986). Since the start of our study in 1982, Cyrnodoceahas had a high fecundity. Staminate and pistillate flowers, fruits and seedlings were collected in each of 7 years in some of the meadows studied. Table 2 shows the vegetative and reproductive shoot density recorded in four stations of the San Pietro meadow in June and July 1984. The highest total flower density usually coincided with the maximum shoot density; however, male and female flowers differed in density in the same station. In June, the total amount of flowering shoots was higher in the deeper stations and decreased towards the coastline. A similar
352
M.C. BUIA AND L. MAZZELLA
F i g . 6. M a l e ( o n t h e l e f t ) a n d f e m a l e
(on the right; arrow indicates the stigmata)
flowers of
Cymodocea nodosa ( s i z e b a r , 1.8 c m ) .
TABLE 2 D e n s i t y ( n u m b e r s p e r s q u a r e m e t r e ) o f Cymodocea nodosa a n d Zostera ers, f r u i t s , s e e d s a n d s e e d l i n g s in t h e S a n P i e t r o m e a d o w in 1 9 8 4
noltii v e g e t a t i v e s h o o t s , f l o w -
Zostera noltii
Cymodocea nodosa Vegetative shoots
Female flowers
991 1176
99 -
1062 722
Male flowers
Fruits
Seeds
Seedlings
Vegetative shoots
Flowers
-
113
127 340
71
1020 991
-
85 -
85 -
142
340 227
14 28
821 1119
-
623 510
42 -
. -
-
-
1232 1076
57
864 1331
3 -
. -
-
-
Station A June July
Station B June July
Station C June July
.
. 14
.
Station D June July
.
. 28
. 14
. 14
.
353
REPRODUCTIVE PHENOLOGY OF MEDITERRANEAN SEAGRASSES JUNE ST.
1984 ST.
C d' o'
d' d' 4' ~/{ d' o, ~l o' ~' d' d' (¢ o' a' ~ c¢ J d'
d d' ~ 9 9 ? g c~ ?
B
o" o' o'
~/~. c¢c¢'
o'eA ~o,o, o' o' o'
9 g
o'~o,
Fig. 7. Microdistribution of male and female flowers of Cymodocea nodosa w i t h i n a 1 m 2 q u a d rat, divided into units of 12.5 c m × 12.5 c m at Stations B and C in June 1984.
TABLE 3
Germination rate of Cymodocea nodosa seeds collected from different sites Ischia
Antibes
Castello
San Pietro
Lacco Ameno
49
32
31
25
37 (76%)
26 (81%)
27 (87%)
13 (52%)
43 (88%)
29 (91%)
27 (87%)
15 (60%)
13/1/1986 No. seeds
collected
12/5/1986 No. seedlings
germinated
5/6/1986 No. seedlings
germinated
pattern was found for fruits and seedlings in July, and for free seeds, collected in the sediment, originating from the previous reproductive season. Investigations on the microdistribution of flowers (Fig. 7 ), showed patches of male flowers separated from female flowers in stands where flower density was low (Station C). In stations where the flower density was higher (Station B ), patches formed by both male and female flowers were recorded together (Fig. 7). In both stations, the flowers showed a contagious distribution. In fact, the Z 2 values were highly significant (Station B: Z2 total, 59.7; male, 24.9; female, 100; P > 0,5%; Station C: Z2 total, 15.8; male, 21.7; female, 226; P>0.5%). Germination occurred in April-May and reached a maximum in June, in all Ischia meadows. However, comparing the germination of seeds from meadows at different latitudes (Ischia, Gulf of Naples and Antibes, France ),
354
M . C . B U I A A N D L. M A Z Z E L L A
6
I~J Z
10
il nnn ,~25 E o 20 0 .=
,. 15
>. .-I ~
~
,-j
5
o 0
,,- 300
Z
"J 25
23456
2O
6[
10 1511
CSLA
C
i1
S
L
i
I< A
Fig. 8. Leaf growing trends of Cymodocea nodosa seedlings, kept in the laboratory at ambient light and temperature conditions (mean _+confidence limits); (the youngest leaf is indicated as 1).
