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http://dx.doi.org/10.4490/algae.2016.31.3.5
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Note
Copyright © 2016 The Korean Society of Phycology 1http://e-algae.kr pISSN: 1226-2617 eISSN: 2093-0860
First record of red macroalgae bloom in Southern Atlantic Brazil
Mateus S. Martins, Thaís F. Massocato, Paulo A. Horta and José Bonomi Barufi*
Botany Department, Federal University of Santa Catarina, Campus Universitário de Trindade, Florianópolis, SC 88040-900,
Brazil
Blooms of macroalgae have grown over the planet in recent decades as a possible result of eutrophication of coastal
waters. Visually, a bloom forming can be identified by dominant presence of an organism at the expense of others. In
mid-January 2014, a forming bloom of red algae was detected on the beach of Garopaba, Santa Catarina State, Brazil.
This aroused the interest of tourists and locals as well as the scientific community. Thus, the objective of this study was
to characterize and quantify the photosynthetic floating organisms contributing to this phenomenon. In addition, we
qualitatively compared algal composition of the bloom to those deposited in the post-beach area and the adjacent rocky
shore community. Five sampling points in random patches of floating material were defined. At each point, five replicates
were taken with a cube of 32,768 cm3, resulting in a total of 25 samples. Samples were collected in the inner area enclosed
by a PVC quadrate of about 900 cm² from the shore and the specimens found in post-beach zone (wrack). Twenty-four
taxa of macroalgae were found in the bloom, with Aglaothamnion uruguayense as the dominance one. Ten taxa were
found on shore. Only four taxa were found in the post-beach area. The biomass estimated for A. uruguayense in the floa-
ting material was 8.35 tons with an estimated area of 52,770 m2. It is possible that this huge biomass value of the bloom is
related to the local nutrient intake, and our results reinforce the necessity of coastal integrative management initiatives.
Key Words: abundance; Aglaothamnion uruguayense; bloom; Garopaba; red algae
INTRODUCTION
A bloom is a developing phenomenon due to the over-
growth of a species in the environment at the expense of
others (Cartensen et al. 2007). Such species can be either
macroalgae or microalgae. There are several studies re-
lated to algal blooms from an international perspective.
Algal diversity inside a bloom can be explained by prefe-
rences of herbivory activity (Lotze et al. 2000). They can
be assigned as red, green, or brown tides, according to the
color of the predominant organism, with “green tides” as
the most common one. They have been reported in the
coast of several European countries (Scanlan et al. 2007),
North America (Nelson et al. 2008), and Asia (Liu et al.
2010, Kang et al. 2015). In some places, macroalgae can
float freely on the beaches (Piriou et al. 1991, Merceron
and Morand 2004).
In Brazil, several blooms have been detected. They are
predominantly made up of microalgae with impacts on
coastal management, resulting in fish kills and changes to
food webs (Freitas et al. 1992). In addition, they can cause
human poisoning by direct or indirect ingestion of toxins.
Many of these phenomena have been linked to anthropic
activities such as discharges from industrial and domes-
tic sewages (Figueiredo et al. 2004).
Blooms of seaweeds are different from the microal-
Received February 17, 2016, Accepted March 5, 2016
*Corresponding Author
E-mail: jose.bonomi@gmail.com
Tel: +55-48-37214765, Fax: +55-48-37218545
This is an Open Access article distributed under the
terms of the Creative Commons Attribution Non-Com-
mercial License (http://creativecommons.org/licenses/by-nc/3.0/) which
permits unrestricted non-commercial use, distribution, and reproduction
in any medium, provided the original work is properly cited.
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MATERIALS AND METHODS
Bloom formation was initially detected in the city of
Garopaba (total population of 18,000 inhabitants) loca-
ted in the south of Santa Catarina State, Brazil (Fig. 1).
Samples were taken in three different environments in-
cluding Garopaba Center Beach and a nearby pocket be-
ach called Vigia Beach. First, samples were taken from the
floating bloom material (Fig. 2A). Then, algal materials
were sampled from the rocky shore near the bloom and
from post-beach zone organisms compounding wracks.
For the floati ng organisms, five points were selected ran-
domly, covering an area of 500 m in linear length.
