Species composition and assemblage structure of microfouling diatoms growing on fiberglass plates off the coast of Yucatán, Mexico

Abstract

Background:
It is generally accepted that exopolymer films secreted by diatoms promote the onset of macrofouling on surfaces of materials used in marine environments. However, few studies provide precise information at species level regarding the microfouling process. The use of anti-fouling paints on different surfaces to create a toxic environment may aid in precluding development of the initial diatom microfilm leading to macrofouling.

Goals:
To describe the species com position and the structure of fouling diatoms.

Methods:
We analyzed assemblages growing on fiberglass plates, coated and uncoated with antifouling paint, fixed on PVC stands submerged at a 10-m depth. Because diatoms are opportunistic, fast growing microalgae that proliferate on many substrates, our hypothesis was that diatom assemblages growing on fiberglass surfaces, coated or uncoated with antifouling paint, would not differ in their structure.

Results:
Floristic analysis yielded 170 diatom taxa and similar assemblages with high values of diversity occurring on both surfaces.

Conclusions:
In keeping with our hypothesis, both colonized fiberglass surfaces compare to living substrata that favor the growth of diatom associations that exhibit high species diversity. This information will be useful in environmental studies, such as pollution abatement, and for the design and maintenance of fishing boats and industrial equipment prone to biofouling.

Full text

Vol. 27 No. 1 • 2017
Species composition and assemblage structure of microfouling diatoms growing on fiberglass plates off the coast of Yucatán, Mexico
Composición de especies y estructura de asociaciones de diatomeas incrustantes sobre fibra de vidrio en costas de Yucatán, México
Francisco Omar López-Fuerte1, 2, David A. Siqueiros-Beltrones3, Lucien Veleva4 and Dora A. Huerta-Quintanilla5
1Laboratorio de Sistemas Arrecifales, Depto. Académico de Economía, Universidad Autónoma de Baja California Sur. Carretera al Sur, Km. 5.5 s/n,
La Paz, Baja California Sur, 23080. México
2Colección de Microalgas, Centro de Investigaciones Biológicas del Noroeste (CIBNOR). Avenida Instituto Politécnico Nacional 195 s/n, Col. Playa Palo de Sta. Rita,
La Paz, Baja California Sur, 23096, México
3Instituto Politécnico Nacional, Departamento de Plancton y Ecología Marina, Centro Interdisciplinario de Ciencias Marinas (CICIMAR). Avenida Instituto Politécnico Nacional
s/n, Col. Playa Palo de Santa Rita, La Paz, Baja California Sur, 23096, México
4 Instituto Politécnico Nacional, Laboratorio de Fisicoquímica, Departamento de Física Aplicada, Centro de Investigación y de Estudios Avanzados-Unidad Mérida (CINVESTAV)
Km. 6 Antigua carretera a Progreso, Cordemex, s/n, Col. Loma Bonita Xcumpich, Mérida, Yucatán, 97310, México
5Instituto Politécnico Nacional, Laboratorio Nacional para el análisis de Nano y Biomateriales, CINVESTAV
e-mail: dsiquei@gmail.com
Recibido: 21 de septiembre de 2015. Aceptado: 15 de septiembre de 2016.
López-Fuerte F. O., D. A. Siqueiros-Beltrones, L. Veleva and D. A. Huerta-Quintanilla. 2017. Species composition and assemblage structure of microfouling diatoms
growing on berglass plates off the coast of Yucatán, Mexico. Hidrobiológica 27 (1): 23-37.
ABSTRACT
Background. It is generally accepted that exopolymer lms secreted by diatoms promote the onset of macrofouling on
surfaces of materials used in marine environments. However, few studies provide precise information at species level
regarding the microfouling process. The use of anti-fouling paints on different surfaces to create a toxic environment may
aid in precluding development of the initial diatom microlm leading to macrofouling. Goals. To describe the species com-
position and the structure of fouling diatoms. Methods. We analyzed assemblages growing on berglass plates, coated
and uncoated with antifouling paint, xed on PVC stands submerged at a 10-m depth. Because diatoms are opportunistic,
fast growing microalgae that proliferate on many substrates, our hypothesis was that diatom assemblages growing on
berglass surfaces, coated or uncoated with antifouling paint, would not differ in their structure. Results. Floristic analysis
yielded 170 diatom taxa and similar assemblages with high values of diversity occurring on both surfaces. Conclusions.
In keeping with our hypothesis, both colonized berglass surfaces compare to living substrata that favor the growth of
diatom associations that exhibit high species diversity. This information will be useful in environmental studies, such as
pollution abatement, and for the design and maintenance of shing boats and industrial equipment prone to biofouling.
Key words: Bacillariophyceae, colonization, Coscinodiscophyceae, berglass substrate, fouling diatoms, Fragilariophyceae.
RESUMEN
Antecedentes. Las películas de exopolímeros secretadas por diatomeas promueven el establecimiento de organismos ma-
croincrustantes en supercies de materiales utilizados en ambientes marinos. No obstante, pocos estudios proveen informa-
ción taxonómica precisa a nivel especie relativa al proceso de microinscrustación. La aplicación de pinturas antiincrustantes
sobre distintas supercies para crear condiciones tóxicas podrían coadyuvar en impedir el desarrollo de la micropelícula
inicial de diatomeas que conlleva a la macroincrustación. Objetivos. Describir la composición de especies y la estructura de
asociaciones de diatomeas incrustantes. Métodos. Se analizaron asociaciones desarrolladas sobre placas de bra de vidrio,
cubiertas con pintura antiincrustante y sin pintura, sujetas a postes de PVC sumergidos a 10 m de profundidad. Dado que
las diatomeas son microalgas oportunistas de rápido crecimiento que proliferan sobre múltiples sustratos, nuestra hipótesis
fue que las asociaciones de diatomeas que colonizarían las placas de bra de vidrio con o sin recubrimiento antiincrustante
no diferirían en estructura o composición de especies. Resultados. El análisis orístico redituó 170 taxa de diatomeas y
asociaciones similares con valores altos de diversidad. Conclusiones. En acuerdo con nuestra hipótesis, ambas supercies
son comparables a sustratos vivos que favorecen el crecimiento de asociaciones de diatomeas con alta riqueza de especies.
Esta información será útil en estudios ambientales sobre contaminación, y en el diseño y mantenimiento de botes de pesca,
así como de equipo industrial marino susceptible a colonización por microalgas.
Palabras clave: Bacillariophyceae, colonización, Coscinodiscophyceae, diatomeas incrustantes, bra de vidrio, Fragila-
riophyceae,
Hidrobiológica 2017, 27 (1): 23-37

