Check List 8(4): 832–838, 2012 © 2012 Check List and Authors Chec List ISSN 1809-127X (available at www.checklist.org.br) Journal of species lists and distribution pecies

S remnant in southeastern Brazil

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Floristic composition of a freshwater * swamp forest ists L Júlio H. Ribeiro Magalhães and Rita C. S. Maimoni-Rodella Botucatu, SP, Brazil. Universidade Estadual Paulista,[email protected] Instituto de Biociências, Departamento de Botânica. Distrito de Rubião Júnior. Caixa Postal 510, CEP 18618-000.

* Corresponding author. E-mail: Abstract:

The floristic composition in a freshwater swamp forest remnant located in the municipality of Botucatu, São Paulo state, Brazil, was studied. Only Angiosperms were collected in the area by means of random walks. A total of 92 species withwere aregistered. continuous The canopy families and with an inferior greater tree species layer richness composed were: mainly Orchidaceae by individuals (17 species), of Euterpe Rubiaceae edulis Mart.. (8) and A comparison Myrtaceae among(5). The the arboreal angiosperms component of the was study predominant. area and those The profile of ten swampdiagram forests of the vegetationin São Paulo showed state suggests a well-defined that the stratification, geographic

position and other ecologic peculiarities of these forests, besides soil flooding, are factors that can influence their similarity concerning the floristic composition.

Introduction municipality covers an area of 1495 km2, and has three Among the several vegetation formations found in distinct physiographic regions: one located in the area Brazil, the freshwater swamp forests are very peculiar called Peripheral Depression, with altitudes ranging from 400 to 600 meters, an intermediate region (or transition zone) composed by a slope, and one located at the top coverand occur a quite in permanently limited area, floodedconsidering soil. Thesethe entire forests country have of the slope, called “Cuesta” region, which altitude varies (Marquescharacteristic et al . structure 2003). The and swamp floristic forests composition, are composed and from 700 to 900 meters (Castro 1966). In the latter region lies the study area, which is surrounded by pastures and by species that occur in confined areas and this make the the points with higher topography, and Hydromorphic environmentalpopulations more factors, vulnerable like water to extinction stress, select in the species short alluvialold fields, soil with in the soil lower classified points as(Comissão Oxisol, sandy de Solos phase, 1960). in whichterm (Rodrigues form large populations,and Leitão-Filho resulting 2001). in theIn these occurrence areas, The sample area is located in a slight slope between 853 of lower species diversity (Toniato et al. 1998; Ivanauskas and 862 meters of altitude, where the soil is constantly et al. 1997; Costa et al. 1997). wet due to the upwelling of water-holes and the intake The protection of swamp forests is highly important, of water from a nearby stream. These features allow the considering that they are so essential to the ecological balance, being generally related to the maintenance of springs and other water bodies. Studies on reforestation 2001).classification of the vegetation as a freshwater swamp and dynamics of fragmented vegetation areas depend forestThe permanently climate of the flooded region (Rodrigues is Cfa according and Leitão-Filho to Koeppen on data provided by surveys and ecological evaluations made at different times, which can provide information on the dynamic of ecological changes in remnants of theclassification, hottest month that is,with warm an average temperate temperature (mesothermal) of 23.1°C, wet, natural vegetation (Kronka et al. 2005). andas determined July is the coldest by Cunha month and with Martins an average (2009). temperature February is of 17.1°C. The highest average rainfall generally occurs to provide a check list of the Angiosperms present in a in January and the lowest generally occurs in August. freshwaterConsidering swamp this, forest a floristic remnant, inventory in the wasmunicipality performed of The average annual temperature and precipitation, Botucatu, central-west region of São Paulo state, Brazil. considering a 36-year period (1971 to 2006) were 20.3°C This study was performed aiming to add information to and 1428.4 mm, respectively (Cunha and Martins 2009). in relation to the non-arboreal species, which are less well-knownthe knowledge than of the the arboreal swamp componentsforests floristic, of the especially studied The floristic survey was carried out from November vegetation. species2009 to preferably October in 2010 reproductive on a bi-monthly phase, present basis in in that an approximately 1 ha area of forest. All the Angiosperm Materials and Methods The studied swamp forest remnant is located at collection,area, were where collected the voucher and identified specimens using were specialized deposited coordinates 22°52’52” S and 48°29’32” W, in the District (“Irinaliterature Delanova and comparison Gemtchújnicov” with the Herbarium, Herbarium Botucatu BOTU west region of São Paulo State, southeastern Brazil. The system was that recommended by the Angiosperm of Rubião Junior, Botucatu Municipality, at the central- Biosciences Institute, UNESP). The adopted classification

