MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

https://doi.org/10.47193/mafis.3532022010901

ABSTRACT. Until 2014 Mar del Plata city discharged its untreated sewage effluents to the inter-

tidal sector. This city has a marked seasonality in the urban discharge, varying between 2.8 and 3.5

m3s-1 of effluents before/after summer. The effect on the intertidal benthic community was evalu-

ated in both spatially, in sewage-impacted and reference sites, and temporarily in both the short

term, before/after summer, and in long term along nine periods between 1997-2014. The bivalve

Brachidontes rodriguezii, the ecosystem engineer, reach the maximum dominance and frequency in

reference areas. Spatially the presence of opportunistic and tolerant species characterized the

impacted areas, while in reference sites sensitive species were prevalent. The opportunistic poly-

chaete species Capitella ‘capitata’ sp. and Alitta succinea were dominant near the sewage discharge

in firsts periods. In other periods the indicator species were Rhynchospio glutaea or Boccardia spp.

From 2008 the invader Boccardia proboscidea characterized the sewage-impacted sites building

massive reefs. The crustaceans Jassa falcata and Caprella sp. were very abundant at intermediate

distances from the sewage discharge, while Monocorophium insidiosum was very abundant in

sewage-impacted areas. The tolerant and opportunistic species are favored after the summer due to

the extra organic matter input. All community parameters showed lower values after the summer,

and also a trend to diminish along the studied period.

Key words: Epilithic community, macrobenthos, mussel bed, long term study, chronic and pulse

disturbance, tendency, SW Atlantic.

La respuesta de la comunidad epilítica intermareal natural e impactada por las aguas

residuales del Atlántico SO a pulsos (antes/después del verano) y descargas crónicas de aguas

residuales en el período 1997-2014

RESUMEN. Hasta 2014 la ciudad de Mar del Plata descargaba sus efluentes cloacales sin trata-

miento al sector intermareal. Esta ciudad tiene una marcada estacionalidad en sus descargas, varian-

do el caudal entre 2,8 a 3,5 m3s-1 antes/después del verano. El efecto sobre la comunidad bentónica

intermareal fue evaluado en la escala espacial, en sitios de referencia y sitios impactados, y también

temporalmente en el corto período de tiempo, antes/después del verano, y a lo largo de nueve perí-

odos entre 1997-2014. El bivalvo Brachidontes rodriguezii, el ingeniero ecosistémico, alcanza su

máxima dominancia y frecuencia en áreas de referencia. Espacialmente la presencia de especies

oportunistas y tolerantes caracterizó los sitios impactados, mientras que en sitios de referencia las

333

*Correspondence:

roelias@mdp.edu.ar

Received: 19 July 2021

Accepted: 21 December 2021

ISSN 2683-7595 (print)

ISSN 2683-7951 (online)

https://ojs.inidep.edu.ar

Journal of the Instituto Nacional de

Investigación y Desarrollo Pesquero

(INIDEP)

This work is licensed under a Creative

Commons Attribution-

NonCommercial-ShareAlike 4.0

International License

Marine and

Fishery Sciences

MAFIS

ORIGINAL RESEARCH

The response of the natural and sewage-impacted intertidal epilithic

community of the SW Atlantic to pulse (before/after summer) and chronic

sewage discharges in the 1997-2014 period

RODOLFO ELÍAS1, *, SEBASTIÁN E. SABATINI2and CONRADO DÁVILA3

1Instituto de Investigaciones Marinas y Costeras (IIMyC), Facultad de Ciencias Exactas y Naturales (FCEyN), Departamento de Ciencias

Marinas, Universidad Nacional de Mar del Plata (UNMdP) - Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). Grupo

Bioindicadores Bentónicos. Funes 3350, B7602AYL - Mar del Plata, Argentina. 2Departamento de Química Biológica, Facultad de Ciencias

Exactas y Naturales, Universidad de Buenos Aires (UBA), Instituto de Química Biológica (IQUIBICEN), Consejo Nacional de Investigaciones

Científicas y Técnicas (CONICET), Intendente Guiraldes 2160, Pabellón II, Ciudad Universitaria, C1428EHA - Buenos Aires, Argentina.

3Freelance researcher. ORCID Rodolfo Elías https://orcid.org/0000-0002-6113-6708

INTRODUCTION

Marine scientists have realized that the sea is

not an inexhaustible sink. The coastal areas first

and now huge ocean areas show that marine pol-

lution is global. Increasingly more or larger dead

zones deoxygenated seas and oceans due to the

discharge of untreated wastewater, which affects

marine ecosystems in an area of 245,000 km2,

with implications for fisheries, livelihoods and

food chains (WWAP 2017). Coastal ecosystems

are highly vulnerable to multiple environmental

human stressors e.g. urban and agricultural runoff

of pollutants and nutrients, habitat alteration,

aquaculture, fishing, acidification, etc. (Fabry et

al. 2008; Halpern et al. 2008).

The main source of organic pollution is associ-

ated with the discharge of sewage generated by

domestic effluents, being considered the oldest

form of pollution (Pearson and Rosenberg 1978;

Bishop et al. 2002; Medeiros and Bicego 2004;

Borja et al. 2006; Martins et al. 2008; Muniz et al.

2006, 2013). Domestic waters provide organic

and inorganic substances, including nutrients

(even those that have primary and secondary

treatment) that produce eutrophication that leads

to changes in structure and functioning of marine

ecosystems (Clarke and Warwick 2001; Gray et

al. 2002). Eutrophication, i.e. over-feeding the

aquatic environment by substances that induce

rapid algae growth (Nixon et al. 2009; Ferreira et

al. 2011). Nutrient loading in coastal waters may

have direct or indirect effects on the environment.

Some of the direct effects may be changes in

chlorophyll levels, in primary production, in

macro- and microalgae biomass and in the sedi-

mentation of organic matter. Indirect effects

include: changes in benthic biomass, benthic

community structure, habitat quality, water trans-

parency, increase in organically enriched sedi-

ments, changes in dissolved oxygen levels, mor-

tality of aquatic organisms, changes in food

chains, among others (Cloern 2001; Islam and

Tanaka 2004; Díaz and Rosenberg 2008).

One of the main challenges in environmental

impact assessment is to distinguish natural vari-

ability of natural communities of that variability

induced by human activities. To assess the quality

of the environment, and thus try to quantify the

damage that man does to the ecosystem, several

indices of environmental quality or ecological

indices are calculated. Many of these indicators

are based on benthic invertebrates because they

have little or no mobility, they form associations

that include species with a different degree of tol-

erance to stress, they respond to disturbances at

supra-specific levels, such as genera, families and

even classes, and finally because integrate the

recent history of disturbance (Warwick 1993;

Salas et al. 2006; Borja et al. 2008; Patricio et al.

2009; Dauvin et al. 2010; Muniz et al. 2013). The

underlying idea that supports the concept of a

biological indicator is that the selected organisms

or groups provide, express or integrate informa-

tion about their habitat. This can be shown

through the condition, presence/absence, relative

334 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

especies sensibles son prevalentes. En los primeros períodos el poliqueto oportunista Capitella “capitata” sp. fue dominante cerca de la

descarga cloacal, y también A. succinea. En períodos posteriores las especies indicadoras fueron Rhynchospio glutaea o Boccardia spp.

Desde 2008 el poliqueto invasor Boccardia proboscidea caracterizó los sitios impactados por la descarga por masivos arrecifes. Los crus-

táceos Jassa falcata y Caprella sp. fueron muy abundantes a distancias intermedias de la descarga, mientras que Monocorophium insi-

diosum fue muy abundante en el área impactada por la descarga cloacal. Las especies tolerantes u oportunistas se vieron favorecidas des-

pués del verano debido al aporte extra de materia orgánica. Todos los parámetros comunitarios mostraron valores menores después del

verano, y también se observa una tendencia a disminuir a lo largo de los períodos estudiados.

Palabras clave: Comunidad epilítica, macrobentos, banco de bivalvos, estudio de largo plazo, disturbio crónico y de pulso, tendencia,

Atlántico SO.

abundance or biomass, reproductive event, asso-

ciation structure (that is, composition and diversi-

ty), community function (such as trophic struc-

ture, or functional diversity) or any other combi-

nation of these characteristics (Muniz et al.

2013).

The city of Mar del Plata (38° S-57° W), in the

SW Atlantic, is the largest summer resort in

Argentina, receiving about 3 million people in

summer time (Bouvet et al. 2005). Although the

city has a functional submarine outfall since

2014, sewage water with only a pretreatment was

discharged directly into the coastline, 9 km from

the city center, for more than 30 years at a mean

rate of 2.8 m3sec-1 and up to 3.5 m3sec-1 in sum-

mer (Scagliola et al. 2006). Fisheries, factories

fishmeal, tourism, restaurants and textile indus-

tries are the main industrial activity in the city

and therefore are responsible for the supplement

large amounts of fat (12 t day-1 of industrial ori-

gin and 6 t day-1 of domestic origin) to urban

wastewater (Scagliola et al. 2006, 2011). The

abundance of fecal indicators (Enterococci 100

ml-1) showed risk to human health along 15 km of

beaches popular use (Comino et al. 2008; 2011).

The scorched mussel Brachidontes rodriguezii

(D’Orbigny, 1842), an ecosystem engineer

inhabits the intertidal hard substrates in large

areas of the SW Atlantic, including places with

sewage discharges. It is a species that has the

peculiarity of dominating natural rocky coasts

(Adami et al. 2004). Its community structure has

served as an indicator of sewage-impact in Mar

del Plata (Vallarino 2002; Jaubet 2013; Sánchez

2013; Llanos 2018). Although the short-term

response of polychaetes to increases in sewage

discharge during summer is partially known

(Elías et al. 2006), its temporal variation in rela-

tion to community, both in short and long term

periods, is unknown. In this context, the present

work describe the spatial-temporal dynamics of

the intertidal community in the period 1997-

2014, analyzing both impacted sites by sewage

(chronic) disturbance by the sewer discharge and

reference sites (not impacted), as well as the

community response to the events before/after

the summer, in response to the increase of the

sewage discharge (pulse disturbance).

