The benthic algal communities of flats and salt marshes in the Grevelingen, a sea-arm in the South-Western Netherlands

Netherlands Journal of Sea Research 5 (1) : 20-49 (1970)

THE BENTHIC ALGAL COMMUNITIES OF FLATS AND SALT MARSHES IN THE GREVELINGEN, A SEA-ARM IN THE SOUTH-WESTERN NETHERLANDS* by P. H. N I E N H U I S

(Delta Institute for Hydrobiological Research, Yerseke, The Netherlands) CONTENTS I. II. III. IV.

V° VI. VII. VIII. IX.

Introduction . . . . . . . . . . . . . . . . . Material, m e t h o d s a n d terminology . . . . . . . . . . . T h e environmental factors . . . . . . . . . . . . . T h e vegetation . . . . . . . . . . . . . . . . A. T h e vegetation on shoals, sand a n d m u d flats in the sublittoral region a n d the lower p a r t o f the eulittoral region . . . . . . . . A. 1. Enteromorpha prolifera--E, linza sociation . . . . . . . . A. 2. Microvegetation i n a n d on shells o f molluscs a n d barnacles A. 3. EnWtomorpha--~ladophora c o m m u n i t y in sea-grass meadows A. 4. Ulva rigida and U. ta.tuca--Furus vesi~ulosus f. mytili sociation . . B. T h e vegetation on flats a n d salt marshes in the u p p e r p a r t of the eulittoral region a n d the supralittoral region . . . . . . . . B. 5. Fucus oesiculosus f. volubilis sociation . . . . . . . . . B. 6. Bostry¢hia scorpioides sociation . . . . . . . . . . . . B. 7. Vautheria thuretii--V, sphaerospora sociation . . . . . . . B. 8. Blidiagia minima sociation . . . . . . . . . . . . B. 9. Vernal Ulothrixsoeiation . . . . . . . . . . . . B. 10. Communities d o m i n a t e d by ~ / a n o p h y c e a e . . . . . . . B. 11. General Oalorophyceae c o m m u n i t y . . . . . . . . . B. 12. Vegetation in salt-marsh pools . . . . . . . . . . Some notes on the genus Enteromorpha . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . .

20 21 23 24 25 25 26 26 27 30 31 32 33 34 34 35 38 39 39 42 44 45 47

I. I N T R O D U C T I O N

The Deltaplan aims at the closing of sea-inlets in the south-western part of the Netherlands, primarily with the object to guarantee the safety of the population and avoid repetition of the flood disaster of 1953. It is the task of the Delta Institute to observe the changes in the composition of the flora and fauna resulting from the closure of * C o m m u n i c a t i o n no. 86 of the I ~ l t a Institute for Hydrobiological Research, Yerseke, T h e Netherlands.

A L G A L COMMUNITIES

21

the river-outlets to the North Sea, and to study the causes of these changes. To this end a survey, as complete as possible, of the vegetable and animal world will be a necessary requirement (VAAS, 1961). The purpose of this paper is to give a qualitative and quantitative survey of the benthic green, brown, red and bluegreen algae of the m u d and sand flats, mussel-banks and salt marshes in the Grevelingen, a sea-arm to be closed at both ends in the near future. Afterwards this area will turn into a tideless fresh-water lake. The epilithic vegetation of dikes, jetties and other kinds of embankments will not be discussed in this paper. Some notes on this component of the algal vegetation can be found in NIENHUIS (1968) and VAAS (1968). No studies on the algal vegetation of the Grevelingen have been published to date. Moreover, extensive literature about algae on salt marshes and flats in the Netherlands is very scarce. Scattered data can be found in BE~rTmK (1958, 1965), VAN GOOR (1923), DEN HAgTOG (1952, 1954, 1955a, 1959), VAN DEN HOEX (1958a, 1963) and KOSTER (1952).DEN HARTOG (1955b, 1956, 1958a, 1958b)and KOSTER (1954, 1955) give more detailed information. II. MATERIAL, METHODS AND TERMINOLOGY

Field-work was done from October 1965 till August 1968, with m a n y interruptions. Most localities were easily accessible at low tide from the shore. The research vessel "Jan Verwey" was used for work on the sand-banks and flats, exposed at low tide; the permanently submerged vegetation was sampled with an oyster dredge from the ship. Fig. 1 gives a survey of the sampling localities, indicated in the text. At m a n y places phytosociological sample-plot analyses were made according to the combined methods of BRAUN-BLANQUET (1951) and DOING KRAFT (1954). The combined abundance and dominance of the plants at a certain sample-plot was expressed in the following scale: r = very sporadic, p = few, a ~ rather abundant, m = abundant, in all cases cover less than 5%; 01 = cover 5 - 15% of the sample-plot, 02 = cover 15 - 25%, and so on to 10 = cover 95 - 100%. The "degree of presence" indicates the percentage of the studied sample-plots of a certain algal community in which the species considered has been observed. The phytosociological results are listed in Table I. The numbers and characters in the columns 1-7 of Table I should be interpreted in the following way: the symbols placed in brackets indicate the lowest and the highest values of the cover in the sample-plot analyses. The number before the first bracket indicates the degree of presence; v/z. first line, column 1 : 70(r-03) ; 70 = the degree of presence; (r-03) = range of the cover. The degree of presence and the range of the cover of the dominating species have been underlined with a solid line, the codominating species with a dotted line.

22

P.H. NIENHUIS

Fig. 1. Survey of the salt marshes (coarse dots) and the sand and mud flats (fine dots) in the Grevelingen; situation at MLWS. Sp. ~ Springersgors; Flak. ----Slikken van Flakkee; Died. = salt marsh off Polder Diederik; He. -- salt marsh between Herkingen and Battenoord; 13o. = salt marsh off Polder Nieuw Bommenee; Ho. = Hompelvoet; Ve. = Veermansplaat; Spr. = Springersdiep; Bro. = Brouwershavense Gat; Grey. dam = Grevelingendam. As to very small algae, the analysis o f the sample-plots was carried out in the l a b o r a t o r y u n d e r the microscope, using samples t a k e n at r a n d o m from small squares, being dug out o f a n a p p a r e n t l y homogeneous vegetation. T h e vegetation units distinguished here are not only based o n these q u a n t i t a t i v e data, but also on m a n y a d d i t i o n a l facts. T h e physico-chemical d a t a were placed at m y disposal b y the divisions " P l a n k t o n " and " C h e m i s t r y " o f the Delta Institute. T h e algal material was conserved in 4 % sea-water formalin, and p a r t o f it was dried. T h e algae are kept in the h e r b a r i u m o f the Delta Institute. Some species have been cultivated in an " E r d - S c h r e i b e r " m e d i u m (VAN DEN HO~K, 1963) in petri-dishes, in order to elucidate t a x o n o m i c a l problems. Besides the papers m e n t i o n e d separately, those o f BLIDING (1963: Blidingia a n d Enteromorpha), VAN DEN HOEK (1963 : Cladopkora), V~.NKATARAMAN (t961 : Vaucheria), GOMONT (1892: "Oscillarides"), BORNET & FLAHAULT ( 1959 : "Nostocacdes h d t d r o c y s t ~ s "), GzrrLER ( t 925 : C y a n o p h y c e a e ) , LINDSTEDT (1943: C y a n o p h y c e a e ) , and DROUST & DAILY (1956 : coccoid C y a n o p h y c e a e ) were used for identifying difficult

23

ALGAL COMMUNITIES

species. Moreover, several samples of bluegreen algae have been compared with specimens in the Rijksherbarium at Leiden. The explanation of some terms used in this paper is as follows: c o m m u n i t y - - a n y abstractly defined vegetation unit, sociadon--plant community containing at least one species or genus with a high degree of presence, and consisting of one or more layers with one dominant in each layer (modified after WSSrHOFF (1951) and DEN H A R T O G (1959). The coastal area can be divided into three regions: supralittoral region--belt between the upper limit of surf and spray, and the mean high-water line (MHW), eulittoral region--belt between the m e a n high-water line and the m e a n low-water line at spring-tide (MLWS), sublittoral region--belt between the mean low,water line at springtide and the line below which no algal growth is possible. III. T H E E N V I R O N M E N T A L

FACTORS

The Grevelingen is a collective name for the waters Brouwershavense Gat, Springersdiep, Hals and Grevelingen. This sea-arm is situated in the south-western part of the Netherlands (51040 ' to 51050 ' NB and 3050 ' to 4°10 ' EL). Before 1964 the Grevelingen formed a part of the Rhine-Meuse estuary, but in 1964 this water was dosed off by a dam at its landside (Grevelingendam; Fig. 1). In 1971 the Grevelingen will be closed at the seaside as well, becoming a tideless water basin. The construction of this d a m started in 1965 and part of it is already rising above the water-level. As all the sea-arms in the SW Netherlands, the Grevelingen is characterized by a system of gullies and fiats, built up of silt and sand. At M L W S more than half of the area is exposed. The sea-arm is about 25 km long and has a width varying from 5 to 10 km. Along the whole coastal strip we find man-built embankments and jetties. Only the most western part of the coast-line has been formed by dunes. The highest situated areas outside the dikes (above M H W ) consist of brackish meadows and salt marshes. The salt marshes are especially to be found at the north side of the Grevelingen. The most important ones to be discussed further are the Springersgors, the salt marsh south of Stellendam, Polder Diederik salt marsh, salt marsh between Herkingen and Battenoord and, at the southern side, the salt marsh at Polder Nieuw Bommenee. The Springersgors deserves a special mentioning, owing to its very differentiated vegetation. A part of this marsh, situated at the foot of the dunes, forms a beach plain. Only the larger fiats were investigated, Slikken van Flakkee, Hompelvoet and Veer-