832 Magalhães and Maimoni-Rodella | Floristics of a freshwater swamp in Brazil

Phylogeny Group III (APG III 2009). The plants habits et al. (2001). There are also similarities in relation to some genera of the non-arboreal species among these surveys but the species occurred only in one location. were defined according to the descriptions found in delimitedGonçalves andand allLorenzi the woody (2007). plants with stem perimeter the non-arboreal species in swamp forests may also be at breastInside height the sampled equal or superior area a 30 to 12 x 5 cm m were transect recorded was peculiarThis seems but tothe indicate scarcity that of data the is floristic an obstacle composition to further of considerations. according to Goldsmith et al. (1986). and drawn, in order to prepare a profile diagram, Calophyllum brasiliense, Protium spruceanum, Cedrela study area with 11 other surveys found in the literature, odorataAccording, Dendropanax to Teixeira cuneatus and Assis, Magnolia (2005) ovata the ,species Styrax performedAiming previously to estimate in the swamp floristic forests similarity located ofin São the pohlii and Tapirira guianensis, all together, constitute an arboreal components of the vegetation was elaborated to the swamp forests of the upcountry of the São Paulo state. Paulo state, a presence/absence matrix including only the important group that defines a similar structure among species that concentrate many individuals in the total calculate the Jaccard similarity index (JSI) according to community.These forests Among are characterized these seven by species, the existence only Cedrela of few algorithmMueller-Dombois for the anddendrogram Ellenberg preparation (1974) and (Sneath to perform and odorata was not found in the Botucatu swamp forest. Sokala cluster 1973). analysis using this Index and the UPGMA Calophyllum brasiliense, Dendropanax cuneatus, Magnolia ovata, Styrax pohlii and Tapirira guianensis occurred Results and Discussion in the swamp forest in Botucatu, and also were present A total of 92 species of angiosperms were collected in other 11 surveys performed in swamp forests in the upcountry of the São Paulo state (Table 2). Despite the fact that these swamp forests possess and identified at least at family level. Among these, 68 a peculiar group of arboreal species, the comparison were identified at the species level, seven had specific identification to be confirmed and 17 species were wereidentified represented only to genus by larger level numbers (Table 1). of In species, this inventory 17 and among different surveys (Figure 1) evidences that in 47 families were sampled and Orchidaceae and Rubiaceae (JSI)some cases can bethere considered is a low floristic low, according similarity, toconsidering Mueller- that the values obtained for the Jaccard similarity index totaleight ofrespectively. species, the In following descending families order, can after be Orchidaceaepointed out: This fact has been already reported elsewhere (Torres and Rubiaceae which together account for 27% of the etDombois al. 1994; and Ivanauskas Ellenberg (1974),et al. 1997). that is, The inferior several to other25%. (four species each), Apocynaceae and Cyperaceae species, which occur less frequently in swamp forests, Myrtaceae (five species), Bromeliaceae and Meliaceae contribute to the greater dissimilarity among these formations. It is known that the presence or absence of and(three Styracaceae species each), (two species Arecaceae, each), Asteraceae, and other 32 Fabaceae, families these other species is related to environmental factors presentMelastomataceae, in the area with Myrsinaceae, only one species Piperaceae, each. Rutaceae such as canopy openness, variations in topography, level The study area presented high family richness, especially concerning the woody components, as et al. commonly found in swamp forests (Ivanauskas et al. of soil flooding (Teixeira and Assis 2009), and soil type 1997, Marques et al. 2003, Torres et al. 1994). In total, (Teixeirabetween fragments and Assis inserted 2009; Kotchetkoff-Henriques in remote regions or, in the each family was represented by few species or even by just opposite2005). Therefore, way, dissimilarity it is possible between to fragments find high located similarity in nearby locations, as is the case of Itatinga and Botucatu, and the areas at Campinas Municipality (Campinas 1/3 wereone species, different as fromobserved this pattern,in 32 families being (68%represented of the totalby a greaternumber number of families). of species. Only the Orchidaceae and Rubiaceae Claro and Bauru forests and the greatest dissimilarity The trees predominated in the area with 40 species wasand 2). obtained The Botucatu in relation forest towas Brotas most similar (1), Itatinga to the andRio

