Susceptibility of different materials and antifouling coating to macro-fouling organisms in a high wave-energy environment

Full text

70
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
Navarrete, Parragué, Osiadacz, Rojas, Bonicelli,
Fernández, Arboleda-Baena, Finke, and Baldanzi
boost our knowledge of biofouling risks in high
wave-energy habitats.
Who should read this paper?
This paper is of interest to experts in the fields of marine renewable energy,
aquaculture, and marine ecology as well as the general public.
Why is it important?
In this paper, the authors present results of an experimental study designed
to evaluate the susceptibility and selectivity of commonly used materials
in the maritime industry to colonization and biomass accumulation of
encrusting subtidal species. Specifically, they assess whether biofouling
composition, main species, and biomass accumulation rates are different
among three materials (aluminum, high-density polyethylene, and steel) at
two different depths (5 m and 15 m) in central Chile.
About the authors
Dr. Sergio Navarrete is a Professor at Pontifical Catholic University of
Chile. His expertise lies within the fields of community ecology, trophic
ecology, population ecology, and biogeography. He focuses on the
dynamics and diversity of coastal marine communities and the influence
they have on oceanographic and climatic processes from local to
regional scales.
Mirtala Parragué is a marine biologist with Universidad de Concepción,
Chile, and Laboratory Manager of the Marine Corrosion and Biofouling
Laboratory in the Marine Energy Research and Innovation Center
(MERIC) at Estación Costera de Investigaciones Marinas owned by
Pontificia Universidad Católica de Chile. Her interests are focused on the
biofouling community in the subtidal zone in south and central Chile,
especially in recruitment patterns, colonization strategies, and risks
evaluation of the species that live in this area and how these processes are
influenced by different biotic and abiotic factors.
Nicole Osiadacz has a degree in administration in ecotourism from Andres
Bello University, is a professional diver of the Chilean Army, and a PADI
diver instructor. Her interest is focused on the subtidal marine ecology and
underwater photography. She is working in the Marine Research Coastal
Station since 2016 as a marine research assistant of subtidal field surveys
with Dr. Sergio Navarrete.
Sergio Navarrete
Mirtala Parragué
Nicole Osiadacz
Francisca Rojas
Jessica Bonicelli
Accumulating Biofouling – and Knowledge
70
The Journal of Ocean Technology, Vol. 15, No. 1, 2020

Copyright Journal of Ocean Technology 2020
Miriam Fernández
Clara Arboleda-Baena
Randy Finke
Simone Baldanzi
Francisca Rojas graduated from the Universidad de Valparaíso as a marine
biologist with interest lying within the fields of marine ecology and
biology. Since 2015, she has worked at the Estación Costera de
Investigaciones Marinas with Dr. Sergio Navarrete. The lab team is
focused on the study of the dynamics and diversity of coastal marine
communities and the influence they have on oceanographic and climatic
processes from local to regional scales. She manages the field surveys in
the intertidal and laboratory logistics.
Jessica Bonicelli is a biological oceanography researcher at the Instituto de
Fomento Pesquero, Chile. Her interests are in numerical simulation,
numerical modelling, and data analysis.
Dr. Miriam Fernández is a Professor at the Pontificial Catholic University
of Chile. Her research focuses on the life history traits of marine
invertebrates and their ecology for the management and conservation of
marine resources.
Clara Arboleda-Baena is a microbial ecologist who specializes in
interactions between micro and macroorganism in aquatic ecosystems. Her
research is interdisciplinary, occurring in the interface between microbial
molecular ecology, microscopy, and field work.
Randy Finke is a Research Support Specialist at the Pontificia Universidad
Católica de Chile’s Estación Costera de Investigaciones Marinas (ECIM)
in Las Cruces, Chile. He is currently responsible for scuba diving, boating,
oceanographic operations and equipment maintenance, management of
ECIM’s environmental (SST, meteorological, tidal) database, and assisting
visiting researchers with the logistics of their research.
Dr. Simone Baldanzi is an Associate Professor at the Faculty of Marine
Science and Natural Resources at the University of Valparaiso, Chile. His
research focuses on experimental marine ecology, ecophysiology, marine
larval ecology, and evolutionary ecology of marine invertebrates.
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
71

72
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
SUSCEPTIBILITY OF DIFFERENT MATERIALS AND ANTIFOULING
COATING TO MACROFOULING ORGANISMS IN A HIGH WAVE-ENERGY
ENVIRONMENT
Sergio A. Navarrete
1,2,3
, Mirtala Parragué
1,2
, Nicole Osiadacz
1,2
, Francisca Rojas
1,2
, Jessica
Bonicelli
1,4
, Miriam Fernández
1,2
, Clara Arboleda-Baena
1
, Randy Finke
1
, and Simone
Baldanzi
1,2,5
1
Estación Costera de Investigaciones Marinas, Las Cruces, Facultad de Ciencias Biológicas, Pontificia
Universidad Católica de Chile, Santiago, Chile
2
Marine Energy Research and Innovation Center (MERIC), Santiago, Chile
3
Center of Applied Ecology and Sustainability (CAPES), Pontificia Universidad Católica de Chile,
Santiago, Chile
4
Departamento de Oceanografía y Medio Ambiente, Instituto de Fomento Pesquero (IFOP), Valparaíso,
Chile
5
Facultad de Ciencias del Mar y Recursos Naturales, Universidad de Valparaíso, Viña del mar, Chile
ABSTRACT
Our knowledge about the interaction of materials used in aquaculture with biofouling species
is largely restricted to sheltered coastal areas. Little is known about the susceptibility and
specificity of different materials, or the effectiveness of antifouling (AF) coatings, to the
incrustation by large biofouling species in high wave-energy environments. Since these
energetic habitats are becoming increasingly targeted by the aquaculture industry, and since
there is increasing concerns about the use of harmful antifouling coatings, it is urgent to
boost our knowledge about biofouling risks in these environments. Here we assessed whether
biofouling composition, main species, and biomass accumulation rates were different among
three materials, aluminum, high-density polyethylene (HDPE), and steel A36, and at two
different depths of exposed shore in central Chile. We hypothesized that either colonization
was material-specific and/or the adhesion of macrofoulers to the different materials (tenacity)
was sufficiently different that waves could remove them from some surfaces more than others.
Additionally, we evaluated the performance of an antifouling paint widely used in aquaculture
operations in Chile. All materials were colonized by macrofouling within three months of
exposure, with no significant differences in either species composition, total cover, or the rate
of biomass accumulation. No significant settlement of macrofouling was found on plates coated
with the antifouling paint after seven months of exposure. The fast growth rates and similar
composition of macrofouling suggest that the large differences in roughness and hydrophobic
character among materials are not sufficient to produce differential settlement or dislodgement
in these biofouling communities. The efficacy of the tested antifouling paint suggest that this
paint could be used as reference when testing more environmentally-friendly coatings, such as
those using biomimetic approaches.

