Spatial and temporal patterns in coastal macrobenthos of ...

Estuaries

Vol. 21, No. 4B, p. 690-699

December 1998

Spatial and Temporal Patterns in Coastal Macrobenthos of Samborombon Bay, Argentina: A Case Study of Very Low Diversity E. N. IENO l R. O. BASTIDA Conicet Universidad Nacional de Mar del Plata F. Mundo Marino Dean Funes 3350 7600 Mar del Plata Argentina ABSTRACT: The benthic community structure of the southernmost part of Samborombon Bay was studied at 13 stations for 2 yr. A detailed examination of the zoobenthos, using similarity indices and cluster analysis, is presented. The area was characterized by low diversity. The Shannon-Weaver information diversity index H' showed low values of 0.28-1.60. The brackish part of the area was dominated by two opportunistic polychaetes species, Heteromastus similis and Laeonereis acuta. The only species found in the transitional marine zone was the bivalve Mesodesma mactroides. Variability in benthic community has been interpreted in terms of spatial and temporal changes. Depending on the area, abundance appeared to be controlled by pollution and intense predation during the warmer months. The observed gradient in species ,composition and dominance of these benthic communities are compared with some other North and South Atlantic estuaries.

Introduction In recent years there has been increased pressure to develop ecological monitoring to evaluate the degree to which human manipulations of coastal areas may alter the physical and biological properties of the system (e.g., Pearson and Rosenberg 1978; Suchanek 1993; Elias and Bremec 1994; Seys et al. 1994). The importance of benthic communities in the ecological processes of coastal areas is now well understood, as witnessed by the vast number of environmental impact statements that include benthic studies. A major question to be addressed is whether human-induced changes in intertidal areas affect the benthic community structure or not. Intertidal areas are not only exploited by recreational activities but also by high numbers of birds, fishes, and invertebrates. In this context, the communities baseline studies, must be well understood before any modification occur. In Argentinean' coasts, descriptive and experimental studies on marine soft-bottom intertidal habitats are scarce (Olivier et al. 1972; Elias 1992; Elias and leno 1993). Even fewer studies have focused on ecological aspects such as distribution patterns, food supply, animal sediment relations, and environmental disturbances of soft-bottom infauna communities (Spivak et al. 1994). Although the subtidal macrobenthos of Sambo1

romb6n Bay plays a key role in the food web of the entire ecosystem, information about the intertidal macrobenthos is not available (Lasta 1995). Polychaetes, bivalves, and crustaceans represent an important link in the food chain from primary producers to predators such as birds, fishes, and marine mammals which are very abundant in the zone. Coastal fishes have received special attention due to high densities occurring at the breeding season. Common demersal and benthic fishes such as Pogonias cromis, Micropogonias furnieri, Paralichthys spp., Mugil platanus, Myliobatis goodei, and Netuma barbus are active predators of polychaetes, crabs, and bivalves (Lasta 1995). The extensive stocks of food organisms are also used by high numbers of birds, wintering in the bay or using it as a stop-over area during their migrations. In particular, this estuary is presently the focus of attention and research on the migration of red knot (Calidris canutus rufa) in South America that undertakes the longest bird flights on earth (Morrison and Harrington 1992). In this general context, the relationship between the distribution of prey populations and their predators should be well documented. This will contribute to an understanding of natural patterns and processes and ultimately, the prediction of trends. The main objective of this study was to characterize the intertidal soft-bottom community in relation to environmental parameters and seasonal

Corresponding author; e-mail: [email protected].

© 1998 Estuarine Research Federation

690

Macrobenthos of Samborombon Bay

691

BRASIL

Uruguay River URUGUAY 50 ..

34'

36'

ARGENTINA

50

' 1llI'

•

i

-!

i

1

BAHIA SAjMBOROMBON

Fig. 1. Map of the La Plata River and its estuary with the location of the three zones and the outer limit of the external zone (oceanic front) (1-4). Map of sampling stations and Samboromb6n Bay (1-13).

variability. Special emphasis was placed on the importance of polychaetes in the community and this was compared with other mudflat habitats. Study Area La Plata River and its estuary, together with its oceanic front, forms a wide ecosystem or "ecosystem complex" of great ecological significance, probably one of the main natural phenomena that regulates, together with the Malvinas and Brazil currents, the general dynamics and biological production of the Argentine biogeographical province.

