Download distribution and temporal variation of the benthic fauna in a tidal flat

Thalassas, 27 (1): 9-20
An International Journal of Marine Sciences
DISTRIBUTION AND TEMPORAL VARIATION OF THE BENTHIC
FAUNA IN A TIDAL FLAT OF THE RIO GALLEGOS ESTUARY,
PATAGONIA, ARGENTINA
ZULMA I. LIZARRALDE & SUSANA PITTALUGA(1)
Key words: benthos; tidal flat; distribution; temporal variation; Patagonia.
ABSTRACT
The aim of this work was to analyze spatial and
temporal variations in composition and abundance
of benthic species assemblages in an intertidal
environment of the Río Gallegos Estuary, Patagonia,
Argentina (51° 35’ S 69° W). Species distribution
and its temporal fluctuations were analyzed using
multivariate statistical methods. Different species
assemblages were observed, their distribution being
related to the tidal level and type of intertidal
sediment. The polychaete Scolecolepides uncinatus
was dominant in a species assemblage restricted to
the high intertidal levels, which are characterized by
silty clay sediments. At the intermediate intertidal
level, the number of species and total macrofauna
abundance increased; at this level, the clam
Darina solenoides and the mussel Mytilus edulis
platensis were dominant. At the low levels, which
are composed of fine sediments, the polychaete
Clymenella minor and the bivalve Mysella sp. were
dominant. Temporal variations detected in species
abundance were mainly due to the incorporation
of recruits in the population, especially of the most
abundant species.
(1) Universidad Nacional de la Patagonia Austral, Lisandro de
la Torre 1070, 9400 Río Gallegos, Santa Cruz, Argentina. Fax:
054-02966 442620, e-mail: [email protected]
INTRODUCTION
Distribution, diversity, and abundance of benthic organisms inhabiting intertidal environments
have been associated with variations of several
factors, such as depth, tidal height, time of exposure, and type of sediment (Dahl, 1952; Beukema,
1976; Mc Lachlan, 1983; Day et al., 1989; Brown &
Mc Lachlan, 1990; Zaixso et al., 1998; Dittmann,
2000; Lizarralde, 2002; Veloso et al., 2003). Food
availability, larval dispersal and settlement, intra
and interspecific competition, and the effects of
predation also inf luence community structure.
Some experimental studies have demonstrated
that biological interactions, such as predation
and competition, affect the benthic community
structure by acting on recruitment, survival, or
migration of organisms (Woddin, 1974; Peterson
& Andre, 1980; Brenchley, 1982; Thrush et al.,
1992; Knox, 2000).
Benthic communities may fluctuate in a cyclic
pattern over time, because of the characteristics of
the life cycle of the species, as well as of the influence
of temporal fluctuations of abiotic factors, such as
environmental temperature or salinity (Day et al.,
1989; Souza & Gianuca, 1995; Veloso et al., 1997; Das
Neves et al., 2008).
9
ZULMA I. LIZARRALDE & SUSANA PITTALUGA
Figure 1:
Study area at the Río Gallegos Estuary, southern Patagonia, Argentina.
Soft-bottom intertidal benthic communities from
the southern portion of Argentine Patagonia have
been poorly studied. The few studies conducted in the
region have provided information on communities
from shallow subtidal environments (Lopez Gappa
& Cruz Sueiro, 2006, Martin & Bastida, 2008).
There are also reports from the Chilean portion
of the Strait of Magellan that contribute to the
knowledge of those organisms in the region and that
allow us to make comparisons at a regional scale
(Espoz et al., 2008).
The Río Gallegos estuary is located in the province
of Santa Cruz, southern Patagonia. Its northern shore
is high, with cliffs and gravel beach plains, whereas
the southern shore is dominated by vast muddy
intertidal flats, saltmarshes, and complex channels
(Perillo et al., 1996). It is a Western Hemisphere
Shorebird Reserve Network (WHSRN) Site of
international importance because it provides habitat
and food for a high number of Nearctic migratory
shorebirds that visit the area during summer, such as
the White-rumped Sandpiper (Calidris fuscicollis),
10
the Red Knot (Calidris canutus), and the Hudsonian
Godwit (Limosa haemastica). These species arrive
from the Northern Hemisphere and use the estuary
as a migration stopover site during the non-breeding
season; the estuary also provides shelter to some
species endemic to southern Patagonia, such as the
Magellanic Plover (Pluvianellus socialis) and the
Magellanic Oystercatcher (Haematopus leucopodus)
(Ferrari et al. 2002, 2007, 2008, Albrieu et al. 2004).