MATERIALS AND METHODS

Study area

The coast of Mar del Plata city (Argentina

38° S-57° W) is dominated by sandy beaches, but

occasionally there are quarzitic outcrops and hor-

izontal abrasion platforms of consolidated loess

formed by silica-cement sandstones (Teruggi

1959; Isla and Ferrante 1997). The tidal regime is

regular and semidiurnal, with average heights of

60 cm in quadrature and up to 90 cm in high tides

of syzygy, but very subjected to weather condi-

tions. A strong littoral current (15 cm s-1) run

from South to North. During autumn-winter fre-

quent storms from the S-SE constantly affect the

coast (Manolidis and Alvarez 1994; Isla and Fer-

rante 1997). The climate is typically marine tem-

perate with regular rains (850 mm year-1). The

area is influenced by derived on advected waters

from the continental shelf (Subantarctic origin),

with temperatures between 8 and 21° C and salin-

ities between 33.3 and 33.8 (Guerrero and Piola

1997; Lucas et al. 2005). The present study was

carried out on one of these horizontal platforms,

which surrounds the sewage effluent of Mar del

Plata city. Similar substrates with similar ecolog-

ical conditions far from the influence of the

sewage were used as reference (or control) sites.

Environmental quality

From the intertidal sewage discharge a gradient

of environmental conditions was generated

towards the south (sampling zone) by the flume

dilution, which was function of the distance from

the outfall. Vallarino and Elías (2006) revealed

335

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

that salinity was almost constant in the area

(around 32-33), but occasionally in some seasons

(i.e. autumn-winter) lower values (26-30) were

recorded in closest sites to sewage discharge

(200-50 m). Dissolved oxygen showed mean val-

ues of 10 mg l-1 in reference site, but less than 7

mg l-1 at 50 m from the effluent. Values of pH

ranged 8.0 to 8.3 in reference site, but low near

the discharge (7.7 to 8.0). Turbidity was constant

in the reference site, reaching mean values of 50

NTU, while increasing to up to 300 NTU in sites

under the influence of sewage discharge, particu-

larly in the summer (see Vallarino and Elías

2006).

Total Organic Carbon (TOC) of the interstitial

sediment was elevated in patches surrounding the

effluent (1.5 to 2.0%), and decreased with dis-

tance and reference sites (mean of 0.5% at 1.000

m from the effluent and also in the Reference site).

Sediment accumulated among mussels also

showed an environmental gradient, being more

abundant in intermediate distances (20-50 kg m-2)

and lower in reference sites (between 20-30 kg m-2),

with a minimum in most near site to sewage site

(10-20 kg m-2).

From 1989-2014 the city’s sewage effluent was

discharged with only a pre-treatment over the

intertidal sector. The construction of the subma-

rine outfall lasted from 2008 to 2014. This includ-

ed a breakwater that alters the dynamics of the

sea by slowing the flux of littoral waters and the

rates of sedimentation around it. The intertidal

sewer stops in December 2014, when the current

submarine outfall was opened, which discharges

the city’s wastewater through 130 nozzles located

in the last section of 500 m long (between 3.9 and

4.4 km offshore).

Sampling design

Monitoring was carried out in three intertidal

areas with different distances from the sewage

outfall. Each area includes a set of three sampling

sites with different condition of organic contami-

nation (Figure 1). In the area called 1S, groups of

samples (12 to 36 sampling units of 78 cm2) were

taken between 50 and 200 m from the point of

discharge. In the area called 2S, groups of sam-

ples were taken between 1,000 and 1,200 m, both

south from the point of discharge and the so-

called Reference area (i.e. areas without sewage

influence) and in different sites between 18,000

to 6,000 m north from the sewer discharge.

Because differences between these ‘References’

were not statistically significant, values were

averaged in one area. For more information, see

Vallarino et al. (2002), Jaubet et al. (2013), and

Sánchez et al. (2013).

Studies lasted for almost 15 years, with differ-

ent objectives and therefore different sampling

designs. However, the constancy of sampling

impacted and reference sites and before/after

summer in 9 periods was maintained. The origi-

nal database includes more periods and different

seasonality (monthly, quarterly), but for the pres-

ent study the nine periods that have a before/after

summer were considered.

In each site, sampling units were taken in the

intertidal benthic community from different and

independent rocks. Each sample was fixed with

10% formalin. In laboratory the material was

washed and sieved through a 1 mm mesh size and

the retained biological material was identified to

the lesser taxonomic level, quantified, and pre-

served in 70% ethanol solution.

Environmental variables

Three 10 g samples of sediments were taken in

each site for determination of Total Organic Car-

bon (TOC) by the method of Walkley and Black

(1965) and expressed as percentage.

Data analysis

Factors analyzed were Sites (1S, 2S, Refer-

ence), Event (before/after summer), and Periods

(9).

336 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

From the similarity matrix with square root

transformation, a Permanova analysis was per-

formed considering Sites, Event (before/after

summer), and Periods (every before/after sum-

mer) as fixed factors. The Permanova analysis is

a multivariate ‘semiparametric’ test which esti-

mates parameters to adjust the distance matrix to

a lineal model (Anderson 2001). Values of p are

the result of permutations without normality sup-

positions, with characteristics of a free distribu-

tion test. Due to the existence of significant inter-

actions in the Permanova analyses interpretation

of results were conducted graphically.

The analysis of data included ordination by n-

MDS and Cluster using a similarity matrix using

the Bray-Curtis index with square root transfor-

mation to diminish the weight of dominant taxa.

In the n-MDS ordination the three sites were dis-

criminated by using different symbols. A cluster

diagram was superimposed showing the groups

corresponding to the factor Event (before/after

summer with different color). In the same graph,

the spearman correlation between sites and

species was added. Species were selected from a

Similarity Percentage (SIMPER) analyses, and

results for every group (Sites, Event) are present-

ed in an Appendix. This graph was made for each

of the 9 periods (with before/after sampling). For

the trend analysis an oversimplification was made

in a n-MDS by averaging the impacted sites (1S,

2S) in one, with averaged reference sites, result-

ing in 18 points (=samples) for impacted sites (9

before, 9 after) and 18 reference sites. This over-

simplification was, however, of little use in clari-

fying the spatial and temporal behavior of the

community. To improve the visualization a new

graph was made showing the course of the

impacted site and the reference site separately.

From the same matrix the following communi-

ty parameters were calculated: Richness (S),

337

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Figure 1. Sampling site. Area 1S is an average of sites located between 50-200 m south to the sewage effluent and Area 2S is an

average of sites located between 1,000-1,200 m to the south of the point of discharge. The Reference Area corresponds

to several reference sites (black circles). The white triangle is where the sewage discharges intertidally.

-56.835-58.865

-34.507

-36.537

-38.567

-62.925 -60.895 -56.835-58.865

.597

0 400

km

Mar del Plata

Buenos Aires

Province

-62.925 -60.895

-37.88

Santa Clara City

Playa Dorada

Mar de Cobo

Mar Chiquita

Reference Area

Eﬂuent

1S Area

2S Area

09

km

-37.88

-57.57

General

Pueyrredón

South America

Argentina

N

Abundance (N), Diversity (H’) and Evenness (J’).

These data were used to run a bi-factorial

ANOVA (with Sites-Periods, and Sites-Events as

fixed factors). Dominance was expressed as the

abundance of the species over the total abun-

dance, while Frequency was defined as percent of

sample with the species over the total of samples.

RESULTS

Percentage of Total Organic Carbon showed

significant differences among sites and periods

(Table 1). Frequently the sewage-impacted sites

showed the greatest values with a slight tendency

to diminish. In the Period 2008-2009 a great peak

of organic matter was evident in all sites, but in

particular in sewage-impacted ones. Although

values decrease, they remained higher compared

to previous periods (Figure 2).

Biological data

Total abundance, considering the 547 sampling

units analyzed, was 459,437 individual, from 95

taxa of macroinvertebrates. Only a few species

were constant and abundant (Appendix, Table

A1). Brachidontes rodriguezii, the ecosystem

engineer, reached maximum dominance (57%)

and frequency (84.6%). Among polychaetes, Syl-

lis prolixa Ehlers, 1901 was the most abundant

338 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

Figure 2. Organic matter from the three sampling Sites, from November 1977 to March 2014. Site 1S is the nearest to sewage

(50 m) and 2S is the farest (1,000 m). Reference sites were between 9 to 18 km north. Data modified from Llanos (2018).

Table 1. ANOVA of Total Organic Carbon (%) by sites and

periods. Data extended from November 1997 to

March 2014.

Effect SC df MS F P

Site 9.7 2 4.84 25.9 0.000*

Period 403.9 10 40.39 216.4 0.000*

Site*Period 51.0 20 2.55 13.7 0.000*

1S

2S

Referenc e

1997-1998

1998-1999

1999-2000

2000-2001

2001-2002

2003-2004

2004-2005

2008-2009

2013-2014

2009-2010

2011-2012

Organic matter (%)

6

5

4

3

2

1

0

Period

Site

species (4.5%), while in frequency S. gracilis

Grube, 1840 and S. prolixa were both very fre-

quent (76 and 70.9%, respectively). Boccardia

spp. reached 19 and 15% in dominance and fre-

quency, respectively, while Boccardia pro-

boscidea Hartman, 1940, the invader species, was

the second in dominance (19.2%) but with a low

frequency (15.4%).

