Marine Environmental Research 179 (2022) 105672

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Marine Environmental Research

journal homepage: www.elsevier.com/locate/marenvrev

Groundwater discharge locally shapes the rocky shore macroinvertebrate

community in South-Southwest Portugal
Londoño-Londoño Julián E a, Condesso de Melo a, A.C.F. Silvaa, b, c, *
a
CERIS, Instituto Superior Técnico, Universidade de Lisboa, Av. Rovisco Pais 1, 1049-001, Lisboa, Portugal
b
Departamento de Engenharia Civil, Arquitectura e Georrecursos, Instituto Superior Técnico, Universidade de Lisboa, Bobadela, Portugal
c
Departamento de Engenharia e Ciências Nucleares (DECN), Instituto Superior Técnico, Universidade de Lisboa, Bobadela, Portugal

A R T I C L E I N F O A B S T R A C T

Keywords: Groundwater discharge is an essential process in the functioning of coastal aquatic ecosystems due to its sig­
Intertidal nificant role in nutrient cycling, geochemical mass balances and primary productivity. However, the occurrence
Coastal ecosystem patterns, importance, and effects of this discharge on rocky shores communities remain largely unknown. We
Freshwater
assessed the importance of groundwater discharge into the highly ecologically important intertidal ecosystems.
Abundance
Local scale
We compared the benthic macroinvertebrate composition and abundance between discharge and no-discharge
Disturbance sites, replicated for five shores in South and Southwest Portugal. This robust replicated feature across shores
Climate change and regions is a particularly novel contribution to the field. Groundwater discharge significantly affected the
Aquifer biological communities’ abundance across all shores, but not biodiversity patterns. The algae Enteromorpha sp.,
snail Melaraphe neritoides and lichen Verrucaria maura can potentially be used as bioindication tools for shifts in
groundwater discharge quantity and qualitative patterns. Our study validates the importance of this commonly
overlooked local disturbance factor in regulating intertidal communities.

1. Introduction which will reduce the recharge and cause a groundwater-level decline
(Kløve et al., 2013; Stigter et al., 2014). The potential importance of
The groundwater discharge into coastal ecosystems such as estuaries, groundwater discharge into coastal ecosystems is greatly intensified in
lagoons and sandy shores is a key factor influencing their biological coastal Mediterranean regions, where groundwater availability for
communities (Félix et al., 2015; Shapouri et al., 2016; Rodellas et al., discharge is hampered by decreasing recharge rates, overexploitation of
2018). This freshwater input is important for setting ecotones by influ­ the resource and climate change effects (Stigter et al., 2014; da Costa
encing parameters like salinity, nutrient loading, sediment type or et al., 2020; Rachid et al., 2021). Groundwater availability can then
organic matter and even as a pollutant source (Capone and Bautista, become a critical factor threatening the sustainability of coastal eco­
1985; Nevill et al., 2010; Lewandowski et al., 2020; Connolly et al., systems and their associated ecosystem services (Erostate et al., 2020).
2020), making aquatic coastal ecosystems potentially groundwater Although aquatic systems are viewed as resilient and able to main­
conditional. tain a healthy and self-sustaining condition despite large year-to-year
In the last decades, the worldwide increased use of groundwater for variations in hydrologic and temperature (Poff et al., 2002), alter­
human consumption and irrigation has negatively influenced ground­ ations to the timing, quality, quantity, and distribution of groundwater
water availability by reducing its aquifer levels (Konikow and Kendy, by natural or anthropogenic means can alter both the form and function
2005). The effects of over-abstraction of groundwater are escalating of associated ecosystems (Foster and Chilton, 2003; Murray et al., 2003
from local problems to become an increasingly regional issue (Bartolino in Lagomasino et al., 2015). Hence, the ecological consequences of
and Cunningham, 2003), especially in arid and semi-arid areas where global change in coastal ecosystems will largely depend on the rate and
groundwater is the main source of freshwater such as in our case studies magnitude of change in critical environmental drivers such as temper­
(Stigter et al., 2014; Erostate et al., 2020). In addition, the predicted ature, sea-level rise, precipitation, runoff, and groundwater discharge.
climate change patterns will exacerbate these problems in many parts of However, and although recognised as essential, features of the hydrau­
the world due to decreasing rainfall and increasing evapotranspiration, lic, chemical and ecological connections between coastal surface and

* Corresponding author. CERIS, Instituto Superior Técnico, Universidade de Lisboa, Av. Rovisco Pais 1, 1049-001, Lisboa, Portugal.
E-mail addresses: julian.londono4@udea.edu.co (L.-L. Julián E), teresa.melo@tecnico.ulisboa.pt (C. de Melo), ana.c.f.silva@tecnico.ulisboa.pt (S. A.C.F.).

