Fottea 11(1): 235–244, 2011 235

Biodiversity and temporal distribution of (Cyanoprokaryota) of an arid mangrove on the east coast of Baja California Sur, Mexico

Hilda Le ó n –Te j e r a 1,, Claudia J. Pé r e z –Es t r a d a 2, Gustavo Mo n t e j a n o 1 & Elisa Se r v i e r e –Za r a g o z a 2

1Department of Biology, Faculty of Sciences, Universidad Nacional Autónoma de Mexico, Apartado Postal 04360, Coyoacán, Mexico, D.F. 04510, Mexico. [email protected] 2Centro de Investigaciones Biológicas del Noroeste, S.C. (CIBNOR), Mar Bermejo 195, Col. Playa Palo de Santa Rita, La Paz, B.C.S. 23090, Mexico

Abstract: Arid mangroves constitute a particular biotope, with very extreme variations in ecological conditions, mainly temperature and salinity, condition that demand specific adaptations to successfully inhabit this ecosystem. Cyanoprokaryotes have not been well studied in Mexican coasts and this is the first study that contributes to the knowledge of the biodiversity of this group in an arid mangrove in Zacatecas estuary, Baja California Sur, Mexico. Samples of Avicennia germinans pneumatophores from Zacatecas estuary were collected between May 2005 and May 2006. The identification of the most representative Chroococcales produced 10 morphotypes, described mor- phologically and digitally registered for the first time for Mexico. We report species of Aphanocapsa, Chroococ- cus, Hydrococcus, Chamaecalyx, Dermocarpella and Xenococcus. Some taxa have been recorded in brackish or even marine environments from other regions, evidencing the wide geographical distribution and ecological adapt- ability of these organisms, but some others are probably new to science. Some species have a specific seasonal and vertical distribution on the pneumatophore but other have a more ample distribution. Aphanocapsa littoralis and cf. obliteratus are new records for benthic biotopes of Pacific Mexico; Dermocarpella cf. stellata is a new record for the Gulf of California.

Key words: Arid region, Chroococcales, New records, Mangrove, Mexico

Introduction ries nutrients vertically and horizontally (Tr a i n o r 1988). Mangrove forest, common along many Mangroves are one of the most biologically im- tropical and some subtropical coastal lagoons are portant ecosystems in the coastal areas, they play inhabited by a diverse cyanoprokaryote commu- important ecological functions taking part in the nity which reside on leaves, roots litter, live roots stabilization of sediments, act as a natural barriers and often form extensive mats on the surrounding for big waves produced by hurricanes, tsunamis, sediment (Po tt s 1979, 1980; Po tt s & Wh i tt o n etc., are an important source of nutrients, home to 1980; Sh e r i d a n 1991; Ph i ll i p s et al. 1994, 1996). a large number of species of flora and associated Also, many of these communities are capable of o l e d o o ff m a n n fauna, and forming areas of breeding, rearing, N2 fixation (T et al. 1995; H 1999). feeding, growth and protection from predators for There have been several studies in different parts a great variety of organisms (Fl o r e s –Ve r d u g o of the world that describe epiphytic algal commu- 1990; Da w e s 1998; Ma n n 2000). nities on pneumatophores, however the cyano- Furthermore, it is one of the most pro- prokaryotes from Eastern Pacific mangroves have ductive ecosystems in the world, functioning as received little attention and only few species have natural traps of organic matter. Their productivity been reported, mainly from order Oscillatoriales values vary with the type of primary producers (Bu r k h o l d e r & Al m o d o v a r 1973; Ba s h a n et al. (mangroves, microalgae and macroalgae) found in 1988; Ro d r i g u e z & St o n e r 1990; Ph i ll i p s et al. this ecosystems, the time of year and water physi- 1994, 1996; To l e d o e t a l . 1995a; Br a n c o et al. cochemical characteristics which depend in turn 1996; La u r s e n & Ki n g 2000; No g u e i r a & Fe r r e i - on the water circulation patterns, since this car- r a –Co r r e i a 2001; Te j a d a –Ri v a s 2002; Ba r r i o s et 236 Le ó n –Te j e r a et al.: Chroococcales of an arid mangrove

