BRAZILIAN JOURNAL OF OCEANOGRAPHY, 64(3):239-248;2016
Bertrán et al.: Variation in Budi Lagoon macrobenthos
239
Macrobenthos of the coastal Budi Lagoon, southern Chile: Changes
associated with seasonal environmental variation
The purpose of the present study was to investigate
the seasonal relationship of macrobenthos richness
and abundance with sediment characteristics
(i.e. texture and organic material) for the coastal
Budi Lagoon in southern Chile. Physicochemical
measurements and macrobenthos samples were
taken over the course of a year at nine sampling
stations. Sandy-muddy sediment was the most
common, and high percentages of organic material
seasons and stations. The recorded organic material
was related to natural (resident wild birds) and
anthropogenic (agriculture) sources. Regarding
fauna, 28 benthonic taxa and 7092 individuals were
most abundant taxa year-round were the molluscs
Littoridina cumingii and Kingiella chilenica and
the bristle worm Prionospio patagonica. Together,
the obtained results evidence the important impact
of organic material on the macrobenthos, with
macrobenthic richness and abundance decreasing
in conditions of high organic material content. The
a response to the land use around the Budi Lagoon,
which is intensely subjected to agricultural and
tourist activities.
AbstrAct
Carlos Bertrán
1
, Pablo Fierro
1
, Elizabeth Encalada
1
, Fernando Peña-Cortés
2
, Jaime Tapia
3
,
Enrique Hauenstein
4
, Luis Vargas-Chaco
1,5
*
1
Institute of Marine Science and Limnology, Universidad Austral de Chile, Chile.
2
Territorial Planning Laboratory, Universidad Católica de Temuco, Chile
3
Institute of Chemistry and Natural Resources, Universidad de Talca, Chile
4
Faculty of Sciences, Universidad Católica de Temuco, Temuco, Chile.
5
Centro Fondap de Investigación de Altas Latitudes (IDEAL), Universidad Austral de Chile, Valdivia, Chile.
*Corresponding author: luis.vargas@uach.cl
Financial Support: This study was possible due to the support of FONDECYT projects 1110798 and 1151375.
Descriptors: Macrobenthos, Budi Lagoon, Araucania,
Sediments, Spatial variability.
O objetivo do presente estudo foi investigar
a relação sazonal entre macrobentos e
características do sedimento, tais como textura
e material orgânico, na lagoa costeira Budi
Lagoon, sul do Chile. Medidas físico-químicas
e amostragem do macrobentos foram realizadas
durante um ano em nove localidades. Sedimento
arenoso-lodoso foi o mais comum na lagoa,
e percentagens elevadas de material orgânico
foram registradas, variando significativamente
entre as estações e locais de coleta. Em relação
a fauna, foram identificados 28 taxas bentônicos
e 7092 indivíduos, que apresentaram variação
temporal e espacial. As espécies mais abundantes
durante todo o ano foram os moluscos Littoridina
cumingii e Kingiella chilenica, e o poliqueta
Prionospio patagonica. Os resultados obtidos
evidenciaram o importante impacto da matéria
orgânica sobre o macrobentos, com riqueza e
abundância da fauna diminuindo em presença de
alto teor de matéria. As variações encontradas
para os diferentes taxons indicaram resposta da
fauna ao uso da terra ao redor de Budi Lagoon,
que intensamente utilizada para agricultura e
atividades turísticas.
resumo
Descritores: Macrobentos, Budi Lagoon, Araucanía,
Sedimentos, Variabilidade espacial.