https://doi.org/10.1016/j.marenvres.2022.105672
Received 6 January 2022; Received in revised form 22 April 2022; Accepted 31 May 2022
Available online 10 June 2022
0141-1136/© 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
L.-L. Julián E et al. Marine Environmental Research 179 (2022) 105672

groundwater bodies in Mediterranean regions remain largely unknown local factor and open the path to consider classifying rocky shores as
(Erostate et al., 2020). groundwater-dependent ecosystems.
Benthic communities are subject to various physical and chemical
gradients that can affect their growth and physiology, and groundwater 2. Methods
discharge is one factor that contributes to these environmental gradients
in coastal waters (Lecher and Mackey, 2018). Freshwater discharge 2.1. Study locations characterization
strongly influences invertebrate communities of transitional waters
(freshwater-saltwater ecotone), showing a marked seasonal variation Two study regions were selected, the Southwest Portuguese coast
mainly related to salinity fluctuations (Chainho et al., 2006; Silva et al., and the western part of the Algarve region on the South coast of Portugal
2012). Several studies have also shown a freshwater effect on estuarine (Fig. 1). Therein, five rocky shores were selected, Azenhas do Mar and
(Canada) and coastal lagoon communities (Yucatan and Mexico) Porto das Barcas in the Southwest, and Olhos de Água, Ferragudo, and
(Lagomasino et al., 2015; Ardisson and Bourget, 1997; Pech et al., 2007; Praia da Luz in the South. These locations were chosen because
Medina-Gómez and Herrera-Silveira, 2006). The identification of such groundwater discharges via adjacent cliff springs were consistently
sensitive communities with associated environmental conditions makes observed throughout the years through surveys supported by parallel
it possible and effective to predict and detect impacts from variations in research initiatives and are documented in official maps (Fig. 1). We also
groundwater discharge. validated the discharge occurrence within our sampling year.
Rocky shores are amongst the most biodiversity-rich coastal eco­ These locations are currently under several statutes and diplomas for
systems (Satyam and Thiruchitrambalam, 2018), yet are under protection and management of their natural assets. In 1988, the
increasing threat due to anthropogenic activities such as increasing Southwest Coast was classified as Protected Landscape Area and in 1997
population, tourism, trampling and seafood gathering activities, and promoted to National Park – Southwest Alentejo and Vicentine Coast
climate change and sea-level rise effects (Mieszkowska, 2016). Natural Park (SAVCNP).
Furthermore, due to their physical adjacency to groundwater discharge
points in cliffs - springs, and runoffs, are highly exposed to groundwater
2.2. Hydrological context
discharge from coastal aquifers. Most available research has focused on
submarine coastal communities (e.g. Bussmann et al., 1999; Johannes,
The Mediterranean Climate, which is associated with a trend of high
1980; Encarnação et al., 2013) and loose sediment sandy shore and mud
average temperature, long, hot summers without rain, and mild winters,
tidal flats (Dale and Miller, 2007; Migné et al., 2011; Ouisse et al., 2011;
with low values of atmospheric precipitation, correspond to the real
Cave and Henry, 2011). Albeit limited in spatial replication, one pre­
conditions found in the study regions. The analysis of the climatic
vious study has shown that submarine groundwater can influence the
component classified this region as dry and semi-arid according to the
rocky shore epibenthic community structure and ecophysiological con­
Aridity Index. The high temperatures recorded during the long summers
dition of midlevel intertidal molluscs (Piló et al., 2018).
have been a significant aspect of the climate, as well as precipitation
Our work contributes to filling the considerable lack of information
rates among the lowest in Europe, mainly distributed over the winter
on the importance and effects of this discharge on the shores’ biological
period, and being practically null throughout the summer. Most rivers
communities by focusing on the influence of groundwater discharge on
and streams have runoff only during the rainy season, being dry during
intertidal macroinvertebrate communities. We specifically tested the
the summer, except for some deeper areas, with springs supplied by
hypothesis that biological communities differ in abundance and/or di­
groundwater, which maintains water throughout the year (Guerra et al.,
versity between sites with and without direct groundwater discharge
2019).
from adjacent cliffs. Our study is the first to test this hypothesis at both
local and regional scales, with a robust spatial replication design. Hence,
our work represents a pioneer assessment of the potential response of 2.3. Hydrogeological context
intertidal rocky shore communities to the influence of groundwater in
southwest Europe. It will fill an important gap in the current state of the The southwest coast of Portugal corresponds to the Maciço Antigo
art by validating the biological importance of this commonly overlooked hydrogeological unit, which is the geological unit that occupies the
greatest extent in Portugal, consisting essentially of igneous and

Fig. 1. Location of the study shores in the South (Olhos d’Água, Ferragudo, and Praia da Luz), and Southwest (Porto das Barcas and Azenhas do Mar) coast
of Portugal.

