Influence of Soil Physical Properties on Plants of the Mussununga Ecosystem, Brazil Amilcar Walter Saporetti-Junior, Carlos Ernesto G. Reynaud Schaefer, Agostinho Lopes de Souza, Michellia Pereira Soares, Dorothy Sue Dunn Araújo, et al. Folia Geobotanica Journal of the Institute of Botany, Academy of Sciences of the Czech Republic ISSN 1211-9520 Volume 47 Number 1 Folia Geobot (2012) 47:29-39 DOI 10.1007/s12224-011-9106-9 1 23 Your article is protected by copyright and all rights are held exclusively by Institute of Botany, Academy of Sciences of the Czech Republic. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self- archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy FoliaGeobot(2012)47:29–39 DOI10.1007/s12224-011-9106-9 Influence of Soil Physical Properties on Plants of the Mussununga Ecosystem, Brazil Amilcar Walter Saporetti-Junior&Carlos Ernesto G. Reynaud Schaefer& Agostinho Lopes de Souza&Michellia Pereira Soares& Dorothy Sue Dunn Araújo&João Augusto Alves Meira-Neto #InstituteofBotany,AcademyofSciencesoftheCzechRepublic2011 Abstract Distribution ranges of plant species are related to physical variables of ecosystems that limit plant growth. Therefore, each plant species response to physical factors builds up the functional diversity of an ecosystem. The higher the speciesrichnessofanecosystem, thelargerthe probabilityof maintaining functions and the higher the potential number of plant functional groups (FGs). Thus, the richness potentially increases the number offunctions of the highly diverse Atlantic Rainforest domain in Brazil. Severe plant growth limitations caused by stress, however, decrease species richness. In the Spodosols of the Mussununga, an associated ecosystem of Atlantic Rainforest, the percentage of fine sand is directly related to water retention. Moreover, the depth of the cementation layer in the Mussununga’s sandy soil is a physical factor that can affect the plants’ stress gradients. When a shallow cementation layer depth is combined with low water retention in soils and with low fine sand percentage, the double stresses of flooding in the rainy season and water scarcity in the dry season result. This study aimed to Electronicsupplementarymaterial Theonlineversionofthisarticle(doi:10.1007/s12224-011-9106-9) containssupplementarymaterial,whichisavailabletoauthorizedusers. : : : A.W.Saporetti-Junior C.E.G.R.Schaefer M.P.Soares J.A.A.Meira-Neto(*) BotanyPost-GraduateProgram,FederalUniversityofViçosa,Viçosa,Brazil e-mail:[email protected] J.A.A.Meira-Neto PlantBiologyDepartment,FederalUniversityofViçosa,Viçosa,Brazil C.E.G.R.Schaefer SoilDepartment,FederalUniversityofViçosa,Viçosa,Brazil A.L.deSouza ForestryDepartment,FederalUniversityofViçosa,Viçosa,Brazil D.S.D.Araújo EcologyDepartment,FederalUniversityofRiodeJaneiro,RiodeJaneiro,Brazil Author's personal copy 30 A.W.Saporetti-Junioretal. identify FGs among Mussununga plant species responding to water stress gradients of soil and to verify the effects of the gradients on plant species richness of the Mussununga.Acanonicalcorrespondenceanalysis(CCA)ofspeciesabundanceand soil texture variables was performed on 18 plots in six physiognomies of the Mussununga.Speciesrichnessrarefactionswerecalculatedforeachvegetationform tocomparediversity.ThetwomainaxesoftheCCAshowedtwoFGsrespondingto soil texture and cementation layer depth: stress tolerator species and mesic species. Physicalvariables affectplant diversity,with speciesrichnessrising asthefine sand proportion also rises in the Mussununga. The effect of the cementation layer is not significantly related to species richness variation. Keywords Atlantictropicalrainforest.Diversity.Metacommunityecology.Plant functionaltypes.Richness.Sandysoils.Spodosols.Waterretention Plant nomenclature Forzza et al. (2010) Introduction Patternsanddistributionrangesofplantspeciesrelatedtophysicalfactorslimitingor favoring their occurrence has become a recent subject for studies of the Atlantic Rainforest and its associated ecosystems (Scarano et al. 2004; Geßler et al. 2005a). Plantresponsestophysicalfactorsarerelatedtofunctionsofecosystems(e.g.,Grime 2001). The higher the species richness of