Odebrechtetal2014 Surf Diatoms

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Surf zone diatoms: A review of the drivers, patterns and role in sandybeaches food chainsClarisse Odebrechta, * , Derek R. Du Preezb, Paulo Cesar Abreua, Eileen E. Campbellba Institute of Oceanography, Federal University of Rio Grande, C.P. 474, 96200-970 Rio Grande, Brazilb 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

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

Keywords:diatom accumulationsgeographical distributionabiotic factorstrophic relation

a b s t r a c t

The accumulation of high biomass of diatoms in the surf zone is a characteristic feature of some sandybeaches where the wave energy is suf ciently high. A few species of diatoms, called surf diatoms, thrivein 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 basedon 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 accumulationswith most (three-quarters) of these being in the southern hemisphere. Their occurrence is controlled byphysical and chemical factors, including wave energy, beach slope and length, water circulation patternsin the surf zone and the availability of nutrients to sustain the high biomass. The main forces driving thepatterns 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 intermediatetime scale (weeks to months), seasonal onshore winds of suf cient strength, as well as storm events areimportant. Furthermore, anthropogenic disturbances that inuence the beach ecosystem as well aslarge-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.

1. Introduction

The surf zones of several exposed sandy beaches presentobvious brownish to greenish water discoloration due to the highabundance of diatoms. The cellular growth of agellates includingdino agellates is hampered by the turbulence found in surf zones,whereas diatoms are dependent on high turbulence to optimizetheir nutrient uptake and light utilization. In addition, some di-

atoms depend on vertical transport to suspend cells or restingspores from the sediment into the water column after sedimenta-tion during calm periods (Reynolds, 2006).

Among diatoms, a few phylogenetically unrelated species,called surf diatoms, are able to successfully exploit the high waveenergy conditions at some sandy beaches. A common feature of surf diatoms is their ability to accumulate in the foam by adheringto air bubbles and, by so doing, form brown patches in the surf zone (Lewin and Schaefer, 1983; Talbot and Bate, 1988a). There are

seven con rmed surf diatom species: the centrics Anaulus australisDrebes et Schulz (Anaulaceae), Attheya armata (West) Crawford(Attheyaceae), Aulacodiscus kittonii Arnott ex Ralfs (Aulacodisca-ceae), and the pennates (Fragilariaceae) Asterionellopsis glacialis(Castracane) Round and Asterionellopsis socialis (Lewin andNorris) Crawford and Gardner (Plate 1). Aulacodiscus africanusCottam, the rst described surf diatom, has not been studied sincethat early record (Van Heurck, 1896). Two other species of Aula-codiscus , Aulacodiscus johnsonii Arnott in Pritchard and Aulaco-discus petersii Ehrenberg are regularly subdominants with othersurf diatoms in South Africa (Campbell, 1996) and New Zealand(Campbell, pers. comm.). It appears that surf diatoms thriveexclusively in surf zones, except for Asterionellopsis glacialis , whichis also a common component of coastal phytoplankton worldwide(Campbell, 1996).

2. Early studies

Surf diatom accumulations are a natural phenomenon knownfor a long time. During a botanic expedition near the Congo River

* Corresponding author.E-mail address: [email protected] (C. Odebrecht).

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http://dx.doi.org/10.1016/j.ecss.2013.07.011

Estuarine, Coastal and Shelf Science 150 (2014) 24 e 35
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mouth (West Africa), greenish waters were observed to be due to ahigh abundance of Aulacodiscus africanus Cottam (Van Heurck,1896). Surf diatom accumulations were rst recognized as animportant food source in the surf zone of sandy beaches along theWashington coast, western USA (McMillin, 1924). McMillin (1924)identi ed two species of diatom: a club-shaped small cell associ-ated with wine-red water and another large, round species asso-

ciated with greenish water. The diatoms were later identied as Aulacodiscus kittonii , the species causing greenish waters, and theclub-shaped responsible for the red surf as Synedra nitzschioidesGrunow, later described as Asterionellopsis socialis (Lewin andNorris) Crawford and Gardner (Lewin and Norris, 1970). At thattime, controversial ideas prevailed about the origin of oil andTolman (1927) postulated its biogenic origin, based on the accu-mulation of diatoms at Copalis Beach on theWashington coast. Thisphenomenon at Copalis Beach, was studied in more detail by theAmerican Petroleum Institute, including a preliminary chemicalcharacterization of the oil secreted by diatoms (Becking et al.,1927). These authors also came to a general understanding of thediatom accumulations, referring to them as epidemics , anddescribing the conditions favoring their occurrence as being to-

wards the end of the rainy season; after a heavy rainstorm; when

rains are followed by gentle westerly winds; and when the rain isfollowed byclear weather and bright sunshine. In theseventies andeighties, studies led by Joyce Lewin revealed the main distributionpatterns, species composition, metabolic and ecological processesof Copalis Beach, stressing the importance of surf diatoms as foodsources (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 reaching1.5 kg dry mass m3 was found to comprise mostly Chaetocerosarmatus Westendorp, now Attheya armata (West.) Crawford. Asterionellospsis glacialis (Castracane) Round was also present inlarge quantities at times. It was suggested that the plankton cyclewas mainly in uenced by the wind regime and in particular to theonshore west winds that coincided with the characteristic phyto-plankton ora, in which zooplankton generally did not thrive(Rapson, 1954). When the winds switched to easterly, this cyclechanged and zooplankton dominated the inshore. The primaryproduction by surf diatoms at Waitarere Beach, New Zealand NorthIsland, reached a maximum of 400 mg C m3 h 1, but this wasprobably underestimated by at least an order of magnitude, ac-

cording to Cassie and Cassie (1960). This production was shown to

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 africanusCottam were available.