The Journal of Ocean Technology, Vol. 15, No. 1, 2020
73
Copyright Journal of Ocean Technology 2020
INTRODUCTION
High wave energy regions of the coastal
oceans are receiving increasing attention
as a source of renewable energy and
as areas where many human activities,
including aquaculture, can expand to reduce
environmental externalities and ameliorate
conflicts with other uses, which currently
concentrate in protected habitats [Gentry et
al., 2017A]. The expansion of aquaculture,
the fastest growing food production sector
in the world, from easily polluted protected
bays and fjords to wave energetic open waters
is imminent according to most industry
projections [Bostock et al., 2010; Gentry et
al., 2017A; Gentry et al., 2017B; Troell et al.,
2009]. At the same time, there is increasing
attention to the great potential for clean marine
renewable energy (MRE) extracted from
waves around the world [Arinaga and Cheung,
2012; Cornett, 2008] and a wide diversity of
technologies are being developed and tested to
harvest this energy [López et al., 2013]. In all
these industrial developments, the materials
employed must not only be able to accomplish
and support the intended work, but must also
cope with the challenges imposed by the
inevitable biofouling of marine organisms
[Lacoste and Gaertner-Mazouni, 2015; Titah-
Benbouzid and Benbouzid, 2017]. Indeed,
the mechanical, buoyancy, and hydrodynamic
features of these human-made infrastructures
interact with different biofouling species in
a manner that can make the entire enterprise
economically or mechanically unfeasible
[Lacoste and Gaertner-Mazouni, 2015; Nall et
al., 2017]. Vast regions of the world’s shores
are highly exposed to waves, including the
coasts of Peru and Chile in the southeastern
Pacific [Lucero et al., 2017; Mork et al.,
2010], but yet, because of the logistical and
safety-related difficulties of conducting
detailed observations in wave exposed
habitats, the characterization of biofouling in
these regions is incomplete, at best. To what
extent biofouling colonization and biomass
accumulation vary among different materials
and what is the effectiveness of commonly
used antifouling paints when subjected to
impounding waves has not been evaluated.
The risks of biofouling to human-made
infrastructures result from the interaction
among three factors. First, the set of attributes
of the biota found within the biogeographic
region where the device is deployed, especially
macrofouling organisms (e.g., domination
by macroalgae, flexible hydrozoans, rigid
barnacles, or perforating organisms), which
determine, for instance, the load, lift, and
drag forces exerted on the infrastructure
[Richmond and Seed 1991; Macleod et al.,
2016]. Second, the properties of the material,
such as surface chemical composition,
compliance, roughness, and wettability,
which can alter the colonization by different
fouling species as well as their tenacity
(adhesion force) once established [Schultz,
2007; Titah-Benbouzid and Benbouzid, 2015].
KEYWORDS
Environmental impact; Engineering; Mathematical models; Hydroacoustic equipment; High
frequency sound sources; Sonar

74
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
Third, the local environmental conditions,
including productivity, temperature, flows, and
hydrodynamic forces that control growth rates
of different fouling species. Thus, information
on materials’ performances in one region of
the world and a given type of habitat cannot
be used to inform decisions on another part
of the world and under widely different
environmental conditions [Want et al., 2017].
Here we present results of a field experiment
designed to assess differential susceptibility to
macrofouling organisms by different materials
commonly used in the seagoing industry, in
a highly wave-exposed subtidal habitat of
central Chile.
Many studies have shown that biofouling
community composition varies profoundly
with time of exposure of the surfaces to the
marine environment; from the biofilm that
settles on the surface within hours of exposure
(microfouling), to the large sessile invertebrates
and algae (macrofouling) that dominate the
surface after few to several months [Callow
and Callow, 2011; Dafforn et al., 2011].
Comparisons of material performance and
antifouling methods must therefore be done by
exposing materials for similar periods of time.
Experimental studies that have done so have
typically shown that early succession stages
vary substantially among different materials,
apparently because the physical-chemical
characteristics of the material surface can affect
the colonization process [Carr and Hixon,
1997; Russ, 1977; Salta et al., 2013; Walters
and Wethey, 1996]. However, such differences
among artificial materials generally tend to be
reduced or disappear towards later successional
stages [Anderson and Underwood, 1994;
Chapman and Clynick, 2006]. In some cases,
however, initial differences in colonization can
lead to persistent differences in composition
of the sessile biofouling community of later
successional stages, which can resist new
invasions [Petraitis and Dudgeon, 2005;
Sutherland, 1974; Vieira et al., 2018]. To
what extent differences in initial stages of
succession, which are commonly observed
in different material surfaces, can determine
longer-term or final community composition
depends on the attributes and diversity
of the species that form part of the local
biofouling community that settle and engage
in competition for space [Navarrete, 2007;
Paine, 1984]. These interactions and species
attributes will determine whether succession is
highly “canalized” towards a common mono-
specific state, regardless of initial differences,
or if alternative states are feasible [Berlow,
1997; Caro et al., 2010; Petraitis and Dudgeon,
1999; Wootton, 2005]. From the point of
view of aquaculture and MRE applications,
different states of the biofouling community can
represent widely different risks for the operation
of the technology and supporting infrastructure,
including maintenance schedules.
Besides differences in initial fouler
colonization among materials, often associated
to differences in surface hydrophobic
properties or wettability, the adhesion strength
of different sessile species to the surface
(tenacity) varies among the different materials,
primarily due to differences in surface
roughness [Howell and Beherends, 2006].
Such differences in tenacity may not amount
to large changes in species composition in
calm waters, but may produce differential
dislodgement of individuals on different
materials in wave-exposed or high fluid

The Journal of Ocean Technology, Vol. 15, No. 1, 2020
75
Copyright Journal of Ocean Technology 2020
speed environments
[e.g. Schultz, 2007].
Indeed, dislodgment of
large sessile organisms
is common in wave
exposed shores [Bertness
et al., 1998; Carrington et
al., 2009] and it may lead
to different biofouling
communities on different
substrates. Thus, we
hypothesize that the
different materials
commonly used in the
aquaculture and MRE
industries can sustain different biofouling
communities, with different cover and
biomass accumulation rates, which represent
widely different risks to the equipment and
infrastructure operation and maintenance.
Here, we experimentally assess the
susceptibility to biofouling of three different
materials commonly used in the aquaculture
and shipping industries, which are also
part of the emerging MRE technologies.
Since previous studies reported differences
in rates of biomass accumulation between
depths [Navarrete et al., 2019], we tested the
materials and paint at two depths, above and
below the thermocline, for a period of nearly
eight months.
MATERIALS AND METHODS
The study was conducted in the Bay of
Cartagena, a section of the coast of central
Chile directly exposed to prevailing southern
waves (Figure 1A). The site represents
an upwelling shadow [sensu Graham and
Largier, 1997], where waters remain slightly
warmer (1-2°C), nutrients slightly lower, and
phytoplankton blooms more common than at
sites to the north and south [Narváez et al.,
2004; Tapia et al., 2009; Wieters et al., 2003].
General hydrographic characteristics of the
study site have been previously described
[Bonicelli et al., 2014A; Bonicelli et al.,
2014B; Kaplan et al., 2003; Lagos et al., 2005;
Narváez et al., 2004; Navarrete et al., 2015;
Piñones et al., 2005]. The name of the study
site is somewhat deceiving because Cartagena
Bay is not a protected bay, but it is fully
exposed to the predominant incoming waves
propagating from the south (see [Parra & Beyá,
2017], www.oleaje.uv.cl/pronostico.html, and
“Results” in this paper).
We deployed four moorings at 20-21 m
bottom depths across the Bay of Cartagena,
covering about 5 km and separated by about
1.5 km (Figure 1A). In this manner, and since
the hydrographic conditions vary between
the northern and southern ends of Cartagena
Bay [Bonicelli et al., 2014A], we expected
Figure 1: A) Map of study site at the open embayment of Cartagena showing position of the moorings
and bathymetry. B) Monthly mean seawater temperature (+ SE) at surface (5 m deep) and deep (15
m deep) depths. C) Maximum daily wave height from the Global Forecast System numerical model
used by Windguru (see text). The map of study site has been adjusted from Navarrete et al. [2019].

