Marine Pollution Bulletin xxx (xxxx) xxxx

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Marine Pollution Bulletin

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

Assessment of seawater quality and bacteriological pollution of rocky shores

in the central coast of San Jorge Gulf (Patagonia, Argentina)
⁎
Romina N. Vergaa,b,c, , Javier A. Tolosanoa,c, Néstor J. Cazzanigad, Damián G. Gila,c
a
Instituto de Desarrollo Costero Dr. Héctor E. Zaixso, Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB), Comodoro Rivadavia, Ruta 1, km4 S/N, 9000,
Chubut, Argentina
b
CIT-Golfo San Jorge, UNPSJB, CONICET, Comodoro Rivadavia, Ruta 1, km4 S/N, 9000, Chubut, Argentina
c
Facultad de Ciencias Naturales y Ciencias de la Salud - UNPSJB, Comodoro Rivadavia, Ruta 1, km4 S/N, 9000, Chubut, Argentina
d
Departamento de Biología, Bioquímica y Farmacia, Universidad Nacional del Sur, San Juan 670, 8000 Bahía Blanca, Buenos Aires, Argentina

A R T I C LE I N FO A B S T R A C T

Keywords: We assessed seasonal and spatial variability of seawater quality and bacterial pollution in two sewage-impacted
Wastewater and two reference rocky shores in the area of Comodoro Rivadavia, the largest city in central Patagonia. Samples
Diffuse outfalls taken from winter 2015 to autumn 2017 at different intertidal levels showed that the impacted sites experienced
Benthos a decrease of salinity—more pronounced towards the autumn—, a slightly higher turbidity, the lowest values of
Health risks
dissolved oxygen, and significantly higher concentrations of nitrates throughout the year. They also were up to
Recreational areas
ten times above the legal limit of fecal indicator bacteria (FIB) for recreation and fishing areas. Enterococci
Shellfish picking
increased particularly during winter. All bacteriological indicators decreased markedly during spring. Principal
component analysis arranged the reference sites mostly by their higher salinity, and the impacted sites by
concentration of FIB, nitrates and phosphates. Impacted and reference sites overlapped towards lower levels,
where the explicative variables were more stable.

1. Introduction
Atlantic Patagonian coasts run along > 2,000 km, from 40° to 54° S,
with a very low population density: less than one million people in
more than twelve towns and cities. The general condition of apparent
wildness and pristine conditions is however threatened by human ac-
tivity. The extent of these impacts was seldom assessed in Patagonia,
especially in terms of seawater quality and bacteriological contamina-
tion.
Marine pollution is a global and complex problem. Chemical com-
pounds and pathogens are mostly introduced to the environment
through human activities, imposing several risks to biota, human health
and ecosystems (Weis, 2014; Kolm et al., 2018). Sewage contains a
diverse array of polluting agents including pathogens, organic sub-
stances, heavy metals, trace elements, and so on, which pose direct and
indirect effects on ecosystems and organisms (Islam and Tanaka, 2004;
Verlecar et al., 2006; Baršienė et al., 2008). In particular, discharges of
sewage into shallow coastal and subtidal environments may favor eu-
trophication processes, leading to deterioration of water and sediment
quality and finally may decrease or affect biodiversity, with related
ecological problems (Littler and Murray, 1975; Cabral-Oliveira et al.,
2014).
The discharge of wastewater into the coasts also provides a large
number of pathogens to the receiving waters increasing the risk of
health problems in coastal communities (Islam and Tanaka, 2004;
Stewart et al., 2011). Some pathogens commonly found in high con-
centrations in raw wastewater include Salmonella spp., Escherichia coli,
Streptococcus spp., Staphylococcus aureus, Pseudomonas aeruginosa, fungi
(Candida spp.), and enterovirus, hepatitis, poliomyelitis, influenza and
herpes viruses (Stewart et al., 2011; Lamparelli et al., 2015). These
pathogens are associated with gastrointestinal, skin, respiratory ill-
nesses, and urinary tract infections (Pruss, 1998; Stewart et al., 2011).
Different indicator levels identified as standards are used in coastal
marine water quality programs worldwide. The most common bacter-
iological indicators are total coliforms, fecal coliforms (FC), E. coli (EC)
— a subset of the FC group, which are most appropriate to indicate fecal
pollution from warm-blooded animals—, and enterococci (Ashbolt
et al., 2001; Noble et al., 2003). Although most strains of fecal indicator

