J Appl Phycol
DOI 10.1007/s10811-010-9602-y
Does biofouling influence Kappaphycus alvarezii (Doty) Doty
ex Silva farming production in Brazil?
Rafael Guedes Marroig & Renata Perpetuo Reis
Received: 24 September 2009 / Revised and accepted: 22 September 2010
# Springer Science+Business Media B.V. 2010
Abstract The commercial cultivation of Kappaphycus
alvarezii is the main source of raw material for the
carrageenan industry. Brazilian commercial farming uses
floating rafts that serve as substrata for fouling organisms
that may affect production of the carrageenophyte seedlings.
The aim of this work was to identify and quantify the
biofouling on floating rafts at Sepetiba Bay, Rio de Janeiro
State (23° 02′ 25″ S and 43° 53′ 39″ W), and to evaluate
seedling damage caused by epibionts and endobionts.
Samples were collected from August 2006 to August 2007.
In each assessment, organisms contained in random sampling areas of 18 quadrats of 0.10 m2 (n=18) were removed
from floating rafts. K. alvarezii seedling samples were
collected to verify the presence of epibionts or endobionts
(n=30). Twenty-four taxa belonging to seven groups of
animals and three groups of seaweed were found. The
percentage occurrence estimated 13 dominant organisms and
amphipod tubes: e.g., Chondracanthus tedii, Cladophora
vagabunda, Gracilariopsis tenuifrons, Hypnea spinella,
Hypnea musciformis, Hincksia mitchelliae, Spyridia spp.,
Ulva spp., Bowerbankia sp., Bugula neritina, Botryllus sp.,
Haplosclerida sp., and Perna perna. Richness, equitability,
diversity, and total biomass varied significantly during the
study period (p<0.001). There was a tendency for higher
biomass values in August 2007. After 6 months, epibionts
(i.e., Chlorophyta, Rhodophyta, Chordata, Cnidaria and
Ectoprocta) were found on K. alvarezii seedlings. Endobionts were not found in this study. The biofouling biomass
was not found to have a significant effect on K. alvarezii
R. G. Marroig : R. P. Reis (*)
Instituto de Pesquisas do Jardim Botânico do Rio de Janeiro,
Rua Pacheco Leão, 915,
CEP 22460-030 Rio de Janeiro, RJ, Brazil
e-mail: [email protected]
daily growth rate, carrageenan yield, or quality (gel strength
and viscosity; p>0.05).
Keywords Kappaphycus alvarezii . Biofouling . Epibionts .
Endobionts . Commercial farming . Floating rafts
Introduction
Kappaphycus alvarezii (Doty) Doty ex Silva has been
introduced around the world for commercial purposes to
supply the carrageenan industry (Ask and Azanza 2002;
Pickering et al. 2007). In Brazil, this species was introduced
in São Paulo State in 1995 for experimental culture (Paula
and Pereira 1998; Paula et al. 2002) and later in Rio de
Janeiro State which now holds the largest Kappaphycus
commercial farms, consisting of 100 floating rafts (Castelar
et al. 2009).
As with any object, the moment the floating rafts and the
seedlings are placed into the sea, fouling colonization
begins and follows a pattern of succession, i.e., 1 min after
immersion, the biochemical conditioning begins; after 1 h,
bacterial colonization follows; and after several days,
unicellular eukaryotic organisms (e.g., yeasts, protozoa,
and diatoms) begin their colonization. After several days,
the multicellular eukaryotes begin fouling, thus changing
the process from physical to predominant biological fouling
(Wahl 1989).
The epibiotic association creates a complex network of
advantages and disadvantages between the epibiont and
basibiont (Wahl 1989). Epibionts may affect the predator–
prey relation negatively or positively since they can repel
the predator/herbivore or alternatively attract them. Epibionts and basibionts compete for space for development
(Wahl et al. 1997). In addition, epibionts can cause damage
J Appl Phycol
to the carrageenophyte seedlings which may be followed by
bacterial diseases (Vairappan 2006; Vairappan et al. 2008).
