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Numerical density and biomass of macrobenthic animals living in the intertidal zone of Surinam, South America
Netherlands Journal of Sea Research 15 (3/4). 406-418 (1982) NUMERICAL DENSITY AND BIOMASS OF MACROBENTHIC ANIMALS LIVING IN THE INTERTIDAL ZONE OF SURINAM, SOUTH AMERICA by C. S W E N N E N , P. D U I V E N Netherlands Institute for Sea Research, P.O. Box 59, 1790 AB Den Burg, Texel, The Netherlands and A.L. SPAANS Research Institute for Nature Management, Kemperbergerweg 67, 6816 RM Arnhem, The Netherlands CONTENTS 1. 2. 3. 4.
Introduction . . . . . . . . . . . . . . Description of the area . . . . . . . . . . Methods . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . a. Upper tidal zone . . . . . . . . . . . b. Tidal mud flats . . . . . . . . . . . c. Eroded mud flat with firm clay . . . . . d. Tidal lagoons . . . . . . . . . . . . e. Bank of tidal creek . . . . . . . . . . f. Sand ridges . . . . . . . . . . . . . g. Observations on population structure crustacean species . . . . . . . . . . 5. Discussion . . . . . . . . . . . . . . . 6. Summary . . . . . . . . . . . . . . . 7. References . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . and reproduction in some . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
406 407 409 410 410 411 413 413 414 414 414 415 417 418
1. I N T R O D U C T I O N T h e r a t h e r i n a c c e s s i b l e t r o p i c a l sea coast o f S u r i n a m , s i t u a t e d o n the n o r t h e a s t e r n f r i n g e of S o u t h A m e r i c a , f o r m s the s t a g i n g g r o u n d o f l a r g e n u m b e r s o f b i r d s of the C i c o n i i f o r m e s a n d C h a r a d r i i f o r m e s , i n c l u d i n g millions of m i g r a t i n g a n d w i n t e r i n g N o r t h A m e r i c a n waders. S t u d i e s o n food a n d f e e d i n g h a b i t s i n d i c a t e t h a t the i n t e r t i d a l z o n e f o r m s the m o s t i m p o r t a n t f e e d i n g g r o u n d for m a n y species of c o a s t a l b i r d s a n d the m a c r o z o o b e n t h o s l i v i n g t h e r e as t h e i r m o s t i m p o r t a n t food (SPAANS, 1978, 1979). T h e p r e s e n t s t u d y was u n d e r t a k e n to g a i n s o m e i n s i g h t i n t o the c o m p o s i t i o n , n u m e r i c a l d e n s i t i e s a n d the biom a s s o f the m a c r o z o o b e n t h o s i n the i n t e r t i d a l h a b i t a t s .
407
M A C R O B E N T H I C ANIMALS OF S U R I N A M
Acknowledgements.--We thank H.A. Reichart and B . H . J . de J o n g of S T I N A S U (Foundation for Nature Preservation in Surinam) and L. Aurar of the Surinam Forest Service for their help and cooperation. We are also very grateful to Dr M. Boeseman, Dr E. Gittenberger and Prof. L.B. Holthuis of the Rijksmuseum van Natuurlijke Historic, Leiden, The Netherlands, for their assistance in identifying various organisms. We also wish to thank Dr J.J. Beukema for the critical reading of the manuscript. The work of A.L. Spaans was partly subsidized (grant W R 87-20) by W O T R O (Netherlands Foundation for the Advancement of Tropical Research). 2. D E S C R I P T I O N
OF THE
AREA
The Surinam coast is situated at about 6 ° N and between 54 ° and 57°W (Fig. 1). Geographically, it forms the central part of the Guiana coast, which consists of almost 2000 km of m u d d y and sandy shore of the Atlantic Ocean, between the mouths of the Amazon (Brazil) and Orinoco (Venezuela) rivers. The intertidal zone of the Surinam coast consists of a series of m u d flats in accretion, with a width of several hundreds to a few thousand metres. These fiats alternate in space and time with sections in erosion. The parts of the m u d flats above mean high tide level, are coverl
!'=y~-~ ',
"l
I
Atlontic
I
Oceon
',LSouthArnerlcoi/) •7 °
I
r"~' I
• Burnside
To~ness
Weg
noor
Zee
Motopico I .. .
•
~rOTOJOpOSl .6 °
.5 °
53 °
Fig. 1. M a p of the coastal area of S u r i n a m showing the n a m e s of locations m e n t i o n e d in the text.
408
C. SWENNEN,
P. D U I V E N
& A.L.
SPAANS
ed with black mangroves Avicennia germinans (L.) Stearn. Therefore, almost the entire intertidal zone is bare. This is in contrast with m any other areas in the tropics where red mangroves form the outer fringe of the vegetation and extend as far as mid-tide level. Along the Surinam coast a species of red mangrove Rhizophora mangle L. dominates only in the intertidal zone of river banks. U n d e r the influence of the G ui a na current and the waves generated by the NE trade wind, the m u d flats are abraded on the east side and silted up on the west side. This results in a westward m ovem ent of the flats with a speed of about 1 km per year (AuGuSTINUS, 1978). T h e succession of accretion and erosion has a cyclic character. For a relatively small area along the G ui ana coast, DIEPHUIS (1966) established that such a cycle takes 30 years. During erosion the mangroves are uprooted. T h e tidal zone along such an eroding coast consists mainly of a narrow, firm and tough bank of clay layers eroding from older deposits. Locally, the coast is fringed with narrow sand and shell grit beaches, which in total cover about 6% of the shore length. T he rapid succession of accretion and erosion results in a rather unstable shore line. Where the natural drainage system of the mangrove forest is temporarily impeded by a high beach platform or a m u d d y creek bank, sea water that has reached the area during spring tides causes a prolonged inundation of the forest floor. This water becomes hypersaline by evaporation, especially during the dry seasons. As a result the Avicennia dies in situ and vast bare salt pans, locally also called lagoons, develop, in which the trunks of the dead mangroves are a dominant feature for m a n y years. After some time the bare m ud bottom of these lagoons may be covered with a vegetation of halophytes, especially along the borders. W h e n the drainage system is restored, a true tidal lagoon develops. T h e mu d deposited along the Surinam coast originates from the Amazon; the sand and shells of the beaches, however, are of local origin (EIsMA & VAN DER MAREL, 1971). T h e mud discharged into the Atlantic Ocean by the A m azon and carried W N W by the Guiana current gives rise to a zone of very turbid water along the coast. AUGUSTXNUS (1978) found silt contents of up to a few g. 1-1 and Secchi-disc visibilities of 1 to 30 cm. As a result of an admixture of fresh water from the Am a z on and the G ui a na rivers the salinity of the near-shore surface water is lowered (EISMA, 1967; AUGUSTINUS, 1978). T he temperature of the surface water is about 28 ° C, but is much higher in pools on the exposed flats during the day. At neap tides the tidal amplitude is 1.00 m, at spring tides 2.80 m, the average being 1.80 m (NEDECO, 1962).