al. 2003; Ba o s –Es t u p i ñ a n 2007; Pe ñ a –Sa l a m a n - developed, but studies that focus specifically on c a 2008; Cr u z –Ma d r i d 2010). mangroves are scarce. To l e d o et al. (1995a) de- In Mexico, there is a lack of knowledge on coast- termined the vertical zonation of cyanoprokary- al Cyanoprokaryotes. In recent years, a more otes on pneumatophores of Avicenia germinans detailed and comprehensive study of marine, (L.) St e a r n L. in Bahia Balandra, Baja Cali- mainly epiphytic and epilithic Cyanoprokaryote fornia Sur, Mexico finding that the bottom part, populations (Le ó n –Te j e r a & Mo n t e j a n o 2000; close to the sediment was colonized mainly by Mo n t e j a n o & Le ó n –Te j e r a 2002; Le ó n –Te j e r a non–heterocystous, filamentous cyanoprokary- et al. 2003; Le ó n –Te j e r a et al. 2005) has been otes resembling Lyngbya sp. and Oscillatoria sp.;

Fig. 1. Map of study area, showing location of Zacatecas estuary in Baja California Sur, Mexico, AG: Avicenia germinans fringe mangrove. Fottea 11(1): 235–244, 2011 237 the central zone mainly by filaments resembling pneumatophores were washed with fresh water to re- Microcoleus sp. and the upper part by colonies move sediment and organic matter. Conspicuous cy- resembling Aphanothece sp. mixed with indeter- anoprokaryotes growths were scraped with a bisturi, and semi–permanent slides in glycerin gel were made. minate filamentous cyanoprokaryotes. Ho l g u i n et al. (1999) inoculated experimentally mangrove Observations, measurements and micrographs were made with an Olympus BX51 microscope and Sigma seedlings with Microcoleus sp. and demonstrated Scan Pro 5 software. Ko m á r e k & An a g n o s t i d i s (1998) that the mangrove assimilate the nitrogen fixed system was used for the systematic of Chroococca- by Microcoleus sp. (Ba s h a n et al. 1988). In this les, Se t c h e ll & Ga r d n e r (1924) and Gu i r y & Gu i r y biotope, the main N2 fixers were cyanoprokary- (2010) for macroalgae. otes (To l e d o et al. 1995b), implying that interac- tion of cyanoprokaryotes and mangrove seedlings is mutually beneficial and suggests the use of the Results first as inoculants for mangrove reforestation and rehabilitation. We present the first report and morphological de- This paper provides information on biodiversity scription of 10 species of chroococcalean cyano- of cyanoprokaryotes of the most conspicuous prokaryotes from a Mexican arid mangrove. They populations of order Chroococcales that grow on belong to 6 families of the order Chroococcales: Avicennia germinans pneumatophores from Za- Merismopediaceae, Chroococcaceae, Hydrococ- catecas estuary, Baja California Sur, Mexico, an caceae, Chamaesiphonaceae, Dermocarpellaceae arid mangrove located in the southwestern Gulf of and Xenocococcaceae and represent the first re- California. Chroococcaleans are of special inter- cords for these species populations for the Gulf est because several species had not been report- of California. Nostocales and Oscillatoriales de- ed since Se t c h e ll & Ga r d n e r (1919, 1924) and scriptions will be presented elsewhere. Ga r d n e r (1918a, b) described them for the Pacific A detailed morphological description with Coast of North America and Gulf of California. data on spatial and temporal distribution on pneu- Zacatecas estuary represents the most northern matophores is provided for the populations that mangrove distribution in the eastern Pacific; in a were most conspicuous and presented different Gulf of California arid zone which does not have stages of their life cycle. a constant supply of fresh water and rainfall. In this site, mangrove grow under suboptimal con- ditions, in strictly tidal saltwater and their com- munities are far shorter and less extensive than in other parts of the tropics (Wh i t m o r e et al. 2005). Family Merismopediaceae El e n k i n 1933 Subfamily Merismopedioideae