an ecosystem, the higher the probability of maintaining ecosystem functions and the higher the number of functional groups (FGs) of that ecosystem (Tilman et al. 1997). The Brazilian Atlantic Rainforest is among the richest tropical ecosystems on Earth (Rosenzweig 1995; Thomas et al. 2008) and is among the most endangered forest types in Brazil because its distributional range coincides with the regions most disturbed by urbanization, industries, agriculture and roads. There has been an effort to find appropriate models to predict the functioning of this tropical ecosystem with high species and functional diversity (e.g., Geßler et al. 2005b). Nevertheless, most of these studies focused on variouswoodyplants,whereasanalysesassessingawiderrangeoflifeformstomatch conservation, management and restoration requirements of the Brazilian Atlantic Rainforestdomainarestilllacking.Environmentalgradientscanaffectthediversityof plants, because environmental gradients affect plant growth and ecosystem produc- tivityaffectsthediversity(e.g.,Leigh1965;Brown1973).Asproductivityrisesfrom low to intermediate levels, species richness also rises (Preston 1962; Wright et al. 1993). Diversity is lower in those habitats where low contents of soil nutrients stronglylimitplantgrowth(HartleyandJones1997).Similarly,alongawatergradient the less productive habitats are those in which water stress causes a severe drought, inducinga stomatalclosure (Mooney and Ehleringer 1997).Thus, acrossa landscape it is expected that gradient extremes of low productivity have lower species richness than moderately productive sites of the same gradient. The Atlantic Rainforest domain of southern Bahia and northern Espirito Santo states has an associated type of ecosystem, the Mussununga, with physiognomic forms ranging from grasslands to woodlands over sandy Spodosols originated from Author's personal copy InfluenceofSoilPhysicalPropertiesonPlants 31 sandstones of the Barreiras Group from the Tertiary period (ca. 16 million years before present). The vegetation on Tertiary sandy soils are called Mussunungas, an AmerindianTupi-Guaraniwordthatmeans“softandwetwhitesand”(Meira-Netoet al. 2005) and is sometimes also called Campo Nativo (Araújo et al. 2008). The pedogenesis of tropical Spodosols by podsolization (Horbe et al. 2004) created sandy, slightly convex and circular/amoeboid shapedpatchesonflatTertiaryterrains. The patches of sandy Spodosols, surrounded by rainforest Podsols, have caused a decrease in the biodiversity and biomass of specialized flora. Mussununga soils are sandy, and their texture strongly influences the water status for plant growth. Sandy soils with finer particles have higher water retention than sandy soils with coarser particles (Mecke et al. 2002). In addition, Mussununga Spodosols have a consistently hard and impermeable cementation layer (ortstein), which causes flooding stress in the rainy season and drought stress in the dry season (Horbe et al. 2004; Meira-Neto et al.2005 ). We have hypothesized that the combination of drought and flooding stresses is a strong limiting factor for most rainforest species that prevents them from establishing in the Mussunungas (Meira-Neto et al. 2005; Saporetti-Junior 2009). Due to the aforementioned Mussununga soil traits and because water availability is the most evident physical factor limiting plant growth in tropical ecosystems (Grace 1997), we hypothesize that FGs in the Mussununga occur as a responsetothesoilwaterstatusforplantgrowth,andthatspeciesrichnessrisesin sites with lower water stress (intermediate productivity) and decreases in areas withhigherwaterstress(lowproductivity)inSpodosol.Thisstudyaimedtoassess the textural (water retention) and cementation depth gradients in Mussununga vegetation to i) detect functional groups of Mussununga plant species responding to the gradients and ii) verify the effects of the gradients on Mussununga plant species richness. Material and Methods Study Site The studied patch of Mussununga is inCaravelas municipality, southern Bahia State, Brazil.ThesiteisonflatterrainthatoriginatedfromTertiarysandstones(ca.16million