Based on environmental characteristics, La Plata River can be divided into three main zones: internal zone, intermediate zone, and external zone (Fig. 1). The external zone is of main interest in relation to the mixohaline communities. The outer limit of the external zone is set by the oceanic front area, where important environmental and biological phenomena take place (Boschi 1982). Our study was carried out at the extreme southeastern section of Samborombon Bay, in the estuarine zone located between Tijeras Creek and Punta Rasa (Fig. 1). The inlet consists of marshland creeks, some shallow (with a maximum depth of

692

E. N. lena and R. O. Bastida

50 cm) and others, like the narrow navigation channel to San Clemente harbor, much deeper. Most of the creeks consist of fine sandy sediments. The silt-clay percentage increases with the distance from the sea (Bertola et al. 1993). The dominant vegetation of the natural marsh is composed of Spartina densiflora, S. alterniflora, Salicornia ambigua, S. virginica, and Scirpus sp. The most important epifaunal component is the mud crab Chasmagnathus granulata, who makes big burrows in the sediment. On the tidal flats, where the crab population reaches very high densities, only Spartina and Scirpus are found. Outside the bay, on the southeastern side of the saltmarshes, marine sandy shores are developed as tourist beaches. Materials and Methods Field work was carried out on tidal and subtidal flats at different sites in the southernmost part of Samboromb6n Bay. Sampling for macrobenthos was conducted bimonthly from April 1993 to February 1995 in three main areas. A total of 13 stations are considered here (Fig. 1). The locations were randomly selected along the intertidal, and grab samples were also taken from the middle of the creek at two stations (6 and 8). Benthic intertidal infauna were sampled with a 12-cm inner diameter core to a depth of 25 cm. The area sampled by the grab (the subtidal) was equal to taking three cores and subsequently pooling them to form one sample with a total area of 0.053 m- 2 • Samples were sieved through 0.5-mm mesh and fixed in a 10% formalin solution. In the laboratory, organisms were sorted, washed, and preserved in a 70% alcohol solution. Motile and sessile organisms were identified to species, and counted. Encrusting organisms were identified but not counted. The core was inadequate for sampling of motile fauna such as grapsid crabs (c. granulata and Cyrtograpsus angulatus). Since this group is a conspicuous constituent of the salt marshes along the southern bay (Boschi 1964) it was included in the discussion, but species densities are underestimated and are not considered in the data analysis. Sorensen's similarity index (Dice 1945) was applied and cluster analyses with single linkage were used to determine the pattern of similarity in the macrobenthic community at site sampled over the 2-yr period. The data were reduced prior to classification by eliminating those species which were colonial or encrusting and not quantifiable, or occurred in only one core or grab sample during the study. To evaluate the quantitative aspect of the community, Czekanowski's similarity index (Czekanowski 1913) was calculated for the two most abundant species. Species diversity is expressed as

the Shannon-Weaver (H') information statistic (Pielou 1966). Evenness (H I /H max ) was also estimated due to the low number of species. For the sediment analysis, a random sample of 200 g was collected from the surface of each station. Sediment was air-dried and 50% of each dried sampled processed through graded sieves. Particles passing through the 64-j.Lm sieve were the mud (silty-clay) fraction. Fractions were weighed and expressed as a percentage of dried weight. The organic matter content of the sediments was determined by wet oxidation (Walkley and Black 1965). Salinity of the water was recorded at each station. Faunal feeding mode, burrowing activities, and mobility patterns of polychaetes were assigned based on information in Fauchald and Jumars (1979) and on personal observations of animal morphologies and dwelling structures. Gut contents of polychaetes and bivalves were examined under a microscope. Visual observations were made for signs of predation on infauna. Results SEDIMENT CHARACTERISTICS AND SALINITY

The dominant sediment type throughout the intertidal and subtidal bottoms was fine, well-sorted sand (average median grain size of 2,6 19'9%

20-34.9% 35-79.9% >80%

Fig. 4. Trellis diagram showing quantitative similarity index (Czekanowski's index) between pairs of samples collected, using polychaete data.

