Estuarine, Coastal and Shelf Science 150 (2014) 24e35

Contents lists available at ScienceDirect

Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier.com/locate/ecss

Surf zone diatoms: A review of the drivers, patterns and role in sandy
beaches food chains
Clarisse Odebrecht a, *, Derek R. Du Preez b, Paulo Cesar Abreu a, Eileen E. Campbell b
a
b

Institute of Oceanography, Federal University of Rio Grande, C.P. 474, 96200-970 Rio Grande, Brazil
Department of Botany, Coastal and Marine Research Unit, Nelson Mandela Metropolitan University, P O Box 77000, Port Elizabeth 6031, South Africa

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 2 February 2013
Accepted 16 July 2013
Available online 25 July 2013

The accumulation of high biomass of diatoms in the surf zone is a characteristic feature of some sandy
beaches where the wave energy is sufciently high. A few species of diatoms, called surf diatoms, thrive
in this harsh environment. The main processes driving the spatial and temporal distribution of surf
diatoms as well as their standing biomass and growth were described twenty to thirty years ago based
on studies conducted on the western coast of the United States of America and South African beaches.
Since then, over fty locations around the world have been reported to have surf diatom accumulations
with most (three-quarters) of these being in the southern hemisphere. Their occurrence is controlled by
physical and chemical factors, including wave energy, beach slope and length, water circulation patterns
in the surf zone and the availability of nutrients to sustain the high biomass. The main forces driving the
patterns of temporal variability of surf diatom accumulations are meteorological. In the short term
(hours), the action of wind stress and wave energy controls the diatom accumulation. In the intermediate
time scale (weeks to months), seasonal onshore winds of sufcient strength, as well as storm events are
important. Furthermore, anthropogenic disturbances that inuence the beach ecosystem as well as
large-scale events, such as the El Nio Southern Oscillation, may lead to signicant changes in surf
diatom populations in the long term (inter-annual). Surf diatoms form the base of a short and very
productive food chain in the inshore of the sandy beaches where they occur. However, the role of surf
diatoms in the microbial food web is not clear and deserves further studies.
2013 Elsevier Ltd. All rights reserved.

Keywords:
diatom accumulations
geographical distribution
abiotic factors
trophic relation

1. Introduction
The surf zones of several exposed sandy beaches present
obvious brownish to greenish water discoloration due to the high
abundance of diatoms. The cellular growth of agellates including
dinoagellates is hampered by the turbulence found in surf zones,
whereas diatoms are dependent on high turbulence to optimize
their nutrient uptake and light utilization. In addition, some diatoms depend on vertical transport to suspend cells or resting
spores from the sediment into the water column after sedimentation during calm periods (Reynolds, 2006).
Among diatoms, a few phylogenetically unrelated species,
called surf diatoms, are able to successfully exploit the high wave
energy conditions at some sandy beaches. A common feature of
surf diatoms is their ability to accumulate in the foam by adhering
to air bubbles and, by so doing, form brown patches in the surf
zone (Lewin and Schaefer, 1983; Talbot and Bate, 1988a). There are
* Corresponding author.
E-mail address: doclar@furg.br (C. Odebrecht).
0272-7714/$ e see front matter 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ecss.2013.07.011

seven conrmed surf diatom species: the centrics Anaulus australis

Drebes et Schulz (Anaulaceae), Attheya armata (West) Crawford
(Attheyaceae), Aulacodiscus kittonii Arnott ex Ralfs (Aulacodiscaceae), and the pennates (Fragilariaceae) Asterionellopsis glacialis
(Castracane) Round and Asterionellopsis socialis (Lewin and
Norris) Crawford and Gardner (Plate 1). Aulacodiscus africanus
Cottam, the rst described surf diatom, has not been studied since
that early record (Van Heurck, 1896). Two other species of Aulacodiscus, Aulacodiscus johnsonii Arnott in Pritchard and Aulacodiscus petersii Ehrenberg are regularly subdominants with other
surf diatoms in South Africa (Campbell, 1996) and New Zealand
(Campbell, pers. comm.). It appears that surf diatoms thrive
exclusively in surf zones, except for Asterionellopsis glacialis, which
is also a common component of coastal phytoplankton worldwide
(Campbell, 1996).
2. Early studies
Surf diatom accumulations are a natural phenomenon known
for a long time. During a botanic expedition near the Congo River

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35

25

Plate 1. Surf diatoms: a) Anaulus australis Drebes et Schulz; b) Attheya armata (West) Crawford; c) Asterionellopsis glacialis (Castracane) Round; d) Asterionellopsis socialis (Lewin et
Norris) Round; e) Aulacodiscus johnsonii Arnott; f) Aulacodiscus kittonii Arnott; g) Aulacodiscus petersii Ehrenberg. Bar indicates 10 mm. No photographs of Aulacodiscus africanus
Cottam were available.

mouth (West Africa), greenish waters were observed to be due to a

high abundance of Aulacodiscus africanus Cottam (Van Heurck,
1896). Surf diatom accumulations were rst recognized as an
important food source in the surf zone of sandy beaches along the
Washington coast, western USA (McMillin, 1924). McMillin (1924)
identied two species of diatom: a club-shaped small cell associated with wine-red water and another large, round species associated with greenish water. The diatoms were later identied as
Aulacodiscus kittonii, the species causing greenish waters, and the
club-shaped responsible for the red surf as Synedra nitzschioides
Grunow, later described as Asterionellopsis socialis (Lewin and
Norris) Crawford and Gardner (Lewin and Norris, 1970). At that
time, controversial ideas prevailed about the origin of oil and
Tolman (1927) postulated its biogenic origin, based on the accumulation of diatoms at Copalis Beach on the Washington coast. This
phenomenon at Copalis Beach, was studied in more detail by the
American Petroleum Institute, including a preliminary chemical
characterization of the oil secreted by diatoms (Becking et al.,
1927). These authors also came to a general understanding of the
diatom accumulations, referring to them as epidemics, and
describing the conditions favoring their occurrence as being towards the end of the rainy season; after a heavy rainstorm; when

rains are followed by gentle westerly winds; and when the rain is
followed by clear weather and bright sunshine. In the seventies and
eighties, studies led by Joyce Lewin revealed the main distribution
patterns, species composition, metabolic and ecological processes
of Copalis Beach, stressing the importance of surf diatoms as food
sources (see review Lewin et al., 1989).
The importance of surf diatoms as main food source of clams
was rst recognized in New Zealand at the North Island beaches
(Rapson, 1954). During the winter, diatom biomass reaching
1.5 kg dry mass m
3 was found to comprise mostly Chaetoceros
armatus Westendorp, now Attheya armata (West.) Crawford.
Asterionellospsis glacialis (Castracane) Round was also present in
large quantities at times. It was suggested that the plankton cycle
was mainly inuenced by the wind regime and in particular to the
onshore west winds that coincided with the characteristic phytoplankton ora, in which zooplankton generally did not thrive
(Rapson, 1954). When the winds switched to easterly, this cycle
changed and zooplankton dominated the inshore. The primary
production by surf diatoms at Waitarere Beach, New Zealand North
Island, reached a maximum of 400 mg C m3 h
1, but this was
probably underestimated by at least an order of magnitude, according to Cassie and Cassie (1960). This production was shown to

