Marine Pollution Bulletin 167 (2021) 112309

Contents lists available at ScienceDirect

Marine Pollution Bulletin

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

The importance of a functional approach on benthic communities for

aquaculture environmental assessment: Trophic groups – A
polychaete view
Carlos Sanchis a, c, Eulogio H. Soto a, *, Eduardo Quiroga b
a
Centro de Observación Marino para Estudios de Riesgos del Ambiente Costero (COSTAR), Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de
Valparaíso, Viña del Mar, Chile
b
Escuela de Ciencias del Mar, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile
c
Programa de Magíster en Oceanografía, Universidad de Valparaíso, Chile

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

Keywords: Polychaetes were studied to assess the effect of aquaculture activity on the seafloor. Very high biodiversity of
Chilean Patagonia species was recorded associated with aquaculture centres with Cirratulidae, Spionidae and Paraonidae families
Aquaculture being the most diverse and abundant families. The spatial distribution of polychaete trophic groups was the best
Seabed pollution
descriptor for detecting changes on the benthos. Surface and subsurface deposit-feeding species dominated the
Feeding modes
Capitella capitata
sites closest to the rafts cages, highlighting Capitella capitata and Cirratulus cirratus as opportunistic species. While
Cirratulus cirratus replacement and species succession were observed with increasing presence of carnivores and omnivores in sites
further away from the salmon cages and experiencing less impact. Analyses based on the distance of feeding
modes and ecological groups from the disturbance source were better indicators of the impact that the traditional
community approach or sediment biogeochemistry. Therefore, functional traits studies should always be
considered on environmental assessments of benthic systems impacted by aquaculture.

1. Introduction Shifts in benthic macrofauna from organic enrichment systems, such

as succession or colonization events, have been widely described in
The aquaculture activity in coastal marine ecosystems is highly coastal ecosystems (Pearson and Rosenberg, 1978; Nilsson and Rosen­
harmful and has a negative impact on marine environments around the berg, 2000; Rosenberg, 2001). These authors describe that the zone with
world (e.g. Weston, 1990; Klinger and Naylor, 2012; Tičina et al., 2020; highest organic pollution is anoxic, and hence without oxygen and
Dauvin et al., 2020). Direct impacts of open-water aquaculture in fauna. Then, there will be a polluted zone dominated by high abundance
different parts of the world have been observed on the seabed under and of small size animals, termed “opportunistic species” e.g. Capitella cap­
in the near vicinity of the fish farms where particulate organic waste itata, a polychaete commonly found in organic-enriched sediments
settles (Stagličić et al., 2017; Jansen et al., 2019) or spreads under (Grassle and Grassle, 1976; Blake, 2009; Riera et al., 2011; Fernández-
different hydrodynamic regimes (Valdemarsen et al., 2015). These in­ Rodríguez and Londoño-Mesa, 2015). Next, there will be a transition
puts cause seafloor organic enrichment and hence change the structure zone with a few species and low abundance and biomass and, finally,
and function of benthic communities and the biogeochemical func­ there will be a “normal population” with richness, diversity, biomass
tioning of the sediment (Tomassetti and Porrello, 2005; Kutti et al., and abundance levels similar to non-impacted sites. This is the classic
2007; Edgar et al., 2010; Bannister et al., 2014; Tomassetti et al., 2016). Pearson and Rosenberg model (Pearson and Rosenberg, 1978), however,
Most of the consequences of this activity on the benthic environment variations may be observed according to different responses shown by
were first recorded in European countries, however, aquaculture is also species.
widespread in Chilean Patagonia where similar impacts on benthos have Polychaetes are a conspicuous and dominant element of benthic
been reported (Buschmann et al., 2009; Niklitschek et al., 2013; Qui­ communities and their spatial distribution patterns have been investi­
ñones et al., 2019). gated widely about environmental variables (Gilberto et al., 2004; Tyler

* Corresponding author at: Avenida Borgoño 16344, Reñaca, Viña del Mar, V Región, Chile.
E-mail address: [email protected] (E.H. Soto).

https://doi.org/10.1016/j.marpolbul.2021.112309
Received 12 November 2020; Received in revised form 22 March 2021; Accepted 23 March 2021
Available online 8 April 2021
0025-326X/© 2021 Elsevier Ltd. All rights reserved.
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

and Kowalewski, 2018). Their broad distribution in marine habitats from fish farms determine the polychaetes ecology. Finally, authors aim
often contributes critically to total macrofaunal diversity and standing to highlight the relevance of functional traits as organic pollution de­
stock abundance in benthic marine and estuarine sediments (Manokaran scriptors by aquaculture activity in the northern Chilean Patagonia.
et al., 2013). Polychaetes assemblages show changes in standing stock
and function as a response to different environmental variables, with the 2. Materials and methods
increase of sediment organic content being one of the most important
consequences of anthropogenic activities (Pearson and Rosenberg, 2.1. Study area
1978; Rosenberg, 2001; Dauvin et al., 2016; Álvarez-Aguilar et al.,
2017). Indeed, in polychaetes, these responses reflect different tolerance The study site was located in the inner marine areas of Chiloé and
levels due to size, mobility, growth rates and reproduction (Dauer, 1993; Aysén, Chilean Patagonia, southern Chile (Fig. 1). Four zones were
Rivero et al., 2005), but also the great variety of feeding modes (Fau­ selected at differing distances from salmon farming centres (SFC). Zone
chald and Jumars, 1979; Jumars et al., 2015). For example, species of 1 belongs to eighteen stations located <670 m from SFC in the Archi­
the Spionidae can switch their feeding mode depending on food avail­ piélago de Las Guaitecas and Archipiélago de Los Chonos areas, Aysén
ability, which enables their distributions to be related to organic region. Zone 2 belongs to six stations located 3200 m from SFC, Zone 3
enrichment (Jumars et al., 2015). Analysis of polychaete trophic struc­ with six stations, 5900 m from SFC and Zone 4 with twenty-four stations
ture allows a functional approach, providing a better understanding of located >10,000 m from SFC. Zones 2, 3 and 4 were located on the
the complexity and compositional shifts of these communities (Weston, southeastern margin of the inner sea of Chiloé Island (Corcovado Gulf),
1990; Gaston et al., 1998; Pagliosa, 2005; Cheung et al., 2008). These south from Palena River mouth (43◦ 46′ – 43◦ 51′ S), inside the jurisdic­
analyses are useful approaches to assess distribution patterns and tion of Pitipalena-Añihué Coastal Marine Protected Multiple Use Area N◦
environmental impacts by aquaculture (Domínguez Castanedo et al., 13/2014 (Ministerio del Medio Ambiente, 2015). The distance from
2012). Changes on functional traits in a far-field component can be used farms for each sampling station and its depth was measured with a
to determine the ecological footprint left by this activity (Wang et al., Samsung GPS Echo Sounder.
2017). In fact, there is growing evidence that grouping polychaete
species into feeding groups can highlight information that may be hid­ 2.2. Oceanographic background
den by taxonomic approaches (Cheung et al., 2008; Shuai et al., 2014)
and hence shifts in trophic structure may be interpreted as disturbance In the inner sea of Chiloé, the local circulation in channels and fjords
indicators (Gaston et al., 1998; Domínguez Castanedo et al., 2012). is influenced by tidal currents and topography that can be important in
Polychaetes are particularly good bioindicators of organic pollution the distribution of particulate organic matter (Sobarzo et al., 2018).
(Dean, 2008; Neave et al., 2013; Mangion et al., 2017) because of their Overall, the surface water has low nutrient content and high availability
high diversity, abundance, and functional significance. Polychaetes can of dissolved oxygen, while more homogeneous nutrients levels, char­
show a quick response due to their short life-cycles. Their wide tolerance acterized by high concentrations, are found in deeper waters (Silva and
to contaminants often means that they are in the first colonization stages Guzmán, 2006). On temporal variability, the hydrographic conditions
after disturbance by organic enrichment (Giangrande et al., 2005; Riv­ appear to be highly influenced by large-scale processes such as tidal
ero et al., 2005; Dean, 2008; Quiroga et al., 2012; Mangion et al., 2014). currents, which control the changes in the chlorophyll-a, dissolved ox­
They are often used to define ecological groups (Grall and Glémarec, ygen and temperature, even in the small channels and bays (Narváez
1997) as part of biotic indexes employed to understand the et al., 2019). Also, the influence of freshwater provided by fjords and
environmental-health status of benthic communities (Borja et al., 2000, subantarctic water masses produces a typical estuarine circulation,
2014). Although some indices use all macrobenthic community (Borja defining saline fronts throughout the fjords region and supporting
et al., 2009), studies show that polychaetes may be used as surrogates retention areas where the biological productivity is enhanced (Sobarzo,
for total macrobenthic diversity (Olsgard et al., 2003; Olsgard and 2009). The study area is characterized by complex marine-terrestrial
Somerfield, 2000). This reflects a pattern from the species to the order interactions that result in high primary production, and pools of high
level along with both natural (Włodarska-Kowalczuk and Kędra, 2007) concentrations of dissolved and particulate organic matter (González
and pollution disturbance gradients (Olsgard and Somerfield, 2000). et al., 2019). In this region, the most important sources of particulate
Despite the importance of functional approach (Gaston et al., 1998; material associated with surface waters, are fluvial runoff and coastal
Bremner et al., 2003), in Chile, the aquaculture environmental regula­ erosion, contributing to 25–50% of the surface primary productivity
tions do not consider trophic structure as disturbance indicators. The reaching the seafloor (Sobarzo, 2009; Zapata-Hernández et al., 2016;
importance of marine biotic indexes have also been suggested but González et al., 2019).
studies exploring their use are limited (Quiroga et al., 2013; Borja et al.,
2014; Pino et al., 2015). However, the species composition and com­ 2.3. Sediment sampling
munity structure remain as the main ecological parameters used to
indicate environmental conditions on the seafloor. This research ana­ Oceanographic samplings for environmental data and fauna were
lyses the polychaete assemblages standing stock and also considers carried out in summer, autumn and spring seasons during 2017. Surface
functional traits for a better understanding of spatial distribution and sediment samples from each station were collected using a van Veen
relationships with environmental parameters. The comparison of func­ grab (0.1 m2). From each sample grain size and total organic matter
tional traits distribution will allow us to know if polychaete feeding (TOM) content were determined using 150 g of sediment. Sediment
modes are good indicators to assess the impacts and the ecological subsamples for chemical analysis were taken immediately after recov­
footprint of aquaculture activity at different spatial scales. The scale of ery, labelled with the date, depth and station number information and
impacts on benthos will be defined by values of reference associated then stored frozen at − 20 ◦ C before analysis. Organic matter content was
with the organic content of sediments, composition, abundance and determined by loss of weight on ignition at 475–500 ◦ C for 5 h and
diversity of polychaete assemblage and the presence or absence of calculated as a percentage (Byers et al., 1978). The grain size was
feeding modes and ecological groups (AMBI index) (Wang et al., 2017; determined using the surface layers of each sediment sample. After a
Klootwijk et al., 2021). homogenizing process, the sample was mixed with 100 ml sodium
Therefore, this study analyses if trophic group variations explain the hexametaphosphate solution and washed on 0.063 mm sieve. The finest
spatial distribution of polychaete communities compared with tradi­ fraction was determined through the weigh difference between the
tional environmental and geochemistry methodologies. This study will removed fraction from 0,063 mm sieve (4 ɸ Wentworth scale) (silt and
investigate whether sediment composition, organic content and distance clays) and total. Particle grain size data were analysed following the Folk