Materials and Methods Aphanocapsa littoralis (Ha n s g i r g ) Ko m á r e k et Anagnostidis 1995. (Fig. 2) Zacatecas estuary (24°10.359’ N; 110°26.080 W) is lo- Colonies obvovoidal, pseudospherical to irregu- cated in the Ensenada de La Paz, Baja California Sur, lar shape, formed by 30 or more cells contained Mexico (Fig. 1). It occupies approximately 17 ha of in a sheath. Sheath homogeneous, hyaline, dif- mangrove forest (Rhizophora mangle L., Laguncularia fluent, up to 55 μm in diameter, with an irregular racemosa L. Ga e r t n . and Avicennia germinans L.), and usually diffuse margin. Sometimes subcolo- and have a main flow tidal channel of 1.3 Km long nies formed by 4 or more cells are found within (Za m o r a n o obs. pers.). Tidal regime was semidiurnal with an average tidal range 1.02 m and 1.74 m ampli- the main colony. Cells light green to blue–green, tude. ovoid to spherical, 1–3.8 × 1.3–2.7 μm length/ During samplings, temperature ranged from wide (l/w), with a light centroplasm. Cells with 17.45 to 32.19 ºC and salinity from 38.12 to 43.08 individual hyaline sheaths, but sometimes not evi- UPS, with almost no rain throughout the year, clearly dent; length/wide 1.2–1.7 μm. Cells divide by bi- classifying it as an arid type of mangrove. nary fission in 3 planes, with daughter cells grow- In Zacatecas estuary pneumatophore samples ing to parental cell size before division. were obtained along Avicennia germinans fringe from Similar to A. littoralis (Ha n s g i r g ) Ko m á r e k et May 2005 to May 2006 (Fig. 1). Two pneumatophores An a g n o s t i d i s , sensu Cr i s p i n o and Sa n t ´An n a were collected for each sample date and these were (2006) for Brazil, but cells are not as aggregat- fixed in 4% formaldehyde in sea water at the site. The 238 Le ó n –Te j e r a et al.: Chroococcales of an arid mangrove

ed as described by Ko m á r e k and An a g n o s t i d i s Chroococcus sp. 1 (Fig. 5) (1998); similar size to A. concharum (Ha n s g i r g ), Colonies of 1–2 cells with both individual and but it is not epizoic. colonial sheath hyaline and firm. Cells brownish Reported for Mediterranean coasts, France, with slightly granulated cytoplasm, ovoid to pyri- Norway, Baltic Sea and probably cosmopolite. form 18–20 × 10–14 μm in diameter, with sheath First report for benthic biotopes of Pacific Mex- 20–28 × 13–17 μm. Cells divide by binary fission ico. mainly in 2 planes. It differs from the latter species by its much Occurrence: Found throughout all the year, from longer cell size and different color. May 2005 to May 2006 near roots as well as in medium part of pneumatophores. Occurrence: It was found throughout the year, from May 2005 to May 2006, growing on the mu- Aphanocapsa sp. (Fig. 3) cilage intermingled with Calothrix sp. and other Colonies ovoid in shape, formed by a few, widely coccal algae in different parts of the pneumato- separated cells. Colonial sheath homogeneous, phore and epiphytic on Rhizoclonium sp. hyaline to yellowish, firm, up to 70 μm in diam- eter, with a regular margin. Cells brownish to yel- Chrococcus sp. 2 (Fig. 6) lowish, ovoid to subspherical, 6–7 × 5–6 μm in Colonies 64 x 45 μm in diameter formed by a diameter, with a light centroplasm. Cells with evi- nested arrangement of smaller colonies 6–11 × dent individual sheaths; length/wide 1.1–1.2 μm. 7–9 μm l/w. Daughter colonies formed by 1–8 Cells divide by binary fission in 2 planes, with cells resulting from three plane divisions. Ma- daughter cells growing to parental cell size before ture cells, 5–6 × 3–6 μm with blue–green, homo- division. geneous cytoplasm. Small colonies sheath firm, We distinguish this morphotype from A. littoralis hyaline, whereas larger colony sheath is diffluent because of a lack of subcolonies, as well as a larg- with many particles and other embed- er cell size, color and wider cell to cell distance. ded. Cells divide before reaching the original cell Occurrence: Reported for July and November size. 2005, as well as January 2006, growing near root pneumatophores. Occurrence: Found throughout all the year, from May 2005 to May 2006, in different parts of the Family Chroococcaceae Nä g e l i 1849 pneumatophore, but with low frequency.

