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Environmental factors driving plant trait distributions in coastal zones of Atlantic Forest

Abstract

Environmental filtering has been defined as the effect of environmental gradients on species in a plant community and can be the dominant driver of community assembly. Here, we evaluate the relationship between plant communities and the environment in the Restinga vegetation. For this, we measured 11 functional traits of plant species present along transects covering a marked edaphic environmental gradient. This gradient was characterized through Principal Component Analysis of soil characteristics. The relationships between the edaphic gradient and functional traits were evaluated using linear models. Finally, we compared the contributions of species turnover and intraspecific variation to among-site variation in functional traits. The gradients associated with soil nutrients (PCA axis 1) and soil acidity and organic matter (PCA axis 2) were then used to test the observed changes in community composition and were significant predictors of the distribution of water potential, leaf dry matter content and K content, height and chlorophyll index. Decomposing the total variation in the distribution of functional traits between species turnover and intraspecific variation revealed that species turnover explains a greater proportion of the observed variation. We conclude that community assembly is strongly limited by environmental filters and mediated by functional traits at the species level.

Key words
assembly rules; community composition; dune; functional trait; Restinga; turnover

Resumo

A filtragem ambiental é o efeito dos gradientes ambientais nas espécies e pode ser o principal fator de montagem de comunidades de plantas. Aqui, avaliamos a relação entre comunidades vegetais e o solo na vegetação Restinga do nordeste do Brasil. Para isso, medimos 11 características funcionais das espécies vegetais presentes ao longo dos transectos, cobrindo um gradiente ambiental marcado. Este gradiente foi caracterizado através da Análise de Componentes Principais (PCA) da composição química do solo. As relações entre o gradiente edáfico e as características funcionais foram avaliadas usando modelos lineares. Finalmente, comparamos as contribuições da substituição de espécies e variação intraespecífica na comunidade vegetal. Os gradientes associados aos nutrientes do solo (eixo 1 da PCA) e acidez do solo e matéria orgânica (eixo 2 da PCA) foram então utilizados para testar as mudanças observadas na composição da comunidade e uma relação significativa foi encontrada com o eixo 2. Os eixos foram preditores significativos da distribuição da altura, teor de clorofila, potencial hídrico, massa seca e teor de K. A decomposição da variação total na distribuição de características funcionais entre a rotatividade de espécies e a variação intraespecífica revelou que a rotatividade de espécies explica uma proporção maior da variação observada. Concluímos que a montagem da comunidade é fortemente limitada por filtros ambientais e mediada por características funcionais no nível das espécies.

Palavras-chave
regras de montagem; estrutura da comunidade; duna; atributos funcionais; Restinga; variação interespecífica

Introduction

A central goal of ecology is to understand the processes that influence community assembly and that control species distributions across environmental gradients (McGill et al. 2006McGill BJ, Enquist BJ, Weiher E & Westoby M (2006) Rebuilding community ecology from functional traits. Trends in Ecology & Evolution 21: 178-85.; Fortunel et al. 2014Fortunel C, Paine CET, Fine PVA, Kraft NJB, Baraloto C & Firme T (2014) Environmental factors predict community functional composition in Amazonian forests. Journal of Ecology 102: 145-155.). Two contrasting deterministic processes have been implicated in structuring plant communities: environmental filters (Weiher & Keddy 1995Weiher E & Keddy PA (1995) Assembly rules, null models, and trait dispersion: new questions from old patterns. Oikos 74: 159-164.; Cornwell et al. 2006Cornwell WK, Schwilk DW & Ackerly DD (2006) A trait-based test for habitat filtering: convex hull volume. Ecology 87: 1465-1471.) and limiting similarity (MacArthur & Levins 1967MacArthur R & Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist 101: 377-385.; Stubbs & Wilson 2004Stubbs WJ & Wilson JB (2004) Evidence for limiting similarity in a sand dune community. Journal of Ecology 92: 557-567.). In relation to the former, community assemblage can be conceptualized as consequence of successive environmental filters which exclude species lacking certain functional traits (adaptations to local abiotic/biotic conditions) from the species pool (Kraft et al. 2015Kraft NJB, Adler PB, Godoy O, James EC, Fuller S & Levine JM (2015) Community assembly, coexistence and the environmental filtering metaphor. Functional Ecology 29: 592-599.). As a consequence, species within a filtered community tend to have similar functional attributes that allow them to survive within the environment. In contrast, the concept of limiting similarity suggests that co-occurring species need to have somewhat different ecological strategies (and traits) in order to avoid high levels of interspecific competition (MacArthur & Levins 1967MacArthur R & Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. The American Naturalist 101: 377-385.).