76
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
to capture sufficient spatial variation in
biofouling across the moorings. Each mooring
consisted of a 150 kg weight and a line of high
tenacity polypropylene rope with a subsurface
buoy at about 1 m deep, and two small (50
cm diameter) buoys along the rope to keep
the line tense even during passing waves.
Testing frames were made of 2.5 cm diameter
hydraulic-rated PVC, forming a 70 x 40 cm
rectangle, and were deployed at two depths in
each mooring line, at about 5 m deep, above
the seasonal thermocline [Bonicelli et al.,
2014A; Narváez et al., 2004], and at about 15
m deep, below the thermocline. One replicate
of a 10 x 10 cm biofouling plate made of each
of the three materials and antifouling paint
(four treatments) was affixed to each frame
in a completely random pattern at each depth.
The size and hydraulic behaviour of the frame
did not allow us to include replicate plates of
each treatment within a frame. Additionally, we
attached temperature loggers (Onset Tidbit®),
which recorded temperature every 10 minutes
at about 2 m depth above the first frame and
at about 19 m depth below the deeper frame
in each mooring line. Wave height data were
obtained from Windguru (www.windguru.
cz), which is based on Global Forecast System
(GFS) numerical model. Predicted wave height
from this model has been shown to correlate
well with in-situ recorded waves at the study
site [Navarrete et al., 2015].
Placing the experimental plates above and
below the seasonal thermocline allowed us
to maximize differences in environmental
conditions within the water column. Besides
the seasonal differences in sea surface
temperature, one of the major drivers of
metabolic activity in ectothermic animals, the
thermocline typically marks abrupt changes in
concentration of Chlorophyll-a (higher right
above or at the thermocline) [Narváez et al.,
2004], the relative abundance of competent
larval stages [Bonicelli et al., 2014A; Vargas
et al., 2006], the influence of river plumes
[Piñones et al., 2005; Vargas et al., 2006], or
the frequency of hypoxic events.
Materials tested were a) aluminum
AA1100 temper h14 (99.0% aluminium,
with aluminium oxide finish), which is
used in many applications because of its
high corrosion resistance, b) High Density
Polyethylene (HDPE), a positively buoyant,
high durability material used in most
aquaculture operations, and c) construction
steel A36, used in the shipping industry and
in the experimental MRE technologies. Since
anticorrosive and antifouling paints do not
adhere well to aluminum and HDPE, they are
typically used without coatings. In addition
to these materials, we tested the efficacy of a
widely used antifouling, copper-based paint
(Ocean Jet, www.jet.com.pe/es) commercially
available in Chile. This antifouling paint is
based on high solid epoxy polyamine (with
micaceous iron oxide). Steel plates (A36)
with antifouling were painted at the ACN
Ltda. in Valdivia, Chile, following the same
procedures used in ships.
We measured surface roughness (SR) and
hydrophobic index (H) for each of the
three materials tested (aluminium AA1100,
HDPE, and steel A36) and for the AF
coating. We haphazardly chose one plate of
each surface and measured SR and H along
two perpendicular transects within a 4 x 2
cm area. Because of the widely different

The Journal of Ocean Technology, Vol. 15, No. 1, 2020
77
Copyright Journal of Ocean Technology 2020
roughness levels of the different plates, two
different instruments were used to measure
SR. The SR of aluminum and HDPE were
measured using a Bruker Innova Atomic
Force Microscope (AFM) and the SR of
steel and AF coating were measured using a
BioLogic Optical Surface Profiler (OSP470).
All measurements were then expressed
as RMS (mean square root) and given in
µm
2
. The surface hydrophobic index was
measured by determining the water contact
angle (WCA) following ASTM D7334-08
(ASTM International, 2013), using water-type
II reagent (distilled) after ASTM D1193-
06 (ASTM International, 2011). The index
was calculated by employing critical surface
tension theory, assigning hydrophilic index
WCA < 45°, hydrophobic index to WCA >
90°, and intermediate index for 45° < WCA <
90°. Finally, the quality of polymer adhesion
was verified by means of a tape-and-peel test,
conducted according to ASTM D3359-09ε2
standard (method A, ASTM International,
2010). Before deployment and during the
second and third monitoring dates (see
below), each plate was weighed in a precision
balance, both in air and submerged in water,
and then individually marked. Monitoring
was conducted by scuba diving. Plates were
photographed in-situ, then removed from the
frame and taken aboard the ILAN research boat
of the Estación Costera de Investigaciones
Marinas (ECIM), where they were weighed
on a precision scale after carefully cleaning
the sides and back, photographed, and then the
cover of all species was recorded with a 10 x
10 cm quadrat with 100 intersection points.
All species observed on the plate surfaces,
without disturbing the settled organisms,
were registered. Plates were then redeployed
in their original positions. Biofouling plates
were initially deployed in July 2017 and
monitored in November 2017 (97 days’
exposure) and then again in March 2018 (219
days’ exposure). On the second monitoring
date, several frames had been lost due to large
waves, which impeded us to analyze time
trajectories. Loss of moorings due to fatigue of
the anchoring lines did not allow us to extend
monitoring beyond March 2018.
Data Analyses
Total biofouling biomass on each plate was
obtained by subtracting the weight of the plate
from the total mass recorded during monitoring.
Total biofouling biomass accumulation rates
were calculated as the weight of biomass (g)
accumulated per plate (100 cm
2
) divided by the
number of days the plates were exposed in the
field (g/day/100 cm
2
).
Statistical comparisons of materials and depths
were conducted for biomass accumulation
rates and total cover and were restricted to the
first monitoring, after 97 days of exposure,
because two of the four replicates were lost
on the second monitoring. The experimental
design corresponded to a randomized complete
block design (four moorings as blocks),
with a two-way orthogonal structure within
each block, which corresponded to materials
(fixed factor with four levels) and depth (fix
factor with two levels). Biomass rates were
log-transformed, and cover data were arcsin-
square root transformed before analysis to meet
homoscedasticity assumptions and improve
normality. Results showed that blocks did
not make a significant contribution to overall
variance, even after using a conservative
significance level alpha =0.1 to reduce

