Floristic composition, structure and soil-vegetation relations in three white-sand soil patches in central Amazonia

Composição florística, estrutura e relação solo-vegetação em três áreas de campinarana na Amazônia central

Layon Oreste DEMARCHI Veridiana Vizoni SCUDELLER Livia Carvalho MOURA Randolpho Gonçalves DIAS-TERCEIRO Aline LOPES Florian Karl WITTMANN Maria Teresa Fernandez PIEDADE About the authors

ABSTRACT

The Amazonian white-sand vegetation presents a set of unique features, such as the dominance of a few species, high endemism and low species richness, which differentiate it from other Amazonian forests. Soil parameters have long been recognized as the main drivers of white-sand vegetation (WSV) characteristics. However, how they influence the composition, richness and structure of this vegetation type is still poorly understood. In this study we investigated the variation in floristic composition between patches and the soil-vegetation relations in three central Amazonian WSV patches. We tested whether slight differences in soil properties are linked with differences in floristic composition, species richness and forest structure in adjacent patches. In each patch three plots of 50 x 50 m were sampled (a total of 2.25 ha). Soil samples were collected for each plot. The sampling cutoff for arboreal individuals was DBH ≥ 5 cm. We sampled a total of 3956 individuals belonging to 40 families and 140 species. In each patch only a few species were dominant, but the dominant species varied among patches. Differences among patches were significant, but plots in the same patch tended to have similar species composition. The variable sum of bases (SB) was directly related to species composition, however, species richness and forest structure were not related to soil parameters. Even small variations in soil parameters can change species composition in WSV, although these variations do not necessarily influence the richness and other structural parameters.

KEYWORDS:
species richness; oligotrophic ecosystems; dominance; sum of bases

RESUMO

As campinaranas amazônicas apresentam uma série de características únicas, como a dominância de poucas espécies, alto grau de endemismos e baixa riqueza de espécies, que as diferenciam de outras formações florestais amazônicas. Parâmetros edáficos têm sido apontados como os principais responsáveis pelas características das campinaranas. Contudo, como estes parâmetros influenciam a composição, riqueza e estrutura deste tipo de vegetação ainda é pouco entendido. Neste estudo investigamos a variação estrutural, a composição florística e a relação solo-vegetação em três áreas de campinarana na Amazônia central, com intuito de testar se pequenas diferenças nos parâmetros edáficos do solo estão relacionados com diferenças na composição, riqueza e estrutura do componente arbóreo em áreas de campinarana adjacentes. Em cada área foram amostradas três parcelas de 50 x 50 m (totalizando 2.25 ha), com o critério de inclusão para os indivíduos de DAP ≥ 5 cm. Amostras de solo foram coletadas em cada parcela. O número total de indivíduos amostrados foi 3956, pertencendo a 40 famílias e 140 espécies. Em cada área poucas espécies foram dominantes, mas estas variaram entre as áreas. Diferenças entre as áreas foram significativas, porém parcelas da mesma área tenderam a ter composição florística similar. A variável soma de bases (SB) foi diretamente relacionada à composição de espécies; contudo, riqueza de espécies e estrutura florestal não foram relacionadas a nenhum dos parâmetros do solo amostrados. Concluimos que mesmo pequenas variações nos parâmetros edáficos do solo podem mudar a composição de espécies em campinaranas, embora esta variação não necessariamente influencie a riqueza e outros parâmetros estruturais da vegetação.

PALAVRAS-CHAVE:
riqueza de espécies; ecossistemas oligotróficos; dominância; soma de bases

INTRODUCTION

The Amazonian region is formed by a mosaic of landscapes with different floristic compositions. Each landscape diversity is related to a variety of habitat characteristics and species preferences (Pitman et al. 2001Pitman, N.C.A.; Terborgh, J.W.; Silman, M.R.; Núñez, P.V.; Neill, D.A.; Cerón, C.E.; et al. 2001. Dominance and distribution of tree species in upper Amazonian Terra Firme forests. Ecology, 82: 2101-2117.; Coronado et al. 2009Coronado, E.N.H.; Baker, T.R.; Phillips, O.L.; Pitman, N.C.A.; Pennington, R.T.; Martínez, R.V.; et al. 2009. Multi-scale comparisons of tree composition in Amazonian Terra Firme Forests. Biogeosciences, 6: 2719-2731.; Junk et al. 2011Junk, W.J.; Piedade, M.T.F.; Schöngart, J.; Cohn-Haft, M.; Adeney, J.M.; Wittmann, F. 2011. A classification of major naturally-occurring Amazonian lowland wetlands. Wetlands, 31: 623:640.). It is estimated that Amazonian forests contain between 12,500 and 16,000 tree species (Hubbell et al. 2008Hubbell, S.P.; He, F.; Condit, R.; Borda-de-Água, L.; Kellner, J.; ter Steege, H. 2008. How many tree species are there in the Amazon and how many of them will go extinct? Proceedings of the National Academy of Sciences, 105: 11498-11504.; ter Steege et al. 2013ter Steege, H.; Pitman, N.C.A.; Sabatier, D.; Baraloto, C.; Salomão, R.P.; Guevara, J.E.; et al. 2013. Hyperdominance in the Amazonian Tree Flora. Science, 342: 325-336.). The formations designated as white-sand vegetation (WSV) or campinarana (Veloso et al. 1991Veloso, H.P.; Rangel Filho, A.L.R.; Lima, J.C.A. 1991. Classificação da vegetação brasileira, adaptada a um sistema universal. Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro , 124p.) constitute a peculiar phytophysiognomy in the Amazon region. Soils beneath white-sand vegetation are composed of heavily leached white-sand of very low fertility (Heyligers 1963Heyligers, P.C. 1963. Vegetation and soil of a White-Sand Savanna in Suriname. Mededelingen van het Botanisch Museum en Herbarium van de Rijksuniversiteit te Utrecht, 191: 1-148.; Anderson 1981Anderson, A.B. 1981. White-sand vegetation of Brazilian Amazonia. Biotropica, 13: 199-210.; Luizão et al. 2007Luizão, F.J.; Luizão, R.C.C.; Proctor, J. 2007. Soil acidity and nutrient deficiency in central Amazonian heath forest soils. Plant Ecology, 192: 209-224. ; Mendonça et al. 2015Mendonça, B.A.F.; Filho, E.I.F.; Schaefer, C.E.G.R.; Simas, F.N.B.; Paula, M.D. 2015. Os solos das Campinaranas na Amazônia Brasileira: Ecossistemas arenícolas oligotróficos. Ciência Florestal, 25: 827-839.); the woody vegetation is scleromorphic and relatively poor in tree species compared to other Amazonian ecosystems (Vicentini 2004Vicentini, A. 2004. A vegetação ao longo de um gradiente edáfico no Parque Nacional do Jaú. In: Borges, S.H.; Iwanaga, S.; Durigan, C.C.; Pinheiro, M.R. (Ed.). Janelas para a biodiversidade no Parque Nacional do Jaú: uma estratégia para o estudo da biodiversidade na Amazônia. Fundação Vitória Amazônica, WWF, IBAMA, Manaus, p.117-143. ; Stropp et al. 2011Stropp, J.; Van Der Sleen, P.; Assunção, P.A.; Silva, A.L.; ter Steege, H. 2011. Tree communities of white-sand and terra-firme forests of the upper Rio Negro. Acta Amazonica, 41: 521-544.,), but rich in endemisms (Janzen 1974Janzen, D. 1974. Tropical blackwater rivers, animals and mast fruiting by Dipterocarpaceae. Biotropica, 6: 69-103.; Anderson et al. 1975; Anderson 1981; Boubli 2002Boubli, J.P. 2002. Lowland floristic assessment of Pico da Neblina National Park, Brazil. Plant Ecology, 160: 149-167.; Fine et al. 2010Fine, P.V.A.; García-Villacorta, R.; Pitman, N.C.A.; Mesones, I.; Kembel, S.W. 2010. A floristic study of the White-sand forests of Peru. Annals of the Missouri Botanical Garden, 97: 283-305.; Adeney et al. 2016Adeney, J.M.; Christensen, N.L.; Vicentini, A.; Cohn-Haft, M. 2016. White-sand Ecosystems in Amazonia. Biotropica, 48: 7-23.; Fine and Baraloto 2016Fine, P.V.A.; Baraloto, C. 2016. Habitat Endemism in White-sand Forests: Insights into the Mechanisms of Lineage Diversification and Community Assembly of the Neotropical Flora. Biotropica, 48: 24-33.; Guevara et al. 2016Guevara, J.E.; Damasco, G.; Baraloto, C.; Fine, P.V.A.; Peñuela, M.C.; Castilho, C. et al. 2016. Low Phylogenetic Beta Diversity and Geographic Neo-endemism in Amazonian White-sand Forests. Biotropica, 48: 34-46.).