⁎
Corresponding author at: Instituto de Desarrollo Costero Dr. Héctor E. Zaixso, Universidad Nacional de la Patagonia San Juan Bosco (UNPSJB), Comodoro
Rivadavia, Ruta 1, km4 S/N, 9000, Chubut, Argentina.
E-mail addresses: romynv@gmail.com (R.N. Verga), javiertolosano@gmail.com (J.A. Tolosano), ficazzan@criba.edu.ar (N.J. Cazzaniga),
gil_damian@hotmail.com (D.G. Gil).

https://doi.org/10.1016/j.marpolbul.2019.110749
Received 6 August 2019; Received in revised form 11 November 2019; Accepted 18 November 2019
0025-326X/ © 2019 Published by Elsevier Ltd.

Please cite this article as: Romina N. Verga, et al., Marine Pollution Bulletin, https://doi.org/10.1016/j.marpolbul.2019.110749
R.N. Verga, et al.
Fig. 1. General map showing the coast of San Jorge Gulf (Argentina) and the location of the studied sites. Sewage-impacted sites: El Puerto and Stella Maris; reference
sites: Punta Maqueda and La Tranquera.
bacteria are not pathogenic, their presence indicates fecal contamina-
tion and therefore a health risk, regardless whether or not specific pa-
thogens are found (Wu et al., 2011; USEPA, 2012).
The assessment of the sea water quality is thus essential for man-
agement of recreational water in coastal communities. Marine coastal
ecosystems in Argentinian Patagonia are highly productive (Torres
et al., 2018), and some of them have been exposed for years to the
effects of a disordered and accelerated demographic and industrial
growth (Raimondo, 2010; Baeza, 2014). The long-term effect of these
shortfalls can compromise human health and affect nearshore ecosys-
tems and the sustainable use of renewable natural resources. In parti-
cular, the coast of San Jorge Gulf presents several coastal fronts and a
great diversity of littoral habitats serving as areas of settlement, re-
production and nursery of important commercial species (e.g., king
crab Lithodes santolla, mussels Mytilus platensis, Aulacomya atra, red
octopus Enteroctopus megalocyathus) (Ré and Boschi, 1998; Vinuesa
et al., 2013; Zaixso et al., 2015). It is also an important area of re-
production, feeding and nursery of marine mammals (Retana and
Lewis, 2017), and as a feeding and resting area for migratory birds
(Yorio et al., 2010). In recent years this region has been chosen as a
strategic priority area of research within the framework of the Pampa
Azul Program of the Science and Technology Policy of Argentina for
marine conservation and commercial fishing (St-Onge and Ferreyra,
2018).
The central coast of the San Jorge gulf is the most populated area in
the Argentinian Patagonia (> 260,000 inhabitants) since the estab-
lishment of a large petrol based industry in the 1920s (Usach and
Freddo, 2015), but there is a poor information about coastal seawater
quality. The settlement and growth of the coastal cities of Comodoro
Rivadavia, Rada Tilly and Caleta Olivia have since increased in a dis-
ordered way on the coastline, and raised serious urban, socioeconomic
and environmental conflicts (Usach and Freddo, 2015). In this regard,
the presence of controlled and illegal coastal dumpsites along with
numerous effluents that release wastewater with no (or low secondary)
treatment are just a few of these environmental problems (Pérez, 2002;
Raimondo, 2010; Usach and Freddo, 2015). In particular, sewage out-
falls in Comodoro Rivadavia are usually complex (i.e., a mixture of
sewage, rainwater and industrial effluents), and sewage facilities (e.g.,
drainage tubes, emissaries) do not present an adequate maintenance, so
2
Marine Pollution Bulletin xxx (xxxx) xxxx
they produce a diffuse, not punctual discharge at different heights of
the intertidal shore (Pérez, 2002; Raimondo, 2010).
Although some grossly-polluted sites are banned for recreational use
during summer, some zones near sewage effluents are still chosen
throughout the year for recreation or for shellfish extraction and fishing
posing a health risk to local residents. The presence of different strains
of bacteriological pathogens and their survival in laboratory conditions
were previously examined on a few sites (Pucci et al., 2009; Acuña
et al., 2011). However, the temporal and spatial variation of coastal
seawater quality and their bacteriological levels have not been yet
considered. Moreover, sea water pollution across contrasting intertidal
shore levels in sewage-impacted sites has not been even evaluated.
Intertidal platform in the Argentinian Patagonia are characterized by
wide rock platforms of gently slopes and thus provide a good region to
explore within site variation across a shore-level gradient.
The aim of this study was to examine the seawater quality and
bacteriological pollution in rocky shores of San Jorge Gulf in Patagonia,
Argentina, and explore its seasonal and spatial variability between
multiple sites and shore zones. Besides, baseline data are essential for
effective monitoring and provide information for management systems
and public health organizations.
2. Materials and methods
2.1. Study area
The study was done in the central coast of the San Jorge Gulf, which
is a large (39,340 km2) semicircular basin that extends from Dos Bahías
Cape (45° S) to Tres Puntas Cape (47° S) (Matano and Palma, 2015). We
selected four rocky shores, two of which are sewage-impacted—El