8 6

M. mactroides during a specific time period (springsummer).

12

E 13 1

Quantitative Data The Trellis diagram constructed with the abundance data (Czekanowski) showed three groups (Fig. 4). The first group was composed of stations of low density, with averages of fewer than 8 ind m- 2 • The second group was composed of six stations, having medium abundances, with values ranging from 25 ind m- 2 to 50 ind m- 2 • Finally, the last group was characterized by a high density, and consisted mainly of juvenile infauna.

oI

0.5

I

I

Similarity

Fig. 3. Dendrogram of the cluster analysis of stations. Five groups of stations A, B, C, D, and E were defined.

represents the two types of communities found in the bay. The major branch of the dendrogram represents the most abundant benthic organisms in this part of the bay (groups A, B, C, and D). These four groups have both H~ similis and L. acuta as common members. Group A consisted of six stations that only included the poychaetes H. similis and L. acuta. Group B clustered sampling units characterized by the presence of T. gibbus. The fiddler crab U. uruguayensis was collected only at site 2 (group C). Taxa in group D, which were collected from the tidal creeks, included P. ligni and C. insidiosum. Group E contains samples taken from the intertidal marine-influenced stations and is composed of

Density and Distribution. Variability in Dominant species

For all species combined, macrobenthic density was highest at the creeks (x = 14,048 ind m- 2 ) (stations 6 and 8) (Table 2). This high density was attributed to the overwhelming abundance of the juvenile polychaetes H. similis and L. acuta, which comprised 74% of the individuals collected at the site. The Pta. Rasa site (stations 10 and 11) had a mean density of 5336 ind m- 2, which was only slightly less than half that observed in the creeks. However, the number of individuals showed a pro-

TABLE 2. Average number per m- 2 of species at the 13 stations sampled for the period 1993-1995. Station

Laeonereis acuta Heteromastus similis Tagelus gibbus Polydora ligni Comphium sp Uca sp. Mesodesma mactmides

210 51 0 0 0 0 0

582 36 0 0 0 136 0

3

4

784 102 0 0 0 0 0

363 1439 32 0 0 0 0

783 38 0 0 0 0 0

6

7

8

9

10

11

4515 3911 0 726 5337 0 0

3051 304 0 0 0 0 0

3726 11,962 0 127 1019 0 0

1033 529 0 0 0 0 0

1168 3935 0 0 0 0 0

2243 3326 64 0 0 0 0

12

0 0 0 0 0 0 70

13

0 0 0 0 0 0 197


nounced seasonal vanatlOn. It increased from about 796 ind m- 2 in February 1994 to >7800 ind m- 2 in August at both stations. The general trend was a decrease in late summer followed by an increase in autumn, especially for H. similis (Fig. 5). Densities in the disturbed areas, such as stations 7 and 9 (San Clemente Harbor), were depressed compared with the sites above. Highest values were observed in February 1995 (x = 8248 ind m- 2 ). Among the Tijeras tidal flats, abundance for all sampling periods followed an erratic pattern, with markedly lower densities (x = 602 ind m- 2 ). Station 5 showed a similar pattern to that observed in Tijeras Creek, while station 4 was closely associated with the Pta. Rasa stations. In addition to temporal and spatial changes in densities, the two dominant species also exhibit the widest spatial distribution in the bay and show significant local shifts in abundance between samples. This is shown in Fig. 5, in which spatial and temporal patterns of distribution for H. similis and L. acuta were examined at the six most important stations. This behavior confirms the initial impression that both species adopt an opportunistic strategy. None of these worms were ever found in large numbers in any sample from the Tijeras channels (stations 1 and 3) where the mud content was highest (more than 20%). U. uruguayensis density population fluctuated from 0 ind m- 2 to 378 ind m- 2 depending on the season and year, while C. granulata occurred in high densities the whole year. Animal-sediment Relationships In the study area, recognizable animal traces such as pellets and fecal fragments were found in stable sediments. A rich variety of traces made by fishes and birds were observed, revealing an intensive predation activity on benthic invertebrates. The deposit-feeding capitellid polychaete H. similis lives in a very fine sand substrate and makes a vertical mucus-lined tube up to a depth of about 30 cm. It moves to the sediment surface to excrete its fecal pellets; laboratory measurements denoted that length of pellets ranged between 0.3 mm and 1 mm. Generally, animals from intertidal populations were larger and heavier and produced bigger pellets than animals from subtidal levels. L. acuta was the other important polychaete species throughout the stations. It is a burrowing polychaete that feeds both on deposited detritus and juvenile infauna within the substrate. An inhabitant of fine sand (>50%), L. acuta was found a few centimeters below the sediment surface and was associated with the epifaunal organisms. Contrary to H. similis, no pellet production was found at the surface. P. ligni lives in muddy tubes in the crevices