C. Odebrecht et al. / Estuarine, Coastal and Shelf Science 150 (2014) 24 e 35 25


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be the main source of food for toheroa (Paphies ventricosa ), thedominant sand-dwelling bivalve mollusc.

In northeastern Argentina and southern Brazil brown surf zonewater at beaches was considered to be due to high iodine content inthe water (Khnemann,1966; Buckup, 1967). Due to the bene cialhealth properties of iodine people used to bathe in the dark-brownwaters and even to rub the ooze on their bodies. Buckup (1967),however, found the discoloration to be due to Asterionellopsis gla-cialis . After this report, high concentrations of A. glacialis were alsofound in So Paulo, southeastern Brazil, where the diatoms weresupposed to be linked to sh mortalities (Zavala-Camin andYamanaka, 1980). Deposition of diatoms on the beach at SantosBay occurred in 1979 and 1980 (Tommasi and Navas-Pereira, 1983).

McLachlan (1980) reported surf diatom accumulations to be aregular occurrence along the south coast of South Africa. Heattempted to relate the accumulations with the mechanisms fortheir maintenance in the surf zone. The surf diatom Anaulus aus-tralis (originally thought to be A. birostratus Grunow) is the mainsurf diatom species in South Africa; occasionally occurring togetherwith Aulacodiscus johnsonii (incorrectly identi ed as Aulacodiscuskittonii by McLachlan and Lewin, 1981), or Asterionellopsis glacialis(Du Preez et al., 1989). Milestone studies from the seventies tonineties led by Guy C. Bate and colleagues provided a compre-hensive understanding of physical, chemical and biological pro-cesses, drivers and patternsof thesurf diatom A. australis in the surf zone of Sundays River Beach, in the Eastern Cape (Campbell andBate, 1987; Campbell et al., 1988a; Du Preez et al., 1990; Talbotet al., 1990; Du Preez and Campbell, 1996a). It was shown thatthe ability of Anaulus australis to rise to the water surface byattachment to wave-entrained bubbles, together with their epi-psammic mode of life at night, were the most important biologicalfactors resulting in the diatom accumulations. These, in conjunc-tion with morphodynamics of the beach and the meteorologicalregime were the key factors for accumulations at the Sundays RiverBeach (see review Talbot et al., 1990).

3. The challenge of sampling in surf zones

The highly variable environment of surf zones both in space andtime, together with its turbulent nature renders the design of areliable sampling strategy an immense challenge. Several studieshave made use of sampling simply by wading into the surf zonewith a bucket, bottle, plankton net or a pipe to collect water orfoam,dependingon the aimof the study. In order tounderstand thespatial and temporal variability of surf diatoms, more compre-hensive studies are less common. The only beach surveyed in detailusing diverse sampling strategies was the Sundays River Beach,South Africa, where aerial surveys were used to quantify rip cur-rents and spatial dynamics of surf diatom accumulations (Talbotand Bate, 1987). These direct sampling methods were used in

conjunction with satellite images to quantify accumulations inrelation to longshore currents and lateral cell losses (Campbell andBate, 1988a). Aerial surveys were used to map the beaches associ-ated with surf diatomaccumulations along the entire South Africanand Namibian coastline (Campbell and Bate,1997).

Thegreat challenge of studying thefullextent of thesurf-zoneinsitu was met by synoptic water sampling achieved by a team of re-searchers wading into the surf zone, sampling from a helicopter inthe deeper portions of the breaker zone, coupled by using a boatbehind the breakers and offshore (Talbot and Bate, 1988b). Thebreaker zonemay also be reachedsuccessfullywitha jetski as itwasshown for sh larvae (Strydom, 2007). The release of a dye (rhoda-mine)inconjunctionwithphotogrammetricaerialphotographywasfound to be helpful to develop an understanding of the role of surf

water circulation in cell transport (Talbot and Bate, 1987). The

shortest time-scalerelatedwithsurf diatomaccumulationsis that of the tumbling of cells andresultant rhythmic uctuation in exposureirradiance with the passing of successive wave bores. These short-term dynamics require sampling at a time scale of seconds to mi-nutes, another challenge that was successfully tackled at the Sun-daysRiverBeach(Campbell etal.,1988b).Thesamplingofcellswhilein the sand at night proved to be the greatest challenge, and highvariability results in the requirement of exorbitantly large numbersof samples to obtain statistically defensible conclusions (Talbot andBate,1986). Estimationof theprimary productionof sucha complexsystem is therefore obtained by modeling approach (Campbell andBate, 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 ac-cording to the aim of the study. Physiological in vitro experimentsrequireonlysimplesampling in thesurf zone and/orsediments, butin situ quantitative studies require different strategies and repli-cation in order to faithfully capture the spatial and/or temporalvariability at a beach. Physical features like the wave height andfrequency, surf zone width, the presence of rip and longshorecurrents, sediments characteristics and information on meteoro-logical regime previously and during the sampling are importantfactors which should be always estimated concomitantly withsampling surf diatoms in any beach.

