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RESEARCH ARTICLE
Successional dynamics of marine fouling
hydroids (Cnidaria: Hydrozoa) at a finfish
aquaculture facility in the Mediterranean Sea
Luis Martell
1,2
*, Roberta Bracale
2
, Steven A. Carrion
3
, Jennifer E. Purcell
4
, Marco Lezzi
2
,
Cinzia Gravili
2,5
, Stefano Piraino
2,5
, Ferdinando Boero
2,5,6
1University Museum of Bergen, Department of Natural History, University of Bergen, Bergen, Norway,
2Dipartimento di Scienze e Tecnologie Biologiche e Ambientali, Universitàdel Salento, Lecce, Italy,
3University of Central Florida, Orlando, Florida, United States of America, 4Western Washington
University, Bellingham, Washington, United States of America, 5CoNISMa, Consorzio Nazionale
Interuniversitario per le Scienze del Mare, Rome, Italy, 6CNR-ISMAR, Istituto di Scienze Marine del
Consiglio Nazionale delle Ricerche, UO Genova, Genoa, Italy
*luisfmartell@gmail.com
Abstract
Aquaculture is increasing rapidly to meet global seafood demand. Some hydroid popula-
tions have been linked to mortality and health issues in finfish and shellfish, but their dynam-
ics in and around aquaculture farms remain understudied. In the present work, two
experiments, each with 36 panels, tested colonization (factors: depth, season of immersion)
and succession (factors: depth, submersion duration) over one year. Hydroid surface cover
was estimated for each species, and data were analyzed with multivariate techniques. The
assemblage of hydrozoans was species-poor, although species richness, frequency and
abundance increased with time, paralleling the overall increase in structural complexity of
fouling assemblages. Submersion duration and season of immersion were particularly
important in determining the species composition of the assemblages in the succession and
colonization experiments, respectively. Production of water-borne propagules, including
medusae, from the hydroids was observed from locally abundant colonies, among them the
well-known fouling species Obelia dichotoma, potentially representing a nuisance for cul-
tured fish through contact-driven envenomations and gill disorders. The results illustrate the
potential importance of fouling hydroids and their medusae to the health of organisms in the
aquaculture industry.
Introduction
Aquaculture is playing an increasing role in meeting the protein needs of the growing world
population [1]. The development of new aquaculture facilities has led to an increase in sub-
merged structures such as floats, ropes, cages and nets that inadvertently provide favourable
substrates for fouling organisms [2]. These biofoulers greatly interfere with culture operations,
produce significant economic impacts on marine aquaculture, and are widely recognized as
PLOS ONE | https://doi.org/10.1371/journal.pone.0195352 April 2, 2018 1 / 18
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OPEN ACCESS
Citation: Martell L, Bracale R, Carrion SA, Purcell
JE, Lezzi M, Gravili C, et al. (2018) Successional
dynamics of marine fouling hydroids (Cnidaria:
Hydrozoa) at a finfish aquaculture facility in the
Mediterranean Sea. PLoS ONE 13(4): e0195352.
https://doi.org/10.1371/journal.pone.0195352
Editor: Erik V. Thuesen, Evergreen State College,
UNITED STATES
Received: December 15, 2017
Accepted: March 20, 2018
Published: April 2, 2018
Copyright: ©2018 Martell et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: This work was supported by grants from
the National Council of Science and Technology of
Mexico (CONACyT, Mexico) [312520 to LM], and
the Ronald E. McNair Post baccalaureate
Achievement Program (Department of Education,
U. S. A.) [P217A120229 to SAC]. The funders had
no role in study design, data collection and
one of the main problems faced by any aquaculture facility: the annual direct economic cost of
controlling biofouling on aquaculture is estimated conservatively around 5–10% of the indus-
try value [3].
Common detrimental effects of biofouling in aquaculture include significant increases in
the weight and drag of submerged structures, reduction of water flow through the nets of the
cages, which compromises the environmental quality for fish and shellfish in terms of oxygen
concentration and food limitation, overgrowth of shellfish stocks, and skin and gill lesions and
disease in fish [2,4–6]. Current antifouling strategies have been unable to cope efficiently with
fouling, and further research on the dynamics of colonization and succession of fouling organ-
isms is needed in order to prevent and manage biofouling in aquaculture [7–8].
Hydrozoans are a common component of biofouling assemblages in aquaculture facilities.
They are renowned for their diverse reproductive patterns, ranging from completely benthic
life cycles to completely pelagic ones, with >700 species having a combination of benthic and
pelagic stages [9]. The most familiar forms, attached hydroids and swimming medusae, occur
in aquaculture facilities worldwide. Benthic hydroids have been linked to a wide array of nega-
tive effects on shellfish and finfish culture, including net occlusion, reduced water flow, smoth-
ering of shells, devaluation of final products, competition with target species for food and
space, disruption of feeding and valve opening, direct lesions, and disease transmission [2,5,
10]. The medusae and other planktonic propagules produced by some of these hydroids can
equally cause skin and gill damage in farmed fish by their stinging cnidocytes and injectable
venoms, making cultured fish prone to bacterial infections and increased mortality [11–14].
Many species of hydrozoans foul aquaculture facilities around the world, yet most scientific
knowledge on hydroid fouling comes from studies on the large and highly damaging species
belonging to the families Tubulariidae (mainly members of genus Ectopleura) and Campanu-
lariidae [15–20]. Unfortunately, studies on biofouling usually put all hydrozoans in one cate-
gory, thus preventing analysis of the hydroid fouling dynamics and medusa production at the
population and species level. An exception to this is the thesis of Bosch-Belmar [13], which
examined both the fouling hydroids attached to the nets of the fish pens and the small repro-
ductive stages they produce that can enter the gill chambers of the fish damaging them with
stinging capsules (nematocysts). The author detailed the composition, growth and reproduc-
tive periods of hydroid assemblages on fish pens, as well as the planktonic stages of hydrozoans
and gill damage and mortality of fish at two aquaculture facilities along the Mediterranean
coast of southern Spain. Production of the planktonic propagules increased beginning 5
months after net installation, while abundances of the hydrozoans peaked in spring and
autumn and coincided with fish kills by planktonic propagules of Ectopleura larynx (Ellis &
Solander, 1786) and gill damage by all hydrozoans in the water [13–14].
The objectives of the present work were to describe the colonization and succession of foul-
ing hydrozoan assemblages on panels immersed beside an aquaculture facility at Taranto, Italy
(Central Mediterranean Sea) to test the roles of seasonality, submersion duration, and depth in
the structuring of the fouling hydroid assemblages and to identify the species of fouling hydro-
zoans potentially harmful to the farmed fish in the aquaculture facility. Two experiments tested
colonization (factors: depth, season of immersion) and succession (factors: depth, submersion
duration) throughout one year in the central Mediterranean Sea.
Material and methods
Study area
The study was conducted at an aquaculture facility that produces sea bass (Dicentrarchus lab-
rax (Linnaeus, 1758)) and sea bream (Sparus aurata Linnaeus, 1758) located in an area of
Hydroid succession dynamics in a fish farm
PLOS ONE | https://doi.org/10.1371/journal.pone.0195352 April 2, 2018 2 / 18
analysis, decision to publish, or preparation of the
manuscript.
