ISSN 1809-127X (online edition) © 2011 Check List and Authors Chec List Open Access | Freely available at www.checklist.org.br Journal of species lists and distribution pecies S

of Plantae, aquatic, amphibian and marginal species, ists L Massaguaçu River Estuary, Caraguatatuba, São Paulo,

Brazil 1* 1 1 2 Jose Pedro N. Ribeiro 1 , Leandro K. Takao , Reginaldo S. Matsumoto , Catia Urbanetz and Maria Inês Salgueiro Lima 1 Universidade Federal de São Carlos, Departamento de Botânica, Laboratório de Sistemática e Ecologia Química. Rodovia Washington Luís, km 235. CEP 13565-905. São Carlos,[email protected] SP, Brasil. 2 Embrapa Pantanal. Rua 21 de Setembro, 1880, Caixa Postal 109. CEP 79320-900. Corumbá, MS, Brasil. * Corresponding author. E-mail: Abstract:

Estuaries are the buffer zones between river and ocean. Because they are under strong tidal influence, their flora must be able to cope with salinity and flooding stress. In the present study we combined results from two surveys we performed in the Massaguaçu River Estuary (23°37’20” S, 54°21’25” W), with the objective of providing a full inventory of its aquatic, amphibian, and marginal flora. We reported 102 species among 77 genera and 47 families, including six Pteridophyta species.

Introduction aestus arium flora from the Massaguaçu River Estuary, Caraguatatuba, Estuaries (from Latin : tide and : receptacle) Materialsstate of São Paulo,and Methods . are the buffer zones between river and ocean. Thus, they Study site are under strong tidal influence (Wolanski 2007). When river and ocean are permanently connected (regular estuaries), this influence happens continuously. However, Massaguaçu River Estuary (23°37’20” S, 54°21’25” W) it is common, particularly in tropical regions, estuaries in is an irregular estuary. Its sandbar breaches several times etwhich al. the ocean builds a sandbar (that breaches from time every year, with cycles that range from a few days to more to time) that seals their connection with a river (Miranda than one month (Figure 1). The duration of the connection 2002). In these cases, the ocean-river connection with the ocean also varies,af from one tidal cycle to more is intermittent (irregular estuaries) and tidal influence than two weeks. The estuary is located in a region with is limited. Regardless of the connection characteristics, humid tropical climate ( ), with mild winter, rain in all estuaries are environments closely related to tide cycles, months and no biological dry season (Koeppen 1948). and therefore, estuarine must be able to cope with The estuary left margin is a sand line that is now salinity and flooding. Furthermore, in coastal environments disturbed. This margin still presents riparian vegetation salt can reach plants and non-flooding soil through salt in almost all its extension. The right margin is better spray (Boyce 1954; Wells and Shunk 1938) and tidal preserved, and is a lowland Atlantic forest in different salinization of the aquifer (Werner and Lockington 2006) degrees of preservation. The right margin is L shaped so, even plants above the estuarine brackish water level (Figure 1 - white line), with the small leg exposed to the are exposed to salt stress. et al. ocean and the long leg protected from it by the sand line. In irregular estuaries, breaching cycles are frequently The estuary presents five major macrophytes banks unpredictable events (Costa 2003). This leads to (Figure 1 - Mb), with dense formations of both aquatic and an unpredictability of tidal influence, and therefore, to amphibian plants. The estuary is under crescent pressure an inconstancy of saline and flooding conditions. This from the growing nearby human neighborhoods. However, increases the importance of stochastic events in to the best of our knowledge, there is no history of main composition, and irregular estuaries are expected to direct disturbance in the last 30 years. The sandbar present several opportunistic amphibian species in breaching is a natural event, but artificial breaching is addition to their aquatic flora. becoming more often, and the effects of this practice on Plant zonation along et al. salinity and flooding gradients Datathe estuary collection flora are uncertain. is one of the main gaps in the knowledge et about al. tidal environments (Crain 2004), and irregular tropical estuaries are particularly poorly et al. studied (Costa et al. 2003). The species list in this work came from two surveys Furthermore,et al. as most studies regarding that matter focus that we performed in the estuary. The first focused on only on few species (Castillo 2000; Costa 2003; the riparian vegetation of the right margin. For that, we Emery 2001; Touchette, 2006), a full estuary species searched the margin collecting the closest (diameter inventory is rarely published. Therefore, there is a great of ≥ 5cm at 1.5m high) to the maximum water line level. In demand for species list in these environments. Here we the second, we surveyed the flora inside the estuary. We presentCheck a List species | Volume 7list | Issue of 2 aquatic, | 2011 amphibian, and marginal randomly placed 400 plots (5x5m, 25m²) in the five main133 Ribeiro et al. | Plantae, aquatic, amphibian and marginal species, Massaguaçu River Estuary, Brazil