cluster analysis lead to the consideration that both the sampled (44%). The epiphytes were the second most geographicRibeirão Preto position forests. and The other dendrogram ecologic produced peculiarities by the of represented with 15 species (16%), followed by herbs with 14 species (15%), lianas with 11 species (12%), shrubsThere with are 10few species data on (11%) the non-arboreal and also two components parasites the swamp forests, besides soil flooding, might be factors of(2%) the (Table swamp 1). forests in São Paulo State. In fact, the thethat similarity can influence analysis their included floristic composition.227 tree species, among comparable data (M. Carboni unpublished data; Spina whichThe eight presence/absence appeared only in matrix the swamp composed forest in to Botucatu. perform et al. They are: Esenbeckia grandiflora, Eugenia paracatuana, that several of these species were registered only in Metrodorea nigra, Myrceugenia ovata, Neomitranthes the present 2001; M.E.S. survey. Paschoal There are unpublished some species data) that indicate were glomerata, Ocotea aciphylla, Styrax leprosus and registered in common, like Voyria aphylla recorded by Trichilia elegans Eugenia Paschoal (unpublished data), Phoradendron piperoides paracatuana and Myrceugenia ovata) were previously by Carboni (unpublished data) and Piper aduncum by . Most of these species (except Spina et al. with some kind of riparian vegetation, although not by Carboni (unpublished data) and others by Spina referred by Rodrigues and Nave (2001) to be associated (2001), besides some Orchidaceae registered specifically with swamp forests. Later, Baptista-Maria833 Magalhães and Maimoni-Rodella | Floristics of a freshwater swamp in Brazil et al. (2009) quoted Eugenia paracatuana as present in trees measuring 13 to 17m tall, and these values are riparian forests of Central Brazil and Myrceugenia ovata higher than those observed by Toniato et al. (1998) was recorded in alluvial forests in southeastern Brazil who found the canopy tree ranging between 7 and 9 m (Silva et al. 2007). These records seem to indicate the et al. association of these species with riparian vegetation, (1997). A discontinuous layer composed by small trees and their record in the present survey may be due to the tall,and but several was individualsmore similar of toEuterpe the findings edulis ,of with Costa heights fact that the area is located on a slope and there were ranging between 4 and 10m was found under the canopy. some spots in the upper side of it where the soil was not A large quantity of Euterpe edulis seedlings was present of the surrounding vegetation (riparian and seasonal E. edulis to be the so flooded. Their presence also reflects the influence especially in flooded areas. These data agree with study area, as previously observed by Ivanauskas et al. TeixeiraClaro municipality. and Assis (2005) Some who emerging found trees belonging to semidecidual(1997) and Costa forests) et al. on (1997) the floristic elsewhere. composition of the themost species important Calophyllum species inbrasiliense a swamp, forestMagnolia located ovata in andRio The genus Zanthoxylum Handroanthus umbellatus also occurred with individuals found in the swamp forests (Kotchetkoff-Henriques et reaching 20m high. In the higher position within the al. 2005; Toniato et al. 1998; (Rutaceae) Torres et alcan. 1994), be frequently but was surveyed slope, where some spots with more drained soil could be found, some individuals of Cariniana estrellensis genera were present (see Table 1). Another interesting absent in the present study, although other Rutaceae both in number of species and density of individuals in exceeding 20m tall were also observed. This specieset al. is thefact neotropicalwas that the vegetation Fabaceae andare alsogenerally in the very swamp significant forests 2008)frequently and mayassociated be one with more riparian case of (Rodriguesintersection and with Nave the neighboring2001) and seasonal vegetation. semidecidual forests (Ramos it was represented only by two species (Clitoria sp. and Ingain São marginata Paulo state) in the (Teixeira present and survey. Assis 2009). However seems to be very frequent among the São Paulo state swampThis survey forests confirmed and to highlight the low thefloristic need similarity to conserve that even small remnants of this vegetation, considering the inferiorThe profile tree layer diagram composed of the vegetation mainly by revealed individuals a well- of Euterpedefined stratification, edulis with a continuous canopy and an occurrencespecies richness of a and well regional established peculiarities population of the of floristicEuterpe collect the apical Mart edible (Figure meristem 2), aof speciesthis palm identified tree (Souza as composition.edulis, a threatened Another species, significant which aspect must is related be preserved to the vulnerable (SMA 2006) due to its abusive exploitation to in the location and serve possibly as a source for future The continuous canopy layer was composed by conservation programs. and Lorenzi 2008).