Puerto (PT: 45°52′S, 67°28′W) and Stella Maris (SM: 45°53′S,
67°30′W)—and two sites were taken as reference—La Tranquera (LT:
46°02′S, 67°36′W) and Punta Maqueda (MQ: 46°01′S, 67°36′W) (Fig. 1).
All study locations have rather similar environmental conditions
regarding orientation (E), wave exposure (exposed to semiexposed),
and a semi-diurnal tide regime of 6.18 and 4.34 m as maximum and
average amplitude, respectively. The substrate is composed of sedi-
mentary rock from the Patagonia Formation, consisting of compacted
sandstones with fossil oyster beds (Sylwan, 2001; Kokot, 2015).
R.N. Verga, et al.
Intertidal platforms are extensive during low tides (~200–300 m) and
have a gentle slope with numerous shallow tide pools, especially in SM
and MQ (Gil et al., 2018). All sites are characterized by the presence
and dominance of the southern ecosystem engineer mussel Perumytilus
purpuratus in the mid-littoral zone and coralline turfs (Corallina offici-
nalis) towards the infralittoral fringe (Liuzzi and López Gappa, 2008;
Zaixso et al., 2015). The intertidal region is considered one the most
physically demanding rocky intertidal shores due to the action of strong
and persistent dry winds producing high desiccation rates (Palma et al.,
2004; Bertness et al., 2006). There are no significant freshwater dis-
charges from rivers in the region (Louge et al., 2004). The climate is
arid to semi-arid with scarce rainfall (~240 mm year−1; Argentina,
SMN, 2018).
Both reference sites are poorly accessible to the local population and
away from urbanized areas (~ 18 km), so they have few visitors
throughout the year. None of the reference sites is urbanized or has
effluent discharges. In both impacted sites, domestic wastewater, urban
runoff and rainwater are collected and conveyed to the coast by a sewer
system that is directly released into the intertidal. The discharge of
storm water in the study area is reduced due to the semi-arid conditions
of the region. Outfalls have an extension of 1–70 m along the intertidal
shore and are immersed only during high tides. There is no treatment of
the wastewater and the sewage pipelines are poorly maintained, so they
show many punctures producing a diffuse leakage of sewage from high
intertidal to midlittoral levels. Both sites are immediately close to ur-
banized area (i.e., downtown and other commercial areas) and are
frequently used for recreational fishing and other outdoor activities.
2.2. Water sampling and microbiological analysis
Seawater samples were seasonally collected between July 2015
(austral winter) and April 2017 (autumn) at different shore levels (total
n = 111). Surface water samples were simultaneously taken at the
moment of mean low tide (MLW) in shallow tide pools (20–30 cm deep)
to standardize measurements. The shore level (height, m) of each
sample was estimated using tide tables (Argentina, SHN, 2015-2016).
Sampling across the four sites were done simultaneously when possible
or at consecutive days, avoiding rainfall periods.
Water samples for physicochemical (turbidity, phosphates, nitrates,
pH, dissolved oxygen) and bacteriological variables (total coliforms,
Enterococci, and E. coli) were collected using conventional methods,
kept chilled during transportation and analyzed within 8 h. In addition,
seawater temperature, conductivity, total dissolved solids (TDS) and
salinity (ppt) were recorded using a multiparameter probe YSI 556.
At the laboratory, turbidity was determined by the nephelometric
method (2130 B), nitrates according to the protocol (4500-NO3, B), and
phosphates were determined by the stannous chloride procedure (4500-
P D). Dissolved oxygen samples were fixed in the field by addition of
1 mL of MnSO4 solution, then 1 mL of alkali-iodide-azide reagent and
evaluated according to the azide modification of the Winkler method
(4500-O C). Concentrations of total coliforms (TC), E. coli (EC) and
Enterococci (ENT) bacteria were analyzed by the analytical method and
the results are expressed as most probable number per 100 mL (MPN
100 mL−1) according to APHA (1995).
Table 1
Two-way ANOVA on effects of site and season on physicochemical variables.
Nitratesa Salinity
df F p df F p
Season (Se) 3 19.19 < 0.01 3 7.39 < 0.01
Site (Si) 3 16.65 < 0.01 3 11.43 < 0.01
Se × Si 9 5.07 < 0.01 9 1.58 0.134
Error 87 95
a
Log-transformed variable.
Marine Pollution Bulletin xxx (xxxx) xxxx
Results for each bacterial indicator were compared to the legal
limits for recreational use of marine water (EC: 126 CFU 100 mL−1,
ENT: 35 CFU 100 mL−1) and shellfish harvesting areas for human
consumption (TC: 77 CFU 100 mL−1) (WHO, 2003; Lee et al., 2010; US
EPA, 2012; Argentina, Ministerio de Salud, 2016).
2.3. Data analysis
Two-way analysis of variance (ANOVA) was used to examine the
effect of the season and site on selected physicochemical variables
(turbidity, nitrates, phosphates, salinity and dissolved oxygen). Tukey-
Kramer post hoc test were assessed for multiple mean comparisons.
Assumptions of normality and homogeneity of variance were tested
using the Shapiro–Wilk and Levene's tests, respectively and log trans-
formations were made when necessary (Sokal and Rohlf, 2012).
Bacteriological pollution indicators (TC, EC, ENT) at each season
and site were expressed as geometric means and were compared to