Small-scale artisanal fisheries are conducted at the
estuary, one of the target species being the Patagonian
blenny Eleginops maclovinus (Caille et. al., 1995),
which also feeds on benthic organisms (Martín &
Bastida, 2008).
Despite the ecological importance of the
estuary, no systematic studies of benthic organisms
inhabiting the variety of intertidal environments
have been conducted; therefore, it is necessary to
generate baseline information that contributes to the
management of the coastal area, which is permanently
influenced by anthropogenic activities (recreation,
sport and commercial fisheries, urban development)
DISTRIBUTION AND TEMPORAL VARIATION OF THE BENTHIC FAUNA
IN A TIDAL FLAT OF THE RIO GALLEGOS ESTUARY, PATAGONIA, ARGENTINA
because of its proximity to the city of Río Gallegos.
The aim of this work was to analyze the composition,
abundance, and distribution of benthic species
assemblages, as well as the temporal variations of
species abundance throughout a year of study at the
Río Gallegos Estuary.
MATERIALS AND METHODS
The Río Gallegos Estuary is located in
southeastern continental Patagonia, Argentina (51°
35’ S 69° W). The tidal regime is semi-diurnal
with a mean tidal range of 10.8 m on spring tides
and 2.9 m on neaps. The cool coastal climate has a
mean annual temperature of 7.2 °C and west winds
blowing at an average speed of 35 km/h. The city
of Río Gallegos, with a population of some 90,000
inhabitants, is located on the southern shore of the
estuary.
The benthic macrofauna was sampled monthly
during 12 months (December 2005 to November
2006) in an extensive tidal flat located on the
southern shore of the estuary (Fig. 1). Samples were
collected with a corer (15 cm diameter, 20 cm deep)
at five tidal levels along a transect perpendicular to
the waterline. Six biological samples were monthly
collected per level (levels 1 to 5). Level 1 was
located on the uppermost intertidal flat region and
Level 5 on the lowest one. Samples were sieved
with a 0.5 mm mesh and frozen. In the laboratory,
organisms were identified to the smallest possible
taxonomic level under a stereoscopic microscope
and quantified.
Sediment samples were taken in December 2005
from each of the five levels. Sediment grain size
was analyzed through sieving and expressed as
proportions. On the same date another sampling was
conducted to determine total organic matter content
(combustion at 550 °C for 5 h).
To analyze distribution and temporal variation of
the benthic macrofauna a nonmetric multidimensional
scaling ordination technique (MDS) was applied
employing the Bray-Curtis similarity index (calculated
on square-root transformed species abundance).
The analysis was performed using PRIMER v5
(Clarke & Warwick, 1994; Clarke & Gorley, 2001).
A similarity analysis (ANOSIM; α = 0.05) was
performed to evaluate differences between sample
levels and between seasons. Similarity percentage
analysis (SIMPER) was used to explore the species
contribution to similarity between the groups formed
(Clarke, 1993).
To analyze temporal variation of the benthic
macrofauna, monthly mean of species abundance
was calculated with the aim of removing the effect of
inter-level variability.
%
100
%
80
3
60
40
2
20
1
0
Level 1 Level 2 Level 3 Level 4 Level 5
Gravel
Mud
Coarse sand
Medium sand
Fine sand
Very fine sand
Figure 2:
Grain size composition of sediment.
0
Level 1
Level 2
Level 3
Level 4
Level 5
Figure 3:
Total organic matter content in sediments.
11
ZULMA I. LIZARRALDE & SUSANA PITTALUGA
To investigate the vertical distribution patterns
from high to low levels, the data from December
2005 were subjected to a Canonical Correspondence
Analysis (CCA) (Ter Braak, 1985), which included
tidal level (levels 1 to 5), sediment (gravel, coarse,
medium, fine, very fine sand; and mud) and total
organic matter content as environmental variables.
Forward selection of environmental and biotic
variables and Monte Carlo permutations were used to
identify a subset of the measured variables that exert
significant and independent influence on the benthic
macrofauna distribution.
