Thalassas, 27 (1): 9-20
                                                                                  An International Journal of Marine Sciences

                                         PATAGONIA, ARGENTINA


Key words: benthos; tidal flat; distribution; temporal variation; Patagonia.

    ABSTRACT                                                              INTRODUCTION

     The aim of this work was to analyze spatial and                          Distribution, diversity, and abundance of ben-
temporal variations in composition and abundance                          thic organisms inhabiting intertidal environments
of benthic species assemblages in an intertidal                           have been associated with variations of several
environment of the Río Gallegos Estuary, Patagonia,                       factors, such as depth, tidal height, time of expo-
Argentina (51° 35’ S 69° W). Species distribution                         sure, and type of sediment (Dahl, 1952; Beukema,
and its temporal fluctuations were analyzed using                         1976; Mc Lachlan, 1983; Day et al., 1989; Brown &
multivariate statistical methods. Different species                       Mc Lachlan, 1990; Zaixso et al., 1998; Dittmann,
assemblages were observed, their distribution being                       2000; Lizarralde, 2002; Veloso et al., 2003). Food
related to the tidal level and type of intertidal                         availability, larval dispersal and settlement, intra
sediment. The polychaete Scolecolepides uncinatus                         and interspecific competition, and the effects of
was dominant in a species assemblage restricted to                        predation also inf luence community structure.
the high intertidal levels, which are characterized by                    Some experimental studies have demonstrated
silty clay sediments. At the intermediate intertidal                      that biological interactions, such as predation
level, the number of species and total macrofauna                         and competition, affect the benthic community
abundance increased; at this level, the clam                              structure by acting on recruitment, survival, or
Darina solenoides and the mussel Mytilus edulis                           migration of organisms (Woddin, 1974; Peterson
platensis were dominant. At the low levels, which                         & Andre, 1980; Brenchley, 1982; Thrush et al.,
are composed of fine sediments, the polychaete                            1992; Knox, 2000).
Clymenella minor and the bivalve Mysella sp. were
dominant. Temporal variations detected in species                             Benthic communities may fluctuate in a cyclic
abundance were mainly due to the incorporation                            pattern over time, because of the characteristics of
of recruits in the population, especially of the most                     the life cycle of the species, as well as of the influence
abundant species.                                                         of temporal fluctuations of abiotic factors, such as
                                                                          environmental temperature or salinity (Day et al.,
(1) Universidad Nacional de la Patagonia Austral, Lisandro de
la Torre 1070, 9400 Río Gallegos, Santa Cruz, Argentina. Fax:
                                                                          1989; Souza & Gianuca, 1995; Veloso et al., 1997; Das
054-02966 442620, e-mail: zlizarralde@uarg.unpa.edu.ar                    Neves et al., 2008).


                                                               Figure 1:
                                Study area at the Río Gallegos Estuary, southern Patagonia, Argentina.

    Soft-bottom intertidal benthic communities from                    the Red Knot (Calidris canutus), and the Hudsonian
the southern portion of Argentine Patagonia have                       Godwit (Limosa haemastica). These species arrive
been poorly studied. The few studies conducted in the                  from the Northern Hemisphere and use the estuary
region have provided information on communities                        as a migration stopover site during the non-breeding
from shallow subtidal environments (Lopez Gappa                        season; the estuary also provides shelter to some
& Cruz Sueiro, 2006, Martin & Bastida, 2008).                          species endemic to southern Patagonia, such as the
There are also reports from the Chilean portion                        Magellanic Plover (Pluvianellus socialis) and the
of the Strait of Magellan that contribute to the                       Magellanic Oystercatcher (Haematopus leucopodus)
knowledge of those organisms in the region and that                    (Ferrari et al. 2002, 2007, 2008, Albrieu et al. 2004).
allow us to make comparisons at a regional scale                       Small-scale artisanal fisheries are conducted at the
(Espoz et al., 2008).                                                  estuary, one of the target species being the Patagonian
                                                                       blenny Eleginops maclovinus (Caille et. al., 1995),
    The Río Gallegos estuary is located in the province                which also feeds on benthic organisms (Martín &
of Santa Cruz, southern Patagonia. Its northern shore                  Bastida, 2008).
is high, with cliffs and gravel beach plains, whereas
the southern shore is dominated by vast muddy                              Despite the ecological importance of the
intertidal flats, saltmarshes, and complex channels                    estuary, no systematic studies of benthic organisms
(Perillo et al., 1996). It is a Western Hemisphere                     inhabiting the variety of intertidal environments
Shorebird Reserve Network (WHSRN) Site of                              have been conducted; therefore, it is necessary to
international importance because it provides habitat                   generate baseline information that contributes to the
and food for a high number of Nearctic migratory                       management of the coastal area, which is permanently
shorebirds that visit the area during summer, such as                  influenced by anthropogenic activities (recreation,
the White-rumped Sandpiper (Calidris fuscicollis),                     sport and commercial fisheries, urban development)

