The phytoplankton biodiversity of the coast of the state of São Paulo, Brazil

A biodiversidade do fitoplâncton do litoral do estado de São Paulo, Brasil

ARTICLES

The phytoplankton biodiversity of the coast of the state of São Paulo, Brazil

A biodiversidade do fitoplâncton do litoral do estado de São Paulo, Brasil

Maria Célia Villac¹; Valéria Aparecida de Paula Cabral-Noronha; Thatiana de Oliveira Pinto

Departamento de Biologia, Universidade de Taubaté - UNITAU, Av. Tiradentes, 500, CEP 12030-180, Taubaté, SP, Brazil

ABSTRACT

The objective of this study is to compile the inventory of nearly 100 years of research about the phytoplankton species cited for the coast of the state of São Paulo, Brazil. A state-of-the-art study on the local biodiversity has long been needed to provide a baseline for future comparisons. This type of data is scattered in old scientific journals and in the so-called "grey literature", and are in need of nomenclature updating. Twenty-six publications are considered. The earliest sampling record is from 1913 (?) and the most recent from 2002. This checklist compiled from the literature was complemented with primary data collected between August 2004 and July 2006, recent surveys of the surf-zone of 20 beaches located along the coast and of a mariculture farm at the Cocanha Beach, Caraguatatuba. The complete species list includes 572 taxa: most are diatoms (82%), seconded by dinoflagellates (16%), with a minor contribution of silicoflagellates, coccolithophorids, ebriideans and cyanobacteria. The most investigated areas were: Ubatuba, São Sebastião, Santos and Cananéia. The recent surveys have a broader spatial coverage. The objectives of the studies have changed over the years from purely taxonomic to process-oriented investigations. Therefore, the longest species lists and most first records for the area were published before the 1980's and later publications, even those in which cell counts were performed, mention only the most abundant/frequent species. Electron microscopy was used for the first time in the present surveys, and new records include 38 diatoms, 42 dinoflagellates, 1 silicoflagellate, 1 ebriidean and 2 cyanobacteria. The use and interpretation of this species list require the perception of some constraints. It is not our role to question the identification made by other researchers. On the other hand, the ability to sample, analyze and identify species has evolved over the years and some considerations in this regard are presented.

Keywords: marine microalgae, inventory, diatoms, dinoflagellates.

RESUMO

O objetivo deste estudo é compilar o inventário de quase 100 anos de pesquisa sobre a composição de espécies do fitoplâncton do litoral do Estado de São Paulo, Brasil. O retrato atualizado da biodiversidade local é necessário para establecer um dignóstico para comparações futuras. Este tipo de informação encontra-se dispersa em antigas publicações e em material considerado como "literatura cinza" e requer atualização nomenclatural. Vinte e seis publicações foram consideradas neste estudo. O registro mais antigo é de 1913 (?) e o mais recente de 2002. Esta lista de espécies, compilada a partir de dados pretéritos, foi complementada com dados primários coletados entre agosto de 2004 e julho de 2006 nas zonas de arrebentação de 20 praias paulistas e em área de maricultura da praia da Cocanha em Caraguatatuba. A lista de espécies completa inclui 572 táxons: a maioria de diatomáceas (82%), seguidas por dinoflagelados (16%), com uma pequena contribuição de silicoflagelados, cocolitoforídeos, ebriideas e cianobactérias. As áreas mais estudadas foram: Ubatuba, São Sebastião, Santos e Cananéia. O levantamento atual tem uma cobertura espacial mais abrangente. Ao longo dos anos, os objetivos dos estudos pretéritos variaram desde puramente taxonômicos até investigações de aspectos funcionais do ecossistema. Desta forma, os inventários mais longos e a maioria dos primeiros registros foram publicados antes de 1980 e as publicações mais recentes fazem menção apenas a espécies mais abundantes/freqüentes. Microscopia eletrônica foi empregada pela primeira vez no levantamento atual e novos registros incluem 38 diatomáceas, 42 dinoflagelados, 1 silicoflagelado, 1 ebriidea e 2 cianobactérias. O uso e interpretação deste inventário exige cautela. Se por um lado, não é viável questionar a identificação feita por outros pesquisadores, por outro lado, a capacidade de amostrar, analisar e identificar espécies evoluiu ao longo do tempo. Algumas considerações sobre esta questão são apresentadas.