Competing interests: The authors have declared
that no competing interests exist.
muddy and sandy bottoms at the eastern sector of the Mar Grande basin in the Gulf of
Taranto, NW Ionian Sea (40˚ 25’ 46.1” N, 17˚ 14’ 23.7” E). No permits were required for the
described study, which complied with all relevant regulations. Mar Grande, with about 36 km
2
area and 42 m of maximum depth [21], is a partially-enclosed basin hosting a wide array of
nautical, industrial, productive, and commercial activities. The waters around Taranto rou-
tinely receive urban and industrial waste, which together with the intense ship traffic, have
contributed to the high environmental stress observed in this area for decades [22]. On the
other hand, the region historically has been one of the most important sea farming areas in
Italy for the production of mussels and other shellfish [23–24]. In recent years, several fish
farms have begun operations in the basin, usually in combination with mussel farming.
No direct observation of negative effects involving hydrozoans were reported in the aqua-
culture facility during the course of this study, but mass mortalities associated with fouling
hydroids and pelagic hydromedusae occurred at the same time along the coast of Spain [13–
14], highlighting the need for prospective studies on hydroid dynamics on aquaculture cages
in our area. Benthic hydroids were observed fouling several hard surfaces at the aquaculture
facility throughout the duration of the study, but monitoring of their succession and coloniza-
tion was exclusively on test panels, as described below. Temperature data in the vicinity of the
studied facility obtained from the Italian National Institute for Environmental Protection and
Research are included as supplementary material (S1 Table).
Experimental set-up and laboratory work
Two simultaneous experiments (one on succession, the other on colonization) began in April
2013. The fieldwork, sampling and laboratory methodologies were identical for both experi-
ments. Different panels were analyzed in each experiment, except the first 9 panels deployed
were the first set of panels analyzed in the succession experiment (submersion duration = 3
months) and in the colonization experiment (season of immersion = spring) (Fig 1). In the
succession experiment, 36 roughened PVC panels (15 x 15 x 0.3 cm) were distributed on 12
vertical longlines that were deployed at 2–3 m intervals around a sea bream cage. Three panels
were positioned on each longline at 0.2, 3, and 6 m depths. The total depth of the water column
was ca. 10 m, while the cage extended to 9 m depth. Every three months, three of these long-
lines were detached and their respective panels taken to the laboratory for analysis. Thus, the
succession panels were submerged for 3, 6, 9, or 12 months.
In the colonization experiment, 36 roughened PVC panels (15 x 15 x 0.3 cm) also were dis-
tributed on twelve vertical longlines deployed at 2–3 m intervals around a sea bream cage, but
only three longlines were deployed and recovered in each sampling event. Thus, all analysed
panels were submerged for a period of three months, having been deployed either in spring
(April 2013), summer (July 2013), autumn (October 2013), or winter (January 2014).
The panels were collected, brought to the laboratory and photographed with a Nikon Cool-
pix E990 camera to estimate species coverage. Panels then were fixed in 4% formaldehyde for
subsequent taxonomic analysis. All of the hydrozoans from the surface facing towards the cage
of each panel were identified under 8x and 25x magnification of a stereomicroscope and pho-
tographed. No protected species were sampled during this study.
The hydrozoans were identified to species or the lowest possible taxonomic level following
specialized literature [25–26]. Species richness (number of hydrozoan species per panel), the
substrate on which each hydroid colony was growing, and the number of reproductive struc-
tures per species (gonothecae or medusa buds) were recorded. The total surface area covered
by each hydrozoan species on each panel was calculated from the photographs with the image
analysis software ImageJ [27]. The standardized area (per 100 cm
2
) was used as the estimate of
Hydroid succession dynamics in a fish farm
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total abundance for each species in subsequent analysis. For each species producing medusae
or planktonic propagules, the number of reproductive structures per 100 cm
2
also was calcu-
lated by directly counting either medusa buds, medusae developing inside gonothecae, or
planktonic propagules. The substrate preference of the fouling hydroids as a whole was calcu-
lated as the percentage of occurrences per available substrate in each combination of depth
and submersion duration in the succession experiment. All specimens were deposited in the
Hydrozoa Collection of the University of Salento (Lecce, Italy) (S2 Table).
Data analysis
Differences in the total abundance and species richness of the fouling hydroids on each panel
were tested through a series of two-way Analysis of Variance (ANOVA). The factors tested
were depth and submersion duration in the succession experiment, and depth and season of
immersion in the colonization experiment. Multivariate analyses were used to compare the
similarity of the assemblages of fouling hydroids on the panels according to the tested factors
in each experiment. Non-metric multidimensional scaling (nMDS) analyses based on Bray-
Curtis distances of square root-transformed surface area data (samples with no hydrozoans
excluded) were performed to visualize changes in species assemblages. To test the differences
in the composition of the assemblages in relation to factors ‘submersion duration’ in the suc-
cession experiment (fixed, four levels), ‘season of immersion’ in the colonization experiment
Fig 1. Experimental design to test hydroid succession and colonization at an aquaculture farm in the Central Mediterranean Sea (2013–2014).
Three replicate test panels at each depth are identified as R1, R2, or R3. Panels for the succession experiment are inside the black rectangle and those for
the colonization experiment are shaded in gray. The number of months that each set of panels spent underwater is indicated.
https://doi.org/10.1371/journal.pone.0195352.g001
Hydroid succession dynamics in a fish farm
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(fixed, four levels), and depth in both experiments (fixed, three levels), distance-based permu-
tational multivariate analysis of variance was used (PERMANOVA, [28]). Finally, the similar-
ity percentage procedure SIMPER enabled calculation of the contribution of each species to
the observed patterns. All multivariate analyses were performed using the PRIMER software
package [29].
Results
Succession experiment
Fouling hydroids were present on the panels on all dates and at all depths during the succes-
sion experiment. An average of 9.8 cm
2
(±6.5) was occupied by hydroids on any of the 36 pan-
els at any immersion time and depth, which represented about 5% (±3.3%) of the available
surface area. Considerable variation was observed in mean surface covered by fouling hydroids
among panels (Fig 2); however, this variation was not statistically significant in relation to the
submersion duration or to the depth of immersion (Table 1).
Fig 2. Variation in species richness (dashed line, total values) and surface cover (bars and error bars, mean ±standard deviation) occupied by
fouling hydroids on the test panels during the succession and colonization experiments.
https://doi.org/10.1371/journal.pone.0195352.g002
Hydroid succession dynamics in a fish farm
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A total of 11 hydrozoan taxa were identified as part of the fouling community on the panels
(Fig 3). Specimens in the family Campanulinidae could not be identified to species level due to
the lack of reproductive structures and few polyps collected. The number of hydroid species
increased significantly with duration underwater, from only 3 species after 3 months to 9 after
12 months. Species richness did not differ significantly on panels at different depths (Table 1).
The hydrozoan species composition of the fouling assemblages changed with submersion
duration, but the panel depth did not significantly affect the assemblages, as shown by the
PERMANOVA analysis (Table 2). The nMDS diagram showed differences between the panels
submerged for 3 months and those submerged for 9 and 12 months, which grouped together.
The hydroid assemblages from 3- and 6-month panels overlapped little with those submerged
for 9 and 12 months (Fig 4).