                                                                   IN A TIDAL FLAT OF THE RIO GALLEGOS ESTUARY, PATAGONIA, ARGENTINA

because of its proximity to the city of Río Gallegos.                     with a 0.5 mm mesh and frozen. In the laboratory,
The aim of this work was to analyze the composition,                      organisms were identified to the smallest possible
abundance, and distribution of benthic species                            taxonomic level under a stereoscopic microscope
assemblages, as well as the temporal variations of                        and quantified.
species abundance throughout a year of study at the
Río Gallegos Estuary.                                                        Sediment samples were taken in December 2005
                                                                          from each of the five levels. Sediment grain size
MATERIALS AND METHODS                                                     was analyzed through sieving and expressed as
                                                                          proportions. On the same date another sampling was
    The Río Gallegos Estuary is located in                                conducted to determine total organic matter content
southeastern continental Patagonia, Argentina (51°                        (combustion at 550 °C for 5 h).
35’ S 69° W). The tidal regime is semi-diurnal
with a mean tidal range of 10.8 m on spring tides                             To analyze distribution and temporal variation of
and 2.9 m on neaps. The cool coastal climate has a                        the benthic macrofauna a nonmetric multidimensional
mean annual temperature of 7.2 °C and west winds                          scaling ordination technique (MDS) was applied
blowing at an average speed of 35 km/h. The city                          employing the Bray-Curtis similarity index (calculated
of Río Gallegos, with a population of some 90,000                         on square-root transformed species abundance).
inhabitants, is located on the southern shore of the                      The analysis was performed using PRIMER v5
estuary.                                                                  (Clarke & Warwick, 1994; Clarke & Gorley, 2001).
                                                                          A similarity analysis (ANOSIM; α = 0.05) was
    The benthic macrofauna was sampled monthly                            performed to evaluate differences between sample
during 12 months (December 2005 to November                               levels and between seasons. Similarity percentage
2006) in an extensive tidal flat located on the                           analysis (SIMPER) was used to explore the species
southern shore of the estuary (Fig. 1). Samples were                      contribution to similarity between the groups formed
collected with a corer (15 cm diameter, 20 cm deep)                       (Clarke, 1993).
at five tidal levels along a transect perpendicular to
the waterline. Six biological samples were monthly                            To analyze temporal variation of the benthic
collected per level (levels 1 to 5). Level 1 was                          macrofauna, monthly mean of species abundance
located on the uppermost intertidal flat region and                       was calculated with the aim of removing the effect of
Level 5 on the lowest one. Samples were sieved                            inter-level variability.

    80                                                                      3
    40                                                                      2
     0                                                                      1
           Level 1 Level 2 Level 3 Level 4 Level 5

         Gravel               Coarse sand         Fine sand                 0
         Mud                  Medium sand         Very fine sand                Level 1   Level 2     Level 3     Level 4    Level 5

                               Figure 2:
                                                                                                     Figure 3:
                  Grain size composition of sediment.
                                                                                     Total organic matter content in sediments.


    To investigate the vertical distribution patterns                                                     Stress: 0,03
                                                                                                        Stress 0.03
from high to low levels, the data from December                                                                              1
2005 were subjected to a Canonical Correspondence
Analysis (CCA) (Ter Braak, 1985), which included                                                                             2
tidal level (levels 1 to 5), sediment (gravel, coarse,
medium, fine, very fine sand; and mud) and total                                                                             3
organic matter content as environmental variables.
Forward selection of environmental and biotic                                                                                4
variables and Monte Carlo permutations were used to
identify a subset of the measured variables that exert                                                                       5

significant and independent influence on the benthic
macrofauna distribution.                                                              Figure 4:
                                                            MDS showing general distribution of samples in the tidal flat.
    Number of species (S), total macrobenthos                1: Level 1, 2: Level 2, 3: Level 3; 4: Level 4; 5: Level 5.

abundance (A), and Shannon-Wiener diversity
index (H’) were also determined for each tidal level       1. Levels 3 and 4 exhibited the highest number of taxa
(Magurran 1989).                                           and diversity index.