24

P. H. N I E N H U I S

mansplaat (Fig. 1). Owing to their large extension the mussel-banks hold a special place. Roughly estimated, 20 - 30% of the bottom of the Grevelingen is occupied by mussel beds, exploited or not, from about M L W N downwards (Fig. 2). The bottom of the Grevelingen consists for the greater part of fineto very fine- grained sands. The average tidal differences in the Grevetingen amount to about 2.5 to 3 m; these have shown only minor changes in consequence of the construction of the Grevelingendam. Since 1964 t h e velocity of the water currents in the eastern part o f t h e former estuary was reduced to nearly zero. I n the period of.lanuary 1964 to July 1967 the temperature of the surtkce water varied between 0 ° C and 22 ° C (measured monthly or bimonthly). In the same period the temperature of the air varied between about 1° C and 19 ° C (measured daily and given as monthly averages, at Nieuwe Tonge on the isle of Goeree Overflakkee, 1.5 m above the earth; data furnished by the Royal Meteorological Institute (K.N.M.I.), De Bilt). As regards the salinity of the water the whole Grevelingen can be classified as belonging to the polyhalinicum (10 - 16.5%o CI'). Since 1964 the mean chlorinity of the surface w a t e r - a t an average river discharge, at half t i d e - v a r i e d between 15~oo in the eastern part to 16.5~00 in the most western part of the sea-arm. The pollution of the water is relatively insignificant. The coastal area is very sparsely populated and industry of some importance is not present. IV. THE VEGETATION The algal vegetation on the salt marshes and the flats can be divided into two categories: A. The vegetation on shoals, sand and mud flats in the sublittoral region and the lower part of the eulittoral region. B. The vegetation on the sand and mud flats and the salt marshes in the upper part of the eulittoral region and the supralittoral region. Studying the algal vegetation, a number of vegetation units could be d i s t i n ~ e d in which one or more species are dominating. As far as possible the limitation of the different algal communities, suggested by CHAPM,~N (1964), was followed. Concerning the phanerogam communities the nomenclature of BssrTXNK (1965) was used.

25

A L G A L COMMUNITIES

A. T H E V E G E T A T I O N O N S H O A L S , S A N D A N D M U D F L A T S IN THE SUBLITTORAL REGION AND THE LOWER PART OF THE EULITTORAL REGION

A.1.

ENTEROMORPHA

PROLIFERA

--

E.

LINZA

SOCIATION

A large part of the flats consists of fine-grained sand. On this substratum several Enteromorpha species come to the fore (Figs. 2 and 3; Tables I and II). Their degree of covering is highly determined by the presence of possibilities for attachment, nearly always shells of molluscs, dead or alive (a.o. Cardium edule). So a large quantity of shells results in a large covering of algae. It is noteworthy that Enteromorpha is often attached to barnacles, being attached in their turn to cockle shells, mostly alive. Lmr,~ (1939) observed the same phenomenon at the tidal flats in northern Germany. Around the low-water line an increase of the concentration of shells can often be found, and consequently the covering of algae can increase to 90%. On this level Ulva spp., C,eramium rubrum, Polysiphonia violacea and Bryopsis plumosa can be found in small quantities among the Enteromorpha species. This sociation goes on some metres below the low-water line, as was proved by dredging. This kind of vegetation covers large areas. In sheltered places vast Enteromorpha "meadows" may develop. In more exposed localities, such as the seaward-directed parts of the sand flats, where coarse-grained sand and shell-grit have been deposited, the environment is too unstable to permit algal growth of some importance. Besides the algae growing on solid substrata, there are some species anchored in the loose sandy soil. Especially the very common Enteromorpha prolifera ssp. radiata is firmly interwoven with the sediment, in dense bundles. Probably the spores of this alga germinate on solid and stable substrata (viz. shells and small stones). Afterwards the small plants will be detached from their bases and will grow on vegetatively, partly buried in the sand. In the eulittoral region E. prolifera ssp. radiata may completely cover many square metres. The subspecies mentioned is rarely found attached to shells. Some remarkable differences exist between the summer aspect of the vegetation described above, and the winter aspect. In the latter period Dumontia incrassata and Petalonia.fascia can be found as scattered plants, whereas the larger part of the Enteromorphavegetation, attached to shells, disappears in winter. This disappearance is probably caused by the effect of the autumnal gales, churning up the upper layer of the sediment, tearing off the algae and washing away the shells. Enteromorpha prolifera ssp. radiata, at many places basically interwoven with the sandy substratum, can less easily be removed. In winter the

26

P. H. N I E N H U I S

sand flats are mostly devoid of algae, but often subspecies radiata is still growing on slightly higher spots, where the sediment is more stable as a consequence of the algal growth. A.2.

MICROVEOETATION

IN AND ON SHELLS OF

MOLLUSCS AND BARNACLES

At the sand flats the shells o f - m o s t l y dead-molluscs a n d adhering barnacles house some species partly perforating the lime, and causing the green to brown-black cover on or in the shells. Due to taxonomical problems no special attention was paid to these time-boring algae. Moreover, the identification of the species is often hampered by a dense carpet of Enttromorpha- and Ulothrix-like germlings. The species distinguished on and in the p a r t y decalcified shells are mentioned in Table II. The lime-boring algae are known as a well delimited group (LTNDSTEDT, 1943). VAN DEN HOgK (1960) distinguished this vegetation type on cockle shells in the lagoons of southern France, which community has Entophysalis deusta, Gomontia polyrhiza and Lyngbya irtfixa ( = Schizothrix calcicola p.p.) in common with the community in the Grevelingen. VAN DEN HOEX (1958) also described the algal micro.vegetation in and on barnacle shells on the Dutch and French coasts. We found several species mentioned in his paper. A.3.

ENTEROMORPHA--CLADOPHORA

COMMUNITY

IN SEA-GRASS MEADOWS

O n the fine-grained sands, where we distinguished the communities A 1 and A 2, sea grasses are relatively scarce. This picture is different o n sheltered spots where the soil is more silty. Here a gradual transition takes place from the Enteromorpha prolifera-E, linza sociation to the sea-grass meadows (Fig. 3). Zostera marina var. stenophylla occurs in the south-western part of the Netherlands at silty, mostly soft soils in the eulittoral region from the low-water line upwards to 30-I50 cm below M H W whereas Zostera noltii grows at firmer and mostly higher parts of the flats in the eulittoral region from about half tide up to t5-70 cm below M H W (BESFTm~, 1965). According to BE~aNK (1965) the Zosteretum marinae stenophyllae often forms a mosaic with the Zosteretum nanae in the upper part of their areas. This picture is most conspicuous at the mud flats along the border of the Grevetingen, but on the isolated shoals, at all sides surrounded by water (Hompelvoet, Veermansplaat) the two species of sea grasses grow together at m a n y places, apparently in disorder.

ALGAL

GOMMUNITIES

27

Except the epiphytic Ascocydus magnusii, and the loose-lying Glado. phora globulina, this community includes no characteristic species. We can often find elements of vegetation unit A 1 (Enteroraorpha species), on shells as well as growing epiphytically on the sea grasses. Looselying algae, probably washed in from other localities may be of local importance (Cladophora, Chaetomorpha, Fucus). A number of red and brown algae can be found, living epiphytically on the leaves of Zostera. These species, however, grow epilithically at many other places in the littoral region. In very dense sea-grass fields the number of epiphytes and accompanying algae is very small. On account of the high percentage of Enteromorpha and Cladophora species, it was decided to call this community "Enteromorpha-Cladophora community in sea-grass meadows" (Fig. 3; Tables I and II). VAN GOOR (1923) distinguished a "Zostera - red algae vegetation" and a "Zostera - green algae vegetation" with several species growing on and among the Zostera marina plants in the Waddenzee (N Netherlands). Most species, however, proved to be unconnected with the sea-grass vegetation. Only Mdobesia jelolisii Rosan was encountered exclusively on the leaves of Zostera. NI~.NBtlRO (1927) recorded this crustaceous species from Zostera marina in NW Germany. COTTON (1912) and R~.~s (1935) described a Zostera community at the coast of Ireland with many associated algae, also occurring in other communities. DnN HARTOO (1958) did not mention any characteristic algal species in the Zosteretum nano-stenophyllae of the Balgzand (Wadden area, N Netherlands). None of the algal species found by him was restricted to this sea-grass vegetation. Except for Ascocyclus magnusii this is in accordance with the situation in the Grevelingen. A.4.