The properties of the substrata, environmental effects, or
regional differences will influence the organisms that are
going to develop in the fouling community (Richmond and
Seed 1991). Organisms that colonize the substrata are
known as biofoulers; those that colonize organic substrata
are epibionts. Endobionts are those that develop inside
other organisms; basibionts are organisms which act as a
substratum for epibionts (Taylor and Wilson 2002).
Biofouling studies are extremely important to understand
the ecological models and processes which maintain species
diversity, avoid bioinvasion, and prevent biofouling on
surfaces used in human activities (Gama et al. 2009).
According to Vairappan et al. (2008), information about
biofouling on floating rafts used for the commercial
cultivation of K. alvarezii can also help to avoid diseases
and epiphyte infections, which reduce production and in
some cases may compromise integrity and value of the crops,
as has been reported in the Philippines, Tanzania, Indonesia,
and Malaysia. A significant epiphyte outbreak was reported
in 1975 but little attention was given to it. Since 2000, there
has been an increase in epiphyte outbreaks and consequently
large impacts on K. alvarezii production related to the red
alga Neosiphonia. Only after understanding the infection
processes was it possible to elaborate a protocol to mitigate
this problem (Hurtado et al. 2008).
The aim of this study was to identify and quantify any
biofouling which occurred on floating rafts at Sepetiba Bay,
Fig. 1 K. alvarezii farm at
Marambaia Bay in Sepetiba
Bay, southern Rio de Janeiro
State, Brazil. Smaller map
shows an outline of Brazil
(gray) with the coastline studied
shaded black
Rio de Janeiro State, and to evaluate any seedling damage
caused by epibionts and endobionts. The effect of the
biofouling biomass on K. alvarezii daily growth rate,
carrageenan yield, and quality (gel strength and viscosity)
was used to determine economic impact.
Material and methods
The largest Brazilian commercial cultivation of K. alvarezii
began in 2004 at Marambaia Bay (MB 23° 03′ 50″ S and
043° 52′ 50″ W), located south of Sepetiba Bay, on the
south coast of Rio de Janeiro State (Castelar et al. 2009)
(Fig. 1).
Based in Köppen’s classification, the macroclimate of
Marambaia Bay is defined as tropical with rainy summers
and dry winters (Aw) and Nimer’s mesoclimate is defined
as tropical, hot, and super humid. Mean monthly air
temperatures vary from 20°C to 27°C. The annual mean
rainfall is 1,240 mm, occurring 37% in summer and 15% in
winter. Throughout the year, the relative air humidity is
approximately 80%, decreasing in the winter. The highest
irradiation occurs in summer, decreasing in winter (Mattos
2005). The mean surface seawater temperature is 25°C
ranging from 19°C to 30°C; the mean water transparency is
0.6 m, ranging from 0.7 to 1.5 m; irradiance can reach a
maximum of 4,235 μmol photons m−2 s−1 with a mean of
435 μmol m−2 s−1. The mean wind speed is 3 m s−1,
reaching up to 27 m s−1, and the mean salinity is 33 ppt
J Appl Phycol
ranging from 27 to 37 ppt (Castelar et al. 2009). Marambaia
Bay is characterized as shallow (about 2 m) with a sandy
beach, approximately 20 km long with no rocky areas
(Fig. 1).
The study was conducted from August 2006 to August
2007. At that time, there were about 100 floating rafts
involved in commercial production. The floating rafts were
composed of 30 modules (5×3 m). In each module, about
220 seedlings were fixed by tie-tie method using ten nylon
lines with a nylon net (60-mm mesh size) suspended below
rafts to avoid loss of seedlings from the module. Rafts with
nearly 45 days of cultivation were randomly selected for
sampling. In each sample period, quadrats (0.10 m2) were
randomly placed on the rafts (n=18), and the biofouling
organisms inside the quadrats were removed and quantified.
Specimens of K. alvarezii were randomly sampled (n=30)
to verify the presence of epibionts and endobionts. The
material was fixed in a seawater (4%) formaldehyde
solution prior to optical microscope observations; the
biofouling organisms were oven-dried (60°C). The epibionts and endobionts were classified following the
terminology adopted by Hurtado et al. (2008) which
grouped organisms according to damage that they cause
to the basibiont.