yearsago),calledtheBarreirasGroup.Thepatchislocatedintheevergreenrainforest vegetational zone (Walter and Breckle 2002). The climate is Am according to the Köppen system, humid tropical with mean precipitation around 1750 mm/y. Rainy summersalternatewithmoderatedrywinters,withoccasionalinterannualinfluenceof the El Niño Southern Oscillation (Borchert 1998; Williamson et al. 2000). Thus, flooding and droughts can be much stronger than expected by the climate type. The predominant vegetation of this landscape is tropical rainforest settled mainly on Podsols. There are patches of savannic vegetation, called Mussunungas, over sandy Spodosols surrounded by rainforests, Eucalyptus plantations and crop fields (Fig. 1).Caravelas’Mussunungahassinuousbordersandanarea of853 haat50m elevation (S 17o40′44″, S 17o42′15″, W 39o27′40″, W 39o30′19″). It is the largest and best-preserved Mussununga in southern Bahia State. Author's personal copy 32 A.W.Saporetti-Junioretal. Fig.1 DiagramofaMussunungawithsurroundingAtlanticRainforest.Soilnamesareaccordingtothe U.S.systemofsoilclassification Plant and Soil Relations Plant species abundance data (Table S1, Table S2 in Electronic Supplementary Material(hereafter ESM))werecollectedin18plotsof4m2(2×2m),inwhichall individual plants of all life forms were counted. The sampling was performed using three plots in six physiognomies of Mussununga according to the Brazilian vegetation classification (Veloso et al. 1991): grassland, open savanna (grassland and woody Bonnetia stricta), savanna (grassland and shrubs), closed savanna (grassland, shrubs and small trees), park savanna and woodland using a systematic andstratifiedsamplingscheme(Figs.S1–S7inESM).Allsamplesweretakeninthe middle of the Mussununga to avoid direct influences of the rainforest. Each physiognomy had three soil samples, each containing a compound sample of ten single samples in 4-m2 vegetation plots. The texture of 18 compound soil samples (0–20 cm depth) was analyzed at the Soil Laboratory of the Federal University of Viçosa. We used the U.S. soil classification system. Among samples, we measured the ortstein depth in meters (depth m), percentage of coarse sand (%CS) and percentageoffinesand(%FS).Thesedatawerecomparedusingtheprobabilityareaofa normal curve, converting the means and standard deviations to the standard normal distributionusingthePNORMfunctionoftheRstatisticalenvironment(Crawley2007). The regular soil type of Mussunungas is a sandy Spodosol with an ortstein depth varying from 0.5 to 2 m (Meira-Neto et al. 2005). Because we wanted to test the relationship of physiognomic variation of Mussununga vegetation to soil traits, a traditional approach was used (Lepš and Šmilauer 2003). A canonical correspondence analysis (CCA) (Ter Braak 1986) was performed using CANOCO 4.5 software (Ter Braak and Šmilauer 2002) to test the relationship of plant abundance with the following physical properties of Mussununga soil: percentage of fine sand (particles finer than 0.2 mm) (%FS), percentage of coarse sand (particles coarser than 0.2 mm) (%CS) and depth from surface to impermeable layer (depth). Because rare species can increase the total inertia of the species dataset (Ter Braak and Šmilauer 2002), only species with at least five individuals were included in the CCA, and the abundance values were Author's personal copy InfluenceofSoilPhysicalPropertiesonPlants 33 logarithmically transformed as species of small life forms tend to be much more abundant than woody species. The CCAwas applied as a data-defined approach to address the clustering of sampled species into groups on the basis of soil traits (Leishman and Westoby 1992; Newton 2007). For that approach, overall trends shared by species and plots related to the physical properties of Mussununga soil weregroupedusingellipsesdrawnoncharts.Theprocedureforverifyingthelength of the largest gradient of the analysis resulted in a value between 3 and 4 (3.09), validating the use of the CCA, a unimodal method (Lepš and Šmilauer 2003). Measures of Richness Diversitymeasuresweremadeusing4010-m²(2×5m)plotsina400-m2(20×20m) grid for each of six vegetation forms (Fig. S7 in ESM). The Mao Tau estimator (T) was used