ULVA

RIGIDA

VESICULOSUS

A N D U. L A C T U C A - F U C U S f. M Y T I L I

SOCIATION

The extensive mussel-beds in the Grevelingen are found at very silty places (Figs. 2 and 3). They are adjacent to the higher situated Zostera fields, preferring a soil which contains also a large quantity of silt. The mussel-banks in the lower part of the eulittoral region harbour a characteristic vegetation (Tables I and II), also noticed by NIZNBURG (1925, 1927, 1932) in northern Germany and by DEN H A R T O G (1958) in the northern part of the Netherlands. The dominating alga is a Fucus species, mostly sterile and proliferating, with an undulating or spirally twisted thallus, hardly ever with air bladders, and never with rhizoids. A remarkable point of most Fucus thalli is the attachment to the substratum by the byssus-threads of mussels. The plants differ from Fucus growing between the phanerogams of the salt mar-

28

P.H. NIENHUIS

shes by their larger dimensions. NI~NI~JRO (1925, 1927, 1932) went deeply into the problems of morphology and ecology of this Fucus. NX~NBURO(1927)concluded that hisFucus is probably an adaptation of F. vesiculosus to silt-inhabitation; afterwards he raised this alga to a specific status: Fucus mytili Nienburg (NxENBURO, 1932). One of the principal characteristics of this new species is that the - r a r e - female receptacula grow on vegetatively at their tips. This character was never observed in the Grevelingen material. A few times, however, Fucus plants were found, attached with byssus-threads, with very large, flat, anomalously developed receptacula. The contents of the conceptacula consisted in some cases of antheridia; a few other plants were hermaphrodite. The sterile rim around the receptacula, characteristic for Fucus spiralis, was in one hermaphroditic plant totally absent and in an other very vaguely present. I can corroborate the remark of DEN H~a~ToG (1959: 182), who discussed the occurrence ofF. mytili in the Netherlands, t h a t " F , mytili is merely an anomalously developed form of the dioecious F. vesiculosus." I propose to call the Fucus form under discussion Fucus vesiculosus f. m_~tili (Nienburg) forma nova. Particular plants however, better could be named hybrids ofFucus vesiculosus and F. spiralis. Although F. vesiculosus var. evesiculosus Cotton is reported by CHAPMAN (1937) from low-lying mud fiats at Norfolk, growing among mussels, it should be stated here that the name "f. evesiculosus" (= f. linearis (Huds.) Powell; POWSLL, 1963) should be reserved for the bladderless forma occurring on exposed rocky coasts, as CoTroN (t912)originatly intended. Both Ulva lactuca and Ulva rigida, raised to specific status (PARKE & DIXON, 1964), Occur at the mussel-beds, often attached with byssusthreads to the substratum. It is difficult to separate the two species. Thalli exceeding a thickness of 60 Ez,with the cells much longer than wide, are classified as U. rigida. Samples collected from mussel-beds showed that the cover of Fucus vesiculosus decreases rapidly in the subIittoral region. Ulva spp., however, occur very abundantly at the sublittoral mussel-banks, especially in the extremely sheltered eastern part of the Grevelingen. In Fig. 2 a survey is given of the most prominent habitats in the Grevelingen where benthic algae (excluding diatoms) play an important role. Data have been borrowed from the survey of Mr. W . J . Wolff c.s. (Delta Institute, Yerseke) who investigated the qualitative distribution of some animal and plant species in the Grevelingen in 1967, in relation to the grain-size distribution of the sediments (unpublished).

A L G A L COMMUNITIES

29

Fig. 2. A survey of the most prominent habitats in the Grevelingen where algae play an important role.

Further data have been derived from the work of Mr. R. Peelen (Delta Institute, Yerseke), who constructed a map of the Grevelingen showing the distribution of the mussel-lots (unpublished). Fig. 2 only pretends to give an impression of the distribution of a number of habitats. More exact data about the densities of the algal vegetation cannot be concluded from this map. The Ulva rigida and U. lactuca-Fueus vesiculosus f. mytili sociation is restricted to the mussel-banks (Mytilus edulis). Especially in the very sheltered eastern part of the Grevelingen large mussel-beds occur in the sublittoral region, at very silty places. At higher situated areas, where the soil is still rather silty, Zostera noltii and Zostera marina occur. These species also show their most extensive distribution in the eastern part of the Grevelingen. The Enteromorpha-Cladophora community is confined to the habitat of the sea-grass meadows. The Enteromorpha vegetation, occurring on fine-grained sand, comprises the Enteromorpha prolifera-E, linza sociation. Going westwards, at the more exposed and unstable parts of the flats, a distinct Enteromorphavegetation cannot be found any more. The differences between the western, more exposed part with rather coarse-grained sediments, and the eastern, very sheltered part of the Grevelingen are very evident.

30

P.

H.

NIENHUIS

Fig. 3 shows the vertical and horizontal distribution of the algal communities discussed before, correlated with the kind of substratum at which they occur. The salt-marsh algal communities will be mentioned in the next chapter. r, SUPRA -

SALT - M A R S H

LITTORAL

ALGAL COMHLINn+IES SEE CC-~E 4

EULITTORAl.

SUB LITTORAL

REGION

~

-

~,NSO SANO ANO SHIELL- ORIT

Fig. 3. Scheme of the horizontal and vertical distribution of the algal communities on flats and salt marshes in the Grevelingen, in relation to the types of substratum. B. THE V E G E T A T I O N ON FLATS AND SALT MARSHES IN THE U P P E R PART OF THE E U L I T T O R A L R E G I O N AND THE S U P R A L I T T O R A L R E G I O N Covering a relatively small area of the Grevelingen, the salt marshes form a differentiated habitat with, likewise, a differentiated vegetation. The algal communities have mainly been delimited in the following associations of phanerogams, named in sequence of their levels with respect to the tides: SaIicornietum strictae, Spartinetum townsendii, PuccineUietum maritimae (including the terminal phase with Limonium vulgare), Halimionetum portutacoidis, Juncetum gerardii and Artemisietum maritimae-nomenclature according to B g s r r m x (1965, 1966). Spartina townsendii has a very large distribution in the Grevelingen. Therefore, in many of the sample-plot analyses Spart/na is represented. A number of algal communities, distinguished for the salt marshes of England ( C ~ T s R , 1932, 1933; CHAPMAN, I937, 1960), Ireland (COTTON, 19t2; REES, 1935) and even for the north-eastern coast of N America ( C H A I ' ~ , 1960) could also be delimited for those of the Grevelingen.

31

ALGAL COMMUNITIES

As many as 8 communities of algae have been distinguished, and it has to be emphasized here that not all aspects of the algal vegetation could be dealt with thoroughly. Only the summer aspect was studied fairly comprehensively. Moreover, owing to difficulties of identification, no complete list of bluegreen algae and Vaucheria species can be given in this paper. Most of the data from the literature discussed here, were used by CHAPMAN(1964) in his concept about nomenclatural rules for saltmarsh algal communities. It remains difficult, however, to interpret the "associations" and "sociations" respectively distinguished by Paxou & SEaPEa~rE (1954) for sandy biotops along the coast of Bretagne (France) and by H;~YR~N (1956) for salt marshes in Sweden and Finland. B.5. Fucus

VESICULOSUS

f. V O L U B I L I S

SOCIATION

Although a certain overlap between the communities B 5 and B 6 exists, there are reasons to separate them (Tables I and II). Fucus vesiculosus f. volubilis ( ~ var. lutarius) occurs at lower situated places of the salt marshes than Bostr)chia scorpioides, for instance in the marshy Spartinetum or in moist depressions of the Salicornietum. In the higher Puccinellia maritima-Limonium vulgate vegetation forma volubilis hardly occurs, whereas Bostrychia is common in such places. In the Grevelingen Fua~s has never been found in the Halimionetum of creek banks (Fig. 4). The covering is often high, but the vegetation is rather monotonous and the companion species are quantitatively subordinate (Table I). Wherever Spartina towns~ndii is growing very densely the forma is absent, probably due to the limiting influence of the light. BEEFrINK (1965) also drew attention to the importance of this factor. Loose-lying plants of Fucus vesiculosus f. volubilis can be found on the mud between the phanerogams. The thallus is undulating or spirally twisted and proliferating; air bladders and rhizoids have never been observed. In a few cases small, warty receptacula were found, male as well as female. The sociation occurs at several places at the northern side of the Grevelingen (Springersgors, salt marsh south of Stellendam, salt marsh off Polder Diederik). According to BAKER (1912) and BAKER & BOHLINO (1916) Fucus vesiculosus megecad limicola ecad volubilis includes F. lutarius Kiitz. ( = F. vesiculosus var. lutarius Chauv.), whereas the smaller turf-like forms (ecad caespitosus) include F. balticus Ag. ( = F. vesiculosus var. baltica), a form distributed in northern Europe. Following POWELL (1963), most of the marsh forms ofFucus vesiculosus might be designated as f. volubilis, better than to maintain the later name f. lutarius. KOSTER

32

P. H. N I E N H U I S

(1952, 1954) and D~N HARTOG (1959) reported the alga from several localities in the SW Netherlands. According to DEN H~TOG (1959) F. vesiculosus var. lutarius reaches the northernmost limit of its distribution area in the Oosterschelde. KOST~R (I952) mentioned its occurrence, however, for the Grevelingen, situated northwards of the Oosterschelde. D~.N HARTOG (1959) himself observed strongly proliferated Fucus thalli on salt marshes in the northern Netherlands, resembling Fucus vesiculo. sus var. lutarius. Several authors distinguished a salt-marsh fueoid community: COTTON (1912) and R~Es (1935) in Ireland, CARTER(t 933b) and CHAPMAN (1937) in Great Britain. CHAPMAN(1964) proposed the name "Fucus limicola consocies" for this community. B.6.