MACROBENTHIC
ANIMALS
OF SURINAM
409
3. M E T H O D S T h e study was carried out in S e p t e m b e r 1980. Areas visited were from west to east: Burnside, Totness, W e g n a a r Zee, M a t a p i c a and Krofajapasi (Fig. 1). N e a r W e g n a a r Zee a relatively stable part of a long existing m u d flat was studied, n e a r T o t n e s s a still growing part of a recently settled flat, n e a r Krofajapasi a m u d flat along a creek and n e a r M a t a p i c a an e r o d e d clay bank. Tidal lagoons were studied n e a r Burnside and Krofajapasi, and sandy beaches n e a r Totness, W e g n a a r Zee and Krofajapasi. T h e last beach is relatively large and k n o w n as Bigi Santi. T h e m u d of the tidal flats and the tidal lagoon n e a r Burnside was so soft that it was impossible to walk on as one sank in to well above the knees. T o study these places use was m a d e of a " m u d - h o r s e " , a large w o o d e n plank with a grip, used by local fishermen to scoot over the m u d flats. T h e top layer o f the m u d in the tidal lagoon n e a r Krofajapasi was as soft as at Burnside, b u t at a b o u t 50 cm depth the m u d b e c a m e m o r e solid. Since the d e p t h of sinking was only knee-high, it was possible to walk there slowly. W a l k i n g on the e r o d e d m u d b a n k at M a t a p i c a and on the sand ridges did not give problems. N e a r W e g n a a r Zee and T o t n e s s samples of the m u d b o t t o m were taken at a b o u t equal distances between m e a n high tide level and the low tide m a r k along a transect p e r p e n d i c u l a r to the coast. In the Uca zone and in the other habitats samples were taken r a n d o m l y . For biomass d e t e r m i n a t i o n s cores with a surface area of 0.018 m -2 and a d e p t h of 35 to 40 cm were used. Along each of the transects on the m u d flats 30 cores were taken, b u t 10 successive cores were taken together and considered as one sample. T i d a l levels were estimated by m e a s u r i n g the d u r a t i o n of exposure of m a r k e d stakes. T h e distances of the stakes f r o m the high tide m a r k were m e a s u r e d with the aid of an optical r a n g e finder. T h e sampled m u d was sieved t h r o u g h a sieve with a m e s h width of 1 m m . T h e r e m a i n i n g animals were counted. Species which contributed significantly to the total biomass were identified to the species level. T h e other organisms were taken together as a g r o u p (polychaetes, n e m e r t e a n s etc.). T h e species or groups of species per sample were dried in the field in a ventilated stove. S u b s e q u e n t l y they were sealed in plastic with some pearls of silicagel and t r a n s p o r t e d to the laboratory at Texel. W i t h i n 3 weeks after sampling they were placed for 2 days in a well-ventilated stove at 60 ° C, weighed, placed for 2 hours in a furnace at 600 ° C and weighed again. T h e weight loss at 600 ° C is considered to r e p r e s e n t the ash-free d r y weight ( A D W ) of the animals and is used as a m e a s u r e for their biomass (BEuKEMA, 1976).
410
C. SWENNEN,
P. D U I V E N
& A.L.
SPAANS
At each place an additional n u m b e r of samples was taken for identification control. T h e s e animals were put in alcohol 70 %. Part of the material has been deposited in the zoological collections of the Rijksm u s e u m van Natuurlijke Historic, L e i d e n , and the S u r i n a a m s Museum, Paramaribo. 4. R E S U L T S a.
UPPER
TIDAL
ZONE
M a n g r o v e forests m a r k e d the m e a n high tide level at all but one of the places visited, the exception being the high beach p l a t f o r m n e a r Krofajapasi (Fig. 2). Between the m a n g r o v e s and other halophytic p h a n e r o g a m s f o u n d in areas i n u n d a t e d b y sea water d u r i n g spring tides, the gastropod Melampus coffea (L.) and the b u r r o w i n g decapods Uca rapax (Smith) and U. vocator (Herbst) were n u m e r o u s with a r a t h e r p a t c h y distribution. Uca reached densities of up to 100 individuals, m -2. T h e large Ucides cordatus (L.) was also f o u n d in this zone; it was less a b u n d a n t but its density could not be estimated because of its living in deep holes between tree roots. Along the borders of tidal creeks in the halophytic vegetation zone the decapod Goniopsis cruentata (Latreille) was often f o u n d in groups of up to 10 per m 2, between the roots and low growing b r a n c h e s of the m a n g r o v e s .
O - -
~,,,s=-
MLW
b
MHW
MLW ,,
.
MLW
--H•
MNW
MLW
Fig. 2. Profiles of the intertidal zones studied, a. Totness, b. Weg naar Zee, c. Burnside, d. Matapica, e. Sandy beach near Krofajapasi.
MACROBENTHIC
ANIMALS
OF
411
SURINAM
Outside the vegetation, around and a little below mean high tide l e v e l , a d e n s e p o p u l a t i o n o f Uca maracoani ( L a t r e i l l e ) w a s f o u n d . F r o m a d i s t a n c e t h i s z o n e is c o n s p i c u o u s b e c a u s e o f t h e w a v i n g r e d p i n c e r s o f t h e m a l e c r a b s . A t close r a n g e , w h e n t h e c r a b s h a v e r e t r e a t e d i n t o their holes, the holes, food-scraps, mud balls and faecal pellets are s t r i k i n g , r e f l e c t i n g t h e i n t e n s i v e b i o t u r b a t i o n o f t h e m u d in this z o n e . T h i s z o n e w a s a b s e n t o n l y at v e r y e r o d e d p l a c e s o r w h e r e a s a n d r i d g e t e m p o r a r i l y o c c u p i e d t h e s p a c e at t h a t l e v e l . A t T o t n e s s a n d W e g n a a r Z e e U. maracoani w a s m i x e d w i t h U. rapax a l o n g t h e b o r d e r l i n e w i t h the low sand ridge. Along the Krofajapasi creek where the zone was sheltered against the direct influence of the oceanic waves by a high b e a c h p l a t f o r m U. maracoani o c c u r r e d t o g e t h e r w i t h t h e s o m e w h a t s m a l l e r U. cumulanta C r a n e at a d e n s i t y o f 236 i n d i v i d u a l s , m -2, 43 % c o n s i s t i n g o f U. maracoani. T h e t o t a l b i o m a s s in t h e U. maracoani z o n e n e a r W e g n a a r Z e e w a s d e t e r m i n e d a t 3 2 . 1 3 g . m -2, m o r e t h a n 9 9 % c o n s i s t i n g o f U. maracoani ( T a b l e I). T h e b i o m a s s o f t h e z o n e n e a r K r o f a j a p a s i w a s d e t e r m i n e d at 3 6 . 9 0 g . m -2. b. TIDAL
MUD
FLATS
O n t h e i n t e r t i d a l m u d flats t h r e e z o n e s w e r e c o n s p i c u o u s . A s i d e f r o m t h e z o n e a b o v e m e a n h i g h t i d e level c o v e r e d w i t h m a n g r o v e s , a n d t h e z o n e a r o u n d m e a n h i g h t i d e l e v e l w i t h Uca maracoani a t h i r d z o n e c o u l d be distinguished. In this zone of bare wet mud the fauna was richer
TABLE
I
Zonal distribution of biomass values ( g . r n 2 ADW) of macrozoobenthos in the relatively stable central part of the mud flat near Weg naar Zee, September 1980. Emergion times (hours, minutes) of zones as determined 2 days before spring tide between brackets.
Species group
Nemerteans Polychaetes Molluscs (bivalves) Crustaceans: mysids and gammarids Discapseudes surinamensis Callinectes bocourti Uca maracoani Fishes (juv. Gobionellus sp.) total
Biomass (g . m-2) at distancesfrom shore line (m). 0-50 (8.50)
50-250 (7.25)
250-450 450-650 (6.10) (3.40)
Mean
+ -
0.16 0.10 +
0.11 -
0.05 0.10 0.18
0.06 0.09 0.05
32.13 -
0.01 4.86 2.14 0.01
4.69 0.13 +
0.41 0.08 +
+ 3.06 0.06 3.13 +
32.13
7.28
4.93
0.82
6.45
412
C. S W E N N E N ,
P. D U I V E N
& A.L.