24 López-Fuerte F. O. et al.
Hidrobiológica
INTRODUCTION
Surfaces of materials used in marine environments rapidly become
coated by a conditioning biolm, also referred to as microfouling,
which is highly variable in time and heterogenous in its composition
(Patil & Anil, 2008). These biolms consist mainly of attached bacteria
and diatoms, with all components enmeshed in a matrix of extracellu-
lar polymers secreted during the construction of biolms (Cooksey et
al., 1980). Microfouling modies the substrate surface chemistry and
strongly inuences the subsequent colonization by macrofouling orga-
nisms. Moreover, it is generally accepted that exopolymer lms secre-
ted by diatoms promote the onset of macrofouling by conditioning the
original substrate for the settlement of invertebrate larvae (Characklis &
Cooksey, 1983; Qian et al., 2003; Patil & Anil, 2005a).
Benthic diatoms usually have been identied as major microfoulers
of articial substrata placed in the marine environment, although the
source may be the water column itself or nearby surfaces that may
function as islets (Fernandes et al., 1999). However, many diatom spe-
cies, which turn out to be abundant in articial substrata, are not consi-
dered typically from rocky or other hard substrata but are epipelic forms
(Siqueiros-Beltrones, 2002).
The structure and composition of the microfouling community ex-
hibits wide temporal and regional variations that are also inuenced
by the substratum (Cooksey et al., 1984; Patil & Anil, 2005b). These
changes in community structure are inuenced by various biotic and
abiotic factors and play an important role in the temporal dynamics
of microfouling and macrofouling. Eventually, any diatom assembla-
ge (regardless of the substratum) may reach a climax; then the lm
may degenerate and clumps of the more abundant taxa detach and
drift away, becoming potential colonizers of any available surface, thus
disrupting the classical colonizing sequence from pioneer (prostrated)
forms to erect climax forms (Siqueiros-Beltrones, 2002). Hence, it is
important to understand the species composition of diatoms during bio-
lm formation. Such information will be useful in environmental studies,
such as pollution abatement and the design and operation of industrial
equipment which are prone to biofouling.
Fouling diatoms. Extensive qualitative studies on the fouling diatom
are important in order to gain understanding about autoecological pro-
cesses and behavior of certain taxa under changing environmental con-
ditions. Few studies provide precise taxonomic information at a species
level in the development of microfouling processes. Of the hundreds
of existing diatom genera, only a few have been documented as cons-
tant components of the microfouling, such as Amphora, Licmophora,
Navicula, Nitzschia, Cocconeis, and Achnanthes. The most commonly
reported species include Halamphora coffeiformis (C. Agardh) Levkov,
Achnanthes longipes C. Agardh, Craspedostauros australis E. J. Cox,
Toxarium undulatum J. W. Bailey, and Navicula perminuta Grunow (Mo-
lino & Wetherbee, 2008).
Studies reveal that diatoms have specic preferences among arti-
cial substrata (Mitbavkar & Anil, 2000), e.g., higher diatom recruitment
has been observed on berglass (hydrophobic) than on glass (hydrophi-
lic) surfaces (Patil & Anil, 2005a), although heavy fouling was inciden-
tally documented on silicon treads used to x aluminum foil collectors
(Siqueiros-Beltrones, 2002).
Glass ber reinforced polymer (GFRP) is one of the structural com-
posite materials widely used in engineering applications in seawater for
building and repairing boats, offshore structures in the oil industry, and
many others. It is composed of two phases: the plastic one is termed
the matrix, which is continuous and surrounds the ber reinforcement
embedded and dispersed into a matrix that holds it together (Loewens-
tein, 1973; Gupta & Kothari, 1997).
Most of these early applications have been driven by the need to
overcome the corrosion problem experienced with steel and aluminum
alloys. Another reason for using GFRP has been to reduce weight, par-
ticularly the topside weight of ships. Over 95% of all composite marine
craft are built with GFRP because of its low cost and excellent degra-
dation (corrosion) resistance in seawater (Loewenstein, 1973). GFRP is
usually almost free of defects, with high berglass content for maxi-
mum stiffness, strength, and fatigue resistance.
However, it has been recognized for several decades now that the
use of anti-fouling paints on different surfaces to create a toxic environ-
ment may aid in precluding development of the initial microlm leading
to macrofouling (Robinson et al., 1985), but the effectiveness of anti-
fouling paints may vary. Thus, because diatoms are opportunistic fast-
growing microalgae that proliferate on almost any substrate, given ade-
quate conditions of humidity and nutrients, the concomitant hypothesis
for this study posits that diatom assemblages growing on berglass
surfaces coated with antifouling paint will not differ in their structure
from assemblages growing on uncoated surfaces. To our knowledge,
this is the rst study on fouling diatoms growing on berglass surfaces,
a common material used in shing boats in the Caribbean Sea, whose
duration is signicantly diminished by fouling processes.
MATERIALS AND METHODS
Exposure of samples and their characterization. Biolms grew for 2,
4, and 18 months on 30 (100x40x2 mm) glass-ber-reinforced polymer
plates (GFRP), with only one side coated with antifouling acrylic paint
(as commercially sold for boat construction) immersed in Caribbean
seawater. The polymer plates were xed on PVC stands submerged at
a 10-m depth, 10 km off the Telchac marine station of CINVESTAV–Mé-
rida, located in Yucatán, Mexico between 21°7’ N and 89°25’ W. The
microfouling assays began in March 2011. After different periods of
exposure, triplicate samples of each material were removed from the
sea for observation to determine the type of biofouling adhered to the
material surfaces. At the end of the essays in August 2012, the rest of
the samples was removed for assessment. Likewise, next to the stands
a sediment sample was collected with a spatula (using the top of a box
of Petri as a mold); this was kept in the same Petri dish in ice and in
darkness.
Seawater chemistry. Physical and chemical data were measured in
the laboratory a day after each sampling. Seawater is a very aggressive
medium for materials and can cause severe damage in a very short
time. Usually seawater contains ions (in decreasing quantities) of Cl-,
Na+, SO42-, Mg2+, Ca2+, K+, HCO3-, Br-, B3+, Sr2+, F-, and dissolved gases,
such as O2 and CO2. Thus, seawater at 10-m depth was analyzed for
total salinity, dissolved oxygen, temperature specic sea nutrients, am-
monium, silicates, phosphates, nitrites, and nitrates.
Diatom flora. Three plates were recovered after two months and pro-
cessed 24 hours after being removed from the stands. Plates obtai-
ned after four and 18 months were stored for 4 weeks to separate
the diatoms. The two-month microalgae lm that was detached from