4. Geographical distribution of surf diatoms

Surf diatom accumulations have been reported in fteen coun-tries at ca. ninety sandy beaches located at latitudes between47 510N and 42100S (Table 1; Fig. 1), extending the geographicdistribution previously reported (Lewin and Schaefer, 1983; Talbotet 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 Zea-land and more recently recorded seven surf diatom species at thesame 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 hemispherethe most important area still comprises the west coast of USA(Washington and Oregon coasts). In Europe, accumulations arecommon in France (Le Gal et al., 1995) and recently were reportedfrom Spain (http:// topasion.blogspot.com.br/2011/10/attheya-el-alga-que-toma-el-sol-en-la.html) and from the oceanic CanaryIslands (Ojeda and O Shanahan, 2005). In Asia, the only countrywhere surf diatom accumulations have been reported is Indiawhere 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 andPanigrahy, 1989). Asterionellopsis glacialis is the only surf diatom that is a truly

cosmopolitan neritic marine species recorded from deeper coastalwaters as well as inshore. The other surf diatom species occur invarious parts of the world, but appear to be conned, for the mostpart, to surf zones. Attheya armata has been recorded fromtemperate areas in the northern (USA, France, Scotland, England,Spain) and southern (Argentina) hemispheres (see Table 1). It hasbeenalso reported from subtropical oceanic islands (Gran Canaria,Santa Cruz de Tenerife; Ojeda and Shanahan, 2005) and we haverecently found a few cells in samples collected from the shores of Algoa Bay, South Africa. By contrast, Asterionellopsis socialis wasconsidered to be endemic to the temperate northern hemisphere,

in the western USA (Lewin et al., 1989), however, recent reports

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

Beach Species Reference Beachlength (km)

Southern HemisphereZaire5 590S Banana, Congo River Aulacodiscus africanus Van Heurck, 1896 5

South Africa33 430S Sundays River Anaulus australis McLachlan and Lewin, 1981 5033 430S Sundays River Asterionellopsis glacialis Du Preez et al., 1989 5034 S Maitland River Anaulus australis McLachlan and Lewin, 1981 3034 070S Muizenberg Anaulus australis McLachlan and Lewin, 1981 834 060S Macassar Anaulus australis Campbell and Bate, 1997 634 470S Struisbaai Anaulus australis Campbell and Bate, 1997 2234 310S De Hoop Anaulus australis Campbell and Bate, 1997 1234 050S Vleesbaai Anaulus australis Campbell and Bate, 1997 1234 030S Glentana Anaulus australis Campbell and Bate, 1997 1134 S Wilderness Anaulus australis Campbell and Bate, 1997 434 020S Sedge eld Anaulus australis Campbell and Bate, 1997 1534 050S Buffalo Bay Anaulus australis Campbell and Bate, 1997 633 580S Van Stadens Anaulus australis Campbell and Bate, 1997 3132 500S Cintsa Anaulus australis Campbell and Bate, 1997 10

Australia

34 370

S Warren Anaulus australis McLachlan and Hesp, 1984 9035 350S Goolwa, Coorong Anaulus australis , Asterionellopsis glacialis McLachlan and Hesp, 1984 18038 300S Venus Bay Unknown McLachlan and Hesp, 1984;

www.vboping.blogspot.com50

38 540S Waratah Bay Anaulus australis Campbell, 1996 2530 060S Woolgoolga Unknown www. ickr.com/photos/47464237@NO7 427 550S Main Beach: Surfer s Paradise Anaulus australis Hewson et al., 2001 10027 360S North Stradbroke Island Anaulus australis D.S. Schoeman, pers. comm. 3326 270S Noosa Anaulus australis T.A. Schlacher, pers. comm. 1542 S Tasmania, west coast Anaulus australis , Attheya armata Lewin and Schaefer, 1983 3042 100S Tasmania, Strahan Beach Asterionellopsis glacialis McLachlan and Hesp, 1984 30

New Zealand35 450 e 36 150S North Island west coast: Ninety

Mile Beach (Scotts Point, Hukatere,Waipapakauri)

Asterionellopsis glacialis , Attheya armata Rapson, 1954 90

North Kaipara (Baileys, Glinks,Round Hill)

Asterionellopsis glacialis , Attheya armata Rapson, 1954 45

Muriwai Beach (South KaiparaHead, Wineh, Rocks) Asterionellopsis glacialis , Attheya armata Rapson, 1954 40

40 250 e 40 350S Wellington beaches (Manawatu,Waitarere, Hokio)

Asterionellopsis glacialis , Attheya armata Rapson, 1954; Cassie, 1955;Cassie and Cassie, 1960

100

35 400 e 35 450S North Island west coast: WaipouaKauri to Maunganui

Attheya armata , Aulacodiscus kittonii Sarma, 1975 12

Unknown North Island east coast Attheya armata , Aulacodiscus kittonii Kindley, 1983 NI37 150S Karioitahe Beach, Waiuku District Anaulus australis , Asterionellopsis glacialis ,

Attheya armata , Aulacodiscus kittoniiCampbell, 1996 35

37 15 S Karioitahe Beach, Waiuku District Anaulus australis , Asterionellopsis glacialis , Asterionellopsis socialis (a single colony), Attheya armata , Aulacodiscus johnsonii , Aulacodiscus kittonii , Aulacodiscus petersii ,Thalassiosira sp.