thresholds established for recreational use according to international
guidelines and national legislation (WHO, 2003; Argentina, Ministerio
de Salud, 2016), and international norms for shellfish harvesting (Lee
et al., 2010).
To explore the variation of seawater quality among shore zones, the
tidal level (m) of each sample were categorized into four ordinal shore
level zones: high-midlittoral (Hi-ML, 3.8–5.3 m), mid-midlittoral (Md-
ML, 2.4–3.8 m), low-midlittoral (Lw-ML, 0.9–2.4 m) and high infra-
littoral fringe (Hi-IF: 0.9–0.2 m). Principal component analyses (PCA)
were subsequently performed at each shore zone, using Euclidean dis-
tance after normalization of the variables (Legendre and Legendre,
2012). Bacteriological indicators and turbidity data were previously
log-transformed to reduce heteroscedasticity after inspection of
draftsman plots. The concentration of E. coli was not included in the
analysis due to its high collinearity (r > 0.80) with other bacter-
iological variables. The statistical analyses were done using the soft-
ware STATISTICA 8.0 for Windows and PRIMER 6 (Clarke and Gorley,
2006). We assume a significance level of 0.05 throughout the study.
3. Results
3.1. Spatial and seasonal variation
Mean highest temperature was recorded during summer
(13.4 ± 0.5 °C; ± SE), while lowest mean temperature occurred in
winter (8.2 ± 0.18 °C). The pH showed an irregular pattern among
sites and seasons, ranging from neutral to slightly alkaline values
(7.26–8.91) and no significant effects were found between sites and
seasons (ANOVA, p > 0.05). A similar situation was detected for TDS
values with oscillations between 32.84 and 35.42 g L−1 with highest
values observed at the impacted sites.
Salinity ranged between 33.0 and 35.4 ppt, and decreased sig-
nificantly at impacted sites (Table 1); the most severe decrease was
recorded at PT (p < 0.05). Higher salinity levels were registered for
the reference site LT (Fig. 2). Seasonal effects showed lower overall
mean values towards autumn, where the lowest values were registered
at impacted sites (Fig. 2). Dissolved oxygen was significantly lower
Phosphatesa Turbiditya Dissolved oxygena
df F p df F p df F p
3 6.13 < 0.01 3 2.35 0.078 3 8.48 < 0.01
3 8.66 < 0.01 3 4.92 < 0.01 3 1.79 0.154
9 1.96 0.053 9 0.20 0.994 9 1.37 0.214
87 91 95
3
R.N. Verga, et al.
Fig. 2. Seasonal variation of physico-chemical variables (mean ± SE) in the
central coast of San Jorge Gulf. Reference sites: LT (La Tranquera) and MQ
(Punta Maqueda); sewage-impacted sites: PT (El Puerto) and SM (Stella Maris).
during spring and summer at all sites (Table 1; Fig. 2). Although there
was no significant effect of sewage exposure on mean values of DO, the
lowest values were recorded at SM during summer (7.47 ± 1.1 mg
L−1). Mean values of turbidity varied significantly only between sites
(Table 1). Impacted sites showed higher levels of turbidity than re-
ference sites throughout the year. However, only SM presented sig-
nificant differences with the reference sites (Tukey, p < 0.05).
Nitrate concentrations were significantly higher at impacted sites as
compared to reference sites across all seasons, with the exception of
autumn (interaction term, Table 1; Fig. 2). Overall nitrate mean values
were particularly higher during winter and showed a clear dis-
crimination between sites (Tukey test, p < 0.05; Fig. 2). The lowest
mean concentration was registered for the reference sites during spring
4
Marine Pollution Bulletin xxx (xxxx) xxxx
Fig. 3. Seasonal variation of bacteriological indicators (MPN 100 mL−1) ex-
pressed as geometric means ( ± SE) (logged scale). Horizontal lines represent
legal limits of total coliforms for mollusc extraction for human consumption
(77 CFU 100 mL−1 and the legal limit of Escherichia coli (126 CFU 100 mL−1)
and Enterococci (35 CFU 100 mL−1) for recreational marine water. Reference
sites: LT (La Tranquera) and MQ (Punta Maqueda); sewage-impacted sites: PT
(El Puerto) and SM (Stella Maris).
(MQ: 1.6 ± 0.1 (SE) mg L−1). Phosphate mean concentration showed
significant differences between sites and seasons (Table 1). The im-
pacted site PT showed significant higher values (< 0.04–0.09 ppm)
throughout the year, as compared to the reference sites
(< 0.04–0.05 ppm). In particular, higher values and variations were
detected during summer in both impacted sites (> 0.09 ppm; Fig. 2).
3.2. Bacteriological indicators
Geometrical means (GM) of the concentration of three indicator
bacteria are shown in Fig. 3. Sites influenced by sewage showed high
values of bacteriological indicators that were above maximum
threshold for recreational use and shellfish extraction (Fig. 3). A slight
departure on this pattern was detected at EC and ENT levels during
spring, where GM concentrations were below the legal limit (Fig. 3). All
reference sites, by contrast, were below the legal limits in all seasons,
with the exception of LT in summer, where Enterococci concentration
was high (74 MPN 100 mL−1). A seasonal variation was clearly ob-
served mainly due to an increase of Enterococci during winter and a
marked decrease of all bacteriological indicators during spring.
3.3. Influence of shore zone
First principal component (PC1) clearly discriminated impacted and
