Ecossistemas Aquáticos em Biomas Tropicais- Analise Comparativa e Implicações para Avaliação Ecológica

1 at the abiotic level the aquatic ecosystems of the three biomes differed which was mostly explained by largescale factors such as temperature precipitation and altitude 2 functional and structural variables did not behave similarly among biomes decomposition and sporulation rates showed larger differences among biomes than invertebrate and aquatic hyphomycete assemblages structure 3 invertebrate assemblages structure differed between the rainforests and Cerrado but not between rainforests Amazon and Atlantic Forest whereas aquatic hyphomycetes were similar among all biomes 4 biofilm growth and algae concentration in biofilms of artificial substrates were highly variable within biomes and not significantly different between biomes Overall aquatic ecosystem processes and community structure differed across biomes being influenced by climatic variables but the variation is not as pronounced as that described for terrestrial systems Considering the potential use of these functional and structural indicators in nationalwide ecological assessments our results indicate the need to define different reference values for different biomes depending on the variable used The approach followed in this study allowed an integrative analysis and comparison of the stream ecosystems across three tropical biomes being the first study of this kind Future studies should try to confirm the patterns evidenced here with more sites from other areas of the three biomes and especially from the Amazon which was the least represented biome in our investigation 2018 Published by Elsevier BV This is an open access article under the CC BYNCND license httpcreativecommonsorglicensesbyncnd40 1 Introduction Largescale studies across biomes provide important insights on natural variations of ecosystems Boyero et al 2011 2012 Understanding their spatial patterns is essential for the definition of reference conditions the basis of modern ecological assessment schemes and effective conservation strategies Hughes et al 1986 Rouget et al 2006 Hawkins et al 2010 Feio et al 2014 Biomes are one of the large spatialscale divisions of nature which are classified by their predominant vegetation and additionally by their climatic or geographical characteristics such as equatorial tropical or boreal Woodward et al 2004 Compared to terrestrial environments little research has focused on aquatic biomes and their biological patterns Earlier studies defended the biome dependency theory high similarity in sites within or among drainage basins of a single biome by aquatic invertebrates Ross 1963 Corkum 1991 1992 associating this with the strong link between them and the terrestrial vegetation In 1983 Minshall et al investigated longitudinal and interbiome differences in benthic organic matter transported organic matter community production and respiration and functional feeding groups in rivers of North America More recently others explored functional aspects across biomes such as stream metabolism Mulholland et al 2001 or nitrogen uptake Webster et al 2003 in North America biomes Headwater streams can be considered metaecosystems composed of riparian and aquatic ecosystems with obvious links between the structural and functional components Gregory et al1991 Loreau et al 2003 Gounand et al 2017 These links occur via the process of decomposition of allochthonous organic matter mainly in the form of leaves from the riparian vegetation that fall in the water and are a direct source of energy for the invertebrates aquatic fungi and bacteria Vannote et al 1980 Graça et al 2015 At the same time primary production is usually reduced in these systems because of light limitation Vannote et al 1980 Danger et al 2013 These processes have been widely studied in temperate streams where headwater streams are called detritusbased ecosystems Moore et al 2004 Richardson and Danehy 2007 Danger et al 2013 and more recently also in tropical systems eg Rezende et al 2017a NeresLima et al 2016 2017 Linares et al 2018 Yet the great diversity of vascular plants and their characteristics eg leaf toughness phenolic content in tropical systems leads to a high variability in breakdown rates with recalcitrant species taking over a year to decompose while others decompose in few days Wantzen et al 2008 Graça et al 2015 Rezende et al 2017b The relative importance of in vertebrates and fungi in leaf decomposition also varies greatly within studies in the tropics showing both low and high abundances of shredders and a more or less importance of microbial decomposition than by invertebrates Alvim et al 2014ab Graça et al 2015 Sales et al 2015 NeresLima et al 2016 In addition some studies found that autochthonous sources such as algae constitute an alternative relevant source of energy to tropical consumers contrary to temperate models Brito et al 2006 Wantzen et al 2008 Lau et al 2009 Dudgeon et al 2010 NeresLima et al 2016 Studying simultaneously the structural and functional components of these aquatic ecosystems can contribute to clarify these aspects while providing useful insights to the construction of integrative ecological assessment schemes for streams Despite recommendations eg European Commission 2000 Gessner and Chauvet 2002 Young and Collier 2009 Feio et al 2010 there currently are no official Brazilian monitoring programs assessing the structural and functional components In Brazil the biological monitoring of freshwaters mandated in laws eg CONAMA 2005 COPAMCERHMG 2008 and structural biological methods have been developed for fish invertebrates algae or cyanobacteria eg Melo