Campbell, pers. comm. 35

Paci c Ocean8 550S Marquesas archipelago, Bay of

TaiOhae: Nuku-Hiva Island Aulacodiscus africanus Sournia and Plessis, 1974 0.8

Venezuela46 150N Boca de Aroa Unknown Gianuca, pers. comm. in Campbell (1996) 33

Brazil3 440S Cear, Praia do Futuro Anaulus sp., Asterionellopsis glacialis ,

Aulacodiscus kittoniiVerde et al., 1990;Pereira da Costa et al., 1997;Pereira da Costa et al., 1998

32

3 440S Cear, Praia do Futuro Anaulus australis M. Garcia, pers. comm. 3210 300Se 11 280S Sergipe beaches: barras de Propri,

Vaza-Barris and Piau-Fundo-Real Asterionellopsis glacialis , Aulacodiscus ,Odontella spp.

Franco, 1998 130

14 300Se 15 050S Bahia, Ilhus: Cururupe Beach Anaulus australis , Asterionellopsis glacialis Tedesco, 2006 6724 110S So Paulo: Itanham Asterionellopsis glacialis Zavala-Camin and Yamanaka, 1980 2023 550Se 23 450S So Paulo: Pernambuco1, Bertioga2,

Indai3, S. Loureno4, Boracia5 Asterionellopsis glacialis Tommasi and Navas-Pereira, 1983 1.51

102&34475(Villac, pers.comm.)

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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 samplestaken from Karioitahe Beach, New Zealand in 2011. Thegeographical distribution of surf diatoms is much wider than thedistribution of surf diatom accumulations and most surf diatomspecies that form accumulations are present in a wide latitudinalrange (seeFig.1). Thus, it canbe concluded that temperature is notan important factor controlling their occurrence and accumula-tion, but may be a limiting factor for the geographical distribution

of some species.

5. Drivers leading to surf diatom accumulations

The main factors leadingto the accumulationof surf diatoms arephysical (beach morphodynamics), chemical (nutrient availability)and biological (species adaptation) factors. It has been shown thatsurf diatoms only accumulate in the surf zones of sandy beacheswhere intermediate to dissipative wave energy conditions prevail(according to the classication of Short and Wright, 1983). Alongsuch beaches, water circulation sets up entrained bodies of waterthat are related to rip currents within the surf zone and these lead

to the retention and concentration of the diatom cells (McLachlan,

Table 1 (continued )

Beach Species Reference Beachlength (km)

23 200Se 23 250S So Paulo: Ocian1, Parque Balnerio2,Guara3, Juria4, Pontal5

Anaulus australis , Asterionellopsis glacialis

Villac and Noronha, 2008 451&223194575

26 540S Santa Catarina: Navegantes Beach Anaulus australis, Asterionellopsis glacialis

Rrig et al., 1997 10

29 e 34 S Rio Grande do Sul: Atlntida,Rainha do Mar, Mostardas,Cassino, Tramanda

Asterionellopsis glacialis Buckup, 1967; Aguiar andCorte-Real, 1973; Gianuca,1983; Rrig and Garcia, 2003;Odebrecht et al., 2010

610

Uruguay33 500S Chuy Beach Asterionellopsis glacialis Baysse et al., 1989 23

Argentina37 170S Villa Gesell Beach Asterionellopsis glacialis Khnemann, 1966 3037 050S Pinamar Beach Asterionellopsis glacialis Khnemann, 1966 3039 S Peuhen-C Beach Asterionellopsis glacialis , Attheya

armataGayoso and Muglia, 1991 10

Northern HemisphereUSA46 550Ne 47 120N Copalis Beach, Washington Asterionellopsis socialis , Aulacodiscus

kittoniiBecking et al., 1927 30

46 550

Ne

47 120

N Copalis Beach, Washington Asterionellopsis socialis , Aulacodiscuskittonii ,Thalassiosira sp.

Campbell, pers. comm. 30

46 150Ne 47 200N Washington coast Asterionellopsis socialis , Attheya armata Lewin and Norris, 1970 12043 100Ne 47 200N Washington and Oregon coast:

Copalis, Fort Stevens, SeaSide,Cannon, Oceanside, Gleneden,Beachside, Hecata, UmpquaLighthous, Horsfall, Bullards beaches

Asterionellopsis socialis , Attheya armata Garver and Lewin, 1981 500

41 N California: Clam Beach Asterionellopsis socialis CDPH Monthly MarineBiotoxin Technical ReportNr. 11-09

60

Central AmericaCosta Rica8 N

Unknown Aulacodiscus africanus Lewin and Schaefer, 1983 NI

Panama8 N

Unknown Aulacodiscus africanus Lewin and Schaefer, 1983 NI

NicaraguaUnknown

Unknown Unknown Thayer, 1935 NI

EuropeFrance47 550N Baie Audierne, Tronon Beach Attheya armata Le Gal et al., 1995 30

Spain42 070N Playa America, Arenal Panxn

(Nigrn, Pontevedra) Attheya armata http:// topasion.blogspot.com.br/

2011/10/attheya-el-alga-que-toma-el-sol-en-la.html

2

Canary Islands27 460N Gran Canaria: Las Burras Attheya armata Ojeda and Shanahan, 2012 227 460N Gran Canaria: San Augustin Attheya armata Ojeda and Shanahan, 2012 227 480N Gran Canaria: Taurito Attheya armata Ojeda and Shanahan, 2012 127 440N Gran Canaria: Meloneras Attheya armata Ojeda and Shanahan, 2012 228 300N Santa Cruz de Tenerife: Las