SPAANS
in species n u m b e r s t h a n in the Uca zone, b u t the b i o m a s s was m u c h lower. C h a r a c t e r i s t i c for this zone was the high density of T a n a i d a c e a , consisting exclusively of Discapseudes surinamensis B~cescu & G u t u , with n u m b e r s of u p to 6000 p e r m 2. T h e b i o m a s s of the z o o b e n t h o s b e t w e e n the high Uca zone and the low tide level d e c r e a s e d with the e x p o s u r e time, b e i n g 7.28 g- m - 2 in the highest part, 4.93 g. m -2 in the central p a r t a n d only 0.82 g. m -2 A D W in the lowest p a r t for the tidal flat n e a r W e g n a a r Zee ( T a b l e I) a n d 2.33, 1.57 a n d 1.20 g. m -2 for the flat n e a r T o t n e s s (Fig. 2a a n d b). I n the relatively stable m u d flat n e a r W e g n a a r Zee the a v e r a g e b i o m a s s (4.34 g. m -2) below the Uca zone was m u c h higher t h a n in the fast g r o w i n g w e s t e r n p a r t of the flat n e a r T o t n e s s (1.96 g. m -2) ( T a b l e II). P r o b a b l y this is not only related to the age of the flats, b u t also to the d u r a t i o n of exposure. O f f W e g n a a r Zee the m e a n e x p o s u r e t i m e was nearly 6 hours, off T o t n e s s only 3 ½ hours. I n the m u d a l o n g b o t h transects, r o u n d holes were f r e q u e n t l y seen. T h e density of these holes was nearly 100 m -2 in the lowest parts. T h e diggers of these holes were not o b s e r v e d , but were s u p p o s e d to be fishes. T h e fishes in the samples, h o w e v e r , s e e m e d to be too small to dig these holes. E x t r a cores t a k e n to a d e p t h of a b o u t 55 c m at places with a high density of holes yielded no l a r g e r fishes. T h e holes m a y h a v e b e e n u n o c c u p i e d , b u t it is possible that larger fishes were resident at still g r e a t e r depths. I f so, the c o n t r i b u t i o n of the fishes to the total b i o m a s s will h a v e b e e n u n d e r e s t i m a t e d . A l o n g b o t h transects the grey m u d discoloured shortly after e m e r gence to b r o w n - g r e e n as a result of the d e v e l o p m e n t of a slightly h y d r o p h o b i c film of benthic d i a t o m s . TABLE
II
Density (n. m -2) and biomass values (g- m ~ ADW) of macrozoobenthos in the growing western part of the mud flat near Totness, September 1980, transect of 800 m length between the narrow (non-sampled) Uca maracoani zone and the low water line. Mean time of emergence 3 ½ hours.
Species group Polychaetes Molluscs Crustaceans: tanaids and amphipods
Clibanarius vittatus Cycloplax pinnotheroides Fishes (GobioneUus sp.) total
Numerical density (m 2)
Biomass (g.m 2)
200 4
0.18 0.01
16 5 8 12
0.01 1.20 0.35 0.21
245
1.96
MACROBENTHIC
c. E R O D E D
MUD
ANIMALS
FLAT
OF SURINAM
WITH
FIRM
413
CLAY
N e a r M a t a p i c a an e r o d e d m u d b a n k was studied where all soft m u d had been carried away by the sea, thus leaving only the m o r e consolidated d e e p e r clay layers. T h e erosion process was still going on. D u r i n g one high tide, a patch of sling m u d with a d i a m e t e r of about 30 m and a height of about 10 cm was deposited on the clay. 24 hours later the m u d gel had disappeared without leaving any trace. Some parts of the surface of the clay b a n k were flat, while others contained m a n y depressions of different sizes. At m a n y places a p a t t e r n of r a t h e r straight parallel channels with steep banks and a depth of 10 to 60 cm was present (Fig. 2d). T h e firm m u d m a d e walking easy but did not p e r m i t sampling with a h a n d c o r e and sieving. T h e clay had to be c r u m b l e d b y h a n d to pick out the animals. Because the animals were distributed u n e v e n l y , no reliable estimate could be m a d e for the biomass. In some banks of the small channels, however, the biomass seemed to be c o m p a r a b l e with that in a densely p o p u l a t e d Uca maracoani zone. O n the flat and cracked parts of the clay b a n k no m a c r o b e n t h i c animals were found, but in the shallow pools the crab Clibanarius vittatus (Bosc) was present with c o n c e n t r a t i o n s of up to 10 m -z. Locally, there were dense clusters of holes with a d i a m e t e r of 3 to 4 m m m a d e by the isopod Sphaeroma annandalei Stebbing. T h e density of Sphaeroma decreased from the m e a n high tide level to the low w a t e r mark. T h e steep banks of the small channels were p e r f o r a t e d with slightly larger holes. In these holes the decapods Upogebia brasiliensis Holthuis, Hexapanopeus schmitti R a t h b u n and Cycloplax pinnotheroides G u i n o t were found, as well as Sphaeroma annandalei and some small sedentary polychaetes. d. T I D A L
LAGOONS
T h e tidal lagoons studied were b o r d e r e d by a small zone of y o u n g
Avicennia. In these lagoons a relatively high zone of bare m u d and a small deep creek were present at low tide (Fig. 2c). T h e r e was no indication that the biomass of the Uca maracoani zone was m u c h different from that f o u n d in similar zones elsewhere along the ~oast and averaged at about 35 g. m-2. In the zone of bare m u d T a n a i d a c e a were almost exclusively found. In the lagoon n e a r Burnside only Discapseudes surinamensis was present with a m e a n density of 25 000 specimens, m -2 and a biomass of 19.44 g. m -2. O t h e r animals f o u n d were the gastropod Cylichnella biplicata (Lea), the bivalve Tellina diantha (Boss) and insect larvae, together a m o u n t i n g to less than 0.01 g - m -~. In the lagoon n e a r
414
c.
SWENNEN,
P. D U I V E N
& A.L.
SPAANS
Krofajapasi 2 species of tanaids were found: Discapseudes surinamensis with a density of 20 500 m -2 and the smaller Halmyrapseudes spaansi B~cescu & G u t u with a m e a n density of 16 000 m -~. In this lagoon, only one specimen of a n o t h e r animal species, an unidentified eyeless a m p h i p o d , was f o u n d in the samples. T h e average biomass of the bare m u d zone in this lagoon a m o u n t e d to 23.22 g- m -2. e. B A N K
OF TIDAL
CREEK
A tidal creek without c o n n e c t i o n with a fresh water system was studied n e a r Krofajapasi. T h e m u d on the b a n k was r a t h e r soft; o u r legs were sinking into 15 to 40 cm. Below the rich Uca zone inhabited by Uca maracoani and U. cumulanta a relatively steep m u d zone was sampled in which the tanaid Halmyrapseudes spaansi was found, with a m e a n density of 13000 m -2, and a small, unidentified polychaete species (length 3 to 6 m m ) with a density of 118 m -2. T h e biomass here was d e t e r m i n e d b y multiplying the n u m b e r of animals and the m e a n A D W per animal calculated from the other places sampled. O n an average the biomass a m o u n t e d to about 3.7 g. m -2. f
SAND
RIDGES
N o m a c r o z o o b e n t h o s was f o u n d in the littoral zone of the small sand ridges that m a r k e d the shorelines n e a r W e g n a a r Zee and Totness. H o w e v e r , b e t w e e n the u p r o o t e d m a n g r o v e trees that had drifted ashore, small n u m b e r s of the isopod Ligia sp. and the decapod Sesarma ricordi H . M i l n e E d w a r d s were located. T h e coarse-sand beaches n e a r M a t a p i c a and Krofajapasi are several kilometres long and m o r e than 100 m wide. T h e beach platform is at a b o u t the same level or a little above that of the spring high tide. T h e sandy beach extends until below the low tide m a r k (Fig. 2e). T h e s e beaches form the nesting places of 4 species of sea turtles (ScHuLz, 1975). A r o u n d the high tide m a r k of these beaches the holes of the large d e c a p o d Oxipode quadrata (Fabricius) were present with a density of 1 to 15 per r u n n i n g m e t r e of shoreline. In the tidal zone a single juvenile specimen of the d e c a p o d Hepatus pudibundus H e r b s t was found and no other m a c r o f a u n a l elements were found neither in beach parts in accretion n o r in e r o d i n g parts. g. O B S E R V A T I O N S
ON POPULATION STRUCTURE AND REPRODUCTION SOME CRUSTACEAN SPECIES
IN
Discapseudes surinamensis.--The duplicate samples taken n e a r Burn-
MACROBENTHIC
ANIMALS
OF SURINAM
415
side, Weg naar Zee and Krofajapasi contained 13.1% adult females with oostegites, 11.7% adult males and 75.2% juveniles (n = 1240). No less than 95.7% of the adult females carried eggs or embryos in their marsupium. O f the females with eggs, the smallest (7.5 mm total body length excluding antennae and uropods) carried on average 11 eggs, the largest (length 12 mm) 54 eggs. At a mean length of 10 mm the mean egg number was 28.5. B~,cEscu & GuTu (1975) also mentioned the occurrence of adults and juveniles of different ages together and described ovigerous females from samples taken in J a n u a r y and in May.
Halmyrapseudes spaansi.--The population in the tidal lagoon and in the creek near Krofajapasi consisted for the greater part of juveniles. O f the 248 specimens in 2 duplicate samples only 24.6% were adults, 27 males and 34 females. Nearly all adult females carried eggs or embryos in their marsupium. As a large number of the embryos were found loose in the alcohol in which the samples were preserved, the number of gravid females could not be determined exactly. The number of eggs varied between 12 in the smallest (length 3.5 mm) and 21 in the largest females (length 5.2 mm).