Number of species (S), total macrobenthos
abundance (A), and Shannon-Wiener diversity
index (H’) were also determined for each tidal level
(Magurran 1989).
Small individuals of Darina solenoides (≤ 5 mm)
and M.e. platensis (≤ 5 mm) were considered recruits
and were counted under a micrometric eyeglass.
RESULTS
Environmental variables
The sediment type of levels 1 and 2 consisted mainly
of mud (more than 50%) and very fine sand (30%).
Sediment of Level 3 was classified as fine sand (41%),
very fine sand (22%), and mud (16%); Level 4 consisted
mainly of fine sand (33%) and gravel (31%); and Level 5
was composed of very fine sand (35%) and mud (26%)
(Fig. 2). Total organic matter content decreased from
Level 1 (2.5%) to Level 5 (1.1%) (Fig. 3).
Benthic macrofauna
A total of 24 taxa were collected (Table 1).
Polychaeta was the most diverse taxa, followed by
Mollusca and Crustacea. Based on mean abundance of
each species in the pooled samples collected, Darina
solenoides and Mytilus edulis platensis contributed
with 59% of the total number of individuals. Species
richness and diversity index values are shown in Table
12
Stress: 0,03
Stress 0.03
1
2
3
4
5
Figure 4:
MDS showing general distribution of samples in the tidal flat.
1: Level 1, 2: Level 2, 3: Level 3; 4: Level 4; 5: Level 5.
1. Levels 3 and 4 exhibited the highest number of taxa
and diversity index.
Spatial distribution
Results of MDS analysis showed a clear pattern
of macrofauna distribution (Fig. 4). Samples were
separated into three groups, indicating differences
in abundance and composition among faunal
assemblages. ANOSIM revealed significant
differences among groups (Table 2). One group
comprised levels 1 and 2, with dominance of the
polychaete Scolecolepides uncinatus; the second
group was composed of samples obtained from levels
3 and 4, characterized by Darina solenoids and
Mytilus edulis platensis; and the third group included
samples from Level 5, characterized by Climenella
mirror and Mysella sp. (Table 3).
According to results of CCA between benthos
species and environmental variables, the most
important variable was tidal level, followed by fine
sand and mud (Fig. 5). The variables coarse, medium,
and very fine sand, and organic matter were not
selected by the CCA. Axes 1 and 2 explained 85% of
the variance of the species-environment relationship
(Table 4). The ordination showed that tidal level, fine
sand, and mud were related to axis 1 and that gravel
was related to axis 2 (Table 5).
DISTRIBUTION AND TEMPORAL VARIATION OF THE BENTHIC FAUNA
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 sculpta were related to high tidal levels and muddy
sediments. Darina solenoides, Kimbergonuphis
dorsalis, Lumbrinereis cingulata, Glycinde armata, Aglaophamus praetiosus, Notocirrus lorum,
Hemipodus patagonicus and Monoculopsis vallentini assemblage was associated with intermediate
levels and fine sand; Clymenella minor and Mysella
sp., were associated with fine sand and lower levels,
and Mytilus edulis platensis-Edotia tuberculata,
with intermediate tidal levels and gravel sediments
(Fig. 5).
Temporal variation
Darina solenoides and M. e. platensis were the
most abundant species throughout the study period
(Fig. 6). Darina solenoides presented highest
abundance values in fall (April-May), with 35%
of recruits in april, and at the end of spring
(November) with 25%; recruitment of Mytilus
edulis platensis was most intense in summer (41%
in January) (Fig.7). Abundance of polychaete and
crustaceans together remained stable throughout
the year evaluated (Fig. 6).
The MDS analysis of temporal variation indicated
a tendency to the formation of two groups: one group
included samples obtained in spring (September to
November) and summer (December to February)
months; the other group was composed of samples
from fall (March to May) and winter (June to August)
(Fig. 8). ANOSIM tests showed significant differences
between groups (Table 6). The SIMPER analysis
showed that Darina solenoides and M.e.platensis
were the organisms that mostly contributed to
formation of the fall-winter and summer-spring
groups, respectively (Table 7).
13
ZULMA I. LIZARRALDE & SUSANA PITTALUGA
number/m2
2000
45
40
35
30
25
20
15
10
5
0
1500
1000
500
0
D
D
J
F
M
A
M
D. solenoides
Polychaeta
J
J
A
S
O
N
F
M
A
M
D. solenoides
J
J
A
S
O
N
M.e. platensis
M.e. platensis
Crustacea
Figure 6: monthly number of dominant species or group of species.