Figure 1. areas are described in Table 2. Cluster analysis using the Jaccard similarity index among twelve freshwater swamp forest areas in São Paulo state, southeastern Brazil. The

834 Magalhães and Maimoni-Rodella | Floristics of a freshwater swamp in Brazil

Figure 2. toward the water course. Vertical line corresponds to the plants height. 1. Calophyllum brasiliense; 2. Handroanthus umbellatus 4. Protium The spruceanum arboreal ;components 5. Euterpe edulis of a freshwater; 6. Tapirira swamp guianensis forest; fragment7. Dendropanax represented cuneatus by a; profile8. Magnolia diagram. ovata Horizontal; 9. Guarea distances kunthiana from; 10. 0 to Myrceugenia 30 m, down ovata; 11. Eugenia sp.. ; 3. Unidentified species;

Table 1. collected. Species recorded on 1 ha of freshwater swamp forest located in Botucatu, São Paulo state, southeastern Brazil. * Reproductive material not FAMILY/SPECIES POPULAR NAME HABIT VOUCHER NUMBER Acanthaceae Ruellia sp. - Shrub 27665 Amaranthaceae Hebanthe paniculata Mart. - 27667 Anacardiaceae Liana Tapirira guianensis Aubl. peito-de-pomba Tree 27668 Apocynaceae Peltastes peltatus (Vell.) Woodson 27672 Marsdenia cf. macrophylla - 27670 cipó-bênção Liana Oxypetalum cf. urbanianum - 27671 Liana Araceae Liana Philodendron sp. 27673 Araliaceae filodendro Epiphyte Dendropanax cuneatus Decne. and Planch. maria-mole Tree 27674 Arecaceae Euterpe edulis Mart. palmito-juçara Tree 27675 Syagrus romanzoffiana (Cham.) Glassman jerivá Tree * Aristolochiaceae Aristolochia sp. - 27676 Asteraceae Liana Dasyphyllum brasiliense (Spreng.) Cabrera guaiapá-parreira 27678 Piptocarpha aff. reitziana - Tree 27679 Liana Balanophoraceae Scybalium fungiforme - Holoparasite 27766 Bignoniaceae Schott and Endl. Handroanthus umbellatus (Sond.) Mattos Tree 27695 Bromeliaceae ipê-amarelo-do-brejo Aechmea cf. bromeliifolia bromélia 27699 Billbergia sp. - 27698 (Rudge) Baker Epiphyte Tillandsia geminiflora Brongn. cravo-do-mato 27700 Epiphyte Tillandsia tenuifolia tilandsia 27697 Epiphyte Burseraceae L. Epiphyte Protium spruceanum almecegueira Tree 27701 Celastraceae (Benth.) Engl. Hippocratea volubilis fava-de-arara 27702 Chloranthaceae L. Liana Hedyosmum brasiliense chá-de-soldado Tree 27703

Mart ex Miq.

835 Magalhães and Maimoni-Rodella | Floristics of a freshwater swamp in Brazil

Table 1. Continued.