Estimates of white-sand vegetation cover ranged from 64,000 km2 (Braga 1979Braga, P.I.S. 1979. Subdivisão fitogeográfica, tipos de vegetação, conservação e inventário florístico da Floresta Amazônica. Acta Amazonica, 9: 53-80.) to 400,000 km2 (Prance and Daly 1989Prance, G.T.; Daly, D. 1989. Brasilian Amazon. In: Campbell, D.G.; Hammond, H.D. (Ed.). Floristic inventory of tropical countries. New York Botanical Garden, New York, p.523-533.). However, more accurate mapping techniques with remote sensing suggest that the coverage might be larger, since surveys of the Negro River basin alone (where continuous areas of white-sand vegetation are common) estimated its coverage to be 104.000 km2 (Junk et al. 2011Junk, W.J.; Piedade, M.T.F.; Schöngart, J.; Cohn-Haft, M.; Adeney, J.M.; Wittmann, F. 2011. A classification of major naturally-occurring Amazonian lowland wetlands. Wetlands, 31: 623:640.), and the most recent estimate of white-sand vegetation coverage in the Amazon basin is 334,879 km2 (Adeney et al. 2016Adeney, J.M.; Christensen, N.L.; Vicentini, A.; Cohn-Haft, M. 2016. White-sand Ecosystems in Amazonia. Biotropica, 48: 7-23.). In many other Amazonian regions, white-sand vegetation distribution is isolated and island-like, a result of the fragmented nature of the distribution of the sandy soils on which this vegetation type occurs (Prance 1996).

The structure of white-sand vegetation varies from grassland and open areas, dominated by herbaceous plants, to open shrub and dense-canopy forest physiognomies (Veloso et al. 1991Veloso, H.P.; Rangel Filho, A.L.R.; Lima, J.C.A. 1991. Classificação da vegetação brasileira, adaptada a um sistema universal. Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro , 124p.; IBGE 2012IBGE. 2012. Manual Técnico da Vegetação brasileira. 2da ed., Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro, 275p.). Many white-sand soils have an underlying hardpan, where any increase in precipitation can quickly elevate the groundwater level, subjecting plants to waterlogging or hydric saturation periods (Richardt et al. 1975Richardt, K.; Santos, A.; Nascimento-Filho, V.; Bacc, O.O.S. 1975. Movimento de água subterrânea em ecossistema Campina Amazônica. Acta Amazonica, 6: 229-290.; Kubitzki 1989aKubitzki, K. 1989a. The ecogeographical differentiation of Amazon inundation forests. Plant Systematics and Evolution, 162: 285-304.; Franco and Dezzeo 1994Franco, W.; Dezzeo, N. 1994. Soils and soil-water regime in the terra-firme-caatinga forest complex near San Carlos de Rio Negro, state of Amazonas, Venezuela. Interciencia, 19: 305-316.). Because of this characteristic, some authors emphasize the comparatively high floristic similarity between white-sand vegetation and Amazonian black-water seasonally-flooded forest (igapó) (Kubitzki 1989aKubitzki, K. 1989a. The ecogeographical differentiation of Amazon inundation forests. Plant Systematics and Evolution, 162: 285-304.; Kubitzki 1989bKubitzki, K. 1989b. Amazon lowland and Guayana highland - historical and ecological aspects of the development of their floras. Amazoniana, 11: 1-12.; Damasco et al. 2013Damasco, G.; Vicentini, A.; Castilho, C.V.; Pimentel, T.P.; Nascimento, H.E.M. 2013. Disentangling the role of edaphic variability, flooding regime and topography of Amazonian white-sand vegetation. Journal of Vegetation Science, 24: 384-394.).

Oligotrophic soils and hydric saturation have been considered the main drivers of white-sand vegetation characteristics (Heyligers 1963Heyligers, P.C. 1963. Vegetation and soil of a White-Sand Savanna in Suriname. Mededelingen van het Botanisch Museum en Herbarium van de Rijksuniversiteit te Utrecht, 191: 1-148.; Pires and Prance 1985Pires, J.M.; Prance, G.T. 1985. The vegetation types of the Brazilian Amazon. In: Prance, G.T.; Lovejoy, T.E. (Ed.). Key Enviroments: Amazonia. Oxford, Pergamon Press, p.109-145.; Franco and Dezzeo 1994Franco, W.; Dezzeo, N. 1994. Soils and soil-water regime in the terra-firme-caatinga forest complex near San Carlos de Rio Negro, state of Amazonas, Venezuela. Interciencia, 19: 305-316.; Tiessen et al. 1994Tiessen, H.; Chacon, P.; Cuevas, E. 1994. Phosphorus and nitrogen status in soils and vegetation along a toposequence of dystrophic rainforests on the upper Rio Negro. Oecologia, 99: 145-150.; Sobrado 2009Sobrado, M.A. 2009. Leaf tissue water relations and hydraulic properties of sclerophyllous vegetation on white sands of the upper Rio Negro in the Amazon region. Journal of Tropical Ecology, 25: 271-280.), since they work as strong environmental filters for tree species establishment and distribution (Targhetta et al. 2015Targhetta, N.; Kesselmeier, J.; Wittmann, F. 2015. Effects of the hydroedaphic gradient on tree species composition and aboveground wood biomass of oligotrophic forest ecosystems in the central Amazon basin. Folia Geobotanica, 50: 185-205.; Adeney et al. 2016Adeney, J.M.; Christensen, N.L.; Vicentini, A.; Cohn-Haft, M. 2016. White-sand Ecosystems in Amazonia. Biotropica, 48: 7-23.). Studies show that white-sand vegetation areas with higher hydric saturation may present lower species richness and smaller individuals (Bongers et al. 1985Bongers, F.; Engelen, D.; Klinge, H. 1985. Phytomass structure of natural plant communities on spodosols in southern Venezuela: the Bana woodland. Vegetatio, 63: 13-34.; Franco and Dezzeo 1994; Targhetta et al. 2015), although under certain edaphic and topographic conditions hydric saturation may provide less adverse conditions for species establishment, thereby these conditions might have a positive effect on species richness and diversity (Damasco et al. 2013Damasco, G.; Vicentini, A.; Castilho, C.V.; Pimentel, T.P.; Nascimento, H.E.M. 2013. Disentangling the role of edaphic variability, flooding regime and topography of Amazonian white-sand vegetation. Journal of Vegetation Science, 24: 384-394.). Though soil properties are directly influenced by hydric saturation, soil texture and fertility have been considered the main factors causing structural and floristic variation of white-sand vegetation (Tiessen et al. 1994; Coomes and Grubb 1996Coomes, D.A.; Grubb, P.J. 1996. Amazonian caatinga and related communities at La Esmeralda, Venezuela: forest structure, physiognomy and floristics, and control by soil factors. Vegetatio, 122: 167-191.; Coomes 1997Coomes, D.A. 1997. Nutrient status of Amazonian caatinga forests in a seasonally dry area: nutrient fluxes in litter fall and analyses of soils. Canadian Journal of Forest Research, 27: 831-839.; Damasco et al. 2013). However, there are few studies that investigated the role of small differences in soil nutrient concentration within this oligotrophic ecosystem.