Rhizophora mangle Laguncularia racemosa Avicennia macrophytes banks (80 per bank), and collected all species mainly characterizedSpartina by fewHibiscus ( Acrostichum L., (including Pteridophyta and rooted lianas) in the plot. et al. (L.) C.F. Gaertn., sp.) and Species were classified according to APG III (APG 2009). herbaceous ( sp., sp. and Voucher specimens were deposited in the Herbarium of sp.) species (Silva 2005). Thus, when compared to the Botanical Department, Federal University of São Carlos this very low species richness (Vannucci 2001), the Results(HUFSCar). and Discussion number of species of Massaguaçu River Estuary is strictly higher. The reasons for those differences are not completely We reported 102 species among 77 genera and 47 clear, and there is a great demand for studies regarding families, including six Pteridophyta species (Table 1, plant zonation and species inventories in tropical Figures 2-6). The richest Angiosperm families were estuaries. It has been proposed that environmentalet al. Cyperaceae (14 species), Fabaceae (9), (8), unpredictability and the wide variation in the hydrological (6), Onagraceae (5) and Melastomataceae, condition lead to a lack of stress etpersistence al. (Costa Myrtaceae and Polygonaceae (4). Thirty-nine families 2003). The unpredictability prevents the competitive were represented by trees or less species (Figure 7). As far balance to be reached (Russell 1985), and allows as we know the present work is the first species inventory species to occur in wide zones along the gradient (Baldwin for an irregular estuary in Brazil. and Mendelssohn 1998). The intermittent flooding stress Its flora seems to be similar to the flora of other allows riparian species to occur in the macrophyte banks, irregular estuaries we have visited in the same region. as several non-aquatic plants can cope with moderate However, to the best of our knowledge there are no studies sporadic flooding (Kozlowski 1997). Although we have not regarding that matter, and this information needs to be performed a formal sampling of the riparian herbaceous confirmed by formal studies. Regular estuaries in the flora, field observations support that the opposite is also same longitude usually present mangrove vegetation. true, and several macrophytes species can live in non- This vegetation is related to wide tide ranges, and is flooded conditions.

Figure 1.

Massaguaçu River Estuary regional location and aerial image. Mb= main macrophyte banks. White line = Riparian vegetation sampling path. Camera icons= approximate location where the photographs (Figure 2-6) were taken. Check List | Volume 7 | Issue 2 | 2011 134 Ribeiro et al. | Plantae, aquatic, amphibian and marginal species, Massaguaçu River Estuary, Brazil

Figure 4. Rhynchospora corymbosa Eleocharis interstincta Region Scleria away frommitis sandbar, with formationsScleria latifolia dominated by Figure 2. Crinum (L.) Britton,Tabebuia cassinoides (Vahl) americanum AnnonaRoem. and glabra Schult., CalophyllumP.J. Bergiusbrasiliense and Sw. In back Area near sandbar, with dense formations of plane, the arboreal compound, manly (Lam.) D.C., L. L. and Cambess.