Multivariate analysis

A permutational analysis was carried out (999

permutations), considering fixed factors: Sites

(1S, 2S, and Reference), Periods (9) and Event

(before/after Summer nested in Periods) (Table

2). Due to the existence of significant interac-

tions among all factors (Sites, Periods and

Event), the analyses cannot be interpreted but

can be analyzed graphically by n-MDS for each

period.

Ordination period-event

Period 1997-1998

The n-MDS (Figure 3 A) showed the Refer-

ence sites separated from those sewage-impacted.

Some sampling units of site 2S were grouped

near the Reference sites, mostly before summer.

The cluster (represented by the 59% similarity

line in the n-MDS) grouped sampling units from

before the summer at the top of the graph, while

those from after the summer were at the bottom.

Sampling units corresponding to the reference

sites were grouped by their affinity for each other

and kept at the top, unchanged by the summer.

The Simper analysis of the percentage of similar-

ity by Sites (Appendix, Table A2) showed B.

rodriguezii been dominant and important in the

Reference area, however decreased in 1S and 2S

reaching the third place in these groups. The crus-

taceans Jassa falcata (Montagu, 1808) and M.

insidiosum (Crawford, 1937) were more impor-

tant in groups 1S and 2S, as well as the poly-

chaete C. ‘capitata’ sp. On the other hand, the

Event (before/after summer) revealed higher

abundances before summer, nevertheless C. ‘cap-

itata’ sp. reached their maximum values after

summer (Appendix, Table A3).

Period 1998-1999

The n-MDS (Figure 3 B) showed most Refer-

ence sites grouped, with some 2S sampling units,

and most impacted sites (1S) and intermediate

sampling units (2S) in the opposite side. Group

before/after were grouped in the top and the bot-

ton of the graph, respectively. The Simper analy-

sis by sites (Appendix, Table A4) showed a great

mean abundance of B. rodriguezii respect the

precedent period and always remained dominant

in the reference site. The polychaetes Boccardia

spp., Capitella ‘capitata’ sp. and S. prolixa

Grube, 1840 were dominant, the first two in

sewage-impacted sites, while Syllis was in refer-

ence site.

Considering Events most species showed

decreasing values after summer, except the most

contributing species, B. rodriguezii and Syllis

prolixa (Appendix, Table A5).

Period 1999-2000

The n-MDS (Figure 3 C) showed sites more or

less separated according to sewage-impact,

339

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Table 2. Results of Permanova. Si: Sites, Pe: Period, Ev:

Event (nested in Period). In bold significant values.

Source fd SS MS Pseudo P

F (perm)

Si 2 1.26E + 05 63186 77.208 0.001

Pe 8 2.61E + 05 32604 39.839 0.001

Ev(Pe) 9 96942 10771 13.162 0.001

SixPe 16 1.95E + 05 12186 14.89 0.001

SixEv(Pe) 18 68098 3783.2 4.6228 0.001

Res 491 4.02E + 05 818.39

Total 544 1.19E + 06

340 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

Figure 3. n-MDS showing sampling units for different periods, separated by sites (sewage-impacted, 1S and 2S, and reference

site of before (white symbols) and after summer (black symbols). Green line also represents the similarity aggrupation

given by the cluster analysis as before/after summer response. Black circle and vectors correspond to the spearman cor-

relation between species (given by SIMPER) and sampling units. A) n-MDS showing sampling units of period 1997-

1998 separated by sites. Green line represents the 59% similarity aggrupation. B) n-MDS of sampling units by sites in

the Period 1998-1999. Green line represents the 57% similarity aggrupation. C) n-MDS in the Period 1999-2000 show-

ing reference site and sewage-impacted sites. Green line represents the 69% similarity aggrupation. D) n-MDS showing

sampling units in the period 2000-2001. Green line represents the 58% similarity aggrupation. E) n-MDS showing sam-

pling units in the period 2001-2002. Green line represents the 60% similarity aggrupation. F) n-MDS showing sampling

units in the period 2002-2003. Green line represents the 60% similarity aggrupation. G) The n-MDS by sites in the

Period 2005-2006. Green line represents the 60% similarity aggrupation. H) n-MDS by sites in the period 2008-2009.

Green line represents the 60% similarity aggrupation. I) n-MDS by sites in the period 2013-2014 showed two groups of

sampling units; one almost avoided of intertidal life in 1S (except to a few Boccardia proboscidea), and the rest of sam-

pling units. Green line represents the 60% similarity aggrupation.

2D Stress: 0.11

2D Stress: 0.14 2D Stress: 0.17

Capitella

‘’capitata sp.

Boccardia spp.

Jassa falcata

Brachidontes rodriguezii

Syllis prolixa

Capitella capitata‘ ’ sp.

Brachidontes rodriguezii

Boccardia spp.

Syllis prolixa

Jassa falcata

Leodamas uncinata

Monocorophium insidiosum

Capitella capitata‘ ’ sp.

Syllis prolixa

Brachidontes

rodriguezii

Boccardia spp.

Siphonaria

lessoni

2D Stress: 0.15

Monocorophium

insidiosum Capitella capitata‘ ’ sp.

Boccardia spp.

Jassa

falcata

Leodamas

uncinata

Syllis

prolixa

Caprella

dilatata

Brachidontes rodriguezii

A

EF

B

Similarity

57

Site and Event

1S before

2S before

Control before

1S after

2S after

Control after

Similarity

59

Site and Event

1S before

2S before

Control before

1S after

2S after

Control after

2D Stress: 0.15

Brachidontes rodriguezii

Syllis prolixa

Capitella

‘’capitata sp.

Siphonaria

lessoni

Boccardia spp.

2D Stress: 0.15

Brachidontes

rodriguezii

Syllis

prolixa

Monocorophium

Insidiosum

Capitella capitata‘ ’ sp.

Boccardia spp.

CD

Similarity

58

Site and Event

1S before

2S before

Control before

1S after

2S after

Control after

Similarity

69

Site and Event

1S before

2S before

Control before

1S after

2S after

Control after

Similarity

60

Site and Event

1S before

2S before

Control before

1S after

2S after

Control after

Similarity

60

Site and Event

1S before

2S before

Control before

1S after

2S after

Control after

except for 1S and 2S mixed, and the reference

site units that are apart. The groups at the bottom

of the graph represented those before summer,

while the upper groups were after summer. The

Simper analysis by Sites (Appendix, Table A6)

showed Brachidontes as the main species con-

tributing to differences among groups, with Boc-

cardia, Capitella and Siphonaria lessoni

Blainville, 1827 were dominant in sewage-

impacted groups, while S. prolixa was dominant

in the Reference site. In relation to factor Events

most species showed decreasing values (Appen-

dix, Table A7), except C. ‘capitata’ sp. and S.

gracilis.

Period 2000-2001

The n-MDS (Figure 3 D) showed a mixed pat-

tern of sampling units, without a clear pattern

about the potential gradient of sewage impact.

The pattern before/after is clearly observed in the

graph; sampling units before are in the left while

sampling units after are in the right, related to

high observed abundance of C. ‘capitata’ sp. The

Simper analysis by Sites (Appendix, Table A8)

showed the polychaetes S. prolixa and C. ‘capita-

ta’ sp. as the most contributing species in sewage-

impacted sites, whereas B. rodriguezii was in the

Reference site. Respect Events most species

showed decreasing values (Appendix, Table A9),

but C. ‘capitata’ sp. and S. gracilis.

Period 2001-2002

The n-MDS did not show a clear pattern (Fig-

ure 3 E). The pattern before/after was also

unclear, although the sampling units of 1S were

separated in two groups, corresponding to before

and after summer, and associate to them were the

polychaetes C. ‘capitata’ sp. and Boccardia spp.

The Simper by sites (Appendix, Table A10)

revealed B. rodriguezii and Caprella dilatata

341

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Figure 3. Continued.

2D Stress: 0.11

Brachidontes rodriguezii

Boccardia spp.

Syllis prolixa

Capitella capitata‘’sp.

Siphonaria lessoni

Rhynchospio glutea

Leodamas uncinata

2D Stress: 0.01

Brachidontes

rodriguezii

Syllis prolixa

Siphonaria lessoni

Boccardia proboscidea

GH

Similarity

60

Site and Event

1S before

2S before

Control before

1S after

2S after

Control after

Similarity

60

Site and Event

1S before

2S before

Control before

1S after

2S after

Control after

I2D Stress: 0.01

Brachidontes rodriguezii

Syllis prolixa

Siphonaria lessoni

Leodamas uncinata

Boccardia proboscidea

Similarity

60

Site and Event

1S before

2S before

Control before

1S after

2S after

Control after

Krøyer, 1843 as dominant species in the Refer-

ence site while impacted sites are dominated by

polychaetes like Boccardia and Capitella. In rela-

tion to Events most species showed decreasing

values (Appendix, Table A11), except Nematode

indet. and Capitella ‘capitata’ sp.

Period 2002-2003

The n-MDS showed well-grouped sampling

units, with impacted Sites in one side and Refer-

ence sites in the other (Figure 3 F). Upper two

clusters represent the before summer, and the oth-

ers the after summer aggrupation. Indicator

species M. insidiosum and C. ‘capitata’ sp. were

associated with 1S site, the closest to sewage dis-

charge. The Simper analysis (Appendix, Table

A12) showed Boccardia spp. as the most impor-

tant species in all sites, been particularly in

sewage-impacted ones. B. rodriguezii was the

second important species in the Reference site.

About Events (Appendix, Table A13) several

species increase their average abundances after

the summer like Mytilus platensis d’Orbigny,

1846, C. ‘capitata’ sp. and M. insidiosum, where-

as other decreases.