The SIMPER analysis showed that Aglaophenia picardi Svoboda, 1979, Obelia dichotoma
(Linnaeus, 1758), and Eudendrium racemosum (Cavolini, 1785) characterized the assemblages
on panels submerged for 3 and 6 months, while variations in the abundances of Halecium
Table 1. Two-way ANOVA analyses of the effects of selected factors on the mean surface covered by fouling hydroids and species richness in the succession and col-
onization experiments.
Succession experiment
Mean surface covered by fouling hydroids
Source DF SS MS F P
Submersion duration (S) 3 169.028 56.343 0.32 0.808
Depth (D) 2 739.078 369.539 2.13 0.141
S x D 6 497.204 82.867 0.48 0.818
Residual 24 4164.574 173.524
Total 35 5569.884
Species richness
Source DF SS MS F P
Submersion duration (S) 3 45.111 15.037 8.59 0.001
Depth (D) 2 16.056 8.029 4.59 0.121
S x D 6 5.056 0.843 0.48 0.816
Residual 24 42.000 1.750
Total 35 108.222
Colonization experiment
Mean surface covered by fouling hydroids
Source DF SS MS F P
Season of immersion (S) 3 1565.525 521.842 4.17 0.010
Depth (D) 2 690.362 345.181 2.76 0.084
S x D 6 860.183 143.364 1.14 0.367
Residual 24 3005.042 125.210
Total 35 6121.111
Species richness
Source DF SS MS F P
Season of immersion (S) 3 1.639 0.546 0.94 0.438
Depth (D) 2 0.167 0.083 0.14 0.868
S x D 6 0.944 0.157 0.27 0.946
Residual 24 14.000 0.583
Total 35 16.750
Statistically significant results (P <0.05) are shaded in grey. DF = degrees of freedom; SS = sum of squares; MS = mean squares; F = F statistic; P = probability value.
https://doi.org/10.1371/journal.pone.0195352.t001
Hydroid succession dynamics in a fish farm
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Fig 3. Percentage of mean surface cover for every species of fouling hydroid on the testpanels during the succession experiment.
https://doi.org/10.1371/journal.pone.0195352.g003
Table 2. PERMANOVA (permutational multivariate analysis of variance) results of tested factors on community composition based on surface cover of species in
the succession and colonization experiments.
Succession experiment
Source DF SS MS Pseudo-F P (perm) Unique perms
Submersion duration (S) 3 12061 4020.2 2.828 0.018 999
Depth (D) 2 9336.1 4668.1 2.284 0.109 998
S x D 6 13336 2222.6 1.564 0.122 996
Residual 16 22742 1421.4
Total 27 62595
Colonization experiment
Source DF SS MS Pseudo-F P (perm) Unique perms
Season of immersion (S) 3 56220 18740 9.312 0.001 998
Depth (D) 2 3571.5 1785.7 0.887 0.592 997
S x D 6 16958 2826.4 1.404 0.059 997
Residual 20 40251 2012.6
Total 31 121000
Statistically significant results (P <0.05) are shaded in grey. DF = degrees of freedom; SS = sum of squares; MS = mean squares; Pseudo-F = Pseudo-F statistic; P (perm)
= probability after the permutations; Unique perms = permutations performed.
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Hydroid succession dynamics in a fish farm
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pusillum Sars, 1856, Kirchenpaueria halecioides (Alder, 1859), Sertularella ellisii (Deshayes &
Milne Edwards, 1836), O.dichotoma, and Bougainvillia muscus (Allman, 1863) characterized
assemblages on panels submerged for 9 and 12 months (Table 3). Aglaophenia picardi,O.
dichotoma, and E.racemosum were the only species present on the panels recovered after 3
months. The surface occupied by these three species decreased over time as other species
appeared on the panels (e.g., Turritopsis dohrnii (Weismann, 1883), K.halecioides,S.ellisii and
H.pusillum). Later stages of succession had more species and more area covered by epibiotic
colonies of B.muscus,Clytia hemisphaerica (Linnaeus, 1767), Halecium petrosum Stechow,
1919, H.pusillum, and Campanulinidae species. The most common and abundant species
through all immersion times and depth levels were A.picardi and O.dichotoma (Fig 3).
Substrate preferences of the fouling hydroids changed with the submersion duration of the
panels (Fig 5). In the first 3 months of immersion, the only surface available for colonization
was the artificial substrate of the PVC panels. After 6 months, new fouling biota appeared
(polychaetes, tunicates, bryozoans, and mussels), which provided new available substrates for
fouling hydrozoans. On the panels submerged for 9 and 12 months, the shells of fouling mus-
sels (Mytilus galloprovincialis Lamarck, 1819) became the main substrate for the epibiotic spe-
cies of hydroids, including many H.pusillum colonies. In later stages of succession, hydroids
grew on other hydroids, especially C.hemisphaerica and Campanulinidae species, which used
S.ellisii and the stem of E.racemosum as substrates.
Four species produced reproductive structures during the experiment: A.picardi,O.dichot-
oma,C.hemisphaerica and B.muscus. The last three species release medusae as part of their life
cycle, with fertile colonies appearing on panels submerged for 3–12 months. The mean num-
ber of medusae produced per 100 cm
2
reached maxima of 2.6 (±19.6) for O.dichotoma, 2.2
(±19.1) for C.hemisphaerica, and 0.2 (±1.7) for B.muscus. Numerous asexually-produced
planktonic propagules were produced by H.pusillum (mean of 3.0 ±21.3 per 100 cm
2
) mostly
on the panels submerged for 9 and 12 months.
Colonization experiment
The pioneer hydrozoan species on the panels were always a subset of those observed in the suc-
cession experiment. All the panels immersed for 3 months at different seasons of the year
Fig 4. Non-metric multidimensional scaling (nMDS) plots based on Bray-Curtis similarity of surface covered by fouling hydroids in the
succession and colonization experiments.
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Hydroid succession dynamics in a fish farm
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included hydrozoans as part of the colonizing fouling fauna. The mean surface covered by the
hydroids differed significantly by season of immersion (Fig 2); however, depth did not have a
significant effect on mean surface cover of fouling hydroids in the colonization experiment
(Table 1).
Table 3. Average similarity (SIMPER) within fouling hydroid assemblages from panels with different submersion duration (succession experiment) and panels
with different seasons of immersion (colonization experiment).
Succession experiment
Av.
Surf.
Av.
Sim.