Figure 3. Bacopa monnieri Area in an intermediaryEleocharis minima position in the estuary, justCrinum after americanumthe mouth closure, Acrostichum showing recently danaeifolium flooded formations of (L.) Pennell and Kunth.Annona In glabra back plane, Dalbergia Figure 5. ecastaphyllum L. and Mimosa bimucronata Langsd. and Fisch. In the back, tree species with several individuals of L,. Higher plots, subjected to sporadic flooding, with arboreal (L.) TAUB., and (DC.) Kuntze. stratum and several amphibian herbaceous species.

Figure 6.

General view of estuary right margin.

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Table 1.

Species inventory of aquatic, amphibian, and marginal flora of Massaguaçu River Estuary, Caraguatatuba, São Paulo, Brazil. H = herb; L = liana; T = tree; Mb = macrophyte banks; R = riparian, Both = both.

DIVISION/FAMILY SPECIES LIFE FORM LOCATION Blechnum serrulatum Pteridophyta meniscioides Blechnaceae Rich. H Mb Lygodium volubile (Willd.) C.Presl H Mb Serpocaulon triseriale Lygodiaceae Sw. H Mb Acrostichum danaeifolium Polypodiaceae (Sw.) A. R. H Mb Thelypteris interrupta Pteridaceae Langsd. and Fisch H Mb Thelypteridaceae (Willd.) K.Iwats. H Mb Sagittaria montevidensis Angiospermae Alternanthera philoxeroides Alismataceae Cham. and Schltdl. H Mb Crinum americanum Amaranthaceae (Mart.) Griseb. H Mb Tapirira guianensis Amaryllidaceae L. H Mb Annona glabra . Anacardiaceae Aubl. T R Guatteria australis Annonaceae L T Both Centella asiatica Annonaceae A. St.-Hil. T R Forsteronia Apiaceae (L.) Urb. H Mb Ilex brevicuspis Apocynaceae sp. L Mb Ilex Aquifoliaceae Reissek T R Ilex theezans Aquifoliaceae sp. T R Astrocaryum aculeatissimum Aquifoliaceae Mart. T R Syagrus romanzoffiana Arecaceae (Schott) Burret T R Eremanthus erythropappus Arecaceae (Cham.) Glassman T Both Mikania hastato-cordata Asteraceae (DC.) MacLeish T R Stifftia fruticosa Asteraceae Malme L Mb Berberis laurina Asteraceae (Velloso) D.J.N. Hind and Semir T R Tabebuia cassinoides Berberidaceae Thunb. T R Cordia curassavica Bignoniaceae (Lam.) DC. T Mb Aechmea distichantha Boraginaceae (Jacq.) Roem. and Schult. H R Calophyllum brasiliense Bromeliaceae Lem. H Mb Clusia criuva Calophyllaceae Cambess. T Both Garcinia gardneriana Clusiaceae Cambess. T Both Commelina schomburgkiana Clusiaceae (Planch.and Triana) Zappi T Both Ipomoea cairica Commelinaceae Klotzsch. H Mb Costus arabicus Convolvulaceae (L.) Sweet L Mb Calyptrocarya longifolia Costaceae L. H Mb Rhynchospora Cyperaceae (Rudge) Kunth H Mb Cyperus Cyperaceae cf. sp. H Mb Eleocharis flavescens Cyperaceae sp. H Mb Eleocharis interstincta Cyperaceae (Poir.) Urb. H Mb Eleocharis minima Cyperaceae (Vahl) Roem. and Schult. H Mb Eleocharis montana Cyperaceae Kunth H Mb Fuirena umbellata Cyperaceae (Kunth) Roem. and Schult. H Mb Rhynchospora holoschoenoides Cyperaceae Rottb. H Mb Rhynchospora corymbosa Cyperaceae cf. (Rich.) Herter H Mb Schoenoplectus californicus Cyperaceae (L.) Britton H Mb Scleria latifolia Cyperaceae (C.A. Mey.) Soják H Mb Scleria mitis Cyperaceae Sw. H Mb Cyperaceae P.J. Bergius H Mb Pera glabrata Cyperaceae undetermined H Mb Abarema brachystachya Euphorbiaceae (Schott) Poepp. ex Baill. T Both Andira fraxinifolia Fabaceae (DC.) Barneby and J.W. Grimes H Mb Dalbergia ecastaphyllum Fabaceae Benth. T R Fabaceae (L.) Taub. T Mb Check List | Volume 7 | Issue 2 | 2011 136 Ribeiro et al. | Plantae, aquatic, amphibian and marginal species, Massaguaçu River Estuary, Brazil