2
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

Fig. 1. Location of the sampling stations and zones in the study area (Z1 ≤ 100 m to 670 m; Z2 = 3200 m, Z3 = 5900 m and Z4 = 10,200 m of distance from farm). R.
M.B. = Raúl Marín Balmaceda.

and Ward scale (Blott and Pye, 2001). Further information about sam­ (2015). Accordingly, polychaete species were divided into five feeding
pling stations is provided in Supplementary data, Table 1. modes: carnivores (C), omnivores (O), surface deposit feeders (S), sub-
surface deposit feeders (or burrowers) (B) and suspension feeders (or
2.4. Polychaetes filters) (F). This classification also considers three categories of motility:
motile (M), discreetly motile (D) and sessile (S); and three morpholog­
Sediment samples for macrofauna analysis were collected using a ical structures used in feeding: jawed (J), tentaculate (T) and other
van Veen grab (0.1 m2). Three replicates were taken on each sampling structures (X). Feeding subcategories (feeding guilds in practice) were
station for this purpose. The sediment was sieved through a 500 μm defined using the species’ mobility and morphological structures asso­
mesh size screen and latterly on 1 mm mesh size for sorting the poly­ ciated with feeding. For the assignment of ecological groups, each
chaete fauna. The biological material was fixed in a 70% ethanol–sea­ polychaete species was also classified according to a schema proposed
water solution. Polychaete fauna was identified at species level using a by Grall and Glémarec (1997), which is based on an organism’s sensi­
NIKON SMZ 800 stereomicroscope and light microscope NIKON eclipse tivity to stress, such as organic enrichment. Therefore, each species was
E200 with the support of several taxonomic keys. Polychaetes were also assigned to one of the following ecological groups: EG I: Sensitive spe­
counted to estimate abundance (number of individuals) and weighed as cies present on normal conditions; EG II: Indifferent species with low
wet weight to calculate biomass in grams using an analytical scale with a densities; EG III: Tolerant species stimulated by organic enrichment; EG
precision of 0.1 mg. All these procedures were carried out at the Benthos IV: Second-degree opportunistic species and, EG V: First-degree oppor­
laboratory of the Universidad de Valparaíso, Chile. tunistic species. To assign these ecological groups the free access library
of the AZTI’s Marine Biotic Index (AMBI) v5 software was used (https
://ambi.azti.es/es/) as well as the knowledge of local experts and the
2.5. Functional traits
authors, who have extensive experience on this issue. This tool is also
used to generate the AMBI index, providing an estimate of the distur­
Each species was classified for overall feeding modes using the
bance level on benthic communities. The assignment of feeding cate­
feeding guilds for polychaete families proposed by Fauchald and Jumars gories and ecological groups are detailed in Table 2.
(1979) in the “Diet of worms” work and its later update by Jumars et al.
2.6. Data analysis
Table 1
Summary of environmental data (mean and standard deviation) in each zone for
The abundance and biomass data obtained in each replicate were
the study area.
standardized by area as individuals per m2 and then used to determine
Location Distance (m) No. Depth (m) %Mud %MOT means and standard deviations per zone. Additionally, the mean indi­
stations
vidual body size (mg wet mass) was calculated as the total macrofauna
Z1 81–670 18
42.7 (±) 14.2 (±) 1.4 (±) community biomass divided by total macrofauna community density per
12.4 15.9 1.0
zone. Community structure was described using traditional diversity
46.4 (±) 37.3 (±) 2.3 (±)
Z2 3230 6
6.7 7.1 0.7 indexes such as Species richness (S′ ), Shannon-Weaver (H′ Log2),
30.8 (±) 21.8 (±) 1.0 (±) Sanders-Hurlbert rarefaction (ES(10)), Simpson dominance (D′ ), and
Z3 5920 6
9.3 15.9 0.3 Evenness (J′ = 1-D). The similarity matrix was calculated using the Bray
28.4 (±) 24.7 (±) 1.1 (±) Curtis index. SIMPER analyses were performed to describe the contri­
Z4 10,200–13,000 24
19.6 25.0 0.4
bution of feeding subcategories (feeding guilds) to similarities within

3
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

Table 2
List of the polychaete species, family, feeding modes, feeding subcategories, ecological groups (AMBI) and total abundance (individuals per m− 2) by zone, recorded in
the study area. Feeding modes; SDF, surface deposit feeder; SSDF, subsurface deposit feeder; CR, carnivore; OM, omnivore; FF, filter-suspension feeder. Feeding
subcategories; first letter, B, subsurface deposit feeder (burrowing); S, surface deposit feeder; C, carnivore; O, omnivore; F, filter feeder. Second letter, M, motile; D,
discreetly motile; S, sessile. Third letter, J, jawed; T, tentaculate; X, other structures. Na: not assigned.
Taxa Family Feeding modes Feeding subcategory Ecological group Z1 Z2 Z3 Z4

Ampharete kerguelensis Ampharetidae SDF SDT III 93 7 10 73

Ampharete sp. SDF SDT I 47 7
Melinna cristata SDF SDT II 13
Pareurythoe chilensis Amphinomidae CR CMX I 20 83
Capitella capitata Capitellidae SSDF BMX V 1137 3
Capitellidae nd. SSDF BMX V 3
Notomastus chilensis SSDF BMX III 253
Notomastus sp. SSDF BMX III 30 3 363
Caulleriella cristata Cirratulidae SDF SDT IV 167 297 997
Caulleriella sp1. SDF SDT III 917 473 3 590
Caulleriella sp2. SDF SDT III 143 50
Caulleriella sp3. SDF SDT III 110 13
Chaetozone curvata SDF SDT IV 57 3 10 593
Chaetozone setosa SDF SDT IV 870 10 3 2603
Chaetozone sp1. SDF SDT IV 880 140 83 283
Chaetozone sp2. SDF SDT IV 387 193 170 1343
Chaetozone sp3. SDF SDT IV 477 163 53 133
Chaetozone sp4. SDF SDT IV 707 3
Cirratulus cirratus SDF SDT IV 4307
Cirratulus sp1. SDF SDT IV 1187
Cirratulus sp2. SDF SDT IV 963 40
Cirriformia sp. SDF SDT IV 3
Dodecaceria multifiligera SDF SDT III 70 17
Kirkegaardia sp1. SDF SDT IV 413 380 40 1040
Kirkegaardia sp2. SDF SDT IV 60 277
Kirkegaardia sp3. SDF SDT IV 47
Cossura sp. Cossuridae SSDF BMX IV 510 10 77
Ctenodrilus sp. Ctenodrilidae SSDF BMX III 10
Dorvillea sp. Dorvilleidae OM OMJ II 13 3
Schistomeringos chilensis SSDF BMX IV 7
Schistomeringos longicornis SSDF BMX II 23
Lamispina gymnopapillata Flabelligeridae SDF SDT I 23
Pherusa sp. SDF SDT I 30
Glycera capitata Glyceridae CR CDJ II 403 107
Glycera sp. CR CDJ II 193
Hemipodia simplex CR CDJ II 197 17 43 1617
Glycinde armata Goniadidae CR CDJ II 337 173 27 243
Goniada sp. CR CMJ II 23
Dalhousiella ancuda Hesionidae OM OMJ II 3
Gyptis sp. OM OMJ II 3
Hesionella sp. OM OMJ II 10
Hesionides sp. OM OMJ III 3 3 53
Leocratides sp. OM OMJ II 10 3 10 83
Lacydonia sp. Lacydoniidae SSDF BMX Na 3
Eranno chilensis Lumbrineridae CR CMJ II 833 37 67 327
Lumbrinerides sp1. CR CMJ II 7 27
Lumbrinerides sp2. CR CMJ II 3
Lumbrinerides sp3. CR CMJ II 3
Lumbrineris cingulata CR CMJ II 13
Lumbrineris sp. CR CMJ II 23 40 7 43
Ninoe leptognatha CR CMJ II 220 710 70 237
Ninoe sp. CR CMJ II 30 33
Magelona annulata Magelonidae SDF SDT I 63 3 3 100
Asychis sp. Maldanidae SSDF BDX II 23 3
Clymenella minor SSDF BDX I 13
Euclymene sp. SSDF BDX II 17 120 253
Maldane sarsi SSDF BDX II 113 3 87
Nicomache sp. SSDF BDX II 23
Praxillella sp. SSDF BDX III 13 7 90
Aglaophamus peruana Nepthyidae CR CMJ II 900 167 103 1203
Nephtys ferruginea CR CMJ I 10
Nephtys magellanica CR CMJ III 197 40 10 393
Nephtys sp. CR CMJ II 3
Nereis callaona Nereididae OM OMJ II 10
Nereis eugeniae OM OMJ II 30 27 40
Nereis sp. OM OMJ III 3
Drilonereis sp. Oenonidae OM OMJ II 7
Onuphis pseudoiridescens Onuphidae OM OMJ I 13 7 3
Ophelia sp. Ophelidae SSDF BMX I 3 37
Leitoscoloplos chilensis Orbiniidae SSDF BMX IV 30 7 50
Leitoscoloplos sp. SSDF BMX IV 7 33
(continued on next page)

4
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

Table 2 (continued )
Taxa Family Feeding modes Feeding subcategory Ecological group Z1 Z2 Z3 Z4