Palavras-chave: microalgas marinhas, inventário, diatomáceas, dinoflagelados.

Introduction

Phytoplankton studies include a variety of taxonomic groups (cyanobacteria, diatoms, dinoflagellates, silicoflagelates, coccolithophorids, and many other flagellates) that inhabit the water column. This is an artificial category, that is, the organisms are not phylogenetically related (Adl et al. 2005). Although these organisms are regarded as unicellular microalgae and most of them are indeed autotrophs, several species or even whole genera (e.g., the dinoflagellates Protoperidinium Bergh) are known to be heterotrophs (Steidinger & Tangen 1997). An extreme case is that of the ebriideans, Ebria tripartita (Schumann) Lemmermann and Hermesinum adriaticum Zacharias, which actually belong to the Phylum Sarcomastigophora (according to Lee et al. 1985 in Throndsen 1997); they are traditionally considered in phytoplankton counts mostly because their taxonomic status has changed over the years to be considered silicoflagellates (Drebes 1974) or dinoflagellates (Sournia 1986).

According to Sournia et al. (1991), marine phytoplankton of the world may include as many as 17 classes and an estimated number of 498 ± 15 genera and 3,910 ± 465 species. The authors recognize that taxonomy is a dynamic science and that these numbers were probably already underestimated at the time of their publication. A more recent source of change in our perception of biodiversity, especially in the protistan realm, is due to the introduction of immunochemical and molecular biological methods that can reveal intra- and infraspecific variations that went unnoticed before.

The objective of this study is to compile and make available the inventory of the phytoplankton species cited for the coast of the state of São Paulo, Brazil. As will be demonstrated, there is almost 100 years of research in the area, but this type of data (species lists) is scattered and in need of nomenclature updating. A state-of-the-art assessment of the biodiversity of the local phytoplankton is long needed to provide a baseline for future comparisons.

Material and Methods

This assessment was based on published information available in scientific journals as well as in the so-called "grey literature" (technical reports, academic thesis and dissertation, expanded abstracts from scientific events) for the coast of São Paulo. For this data set, the earliest sampling year is 1913 (?) and the most recent record reports on samples collected in 2002. The objectives, field and laboratory methods used in these surveys are summarized in Table 1 and will be discussed further below. The publications of Zimmerman, dated from 1913 to 1918, were combined as a sole record because there is no reference for sampling dates and, at times, the same article is published in two different issues.

This species checklist compiled from the literature was complemented with primary data collected between August 2004 and July 2006, using data from 2 different sampling schemes. Phytoplankton samples were taken monthly from the surf-zone of 20 beaches located along the coast (Figure 1). Theses samples were taken almost simultaneously (within 24 hours) by surface net hauls (20 µm-mesh). From June 2005 to May 2006, sampling was also carried out at the mussel mariculture located at the Cocanha Beach, in Caraguatatuba. In this case, vertical net hauls (from 3 m depth to surface, same mesh size) were taken monthly at 5 sites (insert of Figure 1). All samples were initially analyzed with the aid of the Utermöhl's settling chambers using a Nikon TS100 inverted microscope equipped with phase contrast. Specific methods for finer taxonomic study were applied for observation in light microscopy (LM, Olympus BX41 equipped with phase contrast and epifluorescence) and also scanning electron microscopy (SEM, LEO 1450VP Zeiss). For diatoms, it was necessary to clean the cells from the organic matter that obscures the structures of the frustules; for LM, permanent slides were prepared with a medium of high refractive index (Naphrax), whereas for SEM a drop of the cleaned material was air-dried on a cover slip that was then sputtered with gold (Hasle & Fryxell 1970). For armored dinoflagellates, observation of plate patterns in LM were done on wet mounts with the use of hypochlorite to separate plates and/or by the addition of the fluorochrome Calcofluor white (Fritz & Triemer 1985, Boltovskoy 1995); SEM study of the more resistant species was also possible. A few unarmored species were identified from live samples. This is still an ongoing research and the species list presented here should be considered as preliminary.

The complete species list is found in the ^Appendix. Nomenclature was updated to the best of our ability, based on a vast literature and the algae database provided by Guiry & Guiry (2008). The correct names of many taxa should still be regarded under scrutiny, as marked directly on the species list, either because we were unable to locate the validity of the name or the taxonomic status of a genus/species was considered unresolved, as will be illustrated further below. This difficulty is not unexpected, considering that some records are almost 100 years old and collections are not available to verify diagnostic characters. Synonyms were included, although restricted to citations found in the publications considered in this assessment. These shortcomings led to the choice of not adopting a classification system at present and the species list was thus organized in alphabetical order.