http://dx.doi.org/10.1590/S1679-87592016113306403
BJOCE
BRAZILIAN JOURNAL OF OCEANOGRAPHY, 64(3):239-248;2016
Bertrán et al.: Variation in Budi Lagoon macrobenthos
240
INTRODUCTION
Most animal populations show considerable spatial
(UNDERWOOD; CHAPMAN, 1996; BENEDETTI-
CECCHI et al., 2001; BERTRÁN et al., 2001; FIERRO
et al., 2014; FIERRO et al., 2015). In the case of
benthic macrofauna, distribution and abundance are
mainly related to certain variables of the sediment-
and organic enrichment are exerted (GLÉMAREC,
1986). The principal physicochemical variables that
determine macrobenthic distribution are temperature,
salinity, suspended solids, nitrates (HOLLAND et al.,
1987; BEUKEMA, 1990; FIERRO et al., 2015), and
sediment characteristics, such as texture and organic
material content (RITCHER, 1985; NICHOLS et al.,
sediments (HYNES, 1970) over the course of the year
(BERTRÁN, 1989; BERTRÁN et al., 2001; FIERRO et
al., 2012), generating varied distribution and abundance
patterns (JARAMILLO et al., 2001).
The distribution of the macrobenthos has possible
application in estimating the spatial and temporal
lakes and estuaries. Lagoons are a non-continental,
seawater (KJERFVE, 1994; PÉREZ-RUZAFA et al.,
2011). The entrance of high-salinity water into lagoons
JARAMILLO et al., 2008). Additionally, lagoons and
estuaries both present high environmental variability,
leading some authors to consider both as a single
ecosystem unit (STUARDO; VALDOVINOS, 1989;
BERTRÁN et al., 2010).
One such ecosystem unit is the Budi Lagoon,
where the periodic entrance of seawater largely and
seasonally modifies water parameters (BERTRÁN et
al., 2010). Furthermore, the permanent presence of
aquatic birds and anthropic activity in the watershed,
particularly near the shoreline, means that this lagoon
is constantly incorporating organic material (PEÑA-
CORTÉS et al., 2006a; 2006b, 2011). The objective
of this study was to explore the relationship between
seasonal variations in benthic macrofauna communities
and fluctuations in water characteristics of the coastal
Budi Lagoon, including sediment texture and organic
material content.
MATERIAL AND METHODS
The Budi Lagoon (38º49’30” S, 73º23’30” W) begins
about one mile south of the Imperial River estuary in
southern Chile. The Budi Lagoon sporadically connects
autumn until the beginning of spring. This lagoon has a
surface area of 57.4 km
2
, and its basin has a dry coastal
landscape that is highly fragmented by anthropogenic
activities, with native oak-laurel-lingue and temo-pitra
forests (BERTRÁN et al., 2006; 2010).
Sampling was performed in 2005 during each
of the four seasons at nine sampling stations: Budi
River (E1), Temo (E2), Deume 1 (E3), Deume 2
(E4), Deume 3 (E5), Comue (E6), Bolleco (E7),
Allipen (E8), and Botapulli (E9) (Figure 1). At each
station, water was sampled using a Ruhtner bottle,
and the temperature and salinity of the bottom layer
was measured. Sediment samples (5 replicates per
station) were also collected using an Emery Dredge
(0.25 m
2
) to sample the macrobenthos, characterize
sediment texture (FOLK, 1980), and determine
organic material (BYERS et al., 1978). Macrobenthos
samples were sieved through a 0.5 mm mesh, fixed in
10% formalin, transported to the Bentos Laboratory
of the Universidad Austral de Chile, and preserved
in 70% ethanol. In the laboratory, samples were
examined under a stereoscopic microscope, and taxa
were identified to the lowest possible taxonomic level
using specialized literature.
Figure 1. Location of the Budi Lagoon and sampling stations (black
circle). Arrow indicates connection between the lagoon and sea.
BRAZILIAN JOURNAL OF OCEANOGRAPHY, 64(3):239-248;2016
Bertrán et al.: Variation in Budi Lagoon macrobenthos
241
The community structure of the Budi Lagoon
macrobenthos was described for each site and season based
on the following indexes: Number of taxa, Abundance, and
Shannon-Wiener diversity (H’), following BROWER et
al. (1990). Community structure and organic material were
analysed using non-metric multidimensional scaling analysis
as the ordination method, and similitude between sampling
stations was based on a similarity matrix constructed using the
Bray-Curtis similarity index. This analysis was performed in
PRIMER v.6 (Plymouth Routines in Multivariate Ecological
Research) (CLARKE et al., 2005).
normality, independence, and homoscedasticity, a two-way
ANOVA was performed. In all cases, the two factors were
space (sampling stations) and time (season). Sediment
were non-parametric, this variable was assessed using the
p<0.05) were
further analysed using the Tukey’s HSD a posteriori test.