to estimate the mean number of species. The T was calculated by an interpolation that produces a rarefaction. It consists of systematically enumerating all distinct subsets of quadrats from the total number of quadrats of the sample set and findingtheobservedrichnessineachsubsetofquadrats.Themeanspeciesnumberis then calculated, first for one quadrat, then for two quadrats and so on until reaching thetotalnumberofquadrats(Colwelletal.2004).Thus,theTapproachcalculatesthe mean richness and confidence intervals expected for the number of pooled samples, giving a notion of spatiality on the diversity charts. The Mao Tau rarefactions were calculated using Estimates 8.2 software (Colwell 2009). Comparisons were made graphicallyusingprobabilityareasofnormaldistributionwithaconfidenceintervalof 95% (Colwell et al. 2004). Results Soil and Functional Groups (FGs) All plots presented sandy soil containing 90% to 95% sand (Table 1). The CCA species ordination separated two groups of plant species of the Mussununga ecosystem. One group consists of species tolerant to stress caused by low water Table1 MeanvaluesandstandarddeviationsofphysicalfactorsofsoilinphysiognomiesofMussununga vegetation.Depthm–depthofortsteininmeters;%CS–percentageofcoarsesand;%FS–percentageof finesand.Differentlettersindicatestatisticalsignificanceofdifferencesamongmeanvaluesofthesame physicalfactor(P<0.05) Physiognomy Depthm %CS %FS Woodland 1.21±0.16c 70.66±4.04b 23±5.29ab Parksavanna 2.67±0.52a 78.66±7.77b 16±7.21bc Closedsavanna 2.22±0.09a 68.33±4.04b 25.33±3.78a Savanna 1.48±0.04b 70.33±6.11b 23.33±4.51ab Opensavanna 0.582±0.06d 72.33±3.51b 20.33±4.16ab Grassland 1.236±0.08c 86±1a 7.33±1.53c Author's personal copy 34 A.W.Saporetti-Junioretal. retention, hereafter named stress tolerators, with the ability to dominate sites more susceptibletodroughtandcontainingcoarsersand,andwithashallowersubstrateas a result of more superficial ortstein. These soil traits are the cause of the double stresses ofthewaterregime.Anothergroup ofspecieswithan intermediate strategy betweenstresstoleranceandgrowthability,hereafternamedmesic,dominatessandy soils with a higher proportion of fine sand and a deeper impermeable layer. Therefore, mesic species are subjected to moderate double water stresses (Fig. 2). The CCA ordination of plots clustered two groups of samples and revealed a pattern for vegetation forms of the Mussununga ecosystem. One group, formed by grasslandandopensavannaplots,isrelatedtoSpodosolswithhigherproportionsof coarse sand and more superficial ortstein. Anothergroup of physiognomies, formed by savanna, closed savanna, park savanna and woodland, is related to soil with deeper ortstein and with higher percentage of fine sand (Fig. 3 and Table 1). TheaccumulatedvarianceexplainedbythetwofirstaxesoftheCCAwas85%.The probabilityofallCCAaxesbeingcausedbyrandomeventswaslessthan2%(P<0.02). Basedontheanalysisof19specieswithfive ormoreindividuals, stress tolerator species are mainly of therophyte (three species) and chamaephyte (two species) life forms and dominate grassland and open savanna. The mesic group is dominated by eight species of phanerophytes that morphologically influence the vegetation forms Fig. 2 Correspondence canonical analysis ordination with types of species defined by relationships betweenthreesoilvariables:depthofimpermeablelayer(Depth),proportionofcoarsesand(%CS)and proportion of fine sand (%FS). The dotted line encircles the functional group (FG) species related to shallowersoilswithcoarsersand,whereasthedashedlineencirclestheFGspeciesrelatedtodeepersoils with finer sand; a – Panicum trinii (i), b – Syngonanthus nitens (ii), c – Xyris capensis (ii), d – Actinocephalusramosus(ii),e–Comoliaovalifolia(iii),f–Sauvagesiaerecta(iii),g–Myrciaracemosa (iv), h – Davilla macrocarpa (v), i – Lagenocarpus rigidus (i), j – Microlicia sp. (iii), k – Guapira pernambucensis(iv),l–Paepalanthusklotzschianus(ii),m–Bonnetiastricta(iv),n–Eugenialigustrina (iv), o – Humiria balsamifera (iv), p – Pradosia lactescens (iv), q – Ilex psammophila (iv), r – Gaylussaciabrasiliensis(iv),s–Doliocarpusmultiflorus(v).i)Hemicryptophytes,ii)Therophytes,iii) Chamaephytes,iv)Phanerophytes,v)Lianas