The publication of Oliveira (1980) was not taken into account because it dealt with epiphytic diatoms on Sargassum, although we do recognize that some species may be shaken off the thallus of the seaweed and can be, at times, detected in the water column. A wealth of publications that focused mostly on primary production and/or pigment concentrations are key to understand phytoplankton dynamics in the study area (e.g., Galvão 1978, Gaeta et al. 1990, Aidar et al. 1993, Gaeta et al. 1995, Lima 1998, Gaeta et al. 1999, Saldanha-Correa & Gianesella 2004, Barrera-Alba et al. 2008), but they were not included in this account because they did not provide information at the species level.

Results and Discussion

1. The species list in a historical perspective

Phytoplankton studies from the coast of the state of São Paulo date back to 1913 (Zimmerman, 1913). Twenty-six publications are considered in this assessment (Table 1). The species list includes 572taxa (^Appendix). The great majority of the species found are diatoms (82%), seconded by dinoflagellates (16%), and a minor contribution of silicoflagellates, coccolithophorids, ebriideans and cyanobacteria was also reported (Table 2). The most investigated areas were, from north to south: Ubatuba, São Sebastião, Santos and Cananéia (refer to Table 1 and names of municipalities on Figure 1). The recent surveys have a broader spatial coverage (refer to Figure 1).

The objectives of the published studies have changed over the years from purely taxonomic studies to process-oriented investigations. Therefore, the longest species lists and most first records for the area are published in the studies carried out before the 1980's (Figure 2) and later publications, even those in which cell counts were performed, mention only the most abundant/frequent species. New records for the coast of São Paulo state (present study: 2004-2006) includes 38 diatoms, 42 dinoflagellates, 1 silicoflagellate, 1 ebriidean and 2 cyanobacteria (^Appendix).

The larger contribution of diatoms and dinoflagellates is expected and is in accordance with the review of Sournia et al. (1991) that estimates numbers of species for the marine phytoplankton: diatoms (1365-1783), dinoflagellates (1424-1772), coccolithophorids (239-298), chlorophytes (106-121), prasinophytes (95-128), cryptophytes (56-73), euglenophytes (35-36), silicoflagellates (1-3), cyanobacteria (6-9), among others. Brazil (and the state of São Paulo) has a stronger tradition of diatomists, which explains our greater knowledge of diatom species composition (Figure 3). For the state of São Paulo, only the study of Sassi (1978) and the recent surveys made a special effort to augment our understanding of dinoflagellate species composition (Table 2; Figure 3). As a general rule, the identification of flagellates, including naked dinoflagellates, requires the study of live samples and/or electron microscopy, which is not routinely possible in many laboratories. We are still a long ways from grasping the true biodiversity of such taxonomic groups in Brazilian waters.

The most frequently cited species are listed in Table 3 and they are all diatoms commonly found in coastal waters (Hasle & Syvertsen 1997). Except for Phaeodactylum tricornutum Bohlin, Pseudo-nitzschia Hassal and Skeletonema costatum Greville, whose taxonomy will be discussed further below, the other 26 species can be readily identified in wet mounts with light microscopy.

The following taxa have been cited in the literature as bloom-forming species, some of them as potentially toxic (according to Hallegraeff et al. 2003, Fukuyo et al. 1990, Odebrecht et al. 2002, Moestrup 2004): the diatoms Asterionellopsis glacialis (Castracane) Round, Cerataulina pelagica (Cleve) Hendey, Coscinodiscus wailesii Gran & Angst, Cylindrotheca closterium (Ehrenberg) Lewin & Reimann, Guinardia delicatula (Cleve) Hasle, Leptocylindrus minimus Gran, Pseudo-nitzschia calliantha Lundholm, Moestrup & Hasle, Pseudo-nitzschia delicatissima (Cleve) Heiden, Pseudo-nitzschia fraudulenta (Cleve) Hasle, Pseudo-nitzschia multistriata (Takano) Takano, Pseudo-nitzschia pungens (Grunow ex Cleve) Hasle; the dinoflagellates Ceratium fusus (Ehrenberg) Dujardin, Ceratium hircus Schröder, Dinophysis acuminata Claparède & Lachmann, Dinophysis caudata Saville-Kent, Dinophysis rotundata Claparède & Lachmann, Dinophysis tripos Gourret, Noctiluca scintillans (Macartney) Kofoid et Swezy, Peridinium quinquecorne Abé, Prorocentrum micans Ehrenberg; the silicoflagellate Dictyocha fibula Ehrenberg; and the cyanobacteria Trichodesmium erythraeum Ehrenberg ex Gomont and Trichodesmium thiebautii Gomont ex Gomont. Although some of them have been recorded for many years, only A. glacialis has been implicated in patch formation on the surf-zone that has caused a negative effect to tourism (M.C. Villac, personal observation) and was possibly associated with a fishkill event in Itanhaém in 1978 (Zavala-Camin & Yamanaka 1980). The recent report of C. wailesii, a large size and thus conspicuous diatom, is in conformity with the contention of Fernandes et al. (2001) that this is indeed a recently introduced species to the Brazilian coast.