26

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35

be the main source of food for toheroa (Paphies ventricosa), the

dominant sand-dwelling bivalve mollusc.
In northeastern Argentina and southern Brazil brown surf zone
water at beaches was considered to be due to high iodine content in
the water (Khnemann, 1966; Buckup, 1967). Due to the benecial
health properties of iodine people used to bathe in the dark-brown
waters and even to rub the ooze on their bodies. Buckup (1967),
however, found the discoloration to be due to Asterionellopsis glacialis. After this report, high concentrations of A. glacialis were also
found in So Paulo, southeastern Brazil, where the diatoms were
supposed to be linked to sh mortalities (Zavala-Camin and
Yamanaka, 1980). Deposition of diatoms on the beach at Santos
Bay occurred in 1979 and 1980 (Tommasi and Navas-Pereira, 1983).
McLachlan (1980) reported surf diatom accumulations to be a
regular occurrence along the south coast of South Africa. He
attempted to relate the accumulations with the mechanisms for
their maintenance in the surf zone. The surf diatom Anaulus australis (originally thought to be A. birostratus Grunow) is the main
surf diatom species in South Africa; occasionally occurring together
with Aulacodiscus johnsonii (incorrectly identied as Aulacodiscus
kittonii by McLachlan and Lewin, 1981), or Asterionellopsis glacialis
(Du Preez et al., 1989). Milestone studies from the seventies to
nineties led by Guy C. Bate and colleagues provided a comprehensive understanding of physical, chemical and biological processes, drivers and patterns of the surf diatom A. australis in the surf
zone of Sundays River Beach, in the Eastern Cape (Campbell and
Bate, 1987; Campbell et al., 1988a; Du Preez et al., 1990; Talbot
et al., 1990; Du Preez and Campbell, 1996a). It was shown that
the ability of Anaulus australis to rise to the water surface by
attachment to wave-entrained bubbles, together with their epipsammic mode of life at night, were the most important biological
factors resulting in the diatom accumulations. These, in conjunction with morphodynamics of the beach and the meteorological
regime were the key factors for accumulations at the Sundays River
Beach (see review Talbot et al., 1990).
3. The challenge of sampling in surf zones
The highly variable environment of surf zones both in space and
time, together with its turbulent nature renders the design of a
reliable sampling strategy an immense challenge. Several studies
have made use of sampling simply by wading into the surf zone
with a bucket, bottle, plankton net or a pipe to collect water or
foam, depending on the aim of the study. In order to understand the
spatial and temporal variability of surf diatoms, more comprehensive studies are less common. The only beach surveyed in detail
using diverse sampling strategies was the Sundays River Beach,
South Africa, where aerial surveys were used to quantify rip currents and spatial dynamics of surf diatom accumulations (Talbot
and Bate, 1987). These direct sampling methods were used in
conjunction with satellite images to quantify accumulations in
relation to longshore currents and lateral cell losses (Campbell and
Bate, 1988a). Aerial surveys were used to map the beaches associated with surf diatom accumulations along the entire South African
and Namibian coastline (Campbell and Bate, 1997).
The great challenge of studying the full extent of the surf-zone in
situ was met by synoptic water sampling achieved by a team of researchers wading into the surf zone, sampling from a helicopter in
the deeper portions of the breaker zone, coupled by using a boat
behind the breakers and offshore (Talbot and Bate, 1988b). The
breaker zone may also be reached successfully with a jetski as it was
shown for sh larvae (Strydom, 2007). The release of a dye (rhodamine) in conjunction with photogrammetric aerial photography was
found to be helpful to develop an understanding of the role of surf
water circulation in cell transport (Talbot and Bate, 1987). The

shortest time-scale related with surf diatom accumulations is that of

the tumbling of cells and resultant rhythmic uctuation in exposure
irradiance with the passing of successive wave bores. These shortterm dynamics require sampling at a time scale of seconds to minutes, another challenge that was successfully tackled at the Sundays River Beach (Campbell et al.,1988b). The sampling of cells while
in the sand at night proved to be the greatest challenge, and high
variability results in the requirement of exorbitantly large numbers
of samples to obtain statistically defensible conclusions (Talbot and
Bate, 1986). Estimation of the primary production of such a complex
system is therefore obtained by modeling approach (Campbell and
Bate, 1988c), estimation after diatom cultures (Campbell and Bate,
1987) or, when weather conditions permit, in situ measurements
(Schaefer and Lewin, 1984; Kahn and Cahoon, 2012).
Thus, the sampling technique and design must be chosen according to the aim of the study. Physiological in vitro experiments
require only simple sampling in the surf zone and/or sediments, but
in situ quantitative studies require different strategies and replication in order to faithfully capture the spatial and/or temporal
variability at a beach. Physical features like the wave height and
frequency, surf zone width, the presence of rip and longshore
currents, sediments characteristics and information on meteorological regime previously and during the sampling are important
factors which should be always estimated concomitantly with
sampling surf diatoms in any beach.
4. Geographical distribution of surf diatoms
Surf diatom accumulations have been reported in fteen countries at ca. ninety sandy beaches located at latitudes between
47 510 N and 42100 S (Table 1; Fig. 1), extending the geographic
distribution previously reported (Lewin and Schaefer, 1983; Talbot
et al., 1990; Campbell, 1996). At most beaches where they occur,
only one or two species are found together, but Campbell (1996)
reported ve surf diatom species at Karioitahe Beach, New Zealand and more recently recorded seven surf diatom species at the
same beach, albeit some in low abundance (Anaulus australis;
Asterionellopsis glacialis; Attheya armata; Aulacodiscus johnsonii;
Aulacodiscus kittonii; Aulacodiscus petersii; and Thalassiosira sp.).
Most beaches are located in the southern hemisphere (Africa,
Australasia and South America), while in the northern hemisphere
the most important area still comprises the west coast of USA
(Washington and Oregon coasts). In Europe, accumulations are
common in France (Le Gal et al., 1995) and recently were reported
from Spain (http://topasion.blogspot.com.br/2011/10/attheya-elalga-que-toma-el-sol-en-la.html) and from the oceanic Canary
Islands (Ojeda and OShanahan, 2005). In Asia, the only country
where surf diatom accumulations have been reported is India
where Asterionellopsis glacialis sometimes accumulates in the surf
zone (Mishra et al., 2006). However, this species also blooms
frequently offshore in Bengal Bay (Subba Rao, 1969; Choudhury and
Panigrahy, 1989).
Asterionellopsis glacialis is the only surf diatom that is a truly
cosmopolitan neritic marine species recorded from deeper coastal
waters as well as inshore. The other surf diatom species occur in
various parts of the world, but appear to be conned, for the most
part, to surf zones. Attheya armata has been recorded from
temperate areas in the northern (USA, France, Scotland, England,
Spain) and southern (Argentina) hemispheres (see Table 1). It has
been also reported from subtropical oceanic islands (Gran Canaria,
Santa Cruz de Tenerife; Ojeda and Shanahan, 2005) and we have
recently found a few cells in samples collected from the shores of
Algoa Bay, South Africa. By contrast, Asterionellopsis socialis was
considered to be endemic to the temperate northern hemisphere,
in the western USA (Lewin et al., 1989), however, recent reports

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35

27

Table 1
Geographical location of beaches with reports of surf diatom accumulations, respective species and references. The length of the beach was obtained in the reference or
estimated with the aid of the ruler of the Google Earth (GE) if sufcient information was available. Otherwise no information is given (NI).
Beach

Species

Reference

Beach
length (km)

Southern Hemisphere
Zaire
5 590 S
Banana, Congo River

Aulacodiscus africanus

Van Heurck, 1896

South Africa
33 430 S
33 430 S
34 S
34 070 S
34 060 S
34 470 S
34 310 S
34 050 S
34 030 S
34 S
34 020 S
34 050 S
33 580 S
32 500 S

Sundays River
Sundays River
Maitland River
Muizenberg
Macassar
Struisbaai
De Hoop
Vleesbaai
Glentana
Wilderness
Sedgeeld
Buffalo Bay
Van Stadens
Cintsa

Anaulus australis
Asterionellopsis glacialis
Anaulus australis
Anaulus australis
Anaulus australis
Anaulus australis
Anaulus australis
Anaulus australis
Anaulus australis
Anaulus australis
Anaulus australis
Anaulus australis
Anaulus australis
Anaulus australis

McLachlan and Lewin, 1981

Du Preez et al., 1989
McLachlan and Lewin, 1981
McLachlan and Lewin, 1981
Campbell and Bate, 1997
Campbell and Bate, 1997
Campbell and Bate, 1997
Campbell and Bate, 1997
Campbell and Bate, 1997
Campbell and Bate, 1997
Campbell and Bate, 1997
Campbell and Bate, 1997
Campbell and Bate, 1997
Campbell and Bate, 1997

50
50
30
8
6
22
12
12
11
4
15
6
31
10

Australia
34 370 S
35 350 S
38 300 S

Warren
Goolwa, Coorong
Venus Bay

Anaulus australis
Anaulus australis, Asterionellopsis glacialis
Unknown

90
180
50

38 540 S
30 060 S
27 550 S
27 360 S
26 270 S
42 S
42 100 S

Waratah Bay
Woolgoolga
Main Beach: Surfers Paradise
North Stradbroke Island
Noosa
Tasmania, west coast
Tasmania, Strahan Beach

Anaulus australis
Unknown
Anaulus australis
Anaulus australis
Anaulus australis
Anaulus australis, Attheya armata
Asterionellopsis glacialis

McLachlan and Hesp, 1984

McLachlan and Hesp, 1984
McLachlan and Hesp, 1984;
www.vboping.blogspot.com
Campbell, 1996
www.ickr.com/photos/47464237@NO7
Hewson et al., 2001
D.S. Schoeman, pers. comm.
T.A. Schlacher, pers. comm.
Lewin and Schaefer, 1983
McLachlan and Hesp, 1984

25
4
100
33
15
30
30

Asterionellopsis glacialis, Attheya armata

Rapson, 1954

90

Asterionellopsis glacialis, Attheya armata

Rapson, 1954

45

Asterionellopsis glacialis, Attheya armata

Rapson, 1954

40

Asterionellopsis glacialis, Attheya armata

Rapson, 1954; Cassie, 1955;

Cassie and Cassie, 1960
Sarma, 1975

100
12

Unknown
37 150 S

North Island west coast: Ninety

Mile Beach (Scotts Point, Hukatere,
Waipapakauri)
North Kaipara (Baileys, Glinks,
Round Hill)
Muriwai Beach (South Kaipara
Head, Wineh, Rocks)
Wellington beaches (Manawatu,
Waitarere, Hokio)
North Island west coast: Waipoua
Kauri to Maunganui
North Island east coast
Karioitahe Beach, Waiuku District

Kindley, 1983
Campbell, 1996

NI
35

37 15S

Karioitahe Beach, Waiuku District

Attheya armata, Aulacodiscus kittonii

Anaulus australis, Asterionellopsis glacialis,
Attheya armata, Aulacodiscus kittonii
Anaulus australis, Asterionellopsis glacialis,
Asterionellopsis socialis (a single colony),
Attheya armata, Aulacodiscus johnsonii,
Aulacodiscus kittonii, Aulacodiscus petersii,
Thalassiosira sp.