78
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
type II error rate. Therefore, blocks and the
interactions with other factors were pooled
with residual variance (see “Results”). Because
no species settled and grew on the plates with
antifouling paint (see “Results”), this material
was not included in statistical analyses.
To examine possible change in species
composition among materials, we conducted a
non-metric multidimensional scaling (nMDS)
ordination using presence/absence data
including all sessile species recorded on the
plates. A Bray-Curtis similarity index was used.
RESULTS
As shown in previous studies, seawater
temperature was about 2-3 degrees warmer
and more seasonal at 5 m deep above the
thermocline than at 15 m deep below the
thermocline (Figure 1B). The study included
the austral winter period, when the water
column is well mixed and surface and bottom
temperatures are similar. Wave height exceeded
3 m during most of the study, with large storm
waves of over 5 m height in winter months and
a clear decrease towards spring and summer
months (Figure 1C).
The most common components of the
macrofouling were hydrozoans (primarily
Obelia geniculata), barnacles (primarily
Notobalanus flosculus and Austromegabalus
psittacus), mussels, and the tunicate Pyura
chilensis, which reached about 1% cover over
the duration of the study (averaging both
monitoring dates and depths, Table 1). The
encrusting alga Hildenbrandia lecannellieri
reached 30% in one plate of aluminum material
after three months’ exposure, but it was not
present on any other plate of the same or
different material. By the second monitoring
(> seven months), Hildenbrandia lecannellieri
had been completely overgrown by Obelia.
Other species observed on the plate surface
never reached over 1.5% cover.
At both depths, all materials, except plates
with antifouling paint, were rapidly colonized
by biofouling, which covered over 90% of
Table 1: List of encrusting taxa encountered throughout the study period at the two depths (5 and 15 m) and any of the three materials and
exposure times. Mean cover is the long-term average across depths and monitoring times.

The Journal of Ocean Technology, Vol. 15, No. 1, 2020
79
Copyright Journal of Ocean Technology 2020
the plate surface within the three-month time
elapsed between deployment and the first
monitoring (Figures 2-3; Figure S1). Over
this time, no differences between the surface
(5 m) and deeper (15 m) plates were observed
(Figure 3, Table 2). Although total biofouling
cover was slightly lower on aluminum than the
other two materials (91% versus 95%), these
differences were not statistically significant
at any depth (Table 2). The notable exception
was the steel plate painted with antifouling
paint, where virtually no macrofouling
settled throughout the seven months of the
experiment. This treatment was therefore left
out of statistical comparisons. After three
months of exposure, steel plates showed clear
signs of surface corrosion and some bacterial
mats were apparent among hydrozoans. By the
time of the second monitoring, the surface of
these plates had laminated and, in some cases,
peeled off the plate, removing in this way the
fouling organisms (Figure 2).
Rates of biomass accumulation (g/day) in the
100 cm
2
plates varied somewhat among the
three materials (Figure 4), but the differences
were not consistent between depths, and they
were not statistically significant (Table 2).
Overall, similar biomass accumulation rates
were observed in shallow and deeper waters
over the three-month time exposure. Again, no
settlement of macrofoulers was observed on
plates with antifouling paint.
By far the most abundant species in terms of
cover was the hydrozoan O. geniculata, which
covered over 80% of the plate surface after
three months of exposure at 5 m deep and over
70% at 15 m deep in all three materials (Figure
5A, B, C). The large barnacle A. psittacus also
settled in all materials but did not surpass 5%
cover within the first three months of plate
exposure. After seven months, this barnacle
species, as well as the mussel Semimytilus
algosus and the tunicate P. chilensis, were
present in all materials and started to overgrow
O. geniculata and reached over 10% cover
in most plates (Figure 5A, B, C). Biofouling
species composition, i.e., considering only
the presence/absence of species on the
different materials, showed that the biofouling
communities were not different among the
different materials (Figure 5D).
The surface roughness indices were widely
different among the three materials and the AF
coating (Table 3). Particularly, aluminium and
HDPE had similarly low SR values, compared
to steel and the AF paint (Table 3). The water
contact angle of HDPE, steel, and the AF
coating showed similar values of intermediate
hydrophobic character (see Table 3), while
aluminium had WCA exceeding 90°, indicating
high hydrophobic character (Table 3). Regardless
of these physical differences among surface
materials, no correlations were found with
biofouling biomass or cover (see Figure S2).
DISCUSSION
The adverse effects of biofouling growth
on all human-made structures deployed at
sea is an important consideration for all
marine industries. Strategies to reduce the
problem must also reduce the impacts in the
environment and different materials may
exhibit different susceptibility to colonization
and growth by diverse macrofouling species
and under different conditions. Our results
show that three of the most common materials

80
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
Figure 2: Photographs of
representative plates taken
at the first (about three
months’ field exposure) and
second monitoring (about
seven months’ exposure) for
each material used (HDPE,
aluminium, steel), antifouling
paint (AF paint), and at 5 m of
depth and 15 m of depth.
Figure 3: Mean total cover (+SE)
of biofouling that settled on
the experimental plates of the
different materials and at 5 m of
depth and 15 m of depth.

The Journal of Ocean Technology, Vol. 15, No. 1, 2020
81
Copyright Journal of Ocean Technology 2020
Figure 4: Mean rate of biomass
accumulation (g/day/100 cm2)
on the experimental plates of the
different materials observed at 5 m
of depth and 15 m of depth.
Figure 5: Average cover (%) of the main fouling species observed on A) aluminium, B) steel, and C) HDPE, during the first monitoring (about
three months’ field exposure) and at the second monitoring (about seven months’ exposure) and at the two deployment depths (5 and 15
m). D) Multivariate ordination of biofouling community found on plates of the different tested materials at the two depths using non-metric
multidimensional scaling on presence/absence data. Legend with colour codes are reported below the graphs.