Functional traits can represent ecological strategies and determine how plants respond to environmental factors (Pérez-Harguindeguy et al. 2013Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, De Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, Ter Steege H, Van Der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti M V., Conti G, Staver AC, Aquino S & Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61: 167-234.). The distribution of traits in the community should therefore broadly reflect processes that structure plant communities (Bochet & García-Fayos 2015Bochet E & García-Fayos P (2015) Identifying plant traits: A key aspect for species selection in restoration of eroded roadsides in semiarid environments. Ecological Engineering 83: 444-451.). It follows that trait distributions should change along environmental gradients because of environmental filtering, adaptive phenotypic plasticity [e.g., individuals of many plant species are taller in fertile habitat (Lepš et al. 2011Lepš J, de Bello F, Šmilauer P & Doležal J (2011) Community trait response to environment: Disentangling species turnover vs intraspecific trait variability effects. Ecography (Cop) 34: 856-863.)], or a combination of these two effects ( Lepš et al. 2011Lepš J, de Bello F, Šmilauer P & Doležal J (2011) Community trait response to environment: Disentangling species turnover vs intraspecific trait variability effects. Ecography (Cop) 34: 856-863.; Siefert et al. 2014Siefert A, Fridley JD & Ritchie ME (2014) Community functional responses to soil and climate at multiple spatial scales: When does intraspecific variation matter? PLoS One 9: e111189.; Zuo et al. 2017Zuo X, Yue X, Lv P, Yu Q, Chen M, Zhang J, Luo Y, Wang S & Zhang J (2017) Contrasting effects of plant inter- and intraspecific variation on community trait responses to restoration of a sandy grassland ecosystem. Ecology and Evolution 7: 1125-1134.).

Numerous studies examining community assembly have focused on trait variation due to changes in species composition along environmental gradients, because it typically involves clear and easily measurable differences in trait values among species ( Lepš et al. 2011Lepš J, de Bello F, Šmilauer P & Doležal J (2011) Community trait response to environment: Disentangling species turnover vs intraspecific trait variability effects. Ecography (Cop) 34: 856-863.; Kichenin et al. 2013Kichenin E, Wardle DA, Peltzer DA, Morse CW & Freschet GT (2013) Contrasting effects of plant inter- and intraspecific variation on community-level trait measures along an environmental gradient. Functional Ecology 27: 1254-1261.). However, recent studies have shown that intraspecific variation may also play an important role in community trait responses to environmental variation (Jung et al. 2010Jung V, Violle C, Mondy C, Hoffmann L & Muller S (2010) Intraspecific variability and trait-based community assembly. Journal of Ecology 98: 1134-1140.; De Bello et al. 2011De Bello F, Lavorel S, Albert CH, Thuiller W, Grigulis K, Dolezal J, Janeček Š & Lepš J (2011) Quantifying the relevance of intraspecific trait variability for functional diversity. Methods in Ecology and Evolution 2: 163-174.; Siefert et al. 2015Siefert A, Violle C, Chalmandrier L, Albert CH, Taudiere A, Fajardo A, Aarssen LW, Baraloto C, Carlucci MB, Cianciaruso M V., de L. Dantas V, de Bello F, Duarte LDS, Fonseca CR, Freschet GT, Gaucherand S, Gross N, Hikosaka K, Jackson B, Jung V, Kamiyama C, Katabuchi M, Kembel SW, Kichenin E, Kraft NJB, Lagerström A, Bagousse-Pinguet Y Le, Li Y, Mason N, Messier J, Nakashizuka T, Overton JM, Peltzer DA, Pérez-Ramos IM, Pillar VD, Prentice HC, Richardson S, Sasaki T, Schamp BS, Schöb C, Shipley B, Sundqvist M, Sykes MT, Vandewalle M & Wardle DA (2015) A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecology Letters 18: 1406-1419.; Zorger et al. 2019Zorger BB, Tabarelli M, de Queiroz RT, Rosado BHP & Pinho BX (2019) Functional organization of woody plant assemblages along precipitation and human disturbance gradients in a seasonally dry tropical forest. Biotropica 51: 838-850.). While some researchers have proposed that competition for limited resources is the main driver of intraspecific trait variation of co-occurring species ( Lepš et al. 2011Lepš J, de Bello F, Šmilauer P & Doležal J (2011) Community trait response to environment: Disentangling species turnover vs intraspecific trait variability effects. Ecography (Cop) 34: 856-863.; Auger & Shipley 2013Auger S & Shipley B (2013) Inter-specific and intra-specific trait variation along short environmental gradients in an old-growth temperate forest. Journal of Vegetation Science 24: 419-428.), others have suggested that environment filtering is the dominant driver of community assembly (Barros et al. 2017Barros MF, Pinho BX, Leão T & Tabarelli M (2017) Soil attributes structure plant assemblages across an Atlantic forest mosaic. Journal of Plant Ecology 11: 613-622.; Zhang et al. 2018Zhang H, Chen HYH, Lian J, John R, Ronghua L, Liu H, Ye W, Berninger F & Ye Q (2018) Using functional trait diversity patterns to disentangle the scale-dependent ecological processes in a subtropical forest. Functional Ecology 32: 1379-1389.).