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L.-L. Julián E et al. Marine Environmental Research 179 (2022) 105672

metasedimentary rocks (Fig. 1). These lithologies host hard-rock aqui­ uppershore level (supralittoral), where direct runoff was visible. Sam­
fers. In general terms, they can be considered formations with limited pling was made in February–March 2018, after the potential maximum
hydrogeological aptitude, and poor in groundwater resources. However, peak of discharge of the 2017 wet season (October–February 2017
despite the scarcity of groundwater resources, they play an important which corresponds to the period of highest precipitation) and hence,
role, both in supplying the population and in agriculture. In fact, in when discharge cumulative effects were maximized. All organisms were
addition to thousands of small private catchments, most municipalities possible to identify in situ and care was taken to return to original spots
have many groundwater facilities for the supply (Almeida et al., 2000). when dislodgment was necessary for identification.
On the other hand, the south region studied (Algarve), corresponds
to the hydrogeological unit named Orla Meridional, a highly productive 2.5. Data analysis
region with a well-studied set of aquifers (e.g. Monteiro and Costa, 2004;
Stigter et al., 2006; Stigter et al., 2010; Da Costa, 2011; Stigter et al., All biological data statistical tests were made with the software
2014; Hugman et al., 2017; Neves et al., 2020). Groundwater abstrac­ PRIMER-E (Clarke and Gorley, 2015) and using the Bray-Curtis simi­
tion for public supply from these aquifer systems saw a steady increase larity matrix. The null hypothesis of groundwater discharge having no
from the 1950s until the 1990s when dams were built to fulfil the supply effect on the biological communities was tested by comparing the taxa
(Monteiro and Costa, 2004). abundance of sites with discharge with that of no-discharge, using the
The main groundwater flow direction is towards the coast (Almeida multivariate PERMANOVA technique (Anderson et al., 2008). This hy­
et al., 2000). The shift toward surface water use in the early 2000s led to pothesis was tested for both study regions, including shores as replicates
a sharp rise in the water table (Monteiro et al., 2007; Stigter et al., within regions. The experimental design had three factors: “Region”,
2006a,b) and higher groundwater hydraulic gradients. The increased two levels (south and southwest); “Shore”, two levels, random and
discharge led to the reactivation of several springs, forming local nested in region and; “Discharge”, with two levels, “discharge” and
discharge points of the aquifers even during the summer when natural “no-discharge”, nested in shore. A p-value of 0.05 was used for result
recharge is almost null and demand for agriculture and human con­ interpretation. Data were pre-treated with a fourth root to secure the
sumption rises. homogeneity of variances.
Due to the lack of logistic conditions, this study was unable to The ordination technique Principal Component Ordination (PCO)
characterise both the temporal patterns of discharge rates and the was used to visually explore and spatially represent differences in the
chemical composition of the discharge water. There is no available data macroinvertebrate presence across sites. The replicated quadrates are
on intertidal spring flow rates. However, few studies have estimated the individually positioned in the graph, whereby the closest each replicate
contribution of coastal aquifers, especially in the south region of is to each other, the more similar they are in terms of macroinvertebrate
Portugal. Hugman et al. (2014), estimated the spatial and temporal community abundance and composition. The similarity percentages –
distribution of coastal groundwater discharge for two coastal aquifers in species composition (SIMPER) technique identifies the contribution of
the South of Portugal (Albufeira-Ribeira de Quarteira and Quarteira each taxon (%) to the dissimilarity between each two groups, discharge
aquifers) finding, in a scenario of natural state, discharge rates ranging versus no-discharge locations in our study. This technique was used here
from 5 to 10 m3/day per meter of coastline. Steady-state simulations to identify the taxa most contributing to differences between discharge
indicate that the system contributes a range of average annual fresh­ and no-discharge locations. Histograms were used to visually represent
water to coastal discharge between 6.5*106 and 15*106 m3/year from the average abundance of the taxa identified using the SIMPER tech­
the Albufeira-Ribeira de Quarteira aquifer, and 4.5*106 and 11.3*106 nique. Radial graphs were used to show the contribution of each taxon to
m3/year from the Quarteira aquifer (Hugman et al., 2014). For the study the dissimilarity of the samples, the radial axis represents the percentage
cases on the southwest coast of Portugal, which are placed on the Maciço of contribution to the dissimilarity, therefore, the further from the center
Antigo hydrogeological unit, there is no available data regarding the the higher the contribution of each taxon to the dissimilarity of the
discharge rates in coastal springs. However, it is known that this unit is samples.
less productive than the Orla Meridional in the Algarve. Almeida et al.
(2000), estimates that the average availability of hydrogeological re­ 3. Results
sources for the area ranges between 1 L/s*km2 and 3 L/s*km2
approximately. The PERMANOVA analysis rejected the null hypothesis consistently
for all Southwest and South shores, proving that the macroinvertebrate
2.4. Biological sampling community significantly responded to groundwater discharge (Table 1),
differing between discharge and non-discharge sites. The specific bio­
For all shores and based on previous information from parallel logical response patterns on Southwest and South shores are examined
research initiatives and direct visualisation discharge locations were in the next two subsections.
easily identified in the shore rocky section as all sampled shores have
adjacent vertical cliffs and direct spring-like discharge points are visible 3.1. Groundwater effect on biological communities of the Southwest Coast
on the surface cliffs, with running groundwater directly entering adja­ shores
cent horizontal intertidal rocky slabs. These discharges display a
consistent and permanent presence and flow rate (Almeida et al., 2000). The PCO analysis for the samples on the shores of Azenhas do Mar
Other studies have also used visual site identification as a suitable tool to
pinpoint intertidal discharge points (Piló et al., 2018). Then, within each Table 1
shore, the rocky section was divided into two sites, one immediately PERMANOVA analysis of the macroinvertebrate communities for factors Region,
adjacent to the groundwater discharge site and another >50 m distant Shore and Discharge. Significance is considered at a p-value<0.05. Significant
(but within the same shore) where no discharge was apparent or values and italicized.
possible. All other environmental features such as rock slope, type and Source df SS MS Pseudo-F P(perm) Unique perms
exposure to wave action were similar across sites per location.
Region 1 6102.3 6235.1 32.945 0.09 112
On each site, the macroinvertebrate community was visually Shore 3 555.69 185.23 35.816 0.99 6164
assessed and counted (either as abundance or percentage cover for algae Discharge 5 50993 185.23 39.91 0.0001 9930
and similar frond-like organisms) in ten replicated 50 × 50 cm quadrat,
a standard technique in biological studies on these habitat types (Boa­ Res 90 22999 255.54
Total 99 80650
ventura et al., 2002). Quadrates were randomly deployed at each site at