82
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
used in the maritime industry are equally
susceptible to fouling and exhibit similar
biomass accumulation rates and biofouling
community composition in wave exposed
habitats of central Chile. Thus, even though
studies on other shores have found that
surface roughness and hydrophobic index can
have large effects on biofouling composition
and colonization rates [e.g., Calow and Calow,
2011], we found no evidence of such effects
on macrofoulers in our study, highlighting the
strong dependency of macrofouler-surface
interactions on environmental conditions
[Howell and Beherends, 2006]. We also
found that a copper-based antifouling paint
prevents any colonization by macrofoulers
for over seven months under these high-
energy environmental conditions. We suggest
that this paint could be used a reference
when testing more environmentally-friendly
coatings, such as those using biomimetic
approaches [Salta et al., 2010]. We discuss
these findings in light of results obtained in
other wave-exposed shores of the world and
from protected conditions in Chile.
Several studies have shown that the biofouling
community composition varies among different
substrates at the early succession stages because
the physical-chemical characteristics of the
material surface can affect the colonization
process [Carr and Hixon, 1997; Russ, 1977;
Walters and Wethey, 1996]. Anderson and
Underwood [1994] compared different
substrates (concrete, plywood, fibreglass,
and aluminum) in one bay of Australia,
and concluded that the assemblages were
significantly different after one or two months
Table 2: Results of two-way ANOVA (analysis of variance) comparing a) total biofouling cover (% arsin-sqrt-transformed) and b) rates of
biofouling biomass accumulation (g/day, log-transformed) in the 100 cm2 plates among the three materials on which we observed settlement
(aluminum, HDPE, steel) and the two deployment depths (5 and 15 m).
Table 3: Results of the analysis of surface roughness and hydrophobic character of the three materials (aluminium, HDPE, and steel) and
antifouling (AF) paint. RMS=Root Mean Square; WCA=Water Contact Angle; High=WCA<90; Intermediate= 45<WCA<90.

The Journal of Ocean Technology, Vol. 15, No. 1, 2020
83
Copyright Journal of Ocean Technology 2020
of exposure, but they become similar after four
or five months of submersion, depending on
the season of the year. Thus, after a differential
colonization processes on various surfaces,
the community becomes more similar in all
the materials by converging to similar sets of
dominant species [see also Andersson et al.,
2009; McGuiness, 1989]. Similar results were
observed by Chapman and Clynick [2006],
who compared organisms on different types of
waste material (tires, wood, metal, and natural
sandstone) in Australian estuaries and found,
after 19 months, that algal and invertebrate
compositions were similar among the different
substrates. In a different study conducted
along two breakwaters and a natural reef on
the shore of Dubai, United Arab Emirates,
Burt et al. [2009] compared various materials
(concrete, gabbro, granite, and sandstone) and
concluded that, after one year, observed site-
specific differences in recruitment were more
important in determining benthic community
structure and coral recruitment than differences
among substrate materials. Similar results
have been observed along the Mediterranean
shore of Italy [Chapman and Bulleri, 2003].
Thus, most studies that have experimentally
exposed different surfaces to the same or
similar environmental conditions and, in this
manner, they have controlled the time of
biofouling succession, indicate that the type of
substratum can affect initial colonization but
does not usually alter later successional stages
and the final established biofouling community
is generally similar across materials. Similar
results were observed in our experimental
study in wave-exposed subtidal habitats, as
well as in a previous study in which acrylic and
ceramic tiles were compared at the same site
[Navarrete et al., 2019]. Our results show that
after only three months, HDPE, steel A36, and
aluminum were almost completely covered by
biofouling and exhibited the same dominant
species, the hydrozoan Obelia geniculata, and
similar species composition. After seven months
of exposure, competitively dominant species,
especially large-bodied barnacles and tunicates,
started to overcome O. geniculata in all
surfaces, but Obelia was still the most abundant
species in terms of surface cover. Thus, the risks
of fouling among these materials for aquaculture
and MRE applications are the same. It should be
noted, however, that the loss of metal material
(lamination and detachment of surface layers)
in the untreated (unpainted) steel plates after
three months also removed some of the attached
organisms, which would lead to differences in
the established community with other materials.
But loss of structural material can hardly be a
useful antifouling strategy, and we consider that
during the useful period of time untreated steel
can be deployed (< three months), the fouling
risk is similar to the other materials.
As other authors have emphasized, caution
must be exerted when comparing biofouling
communities in different surfaces through
surveys of existing structures in different
habitats and for sometimes unknown periods
of time [Connell and Glasby, 1999; Macleod
et al., 2016; Manríquez et al., 2014; Want et
al., 2017]. For instance, Connell and Glasby
[1999] compared various surfaces (rocky reef,
sandstone (brick) retaining walls, fibreglass,
concrete pontoons, concrete pilings, and wooden
pilings with bark and stripped of bark) with
different times of submersion in an Australian
shore and found differences of compositions
among the surfaces. But such differences
could be best explained by differences in

84
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
environmental conditions, orientation, and wave
exposure, instead of surface materials, as also
shown in other studies [Bulleri and Chapman,
2004]. Because of slight or large differences
in environmental conditions, total biofouling
species diversity is typically higher in studies
conducting surveys across space than in studies
that expose materials to more homogeneous
conditions. Such differences in species richness
may also confuse conclusions regarding true
biofouling susceptibility across materials and
emphasize the importance of testing antifouling
strategies in a replicated test bench where
environmental conditions are similar and time of
succession can be controlled.
Our results also show the very high rates of
biomass accumulation attained in southeastern
Pacific coastal waters [Navarrete et al., 2019;
Viviani and DiSalvo, 1980]. After seven months,
we observed the equivalent of over 30 kg/m
2
of
biofouling biomass. At the end of this period of
time, most of this biomass (> 65%) was due to
large rigid barnacle A. psittacus and the large
tunicate P. chilensis, which, besides the large
weight they impose on the structure, can greatly
increase drag forces in moving objects in the
water, such as boats or turbines. Unfortunately,
loss of replicate mooring lines prevented
us from running more detailed statistical
comparisons. It is interesting to note that in this
study we did not observe differences in biomass
accumulation rates between depths, above (5
m deep) or below (15 m deep) the thermocline.
This result contrasts with a previous study
at the same site showing significantly larger
biomass accumulation on acrylic and ceramic
tiles in water shallower than the thermocline
than below [Navarrete et al., 2019]. We believe
the difference between studies is at least partly
related to the fact that water temperature was
particularly low during most of the spring 2017.
Mean temperatures during austral spring and
summer were between 1 and 1.2 degrees colder
in 2017 than over the equivalent period in 2016,
and more homogeneous between 5 and 15 m
deep. In 2016 surface water remained below
12.5°C until mid-December, while it had already
reached over 13.5° in early November 2017.
Such low temperatures in surface waters into
late spring may have reduced the reported depth-
stratification in biofouling biomass accumulation
in 2016 as compared to previous years.
Application of effective antifouling strategies
is therefore absolutely necessary for most
aquaculture applications [Bostock et al.,
2010] and to test most of the wave-energy
technologies currently being developed
[López et al., 2013; Want et al., 2017]. To
have a reference to compare against the
untreated surface materials, here we tested
the effectivity of a commonly used copper-
based antifouling paint, Ocean Jet, applied
on steel plates following the same procedure
used on ships hulls. This initial comparison
showed that over the >seven-month long
exposure, the antifouling paint was effective
in preventing settlement by all early and
late successional macrofouling species,
including macroalgae, sessile, and mobile
invertebrates. Invertebrates and macroalgae
were observed on the bolt head that held the
plate in place and on the PVC frame right next
to the plate, suggesting that the antifouling
action is primarily by direct contact with
settling organisms. However, copper and
zinc-based coatings leach these elements
into the environment, where over time they
can accumulate and have large negative