Period 2005-2006

The n-MDS (Figure 3 G) showed a crowded

pack of sampling units, more or less separated

into Reference and impacted sites, except sam-

pling units 376 and 398 (2S). Sampling unit 376

was characterized by the absence of B. rodri-

guezii and a peak of almost 4,000 individual of

Rhynchospio glutaea (Ehlers, 1897), while 398

had low values of all species. The group at the left

represent the aggrupation before summer and the

other the after summer samples units. The Simper

analysis by sites in the Period 2005-2006 (Appen-

dix, Table A14) showed higher values of Boccar-

dia sp. and Rhynchospio glutaea in 1S and 2S,

respectively. In addition, Brachidontes was the

dominant species in Reference areas. All species

showed decreasing values related to Event

(Appendix, Table A15).

342 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

Period 2008-2009

The n-MDS showed a pattern of sampling units

ruled by the demographic explosion of the invader

polychaete B. proboscidea (Figure 3 H) resulting

that dominated species were grouped to the right,

while other sampling units were in the left. The

Simper by sites (Appendix, Table A16) showed

the dominance of B. proboscidea over B.

rodriguezii in impacted areas. About Events the

species showed also the impact of the invasion of

B. proboscidea (Appendix, Table A17).

Period 2013-2014

The n-MDS (Figure 3 I) showed two groups of

sampling units. One characterized by absence of

macrofaunal life (left) and the other with the rest

of sampling units. The Simper by sites (Appendix,

Table A18) showed site 1S avoided of the inter-

tidal community, except a few endolithic B. pro-

boscidea. This species has been described as a

endolithic form (boring into the sedimentary

rock), however in Argentine also develops a new

types of habitat, as epilithic form, constructing

tubes over the substrate. On the other hand, in the

site 2S the invader polychaete is dominant over B.

rodriguezii. In relation to Event most species

showed decreasing values (Appendix, Table A19)

but Siphonaria lessoni and B. rodriguezii.

Long-term trend

The n-MDS (Figure 4 A and B) produced by

averaging abundances to made a single impacted

or reference point (=sample) shows good stress

(0.1), meaning good representation of two dimen-

sional ordination of samples. However three

Impacted samples in the upper part of the graph,

far from the others due to high dissimilarity, cor-

responds to the high abundances of the polychaete

B. proboscidea population (November 2008, Feb-

ruary 2009, and November 2009). Large gap

responds to the short-term effect (before/after

summer, an again back to spring). The large effect

of this invasive polychaete distorts the similarity

of the Reference and Impacted site samples. This

is the reflection and consequence of the signifi-

cant interactions of the Permanova that produces

a confusing sampling path.

A basal group is mainly made up of samples

from Reference samples (Figure 4 A), and anoth-

er group of samples located slightly above the

previous group mainly made up of samples from

Impacted sites (Figure 4 B), both with some

inserted samples from the other location.

343

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Figure 4. A) Reference site (green squares) with the general n-MDS inserted in the upper corner. B) Impacted sites (red squares).

The arrows showed the drift of samples from November 1997 to March 2014. The stress is 0.1.

Nov. 2008 Bef

Feb. 2009 Aft

Nov. 2013 Bef

Nov. 2003 Bef

Nov. 1997 Bef

Dec. 2001 Bef

Mar. 2001 Aft

Feb. 2014 Aft

31

29

33

35

9

11

3

17

5

25

13

23

27

15

21

1

B

Nov. 2005 Bef

Mar. 1999 Aft

Nov. 1998 Bef

Feb. 2014 Aft

Nov. 2013 Bef

Nov. 2003 Bef

Mar. 2002 Aft 20

Feb. 2009 Aft

2

4

6

8

10

12

14 18

20

22

24

26

30

36

34

A

Nov. 2000 Bef

28

Mar. 2001 Aft

Mar. 2004 Aft 24

32

16

The basal group of Reference samples (Figure

4 A) is characterized by a great abundance of B.

rodriguezii (1.100 average abundance) and S.

prolixa (80), while in the above group B.

rodriguezii mean abundance is low (385) as well

as S. prolixa (14), but Boccardia spp. (28).

The basal group of Impacted samples (Figure 4

B) differs from the upper group of Impacted sam-

ples in the mean abundance of Brachidontes,

twice in basal group than upper one (767 to 332),

but more close to Reference basal samples

(1.100). Indicator species are more abundant in

Impacted samples, like Boccardia spp. (27-30),

R. glutaea (27-0), M. insidiosum (14-6) and C.

‘capitata’ sp. (18-9).

Same samples were separated from these

groups. For example, the first impacted sample

corresponded to November 1997 (down left). It

shows dominance of several crustaceans, like

indicators Jassa falcata (302), M. insidiosum

(169), and Brachidontes (216), S. prolixa (92),

Caprella (52) and S. gracilis (29). The sample

Impacted November 2003 before summer (left

middle) showed a great abundance of Boccardia

spp. (275) and low Brachidontes (148), and very

low Jassa (4), S. prolixa (3), Caprella (0.1) and

some Monocorophium (19).

The largest gaps between samples correspond-

ed to the short-term change due to seasonal

change (spring-end of summer) in Reference

samples, and due to seasonal change and increas-

ing sewage discharge in Impacted samples.

Except for the gap between samples from

November 2013 (before) to February 2014 (after)

which in fact corresponded to the drastic reduc-

tion in the B. proboscidea abundance.

Community parameters

Community parameters (Richness (S), Abun-

dance (N), Diversity (H’) and Equitativity (J’)

were studied in the three sites (1S and 2S in the

sewage-impacted area, and Reference) along the

nine periods (Figure 5). Data showed highly sig-

nificant differences in Reference versus sewage-

impacted sites, in Periods and also interactions

(Appendix, Table A20).

Mean abundance (Figure 5 A) showed the influ-

ence of the ecosystem engineer B. rodriguezii in

the Reference Site, except in the period 2001-2002

due to the explosive increase in density of R. glu-

taea in 2S, and in the period 2008-2009 due to the

demographic explosion of the invader B. pro-

boscidea. On the other hand, mean richness (Fig-

ure 5 B) showed the opposite pattern, been higher

in sewage-impacted sites 1S and 2S. It was

observed a trend to diminish mean Richness along

the studied periods, nevertheless a great increased

was observed in the last one. In this last period, a

peak in richness was due to the equilibrium

between B. proboscidea and B. rodriguezii. Mean

Diversity (Figure 5 C) and Eveness (Figure 5 D)

showed a similar pattern, been higher in sewage-

impacted sites rather than in Reference site, due to

dominance of the ecosystem engineer in the later,

and the presence of tolerant species in the first one.

The community parameters were also analyzed

to Sites and Event (Figure 6). Data showed highly

significant differences in Reference versus

sewage-impacted sites in Event and interactions

(Appendix, Table A21). All parameters showed

lower values after the summer, and also a trend to

decrease along the studied periods.

DISCUSSION

This was the first study in Argentina that ana-

lyzes the long-term response of the intertidal ben-

thic community to the discharge of sewage with-

out treatment directly to the intertidal sector. It

was also the first study that analyzes the short-

term response of the intertidal epilithic communi-

ty before/after the summer. Due to the high sea-

sonality of the sewage discharge, linked to the

tourism peak in the summer months, the short-

term variation induced by the pulse discharge was

344 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

also analyzed, which in turn over-lapped with the

chronic impact produced by the sewage discharge

from Mar del Plata. In all cases, the study includ-

ed the response of areas affected by sewers and

reference areas.

There was a positive tendency for species that

tolerate organic contamination to prevail in the

sites affected by the sewage discharge, i.e. the

polychaetes C. ‘capitata’ sp., the classic indicator

of organic enrichment, and also the now-classic

B. proboscidea species (Pearson and Rosenberg

1978, Dean 2008).

Recently, for all Latin American and Caribbean

region the indicator species belonging to the

Capitella complex were widely mentioned and

reaffirmed as an indicator polychaete, although

the species identity remains to be determined in

each region (Elías et al. 2021).

In some moments of the first periods Neanthes

(=Alitta) succinea (Leuckart, 1847) was also the

indicator species in agreement with classic litera-

ture (see Pearson and Rosenberg 1978; Dean

2008). In other periods the indicator species was

R. glutaea, as well as Boccardia spp. (a pool of

species). Firstly, the species was initially identi-

fied as B. polybranchia (Haswell, 1885), never-

theless through time seems to be several species.

It was suspected that the invader B. proboscidea

345

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Figure 5. Mean values of Abundance (N) (A), Richness (S) (B), Diversity (H’) (C), and Eveness (J’) (D) in the three sites (1S,

2S in the impacted area in red lines, and Reference in green line) along the nine studied periods.

1997-1998

1998-1999

1999-2000

2000-2001

2001-2002

2003-2004

2005-2006

2008-2009

2013-2014

0

500

1,000

1,500

2,000

2,500

3,000

3,500

N

1S

2S

Reference

1997-1998

1998-1999

1999-2000

2000-2001

2001-2002

2003-2004

2005-2006

2008-2009

2013-2014

0

2

4

6

8

10

12

14

16

18

S

1S

2S

Reference

1997-1998

1998-1999

1999-2000

2000-2001

2001-2002

2003-2004

2005-2006

2008-2009

2013-2014

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

1.8

H’

1S

2S

Reference

1997-1998

1998-1999

1999-2000

2000-2001

2001-2002

2003-2004

2005-2006

2008-2009

2013-2014

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

J’

1S

2S

Reference

A

B

CD

was present before the demographic explosion of

2008, and the present research showed that since

2006 the invader species is present as a compan-

ion species among the community.