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L.-L. Julián E et al. Marine Environmental Research 179 (2022) 105672

(AZM) and Porto das Barcas (PB) showed that the community structure
varied strongly with the discharge factor (Fig. 2). Two clearly differ­
entiated groups are recognised as a response of the discharge (D) and
non-discharge (ND) sites, with approximately 84.5% of the variation
being explained by this factor. The macroinvertebrate community was
very similar between shores for each discharge zone type.

3.1.1. Abundance of species

Figs. 3 and 4 show the average abundance of the sampled species on
both shores. It can be observed that the algae Enteromorpha sp. and the
limpet Patella vulgata were more abundant in discharge sites, with a
higher percentage of bare rock. In contrast, the lichen Verrucaria maura,
the Chthamalus sp. barnacle and several gastropod taxa (limpets and
snails) were more abundant in no-discharge sites.

3.1.2. Identification of key responsive taxa

The algae Enteromorpha sp., the snail Melaraphe neritoides, and the
lichen Verrucaria maura contributed the most to the differences in bio­
logical communities’ structure by discharge factor on both shores
(Table 2 and Fig. 5). Cumulatively, these taxa contributed approxi­
mately 51% for the differences between sampling zones on the shore of
Azenhas do Mar, and approximately 47% for the differences on the shore
of Porto das Barcas.

3.2. Groundwater effect on biological communities of the South Coast

shores

The structure of the macroinvertebrate communities was consis­

tently different between the discharge (D) and no-discharge (ND) zones
on the South coast for Olhos de Água (OA), Ferragudo (FER), and Praia
da Luz (PL) shores. The PCO analysis showed that approximately 79% of
the variation is explained by the discharge factor, meaning the samples
are clearly affected by the occurrence of freshwater discharge (Fig. 6).
Fig. 3. Average abundance (±S.E.) of taxa in Discharge and No-Discharge
zones in Azenhas do Mar shores on the Southwest coast of Portugal.
3.2.1. Abundance of species
In these study cases, the algae Enteromorpha sp., the limpet Patella
vulgata, and the barnacle Chthamalus sp. were the most abundant in the discharge and no-discharge sites was mainly explained by the contri­
discharge zones with a higher percentage of bare rock (Figs. 7–9). In bution of the algae Enteromorpha sp., the snail Melaraphe neritoides and
opposition, the taxa Osilinus lineatus, Melaraphe neritoides, and Siphonaria the lichen Verrucaria maura (Table 3 and Fig. 5). These three taxonomic
pectinata were less abundant in discharge zones. Conversely, the pre­ groups conjunctively explained approximately 44% of the difference in
dominant taxa in the no-discharge zones were the Chthamalus sp. and the the shore Olhos d’Água, 46% of the dissimilarity in Ferragudo, and 40%
lichen Verrucaria maura. of the difference in Praia da Luz. The limpet Patella vulgata was the least
contributing taxa to the average dissimilarity between the discharge and
3.2.2. Identification of key responsive taxa no-discharge zones on the three shores.
In the South study cases, the average dissimilarity between the