Uca maracoani.--At all places visual observation gave the impression that the U. maracoanipopulation consisted for the greater part of adult crabs. However, the core samples taken near Weg naar Zee and Krofajapasi showed that adults were in the minority. Probably the juveniles spend more time in the burrows and behave less conspicuously than the adults. In the Weg naar Zee samples (n = 78) 22% of the specimens had a carapace width of 3 to 10 mm, 57% a carapace width of 11 to 20 m m and 21% a carapace width of more than 20 mm. Most specimens of the last group were considered to be adult. Among the 9 adult females in this group 3 carried eggs. HOLTHmS (1959) mentioned the occurrence of ovigerous females in April and August samples. Ovigerous females were also found of the following decapod species not recorded previously for Surinam: Hexapanopeus schmitti Rathbun, Cycloplax pinnotheroides Guinot, Pinnixa sayana Stimpson (Brachyura), and Upogebia brasiliensis Holthuis (Macrura). 5.
DISCUSSION
With the exception of the banks along the outer rivers, all natural types of intertidal areas were studied. At first sight the number of invertebrate species seems low compared with the wealth of species
416
c
SWENNEN,
P. D U I V E N
& A.L. SPAANS
usually occurring in tropical marine habitats. However, THORSON (1957) already noted that the number of infauna species in levelbottom areas shows no increase from the arctic towards the tropics. No doubt a few more species would have been found if more samples had been taken, but it is unlikely that they would have attributed considerably to the total biomass. It is clear that crustaceans dominate among the benthic invertebrates. Polychaetes and molluscs were poorly represented and their numbers were not impressive. As a result their biomass was only a fraction of that of the crustaceans. Dominance of crustaceans in the intertidal zone has also been found by VERWEY (1930) in Indonesia and by DAY (1967) in Africa and may be characteristic for intertidal m u d d y areas in the tropics. This contrasts with the situation in temperate areas where polychaetes and molluscs dominate in the intertidal mud flats as shown for instance by DEXTER (1947) for North America, DAY (1967) for South Africa and BEUKEMA (1976) for Europe. The highest biomass of invertebrates was found around mean high tide level at all places except firm clay banks. This contrasts with the situation in the European W a d d e n Sea where the highest biomass is found somewhat below mid-tide level (BEUKEMA,1976). The zonation of the biomass can be caused by differences in predation pressure, differences in food supply and differences in habitability of the substratum. Large numbers of Ciconiiform and Charadriiform birds enter the intertidal area from land during low tide. At all places rufous crabhawks Buteogallus aequinoctialis (Gmelin) were seen capturing crabs, and everywhere within the mangrove zone footprints and large quantities of faeces containing crab remains of a raccoon Procyon cancrivorus (Cuvier) were found. Predators entering the intertidal zone from the sea during high tide are the swimming crab Callinectes bocourti A. Milne Edwards and probably a number of prawns, shrimps and fishes. However, without extensive research nothing can be said about the character and magnitude of the predation and the part it plays in reducing the densities of invertebrates in the intertidal. The crustaceans which contributed considerably to the total biomass values were characterized by a high percentage of immatures, a high percentage of adult females carrying eggs or embryos and a reproduction not restricted to a short season, all indicating a high turn-over rate in the population. Concerning the primary food, nearly no planktonic production can be expected in the very turbid coastal water. In fact the only planktonic producer we found was cf. Phaeocystis spec., living in nearly 1 cm
MACROBENTH1C
ANIMALS
OF S U R I N A M
417
large transparent gelatinous bodies which floated at the sea surface. O n the other hand many species of benthic diatoms were found in high densities on the m u d flats; their production will be high. Shortly after emergence the grey colour of the m u d flats changed into a brownishgreen as a result of the development of a film of diatoms. Every day we observed that a considerable part of the diatom film was taken up by the incoming tide and transported into the direction of the high tide line. This supply probably enriches the food available around high tide level and induces the relatively high biomass of secondary producers at these places. On the other hand, the presence of the important film of diatoms on the m u d at the lower levels may indicate that there was more food for secondary producers than actually present. The instability of the tidal flats is probably the decisive factor that caused the low biomass of benthic invertebrates at the lower levels. On the sand beaches at Krofajapasi and Matapica every wave changed the surface of the foreshore considerably. During the 5 days of our stay on the Krofajapasi beach a few hundred metres of beach on the east side disappeared completely while there was an accretion on the west side of about the same length. The sand of the beaches is constantly moved by the waves so that burrowing animals are rare. Also on the lower parts of the flats the mud is so little consolidated that the upper 20 to 30 cm can be fluidized easily. Therefore, this mud is not suitable for burrowing. The absence of red mangroves on the mud flats may also result from the inability of the seedlings to establish themselves in the soft m u d (AuGusTINUS, 1978). The firm clay banks are relatively stable and indeed are occupied by a richer but very patchily distributed benthic fauna. On these banks, however, the sedentary animals, especially those at the lower levels, can be covered in one single tide with thick layers of watery sediments of slingmud from the westward moving mud banks (EISMA & VAN DER MAREL, 1971). 6. SUMMARY The macrobenthic fauna of all types of intertidal area of the Surinam coast, mainly m u d flats, were briefly studied by coring. Crustaceans dominated; polychaetes and molluscs were poorly represented. The highest biomass values (32 to 37 g. m -2 ADW, mainly contributed by Uca maracoani) were found around high tide level, at the border of the mangrove forest. Just outside the Uca zone, on sheltered places also high values (ca 20 g. m -2 ADW, mainly contributed by Tanaidacea) were found. In the middle and lower parts of the flats biomass was low (only a few g • m-2 or less), probably a result of the instability of the sediment. The following crustaceans not recorded
418
c SWENNEN, P. DUIVEN & A.L. SPAANS
p r e v i o u s l y for S u r i n a m w e r e f o u n d l i v i n g i n the i n t e r t i d a l clay a n d m u d : Hexapanopeus schmitti, Cycloplax pinnotheroides, Pinnixa sayana ( B r a c h y u r a ) , a n d Upogebia brasiliensis ( M a c r u r a ) . 7. R E F E R E N C E S AUGUSTINUS,P.G.E.F., 1978. The changing shoreline of Surinam (South America). Publ. Found. Sci. Res. Surinam Neth, Ant. 95" 1-232 (thesis Utrecht). BXcEscu, M. & M. GUTU, 1975. A new genus (Discapseudesn.g.) and three new species of Apseudidae (Crustaeea, Tanaidacea) from the northeastern coast of South America.--Zo61. Meded., Leiden 49: 95-113. BEUKEMA, J.J., 1976. Biomass and species richness of the macro-benthic animals living on the tidal flats of the Dutch Wadden Sea.--Neth. J. Sea Res. 10 (2)" 236-261. DAY, J.H., 1967. The biology of Knysna estuary, South Africa. In: G.H. LAUFF. Estuaries. Am. Ass. Adv. Sci., Washington: 397-407. DEXTER, R.W., 1947. The marine communities of a tidal inlet at Cape Ann, Massachusetts: a study in bioecology.--Ecol. Monogr. 17: 261-294. D1EPHUIS, J.G.H.R., 1966. The Guiana coast.--Tijdschr. K. ned. aardrijksk. Genoot. 83: 145-152. EtSMA, D., 1967. Oceanographic observations on the Surinam shelf.--Hydrogr. Newsletter R. Neth. Navy, Spec. Publ. 5" 21-53. EISMA, D. & H.W. VAN DER MAREL, 1971. Marine muds along the Guiana coast and their origin from the Amazon Basin.--Contr. Mineral. Petrol. 31: 321-334. HOLTHUIS, L.B., 1959. The Crustacea Decapoda of Suriname (Dutch Guiana).-Zool. Verh., Leiden 44: 1-296. NEDECO, 1962. Demerara coastal investigations. Delft: 1-240. SCHULZ, J.P., 1975. Sea turtles nesting in Surinam.--Zool. Verh., Leiden 143: 1-143. SPAANS, A.L., 1978. Status and numerical fluctuations of some North American waders along the Surinam coast.--Wilson Bull. 90: 60-83. ----., 1979. Wader studies in Suriname, South America.--Wader Study Group Bull. 25: 32-37. THORSON, G., 1957. Bottom communities.--Mem, geol. Soc. Am. 67 (1): 461-534. VERWEY, J., 1930. Einiges fiber die Biologic ost-indischer Mangrovekrabben.-Treubia 12 (2): 167-261.