reference sites at all shore zones (Fig. 4); correlation factor loadings for
each PCA are shown in Table 2. A general scheme was observed across
all shore zones: reference sites were mostly on the left characterized by
higher salinity concentrations, while the sewage-impacted sites located
to the right. The concentrations of bacteriological indicators, nitrates,
and to a lesser extent phosphate were higher near the sewage
R.N. Verga, et al.
Fig. 4. Principal Component Analysis (PCA) at different intertidal shore levels.
Explanatory variables: Temp (Temperature), Turb (Turbidity), EC (Escherichia
coli), ENT (Enterococci), DO (dissolved oxygen), Sal (salinity), NO3 (nitrates),
PO4 (phosphates). Reference sites: LT (La Tranquera) and MQ (Punta
Maqueda); sewage-impacted sites: PT (El Puerto) and SM (Stella Maris). Hi-ML:
high-midlittoral; Md-ML: mid-midlittoral; Lw-ML: low-midlittoral; Hi-IF: high
infralittoral fringe.
5
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discharges. The second principal component axis (PC2) seems to dis-
criminate samples on a temporal basis (i.e., by the influence of seawater
temperature). A negative correlation between seawater temperature
and dissolved oxygen was also prevalent in each PCA.
Variations on this overall pattern between shore zones were also
observed. These two groups were clearly discriminated in the Hi-ML
zone with no superposition of the polygon areas (Fig. 4). The first two
axes of the PCA explained 57.8% of the variability. Higher values of
bacteriological indicators (E. coli and Enterococci), turbidity, and in a
lesser extent nutrients were positively related to sewage-impacted sites
and negatively associated with the increase of salinity. The first two
axes of PCA for Md-ML explained 53.8% of the variability, with a slight
overlap between impacted and reference sites. Nevertheless, impacted
and reference sites were clearly disjointed. A similar pattern was ob-
served in the Lw-ML level (57.3% explained variance) although an in-
creased overlap between groups was evident. In this level, the phos-
phate strongly contributed to the differentiation between impact and
reference sites. In the case of Hi-IF levels (47.8% explained variance),
impacted sites were placed more towards the center of the axis, as an
outcome of their higher stability in about all the explicative variables.
However, concentrations of bacteriological indicators and nitrate were
still higher than at reference sites. In this level, SM showed the highest
variability.
4. Discussion
Our study is the first assessment of seawater quality that integrates
physicochemical and bacteriological data in the most populated coastal
area of the Argentinian Patagonia. Since coastal ecosystem services are
vulnerable to pollution, baseline information and monitoring is im-
portant to evaluate the degree of environmental alteration and possible
cascading effects on human health (Costanza et al., 1997; Von Glasow
et al., 2013). Small changes at large scales and large changes at small
scales may dramatically alter aquatic ecosystems, impacting on the
benefits and costs of human welfare (Costanza et al., 1997; Barbier,
2012). Urbanized coastline areas of Patagonia are no longer pristine
and are affected by environmental global problems (e.g., introduction
of species, overfishing, climate change) and poor coastal management
(e.g., sewage discharges, coastal urbanization) (Díaz et al., 2002;
Orensanz et al., 2002).
Despite the concern on organic pollution in marine coastal en-
vironments, the effect of domestic or urban effluents on seawater
quality of the Patagonian coast was seldom analyzed; most of such
studies in the Argentinian seashores were related to localities in the
province of Buenos Aires, which have a different demographic and
oceanographic condition (Pierini et al., 2008, 2012; Streitenberger and
Baldini, 2010; Becherucci et al., 2018). Few studies on sewage con-
tamination of Patagonian seawater focused in Nuevo Gulf (Torres et al.,
2004; Gil et al., 2005) and Ushuaia (Torres et al., 2009; Gil et al., 2011),
i.e., two important centers of tourist attraction with a significant sea-
sonality and a mean stay of 4.5 days (Puerto Madryn, Municipalidad,
2019) or 2.55 days (Ushuaia, Municipalidad, 2019), but with a per-
manent population much smaller than that of the center of the San
Jorge gulf. Seawater quality at rocky shores in the area of Comodoro
Rivadavia, the largest city in central Patagonia (> 260,000 in-
habitants), is noticeably impacted by the permanent disposal of non-
treated sewage, affecting both physicochemical and bacteriological
variables, with some degree of seasonal spatial and temporal variation
as shown in this study.
Seawater quality of impacted sites generally showed a reduction of
salinity, higher values of nutrients (nitrates and phosphates) and tur-
bidity. Low salinity values were expectable due to the disposal of fresh
and run-off waters through the sewage system. The reduction of salinity
was even more severe during the austral autumn at the impacted sites
indicating a strong contribution of rainwater collected by the sewage
system during this season. In this semi-arid region rainfalls accumulate
R.N. Verga, et al. Marine Pollution Bulletin xxx (xxxx) xxxx