BOSTRYCI-IIA

SCORPIOIDES

SOCIATION

Bostrychia scorpioides grows winding around the basal parts of halophytes, or is found loose-lying on the soil. Mostly the phanerogam vegetation is rather dense, but still some light can penetrate. A very dense vegetation does not permit any growth of Bostryckia. Generally spoken the Bostrychia community occurs on a higher level than the Fucus vesiculosus f. votubilis sociation, viz. in the Puccinellietum maridmae and Halimionetum portulacoidis (Fig. 4). Enteromorpha prolifira and E. intestinalis were often encountered as companion species. Parts of the soil covered with unbranched, loose-lying plants of Enteromorpha may form a mosaic with the entangled masses of Bostrychia (species composition Tables I and II). In the Grevelingen Bostrychia was found at the Springersgors, the salt marsh south of Stellendam, the salt marsh off Polder Diederik and in the island Hompelvoet. In the literature (CARTER, 1932, 1933a, 1933b; CHAPMAN, 1937, 1964; CoTroN, 1912; VSN HARTOO, 1956, 1959 and REIn, 1935) the combined occurrence of Bostlychia scorpioides and Ga~adla repens was often mentioned. Although this phenomenon was a~.~rtained at some localities in the SW Netherlands, Catcalls has never been met with on the salt marshes in the Grevelingen. In this aea-inletCateaella exclusively occurs between the boulders of the embankments, whereas Bostryekia was only found at salt marshes. For this reason the Bostrg~kia scorpioides sociation cannot be classified into the Catenella-Bosayekia consocies distinguished by CHAPMAN (1964). The distribution and the ecology of Bostryckia scorpioides in the Netherlands were amplydiscus~d by DSNHARTOO (I 955b, 1956, 1958a) and KOSTSR (1952, 1954, 1955).

ALGAL B.7.

VAUCHERIA

THURETII

COMMUNITIES -- V. S P H A E R O S P O R A

33 SOCIATION

On the rather steep, sandy walls and on the slightly inclining slopes of the creeks, almost without growth of phanerogams, as well as on the creek banks with Halimione portulaxoides an algal vegetation can be distinguished in which Vauchaia species are dominating (Fig. 4). This Vaucheriavegetation is able to cover fairly extensive areas (Springersgors) and appears to have an important silt-binding capacity. Although it is difficult to delimit this vegetation unit with respect to the General Chlorophyceae community, this sociation can clearly be outlined, especially at the lower parts of the marshes without a dense covering of halophytes (Tables I and II). Between Spartina towraendii, where the soil is very soft and muddy, the sociation does not occur. It cannot be found either among the phanerogams at the higher parts of the salt marshes and at the beach plains. It is hardly possible to identify the vegetative plants of Vaucheria. Mr. J. Simons (Amsterdam) kindly identified a number of my samples by means of culturing experiments. It appeared that Vaucheria thuretii and V. sphaerospora are the most important constituents of the sociation under discussion. Sometimes Vaucheria intermediajoins V. thuretii. Vaucheria intcrmedia, however, in combination with other algae, has its main distribution at--mostly higher-- parts of the marshes, overgrown with halophytes (see B 11 : General Chlorophyceae community). The apparently very rare Vaucheria vipera was found in this community on the Springersgors. This is the second record of this species from the European Atlantic coast, as reported by SIMONS& VROMAN (1968). For southern Ireland COTTON (1912) described a "Vaucheria thuretii association", covering extensive areas on muddy sand, especially in the lower part of the littoral region. For the Norfolk salt marshes CHAPMAN (1937) mentioned a Vaucheria thuretii community occurring on the banks of large creeks. The suggested nomenclature of CHAPMAN (1964) for salt-marsh algal communities comprises a "Vaucheria consodes", probably the same community as mentioned by him earlier (CHAPMAN, 1937). The silt-binding Vaucheria vegetation mentioned by DEN HARTOG (1958) from the Balgzand (N Netherlands) probably belongs to the Vaucheria thuretii-V, sphaerospora sociation. JORD~ & KLAV~STAD(1958) noticed the combined occurrence of Vaucheria thuretii and V. sphaerospora at Espegrend (Norway) on a muddy soil near highwater mark.

34

P. H. N I E N H U I S B.8.

BLIDINGIA

MINIMA

SOCIATION

The vegetation unit at the salt marshes in the Grevelingen in which Blidingia minima is dominating is an epiphytic community. Usually Blidingia minima is the only representative, sometimes accompanied by Blidingia marg;amta and Rhizodonium riparium (Table II). Blidingia is growing epiphyticallyon the basal parts of halophytes and on decaying leaves and stems. Detached, viable thalli of Blidingia can be found occasionally on the soil. These fragments show a strong tendency to grow out intestine-like in width. It should be noticed that the looselying plants of Blidingia have been classified among the General Chlorophyceae community. The Blidingia sociation was found on stems of Spartina townsendii, sometimes on the woody parts of the stalks of Salicorniaeuropaea or Aster tripolium, and exceptionally on basal parts of Pucdndlia maritima and Limonium vulgare. However, Blidingia species reach their optimum development on the wooden stems ofmnot too densemHalimione portulacoides stands (Fig. 4). This sociation is common on all salt marshes in the Grevelingen. Blidingia minima is not restricted to the salt marshes; it is also very common on embankments, forming a part of the epilithic Blidingietum minimae (D~N HARTOG, 1959). CARTER (1933) as well as CHAPMAN (1937) distinguished an Enteromorpka ( = Btidingia) minima community at salt marshes in England, where the species shows a preference for the stems of Halimione. CHAPMAN (1964) suggested the name "Enteromorpha minima socies". B.9.

VERNAL

ULOTHRIX

SOCIATION

An important spring aspect of the algal vegetation is the vernal Ulothrix soeiation. In winter swampy places or places covered with a thin layer of water are formed frequently on the higher parts of the marshes (v/z. in the Puccinellietum, in the Halimionetum and in the Juncetum gerardii). In late winter the Ulothrix vegetation develops in these localities, either floating or entangled with dead parts of higher plants. Ulothrix especially prefers small patches of soil, either bare or covered with detritus o f leaves and stems where no other algae are growing yet. At places where the perennial General Chlor0phyceae community grows with a high cover, UIothrix only plays a subordinate role. At the lower parts of the marshes (Spartinetum) only fragments of this type of vegetation occur, entangled with parts of phanerogams. In the course of spring the sociation gradually disappears and is replaced either by a dense stand of halophytes or by other algal

35

ALGAL COMMUNITIES

vegetation units, viz. the General Chlorophyceae community. Ulottlrix flacca is the dominating alga. Other species are Uloazrixpseudoflacca, U. subflaccida, Enteromorphaprolifera, Rhizodonium riparium etc. (Table II). CARTER (1933) and Cn~a'~oz~ (1937) distinguished an Ulothrix (flacca) community on British salt marshes, named by CRAPM~'~(1964) "vernal Ulothrix soeies". The Blidingietum minimae of DEN H~TOO (1959) includes the epilithic analogon of the Ulothrix sociation in the Netherlands. B.10. COMMUNITIES DOMINATED BY CYANOPHYCEAE Bluegreen algae occur on all levels of the salt marshes. Between the phanerogams, where wave action a n d currents h a r d l y play a n y role, a n d at the relatively stable parts of the m u d flats t h e y can be found locally, forming distinguishable patches in the vegetation. Especially on the higher parts of the salt marshes C y a n o p h y c e a e can show a high cover (Fig. 4). It appeared very difficult, however, to distinguish separate communities on account of d o m i n a t i n g bluegreen algae. T h e

m

i

g

I

l

J|

" '

i!

~

l

i ,8

i

i

Fig. 4. Horizontal distribution of the mlt-marsh algal communities in the Grevelingen. ]35 ~ Fucus ~siculosus f. volubilis sociation; B6 ~ Bostrychia scorpioid~s u~ation; B7 = Vauchzria thuretii--V, sphaerospora sociation; 138 ---- Blidingia minima sociation; B9 = Vernal U/othr/xsociation; B10 = Communities dominated by Cyanophyceae; B11 = General Caxlorophyceaecommunity; BI2 = Vegetation in salt-marsh pooh.

36

P. H. N I E N H U I S

limits between the "units" are very vague and it is often arbitrary where to put them. The members of the bluegreen algal vegetation hitherto ascertained are listed in Table II. It should be mentioned that for some species the concept of DROUET (1962, : 1963, 1964) was :followed; according to this author many species could be demonstrated to be ecological variants of a single species. Recently WZBBER (1967) used the same concept for the bluegreens of a Massachusetts salt marsh. On and in the bare silt at the higher parts of the Spartina townsendii vegetation a community of bluegreen algae in which Oscillatoria bonnemaisonii always occurs, can be distinguished at the Springersgors and at the salt marsh off Polder Diederik, especially in late summer. Oscillatoria bonnemaisoniiis a common alga in the soft mud oft_he lower parts of the marshes. Companion species are Oscillatoria limosa and 0. nigroviridis, together with scattered trichomes of Spindina spp., bundles of Microcoleus chthonoplastes and threads of Rlgzodonium riparium and Enteromorpha spp. Black-green, glimmering patches consisting of the dominating Anabaena torulosa,accompanied by Microcoleuschthonoplastes,Lyngbya aestuarii, Agmenellum quadrupIicatum, Schizothrix caldcola, and Rhizodonium riparium were found a few times on the soft mud of a Spartina townsendiivegetation and on the bare soil in a stand of TrigIochin maritima (Springersgors). KOSTER (1954) found Anabaena torulosa forming a closed vegetation between Puccinellia maritima (Oosterschelde, SW Netherlands). C~T~R (1933) distinguished an Anabaena torulosa community at the Canvey and Dovey salt marshes (England) in which also Nodularia harveyana was fairly frequent. CHAPMAN(1964) considered this Anabaena community as belonging to the "Gelatinous Cyanophyceae socies depending on permanence". An often found combination of bluegreen algae on the salt marshes is composed of Lyngbya aestuarii and Microcoleuschthonoplastes.Sometimes the community including both species can hardly be separated from the General Chlorophyceae community. The species especially occur on the higher parts of the salt marshes, at places strongly liable to changes in environmental conditions. They have their highest percentage of cover at the end of the summer. The combination, dominated now here by Microcoleus, now there by Lyngbya, is found on parts of beach plains (Springersgors) with a very open vegetation of halophytes, mostly scattered Salicornia europaea individuals. Further they occur as undergrowth between the phanerogams of open parts of grazed Puccinellion maritimae and Armerion maritimae meadows, and especially on treaded spots as e.g. the borders of foot-paths and cattle tracks. Lyngbya aestuarii can also be found without )¢lirrocoleus. At the