Samplings of the Garopaba Center Beach were per-
formed on 29 January 2014. Floating materials were ob-
tained with a 32,768 cm³ cube built with PVC pipes and
surrounded by canvas of approximately 0.5 mm in poro-
sity (Fig. 2B). The cube was positioned into the water, at
various depth (0.5 m to 1.20 m). The open side was placed
toward the final last wave. It was remained in this position
for about 3 s. Then the cube was suspended, bringing the
floating organisms from the bloom. The materials were
inserted into plastic bags and frozen at -20°C. Algae were
collected at 5 points in the bloom. There were 5 replicates
at each point, resulting in a total of 25 samples.
Considering the difficulty in acessing the Garopaba
Center Beach rocky shores, we performed qualitative col-
lections on the neighbouring rocky shore of Vigia Beach
on January 28, 2014. For this purpose, six 900 cm2 qua-
drats were sampled in the wrack (Fig. 2C & D). Six qua-
drats were also sampled from the rocky shore. The ma-
gae blooms in at least three aspects. First, they have no
direct chemical toxicity. Second, they have a broader
range of ecological effects involved. Third, these forma-
tions extend for a longer period of time (Hay and Fenical
1988). They may remain in place for years to decades. For
example, in the Peel Harvey Estuary in Western Australia,
a Cladophora sp. bloom lasted for twelve years or more
(Gordon and McComb 1989). In Waquoit Bay, Massachu-
setts, Cladophora sp. and Gracilaria sp. bloom has been
present for over 20 years (Valiela et al. 1992). Kapraun
and Searles (1990) have also reported problems caused in
North Carolina (USA) due to overgrowth of filamentous
alga Polysiphonia sp. (Ceramiales) that had not been re-
cognized in that area. Lapointe and Bedford (2010) have
indicated that the proliferation of non-native macroalgae
in areas of coral reefs is threatening native species and the
local dynamic ecosystem.
In the summer of 2013-2014, there was a macroalgae
bloom forming in the city of Garopaba, Santa Catarina
State, Brazil. It aroused the interest of tourists and locals
as well as the scientific community. The aim of this study
was to characterize and quantify photosynthetic organis-
ms present in this bloom that appeared to be floating in
the water column. Moreover, the flora of a neihgbouring
rocky shore was evaluated to test the hypothesis that the
algae present in this bloom could be part of the local flo-
ra. In addition, as algal material was deposited on the
sand beach, sampling was also conducted in these are-
as to compare their compositions to those of the floating
species and local rocky shore flora.
Fig. 1. Study area indicating places of collection in Santa Catarina State, Brazil. Left and right images indicate location of Garopaba, SC, Brazil
and details of Garopaba Center Beach and Vigia Beach, respectively (source: GoogleEarth©).
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Martins et al. Red Algae Bloom in Brazil
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Software PRIMER 7 was utilized to analyze the diffe-
rences between the data of dry biomass of the collection
points associated with taxonomic composition. Permu-
tational multivariate analysis of variance (PERMANO-
VA) and similarity percentages analysis (SIMPER) were
applied to assess the main species contributing to the
phenomenon.
RESULTS
Tw en t y s e ve n t a xa w e r e i d e n t ifi e d i n th e b l o om , i n c lu -
ding three species of bryozoans (Bugula neritina, Mem-
braniporopsis tubigera, and Amathia sp.). Ten taxa were
recorded from the Vigia Beach rocky shore. Only four
species were represented in the wrack material (Ta b l e 1).
In addition to bryozoans, other non-algae such as crus-
taceans, hairs, and even plastic objects were also found
occasionally in the collected samples. However, they were
neglected, because represented only small and slight por-
tions that would not allow appropriate identification, wi-
thout significant influence to the total bloom biomass.
Filamentous red alga Aglaothamnion uruguayense
showed the highest relative abundance in the bloom. It
accounted for 87.1% of the biomass, followed by Hypnea
musciformis with 3.88%, and Pterocladiella capillacea
with 3.15% of the biomass. The remaining taxa presented
lower percentages in these samples (Fig. 3).
terials collected on the shore and wrack were also frozen
at -20°C.
Samples were thawed, sorted, and identified according
to Joly (1967), Cordeiro-Marino (1978), and Pedrini (2011,
2013). Algae were placed in a stove at 40°C until constant
weights were achieved. The weight was recorded as dry
biomass using an analytical balance (fa2104n model; Bio-
precisa, Curitiba, PR, Brazil). After this step, a portion of
the material representing of each taxon was deposited at
the Herbarium FLOR (Department of Botany herbarium,
Florianópolis) at the Federal University of Santa Catarina.