Sim/
SD
Contrib
%
Cum
%
Panels submerged for3 months
Average similarity: 66.67
Obelia dichotoma 0.8 50 1.60 75 75
Aglaophenia picardi 0.6 16.67 0.58 25 100
Panels submerged for 6 months
Average similarity: 49.17
Aglaophenia picardi 0.67 39.17 1.38 79.66 79.6
Eudendrium racemosum 0.33 10 0.5 20.34 100
Panels submerged for 9 months
Average similarity: 46.14
Halecium pusillum 0.75 15.69 1.01 34.01 34.1
Aglaophenia picardi 0.63 13.11 1.03 28.41 62.4
Obelia dichotoma 0.75 11.88 0.74 25.76 88.2
Sertularella ellisii 0.25 2.86 0.38 6.19 94.4
Panels submerged for 12 months
Average similarity: 61.49
Halecium pusillum 0.89 19.99 1.66 32.51 32.5
Obelia dichotoma 0.78 14.35 1.02 23.33 55.8
Bougainvillia muscus 0.44 8.42 0.66 13.7 69.5
Aglaophenia picardi 0.44 7.87 0.66 12.79 82.3
Clytia hemisphaerica 0.44 6.17 0.49 10.04 92.4
Colonization experiment
Panels submerged from May to July 2013
Average similarity: 35.04
Obelia dichotoma 5.89 26.37 1.68 75.27 75.3
Aglaophenia picardi 4.95 8.66 0.58 24.73 100
Panels submerged from August to October 2013
Average similarity: 24.44
Eudendrium racemosum 20.34 46.69 1.45 96.45 96.5
Panels submerged from November 2013 to January 2014
Average similarity: 48.41
Kirchenpaueria halecioides 7.84 23.39 1.67 95.72 95.7
Panels submerged from February to April 2014
Average similarity: 53.90
Aglaophenia picardi 1.86 33.2 1.29 61.59 61.6
Obelia dichotoma 0.75 15.67 0.8 29.07 90.7
Av. Surf. = average surface area covered; Av. Sim. = average similarity; Sim/SD = similarity to standard deviation ratio; Contrib % = percentage contribution; Cum. % =
cumulative percentage contribution.
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Hydroid succession dynamics in a fish farm
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In all, 7 hydroid species (A.picardi,O.dichotoma,E.racemosum,S.ellisii,K.halecioides,H.
petrosum, and B.muscus) colonized the panels immersed for 3 months, although only 2 or 3 of
these species grew simultaneously on any one panel. In fact, the number of fouling hydroid
species observed in the colonization experiment did not differ significantly among depths or
seasons (Table 1).
The season when the panels were immersed significantly affected the composition of foul-
ing hydrozoan assemblages, while the depth of the panels did not significantly affect the colo-
nization, as shown by the PERMANOVA (Table 2). The panels immersed during different
seasons had clearly different fouling hydroid assemblages (Fig 4). The species characterizing
the hydroid communities on the panels (i.e. those with highest percentage of cover and identi-
fied by the SIMPER analysis) were A.picardi and O.dichotoma in spring and winter, E.race-
mosum in summer, and K.halecioides in autumn (Table 3).
Fouling colonies of A.picardi,K.halecioides and O.dichotoma were producing reproductive
structures (sessile gonophores in the first two species and gonothecae with medusa buds in the
third) in the colonization experiment. Fertile colonies appeared on panels submerged in all
seasons: A.picardi in spring and summer, K.halecioides in winter and spring, and O.dichot-
oma all year. The potential number of medusae released by colonies of O.dichotoma during
the colonization experiment reached maximum means of 2.4 (±15.3) per 100 cm
2
on the win-
ter and spring panels, corresponding with the highest reproductive effort of the fouling
hydroid colonies and contrasting with the lowest reproductive effort recorded in summer.
Discussion
Hydrozoans represent a conspicuous component of the fouling assemblages in the studied
aquaculture facility and are likely to regularly interact with cultured fish and shellfish. Their
abilities to grow rapidly and to settle and re-settle on different surfaces allow hydroids to be
among the first metazoans to colonize available substrates and ensure their presence during
Fig 5. Substrate preference (percentage of occurrences per available substrate ineach combination of depth and submersion duration) of the
fouling hydroids in the succession experiment.
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Hydroid succession dynamics in a fish farm
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the entire process of succession [30–31]. The degree and outcomes of the interactions between
fouling hydroids and fish, however, will change in time and space, in part modulated by the
four main patterns emerging from our analysis: (i) increasing species richness as succession
proceeded; (ii) changing species composition according to season and duration of exposure;
(iii) progressively shifting substrate usage to include newly-created biotic surfaces; (iv) produc-
ing numerous planktonic propagules in all stages of succession and throughout the year.
The changes in hydroid composition and abundance follow the same patterns described for
succession in natural hard-substrate communities, with certain species colonizing the sub-
strate and, as succession proceeds, modifying the environment such that it becomes unsuitable
for further recruitment, but facilitating settlement and development of a new group of species
[32–33]. In the studied assemblages, the submersion duration was particularly important in
determining the succession, through variation in larval abundance, arrival of new species, and
biological interactions between biofoulers [34–35]. Successful hydroid biofoulers display
different abundances and growth rates as succession progresses, reflecting their unique life his-
tory traits (e.g. production of planktonic stages, asexual reproduction, survival of the planulae),
which in temperate regions are subjected to severe temporal fluctuations [36–37]. In fact, as
for hydrozoans in natural communities, seasonal variation in environmental conditions affects
the establishment, survival and growth of fouling hydroids [37–38] and, therefore, determines
the composition and structure of biofouling assemblages and succession.
The observed increase in hydrozoan species with time (i.e., submersion duration) reflected
the growing complexity of the fouling assemblages and the ability of hydroids to settle and
grow on their competitors, capitalizing on the increased surface generated by other biofoulers
(e.g., mussels, sponges, tunicates, bryozoans, polychaetes). Despite this, the observed fouling
hydrozoans constituted only a very small portion (ca. 8%) of the total number of species (115)
recorded from the surrounding coastal habitats [26]. More generally, fewer species are often
encountered as biofoulers on artificial substrates compared to species-rich assemblages of nat-
ural habitats [39–41]. Which species colonized depended primarily on the season when the
panels were immersed; specifically, different sets of species were observed on panels deployed
in spring, summer, autumn, and winter. Experimental evidence suggests that both the season
when a structure is immersed and the duration of submersion are more important than the
type of substrate in structuring subtidal biofouling communities [42]. The season of immer-
sion has been widely recognized as one of the most important factors modulating the outcome
of succession in natural and artificial assemblages [34,43–44]. As with the submersion dura-
tion, the time of the year when new substrates become available for colonization has a crucial
influence on succession because of the seasonal differences of environmental conditions,
reproduction, and growth patterns of fouling species, eventually affecting the pattern and rate
of succession [34,44–46]. Nevertheless, season may not determine the outcome in natural
hard-bottom communities, because the stronger competitors eventually monopolize the avail-
able space despite initial differences in colonization, thus making the succession process par-
tially predictable [33].
In contrast, the depths at which our test panels were submerged did not have a significant
role in structuring the fouling hydrozoan assemblages. Although many physical factors change
with depth and strong vertical zonation has been observed in natural and biofouling commu-
nities [47–49], most examples of depth-related vertical zonation come from depth differences
larger than those studied here. Distinctly different communities are not usually found in the
first 5–6 m from the surface on man-made structures [50]; the panels deployed in our study
were assumed not to be subjected to highly different conditions of temperature, pressure, light,
food, or nutrients. Therefore, a lack of vertical zonation in the analyzed biofouling assemblages
was expected.