DISCUSSION
The present study is the first description of benthic
organism assemblages inhabiting the intertidal flat in
an area located on the southern shore of the estuary,
near the city of Río Gallegos. The sediment is
characterized by the presence of high percentages of
silt and clay at the high levels of the intertidal, and
of sand at the intermediate and low levels. Organic
matter content in sediments also differed among
tidal levels, the highest values being recorded at high
levels.
The benthic community was characterized
by low species richness but great abundance of
individuals, mainly the bivalve Darina solenoides
and M. e. platensis. This feature has been mentioned
for different estuarine areas of the South Atlantic,
especially in comparison with the adjacent marine
ecosystems (Ieno & Bastida, 1998; Lopez Gappa
et.al., 2001; Passadore et. al., 2007).
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;
Armonies & Hellwig-Armonies, 1987). This pattern
has been observed in our study, since distribution of
14
J
Figure 7:
Recruits (%) from Darina solenoides and Mytilus edulis platensis.
species in the different habitats remained constant
throughout the study period (12 months). The high
tidal flat (levels 1 and 2) characterized by silty
clay sediments, was dominated by the polychaete
Scolecolepides uncinatus; two other polychaete
species were also present but in low numbers. At
the intermediate levels (3 and 4), the number of
species and total fauna abundance increased. A
group of species associated with sandy sediments,
dominated by the clam Darina solenoides and the
polychaete Kinbergonuphis dorsalis inhabits these
levels. The mussel M.e.platensis was also recorded
at levels 3 and 4, but in sediments with intermediate
Stress: 0.03
1
2
3
4
Figure 8:
MDS showing general ordination of samples.
1: summer months; 2: autumn months,
3: winter months, 4: spring months.
DISTRIBUTION AND TEMPORAL VARIATION OF THE BENTHIC FAUNA
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
Av (SD)
Bivalvia
Darina solenoides
Mytilus edulis platensis
Mysella sp.
Perumytilus purpuratus
Aulacomya atra
Gastropoda
Trophon geversianus
Natica falklandica
Polychaeta
Scolecolepides uncinatus
Eteone sculpta
Hemipodus patagonicus
Aglaophamus praetiosus
Kinbergonuphis dorsalis
Glycinde armata
Lumbrinereis cingulata
Notocirrus lorum
Clymenella minor
Travisia sp.
Nemertea
Nemertea indet.
Crustacea
Anfípodo indet.
Monoculopsis vallentini
Peltarion spinosulum
Halicarcinus planatus
Edotia tuberculata
Priapulid
Priapulus sp.
Number of species S
Shannon-Wiener diversity index H’
LEVEL 2
Av (SD)
---------------------
6.3 (2.7)
-----------------
---------
---------
247.8 (87.1) 190.1 (59.6)
22.8 (5.3) 57.0 (25.2)
----36 (11.0)
------------33.9 (26.7)
--------------------------------------------36.0 (17.0)
--------------------3
0.60
proportions of gravel, because the species requires
coarse sedimentary substrates to settle. The great
abundance of juveniles of both the clam and the
mussel that recruited at the intermediate level also
indicates that this region provides good conditions
as nursery grounds for these species. By contrast,
the low levels seem to favour mainly the polychaete
Clymenella minor and a bivalve, Mysella sp., both
of which are dominant in very fine sands with
intermediate proportions of mud.
In general terms, intertidal zoobenthic
assemblages at the Río Gallegos estuary are notably
similar in composition to those described by Espoz
-----
LEVEL 3
Av (SD)
LEVEL 4
Av (SD)
LEVEL 5
Av (SD)
1832.1 (548.2)
217.6 (197.3)
46.6 (9.9)
---------
1039.5 (216.6)
1834.8 (528.1)
32.1 (12.4)
27.0 (16.0)
18.0 (11.5)
58.5 (67)
9.8 (17)
144.2 (63.6)
---------
----11.3 (6.9)
25.5 (8.7)
22.3 (13.5)
10.0 (8.4)
18.0 (19.7)
129.6 (41.8)
120.9 (22.9)
571.9 (129.2)
161.8 (42.6)
164.0 (33.9)
151.5 (21.5)
---------
--------37.0 (10.5)
----306.0 (155.0)
76.6 (13.8)
-----------------
12.4 (5.2)
------------------------121.0 (19.8)
--------58.7 (18.3)
219.0 (70.4)
16.0 (3.2)
-----
----9.6 (4.0)
-------------
----41.2 (11.4)
-------------
7.4 (5.7)
6
1.0
20.9 (8.1)
14
1.7
12 (3)
----24.8 (13.2)
--------44.7 (20.0)
----13
1.8
6(2.1)
----30.4 (18.9)
2.4 9.6)
----------------11
1.4
Table 2:
Analysis of similarity (ANOSIM) between levels (all months).
