3
MARINE ECOLOGY PROGRESS SERIES Mar Ecol Prog Ser Vol. 301: 303–305, 2005 Published October 11 During the warmest summer reported by the National Institute of Meteorology for Spain (INM Spain) in the Canary Islands since 1912, satellite and in situ obser- vations in August 2004 detected an extensive bloom of the diazotrophic cyanobacterium Trichodesmium erythraeum Ehrenberg, which has never been detected in the NW African Upwelling and adjacent areas before (Capone et al. 1997, Lenes et al. 2001, Hood et al. 2002). At the end of July 2004, quasi-true-colour images from the OrbView-2 SeaWIFS satellite revealed con- © Inter-Research 2005 · www.int-res.com *Email: [email protected] NOTE Bloom of the marine diazotrophic cyanobacterium Trichodesmium erythraeum in the Northwest African Upwelling Antonio G. Ramos 1, *, Antera Martel 2 , Geoffrey A. Codd 3 , Emilio Soler 2 , Josep Coca 1 , Alex Redondo 1 , Louise F. Morrison 3 , James S. Metcalf 3 , Alicia Ojeda 4 , Sonia Suárez 2 , Michel Petit 5 1 SEASnet Canarias, Dpto. de Biología, University of Las Palmas de Gran Canaria, Campus de Tafira, 35017 Las Palmas de Gran Canaria, Canary Islands, Spain 2 National Bank of Algae, Centro de Biotecnología Marina, Muelle de Taliarte s/n 35214-Telde (Gran Canaria), Canary Islands, Spain 3 Division of Applied and Environmental Biology, School of Life Sciences, University of Dundee, Dundee DD1 4HN, UK 4 Instituto Canario de Ciencias Marinas (ICCM), Carretera de Taliarte s/n, PB 56. 35200 Telde (Gran Canaria), Canary Islands, Spain 5 SEASnet Montpellier, Institut de Recherche pour le Développement (IRD), Maison de la Télédétection, 500 Rue JF Breton, 34093 Montpellier Cedex 05, France ABSTRACT: A bloom of the non-heterocystous diazotrophic cyanobacterium Trichodesmium ery- thraeum Ehrenberg is reported in the Canary Islands Archipelago during August of 2004, the warmest period of a meteorological series recorded by the National Institute of Meteorology (Spain) since 1912. Samples showed massive occurrences of T. erythraeum (1000 filaments ml –1 ) in different sectors of northern and southern waters off the central Canary Islands. Water analyses also showed a relatively low presence of dinoflagellates and diatoms. Quasi-true colour satellite images of dust storms, elevated sea surface temperature (the warmest satellite-derived record), chlorophyll a and geostrophic current fields showed satellite-derived optical positives of Trichodesmium in an African upwelling advective, jet-drifting westward current off the south Canary Islands. Analyses for cyan- otoxins using HPLC found microcystins, which was confirmed by immunoassay, at concentrations from 0.1 to 1.0 μg microcystin-LR equivalents (g –1 dry weight of bloom material). A T. erythraeum bloom such as that observed in August 2004 in the NW African Upwelling does not appear to have been recorded for the area previously. The bloom may have developed due to the exceptionally warm weather and/or to the massive dust storms from the Sahara Desert observed in the NE Atlantic in August 2004. KEY WORDS: Cyanobacteria · Trichodesmium erythraeum · Remote sensing · NW African Upwelling · Advective jet · Toxicity Resale or republication not permitted without written consent of the publisher

Bloom of the marine diazotrophic cyanobacterium ...Ramos et al.: Trichodesmium erythraeum bloomcurrent dust storms from the Sahara Desert which covered the NE Atlantic area (Fig. 1a)

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Page 1: Bloom of the marine diazotrophic cyanobacterium ...Ramos et al.: Trichodesmium erythraeum bloomcurrent dust storms from the Sahara Desert which covered the NE Atlantic area (Fig. 1a)

MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol. 301: 303–305, 2005 Published October 11

During the warmest summer reported by the NationalInstitute of Meteorology for Spain (INM Spain) in theCanary Islands since 1912, satellite and in situ obser-vations in August 2004 detected an extensive bloomof the diazotrophic cyanobacterium Trichodesmium

erythraeum Ehrenberg, which has never been detectedin the NW African Upwelling and adjacent areas before(Capone et al. 1997, Lenes et al. 2001, Hood et al. 2002).