Introduction . . . . . . . . . . . . . . Description of the area . . . . . . . . . . Methods . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . a. Upper tidal zone . . . . . . . . . . . b. Tidal mud flats . . . . . . . . . . . c. Eroded mud flat with firm clay . . . . . d. Tidal lagoons . . . . . . . . . . . . e. Bank of tidal creek . . . . . . . . . . f. Sand ridges . . . . . . . . . . . . . g. Observations on population structure crustacean species . . . . . . . . . . 5. Discussion . . . . . . . . . . . . . . . 6. Summary . . . . . . . . . . . . . . . 7. References . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . and reproduction in some . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
406 407 409 410 410 411 413 413 414 414 414 415 417 418
1. I N T R O D U C T I O N T h e r a t h e r i n a c c e s s i b l e t r o p i c a l sea coast o f S u r i n a m , s i t u a t e d o n the n o r t h e a s t e r n f r i n g e of S o u t h A m e r i c a , f o r m s the s t a g i n g g r o u n d o f l a r g e n u m b e r s o f b i r d s of the C i c o n i i f o r m e s a n d C h a r a d r i i f o r m e s , i n c l u d i n g millions of m i g r a t i n g a n d w i n t e r i n g N o r t h A m e r i c a n waders. S t u d i e s o n food a n d f e e d i n g h a b i t s i n d i c a t e t h a t the i n t e r t i d a l z o n e f o r m s the m o s t i m p o r t a n t f e e d i n g g r o u n d for m a n y species of c o a s t a l b i r d s a n d the m a c r o z o o b e n t h o s l i v i n g t h e r e as t h e i r m o s t i m p o r t a n t food (SPAANS, 1978, 1979). T h e p r e s e n t s t u d y was u n d e r t a k e n to g a i n s o m e i n s i g h t i n t o the c o m p o s i t i o n , n u m e r i c a l d e n s i t i e s a n d the biom a s s o f the m a c r o z o o b e n t h o s i n the i n t e r t i d a l h a b i t a t s .
407
M A C R O B E N T H I C ANIMALS OF S U R I N A M
Acknowledgements.--We thank H.A. Reichart and B . H . J . de J o n g of S T I N A S U (Foundation for Nature Preservation in Surinam) and L. Aurar of the Surinam Forest Service for their help and cooperation. We are also very grateful to Dr M. Boeseman, Dr E. Gittenberger and Prof. L.B. Holthuis of the Rijksmuseum van Natuurlijke Historic, Leiden, The Netherlands, for their assistance in identifying various organisms. We also wish to thank Dr J.J. Beukema for the critical reading of the manuscript. The work of A.L. Spaans was partly subsidized (grant W R 87-20) by W O T R O (Netherlands Foundation for the Advancement of Tropical Research). 2. D E S C R I P T I O N
OF THE
AREA
The Surinam coast is situated at about 6 ° N and between 54 ° and 57°W (Fig. 1). Geographically, it forms the central part of the Guiana coast, which consists of almost 2000 km of m u d d y and sandy shore of the Atlantic Ocean, between the mouths of the Amazon (Brazil) and Orinoco (Venezuela) rivers. The intertidal zone of the Surinam coast consists of a series of m u d flats in accretion, with a width of several hundreds to a few thousand metres. These fiats alternate in space and time with sections in erosion. The parts of the m u d flats above mean high tide level, are coverl
!'=y~-~ ',
"l
I
Atlontic
I
Oceon
',LSouthArnerlcoi/) •7 °
I
r"~' I
• Burnside
To~ness
Weg
noor
Zee
Motopico I .. .
•
~rOTOJOpOSl .6 °
.5 °
53 °
Fig. 1. M a p of the coastal area of S u r i n a m showing the n a m e s of locations m e n t i o n e d in the text.
408
C. SWENNEN,
P. D U I V E N
& A.L.
SPAANS
ed with black mangroves Avicennia germinans (L.) Stearn. Therefore, almost the entire intertidal zone is bare. This is in contrast with m any other areas in the tropics where red mangroves form the outer fringe of the vegetation and extend as far as mid-tide level. Along the Surinam coast a species of red mangrove Rhizophora mangle L. dominates only in the intertidal zone of river banks. U n d e r the influence of the G ui a na current and the waves generated by the NE trade wind, the m u d flats are abraded on the east side and silted up on the west side. This results in a westward m ovem ent of the flats with a speed of about 1 km per year (AuGuSTINUS, 1978). T h e succession of accretion and erosion has a cyclic character. For a relatively small area along the G ui ana coast, DIEPHUIS (1966) established that such a cycle takes 30 years. During erosion the mangroves are uprooted. T h e tidal zone along such an eroding coast consists mainly of a narrow, firm and tough bank of clay layers eroding from older deposits. Locally, the coast is fringed with narrow sand and shell grit beaches, which in total cover about 6% of the shore length. T he rapid succession of accretion and erosion results in a rather unstable shore line. Where the natural drainage system of the mangrove forest is temporarily impeded by a high beach platform or a m u d d y creek bank, sea water that has reached the area during spring tides causes a prolonged inundation of the forest floor. This water becomes hypersaline by evaporation, especially during the dry seasons. As a result the Avicennia dies in situ and vast bare salt pans, locally also called lagoons, develop, in which the trunks of the dead mangroves are a dominant feature for m a n y years. After some time the bare m ud bottom of these lagoons may be covered with a vegetation of halophytes, especially along the borders. W h e n the drainage system is restored, a true tidal lagoon develops. T h e mu d deposited along the Surinam coast originates from the Amazon; the sand and shells of the beaches, however, are of local origin (EIsMA & VAN DER MAREL, 1971). T h e mud discharged into the Atlantic Ocean by the A m azon and carried W N W by the Guiana current gives rise to a zone of very turbid water along the coast. AUGUSTXNUS (1978) found silt contents of up to a few g. 1-1 and Secchi-disc visibilities of 1 to 30 cm. As a result of an admixture of fresh water from the Am a z on and the G ui a na rivers the salinity of the near-shore surface water is lowered (EISMA, 1967; AUGUSTINUS, 1978). T he temperature of the surface water is about 28 ° C, but is much higher in pools on the exposed flats during the day. At neap tides the tidal amplitude is 1.00 m, at spring tides 2.80 m, the average being 1.80 m (NEDECO, 1962).
MACROBENTHIC
ANIMALS
OF SURINAM
409
3. M E T H O D S T h e study was carried out in S e p t e m b e r 1980. Areas visited were from west to east: Burnside, Totness, W e g n a a r Zee, M a t a p i c a and Krofajapasi (Fig. 1). N e a r W e g n a a r Zee a relatively stable part of a long existing m u d flat was studied, n e a r T o t n e s s a still growing part of a recently settled flat, n e a r Krofajapasi a m u d flat along a creek and n e a r M a t a p i c a an e r o d e d clay bank. Tidal lagoons were studied n e a r Burnside and Krofajapasi, and sandy beaches n e a r Totness, W e g n a a r Zee and Krofajapasi. T h e last beach is relatively large and k n o w n as Bigi Santi. T h e m u d of the tidal flats and the tidal lagoon n e a r Burnside was so soft that it was impossible to walk on as one sank in to well above the knees. T o study these places use was m a d e of a " m u d - h o r s e " , a large w o o d e n plank with a grip, used by local fishermen to scoot over the m u d flats. T h e top layer o f the m u d in the tidal lagoon n e a r Krofajapasi was as soft as at Burnside, b u t at a b o u t 50 cm depth the m u d b e c a m e m o r e solid. Since the d e p t h of sinking was only knee-high, it was possible to walk there slowly. W a l k i n g on the e r o d e d m u d b a n k at M a t a p i c a and on the sand ridges did not give problems. N e a r W e g n a a r Zee and T o t n e s s samples of the m u d b o t t o m were taken at a b o u t equal distances between m e a n high tide level and the low tide m a r k along a transect p e r p e n d i c u l a r to the coast. In the Uca zone and in the other habitats samples were taken r a n d o m l y . For biomass d e t e r m i n a t i o n s cores with a surface area of 0.018 m -2 and a d e p t h of 35 to 40 cm were used. Along each of the transects on the m u d flats 30 cores were taken, b u t 10 successive cores were taken together and considered as one sample. T i d a l levels were estimated by m e a s u r i n g the d u r a t i o n of exposure of m a r k e d stakes. T h e distances of the stakes f r o m the high tide m a r k were m e a s u r e d with the aid of an optical r a n g e finder. T h e sampled m u d was sieved t h r o u g h a sieve with a m e s h width of 1 m m . T h e r e m a i n i n g animals were counted. Species which contributed significantly to the total biomass were identified to the species level. T h e other organisms were taken together as a g r o u p (polychaetes, n e m e r t e a n s etc.). T h e species or groups of species per sample were dried in the field in a ventilated stove. S u b s e q u e n t l y they were sealed in plastic with some pearls of silicagel and t r a n s p o r t e d to the laboratory at Texel. W i t h i n 3 weeks after sampling they were placed for 2 days in a well-ventilated stove at 60 ° C, weighed, placed for 2 hours in a furnace at 600 ° C and weighed again. T h e weight loss at 600 ° C is considered to r e p r e s e n t the ash-free d r y weight ( A D W ) of the animals and is used as a m e a s u r e for their biomass (BEuKEMA, 1976).