Campbell, pers. comm.

35

Marquesas archipelago, Bay of

TaiOhae: Nuku-Hiva Island

Aulacodiscus africanus

Sournia and Plessis, 1974

0.8

Venezuela
46 150 N

Boca de Aroa

Unknown

Gianuca, pers. comm. in Campbell (1996)

33

Brazil
3 440 S

Cear, Praia do Futuro

Anaulus sp., Asterionellopsis glacialis,

Aulacodiscus kittonii

32

Cear, Praia do Futuro

Sergipe beaches: barras de Propri,
Vaza-Barris and Piau-Fundo-Real
Bahia, Ilhus: Cururupe Beach
So Paulo: Itanham
So Paulo: Pernambuco1, Bertioga2,
Indai3, S. Loureno4, Boracia5

Anaulus australis
Asterionellopsis glacialis, Aulacodiscus,
Odontella spp.
Anaulus australis, Asterionellopsis glacialis
Asterionellopsis glacialis
Asterionellopsis glacialis

Verde et al., 1990;

Pereira da Costa et al., 1997;
Pereira da Costa et al., 1998
M. Garcia, pers. comm.
Franco, 1998

New Zealand
35 450 e36 150 S

40 250 e40 350 S



35 40 e35 45 S

Pacic Ocean
8 550 S

3 440 S
10 300 Se11 280 S
14 300 Se15 050 S
24 110 S
23 550 Se23 450 S

Attheya armata, Aulacodiscus kittonii

32
130

Tedesco, 2006
Zavala-Camin and Yamanaka, 1980
Tommasi and Navas-Pereira, 1983

67
20
1.51
102&3
44
75
(Villac, pers.
comm.)

(continued on next page)

28

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35

Table 1 (continued )
Beach

Species

Reference

Beach
length (km)

23 200 Se23 250 S

So Paulo: Ocian1, Parque Balnerio2,

Guara3, Juria4, Pontal5

Anaulus australis, Asterionellopsis

glacialis

Villac and Noronha, 2008

26 540 S

Santa Catarina: Navegantes Beach

Rrig et al., 1997

29 e34 S

Rio Grande do Sul: Atlntida,

Rainha do Mar, Mostardas,
Cassino, Tramanda

Anaulus australis, Asterionellopsis

glacialis
Asterionellopsis glacialis

451&2
23
194
575
10

Buckup, 1967; Aguiar and

Corte-Real, 1973; Gianuca,
1983; Rrig and Garcia, 2003;
Odebrecht et al., 2010

610

Uruguay
33 500 S

Chuy Beach

Asterionellopsis glacialis

Baysse et al., 1989

23

Argentina
37 170 S
37 050 S
39 S

Villa Gesell Beach

Pinamar Beach
Peuhen-C Beach

Asterionellopsis glacialis
Asterionellopsis glacialis
Asterionellopsis glacialis, Attheya
armata

Khnemann, 1966
Khnemann, 1966
Gayoso and Muglia, 1991

30
30
10

Asterionellopsis socialis,
kittonii
Asterionellopsis socialis,
kittonii,
Thalassiosira sp.
Asterionellopsis socialis,
Asterionellopsis socialis,

Aulacodiscus

Becking et al., 1927

30

Aulacodiscus

Campbell, pers. comm.

30

Attheya armata
Attheya armata

Lewin and Norris, 1970

Garver and Lewin, 1981

120
500

Asterionellopsis socialis

CDPH Monthly Marine

Biotoxin Technical Report
Nr. 11-09

60

Unknown

Aulacodiscus africanus

Lewin and Schaefer, 1983

NI

Unknown

Aulacodiscus africanus

Lewin and Schaefer, 1983

NI

Unknown

Unknown

Thayer, 1935

NI

Baie Audierne, Tronon Beach

Attheya armata

Le Gal et al., 1995

30

Playa America, Arenal Panxn

(Nigrn, Pontevedra)

Attheya armata

http://topasion.blogspot.com.br/
2011/10/attheya-el-alga-quetoma-el-sol-en-la.html

Gran Canaria: Las Burras

Gran Canaria: San Augustin
Gran Canaria: Taurito
Gran Canaria: Meloneras
Santa Cruz de Tenerife: Las
Gaviotas Beach

Attheya
Attheya
Attheya
Attheya
Attheya

Ojeda
Ojeda
Ojeda
Ojeda
Ojeda

2
2
1
2
1.2

Gopalpur Beach

Asterionellopsis glacialis

Northern Hemisphere
USA
Copalis Beach, Washington
46 550 Ne47 120 N


46 55 Ne47 12 N

Copalis Beach, Washington

46 150 Ne47 200 N

43 100 Ne47 200 N

Washington coast
Washington and Oregon coast:
Copalis, Fort Stevens, SeaSide,
Cannon, Oceanside, Gleneden,
Beachside, Hecata, Umpqua
Lighthous, Horsfall, Bullards beaches
California: Clam Beach

41 N

Central America
Costa Rica
8 N
Panama
8 N
Nicaragua
Unknown
Europe
France
47 550 N
Spain
42 070 N

Canary Islands
27 460 N
27 460 N
27 480 N
27 440 N
28 300 N
Asia
India
19  160 N

armata
armata
armata
armata
armata

extend the distribution to the subtropical Caribbean Island of

Belize (http://www.serc.si.edu/labs/phytoplankton/guide/belize.
aspx) and we found a few colonies of this species in samples
taken from Karioitahe Beach, New Zealand in 2011. The
geographical distribution of surf diatoms is much wider than the
distribution of surf diatom accumulations and most surf diatom
species that form accumulations are present in a wide latitudinal
range (see Fig. 1). Thus, it can be concluded that temperature is not
an important factor controlling their occurrence and accumulation, but may be a limiting factor for the geographical distribution
of some species.

and
and
and
and
and

Shanahan,
Shanahan,
Shanahan,
Shanahan,
Shanahan,

2012
2012
2012
2012
2012

Mishra et al., 2006

35

5. Drivers leading to surf diatom accumulations

The main factors leading to the accumulation of surf diatoms are
physical (beach morphodynamics), chemical (nutrient availability)
and biological (species adaptation) factors. It has been shown that
surf diatoms only accumulate in the surf zones of sandy beaches
where intermediate to dissipative wave energy conditions prevail
(according to the classication of Short and Wright, 1983). Along
such beaches, water circulation sets up entrained bodies of water
that are related to rip currents within the surf zone and these lead
to the retention and concentration of the diatom cells (McLachlan,

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35

29

Fig. 1. Geographical distribution of surf diatom accumulations reports and respective species.

1980; Talbot and Bate, 1987, 1988b; Lewin et al., 1989; Talbot et al.,
1990). The length of the beach is considered an important feature as
longshore currents remove cells at the ends of the beach. The
minimum length for retention of surf diatoms in the surf zones of
South African beaches was considered to be 4 km long (Campbell
and Bate, 1997). Two smaller beaches (Bay of Tai O Hae, Marquesas Islands; Playa de las Americas, Canary Islands) have a shore
conguration (substantial rocky headlands) that enables the
retention of surf diatoms (see Table 1).
The surf zone was rst proposed by McLachlan (1980) to be a
self-sustained ecosystem and this idea was largely conrmed for
the Sundays River Beach, where the effects of water circulation on
the spatial and temporal distribution of accumulations, cell abundance and losses from the surf zone, vertical migration, primary
production and the photosynthetic physiology of Anaulus australis
were elucidated (Campbell and Bate, 1988a,b,c; 1991; Talbot et al.,
1990; Du Preez et al., 1990; Du Preez and Campbell, 1996a). It
became clear that the water circulation in the surf zone is the main
factor leading to cell accumulation at the Sundays River Beach. The
surf zone water circulation pattern is closely related with the prevailing meteorological regime. Cells that are washed out of the surf
zone to areas behind the breaker line during calm conditions settle
on the bottom (in the absence of wave-entrained bubbles to take
them to the surface), where they may survive for up to 75 days in
the dark and may be returned to the surf zone by increased turbulence during windy conditions (Du Preez and Bate, 1992). In all
surf zones studied to date, the morphodynamics and meteorological regime are overriding factors in controlling the formation and
maintenance of the accumulations.
The availability of nutrients is obviously a major requirement to
sustain such high cell concentrations in the surf diatom accumulations (103 to 106 cells ml
1) but also outside (102 to 104 cells ml
1).
Nitrogen, rather than phosphorus or silicon was shown to be the
limiting nutrient in the eastern North Pacic (Lewin, 1978), southern Brazil (Niencheski et al., 2007; Odebrecht et al., 2010; Piedras
and Odebrecht, 2012) and South Africa (Campbell and Bate, 1997,
1998). The main nitrogen sources were suggested to be the