differences were found in the rates of germination, being lower for Antibes (Table 3 ). Seedling growth patterns are shown in Fig. 8. The mean leaf number per shoot reached a m a x i m u m in July. The mean leaf length for each leaf class showed a constant pattern in each month. Leaf decay began in August. At the end of the experiment, the mean number of leaf scars on the rhizomes was 6 + 1 plus 2 leaves for Castello, 7 _+0.5 plus 3 leaves for San Pietro, 5 + 1 plus 1 leaf for Lacco Ameno and 5 + 0.5 plus 1 leaf for Antibes. Therefore, the mean leaf production of seedlings was again highest for seedlings from the San Pietro meadow and lowest for Antibes. The number of roots on the seedlings increased for each meadow from June to August (Fig. 9), and the Antibes seedlings gave the highest values (4.0 + 1 ). The mean length increased only for seedlings from the Castello and San Pietro meadows, while seedlings from Lacco Ameno and Antibes showed a decreasing trend (Fig. 9 ). Significant differences were also found in the length and
REPRODUCTIVE PHENOLOGY OF MEDITERRANEAN SEAGRASSES
355
6
6
uJ Z 0 tu~
6
.c
6
0
.A
m 0 0 L.
Z
0
0
°f
4
O <
o CSLA
CSLA Meadows
Fig. 9. Growing trends of roots of Cymodocea nodosa seedlings kept in the laboratory at ambient light and temperature conditions (mean +_confidence limits).
Fig. 10. Inflorescence of Zostera noltii (arrow indicates the erect style and stigmata) (size bar, 0.3 cm). width of seeds among the Ischia meadows (Castello, San Pietro, Fungo, Lacco Ameno, San Montano ). Compared two by two, seeds from Castello and Fungo were significantly different from each other and from the other stations for both parameters. Seeds from San Pietro and Lacco Ameno did not show significant differences.
356
M.C. BUIA AND L. MAZZELLA
JULY ST.
1985
B
[] o
----'1
[]
4 7
3
6 9
i Fig. 11. Microdistribution of rhipidia (class density) of Zostera noltii within a 1 rn 2 quadrat, divided into units of 12.5 c m X 12.5 cm at Station B.
Reproduction ofZostera noltii
In the Ischia meadows, Zostera noltii flowers have been observed every year since the first report in 1984, at the end of June (Buia et al., 1985b) (Fig. 10). The stigmata emerge in July from the spatha. Later, the anthers of the same inflorescences release the pollen, thus preventing self-pollination. Flowering spathes can still be found in August, but these are usually smaller. Fruits were usually found in August (Fig. 4). Seeds were never found in the sediment, but seedlings were observed in July. Flowering shoots were present in the central part of the San Pietro meadow (Station C), notwithstanding the high density of vegetative shoots in other stations (Table 2). In July 1985, the flowering shoots in the San Pietro meadow showed a high density, with a contagious distribution, similar to the flowering shoots of C. nodosa (Fig. 11 ). DISCUSSION
The most striking finding of this study is that the reproductive cycles are phased differently in the three Mediterranean seagrasses. In P. oceanica there is an interval of about 8 months between flowering and germination, including 3 months for anthesis and 5 months for the fruit to mature. In C. nodosa the reproductive cycle lasts 12 months, with about 2 months for anthesis and 2 months for fruit development, followed by a period of seed dormancy of 8 months. Therefore, in April both flowers and seedlings are found in the C. nodosa meadow. The complete life history of Z. noltii cannot be constructed from the data available at present. However, seedlings were found in July together with flowering shoots, which suggests the existence of seed dormancy. Our studies in leaf production and biomass (Buia et al., 1985e) demonstrated that, in the Ischia meadows, Z. noltii is perennial, as reported from other areas (Hootsmans et al., 1987).