Global R: 0.875, P= 0.1%.
Groups
Level 1 vs 2
Level 1 vs 3
Level 1 vs 4
Level 1 vs 5
Level 2 vs 3
Level 2 vs 4
Level 2 vs 5
Level 3 vs 4
Level 3 vs 5
Level 4 vs 5
R
0.297
1.0
1.0
1.0
1.0
1.0
1.0
0.815
0.999
0.995
P
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
0.1
15
ZULMA I. LIZARRALDE & SUSANA PITTALUGA
Table 3:
Results of SIMPER analysis. Main species that contributed (%) to the differences observed among groups.
Groups
Level 1-2
Scolecolepides uncinatus
Kinbergonuphis dorsalis
Clymenella minor
Darina solenoides
Mytilus edulis platensis
Mysella sp.
Level 3-4
Level 5
24.46
20.71
34.62
94.20
33.46
20.10
31.50
Table 4:
Summary of CCA ordination.
Axis
Eigenvalues
species-environment correlations
Cumulative percentage variance
Species data
Species-environment relationship
Sum of all unscontrained Eigenvalues
Sum of all canonical Eigenvalues
et al. (2008) for Bahía Loma in the Chilean portion
of the Strait of Magellan. These authors described
a community dominated by Darina solenoides,
polychaete and crustaceans; however, we did not
record the polychaete Aricidea sp., which has been
mentioned as the most abundant polychaete species.
On the other hand, no similarities were observed
between the species assemblage found in the estuary
and that described by Lopez Gappa & Cruz Suiero
(2006) for a coastal area of the South Atlantic in
Tierra del Fuego (Bahía San Sebastián).
Table 5:
CCA. Weighted correlation matrix of environmental variables with the
species axis.
Name
Tidal Level
Fine sand
Mud
Gravel
16
Axis 1
0.85
-0.78
0.72
-0.02
Axis 2
0.39
-0.15
- 0.01
0.50
1
0.90
0.86
2
0.27
0.80
3
0.134
0.67
25.8
45.9
26.2
85.0
24.9
92.5
Total
1.54
1.54
1.37
During our study we did not observe temporal
variability of species composition. Temporal
fluctuations recorded were related to changes in
species abundance, which were strongly influenced
by the incorporation of recruits to the populations.
Settlement of the clam D. solenoides presented two
peaks: one at the start of fall and the other in
late spring-early summer. The mussel M.e.platensis,
Table 6:
Analysis of similarity (ANOSIM) between seasons.
Global R: 0.852, P= 0.1%.
Groups
R
P
Summer vs Fall
1.0
0.1
Summer vs Winter
1.0
0.1
Summer vs Spring
0.793
0.1
Fall vs Winter
0.385
0.1
Fall vs Spring
1.0
0.1
Winter vs Spring
1.0
0.1
DISTRIBUTION AND TEMPORAL VARIATION OF THE BENTHIC FAUNA
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.
Darina solenoides
Mytilus edulis platensis
Kinbergonuphis dorsalis
Summer-Spring
35.0
54.3
7.2
Fall-Winter
57.8
27.1
9.4
however, exhibited the highest proportion of recruits
in summer. Several authors have mentioned that
recruitment of benthic species affects abundance of
macrofaunal communities (Colling et al., 2007; Das
Neves et al., 2008). But other factors may also be
responsible for changes in the number of individuals,
such as predation pressure exerted by crustacean, fish,
and bird species throughout the year or when these
species are present in coastal environments during
migration (Gianuca 1983; Jaramillo et. al., 1996;
Iribarne & Martinez, 1999; Ferreira et al., 2005).