rainfall related drainage of nutrient-rich interstitial water

(McLachlan and Lewin, 1981; Lewin and Schaefer, 1983) and coastal
upwelling (Lewin, 1978). The annual rainfall is high (1000 to
2500 mm y
1) in some areas such as the USA northwest coast
(Lewin and Schaefer, 1983) and southern Brazil (Klein, 1997), but
low in South Africa (400e600 mm y
1, Campbell and Bate, 1991),
indicating that other factors must be important.
The discharge of subterranean groundwater was the primary
nutrient source for the maintenance of high biomass of surf diatoms at the Sundays River Beach, South Africa (Campbell and
Bate, 1991, 1998) and this was found to also be the case in
southern Brazil (Niencheski et al., 2007). At the Sundays River
Beach, the groundwater discharge from the unconned aquifer
beneath the back-of-beach dune eld contributes sufcient nitrogen to balance the loss of biomass from the surf zone due to
longshore currents (Campbell and Bate, 1991, 1998). In southern
Brazil, Niencheski et al. (2007) found that the nitrogen ux via
groundwater fuels primary production in the surf zone near Patos
Lagoon. A comparison between the groundwater and, in particular nitrogen discharges, from terrestrial sources at the Sundays
River Beach and in southern Brazil (Table 2), indicates that the
source of nitrogen may differ. The nitrate concentration in the
water sampled from wells at Sundays River Beach was two orders
of magnitude higher than in the wells of southern Brazil; while
the ammonium concentration was an order of magnitude higher
in southern Brazil and phosphorus was ve times higher. The
volume of subterranean groundwater discharge was much greater
in southern Brazil (129 m3 running m
1 d
1) than in South Africa
(1.5 m3 m
1 d
1) and may be explained by the advection of
freshwater from the Patos Lagoon through permeable sands of a
barrier spit in response to the hydrological head created by the
lagoon. Furthermore, the annual rainfall is twice to threefold
higher in southern Brazil than at the Sundays River Beach. In both
ecosystems, important nitrogen losses occur (ca. 60e70% of N
groundwater inux), however the main loss from the surf zone at
the Sundays River Beach occurs alongshore while in southern
Brazil losses occur across-shore to the inner shelf. The difference

30

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35

Table 2
Comparison of beach characteristics and nutrients average concentrations in wells,
submarine groundwater discharge (SGD) and Nitrogen uxes in the surf zone of
Sundays River, South Africa, and the beach northwards of Patos Lagoon mouth,
Brazil.
South Africa,
Sundays river*

Southern Brazil,
northward of
Patos lagoon
mouth#

Length (km)
Width (m)
Ammonium (uM)
Nitrate
Phosphorus
Average SGD
N Groundwater ux

50 km
250 m
2.9e3.6
200e280
1.2e1.5
1.5 m3 m
1 d
1
1.5 kg m
1 y
1

N loss

1.1 kg m
1 y
1

(w73% of N)

240 km
100 m
19.6e36.8
2.8e7.8
6.0e8.0
129 m3 m
1 d
1
55.2 kg m
1 y
1
(2.42  106 mol d
1
32 kg m
1 y
1
1.39 106 mol d
1
(w57% of N)
To the inner shelf

Main loss

Along the shore

Data from:
* Campbell and Bate (1998).
#
Niencheski et al. (2007).

could be because the Sundays River Beach (ca. 50 km in length) is

located in an embayment (Algoa Bay) where longshore currents
transport diatom cells outside the beach limits (Campbell and
Bate, 1988a). In southern Brazil, the study area (240 km in
length) forms a third of a very long, straight beach where surf
diatoms occur (ca. 600 km). Here, alongshore losses are less
important compared to the transport to the inner shelf.
6. Temporal patterns and drivers of surf diatom
accumulations
6.1. Diel cycle
Cell metabolism of diatoms and other microalgae present a diel
periodicity in cell division and size (Talbot and Bate, 1986; Du Preez
and Campbell, 1996a). It was rst recognized that Attheya armata
rises to the surface each morning before sunrise and disappears in
the late afternoon before sunset (Lewin and Hruby, 1973). A similar
cycle was observed for Anaulus australis (Sloff et al., 1984; Talbot
and Bate, 1986). Both species present a mucilaginous cell coating,
which was suggested to control the diel cycle for Anaulus australis
in the water column: the thicker coating in the afternoon favors
adherence of particles to the mucilage sheath and the cells would
switch from adhering to air bubbles at the water surface to deposition in the sediment (Talbot and Bate, 1988a). However, based on
histochemical analysis, Du Preez and Campbell (1996b) concluded
that the mucilage was probably not the feature that controls the
diel cycle. This is corroborated by A. armata that presents consistently lower numbers at or near the water surface at night but
exhibit no diel cycle of the mucilage coating (Lewin et al., 1989;
Gayoso and Muglia, 1991). In contrast, Asterionellopsis socialis is
found oating at the water surface during both the day and night
(Lewin and Hruby, 1973).
6.2. Mesoscale
The most important factor driving the mesoscale variability of
surf diatom accumulations in exposed sandy beach surf zones is the
strength of onshore winds that result in increased wave height and
turbulence. The action of onshore wind was recognized in the
earliest studies (see above) and later it was shown that its effect is
direct and indirect (Talbot and Bate, 1988c). The primary factor

leading to cell accumulation is the remote effect of wind due to its

inuence on wave height (Talbot et al., 1990). When waves
approaching the shore reach shallow water, the water motion
suspends cells deposited on the sediment. Once in the water column, wave-entrained bubbles concentrate the cells in the surface
foam. The sudden increase in cell concentrations of surf diatoms in
the surf zone after storms cannot be explained by growth (Rrig
and Garcia, 2003), but their rapid appearance must be caused by
wave-generated resuspension of cells deposited on the sediment of
the nearshore (Lewin, 1978; Talbot and Bate, 1989). Onshore winds
also favor the maintenance and concentration of these surf diatom
colonies in the neuston through their advection towards the beach
(Odebrecht et al., 1995).
6.3. Seasonal variation
Seasonal variations in surf diatom accumulations are unrelated
to latitude and species, but rather depend on seasonal changes in
wave height and turbulence, as indicated by a comparison of
Attheya armata at the beaches Copalis in western USA, Tronon in
France and Peuhen-C in Argentina (Fig. 2a). In Argentina, relatively
high concentrations were observed throughout the year
(104 cells ml
1; Gayoso and Muglia, 1991), while in the USA high
concentrations of cells (104 to 106 cells ml
1) were recorded over a
12-year period as a semipermanent feature, with the exception of
lower values (102 to 104 cells ml
1) recorded in summer (Lewin
et al., 1989). By contrast, Attheya armata presents a clear seasonal
cycle in France where accumulations (max. 104 cells ml
1) only
occurred from the end of autumn through winter until the beginning of spring (Le Gal et al., 1995). At the Canary Islands, accumulations of Attheya armata occurred only in summer and winter
(Ojeda and Shanahan, 2005). The beaches in USA, France and
Argentina are all located in temperate regions, but are subject to
different climatic and oceanographic driving forces. In Argentina,
strong winds blow throughout the year, explaining the persistent
cell accumulations (Gayoso and Muglia, 1991). In the USA and
France the seasonal cycle of wind direction and strength is welldened. At the former, strong southwesterly winds occurring
from autumn to spring, produce a net shoreward transport of surface water, while in summer, weaker northerly and northwesterly
winds prevail and drive surface water seaward, presumably
removing part of the surf diatom (A. armata and Asterionellopsis
socialis) population (Fig. 2b) (Lewin et al., 1989). Also in France, the
wind strength is much greater in autumn and winter, >30 km h
1
for a third of the time, compared to summer (11%) and spring (15%)
(website: http://ru.surf-forecast.com/breaks/Audierne/reliability_
by_season), explaining the observed seasonal cycle of surf diatom
accumulations. In South Africa, the surf diatoms show no seasonal
response to temperature (Campbell and Bate, 1988b), but increased
biomass occurs in the windy spring and autumn seasons (Fig. 2c).
The apparent absence of a seasonal cycle in Attheya armata accumulations at the subtropical beaches of the Canary Islands (Ojeda
and Shanahan, 2005) should be studied in more detail but is
probably related to the trade wind regime.
For Asterionellopsis glacialis, the accumulations in southern
Brazil seemed more conspicuous in autumn and winter (Gianuca,
1983), but during weekly sampling, Rrig and Garcia (2003)
observed surf diatom accumulations all year round, with only a
slight increase in frequency during the winter months, when
onshore winds were more frequent. Further north, Rezende and
Brandini (1997) also related an autumn increase in cell concentrations (up to 102 cells ml
1) to the higher frequency of southerly
fronts. However, a rather irregular pattern of Asterionellopsis glacialis accumulations through the year emerged at Cassino Beach,
when comparing twenty years (1992e2012) of monthly records.