ALGAL COMMUNITIES

37

Springersgors and at the salt marsh off Polder Diederik a film of

Lyngbya aestuarii was observed, at some places covering a Vaucheriavegetation underneath Halimione portulacoides. Among Puccinellia rnaritima and Limonium vulgare a similar film was found on the soil. The opposite of the situation described above can likewise be met with: Microcoleus chthonoplusteswithout L~gbya aestuarii, e.g. at Battenoord in small drains intersecting saline meadows. According to the literature the combination of Lyngbya aestuarii and Mi~rocoleus chthonoplastesis widely known, e.g. CARTER (1933) for England, LINDSTEDT (1943) for the Swedish west coast, and KOSTER(1954) for the Netherlands. For Clare Island (Ireland) COTTON (1912) described a "Microcoleuschthonoplastesassociation" in which Lyngbya aestuarii played a subordinate role. For the Finnish and Swedish coasts H;~YPa~N (1956) mentioned a "Microcoleus chthonoplastes sociation" and, on the other hand a "Lyngbya aestuarii sociation" in which hardly any Microcoleus was found. In the lagoons of southern France VAn D~N HO,'K (1960) distinguished a "groupement ~ Cyanophyc~es flottantes, surtout Lyngbya aestuarii". In this community Microcoleusplayed a very subordinate role. There is not any unanimity in literature about the community in which the two bluegreen algae under discussion should be placed. H~YR~.N (1956) defined small units in which one of the two species predominated. Cx~AP~'~ (1937) distinguished a much larger "sandy Chlorophyceae community" in which, besides the dominating green algae Enteromorpha torta or Rhizodonium implexum Bart., some bluegreen algae were found. CARTZR'S (1933b) vegetation units are still more comprehensive in this particular case. She recognized a "General Chlorophyceae community" in which green algae dominated and Microcoleus chthonoplastes, Lyngbya aestuarii and some other bluegreen algae were locally common. It should be concluded that there are no sufficient reasons to put Lyngbya aestuarii and Microcoleus chthonoplastes together in a single sociation, although the two species are often linked in the field. At the highest parts of the Springersgors, at the foot of the dunes, only within reach of the highest spring floods, an aberrant community could be distinguished on the sand among the stunted phanerogams growing there. Schizothrix calcicolaplays an important role. Other algae to be mentioned are Calothrixspp., Anacystis spp. and Coccochlorisstagnina. When the sand dries out, the community flakes off and disappears almost completely, as was observed during the course of 1968.

38

P. H. N I E N H U I S

B.II.

GENERAL

CHLOROPHYCEAE

COMMUNITY

This preliminary name, adopted from C_zA.RTER(1933) and partly from CHAPMAN (1964), who spoke about the "General Chlorophyceae associes", covers a widely distributed community of algae on the real salt marshes of all parts of the Grevelingen. The most important, locally dominating components are Enterorr~rpha spp., Rtdcoclonium spp. and Vaucheria spp. (Tables I and II). Transitions to the vegetation types with G-hlanophyceae dominating occur frequently. The scheme of the horizontal distribution (Fig. 4) makes clear that notably on the higher parts of the salt marshes this community is the most conspicuous one. Rhizodonium riparium has been found on all levels of the salt marshes, often in small quantities as a companion species. Rhizacl~ium can hold a dominating position at the higher parts of the marshes and at the saline meadows, especially at open spots in the halophytic vegetation, viE. on places beaten by cattle or at small abrasion edges. The species may also occur as a closed mat at places scarcely covered with halophytes (e.g. Salieornia europaea), sometimes mixed with Percursaria p~rcursa. In winter and in spring the woolly mats of POtizoeloniura are very striking. Also Enteromarpha torta may predominate locally, e.g. on places where sods were cut from marshes (Battenoord), or in depressions of highly situated flats, where only a few halophytes are growing (Springersgors; Hompelvoet). Especially in early spring when the flowering plants are still poorly developed, large parts of the soil surface, between the phanerogams are covered with gnteroraorpha prolifera. A short note at the end of this paper refers to the taxonomic pitfalls and ecological problems involved in the study of this genus. Within the community under discussion Vaud~ria spp. may predominate too on the higher parts of the marshes. A few samples were cultivated and indentified by Mr. J. Simons (Amsterdam), showing that Vaueheria ¢oronata and V. intcrr~dia are quite common, e.g. at the Springersgors and at the salt marsh off Polder Diederik (of. also the Vaucheria thuretii-V, sphaerospora sociation). Vaucheria is oRen found together with Rhizoclonium, less often with Enteromorpha. It shows the tendency to grow underneath and among the higher plants, whereas Rhizoclonium prefers the open places in the vegetation.

ALGAL COMMUNITIES

B.12.

VEGETATION

39

IN SALT-MARSH POOLS

In the shallow pools and puddles, here and there present in the salt marshes and flats, an algal flora is encountered, and according to CHAPMAN (1937, 1964) this vegetation has to be considered as a separate unit (Fig. 4). The bottom of the pans consists of fine-grained sand with scattered small stones and shells. At some localities (off Polder Nieuw Bommenee, salt marsh between Herkingen and Battenoord) a part of the marshes was embanked. However, the vegetation occurring on the stony revetment of these embankments, as well as the algae growing on the artificially constructed stony slopes of the runlets, connecting the pools with the open water of the Grevelingen, are strictly epilithic and therefore beyond the scope of this paper. In some cases it is arbitrary where to put the limit between the epilithic algal component and the real pan flora. In fact many of the species occur in both biotopes. In late winter and spring Ulothrix species can be seen frequently in the very shallow pools, floating and entangled with phanerogamic detritus (cf. the Vernal Ulothrix sociation), succeeded by Cladophora sericea, Monostroma sp., Enteromorpha prolifera and E. torta. In deeper pools Enteromorpha linza and E. prolifera are the conspicuous species. On a solid substratum we can find Petalonia fascia, Scytosiphon lomentaria,

PilayeUa littoralis, Fucus vesiculosus, F. spiralis, Dumontia incrassata, Ceramium spp., gladophora spp., Enteromorpha spp. and some other taxa (Table II). The vegetation in very small isolated pools at the higher parts of the marsh is well characterized by the following sample-plot analysis: Monostroma cf. grevillei 05; Enteromorpha prolifera 02; Cladophora sericea 01 ; Petaloniafasda p; Pilaydla littoralisp ; surface area: 1 mS; depth of the water: 15 cm; date: 21 4 1966; locality: salt marsh off Polder Oud Herkingen. In this case Monostroma sp. is dominating, and in other eases Cladophora sp. may do so. In late summer the vegetation is poorer than in spring. Species such as Petalonia fascia and Dumontia incrassata have disappeared then and the genera Monostroma, Cladophora and Enteromorpha are on the decline. V. S O M E

NOTES

ON THE

GENUS

ENTEROMORPHA

Since BLmINO (1963) made order out of the confusion around this notoriously difficult genus, it is possible to distinguish the different species adequately. Without culturing experiments, however, it continues to be rather difficult to identify most species. Representatives of the genus Enteromorpka occur on all levels of the

TABLR

I

Enteromorpha linza Enteromorpha prolifera Enteromorpha torta + E. ralfsii Enteromorpha intestinalis Enteromorpha flexuosa Enteromorpha dathrata Enteromorpha spec, Ulva lactuca + U. rigida Cladophora serieea Cladophora globulina Cladophora spec. Chaetomorpha linum + Ch. crassa Fucus vesiculosus f. mytili Fucus vesiculosus f. volubilis Bostrychia scorpioides Vaucheria thuretii Vaucheria sphaerospora Vaucheria vq~'ra Vaucheria intermedia Vaucheria eoronata Vatwheria spee. Rhizodonium riparium ~- R. implexum

Code Number of sample-plot analyses

Column Community

50(01-02) 50(m-02) ---

70(r-03) 100(a-08) 7(r)

14(p)

7 (r) 28(r-04)

-68(p-01)

50(p-m)

-_

--

17(m)

100(p-07) ----

--

---

.

100(m.08) 17(m)

17(r)

17(p)

. 34(r-a) 17(01) --

50(r-a) 50(p-m) 34(m-01) 17(m)

--

} 50(m-03)}

A3 6

I" 35(p-04) 35(r-m) 42 (r-a)

]

SOC,

co?rim.

$0C.

A1 14

A4 6

3 UlvaFueus

2 Enterom.Cladoph.

1 E. prol.E. linza

.

.

.

40(r-m)

_-

I00(02-08) 20(m-01)

.

.

lO(r)

.

.

30(r-03)

} 20(p-01)

} 40(p-01) 30(r-p)

.

B5 10

$0C,

4 F. y e s . volubilis

.

.

.