25
Microfouling diatoms on berglass plates
Vol. 27 No. 1 • 2017
both sides of the berglass plates (coated and uncoated) and those that
were separated from the sediments were preserved in ethanol (96%).
Microalgae detached from plates submerged four and 18 months were
treated as a compound sample, without differentiating coated from un-
coated surfaces, and were used solely for oristic purposes. Part of the
samples was observed under the microscope to ensure the existence
of live diatoms.
In order to clean the diatom frustules by removing all organic mat-
ter, the samples were oxidized following the technique by Siqueiros-
Beltrones and Voltolina (2000) in which a mild exothermic reaction is
carried out mixing a portion of the sample with commercial ethanol
(96%) and nitric acid at a 1:3:5 ratio. The oxidized material was then
rinsed with tap water until a pH >6 was reached. Afterwards, six per-
manent preparations were mounted using Pleurax and Zrax (IR 1.7).
Cleaned material was also mounted on stubs and covered with a lm
of graphite spray (Aerodag® G, PELCO®) for observation in a scanning
electron microscope (Jeol JSM–7600F). Diatom identication was done
at 400X and 1000X under a Zeiss compound microscope equipped with
phase contrast, following the works of Schmidt et al. (1874-1959), Pe-
ragallo and Peragallo (1897-1908), Navarro (1982), Foged (1984), Wi-
tkowski et al. (2000), Siqueiros-Beltrones (2002), and López-Fuerte et
al. (2010). The oristic list was constructed according to Round et al.
(1990) and updated in www.algaebase.org (Guiry & Guiry, 2014).
Assemblage structure. To determine the relative abundances of the
diatom taxa, a sample size of 150 individuals (frustules) per slide was
chosen. Numerical analyses were done twice, examining one slide from
each plate and one from the sediments.
Species diversity of the diatom assemblages was estimated ba-
sed on information theory (log2) only on the plates submerged for two
months, inasmuch as the four- and 18-month samples were not diffe-
rentiated by surface (coated and uncoated), but rather as a compound
sample, and thus were used for species composition analysis of the
assemblages and similarity measurement by date. Values of diversity
based on information theory were computed using Shannon’s H’ and
Pielou’s evenness (J’). Simpson’s diversity index (1-λ) and dominance
(λ) were also estimated (Brower & Zar, 1984) to better interpret our esti-
mates of diversity by considering criteria that weight rare and common
species differently (Siqueiros-Beltrones, 1990).
To measure similarity among diatom assemblages, samples were
compared on the basis of presence/absence of species using Jaccard
index, considering also their relative abundances using Bray Curtis In-
dex (Magurran, 1988). These were fed into Program Primer V.5 based
on an agglomerative classication module with exible algorithm (Clar-
ke & Gorley, 2001).
RESULTS
Seawater chemistry. The seawater had total salinity of 37.48, a pH of
7.69, dissolved oxygen 1.1 ppm, and a temperature of 21°C, at a depth
of 10 m. Specic nutrients were (expressed in μM L–1): 1.75 ammonium,
2.61 silicates, 0.28 phosphates, 0.04 nitrites, and 1.84 nitrates.
Diatom flora. In general, the diatoms recruited on the berglass plates
during the study were abundant and diverse (Figures 1, 2, 3). Taxono-
mic observations yielded 170 diatom taxa including species, varieties,
and forms within 61 collected genera of diatoms from the berglass
plates and sediments (Table 1). During the quantitative analysis, a total
of 1,117 valves were counted. The Bacillariophyceae were the most
diverse class with 129 taxa, the Coscinodiscophyceae yielded 22, and
the Fragilariophyceae 19. As in other similar studies, diatom assembla-
ges were dominated by several pennate species (Cassé & Swain, 2006;
Molino et al., 2009; Zargiel et al., 2011; Sweat & Johnson, 2013). Out of
the 60 identied genera, the one with most species were Amphora and
Nitzschia with 13 and Diploneis and Mastogloia with 11. Meanwhile, 35
genera were represented by a single species, mostly uncommon. Sixty-
nine taxa were recorded only once during the quantitative phase, while
35 taxa were recorded only from the two-month submerged plates,
nine from the four-month plates, four from the 18-month submerged
plates, and 28 were recorded exclusively from sediments. Thus 83%
of the recorded taxa in the sediments were present in the berglass
plates. Only four taxa occurred in the three periods: Amphora turgida
Gregory, Mastogloia crucicula (Grunow) Cleve, Rhopalodia musculus
(Kützing) O. Müller, and Grammatophora serpentina (Ralfs) Ehrenberg.
Overall, the estimated diversity for three of the four plates sub-
merged for the two- month period was high; these values indicate
that, besides the high species richness, there was also a somewhat
homogeneous distribution of individuals among species with no single
taxon being clearly dominant (Table 1). This is reected in high-mean
estimates of diversity using two indices (Hʼ and 1-λ). Diversity differen-
ces between the values of the coated and uncoated side (Table 2) were
minimal (higher for the assemblage from the coated side). However,
said differences do not support rejection of the proposed hypothesis,
i.e., structure is similar and thus diatom assemblages develop likewise
on both surfaces.
Conspicuous diatom taxa, such as Cocconeis thalassiana Romero
et López-Fuerte, Delphineis surirella (Ehrenberg) G. W. Andrews, Mas-
togloia corsicana Grunow, M. crucicula (Grunow) Cleve, and Rhopalodia
musculus (Kützing) O. Müller showed a noticeable afnity to the ber-
glass plates, either coated or uncoated, both in terms of frequency and
abundance. Similarity measurements using Jaccard´s index segregated
three associations of diatoms on the berglass plates (Fig. 4). However,
the samples from the 4- and 18-month plates showed only a 31% si-
milarity because they had only ve species in common, suggesting two
distinct assemblages. In contrast, between diatom assemblages from
plates submerged 2 months and from the sediments, there was 69% si-
milarity, since they share 89 species and were clearly segregated from
the other two (Fig. 4).
Based on quantitative data, however, the Bray Curtis similarity index
shows no group segregation, either between plates or according to the
side of the plate (coated and uncoated). In this case, the similarity values
between the three plates were very high (>95%), even between coated
and uncoated surfaces of the number two and three plates (Fig. 5).
On the basis of qualitative similarity (Jaccard´s index), the apparent
group formation could be deceiving (Fig. 6). However, because this type
of similarity measurement tends to yield much lower values than the
qualitative approach, in our experience said differences do not evidence
distinct groups; accordingly, the values are relatively high and segrega-
tion is due to heterogeneous distribution of taxa. Therefore, the overall
similarity analysis indicates that no effect exists due to the use of an-
tifouling paint in terms of deterring taxa typical of a diatom lm taxo-
coenosis, either qualitatively or quantitatively, thus supporting the Ho.