Among the crustaceans, the tubiculous M.

insidiosum was highly abundant in areas impact-

ed by sewage discharge. Other crustacean indica-

tors were also very abundant in areas located at

intermediate distances from the sewage discharge

(site 2S) such as J. falcata and Caprella sp. At the

other extreme were the indicator species of good

environmental quality, that was, sensitive or very

sensitive species such as the polychaete Leo-

damas tribulosus (Ehlers, 1897), most Syllids

(see below) and the flatworm Notoplana sp.

recently detected (Cuello et al. 2017).

The Syllidae in the area initially showed a clas-

sic behavior as sensitive species (Elías et al.

2003a, 2003b). However, long-term studies (Elías

et al. 2006; Sánchez et al. 2013) showed erratic

behavior. In some places and on some occasions

they were very abundant at intermediate distances

to the sewage discharge, exhibiting a high degree

of tolerance to organic contamination. This could

be because these species (S. prolixa and S. gra-

cilis) are a complex of species, similar morpho-

logically but with a different physiologyical

response. The same can be said about N. suc-

346 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

Figure 6. Mean values of Richness (S) (A), Abundance (N) (B), Eveness (J’) (C), and Diversity (H’) (D) in the Event before/after

summer along the nine studied periods.

1997-1998

1998-1999

1999-2000

2000-2001

2001-2002

2003-2004

2005-2006

2008-2009

2013-2014

2

4

6

8

10

12

14

16

S

Before

After

1997-1998

1998-1999

1999-2000

2000-2001

2001-2002

2003-2004

2005-2006

2008-2009

2013-2014

0

500

1,000

1,500

2,000

2,500

3,000

N

Before

After

1997-1998

1998-1999

1999-2000

2000-2001

2001-2002

2003-2004

2005-2006

2008-2009

2013-2014

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

J’

Before

After

1997-1998

1998-1999

1999-2000

2000-2001

2001-2002

2003-2004

2005-2006

2008-2009

2013-2014

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

H’

Before

After

AB

CD

cinea, ‘suspiciously cosmopolitan’ (Sánchez et al.

2013). Probably deeper and specific taxonomic

studies must show the real identity of the syllids

and nereidids indicator in the SW Atlantic.

The short-term effect (before/after the sum-

mer) showed that the chronic effect produced by

the sewage discharge was compounded by an

aggravated effect, since all the community

parameters revealed significant reductions. Also,

the analysis of similarity before/after the summer

showed significant reduction of the average abun-

dances of almost all the organisms of the inter-

tidal community but the tolerant ones, which in

many cases even increased after the summer. The

fact that the sewer discharge increases signifi-

cantly, and that during the summer the dominant

winds came from the northern sector, pushing the

discharge flow to the south towards the city and

the sampling sites, (Vallarino et al. 2002) had an

even greater negative impact on the intertidal

benthic community.

Studies in the area, including this one, made

possible to detect the presence of non-native

species and the explosive development of some

of them, giving rise to significant changes in the

structure and functioning of the intertidal com-

munity. In fact, concerning the original descrip-

tion of this community, more than 50 years ago

(Olivier et al. 1966), structural changes were

detected due to the invasion of barnacles (Vallar-

ino and Elías 1997). Other exotic species seem

not to have had significant ecological impacts on

native species, although specific studies are lack-

ing, especially of macroalgae (Becherucci et al.

2016; Palomo et al. 2016). Subsequently, the

demographic explosion of the invasive poly-

chaete B. proboscidea dramatically altered the

structure and function of the intertidal benthic

community (Jaubet et al. 2011, 2013; Garaffo et

al. 2012; Jaubet 2013; Elías et al. 2015; Llanos et

al. 2019).

As a first result, a series of changes were

observed in the arrangement of dominant species.

One of the indicator species in the sewage-

impacted area were Boccardia spp. until year

2008. Since this year, the invader B. proboscidea

exploded and monoculture biogenic reefs were

built with extraordinary densities (Jaubet 2013;

Jaubet et al. 2013). At the time no attempt to sep-

arate species was carried out, but it is suspected

that the B. proboscidea was present with other

species of the genus before the development of

the reefs (2021 pers. comm. L Jaubet). Our

research revealed the presence of the invader in

March 2006. Most of the observed changes in the

intertidal community in those periods were asso-

ciated to the invasion of B. proboscidea, like

mean values of Abundance, Richness, Diversity,

and Evenness (see Elías et al. 2015). No other

place in the world suffers large negative effects

due to the invasion of this polychaete. In Aus-

tralia and New Zealand the species has been

declared ‘pest’ although densities are quite lower

(one order of magnitude lesser respect our study

area) (Hayes et al. 2005; Bradstock 2015).

The bivalve B. rodriguezii is the structuring

organisms in the intertidal community because it

provides shelter from waves and desiccation, and

food for several associated species, i.e. an ecosys-

tem engineer. On the other hand, the invasive

polychaete B. proboscidea also build a tridimen-

sional structure but for itself, been considered an

auto-ecosystem engineer (Jaubet et al. 2013).

However, B. rodriguezii had an unsuspected

behavior about sewage-impact. Although it is the

common and dominant organism of the natural

community, it also shows a high level of tolerance

to organic pollution. Its abundance oscillates in

areas affected by the sewage discharge. In previ-

ous studies, Vallarino et al. (2002) indicated that

B. rodriguezii was present even within 50 m from

the sewage discharge in a pauperized community.

However, at high and intermediate levels of

organic contamination (i.e. at the sites closest to

the sewage discharge, 1S and 2S) this species was

competitively overcome by B. proboscidea

(Jaubet et al. 2013; Elías et al. 2015; Llanos 2017;

Llanos et al. 2018). Due to this behavior (toler-

347

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

ance) the calculation of ecological quality index-

es was carried out with/without this mussel, been

more representative the index without mussel

abundance (Garaffo et al. 2017).

The organic matter underwent a jump-starting

from 2005. Results from Jaubet et al. (2013)

showed that from the year 2005 the value of the

organic matter in the interstitial sediment of the

bivalves doubled. This was probably due to the

by-pass of the pre-treatment plant for sewage

effluents. The maintenance of this plant (and

therefore bypass) occurred twice a year, severely

affecting benthic communities (Elías et al. 2009).

The pre-treatment plant retained between 25 and

30 t per day of sewage sludge (Scagliola et al.

2011). The untreated wastes were released to the

marine environment during bypass, aggravating

the impact of the sewage on the ecosystem. It was

possible that the observed increase of organic

matter in the sediments could be the product of

larger discharges due to the bypass.

Long-term trend

In the long term, the abundances of two species

drive the changes in the epilithic intertidal com-

munity. In one hand the ecosystem engineer, B.

rodriguezii, and in the other hand the ecosystem

self-engineer, the polychaete B. proboscidea.

While the former constructs a three-dimensional

structure, which protrudes from the seafloor and

allows other species to live among themselves

and in the matrix they form (the definition of

ecosystem engineer), the other constructs the

same, but only B. proboscidae could live in their

matrix acting as self-engineer ecosystem (Jaubet

et al. 2013). In the Reference areas, the accompa-

nying species were a few and were subject to sea-

sonal changes, while the species of Impacted

areas are mostly opportunistic or tolerant and

change according to the discharge flow of the

sewer of the Mar del Plata city.

In this same community, a study more limited

in time but including seasonal analyzes (Elías and

Vallarino 2006) showed that the great changes in

similarity occur between spring-summer in

impacted areas, but between winter-spring in ref-

erence areas. These changes were associated to

seasonality but to sewage-induced stress in sites

close to discharge. The Control site behaved in a

cyclic way and in counter clock wise, but the

impacted stations showed no clear pattern.

The decreasing in ‘defender species’ allowed

the introduction of exotic species that finally

become invasive species. An altered environment

creates a potentially favorable environment for

the establishment of introduced or non-indige-

nous species (Dukes and Mooney 1999). Non-

indigenous species are favored in places and at

times when stress is negatively affecting native

flora and fauna, resulting in vacant niches avail-

able for colonization (Occhipinti-Ambrogi and

Savini 2003; Piola and Johnson 2008). When sev-

eral environmental quality indices were calculat-

ed, it was necessary to exclude B. rodriguezii

from these calculations, since it induced the

homogenization of sites of high index value with

sites with low values (Garaffo et al. 2017).

During the 2013-2014 period, the presence of

the polychaete B. proboscidea was observed in

greater abundance at the site near the point of dis-

charge of the sewage effluent (site 2S) but without

generating the impressive reefs recorded during

the years 2008-2009. However, after the demo-

graphic explosion, the population of B. pro-

boscidea decreased and did not completely dis-

place B. rodriguezii near the sewage discharge,

giving a coexistence of both species. In this way,

being the organic pollution lesser, it may on the

one hand have favored the growth and develop-

ment of B. rodriguezii. On the other hand, the

smaller amount of food available for B. pro-

boscidea (a polychaete that feeds by filtration or

facultative by superficial deposit), would tend to

diminish the reproduction rates and densities pre-

viously registered. This ‘balance’ could be the

reason why these two species, an ecosystem engi-

neer and the other an invasive polychaete, could

348 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

coexist in this environment. Because this, the

community has been described as an example of

the ‘bloom and bust’ dynamics (Strayer et al.

2017) since the bloom of the invading B. pro-

boscidea was followed by a decrease in the abun-

dance of this polychaete (the bust) and the coexis-

tence with the ecosystem engineer B. rodriguezii

in areas still affected by sewage discharges

(Llanos et al. 2021). Although the values of total

organic matter decreased since 2008-2009, they

were still almost four times higher than those

recorded by Vallarino (2002) that ranged between

1 and 0.4% in site 1. This decrease in the amount

of organic matter allowed B. rodriguezii to coexist

with B. proboscidea because B. rodriguezii can

tolerate average concentrations of organic matter

(Vallarino et al. 2002; Vallarino and Elías 2006).