RESULTS
The water temperature of the lagoon bottom varied
from 10 ºC (autumn and winter) to 15 °C (spring) and 21
ºC (summer), following a seasonal cycle with maximum
temperatures in the summer and minimums in the winter.
The lowest values of salinity were measured in winter-
spring (1.7%), and the highest values were in the summer
(2.66%) and autumn (4.2%).
Sandy-muddy sediment was the most common in the
lagoon. The highest percentage of sand was registered
in station E8 (97% in winter and autumn), while mud
was the most abundant at station E2 (87% in spring).
Gravel sediment was the least common, with the highest
percentages registered at stations E5 (18.3% in autumn)
and E7 (16.9% in winter) (Table 1).
between seasons (p<0.05). The highest seasonal mean
was 23.5% (station E8 in spring), and the lowest seasonal
means were 1.2% and 1.34% (stations E7 and E8 in
winter, respectively). Considering all stations together, the
highest mean organic content occurred in spring (13.2%;
Table 1).
To examine the patterns in organic material, non-
metric multidimensional scaling and cluster analyses were
performed (Figure 2). During the summer, stations E9
stations; while in the autumn, stations E9 and E8 were the
During the sampling period, a total of 28 taxa were
recorded: Polychaeta (4), Gastropoda (3), Oligochaeta
(1), Bivalvia (3), Amphipoda (1), Isopoda (2), Ostracoda
(1), Nematoda (1), Nemertinea (1), Platyhelminthes (1)
and Insecta (10) (Table 2). A total of 7092 individuals
were sampled, of which, the most frequent taxon was the
Mollusca phylum (47.14%, 3343 individuals), followed
by Annelida (40.65%, 2883 individuals). Together, these
taxons constituted more than 80% of the macrobenthos
(Table 2). The most abundant mollusc was the gastropod
Littoridina cumingii, especially in the winter at stations
E4 (588 ind. m
-2
) and E8 (695 ind. m
-2
). Other abundant
molluscs included the bivalve Kingiella chilenica,
particularly at station E5 in the autumn (413 ind. m
-2
). The
most abundant annelid species was Prionospio patagonica
(Spionidae), which was present at all stations during all
seasons, with the greatest abundance of this species
recorded at station E7 in the spring (798 ind.m
-2
; Table 2).
There were considerable increases in abundance between
seasons, especially at station E5 (1482 total individuals).
The opposite tendency was found at stations E3 and E2,
sampled at these stations over the year were 24 and 187
individuals, respectively (Table 2).
p<0.05). The
greatest total abundance was found in autumn (2375 ind.
m
-2
), and the lowest abundance was recorded in summer
(1196 ind. m
-2
). The season-station interaction was also
p<0.05). The greatest abundances were
found at stations E5 in the autumn, E7 in the spring, E8
in the winter, and E9 in the summer (Figure 4A). The
non-metric multidimensional scaling analysis cluster
analyses (Figure 3) separated station E3 from the rest of
the sampling stations in all seasons, a result due mainly
to the low abundance of macrobenthic organisms at this
station.
BRAZILIAN JOURNAL OF OCEANOGRAPHY, 64(3):239-248;2016
Bertrán et al.: Variation in Budi Lagoon macrobenthos
242
Table 1. Mean percentage (± SD) of sediment textures (i.e. Gravel, Sandy, and Muddy) and organic material (Org. Mat.)
recorded at the nine Budi Lagoon sampling stations.