At the end of July 2004, quasi-true-colour imagesfrom the OrbView-2 SeaWIFS satellite revealed con-

© Inter-Research 2005 · www.int-res.com*Email: [email protected]

NOTE

Bloom of the marine diazotrophic cyanobacteriumTrichodesmium erythraeum in the Northwest

African Upwelling

Antonio G. Ramos1,*, Antera Martel2, Geoffrey A. Codd3, Emilio Soler2, Josep Coca1, Alex Redondo1, Louise F. Morrison3, James S. Metcalf3, Alicia Ojeda4, Sonia Suárez2,

Michel Petit5

1SEASnet Canarias, Dpto. de Biología, University of Las Palmas de Gran Canaria, Campus de Tafira, 35017 Las Palmas de Gran Canaria, Canary Islands, Spain

2National Bank of Algae, Centro de Biotecnología Marina, Muelle de Taliarte s/n 35214-Telde (Gran Canaria), Canary Islands, Spain

3Division of Applied and Environmental Biology, School of Life Sciences, University of Dundee, Dundee DD1 4HN, UK4Instituto Canario de Ciencias Marinas (ICCM), Carretera de Taliarte s/n, PB 56. 35200 Telde (Gran Canaria),

Canary Islands, Spain5SEASnet Montpellier, Institut de Recherche pour le Développement (IRD), Maison de la Télédétection, 500 Rue JF Breton,

34093 Montpellier Cedex 05, France

ABSTRACT: A bloom of the non-heterocystous diazotrophic cyanobacterium Trichodesmium ery-thraeum Ehrenberg is reported in the Canary Islands Archipelago during August of 2004, thewarmest period of a meteorological series recorded by the National Institute of Meteorology (Spain)since 1912. Samples showed massive occurrences of T. erythraeum (1000 filaments ml–1) in differentsectors of northern and southern waters off the central Canary Islands. Water analyses also showed arelatively low presence of dinoflagellates and diatoms. Quasi-true colour satellite images of duststorms, elevated sea surface temperature (the warmest satellite-derived record), chlorophyll a andgeostrophic current fields showed satellite-derived optical positives of Trichodesmium in an Africanupwelling advective, jet-drifting westward current off the south Canary Islands. Analyses for cyan-otoxins using HPLC found microcystins, which was confirmed by immunoassay, at concentrationsfrom 0.1 to 1.0 µg microcystin-LR equivalents (g–1 dry weight of bloom material). A T. erythraeumbloom such as that observed in August 2004 in the NW African Upwelling does not appear to havebeen recorded for the area previously. The bloom may have developed due to the exceptionally warmweather and/or to the massive dust storms from the Sahara Desert observed in the NE Atlantic inAugust 2004.

KEY WORDS: Cyanobacteria · Trichodesmium erythraeum · Remote sensing · NW African Upwelling ·Advective jet · Toxicity

Resale or republication not permitted without written consent of the publisher

Page 2: Bloom of the marine diazotrophic cyanobacterium ...Ramos et al.: Trichodesmium erythraeum bloomcurrent dust storms from the Sahara Desert which covered the NE Atlantic area (Fig. 1a)

Mar Ecol Prog Ser 301: 303–305, 2005304

Fig

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Page 3: Bloom of the marine diazotrophic cyanobacterium ...Ramos et al.: Trichodesmium erythraeum bloomcurrent dust storms from the Sahara Desert which covered the NE Atlantic area (Fig. 1a)

Ramos et al.: Trichodesmium erythraeum bloom

current dust storms from the Sahara Desert whichcovered the NE Atlantic area (Fig. 1a). In this area,the annual average dry flux of Saharan dust canrange from 0.03 to 0.08 g m–2 d–1 or 1.7 × 106 tons yr–1

as inferred from experimental dry deposition (Torreset al. 2002). Dust fluxes produce a significant impacton the biogeochemical cycle of trace elements, pro-viding a source of the Fe required for diazotrophicheterocystous and non-heterocystous cyanobacterialgrowth due to the demand for nitrogenase (Capone etal. 1997, Lenes et al. 2001).

Beginning in August, satellite-derived AVHRR/NOAAsea surface temperature (SST) images recorded 28.5°C,the warmest record within the last 15 yr in CanaryIsland waters. SST imagery also detected convergentwarm (23°C) oceanic waters over the NW African shelfwhere the upwelling originates (Fig. 1b). Chlorophyll aimages from the OrbView-2 SeaWIFS satellite showedrichly productive coastal upwelled waters (chl a > 3 mgm–3) of an advective jet at an anomalously warmer SST(24.5°C) compared to the normal SST for upwelledwaters (i.e. 18 to 22°C). The jet was observed fromsatellite-derived geostrophic current field pictures ofthe CLS-AVISO Altimeter Satellite Data Centre, andadvected westward with the offshore-directed surface-current drift fields to reach the position andconfiguration seen in Fig. 1c.