FAMILY/SPECIES POPULAR NAME HABIT VOUCHER NUMBER Clusiaceae Calophyllum brasiliense Cambess. guanandi Tree 27704 Cyperaceae Calyptrocarya longifolia - Herb 27705 Rhynchospora exaltata Kunth capim-navalha Herb 27706 (Rudge) Kunth Scleria cf. mitis P.J.Bergius - Herb 27707 Euphorbiaceae Croton floribundus Tree 27708 Fabaceae Lund ex Didr. capixingui Inga marginata Willd. ingá-de-folha-lisa Tree 27709 Clitoria sp. - 27710 Gentianaceae Liana Voyria aphylla (Jacq.) Pers. erva-fantasma Herb 27711 Lauraceae Ocotea aciphylla canela-amarela Tree 27712 Lecytidaceae (Nees) Mez Cariniana estrellensis jequitibá-branco Tree 27713 Magnoliaceae (Raddi) Kuntze Magnolia ovata (A. St.-Hil.) Spreng. magnólia-do-brejo Tree 27692 Malpighiaceae Heteropterys sp. - 27693 Malvaceae Liana Pseudobombax grandiflorum embiruçu Tree 27691 Marantaceae (Cav.) A.Robyns Ctenanthe sp. - Herb 27690 Melastomataceae Miconia hymenonervia - Shrub 27688 Miconia sp. - Herb 27689 (Raddi) Cogn. Meliaceae Guarea kunthiana A.Juss. marinheiro Tree 27682 Guarea macrophylla Vahl marinheiro-do-brejo Tree 27683 Trichilia elegans A.Juss. catiguazinho Tree 27684 Trichilia pallida Sw. catiguá Tree 27680 Monimiaceae Mollinedia schottiana (Spreng.) Perkins pimenteira Tree 27718 Moraceae Ficus insipida Willd. Tree 27761 Myrsinaceae figueira Ardisia ambigua Mart. capororoquinha Tree 27764 Myrsine guianensis (Aubl.) Kuntze capororoca Tree 27765 Myrtaceae Eugenia florida DC. guamirim Tree 27720 Eugenia hyemalis Cambess. guamirim-miúdo Tree 27719 Eugenia paracatuana - Tree 27722 Myrceugenia ovata - Tree 27721 O. Berg Neomitranthes glomerata - Tree 27723 (Hook. and Arn.) O. Berg Orchidaceae (D. Legrand) Govaerts Acianthera aphthosa - 27748 Aspidogyne aff. metallescens - Herb 27741 (Lindl.) Pridgeon and M.W. Chase Epiphyte Baskervilla sp. - Herb 27732 (Barb. Rodr.) Garay Brasiliorchis gracilis - 27743 Cattleya loddigesii - 27742 Lodd. Epiphyte Cyclopogon sp. 1 - Herb 27727 Lindl. Epiphyte Cyclopogon sp. 2 - Herb 27746 Encyclia patens Hook. - 27749 Isochilus linearis - 27739 Epiphyte Oeceoclades maculata - Herb 27740 (Jacq.) R. Br. Epiphyte Oncidium crispum - 27737 (Lindl.) Lindl. Oncidium pumilum - 27730 Lodd. ex Lindl. Epiphyte Polystachya estrellensis - 27744 Lindl. Epiphyte Psilochilus modestus - Herb 27729 Rchb. f. Epiphyte Sauroglossum nitidum Schltr. - Herb 27745 Barb. Rodr.

836 Magalhães and Maimoni-Rodella | Floristics of a freshwater swamp in Brazil

Table 1. Continued.