To investigate the relationships between soil parameters and the composition and structural characteristics of the woody plant assemblage, three isolated patches of white-sand vegetation surrounded by upland forest (terra-firme) forest were studied to address the following questions: (1) are the patches different in assemblage composition and (2) if so, are such differences linked to soil characteristics?

MATERIAL AND METHODS

Study Area

WSV was studied in three areas within the Tupé Sustainable Development Reserve (SDR Tupé, Figure 1), located on the left margin of the Negro River, approximately 30 km west of the city of Manaus, in the state of Amazonas, Brazil. The SDR Tupé covers an area of 11.973 ha and, together with other protected areas, forms an important mosaic of protected habitats in the central Brazilian Amazon. The average annual rainfall in the region is 2,100 mm, with a well defined rainy season (165-300 mm month-1) from November to May, and a dry season (<65 mm month-1) from July to September. The average temperature is 27 °C, ranging between 18 °C and 37 °C throughout the year, and average relative humidity is around 85% (Radam Brasil 1978Radam Brasil. 1978. Levantamento de recursos naturais. v.18. Folha SA. 20 Manaus, Departamento Nacional de Produção Mineral, Rio de Janeiro, 747p.). The study area is inserted in the Igarapé Tarumã-mirim basin (a tributary of the Rio Negro). This region is largely covered by WSV areas, which are distributed in patches. The vegetation of the SDR Tupé is predominantly upland forest (terra-firme), with black water river floodplains forest (igapó) dominating the narrow riverine floodplain (Scudeller et al. 2005Scudeller, V.V.; Aprile, F.M.; Melo, S.; Santos-Silva, E.N. 2005. Reserva de Desenvolvimento Sustentável do Tupé: características gerais. In: Santos-Silva, E.N.; Aprile, F.M.; Scudeller, V.V.; Melo, S. (Org.). Biotupé: Meio físico, diversidade biológica e sociocultural do Baixo Rio Negro, Amazônia Central. Instituto Nacional de Pesquisas da Amazônia, Manaus, p. XI-XXI.).

Figure 1
Map locating the white-sand forest patches studied (A, B and C) within the limits of the Tupé Sustainable Development Reserve (SDR Tupé), located on the left margin of the Negro River, west of the city of Manaus, in the state of Amazonas, Brazil. The nine sampling plots (three within each patch) are shown as nine squares in the larger image. The pink color on the smaller satellite image shows urbanized and clear-cut areas, while green shows forested habitats. This figure is in color in the electronic version.

Vegetation sampling

Three white-sand forest patches (A, B and C) were selected within the SDR Tupé. The patches were 40 to 100 ha in size and were surrounded by terra-firme and/or igapó forest. In each patch three 50 x 50 m plots were established, totalling 0.75 ha per patch, and 2.25 ha among the three patches. To avoid sampling transitional areas between WSV and surrounding forest formations, all plots were allocated in the central part of each white-sand forest patch, with a distance of 100 to 180 m among sampling plots within patches, and a distance of 3.5 to 4 km among patches.

All living woody individuals (except lianas), with diameter at breast height (DBH) ≥ 5 cm were marked with numbered aluminum tags, and had their diameter measured. Tree height was estimated with a hypsometer. Vouchers from all individuals were collected, dried, pressed, and subsequently deposited in the herbarium of the National Institute of Amazon Research (Instituto Nacional de Pesquisas da Amazônia - INPA) and in the herbarium of the Federal Institute of Amazonas (Instituto Federal do Amazonas - IFAM) (EAFM). Species were identified using analytical keys, comparison with herbarium specimens and consulting specialists (see acknowledgements). Species were classified according to APG IV (2016APG IV. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181: 1-20.), and their names were standardized according to the classification of the REFLORAReflora - Flora do Brasil 2020 em construção. Jardim Botânico do Rio de Janeiro. ( (http://floradobrasil.jbrj.gov.br/ ). Accessed on 22/05/2017.
http://floradobrasil.jbrj.gov.br/...
program.

Chemical and physical soil characterization

Soil samples at 0 to 20 cm depth were collected in the four corners and in the center of each sampling plot. The samples were homogenized in the field and joined in one composite sample per plot. The analyses were performed according to the Embrapa soil analysis protocol (Embrapa 1997Embrapa. 1997. Manual de Métodos de Análise de Solos. 2da ed., Centro Nacional de Pesquisa de Solos, Rio de Janeiro, 212p.). Twenty-four variables were analyzed: fine sand (0.2-0.05 mm grain diameter), coarse sand (2.0-0.2 mm), total sand (2.0-0.05 mm), silt (0.05-0.002 mm) and clay (>0.002 mm), C (carbon), OM (organic matter), pH, P, K+, Na+, Ca2+, Mg2+, Al3+, H+AL (potential acidity), SB (sum of bases: Ca²+ + Mg²+ + K+ + Na+), CEC(t) (effective cation exchange capacity), CEC(T) (cation exchange capacity under neutral pH), V (saturation index for bases), m (saturation index for aluminum), Fe, Zn+, Mn2+ and Cu.

Data analysis

The forest structure parameters Relative Density (RDe), Relative Dominance (RDo), Relative Frequency (RFr) and the Importance Value Index (IVI) (Curtis and McIntosh 1951Curtis, J.T.; McIntosh, R.P. 1951. An upland forest continuum in the prairie-forest border region of Wisconsin. Ecology, 32: 476-496.) were calculated using the software Fitopac 2.1.2 (Shepperd 2010Shepherd, G.J. 2010. Fitopac - Manual do usuário. Departamento de Botânica, Universidade Estadual de Campinas, Campinas, Brazil, 91p.). To evaluate the local effect on species composition between the patches, two NMDS axes were generated and a MANOVA was applied to test for statistical difference in species composition among patches. Ranking was based on dissimilarity between samples (in a presence and absence matrix) calculated with the Jaccard Index (Borcard et al. 2011Borcard, D.; Gillet, F.; Legendre, P. 2011. Numerical Ecology with R. Springer, New York, 306p.). To evaluate the effect of soil parameters in tree assemblages, we generated a new NMDS axis (k =1), based on dissimilarity between samples (in a presence and absence matrix) calculated with the Jaccard Index. The relationship between environmental variables and species composition was assessed using a Generalized Linear Mixed Model (GLMM). For the model, we used only variables that were not correlated with each other (see Supplementary Material, Table S1), as correlated variables carry the same information and could potentially mask or enhance patterns in additive multiple linear models (Magnusson and Mourão 2005Magnusson, W.E; Mourão, G. 2005. Estatística sem Matemática. 2da ed., Publisher Planta, Londrina, 138p.). We used the patches as a random variable. Therefore, our overall multiple regression model was: NMDS = a + b (Mn2+) + b (Silt %) + b (SB) + b (1 | patches).

To evaluate the effect of soil parameters on species richness and vegetation structure variation the GLMM was used separately for each parameter (species richness, relative density, average height and average basal area). Thus we used the same model (mentioned above) replacing the dependent variable for the vegetation structural parameters. To test the effects of soil variables on vegetation without the influence of the sampled patch, we included in the model the variable patches (study areas) as a random variable, so it was possible to control the effect of this variable and verify the real effect of the edaphic variables. All the multivariate analyses were performed using R vegan (R Core Team, 2014R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (http://www.R-project.org/).
http://www.R-project.org/...
; Oksanen et al. 2013Oksanen, J.F.; Blanchet, G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’Hara, R.B.; et al. 2013. vegan: Community Ecology Package, R package version 2.0-7. (http://CRAN.R-project.org/package=vegan).
http://CRAN.R-project.org/package=vegan...
).