Table 2
Factor loadings from PCAs of seawater quality variables at each shore level. Hi-ML: high-midlittoral; Md-ML: mid-midlittoral; Lw-ML: low-midlittoral; Hi-IF: high
infralittoral fringe.
Variable Hi-ML Md-ML Lw-ML Hi-IF

PC1 PC2 PC1 PC2 PC1 PC2 PC1 PC2

Turbidity 0.285 0.096 0.328 −0.129 0.405 0.054 0.114 0.515

Nitrate 0.339 −0.270 0.384 −0.433 0.274 −0.519 0.330 −0.183
Phosphate 0.248 0.534 0.251 0.440 0.457 0.115 0.149 −0.353
Escherichia coli 0.573 −0.048 0.589 0.167 0.516 −0.131 0.639 0.007
Enterococci 0.559 −0.043 0.505 0.143 0.408 −0.044 0.549 −0.137
Temperature 0.073 0.591 −0.083 0.574 0.171 0.631 0.054 −0.519
Salinity −0.302 0.093 −0.245 −0.117 −0.288 −0.001 −0.373 −0.348
DO 0.061 −0.521 0.116 −0.459 −0.083 −0.545 0.058 0.409
Eigenvalues 2.77 1.85 2.42 1.89 2.86 1.72 2.2 1.62
Variation (%) 34.6 23.2 30.2 23.6 35.8 21.5 27.5 20.3
Cumulative 34.6 57.8 30.2 53.8 35.8 57.3 27.5 47.8