REPRODUCTIVE PHENOLOGY OF MEDITERRANEAN SEAGRASSES
3 57
This study also shows a difference in the length of the post-fertilization development period between P. oceanica and C. nodosa, with a longer fruit development in the former and dormancy in the latter. Thus, in P. oceanica, a lower vegetative growth in winter (Buia et al., 1991 ), coincides with higher energy costs that last until fruit maturation. Moreover, sexual reproduction can depress leaf growth and production in this season (Panayotidis, 1986 ). Another important difference between P. oceanica and C. nodosa is the success of fruit maturation. Posidonia oceanica usually bore two, or very rarely, four fruits, as against six to eight flowers per inflorescence (Caye and Meinesz, 1984a). In C. nodosa, the two ovaries per flowering unit usually became mature fruits, the latter being always found in couples at the bases of the leaf shoots. Posidonia oceanica and C. nodosa use different strategies for seed dispersal. Our results indicate that C. nodosa seeds remain buried in the sediment for a dormant period of 8-10 months. In P. oceanica, characterized by a very slow vegetative growth (Pirc, 1983; Caye and Rossignol, 1983), the buoyant period of the fruits seems to ensure species dispersion, and avoids competition with the parent plants. By contrast, in C. nodosa sexual reproduction seems to ensure the maintenance of meadow stability: it increases the density, which can vary greatly from year to year, as a result of uprooting in winter and fast rhizome growth and production in spring (Caye and Meinesz, 1985b; L. Mazzella, G.F. Russo and M.C. Buia, unpublished data, 1985). Posidonea oceanica can be germinated with some degree of success in controlled experiments both in situ (Cooper, 1979 ) and in the laboratory (Caye and Meinesz, 1984a; present paper) despite the few records of seedlings in situ (Pergent, 1987; Buia and Piraino, 1989 ). This apparent discrepancy could be due to the mechanism of seed dissemination that results in a high loss of fruits on the shoreline and to the difficulty of finding seedlings in very dense stands. However, the frequent findings of fruits and seedlings in south Italy (mainly along the Sicilian coasts) (Giaccone and Sortino, 1974; Buia et al., 1985a; Frad~t Orestano et al., 1989; M.C. Gambi, personal observation, 1987; S. Piraino, personal observation, 1986; our observations) seem to support the hypothesis that sexual reproduction might influence the species variability and distribution more in this part of the Mediterranean than at other latitudes. The reproductive success of C. nodosa seems also to differ at different latitudes. In fact, we found for Ischia that germination occurred every year, while germination seems to be occasional along the French coast, notwithstanding frequent flowering (Caye and Meinesz, 1985a). Moreover, seed size and seedling features differed between Ischia and Antibes. This morphological variability, already observed by den Hartog (1977) could correspond to different genotypes, as two karyotypes seem to be found in different Mediterranean regions (den Hartog et al., 1987 ). Environmental factors such as salinity, temperature and nutrient supply in the sediment also influence
358
M.C. BUIA AND L. MAZZELLA
germination (Caye and Meinesz, 1986). To clarify the life history of C. nodosa, further studies are required both on the species variability and on the factors influencing germination, in particular on the influence of sediment features, which can vary greatly in C. nodosa meadows. In C. nodosa and P. oceanica, flower abundance seems to be related to the structure of the meadow, while the occurrence of flowering seems to be regulated by environmental factors. In particular, in the three species studied here, the m a x i m u m flower density was usually found in the densest stands, as reported for other seagrasses (Durako and Moffler, 1987). This appears to enhance the success of pollination among flowering shoots that probably belong to the same parent plant (Mazzella et al., 1984). Temperature changes over the year seem to play an important role in regulating the reproductive cycle ofP. oceanica and C. nodosa. In P. oceanica, the time delay observed for the deep beds can be related to the summer thermocline, which also influences leaf growth and production (Pirc, 1984; Mazzella and Ott, 1984 ). The different response to the annual temperature range could be related to the origin and geographical distribution of these plants. In P. oceanica, which belongs to a temperate genus, the reproductive process takes place in the colder months, whereas in C. nodosa whose genus is typical of tropical waters (den Hartog, 1970), it occurs in the warmer months, unlike the congeneric tropical species which have an almost continuous germination over the year (McMillan, 1980, 1982). In relation to the theory of r- and K-selection (Pianka, 1970), for the Mediterranean seagrasses, taking into account a continuum from the two strategies, we can classify P. oceanica as a K-selected species, Z. noltii as an r-selected species and C. nodosa as having a strategy more similar to that of the latter. In fact, as a K-selected plant, P. oceanica, which lives in a more constant and predictable environment, has a long lifespan (it is perennial) and a low growth rate. Moreover, P. oceanica, which has the largest size among Mediterranean phanerogams, has a shoot density and a leaf canopy fairly constant in time, and the maintenance of the bed via rhizomes and roots is ensured by the use of a large portion of its resources. In contrast, Z. noltii, which lives in a highly variable environment, has a short lifespan (it is perennial, but can also be annual) and grows rapidly during spring; however, the population size is greatly reduced when the temperature drops. Cymodocea nodosa, whose size is intermediate, lives in a less predictable environment than P. oceanica. It has a long lifespan (it is perennial) but a rapid development, although slower than Z. noltii, with higher rhizome and leaf growth than P. oceanica and a clear seasonality in meadow structure (e.g. shoot density). Maintenance of the meadow is ensured by many offspring via sexual reproduction. Following Pianka's (1970) classification, various schemes of life strategies of terrestrial and aquatic plants have been postulated (Grime, 1974; Jacobs 1982; Kautsky, 1988). Present knowledge about the life histories and
REPRODUCTIVE PHENOLOGY OF MEDITERRANEAN SEAGRASSES
359
physiological requirements suggests that P. oceanica is a "competitive" plant or "biomass storer", Z. noltii a "ruderal" and C. nodosa seems to be a ruderal or a competitive plant. However, more studies, aimed at clarifying the adaptive processes that allowed the evolution of these plants and the ability to live in Mediterranean areas, are required. ACKNOWLEDGEMENTS
We are indebted to colleagues of the Oceanographic Laboratory of the Stazione Zoologica for the temperature data. Thanks are due to Maurizio Lorenti for his collaboration during the SCUBA diving observations, and Antonio Rando for his assistance in field activities. The authors gratefully acknowledge Dr. Gilberte Caye and Dr. Alexander Meinesz for providing C. nodosa seeds from Antibes (France).