An optical model of water leaving radiance imagesfrom the OrbView-2 SeaWIFS satellite parameterizedfor Trichodesmium (Hood et al. 2002) was testedduring the bloom event (Fig. 1d). The model detectedsignificant remote-sensed optical positives of Tri-chodesmium in the NW African shelf. It also showedoptical positives in the advective jet drifting westwardoff the south Canary Islands.

Subsurface water samples (2 l) were collected aroundthe seashore at different locations off the islands offGran Canaria and Tenerife during August 2004. Sam-ples were fixed in 1% Lugol’s Iodine immediately andtrichomes were counted after a 24 h settling period.Cyanobacteria were identified according to Anagnos-tidis & Komàrek (1998). Concentrations of hetero-cystous and non-heterocystous cyanobacteria, togetherwith other phytoplankton counts, were carried outwith an inverted microscope using the Utermöhl tech-nique. Results showed the absence of heterocystousdiazotrophic cyanobacteria. Ninety-seven percent ofthe cells consisted of the non-heterocystous diazo-trophic cyanobacterium Trichodesmium erythraeum(1240 filaments ml–1). The remaining cells (10 cellsml–1) consisted of dinoflagellates and diatoms (Gymno-dinium, Ostreopsis and Zygabikodinium). The highwater temperatures may have accounted for the domi-nance of the bloom by T. erythraeum, rather than by

heterocystous diazotrophic cyanobacteria. Indeed, dif-ferences in temperature-dependent O2 flux activity,respiration and of O2-sensitive nitrogen fixation appearto favour the diazotrophic growth of Trichodesmium atelevated temperatures, rather than that of heterocys-tous cyanobacteria (Staal et al. 2003).

In order to determine environmental and healthimpacts of the Trichodesmium erythraeum blooms offthe Canary Islands the cyanotoxins were analysed:microcystins by means of HPLC and immunoassay,and anatoxin-a and cylindrospermopsin by HPLC(Metcalf et al. 2000, Codd et al. 2001). Anatoxin-a andcylindrospermopsin were not detectable, but micro-cystins were found by HPLC, with photodiode arraydetection, with confirmation by immunoassay at con-centrations from 0.1 to 1.0 µg microcystin-LR equiva-lents (g–1 dry weight of bloom material).

Such Trichodesmium erythraeum blooms have appar-ently not been recorded previously anywhere alongthe coast bordering the NW African Upwelling. Reli-able satellite observations and verification on theground have confirmed that the early stages of thisanomalous event are associated with the exceptionallywarm weather and dust storms observed in this area inAugust 2004. This phenomenon may be an increas-ingly observed characteristic of higher temperatures(global warming), with consequent increases in pri-mary production and N2 fixation, which may be accom-panied by bloom toxicity.

LITERATURE CITED

Anagnostidis K, Komárek J (1988) Modern Approach to theclassification system of Cyanophytes. 3-Oscillatoriales.Algol Stud 50–53:327–472

Capone DG, Zehr JP, Paerl HW, Bergman B, CarpenterEJ (1997) Trichodesmium a globally significant marinecyanobacterium. Science 276:1221–1229

Codd GA, Metcalf JS, Ward CJ, Beattie KA, Bell SG, Kaya K, PoonGK (2001) Analysis of cyanobacterial toxins by physicochem-ical and biochemical methods. J AOAC Int 84:1626–1635

Hood RR, Subramaniam A, May LR, Carpenter EJ, CaponeDG (2002) Remote sensing of nitrogen fixation by Tricho-desmium. Deep-Sea Res II 49:23–147

Lenes J, Darrow B, Cattrall C, Heil CA and 7 others (2001)Iron fertilization and the Trichodesmium response on theWest Florida shelf. Limnol Oceanogr 46:1261–1277

Metcalf JS, Bell SG, Codd GA (2000) Production of novelpolyclonal antibodies against the cyanobacterial toxinmicrocystin-LR and their application for the detection andquantification of microcystins and nodularin. Water Res34:2761–2769

Staal M, Meysman FJR, Stal LJ (2003) Temperature excludesN2-fixing heterocystous cyanobacteria in the tropicaloceans. Nature 425:504–507

Torres M, Gelado M, Collado C, Siruela V, Cardona P,Hernández-Brito J (2002) Variability of dust inputs to theCANIGO zone. Deep-Sea Res II 49:3455–3464

305

Editorial responsibility: Otto Kinne (Editor-in-Chief), Oldendorf/Luhe, Germany

Submitted: November 30, 2004; Accepted: July 17, 2005Proofs received from author(s): August 8, 2005