26 López-Fuerte F. O. et al.
Hidrobiológica
Table 1. Overall oristic list of diatoms observed growing on submerged berglass plates during 2 months (FG2), 4 months (FG4), and 18 months
(FG18), and in sediments (SED), 10 km off the coast of Telchac, Yucatán, Mexico. Recorded only from sediments (▲) .
Taxon FG 2 FG 4 FG 18 SED
Bacillariophyceae Haeckel
Coscinodiscophycidae Round et R. M. Crawford
Coscinodiscales Round et R. M. Crawford
Coscinodiscaceae Kützing
Coscinodiscus Ehrenberg
1. Coscinodiscus nitidus W. Gregory + +
2. C. oculus-iridis (Ehrenberg) Ehrenberg + +
Heliopeltaceae H. L. Smith
Actinoptychus Ehrenberg
3. Actinoptychus senarius (Ehrenberg) Ehrenberg + +
Lithodesmiales Round et R. M. Crawford
Lithodesmiaceae Round
Tropidoneis Cleve
4. Tropidoneis pusilla (Gregory) Cleve +
Melosirophycidae E. J. Cox
Melosirales R. M. Crawford
Hyalodiscaceae R. M. Crawford
Hyalodiscus Ehrenberg
5. Hyalodiscus laevis Ehrenberg +
Podosira Ehrenberg
6. Podosira stelligera (Bailey) A. Mann + + +
Paraliaceae R. M. Crawford
Paralia Heiberg
7. Paralia sulcata (Ehrenberg) Cleve + + +
8. P. sulcata var. coronata (Ehrenberg) Andrews + +
9. P. fenestrata Sawai et Nagumo +
Fragilariophyceae Round et R. M. Crawford
Climacospheniales Round
Climacospheniaceae Round
Climacosphenia Ehrenberg
10. Climacosphenia moniligera Ehrenberg +
Fragilariales P. C. Silva
Fragilariaceae Greville
Martyana Round
11. Martyana martyi (Héribaud-Joseph) Round +
Podocystis J. W. Bailey
12. Podocystis adriatica (Kützing) Ralfs ▲
Licmophorales Round et R. M. Crawford
Licmophoraceae Kützing
Licmophora C. Agardh
13. Licmophora paradoxa (Lyngbye) C. Agardh +
14. L. remulus Grunow +
Ulnariaceae E. J. Cox
Hyalosynedra D. M. Williams et F. E. Round
15. Hyalosynedra laevigata (Grunow) D. M. Williams et Round + + +
Opephora Petit
16. Opephora burchardtiae A. Witkowski, D. Metzeltin et H. Lange-Bertalot ▲
17. O. pacifica (Grunow) Petit ▲
Synedra Ehrenberg