In heterogeneous environments such as sand dune ecosystems, vegetation mosaics are often associated with environmental filtering imposed by strong edaphic gradients (Cardoso & Lomônaco 2003Cardoso G & Lomônaco C (2003) Variações fenotípicas e potencial plástico de Eugenia calycina Cambess. (Myrtaceae) em uma área de transição cerrado-vereda. Rev Bras Botânica. Brazilian Journal of Botany 26: 131-140.). The mosaic of plant communities of the coastal zones of Brazil, generally known as Restinga, is a good example of such a heterogeneous habitat subject to intense biophysical selection pressures. Specifically, Restinga communities are subject to a wide array of environmental conditions, such as high temperatures, flooding, high salinity and lack of nutrients (Assumpção & Nascimento 2000Assumpção J & Nascimento MT (2000) Estrutura e composição florística de quatro formações vegetais de restinga no complexo lagunar Grussaí/Iquipari, São João da Barra, RJ, Brasil. Acta Botanica Brasilica 14: 301-315.; Scarano 2002Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Annals of Botany 90: 517-524.). Plant survival and reproduction is therefore closely associated with levels of soil exposure, edaphic factors, and vegetation critical mass required to stabilize nutrient relations of the system (Reinert et al. 1997Reinert F, Roberts a, Wilson JM, Deribas L, Cardinot G & Griffith H (1997) Gradation in nutrient composition and photosynthetic pathways across the restinga vegetation of Brazil. Acta Botanica Brasilica 110: 135-142.). Thus, the Restinga ecosystem provides an interesting opportunity to evaluate the role of environmental filtering in plant community composition, and to compare the relative importance of intraspecific variation and species turnover in determining functional trait distributions.

Several studies have already focused on functional trait variation and distribution contributes to structure the diverse communities of species rich tropical plant communities through differential niche-based processes (Kraft et al. 2008Kraft NJB, Valencia R & Ackerly DD (2008) Functional traits and niche-based tree community assembly in an Amazonian forest. Science 322: 580-582.; Malhado et al. 2009Malhado ACM, Whittaker RJ, Malhi Y, Ladle RJ, ter Steege H, Butt N, Aragao LEOC, Quesada CA, Murakami-Araujo A, Phillips OL, Peacock J, Lopez-Gonzalez G, Baker TR, Anderson LO, Arroyo L, Almeida S, Higuchi N, Killeen TJ, Monteagudo A, Neill DA, Pitman NCA, Prieto A, Salomao RP, Vasquez R, Laurance WF & Ramirez H (2009) Spatial distribution and functional significance of leaf lamina shape in Amazonian forest trees. Biogeosciences 6: 1577-1590.; Neyret et al. 2016Neyret M, Bentley LP, Oliveras I, Marimon BS, Marimon-Junior BH, Almeida de Oliveira E, Barbosa Passos F, Castro Ccoscco R, dos Santos J, Matias Reis S, Morandi PS, Rayme Paucar G, Robles Cáceres A, Valdez Tejeira Y, Yllanes Choque Y, Salinas N, Shenkin A, Asner GP, D??az S, Enquist BJ & Malhi Y (2016) Examining variation in the leaf mass per area of dominant species across two contrasting tropical gradients in light of community assembly. Ecology and Evolution 6: 5674-5689.). Although some studies carried out on sandy soil and Restingas have demonstrated functional responses of plants to different environmental conditions (see Mahdavi & Bergmeier 2016Mahdavi P & Bergmeier E (2016) Plant functional traits and diversity in sand dune ecosystems across different biogeographic regions. Acta Oecologica 74: 37-45.; Rosado & De Mattos 2010Rosado B enrique P & De Mattos EA (2010) Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.; Scarano 2002Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Annals of Botany 90: 517-524.; Scarano et al. 2001Scarano FR, Duarte HM, Ribeiro KT, Rodrigues PJFP, Barcellos EMB, Franco AC, Brulfert J, DelÉens E & Lüttge U (2001) Four sites with contrasting environmental stress in southeastern Brazil: Relations of species, life form diversity, and geographic distribution to ecophysiological parameters. Botanical Journal of the Linnean Society 136: 345-364.), information on how species turnover and intraspecific variation contribute to these responses is still lacking. Preliminary observations suggest that the distribution of plant traits in Restinga systems may be strongly influenced by edaphic factors, such as pH, aluminium content, organic matter and salinity (Giaretta et al. 2013Giaretta A, Menezes LFT De & Pereira OJ (2013) Structure and floristic pattern of a coastal dunes in southeastern Brazil. Acta Botanica Brasilica 27: 87-107.; Santos-Filho et al. 2013Santos-Filho FS, Almeida Jr E & Zickel CS (2013) Do edaphic aspects alter vegetation structures in the Brazilian restinga? Acta Botanica Brasilica 27: 613-623.). Given the strong environmental gradients present in the Restinga, we hypothesized that environmental filters play a significant role in community composition, mediated by the distribution of functional traits associated with survival-related pathways. Specifically, we predict that: 1) there will be significant changes in community composition in response to observed environmental gradients; 2) changes in community composition will reflect the distribution of plant functional traits along the same environmental gradients, and; 3) observed functional changes will be mostly driven by community turnover rather than intraspecific variation.