Table 1. Continued.

DIVISION/FAMILY Erythrina crista-galli SPECIES LIFE FORM LOCATION Inga minutula Fabaceae L. T R Machaerium uncinatum Fabaceae (Schery) T.S. Elias T R Mimosa bimucronata Fabaceae (Vell.) Benth. T R Mysanthus uleanus Fabaceae (DC.) Kuntze T R Zollernia ilicifolia Fabaceae (Harms) G.P. Lewis and A. Delgado T R Ocotea oppositifolia Fabaceae (Brongn.) Vogel T R Spigelia Lauraceae S. Yasuda T R Stigmaphyllon ciliatum Loganiaceae sp. H Mb Eriotheca pentaphylla Malpighiaceae (Lam.) A. Juss L Mb Hibiscus pernambucensis Malvaceae (Vell.) A. Robyns T Mb Clidemia bullosa Malvaceae Arruda T Mb Miconia cinnamomifolia Melastomataceae cf. DC. H Mb Miconia fallax Melastomataceae (DC.) Naudin T R Miconia prasina Melastomataceae DC. T R Nymphoides Melastomataceae (Sw.) DC. T R Eugenia umbelliflora Menyanthaceae sp. H Mb Eugenia uniflora Myrtaceae L. T Both Myrcia splendens Myrtaceae L. T Both Psidium cattleianum Myrtaceae (Sw.) DC. T R Guapira opposita Myrtaceae Sabine T R Brosimum guianense Nyctaginaceae (Vell.) Reitz T R Ficus enormis Moraceae Huber ex Ducke T R Nymphaea caerulea Moraceae cf. (Mart. ex Miq.) Mart. T R elegans Nymphaeaceae Savigny H Mb Ludwigia erecta Onagraceae (Cambess.) H. Hara H Mb Ludwigia filiformis Onagraceae (L.) H. Hara H Mb Onagraceae (Micheli) Ramanoorthy H Mb Onagraceae (G. Don) Excell H Mb Bacopa monnieri Onagraceae (Jacq.) P.H.Raven H Mb Acroceras zizanioides Plantaginaceae (L.) Wettst. H Mb Axonopus Poaceae (Kunth) Dandy H Mb mutica Poaceae sp. H Mb polystachya Poaceae (Forssk.) Stapf H Mb Hymenachne amplexicaulis Poaceae (Kunth) Hitchc. H Mb Poaceae (Rudge) Ness H Mb Panicum Poaceae sp.1 H Mb Paspalum Poaceae sp.2 H Mb Polygonum ferrugineum Poaceae sp. H Mb Polygonum hydropiperoides Polygonaceae Wedd. H Mb Polygonum meisnerianum Polygonaceae Michx. H Mb Coccoloba Polygonaceae Cham. and Schltdl. H Mb Myrsine coriacea Polygonaceae sp. T R Myrsine guianensis Primulaceae (Sw.) R. Br. ex Roem. and Schult. T Both Myrsine parvifolia Primulaceae (Aubl.) Kuntze T Both Myrsine umbellata Primulaceae A. DC. T Both Myrsine venosa Primulaceae (Mart.) Mez T Both Myrsine Primulaceae A. DC. T Both Tocoyena bullata Primulaceae sp. T Both Cupania oblongifolia Rubiaceae (Vell.) Mart. T Mb Typha domingensis Sapindaceae cf. Mart. T R Coussapoa microcarpa Typhaceae Pers. H Mb Urticaceae (Schott) Rizzini T Both

Check List | Volume 7 | Issue 2 | 2011 137 Ribeiro et al. | Plantae, aquatic, amphibian and marginal species, Massaguaçu River Estuary, Brazil

Figure 7.