   Small individuals of Darina solenoides (≤ 5 mm)         Spatial distribution
and M.e. platensis (≤ 5 mm) were considered recruits
and were counted under a micrometric eyeglass.                 Results of MDS analysis showed a clear pattern
                                                           of macrofauna distribution (Fig. 4). Samples were
RESULTS                                                    separated into three groups, indicating differences
                                                           in abundance and composition among faunal
Environmental variables                                    assemblages. ANOSIM revealed significant
                                                           differences among groups (Table 2). One group
    The sediment type of levels 1 and 2 consisted mainly   comprised levels 1 and 2, with dominance of the
of mud (more than 50%) and very fine sand (30%).           polychaete Scolecolepides uncinatus; the second
Sediment of Level 3 was classified as fine sand (41%),     group was composed of samples obtained from levels
very fine sand (22%), and mud (16%); Level 4 consisted     3 and 4, characterized by Darina solenoids and
mainly of fine sand (33%) and gravel (31%); and Level 5    Mytilus edulis platensis; and the third group included
was composed of very fine sand (35%) and mud (26%)         samples from Level 5, characterized by Climenella
(Fig. 2). Total organic matter content decreased from      mirror and Mysella sp. (Table 3).
Level 1 (2.5%) to Level 5 (1.1%) (Fig. 3).
                                                               According to results of CCA between benthos
Benthic macrofauna                                         species and environmental variables, the most
                                                           important variable was tidal level, followed by fine
    A total of 24 taxa were collected (Table 1).           sand and mud (Fig. 5). The variables coarse, medium,
Polychaeta was the most diverse taxa, followed by          and very fine sand, and organic matter were not
Mollusca and Crustacea. Based on mean abundance of         selected by the CCA. Axes 1 and 2 explained 85% of
each species in the pooled samples collected, Darina       the variance of the species-environment relationship
solenoides and Mytilus edulis platensis contributed        (Table 4). The ordination showed that tidal level, fine
with 59% of the total number of individuals. Species       sand, and mud were related to axis 1 and that gravel
richness and diversity index values are shown in Table     was related to axis 2 (Table 5).

                                                                   IN A TIDAL FLAT OF THE RIO GALLEGOS ESTUARY, PATAGONIA, ARGENTINA

                                                                   Figure 5:
                                   Biplot of CCA analysis between benthic species and environmental variables.
  GRA: gravel; MUD: mud; F SAND: fine sand; LEV: level; Myti: Mytilus edulis platensis; Scole: Scolecolepides uncinatus; Clymen: Clymenella
minor; Mysella: Mysella sp.; Noto: Notocirrus lorum; Dari: Darina solenoides; Kinberg: Kinbergonuphis dorsalis; Lumbri: Lumbrinereis cingulata;
 Hemi: Hemipodus patagonicus; Aglao: Aglaophamus praetiosus; Eteo: Eteone sculpta; Glyci; Glycinde armata; Monoc: Monoculopsis vallentini.

     Solecolepides uncinatus and Eteone sculp-                              of recruits in april, and at the end of spring
ta were related to high tidal levels and muddy                              (November) with 25%; recruitment of Mytilus
sediments. Darina solenoides, Kimbergonuphis                                edulis platensis was most intense in summer (41%
dorsalis, Lumbrinereis cingulata, Glycinde arma-                            in January) (Fig.7). Abundance of polychaete and
ta, Aglaophamus praetiosus, Notocirrus lorum,                               crustaceans together remained stable throughout
Hemipodus patagonicus and Monoculopsis vallen-                              the year evaluated (Fig. 6).
tini assemblage was associated with intermediate
levels and fine sand; Clymenella minor and Mysella                              The MDS analysis of temporal variation indicated
sp., were associated with fine sand and lower levels,                       a tendency to the formation of two groups: one group
and Mytilus edulis platensis-Edotia tuberculata,                            included samples obtained in spring (September to
with intermediate tidal levels and gravel sediments                         November) and summer (December to February)
(Fig. 5).                                                                   months; the other group was composed of samples
                                                                            from fall (March to May) and winter (June to August)
Temporal variation                                                          (Fig. 8). ANOSIM tests showed significant differences
                                                                            between groups (Table 6). The SIMPER analysis
    Darina solenoides and M. e. platensis were the                          showed that Darina solenoides and M.e.platensis
most abundant species throughout the study period                           were the organisms that mostly contributed to
(Fig. 6). Darina solenoides presented highest                               formation of the fall-winter and summer-spring
abundance values in fall (April-May), with 35%                              groups, respectively (Table 7).


             2000                                                                45
             1500                                                                35

             1000                                                                20
               0                                                                      D    J   F    M    A   M     J   J   A    S   O     N
                    D   J   F   M    A    M     J   J     A    S    O    N                         D. solenoides   M.e. platensis
                                D. solenoides           M.e. platensis
                                Polychaeta              Crustacea

                                                                                                         Figure 7:
 Figure 6: monthly number of dominant species or group of species.            Recruits (%) from Darina solenoides and Mytilus edulis platensis.