To estimate the algal biomass present in the bloom on
the beach of Garopaba center, we used the Eq. (1) where
was the individual density per point, m was the average
biomass of the collection points (g), and v was the cube
volume collection (m³). Average density of flowering (X)
were calculated from all Eq. (1) density values (), and to-
tal bloom dry biomass (TBDW) were calculated using Eq.
(2). For this parameter’s calculation, a conservative esti-
mation was taken into account, considering a bloom thi-
ckness of 0.1 m (average depth, h). The area detectable by
the naked-eye (A) was delimited using Google Earth Pro
software.
= m
(1)
TBDW = X · (A · h)(2)
Fig. 2. General aspect of red algal bloom and sampling procedures. (A) Floating algae at Garopaba Center Beach. (B) Cube used for sampling
floating material in bloom at Garopaba Center Beach. Note the cube corners made from PVC tubing and the sides were filled with canvas screen
with 0.5 mm porosity. (C) Appearance of algal material deposited on the sand of Vigia Beach. (D) PVC Square (30 × 30 cm) utilized to collect sam-
ples at the Vigia Beach (wrack and rocky shore zones).
A
CD
B
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Overall, the biomass found at each of collection points
were statistically different (PERMANOVA, Pseudo-F4,20 =
8.538, p = 0.001), indicating heterogeneity in the bloom.
Based on SIMPER analysis, the contribution of species
in the bloom at each point could be verified. The main
species that contributed to the bloom biomass at any of
the five points was A. uruguayense (Ta b l e 2). The biomass
estimated for this species in the floating material was 8.35
tons with an estimated area of 52,770 m2.
Ta bl e 1 . Organisms identified in three environments (bloom floating species at Garopaba Center Beach, wrack material at Vigia Beach, and
Vigia Beach rocky shore community of Garopaba, Santa Catarina)
Taxa Bloom Garopaba
Center Beach
Vigia Beach
wrack
Vigia Beach
rocky shore
Rhodophyta
Aglaothamnion uruguayense (W. R. Taylor) N. E. Aponte,
D. L. Ballantine & J. N. Norris ×- -
Hypnea musciformis (Wulfen) J. V. Lamouroux × × ×
Pterocladiella capillacea (S. G. Gmelin) Santelices & Hommersand × × ×
Pterosiphonia parasitica (Hudson) Falkenberg ×-×
Centroceros clavulatum (C. Agardh) Montagne ×-×
Plocamium brasiliense (Greville) M. A. Howe & W. R. Taylor ×- -
Gracilaria sp. Greville ×- -
Jania rubens (Linnaeus) J. V. Lamouroux ×-×
Jania cubensis Montagne ex Kützing ×-×
Bryothamnion sp. Kützing ×- -
Arthrocardia sp. Decaisne ×-×
Grateloupia sp. C. Agardh ×- -
Gelidium sp. J. V. Lamouroux ×- -
Cheilosporum sp. (Decaisne) Zanardini ×- -
Cryptopleura ramosa (Hudson) L. Newton ×- -
Chlorophyta - -
Ulva sp. Linnaeus × × ×
Codium sp. Stackhouse × × -
Chaetomorpha sp. Kützing ×- -
Ulva sp. Link 1820 - ×
Cladophora sp. Kützing ×- -
Phaeophyceae - -
Sargassum sp. C. Agardh ×-×
Dictyota sp. J. V. Lamouroux ×- -
Dictyopteris sp. J. V. Lamouroux ×- -
Padina sp. Adanson ×- -
Bryozoa - -
Amathia sp. Busk ×- -
Bugula neritina Linnaeus ×- -
Membraniporopsis tubigera Osburn ×- -
×, taxon occurrence; -, not observed.
Fig. 3. Percentage of total dry biomass found in the floating
material of Garopaba Center Beach bloom during summer 2014.
Dry biomass
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Martins et al. Red Algae Bloom in Brazil
5http://e-algae.kr
mentous species such as Cladophora sp. and Chaetomor-
pha sp. Other species containing different types of cellu-
lar organization have already been reported (Morand and
Briand 1996, Nelson et al. 2003, Lapointe et al. 2005, Tei-
chberg et al. 2010). In the case of Garopaba bloom, the
main species recorded, i.e., A. uruguayense, also shows a
simple morphology with branched uniseriate filaments.
Bloom formation of H. musciformis in Florida, USA
has been recorded in areas where there is enrichment in
organic matter (Lapointe and Bedford 2007). Dailer et al.