Frequency histogram of families with number of Angiospermae species of aquatic, amphibian, and marginal flora of Massaguaçu River LiteratureEstuary, Caraguatatuba, Cited state of São Paulo, Brazil.

Botanical Miranda, L. B. d., B. M. d. Castro and b. Kjerfve. 2002. Principios de APG.Journal 2009. Anof the update Linnean of the Society Angiosperm Phylogeny Group classification oceanografia física de estuários. São Paulo: Edusp. 424 p. for the orders and families of flowering plants: APG III. Russell, P. J., T. K. ,Vegetatio M. J. Hutchings and T. J. Flows. 1985. Comparison 161: 105-121. of niche breadths and overlaps of halophytes on salt marshes of Baldwin, A. H. and I. A. Mendelssohn.Aquatic 1998. Botany Effects of salinity and water differing diversity. 61 (1): 171-178. level on coastal marshes: an experimentalEcological test of disturbance Monographs as a Silva, M. A.Acta B. D.,Botanica E. Bernini Brasilica and T. M. S. Carmo. 2005. Características catalyst for vegetation change. 61 (4): 255-268. estruturais de bosques de mangue do estuárioJuncus roemerianusdo rio São Mateus, ES, Boyce, S. G. 1954. The Salt Spray Community. 24 Brasil. 9 (3): 465-471. Journal of (1): 29-67. Spartina densiflora Touchette,Experimental B. W. 2006. Marine Salt Biology tolerance and Ecology in a brackish Castillo,S. maritima J. M., L. Fernández-Baco, E. M. Castellanos, C. J. Luqe, M. E. marsh: Spatial variations in plant water relations.Brazilian Journal Figueroa and A. J. Davy. 2000.Journal Lowe oflimits Ecology of and of Biology 337 (1): 1-12. in a Meditarranean salt marsh determined by different Vannucci, M. 2001. What is so special about mangroves? ecophysiological tolerances. 88: 801-812. 61: 599-603.Bulletin of Torrey Botanical Club Costa, C. S. B., J. C. Marangoni and A. M. G. JournalAzevedo. of Ecology2003. Plant zonation Wells, B. W. and I. V. Shunk. 1938. Salt spray: An important Factor in in an irregular flooded salt marshes: relative importance of stress Coastal Ecology. Journal of Hydrology 65 (7): 485-492. tolerance and biological interactions. 91: 951-965. Werner, A. D. and D. A. Lockington. 2006. Tidal impacts on riparian Crain, C. M., B. R.Ecology Silliman, S. L. Bertness and M. D. Bertness. 2004. Physical salinities near estuaries. 328 (3-4): 511-522. and biotic drivers of plant distribution across estuarine salinity Wolanski, E. 2007. Estuarine Ecohydrology. Amsterdam, Netherlands: gradients. 85 (9): 2539-2549. Elsevier. 168 p. Emery, N. C., P. J.Ecology Ewanchuk and M. D. Bertness. 2001. Competition and salt-mash plant zonation: stress tolerators may be dominant competitors. 82 (9): 2471-2485. Received: December 2010 Koeppen, W. 1948. Climatología: con un estudio de los climas de la tierra. Last Revised: January 2011 TreeCiudad physiology del Mexico, Monograph Mexico: Fondo de la Cultura Económica. 479 p. Accepted: February 2011 Kozlowski, T. T. 1997. Responses of woody plants to flooding and salinity. Published online: March 2011 1 (1): 1-29. Editorial responsibility: Frederico Augusto Guimarães Guilherme Check List | Volume 7 | Issue 2 | 2011 138