DISCUSSION                                                                   species in the different habitats remained constant
                                                                             throughout the study period (12 months). The high
     The present study is the first description of benthic                   tidal flat (levels 1 and 2) characterized by silty
organism assemblages inhabiting the intertidal flat in                       clay sediments, was dominated by the polychaete
an area located on the southern shore of the estuary,                        Scolecolepides uncinatus; two other polychaete
near the city of Río Gallegos. The sediment is                               species were also present but in low numbers. At
characterized by the presence of high percentages of                         the intermediate levels (3 and 4), the number of
silt and clay at the high levels of the intertidal, and                      species and total fauna abundance increased. A
of sand at the intermediate and low levels. Organic                          group of species associated with sandy sediments,
matter content in sediments also differed among                              dominated by the clam Darina solenoides and the
tidal levels, the highest values being recorded at high                      polychaete Kinbergonuphis dorsalis inhabits these
levels.                                                                      levels. The mussel M.e.platensis was also recorded
                                                                             at levels 3 and 4, but in sediments with intermediate
    The benthic community was characterized
by low species richness but great abundance of
individuals, mainly the bivalve Darina solenoides                                                                          Stress: 0.03
and M. e. platensis. This feature has been mentioned
for different estuarine areas of the South Atlantic,
especially in comparison with the adjacent marine                                                                                                 2

ecosystems (Ieno & Bastida, 1998; Lopez Gappa
et.al., 2001; Passadore et. al., 2007).                                                                                                           3

    In most tidal flats macrofauna distribution
patterns vary with environmental conditions
following an intertidal gradient (Whitlatch, 1977;
Junoy & Vieitez, 1990); species diversity is in general
greatest at the intermediate levels (Beukema, 1976;                                                    Figure 8:
                                                                                        MDS showing general ordination of samples.
Armonies & Hellwig-Armonies, 1987). This pattern                                          1: summer months; 2: autumn months,
has been observed in our study, since distribution of                                      3: winter months, 4: spring months.

                                                                IN A TIDAL FLAT OF THE RIO GALLEGOS ESTUARY, PATAGONIA, ARGENTINA

                                                                  Table 1:
      Mean densitiy (indiv/m2) of each macrobenthos taxon in the pooled samples collected between December 2005 and November 2006;
                                                         (SD= standard deviation).

                                                    LEVEL 1          LEVEL 2            LEVEL 3              LEVEL 4            LEVEL 5
                                                    Av (SD)          Av (SD)            Av (SD)              Av (SD)            Av (SD)

Darina solenoides                                     -----            6.3 (2.7)     1832.1 (548.2)       1039.5 (216.6)         58.5 (67)
Mytilus edulis platensis                              -----            -----          217.6 (197.3)       1834.8 (528.1)           9.8 (17)
Mysella sp.                                           -----            -----             46.6 (9.9)          32.1 (12.4)       144.2 (63.6)
Perumytilus purpuratus                                -----            -----             -----               27.0 (16.0)         -----
Aulacomya atra                                        -----            -----             -----               18.0 (11.5)         -----
Trophon geversianus                                   -----            -----               -----               25.5 (8.7)        12.4 (5.2)
Natica falklandica                                    -----            -----               11.3 (6.9)         22.3 (13.5)        -----
Polychaeta                                                                                                                       -----
Scolecolepides uncinatus                           247.8 (87.1) 190.1 (59.6)              10.0 (8.4)          -----              -----
Eteone sculpta                                       22.8 (5.3) 57.0 (25.2)              18.0 (19.7)          -----              -----
Hemipodus patagonicus                                -----       36 (11.0)              129.6 (41.8)         37.0 (10.5)         -----
Aglaophamus praetiosus                               -----         -----                120.9 (22.9)          -----              -----
Kinbergonuphis dorsalis                              -----       33.9 (26.7)           571.9 (129.2)       306.0 (155.0)       121.0 (19.8)
Glycinde armata                                      -----         -----                161.8 (42.6)         76.6 (13.8)         -----
Lumbrinereis cingulata                               -----         -----                164.0 (33.9)          -----              -----
Notocirrus lorum                                     -----         -----                151.5 (21.5)          -----             58.7 (18.3)
Clymenella minor                                     -----         -----                  -----               -----            219.0 (70.4)
Travisia sp.                                         -----         -----                  -----               -----              16.0 (3.2)
Nemertea indet.                                       -----            -----               -----              12 (3)             6(2.1)
Anfípodo indet.                                     36.0 (17.0)        -----               -----              -----               -----
Monoculopsis vallentini                              -----             9.6 (4.0)          41.2 (11.4)        24.8 (13.2)        30.4 (18.9)
Peltarion spinosulum                                 -----             -----               -----              -----                 2.4 9.6)
Halicarcinus planatus                                -----             -----               -----              -----               -----
Edotia tuberculata                                   -----             -----               -----           44.7 (20.0)            -----
Priapulid                                                                                                                         -----
Priapulus sp.                                         -----            7.4 (5.7)           20.9 (8.1)          -----              -----
Number of species S                                     3                      6                  14            13                 11
Shannon-Wiener diversity index H’                     0.60                   1.0                  1.7          1.8                1.4