. .

.

.

.

44(p-02)

_-

33(a-05) 100(01-05)

.

22 (p-a)

.

--

.

66(p-05)

.

} 11(01)

/

/

B6 9

$0c.

5 Bostrychia scorp.

.

.

.

-

-....

--

34(r-p)

.

17(p)

~

} 34(r-p) 17(02)

B7 6

SOC.

6 V. thuretii -V. sphaer.

]

...8.2.(.r._.-~. _.)....

..............

9(r-p) 9(r-a)

4(r ° )

--

__

.] ~ lO0(p-08)

B 11 23

comm.

7 General Chloroph.

Results of the phytosociological sample-plot analyses of the algal communities on fiats and salt marshes in the Orevelingen. For explanation see text on page. 21.

Addenda:

100(<5%50%)

-.

.

not estimated

. .

.

.

-.

.

.

.

.

.

.

lO0(a-08) 34(07) -----. . --

17 (01) 17(r-p) 17 (r) --34(r-a)

7 (p) 7(r) 7 (r) --21(r-p) 7(r) -14(p-05) 14(r-a) ---. --

--

.

. ~

.

.

--

100(30%70%)

.

.

50(r-p) . -----. --

. 17(r) 17 (r) 50(p-01) ---

. --

.

.

lO(r)

not estimated

.

.

10(r)

lO(p)

. 100(r-08) 60(p-07) 50(r-03) 50(r-p) 40(r-09)

.

. . . lO(p) 20(r°-a) 30(p-03)

.

.

.

.

.

. .

. .

.

--

. . . 77(p-08) 66(p-02) 88(p-02) 22 ( m - 0 2 ) 4-4(r-02) 33(01-02) 44(p-06) 44 (r-07) 11 (r) 11 (r)

-11 (r) --

.

~

--17(03)

--

34(p) 68(r-07) --34(07-09) -17(01) ----

.

. .

--

--

43(r-07) 52(r-05) 34(m-05) 39(r-04) 52(p-09) 56(r-02) 39(r-08) 13 (01-1 O) 39 (r-02) 21 (13-01) 34(p-03) 17 ( a - 0 4 )

--47(r-04)

26(r-01) 13(r-m)

c o l u m n 1: Enteromorpha compressa 14(r), E. aldneriana 7 ( 0 2 ) , Monostroma oxyspermum and M . cf. grevillei 7 ( a ) , Bryopsis plumosa 7 (r), Erythrotrichia oarnea 7 ( r ) , Acrochaetium s p e e . 7 ( r ) , Goniotrichum alsidii 7 ( r ) , Chondrus cr/spus 7 ( r ) , Ceramium deslongchampsii 7 (r), Ectocarpus oonfervoides 7 ( r ) , Codiumfragile 7 ( r ) , Polysiphonia nigrescens 7 (r) ; c o l u m n 2 : Cladophora laetevirens 17 ( a ) , Erythrotrichia carnea 17 ( r - p ) , Acrochaetium s p e c . 17 ( r - p ) , Evtocarpus confervoides 17 ( r ) , Ascocyclus magnusii 17 (p) ; c o l u m n 4 : Ulothrix pseudoflavca 1 0 ( r - p ) , U. subflardda 1 0 ( r ) ; c o l u m n 7: Monostroma oxyspermum and M . el. grevillei 4 ( a ) , Ulothrix subfla~dda 9 ( r ) , Spergularia salina 9 ( p - a ) , Elytrig/a pungens 4 ( p ) , Festu~a rubra 9 ( m - 0 3 ) , ~Tuncus gerardii 4 ( p ) . Artemisia maritima 4(07).

Shells o f m o l l u s c s (viz. Mytilus edulis a n d Cardium edule)

Limonium vulgate Triglochin maritima Spergularia marginata Plantago marit/ma Glaux maritima Armeria mar/t/ma

~uaeda marit/ma

Zostera marina Zostera noltii Spartina townsendii Salivornia europaea Purcinellia maritima Aster tripolium Halimioneportulacoides

Cyanophyceae

Peru~rsaria p e r c u r s a Blidingia minima + B. marginata Fucus vesieulosus vat. vadorum Ceramium rubrum Pol)siphonia violacea Porphyra umbilicalis Ulothrixflacca

42

P.H.

NIENHUIS

sand and mud flats and the salt marshes. In fact the genus is the most common one in these habitats, and among all species Enteromorpha prolifera can be found most frequently. Within E. prolifera the habitus of the thallus may vary between strongly branched or proliferated and unbranched. The cells are often arranged in longitudinal rows, but especially in the wider parts the arrangement may be very indistinct. The cells contain one or sometimes two (mostly large) pyrenoids and the length of the cells is less than about 20~. Very slender, unbranched proliferations of E. prolifera may easily be confused with Enteromorpha torta. In our samples the border line between these two species is not sharp. On the other hand, wider unbranched thalli can hardly be distinguished sometimes from Enteromorpha intestinalis. The distinction between E. prolifera and E. intestinalis is hampered because the thalli ofE. prolifera, developing in spring, show the tendency to thicken their cell walls and to get a more irregular arrangement of the cells in the course of summer. Moreover, this mode of growing obliterates the form and the position of the chloroplast. Enteromorphaflexgosa can rather easily be distinguished from E. prolifera by its larger cells and especially by its larger number of pyrenoids. Some interesting data were noticed concerning the quantitative distribution of some Enteromorpha species over the flats and marshes. Enteromorpha prolifera subsp, radiata occurs almost exclusively on the sand flats (sociation A 1). E. prolifera subsp, prolifera grows attached on lower levels and detached on higher levels. When detached it is found loose-lying in mats, often consisting of narrow, hardly branched thalli. Enteromorpha torta shows its most dense occurrence on the salt marshes where it grows in loose-lying masses, often mixed with E. prolifera. Enteromorphaflexuosa occurs on nearly all levels of the flats and marshes, but develops best at the lower, sandy parts, either attached to solid substrata (subsp. linziformis) or anchored in the sand. In the Grevelingen Enteromorpha intestinalis was exclusively found between the phanerogams of the salt marsh proper, as loose-lying, often intestinelike swollen thalli. Finally, attached thalli of Enteromorpha linza are mainly growing at the lower parts of sand flats and in deeper pools. VI. DISCUSSION It is one of the merits of CHAPMAN (1964) that he attempted to make a concept for nomenclatural rules for salt-marsh algal communities, by taking together the data of (a.o.) C A g T ~ (1933b), Cg.~M~a~ (1937) COTTON (1912) and R ~ s (1935). Basically I followed this concept. However, with regard to the Cyanophyceae I do not Share his opinion.

ALGAL COMMUNITIES

43

CHAPMAN (1964) splitted up the communities of bluegreen algae and companion species in five (con)sociatiom. I will not go to that extent for the Cyanophyceae from the Grevelingen. The reason is threefold: (1) The most important one is that it appeared very difficult to place bluegreen algae in socio-ecological units. Many of the species are ubiquitous throughout the marshes and, moreover, often covered with a thin layer of sediment, thus invisible with the naked eye. Culturing mud samples, STSWART & PUOH (1963) showed that although no marked growth was evident in the field, an abundant flora ofbluegreen algae (18 species) occurred in the developing salt marsh at Gibraltar Point (England). (2) Some of CHAPMAN'S (1964) communities could not be outlined in the Grevelingen. The widely distributed "Rivularia-Phaeococ~s socies" (CHAPMAN, 1964) occurring a.o. on the salt marshes of Clare Island (COTTON, 1912), Canvey and Dovey (CART~.R, 1932, 1933), Lough Ine (REIn, 1935) and Norfolk (CHAPMAN, 1937), has not been met with in the Grevelingen. The dominating species Rivularia atra or Rivularia nitida are not mentioned either by KOSTSR (1954, 1955), who identified a great number of bluegreens from the salt marshes in the south-western Netherlands. The sociation mentioned was found in England and Ireland on the firm soil of vertical faces of escarpments or on peat banks.This kind ofsubstratumis not present in the Grevelingen, where the creek banks are built up of rather unstable sediments. This may be the explanation for the absence of the Rivularia-Phaeococcus community. The same applies to the "Marginal Cyanophyceae consociation" (CHAPMAN, 1964). (3) The nomenclature of CrlAPMAN (1964) for the various communities gives rise to confusion, as is illustrated by the next example. On the Canvey marsh CARTER (1933b) distinguished an "Autumn Cyanophyceae community" in which OsciUatoria bonnemaisonii, O. nigroviridis, O. brevis and Microcoleus chthonoplastes were codominants. CHAPMAN (1937) mentioned an autumnal Cyanophyceae community dominated by Ghroococcusturgidus Naeg. var. maximus Nygaard, mixed with felts of Lyngbya for the higher parts at the Norfolk salt-marsh. Although CHAPMAN (1964) suggested the name "Autumn Cyanophyceae consoties" for both communities mentioned by CARTSR (1933b) and CHAPMAN (1937), it is not certain whether these two vegetation units are identical. For the reasons above I prefer to speak only about "communities dominated by Cyanophyceae", to be distinguished in the Grevelingen. Some final remarks on the correlation of the algal communities with the associations ofhalophytes should be made. Although the dominant vegetation of salt marshes consists of flowering plants, marine algae