RESULTS

Vegetation structural variation

A total of 3956 trees belonging to 40 families and 140 species were recorded in the three patches (Table 1). The families with highest species richness were Fabaceae (15 species), Sapotaceae and Lauraceae (14 species each), Burseraceae, Moraceae and Myrtaceae (7 species each) and Sapindaceae (6 species).

Table 1
Number of individuals, families, richness (total number of species), number of rare species (only one or two recorded individuals) and number of exclusive species (present in only one patch) for nine sampling plots in three white-sand forest patches in Tupé Sustainable Development Reserve (SDR Tupé), Amazonas, Brazil.

The average DBH was 10.4 cm, with a maximum of 94.2 cm. Among the 36 individuals with DBH >45 cm, 33 were Aldina heterophylla Spruce ex Benth. The average height of individual trees was 7 m, with some emergent individuals, mostly A. heterophylla, reaching 22 m.

The highest similarity (41%) occurred between patches A and B, followed by patches A and C (27%) and B and C (22%). Many species occurred only in one patch (51.4% of all recorded species). Overall, the 10 most abundant species corresponded to 54.2% of recorded individuals. Likewise, the 10 most important species corresponded to 44.3% of the total IVI values. Only Aldina heterophylla was among the 10 most important (IVI) species in all three patches, and only Aspidosperma aff. verruculosum Müll.Arg., Clusia nemorosa G.Mey., Simaba guianensis Aubl., Pradosia schomburgkiana (A.DC.) Cronquist, and Conceveiba terminalis (Baill.) Müll.Arg. were among the 10 most important species in at least two of the sampled patches (Table 2). For 38 species only one individual was recorded, and for 13 species only two individuals. Together, these species corresponded to 36.4% of the total species richness. Phytosociological parameters and herbarium voucher numbers for all recorded species are available as Supplementary Material, Table S2.

Table 2
Phytosociological parameters for the 10 species with highest IVI per patch of white-sand forest patches in the Tupé Sustainable Development Reserve (SDR Tupé), Amazonas (Brazil). N = number of individuals, RDe = Relative Density, RDo = Relative Dominance, RFr = Relative Frequency, IVI = Importance Value Index. Values of RDe, RDo and RFr are in percentage.

Tree height and basal area differed significantly among sampling plots (ANOVA F = 0.38; P = 0.00; F = 1.92; P = 0.05 respectively) (Figure 2). However, only basal area differed significantly among patches (ANOVA F = 4.45; P = 0.01), due to a significant difference between patches A and C (Tukey test, P = 0.01). Plot ordination along the two NMDS axes captured 92.76% of the variation in species composition. Tree assemblages differed significantly among patches (MANOVA: Pillai trace = 1.5449; F = 10.182; P <0.001) (Figure 3).

Figure 2
Comparison of forest structure parameters (tree height, A; basal area, B; and relative density, C) among nine sampling plots in three white-sand vegetation patches in the Tupé Sustainable Development Reserve (SDR Tupé), Amazonas, Brazil. The box indicates the 25th and 75th percentiles, the line inside the box represents the median, the capped bars indicate the 10th and 90th percentiles, and the circles represent the extreme values. Different grey tones group plots belonging to each of the three forest patches. This figure is in color in the electronic version.

Figure 3
NMDS ordination diagram of the nine sampling plots in three white-sand forest patches in the Tupé Sustainable Development Reserve (SDR Tupé), Amazonas (Brazil) based on species occurrence of trees with DBH ≥ 5 cm.

Vegetation variation and soil fertility

The three patches were characterized by sand predominance and nutrient-poor soils (Table 3). The single NMDS axis (k=1) explained 58.8% of the variation in species composition. The GLMM using this NMDS axis as dependent variable and soil parameters as independent variables explained 60.50% of the variation in species composition (NMDS = - 1.165-17 + 1.286-1 QM - 2.489-2 PS - 4.083-1 SB; χ2 = 9.7086; R2 = 0.6050; P = 0.02), yet only the variable sum of bases (SB) contributed significantly to the model (t = - 3.094; P = 0.03) (Table 4). However, there was no significant effect of soil parameters on species richness and structural variation.

Table 3
Soil parameter values for three white-sand forest patches (A, B and C) in the Tupé Sustainable Development Reserve (SDR Tupé), Amazonas (Brazil) and for other WSV areas in other studies. Values are the mean ± standard deviation [except * = variation coefficient (%)].

Table 4
Effects of edaphic variables on tree species composition in three white-sand forest patches in the Tupé Sustainable Development Reserve (SDR Tupé), Amazonas (Brazil). Estimate = β value of analyzed fixed variables; Std. Error = standard error; t value = t-test value; P value: probability value.

Some species were widely distributed along the fertility gradient, while others were restricted to parts of it. Species such as Ocotea amazonica (Meisn.) Mez and Pouteria oblanceolata Pires were strongly associated with localities with the lowest fertility, while Mauritiella armata (Mart.) Burret and Protium heptaphyllum (Aubl.) Marchand were more frequently found in plots with the greatest fertility (Figure 4).

Figure 4
Species ordination along the soil fertility gradient represented by the sum of bases SB content of the nine sampling plots in three white-sand forest patches in the Tupé Sustainable Development Reserve (SDR Tupé), Amazonas, Brazil. Only species that had five or more recorded individuals with DBH ≥ 5 cm were included.

DISCUSSION

Our results show that, although the floristic composition and basal area differed significantly between patches and the height differed significantly among plots, only the variation in species composition was related to soil parameters. This soil effect on species composition may explain why the most important species (IVI) varied among relatively nearby patches.

Fabaceae, followed by Sapotaceae, were the families with the highest species richness, which agrees with previous studies in other WSV areas in the Amazon (Anderson 1981Anderson, A.B. 1981. White-sand vegetation of Brazilian Amazonia. Biotropica, 13: 199-210.; Coomes and Grubb 1996Coomes, D.A.; Grubb, P.J. 1996. Amazonian caatinga and related communities at La Esmeralda, Venezuela: forest structure, physiognomy and floristics, and control by soil factors. Vegetatio, 122: 167-191.; Ferreira 2009Ferreira, C.A.C. 2009. Análise comparativa de vegetação lenhosa do ecossistema campina na Amazônia brasileira. PhD thesis, Instituto Nacional de Pesquisas da Amazônia, Universidade Federal do Amazonas, Manaus, Brazil, 277p.; Fine et al. 2010Fine, P.V.A.; García-Villacorta, R.; Pitman, N.C.A.; Mesones, I.; Kembel, S.W. 2010. A floristic study of the White-sand forests of Peru. Annals of the Missouri Botanical Garden, 97: 283-305.; Stropp et al. 2011Stropp, J.; Van Der Sleen, P.; Assunção, P.A.; Silva, A.L.; ter Steege, H. 2011. Tree communities of white-sand and terra-firme forests of the upper Rio Negro. Acta Amazonica, 41: 521-544.; Damasco et al. 2013Damasco, G.; Vicentini, A.; Castilho, C.V.; Pimentel, T.P.; Nascimento, H.E.M. 2013. Disentangling the role of edaphic variability, flooding regime and topography of Amazonian white-sand vegetation. Journal of Vegetation Science, 24: 384-394.; Targhetta et al. 2015Targhetta, N.; Kesselmeier, J.; Wittmann, F. 2015. Effects of the hydroedaphic gradient on tree species composition and aboveground wood biomass of oligotrophic forest ecosystems in the central Amazon basin. Folia Geobotanica, 50: 185-205.; Guevara et al. 2016Guevara, J.E.; Damasco, G.; Baraloto, C.; Fine, P.V.A.; Peñuela, M.C.; Castilho, C. et al. 2016. Low Phylogenetic Beta Diversity and Geographic Neo-endemism in Amazonian White-sand Forests. Biotropica, 48: 34-46.). Apocynaceae and Burseraceae are also important, mainly due to the high abundance of Aspidosperma aff. verruculosum and Protium paniculatum var. modestum Daly, respectively. Lauraceae, Moraceae and Myrtaceae had high richness, but low abundance in the study patches. Common families in other Amazonian forests, such as Lecythidaceae and Myristicaceae (Gentry 1988Gentry, A.H. 1988. Changes in plant community diversity and floristic composition on enviromental and geographical gradients. Annals of the Missouri Botanical Garden, 75: 1-34.), were poorly represented in the white-sand forest patches in SDR Tupé.