Chroococcus cf. obliteratus Ri c h t e r 1886. (Fig. 4) Family Hydrococcaceae Kü t z i n g 1843 Colonies of 2–4 cells hemispherical to a slightly rounded prism in shape, 6–8 μm in diameter. Cells Hydrococcus sp. (Fig. 7) blue–green to slightly yellowish, without cyto- Colonies 25 μm in diameter, formed by the aligned plasmic granulations, separated and surrounded arrangement of erect pseudofilaments, forming by an ample hyaline sheath, 2–3 × 1–1.9 μm in discs that grow radially. Pseudofilaments 3–4 diameter. Colony sheath not lamellate, firm inside cells high, perpendicular to the substrate. In su- and diffluent outside. Reproduction by regular bi- perior sight only discs are perceived. Cells mostly nary fission in 3 planes. cylindrical to cubical in shape and apical ones It differs from Ko m á r e k and An a g n o s t i d i s hemispherical to irregular, with homogeneous (1998) description in the presence of a defined co- blue–green cytoplasm, 1–2 × 1–1.2 μm long/wide lonial sheath and shorter cell size. Reported previ- without sheath. Cell sheath hyaline, evident, 0.2 ously for brackish and freshwater biotopes, possi- to 0.7 μm wide. bly cosmopolite. First report for benthic biotopes Not very well known group, with 4 spe- of Pacific Mexico. cies described. The three freshwater and only one marine species: H. marinus Gr u n o w have cells Occurrence: Found throughout all the year, from several (up to 4–5) times larger. Very different in May 2005 to May 2006, on the mucilage that cov- biotope, general colony aspect, cell size and mor- ers different parts of the pneumatophores and epi- phology from descriptions and drawings of spe- phytic on Rhizoclonium sp. cies previously described, therefore it is probably Fottea 11(1): 235–244, 2011 239

Fig. 2. Aphanocapsa littoralis (Ha n s g i r g ) Ko m á r e k et An a g n o s t i d i s 1995. Fig. 3. Aphanocapsa sp. Fig. 4. Chroococcus cf. obliteratus Ri c h t e r 1886. Fig. 5. Chroococcus sp. 1. Fig. 6. Chrococcus sp. 2. Scale bar 10 mm. a new species. When undivided, the cell has maze shape; some- times basal part is slightly thinned upwards and Occurrence: Found in October, November, 2005 subsequently widens towards to the top. Initially and May 2006, not close to pneumatophore roots cell divides parallel to the substrate 1–3 times on Rhizoclonium sp. producing 2–4 cells lengthwise oriented, and later perpendicular and irregular division planes occur, generating 6–8 exocytes. Family Chamaesiphonaceae Bo r z ì 1882 Similar in cell size to Ch. leibeiniae (Re- i n s c h ) Ko m á r e k et An a g n o s t i d i s , but cell shape Chamaecalyx sp. (Fig. 8) is different and length/width reason is larger. Ch. Heteropolar cell pyriform or maze shaped, iso- algarvensis (Ar d r é ) Ko m á r e k et An a g n o s t i d i s is lated or in small groups. Mother cell blue–green, different as it has much shorter cell size, is red with very granulose cytoplasm, up to 30 μm long and with many exocytes. Probably an undescribed with a firm and hyaline sheath, adhered to the species. substrate by a narrower base. Apical part 11–13 Species of this genus are reported for the μm in diameter and basal part 6.7 to 9.2 μm wide. Mediterranean sea, both sides of Atlantic and also 240 Le ó n –Te j e r a et al.: Chroococcales of an arid mangrove

Fig. 7. Hydrococcus sp. Figs. 8. Chamaecalyx sp. Fig. 9. Dermocarpella cf. stellata Mo n t e j a n o et Le ó n 2000. Fig. 10. Xeno- coccus cf. chaetomorphae Se t c h e ll et Ga r d n e r 1918a. Fig. 11. Xenococcus sp. Scale bar 10 mm. for the Pacific and Indic oceans. sheath. Undivided cells have a dome shape and are 9.7–11.8 μm in wider diameter and 7.5–10.5 Occurrence: Found throughout all the year, from μm in height. Sheath 12.8– 1.7 μm in diameter May 2005 to May 2006, but more frequent in au- and 9.7 a 15.2 μm in height. Basal cell is 3–4.6 μm tumn (October 2005) and winter (January 2006), high and the apical one is 3.2–5.6 μm high. Some on Bostrychia sp. and Rhizoclonium sp., in differ- cells sometimes present a dark spot and an apical ent parts of the pneumatophore; protuberance called “papilla” that also is seen in the sheath. Sometimes the cell divides parallel to Family Dermocarpellaceae Gi n s b u r g –Ar d r é the substrate. No baeocytes were observed. It is ex Ch r i s t e n s e n 1980 similar to the species description (Le ó n –Te j e r a & Mo n t e j a n o 2000), but some cells are slightly Dermocarpella cf. stellata Mo n t e j a n o et Le ó n – larger. First report for benthic biotopes of the Gulf Te j e r a 2000. (Fig. 9) of California. It is one of the six described spe- Hemispheric cell with a thick, firm, hyaline cies for the genus, and one of two reported for Fottea 11(1): 235–244, 2011 241