et al 2015 Macedo et al 2016 Carvalho et al 2017 Silva et al 2017 Yet functional approaches are also not officially used One of the predominant biomes in Brazil is the Cerrado a neotropical savannah that covers most of the centre of the country and houses three of the largest catchments in South America Strassburg et al 2017 It is characterized by a dry MJ Feio et al Global Ecology and Conservation 16 2018 e00498 2 season between May and September and the vegetation is adapted to the periodic lack of water with scattered trees and shrubs small palms and a ground layer of grasses Quesada et al 2008 The Atlantic Forest biome composed of alwaysgreen dense forests covers a large section of the Brazilian coast but differently from the Cerrado the high precipitation is distributed throughout the entire year Joly et al 2014 The Amazon the largest biome of Brazil covers ca 40 of the country and has permanently high humidity This biome is highly diverse Cheng et al 2013 Castello and Macedo 2016 and provides essential ecosystem services to the world Fearnside 2005 In Cerrado watersheds in spite of the surrounding sparse and low vegetation most streams are enclosed by dense riparian forests 50200 m wide and with high plant diversity Nóbrega et al 2017 This vegetation has transitional characteristics between the Amazon forest Atlantic forest Pantanal and Caatinga Silva Júnior 2004 Felfili and Silva Júnior 2005 Bambi et al 2017 leading to similarities in riparian vegetation structure and composition among those biomes Mean annual temperatures a factor known to affect litter decomposition rates aquatic communities eg Ferreira and Chauvet 2011 Martínez et al 2017 and primary production Rasmussen et al 2011 are also similar among those biomes Woodward et al 2004 In view of this we expected that contrary to the biome dependency hypothesis Ross 1963 Corkum 1991 1992 the structure and processes of leastdisturbed small stream sites would not differ significantly among Cerrado Amazon and Atlantic Forest biomes To test this we compared biological structural and functional patterns of Cerrado stream sites to those of Amazon and Atlantic Forest We selected ecosystem variables that are also potential indicators of stream quality Feio et al 2010 benthic invertebrate and aquatic hyphomycete assemblage structure as well as decomposition rates biofilm primary production Chla biofilm growth and aquatic hypomycete sporulation rate 2 Methods 21 Study areas We considered three Brazilian tropical biomes Fig 1 the Cerrado Atlantic Forest and Amazon The Cerrado biome has a typical Aw climate humid tropical savannah with two welldefined seasons dry from May to September and wet from October to April when 80 of the precipitation falls Hunke et al 2015 In the wet season the average temperature is 22 1C rainfall of 197 60 mmmonth with peaks between January and March In the dry season the average temperature is 20 1C and rainfall of 2 3 mmmonth Scattered trees and shrubs small palms and a ground layer of grasses characterize the area The rainfall variability strongly influences the composition of vegetation with grasses remaining dead or dormant during the dry season until the next wet season Quesada et al 2008 The Cerrado is a world biodiversity hotspot Myers et al 2000 because of the high level of endemism but is also one of worlds most threatened biomes because of the rapid deforestation since the 1980s double than that in the Amazon between 2008 and 2010 and replacement of natural vegetation with pasture and row crop agriculture such as soybean maize cotton and sugarcane Lambin et al 2013 Redo et al 2012 Hunke et al 2015 Part of the study sites are located in an area of Chapada Diamantina mountain which is located inside the large area of bioma Caatinga but is can considered an enclave of Cerrado due to its ecological characteristics specially near the streams Sales et al 2015 The Atlantic Forest according to Joly et al 2014 is a continuum of tree species distributions composed of five main types of forest dense ombrophilous open ombrophilous mixed ombrophilous semideciduous seasonal and deciduous seasonal The study sites are representative of dense ombrophilous forest and the KööppenGeiger climate classification includes Af tropical rainforest in the states of Espírito Santo and Rio de Janeiro mean annual temperatures of 232 C and average annual precipitation of 1791 mm NeresLima et al 2016 and Cfa humid subtropical mean annual precipitation of 201 C average precipitation of 1462 mm in the states of Santa Catarina and Paraná with high rainfall distributed evenly throughout the year The alwaysgreen dense forest occurs in the tropical rainforest without a biologically dry period throughout the year and exceptionally with two months of scarce humidity Colombo and Joly 2010 The dense vegetation consists of tree species shrubs lianas epiphytes and herbaceous species Lisboa et al 2015 This biome is one of 34 world hotspots for biodiversity being a priority for conservation Ribeiro et al 2009 Yet currently 11416 of the original forest cover is made up of small fragments 50 ha with a high degree of isolation Myers et al 2000 Ribeiro et al 2009 The climate can be classified as Af Am or Aw Peel et al 2007 Specifically in the Ducke Reserve where study sites are located the climate is Afi tropical humid equatorial with rainy NovemberMay and dry JuneOctober seasons The mean annual precipitation is 2286 mm and mean annual temperature is 267 C Mendonça et al 2005 The mean monthly temperature is always greater than 18 C Lopes et al 2014 The dominant vegetation in Duke reserve is of the type terra firme which covers most of the Amazon region 65 and is