Gaviotas Beach Attheya armata Ojeda and Shanahan, 2012 1.2

Asia

India19 160N Gopalpur Beach Asterionellopsis glacialis Mishra et al., 2006 35

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1980; Talbot and Bate,1987, 1988b; Lewin et al., 1989; Talbot et al.,1990). The lengthof the beach is considered an important feature aslongshore currents remove cells at the ends of the beach. Theminimum length for retention of surf diatoms in the surf zones of South African beaches was considered to be 4 km long (Campbelland Bate, 1997). Two smaller beaches (Bay of Tai O Hae, Mar-quesas Islands; Playa de las Americas, Canary Islands) have a shorecon guration (substantial rocky headlands) that enables theretention of surf diatoms (see Table 1).The surf zone was rst proposed by McLachlan (1980) to be aself-sustained ecosystem and this idea was largely conrmed forthe Sundays River Beach, where the effects of water circulation onthe spatial and temporal distribution of accumulations, cell abun-dance and losses from the surf zone, vertical migration, primaryproduction and the photosynthetic physiology of Anaulus australiswere elucidated (Campbell and Bate, 1988a,b,c; 1991; Talbot et al.,1990; Du Preez et al., 1990; Du Preez and Campbell, 1996a). Itbecame clear that the water circulation in the surf zone is the mainfactor leading to cell accumulation at the Sundays River Beach. Thesurf zone water circulation pattern is closely related with the pre-vailing 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 takethem to the surface), where they may survive for up to 75 days inthe dark and may be returned to the surf zone by increased tur-bulence during windy conditions (Du Preez and Bate, 1992). In allsurf zones studied to date, the morphodynamics and meteorolog-ical regime are overriding factors in controlling the formation andmaintenance of the accumulations.

The availability of nutrients is obviously a major requirement tosustain such high cell concentrations in the surf diatom accumu-lations (103 to106 cells ml 1) butalsooutside (102 to104 cells ml 1).Nitrogen, rather than phosphorus or silicon was shown to be thelimiting nutrient in the eastern North Pacic (Lewin, 1978), south-ern Brazil (Niencheski et al., 2007; Odebrecht et al., 2010; Piedrasand 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 coastalupwelling (Lewin, 1978). The annual rainfall is high (1000 to2500 mm y 1) in some areas such as the USA northwest coast(Lewin and Schaefer, 1983) and southern Brazil (Klein, 1997), butlow in South Africa (400e 600 mm y 1, Campbell and Bate, 1991),indicating that other factors must be important.

The discharge of subterranean groundwater was the primarynutrient source for the maintenance of high biomass of surf di-atoms at the Sundays River Beach, South Africa (Campbell andBate, 1991, 1998) and this was found to also be the case insouthern Brazil (Niencheski et al., 2007). At the Sundays RiverBeach, the groundwater discharge from the unconned aquiferbeneath the back-of-beach dune eld contributes suf cient ni-trogen to balance the loss of biomass from the surf zone due tolongshore currents (Campbell and Bate, 1991, 1998). In southernBrazil, Niencheski et al. (2007) found that the nitrogen ux viagroundwater fuels primary production in the surf zone near PatosLagoon. A comparison between the groundwater and, in partic-ular nitrogen discharges, from terrestrial sources at the SundaysRiver Beach and in southern Brazil (Table 2), indicates that thesource of nitrogen may differ. The nitrate concentration in the

water sampled from wells at Sundays River Beach was two ordersof magnitude higher than in the wells of southern Brazil; whilethe ammonium concentration was an order of magnitude higherin southern Brazil and phosphorus was ve times higher. Thevolume of subterranean groundwater discharge was much greaterin 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 abarrier spit in response to the hydrological head created by thelagoon. Furthermore, the annual rainfall is twice to threefoldhigher in southern Brazil than at the Sundays River Beach. In bothecosystems, important nitrogen losses occur (ca. 60e 70% of N groundwater in ux), however the main loss from the surf zone atthe Sundays River Beach occurs alongshore while in southern

Brazil losses occur across-shore to the inner shelf. The difference

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



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could be because the Sundays River Beach (ca. 50 km in length) islocated in an embayment (Algoa Bay) where longshore currentstransport diatom cells outside the beach limits (Campbell andBate, 1988a). In southern Brazil, the study area (240 km inlength) forms a third of a very long, straight beach where surf diatoms occur (ca. 600 km). Here, alongshore losses are lessimportant compared to the transport to the inner shelf.