proportions of gravel, because the species requires
coarse sedimentary substrates to settle. The great                                                       Table 2:
abundance of juveniles of both the clam and the                                Analysis of similarity (ANOSIM) between levels (all months).
                                                                                                Global R: 0.875, P= 0.1%.
mussel that recruited at the intermediate level also
indicates that this region provides good conditions
as nursery grounds for these species. By contrast,                                 Groups                     R                  P
                                                                                   Level 1 vs 2             0.297                0.1
the low levels seem to favour mainly the polychaete                                Level 1 vs 3               1.0                0.1
Clymenella minor and a bivalve, Mysella sp., both                                  Level 1 vs 4               1.0                0.1
of which are dominant in very fine sands with                                      Level 1 vs 5               1.0                0.1
intermediate proportions of mud.                                                   Level 2 vs 3               1.0                0.1
                                                                                   Level 2 vs 4               1.0                0.1
                                                                                   Level 2 vs 5               1.0                0.1
    In general terms, intertidal zoobenthic                                        Level 3 vs 4             0.815                0.1
assemblages at the Río Gallegos estuary are notably                                Level 3 vs 5             0.999                0.1
                                                                                   Level 4 vs 5             0.995                0.1
similar in composition to those described by Espoz


                                                                   Table 3:
                    Results of SIMPER analysis. Main species that contributed (%) to the differences observed among groups.

                        Groups                                     Level 1-2          Level 3-4            Level 5
                        Scolecolepides uncinatus                       94.20
                        Kinbergonuphis dorsalis                                           24.46             20.71
                        Clymenella minor                                                                    34.62
                        Darina solenoides                                                 33.46
                        Mytilus edulis platensis                                          20.10
                        Mysella sp.                                                                         31.50

                                                                 Table 4:
                                                         Summary of CCA ordination.

                      Axis                                                       1         2          3              Total
                      Eigenvalues                                              0.90      0.27       0.134            1.54
                     species-environment correlations                          0.86      0.80       0.67
                     Cumulative percentage variance
                        Species data                                           25.8      26.2       24.9
                        Species-environment relationship                       45.9      85.0       92.5
                     Sum of all unscontrained Eigenvalues                                                            1.54
                     Sum of all canonical Eigenvalues                                                                1.37

et al. (2008) for Bahía Loma in the Chilean portion                             During our study we did not observe temporal
of the Strait of Magellan. These authors described                          variability of species composition. Temporal
a community dominated by Darina solenoides,                                 fluctuations recorded were related to changes in
polychaete and crustaceans; however, we did not                             species abundance, which were strongly influenced
record the polychaete Aricidea sp., which has been                          by the incorporation of recruits to the populations.
mentioned as the most abundant polychaete species.                          Settlement of the clam D. solenoides presented two
On the other hand, no similarities were observed                            peaks: one at the start of fall and the other in
between the species assemblage found in the estuary                         late spring-early summer. The mussel M.e.platensis,
and that described by Lopez Gappa & Cruz Suiero
                                                                                                            Table 6:
(2006) for a coastal area of the South Atlantic in                                    Analysis of similarity (ANOSIM) between seasons.
Tierra del Fuego (Bahía San Sebastián).                                                           Global R: 0.852, P= 0.1%.

                                                                                 Groups                            R                P
                             Table 5:
CCA. Weighted correlation matrix of environmental variables with the            Summer vs Fall                    1.0               0.1
                           species axis.
                                                                                 Summer vs Winter                 1.0              0.1
                                                                                 Summer vs Spring                 0.793            0.1
 Name                                  Axis 1            Axis 2
 Tidal Level                            0.85               0.39                  Fall vs Winter                   0.385             0.1
 Fine sand                              -0.78              -0.15                 Fall vs Spring                   1.0               0.1
 Mud                                     0.72             - 0.01
 Gravel                                 -0.02               0.50                Winter vs Spring                  1.0              0.1

                                                                 IN A TIDAL FLAT OF THE RIO GALLEGOS ESTUARY, PATAGONIA, ARGENTINA

                                                                 Table 7:
              Results of SIMPER analysis. The main species that contributed (%) to the formation of the groups are presented.

                                                                Summer-Spring                 Fall-Winter
                     Darina solenoides                               35.0                         57.8
                     Mytilus edulis platensis                       54.3                          27.1
                     Kinbergonuphis dorsalis                         7.2                           9.4

however, exhibited the highest proportion of recruits                     be developed, since salinity, which has not been
in summer. Several authors have mentioned that                            considered in the present work, has been mentioned
recruitment of benthic species affects abundance of                       as a determining factor in the species distribution of
macrofaunal communities (Colling et al., 2007; Das                        estuarine environments (Dittmann, 2000). Thus, a
Neves et al., 2008). But other factors may also be                        more detailed record of the number of benthic species
responsible for changes in the number of individuals,                     present at the estuary could be obtained and the species
such as predation pressure exerted by crustacean, fish,                   contribution to energy flow and especially to the diet
and bird species throughout the year or when these                        of birds and fishes could be elucidated. Moreover, long-
species are present in coastal environments during                        term studies will help us understand whether changes
migration (Gianuca 1983; Jaramillo et. al., 1996;                         detected in benthic communities are naturally induced
Iribarne & Martinez, 1999; Ferreira et al., 2005).                        or are a consequence of urban development and plan
The arrival of flocks of some bird species on their                       management strategies for the area accordingly.
migration flight agrees with the peak of macrofauna
abundance in southern Brazil (Vooren, 1998).                              ACKNOWLEDGMENTS