The greatest height and DBH values achieved by Aldina heterophylla exemplify the important ecological role of this species in WSV, as was also found in other studies (Anderson et al. 1975Anderson, A.B.; Prance, G.T.; Albuquerque, B.W.P. 1975. Estudos sobre as vegetações de Campinas Amazônica III: a vegetação lenhosa da Campina da Reserva Biológica INPA-SUFRAMA (Manaus-Caracaraí, km 62). Acta Amazonica, 5: 225-246.; Stropp et al. 2011Stropp, J.; Van Der Sleen, P.; Assunção, P.A.; Silva, A.L.; ter Steege, H. 2011. Tree communities of white-sand and terra-firme forests of the upper Rio Negro. Acta Amazonica, 41: 521-544.; Targhetta et al. 2015Targhetta, N.; Kesselmeier, J.; Wittmann, F. 2015. Effects of the hydroedaphic gradient on tree species composition and aboveground wood biomass of oligotrophic forest ecosystems in the central Amazon basin. Folia Geobotanica, 50: 185-205.). The smaller size of the majority of species when compared to other dominant forest formations in Amazonia, such as terra-firme and seasonal flooded forests, justifies the adoption of the individual inclusion criteria of DBH ≥ 5 cm. If the inclusion criteria commonly used in Amazon forests of DBH ≥ 10 cm had been adopted, 60% of the individuals in our sampling plots, including abundant species such as Pagamea duckei Standl., would not have been sampled.

Patches had significantly different floristic composition, but plots in the same patch tended to have similar species composition. Previous studies have related differences in floristic composition to factors such as the insular characteristics of WSV (Anderson 1981Anderson, A.B. 1981. White-sand vegetation of Brazilian Amazonia. Biotropica, 13: 199-210.; Prance 1996Prance, G.T. 1996. Islands in Amazonia. Philosophical Transactions of the Royal Society of London. Series B, 351: 823-833.), the dispersion capacity limited to anemochory and ornithochory (Macedo and Prance 1978Macedo, M.; Prance, G.T. 1978. Notes on the vegetation of Amazonia II. The dispersal of plants in Amazonian white sand campinas: The campinas as functional islands. Brittonia, 30: 203-215.), the effect of fire (Vicentini 2004Vicentini, A. 2004. A vegetação ao longo de um gradiente edáfico no Parque Nacional do Jaú. In: Borges, S.H.; Iwanaga, S.; Durigan, C.C.; Pinheiro, M.R. (Ed.). Janelas para a biodiversidade no Parque Nacional do Jaú: uma estratégia para o estudo da biodiversidade na Amazônia. Fundação Vitória Amazônica, WWF, IBAMA, Manaus, p.117-143. ; Adeney et al. 2016Adeney, J.M.; Christensen, N.L.; Vicentini, A.; Cohn-Haft, M. 2016. White-sand Ecosystems in Amazonia. Biotropica, 48: 7-23.), past anthropogenic actions (Prance and Schubart 1978Prance, G.T.; Schubart, H.O.R. 1978. Nota preliminar sobre a origem das campinas abertas de areia branca do rio Negro. Acta Amazonica, 3: 567-570.) and differences in abiotic characteristics among patches (Tiessen et al. 1994Tiessen, H.; Chacon, P.; Cuevas, E. 1994. Phosphorus and nitrogen status in soils and vegetation along a toposequence of dystrophic rainforests on the upper Rio Negro. Oecologia, 99: 145-150.; Damasco et al. 2013Damasco, G.; Vicentini, A.; Castilho, C.V.; Pimentel, T.P.; Nascimento, H.E.M. 2013. Disentangling the role of edaphic variability, flooding regime and topography of Amazonian white-sand vegetation. Journal of Vegetation Science, 24: 384-394.; Adeney et al. 2016).

The dominance of just a few species, as found in this study, is common in WSV; the sum of the 10 most abundant species often exceeds 50% of all individuals (Boubli 2002Boubli, J.P. 2002. Lowland floristic assessment of Pico da Neblina National Park, Brazil. Plant Ecology, 160: 149-167.; Fine et al. 2010Fine, P.V.A.; García-Villacorta, R.; Pitman, N.C.A.; Mesones, I.; Kembel, S.W. 2010. A floristic study of the White-sand forests of Peru. Annals of the Missouri Botanical Garden, 97: 283-305.; Stropp et al. 2011Stropp, J.; Van Der Sleen, P.; Assunção, P.A.; Silva, A.L.; ter Steege, H. 2011. Tree communities of white-sand and terra-firme forests of the upper Rio Negro. Acta Amazonica, 41: 521-544.). This pattern also occurs in other Amazonian forest formations (Pitman et al. 2001Pitman, N.C.A.; Terborgh, J.W.; Silman, M.R.; Núñez, P.V.; Neill, D.A.; Cerón, C.E.; et al. 2001. Dominance and distribution of tree species in upper Amazonian Terra Firme forests. Ecology, 82: 2101-2117.; ter Steege et al. 2013ter Steege, H.; Pitman, N.C.A.; Sabatier, D.; Baraloto, C.; Salomão, R.P.; Guevara, J.E.; et al. 2013. Hyperdominance in the Amazonian Tree Flora. Science, 342: 325-336.). Only one species was among the 10 most dominant species in all patches, and only three were among the 10 most dominant species in at least two of the sampled patches. This disagrees with Fine et al. (2010) who, on a regional scale, proposed that dominant species in an area of WSV tend also to be dominant in other nearby WSV areas. However, the reduced spatial scale and the limited number of sampling units in our study preclude any further extrapolations.

Variations in edaphic characteristics change significantly the distribution and abundance of woody species in local environments (Comes and Grubb 1996; Clark et al. 1998Clark, D.B.; Clark, D.A.; Read, J. 1998. Edaphic variation and the mesoscale distribution of tree species in a neotropical rain forest. Journal of Ecology, 86: 101-112.; Tuomisto et al. 2003Tuomisto, H.; Ruokolainem, K.; Aguilar, M.; Sarmiento, A. 2003. Floristic patterns along a 43-km long transect in an Amazonian rain forest. Journal of Ecology, 91: 743-756.; John et al. 2007John, R.; Dalling, J.W.; Harms, K.E.; Yavitt, J.B.; Stallard, R.F.; Mirabello, M.; et al. 2007. Soil nutrients influence spatial distributions of tropical tree species. Proceedings of the National Academy of Sciences, 104: 864-869.), and our results showed that this effect occurs even among nearby white-sand forest patches, and should be investigated in more detail.