6. Temporal patterns and drivers of surf diatomaccumulations

6.1. Diel cycle

Cell metabolism of diatoms and other microalgae present a dielperiodicity in cell division and size (Talbot and Bate,1986; Du Preezand Campbell, 1996a). It was rst recognized that Attheya armatarises to the surface each morning before sunrise and disappears inthe late afternoon before sunset (Lewin and Hruby,1973). A similarcycle was observed for Anaulus australis (Sloff et al., 1984; Talbotand Bate, 1986). Both species present a mucilaginous cell coating,which was suggested to control the diel cycle for Anaulus australisin the water column: the thicker coating in the afternoon favorsadherence of particles to the mucilage sheath and the cells wouldswitch from adhering to air bubbles at the water surface to depo-sition in the sediment (Talbot and Bate, 1988a). However, based onhistochemical analysis, Du Preez and Campbell (1996b) concludedthat the mucilage was probably not the feature that controls the

diel cycle. This is corroborated by A. armata that presents consis-tently lower numbers at or near the water surface at night butexhibit no diel cycle of the mucilage coating (Lewin et al., 1989;Gayoso and Muglia, 1991). In contrast, Asterionellopsis socialis isfound 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 diatomaccumulations in exposed sandy beach surf zones is thestrength of onshore winds that result in increased wave height andturbulence. The action of onshore wind was recognized in theearliest 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 itsin uence on wave height (Talbot et al., 1990). When wavesapproaching the shore reach shallow water, the water motionsuspends cells deposited on the sediment. Once in the water col-umn, wave-entrained bubbles concentrate the cells in the surfacefoam. The sudden increase in cell concentrations of surf diatoms inthe surf zone after storms cannot be explained by growth (Rrigand Garcia, 2003), but their rapid appearance must be caused bywave-generated resuspension of cells deposited on the sediment of the nearshore (Lewin, 1978; Talbot and Bate,1989). Onshore windsalso favor the maintenance and concentration of these surf diatomcolonies in the neuston through their advection towards the beach(Odebrecht et al., 1995).

6.3. Seasonal variation

Seasonal variations in surf diatom accumulations are unrelatedto latitude and species, but rather depend on seasonal changes inwave height and turbulence, as indicated by a comparison of Attheya armata at the beaches Copalis in western USA, Tronon inFrance andPeuhen-C in Argentina (Fig.2a). In Argentina, relativelyhigh concentrations were observed throughout the year(104 cells ml 1; Gayoso and Muglia, 1991), while in the USA highconcentrations of cells (104 to 106 cells ml 1) were recorded over a12-year period as a semipermanent feature, with the exception of lower values (102 to 104 cells ml 1) recorded in summer (Lewinet al., 1989). By contrast, Attheya armata presents a clear seasonalcycle in France where accumulations (max. 104 cells ml 1) onlyoccurred from the end of autumn through winter until the begin-ning of spring (Le Gal et al., 1995). At the Canary Islands, accumu-lations of Attheya armata occurred only in summer and winter(Ojeda and Shanahan, 2005). The beaches in USA, France andArgentina are all located in temperate regions, but are subject todifferent climatic and oceanographic driving forces. In Argentina,strong winds blow throughout the year, explaining the persistentcell accumulations (Gayoso and Muglia, 1991). In the USA andFrance the seasonal cycle of wind direction and strength is well-de ned. At the former, strong southwesterly winds occurringfrom autumn to spring, produce a net shoreward transport of sur-face water, while in summer, weaker northerly and northwesterlywinds prevail and drive surface water seaward, presumablyremoving part of the surf diatom ( A. armata and Asterionellopsissocialis ) population (Fig. 2b) (Lewin et al., 1989). Also in France, thewind strength is much greater in autumn and winter,> 30 km h 1for 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 diatomaccumulations. In South Africa, the surf diatoms show no seasonalresponse to temperature (Campbell and Bate,1988b), but increasedbiomass occurs in the windy spring and autumn seasons (Fig. 2c).

The apparent absence of a seasonal cycle in Attheya armata accu-mulations at the subtropical beaches of the Canary Islands (Ojedaand Shanahan, 2005) should be studied in more detail but isprobably related to the trade wind regime.

For Asterionellopsis glacialis , the accumulations in southernBrazil 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 aslight increase in frequency during the winter months, whenonshore winds were more frequent. Further north, Rezende andBrandini (1997) also related an autumn increase in cell concen-trations (up to 102 cells ml 1) to the higher frequency of southerlyfronts. However, a rather irregular pattern of Asterionellopsis gla-cialis accumulations through the year emerged at Cassino Beach,

when comparing twenty years (1992e

2012) of monthly records.

Table 2Comparison 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 lagoonmouth#

Length (km) 50 km 240 kmWidth (m) 250 m 100 mAmmonium (uM) 2.9e 3.6 19.6e 36.8Nitrate 200e 280 2.8e 7.8Phosphorus 1.2e 1.5 6.0e 8.0Average SGD 1.5 m3 m 1 d 1 129 m3 m 1 d 1N Groundwater ux 1.5 kg m 1 y 1 55.2 kg m 1 y 1

(2.42 106 mol d 1N loss 1.1 kg m1 y 1

(w 73% of N)32 kg m 1 y 11.39 106 mol d 1(w 57% of N)

Main loss Along the shore To the inner shelf

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

http://ru.surf-forecast.com/breaks/Audierne/reliability_by_seasonhttp://ru.surf-forecast.com/breaks/Audierne/reliability_by_seasonhttp://ru.surf-forecast.com/breaks/Audierne/reliability_by_seasonhttp://ru.surf-forecast.com/breaks/Audierne/reliability_by_season


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Both the lowest (August) and highest (July, September) meanconcentrations were observed in the austral winter to early spring(Fig. 2d). At the rst glance the August minimum seems an oddoutlier, however consistently low concentrations in August wereobserved together with theabsence of cell accumulations as well asthe minimum chlorophyll a average over the twenty-year period.The absence of a consistent seasonal cycle for A. glacialis at CassinoBeach resembles the result for Attheya armata in Argentina.