The arrival of flocks of some bird species on their
migration flight agrees with the peak of macrofauna
abundance in southern Brazil (Vooren, 1998).
be developed, since salinity, which has not been
considered in the present work, has been mentioned
as a determining factor in the species distribution of
estuarine environments (Dittmann, 2000). Thus, a
more detailed record of the number of benthic species
present at the estuary could be obtained and the species
contribution to energy flow and especially to the diet
of birds and fishes could be elucidated. Moreover, longterm studies will help us understand whether changes
detected in benthic communities are naturally induced
or are a consequence of urban development and plan
management strategies for the area accordingly.
The Río Gallegos estuary has been mentioned
as an important wetland for the Red knot Calidris
canutus and the Hudsonian Godwit Limosa
haemastica (Ferrari et al., 2002, 2007; Albrieu et
al., 2004). These species are of conservation concern
because of the reduction observed in their populations
at the global scale (Baker et al., 2004; González
et al., 2004; Morrison et al., 2004, 2006); they use
the estuary as feeding and roosting sites during
their transcontinental migrations. Darina solenoides
has been mentioned as the main prey item in the
diet of the Hudsonian godwit and the Red knot in
several intertidal sectors in southern Patagonia, both
in Argentina and Chile. The mussel and several
polychaete species are also secondary prey for those
bird species (Espoz et. al., 2008; Hernández et. al.,
2004, 2008; Lizarralde et. al., 2010).
This work was totally supported by the
Universidad Nacional de la Patagonia Austral (Project
PI 29 A-180).
A monitoring program to study different sites
of the estuary along a salinity gradient needs to
ACKNOWLEDGMENTS
REFERENCES
Albrieu C, Imberti S & Ferrari S (2004). Las Aves de la
Patagonia Sur, el Estuario del Río Gallegos y zonas
aledañas. Ed. Universidad Nacional de la Patagonia
Austral, Río Gallegos, 204 pp.
Armonies W & Hellwig-Armonies M (1987). Synoptic
patterns of meiofaunal abundances and specific
composition in littoral sediments. Helgoländer
Meeresunters 41: 83-111.
Baker A, González P, Piersma T, Niles LJ, do Nascimento
I, Atkinson PW, Clark NA, Minton CDT, Peck MK &
Aarts G (2004). Rapid population decline in red knots:
fitness consequences of decreased refuelling rates and
late arrival in Delaware Bay. Proceeding of the Royal
Society of London B 271: 875–882.
17
ZULMA I. LIZARRALDE & SUSANA PITTALUGA
Beukema JJ (1976). Biomass and species richness of the
macrobenthic animals living on the tidal flats of
the Dutch Wadden Sea. Netherlands Journal of Sea
Research 10, 236-261.
Brenchley GA (1982). Mechanisms of spatial competition
in marine soft-bottom communities. Journal of
Experimental Marine Biology and Ecology 60: 17-33.
Brown AC & MC Lachlan A (1990). Ecology of sandy
shores. Elsevier, Amsterdam, 326 pp.
Caille G, Ferrari S & Albrieu C (1995). Los peces de la
Ría de Gallegos, Santa Cruz, Argentina. Naturalia
Patagónica, Serie Ciencias Biológicas 3: 191–194.
Clarke KR (1993). Non-parametric multivariate analysis of
changes in community structure. Australian Journal of
Ecology, 18: 117-143.
Clarke KR & Gorley RN (2001). PRIMER v5: User Manual/
Tutorial. PRIMER-E, Plymouth, 91 pp.
Clarke KR & Warwik RM (1994). Similarity-based testing
for community pattern: the 2-way layout with no
replication. Marine Biology 118: 167-176.
Colling LA, Bemvenuti CE & Gandra MS (2007).
Seasonal variability on the structure of sublittoral
macrozoobenthic association in the Patos Lagoon
estuary, sothern Brazil. Iheringia, Serie Zoologia 97
(3): 257-262.
Dahl E (1952). Some aspects of the ecology and zonation of
the fauna on sandy beaches. Oikos 4: 1-27.
Das Neves LP, da Silva P de SR & Bemvenuti CE (2008).
Temporal variability of benthic macrofauna on Cassino
beach, southernmost Brazil. Iheringia, Serie Zoologia
98 (1): 36-44.
Day JW, Hall CAS, Kemp WM & Yañez-Arancibia A
(1989). The estuarine bottom and benthic subsystem.