Summer Winter Autumn Spring
Average SD Average SD Average SD Average SD
E1 Gravel 0.9 ± 0.6 0.3 ± 0.1 0.6 ± 0.8 1.0 ± 1.0
Sandy 86.3 ± 7.4 34.4 ± 7.6 32.8 ± 19.8 48.4 ± 15.0
Muddy 12.8 ± 7.0 65.4 ± 7.6 66.6 ± 20.1 50.6 ± 15.0
Org. Mat.
2.5 ± 1.0 8.1 ± 0.2 7.7 ± 0.9 6.9 ± 1.5
E2 Gravel 0.5 ± 0.6 0.2 ± 0.2 1.3 ± 0.8 0.8 ± 1.0
Sandy 14.6 ± 5.0 17.7 ± 6.0 24.5 ± 15.8 11.8 ± 7.1
Muddy 84.9 ± 5.0 82.1 ± 6.1 74.3 ± 15.1 87.4 ± 6.8
Org. Mat.
16.1 ± 0.5 14.8 ± 2.1 17.2 ± 2.1 17.7 ± 0.4
E3 Gravel 1.3 ± 2.0 0.6 ± 0.4 0.7 ± 0.5 0.4 ± 0.6
Sandy 23.5 ± 5.3 33.0 ± 8.4 48.9 ± 13.5 34.1 ± 10.1
Muddy 75.2 ± 4.8 66.3 ± 8.5 50.5 ± 13.2 65.5 ± 10.2
Org. Mat.
19.7 ± 0.5 19.1 ± 2.6 22.6 ± 1.1 19.1 ± 1.0
E4 Gravel 1.5 ± 0.7 3.6 ± 3.5 10.5 ± 5.1 2.4 ± 1.6
Sandy 62.2 ± 4.3 88.8 ± 4.4 58.9 ± 15.0 35.2 ± 15.6
Muddy 36.3 ± 4.6 7.6 ± 2.1 30.6 ± 19.6 62.4 ± 15.5
Org. Mat.
20.1 ± 1.9 1.9 ± 0.3 5.5 ± 2.1 5.2 ± 1.1
E5 Gravel 10.1 ± 18.5 1.6 ± 0.6 18.3 ± 15.6 1.2 ± 1.8
Sandy 41.1 ± 7.3 44.2 ± 10.5 44.0 ± 12.1 14.9 ± 8.3
Muddy 48.8 ± 22.6 54.3 ± 10.9 37.8 ± 18.4 83.9 ± 8.4
Org. Mat.
14.8 ± 1.2 14.6 ± 1.0 15.9 ± 4.3 16.0 ± 0.4
E6 Gravel 1.8 ± 1.7 0.5 ± 0.4 12.8 ± 7.1 4.9 ± 7.2
Sandy 39.4 ± 10.9 26.9 ± 3.0 72.6 ± 4.6 38.7 ± 7.0
Muddy 58.7 ± 12.0 72.6 ± 2.8 14.6 ± 7.9 56.4 ± 10.9
Org. Mat.
12.6 ± 3.2 12.1 ± 1.4 4.8 ± 2.5 11.9 ± 1.4
E7 Gravel 7.5 ± 7.8 16.9 ± 3.7 0.3 ± 0.2 6.9 ± 2.7
Sandy 52.6 ± 24.0 82.1 ± 4.0 34.2 ± 9.3 78.3 ± 12.9
Muddy 39.9 ± 17.1 1.1 ± 0.6 65.5 ± 9.4 14.8 ± 15.0
Org. Mat.
12.7 ± 3.1 1.2 ± 0.2 10.7 ± 1.3 5.4 ± 2.8
E8 Gravel 1.6 ± 2.7 0.4 ± 0.2 0.1 ± 0.1 1.5 ± 1.9
Sandy 15.5 ±
7.0 97.1 ± 1.2 96.6 ± 1.3 28.8 ± 11.1
Muddy 83.0 ± 7.0 2.5 ± 1.3 3.3 ± 1.4 69.7 ± 12.4
Org. Mat.