Hydroid succession dynamics in a fish farm
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All of the hydrozoan species observed have been recorded previously from the surrounding
hard-bottom benthic community [25–26], which can be considered the basic pool of coloniz-
ers. Furthermore, previously reported fouling hydroids in the area include O.dichotoma as
well as species of Aglaophenia,Sertularella, and Eudendrium [39,51]. In general, the species
recorded here can be classified into two main groups: (i) ‘colonizers’ or ‘early successional
species’ with tendencies to produce abundant asexual propagules and display rapid growth
rates, and (ii) ‘mid- and late-successional species’, which tend to rely on efficient utilisation of
resources to outcompete colonizers. The first group included A.picardi,O.dichotoma,E.race-
mosum, and K.halecioides, depending on the season. The second group was formed by epibio-
tic, less generalist species such as H.pusillum,H.petrosum, and Campanulinidae sp.
The best example of the pioneering and early successional hydrozoans recorded here may
be O.dichotoma, a common and abundant species often encountered in disturbed sites and
fouling communities. Contardo-Jara et al. [52] found it to be particularly abundant in dis-
turbed communities growing on PVC panels in the southwestern Atlantic. It also has been
reported as part of the biofouling assemblages of fish farms in the southwestern Pacific and
northeastern Atlantic oceans, growing on coated and uncoated nets [5,53]. It is a frequent spe-
cies in harbours [40], where it often predominates over other fouling species [54], which may
explain its ubiquity in the studied fouling assemblages. It is also one of the most common and
abundant fouling hydrozoans on power stations and other artificial substrates along Italian
coasts [55–57]. Blooms of Obelia spp. jellyfish occur along temperate coasts together with mas-
sive occurrence of hydroids [58]. Obelia species are frequent and widespread fouling organ-
isms found abundantly virtually everywhere in aquaculture facilities: Obelia longissima (Pallas
1766) is common on Atlantic salmon cages and mussel nets at high latitudes in the Northern
hemisphere [59–60], while Obelia spp. have been reported growing on finfish aquaculture
cages in the Mediterranean [60], northeastern Pacific [61], and North Atlantic [62], in some
cases contributing to problems due to occlusion of the net mesh aperture in the cages. Obelia
spp. were also recorded growing on shellfish aquaculture facilities and on the shells of target
species, as observed in the Eastern Mediterranean for mussels [63] and in the tropical south-
western Pacific for pearl oysters [64]. The high abundance of fouling Obelia spp. hydroids was
suggested to be one of the factors potentially causing the observed high mortalities in shellfish
aquaculture facilities, while the massive production of medusae by those hydroids substantially
changed the quality of the nearby plankton community [65].
The dynamics of early successional species such as Obelia spp. contrast sharply with that of
mid- and late-successional taxa such as H.pusillum or H.petrosum, which are smaller, slightly
more specialized species commonly found growing on living substrates [66]. Other fouling
hydrozoan species observed at the fish farm in Taranto also have been reported from aquacul-
ture facilities around the world. As examples, eudendriid and bougainvilliid hydroids (includ-
ing B.muscus) grow on nets containing scallops (Pecten maximus (Linnaeus, 1758)) or
Atlantic salmon (Salmo salar Linnaeus, 1758) in the northern Atlantic and Pacific oceans [62,
67–68]; Clytia spp. are commonly recorded on culture tanks, nets, and PVC panels worldwide
[62,67,69–70]; species of Kirchenpaueria and Sertularella may grow on ropes and nets of fin-
fish and shellfish farms [60,71].
Hydrozoan species that require the development of some structural elements prior to their
settlement arrive after the rapidly growing, opportunistic colonizers. This implies a strong rela-
tionship between the development of the fouling community as a whole and the associated
hydrozoan component during succession. During early succession almost 100% of hydrozoans
found on the panel surface were growing directly on the PVC, but this percentage decreased
sharply with immersion duration after the diversity and abundance of substrates on the panels
increased. Eventually, some species (including E.racemosum and S.ellisii) became substrates
Hydroid succession dynamics in a fish farm
PLOS ONE | https://doi.org/10.1371/journal.pone.0195352 April 2, 2018 12 / 18
for other hydrozoans, while other hydroids thrived by closely following the dynamics of their
invertebrate substrates (e.g., mussels, ascidians, etc.). The latter is best exemplified by H.pusil-
lum growing on the mussel M.galloprovincialis and the non-indigenous tunicate Polyandro-
carpa zorritensis (Van Name, 1931). Because mussels and ascidians gradually covered the
experimental panels, the fouling hydrozoan biota shifted towards epibiotic species that are able
to colonize and survive on mussel shells and effectively take advantage of the newly available
living space. The same occurred on panels submerged near the study area on which M.gallo-
provincialis eventually became very abundant, leading to a profound change in the number of
other biofoulers [39]. Mytilus galloprovincialis is known to effectively deter fouling on its shell
surface, which limits the available space for colonization by other biofoulers and creates spe-
cific conditions that permits settlement of only a few species (such as H.pusillum) on its shell
[72].
Dispersive free-swimming medusae or asexual planktonic propagules were released by
fouling hydroids into the water column during all the stages of succession and in all seasons.
Halecium pusillum asexually produces complex, heterotrophic propagules adapted to pelagic
life and released independently of the environmental conditions [66,73]. The release of these
propagules is common in the life cycle of some Halecium species and has been hypothesized to
promote dispersal [74]. Dispersion through asexual propagules can be a very important demo-
graphic process in a wide array of taxa (e.g., sponges, tunicates, bryozoans, algae) [75] and is
particularly important among benthic hydrozoans [31], especially to maintain populations of
H.pusillum in the Mediterranean Sea [66]. The planktonic propagules of H.pusillum carry
nematocysts [73] and could damage the skin and gills of fish in the cages.
The potential effects of pelagic cnidarians on the health of farmed fish in aquaculture facili-
ties are beginning to be recognized through recent studies showing that abundances of sting-
ing species are strongly correlated with gill and skin lesions, as well as fish mortality [12,14,
76]. In the case of the facility we studied, the observed medusa production in O.dichotoma,
C.hemisphaerica, and B.muscus, with colonies of O.dichotoma releasing particularly high
numbers of medusae from early stages of colonization and throughout the entire succession,
could easily generate damage associated with nematocyst discharge and venom injection. Jelly-
fish of O.dichotoma,C.hemisphaerica and B.muscus represent a potential problem for the
farmed fish of Taranto. Jellyfish also have been suggested to be important as vectors of bacte-
rial diseases for farmed fish [11] and some hydromedusae are intermediate hosts of fish para-
sites [77–78].
Altogether, the observed fouling hydroid assemblages may pose substantial problems for
aquaculture in terms of fish health and increased production costs. In addition to medusae,
actinula larvae and planktonic propagules, the benthic stages of fouling hydrozoans can
directly harm the skin and gills of fish, as has been documented for E.larynx in Irish salmon
farms [19]. Hydroid species also negatively affect shellfish and crustacean cultures by compet-
ing for food [69,79–80], predating on larvae of the target species [20,81], and inhibiting
spat settlement [82]. More commonly, the presence of fouling hydroids has been linked to
decreased water flow and increased net weight in fish cages [17,62,68]. Any of these negative
impacts could occur in aquaculture facilities as the abundance of fouling hydrozoans increases.