In: JW Day ed, Estuarine Ecology. Wiley & Sons,New
York, p. 338-376.
Dittmann S (2000). Zonation of benthic communities in a
tropical tidal flat of north-east Australia. Journal of sea
Research 43: 33-51.
Dittmann S (2002). Benthic fauna in tropical tidal flats
of Hinchinbrook Channel, NE Australia: diversity,
abundance and their spatial and temporal variation.
Wetlands Ecology and Management 10: 323-333.
Espoz C, Ponce A, Matus R, Blank O, Rozbaczylo N, Sitters
HP, Rodriguez S, Dey AD & Niles LJ (2008). Trophic
18
ecology of the Red Not Calidris canutus rufa at Bahia
Lomas, Tierra del Fuego, Chile. Wader study group
Bulletin 115 (2): 69-79.
Ferrari SN (2001). Identificación de áreas óptimas para la
conservación de aves playeras en el estuario del río
Gallegos, Santa Cruz, Argentina. Tesis de Maestría.
Universidad Nacional de Córdoba.
Ferrari S, Albrieu C & Gandini P (2002). Importance of
the Rio Gallegos estuary, Santa Cruz, Argentina, for
migratory shorebirds. Wader Study Group Bulletin 99:
35–40.
Ferrari S, Albrieu C & Imberti S (2005). Áreas de
importancia para la conservación de las aves de Santa
Cruz: estuario del río Gallegos. In: Di Giacomo AS ed,
Áreas de importancia para la conservación de las aves
en Argentina, sitios prioritarios para la conservación de
la biodiversidad. Temas de Naturaleza y Conservación
5. Aves Argentinas, Asociación Ornitológica del Plata,
Buenos Aires, 412– 414.
Ferrari S, Ercolano B & Albrieu C (2007). Pérdida de hábitat
por actividades antrópicas en las marismas y planicies
de marea del estuario del río Gallegos (Patagonia
austral, Argentina). In: M Castro Lucic & L Fernández
Reyes, eds. Gestión Sostenible de Humedales, CYTED
y Programa Internacional de Interculturalidad, Santiago
de Chile, 319-327.
Ferrari S, Sawicki Z, Albrieu C, Loekemeyer N, Gigli S
& Bucher EH (2008). Manejo y conservación de aves
playeras migratorias en Argentina: experiencias locales
en cuatro sitios de la Red Hemisférica de Reservas para
Aves Playeras (RHRAP). Ornitología Neotropical 19
(Suppl.): 311-320.
Ferreira WS, Bemvenuti CE & Rosa LC (2005). Effects of
the shorebirds predation on the estuarine macrofauna of
the Patos Lagoon, South Brazil. Thalassas 21 (2): 77-82.
Gianuca NM (1983). A preliminary account of the ecology
of Sandy beaches in southern Brazil. In: AT Mc
Lachlan, T Erasmus, eds. Sandy beaches as ecosystems.
The Hague, W. Junk, 413-420.
González PM, Carbajal M, Morrison RIG & Baker AJ
(2004). Tendencias poblacionales del Playero Rojizo
(Calidris canutus rufa) en el sur de Sudamérica.
Ornitología Neotropical 15 (Suppl.): 357–365. The
Neotropical Ornithological Society.
DISTRIBUTION AND TEMPORAL VARIATION OF THE BENTHIC FAUNA
IN A TIDAL FLAT OF THE RIO GALLEGOS ESTUARY, PATAGONIA, ARGENTINA
Guerreiro JS, Freitas P, Pereira J & Macia A (1996).
Sediment macrobenthos of mangrove flats at Inhaca
Island, Mozanbique. Cahiers de Biologie Marine 37:
309-327.
Hernández MA, D´Amico V & Bala L (2004). Presas
consumidas por el Playero Rojizo (Calidris canutus) en
Bahía de San Julián, Santa Cruz, Argentina. Hornero
19(1):7-11.
Hernández MA, Bala LO & Musmeci LR (2008). Dieta de
tres especies de aves playeras migratorias en Península
Valdés, Patagonia, Argentina. Ornitología Neotropical
19 (Suppl.): 605-611.
Ieno E & Bastida R (1998). Spatial and temporal patterns
in coastal macro benthos of Samborombon Bay,
Argentina: A case study of very low diversity. Estuaries
21 (4): 690-699.