410
C. SWENNEN,
P. D U I V E N
& A.L.
SPAANS
At each place an additional n u m b e r of samples was taken for identification control. T h e s e animals were put in alcohol 70 %. Part of the material has been deposited in the zoological collections of the Rijksm u s e u m van Natuurlijke Historic, L e i d e n , and the S u r i n a a m s Museum, Paramaribo. 4. R E S U L T S a.
UPPER
TIDAL
ZONE
M a n g r o v e forests m a r k e d the m e a n high tide level at all but one of the places visited, the exception being the high beach p l a t f o r m n e a r Krofajapasi (Fig. 2). Between the m a n g r o v e s and other halophytic p h a n e r o g a m s f o u n d in areas i n u n d a t e d b y sea water d u r i n g spring tides, the gastropod Melampus coffea (L.) and the b u r r o w i n g decapods Uca rapax (Smith) and U. vocator (Herbst) were n u m e r o u s with a r a t h e r p a t c h y distribution. Uca reached densities of up to 100 individuals, m -2. T h e large Ucides cordatus (L.) was also f o u n d in this zone; it was less a b u n d a n t but its density could not be estimated because of its living in deep holes between tree roots. Along the borders of tidal creeks in the halophytic vegetation zone the decapod Goniopsis cruentata (Latreille) was often f o u n d in groups of up to 10 per m 2, between the roots and low growing b r a n c h e s of the m a n g r o v e s .
O - -
~,,,s=-
MLW
b
MHW
MLW ,,
.
MLW
--H•
MNW
MLW
Fig. 2. Profiles of the intertidal zones studied, a. Totness, b. Weg naar Zee, c. Burnside, d. Matapica, e. Sandy beach near Krofajapasi.
MACROBENTHIC
ANIMALS
OF
411
SURINAM
Outside the vegetation, around and a little below mean high tide l e v e l , a d e n s e p o p u l a t i o n o f Uca maracoani ( L a t r e i l l e ) w a s f o u n d . F r o m a d i s t a n c e t h i s z o n e is c o n s p i c u o u s b e c a u s e o f t h e w a v i n g r e d p i n c e r s o f t h e m a l e c r a b s . A t close r a n g e , w h e n t h e c r a b s h a v e r e t r e a t e d i n t o their holes, the holes, food-scraps, mud balls and faecal pellets are s t r i k i n g , r e f l e c t i n g t h e i n t e n s i v e b i o t u r b a t i o n o f t h e m u d in this z o n e . T h i s z o n e w a s a b s e n t o n l y at v e r y e r o d e d p l a c e s o r w h e r e a s a n d r i d g e t e m p o r a r i l y o c c u p i e d t h e s p a c e at t h a t l e v e l . A t T o t n e s s a n d W e g n a a r Z e e U. maracoani w a s m i x e d w i t h U. rapax a l o n g t h e b o r d e r l i n e w i t h the low sand ridge. Along the Krofajapasi creek where the zone was sheltered against the direct influence of the oceanic waves by a high b e a c h p l a t f o r m U. maracoani o c c u r r e d t o g e t h e r w i t h t h e s o m e w h a t s m a l l e r U. cumulanta C r a n e at a d e n s i t y o f 236 i n d i v i d u a l s , m -2, 43 % c o n s i s t i n g o f U. maracoani. T h e t o t a l b i o m a s s in t h e U. maracoani z o n e n e a r W e g n a a r Z e e w a s d e t e r m i n e d a t 3 2 . 1 3 g . m -2, m o r e t h a n 9 9 % c o n s i s t i n g o f U. maracoani ( T a b l e I). T h e b i o m a s s o f t h e z o n e n e a r K r o f a j a p a s i w a s d e t e r m i n e d at 3 6 . 9 0 g . m -2. b. TIDAL
MUD
FLATS
O n t h e i n t e r t i d a l m u d flats t h r e e z o n e s w e r e c o n s p i c u o u s . A s i d e f r o m t h e z o n e a b o v e m e a n h i g h t i d e level c o v e r e d w i t h m a n g r o v e s , a n d t h e z o n e a r o u n d m e a n h i g h t i d e l e v e l w i t h Uca maracoani a t h i r d z o n e c o u l d be distinguished. In this zone of bare wet mud the fauna was richer
TABLE
I
Zonal distribution of biomass values ( g . r n 2 ADW) of macrozoobenthos in the relatively stable central part of the mud flat near Weg naar Zee, September 1980. Emergion times (hours, minutes) of zones as determined 2 days before spring tide between brackets.
Species group
Nemerteans Polychaetes Molluscs (bivalves) Crustaceans: mysids and gammarids Discapseudes surinamensis Callinectes bocourti Uca maracoani Fishes (juv. Gobionellus sp.) total
Biomass (g . m-2) at distancesfrom shore line (m). 0-50 (8.50)
50-250 (7.25)
250-450 450-650 (6.10) (3.40)
Mean
+ -
0.16 0.10 +
0.11 -
0.05 0.10 0.18
0.06 0.09 0.05
32.13 -
0.01 4.86 2.14 0.01
4.69 0.13 +
0.41 0.08 +
+ 3.06 0.06 3.13 +
32.13
7.28
4.93
0.82
6.45
412
C. S W E N N E N ,
P. D U I V E N
& A.L.
SPAANS
in species n u m b e r s t h a n in the Uca zone, b u t the b i o m a s s was m u c h lower. C h a r a c t e r i s t i c for this zone was the high density of T a n a i d a c e a , consisting exclusively of Discapseudes surinamensis B~cescu & G u t u , with n u m b e r s of u p to 6000 p e r m 2. T h e b i o m a s s of the z o o b e n t h o s b e t w e e n the high Uca zone and the low tide level d e c r e a s e d with the e x p o s u r e time, b e i n g 7.28 g- m - 2 in the highest part, 4.93 g. m -2 in the central p a r t a n d only 0.82 g. m -2 A D W in the lowest p a r t for the tidal flat n e a r W e g n a a r Zee ( T a b l e I) a n d 2.33, 1.57 a n d 1.20 g. m -2 for the flat n e a r T o t n e s s (Fig. 2a a n d b). I n the relatively stable m u d flat n e a r W e g n a a r Zee the a v e r a g e b i o m a s s (4.34 g. m -2) below the Uca zone was m u c h higher t h a n in the fast g r o w i n g w e s t e r n p a r t of the flat n e a r T o t n e s s (1.96 g. m -2) ( T a b l e II). P r o b a b l y this is not only related to the age of the flats, b u t also to the d u r a t i o n of exposure. O f f W e g n a a r Zee the m e a n e x p o s u r e t i m e was nearly 6 hours, off T o t n e s s only 3 ½ hours. I n the m u d a l o n g b o t h transects, r o u n d holes were f r e q u e n t l y seen. T h e density of these holes was nearly 100 m -2 in the lowest parts. T h e diggers of these holes were not o b s e r v e d , but were s u p p o s e d to be fishes. T h e fishes in the samples, h o w e v e r , s e e m e d to be too small to dig these holes. E x t r a cores t a k e n to a d e p t h of a b o u t 55 c m at places with a high density of holes yielded no l a r g e r fishes. T h e holes m a y h a v e b e e n u n o c c u p i e d , b u t it is possible that larger fishes were resident at still g r e a t e r depths. I f so, the c o n t r i b u t i o n of the fishes to the total b i o m a s s will h a v e b e e n u n d e r e s t i m a t e d . A l o n g b o t h transects the grey m u d discoloured shortly after e m e r gence to b r o w n - g r e e n as a result of the d e v e l o p m e n t of a slightly h y d r o p h o b i c film of benthic d i a t o m s . TABLE
II
Density (n. m -2) and biomass values (g- m ~ ADW) of macrozoobenthos in the growing western part of the mud flat near Totness, September 1980, transect of 800 m length between the narrow (non-sampled) Uca maracoani zone and the low water line. Mean time of emergence 3 ½ hours.