The common local biofouler O.dichotoma, for instance, has been linked to decreased water
flow and increased net weight in cultures of the deep-sea scallop Placopecten magellanicus
(Gmelin 1791) in the northwestern Atlantic [15] and is one of the parasite reservoirs for amoe-
bic gill disease of cultured salmon in southwestern Pacific waters [83]. In the Mediterranean
Sea, however, few estimates exist of the damage caused to finfish aquaculture by fouling hydro-
zoans [14] and, generally, no information is available on the agents causing mortality or dis-
ease of cultured fish. Thus, regular monitoring of the hydrozoan fouling assemblages is
Hydroid succession dynamics in a fish farm
PLOS ONE | https://doi.org/10.1371/journal.pone.0195352 April 2, 2018 13 / 18
necessary to further increase understanding of their potential effects on the health of cultured
fish and shellfish.
Supporting information
S1 Table. Temperature data for the Gulf of Taranto thoughout the study period.
(XLSX)
S2 Table. Standardized surface area covered by each hydrozoan species on each panel.
(XLSX)
Acknowledgments
The authors thank Prof. Adriana Giangrande for providing the samples for this study, and Dr.
Joan Josep Soto Àngel for helping with the preparation of the figures and commenting on an
earlier version of the manuscript. Thanks are also due to the reviewers and associated editor
for their valuable comments.
Author Contributions
Conceptualization: Luis Martell, Jennifer E. Purcell.
Data curation: Luis Martell, Roberta Bracale, Steven A. Carrion, Marco Lezzi.
Formal analysis: Luis Martell, Roberta Bracale, Steven A. Carrion, Marco Lezzi.
Investigation: Luis Martell, Roberta Bracale, Steven A. Carrion, Marco Lezzi.
Methodology: Luis Martell, Roberta Bracale, Steven A. Carrion, Marco Lezzi.
Resources: Cinzia Gravili, Stefano Piraino, Ferdinando Boero.
Supervision: Jennifer E. Purcell, Stefano Piraino, Ferdinando Boero.
Writing – original draft: Luis Martell.
Writing – review & editing: Jennifer E. Purcell, Cinzia Gravili, Stefano Piraino, Ferdinando
Boero.
References
1. FAO. World review of fisheries and aquaculture. The state of world fisheries and aquaculture (SOFIA).
Part I. 2014.
2. Du¨rr S, Watson DI. Biofouling and antifouling in aquaculture. In: Du¨rr S, Thomason JC, editors. Biofoul-
ing. Blackwell Publishing Ltd.; 2010. pp. 267–287.
3. Lane A, Willemsen P. Collaborative effort looks into biofouling. Fish Farm Int. 2004; 44: 34–35.
4. De Nys R, Guenther J. The impact and control of biofouling in marine finfish aquaculture. In: Hellio C,
Yebra DM., editors. Advances in marine antifouling coatings and technologies. Woodshead Publishing;
2009; pp. 177–221.
5. Fitridge I, Dempster T, Guenther J, de Nys R. The impact and control of biofouling in marine aquacul-
ture: a review. Biofouling. 2012; 28(7): 649–669. https://doi.org/10.1080/08927014.2012.700478
PMID: 22775076
6. Lacoste E, Gaertner-Mazouni N. Biofouling impact on production and ecosystem functioning: a review
for bivalve aquaculture. Rev Aquacult. 2015; 7(3): 187–196.
7. Braithwaite RA, McEvoy LA. Marine biofouling on fish farms and its remediation. Adv Mar Biol. 2005;
47:215–252. https://doi.org/10.1016/S0065-2881(04)47003-5 PMID: 15596168
8. Willemsen P. Biofouling in European aquaculture: is there an easy solution. Spec Publ Eur Aquacult.
Soc. 2005; 35: 82–87.
Hydroid succession dynamics in a fish farm
PLOS ONE | https://doi.org/10.1371/journal.pone.0195352 April 2, 2018 14 / 18
9. Bouillon J, Gravili C, Page
´s F, Gili JM, Boero F. An introduction to Hydrozoa. Me
´m Mus Natl Hist Nat.
2006; 194: 1–591.
10. Morri C, Boero F. Marine fouling hydroids. In: Catalogue of the main marine fouling organisms 7,
Hydroids. 1986. pp. 1–91.
11. Ferguson HW, Delannoy CMJ, Hay S, Nicolson J, Sutherland D, Crumlish M. Jellyfish as vectorsof bac-
terial disease for farmed salmon (Salmo salar). J Vet Diagn Invest. 2010; 22: 376–382. https://doi.org/
10.1177/104063871002200305 PMID: 20453210
12. Baxter EJ, Rodger HD, McAllen R, Doyle TK. Gill disorders in marine-farmed salmon: investigating the
role of hydrozoan jellyfish. Aquac Environ Interact. 2011; 1: 245–257.
13. Bosch-Belmar M. Jellyfish blooms impacts on Mediterranean aquaculture: a multidisciplinary approach.
PhD thesis, University of Salento. 2016.
14. Bosch-Belmar M, Milisenda G, Girons A, Taurisano V, Accoroni S, Totti C, et al. Consequences of sting-
ing plankton blooms on finfish mariculture in the Mediterranean Sea. Front Mar Sci. 2017; 4:240.
15. Claereboudt MR, Bureau D, Co
ˆte
´J, Himmelman JH. Fouling development and its effect on the growth
of juvenile giant scallops (Placopecten magellanicus) in suspended culture. Aquaculture. 1994; 121(4):
327–342.
16. Guenther J, Carl C, Sunde LM. The effect of color and copper on the settlement of the hydroid Ecto-
pleura larynx on the aquaculture nets in Norway. Aquaculture. 2009; 292: 252–255.
17. Guenther J, Misimi E, Sunde LM. The development of biofouling, particularly the hydroid Ectopleura lar-
ynx, on commercial salmon cage nets in Mid-Norway. Aquaculture. 2010; 300: 120–127.
18. Guenther J, Fitridge I, Misimi E. Potential antifouling strategies for marine finfish aquaculture: the effects
of physical and chemical treatments on the settlement and survival of the hydroid Ectopleura larynx.
Biofouling. 2011; 27(9): 1033–1042. https://doi.org/10.1080/08927014.2011.627092 PMID: 22017479
19. Baxter EJ, Sturt MM, Ruane NM, Doyle TK, McAllen R, Rodger D. Biofouling of the hydroid Ectopleura
larynx on aquaculture nets in Ireland: Implications for finfish health. Fish Vet J. 2012; 13: 17–29.
20. Fitridge I, Keough MJ. Ruinous resident: the hydroid Ectopleura crocea negatively affects suspended
culture of the mussel Mytilus galloprovincialis. Biofouling. 2013; 29(2): 119–131. https://doi.org/10.
1080/08927014.2012.752465 PMID: 23327223
21. Istituto Idrografico della Marina. Carta Nautica Ufficiale dello Stato, Porto di Taranto. 2002.
22. Cardellicchio N, Annicchiarico C, Di Leo A, Giandomenico S, Spada L. The Mar Piccolo of Taranto: an
interesting marine ecosystem for the environmental problems studies. Environ Sci Pollut Res. 2015;
23(13): 12495–12501.
23. Mattei N, Pellizzato M. Mollusk fisheries and aquaculture in Italy. In: MacKenzie Jr. CL, Burrell Jr. VG,
Rosenfield A, Hobart WL, editors. The history, present condition, and future of the molluscan fisheries
of North and Central America and Europe Volume 3. U.S. Department of Commerce, NOAA Technical
Reports; 1997. pp. 201–216.