Author's personal copy InfluenceofSoilPhysicalPropertiesonPlants 35 Fig. 3 Correspondence canonical analysis ordination with groups of plots defined by relationships betweenthreesoilvariables:depthofimpermeablelayer(Depth),proportionofcoarsesand(%CS)and proportionoffinesand(%FS).Thedottedlineencirclesplotsofgrassland[1]andopensavanna(grassland +woodyBonnetia stricta) [2], both related to shallower soils with coarser sand, whereas the dotted line encirclesplotsofsavanna(grassland+shrubs)[3],closedsavanna(grassland+shrubs+smalltrees)[4], parksavanna[5]andwoodland[6]relatedtodeepersoilswithfinersand ofsavanna,closedsavanna,parksavannaandwoodland.Bothgroupsrevealatrade-off betweenstresstoleranceandgrowthstrategies.Indeed,thistrade-offislargelytheresult ofdifferencesamongthelifeforms’abilitiestotoleratewaterstressandtogrow(Table S1, Table S2, Table S3; Fig. S1, Fig. S2 in ESM). Richness Richness varies across the gradient of the percentage of fine sand (Fig. 4, Tables 1 and 2). Observed richness was lowest in the grassland (the environment with less Fig.4 EstimatesofrichnessusingtheMaoTauestimatorbymeansofsimulationsfor40plotsineachofthesix vegetationformsofMussununga:agrassland,bopensavanna,csavanna,dclosedsavanna,eparksavanna,f woodland.Solidlinesaremeanvaluesofrichness;dashedlinesareconfidenceintervalsof95%(±1.96s.d.) Author's personal copy 36 A.W.Saporetti-Junioretal. Table 2 Observed richness (richness) and standard deviation (s.d.) of Mao Tau rarefactions for 40 samples in each physiognomy of Mussununga. Different letters indicate statistical difference among richness (P<0.05) Physiognomy Woodland Parksavanna Closedsavanna Savanna Opensavanna Grassland Richness 81a 65b 43c 46c 32d 13e s.d. 3.37 4.39 2.59 1.12 1.96 0.0 fine sand) with 13 sampled species. As the fine sand proportion increases, observed richnesssignificantlyrisesalongthegradientthroughopensavanna,savanna,closed savanna, park savanna and woodland. Only savanna and closed savanna show no significant differences in richness (Table 2). The number of species sampled increased in each habitat with the highest number, 81, sampled in the woodland (Table S4; Fig. S4 in ESM). Discussion Functional Groups (FGs) Two FGs of Mussununga vegetation were detected: i) the stress tolerator species related to low percentage of fine sand in the Spodosol; and ii) the mesic species related to high proportion of fine sand in the Spodosol. The stress tolerators were also related to more superficial ortstein (Figs. 2 and 3). The 85% of variance explained by the two main CCA axes showed physical properties of soil that separated two sets of species, each influenced independently by the amount of fine sand and the ortstein depth of Mussununga soils. Fine sand percentage is related to moisture, which is affected by the water retention capacity. The depth of ortstein drives the drainage regime in Mussununga’s Spodosol (Saporetti-Junior 2009) and is related to flooding stress. Nevertheless, if only the variation of fine sand proportion is analyzed, this one-dimensional gradient significantly explains the abundance of species of two FGs: stress tolerator and mesic.BothFGswerenamedaccordingtotheCSRtheoryofprimaryandsecondary plantstrategies(Grime2001).Theabundanceofstresstolerators,aprimarystrategy, is negatively correlated to the fine sand proportion. The abundance of mesic FG species,a secondarystrategy between stress tolerators andcompetitors, ispositively relatedtotheamountoffinesand.Sandysoilshavehighwaterretentionvarianceas a capillary effect (Huang and Zhang 2005), because finer sand particles have a higher capillary tension head than coarser sand particles. Particle size distribution influences the soil water retention curve, and both fit power-law models. These models are influenced by the power-law relations of surface-volume and surface- void volume (Ghilardi and Menduni 1996; Huang et al. 2006), because water is bonded to soil particles forming water films (Davidson and Janssens 2006), directly relatedtotheparticlearea.Itisimportanttorememberthatthehighertheproportion of fine sand is, then the lower the proportion of coarse sand in Mussununga