Leodamas sp. SSDF BMX I 13 7 153

Naineris chilensis SSDF BMX I 20
Phylo felix SSDF BMX I 3
Aricidea (Aedicira) antarctica Paraonidae SDF SMX III 373 37 613
Aricidea (Acmira) finitima SDF SMX III 1043 73 10 3817
Aricidea (Acmira) strelzovi SDF SMX II 17
Aricidea sp. SDF SMX II 7
Cirrophorus sp1. SDF SMX II 67
Cirrophorus sp2. SDF SMX II 33 37 17 80
Cirrophorus sp3. SDF SMX II 3 10
Levinsenia antárctica SDF SMX III 1223 13 13 1690
Paradoneis sp. SDF SMX III 17
Paraonides sp. SDF SMX III 3
Paraonis sp. SDF SMX III 3
Cistenides ehlersi Pectinaridae SSDF BDX II 10 3
Eteone sculpta Phyllodocidae CR CMX II 13 7 10 17
Eteone sp1. CR CMX II 20
Eteone sp2. CR CMX I 10 3
Eulalia sp. CR CMX II 27 143 7 43
Paranaitis sp. CR CMX II 7
Phyllodoce sp1. CR CMX II 63 60
Phyllodoce sp2. CR CMX II 10
Ancistrosyllis sp. Pilargidae CR CMJ III 10
Halosydna patagonica Polynoidae CR CMJ II 7
Harmothoe exanthema CR CMJ II 37 47
Harmothoe patagonica CR CMJ II 3
Harmothoe sp. CR CMJ II 20 7 13
Harmothoe spinosa CR CMJ II 13 23 3 67
Hermadion magalhaensi CR CMJ II 10
Acromegalomma pigmentum Sabellidae FF FST III 7
Amphicorina sp. FF FST II 3
Chone striata FF FST II 30 3 7
Parasabella sp. FF FST III 7 3
Sabellidae nd. FF FST I 3
Scalibregma inflatum Scalibregmatidae SSDF BMX III 17 3 37
Apomatus sp. Serpulidae FF FST I 3
Leanira quatrefagesi Sigalionidae CR CMJ II 13 47 63 227
Sigalion sp. CR CMJ II 3
Sthenelais helenae CR CMJ II 10
Boccardia sp. Spionidae SDF SDT IV 13
Boccardia polybranchia SDF SDT IV 3
Dipolydora socialis SDF SDT IV 10 147
Dispio uncinata SDF SDT III 3 7 7
Laonice sp. SDF SDT III 30
Prionospio ehlersi SDF SDT IV 3 60
Prionospio orensanzi SDF SDT IV 20 360
Prionospio patagonica SDF SDT IV 37 3 130
Prionospio peruana SDF SDT IV 10
Prionospio sp1. SDF SDT III 30
Prionospio sp2. SDF SDT III 13
Prionospio steenstrupi SDF SDT IV 7
Scolelepis chilensis SDF SDT IV 3
Spiophanes bombyx SDF SDT III 110 3 20 477
Spiophanes duplex SDF SDT III 10 3
Sternaspis scutata Sternapsidae SSDF BMX III 10
Sternaspis sp. SSDF BMX III 3
Erinaceusyllis sp. Syllidae OM OMJ II 3
Exogone sp1. OM OMJ I 3 7
Exogone sp2. OM OMJ I 7
Exogoninae nd. OM OMJ II 7
Paraehlersia sp. OM OMJ II 3
Parapionosyllis sp. OM OMJ II 207
Parapionosyllis brevicirra OM OMJ II 7
Parexogone sp. OM OMJ II 17 87
Salvatoria sp. OM OMJ II 3 3
Syllinae sp. OM OMJ II 7
Syllis sp. OM OMJ II 3
Amaeana occidentalis Terebellidae SDF SDT II 7
Amphitrite sp. SDF SDT II 7
Artacama valparaisiensis SDF SDT III 33 10 13 13
Loimia sp. SDF SDT II 17 7
Streblosoma bairdi SDF SDT I 10 3
Streblosoma sp. SDF SST I 3
Terebella plagiostoma SDF SST II 7
Thelepus sp. SDF SDT II 7 23
Travisia chiloensis Travisiidae SSDF BDX I 3 27
Travisia sp. SSDF BDX I 7

5
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

and dissimilarities between groups. The species abundance data matrix species with 18, 15, 11 and 11, respectively. The five species with the
was transformed (y = √√x) for the ordination method nonmetric largest abundances were Aricidea finitima (Paraonidae) (4943 indiv.
multidimensional scaling (nMDS) analysis (Clarke and Gorley, 2006). m− 2), Cirratulus cirratus (Cirratulidae) (4307 indiv m− 2), Chaetozone
We then tested for significant differences among stations and sampling setosa (Cirratulidae) (3487 indiv. m− 2), Levinsenia antarctica (Para­
sites using 1 o 2-way permutational multivariate analysis of variance onidae) (2940 indiv. m− 2) and Aglaophamus peruana (Nephtyidae) (2373
(PERMANOVA) (Anderson, 2001). To relate the trophic structure and indiv. m− 2). This last species also showed the highest occurrence in the
environmental variables, a Canonical Correspondence Analysis (CCA) study being recorded at 89% of sampling stations (details in Table 2).
was realized (Jongman et al., 1987). Additionally, Spearman correla­ The different zones showed variations in the number of species and
tions were made including ecological parameters where biological and individuals. Z1 and Z4 recorded the highest number of species with
environmental data were transformed according to Zar (1999). All sta­ mean values over 20 species, while the lowest mean values were
tistical analyses were carried out using both Primer-e v6 (Clarke and recorded at Z3 (Fig. 2). The total number of species per sampling station
Gorley, 2006) and Past v4 (Hammer et al., 2001) statistical software. showed higher differences with values between 5 and 39 species (Sup­
plementary data). The mean number of individuals recorded the highest
3. Results value at Z1 and the lowest value at Z3 (Fig. 2), showing a range from
1120 individuals per m− 2 to 183 individuals per m− 2. However, the total
3.1. Environmental parameters of the sediment number of individuals was higher at Z4 with 22,990 individuals per m− 2
and lower at Z3 with 1100 individuals per m− 2. Data are summarized in
The TOM content varied between 0.41 and 4.95% between zones Fig. 2 and Supplementary data.
with mean values lower than 2.35%. Highest values were recorded in Z1 A subtle spatial pattern was observed on Shannon diversity (H′ ),
(4.95%) and Z2 (3.64%). The sediment grain size was dominated by Expected number of species (ES10), Dominance (D′ ) and Evenness (J′ ).
sandy fractions with mean values always above 60%, while mud mean H′ , ES10 and J′ slightly increased with increasing distance from aqua­
values were lower at 38%. The highest individual sample values for mud culture centres, while D′ decreased (Fig. 2). Mean values showed high
were recorded in Z4 (up 70%), however, the overall average for this variability between zones. Z1 recorded the highest dominance (D′ )
zone was lower (24.7% ± 25.0), indicating a high heterogeneity for the (0.26 ± 0.15) but the lowest ES10 (4.98 ± 1.34) and J′ (0.74 ± 0.15). Z2
study site. In Z2 mud concentrations were 37.3% on average, while in Z3 recorded the higher ES10 (5.94 ± 0.37) and J′ (0.87 ± 0.03), but lowest
a decrease in mud content was recorded with a mean value of 21.8%. D′ (0.13 ± 0.03). Z3 recorded the lowest H′ (2.72 ± 0.65), while Z4 the
The lowest mean mud content was recorded at Z1 with just 14.2%. highest H′ (3.25 ± 0.5) (Fig. 2).
Depths on sampling stations varied between 1.8 and 64 m, with Z1 and Biomass (wet weight) was highly variable between zones with total
Z2 being the deepest (>40 m) and Z3 and Z4 the shallowest on average values per station from 0.1 g m− 2 to 21 g m− 2 (Supplementary data).
(further information in Table 1 and Supplementary data). Mean values recorded less variation ranging from 3 to 6 g m− 2. This
variability was characterized by lower values in Z1 and Z2, and higher
values in Z3 and Z4, furthest from farms (Fig. 2 and Supplementary
3.2. Composition, abundance, diversity and biomass of polychaete data). Mean animal body size varied from 4 to 47 wet mg indiv− 1 at the
assemblage Z1 and Z3, respectively (Fig. 2). In Z1 and Z2, a higher number of small-
bodied polychaetes were found, while large-bodied size polychaetes
A total of 14,364 polychaetes were collected in the current study, were more abundant in zones further away from farms. Since small-size
corresponding to 35 families, 95 genera and 148 species of polychaetes. species dominated the current study the presence of large-size species
The total abundance was 47,880 (indiv. m− 2) with Cirratulidae and such as Aglaophamus peruana (Nephtyidae), Glycinde armata (Goniadi­
Paraonidae as the most abundant families with 21,770 (45%) and 9200 dae), Ninoe leptognatha (Lumbrineridae), Euclymene sp. (Maldanidae),
(19%) individuals per m− 2, respectively. Cirratulidae, Spionidae, Syl­ Leanira quatrefagesi (Sigalionidae) and Cirratulus cirratus (Cirratulidae)
lidae and Paraonidae were the families with the highest number of

Fig. 2. Distribution per zone of the number of species (S), number of individuals (ind. m− 2), biomass (g m− 2), body size (mg ind− 1), expected number of species
(ES10), diversity (H′ ), evenness (J′ ) and dominance (D) in the study area. Mean and standard deviation values are shown.