Regulation trend

What is the underlying mechanism that

explains the community structure and dynamics

of intertidal epilithic mussel beds? The communi-

ty was described as lacking the barnacle belt, as

well as lygiid isopods, littorinids snails, echino-

derms and a top predatory (Olivier et al. 1966;

Adami et al. 2004, 2008; Bertness et al. 2006;

Hidalgo et al. 2007). Most macrophytes were sea-

sonal, and their cycles do not significantly affect

the availability of the substrate and there are also

no herbivores that significantly regulate the algal

cover as shown Penchaszadeh (1973). Space

competition has being pointed out as the major

biological structuring force in the 2-4 years peri-

od, while later successional stages were charac-

terized by space monopolization (Nugent 1986).

The regulation and stability of the intertidal com-

munity of the Mar del Plata rocky shore is also

influenced by the degree and frequency of distur-

bance, as well as by the population dynamics of

both mussels and introduced barnacles (Vallarino

and Elías 1997). Therefore the top-down mecha-

nism could not be the prevalent one. Is it a bot-

tom-up effect?

The particulate matter from sewage discharge

could be an extra supply, a bottom-up factor, but

their effect is limited to the influence of the

flume. Vallarino and Elías (2006) and the present

work has shown great changes in sewage-impact-

ed sites due to the short term effect before/after

the summer when sewage discharge increased

60% and wind flow from the north. On the other

hand, the detritus supply from subtidal macro-

phytes could be a structuring factor, but it was

only present near the study site because there are

hard substrates in the subtidal around Mar del

Plata city. However, the extended distribution of

Brachidontes beds were far away from detritus

supply, because in all the distribution there were

not extended subtidal macrophytes due to sand

bottoms. Nevertheless, Perumytilus beds are dis-

tributed in southern cold-temperate regions

(Patagonia), where submersed macrophytes are

abundant. In here, macrophytes detritus would be

present (but it was not quantified), but top-drown

forces (herbivory) are weak, due to environ-men-

tal hardness because the evaporation pressure

induced by the wind and the dryness of the air

(see Bertness et al. 2006; Hildalgo et al. 2007). In

South Africa, Bustamante and Branch (1996)

observed that the in situ productivity was insuffi-

cient to support the high biomass of filter-feeders

on exposed shores, suggesting dependence on

external subsidies, and isotope analyses showed

60-85% of the food of filter-feeders came from

particulate subtidal kelp.

Bottom-up processes can have important

effects on rocky intertidal community structure.

Oceanographic effects could generate large eco-

logical variability in the basal levels, increasing

the input of phytoplankton, detritus, and/or lar-

vae, and through upward-flowing food chain

effects, lead to variation in top-down trophic

effects. Under these conditions the invertebrates

can dominate the structure and dynamics of rocky

intertidal communities (Menge 2000). In this

context, the continuous recruitment of Brachi-

dontes (Torroglosa 2015) could be a bottom-up

349

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

factor, as mentioned by Menge (2000). Other bot-

tom-up effect was observed by Montoya et al.

(2021) by showing high concentrations of Cla in

the period studied for the two localities near the

study area (Santa Teresita and Villa Gesell),

varies from 4.71 to 65.67 μg l-1 and from 0.10 to

33.73 μg l-1 (respectively), due to high input of

nutrients in the Buenos Aires intertidal region

(although with marked temporal variability).

The dominant covered of mussels mono-cul-

tures suggests that predators did not have a strong

impact in the mid intertidal, perhaps due to their

small size or due to the phylogeographic history

of the Patagonian region (Hidalgo et al. 2007). As

a general phenomenon, physical factors appear

been the dominating structuring force in these

communities and were likely to be evolutionarily

and ecologically responsible for weakening the

effects of consumers (Bertness et al. 2006).

Ultimately the changes that take place in the

intertidal community of impacted areas are

changes within the same community, in response

to organic contamination induced by the sewage

discharge. This basically corresponds to what is

stated by Pearson and Rosenberg (1978). The

intertidal epilithic community dominated by the

mussel B. rodriguezii shown a great capacity to

absorb a disturbance, and back to revert to a pre-

disturbance situation, to finally reach again the

initial state. This mean resistance, recovery and

reversibility, was defined as ecological resilience

(see review by Gollner et al. 2017).

Although the sewage discharge of the Mar del

Plata city no longer occurs in the coastal zone,

studies of the intertidal community are still valid.

Although Mar del Plata has a submarine outfall

functionally since the beginning of 2014, practi-

cally all of Argentina’s coastal towns discharge

their sewage without treatment directly into the

coastal marine environment. This situation

should stopped as soon as possible, and for this,

this study and the preceding ones will be of great

value to evaluate the environmental impact and

take eventual mitigation measures. As previously

mentioned, both in Europe and in the United

States, guidelines were drafted to improve the

quality of recreational waters and monitor and

evaluate their quality (Water Framework Direc-

tive and the Clean Water Act, respectively). The

Republic of Argentina and eventually all Latin

America countries should direct its attention to

the environmental quality of its waters and draft

its water act.

We do not predict how climate change, sea

level, and acidification could affect intertidal

rocky shores in the SW Atlantic. Community

assemblages are expected to change in response

to ocean acidification because of relative shifts in

abundance between ecological winners and losers

(Fabry et al. 2008). This work could be a baseline

study of how the benthic epilithic community

responds in both sewage-impacted and reference

sites during a long term time period.

CONCLUSIONS

•The intertidal benthic community structure

response to natural changes at non-impacted

sites and to changes induced by organic pollu-

tion at sewage discharge sites.

•The structural changes in the community

parameters and in the multivariate abundance

of the benthic species showed significant

changes in both the spatial and the temporal

scale.

•The temporal change was reflected in both the

short-term (before/after the summer) and the

long-term (15 years from November 1997 to

March 2014). Unexpected quickly benthic

response occurs between spring and summer

(three months) in relation to sewage increase

and wind direction.

•Spatially the areas affected by sewage dis-

charges showed the ecosystem engineer B.

rodriguezii pauperized, as well as all the sensi-

tive species, while tolerant and opportunistic

350 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

species increased, as a consequence the rich-

ness and diversity were high respect natural-

low diversity areas.

•Indicator species change from period to period,

tolerant/opportunistic polychaete species were

C. ‘capitata’ sp., A. succinea, R. glutaea, Boc-

cardia spp., and B. proboscidea; while among

the crustaceans were Monocorophium insidio-

sum and J. falcata; sensitive species were

Nemerteans, Syllids, L. tribulosus, and recently

the flatworm Notoplana sp.

•The abundance of organic matter in the sedi-

ments trapped by the bivalve matrix showed

increasing values near the sewage discharge,

and a temporal pattern of increasing values

throughout the period studied, resulting in

increasing environmental degradation.

•The major impact to the community was the

bloom of the invader polychaete B. pro-

boscidea. This community has been described

as an example of the ‘bloom and bust’ dynam-

ics since the bloom of the invading B. pro-

boscidea was followed by a decrease in the

abundance of this polychaete (the bust) and the

coexistence with the ecosystem engineer B.

rodriguezii.

•The intertidal community dominated by the

mussel B. rodriguezii shows resistance, recov-

ery and reversibility, i.e. resilience.

ACKNOWLEDGEMENTS

We thank four doctoral students who did their

research at different moments of the long-term

data, E. Vallarino, L. Jaubet, M. A. Sanchez and E.

N. Llanos, as well as other Biology students that

helped along the period. Dr Lourdes Jaubet also

identified B. proboscidea in material from 2006.

Elizabeth Llanos made the Figure 1 and improve

all the figures. Analyses of long data series consti-

tuted the MSc. Thesis of Conrado Dávila at the

Universidad de Buenos Aires (UBA). Drs Juan

López Gappa, Juliana Gimenez and Valeria Teso,

Jurors of the Thesis also contributed to the origi-

nal work. Drs Griselda Garaffo, Lourdes Jaubet

and Elizabeth Llanos read and improved the man-

uscript, as well as two anonymous reviewers. Dr

Diego Giberto was the editor in charge of this

work, and thanks to his perseverance and sugges-

tions this work presents a long-term vision. Fun-

ding was provided to Dr Rodolfo Elías by the

Facultad de Ciencias Exactas y Naturales, Univer-

sidad Nacional de Mar del Plata.

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358 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

APPENDIX

Table A1. Ranking of dominance (abundance/total abundance) and frequency (%) of all recorded species in the period 1997-

2014. MOL: Mollusca, POL: Polychaeta. CRU: Crustacea, NMER: Nemertean, NEMA: Nematoda, QUIR: Quironomi-

dae (Insecta), TUR: Turbelaria, OLIG: Oligochaeta, TAN: Tanaidacea (CRU), ANEM: Anemone, PIC: Picnogonida,

SIPUN: Sipuncula, NUD: Nudibranchia (MOL), ASC: Ascidea, INS: Insecta, PRIA: Priapulida, OPHIU: Ophiura (Echi-

noderma).