mainly on March–April (autumn; Argentina, SMN, 2018). Since Co-
modoro Rivadavia city has a fragmented and dispersed urban extension
of nearly 100 km2, sewage and drain systems strongly concentrate in
the monitored areas. An insufficient dilution of the wastewater in sea-
water allows a greater survival of the fecal indicator bacteria (Darakas
et al., 2009).
Nutrient concentrations are also a good indicator of water quality
relative to sewage pollution and although other non-sewage watershed
sources are known to affect nutrient concentrations (Abaya et al.,
2018), the arid climate of the region suggests that sewage discharges
are the major source of nutrient input to the impacted sites. A seasonal
pattern of nutrient enrichment (nitrates and phosphates) is not clear, as
high values of nutrients were recorded throughout the year; between-
site variation instead occurred. Although higher values of nitrates were
detected during summer at impacted sites, there was not a clear sea-
sonal peak value. A decrease of dissolved oxygen was expected at im-
pacted sites as recorded for other polluted sites (Bonsdorff et al., 1997;
Braga et al., 2000; Cloern, 2001). However, in our study dissolved
oxygen did not show a significant difference between impacted and
reference sites, although lowest values were found during summer at
some impacted sites, suggesting some temperature-dependent effect.
The absence of a clear site effect, even at high shore levels, could be
attributed to the semi-exposed condition of rocky shores and high en-
vironmental and biological heterogeneity (e.g. influence of seaweeds).
Ryther and Dunstan (1971) observed that the available nitrogen
from the center of high pollution within the New York bight seems to be
used by microorganisms as quickly as it becomes available, but a
phosphate surplus is carried seaward and distributed throughout the
continental shelf; therefore phosphate is persistent where other pro-
ducts of organic decomposition, such as nitrogenous compounds, al-
ready disappeared from the environment. In our study, it is likely that a
similar event was occurring at the impacted sites, obscuring the sea-
sonal relationships between nitrates and phosphates; however, the
significant correlation found at the lowest level of the intertidal zone
suggests a reduction of the bacteriological load. The presence of benthic
autotrophs (macroalgae, microalgae and cyanobacteria) and wave ac-
tion on the lower shore of rocky shores could have contributed for this
effect.
The global problem of eutrophication requires well-planned and
efficient management strategies. Increase in nutrient inputs to coastal
marine systems of little circulation such as estuaries or bays can trigger
that process (Islam and Tanaka, 2004; Muniz et al., 2013; Kucuksezgin
et al., 2019). Although our study sites are on semi-exposed rocky shores
that could prevent large eutrophication events, significant temporal and
spatial small-scale effects could occur (Cloern, 2001).
Continuous discharge of urban effluents with no treatment over
nearshore ecosystems permanently contributes to microbial con-
tamination. Several studies demonstrated a relationship between
infectious disease rates and the abundance of E. coli and intestinal en-
terococci in the aquatic environments (Liberatore et al., 2015; Lušić
et al., 2017; Abaya et al., 2018). The beaches here studied are usually
banned for recreational uses during summer, but inhabitants of the city
still use them for fishing and edible shellfish picking (bivalves, limpets,
octopuses) throughout the year. We have detected geometric mean
values of bacteriological contaminations up to ten times higher than the
legal limit permitted for both recreational use of marine water (WHO,
2003; Argentina, Ministerio de Salud, 2016) and shellfish harvesting
areas (Lee et al., 2010) most of the year, with the exception of spring.
Several studies have shown that fecal bacteria, including human pa-
thogens, can accumulate and persist in clams, mussels, oysters, and
other sessile filtering feeders inhabiting the benthic environment (Kay
et al., 2008; Stewart et al., 2008; Roslev et al., 2009).
High levels of enterococci were detected in summer at the reference
site La Tranquera (LT), where fecal contamination is not attributable to
direct sewage. However, fecal indicator bacteria can be also found in
feces of animals like seabirds (Alderisio and DeLuca, 1999; Fogarty
et al., 2003), their fecal droppings having been occasionally observed in
large amounts on the shoreline of LT (R. N. Verga, pers. obs.). More-
over, enterococci have high persistence without multiplication in the
marine environment (Ashbolt et al., 2001; Kaper et al., 2004). High
levels of enterococci are also known to be related with human recrea-
tion activities (Fogarty et al., 2003; Wang et al., 2010) and, even though
our reference sites do not show a high influx of people, this potential
source cannot be disregarded. Further studies should typify the bac-
teriological strains and identify the presence of strains associated with
specific pathologies, such as antibiotic-resistant bacteria, a health issue
that is gaining more attention in coastal environments (Vignesh et al.,
2012; Leonard et al., 2018; O'Flaherty et al., 2019).
Variations of physico-chemical proprieties of water quality and
bacteriological indicators along a gradient of intertidal height suggest a
relatively low diffusion of the pollutants to the depth. The impacted
sites have mixed origin emissaries discharging directly into the high-
midlittoral coastline, while others extend to intermediate levels. This
contributes to a major level of disturbance and variation at higher shore
levels, and a more diluted effect towards lower levels. However, sea-
water quality in the infralittoral fringe (e.g., below waterline during
low tides) also showed evidence of bacteriological pollution at the
impacted sites. Since this particular zone is commonly used by local
fisherman to extract shellfish, an actual health risk may exist in that
area.
Comodoro Rivadavia city has a large number of non-point sources of
contamination of significant concern with respect to transport of pa-
thogens and their indicators into the marine environment. This type of
pollution is generally diffuse, intermittent, and occurs through an in-
direct route. Such non-point sources include runoff from urban areas,
leaking from septic systems and sewerage lines, combined with sewer