Species group Polychaetes Molluscs Crustaceans: tanaids and amphipods
Clibanarius vittatus Cycloplax pinnotheroides Fishes (GobioneUus sp.) total
Numerical density (m 2)
Biomass (g.m 2)
200 4
0.18 0.01
16 5 8 12
0.01 1.20 0.35 0.21
245
1.96
MACROBENTHIC
c. E R O D E D
MUD
ANIMALS
FLAT
OF SURINAM
WITH
FIRM
413
CLAY
N e a r M a t a p i c a an e r o d e d m u d b a n k was studied where all soft m u d had been carried away by the sea, thus leaving only the m o r e consolidated d e e p e r clay layers. T h e erosion process was still going on. D u r i n g one high tide, a patch of sling m u d with a d i a m e t e r of about 30 m and a height of about 10 cm was deposited on the clay. 24 hours later the m u d gel had disappeared without leaving any trace. Some parts of the surface of the clay b a n k were flat, while others contained m a n y depressions of different sizes. At m a n y places a p a t t e r n of r a t h e r straight parallel channels with steep banks and a depth of 10 to 60 cm was present (Fig. 2d). T h e firm m u d m a d e walking easy but did not p e r m i t sampling with a h a n d c o r e and sieving. T h e clay had to be c r u m b l e d b y h a n d to pick out the animals. Because the animals were distributed u n e v e n l y , no reliable estimate could be m a d e for the biomass. In some banks of the small channels, however, the biomass seemed to be c o m p a r a b l e with that in a densely p o p u l a t e d Uca maracoani zone. O n the flat and cracked parts of the clay b a n k no m a c r o b e n t h i c animals were found, but in the shallow pools the crab Clibanarius vittatus (Bosc) was present with c o n c e n t r a t i o n s of up to 10 m -z. Locally, there were dense clusters of holes with a d i a m e t e r of 3 to 4 m m m a d e by the isopod Sphaeroma annandalei Stebbing. T h e density of Sphaeroma decreased from the m e a n high tide level to the low w a t e r mark. T h e steep banks of the small channels were p e r f o r a t e d with slightly larger holes. In these holes the decapods Upogebia brasiliensis Holthuis, Hexapanopeus schmitti R a t h b u n and Cycloplax pinnotheroides G u i n o t were found, as well as Sphaeroma annandalei and some small sedentary polychaetes. d. T I D A L
LAGOONS
T h e tidal lagoons studied were b o r d e r e d by a small zone of y o u n g
Avicennia. In these lagoons a relatively high zone of bare m u d and a small deep creek were present at low tide (Fig. 2c). T h e r e was no indication that the biomass of the Uca maracoani zone was m u c h different from that f o u n d in similar zones elsewhere along the ~oast and averaged at about 35 g. m-2. In the zone of bare m u d T a n a i d a c e a were almost exclusively found. In the lagoon n e a r Burnside only Discapseudes surinamensis was present with a m e a n density of 25 000 specimens, m -2 and a biomass of 19.44 g. m -2. O t h e r animals f o u n d were the gastropod Cylichnella biplicata (Lea), the bivalve Tellina diantha (Boss) and insect larvae, together a m o u n t i n g to less than 0.01 g - m -~. In the lagoon n e a r
414
c.
SWENNEN,
P. D U I V E N
& A.L.
SPAANS
Krofajapasi 2 species of tanaids were found: Discapseudes surinamensis with a density of 20 500 m -2 and the smaller Halmyrapseudes spaansi B~cescu & G u t u with a m e a n density of 16 000 m -~. In this lagoon, only one specimen of a n o t h e r animal species, an unidentified eyeless a m p h i p o d , was f o u n d in the samples. T h e average biomass of the bare m u d zone in this lagoon a m o u n t e d to 23.22 g- m -2. e. B A N K
OF TIDAL
CREEK
A tidal creek without c o n n e c t i o n with a fresh water system was studied n e a r Krofajapasi. T h e m u d on the b a n k was r a t h e r soft; o u r legs were sinking into 15 to 40 cm. Below the rich Uca zone inhabited by Uca maracoani and U. cumulanta a relatively steep m u d zone was sampled in which the tanaid Halmyrapseudes spaansi was found, with a m e a n density of 13000 m -2, and a small, unidentified polychaete species (length 3 to 6 m m ) with a density of 118 m -2. T h e biomass here was d e t e r m i n e d b y multiplying the n u m b e r of animals and the m e a n A D W per animal calculated from the other places sampled. O n an average the biomass a m o u n t e d to about 3.7 g. m -2. f
SAND
RIDGES
N o m a c r o z o o b e n t h o s was f o u n d in the littoral zone of the small sand ridges that m a r k e d the shorelines n e a r W e g n a a r Zee and Totness. H o w e v e r , b e t w e e n the u p r o o t e d m a n g r o v e trees that had drifted ashore, small n u m b e r s of the isopod Ligia sp. and the decapod Sesarma ricordi H . M i l n e E d w a r d s were located. T h e coarse-sand beaches n e a r M a t a p i c a and Krofajapasi are several kilometres long and m o r e than 100 m wide. T h e beach platform is at a b o u t the same level or a little above that of the spring high tide. T h e sandy beach extends until below the low tide m a r k (Fig. 2e). T h e s e beaches form the nesting places of 4 species of sea turtles (ScHuLz, 1975). A r o u n d the high tide m a r k of these beaches the holes of the large d e c a p o d Oxipode quadrata (Fabricius) were present with a density of 1 to 15 per r u n n i n g m e t r e of shoreline. In the tidal zone a single juvenile specimen of the d e c a p o d Hepatus pudibundus H e r b s t was found and no other m a c r o f a u n a l elements were found neither in beach parts in accretion n o r in e r o d i n g parts. g. O B S E R V A T I O N S
ON POPULATION STRUCTURE AND REPRODUCTION SOME CRUSTACEAN SPECIES
IN
Discapseudes surinamensis.--The duplicate samples taken n e a r Burn-
MACROBENTHIC
ANIMALS
OF SURINAM
415
side, Weg naar Zee and Krofajapasi contained 13.1% adult females with oostegites, 11.7% adult males and 75.2% juveniles (n = 1240). No less than 95.7% of the adult females carried eggs or embryos in their marsupium. O f the females with eggs, the smallest (7.5 mm total body length excluding antennae and uropods) carried on average 11 eggs, the largest (length 12 mm) 54 eggs. At a mean length of 10 mm the mean egg number was 28.5. B~,cEscu & GuTu (1975) also mentioned the occurrence of adults and juveniles of different ages together and described ovigerous females from samples taken in J a n u a r y and in May.
Halmyrapseudes spaansi.--The population in the tidal lagoon and in the creek near Krofajapasi consisted for the greater part of juveniles. O f the 248 specimens in 2 duplicate samples only 24.6% were adults, 27 males and 34 females. Nearly all adult females carried eggs or embryos in their marsupium. As a large number of the embryos were found loose in the alcohol in which the samples were preserved, the number of gravid females could not be determined exactly. The number of eggs varied between 12 in the smallest (length 3.5 mm) and 21 in the largest females (length 5.2 mm).