The Journal of Ocean Technology, Vol. 15, No. 1, 2020
85
Copyright Journal of Ocean Technology 2020
environmental impacts [Dafforn et al., 2011;
Soroldoni et al., 2017; Turner, 2010]. Yet,
over the short term, some studies show no
negative effect of exposure to antifouling
copper paints on key intertidal grazers [Corte
et al., 2017]. It is therefore urgent to increase
research on alternative antifouling products
and strategies that are naturally found in the
environment where human-made structures
are deployed [Silva-Aciares and Riquelme,
2008; Almeida and Vasconcelos, 2015; Salta
et al., 2010] and to evaluate the effect of
these artificial habitats on macroinvertebrates
colonization [Fernandez-Gonzalez et al.,
2016]. The efficiency of the tested antifouling
paint and apparent harmless local effects in
nearby surfaces suggest this paint can be used
as a reference to contrast environmentally-
friendly antifouling strategies in wave-
exposed environments.
In summary, different artificial materials
commonly used in the maritime industry
were rapidly colonized and overgrown
by encrusting biofouling species of wave
exposed shores of central Chile. The
composition, cover, and the rate of biomass
accumulation of the main fouling species
were similar among the three materials tested,
and similar at two different depths, above
and below the thermocline. The hydrozoan
Obelia geniculata was the most frequent and
abundant (cover) species in all surfaces, and
the larger bodied barnacle Austromegabalus
psittacus, mussels, and tunicates increased
in abundance later in succession, accounting
for most of the wet biomass. We also
showed that differences in surface roughness
and hydrophobic properties among tested
materials were not sufficient to affect the
rapid growth rate of the most common
biofouling species found in the species pool
at our study site. Finally, an antifouling
paint widely used in shipping operations
was very effective in preventing all fouling,
macroalgae, and invertebrates at both depths
and through more than seven months.
ACKNOWLEDGMENTS
The authors thank Professor J. Francisco Armijo
(Faculty of Chemistry and Pharmacy, Pontifical
Catholic University of Chile) for providing the
analysis of surface roughness and hydrophobic
character for the materials tested in this study.
This study was possible thanks to financial
support of the Marine Energy Research and
Innovation Center, MERIC, an applied research
centre funded by the Ministry of Energy and the
Production Development Corporation, project
CORFO 14CEI2-28228. Additional funding was
provided by FONDECYT, grant N°3160294
to Jessica Bonicelli, grant #1151095 and grant
#1160289 to Sergio A. Navarrete.
CONTRIBUTION STATEMENT
Sergio A. Navarrete , Mirtala Parragué , Nicole
Osiadacz, and Randy Finke conceived the
experiment, the experimental design, and the
mooring test frame system. Mirtala Parragué,
Nicole Osiadacz, Francisca Rojas, Jessica
Bonicelli, and Randy Finke participated in
the field work and/or laboratory analyses.
Sergio A. Navarrete, Mirtala Parragué, Nicole
Osiadacz, Francisca Rojas, Jessica Bonicelli,
Miriam Fernández, Clara Arboleda-Baena,
Randy Finke, and Simone Baldanzi discussed
the results, analyzed data, and contributed to
manuscript preparation.

86
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
APPENDICES
Figure S1: Total cover of
biofouling by monitoring date
after 97 and 219 days.
Figure S2: Scatter plots between
biofouling measures and the physical
properties of the materials used (HDPE,
aluminum, steel, and antifouling paint).
A) Total biofouling biomass and surface
roughness; B) Total biofouling biomass
and hydrophobic index; C) Total cover
and surface roughness; D) Total cover
and hydrophobic index.

The Journal of Ocean Technology, Vol. 15, No. 1, 2020
87
Copyright Journal of Ocean Technology 2020
REFERENCES
Almeida, J.R. and Vasconcelos, V. [2015].
Natural antifouling compounds:
Effectiveness in preventing invertebrate
settlement and adhesion. Biotechnology
Advances, Vol. 33, No. 3-4, pp. 343-357.
Anderson, M.J. and Underwood, A.J. [1994].
Effects of substratum on the recruitment
and development of an intertidal estuarine
fouling assemblage. Journal of
Experimental Marine Biology and Ecology,
Vol. 184, pp. 217-236.
Andersson, M.H.; Berggren, M.; Wilhelmsson,
D.; and Ohman, M.C. [2009]. Epibenthic
colonisation of concrete and steel pilings
in a cold-temprate embayment: a field
experiment. Helgoland Marine Research,
Vol. 63, pp. 249-260.
Arinaga, R.A. and Cheung, K.F. [2012].
Atlas of global wave energy from 10 years
of reanalysis and hindcast data. Renewable
Energy, Vol. 39, pp. 49-64.
Berlow, E.L. [1997]. From canalization to
contingency: historical effects in a successional
rocky intertidal community. Ecological
Monographs, Vol. 67, pp. 435-460.
Bertness, M.D.; Gaines, S.D.; and Yeh, S.M.
[1998]. Making mountains out of barnacles:
the dynamics of acorn barnacle hummocking.
Ecology, Vol. 79, pp. 1382-1394.
Bonicelli, J.; Moffat, C.; Navarrete, S.A.;
and Tapia, F.J. [2014A]. Spatial differences
in thermal structure and variability within a
small bay: interplay of diurnal winds and
tides. Continental Shelf Research, Vol. 88,
pp. 72-80.
Bonicelli, J.; Tapia, F.J.; and Navarrete, S.A.
[2014B]. Wind-driven diurnal temperature
variability across a small bay and the spatial
pattern of intertidal barnacle settlement.
Journal of Experimental Marine Biology
and Ecology, Vol. 461, pp. 350-356.
Bostock, J.; McAndrew, B.; Richards, R.;
Jauncey, K.; Telfer, T.; Lorenzen, K.; Little,
D.; Ross, L.; Handisyde, N.; Gatward, I.;
and Corner, R. [2010]. Aquaculture: global
status and trends. Philosophical Transactions
of the Royal Society B - Biological Sciences,
Vol. 365, pp. 2897-2912.
Bulleri, F. and Chapman, M.G. [2004].
Intertidal assemblages on artificial and
natural habitats in marinas on the north-
west coast of Italy. Marine Biology, Vol.
145, pp. 381-391.
Burt, J.; Bartholomew, A.; Bauman, A.; Saif,
A.; and Sale, P.F. [2009]. Coral recruitment
and early benthic community development
on several materials used in the construction
of artificial reefs and breakwaters. Journal
of Experimental Marine Biology and
Ecology, Vol. 373, pp. 72-78.
Callow, J.A. and Callow, M.E. [2011]. Trends
in the development of environmentally
friendly fouling-resistant marine coatings.
Nature Communications, Vol. 2, pp. 244.
Caro, A.U.; Navarrete, S.A.; and Castilla, J.C.
[2010]. Ecological convergence in a rocky
intertidal shore metacommunity despite
high spatial variability in recruitment
regimes. Proceedings of the National
Academy of Sciences of the United States
of America, Vol. 107, pp. 18528-18532.
Carr, M.H. and Hixon, M.A. [1997]. Artificial
reefs: the importance of comparison with
natural reefs. Fisheries, Vol. 22, pp. 28-33.
Carrington, E.; Moeser, G.M.; Dimond,
J.; Mello, J.J.; and Boller, M.L. [2009].
Seasonal disturbance to mussel beds: field
test of a mechanistic model predicting wave