REFERENCES Benacchio, N., 1938. Osservazioni sistematiche e biologiche sulle Zosteraceae dell'alto Adriarico. Thalassia, 3 (3): 2-41. Bornet, E., 1864. Recherches sur le Phucagrostis major Cavol. Ann. Sci. Nat. Ser. Bot., 1: 5-51. Boudouresque, C.F., Jeudy De Grissac, A. and Olivier, J., 1984. International Workshop on Posidonia Beds. G.I.S. Posidonie, Oceanica, 1. 454 pp. Boudouresque, C.F., Meinesz, A., Fresi, E. and Gravez, V., 1989.2nd International Workshop on Posidonia oceanica Beds. G.I.S. Posidonie, Oceanica, 2, 322 pp. Buia, M.C. and Piraino, S., 1989. Record of a Posidonia oceanica (L.) Delile seedling in the Egadi Island (Sicily, Italy ). Posidonia Newsl., 2 (2): 19-22. Buia, M.C., Cormaci, M. Furnari, G. and Mazzella, L., 1985a. Osservazioni sulla struttura delle praterie di Posidonia oceanica (L.) Delile di Capo Passero (Siracusa) e studio della macroflora epifita delle foglie. Boll. Accad. Gioenia Sci. Nat., 18: 463-484. Buia, M.C., Mazzella, L., Pirc, H. and Russo, G.F., 1985b. Fioritura di Zostera noltii Hornem. a Ischia (Golfo di Napoli). Oebalia, 11, N.S.: 861-862. Buia, M.C., Mazzella, L. and Russo, G.F., 1985c. Fenomeni riproduttivi della Cymodocea nodosa (Ucria) Aschers. in rapporto alia struttura della prateria. Oebalia, 11, N.S. :377. Buia, M.C., Mazzella, L., Russo, G.F. and Scipione, M.B., 1985d. Observations on the distribution of Cymodocea nodosa (Ucria) Aschers. prairies around the Island of Ischia (Gulf of Naples). Rapp. Comm. Int. Mer M6dit., 29 (6): 205-208. Buia, M.C., Russo, G.F. and Mazzella, L., 1985e. Interrelazioni tra Cymodocea nodosa (Ucria) Aschers. e Zostera noltii Hornem. in un prato misto superficiale dell'isola di Ischia. Nova Thalassia, 7: 406-408. Buia, M.C., Zupo, V. and Mazzella, L., 1991. Primary production and growth dynamics in Posidonia oceanica. P.S.Z.N.I. Mar. Ecol., in press. Caye, G. and Meinesz, A., 1984a. Observations sur la floraison et la fructification de Posidonia oceanica dans la baie de Villefrance et en Corse du Sud. In: C.F. Boudouresque, A. Jeudy de Grissac and J. Olivier (Editors), International Workshop on Posidonia oceanica Beds, GIS Posidonie, Marseille, pp. 193-201. Caye, G. and Meinesz, A., 1984b. Floraison et fructification des phan6rogames marines
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M.C. BUIA AND L. MAZZELLA
Cymodocea nodosa (Ucria) Ascherson et Zostera noltii Hornemann ~ Port-Cros (France). Trav. Sci. Parc nation. Port-Cros, Notes br6ves, 10:153-156. Caye, G. and Meinesz, A., 1985a. Observations on the vegetative development, flowering and seeding of Cymodocea nodosa (Ucria) Ascherson on the Mediterranean coasts of France. Aquat. Bot., 22: 277-289. Caye, G. and Meinesz, A., 1985b. Evaluation de la longevit6 des rhizomes de Cymodocea nodosa d'apres les variations cycliques de la longeur des entre-noeuds. Rapp. Comm. Int. Met Mddit., 29: 187-188. Caye, G. and Meinesz, A., 1986. Experimental study of seed germination in the seagrass Cvmodocea nodosa. Aquat. Bot., 26: 79-87. Caye, G. and Rossignol, M., 1983. Etude des variations saisonni6res de la croissance des feuilles et des racines de Posidonia