Estuarine, Coastal and Shelf Science 97 (2012) 38e43

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Estuarine, Coastal and Shelf Science

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Estuarine biodiversity as an indicator of groundwater discharge

A.C.F. Silva a, *, P. Tavares a,1, M. Shapouri a, T.Y. Stigter a, c, J.P. Monteiro a, c, M. Machado b,
L. Cancela da Fonseca c, d, L. Ribeiro a
a
Centro de Geosistemas-CVRM, Instituto Superior Técnico, Av. Rovisco Pais, 1049-001 Lisboa, Portugal
b
Universidade do Algarve, FCT, CCMAR, Campus de Gambelas, 8005-139 Faro, Portugal
c
Universidade do Algarve, Centro de Tecnologias da Água, Campus de Gambelas, 8005-139 Faro, Portugal
d
Laboratório Marítimo da Guia/Centro de Oceanografia, FCUL, Av. N. Sra. do Cabo, 939, 2750-374 Cascais, Portugal

a r t i c l e i n f o a b s t r a c t

Article history: Communities located in the interface between marine/brackish and freshwater habitats are likely to be
Received 8 February 2011 early responders to climatic changes as they are exposed to both saline and freshwater conditions, and
Accepted 3 November 2011 thus are expected to be sensitive to any change in their environmental conditions. Climatic effects are
Available online 18 November 2011
predicted to reduce the availability of groundwater, altering the hydrological balance on estuarine-
aquifer interfaces. Here, we aimed to characterise the estuarine faunal community along a gradient
Keywords:
dependent on groundwater input, under a predicted climatic scenario of reduction in groundwater
benthic macrofauna
discharge into the estuary. Sediment macrofauna was sampled along a salinity gradient following both
salinity gradient
groundwater
the wet and dry seasons in 2009. Results indicated that species abundance varied significantly with the
habitat interface salinity gradient created by the groundwater discharge into the estuarine habitat and with sampling
climatic and human pressures time. The isopode Cyathura carinata (Krøyer, 1847) and the polychaetes Heteromastus filiformis (Clapar-
ède, 1864) and Hediste diversicolor O.F. Muller, 1776 were associated with the more saline locations, while
oligochaeta and Spionidae were more abundant in areas of lower salinity. The polychaete Alkmaria
romijni Horst, 1919 was the dominant species and ubiquitous throughout sampling stations. This study
provides evidence for estuarine fauna to be considered as a potentially valuable indicator of variation in
the input of groundwater into marine-freshwater interface habitats, expected from climatic pressures on
aquifer levels, condition and recharge rates. For instance, a reduction in the abundance of some poly-
chaete species, found here to be more abundant in freshwater conditions, and increasing Oligochaeta
found here on higher salinities, can potentially be early warnings of a reduction in the input of
groundwater into estuaries. Estuarine benthic species are often the main prey for commercially
important fish predators such as in our case study, making it important to monitor the aquatic habitat
interfaces taking into consideration the estuarine macrobenthos and groundwater availability in the
system.
Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction which are subject to groundwater influence (McKenna and Martin,

2004), as this key resource is under severe climatic and human
Freshwater ecosystems have been important sources for the pressure (Danielopol et al., 2003).
development of environmental monitoring programmes (De Pauw The evaluation of shifts in the species presence on an ecosystem
et al., 1992), but these solutions are hardly applicable to the very is a valid strategy for environmental monitoring (Van Hoey et al.,
variable tide-related characteristics of the brackish estuarine 2010), because the life cycle of organisms integrates alterations
environment such as salinity variation. Hence, there is a necessity on the environmental characteristics in a relatively wide period of
of developing rapid tools for monitoring the marked estuarine time. This approach overcomes the limitations of an evaluation of
environmental gradients such as salinity, particularly for habitats the environmental condition singly based on physicalechemical
parameters, which does not considers the consequences of envi-
ronmental alterations on the ecosystem (Cairns et al., 1993).
* Corresponding author.
Management plans which include biological indicators are advan-
E-mail address: ana.c.f.silva@ist.utl.pt (A.C.F. Silva). tageous because they incorporate the conjugated action of envi-
1
Deceased. ronmental conditions and make the impact easily detectable.