6
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

contributed to increases in the biomass from some specific sampling and Cirratulus sp. 2, EG: IV). Zones farthest from aquaculture centres the
stations (see Table 2). polychaete assemblage was mainly formed of second-degree opportu­
nistic species (EG: IV), tolerant species (EG: II) and indifferent species
3.3. Feeding modes and ecological groups (EG: III). These three ecological groups were widely represented in 90%
of sampling stations due to their high abundance. Sensitive species (EG:
Five feeding modes and ten subcategories (feeding guilds) were I), common under natural conditions, represented less than 1,5% of the
identified in polychaete assemblage (Table 2). Surface deposit feeders overall total, recording a very low percentage (2,5%) at Z4 with species
(SDF), which includes the subcategories SMX and SDT, was the most like Leodamas sp. (Orbiniidae) and Magelona annulata (Magelonidae)
frequent feeding mode followed by carnivores (subcategories CMJ and (Fig. 4). Species unassigned to any ecological group were mainly found
CDJ) and sub-surface deposit feeders (SSDF). These three feeding modes at Z3 with values less than 10% and highlighting the presence of
dominated all study zones (Table 2). Omnivores and filter feeders were Euclymene sp. (BDX).
also recorded but with less frequency. Concerning mobility, both motile Results obtained from SIMPER analysis (Figs. 3 and 4c) demon­
and discretely motile organisms represented 99% of the polychaete strated that stations located at zones closer to the aquaculture centres
assemblage (41 and 58%, respectively). About morphological structures were dominated by a low number of species belonging mainly to Cap­
associated with feeding, tentaculate polychaetes were the most common itellidae and Cirratulidae families. While zones further away were
with 50% followed by non-jawed polychaetes (28%) and, finally, jawed characterized by more species which were recorded with high abun­
polychaetes (21%). dance and distributed among several families such as Paraonidae,
The trophic structure distribution shown by nMDS ordination Lumbrineridae, Cirratulidae, Maldanidae, Sigalionidae and Glyceridae.
allowed us to identify four groups in the four studied zones (Fig. 3)
(PERMANOVA, p < 0.05). A first group (a) exclusively associated with 3.4. Relationships between environmental and biological data
the influence of salmon farming activity (Z1) and was characterized by a
dominance of burrowing sub-surface deposit feeders (BMX) represented The Spearman correlation analysis showed significant positive cor­
by Capitella cf. capitata (Capitellidae). A second group (b) was formed by relations (p < 0.05) for distance from farms with the expected number of
one sampling station from Z4 characterized by the dominance of surface species (r = 0.36), diversity (r = 0.35) and evenness (r = 0.34),
deposit feeder species Kirkegaardia sp. and Chaetozone sp.2 (SDT) and by respectively. Meanwhile, negative correlations with dominance and the
the carnivore Hemipodia simplex (CDJ) but this last species showed less ecological group V were observed. Depth exhibited a negative correla­
overall dominance. The third group was formed by deposit feeders and tion with CDJ (r = − 0.35). In contrast, mud percentage was positively
carnivores families (Cirratulidae; SDT, Paraonidae; SMX, Lumbrineridae related with CDJ (r = 0.37), but negatively related to CMJ (r = − 0.27)
and Nephtyidae; CMJ, Glyceridae and Goniadidae; CDJ) and was trophic subcategories. The TOM in sediment did not show a significant
recorded from Z1 (close to salmon farming) to Z4 (far from salmon relationship with biological variables (p > 0.05) (further information is
farming; >10 km), representing 83% of sampling stations. Lastly, a provided in Table 3).
fourth group where suspension-subsurface deposit feeding (Maldanidae; The results of the CCA are shown in Fig. 5. This analysis showed that
BDX) and carnivore polychaetes (Sigalionidae and Nephtyidae; CMJ) there were four environmental variables, which explained most of the
were dominant in five sampling stations from Z3 and Z4 (Fig. 3). variance (i.e. distance from farms, depth, TOM and mud%). The first two
The ecological group analysis identified that in sampling stations CCA axis eigenvalues accounted for 87% of the total variance. For the
close to salmon farming centres, there were higher numbers of first- functional traits, the first axis indicated that distance from farms, depth,
degree opportunistic species (e.g. Capitella capitata, EG: V) and and TOM were the most important variables, while the percentage of
second-degree opportunistic species (Cirratulus cirratus, Cirratulus sp. 1 mud explained better the variance along the second axis (Fig. 5, p <

Fig. 3. Non-metric multidimensional scaling (nMDS) ordination plot for polychaete assemblages based on feeding subcategories. Percentage of similarity is shown
for every group.

7
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

Fig. 4. Upper panel: percentage contribution of feeding mode (a) and ecological groups (b) (I, II, III, IV and V) for the different zones. Lower panel: dominant
polychaete species for impacted zones and less impacted zones (70% similarity) (c). SSDF: sub-surface deposit feeders, SDF: surface deposit feeders, OM: omnivores,
CR: carnivores and FF: filter-suspension feeders.

0.05). The stations close to the salmon farming (Z1 and Z2) appear to be dominated by small-size organisms with short life-history. Species
related with higher TOM and depth, in turn, associated with BMX belonging to the Cirratulidae and Paraonidae families were the most
(Capitellidae) and SDT (Cirratulidae) trophic subcategories. It is abundant. These findings are similar to those reported for soft-bottom
important to note that CDJ was related to sampling stations in Z1 with environments from Chilean Patagonia (Thatje and Brown, 2009; Mon­
shallow depths (Fig. 5). In contrast, the sampling stations in Z3 and Z4 tiel et al., 2011; Quiroga et al., 2012, 2013). However, such a high
were related to distance from farms and associated with CDJ, OMJ and polychaete diversity is not usual for a small geographic area (Pabis et al.,
SMX. These results were consistent with Spearman correlation analysis 2015; Wouters et al., 2018).
(Table 3; Fig. 5). The anthropogenic pressure originated from marine fish farming
causes an increased load of organic matter and nutrients (e.g. Johansen
4. Discussion et al., 2018; Keeley et al., 2019; Klootwijk et al., 2021). In general, lower
values of the expected number of species and diversity in the stations at
4.1. High polychaetes biodiversity associated with aquaculture centres Z1 were registered, their values increasing gradually with increasing
distance to the farms. Besides, values of evenness and dominance of the
The analysis of aquaculture impacts on marine sediments and the polychaete assemblages exhibited a converse pattern, characterized by
identification of pollution indicator species have been widely developed low values evenness and high values of dominance in the stations at Z1.
(e.g. Borja et al., 2014; Keeley et al., 2014; Martínez-García et al., 2015, It is important to note that the number of individuals, biomass and body
2019). However, Chile despite being one of the most important coun­ size were highly variable about the distance from farms, in particular
tries in this activity, with 1409 centres (723 at Aysén region) (https:// those stations at Z3 and Z4 (Fig. 2). We found a low number of in­
mapas.subpesca.cl/ideviewer/), lacks studies that analyse the impact dividuals at Z3, which were dominated by large-bodied size polychaetes
on benthic communities and the associated time-spatial variability as Euclymene sp. and Maldane sarsi (Family Maldanidae); by contrast in
(Niklitschek et al., 2013; Quiroga et al., 2013). Most studies have a the stations at Z4 there was a high number of individuals with small-
social-economic approach and do not consider the bentos on their bodied size. This heterogeneity may be related to the influence of
environmental assessments (Quiñones et al., 2019). Therefore, the cur­ allochthonous OM or too high spatial variability in grain size in the
rent research is a relevant contribution to understanding these impacts study area. The influence of rivers such as the Palena River maybe af­
taking as an example the polychaete assemblage. Despite these organ­ fects the macrobenthic composition and community structure as has
isms are important indicators of the benthic ecosystem health, little is been observed in other locations in Chilean Patagonia (Quiroga et al.,
known about their ecology. This knowledge will serve to understand the 2012, 2016).
effects of different activities such as aquaculture, overfishing or Overall hydrodynamic conditions result in the transport of fine
conservation. particles and organic matter (Dauvin et al., 2020). In our study area,
The study zone was characterized by high abundance, species TOM concentrations were similar to those reported by Silva (2006) but
number and diversity. The number of species recorded - 148 species - without evidence of organic enrichment in the sediments, however,
representing a quarter of the polychaete fauna described for Chile to Stead et al. (2011) have reported higher mean values (~3%) on sites
date (Rozbaczylo et al., 2017). These numbers could increase as several near our study area. There was no clear spatial pattern with distance
taxa have not yet been identified or classified. Studies recently published despite what was expected and there were higher organic matter values
(Blake, 2018) and “in progress” on bitentaculate cirratulids would in sampling stations from different zones regardless of their distance
indicate the presence of more morphotypes than currently recognized from aquaculture centres. Z1 did not show the highest mean organic
(Soto EH, Personal Communication). The polychaete assemblages were matter value despite its closeness to aquaculture centres, recording

8
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

lower mean concentrations than those commonly observed from sedi­

ments close to this type of activity – often >5% (Shakouri and
Auðunsson, 2006; Neofitou et al., 2010; Huang et al., 2012). Overall
concentrations recorded in this study were widely below the limits
established by environmental authorities (<9%) (Resolución Exenta
1508-2014/SUBPESCA). Some studies have reported that the impacted
area by aquaculture activities would be restricted to sediments located
under rafts cages and up to 500 m around the cages (Kutti et al., 2007;
Huang et al., 2012; Zhulay et al., 2015). In the current research there
were no sites under raft cages. Such an area would receive the different
inputs from aquaculture centre and the degree of impact would be
related to several factors, for example, the exported organic matter,
water column depth, distance between rafts cages, winds, currents and
benthic processes (Tomassetti and Porrello, 2005; 2016; Huang et al.,
2012; Keeley et al., 2013). We suggest that in our study area the depo­
sition of organic matter is related to local hydrodynamic conditions
transporting particulate organic matter far from the farms (Sobarzo
et al., 2018), thus explaining some of the variations in observed organic Fig. 5. Correspondence canonical analysis (CCA) ordination plot of feeding
subcategories and environmental variables by sampling zones.
matter values. Large variations on the tidal regime are common on study
sites and could also explain the low accumulation of organic matter
around cages as reported by Dauvin et al. (2020) for Cherbourg, France. lower percentage of fine particles around cages but with similar indi­
Our results would indicate that disturbances of polychaete assem­ cator species such as Capitella minima. In a semi-enclosed Gulf in Greece,
blages associated with aquaculture activities were mainly observed at the Mediterranean Sea, Neofitou et al. (2010) recorded sediments
sites located up to 150 m from rafts cages because the main re­ mainly composed of sand (62–79%) at the farm stations. These results
placements of the dominant species and trophic groups were recorded at may be compared to our study, coinciding with a higher presence of
these distances. It is expected that the organic content of sediments carnivore species such as Nephthys hystricis on sediments with a higher
should be determining the composition, abundance and diversity in content of sand (49–60%). In this study, sediment grain size variations
benthic polychaetes. However, despite there was no significant corre­ between zones were recorded although mean mud percentages were
lation observed the analysis of organic matter, as well as grain size, have always lower than 38%. The effects of these changes would be related to
proven to be conclusive to assess the benthic community response to the presence or dominance of specific trophic groups such as deposit-
aquaculture effects (Kutti et al., 2007; Neofitou et al., 2010; Keeley et al., feeders or carnivores.
2014; Huang et al., 2012; Dauvin et al., 2020). The dominance of sandy bottoms also would explain the regular and
This study does not originally consider the study of benthic poly­ abundant occurrence of some carnivore polychaetes found by this study
chaetes under farms. However studies made on nearby sites report a as demonstrated by correlation analysis (Spearman correlation, r =
similar trophic groups composition, lower diversity and abundance − 0.27, p < 0.05, Table 3), as well as the presence of filter feeders and
under farm cages. In addition, deposit feeders (SSDF and SDF feeding omnivorous. In soft-bottom benthic ecology, a higher presence of car­
modes) were widely dominant in abundance and number of species nivores and hence a less impacted benthic community has been associ­
highlighting Cirratulidae, Capitellidae and Paraonidae families. The ated with sandy sediments (Gray and Elliot, 2009). Finer sediments
higher level of occurrence on sites was observed in Capitellidae species usually hold higher organic matter (Tomassetti et al., 2016), however in
such as Mediomastus branchiferus and Capitella capitata, while several this study sediments with low organic matter content were mainly
species were recorded on one or two sites (Muñoz and Quiroga, 2018). found. While the proportion of mud was negatively correlated with
Physically the sediments were characterized by a higher proportion depth (Spearman correlation, r = − 0.35, p < 0.05, Table 3), overall
of sand with just a few stations at Z4 showing higher mud. These results depth was not an important parameter to explain polychaete
are similar to those reported by Stead et al. (2011) though these authors distributions.
record a higher mud percentage in only one site close to Z1. Coastal The main parameter correlated with the polychaetes response and
sedimentation processes determined by high riverine inputs (Palena that could be used to detect the influence of aquaculture was the dis­
River) may explain the higher content of sandy sediments mainly at Z2, tance from the disturbance source. The analysis of this parameter was
Z3 and Z4 since these stations were located close to the river mouth. The particularly useful to identify whether and what groups changed due to
sediment conditions at Z1 could be explained by oceanic inputs and specific environmental conditions. This approach is suitable in assessing
downward transport from the water column. the changes in functional diversity caused by aquaculture impacts
Sediment grain size distribution did not show a clear spatial pattern (Tomassetti and Porrello, 2005; Dimitriadis and Koutsoubas, 2011;
related to distance from farms, demonstrating the high heterogeneity of Riera et al., 2015) and other anthropogenic pressures (Manokaran et al.,
studied sediments. This sediment heterogeneity was also recorded by 2013; Punzo et al., 2015).
Dauvin et al. (2020) on Rade de Cherbourg, English Channel, with a