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35

31

Fig. 2. Seasonal variation of abundance or biomass of (a) Attheya armata at the beaches of Copalis (USA), Pehuen-C (Argentina) and Tronon (France) based on data presented by
Lewin et al. (1989), Gayoso and Muglia (1991) and Le Gal et al. (1995); (b) Asterionellopsis socialis at Copalis Beach based on data presented by Lewin et al. (1989); (c) Asterionellopsis
glacialis at Cassino Beach, Brazil (original data) and (d) Anaulus australis at Sundays River, South Africa (original data).

Both the lowest (August) and highest (July, September) mean

concentrations were observed in the austral winter to early spring
(Fig. 2d). At the rst glance the August minimum seems an odd
outlier, however consistently low concentrations in August were
observed together with the absence of cell accumulations as well as
the minimum chlorophyll a average over the twenty-year period.
The absence of a consistent seasonal cycle for A. glacialis at Cassino
Beach resembles the result for Attheya armata in Argentina.
The tropical Brazilian Cururupe Beach, Bahia, is an interesting
example, because both Anaulus australis and Asterionellopsis glacialis presented a seasonal cycle with higher cell concentrations in
autumn and winter, when the passage of cold fronts and onshore
winds are more frequent (Tedesco, 2006).
6.4. Changes in species composition
Global impacts like seawater temperature changes, sea-level
rise, ocean acidication, accelerated eutrophication leading to

dead zones and overshing have major effects on the marine

environment (Defeo et al., 2009; Doney et al., 2012) and they may
inuence the health of sandy beaches, their surf zones and the surf
diatoms in them. Signicant changes in the long-term species
composition and abundance of surf diatoms have been recorded at
three sandy beaches. At Copalis Beach, Lewin et al. (1989) reported
the replacement of the main species, Aulacodiscus kittonii, dominant in the early 1920s, with Attheya armata in the 1950s and the
complete disappearance of the former after the 1940s. Based on a
12- year study (1971e1982) and in comparison with earlier studies,
Attheya armata was rst observed in about 1950, when it was
considered to be an introduced species. The dramatic changes
leading to the disappearance of A. kittonii were suggested to be
possibly related with the construction of the rst major dam on the
Columbia River, which inuenced the river discharge along the
southern Washington coast and modied the water volume, timing
of river discharge, as well as nutrient and sediment loads reaching
the beach (Lewin et al., 1989).

Fig. 3. Interannual variability (1992e2012) of Asterionellopsis glacialis cell concentrations at Cassino Beach related to mud deposition events. Circles indicate periods of lower cell
concentration, the arrows and their width indicate mud deposition events and the magnitude of this impact.

32

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35

At the Sundays River Beach, Du Preez et al. (1989) reported a

nearly complete switch from Anaulus australis to Asterionellopsis
glacialis for a month. However this has never been observed to
occur again. Long-term monthly sampling (1992e2012) at a single station at Cassino Beach provided an opportunity to examine
the effect of climatic oscillations. These, in conjunction with
environmental impacts due to human activities, signicantly
altered the abundance and composition of the phytoplankton
(Fig. 3). A reduction in the frequency of surf diatom accumulations followed extreme mud deposition events in 1998 and 2002
(Odebrecht et al., 2003; 2010). Mud deposits are a recurrent
phenomenon at Cassino Beach because the beach is just south of
the mouth of the Patos Lagoon containing high sediment loads
(Calliari et al., 2009). Regular harbor dredging suspends sediments in the lagoons main channel, which are transported to the
nearshore, especially during high rainfall periods. The impact of
mud deposits on the beach is strongest during extreme El Nio
periods during which southern Brazil experiences high rainfall.
The effects of the mud deposition include the attenuation of wave
action through altered water viscosity, the burial of large
numbers of cells, and alteration of the nutrient concentrations in
the water (Odebrecht et al., 2010).
6.5. The role of surf diatoms in food webs
High abundance of surf diatoms results in high levels of primary
production in sandy beach surf zones (Campbell and Bate, 1988c),
normally considered as oligotrophic ecosystems (Pearse et al.,
1942). According to McLachlan and Brown (2006), accumulations
may generate exceptionally high primary production rates (500e
2000 g C m
3 y
1) and a signicant part (more than 50%) may be
produced as dissolved organic carbon (Campbell et al., 1985;
McLachlan and Bate, 1985; Du Preez and Campbell, 1996b).
Despite the high cell concentrations and production rates of surf
diatoms, Talbot and Bate (1988d) draw attention to the fact that
most particulate organic carbon present in the surf zone of Sundays
River Beach is in the form of detritus and not live material. Even
during surf diatom accumulations, detritus may compose ca. 50% of
the total particulate organic carbon in the water column.
Surf diatoms, organic matter and detritus in the surf zone of
beaches where accumulations occur sustain a short and highly
productive food web. In these beaches, macrobenthic lter feeders
are the main consumers and form a link between diatoms and the
higher trophic levels (Garcia and Gianuca, 1997). According to these
authors, 95% of the secondary production in the surf zone of
Cassino Beach comprises lter feeders: mostly the molluscs Mesodesma mactroides, Donax hanleyanus and the decapod crustacean
Emerita brasiliensis. These feed heavily on the surf diatom Asterionellopsis glacialis. However, mysids and copepods present in the
surf zone can also be important consumers of surf diatoms, transferring substantial portions of the organic matter to secondary and
tertiary consumers such as sh, birds and even marine mammals
(Garcia and Gianuca, 1997; McLachlan and Brown, 2006). Particulate organic matter produced by surf diatoms is not restricted to the
surf zone, but spreads to the supralittoral. At Cassino Beach, lter
feeders such as polychaetes, molluscs (Amiantis purpuratus, Tivela
ventricosa and Mactra isabellana) and detritivores ingest diatoms
that are deposited on the sediments. Similarly, large amounts of
Asterionellopsis glacialis deposited in the supratidal after storm
events feed insects such as the beetles, Bledius bonariensis,
B. microcephalus and B. fernandezi as well as ghost crabs, Ocypode
quadrata (Garcia and Gianuca, 1997).
Interstitial food chains in surf zones also benet from the
abundant primary production in the water column, although
pelagic organisms rarely consume meiofauna. Thus, the interstitial

environment functions as a mineralization site, providing dissolved

inorganic nutrients to sustain the primary production in the water
column (McLachlan and Brown, 2006). On the other hand, the large
amount of dissolved organic carbon produced by surf diatoms is
considered to be available to be taken up by bacteria and should
fuel the surf zone microbial loop (McLachlan and Bate, 1985;
McLachlan and Brown, 2006). McGwynne (1991) found that
almost half of the carbon required that sustain the growth of heterotrophic bacteria was provided by Anaulus australis at the Sundays River Beach. Conversely, in accumulations of the surf diatoms,
between 3 and 46% of the exuded carbon is consumed by bacteria
indicating ample provision of substrate for bacteria when the surf
diatom biomass is sufciently high for accumulations to form.
McGwynne (1991) found that 41% of the total annual primary
production (120 kg C m
1 y
1), enters the microbial loop. This was
considered a valid estimate because bacteria are extremely active in
most aquatic ecosystems absorbing and mineralizing large
amounts (>90%) of dissolved organic carbon (McLachlan and Bate,
1985). However, according to McLachlan and Brown (2006) the
microbial loop would be inefcient in transferring matter and
energy to larger consumers in the surf zone, since a minimum of at
least four food-web levels are necessary to incrementally alter
particle size and, in this case, very little energy would reach the
higher trophic levels. Thus, the surf zone microbial loop would
mainly play a role in the nutrient cycling of this environment, but
not represent a source of matter and energy for macroorganisms.
At Cassino Beach, however, a decoupling between the surf zone
diatom Asterionellopsis glacialis and bacteria was found (Abreu et al.,
2003). At this beach bacterial abundance remained exceptionally
low in the presence of A. glacialis accumulations. This was an unexpected observation as A. glacialis produces large amount of
mucus. Bacteria cultivated in water where A. glacialis was present in
high cell concentrations showed a long lag phase in the bacterial
growth response, probably as a result of the presence of bacteriostatic antibiotics produced by the diatoms (Abreu et al., 2003). The
results indicate that, at least for the surf zone at Cassino Beach, the
microbial loop does not form the major channel for dissolved
carbon produced by the surf diatom Asterionellopsis glacialis and it is
neither recycling nutrients, nor serving as food source for other
organisms in the food web. According to Abreu et al. (2003) the
surplus dissolved organic carbon in the water at Cassino Beach is
most likely transformed into amorphous mucilaginous aggregates
due to the turbulence, in similar fashion to the production of marine snow in the ocean (Larson and Shanks, 1996; Passow et al.,
2001). Thus diatoms and amorphous mucilaginous aggregates
could be consumed by benthic and pelagic lter feeders enhancing
the surf zone macro-food web. However, as observed by many authors (Abreu et al., 2003; McLachlan and Brown, 2006; Bergamino
et al., 2011), information about the microbial ecology in sandy
beach surf zones is still scarce and deserves further research in order to better understand the role played by bacteria and protozoans
in the ecology of high energy surf zones of sandy beaches.
7. Conclusion and perspectives
At present, the number of beaches where surf diatom accumulations have been reported is approximately double (90 beaches) the number compared to assessments of some twenty years
ago (Talbot et al., 1990; Campbell, 1996). The latitudinal range has
not changed (ca. 42 100 S to 42 N), although tropical and European examples are included now in the list of active areas,
which were not known previously. Despite the relatively large
number of beaches worldwide, there are still only a few places
where surf diatoms have been studied in detail; this applies in
stark contrast with their importance as primary producers. The