Materials and Methods

Study area and collection

We conducted this study in six plots (50 × 200 m) distributed in two Restingas areas (09º42’S, 35º47’W; 09º47’S, 35º52’W) in the Santa Rita Sustainable Development Reserve, Northeast Brazil. This reserve is within an area has a typical tropical climate, with a mean annual temperature around 24.7 °C and mean annual precipitation of 1,726 mm. The natural vegetation is characterized by a mosaic of plant communities that occupy sandy plains formed by marine deposits of the late Quaternary which lie between the sea and the tabuleiros (large, flat areas formed from Tertiary deposits of crystalline rock) occupied by Atlantic Forest (Scarano 2002Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Annals of Botany 90: 517-524.). The first vegetation encountered along the beach-to-inland gradient is a narrow strip of beach vegetation, in which creeping psammophytes grow on the shifting sands of the upper part of the beach. Behind these embryo dunes is the foredune, a slightly higher and older beach ridge dominated by grasses (Castanho et al. 2012Castanho CT, Oliveira AA & Ina P (2012) The importance of plant life form on spatial associations along a subtropical coastal dune gradient. Journal of Vegetation Science 23: 952-961.).

Based on Reinert et al. (1997)Reinert F, Roberts a, Wilson JM, Deribas L, Cardinot G & Griffith H (1997) Gradation in nutrient composition and photosynthetic pathways across the restinga vegetation of Brazil. Acta Botanica Brasilica 110: 135-142. and Souza et al.(2008Souza CRDG, Hiruma ST, Sallun AEM, Ribeiro RR & Sobrinho JMA (2008) “Restinga” - Conceitos e empregos do termo no Brasil e implicações na legislação ambiental. Instituto Geológico, São Paulo. ), we divided Restingas areas into four plots/zones (50 × 200 m each) characterized according edaphic factors and non-vegetation types: zone a- areas nearest to the sea, where psammophilous and halophyte species dominate, particularly rhizomatous, cespitose, and creepy herbaceous; zone b- intermediate zones, 2 kilometres from the sea, composed of dense 0.5 to 1 m high shrub mosaics; zone c- zones located furthest from the sea (3 kilometres), composed by shrubs and trees between 2 and 5 m high, and; (zone d) flooded areas (3,5 kilometres from the sea) (Fig. 1).

Figure 1
Representation of sampling in zones of Restingas.

Plant morphophysiological traits were measured between March and June 2016, in order to sample the plant community at peak standing biomass during the rainy season. In Restinga environments, nurse plants promote facilitation by enhancing fitness, survival and/or growth of associated species (Callaway et al. 2002Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D & Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417: 844-848.). This often results in the process of nucleation, i.e. the formation of vegetation clumps or islands, and the vegetation becomes organized in small islands separated by sandy stretches with clumps (Pimentel et al. 2007Pimentel MCP, Barros MJ, Cirne P, Mattos EADE, Oliveira RC, Pereira MCA, Scarano FR, Zaluar HLT & Araujo DSD (2007) Spatial variation in the structure and floristic composition of “restinga” vegetation in southeastern Brazil 1. Brazilian Journal of Botany 30: 543-551.). Because of this, for each type of zone, two transects (200 m) were established perpendicular to the seashore. We collected all individuals in each transect.