The tropical Brazilian Cururupe Beach, Bahia, is an interestingexample, because both Anaulus australis and Asterionellopsis gla-cialis presented a seasonal cycle with higher cell concentrations inautumn and winter, when the passage of cold fronts and onshorewinds are more frequent (Tedesco, 2006).

6.4. Changes in species composition

Global impacts like seawater temperature changes, sea-levelrise, ocean acidi cation, accelerated eutrophication leading to

dead zones and over shing have major effects on the marineenvironment (Defeo et al., 2009; Doney et al., 2012) and they mayin uence the health of sandy beaches, their surf zones and the surf diatoms in them. Signicant changes in the long-term speciescomposition and abundance of surf diatoms have been recorded atthree sandy beaches. At Copalis Beach, Lewin et al. (1989) reportedthe replacement of the main species, Aulacodiscus kittonii , domi-nant in the early 1920s, with Attheya armata in the 1950s and thecomplete disappearance of the former after the 1940s. Based on a12- year study (1971e 1982) and in comparison with earlier studies, Attheya armata was rst observed in about 1950, when it wasconsidered to be an introduced species. The dramatic changesleading to the disappearance of A. kittonii were suggested to bepossibly related with the construction of the rst major damon theColumbia River, which inuenced the river discharge along thesouthern Washington coast and modi ed the water volume, timingof river discharge, as well as nutrient and sediment loads reachingthe beach (Lewin et al., 1989).

Fig. 3. Interannual variability (1992 e 2012) 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.

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 byLewin 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).



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At the Sundays River Beach, Du Preez et al. (1989) reported anearly complete switch from Anaulus australis to Asterionellopsis glacialis for a month. However this has never been observed tooccur again. Long-term monthly sampling (1992e 2012) at a sin-gle station at Cassino Beach provided an opportunity to examinethe effect of climatic oscillations. These, in conjunction withenvironmental impacts due to human activities, signicantlyaltered the abundance and composition of the phytoplankton(Fig. 3). A reduction in the frequency of surf diatom accumula-tions followed extreme mud deposition events in 1998 and 2002(Odebrecht et al., 2003; 2010). Mud deposits are a recurrentphenomenon 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 sedi-ments in the lagoon s main channel, which are transported to thenearshore, especially during high rainfall periods. The impact of mud deposits on the beach is strongest during extreme El Nioperiods during which southern Brazil experiences high rainfall.The effects of the mud deposition include the attenuation of waveaction through altered water viscosity, the burial of largenumbers of cells, and alteration of the nutrient concentrations inthe 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 primaryproduction in sandy beach surf zones (Campbell and Bate, 1988c),normally considered as oligotrophic ecosystems (Pearse et al.,1942). According to McLachlan and Brown (2006), accumulationsmay generate exceptionally high primary production rates (500e2000 g C m3 y 1) and a signi cant part (more than 50%) may beproduced 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 thatmost particulate organiccarbonpresent in thesurf zone of SundaysRiver Beach is in the form of detritus and not live material. Evenduring surf diatom accumulations, detritus may composeca. 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 highlyproductive food web. In these beaches, macrobenthic lter feedersare the main consumers and form a link between diatoms and thehigher trophic levels (Garcia and Gianuca,1997). According to theseauthors, 95% of the secondary production in the surf zone of Cassino Beach comprises lter feeders: mostly the molluscs Meso-desma mactroides , Donax hanleyanus and the decapod crustaceanEmerita brasiliensis . These feed heavily on the surf diatom Aster-ionellopsis glacialis . However, mysids and copepods present in thesurf zone can also be important consumers of surf diatoms, trans-

ferring substantial portions of the organic matter to secondary andtertiary consumers such as sh, birds and even marine mammals(Garcia and Gianuca, 1997; McLachlan and Brown, 2006). Particu-late organicmatterproduced by surf diatoms is not restricted to thesurf zone, but spreads to the supralittoral. At Cassino Beach, lterfeeders such as polychaetes, molluscs ( Amiantis purpuratus , Tivelaventricosa and Mactra isabellana ) and detritivores ingest diatomsthat are deposited on the sediments. Similarly, large amounts of Asterionellopsis glacialis deposited in the supratidal after stormevents feed insects such as the beetles, Bledius bonariensis ,B. microcephalus and B. fernandezi as well as ghost crabs, Ocypodequadrata (Garcia and Gianuca, 1997).

Interstitial food chains in surf zones also benet from theabundant primary production in the water column, although

