DISTRIBUTION AND TEMPORAL VARIATION OF THE BENTHIC FAUNA IN A TIDAL FLAT OF THE RIO GALLEGOS ESTUARY, PATAGONIA, ARGENTINA
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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 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).
9ZULMA I. LIZARRALDE & SUSANA PITTALUGA
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)
10DISTRIBUTION 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. 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.
%
100
%
80 3
60
40 2
20
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.
11ZULMA I. LIZARRALDE & SUSANA PITTALUGA
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).
12DISTRIBUTION 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 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).
13ZULMA I. LIZARRALDE & SUSANA PITTALUGA
2000 45
40
1500 35
number/m2
30
25
1000 20
15
10
500
5
0
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
1
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
4
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.
14DISTRIBUTION 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 LEVEL 2 LEVEL 3 LEVEL 4 LEVEL 5
Av (SD) Av (SD) Av (SD) Av (SD) Av (SD)
Bivalvia
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) -----
Gastropoda
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
Nemertea indet. ----- ----- ----- 12 (3) 6(2.1)
Crustacea
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
15ZULMA I. LIZARRALDE & SUSANA PITTALUGA
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
16DISTRIBUTION 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.
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
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(Received: October, 23, 2009; Accepted: May, 26, 2010)
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