695

between rocky structures and in empty C. insidiosum tubes. Specimens were abundant in the subtidal levels but no evidence of intertidal distribution was found. Sediment characteristics affect the depth to which Polydora and its tube penetrates the substrate since the proportion of worms decreased rapidly bellow the sediment. The razor clam T. giblms occurred from 20 cm to 50 cm sediment depth. It inhabited only mixohaline waters, where sediments traps filled slowly, indicating more stable sediments. Juvenile specimens were rarely observed in areas not inhabited by adults. Under field conditions, the siphons were never visible; however, siphon holes were shown to be occupied by clams. Burrow walls were blue-grey in color. The anterior part of the digestive tract of T. giblms regularly contained detritus, benthic diatoms, and silty-clay size sediments, characteristic of deposit-feeding organisms. The yellow clam, M. mactroides, inhabited the sandy beaches areas exposed to oceanic waters and is limited in its Argentine northern distribution by water salinity. The seasonal intertidal distribution of this clam is one of the most important patterns, as well as its high mobility in the substrate. M. mactroides is a typical suspension-feeder bivalve with a highly mobile inhalant siphon with which it indiscriminately collects material in the water-sediment interface. The two intertidal clams show clear preferences for a particular type of sediment, which is in agreement with their life strategies. Finally, the intertidal mobile epifaunal assemblage in the muddy areas was characterized by crabs, which occupied hundreds of hectares. This so-called "cangrejales" (crab zone) contains relatively high densities of the grapsid crab C. granulata. At the upper edges, it is bordered by a sandier zone dominated by the fiddler crab U. uruguayensis. This zonation pattern is likely to be found over the entire Samboromb6n Bay. The fiddler crab U. uruguayensis lives in a homogeneous intertidal habitat near the Spartina seagrass beds. Individuals dig deep burrows according to their caparace width which can be seen opened during low tide. Large casts of fecal pellets composed of indigestible sediment were found in the vicinity of each burrow where Uca feeds. In contrast, this feeding behavior was not found among the grapsid crab C. granulata. Other important member of the macrozoobenthos assemblages of subtidal bottoms was the amphipod C. insidiosum. The distribution of this amphipod extended into the subtidal channels where the species formed part of the estuarine fouling community on wooden pilings, rocks, and other artificial structures. High abundance coincided with an intense reproductive activity during the

696

E. N. lena and R. O. Bastida

Station 6

Station 7

Subtidal

Harbour

120 , - - - - - - - - - - - - - - - - - , (I)

o

100

80,---------------,

8 60

I:

I:

-l!l 80

-l!l I:

~ 60

~ 40

I: ::J

~

::J

l!l,

40

(I)

~

!! (I)

~ 20

20

o

J'93 A'93 0'93 0'93 F'94 A'94 J'94 A'94 0'94 F'95

J'93 A'93 0'93 0'93 F'94 A'94 J'94 A'94 0'94 F'95

Station 8

Station 9

Subtidal

Harbour

300,...--------------------, (I)

o

250

100 - , - - - - - - - - - - - - - - - - - - - - - - ,

8

I:

I:

-l!l200

-l!l

~ 150

~

I: ::J

I:

l!l,

80 60

~40

!! 100 (I)

(I)

~ 50

~ 20

o

J'93 A'93 0'93 0'93 F'94 A'94 J'94 A'94 0'94 F'95

Station 10

Station 11

Punta Rasa

Punta Rasa

80 . - - - - - - - - - - - - - - - - - - - ,

70 , - - - - - - - : : - : : : : - - - - - - - - - - - ,

i

8 60

I:

-l!l I: ::J

J'93 A'93 0'93 0'93 F'94 A'94 J'94 A'94 0'94 F'95

60 50

§ 40 ~

~ 40

i

~30 lii 20 ~

~ 20

10

J'93 A'93 0'93 0'93 F'94 A'94 J'94 A'94 0'94 F'95

I_ L. acuta • H. similis I

o +-_----+'~"+

J'93 A'93 0'93 0'93 F'94 A'94 J'94 A'94 0'94 F'95

'BIlL. acuta .H. similisl

Fig. 5. Average abundance (individuals per sample) of the two most abundant species: the polychaetes Laeonereis acuta and Heteromastus similis at partial stations for all sampling periods.


warm season, evidenced by the presence of females with eggs and young in samples. Discussion This is the first study of Samborombon Bay investigating the intertidal and coastal subtidal macrobenthos along the estuarine gradient (the brackish and marine part of the estuary). Previous studies have dealt mainly with crustacean fauna and mostly in the marine and mixohaline zone. (Boschi 1964). Studies of the sublittoral zone focusing on phytoplankton primary production and fishes have demonstrated the important role of this estuary as a nursery area for many commercial fishes and invertebrates. (Lasta 1995). Most of the sites are characterized by well-sorted to moderately well-sorted fine sand. Sediments are muddier in the inlet marshes and became coarser toward the Atlantic Ocean. This is in agreement with earlier studies showing that mud content is highest farthest from the marine influence (Bertola et al. 1993). The organic matter content values were moderate and peaked at the harbor, also consistent with previous reports (Bertola et al. 1993).

Low DIVERSITY The cluster analysis indicated the presence of two benthic communities in the south of Samborombon: a mixohaline, muddy fine-sand, H. similis and L. acuta-dominated community, and a marine sand-bottom community, characterized by the bivalve M. mactroides (Figs. 2 and 3). The H. similisL. acuta community is characterized by sediment texture, mud percentage, and organic matter content, whereas the M. mactroides community is determined largely by salinity and rarely occurs below 24 PSU. The distribulion of this clam is interrupted by La Plata River due to salinity differences and turbidity; it reappears in the Uruguayan coast and is found to Sao Pablo. Brazil. The most interesting aspect about the data obtained from the present survey is the evidence of marked differences in the abundance and in the low number of benthic species. Most of the stations showed very low values of both H' and H' / max' being 1,60 and 1 the highest values at St. 6, respectively. Low diversity values with a high dominance of polychaetes had been recorded previously at Mar Chiquita (Argentina), the southernmost coastal lagoon to occur along the temperate Atlantic coast of South America (Olivier et al. 1972; leno and Elias 1995). The same investigation was done by Bemvenuti (1987) relative to the dominance of three infaunal species (Kalliapseudes schubartii, H. similis and Nephtys fluvialilis) in the mixohaline zone of the Patos Lagoon, RS, Brazil. Compared with European estuaries, our results showed a very