6
R.N. Verga, et al.
overflows and atmospheric deposition of aerosols (Stewart et al., 2008).
This study evidences that seawater quality is highly disturbed in the
urban coastal area of central Patagonia. It is clear that beaches with an
impact due to pollution from urban effluents show greater variability in
environmental characteristics, which could interact negatively along
the intertidal gradient where abiotic factors are more extreme on higher
shore levels. The continuous intake of organic matter and fresh water to
the intertidal fringe could be affecting the benthic communities in-
habiting the rocky coasts as observed in other intertidal systems (López
Gappa et al., 1990; Elías et al., 2003; Cabral-Oliveira et al., 2014).
The release of raw sewage into the marine environment not only has
adverse impacts on the environment and may pose health risks but it
also constitutes a non-sustainable management of freshwater resources
in the semi-arid region of Patagonia. Wastewater treatment plants are
not widespread in Argentina, as only 35% of the produced wastewater
(1.3 km3) is treated; the rest is discharged directly into rivers and seas
(FAO, 2014). In particular, only a few cities along the Atlantic coast of
Patagonia (e.g., Luis Piedra Buena, Puerto Pirámides, Puerto Madryn
and to a lesser extent Rada Tilly and Trelew) have got partial waste-
water treatment systems for irrigation use (Faleschini and Esteves,
2017). When sewage is framed as a waste and not as a resource, it is
expected to generate costs and the conventional linear end-of-pipe so-
lution becomes the usual way to manage it (Öberg et al., 2014). We
consider it necessary to have a sustainable policy approach to improve
the management of coastal areas, especially in highly urbanized coastal
areas of San Jorge Gulf.
Therefore, since the incidence of pollution on intertidal platforms is
an important ecological problem and a public health risk, this con-
tribution gives the first baseline data and reasons for further environ-
mental monitoring work in case of either construction of new offshore
outfalls or future implementation of treatment plants in Central
Patagonia.
Credit author statement
Romina N. Verga: Conceptualization, investigation, formal analysis,
Visualization, Writing - Original Draft.
Javier A. Tolosano: Resources, Project administration.
Néstor Cazzaniga: Writing - Review & Editing, Project administra-
tion.
Damián G. Gil: Conceptualization, Formal analysis, Visualization,
Writing - Review & Editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgments
We dedicate this manuscript to the memory of our friend and col-
league Dr. Hector E. Zaixso (1947-2015) who initiated this project
along with other related environmental studies in the Patagonian re-
gion. We especially thank Jorge Rubilar and Jorge Hernández
(Laboratorio de Aguas, Comodoro Rivadavia) for providing their ser-
vices and experience. We are also grateful to the staff of IDC-UNPSJB,
especially Julia Colombo, and the students Marina Epulef, Fernando
Contreras Barrientos, Juliana Giménez and Aldana Bustamante for the
their valuable help during fieldwork. We acknowledge two anonymous
reviewers for their constructive comments.
Funding
This work was supported by a Doctoral scholarship to R. Verga from
the Consejo Nacional de Investigaciones Científicas y Técnicas de
7
Marine Pollution Bulletin xxx (xxxx) xxxx
Argentina (CONICET, CIT Golfo San Jorge), and was partially funded by
Universidad Nacional de la Patagonia San Juan Bosco (Project UNPSJB
N°1259). Néstor J. Cazzaniga is a staff researcher at the Comisión de
Investigaciones Científicas de la Provincia de Buenos Aires, Argentina.
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