Table 3
Spearman correlation analysis for diversity parameters and feeding subcategories with environmental variables (distance from farms, depth, mud% and TOM%) for the
study area. Bold letter = p < 0.05 statistical significance.
D′ Es(10) H′ J′ CDJ CMJ OMJ EGV

Distance (m) − 0.35 0.36 0.35 0.34 0.33 − 0.05 0.34 − 0.49
Depth (m) 0.09 − 0.1 − 0.04 − 0.08 − 0.35 0.11 − 0.15 0.13
Mud (%) 0.07 0.04 0.04 − 0.06 0.37 − 0.27 − 0.05 0.06
TOM (%) 0.02 0.02 0.05 − 0.01 0.15 − 0.1 0.01 − 0.09

9
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

4.2. The importance of a functional view on benthos environmental describing a generalized pattern of response for benthic communities in
assessment relation to organic enrichment.
The oceanographic and hydrodynamic settings outlined above may
Surface deposit feeder (mostly Cirratulidae and Paraonidae) and have resulted in an increase of species belonging to ecological groups II
carnivore (mostly Nephtyidae, Lumbrineridae and Polynoidae) poly­ and III, mainly carnivores (e.g. Ninoe leptognatha) and bitentaculate
chaetes were the main feeding modes. It is probably that the great cirratulids together with the presence of species of the group I,
amount and variety of food supply reaching the seabed favoured the explaining the succession indicated in Fig. 4b and c. At Z4 successional
surface deposit feeders and hence, with the increase of prey, the carni­ change is still more evident with the record of omnivores, suspension
vore species too (Iken et al., 2010; Bluhm et al., 2011). However, this and filter feeder polychaetes contributing to a higher diversity of species
trophic composition is also recorded on soft-bottom systems without and trophic groups. Finally, the polychaete assemblage is again domi­
organic inputs by anthropogenic activity (Paiva, 1993; Mattos et al., nated by surface deposit feeders reaching an apparent condition of
2012). ecological stability (Fig. 4a).
Studies made by different authors have highlighted the close rela­ In this study, the trophic structure was dominated by deposit feeders.
tionship between deposit feeder polychaetes and organic matter content According to Rivero et al. (2005) and Hossain (2018), this feeding mode
(Quiroga et al., 2013; Zhulay et al., 2015). In our study area, deposit would be generally associated with environments under stress with the
feeders and also carnivore polychaetes appear to prefer sandy sediments presence of opportunists species. However, not all deposit feeder poly­
rather than muddy ones. They may take advantage of the sediment chaetes are pollution indicators. Some of these species have been widely
interstitial spaces where there is more food available together with high recorded in zones without apparent perturbation demonstrating a var­
availability of preys (Muniz and Pires, 1999; Domínguez Castanedo iable response to environmental conditions. This is the case of Chaeto­
et al., 2012). Nevertheless, both feeding modes may be found in sandy zone setosa and Aricidea (Acmira) finitima, which recorded high densities
and muddy bottoms (Jumars et al., 2015). Discreetly motile carnivore at Z4 (Table 2) and so they could not be associated with opportunistic
polychaetes (CDJ) were positively correlated with mud % variable, behaviour caused by anthropogenic disturbances.
where sandy sediments dominated in this study (r = 0.37). Despite The diversity of feeding modes and subcategories observed would
muddy bottoms were not dominant a higher abundance of glycerid indicate abundant food supply with detritus. In the study area, high
polychaetes (Hemipodia simplex) at zones 1 and 4 would be explained by levels of primary productivity have been reported (Silva et al., 2011;
a higher content of sand (Table 2). Manokaran et al. (2013) also Vargas et al., 2011). This food source originated from the surface ulti­
recorded the presence of carnivore polychaetes but on sediment with a mately sinks and reaches the seabed supporting diverse and heteroge­
higher proportion of mud (<50%). It would appear that carnivore neous benthic communities (Zapata-Hernández et al., 2016; Cari et al.,
polychaetes inhabit soft sediments as mentioned before. 2020). However, it is not the only food source influencing this diversity
nMDs analysis of trophic groups per zones is shown in Fig. 3, indi­ since high particulate material (enriched organically) from aquaculture
cating that the burrower deposit feeders (BMX), characterized mainly by centres and terrigenous inputs from Palena River are also present.
high densities of Capitella capitata (Capitellidae), were important in The analysis of the spatial distribution of functional groups was a key
stations close to farming centres (<100 m) C. capitata was one of the factor in gaining a better understanding of the influence of aquaculture
most abundant species at Z1 which had some of the highest organic on polychaete assemblages ecology. This approach, focused mainly on
matter concentrations (4.95 and 3.19%). Also, CCA confirmed the close trophic structure, elucidated ecological patterns that usually are less
relationship between C. capitata and organic matter content (Fig. 5). evident under a structural methodology as reported by several authors
This species is widely known as an important ecological indicator due to (Domínguez Castanedo et al., 2012; Cheung et al., 2008). Our results
its high densities in polluted ecosystems (Albano et al., 2013) and ap­ also confirmed the relevance of using trophic subcategories such as
pears to benefit from organically enriched sediments with low dissolved feeding guilds (Pagliosa, 2005), because they showed correlations with
oxygen levels (Tsutsumi et al., 1990; Weston, 1990). In our study, key environmental parameters. The practical importance of functional
C. capitata showed high density very close to the rafts cages however this approach is increasingly relevant. Authors consider functional diversity
high density likely corresponds to a complex of distinct species of Cap­ not only as a component of biodiversity also as an indicator of ecosystem
itella genus (Silva et al., 2017). functioning (Heemsbergen et al., 2004; Hooper et al., 2005). Pacheco
An analysis at Z1 (Fig. 4a) showed a clear replacement of dominant et al. (2011) mention that the analysis of functional traits should be
species. C. capitata dominated at sites located <100 m from farms, considered in traditional studies related to species diversity because
however, disappeared totally at sites >100 m and <150 m, where cir­ they provide indicators of ecosystem stress.
ratulid species (SDT) dominated like Cirratulus cirratus. On these sites
both species contributed over 70% of the abundance, explaining their 5. Conclusions
dominance. Cirratulids are considered second-degree opportunist spe­
cies (EG IV) and C. cirratus has been recognized as a bioindicator of The analysis of the structure and function of polychaete assemblages
polluted environments (Bellan, 1980) associated with aquaculture cen­ showed the impact of aquaculture activity on the benthic community.
tres (Elías et al., 2003; Tomassetti et al., 2016). On sites furthest from the This impact was more evident on trophic groups revealing a gradient of
farms (<670 m), the dominance of surface deposit feeders was not so species succession mainly determined by the distance from the distur­
evident and a more diverse trophic structure was observed. Paraonid bance source. We suggest that Cirratulus cirratus (surface deposit feeder)
polychaetes (BMX) and carnivores (CMJ and CDJ) mainly colonized be considered an indicator of zones impacted by aquaculture at Chilean
these sites with high abundance indicating better environmental con­ Patagonia. We also recommend monitoring the ecology of Chaetozone
ditions (Pagliosa, 2005; Cheung et al., 2008). Families commonly setosa (Cirratulidae), Aricidea (Acmira) finitima and Levinsenia antarctica
associated with low pollution like Terebellidae and Syllidae (Gian­ (both Paraonidae). These species were shown to be tolerant in impacted
grande et al., 2005; Dean, 2008) were also found. Even on those sites zones but dominants in the farthest zones of aquacultures centres. These
where the trophic structure was completely different, as shown by nMDS species could be selected as pollution indicators with further evidence.
(Fig. 3, groups “a” and “c”), the presence of carnivores (Eranno chilensis) The current study represents a relevant contribution to a greater
and specially maldanids (Euclymene sp., Maldane sarsi) would indicate a understanding of soft-bottom polychaete biodiversity of the northern
clear transition zone. Toward less impacted zones further from aqua­ Patagonia area. The high diversity of polychaetes should be highlighted,
culture centres, assemblage succession was evident with the coloniza­ considering that the area is under strong and permanent anthropogenic
tion by other species. Functional traits described here agree with the threats (aquaculture, pollution, fisheries, global change) that contribute
Pearson-Rosenberg conceptual model (Pearson and Rosenberg, 1978) to the loss of biodiversity. We suggest that the biological information