Fig. 2. PCO (Principal Coordinates analysis) plot based on Bray-Curtis resemblance matrix of the macroinvertebrate communities comparing Discharge and Non-
Discharge zones on the Southwest Coast shores.

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L.-L. Julián E et al. Marine Environmental Research 179 (2022) 105672

dynamics in locations elsewhere where groundwater discharges directly

into the rocky intertidal. It also signals that discharge patterns are
consistent at least within a full season’s cycle as specific slow-growing
taxa such as lichens had time to respond to groundwater influence.
On one hand, these results are in line with previous studies that have
also shown equivalent biological responses to the influence of ground­
water in other types of ecosystems such as sandy shores, sandy subtidal,
estuaries, and reefs. For example, Silva et al. (2012) reported a biolog­
ical response to a salinity gradient established by groundwater discharge
into the Arade river estuarine habitat. Kotwicki et al. (2013) provided
evidence that the discharge of groundwater has a clear effect on meio­
faunal assemblages in the shallow area of Puck Bay (Baltic Sea), re­
flected in a significant decline of certain meiofaunal taxa, as well as in
altered patterns of temporal distribution and small-scale (vertical)
zonation of meiofaunal assemblages. Similarly, Encarnação et al. (2015)
investigated the local and temporal variations in nearshore sandy
macrobenthic communities associated with submarine groundwater
discharges, finding that differences in community structure between
locations with and without the influence of groundwater discharge
occurred mainly during spring when the magnitude of groundwater
discharge was higher.
The groundwater influence can also extend beyond changes in
biodiversity and abundance patterns. Piló et al. (2018) revealed signif­
icant differences at the level of the structure of the benthic intertidal
community, area coverage, body size and ecophysiological condition of
the target epibenthic species between reference and groundwater
discharge sites, supporting the hypothesis that the morphological and
physiological responses of key intertidal mollusc species can be used to
detect the effects of groundwater discharge into coastal ecosystems.
Furthermore, Flores (2018) reported that the benthic algal and inver­
tebrate community structure was significantly related to spatial and
temporal dynamics of the delivery of groundwater discharge on two
subtidal reefs in the Maunalua Bay (Hawaii).
Fig. 4. Average abundance (±S.E.) of taxa in Discharge and No-Discharge On the other hand, our study is the first robustly proving that coastal
zones in Porto das Barcas shore on the Southwest coast of Portugal. groundwater discharge can be an important factor shaping the intertidal
rocky shore macroinvertebrate and algae communities across small
(within shores) and large spatial scales (regional scales); previous
Table 2 studies have focused on single locations. We showed that the algae
Relative and Cumulative Contribution of macroinvertebrate taxa to the dissim­
Enteromorpha sp. had increased abundance in groundwater-influenced
ilarity of samples in the Southwest study shores.
locations, whereas the opposite was verified for the periwinkle
Azenhas do Mar Porto das Barcas M. neritoides. These response patterns may have important cascading
Taxa Contrib Cum. Taxa Contrib Cum. associated shifts in their interspecific biotic relationships. Given that
% % % % competition for space is a shaping factor in intertidal communities
Enteromorpha sp. 21.7 21.7 Enteromorpha sp. 23.5 23.5 (Dayton, 1971), the fact that the above-mentioned algae and the lichen
(% cover) (% cover) occupy most space, potentially resulting in the displacement of other
Melaraphe 15.7 37.4 Melaraphe 11.9 35.4 species less tolerant of freshwater, altering the competing outcomes. In
neritoides neritoides
turn, this may have cascading effects on their interdependent prey and
Verrucaria maura 13.3 50.7 Verrucaria maura 11.5 46.9
(% cover) (% cover) predator species, hence altering habitat biodynamics and food webs,
Siphonaria 8.9 59.6 Siphonaria 11.3 58.1 similar to other coastal marine ecosystems such as seagrass beds (Schanz
pectinata pectinata et al., 2002). Concerning our study species, the fast-growing Enter­
Chthamalus sp. (% 7.8 67.4 Chthamalus sp. (% 8.9 67.1
omorpha algae are well established to cause widespread blooms and
cover) cover)
Bare rock (% 7.2 74.6 Bare rock (% 6.1 73.2
eutrophication (Sousa et al., 2007), hence in groundwater-influenced
cover) cover) locations, it may limit the space availability. In opposition, the peri­
Patella vulgata 5.6 80.2 Gibbula umbilicalis 6.1 79.3 winkle M. neritoides, a known bioeroder and important grazer in the
Fucus sp. (% 5.5 85.7 Patella vulgata 6.1 85.4 upper tidal zone (Palmer et al., 2003) may have diminished influence
cover)
due to lower salinity tolerance, hence likely contributing to algae
Gibbula umbilicalis 5.5 91.2 Fucus sp. (% 5.3 90.7
cover) overgrowth.
A bioindicator tool is useful in biodiversity monitoring programmes
in coastal zones and ecosystems. This approach is especially useful for
4. Discussion environmental assessments because it overcomes the limitations of
evaluating the system merely based on physical-chemical parameters,
Our study showed that the macroinvertebrate community is signifi­ which does not consider the longer-term consequences of environmental
cantly affected by direct groundwater discharge related to abundance alterations on biological communities. For example, Hwang et al. (2010)
patterns, not biodiversity. The consistency of the biological response associated high shellfish farming productivity in an enclosed bay with
across all shores and regions signals that albeit this is a local scale the influence of nearby groundwater discharge-driven nutrients and
disturbance, it represents an important factor shaping the habitat stimulation of primary production. Dean (2008) also reported that