697

impoverished species composition, less than that reported for macrofauna along the estuarine gradient of the Schelde Estuary near the Dutch-Belgian border (Seys et al. 1994). These authors pointed out the presence of Heteromastus filiformis as a very abundant species both in the marine and brackish part of the estuary. Tenore (1972) also reported H. filiformis as the species showing greatest numbers at the Pamlico River Estuary, North Carolina: the macrobenthiccommunity of 18 species had a similar low diversity index (0.66-1.77). Salinity conditions and unstable sediments were the factors that made Pamlico River Estuary unfavorable for the benthos (Tenore 1972). Seasonally predictable changes in freshwater inflow, wind and tidal mixing, microalgal biomass and sediment erosion and deposition patterns all contributed to observed seasonal changes in abundance as studied by Nichols and Thompson (1985) in estuarine San Francisco Bay. It should be noted that H. similis and L. acuta characteristic of unpredictable environments, tend to fluctuate widely in abundance. The decline in numbers of both species during some months of the study reflects short-lived species. Thus, recruitment of H. similis is not restricted to any season due to the presence of young worms throughout the year (Ieno unpublished data). In Brazil, this species also displays similar pattens (Bemvenuti 1987). The benthic species structure in this survey . is therefore not qualitatively different from other south Atlantic estuaries (Olivier et al. 1972; Capitoli et al. 1978; leno and Elias 1995). The superdominance exhibited by L. acuta and H. similis, with seasonal peaks followed by sharp declines in densities, denotes an opportunistic strategy. These kind of short-lived species have been reported in benthic studies from all over the world (Grassle and Grassle 1974; Pearson and Rosenberg 1978; Elias 1992). A classic example of year-to-year variability and decline in both size classes number and abundance due to over exploitation is provided by M. mactroides. The results from two monitoring programs conducted in 1960 and 1989 demonstrate a precipitous decrease at several localities (Bastida et aI. 1991). Moreover, during spring 1995, a rapid disappearance of much of the yellow clam adult population occurred along the Brazilian, Uruguayan, and Argentine Atlantic coast. This massive mortality phenomena has not been reported in Argentina before but was documented both in Brazilian and Uruguayan beaches in 1993 and 1994 respectively. THE EFFECT OF PERTURBATIONS

Disturbances caused by pollution are widely mentioned in the literature on benthic environ-

698

E. N. leno and R. O. Bastida

ments (e.g., Pearson and Rosenberg 1978; Suchanek 1993). These alterations in the community structure are often related to sewage disposal and oil impacts. This seems to be the case for stations 7 and 9, which are near the head of the local harbor and showed a complete defaunation, coincident with periods of oil runoff. Comparisons of the histograms of the harbor site with other locations showed the dominance of the polychaete L. acuta, indicating its higher tolerance to stress and high organic matter levels (Fig. 5). Other important natural sediment disturbance in the survey area is the effect of predation. Abundance ofjuvenile fish predators, such as Odonthestes spp. and Paralicthys spp. which frequently consume macrobenthic prey, were highest in spring and summer in both subtidal and intertidal areas. Among shore birds, the sandpipers (Scolopacidae) Calidris canutus rufa, Calidris fuscicollis, Limosa haemastica, and Tringa flavipes and the plovers (Charadriidae) Pluvialis dominica, Charadrius falklandicus, and Charadrius collaris are important predators of polychaetes and biva.lves (Bertola et al. 1993). Heavy predation would occur only in intertidal areas where there are large numbers of worms mainly in the warm season, suggesting that increased predation on infauna may be another reason for observed decreases in densities. FEEDING MECHANISMS OF BENTHIC ORGANISMS AND SEDIMENT REWORKING ACTIVITIES

The most abundant macrobenthic species are deposit or deposit resuspension feeders (mainly polychaetes) with opportunistic life strategies whose local abundance would be expected to be correlated with organic content of the sediments (Pearson and Rosenberg 1978; Fauchald and Jumars 1979). Biological studies carried out on H. similis showed a close similarity in the feeding behavior and fecal pellet production of H. filiformis, the northern species, suggesting the importance of the genus in sediment reworking activities (Cadee 1979). Another aspect to be considered in the feeding mechanisms, is the alternative role of M. mactroides as a suspension- and deposit-feeder. Originally, the yellow clam was described as an exclusively suspension-feeder (Olivier et al. 1971; Gianuca 1983). However, laboratory experiments carried out in Uruguay and in our facilities found the existence of a deposit-feeder mechanism under . extreme conditions (Defeo and Scarabino 1990). This seems to be the case of specimens analyzed from the transition zone, due to the high percentage of detritus and fine sand in their digestive tracts. Sediment reworking by crabs also plays an important part in intertidal mud flat areas. C. granu-