The sum of bases SB was the only parameter strongly linked to floristic composition. SB is a good indicator of soil fertility and was closely related to floristic composition in oligotrophic ecosystems (Assis et al. 2011Assis, M.A.; Prata, E.M.B.; Pedroni, F.; Sanchez, M.; Eisenlohr, P.V.; Martins, F.R.; et al. 2011. Florestas de restinga e de terras baixas na planície costeira do sudeste do Brasil: vegetação e heterogeneidade ambiental. Biota Neotropica, 11: 103-121.). In other vegetation types on less oligotrophic soils, SB was also the best predictor of species composition (Ruggiero et al. 2002Ruggiero, P.G.C.; Batalha, M.A.; Pivello, V.R.; Meirelles, S.T. 2002. Soil-vegetation relationships in cerrado (Brazilian savanna) and semideciduous forest, Southeastern Brazil. Plant Ecology, 160: 1-16.; Zuquim et al. 2014Zuquim, G.; Tuomisto, H.; Jones, M.M.; Prado, J.; Figueiredo, F.O.G.; Moulatlet, G.M.; et al. 2014. Predicting environmental gradients with fern species composition in Brazilian Amazonia. Journal of Vegetation Science, 25: 1195-1207.). SB is composed of macronutrients that influence directly the basic processes of plants, such as hydration regulation, stomatal movement and photosynthesis, having an essential role in all stages of plant development (Larcher 2000Larcher, W. 2000. Ecofisiologia vegetal. RiMa Artes e Textos, São Carlos, 531p.). The presence and quantity of the elements that compose the SB are directly related to other soil parameters such as soil texture and variation in groundwater level. Although soil texture is not a physiologically important edaphic factor, elements such as silt and clay may increase water-holding and nutrient retention capacity (Mendonça et al. 2015Mendonça, B.A.F.; Filho, E.I.F.; Schaefer, C.E.G.R.; Simas, F.N.B.; Paula, M.D. 2015. Os solos das Campinaranas na Amazônia Brasileira: Ecossistemas arenícolas oligotróficos. Ciência Florestal, 25: 827-839.). The continuous variation in groundwater level, intrinsically related to soil properties, leaches the soil components to lower layers (Franco and Dezzeo 1994Franco, W.; Dezzeo, N. 1994. Soils and soil-water regime in the terra-firme-caatinga forest complex near San Carlos de Rio Negro, state of Amazonas, Venezuela. Interciencia, 19: 305-316.). Thus, the interaction between texture and groundwater level is essential to predict soil fertility and species composition (Targhetta et al. 2015Targhetta, N.; Kesselmeier, J.; Wittmann, F. 2015. Effects of the hydroedaphic gradient on tree species composition and aboveground wood biomass of oligotrophic forest ecosystems in the central Amazon basin. Folia Geobotanica, 50: 185-205.).

The variation in SB was significantly related to species composition, but it was not related to species richness nor vegetation structure. In the WSV of Viruá National Park, soil fertility directly influenced the vegetation structure in different phytophysiognomies and may counterbalance the negative effects of flooding (Damasco et al. 2013Damasco, G.; Vicentini, A.; Castilho, C.V.; Pimentel, T.P.; Nascimento, H.E.M. 2013. Disentangling the role of edaphic variability, flooding regime and topography of Amazonian white-sand vegetation. Journal of Vegetation Science, 24: 384-394.). In our study soil fertility in white-sand forest patches was less variable than in Viruá NP, but was nevertheless enough to influence floristic composition.

This lack of relation between soil fertility and vegetation structure may reflect the need for plants growing in oligotrophic environments to allocate much of their energy to form secondary compounds for defending themselves against herbivory, in detriment of both growth in height and diameter (Jansen 1974; Fine et al. 2006Fine, L.V.; Miller, Z.J.; Mesones, I.; Irazuzta, S.; Appel, H.M.; Stevens, M.H.H.; et al. 2006. The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology, 87: 150-162.). It also suggests that other factors rather than soil may be involved in structuring the vegetation.

A significant change in species composition related to small changes in soil parameters is compatible with the extreme condition experienced by WSV. In addition to the extreme nutrient poverty of the soil, seasonal hydric saturation can act as an additional filter, selecting species capable of surviving periods of soil anoxia (Parolin and Wittmann 2010Parolin, P.; Wittmann, F. 2010. Struggle in the flood: tree responses to flooding stress in four tropical floodplain systems. AoB Plants, v2010: plq003.; Piedade et al. 2013Piedade, M.T.F.; Schöngart, J.; Wittmann, F.; Parolin, P.; Junk, W.J. 2013. Impactos da inundação e seca na vegetação de áreas alagáveis amazônicas. In: Borma, L.S.; Nobre, C.A. (Org.). Secas na Amazônia: causas e consequências. São Paulo, Oficina de Textos, p.268-305.). In contrast, periods of moisture loss accentuated by high light penetration, high porosity and low water retention capacity of sandy soils, can subject WSV to physiological constraints during the dry season, when effective drought conditions prevail (Franco and Dezzeo 1994Franco, W.; Dezzeo, N. 1994. Soils and soil-water regime in the terra-firme-caatinga forest complex near San Carlos de Rio Negro, state of Amazonas, Venezuela. Interciencia, 19: 305-316.; Vicentini 2004Vicentini, A. 2004. A vegetação ao longo de um gradiente edáfico no Parque Nacional do Jaú. In: Borges, S.H.; Iwanaga, S.; Durigan, C.C.; Pinheiro, M.R. (Ed.). Janelas para a biodiversidade no Parque Nacional do Jaú: uma estratégia para o estudo da biodiversidade na Amazônia. Fundação Vitória Amazônica, WWF, IBAMA, Manaus, p.117-143. ).

Our results highlight the role of edaphic variations in promoting species composition heterogeneity in white-sand forest patches. In this extremely nutrient-poor ecosystem, any nutrient addition may change the habitat partitioning of component species, and therefore may cause changes in species distribution and assemblage composition (Grubb 1977Grubb, P.J. 1977. The Maintenance of Species-richness in Plant Communities: The Importance of the Regeneration Niche. Biological Reviews, 52: 107-145.; Oliveira et al. 2014Oliveira, A.A.; Vicentini, A.; Chave, J.; Castanho, C.T.; Davies, S.J.; Martini, A.M.Z. et al. 2014. Habitat specialization and phylogenetic structure of tree species in a coastal Brazilian white-sand forest. Journal of Plant Ecology, 7:134-144.). The differentiation of species composition based on minor resource variations may be an important mechanism for niche differentiation in plant communities.

CONCLUSIONS

We detected significant differences among white-sand forest patches located at about 4 km from each other in an area in the central Brazilian Amazon. Sampling plots within patches tended to have similar species composition. We also found that small differences in soil parameters explained species composition heterogeneity in the white-sand forest patches, reflected in the large number of species (51.4%) that were exclusive to only one patch. Changes in the sum of bases were likely to be linked to species composition variation. Although these changes do not necessarily influence species richness and other structural parameters, they may be related to differential responses of a species abundance, or whether it is present or absent from a white-sand area.

ACKNOWLEDGEMENTS

We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES for the first author’s scholarship, Aline Lopes received scholarship from the Programa de Apoio à Fixação de Doutores no Amazonas - FIXAM/AM. We also would like to thank the Fundação de Amparo à Pesquisa do Estado do Amazonas - FAPEAM (public call: 021/2011) and Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq/PELD-MAUA (grant number: 403792/2012-6) for financing the research, as well as Instituto Nacional de Pesquisas da Amazônia -INPA and MAUA-INPA technicians for all the support. Special thanks to the SDR Tupé dwellers for the hospitality, Affonso Henrique, Bruno Cintra, Paula Guarido, Álvaro Bastos, Diego Ken, José Ferreira, Marco Volpato and David Marical for helping in the field, Antônio Mello, José Ramos, Mario Terra, Fátima Melo, Alberto Vicentini, André Correa, and Jhennyffer Alves for helping to identify the plants, and Maria Julia Ferreira for editing the figures.