oceanica. Mar. Biol., 75: 79-88. Cinelli, F. and Salghetti-Drioli, U., 1983. Observations en plongde sur les peuplements a Penicillus capitatus et sur la floraison de Posidonia oceanica de l'Ile d'Elbe (Mdditerrande Occidentale). Rapp. Comm. Int. Mer Mddit., 28(8): 169-170. Colantoni, P., Gallignani, P., Fresi, E. and Cinelli, F., 1982. Patterns ofPosidonia oceanica (L.) Delile beds around the Island of Ischia (Gulf of Naples) and in adjacent waters. P.S.Z.N.I. Mar. Ecol., 3: 53-74. Cooper, G., 1979. Posidonia oceanica: un arbre. Jardinier de la Mer, 3: 1-65. Den Hartog, C., 1970. The Seagrasses of the World. North-Holland, Amsterdam, 275 pp. Den Hartog, C., 1977. Structure, function, and classification in seagrass communities. In: C.P. McRoy and C. Helfferich (Editors), Seagrass Ecosystems: a Scientific Perspective. Marcel Dekker, New York, pp. 89-121. Den Hartog, C., Hennen, J., Noten, Th.M.P.A. and van Wijk, R.J., 1987. Chromosome numbers of the European seagrasses. Plant Syst. Evol., 156: 55-59. Durako, M.J. and Moffier, M.D., 1987. Factors affecting the reproductive ecology of Thalassia testudinum (Hydrocharitaceae). Aquat. Bot., 27: 79-95. Frad~ Orestano, C., Calvo, S., Abbadessa, P. and Aric6, S., 1989. Fioritura e fruttificazione di Posidonia oceanica nella Baia di San Nicola (Palermo). Oebalia, 15, N.S. :137-144. Gambi, M.C., Russo, G.F. and Chessa, L.A., 1984. Fioritura de Posidonia oceanica (L.) Delile in una prateria superficiale della rada di Porto Conte (Sardegna Nord-Occidentale). Rend. Sem. Fac. Sci. Univ. Cagliari, 54 (Suppl.): 189-196. Giaccone, G. and Calvo, S., 1980. Restaurazione del manto vegetale mediante trapianto di Posidonia oceanica (Linneo) Delile. Risultati preliminari. Mere. Biol. Marine e Oceanogr., Suppl. 10:207-211. Giaccone, G. and Sortino, M., 1974. Zonazione della vegetazione marina delle Isole Egadi (Canale di Sicilia). Lav. 1st. Bot. Giardino Colon Palermo, 25:165-183. Giraud, G., 1977. Contribution ~ la description et/l la phdnologie quantitative des herbiers de Posidonia oceanica (L.) Delile. Th6se, Universit6 d'Aix-Marseille. Giraud, G., Boudouresque, C.F., Cinelli, F., Fresi, E. and Mazzella, L., 1979. Observations sur l'herbier de Posidonia oceanica (L.) Delile autour de l'Ile d'Ischia (Italie). G. Bot. ltal., 113: 261-274. Grime, J.P., 1974. Vegetation classification by reference to strategies. Nature, 250:26-31. Hootsmans, M.J.M., Vermaat, J.E. and van Vierssen, W., 1987. Seed-bank development, germination and early seedling survival of two seagrass species of The Netherlands: Zostera marina L. and Zostera noltii Hornem. Aquat. Bot., 28: 275-285. Jacobs, R.P.W.M., 1982. Reproductive strategies of two seagrass species (Zostera marina and Z. Noltii) along west European Coasts. In: J.J. Symoens; S.S. Hooper and P. Comp6re (Editors), Studies on Aquatic Vascular Plants. Royal Botanical Society of Belgium, Brussels, pp. 150-155. Kautsky, L., 1988. Life strategies of aquatic soft bottom macrophytes. Oikos, 53:126-135. Mazzella, L. and Ott, J., 1984. Seasonal changes in some features of Posidonia oceanica (L.)
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