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L.-L. Julián E et al. Marine Environmental Research 179 (2022) 105672

Fig. 5. Percentage of the contribution of each taxon (and others) to the dissimilarity of samples for all factors. The vector lines represent the percentage of
contribution to the dissimilarity, therefore, the longer the vector the higher the contribution of each taxon to the dissimilarity of the samples.

Fig. 6. PCO (Principal Coordinates analysis) plot based on Bray-Curtis resem­

blance matrix of the macroinvertebrate communities comparing Discharge and
Non-Discharge zones in the South Coast shores.

numerous species of polychaetes have been identified as useful in­

dicators of various types of environmental pollutants (e.g. organic
enrichment, pesticides, and heavy metal) in the estuarine environment
of the Gulf of Nicoya, Costa Rica. Since the input of those pollutants can
be driven by groundwater discharge, shifts in polychaete communities
can be as changes in the quantity and/or quality of the groundwater
discharge. Assuming from our study that changes in quality and/or
quantity of groundwater will potentially result in changes in the
ecological configuration of interconnected systems, we particularly
suggest the algae Enteromorpha sp and the snail M. neritoides as useful
bioindicator taxa for monitoring programmes. Hence, when these taxa
are in high abundance, increased groundwater discharge is more likely.
Furthermore, consideration of biological communities’ response to
changes in groundwater discharge contributes to improving the under­
standing of climate change effects on coastal aquifers and associated Fig. 7. Average abundance (±S.E.) of taxa in Discharge and No-Discharge
ecosystems. The current tendencies of global change for Mediterranean zones in Olhos d’Água shore on the South coast of Portugal.
regions are increasing temperature and decreasing precipitation and a
likely decrease in groundwater levels due to a reduction in recharge
directly affect the structure of biological communities in the receiving
rates and increasing abstraction to supply anthropogenic demands
ecosystems, which, in turn, will affect the dynamics and functioning of
(Stigter et al., 2014; da Costa et al., 2020; Rachid et al., 2021). Hence,
those essential environmental services they provide. For example, a
this results in a lowering of the regional hydraulic gradient, which can
spring increase in the diversity of meiofauna when the magnitude of
affect the amount and distribution of groundwater discharge feeding
groundwater discharge was higher has already been documented for the
into coastal ecosystems. Consequently, the availability of freshwater can
‘Olhos d’Água submarine area (Encarnação et al., 2013).

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L.-L. Julián E et al. Marine Environmental Research 179 (2022) 105672

Fig. 8. Average abundance (±S.E.) of taxa in Discharge and No-Discharge Fig. 9. Average abundance (±S.E.) of taxon in Discharge and No-Discharge
zones in Ferragudo shore on the South coast of Portugal. zones in Praia da Luz shore on the South coast of Portugal.