27
Microfouling diatoms on berglass plates
Vol. 27 No. 1 • 2017
Taxon FG 2 FG 4 FG 18 SED
18. Synedra sp. + +
Plagiogrammales E. J. Cox
Plagiogrammaceae De Toni
Dimeregramma Ralfs
19. Dimeregramma minor (Gregory) Ralfs + +
Plagiogramma Greville
20. Plagiogramma pulchellum Greville + +
21. P. pulchellum var. pygmaeum (Greville) H. Peragallo et M. Peragallo + +
22. P. rhombicum Hustedt + +
23. P. wallichianum Greville + + +
Rhabdonematales Round et R. M. Crawford
Grammatophoraceae Lobban et Ashworth
Grammatophora Ehrenberg
24. Grammatophora hamulifera Kützing + +
25. G. marina (Lyngbye) Kützing +
26. G. oceanica Ehrenberg + +
27. G. serpentina (Ralfs) Ehrenberg + + + +
28. G. undulata Ehrenberg +
Rhabdonemataceae Round et R. M. Crawford
Rhabdonema Kützing
29. Rhabdonema adriaticum Kützing + +
Rhaphoneidales Round
Psammodiscaceae Round et D. G. Mann
Psammodiscus Round et D. G. Mann
30. Psammodiscus calceatus T. Watanabe, T. Nagumo et J. Tanaka ▲
Rhaphoneidaceae Forti
Delphineis G. W. Andrews
31. Delphineis livingstonii Prasad +
32. D. minutissima (Hustedt) Simonsen ▲
33. D. surirella (Ehrenberg) G. W. Andrews + +
34. D. surirella var. australis (P. Petit) P. M. Tsarenko + +
35. D. surirelloides (Simonsen) G. W. Andrews ▲
Anaulales Round et R. M. Crawford
Anaulaceae (F. Schütt) Lemmerm
Eunotogramma J. F. Weisse
36. Eunotogramma laeve Grunow +
Biddulphiales Krieger
Biddulphiaceae Kützing
Biddulphia S. F. Gray
37. Biddulphia biddulphiana (J. E. Smith) Boyer +
38. B. spinosa (J. W. Bailey) Boyer +
Terpsinoë Ehrenberg
39. Terpsinoë americana (Bailey) Grunow +
Triceratiales Round et R. M. Crawford
Triceratiaceae (Schuett) Lemmermann
Auliscus Ehrenberg
40. Auliscus sculptus (W. Smith) Brightwell + +
Auricula Castracane
41. Auricula intermedia (Lewis) Cleve + +
Odontella C. Agardh
Table 1 (continuation).

28 López-Fuerte F. O. et al.
Hidrobiológica
Taxon FG 2 FG 4 FG 18 SED
42. Odontella aurita (Lyngbye) C. Agardh +
Triceratium Ehrenberg
43. Triceratium balearicum Cleve et Grunow + +
44. T. favus Ehrenberg + +
45. T. pentacrinus (Ehrenberg) Wallich + +
46. T. reticulum Ehrenberg +
Cymatosirales Round et R. M. Crawford
Cymatosiraceae Hasle, Stosch et Syvertsen
Cymatosira Grunow
47. Cymatosira lorenziana Grunow + +
Plagiogrammopsis Hasle, Stosch et Syvertsen
48. Plagiogrammopsis vanheurckii (Grunow) Hasle, von Stosch et Syvertsen +
Thalassiosirales Glezer et Makarova
Thalassiosiraceae M. Lebour
Ehrenbergiulva Witkowski, Lange-Bert. et Metzeltin
49. Ehrenbergiulva granulosa (Grunow) Witkowski, Lange-Bertalot et Metzeltin + +
Shionodiscus A. J. Alverson, S. H. Kang et E. C. Theriot
50. Shionodiscus oestrupii (Ostenfeld) A. J. Alverson, S. H. Kang et E. C. Theriot + +
Thalassiosira Cleve
51. Thalassiosira eccentrica (Ehrenberg) Cleve + +
Bacillariophycidae D. G. Mann
Achnanthales Silva
Achnanthaceae Kützing
Achnanthes Bory de Saint Vincent
52. Achnanthes citronella (A. Mann) Hustedt +
53. A. curvirostrum J. Brun ▲
Amphicocconeis M. De Stefano et D. Marino
54. Amphicocconeis disculoides (Hustedt) Stefano et Marino + +
Cocconeidaceae Kützing
Cocconeis Ehrenberg
55. Cocconeis britannica Naegeli + + +
56. C. discrepans A. W. F. Schmidt + +
57. C. guttata Hustedt et Aleem ▲
58. C. hoffmannii Simonsen ▲
59. C. krammeri Lange-Bertalot et Metzeltin + +
60. C. peltoides Hustedt + +
61. C. pseudomarginata Gregory + +
62. C. scutellum Ehrenberg + +
63. Cocconeis sp. +
64. C. thalassiana Romero et López-Fuerte + +
Bacillariales Hendey
Bacillariaceae Ehrenberg
Denticula Kützing
65. Denticula kuetzingii Grunow + ▲
Nitzschia Hassall
66. Nitzschia amabilis Suzuki +
67. N. angularis var. affinis (Grunow) Grunow +
68. N. bicapitata Cleve + +
69. N. cf. distans W. Gregory + +
70. N. dissipata (Kützing) Grunow + + +
71. N. longissima (Brébisson) Ralfs ▲
Table 1 (continuation).