The biofouling samples were quantified and percentage dry mass in relation to total dry mass of organisms
calculated, using the formula: percentage occurrence
(PO)=(organism mean dry mass/mean of total organism
dry mass)×100 (Amado Filho et al. 2003; Reis 2009).
The organisms with POs lower than 5% were grouped and
classified as “others.” A richness, biomass, and diversity
index (Shannon–Wiener H′) and equitability index (Pielou
J′) were calculated for each sampling period (Brower et al.
1997). The algae were also allocated into their respective
functional form groups (Littler and Littler 1980) and
classified in accordance to the model proposed by Steneck
and Dethier (1994) based on anatomical and morphological characteristics that often correspond to ecological
characteristics. Taxonomic nomenclature followed Algae
Base (Guiry and Guiry 2009). The identified specimens
are deposited in the Herbarium of the Botanical Garden of
Rio de Janeiro (RB).
The Shapiro–Wilk (Zar 1996) test was used to evaluate
the normality of the data, and Cochran’s (Zar 1996) test
was used to verify homogeneity of the variances prior to
the use of parametric statistical analysis. Nonparametric
data were transformed according to Zar (1996). Differences between richness, diversity, and equitability of an
organism during the sampling period were tested by oneway analysis of variance (ANOVA), and the means were
compared by a Tukey post hoc test (Zar 1996). Differences
in biomass for nonparametric data during the sampling
period were tested using the Kruskal–Wallis test (Zar
1996). The effect of biofouling biomass on K. alvarezii
daily growth rate was verified during the sampling period
by polynomial regression and in relation to carrageenan
yield and quality (gel strength and viscosity) in August
2007.
Statistica 6.0 StatSoft Inc. was used for statistical
analysis. The confidence interval for tests of significance
was 95% (p=0.05).
Results and discussion
Twenty-four taxa belonging to 7 invertebrate groups (i.e.,
Annelida, Chordata, Cnidaria, Crustacea, Ectoprocta,
Mollusca, and Porifera), 3 macroalgae (i.e., Chlorophyta,
Heterokontophyta, and Rhodophyta), and amphipod tubes
were identified in the biofouling community (Table 1). No
new records were found for Sepetiba Bay (Amado Filho et
al. 2003; Amado Filho and Marins 2004; Junqueira et al.
2004; Breves-Ramos et al. 2005). The low number of taxa
obtained was a consequence of samples being taken from
the rafts 45 days after the structures were placed in the sea
and probably represented organisms at an early stage of
ecological succession.
A number of organisms and particularly amphipod tubes
showed a temporal variation, and in general, in each
sample, the most representative groups were Ectoprocta,
Rhodophyta, and amphipods tubes (Fig. 2). Bugula neritina
and amphipod tubes occurred during all months sampled
(Table 1). In the last 2 months, the abundance of amphipods
tubes was lower than 5% (Fig. 2). From August to October
2006 and from July to August 2007, B. neritina made a
high contribution, though between January and April 2006,
its abundance was lower while that of Bowerbankia sp. was
higher. Bowerbankia sp. replaced B. neritina in its absence
or low frequency. It is known that Bugula spp. are common
on marine farming structures and compete for space and
nutrients with other organisms such as oysters, mussels,
barnacles and filamentous algae (Cetto, personal communication). This can be considered as a positive factor for the
farming of K. alvarezii as the rafts can sink below the
waterline due to the weight of the calcareous organisms,
thus requiring more laborious management in order to clean
the rafts. A positive feature is that it also reduces
competition with filamentous algae that may cause diseases, e.g., in the Indo Pacific with Neosiphonia spp.
(Vairappan et al. 2008).