88
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
dislodgment. Limnology and Oceanography,
Vol. 54, pp. 978-986.
Chapman, M.G. and Bulleri, F. [2003].
Intertidal seawalls: new features of
landscape in intertidal environments.
Landscape and Urban Planning, Vol. 62, pp.
159-172.
Chapman, M.G. and Clynick, B.G. [2006].
Experiments testing the use of waste
material in estuaries as habitat for subtidal
organisms. Journal of Experimental Marine
Biology and Ecology, Vol. 338, pp. 164-178.
Connell, S.D. and Glasby, T.M. [1999]. Do
urban structures influence local abundance
and diversity of subtidal epibiota? A case
study from Sydney Harbour, Australia.
Marine Environmental Research, Vol. 47,
pp. 373-387.
Cornett, A.M. [2008]. A global wave enery
resource assessment. In: Chung, J.S. (ed.).
Proceedings of the Eighteenth International
Society Offshore and Polar Engineers,
Cupertino, pp. 318-326.
Corte, G.N.; Martinez, A.S.; and Coleman,
R.A. [2017]. Short-term exposure to
antifouling copper paint does not affect a
key intertidal grazer. Journal of
Experimental Marine Biology and Ecology,
Vol. 493, pp. 14-19.
Dafforn, K.A.; Lewis, J.A.; and Johnston, E.L.
[2011]. Antifouling strategies: history and
regulation, ecological impacts and
mitigation. Marine Pollution Bulletin, Vol.
62, pp. 453-465.
Fernandez-Gonzalez, V.; Martinez-Garcia, E.;
and Sánchez-Jerez, P. [2016]. Role of
fish farm fouling in recolonisation of
nearby soft-bottom habitats affected by
coastal aquaculture. Journal of
Experimental Marine Biology and Ecology,
Vol. 474, pp. 210-215.
Gentry, R.R.; Froehlich, H.E.; Grimm, D.;
Kareiva, P.; Parke, M.; Rust, M.; Gaines,
S.D.; and Halpern, B.S. [2017A]. Mapping
the global potential for marine aquaculture.
Nature Ecology and Evolution, Vol. 1, pp.
1317-1324.
Gentry, R.R.; Lester, S.E.; Kappel, C.V.;
White, C.; Bell, T.W.; Stevens, J.; and
Gaines, S.D. [2017B]. Offshore
aquaculture: spatial planning principles
for sustainable development. Ecology and
Evolution, Vol. 7, pp. 733-743.
Graham, W.M. and Largier, J.L. [1997].
Upwelling shadows as nearshore retention
sites: the example of northern Monterey
Bay. Continental Shelf Research, Vol. 17,
pp. 509-532.
Howell, D. and Beherends, B. [2006]. A review
of surface roughness in antifouling coatings
illustrating the importance of cutoff length.
Biofouling, Vol. 22, pp. 401-410.
Kaplan, D.M.; Largier, J.L.; Navarrete, S.A.;
Guiñez, R.; and Castilla, J.C. [2003]. Large
diurnal temperature fluctuations in the
nearshore water column. Estuarine Coastal
and Shelf Science, Vol. 57, pp. 385-398.
Lacoste, E. and Gaertner-Mazouni, N. [2015].
Biofouling impact on production and
ecosystem functioning: a review for bivalve
aquaculture. Reviews in Aquaculture, Vol.
7, pp. 187-196.
Lagos, N.; Navarrete, S.A.; Véliz, F.; Masuero,
A.; and Castilla, J.C. [2005]. Meso-scale
spatial variation in settlement and
recruitment of intertidal barnacles along
central Chile. Marine Ecology Progress
Series, Vol. 290, pp. 165-178.
López, I.; Andreu, J.; Ceballos, S.; I.M., d.A.;
and Kortabarria, I. [2013]. Review of wave

The Journal of Ocean Technology, Vol. 15, No. 1, 2020
89
Copyright Journal of Ocean Technology 2020
energy technologies and the necessary
power-equipment. Renewable and Sustainable
Energy Reviews, Vol. 27, pp. 413-434.
Lucero, F.; Catalan, P.A.; Ossandon, A.; Beya,
J.; Puelma, A.; and Zamorano, L. [2017].
Wave energy assessment in the central-
south coast of Chile. Renewable Energy,
Vol. 114, pp. 120-131.
Macleod, A.K.; Stanley, M.S.; Day, J.G.; and
Cook, E.J. [2016]. Biofouling community
composition across a range of
environmental conditions and geographical
locations suitable for floating marine
renewable energy generation. Biofouling,
Vol. 32, pp. 261-276.
Manríquez, P.H.; Fica, E.; Ortiz, V.; and
Castilla, J.C. [2014]. Bio-incrustantes
marinos en el canal de Chacao, Chile: un
estudio sobre potenciales interacciones con
estructuras manufacturadas por el hombre.
Revista de Biologia Marina y Oceanografria,
Vol. 49, pp. 243-265.
McGuiness, K.A. [1989]. Effects of some
natural and artificial substrata on sessile
marine organisms at Galeta Reef, Panama.
Journal of Experimental Marine Biology
and Ecology, Vol. 104, pp. 97-123.
Mork, G.; Barstow, S.; Kabuth, A.; and Pontes,
M.T. [2010]. Assessing the global wave
energy potential. 29th International
Conference on Ocean, Offshore Mechanics
and Arctic Engineering. OMAE2010 –
20473.
Nall, C.R.; Schläppy, M.-L.; and Guerin, A.J.
[2017]. Characterisation of the biofouling
community on a floating wave energy
device. Biofouling, Vol. 33, pp. 379-396.
Narváez, D.A.; Poulin, E.; Leiva, G.;
Hernández, E.; Castilla, J.C.; and Navarrete,
S.A. [2004]. Seasonal and spatial variation
of nearshore hydrographic conditions in
central Chile. Continental Shelf Research,
Vol. 24, pp. 279-292.
Navarrete, S.A. [2007]. Maintenance of
biodiversity. In: Denny, M.W. and Gaines,
S.D. (eds.). Encyclopedia of tidepools and
rocky shores. University of California
Press, Los Angeles, pp. 76-81.
Navarrete, S.A.; Largier, J.L.; Vera, G.; Tapia,
F.J.; Parrague, M.; Ramos, E.; Shinen,
J.L.; Stuardo, C.A.; and Wieters, E.A.
[2015]. Tumbling under the surf: wave-
modulated settlement of intertidal mussels
and the continuous settlement-relocation
model. Marine Ecology Progress Series,
Vol. 520, pp. 101-121.
Navarrete, S.A.; Parragué, M.; Osiadacz,
N.; Rojas, F.; Bonicelli, J.; Fernandez, M.;
Arboleda-Baena, C.; Perez-Matus, A.; and
Finke, G.R. [2019]. Biofouling abundance
and composition in high wave-energy
coastal environments of Central Chile:
temporal and depth variation. Journal of
Experimental Marine Biology and Ecology,
Vol. 512, pp. 51-62.
Paine, R.T. [1984]. Ecological determinism in
the competition for space. Ecology, Vol. 65,
pp. 1339-1348.
Parra, C. and Beyá, J. [2017]. Pronóstico
operacional de oleaje para las costas
y puertos de Chile. Sociedad Chilena de
Ingeniería Hidráulica. XXIII Congreso
Chileno de Ingeniería Hidráulica.
Petraitis, P.S. and Dudgeon, D. [1999].
Experimental evidence for the origin of
alternative communities on rocky intertidal
shores. Ecology,Vol. 80, pp. 429-442.
Petraitis, P.S. and Dudgeon, S.R. [2005].
Divergent succession and implications for
alternative states on rocky intertidal shores.