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35

challenge of sampling the surf zone comprehensively may

contribute to this disparate. However, rather simple sampling
procedures may be used if consistently replicated in space and/or
time, and laboratory studies may be conducted to test various
research questions.
Despite the increase in number of beaches where surf diatoms
have been recorded, the southern hemisphere still has a greater
number of beaches with accumulations. Coastal conguration and
morphodynamics may partially explain this, but the lack of information for the Asian beaches leaves this part of the northern
hemisphere an open question. Recently, three additional species,
were found to accumulate in the surf zone. A species of Thalassiosira, which appears to be a new species and remains to be
described, was recorded from accumulations in New Zealand and
the Washington coast of the USA (Campbell, pers. comm.), and
Amphitetras antediluviana and Biddulphia biddulphiana were reported in high abundance in brown water at Camboriu Beach, Brazil
(Rrig, pers. comm). These are interesting species for future studies.
The apparent geographical barriers in eastern South America,
where the distribution of the different species are conned to regions remains to be addressed: Attheya armata thrives in the south
only (39 S, Argentina) and Anaulus australis north of 28 S, while
Asterionellopsis glacialis is found from the tropical to temperate
areas. Physiological studies should be conducted in order to test
whether factors such as temperature, light, salinity or sediment
characteristics may explain this geographical distribution of surf
diatoms.
The general processes leading to surf diatom accumulations in
high-energy beaches with sufcient nutrient supply, are well understood, as is the inuence of the meteorological regime, beach
length and morphodynamics. However several questions remain
to be answered. For example, the cell diel cycle and mucus production, considered very important to maintain the diatoms in the
surf zone, is only known in detail for Anaulus australis. It is clear
that not all species are dependent on this cycle of mucilage production and removal, as evidenced for Asterionellopsis socialis.
Even for Attheya armata, which also accumulates in the surf zone
during the day as is found for A. australis, the mechanism appears
to be different. Investigations of the diel cycle of other surf diatom
species is required in order to extrapolate the model proposed for
Anaulus australis to other beaches. For this, the cell division cycle,
chemical composition of the mucus and the benthic pelagic
coupling should be tested for the other species in the eld and
laboratory.
Acknowledgments
C. Odebrecht and P. Abreu are fellows of the Brazilian National
Research Council-CNPQ and the research was funded through the
Long Term Ecological Research Program (BR-LTER). Research by E.
Campbell and D. du Preez was funded by the South African National
Research Foundation and the Nelson Mandela Metropolitan
University.
References
Abreu, P.C., Rrig, L.R., Garcia, V.M., Odebrecht, C., Biddanda, B.B., 2003. Decoupling
between bacteria and surf-zone diatom Asterionellopsis glacialis (Castracane) in
Cassino Beach, Brazil. Aquatic Microbial Ecology 32, 219e228.
Aguiar, L.W., Corte-Real, M., 1973. Sobre uma orao de Asterionella japonica Cleve
(1978) na costa do Rio Grande do Sul. Iheringia, Srie Botnica 17, 18e27.
Baysse, C., Elgue, J.C., Burone, F., 1989. Variaciones en la distribucin y relaciones
interespecicas del toplancton en una playa arenosa de la costa Atlantica
Uruguaya. Frente Maritimo 5 (A), 95e114.
Becking, L.B., Tolman, C.F., McMillin, H.C., Field, F., Hashimoto, T., 1927. Preliminary
statement regarding the diatom epidemics at Coaplis Beach, Washington, and
an analysis of diatom oil. Economic Geology 22, 356e368.

33

Bergamino, L., Lercari, D., Defeo, O., 2011. Food web structure of sandy beaches:
temporal and spatial variation using stable isotope analysis. Estuarine, Coastal
and Shelf Science 91, 536e543.
Buckup, L., 1967. Quando o mar se torna pardacento: iodo ou plancton marinho?
Correio do Povo, Suplemento Rural, 8e11.
Calliari, L.J., Winterwerp, J.C., Fernandes, E., Cuchiara, D., Vinzon, S.B., Sperle, M.,
Holland, K.T., 2009. Fine grain sediment transport and deposition in the Patos
Lagoon Cassino beach sedimentary system. Continental Shelf Research 29,
515e529.
Campbell, E.E., 1996. The global distribution of surf diatom accumulations. Revista
Chilena de Historia Natural 69, 495e501.
Campbell, E.E., Bate, G.C., 1987. Factors inuencing the magnitude of phytoplankton
primary production in a high-energy surf zone. Estuarine, Coastal and Shelf
Science 24, 741e750.
Campbell, E.E., Bate, G.C., 1988a. The inuence of current direction on longshore
distribution of surf phytoplankton. Botanica Marina 31, 257e262.
Campbell, E.E., Bate, G.C., 1988b. The photosynthetic response of surf phytoplankton
to temperature. Botanica Marina 31, 251e255.
Campbell, E.E., Bate, G.C., 1988c. The estimation of annual primary production in a
high energy surf-zone. Botanica Marina 31, 337e343.
Campbell, E.E., Bate, G.C., 1991. Ground water in the Alexandria dune eld and its
potential inuence on the adjacent surf-zone. Water SA 17, 155e160.
Campbell, E.E., Bate, G.C., 1997. Coastal features associated with diatom discoloration of surf-zones. Botanica Marina 40, 179e185.
Campbell, E.E., Bate, G.C., 1998. Tide-induced pulsing of nutrient discharge from an
unconned aquifer into an Anaulus australis e dominated surf-zone. Water SA
24, 365e370.
Campbell, E.E., Fock, H.P., Bate, G.C., 1985. Exudation of recently xed photosynthetic products from surf zone phytoplankton of the Sundays River Beach.
Botanica Marina 28, 399e405.
Campbell, E.E., Du Preez, D.R., Bate, G.C., 1988a. The light environment in a high
energy surf-zone with high phytoplankton biomass. Botanica Marina 31,
329e335.
Campbell, E.E., Du Preez, D.R., Bate, G.C., 1988b. Photosynthetic rates and
photoinhibition of surf diatoms in uctuating light. Botanica Marina 31, 411e
416.
Cassie, R.M., 1955. Population studies on the toheroa, Amphidesma ventricosum
Gray (Eulamellibranchiata). Australian Journal of Marine and Freshwater
Research 6, 348e391.
Cassie, R.M., Cassie, V., 1960. Primary production in a New Zealand west coast
phytoplankton bloom. New Zealand Journal of Science 3, 173e199.
CDPH, January 2011. California Department of Public Health, Environmental
Management Branch. In: Monthly Marine Biotoxin, p. 6. Technical Report
Nr. 11-09.
Choudhury, S.B., Panigrahy, R.C., 1989. Occurrence of bloom of diatom Asterionella
glacialis in nearshore waters of Gopalpur, Bay of Bengal. Indian Journal of Marine Science 18, 204e206.
Defeo, O., McLachlan, A., Schoeman, D.S., Schlacher, T.A., Dugane, J., Jones, A.,
Lastra, M., Scapini, F., 2009. Threats to sandy beach ecosystems: a review.
Estuarine, Coastal and Shelf Science 81, 1e12.
Doney, S.C., Ruckelshaus, M., Duffy, J.E., Barry, J.P., Chan, F., English, C.A.,
Galindo, H.M., Grebmeier, J.M., Hollowed, A.B., Knowlton, N., Polovina, J.,
Rabalais, N.N., Sydeman, W.J., Talley, L.D., 2012. Climate change impacts on
marine ecosystems. Annual Review of Marine Science 4, 11e37.
Du Preez, D.R., Bate, G.C., 1992. Dark survival of the surf diatom Anaulus australis
Drebes et Schulz. Botanica Marina 35, 315e319.
Du Preez, D.R., Campbell, E.E., 1996a. The photophysiology of surf diatoms e a review. Revista Chilena de Historia Natural 69, 545e551.
Du Preez, D.R., Campbell, E.E., 1996b. Cell coatings of surf diatoms. Revista Chilena
de Historia Natural 69, 539e544.
Du Preez, D.R., Campbell, E.E., Bate, G.C., 1989. First recorded bloom of the diatom
Asterionella glacialis Castracane in the surf-zone of the Sundays River Beach.
Botanica Marina 32, 503e504.
Du Preez, D.R., Campbell, E.E., Bate, G.C., 1990. Photoinhibition of photosynthesis
in the surf diatom, Anaulus australis Drebes et Schulz. Botanica Marina 33,
539e543.
Franco, C.R.P., 1998. Notas sobre orescimentos de diatomceas na costa de Sergipe,
Brasil: ocorrncias de Asterionellopsis glacialis (Castracane) Round, Aulacodiscus
crux Ehrenberg e Odontella spp, vol. 2. Publicaes Avulsas do Centro Acadiemcio Livre de Biologia, Universidade de Sergipe, pp. 43e47.
Garcia, V.M.T., Gianuca, N.M., 1997. The beach and surf-zone. In: Seeliger, U.,
Odebrecht, C., Castello, J.P. (Eds.), Subtropical Convergence Environments:
the Coast and Sea in the Southwestern Atlantic. Springer Verlag, Berlin,
pp. 166e170.
Garver, J.L., Lewin, J., 1981. Persistent blooms of surf diatoms along the Pacic
Coast. USA.I. Physical characteristics of the coastal region in relation to the
distribution and abundance of the species, Estuarine. Coastal and Shelf Science
12, 217e229.
Gayoso, A.M., Muglia, V.H., 1991. Blooms of the surf-zone diatom Gonioceros
armatus (Bacillariophyceae) on the South Atlantic coast (Argentina). Diatom
Research 6, 247e253.
Gianuca, N.M., 1983. A preliminary account of the ecology of sandy beaches in
southern Brazil. In: McLachlan, A., Erasmus, T. (Eds.), Sandy Beaches as Ecosystems. Dr. W. Junk, The Hague, pp. 413e419.