29
Microfouling diatoms on berglass plates
Vol. 27 No. 1 • 2017
Taxon FG 2 FG 4 FG 18 SED
72. N. martiana (C. Agardh) Van Heurck + +
73. N. panduriformis var. continua Grunow +
74. N. persuadens Cholnoky +
75. N. punctata var. coarctata (Grunow) Hustedt +▲
76. N. sigma (Kützing) W. Smith + +
77. N. sigma var. sigmatella Grunow ▲
78. N. socialis Gregory + +
Tryblionella W. Smith
79. Tryblionella coarctata (Grunow) D. G. Mann +
Cymbellales D. G. Mann
Anomoeoneidaceae D. G. Mann
Staurophora Mereschkowsky
80. Staurophora salina (W. Smith) Mereschkowsky ▲
Gomphonemataceae Kützing
Gomphoneis Cleve
81. Gomphoneis clevei (Fricke) Gil + +
Dictyoneidales D. G. Mann
Dictyoneidaceae D. G. Mann
Dictyoneis Cleve
82. Dictyoneis marginata Cleve f. elongata +
Eupodiscales V. A. Nikolajev et Harwood
Eupodiscaceae Kützing
Eupodiscus J. W. Bailey
83. Eupodiscus radiatus Bailey
Lyrellales D. G. Mann
Lyrellaceae D. G. Mann
Lyrella Karayeva
84. Lyrella approximatoides (Hustedt) D. G. Mann +
85. L. barbara (Heiden) D. G. Mann + +
86. L. clavata (Gregory) D. G. Mann + +
87. L. clavata var. subconstricta (Hustedt) Moreno + +
88. L. diffluens (A. Schmidt) D. G. Mann + +
89. L. exsul (A. Schmidt) D. G. Mann +
90. L. irrorata (Greville) D. G. Mann +
91. L. lyra (Ehrenberg) Karajeva + +
92. L. praetexta (Ehrenberg) D. G. Mann + +
Petroneis Stickle et D. G. Mann
93. Petroneis marina (Ralfs) D. G. Mann + +
94. P. plagiostoma (Grunow) D. G. Mann + +
Mastogloiales D. G. Mann
Mastogloiaceae Mereschkowsky
Mastogloia Thwaites
95. Mastogloia binotata (Grunow) Cleve + +
96. M. cf. rigida Hustedt + +
97. M. corsicana Grunow + + +
98. M. crucicula (Grunow) Cleve + + + +
99. M. crucicula var. alternans Zanon + +
100. M. cuneata (Meister) R. Simonsen + +
101. M. fimbriata (T. Brightwell) Grunow + +
102. M. gibbosa Brun ▲
103. M. ovulum Hustedt +
Table 1 (continuation).

30 López-Fuerte F. O. et al.
Hidrobiológica
Taxon FG 2 FG 4 FG 18 SED
104. M. pseudolatecostata T. A. Yohn et R. A. Gibson + +
105. M. splendida (Gregory) Peragallo + +
Naviculales Bessey
Amphipleuraceae Grunow
Halamphora (Cleve) Levkov
106. Halamphora coffeaeformis (C. Agardh) Levkov + +
107. H. cymbifera (Gregory) Levkov + +
108. H. luciae (Cholnoky) Levkov +
109. H. turgida (Gregory) Levkov + + + +
Diadesmidaceae D. G. Mann
Diploneis Ehrenberg
110. Diploneis bomboides (A. W. F. Schmidt) Cleve + +
111. D. chersonensis (Grunow) Cleve + +
112. D. crabro (Ehrenberg) Ehrenberg + +
113. D. crabro var. dirhombus (A. Schmidt) Cleve + +
114. D. litoralis (Donkin) Cleve + +
115. D. litoralis var. clathrata (Østrup) Cleve + +
116. D. notabilis (Greville) Cleve ▲
117. D. papula (A. W. F. Schmidt) Cleve var. papula + +
118. D. papula var. constricta Hustedt +
119. D. suborbicularis (W. Gregory) Cleve + +
120. D. vacillans (A. Schmidt) Cleve + +
Caloneis Cleve
121. Caloneis fossilis Cleve-Euler + +
122. C. liber (W. Smith) Cleve ▲
123. C. linearis (Grunow) Boyer ▲
124. C. robusta (Grunow) Cleve ▲
125. Caloneis sp. +
Haslea Simonsen
126. Haslea sp. +
Naviculaceae Kützing
Navicula Bory
127. Navicula (Lyrella) clavata var. distenta (Kuntz) Hustedt + +
128. N. arenaria Donkin + +
129. N. cancellata Donkin ▲
130. N. clavata var. indica (Greville) Cleve +
131. N. digito-radiata (Gregory) Ralfs ▲
132. N. directa (W. Smith) Ralfs + +
133. N. duerrenbergiana Hustedt +
134. N. lusoria Giffen + +
135. N. longa (Gregory) Ralfs + + +
Trachyneis Cleve
136. Trachyneis aspera (Ehrenberg) Cleve +
Pinnulariaceae D. G. Mann
Oestrupia Heiden
137. Oestrupia zanardiniana (Grunow) Schrader + +
Plagiotropidaceae D. G. Mann
Plagiotropis Ptzer
138. Plagiotropis delicatula (Greville) T. B. B. Paddock ▲
139. P. pusilla (Greville) Kuntze + +
Pleurosigmataceae Mereschowsky
Pleurosigma W. Smith
Table 1 (continuation).