0272-7714/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2011.11.006
 A.C.F. Silva et al. / Estuarine, Coastal and Shelf Science 97 (2012) 38e43 39

Biological indicators also allow evaluating factors not directly (Goodsell et al., 2009). To accomplish this in the context of the
measurable, such as biological complexity and ecological value and, present study, differing groundwater availability would have to be
no expensive laboratorial chemical analysis are required such as for supplied to faunal communities and their response (e.g. presence-
chemical indicators (Ambrogi and Forni, 2004). absence, abundance, etc) measured. Such manipulations would be
Biological indicators can be defined as the presence or abun- logistically challenging and are out of scope of the present work.
dance of some taxa which may be considered to represent biodi- Instead, the aim of the present study was to identify taxonomic
versity of a large assemblage, of species living in a particular habitat groups and/or species of estuarine sediment which can potentially
or the presence or abundance of other taxa (MacNally and be monitored to detect a reduction in groundwater availability.
Fleishman, 2002). They are expected to be useful in identifying It was expected that due to discriminating tolerances, benthic
areas that warrant special protection and specific conservation species were distributed accordingly to the salinity gradient origi-
measures, and are based on the presence of specific taxonomic nated by the freshwater output into the estuary. The null hypoth-
groups. Within an aquatic ecosystem, the benthic fauna is often eses tested were that there are no differences: a) in the identity and
used as indicator of environmental changes and considered to be: abundance of species between near and far locations in relation to
(i) key precursor of the implementation of the Water Framework the point of groundwater input to the sampled estuarine habitat
Directive to the very recent implementation of the Marine Strategy and, b) between the end of the dry and wet sampling times.
Framework Directive (Van Hoey et al., 2010) and; (ii) the most
adequate descriptor of estuarine habitats because organisms are 2. Methods
mostly sedentary and thus, reliable local indicators over time of
environmental conditions (Warwick, 1993). 2.1. Study site
Groundwater is currently considered a key resource under severe
threat due to human consumption, pollution and climatic pressures The present study was undertaken in southern Portugal, at the
(Danielopol et al., 2003). Groundwater is also regarded as the second largest estuary of this region which is associated with the
primary provider for human freshwater demands such as agricul- Arade river. The estuary receives freshwater contributions from
ture and industry (Santos et al., 2001; Danielopol et al., 2003). In rivers in the winter and groundwater all year round. Groundwater
southern Portugal, where the present study was conducted, discharges into a branching channel of the estuary from the
groundwater represents 60% of freshwater human usage and nearly Querença-Silves aquifer. The aquifer is built up of carbonate sedi-
80% of agricultural demand. These demands are likely to increase in mentary rock, has a total areal extent of 324 km2 and a mean annual
the future as a result of global warming (Santos et al., 2001). recharge of 100
106 m3 (Monteiro et al., 2007; Mendes Oliveira
Estuaries often interface with coastal aquifers and receive et al., 2008; Stigter et al., 2009). The aquifer is mainly explored
groundwater discharge, implying that communities therein are for agronomic irrigation purposes (31
106 m3/year) and public
subject to changes in the salinity due to both the marine and water supply (w10
106 m3/year). In extremely dry years (such as
freshwater influences. The groundwater discharge into estuarine of 2005), total abstractions of the aquifer reached 60
106 m3/year,
habitats may be reduced by the climatic-driven pressures on its which is more than half of the aquifer annual recharge rate.
availability, and thereby induce changes the ecosystem stability. Sampling was made at a branching channel of the main estua-
The interface or border habitats such as estuaries and wetlands are rine channel near Silves (Estômbar site: 37 90 42.8700 N,
considered to be highly vulnerable to alterations in variables such 8 290 10.6100 W). This branching channel was located approximately
as salinity, sediment and nutrient availability (Bates et al., 2008). half-way between the river and sea points of the estuary.
This is the case of the estuary associated with the Arade River at the It represents an interface area between the main estuary channel
south coast of Portugal, a system of ecological and economic and a point of groundwater discharge into the estuary. Average
importance. The estuary permanently receives groundwater from groundwater discharge from the aquifer into the branching channel
the Querença-Silves aquifer, the largest and most productive is 400 l s-1, approximately 25% of total outflow, though this
aquifer in the south of Portugal. If the average temperature rises in percentage varies between seasons and years. In the past two years
the near future as predicted in climate change scenarios for this (2008e2010), continuous recording of salinity in this lateral
region (Santos et al., 2001), more drought periods will occur. In channel at the point of groundwater discharge has been performed,
these scenarios, the groundwater withdraws will rise and its output thus providing reliable measurements of salinity variation with
to adjacent habitats such as estuaries will be reduced and aquifer discharge. At the end of the summer of 2009, salinity in the
ecosystem stability be altered (Ranjan et al., 2006). Coastal aquifers estuary ranged from 20% (location C at low tide) to 100% (location E
such as the Querença-Silves are also highly vulnerable to the threat at high tide) of seawater, hence indicating a continued effect of
of saline intrusion due to sea level rise (Ranjan et al., 2006). Hence, aquifer discharge. Sediment at the different stations was muddy
the fauna of associated habitats such as the Arade estuary will likely (mostly silt and clay), with a moderately abundant biogenic fraction
be exposed to increased salinities, becoming important to under- (shell fragments).
stand how benthic estuarine species respond in the present day to
the groundwater-estuarine interaction. Invertebrate communities 2.2. Sampling design
of transitional waters (freshwater-saltwater ecotone) are highly
influenced by freshwater discharge, showing marked seasonal Sampling was carried out at low-water. Five replicate cores
variation mainly related to salinity fluctuations (Chainho et al., (0.01 m2) were sampled at each location using hand corer devices.
2006). Alterations in the benthic community will likely have The sediment was sieved in situ through a 0.5 mm square mesh for
cascade trophic consequences for their predators, which in the macrofaunal studies. The retained material was fixed in 4% buffered
studied estuary correspond mainly to commercially important fish formalin stained with Rose Bengal until further analysis. Five
species (Cabral, 2000; Gonçalves et al., 2004). The salinity variation locations were sampled in the Estômbar site and their position
related to the groundwater discharge into the estuary and the reflected a distance-based gradient, starting at the point of
benthic species tolerances to salinity levels have an important role groundwater surface discharge into the estuary. Hence, locations
in determining prey availability for their predators. were chosen along a line of flow from low salinity at the point of
Identification of bioindicators demands establishing a causal groundwater discharge to higher salinity, close to the main estuary
relationship and this ideally requires in situ manipulative tests channel. Location C was adjacent to the point of groundwater
40 A.C.F. Silva et al. / Estuarine, Coastal and Shelf Science 97 (2012) 38e43