Species Group Dominance Frequency (%)

Brachidontes rodriguezii MOL 57.08 84.6

Boccardia proboscidea POL 19.25 15.4

Syllis prolixa POL 4.50 70.9

Boccardia spp. POL 3.27 47.2

Jassa falcata CRU 2.55 33.1

Monocorophium insidiosum CRU 2.09 32.0

Rhynchospio glutaea POL 2.02 18.1

Siphonaria lessoni MOL 1.38 59.4

Leodamas tribulosus POL 1.36 43.5

Syllis gracilis POL 1.11 76.2

Capitella ‘capitata’ sp. POL 1.05 34.0

Caprella dilatata CRU 0.81 19.9

Mytilus platensis d’Orbigny, 1842 MOL 0.72 51.2

Nemertina indet. NMER 0.42 38.4

Nematode indet. NEMA 0.39 23.8

Hyale grandicornis (Krøyer, 1845) CRU 0.28 28.7

Quironomidae indet. QUIR 0.22 16.6

Protocirrineris angelicollatio Elías y Rivero, 2009 POL 0.16 21.8

Caulleriella bremecae Elías y Rivero, 2009 POL 0.15 12.4

Idotea balthica (Pallas, 1772) CRU 0.14 13.3

Balanus sp. CRU 0.13 12.2

Alitta succinea POL 0.11 25.4

Sphaeroma serratum (Fabricius, 1787) CRU 0.09 13.3

Copepoda sp. 1 CRU 0.07 2.2

Halicarcinus planatus (Fabricius, 1775) CRU 0.04 4.2

Lineus bonaerensis Moretto, 1971 NMER 0.04 5.5

Nereididae indet. POL 0.04 5.3

Notoplana sp. TUR 0.03 4.6

Spionidae indet. 1 POL 0.03 1.8

Pachycheles haigae Rodrigues da Costa, 1960 CRU 0.02 2.2

Zoeas CRU 0.02 6.2

359

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Barnea lamelosa (d’Orbigny, 1841) MOL 0.02 9.1

Copepodo harpac. indet. CRU 0.02 5.9

Polydora sp. POL 0.02 2.2

Lyonsia sp. MOL 0.01 2.9

Capitellidae indet. POL 0.01 2.9

Polychaeta indet. 2 POL 0.01 3.1

Lumbrinelidae indet. POL 0.01 3.1

Oligochaeta sp. 4 OLIG 0.01 2.9

Oligochaeta sp. 1 OLIG 0.01 1.8

Lumbrineris tetraura (Schmarda, 1861) POL 0.01 5.1

Polychaeta indet. 1 POL 0.001 4.2

Cyrtograpsus affinis (Dana, 1851) CRU 0.001 2.6

Hemigrapsus crenulatus (H. Milne Edwards, 1837) MOL 0.001 4.9

Cyrtograpsus angulatus Dana, 1851 CRU 0.001 2.9

Dodecaceria meridiana Elías y Rivero, 2009 POL 0.001 1.6

Tanaidacea TAN 0.001 2.0

Syllis sp. POL 0.001 3.1

Stenothoe sp. CRU <0.001 1.6

Polynoidae indet. POL <0.001 2.9

Erichtonius brasiliensis Dana, 1853 CRU <0.001 0.5

Joeropsis sp. CRU 0.004 2.0

Syllidae indet. POL <0.001 0.9

Anemona indet. 1 ANEM <0.001 2.2

Phyllodocidae indet. POL <0.001 0.7

Phyllodoce sp. POL <0.001 2.0

Isopoda Valvifera CRU <0.001 0.7

Cyrtograpsus altimanus Rathbun, 1914 CRU <0.001 0.5

Isopoda indet. CRU <0.001 0.9

Oligochaeta sp. 2 OLIG <0.001 0.9

Polychaeta sp. 3 POL < 0.001 1.5

Bivalvia indet. 1 MOL <0.001 1.5

Pignogonida indet. PIC <0.001 1.1

Sipunculida indet. SIPUN <0.001 0.9

Anphipoda indet. CRU <0.001 0.7

Nudibranchia indet. NUD <0.001 0.7

Ascidea indet. ASC <0.001 0.4

Insecta indet. INS <0.001 0.7

Priapulida indet. PRIA <0.001 0.5

Table A1. Continued.

Species Group DominanceFrequency (%)

360 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

Table A1. Continued.

Species Group Dominance Frequency (%)

Pachycheles laevidactylus Ortmann, 1892 CRU <0.001 0.2

Isopoda Flabellifera CRU <0.001 0.5

Crepidula sp. MOL <0.001 0.7

Hesionidae indet. POL < 0.001 0.2

Polychaeta indet. POL <0.001 0.5

Oligochaeta sp. 3 OLIG <0.001 0.5

Bivalvia indet. 2 MOL <0.001 0.5

Halosydnella australis (Kinberg, 1856) POL <0.001 0.4

Nemertina sp. 2 NMER <0.001 0.4

Glycera americana Leidy, 1855 POL <0.001 0.4

Spionidae indet. 3 POL <0.001 0.2

Oeonidae indet. POL <0.001 0.4

Hyperida indet. CRU <0.001 0.2

Heteromastus similis Southern, 1921 POL <0.001 0.2

Corbula sp. MOL < 0.001 0.4

Anemona indet. 2 ANEM < 0.001 0.4

Elasmopus marplatensis Alonso de Pina, 1997 CRU <0.001 0.5

Ostracoda indet. CRU <0.001 0.2

Crysopetallidae indet. POL <0.001 0.2

Terebellidae indet. POL <0.001 0.2

Sabellaridae indet. POL <0.001 0.2

Onuphidae indet. POL <0.001 0.2

Ophiuroidea indet. OPHIU <0.001 0.2

Lumbrineriopsis mucronata (Ehlers, 1908) POL <0.001 0.2

Acari INS <0.001 0.2

361

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Table A2. Species that most contributed to the differences among Sites in the Period 1997-1998. The species are given in the

order shown by the Simper analysis in the comparison between sewage-impacted sites, 1S and 2S with their contribution

percentage. Reference site was added before, but the order follows the first comparison.

1S 2S Reference

Species Average Average Contrib% Average Contrib%

abundance abundance abundance

Jassa falcata 5.54 12.43 15.25 2.73 15.38

Monocorophium insidiosum 9.23 9.95 10.35 1.06 13.14

Brachidontes rodriguezii 14.14 17.95 9.61 30.66 19.42

Syllis prolixa 4.08 6.94 8.15 6.99 7.5

Caprella dilatata 0.3 5.31 7.09 1.35 7.06

Capitella ‘capitata’ sp. 4.12 0.21 6.54 0 6.55

Nemertina indet. 0.33 3.23 5 1.38 4.35

Syllis gracilis 2.24 4.97 4.89 4.14 3.63

Leodamas tribulosus 0.55 1.95 2.61 2.86 3.4

Table A3. Species that most contributed to the differences between before/after summer in the Period 1997-1998.

Before After

Species Average abundance Average abundance Contrib%

Jassa falcata 12.74 2.1 15.88

Brachidontes rodriguezii 19.35 20.05 14.05

Monocorophium insidiosum 9.53 5.38 11.39

Syllis prolixa 7.95 3.82 8.32

Caprella dilatata 4.42 0.46 5.84

Capitella ‘capitata’ sp. 0.71 2.53 4.37

Syllis gracilis 4.66 2.82 4.22

362 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

Table A4. Species that most contributed to the differences among Sites in the Period 1998-1999. The species are given in the

order shown by the Simper analysis in the comparison between sewage-impacted sites, 1S and 2S with their contribution

percentage. Reference site was added before.

1S 2S Reference

Species Average Average Contrib% Average Contrib%

abundance abundance abundance

Brachidontes rodriguezii 393.68 774.82 57.69 1475 68.26

Boccardia spp. 36 37.23 7.85 39.08 5.99

Syllis prolixa 27.36 47.64 6.28 128 10.12

Caprella dilatata 6 36.73 4.78 8.85 3.61

Capitella ‘capitata’ sp. 19.55 2.95 2.91 0 0

Syllis gracilis 26.69 3.77 1.59 26.69 2.09

Table A5. Species that most contributed to the differences between before/after summer in the Period 1998-1999.

Before After

Species Average abundance Average abundance Contrib%

Brachidontes rodriguezii 22.82 30.09 21

Syllis prolixa 4.95 5.78 9.46

Boccardia spp. 5.46 2.93 8.7

Leodamas tribulosus 3.1 0.34 4.97

Jassa falcata 3.09 0.56 4.84

Monocorophium insidiosum 2.97 1.13 4.69

Caprella dilatata 2.71 0.79 4.5

Capitella ‘capitata’ sp. 1.88 1.65 4.4

363

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Table A6. Species that most contributed to the differences among Sites in the Period 1999-2000. The species are given in the

order shown by the Simper analysis in the comparison between sewage-impacted sites, 1S and 2S with their contribution

percentage. Reference site was added before.

1S 2S Reference

Species Average Average Contrib% Average Contrib%

abundance abundance abundance

Brachidontes rodriguezii 18.00 21.67 17.11 32.5 31.23

Boccardia spp. 4.52 4.08 15.17 1.56 8.16

Capitella ‘capitata’ sp. 5.6 1.22 14.49 0 11.61

Siphonaria lessoni 4.67 2.15 10.28 1.8 3.67

Syllis prolixa 3.15 3.75 10.24 7.35 14.46

Leodamas tribulosus 0.78 1.8 5.37 0.5 1.9

Table A7. Species that most contributed to the differences between before/after summer in the Period 1999-2000.

Before After

Species Average abundance Average abundance Contrib%

Syllis prolixa 8.25 5.33 12.97

Brachidontes rodriguezii 18.12 14.5 11.78

Capitella ‘capitata’ sp. 0.04 3.91 8.65

Rhynchospio glutaea 3.35 0 7.01

Leodamas tribulosus 2.68 0.08 5.97

Syllis gracilis 3 3.51 5.64

Jassa falcata 2.74 0.03 5.5

Boccardia spp. 1.98 1.12 5.46

364 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

Table A8. Species that most contributed to the differences among Sites in the Period 2000-2001. The species are given in the

order shown by the Simper analysis in the comparison between sewage-impacted sites, 1S and 2S with their contribution

percentage. Reference site was added before.