Selection and measurements of functional traits

Trait-based community analysis requires the selection of traits that are critical to the community processes of interest (Cornelissen et al. 2003Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, Ter Steege H, Morgan HD, Van Der Heijden MG a, Pausas JG & Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380.; Baraloto et al. 2010Baraloto C, Timothy Paine CE, Patiño S, Bonal D, Hérault B & Chave J (2010) Functional trait variation and sampling strategies in species-rich plant communities. Functional Ecology 24: 208-216.). Our selection of traits thus represented the leaves and the overall life form of each species, covering a wide range of traits frequently deemed essential for plant survival and establishment in extreme environments (Tab. 1) (Pérez-Harguindeguy et al. 2013Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, De Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, Ter Steege H, Van Der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti M V., Conti G, Staver AC, Aquino S & Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61: 167-234.). We selected adult individuals and minimum and preferred number of replicates for different traits according Pérez-Harguindeguy et al. (2013)Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, De Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, Ter Steege H, Van Der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti M V., Conti G, Staver AC, Aquino S & Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61: 167-234..

Table 1
Measured functional traits, their respective biological significances and expected relation with different environmental factors

Specifically, we measured leaf area (cm²) -l0 leaves per individual- with LAI 3000 (Li-Cor). Leaf dry matter content (LDMC) (g) was measured following drying to constant mass at 60 ºC (around 72 h), and specific leaf area -SLA- was calculated for each lamina as the ratio of leaf area to leaf dry matter content (cm²/g). We considered the rachis as part of the leaf for the SLA calculation (Pérez-Harguindeguy et al. 2013Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, De Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, Ter Steege H, Van Der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti M V., Conti G, Staver AC, Aquino S & Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61: 167-234.). Chlorophyll index was estimated from five measurements per lamina using a portable, non-destructive chlorophyll meter Minolta SPAD 502DL (Spectrum Technologies, Plainfield, IL, USA). Maximum quantum efficiency of PSII (Fv/Fm) was determined after 20 min of leaf dark adaptation period using the saturation pulse of actinic light (8000 lmol/ m2) through a modulated fluorometer (PAM 2500). Leaf water potential (MPa) was measured around 12:00 PM using a Scholander pressure chamber. Leaf phosphorus (P), sodium (Na+) and potassium (K+) were measured in mg/g according to the methodology recommended by EMBRAPA (Carmo et al. 2000Carmo CAFS, Araújo WS, Bernardi ACC & Saldanha MFC (2000) Métodos de análise de tecidos vegetais utilizados na Embrapa Solos. 41. Embrapa Solos-Circular Técnica (INFOTECA-E), Rio de Janeiro. 41p.).

Measurement of environments variables

We collected ten soil samples in each zone at a depth of 15 cm. We mixed the sample soil to obtain a composite sample per zone. Organic matter content (OM, g/Kg), ion exchange capacity (IEC, cmolc/ dm3), pH in water, Calcium (Ca2+, cmolc/ dm3), magnesium (Mg2+, cmolc/ dm3, phosphorus (P, mg/dm3), sodium (Na+, mg/dm3) and potassium (K+, mg/dm3) were extracted according to a methodology recommended by EMBRAPA (2013).

Data analysis

We used a Principal Component Analysis (PCA) with soil composition variables to characterize the edaphic gradients present in the study site. The first two PCA axis explained a large proportion of the variation and were thus used to represent the environmental gradients in subsequent analyses. Community composition changes along the environmental gradient were detected using a multivariate model (ManyGLM) in the R package mvabund (Wang et al. 2012Wang Y, Naumann U, Wright ST & Warton DI (2012) Mvabund- an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution 3: 471-474.; Warton et al. 2012Warton DI, Wright ST & Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution 3: 89-101.). This methodology was specifically developed for complex community composition data and was used for parameter estimates for generalised linear models simultaneously fitted to each of many variables, critically, takes into account the interactions between species commonly that are absent in standard GLM approaches (Milazzo et al. 2016Milazzo M, Quattrocchi F, Azzurro E, Palmeri A, Chemello R, Di Franco A, Guidetti P, Sala E, Sciandra M, Badalamenti F & García-Charton JA (2016) Warming-related shifts in the distribution of two competing coastal wrasses. Marine Environmental Research 120: 55-67.). According Warton et al. (2012)Warton DI, Wright ST & Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution 3: 89-101. this approach detects differences in communities of less abundant species that may be more poorly represented by distance-based approaches. Subsequently, we also analysed the relationships between edaphic gradients and functional traits using linear models. Trait averages were calculated from ‘specific average’ using trait values for individual species that are specific to each habitat where the species are found (Lepš et al. 2011Lepš J, de Bello F, Šmilauer P & Doležal J (2011) Community trait response to environment: Disentangling species turnover vs intraspecific trait variability effects. Ecography (Cop) 34: 856-863.) (Table S1, available on supplementary material <https://doi.org/10.6084/m9.figshare.16879834.v1>). Linear models were performed separately for each sampled trait and considered as explanatory variables the two main axis resulting from the PCA described above.