(2012) have shown that H. musciformis is an opportunis-
tic macroalga that can physiologically respond to excess
nutrients in a similar way as Ulva spp. in areas near the
coast of Maui affected by anthropogenic enrichment of
nutrients. These studies have demonstrated that many
taxa found in the samples of Garopaba are already re-
cognized as members of populations present in blooms
whose formation is due to the eutrophication of coastal
waters. This seems to be the case for A. uruguayense. Pe-
dersen and Borum (1996) have concluded that opportu-
nistic macroalgae have fast growth and high nutrient up-
take content (nitrogen and phosphorus), suggesting that
Garopaba Center Beach is an eutrophic environment.
This condition can be assigned following the historic data
of balneability conditions of the zone. Balneability data
for Garopaba Center Beach provided by the Santa Catari-
na State Environmental Foundation (FATMA) has shown
that this beach is qualified as improper for bathing or so-
cial utilization (CONAMA 274/2000).
Other alternatives to the elucidation of this problem
involving the bloom in the city of Garopaba may be rela-
ted to the operation of currents, local oceanographic con-
ditions, and / or decline in populations of predators. No
related studies regarding the first two parameters have
been found. In the case of predation, different studies
suggest that the productivity of the system and higher
trophic level consumers can jointly control the produc-
tion of algae, suggesting that the effect of nutrients on the
growth of algae blooms also depends on the top-down
force (Worm et al. 2002).
DISCUSSION
The macroalgal bloom of Garopaba, Santa Catarina,
occurred in the summer season in 2014. It was primarily
consisted of A. uruguayense. This study is the first report
of this species as a dominant species in an algae bloom
phenomenon in the marine environment. This species
has been proposed as one of the eight most common spe-
cies on Santa Catarina Island of Brazil by Batista (2012).
The occurrence of A. uruguayense has been repor-
ted in Cuba ( Taylor 1960), Brasil (Taylor 1960), Uruguay
(Taylor 1960), Florida, USA (Littler et al. 2008), and Ar-
gentina (Boraso de Zaixso 2013), all of them are limited
to the Atlantic Ocean. The predominant filamentous alga
A. uruguayense in the floating material was not found in
samples of wrack nor on the near rocky shore. Sampling
of the post-beach area and the Vigia Beach rocky shore
showed a reduced number of taxa, suggesting that this
deposition may have taken place only with significantly
robust sized algae. Another possible explanation for this
absence is that the sampling points might be too small.
The constant presence of bryozoans in these samples
suggests the importance of understanding other aspects
of a forming bloom. M. tubigera has been found and des-
cribed in plastic and drifting algae (Taylor and Monks
1997), providing evidence of rafting as a mechanism of
dispersal. Although it is currently unclear where M. tubi-
gera is originally native, it is already considered as inva-
sive in many places where it dwells today. According to
the variety of possible dispersion methods, it is expected
that M. tubigera can reach new locations in other parts of
the oceans in a short period of time (Vieira and Migotto
2014).
Most macroalgae blooms consists of one or two spe-
cies, suggesting that they are more sensitive to excess
nutrients than other macroalgae in the area (Dailer et
al. 2012). In temperate and tropical regions, increasing
eutrophication can lead to the accumulation of biomass
of opportunistic macroalgae of Chlorophyta with simple
morphologies, including Ulva sp., Codium sp., and fila-
Table 2. Contribution of different species present to floating algal biomass at Garopaba Center Beach
Taxa Contribution (%) / Collection point
12345
Aglaothamnion uruguayense 98.78 96.55 97.21 87.66 89.74
Hypnea musciformis 0.93 2.48 0.85 4.25 2.94
Pterocladiella capillacea 0.16 0.23 0.53 3.50 2.76
Others 0.12 0.74 1.40 4.60 4.56
Data were recorded from five collection points and calculated following similarity percentages analysis (SIMPER).
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460.
Batista, M. B. 2012. Macrófitas Marinhas da Ilha de Santa
Catarina, Brasil. M.S. thesis, Federal University of Santa
Catarina, Florianópolis, SC, Brazil, 104 pp.
Boraso de Zaixso, A. L. 2013. Elementos para el estudio de
las macroalgas de Argentina. Con colaboración de J. M.
Zaixso. Universitaria de la Patagonia, Comodoro Rivada-
via, 204 pp.
Carmichael, W. W., Drapeau, C. & Anderson, D. M. 2000. Har-
vesting of Aphanizomenon flos-aquae Ralfs ex Born. &
Flah. var. flos-aquae (Cyanobacteria) from Klamath Lake
for human dietary use. J. Appl. Phycol. 12:585-595.