2. Interpreting the species list

The use and interpretation of this species list require the perception of some constraints. It is not our role to question the identification made by other researchers. On the other hand, the ability to sample, analyze and identify species has evolved over the years and some considerations in this regard are called for.

Some difficulties in updating nomenclature, for instance, are due to the fact that the genera of the nominate species have changed but the revision of all forms/varieties has not been carried out. The reader will find several examples of this case in the species list, such as:

Diploneis crabro Ehrenberg (= Navicula crabro) was updated,

BUT Navicula crabro var. multicostata (Grunow) Grunow was maintained;

Lyrella hennedyi (W. Smith) Stickle & Mann (= Navicula hennedyi W. Smith) was updated,

BUT Navicula hennedyi var. campechiana Peragallo and Navicula hennedyi var. clavata Cleve were maintained;

Pinnularia stauroptera (Grunov) Rabenhorst (= Navicula stauroptera) was updated,

BUT Navicula stauroptera var. parva (Ehrenberg) Grunow was maintained;

Psammodictyon panduriforme (Gregory) Mann (= Nitzschia panduriformis) was updated,

BUT Nitzschia panduriformis var. minor Gregory was maintained.

Other cases are even more difficult to resolve as Round et al. (1990; pg. 232) states: "genera in the order Biddulphiales is still in a state of flux. Amphipentas is possibly to be included within Amphitetras but a position in Stictodiscus also needs consideration". The genera Biddulphia Gray, Odontella Agardh and Triceratium Ehrenberg, which are often mentioned in the older literature, fall into this nomenclature/taxonomic problem.

Special taxonomic cases are those regarding the diatoms P. tricorcutum, S. costatum and the genus Pseudo-nitzschia. Frequently considered in the literature as cosmopolitan and opportunistic, S. costatum was the subject of a taxonomic review that revealed that the biodiversity of the genus at any given place is most likely underestimated and it may include more than one species among S. ardens Sarno & Zingone, S. dohrnii Sarno & Koistra, S. grethae Zingone & Sarno, S. grevillei Sarno & Zingone, S. japonicum Zingone & Sarno, S. marinoi Sarno & Zingone, S. menzelii Guillard, Carpenter & Reimann, S. potamus (Weber) Hasle, S. pseudocostatum Medlin, S. subsalsum (Cleve) Bethge and/or S. costatum itself (Sarno et al. 2007). Electron microscopy and/or molecular biology are required to study the biodiversity of Skeletonema species (Kooistra et al. 2008).

The record of Pseudo-nitzschia requires some explanation. Most reports for Brazilian waters follow the nomenclature suggested in Hasle (1965) that divides the species of the genus Nitzschia that form stepped colonies into two complexes: those cells whose widths are equal or smaller than 3 µm belong to the "delicatissima complex" and those wider than 3 µm belong to the "seriata complex". Alternatively, some publications actually refer just to the occurrence of N. delicatissima and/or N. seriata. All these can be considered questionable identifications because the methods of analysis used (counting by the settling technique with the inverted microscope) are not adequate for the definite identification, which requires electron microscopy. Therefore, all records were here combined into the two categories suggested by Hasle (1965) and the nomenclature updated to Pseudo-nitzshia (Hasle 1994). The present survey is making an effort to determine the biodiversity of this genus, especially because several species are neurotoxin producers, as mentioned above.