34

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35

Hewson, I., ONeil, J.M., Abal, E., 2001. A low-latitude bloom of the surf-zone diatom,
Anaulus australis (Centrales, Bacillariophyta) on the coast of Southern
Queensland (Australia). Journal of Plankton Research 23, 1233e1236.
Kahn, A.E., Cahoon, L., 2012. Phytoplankton productivity and physiology in the surf
zone of sandy beaches in North Caroline, USA. Estuaries and Coasts 35, 1393e
1400.
Kindley, M.M., 1983. Physiological Ecology of Surf Zone Diatoms. University of
Auckland, New Zealand, p. 122 (MSc dissertation).
Klein, A.H.F., 1997. Regional climate. In: Seeliger, U., Odebrecht, C., Castello, J.P.
(Eds.), Subtropical Convergence Environments: the Coast and Sea in the
Southwestern Atlantic. Springer Verlag, Berlin, pp. 5e7.
Khnemann, O., 1966. Floraciones acuticas y nivales ocasionadas por algas. Anales
de la Sociedade Cientca Argentina Ser. 2, Ciencia Aplicada 180, 3e47.
Larson, E.T., Shanks, L., 1996. Consumption of marine snow by two species of juvenile mullet and its contribution to their growth. Marine Ecology and Progress
Series 130, 19e28.
Le Gal, D., Raguenes, P., Nezan, E., Piclet, G., 1995. Chaetoceros armatum. Diatommee
de la zone de ressac vecteur deforescences colorees hivernales. In: Cas de la
Baie dAudierne, Plage de Tronoen. FREMER del Concarneau, p. 16.
Lewin, J., 1978. Blooms of surf-zone diatoms along the coast of the Olympic
Peninsula, Washington. IX: factors controlling the seasonal cycle of nitrate in
the surf at Copalis Beach (1971 through 1975). Estuarine and Coastal Marine
Science 7, 173e183.
Lewin, J., Hruby, T., 1973. Blooms of the surf-zone diatoms along the coast of the
Olympic Peninsula, Washington. II. A diel periodicity in buoyancy shown by the
surf-zone diatom species, Chaetoceros armatum T. West. Estuarine and Coastal
Marine Science 1, 101e105.
Lewin, J., Norris, R.E., 1970. Surf-zone diatoms of the coasts of Washington and
New Zealand (Chaetoceros armatum T. West and Asterionella spp.). Phycologia
9, 143e149.
Lewin, J., Schaefer, C.T., 1983. The role of phytoplankton in surf ecosystems. In:
McLachlan, A., Erasmus, T. (Eds.), Sandy Beaches as Ecosystems. Dr. W. Junk, The
Hague, pp. 413e419.
Lewin, J., Schaefer, C.T., Winter, D.F., 1989. Surf-zone ecology and dynamics. In:
Landry, M.R., Hickey, B.M. (Eds.), Coastal Oceanography of Washington and
Oregon, Elsevier Oceanography Series, vol. 47. Elsevier, Amsterdam,
pp. 567e594.
McGwynne, L.E., 1991. The Microbial Loop: its Role in a Diatom-enriched Surf Zone.
University of Port Elizabeth, p. 191 (PhD thesis).
McLachlan, A., 1980. Exposed sandy beaches as semi-closed ecosystems. Marine
Environmental Research 4, 59e63.
McLachlan, A., Bate, G.C., 1985. Carbon budget for a high energy surf zone. Vie
Milieu 34, 67e77.
McLachlan, A., Brown, A.C., 2006. The Ecology of Sandy Shores, second ed. Elsevier,
Amsterdam, p. 373.
McLachlan, A., Hesp, P., 1984. Surf zone diatom accumulations on the Australian
coast. Search 15, 230e231.
McLachlan, A., Lewin, J., 1981. Observations on surf phytoplankton blooms along the
coasts of South Africa. Botanica Marina 24, 553e557.
McMillin, H.C., 1924. The Life-history and Growth of the Razor Clam, 34th Annual
Report. Washington Department of Fisheries, Olympia, p. 52.
Mishra, G.S., Mohant, A.K., Singh, S.K., Panigrahy, R.C., 2006. Asterionella glacialis
Castracane bloom on the water quality and phytoplankton community structure in coastal waters of Gopalpur Sea, Bay of Bengal. Asian Journal of Water,
Environment and Pollution 3, 71e77.
Niencheski, L.F.H., Windom, H.L., Moore, W.S., Jahnke, R.A., 2007. Submarine
groundwater discharge of nutrients to the ocean along a coastal lagoon barrier,
Southern Brazil. Marine Chemistry 106, 546e561.
Odebrecht, C., Segatto, A.Z., Freitas, C.A., 1995. Surf-zone chlorophyll a variability
at Cassino Beach, Southern Brazil. Estuarine Coastal and Shelf Science 41,
81e90.
Odebrecht, C., Abreu, P.C., Fujita, C., Bergesch, M., 2003. The impact of mud deposition on the long term variability of the surf-zone diatom Asterionellopsis
glacialis (Castacane) Round at Cassino Beach, Brazil. Journal of Coastal Research,
SI 35, 486e491.
Odebrecht, C., Bergesch, M., Rrig, L.R., Abreu, P.C., 2010. Phytoplankton interannual variability at Cassino Beach, Southern Brazil (1992e2007), with
emphasis on the surf zone diatom Asterionellopsis glacialis. Estuaries and
Coasts 33, 570e583.
Ojeda, A., Shanahan, L., September 2012. Discolorations of the Surf Zone Diatom
Attheya Armatus (Centrales, Bacillariophyta) on Sandy Beaches in Gran Canaria
(Canary Islands, Spain). Gobierno de Canarias, Agencia Canaria de Investigacion,
Innovacin y Sociedad de la Informacin, p. 15.
Ojeda, A., OShanahan, L., 2005. Discoloraciones por acumulaciones de la diatomea
bentnica epipsmica Attheya armatus (Centrales, Bacillariophyta) en playas de
arena del S y SW de Gran Canaria (Canarias, Espaa). Vieraea 33, 51e58.
Passow, U., Shipe, R.F., Murray, A., Pak, D.K., Brzezinski, M.A., Alldredge, A.L.,
2001. The origin of transparent exopolymer particles (TEP) and their role
in the sedimentation of particulate matter. Continental Shelf Research 21,
327e346.
Pearse, A.S., Humm, H.J., Wharton, G.W., 1942. Ecology of sand beaches at Beaufort,
N. C. Ecological Monographs 12, 135e190.
Pereira da Costa, F.A., Moreira, M.O.P., Sales, M.F., 1997. Monitoramento dos orescimentos de toplncton na Praia do Futuro, Fortaleza, CE: primeiro registro
do gnero Anaulus Ehrenberg como responsvel pelo fenmeno na costa