  • Adeney, J.M.; Christensen, N.L.; Vicentini, A.; Cohn-Haft, M. 2016. White-sand Ecosystems in Amazonia. Biotropica, 48: 7-23.
  • Anderson, A.B.; Prance, G.T.; Albuquerque, B.W.P. 1975. Estudos sobre as vegetações de Campinas Amazônica III: a vegetação lenhosa da Campina da Reserva Biológica INPA-SUFRAMA (Manaus-Caracaraí, km 62). Acta Amazonica, 5: 225-246.
  • Anderson, A.B. 1981. White-sand vegetation of Brazilian Amazonia. Biotropica, 13: 199-210.
  • APG IV. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181: 1-20.
  • Assis, M.A.; Prata, E.M.B.; Pedroni, F.; Sanchez, M.; Eisenlohr, P.V.; Martins, F.R.; et al 2011. Florestas de restinga e de terras baixas na planície costeira do sudeste do Brasil: vegetação e heterogeneidade ambiental. Biota Neotropica, 11: 103-121.
  • Borcard, D.; Gillet, F.; Legendre, P. 2011. Numerical Ecology with R Springer, New York, 306p.
  • Boubli, J.P. 2002. Lowland floristic assessment of Pico da Neblina National Park, Brazil. Plant Ecology, 160: 149-167.
  • Braga, P.I.S. 1979. Subdivisão fitogeográfica, tipos de vegetação, conservação e inventário florístico da Floresta Amazônica. Acta Amazonica, 9: 53-80.
  • Bongers, F.; Engelen, D.; Klinge, H. 1985. Phytomass structure of natural plant communities on spodosols in southern Venezuela: the Bana woodland. Vegetatio, 63: 13-34.
  • Clark, D.B.; Clark, D.A.; Read, J. 1998. Edaphic variation and the mesoscale distribution of tree species in a neotropical rain forest. Journal of Ecology, 86: 101-112.
  • Coomes, D.A.; Grubb, P.J. 1996. Amazonian caatinga and related communities at La Esmeralda, Venezuela: forest structure, physiognomy and floristics, and control by soil factors. Vegetatio, 122: 167-191.
  • Coomes, D.A. 1997. Nutrient status of Amazonian caatinga forests in a seasonally dry area: nutrient fluxes in litter fall and analyses of soils. Canadian Journal of Forest Research, 27: 831-839.
  • Coronado, E.N.H.; Baker, T.R.; Phillips, O.L.; Pitman, N.C.A.; Pennington, R.T.; Martínez, R.V.; et al 2009. Multi-scale comparisons of tree composition in Amazonian Terra Firme Forests. Biogeosciences, 6: 2719-2731.
  • Curtis, J.T.; McIntosh, R.P. 1951. An upland forest continuum in the prairie-forest border region of Wisconsin. Ecology, 32: 476-496.
  • Damasco, G.; Vicentini, A.; Castilho, C.V.; Pimentel, T.P.; Nascimento, H.E.M. 2013. Disentangling the role of edaphic variability, flooding regime and topography of Amazonian white-sand vegetation. Journal of Vegetation Science, 24: 384-394.
  • Embrapa. 1997. Manual de Métodos de Análise de Solos 2da ed., Centro Nacional de Pesquisa de Solos, Rio de Janeiro, 212p.
  • Ferreira, C.A.C. 2009. Análise comparativa de vegetação lenhosa do ecossistema campina na Amazônia brasileira PhD thesis, Instituto Nacional de Pesquisas da Amazônia, Universidade Federal do Amazonas, Manaus, Brazil, 277p.
  • Fine, L.V.; Miller, Z.J.; Mesones, I.; Irazuzta, S.; Appel, H.M.; Stevens, M.H.H.; et al 2006. The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology, 87: 150-162.
  • Fine, P.V.A.; García-Villacorta, R.; Pitman, N.C.A.; Mesones, I.; Kembel, S.W. 2010. A floristic study of the White-sand forests of Peru. Annals of the Missouri Botanical Garden, 97: 283-305.
  • Fine, P.V.A.; Baraloto, C. 2016. Habitat Endemism in White-sand Forests: Insights into the Mechanisms of Lineage Diversification and Community Assembly of the Neotropical Flora. Biotropica, 48: 24-33.
  • Franco, W.; Dezzeo, N. 1994. Soils and soil-water regime in the terra-firme-caatinga forest complex near San Carlos de Rio Negro, state of Amazonas, Venezuela. Interciencia, 19: 305-316.
  • Gentry, A.H. 1988. Changes in plant community diversity and floristic composition on enviromental and geographical gradients. Annals of the Missouri Botanical Garden, 75: 1-34.
  • Grubb, P.J. 1977. The Maintenance of Species-richness in Plant Communities: The Importance of the Regeneration Niche. Biological Reviews, 52: 107-145.
  • Guevara, J.E.; Damasco, G.; Baraloto, C.; Fine, P.V.A.; Peñuela, M.C.; Castilho, C. et al 2016. Low Phylogenetic Beta Diversity and Geographic Neo-endemism in Amazonian White-sand Forests. Biotropica, 48: 34-46.
  • Heyligers, P.C. 1963. Vegetation and soil of a White-Sand Savanna in Suriname. Mededelingen van het Botanisch Museum en Herbarium van de Rijksuniversiteit te Utrecht, 191: 1-148.
  • Hubbell, S.P.; He, F.; Condit, R.; Borda-de-Água, L.; Kellner, J.; ter Steege, H. 2008. How many tree species are there in the Amazon and how many of them will go extinct? Proceedings of the National Academy of Sciences, 105: 11498-11504.
  • IBGE. 2012. Manual Técnico da Vegetação brasileira 2da ed., Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro, 275p.
  • Janzen, D. 1974. Tropical blackwater rivers, animals and mast fruiting by Dipterocarpaceae. Biotropica, 6: 69-103.
  • John, R.; Dalling, J.W.; Harms, K.E.; Yavitt, J.B.; Stallard, R.F.; Mirabello, M.; et al 2007. Soil nutrients influence spatial distributions of tropical tree species. Proceedings of the National Academy of Sciences, 104: 864-869.
  • Junk, W.J.; Piedade, M.T.F.; Schöngart, J.; Cohn-Haft, M.; Adeney, J.M.; Wittmann, F. 2011. A classification of major naturally-occurring Amazonian lowland wetlands. Wetlands, 31: 623:640.
  • Kubitzki, K. 1989a. The ecogeographical differentiation of Amazon inundation forests. Plant Systematics and Evolution, 162: 285-304.
  • Kubitzki, K. 1989b. Amazon lowland and Guayana highland - historical and ecological aspects of the development of their floras. Amazoniana, 11: 1-12.
  • Larcher, W. 2000. Ecofisiologia vegetal RiMa Artes e Textos, São Carlos, 531p.
  • Luizão, F.J.; Luizão, R.C.C.; Proctor, J. 2007. Soil acidity and nutrient deficiency in central Amazonian heath forest soils. Plant Ecology, 192: 209-224.
  • Macedo, M.; Prance, G.T. 1978. Notes on the vegetation of Amazonia II. The dispersal of plants in Amazonian white sand campinas: The campinas as functional islands. Brittonia, 30: 203-215.
  • Magnusson, W.E; Mourão, G. 2005. Estatística sem Matemática 2da ed., Publisher Planta, Londrina, 138p.
  • Mendonça, B.A.F.; Filho, E.I.F.; Schaefer, C.E.G.R.; Simas, F.N.B.; Paula, M.D. 2015. Os solos das Campinaranas na Amazônia Brasileira: Ecossistemas arenícolas oligotróficos. Ciência Florestal, 25: 827-839.
  • Oksanen, J.F.; Blanchet, G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’Hara, R.B.; et al 2013. vegan: Community Ecology Package, R package version 2.0-7. (http://CRAN.R-project.org/package=vegan).
    » http://CRAN.R-project.org/package=vegan
  • Oliveira, A.A.; Vicentini, A.; Chave, J.; Castanho, C.T.; Davies, S.J.; Martini, A.M.Z. et al 2014. Habitat specialization and phylogenetic structure of tree species in a coastal Brazilian white-sand forest. Journal of Plant Ecology, 7:134-144.
  • Parolin, P.; Wittmann, F. 2010. Struggle in the flood: tree responses to flooding stress in four tropical floodplain systems. AoB Plants, v2010: plq003.
  • Piedade, M.T.F.; Schöngart, J.; Wittmann, F.; Parolin, P.; Junk, W.J. 2013. Impactos da inundação e seca na vegetação de áreas alagáveis amazônicas. In: Borma, L.S.; Nobre, C.A. (Org.). Secas na Amazônia: causas e consequências São Paulo, Oficina de Textos, p.268-305.
  • Pires, J.M.; Prance, G.T. 1985. The vegetation types of the Brazilian Amazon. In: Prance, G.T.; Lovejoy, T.E. (Ed.). Key Enviroments: Amazonia Oxford, Pergamon Press, p.109-145.
  • Pitman, N.C.A.; Terborgh, J.W.; Silman, M.R.; Núñez, P.V.; Neill, D.A.; Cerón, C.E.; et al 2001. Dominance and distribution of tree species in upper Amazonian Terra Firme forests. Ecology, 82: 2101-2117.
  • Prance, G.T.; Schubart, H.O.R. 1978. Nota preliminar sobre a origem das campinas abertas de areia branca do rio Negro. Acta Amazonica, 3: 567-570.
  • Prance, G.T.; Daly, D. 1989. Brasilian Amazon. In: Campbell, D.G.; Hammond, H.D. (Ed.). Floristic inventory of tropical countries New York Botanical Garden, New York, p.523-533.
  • Prance, G.T. 1996. Islands in Amazonia. Philosophical Transactions of the Royal Society of London. Series B, 351: 823-833.
  • R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (http://www.R-project.org/).
    » http://www.R-project.org/
  • Radam Brasil. 1978. Levantamento de recursos naturais v.18. Folha SA. 20 Manaus, Departamento Nacional de Produção Mineral, Rio de Janeiro, 747p.
  • Reflora - Flora do Brasil 2020 em construção. Jardim Botânico do Rio de Janeiro. ( (http://floradobrasil.jbrj.gov.br/ ). Accessed on 22/05/2017.
    » http://floradobrasil.jbrj.gov.br/
  • Richardt, K.; Santos, A.; Nascimento-Filho, V.; Bacc, O.O.S. 1975. Movimento de água subterrânea em ecossistema Campina Amazônica. Acta Amazonica, 6: 229-290.
  • Ruggiero, P.G.C.; Batalha, M.A.; Pivello, V.R.; Meirelles, S.T. 2002. Soil-vegetation relationships in cerrado (Brazilian savanna) and semideciduous forest, Southeastern Brazil. Plant Ecology, 160: 1-16.
  • Scudeller, V.V.; Aprile, F.M.; Melo, S.; Santos-Silva, E.N. 2005. Reserva de Desenvolvimento Sustentável do Tupé: características gerais. In: Santos-Silva, E.N.; Aprile, F.M.; Scudeller, V.V.; Melo, S. (Org.). Biotupé: Meio físico, diversidade biológica e sociocultural do Baixo Rio Negro, Amazônia Central Instituto Nacional de Pesquisas da Amazônia, Manaus, p. XI-XXI.
  • Shepherd, G.J. 2010. Fitopac - Manual do usuário Departamento de Botânica, Universidade Estadual de Campinas, Campinas, Brazil, 91p.
  • Sobrado, M.A. 2009. Leaf tissue water relations and hydraulic properties of sclerophyllous vegetation on white sands of the upper Rio Negro in the Amazon region. Journal of Tropical Ecology, 25: 271-280.
  • Stropp, J.; Van Der Sleen, P.; Assunção, P.A.; Silva, A.L.; ter Steege, H. 2011. Tree communities of white-sand and terra-firme forests of the upper Rio Negro. Acta Amazonica, 41: 521-544.
  • Targhetta, N.; Kesselmeier, J.; Wittmann, F. 2015. Effects of the hydroedaphic gradient on tree species composition and aboveground wood biomass of oligotrophic forest ecosystems in the central Amazon basin. Folia Geobotanica, 50: 185-205.
  • ter Steege, H.; Pitman, N.C.A.; Sabatier, D.; Baraloto, C.; Salomão, R.P.; Guevara, J.E.; et al 2013. Hyperdominance in the Amazonian Tree Flora. Science, 342: 325-336.
  • Tiessen, H.; Chacon, P.; Cuevas, E. 1994. Phosphorus and nitrogen status in soils and vegetation along a toposequence of dystrophic rainforests on the upper Rio Negro. Oecologia, 99: 145-150.
  • Tuomisto, H.; Ruokolainem, K.; Aguilar, M.; Sarmiento, A. 2003. Floristic patterns along a 43-km long transect in an Amazonian rain forest. Journal of Ecology, 91: 743-756.
  • Veloso, H.P.; Rangel Filho, A.L.R.; Lima, J.C.A. 1991. Classificação da vegetação brasileira, adaptada a um sistema universal Instituto Brasileiro de Geografia e Estatística, Rio de Janeiro , 124p.
  • Vicentini, A. 2004. A vegetação ao longo de um gradiente edáfico no Parque Nacional do Jaú. In: Borges, S.H.; Iwanaga, S.; Durigan, C.C.; Pinheiro, M.R. (Ed.). Janelas para a biodiversidade no Parque Nacional do Jaú: uma estratégia para o estudo da biodiversidade na Amazônia Fundação Vitória Amazônica, WWF, IBAMA, Manaus, p.117-143.
  • Zuquim, G.; Tuomisto, H.; Jones, M.M.; Prado, J.; Figueiredo, F.O.G.; Moulatlet, G.M.; et al 2014. Predicting environmental gradients with fern species composition in Brazilian Amazonia. Journal of Vegetation Science, 25: 1195-1207.