discharge, location B was w100 m away, location A was w200 m

away, location D was w400 m away, and location E was situated
where the sampled branching channel meets the main estuarine
channel, approximately 600 m away from the groundwater
discharge point. The temporal variation of macrofauna abundance
was also examined at the end of dry (OctobereNovember 2009)
and wet (April 2010) periods. Prior to identification, organisms
were sorted into major taxonomic groups using a stereoscopic
microscope, identified to the lowest practical taxonomic level
(usually species level) and counted.

2.3. Experimental design and data analysis

The presented study considered a two factor design: Location

(orthogonal, fixed, 5 levels (Salinity A to salinity E) and Time
(orthogonal, fixed, 2 levels: end of dry and wet seasons). This
design does not allow withdrawing conclusions on seasonal Fig. 1. MDS ordination of fauna sediment samples collected at the end of the dry and
patterns as no replicated times were measured within seasons. Five wet times, in the distance gradient of locations in relation to point of groundwater
replicates were taken at each location and time combination. input (AeE).
Multifactorial analyses were used in the PRIMER þ package (Clarke
and Warwick, 2007; Anderson et al., 2008), including the PERMA-
NOVA hypothesis test, the SIMPER routine to identify the species abundances in the dry than on the wet times (SIMPER routine). The
most contributing for significant factorial differences, and MDS and Alkmaria romijni Horst, 1919, Hediste diversicolor O.F. Müller, 1776
dbRDA to graphically examine those differences and the underlying and the Spionidae, were shown to be more abundant in the wet
species. The DIVERSE tool was used to calculate the total number of sampling time. Together, these taxonomic groups contributed
species and individuals, the species richness (Margalef index), and approximately 50% for the differences between sampling times. The
the diversity indexes Simpson dominance and Shannon-Weaver. SIMPER routine showed that locations close to the freshwater
These indexes allow describing the relationship of individuals of source (A, B and C) had higher abundances of Oligochaeta, Spio-
varying subspecies within a zone. For all tests, the BrayeCurtis nidae and C. capitata than locations in more saline conditions.
similarity measure, the fourth-root transformation and 9999 Locations closer to the main estuary channel and therefore in more
permutations were used. brackish conditions (D & E), differed from less saline conditions
locations (A, B and C) mainly due to larger abundances of
H. diversicolor, Cyathura carinata (Krøyer, 1847) and Heteromastus
3. Results
filiformis (Claparède, 1864). The polichaete A. romijni was ubiqui-
tous throughout all sampling locations although generally more
3.1. Species distribution
abundant in locations closer to freshwater conditions.
The species distribution was explained by the interaction of the
distance to the point of groundwater discharge into the estuary and 3.2. Species contribution for spatial and temporal differences
sampling time (Table 1). The MDS ordination showed that the
community structure varied strongly with sampling time, and The dbRDA ordination was considered to be a considerably good
relatively less with location, although location D is clearly separated representation of the sample variation as both axes included w50%
from the remaining locations, which are more homogenous in of the total variation (Fig. 2). Only variables, i.e. species, with
between (Fig. 1). The benthic community only varied significantly correlations R > 0.4 were considered. This representation clearly
between the dry and wet times at locations near the main estuary
channel (Pair-wise tests, p (perm) < 0.05 for location E;
p (perm) ¼ 0.05 for location D). As expected, pair-wise tests for
term location only showed significant differences in the abundance
in pairs with locations D or E (including A, D; A,E; B,D; B,E; C,D; C,E).
Anelida (Polychaeta and Oligochaeta) and Crustacea (Isopoda
and Amphipoda) were the dominant sampled groups of macro-
invertebrates. The species which contributed the most for differ-
ences between sampled times were Oligochaeta (w11%) which,
together with the polychaete Capitella capitata (Fabricius, 1780) and
the bivalve Scrobicularia plana (da Costa, 1778), had higher