Nordeste. In: 480 Congresso Nacional de Botnica, Sociedade Botnica do Brasil,

Crato, Brazil, p. 22.
Pereira da Costa, F.A., Moreira, M.O.P., Sales, M.F., 1998. Florescimentos de diatomceas no litoral leste de Fortaleza, Cear (Praia do Futuro). In: 50 Encontro
Brasileiro de Ecotoxicologia, 10 Colquio Brasileiro de Algas Nocivas, Universidade do Vale do Itaja-UNIVALI, Itaja, Brazil, p. 67.
Piedras, F.R., Odebrecht, C., 2012. The response of surf-zone phytoplankton to
nutrient enrichment (Cassino Beach, Brazil). Journal of Experimental Marine
Biology and Ecology 432e433, 156e161.
Rapson, A.M., 1954. Feeding and control of toheroa (Amphidesma ventricosum Gray)
(Eulamellibranchiata) populations in New Zealand. Australian Journal of Marine
and Freshwater Research 5, 486e512.
Reynolds, C., 2006. Ecology of Phytoplankton. Cambridge University Press, Cambridge, p. 535.
Rezende, K.R.V., Brandini, F.P., 1997. Variao sazonal do toplncton na zona de
arrebentao da Praia do Pontal do Sul (Paranagu, Paran), vol. 11. Nertica,
Curitiba, pp. 49e62.
Rrig, L.R., Garcia, V.M.T., 2003. Accumulations of the surf-zone diatom Asterionellopsis glacialis (Castracane) Round in Cassino Beach, Southern Brazil, and
its relationship with environmental factors. Journal of Coastal Research 19,
167e177.
Rrig, L.R., Resgalla Jr., C., Pezzuto, P.R., Alves, E., dos, S., Morellli, F., 1997. Anlise
ecolgica de um processo de acumulao da diatomcea Anaulus sp.na zona de
arrebentao da Praia de Navegantes (Santa Catarina, Brasil). In: Absalo, R.,
Esteves, A.M. (Eds.), Ecologia de Praias Arenosas do litoral brasileiro, Oecologia
Brasiliensis, vol. 3. Federal University of Rio de Janeiro, pp. 9e43.
Sarma, P., 1975. A note on the algal bloom at Kawerua coast, North Island, New
Zealand. Tane 21, 55e58.
Schaefer, C.T., Lewin, J., 1984. Persistent blooms of surf diatom along the Pacic
coast, USA. IV Diatom productivity and its relation to standing stock. Marine
Biology 83, 205e217.
Short, A.D., Wright, L.D., 1983. Physical variability of sandy beaches. In:
McLachlan, A., Erasmus, T. (Eds.), Sandy Beaches as Ecosystems. Dr. W. Junk, The
Hague, pp. 133e144.
Sloff, D.S., McLachlan, A., Bate, G.C., 1984. Spatial distribution and diel periodicity of
Anaulus birostratus Grunow in the surf zone of a sandy beach in Algoa Bay,
South Africa. Botanica Marina 27, 461e465.
Sournia, A., Plessis, Y.B., 1974. A red-water diatom, Aulacodiscus kittonii var. africanus, in Marquesas Islands, Pacic Ocean. Botanica Marina 17, 124.
Strydom, N.A., 2007. Jetsky-based plankton towing as a new method of sampling
larval shes in shallow marine habitats. Environmental Biology of Fishes 78,
299e306.
Subba Rao, D.V., 1969. Asterionella japonica bloom and discoloration off Waltair, Bay
of Bengal. Limnology and Oceanography 14, 632e634.
Talbot, M.M.B., Bate, G.C., 1986. Diel periodicities in cell characteristics of the
surfzone diatom Anaulus birostratus: their role in the dynamics of cell patches.
Marine Ecology and Progress Series 32, 81e89.
Talbot, M.M.B., Bate, G.C., 1987. Rip current characteristics and their role in the
exchange of water and surf diatoms between the surf-zone and nearshore.
Estuarine Coastal and Shelf Science 25, 707e720.
Talbot, M.M.B., Bate, G.C., 1988a. The use of false buoyancies by the surf diatom
Anaulus birostratus in the formation and decay of cell patches. Estuarine, Coastal
and Shelf Science 26, 155e167.
Talbot, M.M.B., Bate, G.C., 1988b. Distribution patterns of the surf diatom Anaulus birostratus in an exposed surfzone. Estuarine, Coastal and Shelf Science 26, 137e153.
Talbot, M.M.B., Bate, G.C., 1988c. The response of diatom populations to environmental conditions, changes in the extent of the planktonic fraction and surface
patch activity. Botanica Marina 31, 109e118.
Talbot, M.M.B., Bate, G.C., 1988d. The relative quantities of live and detrital organic
matter in a beach-surf ecosystem. Journal of Experimental Marine Biology and
Ecology 121, 255e264.
Talbot, M.M.B., Bate, G.C., 1989. Beach morphodynamics and surf-zone diatom
populations. Journal of Experimental Marine Biology and Ecology 129,
231e241.
Talbot, M.M.B., Bate, G.C., Campbell, E.E., 1990. A review of the ecology of surf-zone
diatoms, with special reference to Anaulus australis. Oceanography and Marine
Biology, an Annual Review 28, 155e175.
Tedesco, E.C., 2006. Estudo das diatomceas da zona de arrebentao da Praia do
Cururupe, Ilhus, Ba. Santa Cruz State University, Ilhus, Brazil (MSc thesis).
Thayer, L.A., 1935. Diatom water blooms on the coast of Washington. Proceedings of
the Lousiana Academy of Science 2, 67e71.
Tolman, C.F., 1927. Biogenesis of hydrocarbons by diatoms. Economic Geology 22,
454e474.
Tommasi, L.R., Navas-Pereira, D., 1983. Nota sobre a ocorrncia de orescimentos
dediatomceas, na Baa de Santos (SP) e adjacncias (Estado de So Paulo,
Btasil). Cincia e Cultura 35, 507e512.
Van Heurck, H.F., 1896. A Treatise on the Diatomaceae. Translated by W.E. Baxter.
William Wesley & Son, London.
Verde, N.G.L., Tahim, E.F., Lea, E.E., 1990. Florescimentos de algas planctnicas na
Praia do Futuro (Fortaleza, CE). In: IV Encontro Brasileiro de Plncton. Editora
Universitria da UFPE, Recife, Brazil, p. 45.
Villac, M.C., Noronha, V.A.P., 2008. The surf-zone phytoplankton of the state of So
Paulo, Brazil. I. Trends in space-time distribution with emphasis on Asterionellopsis glacialis and Anaulus australis (Bacillariophyceae). Nova Hedwigia,
Beiheft 133, 115e129.

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24e35
Zavala-Camin, L.A., Yamanaka, N., 1980. Notas sobre um caso de mortalidade de
peixes, ocorrida em Itanham, So Paulo, Brasil. Boletim do Instituto Oceanogrco, S. Paulo 29, 377.

Internet references
Phytoplankton Guide to the Chesapeake Bay & other regions. Belize, Carrie Bow Cay.
Smithonian Environmental Research Center. Asterionella socialis in the Caribe,
Belize. http://www.serc.si.edu/labs/phytoplankton/guide/belize.aspx (accessed
11.01.12.).
Venus Bay Observation Project. Bad weather for sailors, but good for diatoms
(Posted April 8, 2012); Surf diatom blooms (Posted May 14, 2011); Surf Diatoms

35

on Beach Four (Posted January 3, 2011); Plenty of diatoms blooms (Posted

September 2, 2010); Small blooms in the surf (Posted July 7, 2010); Those
brown sludges (Posted July 3, 2010). www.vboping.blogspot.com (accessed
07.01.12.)
Wind regime at Tronoen Beach, Audierne Bay, France http://ru.surf-forecast.com/
breaks/Audierne/reliability_by_season) (accessed 11.01.12.).
Rodriguez, F., Attheya, El alga que toma el sol en la arena. Beaches Playa America
and Arenal de Panxn, Pontevedra, Spain. http://topasion.blogspot.com.br/
2011/10/attheya-el-alga-que-toma-el-sol-en-la.html (accessed 11.01.12.).
Australia, New South Wales: Woolgolga DGreenhalgh, D., DECCW, Naturally occurring phenomena known as surf diatoms at Woolgoolga, 11th February 2010.
http://www.ickr.com/photos/47464237@N07/4350225800/in/photostream/
(accessed 11.01.12.).