FAMILY/SPECIES POPULAR NAME HABIT VOUCHER NUMBER Specklinia cf. uniflora - 27771 Zygostates lunata - 27731 (Lindl.) Pridgeon and M.W. Chase Epiphyte Piperaceae Lindl. Epiphyte Piper aduncum pimenta-de-macaco Shrub 27716 Piper sp. - Shrub 27717 L. Poaceae Parodiolyra micrantha (Kunth) Davidse and Zuloaga - Herb 27715 Rosaceae Prunus myrtifolia pessegueiro-bravo Tree 27753 Rubiaceae ( L. ) Urb. Faramea torquata Müll. Arg. - Tree 27763 Ixora venulosa Benth. Tree 27759 Palicourea macrobothrys - Shrub 27724 ixora-do-mato Palicourea marcgravii A. St.-Hil. erva-de-rato Shrub 27757 (Ruiz and Pav.) Roem. et Schult. Psychotria vellosiana Benth. café-do mato Tree 27756 Psychotria carthagenensis Jacq. - Shrub 27760 Psychotria sp. - Shrub 27725 Chomelia sp. - Shrub 27754 Rutaceae Esenbeckia grandiflora Mart. pau-de-cotia Tree 27758 Metrodorea nigra A. St.-Hil. carrapateira Tree 27752 Salicaceae Casearia sylvestris Sw. lagarteira Tree 27755 Santalaceae Phoradendron piperoides (Kunth) Trel. erva-de-passarinho Hemiparasite 27714 Sapindaceae Serjania sp. - 27734 Sapotaceae Liana Chrysophyllum gonocarpum guatambu-de-leite Tree 27736 Siparunaceae (Mart. and Eichler ex Miq.) Engl. Siparuna guianensis Aubl. pau-bosta Tree 27728 Solanaceae Cestrum sp. - Tree 27738 Styracaceae Styrax leprosus Hook. and Arn. canela-seiva Tree 27726 Styrax pohlii A.DC. benjoeiro Tree 27735 Theophrastaceae Clavija sp. - Shrub 27751 Verbenaceae Petrea subserrata Cham. - 27733

Liana Table 2.

Freshwater swamp forest areas previously studied in São Paulo state, southeastern Brazil, compared with the present study. T & S: trees and shrubs. Random: random walksGEOGRAPHIC in the sampling area.ALTITUDE CLIMATE SAMPLED SAMPLE NUMBER MUNICIPALITY REFERENCE COORDINATES (M) TYPE* HABITS METHOD OF SPECIES 1. Botucatu 22°52’52” S, 48°29’32” W 860 Cfa All 92 Present study 2. Bauru 22°20’ S, 49°01’ W 560 Cwa All 108 Carboni (unpublished data) Random 3. Campinas (1) 22°49’45” S, 47°06’33” W 600 Cwa T & S Plots 55 Toniato et al. (1998) Random 4. Campinas (2) 22°55’ S, 47°05’ W 660 Cwa Trees Census 33 Torres et al. (1994) 5. Itatinga 23°17’41” S, 48°38’53” W 570 Cwa T & S Census 39 Ivanauskas et al. (1997) Paschoal and Cavassan 6. Agudos (1) 22°30’ S, 48°55’ W 550 Cwa Trees 38 (1999) 7. Campinas (3) 22°49’55” S, 47°06’33”W 580-610 Cwa All Random 134 Spina et al. (2001) 8. Brotas (1) 22°16’ S, 48°06’ W 470 Cwa T & S 51 Marques et al. (2003) Random 22°21’ S, 47°28’ W 640 Cwa T & S Plots 49 Random Kotchetkoff-Henriques et al. 21°11’ S, 47°48’ W 510-800 Aw Trees 157 9. Rio Claro (2005) Teixeira and Assis (2005) 10. Ribeirão Preto Expedite Survey Paschoal (unpublished 11. Agudos (2) 22°15’ S, 48°15’ W 550 Cwa All 41 data) 12. Brotas (2) 22°10’ S, 47°55’ W 470 Cwa T & S RandomPlots 33 Costa et al. (1997)

* According to Koeppen Classification

837 Magalhães and Maimoni-Rodella | Floristics of a freshwater swamp in Brazil

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Marques, .M.C.M., São Paulo: S.M. SecretariaSilva and A. do Salino. Meio Ambiente/ Instituto Florestal/ Imprensa Oficial. 200 p. : May 2012 . Acta2003. Botanica Florística Brasilica e estrutura 17(4): do Received: November: August 2011 2012 495-506.componente arbustivo-arbóreo de uma floresta higrófila da bacia do Accepted Rio Jacaré-Pepira, São Paulo, Brasil Published online Editorial responsibility: Pedro V. Eisenlohr

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