     The Río Gallegos estuary has been mentioned                              This work was totally supported by the
as an important wetland for the Red knot Calidris                         Universidad Nacional de la Patagonia Austral (Project
canutus and the Hudsonian Godwit Limosa                                   PI 29 A-180).
haemastica (Ferrari et al., 2002, 2007; Albrieu et
al., 2004). These species are of conservation concern                     REFERENCES
because of the reduction observed in their populations
at the global scale (Baker et al., 2004; González                         Albrieu C, Imberti S & Ferrari S (2004). Las Aves de la
et al., 2004; Morrison et al., 2004, 2006); they use                          Patagonia Sur, el Estuario del Río Gallegos y zonas
the estuary as feeding and roosting sites during                              aledañas. Ed. Universidad Nacional de la Patagonia
their transcontinental migrations. Darina solenoides                          Austral, Río Gallegos, 204 pp.
has been mentioned as the main prey item in the                           Armonies W & Hellwig-Armonies M (1987). Synoptic
diet of the Hudsonian godwit and the Red knot in                              patterns of meiofaunal abundances and specific
several intertidal sectors in southern Patagonia, both                        composition in littoral sediments. Helgoländer
in Argentina and Chile. The mussel and several                                Meeresunters 41: 83-111.
polychaete species are also secondary prey for those                      Baker A, González P, Piersma T, Niles LJ, do Nascimento
bird species (Espoz et. al., 2008; Hernández et. al.,                         I, Atkinson PW, Clark NA, Minton CDT, Peck MK &
2004, 2008; Lizarralde et. al., 2010).                                        Aarts G (2004). Rapid population decline in red knots:
                                                                              fitness consequences of decreased refuelling rates and
    A monitoring program to study different sites                             late arrival in Delaware Bay. Proceeding of the Royal
of the estuary along a salinity gradient needs to                             Society of London B 271: 875–882.