1S 2S Reference

Species Average Average Contrib% Average Contrib%

abundance abundance abundance

Syllis prolixa 5.56 7.76 14.69 6.17 14.15

Capitella ‘capitata’ sp. 4.32 1.45 11.94 0 11

Brachidontes rodriguezii 14.06 15.93 10.16 19.82 15.71

Syllis gracilis 2.35 4.54 7.75 3 6.17

Siphonaria lessoni 1.91 2.31 6.73 2.28 4.59

Boccardia spp. 1.8 1.52 6.31 0.69 4.47

Rhynchospio glutaea 1.19 1.42 5.2 1.55 4.11

Jassa falcata 1.72 0.46 4.24 1.1 4.25

Table A9. Species that most contributed to the differences between before/after summer in the Period 2000-2001.

Before After

Species Average abundance Average abundance Contrib%

Syllis prolixa 8.25 5.33 12.97

Brachidontes rodriguezii 18.12 14.5 11.78

Capitella ‘capitata’ sp. 0.04 3.9 8.65

Rhynchospio glutaea 3.35 0 7.01

Leodamas tribulosus 2.68 0.08 5.97

Syllis gracilis 3 3.51 5.64

Jassa falcata 2.74 0.03 5.5

Boccardia spp. 1.98 1.12 5.46

365

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Table A10. Species that most contributed to the differences among Sites in the Period 2001-2002. The species are given in the

order shown by the Simper analysis in the comparison between sewage-impacted sites, 1S and 2S with their contribution

percentage. Reference site was added before.

1S 2S Reference

Species Average Average Contrib% Average Contrib%

abundance abundance abundance

Brachidontes rodriguezii 19.33 32.69 25.34 30.92 28.18

Syllis prolixa 3.41 8.81 13.21 5 10.25

Boccardia spp. 4.23 4.25 8.95 0.84 8.15

Jassa falcata 3.85 3.95 7.56 1.22 6.49

Caprella dilatata 0.81 3.35 5.09 1.8 3.48

Capitella ‘capitata’ sp. 3.15 0.77 4.91 0.08 6.74

Leodamas tribulosus 0.64 2.81 4.79 0.74 2.15

Table A11. Species that most contributed to the differences between before/after summer in the Period 2001-2002.

Before After

Species Average abundance Average abundance Contrib%

Brachidontes rodriguezii 27.31 26.00 21.51

Syllis prolixa 7.36 3.92 12.59

Boccardia spp. 4.54 2.39 9.27

Jassa falcata 3.55 3.09 7.45

Nematode indet. 1.24 2.95 5.07

Leodamas tribulosus 2.78 0 4.97

Caprella dilatata 2.48 1.37 4.78

Capitella ‘capitata’ sp. 1.45 1.82 4.65

366 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

Table A12. Species that most contributed to the differences among Sites in the Period 2002-2003. The species are given in the

order shown by the Simper analysis in the comparison between sewage-impacted sites, 1S and 2S with their contribution

percentage. Reference site was added before.

1S 2S Reference

Species Average Average Contrib% Average Contrib%

abundance abundance abundance

Boccardia spp. 9.14 5.96 19.36 5.71 16.13

Brachidontes rodriguezii 13.11 16.3 12.5 22.25 18.66

Monocorophium insidiosum 4.99 0.93 9.68 0.08 9.71

Mytilus platensis 1.91 3.13 6.15 0.14 3.62

Syllis prolixa 1.22 3.28 5.62 0.45 3.03

Siphonaria lessoni 3.34 2.12 5.32 5.19 6.17

Capitella ‘capitata’ sp. 2.38 0.55 5.11 0.08 4.7

Table A13. Species that most contributed to the differences between before/after summer in the Period 2002-2003.

Before After

Species Average abundance Average abundance Contrib%

Boccardia spp. 12.12 1.83 21.46

Brachidontes rodriguezii 13.67 19.03 14.86

Monocorophium insidiosum 1.87 3.11 6.9

Siphonaria lessoni 4.16 2.3 5.94

Leodamas tribulosus 2.98 0.36 5.62

Mytilus platensis 1.87 2.12 5.12

Syllis prolixa 0.96 2.77 4.65

Capitella ‘capitata’ sp. 0.46 2.07 4.2

367

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Table A14. Species that most contributed to the differences among Sites in the Period 2005-2006. The species are given in the

order shown by the Simper analysis in the comparison between sewage-impacted sites, 1S and 2S with their contribution

percentage. Reference site was added before.

1S 2S Reference

Species Average Average Contrib% Average Contrib%

abundance abundance abundance

Boccardia spp. 7.14 1.24 16.74 3.23 16.67

Brachidontes rodriguezii 18.64 15.62 11.03 21.07 13.2

Rhynchospio glutaea 1.36 4.89 10.44 0.22 3.94

Leodamas tribulosus 2.5 4.16 10.33 0.96 7.59

Siphonaria lessoni 3.63 2.32 9.06 1.58 10.38

Capitella ‘capitata’ sp. 3.41 0.49 7.84 0.36 9.51

Syllis prolixa 3.08 4.99 6.33 0.8 8

Table A15. Species that most contributed to the differences between before/after summer in the Period 2005-2006.

Before After

Species Average abundance Average abundance Contrib%

Brachidontes rodriguezii 20.49 17.59 14.51

Boccardia spp. 6.11 1.38 13.9

Siphonaria lessoni 4.8 0.12 12.58

Leodamas tribulosus 4.91 0 12.53

Rhynchospio glutaea 4.02 0 7.82

Syllis prolixa 3.26 1.94 7.42

368 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

Table A16. Species that most contributed to the differences among Sites in the Period 2008-2009. The species are given in the

order shown by the Simper analysis in the comparison between sewage-impacted sites, 1S and 2S with their contribution

percentage. Reference site was added before.

1S 2S Reference

Species Average Average Contrib% Average Contrib%

abundance abundance abundance

Boccardia proboscidea 16.75 28.59 52.18 1.5 25.11

Brachidontes rodriguezii 6.89 9.51 19.85 21.3 50.61

Syllis prolixa 2.15 1.26 4.4 0.48 3.86

Siphonaria lessoni 0.6 1.78 4.38 1.28 3.41

Table A17. Species that most contributed to the differences between before/after summer in the Period 2008-2009.

Before After

Species Average abundance Average abundance Contrib%

Boccardia proboscidea 24.55 6.67 44.81

Brachidontes rodriguezii 14.01 11.12 29.21

Siphonaria lessoni 1.18 1.26 3.85

Syllis prolixa 1.12 1.47 3.79

369

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Table A18. Species that most contributed to the differences among Sites in the Period 2013-2014. The species are given in the

order shown by the Simper analysis in the comparison between sewage-impacted sites, 1S and 2S with their contribution

percentage. Reference site was added before.

1S 2S Reference

Species Average Average Contrib% Average Contrib%

abundance abundance abundance

Boccardia proboscidea 0.1 33.12 30.56 9.26 10.06

Brachidontes rodriguezii 0 22.92 29.59 33.45 37.86

Syllis prolixa 0 5.6 6.67 3.61 3.52

Leodamas tribulosus 0 6.91 6.62 5.45 4.94

Siphonaria lessoni 0 2.84 3.89 8.08 9.86

Table A19. Species that most contributed to the differences between before/after summer in the Period 2013-2014.

Before After

Species Average abundance Average abundance Contrib%

Brachidontes rodriguezii 19.59 21.47 24.67

Boccardia proboscidea 22.45 7.64 22.77

Leodamas tribulosus 8.07 0.31 8.09

Siphonaria lessoni 3.56 4.37 6.38

Rhynchospio glutaea 5.86 0.11 5.43

Syllis prolixa 3.82 2.85 4.72

370 MARINE AND FISHERY SCIENCES 35 (3): 333-371 (2022)

Table A20. Results of ANOVA between Sites and Periods. In all cases there were highly significant differences between factors

and interactions.

Effect SS df MS F p

Eveness

Site 1.934 2 0.967 49.11 0.00*

Period 4.113 8 0.514 26.1 0.00*

Site*Period 3.825 16 0.239 12.14 0.00*

Diversity

Site 13.23 2 6.615 57.55 0.00*

Period 27.87 8 3.484 30.31 0.00*

Site*Period 25.02 16 1.564 13.61 0.00*

Richness

Site 157 2 78.7 8.99 0.000*

Period 2589 8 323.6 36.98 0.000*

Site*Period 2323 16 145.2 16.59 0.000*

Abundance

Site 3.88E +07 2 1.94E +07 38.62 0.000*

Period 4.80E +07 8 6.00E +06 11.94 0.000*

Site*Period 6.84E +07 16 4.28E +06 8.52 0.000*

371

ELÍAS ET AL.: NATURAL AND SEWAGE-INDUCED TREND ALONG 15 YEARS IN SW ATLANTIC INTERIDAL COMMUNITY

Table A21. Results of ANOVA between Event and Periods. In all cases, there were highly significant differences between factors

and interactions.

Effect SS df MS F p

Eveness

Event 0.596 1 0.596 21.6 0.000*

Period 4.231 8 0.529 19.17 0.000*

Event*Period 0.959 8 0.12 4.34 0.000*

Diversity

Event 6.69 1 6.692 41.13 0.000*

Period 31.67 8 3.959 24.34 0.000*

Event*Period 6.21 8 0.776 4.77 0.000*

Richness

Event 423 1 423.2 35.94 0.000*

Period 2861 8 357.6 30.37 0.000*

Event*Period 391 8 48.8 4.15 0.000*

Abundance

Event 2.05E + 07 1 2.05E + 07 35.56 0.000*

Period 5.34E + 07 8 6.68E + 06 11.6 0.000*

Event*Period 3.77E + 07 8 4.72E + 06 8.2 0.000*