24. Caroppo C, Giordano L, Palmieri N, Bellio G, Bisci AP, Portacci G, et al. Progress toward sustainable
mussel aquaculture in Mar Piccolo, Italy. Ecol Soc. 2012; 17(3):10.
25. Bouillon J, Medel MD, Pagès F, Gili JM, Boero F, Gravili C. Fauna of the Mediterranean Hydrozoa. Sci
Mar 2004; 68(2): 5–438.
26. Gravili C, De Vito D, Di Camillo CG, Martell L, Piraino S, Boero F. The non-Siphonophoran Hydrozoa
(Cnidaria) of Salento, Italy with notes on their life-cycles: an illustrated guide. Zootaxa. 2015; 3908(1):
1–187.
27. Abramoff MD, Magalhaes PJ, Ram SJ. Image Processing with ImageJ. Biophoton Int. 2004; 11(7): 36–
42.
28. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001;
26: 32–46.
29. Clarke KR, Gorley RN. PRIMER version 6: user manual/tutorial. PRIMER-E, Plymouth, UK. 2006.
30. Boero F. The ecology of marine hydroids and effects of environmental factors: a review. Mar Ecol.
1984; 5: 93–118.
31. Gili JM, Hughes RG. The ecology of marine benthic hydroids. Oceanogr Mar Biol. 1995; 33: 351–426.
32. Connell JH, Slayter RO. Mechanisms of succession in natural communities and their role in community
stability and organization. Am Nat. 1977; 111: 1119–1144.
33. Jenkins SR, Martins GM. Succession on hard substrata. In: Du¨rr S, Thomason JC, editors. Biofouling.
Blackwell Publishing Ltd.; 2010. pp. 60–72.
34. Sutherland J., Karlson R. Development and stability of the fouling community at Beaufort North Caro-
lina. Ecol Monogr. 1977; 47: 425–446.
Hydroid succession dynamics in a fish farm
PLOS ONE | https://doi.org/10.1371/journal.pone.0195352 April 2, 2018 15 / 18
35. Terlizzi A, Faimali M. Fouling on artificial substrata. In: Du¨rr S, Thomason JC, editors. Biofouling. Black-
well Publishing Ltd.; 2010. pp. 170–184.
36. Coma R, Ribes M, Gili JM, Zabala M. Seasonality in coastal benthic ecosystems. Trends Ecol Evol.
2000; 15(11): 448–453. PMID: 11050347
37. Bavestrello G, Puce S, Cerrano C, Zocchi E, Boero F. The problem of seasonality of benthic hydroids in
temperate waters. Chem Ecol. 2006; 22(1): S197–S205.
38. Calder DR. Seasonal cycles of activity and inactivity in some hydroids from Virginia and South Carolina,
USA. Can J Zool. 1990; 68(3): 442–450.
39. Pierri C, Longo C, Giangrande A. Variability of fouling community in the Mar Piccolo of Taranto (North-
ern Ionian Sea, Mediterranean Sea). J Mar Biol Assoc U.K. 2010; 90(1): 159–167.
40. Megina C, Gonza
´lez-Duarte MM, Lo
´pez-Gonza
´lez PJ, Piraino S. Harbours as marine habitats: hydroid
assemblages on sea-walls compared with natural habitats. Mar Biol. 2013; 160(2): 371–381.
41. Antoniadou C. Succession patterns of polychaetes on algal-dominated rocky cliffs (Aegean Sea, East-
ern Mediterranean). Mar Ecol. 2014; 35(3): 281–291.
42. Lin HJ, Shao KT. The development of subtidal fouling assemblages on artificial structures in Keelung
Harbor, Northern Taiwan. Zool Stud. 2002; 41: 170–182.
43. Anderson MJ, Underwood AJ. Effects of substratum on the recruitment and development of an intertidal
estuarine fouling assemblage. J Exp Mar Biol Ecol. 1994; 184: 217–236.
44. Underwood AJ, Chapman MG. Early development of subtidal macrofaunal assemblages: relationships
to period and timing of colonization. J Exp Mar Bio Ecol. 2006; 330: 221–233.
45. Breitburg DL. Development of a subtidal epibenthic community—factors affecting species composition
and the mechanisms of succession. Oecologia 1985; 65: 173–184. https://doi.org/10.1007/
BF00379215 PMID: 28310663
46. Benedetti-Cecchi L, Cinelli F. Early patterns of algal succession in a mid-littoral community of the Medi-
terranean Sea: a multifactorial experiment. J Exp Mar Biol Ecol. 1993; 169: 15–31.
47. Logan A, Page FH, Thomas MLH. Depth zonation of epibenthos on sublittoral hard substrates off Deer
Island, Bay of Fundy, Canada. Estuar Coast Shelf Sci. 1984; 18: 571–592.
48. Stachowitsch M, Kikinger R, Herler J, Zolda P, Geutebru¨ck E. Offshore oil platforms and fouling com-
munities in the southern Arabian Gulf (Abu Dhabi). Mar Pull Bull. 2002; 44(9): 853–860.
49. Terlizzi A, Anderson MJ, Fraschetti S, Benedetti-Cecchi L. Scales of spatial variation in Mediterranean
subtidal sessile assemblages at different depths. Mar Ecol Prog Ser. 2007; 332: 25–29.
50. Cowie PR. Biofouling patterns with depth. In: Du¨rr S, Thomason JC, editors. Biofouling. Blackwell Pub-
lishing Ltd.; 2010. pp 87–99.
51. Montanari M, Morri C. Fouling di alcune piattiforme off-shore dei mari italiani: V. Gli Idroidi. In: Atti IX
Congresso della SocietàItaliana di Biologia Marina; 1977. pp. 293–302.
52. Contardo Jara V, Miyamoto JHS, da Gama BA, Molis M, Wahl M, Pereira RC. Limited evidence of inter-
active disturbance and nutrient effects on the diversity of macrobenthic assemblages. Mar Ecol Prog
Ser. 2006; 308: 37–48.
53. Hodson SL, Burke CM, Bissett AP. Biofouling of fish-cage netting: the efficacy of a silicone coating and
the effect of netting colour. Aquaculture. 2000; 184(3): 277–290.
54. Standing J. Fouling community structure: effects of the hydroid Obelia dichotoma on larval recruitment.
In: Mackie G. O., editor. Coelenterate Ecology and Behaviour. Plenum Press; 1976. pp. 155–164.
55. Morri C. Remarques sur les hydraires vivants dans les salissures biologiques de quelques centrales
thermo-e
´lectriques co
ˆtières italiennes. In: XI. Congresso della SocietàItaliana di Biologia Marina. Atti
Soc Toscana Sci Nat Pisa Mem. 1979; 86: 305–307.
56. Morri C. Osservazioni sugli idroidi raccolti nelle condotte della centrale termoelettrica di Torvaldaglia
(Civitavecchia). Natura. 1980; 71(1–2): 3–14.
57. Morri C, Bianchi CN. Studio quantitativo sull’insediamento degli Idroidi (Cnidaria, Hydrozoa) su substrati
artificiali immersi a diverse profonditànell’avamporto di Genova. Boll Mus Civico Storia Nat Venezia.