The effects of groundwater discharge will likely vary with the

Table 3
chemical composition of the discharged water and the biological com­ Relative (RC) and Cumulative Contribution (CC) of macroinvertebrate taxa to
munities present in the areas where it enters (Garcia-Solsona et al., 2010 the dissimilarity of samples in the southern shores.
Flores, 2018; Robinson et al., 2018). Although the solutes associated
Olhos d’Água Ferragudo
with groundwater discharge vary with many factors including soil
characteristics, flow path and length, land use, recharge and discharge Taxa RC CC Taxa RC CC
% % % %
rates, and residence time (Flores, 2018), significant impacts on near­
shore biota have been observed at locations where groundwater Enteromorpha sp. (% 16.6 16.6 Verrucaria maura (% 17.2 17.2
cover) cover)
discharge was enriched with moderate to high levels of anthropogenic
Melaraphe neritoides 14.1 30.7 Enteromorpha sp. (% 15.1 32.3
nutrients. In Gamak Bay, Korea, driven nutrient fluxes driven by sub­ cover)
marine groundwater discharge were respectively 85–90% and 10–30% Verrucaria maura (% 13.7 44.4 Melaraphe neritoides 13.2 45.5
of the total input fluxes for dissolved inorganic nitrogen and dissolved cover)
inorganic phosphorous (Hwang et al., 2010). Amato et al. (2016) sug­ Osilinus lineatus 11.6 56.0 Chthamalus sp. (% 9.5 55.1
cover)
gest that fertilizer-derived nitrogen that is delivered to reefs via Siphonaria pectinata 9.5 65.5 Osilinus lineatus 9.5 64.6
groundwater discharge likely plays a major role in supporting the Chthamalus sp. (% 9.4 74.9 Siphonaria pectinata 9.1 73.6
growth and dominance of macroalgae at both Māʻalaea and Kūʻau Bays cover)
(Hawaii). Garcia-Solsona et al. (2010) demonstrated that inorganic ni­ Gibbula umbilicalis 6.7 81.7 Gibbula umbilicalis 8.0 81.6
Bare rock (% cover) 6.7 88.4 Bare rock (% cover) 7.1 88.7
trogen and silica fluxes alone are substantial enough to promote recur­
Patella vulgata 6.3 94.7 Patella vulgata 6.0 94.6
rent phytoplankton blooms observed in the Balearic Island of Menorca.
Donis et al. (2017) showed that silicate and phosphate supplied by Praia da Luz

groundwater discharge promoted a seep-site net community production Taxa RC% CC %

rate that is more than twice compared to adjacent non-seeping sites in Enteromorpha sp. (% cover) 15.2 15.2
sandy sediments of Hel Bight (Poland) in the shallow southern Baltic Melaraphe neritoides 12.6 27.7
Sea. Verrucaria maura (% cover) 12.6 40.3
Siphonaria pectinata 11.1 51.4
Chemical parameters were not measured in this study due to logistic
Bare rock (% cover) 9.2 60.5
constraints. However, anthropogenic pressures (e.g., agriculture, ur­ Chthamalus sp. (% cover) 8.6 69.1
banization, tourism) and altered nutrient concentrations were reported Osilinus lineatus 8.0 77.1
for aquifer systems in the study area (Stigter et al., 2006a,b; Fernandes Gibbula umbilicalis 7.5 84.7
et al., 2015; Rocha et al., 2016; Piló et al., 2018) suggest that the Patella vulgata 7.3 92.0