Iribarne O & Martinez M (1999). Predation on the
southwestern Atlantic fiddler crab (Uca uruguayensis)
by migrant shorebirds (Pluvialis dominica, P. squatarola,
Arenaria interpres and Numenius phaeopus). Estuaries
22: 47-54.
Jaramillo E, Stead R, Quijón P, Contreras H & Gonzalez
M (1996). Temporal variability of the sand beach
macroinfauna in south central Chile. Revista Chilena
de Historia Natural 69: 641-653.
Junoy J & JM Vieitez (1990). Macrozoobenthic community
structure in the Ría de Foz, an intertidal estuary
(Galicia, Northwest Spain). Mar. Biol. 107: 329-339.
Knox GA (2000). The ecology of sea shores. CRC Press,
New York, 555 pp.
Lizarralde ZI (2002). Distribución y abundancia de Tellina
petitiana (Bivalvia, Tellinidae) en Cerro Avanzado,
Chubut, Argentina. Physis (A), 60 (138-139): 7-14.
Lizarralde Z, S Ferrari, S Pittaluga & C Albrieu (2010).
Seasonal abundance and trophic ecology of Hudsonian
Godwit (Limosa haemastica) at Rio Gallegos estuary
(Patagonia, Argentina). Ornitologia Neotropical 21:
283–294
Lopez Gappa J & Cruz Sueiro M (2006). The subtidal
macrobenthic assemblages of Bahia San Sebastián
(Tierra del Fuego, Argentina). Polar Biology 30 (6):
679-687.
Lopez Gappa J, Tablado A, Fonalleras MC & Adami
ML (2001). Temporal and spatial patterns of annelid
populations in intertidal sediments of the Quequén
Grande estuary (Argentina). Hydrobiologia 455: 61-69.
Martin JP & Bastida R (2008). Contribución de las
comunidades bentónicas en la dieta del róbalo
(Eleginops maclovinus) en la ría Deseado (Santa
Cruz, Argentina). Latin American Journal of Aquatic
Research 36(1): 1-13.
Mc Lachlan A (1983). Sandy beaches ecology, a review. In
Mc Lachlan, A. and Erasmus, T. eds. Sandy beaches as
ecosystems. The Hague, W. Junk, 321-390.
Magurran A (1989). Diversidad ecológica y su medición.
Editorial Vedrá. 200 pp.
Morrison RIG, Ross RK & Niles LJ (2004). Declines in
wintering populations of Red Knots in southern South
America. Condor 106:60–70.
Morrison RI, McCaffery GBJ, Gill RE, Skagen SK, Jones
SL, Page GW, Gratto-Trevor CL & Andres BA (2006).
Population estimates of North American shorebirds.
Wader Study Group Bulletin 111: 67-85.
Passadore C, Giménez L & Acuña A (2007). Composition
and intra-annual variation of the macroinfauna in
the estuarine zone of the Pando Stream (Uruguay).
Brazilian Journal of Biology 67 (2):197-202.
Perillo GME, Ripley MD, Piccolo MC & Dyer KR (1996).
The formation of tidal creeks in a salt marsh: new
evidence from the Loyola Bay salt marsh, Rio Gallegos,
Estuary, Argentina. Mangroves and Salt Marshes 1(1):
37-46.
Peterson CH (1991). Intertidal zonation of marine
invertebrate in sand and mud. American Scientist 79:
236-249.
Peterson CH & Andre SV (1980). An experimental analysis
of interespecific competition among marine filter
feeders in a soft-sediment environment. Ecology 61
(1): 129-139.
Piersma T, De Goeij P & Tulp I (1993). An evaluation of
intertidal feeding habitats from a shorebird perspectiva:
towards relevant comparisons between temperate and
tropical mudflats. Netherlands Journal of Sea Research
31: 503-512.
Souza JBR & Gianuca NM (1995). Zonation and seasonal
variation of the intertidal macrofauna on a sandy beach
of Parana State, Brazil. Scientia Marina 59 (2): 103-111.
Ter Braak CJF (1985). Correspondence analysis of incidence
19
ZULMA I. LIZARRALDE & SUSANA PITTALUGA
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):
393-402.
Veloso VG, Cardoso RS & Fonseca DB (1997). Spatiotemporal 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:
171-187.
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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