1982/1983; 33: 73–89.
58. Genzano G, Mianzan H, Diaz-Briz L, Rodriguez C. On the occurrence of Obelia medusa blooms and
empirical evidence of unusual massive accumulations of Obelia and Amphisbetia hydroids on the
Argentina shoreline. Lat Am J Aquat Res. 2008; 36(2): 301–307.
59. Khalaman VV. Succession of fouling communities on an artificial substrate of a mussel culture in the
White Sea. Russ J Mar Biol. 2001; 27(6): 345–352.
Hydroid succession dynamics in a fish farm
PLOS ONE | https://doi.org/10.1371/journal.pone.0195352 April 2, 2018 16 / 18
60. Cook EJ, Black KD, Sayer MDJ, Cromey CJ, Angel DL, Spanier E, et al. The influence of caged maricul-
ture on the early development of sublittoral fouling communities: a pan-European study. ICES J Mar
Sci. 2006; 63: 637–649.
61. Edwards CD, Pawluk KA, Cross SF. The effectiveness of several commercial antifouling treatments at
reducing biofouling on finfish aquaculture cages in British Columbia. Aquacult Res. 2015; 46(9): 2225–
2235.
62. Bloecher N, Olsen Y, Guenther J. Variability of biofouling communities on fish cage nets: A 1-year field
study at a Norwegian salmon farm. Aquaculture. 2013; 416: 302–309.
63. Antoniadou C, Voultsiadou E, Rayann A, Chintiroglou C. Sessile biota fouling farmed mussels: diversity,
spatio-temporal patterns, and implications for the basibiont. J Mar Biol Assoc U. K. 2013; 93(06):
1593–1607.
64. Guenther J, Southgate PC, de Nys R. The effect of age and shell size on accumulation of fouling organ-
isms on the Akoya pearl oyster Pinctada fucata (Gould). Aquaculture. 2006; 253(1–4): 366–373.
65. Mortensen S, Meeren T, Fosshagen A, Hernar I, Harkestad L, Torkildsen L, et al. Mortality of scallop
spat in cultivation, infested with tube dwelling bristle worms, Polydora sp. Aquacult Int. 2000; 8(2–3):
267–271.
66. Coma R, Llobet I, Zabala M, Gili JM, Hughes RG. The population dynamics of Halecium petrosum and
Halecium pusillum (Hydrozoa, Cnidaria), epiphytes of Halimeda tuna in the northwest Mediterranean.
Sci Mar 1992; 56(2–3): 161–169.
67. Chaplygina SF. Hydroids in the fouling of mariculture installations in Peter the Great Bay, Sea of Japan.
Russ J Mar Biol. 1994; 19(2): 85–89.
68. Ross KA, Thorpe JP, Brand AR. Biological control of fouling in suspended scallop cultivation. Aquacul-
ture. 2004; 229: 99–116.
69. Sandifer PA, Smith TI, Calder DR. Hydrozoans as pests in closed-system culture of larval decapod
crustaceans. Aquaculture. 1974; 4: 55–59.
70. Phillippi AL, O’Connor NJ, Lewis AF, Kim YK. Surface flocking as a possible anti-biofoulant. Aquacul-
ture. 2001; 195(3): 225–238.
71. Woods CM, Floerl O, Hayden BJ. Biofouling on Greenshell™mussel (Perna canaliculus) farms: a pre-
liminary assessment and potential implications for sustainable aquaculture practices. Aquac Int 2012;
20(3): 537–557.
72. Scardino A, de Nys R. Fouling deterrence on the bivalve shell Mytilus galloprovincialis: a physical phe-
nomenon? Biofouling. 2004; 20(4–5): 249–257. https://doi.org/10.1080/08927010400016608 PMID:
15621646
73. Huve
´P. Sur des propagules planctoniques de l’hydroïde Halecium pusillum (Sars). Bull Inst Oceanogr
(Monaco). 1955; 52(1064): 1–12.
74. Gravier-Bonnet N, Bourmaud C. Cloning by releasing specialized frustules in a successful epiphytic
zooxanthellate haleciid (Cnidaria, Hydrozoa, Haleciidae), with comments on stolonization and frustula-
tion. Invertebr Reprod Dev. 2005; 48(1–3): 63–69.
75. Havenhand JN, Styan CA. Reproduction and larvae/spore types. In: Du¨rr S, Thomason JC, editors. Bio-
fouling. Blackwell Publishing Ltd.; 2010. pp. 1–15.
76. Purcell JE, Baxter EJ, Fuentes V. Jellyfish as products and problems of aquaculture. In: Allen G, Burnell
G, editors. Advances in aquaculture hatchery technology. Woodhead Publishing Series in Food Sci-
ence, Technology and Nutrition; 2013. pp. 404–430.
77. Martell-Herna
´ndez LF, Ocaña-Luna A, Sa
´nchez-Ramı
´rez M. Seasonal occurrence of Opechona pyri-
forme metacercariae (Digenea: Lepocreadiidae) in Eirene tenuis medusae (Hydrozoa: Leptothecata)
from a hypersaline lagoon in western Gulf of Mexico. J Parasitol. 2011; 97(1): 68–71. https://doi.org/10.
1645/GE-2384.1 PMID: 21348609
78. Dı
´az-Briz LM, Martorelli SR, Genzano GN, Mianzan HW. Parasitism (Trematoda, Digenea) in medusae
from the southwestern Atlantic Ocean: medusa hosts, parasite prevalences, and ecological implica-
tions. Hydrobiologia. 2012; 690(1): 215–226.
79. Lawler AR, Shepard SL. Procedures for eradication of hydrozoan pests in closed-system mysid culture.
Gulf Caribb Res. 1978; 6(2): 177–178.
80. Guenther J, de Nys R. Differential community development of fouling species on the pearl oysters Pinc-
tada fucata,Pteria penguin and Pteria chinensis (Bivalvia, Pteriidae). Biofouling. 2006; 22(3): 151–159.
81. Sievers M, Dempster T, Fitridge I, Keough MJ. Monitoring biofouling communities could reduce impacts
to mussel aquaculture by allowing synchronisation of husbandry techniques with peaks in settlement.
Biofouling. 2014; 30(2): 203–212. https://doi.org/10.1080/08927014.2013.856888 PMID: 24401014
Hydroid succession dynamics in a fish farm
PLOS ONE | https://doi.org/10.1371/journal.pone.0195352 April 2, 2018 17 / 18
82. Dabo KK. Development of aquaculture in Sierra Leone with a brief reference to oyster culture. In: Pro-
ceedings of the International Workshop on Pen Cage Culture of Fish, 11–12 February 1979, Tigbauan,
Iloilo, Philippines. Aquaculture Department, Southeast Asian Fisheries Development Center, Interna-
tional Development Research Centre. 1979. pp. 118–119.
83. Tan CK, Nowak BF, Hodson SL. Biofouling as a reservoir of Neoparamoeba pemaquidensis (Page,
1970), the causative agent of amoebic gill disease in Atlantic salmon. Aquaculture. 2002; 210(1): 49–
58.
Hydroid succession dynamics in a fish farm
PLOS ONE | https://doi.org/10.1371/journal.pone.0195352 April 2, 2018 18 / 18