  • ASSOCIATE EDITOR:

    Natália Ivanauskas
  • CITE AS:

    Demarchi, L.O.; Scudeller, V.V.; Moura, L.C.; Dias-Terceiro, R.G.; Lopes, A.; Wittmann, F.K.; Piedade, M.T.F. 2018. Floristic composition, structure and soil-vegetation relations in three white-sand soil patches in central Amazonia. Acta Amazonica, 48: 46-56. doi: 10.1590/1809-4392201603523.

SUPPLEMENTARY MATERIAL

(only available in the electronic version)

DEMARCHI et al. Floristic composition, structure and soil-vegetation relations in three white-sand soil patches in central Amazonia.

Table S1
Correlation matrix of soil parameters collected in three white-sand vegetation patches in Tupé Sustainable Development Reserve, in the central Brazilian Amazon.

Table S2
Phytosociological parameters of species found in the three areas of white-sand vegetation sampled in Tupé Sustainable Development Reserve, central Brazilian Amazon. N. = number of individuals, N Par = number of parcels in wich species occurred, RDe = Relative Density, RDo = Relative Dominance, RFr = Relative Frequency, IVI = Importance Value Index. Voucher number refers to material deposited in the herbaria of Instituto Nacional de Pesquisas da Amazônia (INPA) and Instituto Federal do Amazonas (EAFM).

Publication Dates

  • Publication in this collection
    Jan-Mar 2018

History

  • Received
    30 Dec 2016
  • Accepted
    04 Sept 2017
Instituto Nacional de Pesquisas da Amazônia Av. André Araujo, 2936 Aleixo, 69060-001 Manaus AM Brasil, Tel.: +55 92 3643-3030, Fax: +55 92 643-3223 - Manaus - AM - Brazil
E-mail: acta@inpa.gov.br