Beukema JJ (1976). Biomass and species richness of the                ecology of the Red Not Calidris canutus rufa at Bahia
    macrobenthic animals living on the tidal flats of                 Lomas, Tierra del Fuego, Chile. Wader study group
    the Dutch Wadden Sea. Netherlands Journal of Sea                  Bulletin 115 (2): 69-79.
    Research 10, 236-261.                                         Ferrari SN (2001). Identificación de áreas óptimas para la
Brenchley GA (1982). Mechanisms of spatial competition                conservación de aves playeras en el estuario del río
    in marine soft-bottom communities. Journal of                     Gallegos, Santa Cruz, Argentina. Tesis de Maestría.
    Experimental Marine Biology and Ecology 60: 17-33.                Universidad Nacional de Córdoba.
Brown AC & MC Lachlan A (1990). Ecology of sandy                  Ferrari S, Albrieu C & Gandini P (2002). Importance of
    shores. Elsevier, Amsterdam, 326 pp.                              the Rio Gallegos estuary, Santa Cruz, Argentina, for
Caille G, Ferrari S & Albrieu C (1995). Los peces de la               migratory shorebirds. Wader Study Group Bulletin 99:
    Ría de Gallegos, Santa Cruz, Argentina. Naturalia                 35–40.
    Patagónica, Serie Ciencias Biológicas 3: 191–194.             Ferrari S, Albrieu C & Imberti S (2005). Áreas de
Clarke KR (1993). Non-parametric multivariate analysis of             importancia para la conservación de las aves de Santa
    changes in community structure. Australian Journal of             Cruz: estuario del río Gallegos. In: Di Giacomo AS ed,
    Ecology, 18: 117-143.                                             Áreas de importancia para la conservación de las aves
Clarke KR & Gorley RN (2001). PRIMER v5: User Manual/                 en Argentina, sitios prioritarios para la conservación de
    Tutorial. PRIMER-E, Plymouth, 91 pp.                              la biodiversidad. Temas de Naturaleza y Conservación
Clarke KR & Warwik RM (1994). Similarity-based testing                5. Aves Argentinas, Asociación Ornitológica del Plata,
    for community pattern: the 2-way layout with no                   Buenos Aires, 412– 414.
    replication. Marine Biology 118: 167-176.                     Ferrari S, Ercolano B & Albrieu C (2007). Pérdida de hábitat
Colling LA, Bemvenuti CE & Gandra MS (2007).                          por actividades antrópicas en las marismas y planicies
    Seasonal variability on the structure of sublittoral              de marea del estuario del río Gallegos (Patagonia
    macrozoobenthic association in the Patos Lagoon                   austral, Argentina). In: M Castro Lucic & L Fernández
    estuary, sothern Brazil. Iheringia, Serie Zoologia 97             Reyes, eds. Gestión Sostenible de Humedales, CYTED
    (3): 257-262.                                                     y Programa Internacional de Interculturalidad, Santiago
Dahl E (1952). Some aspects of the ecology and zonation of            de Chile, 319-327.
    the fauna on sandy beaches. Oikos 4: 1-27.                    Ferrari S, Sawicki Z, Albrieu C, Loekemeyer N, Gigli S
Das Neves LP, da Silva P de SR & Bemvenuti CE (2008).                 & Bucher EH (2008). Manejo y conservación de aves
    Temporal variability of benthic macrofauna on Cassino             playeras migratorias en Argentina: experiencias locales
    beach, southernmost Brazil. Iheringia, Serie Zoologia             en cuatro sitios de la Red Hemisférica de Reservas para
    98 (1): 36-44.                                                    Aves Playeras (RHRAP). Ornitología Neotropical 19
Day JW, Hall CAS, Kemp WM & Yañez-Arancibia A                         (Suppl.): 311-320.
    (1989). The estuarine bottom and benthic subsystem.           Ferreira WS, Bemvenuti CE & Rosa LC (2005). Effects of
    In: JW Day ed, Estuarine Ecology. Wiley & Sons,New                the shorebirds predation on the estuarine macrofauna of
    York, p. 338-376.                                                 the Patos Lagoon, South Brazil. Thalassas 21 (2): 77-82.
Dittmann S (2000). Zonation of benthic communities in a           Gianuca NM (1983). A preliminary account of the ecology
    tropical tidal flat of north-east Australia. Journal of sea       of Sandy beaches in southern Brazil. In: AT Mc
    Research 43: 33-51.                                               Lachlan, T Erasmus, eds. Sandy beaches as ecosystems.
Dittmann S (2002). Benthic fauna in tropical tidal flats              The Hague, W. Junk, 413-420.
    of Hinchinbrook Channel, NE Australia: diversity,             González PM, Carbajal M, Morrison RIG & Baker AJ
    abundance and their spatial and temporal variation.               (2004). Tendencias poblacionales del Playero Rojizo
    Wetlands Ecology and Management 10: 323-333.                      (Calidris canutus rufa) en el sur de Sudamérica.
Espoz C, Ponce A, Matus R, Blank O, Rozbaczylo N, Sitters             Ornitología Neotropical 15 (Suppl.): 357–365. The
    HP, Rodriguez S, Dey AD & Niles LJ (2008). Trophic                Neotropical Ornithological Society.