10
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

provided on this study should be used for supporting conservation and Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of
variance. Austral Ecol. 26, 32–46. https://doi.org/10.1111/j.1442-
management strategies mainly on those areas where multiple uses take
9993.2001.01070.pp.x.
place. It is worth noting that in the area there are two coastal marine Bannister, R.J., Valdemarsen, T., Hansen, P.K., Holmer, M., Ervik, A., 2014. Changes in
protected areas (Tic-Toc and Pitipalena-Añihué), a marine reserve (Las benthic sediment conditions under an Atlantic salmon farm at a deep, well-flushed
Guaitecas National Reserve) and all northern Patagonia region is being coastal site. Aquac. Environ. Interac. 5, 29–47. https://doi.org/10.3354/aei00092.
Bellan, G., 1980. Relationship of pollution to rocky substratum polychaetes on the French
proposed like a global Ecologically and Biologically Significant Area Mediterranean coast. Mar. Pollut. Bull. 11, 318–321. https://doi.org/10.1016/0025-
(EBSA N◦ 20; West Wind Drift Convergence; CBD Report, June 2013). 326X(80)90048-X.
Finally, the functional traits approach presented in this research Blake, J.A., 2009. Redescription of Capitella capitata (Fabricius) from West Greenland
and designation of a neotype (Polychaeta, Capitellidae). Zoosymposia 2, 55–80.
revealed the environmental condition of the benthos that may not have Blake, J., 2018. Bitentaculate Cirratulidae (Annelida, Polychaeta) collected chiefly
been recorded with the information only provided by sediment during cruises of the R/V Anton Bruun, USNS Eltanin, USCG Glacier, R/V Hero, RVIB
geochemistry. Therefore, we suggest that functional traits studies on Nathaniel B. Palmer, and R/V Polarstern from the Southern Ocean, Antarctica, and
off Western South America. Zootaxa 4537, 001–130. https://doi.org/10.11646/
benthic communities must be considered as part of environmental as­ zootaxa.4537.1.1.
sessments associated with aquaculture activities complementing tradi­ Blott, S.J., Pye, K., 2001. GRADISTAT: a grain size distribution and statistics package for
tional methods. This study has demonstrated that trophic and ecological the analysis of unconsolidated sediments. Earth Surf. Process. Landforms. 26,
1237–1248. https://doi.org/10.1002/esp.261.
attributes are good proxies which can detect impacts and additionally Bluhm, B.A., Gradinger, R., Hopcroft, R.R., 2011. Arctic ocean diversity synthesis. Mar.
may provide relevant information on ecosystem functioning and ser­ Biodivers. 41, 1–14. https://doi.org/10.1007/s12526-010-0080-x.
vices in areas influenced by aquaculture at Chilean Patagonia. The un­ Borja, A., Franco, F., Pérez, V., 2000. A marine biotic index to establish the ecological
quality of soft-bottom benthos within european estuarine and coastal environments.
controlled expansion of aquaculture toward more southern areas forces
Mar. Pollut. Bull. 40, 1100–1114. https://doi.org/10.1016/S0025-326X(00)00061-
the development of better and more precise tools for a more complete 8.
environmental evaluation of marine ecosystems. Borja, A., Ranasinghe, J.A., Weisberg, S.B., 2009. Assessing ecological integrity in marine
waters using multiple indices and ecosystem components: challenges for the future.
Mar. Pollut. Bull. 59, 1–4. https://doi.org/10.1016/j.marpolbul.2008.11.006.
CRediT authorship contribution statement Borja, A., Marín, S., Núñez, R., Muxika, I., 2014. Is there a significant relationship
between the benthic status of an area, determined by two broadly-used indices, and
Carlos Sanchis: Validation, Formal analysis, Investigation, Data best professional judgment? Ecol. Indic. 45, 308–312. https://doi.org/10.1016/j.
ecolind.2014.04.015.
curation, Writing – original draft, Writing – review & editing, Visuali­ Bremner, J., Rogers, S.I., Frid, C.L.J., 2003. Assessing functional diversity in marine
zation. Eulogio H. Soto: Conceptualization, Methodology, Validation, benthic ecosystems: a comparison of approaches. Mar. Ecol. Prog. Ser. 254, 11–25.
Investigation, Resources, Data curation, Writing – original draft, Writing https://doi.org/10.3354/meps254011.
Buschmann, A.H., Cabello, F., Young, K., Carvajal, J., Varela, D.A., Henríquez, L., 2009.
– review & editing, Visualization, Supervision, Funding acquisition. Salmon aquaculture and coastal ecosystem health in Chile: analysis of regulations,
Eduardo Quiroga: Conceptualization, Methodology, Validation, environmental impacts and bioremediation systems. Ocean Coast. Manag. 52,
Formal analysis, Investigation, Data curation, Writing – original draft, 243–249. https://doi.org/10.1016/j.ocecoaman.2009.03.002.
Byers, S.C., Mills, E.L., Stewart, P.L., 1978. A comparison of methods of determining
Writing – review & editing, Visualization. organic carbon in marine sediments, with suggestions for a standard method.
Hydrobiologia. 58, 43–47.
Cari, I., Andrade, C., Quiroga, E., Mutschke, E., 2020. Benthic trophic structure of a
Declaration of competing interest Patagonian fjord (47◦ S): the role of hydrographic conditions in the food supply in a
glaciofluvial system. Estuar. Coast. Shelf Sci. 223, 106536. https://doi.org/10.1016/
The authors declare that they have no known competing financial j.ecss.2019.106536.
Cheung, S.G., Lam, N.W.Y., Wu, R.S.S., Shin, P.K.S., 2008. Spatio-temporal changes of
interests or personal relationships that could have appeared to influence
marine macrobenthic community in sub-tropical waters upon recovery from
the work reported in this paper. eutrophication. II. Life-history traits and feeding guilds of polychaete community.
Mar. Pollut. Bull. 56, 297–307. https://doi.org/10.1016/j.marpolbul.2007.10.019.
Clarke, K.R., Gorley, R.N., 2006. PRIMER v6: UserManual/Tutorial.PRIMER-E Ltd.
Acknowledgements
Plymouth Marine Laboratory, UK, p. 190.
Dauer, D.M., 1993. Biological criteria, environmental health and estuarine macrobenthic
Authors thank FIPA project, Grant N◦ 2016-02 funded by Subpesca community structure. Mar. Pollut. Bull. 26, 249–257. https://doi.org/10.1016/
agency through the Economy Ministry of Chile and its manager Sandra 0025-326X(93)90063-P.
Dauvin, J.C., Andrade, H., De-la-Ossa-Carretero, J.A., Del-Pilar-Ruso, Y., Riera, R., 2016.
Marin for enabling the use of data for academic purposes. Nelson Silva Polychaete/amphipod ratios: an approach to validating simple benthic indicators.
assisted with sediment biogeochemistry data and discussion. Finally, we Ecol. Indic. 63, 89–99. https://doi.org/10.1016/j.ecolind.2015.11.055.
thank Dr. Gordon Paterson, Natural History Museum, London by assis­ Dauvin, J.C., Pezy, J.P., Baffreau, A., Bachelet, Q., Baux, N., Méar, Y., Murat, A.,
Poizot, E., 2020. Effects of a salmon fish farm on benthic habitats in a high-energy
tance on English language and manuscript improvements, and two hydrodynamic system: the case of the Rade de Cherbourg (English Channel).
anonymous referees for very useful comments, corrections and sugges­ Aquaculture 518, 734832. https://doi.org/10.1016/j.aquaculture.2019.734832.
tions. This manuscript is dedicated to the memory of Nelson Silva, Dean, H.K., 2008. The use of polychaetes (Annelida) as indicator species of marine
pollution: a review. Rev. Biol. Trop. 56, 11–38. https://doi.org/10.15517/RBT.
chemical oceanographer and pioneer of marine investigations at Chilean V56I4.27162.
Patagonia. Dimitriadis, C., Koutsoubas, D., 2011. Functional diversity and species turnover of
benthic invertebrates along a local environmental gradient induced by an
aquaculture unit: the contribution of species dispersal ability and rarity.
Appendix A. Supplementary data Hydrobiologia. 670, 307–315. https://doi.org/10.1007/s10750-011-0668-6.
Domínguez Castanedo, N., Hernández Alcántara, P., Solís-Weiss, V., Granados Barba, A.,
Supplementary data to this article can be found online at https://doi. 2012. Distribution of polychaete feeding guilds in sedimentary environments of the
Campeche Bank, Southern Gulf of Mexico. Helgol. Mar. Res. 66, 469–478. https://
org/10.1016/j.marpolbul.2021.112309. doi.org/10.1007/s10152-011-0283-y.
Edgar, G., Davey, A., Shepherd, C., 2010. Application of biotic and abiotic indicators for
References detecting benthic impacts of marine salmonid farming among coastal regions of
Tasmania. Aquaculture. 307, 212–218. https://doi.org/10.1016/j.
aquaculture.2010.07.018.
Albano, M.J., da Cunha Lana, P., Bremec, C., Elías, R., Martins, C.C., Venturini, N.,
Elías, R., Rivero, M.S., Vallarino, E.A., 2003. Sewage impact on the composition and
Muniz, P., Rivero, S., Vallarino, E.A., Obenat, S., 2013. Macrobenthos and multi-
distribution of Polychaeta associated to intertidal mussel beds of the Mar del Plata
molecular markers as indicators of environmental contamination in a South
rocky shore. Argentina. Iheringia. Série Zool. 93, 309–318. https://doi.org/10.1590/
American port (Mar del Plata, Southwest Atlantic). Mar. Pollut. Bull. 73, 102–114.
S0073-47212003000300009.
https://doi.org/10.1016/j.marpolbul.2013.05.032.
Fauchald, K., Jumars, P.A., 1979. The diet of worms: a study of polychaete feeding
Álvarez-Aguilar, A., Rodríguez-Villanueva, V., Macías-Zamora, J.V., Ramírez-Álvarez, N.,
guilds. Oceanogr. Mar. Biol. An Annu. Rev. 17, 193–284.
Hernández-Guzmán, F.A., 2017. Spatio-temporal analysis of benthic polychaete
Fernández-Rodríguez, V., Londoño-Mesa, M.H., 2015. Poliquetos (Annelida: Polychaeta)
community structure in the north-western coast of Baja California, Mexico. J. Mar.
como indicadores biológicos de contaminación marina: casos en Colombia. Gestión y
Biol. Assoc. United Kingdom 97, 993–1005. https://doi.org/10.1017/
Ambiente. 18, 189–204.
S0025315417000637.