44

P. H. N I E N H U I S

may play a considerable part in the general physiognomy. CHAPMAN (1960) who studied the salt-marsh vegetation for more than twentyfive years, involved the algae very frequently in his investigations. In many cases the relation between certain algae and a certain association of halophytes was very vague. In my opinion CHAPMAN (1964) in suggesting a concept for the nomenclature of salt-marsh algal communities, proved that he regarded the two systems (viz. those of the communities of halophytes and the algal communities) as two separate units. For the time being I have the same opinion. My reasons are: (1) Within a homogeneous stand of halophytes the algal vegetation may show large floristic and structural differences from place to place, and (2) owing to the stratification of the algal vegetation, two or more vegetation units can be distinguished at one and the same spot. (3) Some algal communities are closely confined to special seasonal influences, in contrast with most of the communities of phanerogams. VII. SUMMARY The benthic algal communities of sand and m u d flats and salt marshes in the Grevelingen were studied during three years. A survey of the most prominent environmental factors was given. The algal vegetation was divided into two categories (A and B); in both several algal communities could be distinguished on the base of a phytosociologicat analysis of a number of sample plots and many additional data. The vegetation on shoals, sand and mud flats in the sublittoral region and the lower part of the eulittoral region: (A 1) Enteromorpha prolifera-E. linza sociation on fine-grained sand; (A 2) Microvegetation in and on shells of molluscs and barnacles; (A 3) Enteromorpha-Gladophora community in sea-grass meadows; (A 4) Ulva rigida and U. lactuca-Fucus vesiculosus f. mytili sociation on mussel-banks. The vegetation on flats and salt marshes in the upper part of the eulittoral region and the supralittoral region: (B 5) Fucus vesiculosus f. votubilis sociation on the lower parts of the marshes, especially among Spartina townsendii; (B 6) Bostrychia scorpioides sociation in rather dense stands of halophytes; (B 7) Vaucheria thuretii-V, sphaerospora sociation on creek banks; (B 8) Blidingia minima sociation, an epiphytic community; (B 9) Vernal Ulothrix sociation; (B 10) Communities dominated by Cyanophyceae; (B 11) General Chlorophyceae community where the genera Rhizoclonium, Enteromorpha and Vaucheria are conspicuous; (B 12) Vegetation in salt-marsh pools. Some notes on the ecology of the genus Enteromorpha were attached. The pattern of the most conspicuous habitats in the Grevelingen was indicated and a map showing these habitats was given.

45

A L G A L COMMUNITIES

The validity of the nomenclatural concept of CHAPMAN (1964) for salt-marsh algal communities, and the relation between the associations of halophytes and the algal communities were discussed. Finally, a complete list of species was given. VIII. ACKNOWLEDGEMENTS

The author wishes to express his gratitude to Prof. Dr. C. van den Hoek (State University, Groningen) for identifying some Cladophorasamples, and to Mr. J. Simons (Free University, Amsterdam) for identifying the Vaucheriaspp. He is much indebted to Messrs. R. Peelen and W. J. Wolff (Delta Institute, Yerseke) for placing data about some environmental factors and the distribution of some organisms at his disposal. His further thanks go to Dr. W. G. Beeftink (Delta Institute, Yerseke) and Dr. C. den Hartog (Rijksherbarium, Leiden) for critically reading the manuscript, and to Dr. K. F. Vaas (Delta Institute, Yerseke) for correcting the English text. TABLE

II

The algal vegetation on fiats and salt marshes in the Grcvelingen. List of species and vegetation units in which the species occur. For the code A 1 up to and including B 12, see text; x indicates a dominating and . x a codominating position.

Vegetation units in which the spedes occur ~ s

A A A A B B B B B B B B 1 2 3 4 5 6 7 8 9 1 0 1 1 1 2

Cyanophyceae

A ~ l l u m quadruplicatum (Menegh.) Br6b. AgmeneUura thermale (Ktitz.) Dr. et Daily Anabaena torulosa (Carm. ) Lag. Ana~stis aeruginosa (Zanard) Dr. et Daily Ana~stis dimidiata (Ktitz.) Dr. et Daily Calothrix pulvinata (Mert.) C. Ag. Calothrix scopulorum (Web. et Molar) C. Ag. Coccochloris stagnina Spreng. Entophysalis deusta (Menegh.) Dr. et Daily Hydrocoleum lyngbyazeura (Ktitz.) Gore. Lyngbya aestuarii (Mert.) Liebm. ex. Gore. Lyngbya confervoides Ag. ex Com. L3ngbya semiplena (Ag.) J. Ag. ex Gore. Microeoleus chthonoplastes (Mert.) Zanard Microcoleus tenerriraus Com. Mierocoleus vaginatus (Vauch.) Gore. dVodularia hameyana (Thwaites) Thuret ex

X X X -

X

--

X

--

X

-

X -

X

X

X X X X -

X

X

X X X

X X X X X X -

X

-

X

X

X -

X

X X -

Born. et Flah.

Oscillatoria bonnemaisonii (Crouan) Com.

X X -

X

X X

X

X

X

-

X

X

-

46

P.

H.

NIENHUIS

TABLE

II

(continued)

Vegetation units inwhich the sped~ occur Species

A A A A

B

B B B

B B B B

1 2 3 4 5 6 7 8 9 1 0 1 1 1 2 Cyanophyceae (continued) Oscillataria limosa (C. Ag.) Gore. Osdllatoriam'groviridis ( T h w a i t e s i n H a r v . ) Gore. Schizothrixcaldcola ( A g . ) C o m . × Spirulina subsalsa (Orsted) Com. × Spirulina subtilissima (Ktitz.) Gom.

Spirulina tenerrima ( K i i t z , )

× . . . . . . × × - x × . . .

...... × . . . × × - x × × . . . . . . .

x

Gore.

x

×

-

×

-

X

-

~,<

X

-

X

X

-

-

×

Chlorophyceae

Blidingia marginata (J. Ag.) P. Dang. subsp. marginata Blid. Blidingia minima (N~ig. ex Kfitz.) Kyl. Bryopsis plumosa (Huds.) C. Ag, Ghaetomorpha capillaris (Ki.itz.) Borg. Ghaetomorpha crassa (C. Ag.) KOtz. Chaetomorpha linum (O. F. Mtill.) Kiitz. Cladophora globulina (Kfitz.) Ktitz. Cladophora laetem'rens (Dfllw.)KiRz. Cladophora sericea (Huds.) Kfitz. Cladophora spec. Codiumfragile (Sur.) Hariot Enteromarpha ahlneriana Blid. Enteromorpha clathrata (Roth) Greville Enteromorpha compressa (L.) Grey. var. compressa Blid. Enteromorphaflexuosa (Wulfen ex Roth) J . Ag. Enteromorpha intestlnalis (L.) Link var. intestinalis Enteromorpha linza (L.) J . Ag. Enteromorpha prolifera (O. F. Mtiller) J . Ag. Enteromorpha ralfsii H a r v e y Enteromarpha spec. Enteromorpha torta (Mertens) Reinb. el'. Entadadia spec. Gomantia polyrhiza (Lagerh.) Born. et Flah. Monostroma el. grevillei (Thur.) Wittr. Monostroma oxyspermum (KiRz.) Doty Percursaria percursa (C. Ag.) Bory Rhizodonium implexum (Dillw,) Ktitz. Rhizocloniura riparium (Roth) Harv. Ulothrixflacca (Dillw.) Thur. Ulothrix pseudoflacca Wille Ulothrix subflacdda Wille Ulva tactuxa L. Ulva rlgida (C. Ag.) Thur.

.

.

.

X

.

.

.

.

.

.

.

.

.

.

X

X

.

.

.

.

X

.

.

.

.

X

-

X

.

.

.

.

X

X

. .

. .

.

. .

.

.

.

.

.

.

-

.

.

X

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

. .

.

. .

.

-

X

X

-

.

.

.

X

X

X

.

X

.

.

.

.

X

-

X

-

. .

.

.

.

.

.

.

.

X

X

X X X X

-

X

w

.

X

.

.

.

x

X

.

X

.

x

X

.

X

X

.

.

-

X

X

.

x )< . . . . . x ,"< . . . . . . . . . . .

-

.

.

x X

X

X

.

.

X

X X -

.

X

.

.

X

.

X

.

.

X

X

X

X

X

X -

X

X

X

X X X X

X

-

X

X X X X

- X -

X

X X

X

X

X

- X

X X

X X

X

X

X

X

X

X

X

X

X

X

X X

X X

X

X

X X X

X X

X X

X

-

X

-

-

X X

X

X X X

X

-

X

X

X

X

-

X

X

X

47

A L G A L COMMUNITIES

TABL~ IX (continued)

Vegaation units in which the species occur Species

A A A A 1

2

3

4

B B B

B B B B B

5

7

8

9 10 11 12

X

-

-

6

Xanthophyceae

Vaucheria ¢oronata Nordst. Vaucheria intermedia Nordst. Vaucheria minuta Blum et Conover Vaucheria spec. Vaucheria sphaerospora Nordst. Vaucheria thuraii Woron. Vaucheria vi/ma Blum

X

X

-

X

X X

-

x

-

X X X x x

Phaeophyceae

Ascocyclus magnusii Sauv. Eaocarpus confirooides (Roth) Le Jolis Fucus spiralis L. Fucus vesiculosus L. f. mytili (Nienburg) forma

X

X

-

X

x x

x

x

llOVa

Fuats vesi~losus L. var. vadorum Aresch. Futus vesiculosus L. f. volubilis Powell cf. Lithoderma spec. Petaloniafasda ( 0 . F. Miill.) K u n t z e Pilayella littoralis (L.) Kjellm. Ralfsm verrucosa (Aresch.) J . Ag. Scytosiphon lomentaria (Lyngb.) Link

x

-

x

x

x

-

x

x

X X

--

× X -

X

-

X

X X X

Rhodophyceae

Acrochaetium spec. Bostrychia scorpioi&s (Huds.) Mont. Ceramium rubrum (Huds.) J . Ag. Ceramium deMongchampsii Chauv. Chrondrus ,v/spus Stackh. Dumontia incrassata ( 0 . F. Miill.) Lamour. ca.

a

(ViUw.)j, Ag.