Table 1
Permanova analysis of the sediment fauna for factors time (dry and wet) and loca-
tion (AeE). The number of permutation used was 9999.

Source df SS MS Pseudo-F P (perm) U. perms P (MC)

Pe 1 3347.7 3347.7 3.5409 0.0021 9946 0.0049
Lo 4 12959 3239.7 3.4267 0.0001 9913 0.0001
PexLo 4 9498 2374.5 2.5115 0.0008 9899 0.0013
Res 40 37818 945.44
Total 49 63622 Fig. 2. dbRDA ordination of the sample variation in abundance of species, where the
overlying vectors are the species which had correlation >0.4.
 A.C.F. Silva et al. / Estuarine, Coastal and Shelf Science 97 (2012) 38e43 41

showed that the species H. ulva isolated almost all samples from which generally follows the tidal oscillations measured at 20 km
location D, while Alkmaria romijni, Spionidae, Capitella capitata, distance, with a small time lag, but stabilizes during low tide, due to
Oligochaeta and Sepia plana separated location A, B and C from the input of groundwater. No difference was found in sediment
most of samples of location E (Fig. 2). No pattern was detected for particle size between stations.
separation of dry and wet times. No significant differences were
found between the diversity indexes and measures calculated by 4. Discussion
the DIVERSE tool for all factors and their interaction (Time: Pseudo-
F1.49 ¼ 1.78, P(perm) ¼ 0.17; Location: Pseudo-F4.49 ¼ 1.87, 4.1. Groundwater availability and community predictions
P(perm) ¼ 0.08; Time
Location: Pseudo-F4.49 ¼ 1.71,
P(perm) ¼ 0.31). The present work represents the first study in Portugal exam-
ining the influence of groundwater availability on estuarine biodi-
3.3. Physical measurements versity. There was a biological response to a salinity gradient
established by groundwater discharge into the estuary. There was
Variation in levels of electrical conductivity (EC, an indicator of also indication that temporal differences in macrobenthic presence
salinity) and temperature can be observed in Fig. 3 for location A. may occur between in dry and wet season, although further
Location A is particularly interesting to observe as it simultaneously evidence is required. Taken together these results indicate that the
responds to the highest level of influence of groundwater discharge benthic estuarine community can be used as a surrogate for eval-
and to typical estuarine brackish water (Fig. 3). There were striking uating changes in the ecosystem salinity. Climatic predictions
differences in conductivity between summer and winter, with indicate that groundwater will be used in higher human demands
higher influence of groundwater discharge into the branching due to increased drought periods (Santos et al., 2001), and that
channel in the winter and lower in the summer. The influence of groundwater availability and quality will diminish (Danielopol
groundwater discharge can also be observed in the water level, et al., 2003). There is a predicted scenario of reduced aquifer