31
Microfouling diatoms on berglass plates
Vol. 27 No. 1 • 2017
Taxon FG 2 FG 4 FG 18 SED
140. Pleurosigma formosum W. Smith + +
141. P. inflatum Shadbolt ▲
Scoliotropidaceae Mereschowsky
Biremis D. G. Mann et Cox
142. Biremis ambigua (Cleve) D. G. Mann + +
Sellaphoraceae Mereschowsky
Fallacia Stickle et D. G. Mann
143. Fallacia forcipata (Greville.) Stickle et Mann +
144. F. nummularia (Greville) D. G. Mann ▲
145. F. vittata (Cleve) D. G. Mann ▲
Rhopalodiales D. G. Mann
Rhopalodiaceae (Karsten) Topachevs’kyj et Oksiyuk
Epithemia Kützing
146. Epithemia intermedia Fricke + +
Rhopalodia O. Müller
147. Rhopalodia acuminata Krammer + +
148. R. gibberula var. producta (Grunow) Cleve-Euler +
149. R. musculus (Kützing) O. Müller + + + +
150. R. pacifica Krammer +
Surirellales D. G. Mann
Entomoneidaceae Reimer
Entomoneis Ehrenberg
151. Entomoneis alata (Ehrenberg) Reimer + +
Surirellaceae Kützing
Campylodiscus Ehrenberg
152. Campylodiscus samoensis Grunow +
Psammodictyon D. G. Mann
153. Psammodictyon panduriforme (W. Gregory) D. G. Mann + +
154. P. panduriforme var. minor (W. Gregory) E. Y. Haworth et M. G. Kelly + +
Surirella Turpin
155. Surirella fastuosa (Ehrenberg) Ehrenberg + +
156. S. fastuosa var. cuneata O. Witt + +
157. S. fluminensis Grunow +
158. S. hybrida var. contracta H. Peragallo et M. Peragallo ▲
Thalassiophysales D. G. Mann +
Catenulaceae Mereschowsky
Amphora Ehrenberg
159. Amphora abludens R. Simonsen + +
160. A. arenicola Grunow ▲
161. A. bigibba var. interrupta (Grunow) Cleve ▲
162. A. cingulata Cleve + +
163. A. graeffeana Hendey ▲
164. A. immarginata Nagumo ▲
165. A. kolbei Aleem +
166. A. marina W. Smith + +
167. A. ocellata Donkin +
168. A. ostrearia var. vitrea Cleve +
169. A. proteus Gregory + + +
170. A. proteus var. contigua Cleve + +
Table 1 (continuation).

32 López-Fuerte F. O. et al.
Hidrobiológica
Figures 1a-l. a-b) Cocconeis sp. c) Paralia sulcata. d) Paralia fenestrata. e) Delphineis surirella. f) Mastogloia crucicula var. alternans. g) Rhopalodia musculus.
h) Cocconeis discrepans. i) Diploneis bomboides. j) Mastogloia corsicana. k) Psammodictyon panduriforme var. minor. l) Fallacia forcipata. Escala: Figs. a-b, d = 10 µm;
Figs. c, e-l = 1 µm.
Table 2. Diversity values describing the structure of the diatom assemblages found growing on berglass plates (FG PLATES) off the coast of Yu-
catán, Mexico. C = coated, NC = Uncoated. S = Species richness; H’ = Shannon´s species diversity; J’ = Equitatibility; 1- λ = Simpson´s diversity;
λ = Dominance.
FG PLATES S N JʼHʼ λ 1-λ
1C 54 153 0.85 4.90 0.05 0.95
1NC 45 151 0.81 4.42 0.08 0.92
2C 44 159 0.84 4.60 0.06 0.94
2NC 38 152 0.81 4.27 0.09 0.91
3C 41 154 0.82 4.38 0.08 0.92
3NC 31 151 0.80 3.96 0.10 0.90
a) b)
c)
d) j) k) l
e)
f)
g) h) i)

33
Microfouling diatoms on berglass plates
Vol. 27 No. 1 • 2017
Figures 2a-m. a) Actinoptychus senarius. b) Coscinodiscus nitidus. c) Shionodiscus oestrupii. d) Paralia sulcata var. coronata. e) Grammatophora serpentina.
f-g) Rhabdonema adriaticum. h) Triceratium reticulum. i) T. favus. j) Campylodiscus samoensis. k) Odontella aurita. l) Terpsinoë americana. m) Auricula intermedia.
Escala = 10 µm.
a)
b)
c)
d)
e
f) g)
h)
i)
j)
k)
l) m)
DISCUSSION
Our results reveal that the fouling populations were heterogenous and
included epipsammic, epiphytic, and epipelic (tychoplankton) species
with different afnities (marine, brackish, and even freshwater). The
species composition and structure (diversity, dominance, and equita-
bility) of the diatom assemblage growing on the surface coated with
antifouling paint was very similar to that of the uncoated surface, re-
gardless of the time the plate had been submerged. Even though the
computed diversity values were high, they do fall within the range-esti-
mated values for this type of taxocoenosis (Siqueiros-Beltrones, 2005).
They do, however, suggest that the colonized substrata (coated and
uncoated) may be compared to those that favor the growth of diatoms
such as macroalgae and seagrasses, which harbor abundant epiphytic
forms. Although the number of taxa per plate appeared to be the main
component of the high diversity values estimated, the distribution of
individuals among the taxa was also uniform, deriving in high values
of equitability.

34 López-Fuerte F. O. et al.
Hidrobiológica
Many of the species found in this study belong to genera from
estuarine environments that occur commonly as biofouling (Molino
& Wetherbee, 2008), including Amphora, Nitzschia, Diploneis, Masto-
gloia, and Navicula. As in similar studies (Characklis & Cooksey, 1983;
Cooksey et al., 1984), the assemblage in the biolm was dominated
by pennate diatoms, irrespective of the nature of the substratum and
the exposure period. Anil et al. (2006) observed that pennate diatoms
such as Amphora, Navicula, and Nitzschia species often dominate the
fouling assemblage as well as epibiotic populations, since they are able
to attach to substrates. Our observations partly agree with Amphora,
Nitzschia, Mastogloia, and Diploneis being the dominant taxa; the latter
two taxa are very common in sediments.
Figures 3a-q. a) Surirella fastuosa. b) S. fastuosa var. cuneata. c) Mastogloia splendida. d) M. fimbriata. e) Lyrella approximata. f) L. barbara. g) Navicula (Lyrella)
clavata var. distenta. h) Navicula (Lyrella) caribaea. i) Lyrella lyra. j) Trachyneis aspera. k) Diploneis bomboides. l) D. crabro var. dirhombus. m) D. papula var. papula.
n) Navicula arenaria var. arenaria. o) N. longa. p) Amphora proteus. q) A. ostrearia var. vitrea. Escala = 10 µm.
a) b)
c) d)
f)
e)
j)
i) k)
n)
g) h) p) q) m) l) o)