                                                                IN A TIDAL FLAT OF THE RIO GALLEGOS ESTUARY, PATAGONIA, ARGENTINA

Guerreiro JS, Freitas P, Pereira J & Macia A (1996).                       populations in intertidal sediments of the Quequén
    Sediment macrobenthos of mangrove flats at Inhaca                      Grande estuary (Argentina). Hydrobiologia 455: 61-69.
    Island, Mozanbique. Cahiers de Biologie Marine 37:                 Martin JP & Bastida R (2008). Contribución de las
    309-327.                                                               comunidades bentónicas en la dieta del róbalo
Hernández MA, D´Amico V & Bala L (2004). Presas                            (Eleginops maclovinus) en la ría Deseado (Santa
    consumidas por el Playero Rojizo (Calidris canutus) en                 Cruz, Argentina). Latin American Journal of Aquatic
    Bahía de San Julián, Santa Cruz, Argentina. Hornero                    Research 36(1): 1-13.
    19(1):7-11.                                                        Mc Lachlan A (1983). Sandy beaches ecology, a review. In
Hernández MA, Bala LO & Musmeci LR (2008). Dieta de                        Mc Lachlan, A. and Erasmus, T. eds. Sandy beaches as
    tres especies de aves playeras migratorias en Península                ecosystems. The Hague, W. Junk, 321-390.
    Valdés, Patagonia, Argentina. Ornitología Neotropical              Magurran A (1989). Diversidad ecológica y su medición.
    19 (Suppl.): 605-611.                                                  Editorial Vedrá. 200 pp.
Ieno E & Bastida R (1998). Spatial and temporal patterns               Morrison RIG, Ross RK & Niles LJ (2004). Declines in
    in coastal macro benthos of Samborombon Bay,                           wintering populations of Red Knots in southern South
    Argentina: A case study of very low diversity. Estuaries               America. Condor 106:60–70.
    21 (4): 690-699.                                                   Morrison RI, McCaffery GBJ, Gill RE, Skagen SK, Jones
Iribarne O & Martinez M (1999). Predation on the                           SL, Page GW, Gratto-Trevor CL & Andres BA (2006).
    southwestern Atlantic fiddler crab (Uca uruguayensis)                  Population estimates of North American shorebirds.
    by migrant shorebirds (Pluvialis dominica, P. squatarola,              Wader Study Group Bulletin 111: 67-85.
    Arenaria interpres and Numenius phaeopus). Estuaries               Passadore C, Giménez L & Acuña A (2007). Composition
    22: 47-54.                                                             and intra-annual variation of the macroinfauna in
Jaramillo E, Stead R, Quijón P, Contreras H & Gonzalez                     the estuarine zone of the Pando Stream (Uruguay).
    M (1996). Temporal variability of the sand beach                       Brazilian Journal of Biology 67 (2):197-202.
    macroinfauna in south central Chile. Revista Chilena               Perillo GME, Ripley MD, Piccolo MC & Dyer KR (1996).
    de Historia Natural 69: 641-653.                                       The formation of tidal creeks in a salt marsh: new
Junoy J & JM Vieitez (1990). Macrozoobenthic community                     evidence from the Loyola Bay salt marsh, Rio Gallegos,
    structure in the Ría de Foz, an intertidal estuary                     Estuary, Argentina. Mangroves and Salt Marshes 1(1):
    (Galicia, Northwest Spain). Mar. Biol. 107: 329-339.                   37-46.
Knox GA (2000). The ecology of sea shores. CRC Press,                  Peterson CH (1991). Intertidal zonation of marine
    New York, 555 pp.                                                      invertebrate in sand and mud. American Scientist 79:
Lizarralde ZI (2002). Distribución y abundancia de Tellina                 236-249.
    petitiana (Bivalvia, Tellinidae) en Cerro Avanzado,                Peterson CH & Andre SV (1980). An experimental analysis
    Chubut, Argentina. Physis (A), 60 (138-139): 7-14.                     of interespecific competition among marine filter
Lizarralde Z, S Ferrari, S Pittaluga & C Albrieu (2010).                   feeders in a soft-sediment environment. Ecology 61
    Seasonal abundance and trophic ecology of Hudsonian                    (1): 129-139.
    Godwit (Limosa haemastica) at Rio Gallegos estuary                 Piersma T, De Goeij P & Tulp I (1993). An evaluation of
    (Patagonia, Argentina). Ornitologia Neotropical 21:                    intertidal feeding habitats from a shorebird perspectiva:
    283–294                                                                towards relevant comparisons between temperate and
Lopez Gappa J & Cruz Sueiro M (2006). The subtidal                         tropical mudflats. Netherlands Journal of Sea Research
    macrobenthic assemblages of Bahia San Sebastián                        31: 503-512.
    (Tierra del Fuego, Argentina). Polar Biology 30 (6):               Souza JBR & Gianuca NM (1995). Zonation and seasonal
    679-687.                                                               variation of the intertidal macrofauna on a sandy beach
Lopez Gappa J, Tablado A, Fonalleras MC & Adami                            of Parana State, Brazil. Scientia Marina 59 (2): 103-111.
    ML (2001). Temporal and spatial patterns of annelid                Ter Braak CJF (1985). Correspondence analysis of incidence


    and abundance data: properties in terms of a unimodal
    response model. Biometrics 41: 859-873.
Thrush SF, Pridmore RD, Hewitt JE & Cummings VJ
    (1992). Adult infauna as facilitators of colonization on
    intertidal sandflats. Journal of Experimental Marine
    Biology and Ecology 159: 253-265.
Veloso VG, Caetano CHS & Cardoso RS (2003). Composition,
    structure and zonation of intertidal macroinfauna in
    relation to physical factors in microtidal sandy beaches
    in Río de Janeiro State, Brazil. Scientia Marina 67 (4):
Veloso VG, Cardoso RS & Fonseca DB (1997). Spatio-
    temporal characterization of intertidal macrofauna
    at Prainha beach (Rio de Janeiro State). Oecologia
    Brasiliensis 435: 213-225.
Vooren CM (1998). Aves marhinas e costeiras. In: Seeliger
    U, Odebrecht C, Castello JP eds. Os Ecossistemas
    costeiro e marhino do extremo sul do Brasil. Rio
    Grande, Ecoscientia: 170-176.
Whitlatch RB (1977). Seasonal changes in the community
    structure of the macrobenthos inhabiting the intertidal
    sand and mud flats of Barnstable Harbor, Massachusetts,
    Biological Bulletin 152: 275-294.
Woodin SA (1974). Polychaete abundance patterns in a
    marine soft-sediment environment: the importance of
    biological interactions. Ecological Monographs 44:
Zaixso HE, Lizarralde ZI, Pastor C, Gomes Simes E,
    Romanello E & Pagnoni E (1998). Distribución espacial
    del macrozoobentos submareal del golfo San José
    (Chubut, Argentina). Revista de Biología Marina y
    Oceanografía 33 (1): 43-72.

     (Received: October, 23, 2009; Accepted: May, 26, 2010)

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