Hypnea spinella dominated almost all sampling times,
and Spyridia could be frequently found as dominant—
except in July and August 2007. According to the formfunctional model proposed by Steneck and Dethier (1994),
the first species belongs to the corticated group which is
regarded as more resistant to biological and physical
x
x
x
x
Jan
x
x
x
o
o
x
x
x
x
x
x
x
o
x
x
x
x
x
x
x
x
x
x
x
x
o
x
x
x
o
o
x
x
x
x
x
x
x
x
x
x
x
Apr
x
x
o
x
x
x
o
x
x
x
x
x
x
x
Jul
x
x
x
x
x
o
x
x
x
Aug 2007
(o) indicates organisms with less than 0.1 g m−2 and (x) organisms with more than 0.1 g m−2 . Form-functional groups are represented by (1)=filamentous, (2)=foliose, and (3)=corticated algae
x
x
x
x
x
o
Amphipods tubes
x
o
x
x
x
Botrylloides nigrum Herdman
Botrylloides sp1. Milne-Edwards
Urochordata–Ascidiacea
Tetraclita sp. Lamarck
Crustacea Cirripedia
o
x
o
x
x
x
x
x
x
x
x
x
x
x
o
x
x
x
x
x
x
x
Mar
Perna perna Linnaeus
x
o
x
x
x
x
x
x
x
x
Feb
Noetia bisulcata Lamarck
Mollusca
o
x
Polychaeta sp1.
o
x
x
x
x
x
Polychaeta sp2.
Annelida Polychaeta
x
x
Bowerbankia sp. Farre
Crisia eburnea Linnaeus
x
Bugula neritina Linnaeus
Ectoprocta
Actinia sp. Linnaeus
Cnidaria Anthozoa
Hymeniacidon sp. Parker
Haplosclerida sp. Topsent
x
Spyridia filamentosa (Wulfen) Harvey (1)
Porifera
x
Spyridia hypnoides (Bory) Papenfuss (1)
x
x
Hypnea spinella (C. Agardh) Kützing (3)
x
o
x
x
Hypnea musciformis (Wulfen) J.V. Lamouroux (3)
x
x
x
o
Dec
x
x
x
o
Oct
Gracilariopsis tenuifrons (C.J. Bird and E.C. Oliveira) Fredericq and Hommersand (3)
x
x
Chondracanthus teedei (Mertens ex Roth) Fredericq (3)
o
o
Sep
Acanthophora spicifera (Vahl) Börgesen (3)
Rhodophyta
Hincksia mitchelliae (Harvey) P.C. Silva (1)
Ochrophyta
o
x
Ulva flexuosa Wulfen ssp. flexuosa Wulfen (2)
Ulva lactuca Linnaeus (2)
o
Cladophora vagabunda (L.) C .Hoek (1)
Chlorophyta
Aug 2006
Table 1 Biofouling, between August 2006 and August 2007, on the floating rafts at Marambaia Bay in Sepetiba Bay, Rio de Janeiro State, Brazil
J Appl Phycol
J Appl Phycol
Fig. 2 Abundance of the dominant biofouling on rafts at
Marambaia Bay in Sepetiba
Bay, southern Rio de Janeiro
State, Brazil, between August
2006 and August 2007
disturbance. In fact, the rafts are positioned 60 cm below
the surface and are consequently exposed to strong water
motion caused by winds during storms (Castelar et al.
2009) which may favor their growth (Reis and YoneshigueValentin 1998). Herbivory by fish and amphipods, apparently abundant at this site, might have removed some filamentous and foliose algae that are more palatable than the
corticated group (Steneck and Dethier 1994). Cladophora
vagabunda abundance was high on two occasions (40% in
July and 21% in August) when the abundance of amphipod
tubes was also lower than average at 6–35%. Other
organisms occasionally presented high abundance values.
For example, Gracilariopsis tenuifrons contributed 40% in
February 2007 and an impressive beach-cast biomass
(Castelar et al. 2009). When compared to corticated groups
in macroalgal assemblage previously studied at Sepetiba
Bay (Amado Filho et al. 2003; Reis 2009), we found a
similar response, in general nearly 50%. However, in 1999,
Spyridia spp. were not as abundant (Amado Filho et al.
2003) as in the present study.
In most samples (six), Botryllus spp. (Ascidia) were
found covered by silt and clay (September 2006 and April,
July, and August 2007). Ascidia are known to be sensitive
to turbidity (Junqueira et al. 2004) which is a characteristic
of Marambaia Bay (mean 0.6 m), and Botryllus spp. are
commonly found at Rio de Janeiro State (Breves-Ramos et
al. 2005). The abundance of amphipod tubes, invertebrates,
and algae varied on the net below the K. alvarezii rafts. In
winter and spring, the amphipod tubes and animals
predominated while in other seasons algae were more
abundant. The biomass of amphipod tubes was overestimated since it also contained inorganic matter, but it was
considered in this work because it was indicative of a
greater number of amphipods that can influence the growth
of seedlings as also observed by Reis et al. (2003) for
Hypnea musciformis. The highest number of taxa (eight)
occurred in early summer (December).