Goniotrichum alsidii ( Z a . a r d . ) H o w e Polysiphonia nigrescem (Huds.) Grey. Polysiphonia vlola¢ea (Roth) Grey. Porphyraumbili, alis ( L . ) J . Ag.

X X X X

-

X

X

X X

X X

X

X

x

x

x x

-

X

-

X

X

x

x

X X X X

x

x

-

x

IX. REFERENCES BAKER, S. M., 1912. O n the brown seaweeds of the salt m a r s h . - - J . Linn. Soc. (Bot.) 40: 275-291. B ~ R , S. M. & M. H. BOHLmO, 1916. O n the brown seaweeds of the salt marsh I I . - J . L i n n . Soc. (Bot.) 4 3 . 3 2 5 - 3 8 0 .

~8

P. H. NII~.NHUIS

BEEFTINK, W. G., 1958. De betekenis van de natuurterreinen in het Deltagebied voor de b o t a n i e . I N a t u r a , Am_st. 55: 102-106. - - , 1965. De zoutvegetatievanZ.W.-NederlandbeschouwdinEuropeesv e r b a n d . u Meded. Landb.:Hoogesch. Wageningen 65 (1), 1-t67. - - , 1966. Vegetation and habitat of the salt marshes and beach plains in the southwestern part of the Netherlands.--Wentia 15: 83-108. BLXDING, C., 1963. A critical survey of European taxa in Ulvales I . - - O p . bot. Soc. bot. Lund 8 (3): 1-160. BORNET, E. & CH. FLArrAULT,1959 (reprint of t886--1888). Revision des Nostocac~es hdtdrocyst~es. BRAuN-BLANQU~.T,J., 1951, Pflanzensoziologie: 1-631. CARTER, N., 1932. A comparative study of the alga flora of two salt marshes I . - ]. Ecol. 20: 341-370. - - , 1933a. A comparative study of the alga flora of two salt marshes I I . - - J . Ecol. 21: 128-208. - - , t933b. A comparative study of the alga flora of two salt marshes III.--3. Ecol. 21 : 385-403. CHAPMAN, V. J., 1937. A revision of the marine algae of Norfolk.--J. Linn. Soc. (Bot.) 51: 205-263. - - , 1960. Salt marshes and salt deserts of the world: 1-392. ---, 1964. The Algae: 1-472. COTTON, A. D., 1912. A biological survey of Clare Island in the county of Mayo, Ireland. Marine algae,--Proc. R. Ir. Acad. 31 (15): 1-178. Doing KRAFT,H., 1954. L'analyse des carr~s permanents.--Acta bot. need. 3: 421424. DROUET, F., 1962. Gomont's ecophenes of the bluegreen alga, Microadeus vaginatus (Oscillatoriaceae).--Proc. Acad. nat. Sci. Philad, 114: 191-205. - - , 1963. Ecophenes of Schizothrix ¢aldeola (Oscillatoriaceae).--Proc. Aead. nat, Sci. Philad. 115: 261-281. - - , 1964. Ecophenes of Microeoleus chthonoplastes.--Revue algol. 4: 315-324. DROUET, F. & W. A. DAILy, 1956. Revision of the coccoid Myxophyeeae.--Butler Univ. bot. Stud. 12' 1-222. GrITLER, L., 1925. Cyanophyceae. In: Die Sfisswasser-Flora DeutscMands, Osterreichs und der Schweiz 12: 1-481. GOMONT,M., 1892. Monographie des Oscillari~es.--Annls. Sci. nat. (7) 15-"263-368; 16: 91-282. GooR, A. C. J. VAN, 1923. Die Holl~indischen Meeresalgen.--Verh. Ned. Akad. Wet., Amst. (2) 23: 1-232. HARTOG, C. DEN, 1952. Sociologische waarnemingen op Schiermonnikoog.--Kruipnieuws 14 (2): 2-24. - - , 1954. De vegetatie van wad en kwelder.--Amoeba 30: 155-161. - - , 1955a. De groenalg Monostroma grevillei (Thur.) Wittr. in NederLand.--Het Zeepaard 15-" A~ .A6. - - , 1955b. Roodwieren van de kwelders van Terschelling.--LevendeNat. 58-"69-73. - - , 1956' De verspreiding van Bostrychia scorpioides in Nederland.--Natura, Amst. 53: 71-73. - - , 1958a. Nieuwe gegevens over de kwelder-roodwieren van Terschelling.--Levende Nat. 61: 231-235. - - , 1958b. De vegetatie van het Balgzand en de oeverterreinen van bet Balgkanaal. --Wet. Meded. K. ned. natuurh. Veren. 2r/: 1-28. - - , 1959. The epilithic algal communities occurring along the coast of the Netherlands.--Wentia 1: 1-241.

A L G A L COMMUNITIES

49

I-~YR~N, E., 1956. Ober die Algenvegetation des sandigen Gcolitorals am IV[eere in Schweden und in Finnland.---Svemk bot. Tidskr. 50s 257-269. HoB~, C. VAN DEN, 1958a. Zeewieren van Voorne, waaronder Symphori~¢us st~llaris (Arcs.) Kuck. nlcuw voor de Nederlandse kust.mHet Zeepaard 18:3-11. m , 1958b. The algal mierovegetatlon in and on barnacle-shells, collected along the Dutch and French coasts.~Blumea 9z 206-214. ~ , 1960. Groupements d'algucs des dtangs saum~trcs m6diterrandens de la cSte franqaise.--Vie Milieu 11: 390-412. ~ , 1963. Revision of the European species of C/adophora (Dim. Leiden): 1-248. JoRv~-, I. & N. KLAV~STAD, 1958. Marine species of Vaudwria from the West coast of Norway.--Univ. Bergen Axb. (Naturvltcmk. rekke) 12. I-7. KOSTZR, J. TH., 1952. Rare or otherwise interesting marine algae from the Nethcrlands.--Acta bot. neerl. 1: 201-215. --, 1954. Sur la vdgdtation d'algucs marines de la Zdlande.--Blumea 7" 558-569. --, 1955. The genus Rhizodoniwn Kiitz. in the Nethcrlands.--Publ. Staz. Zool. Napoli 27: 335-357. LINDSTEDT, A., 1943. Die Flora dcr rnarinen Cyanophyccen der Schwedischcn Wcstk~te: 1-121. LINKS, O., 1939. Dic Biota des Jadcbuscnwattcs.--Hclgol~inder wiss. Mccrcsunters. I: 201-348. Nmm3URO, W., 1925. FAnc cigcnartigc Lebcnsgemcinschaft zwischcn Fucus und Myt//us (Vorlgulige Mittcilung).--Ber. dt. bot. Gcs. dk~, 292-298. --, 1927. Zur Okologic der Flora des Wattenmccrcs. I. Dcr KSnighafen bci List auf Sylt.~Wiss. Mecrcsuntcrs., Abt. Kid (N.F.) 20: 145-196. --, 1932. Fucus Mytilispcc. nov.~Ber, dt. bot. Gcs. 50a: 28-41. NmNHUm, P. H., 1968. Enkclc aspccten van het milieu en de bcnthonischc wiervcgctatie van dc Grcvclingen.--Mededclingen hydrobiologische Vcreniging

2 (l): 6-7. PARK~, M. & P. S. DIxoN, 1964. A revised checklist of British marine algae.mJ. mar. biol. Ass. U.K. 44: 499-542. POWELL, H. T., 1963. Speciation in the genus Fucus L., and related genera. In: Spcciation in the sca.~Publs. Syst. Ass. 5: 63-77. PRXOU, M. L. & M. SERPSZ'rs, 1954. Sur Ics associations allgalcs des anscs vaseuscs du sud de la Bretagne. Revue algol. (N.S.) 1: 25-28. Rzzs, T. K., 1935. The marine algae of Lough Ine.--J. Ecol. 23.69-133. SXMONS,J. & M. VROSt~, 1968. Some remarks on the genus Vaudw'ia in the Netherlands.-Acta bot. neerl. 17 (6), 461-466. SrSWART, W. D. P. & G . J . F . PUOH, 1963. Bluegreen algae of a developing salt marsh.--J, mar. biol. Ass. U.K. 43.309-317. VAAS, K. F., 1961. Das Arbeitsfeld des Hydrobiologischen Institutes, Abteilung Dclta-Untersuchungcn in den Niedcrlanden.~Int. Revue gcs. Hydrobiol. Hydrogr. 46. 292-295. - - , 1968. Annual report of the Division Delta Research of the Royal Netherlands' Academy of Sciences for the year 1967.-Neth. J. Sea. Res. 4 (2): 268-281. VENKATARAMAN,G. S., 1961. Vauchcriaceae: 1-112. WEBBER, E. E., 1967. Bluegreen algae from a Massachusetts salt marsh.~Bull. Torrcy hot. Club 94, 99-106. WESTHO~, V., 1951. An analysis of some concepts and terms in vegetation study or phytocenology.---Synthese 8: 194-206.