Mexico´s tropical Pacific, therefore considering sheath ruptures probably through gelatinization. its small size, probably it is more common than it Probably a new species. is reported in tropical marine biotopes. Occurrence: It grows on mucilage that covers part Occurrence: It was found growing as epiphyte on of the pneumatophore, near the roots. Found in Boodleopsis sp., Rhizoclonium sp., as well as on November 2005. the pneumatophore cortex, next to the roots. It was relatively frequent in November 2005. Discussion Family Xenococcaceae Er c e g o v i ć 1932 This study is the first one in the area and in this Xenococcus cf. chaetomorphae Se t c h e l l et particular biotope that describes in detail local Ga r d n e r in Ga r d n e r 1918a. (Fig. 10) cyanoprocaryote populations. Even though the Colony formed by subspherical to ovoid cells that results concern only the most representative mor- can develop a polyhedral or rhomboid shape when photypes found on the pneumatophores, results compressed by neighboring cells in the middle of obtained show a considerable number of new the colony. Cells with blue–green to brownish records for the Gulf of California and probably granulose cytoplasm 9–17.5 × 5–16 μm in diam- some will be later characterized as new species to eter. Sheaths very evident, hyaline to yellowish, science, but more detailed studies are necessary to firm, 1.5–2.2 μm wide. Some cells show a dark confirm this. spot near the cell wall. No baeocytes observed. Considering reports from other Latin Reported for Pacific USA and Southeast America mangrove studies such as Br a n c o et al. Asia. It is considered by some authors as a taxo- (1996), it is evident that Chroococcales constitute nomic synonym of Dermocarpa chaetomorphae an important element of this type of biotope but (Se t c h e ll et Ga r d n e r ) P.C. Si l v a , however Der- there are geographical differences at the species mocarpa is no longer considered as a valid ge- and even generic composition. For example, we nus. share with Br a n c o et al. (1996) only genus Xeno- Similar to X. pyriformis Se t c h e ll et Ga r d - coccus and Chroococcus, but with different spe- n e r but with slightly larger cells and different cies. In the case of No g u e i r a & Fe r r e i r a –Co r r e i a colony and cell shape. It differs from X. gaditanus (2001), we share only genus Xenococcus. Pacific Go n z á l e z in colony disposition, division pattern Mexico marine algae studies deal mainly with and its epiphytic versus epizoic habit. macroalgae, those on mangroves are few and most A previous report for genus Xenococcus, X. of them don’t include descriptions. The compari- kernerii reported by Me n d o z a –Go n z á l e z & Ma- son with local studies reveals a different composi- t e o –Ci d (1985) for the Pacific of Baja California, tion, probably derived from being just a few and actually is not a valid species. all of them non taxonomic studies. For the Pacific coast of Baja California Occurrence: It was found on May and November there are very few studies dealing with chroococ- 2005. It grows on mucilage that covers part of the cales, Me n d o z a –Go n z á l e z & Ma t e o –Ci d (1985) pneumatophore, near the roots. report Dermocarpa prasina (Re i n s c h ) Bo r n e t , Xenococcus kerneri Ha n s g . and Chroococcus tur- gidus (Kü t z i n g ) Na g e l i but Dermocarpa is not a Xenococcus sp. (Fig. 11) valid genus and X. kerneri, that actually belongs Colony formed by an agglomeration of contiguous to genus Xenotholos, and Ch. turgidus that ac- cells of different sizes. Cells heteropolar with a cording to Ko m á r e k & An a g n o s t i d i s (1998) are pyriform or droplet shape and a very narrow base, found mainly in continental waters, so probably covered by an individual hyaline evident sheath. were misidentified. Concerning Gulf of California Cells up to 30 x 15 μm l/w with cytoplasm blue– studies, we do not share any genus or species with green, very granulose and frequently with a dark those of Ba s h a n et al. (1988) and To l e d o et al. spot near the cell wall, Cells divide by sequential (1995a) as they report only one Chroococcalean, binary division