lata and the fiddler crab U. uruguayensis are both semiterrestial burrowing species. Both crabs are common constituents of the salt-marsh community in the south of Samboromb6n Bay (Boschi 1964). C. granulata reached its highest population density at Tijeras Creek (69 ind m- 2) were the mud content was about 25%. Spivak et al. (1994) found a maximum population density value of 53 ind m~2 at Mar Chiquita Lagoon. Moreover, these authors, suggested that "dry mud" habitats constitute the suitable conditions to burrow. Analysis of sediment reworking activities such as sediment ingestion and ventilation of dwelling, may be required to assess more accurately how infauna alter the chemistry of this particular environment. Furthermore, important factors in the organization of this soft-bottom community such as predation by birds and fishes should be examined in detail. ACKNOWLEDGMENTS This study was financially supported by CIC, CONICET and Foundation Mundo Marino. The campaigns could not have been done without the help of Jorge Rebollo. We are grateful to Bruno J. Ens (IBN. Texel, The Netherlands) and R. Elias (Cs. Marinas, U.N.M.d.P.) for critical readings of this paper and their valuable suggestions for the final manuscript. We are also indebted to J. c. Dauvin, and two anonymous reviewers for valuable suggestions to earlier versions of the manuscript. This work constitutes part of a doctoral dissertation being developed by the first author. LITERATURE CITED BASTIDA, R. 0., A. Roux, C. BREMEC, M. GERPE, AND M. SORENSEN. 1991. Estructura poblacional de la almeja amarilla (Mesodesma mactroides) durante el verano de 1989 en la Provincia de Buenos Aires, Argentina. Frente Maritimo 9 Sec. A:83-92. BERTOLA, G. R., H. MASONE, AND M. OSTERRIETH. 1993. Estudio geologico integral de Punta Rasa, Cabo San Antonio, Provincia de Buenos Aires. Serie Situaci6n Ammental de la Provincia de Buenos Aires (CIC) 25:1-28. BEMVENUTI, C. E. 1987. Macrofauna bentonica da regiao estuarial da lagoa Dos Patos, rs, Brasil. Simposio sobre ecossistemas da costa sui e sudeste brasileira. Publicaci6n Aciesp 54:428459. BOSCH!, E. E. 1964. Los crustaceos decapodos brachyura del litoral bonaerense (R. Argentina). Boletin del Instituto de Biologia Marina 6:1-99. BOSCH!, E. E. 1982. Investigaciones biologico pesqueras del ecosistema costero bonaerense. Simposio Internacional sobre utilizacao de ecosistemas Costeiros, planejamento, poluicao e produtiuidade. Atlantica Rio Grande 5:1-5. CADEE G. C. 1979. Sediment reworking by the polychaete Heteromastus filiformis on a tidal flat in the Dutch Wadden Sea. Netherlands Journal of Sea Research 13:441-456. CAPITOL!, R. R., C. BEMVENUTI, AND N. GIANUCA. 1978. Estudos de ecologia bentonica na regiao estuarial de Lagoa Dos Patos. I-As comunidades bentonicas. Atlantica 3:5-22. CZEKANOWSKI, J. 1913. Zarys Metod. Statystycznyck. Warsaw, Poland. DEFEO, O. AND V. SCARABINO. 1990. Ecological significance of a possible deposit-feeding strategy in Mesodesma mactroides (Deshayes, 1854) (Mollusca: Pelecypoda). Atlantica 12:55-65.