18.6 ± 1.5 1.3 ± 1.4 1.8 ± 0.2 23.5 ± 6.8
E9 Gravel 0.2 ± 0.1 2.0 ± 0.8 5.8 ± 3.0 0.8 ± 0.8
Sandy 96.5 ± 1.8 38.0 ± 5.9 90.3 ± 2.9 95.7 ± 1.6
Muddy 3.3 ± 1.9 60.0 ± 5.7 3.9 ± 0.7 3.5 ± 2.0
Org. Mat.
1.6 ± 1.0 18.4 ± 1.6 2.8 ± 0.7 1.5 ± 0.3
The greatest species richness was found in autumn,
especially at station E8, where 12 species were recorded.
Among the sampling stations, station E3 had the lowest
number of species during all seasons.
Diversity in the spring and summer was greater than in the
autumn and winter. The highest diversity values were found
in the summer and ranged from 0.89 to 2.37 (Figure 4B, C, D).
BRAZILIAN JOURNAL OF OCEANOGRAPHY, 64(3):239-248;2016
Bertrán et al.: Variation in Budi Lagoon macrobenthos
243
Figure 2. Non-metric multidimensional scaling ordination plot for Budi Lagoon organic material calculated for the four seasons of 2005 (A:
summer, B: autumn, C: winter, D: spring).
DISCUSSION
The high amount of organic material found in the
sediment of the Budi Lagoon is due to its semi-closed
condition and the large amount of nutrients that enter
(PEÑA-CORTÉS et al., 2006a;b) and from resident wild
birds (BERTRÁN et al., 2010). Indeed, more than 10,000
birds were registered in a 2014 census of the lagoon
area. The levels of organic material at Budi Lagoon were
quite high compared to the lower levels of other aquatic
ecosystems, such as the lagoon in the Cádiz Bay, Spain
(DRAKE; ARIAS, 1997), the lower course of the Biobio
River, Chile (BERTRÁN et al., 2001), and the estuary of
the Queule River, Chile (JARAMILLO et al., 1984).
The temporal variations in organic material and
texture characteristics of the sediment were similar to
patterns of variation found in other studies, where. For
example, the Queule River (QUIJÓN; JARAMILLO,
1993) and Biobio River (BERTRÁN et al., 2001), similar
to the Budi Lagoon, registered a predominance of sand
and less organic material in winter while summer was
at the Budi Lagoon may be due mainly to the input of
biogenic and terrigenous material produced by intense
precipitations, which, during 2005, occurred in autumn
and winter, particularly between May and August (DGAC,
2006). In turn, the summer months lacked rain, a situation
that has been associated with greater deposition and,
consequently, increased organic material (BERTRÁN et
al., 2001).
The observed macrobenthic richness of the Budi
Lagoon was similar to that described for other coastal lakes,
lagoons, and estuaries (STONER; ACEVEDO, 1990;
BERTRÁN et al., 2001; SFRISO et al., 2001; PEQUEÑO
et al., 2010; FIERRO et al., 2014), showing relatively
low density and high dominance (MISTRI et al., 2001;
BERTRÁN et al., 2013). The Budi Lagoon macrobenthos
in other soft-bottom ecosystems, such as the estuary of
the Berg River, South Africa (KALEJTA; HOCKEY,
1991) and the Cádiz Bay (ARIAS; DRAKE, 1994), where
abundance was greatest in the spring, closely followed
by autumn. These patterns were also comparable to those
of rivers near the study area, with FIERRO et al. (2015)
reporting the highest abundance of macroinvertebrates
in the summer-autumn. This tendency could represent
transitional periods related to increased primary
production in the summer and the increased precipitation,
decreased salinity, and increased re-suspension of
deposited materials as a consequence of forceful winds in
the winter. The increases in abundance may also be related
to reproductive and recruitment periods, which normally
occur in the summer and autumn (GALLARDO, 1993;
CONTRERAS et al., 2003). Notably, the diversity and
species richness values recorded in these seasons mainly
corresponded to immature insects.
The temporal variation of the macrobenthos showed