The richness, dry biomass, equitability, and diversity
varied over time (Fig. 3). A significant difference was
observed through time (one-way ANOVA, F=11.45, p<
0.001) with the highest richness in August and September
2006 and lowest in February, July, and August 2007.
There was a tendency for decreasing biomass through time
being significantly higher in August and December 2006
(H=56.71, p<0.001), probably due to the presence of B.
neritina, amphipods tubes, Ascidia, and corticated algae
(Gracilariopsis and Spyridia spp.). Diversity (one-way
ANOVA, F=6.98, p<0.001) and equitability (one-way
ANOVA, F=4.48, p<0.001) had lower values in August
2006 and February, July, and August 2007.
During the sampling period, no effect of biofouling
biomass was found on the daily growth rate (r2 =0.02, p=
0.44) of K. alvarezii. The same occurred in August 2007 in
relation to carrageenan yield (r2 = 0.53, p = 0.32), gel
strength (r2 =0.51, p=0.34), and viscosity (r2 =0.38, p=
0.49).
Since February 2007 we have found epibionts on K.
alvarezii seedlings, e.g., amphipods tubes, Bowerbankia
sp., Anemonia sargassensis, Botryllus sp., G. tenuifrons,
C. vagabunda, Ulva flexuosa ssp. flexuosa, Hypnea
musciformis, and H. spinella. In accordance with the
terminology adopted by Hurtado et al. (2008), we found
macroepiphytes, types 1 and 2, that did not cause
significant damage to the seedlings. Since Hurtado et al.
(2008) did not classify the animals, we considered them
similar to the macroalgal types 1 and 2 because they did
not cause damage to the host. All the organisms found as
epibionts were observed as biofouling in the rafts, except
J Appl Phycol
Fig. 3 Biomass (a), richness (b), diversity (c), and equitability (d) of the
biofouling on the floating rafts at Marambaia Bay in Sepetiba Bay,
southern Rio de Janeiro State, Brazil. In a, lozenge=median, rectangle =
quartile (25, 75%), vertical bar = nonoutlier range, circle = outliers, and
asterisks = extremes. In b, c, and d, square = mean, rectangle = standard
error, vertical bar = standard deviation, circle = outliers, and asterisks =
extremes
A. sargassensis, sampled in February that was observed
only on K. alvarezii.
A positive fact was the absence of “goose bumps”
that indicate the initial stages of endophytic algal
infestation which can lead to the degradation of the
seedling by opportunistic bacteria, such as Alteromonas,
Flavobacterium and Vibrio (Vairappan et al. 2008). A
negative impact of the epibionts on the Kappaphycus
seedlings could be competition for space, nutrients,
dissolved gasses, and sunlight that might limit the growth
rate of the carrageenophyte (Hurtado et al. 2008).
However, epibionts on K. alvarezii seedlings did not
overgrow the thallus of the host, and most species were
not perennial so they did not stay long enough to deplete
nutrient absorption on light incidence. The impact of
filamentous algae on the seedlings might have been also
minimized by herbivory due to the presence of amphipods
(Brawley and Adey 1981).
In conclusion, we did not observe damage on Brazilian
seedlings of K. alvarezii by biofouling. However, the
management practices are more laborious when fouling
biomass, especially of calcareous organisms, is present. The
biofouling forming on the rafts may include the potential
source of epibionts and/or endobionts of K. alvarezii. Thus,
the cultivation systems must be maintained as clean as
possible to avoid future damage to the farming activities.
Acknowledgements The authors thank Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPQ) and Sete Ondas
Biomar Cultivo de Algas Ltda for financial support and to Henrique
Góes for field support and data from K. alvarezii daily growth rate and
carrageenan (yield and quality). We also thank the anonymous
reviewer for all the constructive advices.
J Appl Phycol
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