pelagic organisms rarely consume meiofauna. Thus, the interstitial

environment functions as a mineralization site, providing dissolvedinorganic nutrients to sustain the primary production in the watercolumn (McLachlan and Brown, 2006). On the other hand, the largeamount of dissolved organic carbon produced by surf diatoms isconsidered to be available to be taken up by bacteria and shouldfuel the surf zone microbial loop (McLachlan and Bate, 1985;McLachlan and Brown, 2006). McGwynne (1991) found thatalmost half of the carbon required that sustain the growth of het-erotrophic bacteria was provided by Anaulus australis at the Sun-days River Beach. Conversely, in accumulations of the surf diatoms,between 3 and 46% of the exuded carbon is consumed by bacteriaindicating ample provision of substrate for bacteria when the surf diatom biomass is suf ciently high for accumulations to form.McGwynne (1991) found that 41% of the total annual primaryproduction (120 kg C m1 y 1), enters the microbial loop. This wasconsidered a valid estimate because bacteria areextremely active inmost aquatic ecosystems absorbing and mineralizing largeamounts (> 90%) of dissolved organic carbon (McLachlan and Bate,1985). However, according to McLachlan and Brown (2006) the microbial loop would be inef cient in transferring matter andenergy to larger consumers in the surf zone, since a minimum of atleast four food-web levels are necessary to incrementally alterparticle size and, in this case, very little energy would reach thehigher trophic levels. Thus, the surf zone microbial loop wouldmainly play a role in the nutrient cycling of this environment, butnot represent a source of matter and energy for macroorganisms.

At Cassino Beach, however, a decoupling between the surf zonediatom Asterionellopsis glacialis andbacteriawas found (Abreu et al.,2003). At this beach bacterial abundance remained exceptionallylow in the presence of A. glacialis a ccumulations. This was an un-expected observation as A. glacialis produces large amount of mucus. Bacteria cultivated in waterwhere A. glacialis was present inhigh cell concentrations showed a long lag phase in the bacterialgrowth response, probably as a result of the presence of bacterio-static antibiotics produced by the diatoms (Abreu et al., 2003). Theresults indicate that, at least for the surf zone at Cassino Beach, the

microbial loop

does not form the major channel for dissolvedcarbonproducedby thesurf diatom Asterionellopsis glacialis anditisneither recycling nutrients, nor serving as food source for otherorganisms in the food web. According to Abreu et al. (2003) thesurplus dissolved organic carbon in the water at Cassino Beach ismost likely transformed into amorphous mucilaginous aggregatesdue to the turbulence, in similar fashion to the production of ma-rine snow in the ocean (Larson and Shanks, 1996; Passow et al.,2001). Thus diatoms and amorphous mucilaginous aggregatescould be consumed by benthic and pelagic lter feeders enhancingthe surf zone macro-food web. However, as observed by many au-thors (Abreu et al., 2003; McLachlan and Brown, 2006; Bergaminoet al., 2011), information about the microbial ecology in sandybeach surf zones is still scarce and deserves further research in or-

der to better understand the role played by bacteria and protozoansin the ecology of high energy surf zones of sandy beaches.

7. Conclusion and perspectives

At present, the number of beaches where surf diatom accu-mulations have been reported is approximately double (90 bea-ches) the number compared to assessments of some twenty yearsago (Talbot et al., 1990; Campbell, 1996). The latitudinal range hasnot changed (ca. 42 100 S to 42 N), although tropical and Eu-ropean examples are included now in the list of active areas,which were not known previously. Despite the relatively largenumber of beaches worldwide, there are still only a few placeswhere surf diatoms have been studied in detail; this applies in

stark contrast with their importance as primary producers. The



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challenge of sampling the surf zone comprehensively maycontribute to this disparate. However, rather simple samplingprocedures may be used if consistently replicated in space and/ortime, and laboratory studies may be conducted to test variousresearch questions.

Despite the increase in number of beaches where surf diatomshave been recorded, the southern hemisphere still has a greaternumber of beaches with accumulations. Coastal conguration andmorphodynamics may partially explain this, but the lack of infor-mation for the Asian beaches leaves this part of the northernhemisphere an open question. Recently, three additional species,were found to accumulate in the surf zone. A species of Thalassio-sira , which appears to be a new species and remains to bedescribed, was recorded from accumulations in New Zealand andthe Washington coast of the USA (Campbell, pers. comm.), and Amphitetras antediluviana and Biddulphia biddulphiana were re-portedin highabundance in brownwaterat Camboriu Beach,Brazil(Rrig, pers. comm). These are interestingspecies for futurestudies.

The apparent geographical barriers in eastern South America,where the distribution of the different species are conned to re-gions remains to be addressed: Attheya armata thrives in the southonly (39 S, Argentina) and Anaulus australis north of 28 S, while Asterionellopsis glacialis is found from the tropical to temperateareas. Physiological studies should be conducted in order to testwhether factors such as temperature, light, salinity or sedimentcharacteristics may explain this geographical distribution of surf diatoms.

The general processes leading to surf diatom accumulations inhigh-energy beaches with suf cient nutrient supply, are well un-derstood, as is the in uence of the meteorological regime, beachlength and morphodynamics. However several questions remainto be answered. For example, the cell diel cycle and mucus pro-duction, considered very important to maintain the diatoms in thesurf zone, is only known in detail for Anaulus australis . It is clearthat not all species are dependent on this cycle of mucilage pro-duction and removal, as evidenced for Asterionellopsis socialis .Even for Attheya armata , which also accumulates in the surf zoneduring the day as is found for A. australis , the mechanism appearsto be different. Investigations of the diel cycle of other surf diatomspecies 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 pelagiccoupling should be tested for the other species in the eld andlaboratory.

Acknowledgments

C. Odebrecht and P. Abreu are fellows of the Brazilian NationalResearch Council-CNPQ and the research was funded through theLong Term Ecological Research Program (BR-LTER). Research by E.

Campbell and D. du Preez was funded by the South AfricanNationalResearch Foundation and the Nelson Mandela MetropolitanUniversity.

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