Cartensen, J., Henriksen, P. & Heiskanen, A. -S. 2007. Sum-
mer algal blooms in shallow estuaries: definition, mech-
anisms, and link to eutrophication. Limnol. Oceanogr.
52:370-384.
Cordeiro-Marino, M. 1978. Rodofíceas bentônicas marinhas
do estado de Santa Catarina. Rickia 7:1-243.
Dailer, M. L., Smith, J. E. & Smith, C. M. 2012. Responses of
bloom forming and non-bloom forming macroalgae
to nutrient enrichment in Hawaii, USA. Harmful Algae
17:111-125.
Figueiredo, D. R., Azeiteiro, U. M., Esteves, S. M., Gonçalves,
F. J. M. & Pereira, M. J. 2004. Microcystin-producing
blooms: a serious global public health issue. Ecotoxicol.
Environ. Saf. 59:151-163.
Freitas, J. C., Ogata, M., Kodama, M., Martinez, S. C. G., Lima,
M. F. & Monteiro, C. K. 1992. Possible microbial source of
guanidine neurotoxins found in the mussel Perna perna
(Mollusca, Bivalvia, Mytilidae). In Gopalakrishnakone,
P. & Ta n , C . K . ( E d s . ) Recent Advances in Toxicology Re-
search, Vol. 2. National University of Singapore, Singa-
pore, pp. 589-596.
Glazer, A. N. 1994. Phycobiliproteins: a family of valuable,
widely used fluorophores. J. Appl. Phycol. 6:105-112.
Gordon, D. M. & McComb, A. J. 1989. Growth and produc-
tion of the green alga Cladophora montagneana in a eu-
trophic Australian estuary and its interpretation using a
computer program. Water Res. 23:633-645.
Gupta, S., Sharma, R., Soni, S. K. & Sharma, S. 2012. Biomass
utilization of waste algal consortium for extraction of al-
gal oil. J. Algal Biomass Util. 3:34-38.
Hay, M. E. & Fenical, W. 1988. Marine pl ant-herbivore in-
teractions: the ecology of chemical defense. Annu. Rev.
Ecol. Evol. Syst. 19:111-145.
Joly, A. B. 1967. Gêneros de algas marinhas da Costa Atlan-
tica Latino-Americana. Universidade de São Paulo, São
Paul o, 461 pp.
Kang, E. J., Kim, J. -H., Kim, K., Choi, H. -G. & Kim, K. Y. 2015.
Re-evaluation of green tide-forming species in the Yel-
The destination of algae biomass is a problem for
coastal communities. They are likely to thrown out fre-
quently. However, it can also have intrinsic economic
value (Carmichael et al. 2000, Gupta et al. 2012). In the
case of the Garopaba bloom, the dominant species A.
uruguayense may have a high concentration of acces-
sory photosynthetic pigments, phycocyanin, and phyco-
erythrin (Martins 2013). In addition, this species has high
protein content (Barbarino and Lourenço 2005). There-
fore, it is possible to use it as a food supplement (Martins
2013). Silva (2008) has suggested that the primary poten-
tial of these pigment molecules is that they can be used
as natural dyes. However, a growing number of investiga-
tions have found that they have health properties, includ-
ing pharmaceutical applications (Glazer 1994).
In summary, the marine macroalgal bloom on Garo-
paba Center Beach of Santa Catarina consisted of twenty-
four algal taxa. It also included three species of bryozoans.
This bloom was considered to be composed of heteroge-
neous biomass strains. This is the first time that A. uru-
guayense, a turf forming species, is found to be dominant
in this type of phenomenon. However, other minor ma-
croalgae have been described previously as participants
in bloom forming. Little is known about the food chain, or
the local ocean circulation that might have influenced the
sampling sites and the bloom formation on the Garopaba
Center Beach. However, the absence of appropriate sewa-
ge treatment, as observed in many other countries arou-
nd the world, is related to this phenomenon. In addition,
the described environmental transformation resulted in
loses of health quality of coastal areas. Our results rein-
force the urgence of coastal integrate management initia-
tives including continuous monitoring efforts, in order to
anticipate such phenomena and seek workable solutions
to use this biomass as a resource to benefit of the city.
ACKNOWLEDGEMENTS
The authors thank Antonio João, Erica H. Ricardo, Lu-
ana Silva, Manuela B. Batista, Pablo Riul, and Wellington
Gonçalves for their technical support, including sample
collection, identification, and statistic analysis.
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