Fig. 3. Variation of water level, electrical conductivity (EC) and temperature at the location of groundwater discharge into the Estômbar channel of the Arade estuary (location A);
two representative times are indicated, at the end of the dry season (summer, upper graph) and in the middle of the rainy season (nearly winter, lower graph); also indicated are the
tidal fluctuations measured in Lagos, located 20 km towards the west.
42 A.C.F. Silva et al. / Estuarine, Coastal and Shelf Science 97 (2012) 38e43

recharge and increased sea level rise followed by a potential saline (Krøyer, 1838) represent w 80% of the dominant fish in the Arade
intrusion, which can change the salinity condition of the Querença- estuary (Gonçalves et al., 2004), and their diet is mainly composed
Silves aquifer (Santos et al., 2001; Monteiro et al., 2007). This of small crustaceans and polychaetes (Leitão et al., 2006). There are
condition is aggravated by the risk of overexploitation for irrigation 36 commercially important fish species in the Arade estuary,
and public water supply and thus, the biological community is indicating the importance of this ecosystem as a nursery for many
likely to suffer specific shifts related to salinity which can be commercial species (Gonçalves et al., 2004). Hence, under a pre-
detected under a biologically orientated monitoring programme. dicted climatic scenario of reduction in the groundwater discharge
Other physical factors such as grain size were considered not to rate into the estuary, the macrobenthic species found here to be
have had an important influence on species distribution, because more associated with the groundwater discharge point such as the
grain size (Shapouri, pers.obs.) did not differ across the maximum Oligochaeta, will likely have their abundance reduced. This may
extension of our sampling points (w600 m). The level organic have bottom-up cascade effects into their predatory fish mentioned
matter (OM) present in the sediment and salinity are known to be above, which will see their prey availability reduced. Such
the two most important physic-chemical features influencing cascading trophic links and effects should be evaluated and taken
benthic distribution in other Portuguese estuarine systems (Nunes into consideration in a monitoring programme, as shifts in the
et al., 2008; Teixeira et al., 2008). OM was not measured in the abundance of those fish species can be also early warnings signals
present study due to logistic constraints. However, it is possible of changes in prey availability, albeit sampling of invertebrates is
that OM varied across sampling stations and potentially accounted logistically easier. Global climate change effects are considered
for w50% of the unexplained variation within the total variation a major threat to estuarine fishes and their fishery (Roessig et al.,
found in our data. 2004), to the structure and dynamics of estuarine macrobenthic
The community showed clear evidence of responding to the communities (Grilo et al., 2011), and also to coastal fresh ground-
influence of groundwater discharge and times. For instance, water resources (Ranjan et al., 2006). Hence, groundwater input
Oligochaetes and isopods were more abundant at the freshwater into estuarine systems can be a key bottom-up factor regulating
discharge location and at the end of wet time. Similar groundwater both food webs and biodiversity levels.
dependence has been found for rotifers in Brazilian estuaries but in Benthic communities were shown here to provide an indirect
their case for the dry season (Medeiros et al., 2010). Our study method to evaluate changes in salinity in the interface between
allows the prediction that an increase in the abundance of the some aquatic habitats encompassing groundwater systems. It is impor-
polychaete species and decreasing oligochaeta, are potentially early tant that future monitoring programmes include an assessment of
warnings of a reduction in groundwater input into this habitat the spatial and temporal variability of the species identified here as
interaction. The abundance of the Oligochaetes, Spionidae and potential responders to groundwater availability.
Capitella capitata will potentially diminish greatly under severe
reduction of groundwater discharge into estuarine ecosystems. This Acknowledgements
is potentially more visible at the end of the dry season when
groundwater availability is likely more limited. Conversely, the This study could not have been possible without the key role
polychaete Alkmaria romijni, the dominant benthic species played by Paula Tavares who sadly gave her life to this research
sampled, will potentially remain in the current abundance level programme. We are also very grateful to the macrobenthic research
unless other environmental parameters such as organic matter or team of Centro de Oceanografia, FCUL-University of Lisbon, namely
environmental variables (e.g. pH, temperature) shift. This species is Paula Chainho, Gilda Silva and João Paulo Medeiros, who provided
known to: i) tolerate a wide range of salinities (see Chaouti and invaluable support in the faunal identification. This work was part
Bayed, 2006), ii) be associated with sheltered estuarine condi- of the CLIMWAT project - Assessing and managing the impact of
tions (Gilliland and Sanderson, 2000) and, iii) was common in all climate change on coastal groundwater resources and dependent
sampled stations, it was considered not to be a good indicator of ecosystems, funded by ERA-CIRCLE/0002/2007.
groundwater influence in the studied estuarine system.
Our studied area is a protected site where aquatic biodiversity is
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