7
L.-L. Julián E et al. Marine Environmental Research 179 (2022) 105672

quantity and chemical composition of groundwater discharge has a Bussmann, I., Dando, P.R., Niven, S.J., Suess, E., 1999. Groundwater seepage in
themarine environment: role for massflux and bacterial activity. Mar. Ecol. Prog. Ser.
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5. Conclusions ecss.2011.01.019.
Chainho, P., Costa, J.L., Chaves, M.L., Lane, M.F., Dauer, D.M., Costa, M.J., 2006.
Seasonal and spatial patterns of distribution of subtidal benthic invertebrate
Our study fills an important gap in knowledge by providing missing
communities in the Mondego River, Portugal - a poikilohaline estuary.
information on the dynamics of intertidal communities under the in­ Hydrobiologia 555 (1), 59–74. https://doi.org/10.1007/s10750-005-1132-2.
fluence of direct coastal groundwater discharge across several spatial Clarke, K.R., Gorley, R.N., 2015. PRIMER V7: User Manual/Tutorial. PRIMER-E.
scales. The study showcases the importance of considering local scale Plymouth, p. 300.
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contribution, an expected variation due to climate change predictions. da Costa, L., Monteiro, J.P., Hugman, R., 2020. Assessing the use of harvested
greenhouse runoff for managed aquifer recharge to improve groundwater status in
Important cascading ecological effects are likely to occur in the affected South Portugal. Environ. Earth Sci. 79, 253. https://doi.org/10.1007/s12665-020-
biological community, particularly regarding competition for space. 09003-5.
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the groundwater discharge and understand the role of spatial-temporal
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heterogeneity across multiple scales. Replicated experiments over time Monogr. 41 (4), 351–389.
will also help to assess the evolution of benthic communities, therefore, Dean, H.K., 2008. The use of polychaetes (Annelida) as indicator species of marine
pollution : a review. Rev. Biol. Trop. 56 (Suppl. 4), 11–38.
opening the path to assess a potential groundwater dependency of these
Donis, D., Janssen, F., Liu, B., Wenzhöfer, F., Dellwig, O., Escher, P., Spitzy, A.,
coastal ecosystems. Böttcher, M.E., 2017. Biogeochemical impact of submarine ground water discharge
on coastal surface sands of the southern Baltic Sea. Estuar. Coast Shelf Sci. https://
doi.org/10.1016/j.ecss.2017.03.003. August 2018.
CRediT authorship contribution statement
Encarnação, J., Leitão, F., Range, P., Piló, D., Chícharo, M.A., Chícharo, L., 2013. The
influence of submarine groundwater discharges on subtidal meiofauna assemblages
Londoño-Londoño Julián E: Writing – original draft, Methodology, in south Portugal (Algarve). Estuar. Coast Shelf Sci. 130, 202–208.
Encarnação, J., Leitão, F., Range, P., Piló, D., Chícharo, M.A., Chícharo, L., 2015. Local
Formal analysis. Condesso de Melo: Writing – review & editing,
and temporal variations in nearshore macrobenthic communities associated with
Funding acquisition. A.C.F. Silva: Formal analysis, Resources, submarine groundwater discharges. Mar. Ecol. 36 (4), 926–941. https://doi.org/
Conceptualization, Visualization, Writing – review & editing. 10.1111/maec.12186.
Erostate, M., Huneau, F., Garel, E., Ghiotti, S., Vystavna, Y., Garrido, M., Pasqualini, V.,
2020. Groundwater-dependent ecosystems in coastal Mediterranean regions:
Declaration of competing interest characterization, challenges and management for their protection. In: Water
Research, vol. 172. https://doi.org/10.1016/j.watres.2019.115461.
Félix, P.M., Correia, M.J., Chainho, P., Costa, J.L., Chaves, M.L., Cruz, T., Castro, J.J.,
The authors declare the following financial interests/personal re­ Mirra, C., Domingos, I., Silva, A.C.F., Cancela da Fonseca, L., 2015. Impact of
lationships which may be considered as potential competing interests: freshwater inputs on the spatial structure of benthic macroinvertebrate communities
Londono-Londono, Julian E reports financial support was provided in two landlocked coastal lagoons. Hydrobiologia 758 (1), 197–209. https://doi.org/
10.1007/s10750-015-2290-5.
by European Comision. Fernandes, J., Carrara, G., Terrinha, P., Sousa, F., Leitão, F., Loureiro, M., Roque, C.,
Noiva, J., Boutov, D., Range, P., Dills, A., Almeida, C., 2015. Descargas do sistema
Acknowledgements aquífero Albufeira-Ribeira de Quarteira em meio marinho: métodos e cartografia.
Flores, F., 2018. The Effects of Submarine Groundwater Discharge on Tropical Reef
Benthic Community Composition, Structure, and Primary Productivity, p. 110.
We would like to thank the European Commission for funding a 2- Foster, S.S.D., Chilton, P.J., 2003. Groundwater: the processes and global significance of
year Erasmus Mundus scholarship for following the Joint Master De­ aquifer degradation. Philos. Trans. R Soc. Lond. B Biol. Sci. 358, 1957–1972. https://
doi.org/10.1098/rstb.2003.1380.
gree Programme on Groundwater and Global Change – Impacts and Garcia-Solsona, E., Garcia-Orellana, A.J., Masqué, A.P., Garcés, A.E., Radakovitch, A.O.,
Adaptation (acronym GroundwatCh), and the research center CERIS – Mayer, A.A., Estradé, A.S., Basterretxea, A.G., Garcia-Orellana, J., Masqué, Á.P.,
Civil Engineering Research and Innovation for Sustainability at the Civil Garcés, E., Radakovitch, O., Mayer, Á.A., Estradé, S., Basterretxea, G., 2010. An
assessment of karstic submarine groundwater and associated nutrient discharge to a
Engineering, Architecture and Georesources Department of Instituto Mediterranean coastal area (Balearic Islands, Spain) using radium isotopes. htt
Superior Técnico of Lisbon. The authors are grateful for the Foundation ps://doi.org/10.1007/s10533-009-9368-y, 97, 211-229.
for Science and Technology support through funding UIDB/04625/2020 Guerra, M.D., Ribeiro, R., Rodrigues, S., 2019. State of Environment Report Portugal.
Hugman, R., Stigter, T., Costa, L., Monteiro, J.P., 2017. Numerical modelling assessment
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