Finally, we compared the relative contribution of species turnover and intraspecific variation in explaining among-site variation in functional traits by partitioning the variance explained by each component. For this, we used the method proposed by Lepš et al. (2011)Lepš J, de Bello F, Šmilauer P & Doležal J (2011) Community trait response to environment: Disentangling species turnover vs intraspecific trait variability effects. Ecography (Cop) 34: 856-863. based on the decomposition of the sum of squares of the trait variation along the gradient. To assess the respective contribution of species turnover and intraspecific variability, we used function “trait.flex.anova” developed by the authors for the R software (R Development Core Team <https://www.r-project.org>).

Results

We found a marked environmental gradient characterized by chemical changes in soil. The first two PCA components explained 93% of the total variance of environmental attributes according to soil composition variables (Fig. 2). PCA axis 1 was mainly associated with soil nutrients (P, Na, K, Mg and IEC) and explained 59.2% of the variation observed between sampled sites, while the PCA axis 2 related mainly to pH, H+Al, OM and Ca variables, and explained 33.8% of the total observed variance (Fig. 2). Both axes were then used to test the observed changes in community composition between zones, and a significant relationship was found with axis 2 (Tab. 2).

Figure 2
Principal component analysis for edaphic attributes (Na, K, Mg, IEC, OM, Ca, Hal, pH) from two Restinga study sites.
Table 2
ManyGLM testing the relationship between predictors (axis1 and axis 2 from PCA) and community composition. Significant results are in bold.

Plant functional traits were measured in 200 individuals of 18 wood plant species (Tab. 3) and the environmental gradients represented by the two PCA axes were significant predictors of the distribution of five out of the eleven study traits (Fig. 3; Tab. 4). There was a relationship with both predictors for water potential, LDMC and K content, while two other traits (height and chlorophyll index) only showed a significant relationship with axis 2. Effect sizes (standardized estimates) were generally higher for axis 2 than for axis 1 (Tab. 4). Higher values of PCA axis 2 were positively associated with height, but negatively associated with chlorophyll index, water potential and LDMC. In contrast, higher values of PCA axis 1 were associated with increasing water potential, LDMC and K content (Fig. 3).

Figure 3
Relationship between PCA derived environmental gradients (axis 1 and 2) and height, chlorophyll, water potential, LDMC and K contend.
Table 3
Plants found in the six plots of Restinga
Table 4
Linear models testing the relationship between predictors (axis1 and axis 2 from PCA) and functional traits. Significant results are in bold.

Decomposition of total variation in the distribution of each functional trait demonstrated that species turnover accounts for a much larger proportion of total trait variation than intraspecific variation (Tab. 5). The percentage of variation explained by the turnover component varied between ~87 and 100 whereas that of intraspecific variability varied between 0 and 22%. For foliar area, chlorophyll index, nitrogen, sodium and potassium concentration, all observed variation was due to species turnover (Tab. 5). There was a positive covariation between species turnover and intraspecific variation for height, Fv/Fm, leaf area, LDMC and SLA, indicating that the effects of species turnover and intraspecific variation reinforced each other (i.e., sites dominated by species with high values of those traits also tended to have individuals with high trait values for their species). Co-variation between intraspecific variation and turnover was negative for chlorophyll index, water potential and phosphorus.

Table 5
Percentage of total variation in community-weighted mean trait values explained due to species turnover, intraspecific variation, and their covariation.

Discussion

Our results showed that the previously established vegetation zones are characterized by a significant difference in the chemical soil characteristics, framing an environmental gradient. Furthermore, the observed changes in community composition and environmental gradients correlated strongly with plant functional traits, generating additional insights into mechanisms behind the observed environmental filtering. Plant community composition and associated functional traits are known to be affected by a combination of environmental factors whose relative influence may be difficult to tease apart (Fortunel et al. 2014Fortunel C, Paine CET, Fine PVA, Kraft NJB, Baraloto C & Firme T (2014) Environmental factors predict community functional composition in Amazonian forests. Journal of Ecology 102: 145-155.). However, our results showed that some edaphic factors have a significant effect on community composition in Restinga habitats.