90
The Journal of Ocean Technology, Vol. 15, No. 1, 2020
Copyright Journal of Ocean Technology 2020
Journal of Experimental Marine Biology
and Ecology, Vol. 326, pp. 14-26.
Piñones, A.; Valle-Levinson, A.; Narváez,
D.A.; Vargas, C.A.; Navarrete, S.A.; Yuras,
G.; and Castilla, J.C. [2005]. Wind-induced
diurnal variability in river plume motion.
Estuarine Coastal and Shelf Science, Vol.
65, pp. 513-525.
Richmond, M.D. and Seed, R. [1991]. A review
of marine macrofouling communities with
special reference to animal fouling.
Biofouling, Vol. 3, pp. 151-168.
Russ, G. [1977]. A comparison of marine
fouling occurring at the two principle
Australian Naval Dockyards (ReportMRL-
R-688). In: Melbourne: Department of
Defense, M.R.L. (ed.), Melbourne, Australia.
Salta, M.; Wharton, J.A.; Stoodley, P.;
Dennington, S.P.; Goodes, L.R.; Werwinski,
S.; Mart, U.; Wood, R.J.; and Stokes, K.R.
[2010]. Designing biomimetic antifouling
surfaces. Philosophical Transactions of the
Royal Society A - Mathematics Physical
and Engineering Sciences, Vol. 368, pp.
4729-4754.
Salta, M.; Wharton, J.; Blanche, Y.; Stokes,
K.; and Briand, J.-F. [2013]. Marine
biofilms on artificial surfaces: structure and
dynamics. Environmental Microbiology,
Vol. 15, No. 11, pp. 2879-2893.
Schultz, M.P. [2007]. Effects of coating roughness
and biofouling on ship resistance and
powering. Biofouling, Vol. 23, pp. 331-341.
Silva-Aciares, F.R. and Riquelme, C.E.
[2008]. Comparisons of the growth of six
diatom species between two configurations
of photobioreactors. Aquacultural
Engineering, Vol. 38, No. 1, pp. 26-35.
Soroldoni, S.; Abreu, F.; Castro, I.B.; Duarte,
F.A.; and Pinho, G.L.L. [2017]. Are
antifouling paint particles a continuous
source of toxic chemicals to the marine
environment? Journal of Hazardous
Materials, Vol. 30, pp. 76-82.
Sutherland, J.P. [1974]. Multiple stable points
in natural communities. American
Naturalist, Vol. 108, pp. 859-873.
Tapia, F.J.; Navarrete, S.A.; Castillo, M.;
Menge, B.A.; Castilla, J.C.; Largier, J.;
Wieters, E.A.; Broitman, B.L.; and Barth,
J.A. [2009]. Thermal indices of upwrelling
effects on inner-shelf habitats. Progress in
Oceanography, Vol. 83, pp. 278-287.
Titah-Benbouzid, H. and Benbouzid, M.
[2015]. Marine renewable energy converters
and biofouling: a review on impacts and
rrevention. 2015 EWTEC, Nantes, France.
Titah-Benbouzid, H. and Benbouzid, M. [2017].
Biofouling issue on marine renewable energy
converters: a state of the art review on impacts
and prevention. International Journal on
Energy Conversion, Vol. 5, pp. 67-78.
Troell, M.; Joyce, A.; Chopin, T.; Neori, A.;
Buschmann, A.H.; and Fang, J.G. [2009].
Ecological engineering in aquaculture -
potential for integrated multi-trophic
aquaculture (IMTA) in marine offshore
systems. Aquaculture, Vol. 297, pp. 1-9.
Turner, A. [2010]. Marine pollution from
antifouling paint particles. Marine Pollution
Bulletin, Vol. 60, pp. 159-171.
Vargas, C.A.; Narváez, D.A.; Piñones, A.;
Navarrete, S.A.; and Lagos, N.A. [2006].
River plume dynamic infuences transport
of barnacle larvae in the inner shelf of
central Chile. Journal of the Marine
Biological Association, U.K., Vol. 86, pp.
1057-1065.
Vieira, E.A.; Flores, A.A.V.; and Dias, G.M.
[2018]. Persistence and space preemption

The Journal of Ocean Technology, Vol. 15, No. 1, 2020
91
Copyright Journal of Ocean Technology 2020
explain species-specific founder effects on
the organization of marine sessile
communities. Ecology and Evolution, Vol.
8, pp. 3430-3442.
Viviani, C.A. and DiSalvo, D.H. [1980].
Biofouling in a north central coastal bay.
5th International Congress on Marine
Corrosion and Biofouling. Editorial Garsi,
Barcelona, Spain, pp. 69-74.
Walters, L.J. and Wethey, D.S. [1996].
Settlement and early post-settlement
survival of sessile marine invertebrates
on topographically complex surfaces: the
importance of refuge dimension and adult
morphology. Marine Ecology Progress
Series, Vol. 137, pp. 161-171.
Want, A.; Crawford, R.; Kakkonen, J.; Kiddie,
G.; Miller, G.; Harris, R.E.; and Porter,
J.S. [2017]. Biodiversity characterisation
and hydrodynamic consequences of marine
fouling communities on marine renewable
energy infrastructure in the Orkney Islands
Archipelago, Scotland, UK. Biofouling, Vol.
33, No. 7, pp. 567-579.
Wieters, E.A.; Kaplan, D.M.; Navarrete, S.A.;
Sotomayor, A.; Largier, J.; Nielsen, K.J.;
and Véliz, F. [2003]. Alongshore and
temporal variability in chlorophyll a
concentration in Chilean nearshore waters.
Marine Ecology Progress Series, Vol. 249,
pp. 93-105.
Wootton, J.T. [2005]. Field parameterization and
experimental test of the neutral theory of
biodiversity. Nature, Vol. 433, pp. 309- 312.