11
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

Gaston, G., Rakocinski, C.F., Brown, S.S., Cleveland, C.M., 1998. Trophic structure in Manokaran, S., Khan, S.A., Lyla, S., Raja, S., Ansari, K.G.M.T., 2013. Feeding guild
estuaries: response of macrobenthos to natural and contaminant gradients. Mar. composition of shelf macrobenthic polychaetes of southeast coast of India. Trop.
Freshw. Res. 49, 833–846. https://doi.org/10.1071/MF97089. Zool. 26, 120–139. https://doi.org/10.1080/03946975.2013.825425.
Giangrande, A., Licciano, M., Musco, L., 2005. Polychaetes as environmental indicators Martínez-García, E., Sundstein Carlsson, M., Sanchez-Jerez, P., Sánchez-Lizaso, J.L.,
revisited. Mar. Pollut. Bull. 50, 1153–1162. https://doi.org/10.1016/j. Sanz-Lazaro, C., Holmer, M., 2015. Effect of sediment grain size and bioturbation on
marpolbul.2005.08.003. decomposition of organic matter from aquaculture. Biogeochemistry. 125, 133–148.
Gilberto, D.A., Bremec, C.S., Acha, E.M., Mianzan, H., 2004. Large-scale spatial patterns https://doi.org/10.1007/s10533-015-0119-y.
of benthic assemblages in the SW Atlantic: the Río de la Plata estuary and adjacent Martínez-García, E., Capaccioni-Azzati, R., Sánchez-Lizaso, J.L., Sanchez-Jerez, P., 2019.
shelf waters. Estuar. Coast. Shelf Sci. 61, 1–13. https://doi.org/10.1016/j. Application of a new protocol to evaluate the benthic impacts of aquaculture:
ecss.2004.03.015. colonization of experimental units for monitoring by polychaeta. Ecol. Indic. 101,
González, H.E., Nimptsch, J., Giesecke, R., Silva, N., 2019. Organic matter distribution, 50–61. https://doi.org/10.1016/j.ecolind.2019.01.006.
composition and its possible fate in the Chilean North-Patagonian estuarine system. Mattos, G., Cardoso, R.S., Dos Santos, A.S., 2012. Environmental effects on the structure
Sci. Total Environ. 657, 1419–1431. https://doi.org/10.1016/j. of polychaete feeding guilds on the beaches of Sepetiba Bay, south-eastern Brazil.
scitotenv.2018.11.445. J. Mar. Biol. Ass. United Kingdom. 93, 973–980. https://doi.org/10.1017/
Grall, J., Glémarec, M., 1997. Using biotic indices to estimate macrobenthic community S0025315412000707.
perturbations in the Bay of Brest. Estuar. Coast. Shelf Sci. 44, 43–53. https://doi.org/ Ministerio del Medio Ambiente, 2015. Crea Área Marina Costera Protegida de Múltiples
10.1016/S0272-7714(97)80006-6. Usos “Pitipalena - Añihué”, en la Región de Aysén del General Carlos Ibáñez del
Grassle, J.P., Grassle, J.F., 1976. Sibling species in the marine pollution indicator Campo. Decreto 13.
Capitella (Polychaeta). Science. 192, 567–569. Montiel, A., Quiroga, E., Gerdes, D., 2011. Diversity and spatial distribution patterns of
Gray, J.S., Elliot, M., 2009. Ecology of Marine Sediments. From Science to Management, polychaete assemblages in the Paso Ancho, Straits of Magellan Chile. Cont. Shelf Res.
2nd edn. Oxford University Press, Oxford, UK. 31, 304–314. https://doi.org/10.1016/j.csr.2010.11.010.
Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: paleontological statistics software Muniz, P., Pires, A.M.S., 1999. Trophic structure of polychaetes in the São Sebastião
package for education and data analysis. Palaeontologia Electron. 4, 1–9. http://pal Channel (southeastern Brazil). Mar. Biol. 134, 517–528. https://doi.org/10.1007/
aeo-electronica.org/2001_1/past/issue1_01.htm. s002270050567.
Heemsbergen, D.A., Berg, M.P., Loreau, M., van Hal, J.R., Faber, J.H., Verhoef, H.A., Muñoz, C., Quiroga, E., 2018. Influence of salmon farming on alpha diversity in soft-
2004. Biodiversity effects on soil processes explained by interspecific functional bottom macrobenthic communities in the Puyuhuapi channel (Northern Patagonia,
dissimilarity. Science. 306, 1019–1020. https://doi.org/10.1126/science.1101865. 44 ◦ S). XXXIII Sciences Marine Meeting, p. 463. Universidad Austral de Chile,
Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J.H., Valdivia (Chile). In spanish. https://www.schcm.cl/web/images/congresos/
Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setälä, H., Symstad, A.J., XXXVIIICongresodeCienciasdelMar2018.pdf.
Vandermeer, J., Wardle, D.A., 2005. Effects of biodiversity on ecosystem Narváez, D.A., Vargas, C.A., Cuevas, L.A., García-Loyola, S.A., Lara, C., Segura, C.,
functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35. https://doi. Tapia, F.J., Broitman, B.R., 2019. Dominant scales of subtidal variability in coastal
org/10.1890/04-0922. hydrography of the Northern Chilean Patagonia. J. Mar. Syst. 193, 59–73. https://
Hossain, M.B., 2018. Trophic functioning of macrobenthic fauna in a tropical acidified doi.org/10.1016/j.jmarsys.2018.12.008.
Bornean estuary (Southeast Asia). Int. J. Sediment Res. 34, 48–57. https://doi.org/ Neave, M.J., Glasby, C.J., McGuinness, K.A., Parry, D.L., Streten-Joyce, C., Gibb, K.S.,
10.1016/j.ijsrc.2018.08.002. 2013. The diversity and abundance of polychaetes (Annelida) are altered in
Huang, Y.-C.A., Huang, S.-C., Hsieh, H.J., Meng, P.-J., Chen, C.A., 2012. Changes in sediments impacted by alumina refinery discharge in the Northern Territory,
sedimentation, sediment characteristics, and benthic macrofaunal assemblages Australia. Mar. Environ. Res. 92, 253–263. https://doi.org/10.1016/j.
around marine cage culture under seasonal monsoon scales in a shallow-water bay in marenvres.2013.10.005.
Taiwan. J. Exp. Mar. Biol. Ecol. 422–423, 55–63. https://doi.org/10.1016/j. Neofitou, N., Vafidis, D., Klaoudatos, S., 2010. Spatial and temporal effects of fish
jembe.2012.04.008. farming on benthic community structure in a semi-enclosed gulf of the Eastern
Iken, K., Bluhm, B., Dunton, K., 2010. Benthic food-web structure under differing water Mediterranean. Aquacult. Environ. Interact. 1, 95–105. https://doi.org/10.3354/
mass properties in the southern Chukchi Sea. Deep-Sea Res. Part II Top. Stud. aei00010.
Oceanogr. 57, 71–85. https://doi.org/10.1016/j.dsr2.2009.08.007. Niklitschek, E.J., Soto, D., Molinet, C., Toledo, P., Lafon, A., 2013. Southward expansion
Jansen, H.M., Hansen, P.K., Brennan, N., Dahlgren, T.G., Fang, J., Nederlof, M.A.J., of the Chilean salmon industry in the Patagonian Fjords: main environmental
Strohmeier, T., Sveier, H., Strand, Ø., 2019. Enhancing opportunistic polychaete challenges. Rev. Aqua. 4, 1–24. https://doi.org/10.1111/raq.12012.
communities under fish farms: an alternative concept for integrated aquaculture. Nilsson, H.C., Rosenberg, R., 2000. Succession in marine benthic habitats and fauna in
Aquacult. Environ. Interact. 11, 331–336. https://doi.org/10.3354/aei00318. response to oxygen deficiency: analyzed by sediment profile-imaging and by grab
Johansen, P.O., Isaksen, T.E., Bye-Ingebrigtsen, E., Haave, M., Dahlgren, T.G., Kvalø, S. samples. Mar. Ecol. Prog. Ser. 197, 139–149. https://doi.org/10.3354/meps197139.
E., Greenacre, M., Durand, D., Rapp, H.T., 2018. Temporal changes in benthic Olsgard, F., Somerfield, P.J., 2000. Surrogates in marine benthic investigations – which
macrofauna on the west coast of Norway resulting from human activities. Mar. taxonomic unit to target? J. Aquat. Ecosyst. Stress Recovery. 7, 25–42. https://doi.
Pollut. Bull. 128, 483–495. https://doi.org/10.1016/j.marpolbul.2018.01.063. org/10.1023/A:1009967313147.
Jongman, R., Ter Braak, C., van Tongeren, O., 1987. Data análisis in Community and Olsgard, F., Brattegard, T., Holthe, T., 2003. Polychaetes as surrogates for marine
Landscape Ecology. Wageningen, PUDOC. biodiversity: lower taxonomic resolution and indicator groups. Biodivers. Conserv.
Jumars, P.A., Dorgan, K.M., Lindsay, S.M., 2015. Diet of worms emended: an update of 12, 1033–1049. https://doi.org/10.1023/A:1022800405253.
polychaete feeding guilds. Annu. Rev. Mar. Sci. 7, 497–520. https://doi.org/ Pabis, K., Kędra, M., Gromisz, S., 2015. Distinct or similar? Soft bottom polychaete
10.1146/annurev-marine-010814-020007. diversity in Arctic and Antarctic glacial fjords. Hydrobiologia 742, 279–294. https://
Keeley, N.B., Cromey, C.J., Goodwin, E.O., Gibbs, M.T., Macleod, C.M., 2013. Predictive doi.org/10.1007/s10750-014-1991-5.
depositional modelling (DEPOMOD) of the interactive effect of current flow and Pacheco, A.S., González, M.T., Bremner, J., Oliva, M., Heilmayer, O., Laudien, J.,
resuspension on ecological impacts beneath salmon farms. Aquacult. Environ. Riascos, J.M., 2011. Functional diversity of marine macrobenthic communities from
Interact. 3, 275–291. https://doi.org/10.3354/aei00068. sublittoral soft-sediment habitats off northern Chile. Helgol. Mar. Res. 65, 413–424.
Keeley, N.B., Macleod, C.K., Hopkins, G.A., Forrest, B.M., 2014. Spatial and temporal https://doi.org/10.1007/s10152-010-0238-8.
dynamics in macrobenthos during recovery from salmon farm induced organic Pagliosa, P.R., 2005. Another diet of worms: the applicability of polychaete feeding
enrichment: when is recovery complete? Mar. Pollut. Bull. 250, 250–262. https:// guilds as a useful conceptual framework and biological variable. Mar. Ecol. 26,
doi.org/10.1016/j.marpolbul.2013.12.008. 246–254. https://doi.org/10.1111/j.1439-0485.2005.00065.x.
Keeley, N., Valdemarsen, T.B., Woodcock, S., Holmer, M., Husa, V., Bannister, R., 2019. Paiva, P.C., 1993. Trophic structure of a shelf polychaete taxocoenosis in southern Brazil.
Resilience of dynamic coastal benthic ecosystems in response to large-scale finfish Cah. Biol. Mar. 35, 39–55.
farming. Aquacult. Environ. Interact. 11, 161–179. https://doi.org/10.3354/ Pearson, T.H., Rosenberg, R., 1978. Macrobenthic succession in relation to organic
aei00301. enrichment and pollution of the marine environment. Oceanogr. Mar. Biol. Ann.
Klinger, D., Naylor, R., 2012. Searching for solutions in aquaculture: charting a Rev. 16, 229–311. https://doi.org/10.2983/035.034.0121u1.10.
sustainable course. Annu. Rev. Environ. Resour. 37, 247–276. https://doi.org/ Pino, L., Marín, S.L., Núñez, R., 2015. Indicadores bióticos y fracción de tamaños en la
10.1146/annurev-environ-021111-161531. definición de la macrofauna. Lat. Am. J. Aquat. Res. 43, 329–336. https://doi.org/
Klootwijk, A.T., Alve, E., Hess, S., Renaud, P.E., Sørlie, C., Dolven, J.K., 2021. Monitoring 10.3856/vol43-issue2-fulltext-9.
environmental impacts of fish farms: comparing reference conditions of sediment Punzo, E., Strafella, P., Scarcella, G., Spagnolo, A., De Biasi, A.M., Fabi, G., 2015. Trophic
geochemistry and benthic foraminifera with the present. Ecol. Indic. 120, 106818. structure of polychaetes around and offshore gas platform. Mar. Pol. Bull. 99,
https://doi.org/10.1016/j.ecolind.2020.106818. 119–125. https://doi.org/10.1016/j.marpolbul.2015.07.049.
Kutti, T., Hansen, P.K., Ervik, A., Høisæter, T., Johannessen, P., 2007. Effects of organic Quiñones, R.A., Fuentes, M., Montes, R.M., Soto, D., León-Muñoz, J., 2019.
effluents from a salmon farm on a fjord system. II. Temporal and spatial patterns in Environmental issues in Chilean salmon farming: a review. Rev. Aquac. 11, 375–402.
infauna community composition. Aquaculture 262, 355–366. https://doi.org/ https://doi.org/10.1111/raq.12337.
10.1016/j.aquaculture.2006.10.008. Quiroga, E., Ortiz, P., Gerdes, P., Reid, B., Villagran, S., Quiñones, R., 2012. Organic
Mangion, M., Borg, Thompson, R., Schembri, P.J., 2014. Influence of tuna penning enrichment and structure of macrobenthic communities in the glacial Baker Fjord,
activities on soft bottom macrobenthic assemblages. Mar. Pollut. Bull. 79, 164–174. Northern Patagonia, Chile. J. Mar. Biol. Ass. United Kingdom 92, 73–83. https://doi.
https://doi.org/10.1016/j.marpolbul.2013.12.021. org/10.1017/S0025315411000385.
Mangion, M., Borg, J.A., Schembri, P.J., Sanchez-Jerez, P., 2017. Assessment of benthic Quiroga, E., Ortiz, P., Reid, P., Gerdes, D., 2013. Classification of the ecological quality of
biological indicators for evaluating the environmental impact of tuna farming. the Aysen and Baker Fjords (Patagonia, Chile) using biotic índices. Mar. Pollut. Bull.
Aquac. Res. 48, 5797–5811. https://doi.org/10.1111/are.13403. 63, 117–126. https://doi.org/10.1016/j.marpolbul.2012.11.041.