Soil pH is a factor that is known to affect the establishment of plant communities in Restingas (Santos-Filho et al. 2013Santos-Filho FS, Almeida Jr E & Zickel CS (2013) Do edaphic aspects alter vegetation structures in the Brazilian restinga? Acta Botanica Brasilica 27: 613-623.), because acidic pH reduces the rates of decomposition in the soil and consequently decreases soil organic matter (OM). Areas with higher OM availability are more favourable to the development of taller woody plants (Lammerts et al. 1999Lammerts EJ, Pegtel DM, Grootjans AP & Van Der Veen A (1999) Nutrient limitation and vegetation changes in a coastal dune slack. Journal of Vegetation Science 10: 111-122.), which explains the relationship between plant height and PCA axis 2. Plant height is often related with water potential (van der Weele et al. 2000van der Weele CM, Spollen WG, Sharp RE & Baskin TI (2000) Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. Journal of Experimental Botany 51: 1555-1562.). Leaf water potential is an indicator of the leaf’s water status and shows the balance between water availability in the soil. It tends to decrease as evaporative demand (evapotranspiration potential) increases (Bréda et al. 2006Bréda N, Huc R, Garnier A, Dreyer E, Granier A & Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Annals of Forest Science 63: 625-644.), potentially explaining our observation of higher water potential in leaves with lower levels of OM and pH in soil.

A growing availability of P and K in soils promotes a gradual biomass allocation (Marschner 1995Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London. 889p.; Lawrence 2001Lawrence D (2001) Nitrogen and phosphorus enhance growth and luxury consumption of four secondary forest tree species in Borneo. Journal of Tropical Ecology 17: 859-869.), as observed in the positive relationship between the availability of such nutrients and LDMC. Nutrient availability is also an important indicator of strategies of habitat preferences and of productivity of plants related to environments under stress (Niklas & Christianson 2011Niklas KJ & Christianson ML (2011) Differences in the scaling of area and mass of Ginkgo biloba (Ginkgoaceae) leaves and their relevance to the study of specific leaf area. American Journal of Botany 98: 1381-1386.). Under conditions of water stress, such as found in Restinga (Scarano 2002Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Annals of Botany 90: 517-524.; Neves et al. 2009Neves NR, Oliva MA, Centeno C, Costa AC, Ribas RF & Pereira EG (2009) Science of the Total Environment Photosynthesis and oxidative stress in the restinga plant species Eugenia uni flora L . exposed to simulated acid rain and iron ore dust deposition : Potential use in environmental risk assessment. Science of the Total Environment 407: 3740-3745.), the survival of plants may be partly due to their ability to maintain turgor as a result of the slow decline in leaf water potential brought about by low transpiration rate and continued uptake of nutrients, especially K (Tanguilig et al. 1987Tanguilig V., Yambao EB, O’Toole JC & De Datta SK (1987) Water stress effects on leaf elongation, leaf water potential, transpiration, and nutrient uptake of rice, maize, and soybean. Plant Soil 103: 155-168.). Increased K uptake suggests that, under water stress conditions, K may be absorbed preferably and may result in an osmotic adjustment which contributes to higher leaf-water potential (Tanguilig et al. 1987). We observed a similar pattern in the positive relationship between K availability and water potential.

These mechanisms suggest that the environmental gradients observed in Restinga areas ultimately structure the distribution of local plant communities and their associated traits. Different environmental conditions result in an increase of number of ecological niches within each site reflecting in a great variation in the richness of local species and a species turnover among plots. The dominance of interspecific trait variation for all eleven traits suggests that that changes in the relative abundances of species are caused by habitat changes (Lepš et al. 2011Lepš J, de Bello F, Šmilauer P & Doležal J (2011) Community trait response to environment: Disentangling species turnover vs intraspecific trait variability effects. Ecography (Cop) 34: 856-863.; Zuo et al. 2017Zuo X, Yue X, Lv P, Yu Q, Chen M, Zhang J, Luo Y, Wang S & Zhang J (2017) Contrasting effects of plant inter- and intraspecific variation on community trait responses to restoration of a sandy grassland ecosystem. Ecology and Evolution 7: 1125-1134.). It has been suggested that intraspecific effects are more important in short environmental gradients, where changes in species composition are small ( Wright et al. 2004Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ & Villar R (2004) The worldwide leaf economics spectrum. Nature 428: 821-7.; Albert et al. 2011Albert CH, Grassein F, Schurr FM, Vieilledent G & Violle C (2011) When and how should intraspecific variability be considered in trait-based plant ecology? Perspectives in Plant Ecology, Evolution and Systematics 13: 217-225.). However, in resource-poor environments the effect of environmental filters tends to be more intense and the plant communities are correspondingly more influenced by species selection and show higher levels of functional convergence (Kraft et al. 2008Kraft NJB, Valencia R & Ackerly DD (2008) Functional traits and niche-based tree community assembly in an Amazonian forest. Science 322: 580-582.; Lohbeck et al. 2014Lohbeck M, Poorter L, Martínez-Ramos M, Rodriguez-Velázquez J, van Breugel M & Bongers F (2014) Changing drivers of species dominance during tropical forest succession. Functional Ecology 28: 1052-1058.).