Uca maracoani.--At all places visual observation gave the impression that the U. maracoanipopulation consisted for the greater part of adult crabs. However, the core samples taken near Weg naar Zee and Krofajapasi showed that adults were in the minority. Probably the juveniles spend more time in the burrows and behave less conspicuously than the adults. In the Weg naar Zee samples (n = 78) 22% of the specimens had a carapace width of 3 to 10 mm, 57% a carapace width of 11 to 20 m m and 21% a carapace width of more than 20 mm. Most specimens of the last group were considered to be adult. Among the 9 adult females in this group 3 carried eggs. HOLTHmS (1959) mentioned the occurrence of ovigerous females in April and August samples. Ovigerous females were also found of the following decapod species not recorded previously for Surinam: Hexapanopeus schmitti Rathbun, Cycloplax pinnotheroides Guinot, Pinnixa sayana Stimpson (Brachyura), and Upogebia brasiliensis Holthuis (Macrura). 5.
DISCUSSION
With the exception of the banks along the outer rivers, all natural types of intertidal areas were studied. At first sight the number of invertebrate species seems low compared with the wealth of species
416
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P. D U I V E N
& A.L. SPAANS
usually occurring in tropical marine habitats. However, THORSON (1957) already noted that the number of infauna species in levelbottom areas shows no increase from the arctic towards the tropics. No doubt a few more species would have been found if more samples had been taken, but it is unlikely that they would have attributed considerably to the total biomass. It is clear that crustaceans dominate among the benthic invertebrates. Polychaetes and molluscs were poorly represented and their numbers were not impressive. As a result their biomass was only a fraction of that of the crustaceans. Dominance of crustaceans in the intertidal zone has also been found by VERWEY (1930) in Indonesia and by DAY (1967) in Africa and may be characteristic for intertidal m u d d y areas in the tropics. This contrasts with the situation in temperate areas where polychaetes and molluscs dominate in the intertidal mud flats as shown for instance by DEXTER (1947) for North America, DAY (1967) for South Africa and BEUKEMA (1976) for Europe. The highest biomass of invertebrates was found around mean high tide level at all places except firm clay banks. This contrasts with the situation in the European W a d d e n Sea where the highest biomass is found somewhat below mid-tide level (BEUKEMA,1976). The zonation of the biomass can be caused by differences in predation pressure, differences in food supply and differences in habitability of the substratum. Large numbers of Ciconiiform and Charadriiform birds enter the intertidal area from land during low tide. At all places rufous crabhawks Buteogallus aequinoctialis (Gmelin) were seen capturing crabs, and everywhere within the mangrove zone footprints and large quantities of faeces containing crab remains of a raccoon Procyon cancrivorus (Cuvier) were found. Predators entering the intertidal zone from the sea during high tide are the swimming crab Callinectes bocourti A. Milne Edwards and probably a number of prawns, shrimps and fishes. However, without extensive research nothing can be said about the character and magnitude of the predation and the part it plays in reducing the densities of invertebrates in the intertidal. The crustaceans which contributed considerably to the total biomass values were characterized by a high percentage of immatures, a high percentage of adult females carrying eggs or embryos and a reproduction not restricted to a short season, all indicating a high turn-over rate in the population. Concerning the primary food, nearly no planktonic production can be expected in the very turbid coastal water. In fact the only planktonic producer we found was cf. Phaeocystis spec., living in nearly 1 cm
MACROBENTH1C
ANIMALS
OF S U R I N A M
417
large transparent gelatinous bodies which floated at the sea surface. O n the other hand many species of benthic diatoms were found in high densities on the m u d flats; their production will be high. Shortly after emergence the grey colour of the m u d flats changed into a brownishgreen as a result of the development of a film of diatoms. Every day we observed that a considerable part of the diatom film was taken up by the incoming tide and transported into the direction of the high tide line. This supply probably enriches the food available around high tide level and induces the relatively high biomass of secondary producers at these places. On the other hand, the presence of the important film of diatoms on the m u d at the lower levels may indicate that there was more food for secondary producers than actually present. The instability of the tidal flats is probably the decisive factor that caused the low biomass of benthic invertebrates at the lower levels. On the sand beaches at Krofajapasi and Matapica every wave changed the surface of the foreshore considerably. During the 5 days of our stay on the Krofajapasi beach a few hundred metres of beach on the east side disappeared completely while there was an accretion on the west side of about the same length. The sand of the beaches is constantly moved by the waves so that burrowing animals are rare. Also on the lower parts of the flats the mud is so little consolidated that the upper 20 to 30 cm can be fluidized easily. Therefore, this mud is not suitable for burrowing. The absence of red mangroves on the mud flats may also result from the inability of the seedlings to establish themselves in the soft m u d (AuGusTINUS, 1978). The firm clay banks are relatively stable and indeed are occupied by a richer but very patchily distributed benthic fauna. On these banks, however, the sedentary animals, especially those at the lower levels, can be covered in one single tide with thick layers of watery sediments of slingmud from the westward moving mud banks (EISMA & VAN DER MAREL, 1971). 6. SUMMARY The macrobenthic fauna of all types of intertidal area of the Surinam coast, mainly m u d flats, were briefly studied by coring. Crustaceans dominated; polychaetes and molluscs were poorly represented. The highest biomass values (32 to 37 g. m -2 ADW, mainly contributed by Uca maracoani) were found around high tide level, at the border of the mangrove forest. Just outside the Uca zone, on sheltered places also high values (ca 20 g. m -2 ADW, mainly contributed by Tanaidacea) were found. In the middle and lower parts of the flats biomass was low (only a few g • m-2 or less), probably a result of the instability of the sediment. The following crustaceans not recorded
418
c SWENNEN, P. DUIVEN & A.L. SPAANS
p r e v i o u s l y for S u r i n a m w e r e f o u n d l i v i n g i n the i n t e r t i d a l clay a n d m u d : Hexapanopeus schmitti, Cycloplax pinnotheroides, Pinnixa sayana ( B r a c h y u r a ) , a n d Upogebia brasiliensis ( M a c r u r a ) . 7. R E F E R E N C E S AUGUSTINUS,P.G.E.F., 1978. The changing shoreline of Surinam (South America). Publ. Found. Sci. Res. Surinam Neth, Ant. 95" 1-232 (thesis Utrecht). BXcEscu, M. & M. GUTU, 1975. A new genus (Discapseudesn.g.) and three new species of Apseudidae (Crustaeea, Tanaidacea) from the northeastern coast of South America.--Zo61. Meded., Leiden 49: 95-113. BEUKEMA, J.J., 1976. Biomass and species richness of the macro-benthic animals living on the tidal flats of the Dutch Wadden Sea.--Neth. J. Sea Res. 10 (2)" 236-261. DAY, J.H., 1967. The biology of Knysna estuary, South Africa. In: G.H. LAUFF. Estuaries. Am. Ass. Adv. Sci., Washington: 397-407. DEXTER, R.W., 1947. The marine communities of a tidal inlet at Cape Ann, Massachusetts: a study in bioecology.--Ecol. Monogr. 17: 261-294. D1EPHUIS, J.G.H.R., 1966. The Guiana coast.--Tijdschr. K. ned. aardrijksk. Genoot. 83: 145-152. EtSMA, D., 1967. Oceanographic observations on the Surinam shelf.--Hydrogr. Newsletter R. Neth. Navy, Spec. Publ. 5" 21-53. EISMA, D. & H.W. VAN DER MAREL, 1971. Marine muds along the Guiana coast and their origin from the Amazon Basin.--Contr. Mineral. Petrol. 31: 321-334. HOLTHUIS, L.B., 1959. The Crustacea Decapoda of Suriname (Dutch Guiana).-Zool. Verh., Leiden 44: 1-296. NEDECO, 1962. Demerara coastal investigations. Delft: 1-240. SCHULZ, J.P., 1975. Sea turtles nesting in Surinam.--Zool. Verh., Leiden 143: 1-143. SPAANS, A.L., 1978. Status and numerical fluctuations of some North American waders along the Surinam coast.--Wilson Bull. 90: 60-83. ----., 1979. Wader studies in Suriname, South America.--Wader Study Group Bull. 25: 32-37. THORSON, G., 1957. Bottom communities.--Mem, geol. Soc. Am. 67 (1): 461-534. VERWEY, J., 1930. Einiges fiber die Biologic ost-indischer Mangrovekrabben.-Treubia 12 (2): 167-261.