12
C. Sanchis et al. Marine Pollution Bulletin 167 (2021) 112309

Quiroga, E., Ortiz, P., González-Saldías, R., Reid, B., Tapia, F.J., Pérez-Santos, I., sediment biochemistry. Cienc. y Tecnol. del Mar. 34, 49–68. http://www.redalyc.
Rebolledo, L., Mansilla, R., Pineda, C., Cari, I., Salinas, N., Montiel, A., Gerdes, D., org/articulo.oa?id=62428721004.
2016. Seasonal benthic patterns in a glacial Patagonian fjord: the role of suspended Thatje, S., Brown, A., 2009. The macrobenthic ecology of the straits of Magellan and The
sediment and terrestrial organic matter. Marine Ecol. Progr. Ser. 561, 31–50. Beagle Channel. An. del Inst. la Patagon. 37, 17–27. https://doi.org/10.4067/S0718-
https://doi.org/10.3354/meps11903. 686X2009000200002.
Riera, R., Monterroso, Ó., Rodríguez, M., Ramos, E., 2011. Biotic indexes reveal the Tičina, V., Katavić, I., Grubišić, L., 2020. Marine aquaculture impacts on marine biota in
impact of harbour enlargement on the benthic fauna. Chem. Ecol. 27 (4), 311–326. oligotrophic environments of the Mediterranean Sea – a review. Front. Mar. Sci. 7
https://doi.org/10.1080/02757540.2011.570753. https://doi.org/10.3389/fmars.2020.00217.
Riera, F., Tuya, F., Pérez, O., Ramos, E., Rodríguez, M., Monterroso, O., 2015. Effects of Tomassetti, P., Porrello, S., 2005. Polychaetes as indicators of marine fish farm organic
proximity to offshore fish farms over soft-bottom macrofauna. J. Mar. Biol. Ass. enrichment. Aquacult. Int. 13, 109–128. https://doi.org/10.1007/s10499-004-
United Kingdom. 95, 255–263. https://doi.org/10.1017/S0025315414001386. 9026-2.
Rivero, M.S., Elías, R., Vallarino, E.A., 2005. First survey of macroinfauna in the Mar del Tomassetti, P., Gennaro, P., Lattanzi, L., Mercatali, I., Persia, E., Vani, D., Porrello, S.,
Plata Harbor (Argentina), and the use of polychaetes as pollution indicators. Rev. 2016. Benthic community response to sediment organic enrichment by
Biol. Mar. Oceanogr. 40, 101–108. https://doi.org/10.4067/S0718- Mediterranean fish farms: case studies. Aquaculture. 450, 262–272. https://doi.org/
19572005000200002. 10.1016/j.aquaculture.2015.07.019.
Rosenberg, R., 2001. Marine benthic faunal successional stages and related sedimentary Tsutsumi, H., Fukunaga, S., Fujita, N., Sumida, M., 1990. Relationship between growth of
activity. Sci. Mar. 65, 107–119. https://doi.org/10.3989/scimar.2001.65s2107. Capitella sp. and organic enrichment of the sediment. Mar. Ecol. Progr. Ser. 63,
Rozbaczylo, N., Moreno, R.A., Díaz-Díaz, O., 2017. Poliquetos bentónicos en Chile. 157–162. https://doi.org/10.3354/meps063157.
Boletín del Instituto Oceanográfico de Venezuela, Publicación Especial 2017, 51–70. Tyler, C.L., Kowalewski, M., 2018. Regional surveys of macrobenthic shelf invertebrate
https://doi.org/10.4067/S0718-686X2017000200051. communities in Onslow Bay, North Carolina, U.S.A. Sci. Data 5, 180054. https://doi.
Shakouri, M., Auðunsson, G.A., 2006. Impact of Atlantic salmon cage culture on org/10.1038/sdata.2018.54.
sediment chemistry in Mjoifjordur. Iceland. Iran. J. Fish Sci. 6, 83–102. Valdemarsen, T., Hansen, P.K., Ervik, A., Bannister, R.J., 2015. Impact of deep-water fish
Shuai, X., Bailey-Brock, J.H., Lin, D.T., 2014. Spatio-temporal changes in trophic farms on benthic macrofauna communities under different hydrodynamic
categories of infaunal polychaetes near the four wastewater ocean outfalls on Oahu, conditions. Mar. Pollut. Bull. 101, 776–783. https://doi.org/10.1016/j.
Hawaii. Water Res. 58, 38–49. https://doi.org/10.1016/j.watres.2014.03.058. marpolbul.2015.09.036.
Silva, N., 2006. Características físicas y químicas de los sedimentos superficiales de Vargas, C.A., Martinez, R.A., San Martin, V., Aguayo, M., Silva, N., Torres, R., 2011.
canales y fiordos australes. Av. en el Conocimiento. Ocean. las Aguas Inter. Chil. Allochthonous subsidies of organic matter across a lake–river–fjord landscape in the
69–75. Chilean Patagonia: implications for marine zooplankton in inner fjord áreas. Cont.
Silva, N., Guzmán, D., 2006. Condiciones oceanográficas físicas y químicas, entre Boca Shelf Res. 31, 187–201. https://doi.org/10.1016/j.csr.2010.06.016.
del Guafo y fiordo Aysén (Crucero CIMAR 7 Fiordos). Cienc. Tecnol. Mar. 29, 25–44. Wang, L., Fan, Y., Yan, C., Gao, C., Xu, Z., Liu, X., 2017. Assessing benthic ecological
Silva, N., Vargas, C.A., Prego, R., 2011. Land–ocean distribution of allochthonous impacts of bottom aquaculture using macrofaunal assemblages. Mar. Poll. Bull. 114
organic matter in surface sediments of the Chiloé and Aysén interior seas (Chilean (1), 258–268. https://doi.org/10.1016/j.marpolbul.2016.09.032.
Northern Patagonia). Cont. Shelf Res. 31, 330–339. https://doi.org/10.1016/j. Weston, D.P., 1990. Quantitative examination of macrobenthic community changes
csr.2010.09.009. along an organic enrichment gradient. Mar. Ecol. Progr. Ser. 61, 233–244. https://
Silva, C.F., Seixas, V.C., Barroso, R., Di Domenico, M., Amaral, A.C.Z., Paiva, P.C., 2017. doi.org/10.3354/MEPS061233.
Demystifying the Capitella capitata complex (Annelida, Capitellidae) diversity by Włodarska-Kowalczuk, M., Kędra, M., 2007. Surrogacy in natural patterns of benthic
morphological and molecular data along the Brazilian coast. PLoS ONE 12, distribution and diversity: selected taxa versus lower taxonomic resolution. Mar.
e0177760. https://doi.org/10.1371/journal.pone.0177760. Ecol. Prog. Ser. 351, 53–63. https://doi.org/10.3354/meps07127.
Sobarzo, M., 2009. La región de los fiordos de la zona sur de Chile: Aspectos Wouters, J.M., Gusmao, J.B., Mattos, G., Lana, P., 2018. Polychaete functional diversity
oceanográficos. Fauna Marina bentónica De La Patagonia Chilena. 53–60. in shallow habitats: shelter from the storm. J. Sea Res. 135, 18–30. https://doi.org/
Sobarzo, M., Bravo, L., Iturra, C., Troncoso, A., Riquelme, R., Campos, P., Agurto, C., 10.1016/j.seares.2018.02.005.
2018. Hydrodynamics of a channel occupied by the aquaculture industry in southern Zapata-Hernández, G., Sellanes, J., Thiel, M., Henriquez, C., Hernández, S., Fernández, J.
Chile: implications for connectivity between farms. Aquacul. Envir. Int. 10, 291–307. C.C., Hajdu, E., 2016. Community structure and trophic ecology of megabenthic
https://doi.org/10.3354/aei00268. fauna from the deep basins in the Interior Sea of Chiloé, Chile (41◦ –43◦ S). Cont.
Stagličić, N., Šegvić-Bubić, T., Ugarković, P., Talijančić, I., Žužul, I., Tičina, V., Shelf Res. 130, 47–67. https://doi.org/10.1016/j.csr.2016.10.002.
Grubišić, L., 2017. Ecological role of bluefin tuna (Thunnus thynnus) fish farms for Zar, J.H., 1999. Biostatistical Analysis, 4th ed. Prentice-Hall, Upper Saddle River, New
associated wild fish assemblages in the Mediterranean Sea. Mar. Environ. Res. 132, Jersey, USA.
79–93. https://doi.org/10.1016/j.marenvres.2017.10.015. Zhulay, I., Reiss, K., Reiss, H., 2015. Effects of aquaculture following on the recovery of
Stead, R., Schmidt, A., Pereda, S., Anzieta, M., Asencio, G., Clasing, E., 2011. macrofauna communities. Mar. Pollut. Bull. 97, 381–390. https://doi.org/10.1016/
Relationship between north Patagonian Channel meiofauna community and j.marpolbul.2015.05.064.

13