Environmental filter should weaken the intraspecific variation, because rather than being excluded from a habitat species can adjust their characteristics to the environment (Kichenin et al. 2013Kichenin E, Wardle DA, Peltzer DA, Morse CW & Freschet GT (2013) Contrasting effects of plant inter- and intraspecific variation on community-level trait measures along an environmental gradient. Functional Ecology 27: 1254-1261.). Nevertheless, in our study it is likely that intraspecific trait plasticity is insufficient to buffer against environmental filtering. The greatest contribution of intraspecific variation was observed in water potential (22%). The intraspecific variation observed in this characteristic show negative covariation indicating that areas dominated by species with high water potential values tend to contain individuals with low trait values for their species (Siefert et al. 2014Siefert A, Fridley JD & Ritchie ME (2014) Community functional responses to soil and climate at multiple spatial scales: When does intraspecific variation matter? PLoS One 9: e111189.). It follows that species turnover and intraspecific variation compensate for each other, leading to an absence of response of community-average trait values (Lepš et al. 2011Lepš J, de Bello F, Šmilauer P & Doležal J (2011) Community trait response to environment: Disentangling species turnover vs intraspecific trait variability effects. Ecography (Cop) 34: 856-863.).

The effect of environmental filtering observed in our study implies similar ecological needs of co-occurring species. Others studies have observed that species in dunes from the same habitat type have similar traits as result of exposure to the same environmental stress (Scarano et al. 2001Scarano FR, Duarte HM, Ribeiro KT, Rodrigues PJFP, Barcellos EMB, Franco AC, Brulfert J, DelÉens E & Lüttge U (2001) Four sites with contrasting environmental stress in southeastern Brazil: Relations of species, life form diversity, and geographic distribution to ecophysiological parameters. Botanical Journal of the Linnean Society 136: 345-364.; Mahdavi & Bergmeier 2016Mahdavi P & Bergmeier E (2016) Plant functional traits and diversity in sand dune ecosystems across different biogeographic regions. Acta Oecologica 74: 37-45.). These results do not support the action of limiting similarity in dunes as proposed by Stubbs & Wilson (2004)Stubbs WJ & Wilson JB (2004) Evidence for limiting similarity in a sand dune community. Journal of Ecology 92: 557-567.. According to these authors species can more readily coexist if they differ in their resource use patterns. Rosado & De Mattos (2010) also observed that traits of the leaf economic spectrum showed small interspecific variation. However, these authors also noted that traits with physiological significance for the Restinga, such as water potential, showed considerable interspecific variation and recommend considerable caution when selecting functional traits to describe whole-plant responses to environmental drivers. In summary, the ability of a given species to colonize the dune habitat depends on integrative traits resulting from multiple trait arrays, not necessarily captured by the leaf economic spectrum (Rosado & De Mattos 2017Rosado BHP & de Mattos EA (2017) On the relative importance of CSR ecological strategies and integrative traits to explain species dominance at local scales. Functional Ecology 31: 1969-1974.).

This study provides important insights about how environmental factors influence the distribution of plant traits in the Restinga. The strong environmental gradients observed are clear and intuitive. Still, it would be interesting to explore similar questions in other tropical systems where, like the Restinga, vegetation is established in sandy soils. Such habitats are likewise somewhat poorly studied and may provide important insights into plant community dynamics under strong environmental gradients.

Acknowledgements

We also thank Francesco de Bello, for suggestions for data analysis; and Richard Ladle, for the English language review. RAC is currently funded by a post-doctoral scholarship from FCT - Fundação para a Ciência e Tecnologia (SFRH/BPD/118635/2016). ACMM is funded by CNPq- Conselho Nacional de Desenvolvimento Científico e Tecnológico (#309980/2018-6).

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Supplementary Material

See supplementary material at <https://doi.org/10.6084/m9.figshare.16879834.v1 >

Edited by

Area Editor: Dr. Mário Luís Garbin

Publication Dates

  • Publication in this collection
    03 Dec 2021
  • Date of issue
    2021

History

  • Received
    12 Feb 2020
  • Accepted
    08 Dec 2020
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