The frequent record of P. tricornutum is also troublesome because its minute size would necessarily require the use of electron microscopy to differentiate its fusiform form from other small pennate diatoms, a technique that was not used by any of the published studies considered in this assessment. The presence of the triradiate form (see Hasle & Syvertsen 1997, page 269) would certainly confirm the report of this species, but the studies in which P. tricornutum was found (refer to ^Appendix) did not make any reference to detailed morphology.

The listing of some species may raise some questioning in regard to ecological issues. This will be especially true for the oldest records from Zimmermann's publications. There is no information about the exact sampling date and the exact locations are not clear. There is mention of "Santos", "Port of Santos" and "Guaruja beach across from Island Santo Amaro", which is the city of Santos. We suspect that some of the samples might have been taken from places of strong freshwater influence, as indicated by the occurrence of the following genera: Amphicampa (Ehrenberg) Ralfs in Pritchard, Cymbella Agardh, Cystopleura Brébisson ex Kuntze, Dicladia Ehrenberg, Encyonema Kützing, Gomphonema Ehrenberg, Hantzschia Grunow, Melosira Agardh, Navicula Bory de Saint-Vincent, Nitzschia Hassall, Stauroneis Ehrenberg, Surirella Turpin. His species list also includes several genera that are usually epiphytic on marine plants or epipelic on sand or silt, such as Licmophora Agardh, Cocconeis Ehrenberg and Surirella Turpin. We also chose not to exclude the mention of Stictodiscus californicus Greville and Campyloneis curvirotunda Tempère et Brun that have been cited in the literature as fossil, nor Goniothecium gastridium Ehrenberg and Goniothecium hispidum Ehrenberg that have been considered as resting spores of Chaetoceros Ehrenberg (Round et al. 1990).

Conclusion

The composition and abundance of the phytoplankton of a certain region is certainly associated with the local hydrography. The southern portion of the Brazilian coast, where the state of São Paulo is located, is fairly well studied in terms of meso-scale circulation patterns and contribution of water masses on the continental shelf (Emilsson 1960, Matsuura 1986, Castro Filho & Miranda 1998). The studies considered in this assessment, however, took place in inshore areas where small-scale features should be taken into account. The contribution of warm and oligotrophic waters transported by the Brazil Current will have to be understood in association with different types of land-sources of freshwater, and corresponding levels of nutrient enrichment, coupled with various scenarios of local geomorphology. The northern area of the coast, between Ubatuba and Guarujá, is located in more sheltered areas of half-heart small bays with several points of minor freshwater contribution when compared with the much more conspicuous input of freshwater and nutrient enrichment that come from the metropolitan area of Santos, as well as the Cananéia estuarine system at the southernmost limit of the state (Lamparelli & Moura 1999). Nonethelesss, intrusions of the colder and nutrient-rich South Atlantic Central Water have been related to higher productivity at inshore areas of the northern portion of the coast, especially during the prevailing NE winds of summer months (Castro Filho et al. 1987, Aidar et al. 1993, Gaeta et al. 1995).

The species list provided at present is, therefore, a composite of a very broad spectrum of environmental conditions, dating back to those times of more pristine waters sampled by Zimmermann in the early 1900's. It is beyond the scope of this study to evaluate, case by case, the relationship between species composition and their possible environmental controls. Nevertheless, the results are structured in such a way as to allow the cross-reference between the information provided in Table 1 and the ^Appendix. A future user will be able to create a species list for a given location, appropriate for a specific need. The understanding of biodiversity and environmental conditions for a particular area of interest could thus result.

Acknowledgements

This work was funded by Biota-FAPESP to MC Villac, by a FAPESP TT3 fellowship to VAP Cabral-Noronha, and by a PIBIC/CNPq fellowship to TO Pinto. Field sampling for the beach monitoring program was supported by CETESB and the sampling at the mariculture farm received support from the Butantan Institute through a CAT-CEPID project and from the Mariculture Association of the Cocanha Beach. We are thankful for the suggestions of two anonymous reviewers.

Recebido em 28/04/08

Versão reformulada recebida em 29/08/08

Publicado em 12/09/08

Appendix

Appendix - Click to extend

Appendix - Click to extend

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Appendix

Appendix - Click to extend

Publication Dates

• Publication in this collection
  18 Dec 2008
• Date of issue
  Sept 2008

History

• Accepted
  12 Sept 2008
• Received
  28 Apr 2008
• Reviewed
  29 Aug 2008