35
Microfouling diatoms on berglass plates
Vol. 27 No. 1 • 2017
The examination of the sediment adjacent to the structure holding
the berglass plates rendered an accurate reference of the origin of the
diatoms found on the plates, because many of the diatom taxa have
been recorded from sediments (83 %). These observations indicate that
the dominance of certain species in the biolm can be attributed to
their dominance in the adjacent sediments, resulting in a higher subs-
tratum-encountering probability. Benthic diatoms that are frequently
re-suspended by hydrodynamic or biotic processes may, after a whi-
le, colonize a different available substrate (Breznak et al., 1985). Once
attached, the growth and assemblage structure is further dependent
upon the physicochemical and biological nature of both the ambient
water and the substrate surface. Studies reveal that diatoms have spe-
cic substrate preferences (Mitbavkar & Anil, 2000), and higher diatom
recruitment has been observed on berglass (hydrophobic) than on a
hydrophilic surface such as glass (Patil & Anil, 2005a). Due to its physi-
cal characteristics, the berglass plates allow initially for the settlement
of small forms (<20 µm) of diatoms (Figures 1a-b), which in turn make
the substrate favorable for large forms (Figures 1c-l). Also, the presence
of sand on both sides of the plates may be a factor because diatoms
from the sediments (epipelic and epipsammic) may migrate from the
sediments (Round et al., 1990) to the available space in the plates,
nding it suitable for growth and colonizing it, as observed in this expe-
riment. Heavy diatom growth has been known to occur as thick lms in
certain articial substrata such as PVC surfaces and silicon, where up
to 178 taxa have been recorded for colonization periods of three weeks
(Siqueiros-Beltrones, 2002).
The assemblage structure was similar to that recorded for many
studies on benthic diatoms, i.e., few abundant species, many common
species, and many more rare species, but once either in the qualitative
or quantitative analysis. The number of identied taxa in this investi-
gation is similar to diatom assemblages from natural substrata, e.g.,
López-Fuerte et al. (2013), in which 106 taxa were recorded living as
epiphytes of Thalassia testudinum K. D. Koenig in Yalahau lagoon, Quin-
tana Roo, Mexico. On the other hand, in comparison with other studies
that used articial substrata, the number of diatom taxa recorded here
is much higher, e.g., Fernandes et al. (1999) and Patil & Anil (2005b)
reported 60 and 51 taxa, respectively, growing on glass slides.
The marked difference in the number of taxa recovered from the
berglass plates from one period of submergence to another, i.e.,
135 taxa in the two-month plates vs. 11 and 21 taxa for the four- and
eighteen-month plates, may be explained by the fact that when diatom
lms reach a certain degree of growth, lumps then begin to detach
from the lms and so provide colonizing material for other substrata
(Siqueiros-Beltrones, 2002). Thus, much of the diatom ora from the
late phases of succession would be lacking in the plates submerged
for longer periods.
Because exopolymer lms secreted by diatoms promote the onset
of macrofouling by conditioning the original substrate for invertebrate
larvae, it is necessary to acquire a precise knowledge of the micro-
fouling species from the initial phases of microfouling in order to better
understand the ecological processes that may be helpful for controlling
fouling events. Likewise, the development of anti-fouling paints should
focus on avoiding the settlement and growth of diatoms, thus delaying
the onset of macrofouling that generally depends on the modulation of
the substrate by pioneer microfouling diatoms.
Figure 4. Similarity of diatom assemblages grown on berglass (FG) plates and
sediments (SED), based on Jaccard’s similarity index. M = Months.
FG 18M
FG 4M
FG 2M
SED
0 20 40 60 80 100
Figure 5. Similarity (Bray Curtis) of diatom assemblages grown only on berglass
plates, with no group segregation. C = coated, NC = uncoated, surfaces.
PLATE 3NC
PLATE 2NC
PLATE 1NC
PLATE 1C
PLATE 3C
PLATE 2C
60 70 80 90 100
Figure 6. Similarity of diatom assemblages grown only on berglass plates, ba-
sed on Jaccard’s index with group segregation. C = coated, NC = uncoated,
surfaces.
PLATE 3NC
PLATE 1C
PLATE 1NC
PLATE 3C
PLATE 2NC
PLATE 2C
95 96 97 98 99 100
Overall, the above results suggest a greater ability of benthic dia-
toms to colonize berglass surfaces, which is probably explained by a
higher degree of contact between the cells and the surface. Moreover,
as observed in natural substrata, the structure of diatom assemblages
showed variations that may be attributed to how long the plates were
submerged. In order to sustain this, intermediate submersion times
should be implemented in order to allow other successional phases to
be detected.

36 López-Fuerte F. O. et al.
Hidrobiológica
Because the microfouling diatom assemblages may provide sui-
table conditions for the onset of macrofouling, we suggest further re-
search be undertaken in order to better understand their successional
processes, which may aid in developing an efcient strategy for pre-
venting or delaying the settlement of macrofouling organisms.
ACKNOWLEDGEMENTS
This research was supported by the Mexican Council of Science
and Technology (CONACYT) under Grant 179110. SEM micrographs
were obtained at the Laboratory of Microscopy, CINVESTAV, Unidad Mé-
rida, Mexico. FOLF currently holds a postdoctoral research grant from
CONACYT. DASB is COFAA and EDI fellow at the IPN. We acknowledge
reviews by the appointed referees and editors.
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