originating cells of different sizes an Aphanothece morphotype, and with Ló p e z – up to the smallest: blue–green spherical baeocytes Co r t é s (1990) also we do not share any species 1.8–2.2 μm in diameter. Baeocyte containing as his marine reports are mainly from peculiar 242 Le ó n –Te j e r a et al.: Chroococcales of an arid mangrove biotopes such as intertidal microbial mats and restricted area in Mexico and are specially distrib- shrimp ponds. uted in the Gulf of California, therefore it is ex- Previous non taxonomic studies performed pected that further studies will increase the inven- nearby (Balandra mangroves by To l e d o et al. tory as well as new records of cyanoprokaryotes, 1995a) showed a particular vertical distribution both for the region and this particular biotope. where members of Oscillatoriales colonized main- ly parts closer to the sediments and central parts, whereas upper parts were covered by coccal cy- Acknowledgements anobacteria such as Aphanothece. In this study we This study was funded by CIBNOR–PAC–Biodiversi- didn´t find this type of evidence. Even though we dad del noroeste de Mexico: problemática, usos y con- didn´t include Oscillatoriales in our study, concern- servación: Estudio integral de los manglares de Baja ing the Chroococcales as a group, we didn´t find California Sur and DGAPA–UNAM–IN221410 pro- a common pattern in their vertical distribution. At ject. Thanks to Dr. Amaury Cordero Tapia and M. en C. Ernesto Goytortua Bores for the facilities provided species levels, however, some were found mainly for observation of biological material at the Olympus in a particular area such as near the roots but oth- BX51 microscope, Alejandra Mazariegos–Villarreal, ers were found throughout all the pneumatophore, Alma Rivera Camacho, Mabilia Urquidi and Juan José such as Chamaecalyx sp. and Chroococcus spp. Ramírez–Rosas for collection of samples, Mónica Per- All of the reported species were epiphytic either alta for editing the photographs and plates; Jesus Al- directly on the Avicennia germinans cortex, or on fredo Díaz Sánchez –INEGI for the map, Dr. Carlos H. Rhizoclonium sp., Boodleopsis sp. or Bostrychia Lechuga Deveze and Dr. Renato Mendoza for informa- sp. that were also mangrove epiphytes. Concern- tion about physicochemical parameters of Zacatecas ing temporal distribution, each species also had a mangrove area. different pattern; some like Chroococcus sp2 had an ample temporal presence whereas others such References as Dermocarpella cf. stellata were registered only for a certain season. Ba o s –Es t u p i ñ a n , R.A. & Ve l a s c o , S.M. (2007): Algas It is probable that the spatial and temporal asociadas a un manglar en el Pacifico Colom- distribution of several morphotypes is underesti- biano. Municipio de Buanventura – Valle de mated due sometimes to the difficulties obtaining Cauca. – Rev. Biotec. Sec. Agropec. Inds. 5: representatives of different stages in species with 84–89. complex life cycles that could allow obtaining a Ba r r i o s , J.E., Má r q u e z , B. & Ji m é n e z , M. (2003): clear taxonomic identification. Macroalgas asociadas a Rhizophora mangle L. Pristine mangroves may present higher en el Golfo de Santa Fe, Estado de Sucre, Ve- nezuela. – Bull. Inst. Ocenogr. Venezuela Univ. richness that perturbed ones (Sj o l i n g et al. 2005). Oriente. 42: 37–45. In this case, Zacatecas mangrove can be consid- Ba s h a n , Y., Pu e n t e , M.E. & My r o l d , D.D. (1988): ered a fairly pristine one, but the inventory is not In vitro transfer of fixed nitrogen from diazot- complete and there are nonequivalent taxonomic rophic to black mangrove seed- studies in the region to compare, therefore more lings. – Microbiol. Ecol. 26: 165–170. intensive and extensive studies in the area are Br a n c o , L.H.Z., Sa n t ´An n a , C.L., Az e v e d o , M.T.P. needed to confirm that idea. Besides, we want to & So r m u s , L. (1996): Cyanophyte flora from stress that as Su n d a r a r a m a n et al. (2007) remark, Cardoso Island mangroves, São Paulo State, studies on cyanoprokaryotes associated with man- Brazil. 1. 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