DICE, L. R 1945. Measures of the amount of ecological association between species. Ecology 26:297-302. ELIAS, R 1992. Quantitative benthic community structure and its relationship with organic enrichment. Marine Ecology 13: 189-201. ELIAS, R. AND C. BREMEC. 1994. Biomonitoring of water quality using benthic communities in Blanca Bay (Argentina). The Science of the Total Environment 158:45-49. ELIAS, R AND E. IENO. 1993. La Asociacion de Laeonereis acuta Treadwell, 1923 (Polychaeta, Nereididae) en la Bahia Blanca, Argentina. Iheringia Serie Zoologia 75:3-13. FAUCHALD, K. AND A. JUMARS. 1979. The diet of worms: A study of polychaetes feeding guilds. Oceanography Marine Biology Annual Review 17:193-284. GIANUCA, N. M. 1983. A preliminary account of the ecology of sandy beaches in southern Brasil, p. 413-419. In A. McLachlan and T. Erasmus (eds.), Sandy Beaches as Ecosystems. W. Junk, The Hague. GRASSLE, J. F. AND J. P. GRASSLE. 1974. Opportunistic life histories and genetics systems in marine benthic polychaetes.Journal of Marine Research 32:253-255. IENO, E. N. AND R ELIAS. 1995. Studies on a southern polychaete Capitellidae Heteromastus similis Southern, 1921 in Mar Chiquita brackish coastal lagoon, Argentina. Neritica 9:23-32. LASTA, C. A. 1995. La Bahia Samborombon: Zona de desove y cria de peces. Tesis doctoral. Facultad de Ciencias Naturales y Museo. Universidad Nacional de La Plata, Argentina. MORRISON, R I. G. AND B. A. HARRINGTON. 1992. The migration system of the Red Knot Calidris canutus rufa in the New World. Wader Study Group Bulletin 64 Suppl:71-84. NICHOLS, F. H. ANDJ. K. THOMPSON. 1985. Time scales of change in the San Francisco Bay benthos. Hydrobiologia 129:121-138. OLIVIER, S. R, D. A. CAPEZZANI, J. CARRETO, H. CHRISTIANSEN, V. MORENO, J. A. DE MORENO, AND P. E. PENCHASZADEH. 1971.

699

Estructura de la comunidad, dinamica de la poblacion y biologia de la almeja amarilla (Mesodesma mactroides Desh., 1854) en Mar Azul (Pdo de Gral. Madariaga, Bs. As., Argentina). Proyecto Desarrollo Pesquero Fao Servicio Informacion Tecnica Publicacion 27: 1-90. OLIVIER, S. R, A. ESCOFET, P. PENCHASZADEH, AND J. M. ORENSANZo 1972. Estudios ecologicos en la region estuarial de Mar Chiquita (Buenos Aires, Argentina). 1: Las comunidades bentonicas. Annates Sociedad Cientifica Argentina 193:237-261. PEARSON, T. H. AND R ROSENBERG. 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanography Marine Biology Annual Review 16:229-311. PIELOU, E. C. 1966. The measurement of diversity in different types of biological collection. Journal of Theoretical Biology 13: 131-144. SElS,J.J., P. M. MElRE,J. COOSEN, ANDJ. A. CRAEYMEERSCH. 1994. Long-term changes (l979-89) in the intertidal macrozoobenthos of the Oosterschelde estuary: Are patterns in total density, biomass and diversity induced by the construction of the storm-surge barrier? Hydrobiologia 282/283:251-264. SPIVAK, E., K. ANGER, T. LUPPI, C. BAS, AND D. ISMAEL. 1994. Distribution and habitat preferences of two grapsid crab species in Mar Chiquita Lagoon (Province of Buenos Aires, Argentine) Helgolaender Meeresuntersuchungn 48:59-78. SUCHANEK, T. H. 1993. Oil impacts on marine invertebrate populations and communities. American Zoology 33:510-523. TENORE, K. R 1972. Macrobenthos of the Pamlico River Estuary, North Carolina. Ecological Monographs 42:51-69. WALKLEY, A. AND A. BLACK. 1965. Organic carbon, p. 1372-1375. In A. Black and J. Evans (eds.), Method of Soils Analysis. American Society of Agronomy. Madison, Wisconsin. Received for consideration, January 6, 1997 Accepted for publication, February 19, 1998