characterized by high richness and diversity of species Silva et al 2016 Only in the 10000 ha of Ducke reserve 1200 tree species were recorded Costa et al 2008 The Amazon aquatic systems have been highly altered by deforestation and construction of dams and this region has suffered from increased droughts in recent decades because of climate change amplified by changes in land use Malhi et al 2008 Castello and Macedo 2016 22 Study sites Fiftythree stream sites 11 in the Atlantic Forest 3 in the Amazon and 39 in the biome of Cerrado were selected for this study conducted in 2015 avoiding periods of high flow dry season in Cerrado The sites included in this study were clearwaters with the exception of the Amazonian blackwater streams They covered a wide range of geographic locations Table 1 Fig 1 from near the Equator 2 S in the Amazon to intermediate latitudes in the Cerrado 1219 S and latitudes closer to the tropic of Capricorn in the Atlantic Forest 1925 S The site longitudes also vary with the Atlantic Forest covering longitudes ranging between 40 and 54 W the Cerrado sites ranging between 46 and 48 W and the Amazon sites at 59 W To select leastdisturbed streams all streams were analysed by experts of each region through an a priori classification system with 8 categorical variables describing alterations in the segment ca 500 m centred at the sampling site and the site ca 50 m This evaluation of streams was based on visual inspection and preexisting information and knowledge At the segment level were evaluated 1 the natural connectivity considering the presence of transversal barriers dams roads 2 riparian vegetation cuts and presence of exotic species 3 land use alterations to natural vegetation 4 urban area impervious surfaces and construction and 5 the sediment load related into turbidity At the site level the aspects evaluated were 6 the morphology instream habitats and modifications in the channel and margins 7 toxic acidification of the water alteration of pH or oxygenation and 8 nutrients and organic contamination adapted from Pont et al 2006 Feio et al 2009 One of 5 qualitative classes were attributed to each variable 1 no evidence of degradationno alteration from natural condition 2 slight degradation with no reflex on the aquatic communities 3 moderate degradation 4 evident degradation 5 strong degradation The leastdisturbed sites selected were those classified with only class 1 or 2 for all variables 23 Abiotic characterization of sites All streams were characterized using abiotic variables that could be related to ecological largescale differences such as biome Cerrado Atlantic Forest Amazon rainforest hereafter referred as Amazon geographic location latitude and longitude lithology and water pH climate mean annual precipitation and air temperature altitude size distance to source km stream order Strahler system Strahler 1952 drainage area km2 and hydromorphological characteristics valley form flat U or V shape channel width m channel form naturally contained meandering and canopy cover shading at zenith Data was obtained in the field coordinates altitude valley and channel form canopy cover of shadow in the channel lithology pH from Geographical Information Systems with QGIS software distance to source stream order drainage area Table 1 Characterization of the study sites by biome average SD and predominant lithology valley form and channel form Biome Cerrado n 39 Atlantic Forest n 11 Amazon n 3 Latitude range 1219S 1925S 2S Longitude range 4148W 4054W 59W Mean annual precipitation mm 116 23 897 533 2438 0 Mean annual air temperature C 23 3 22 3 25 1 Water temperature C 20 1 20 1 25 1 Stream order minmax 14 13 1 Distance to source km 35 34 18 10 07 01 Altitude m 1005 89 318 238 79 29 Lithology dominant clay 1 sand 2 schist 3 granite 4 25 08 30 16 20 00 Valley form dominant flat 1 U shaped 2 V shaped 3 15 06 22 11 10 00 Channel form dominant meandering 1 naturally contained 2 14 05 16 05 20 00 Canopy cover shading at zenith 672 218 901 98 100 00 pH 76 10 72 09 42 00 25 Data analyses 251 Abiotic Principal Components Analysis data transformed by log x 1 and normalized was used to assess the distribution of study sites across biomes based on Euclidean distance resemblance of multivariate data Legendre and Legendre 2012 Significant differences between biomes were assessed by a multivariate PERMANOVA Permutational Multivariate Analysis of Variance Euclidean distance 999 permutations Anderson 2001 The PERMANOVA main outputs are a distancebased pseudoF value of the test analogue to the F statistic for multifactorial ANOVA and a significance p value given by an appropriate permutation procedure for each term Anderson et al 2008 252 Processes patterns Functional differences considering all functional parameters among biomes were assessed through a multivariate PERMANOVA main test and pairwise tests followed by the individual analysis of patterns in total and microbial decomposition primary productivity biofilm growth rates and sporulation rates across biomes with univariate PERMANOVA Data were a priori transformed by log x1 A Canonical analysis of principal coordinates CAP Euclidean distance was also performed to find axes through multivariate cloud of points that best discriminate among a priori defined groups and provide a visual distribution of sites Anderson et al 2008 253 Assemblage structural patterns Macroinvertebrate abundance data were pretreated with log x1 to down weight the effect of abundant species and potential effects of differences in sampling effort between teams in spite of common protocols The hyphomycete assemblages were analysed for only 36 sites 25 Cerrado 8 Atlantic Forest and 3 Amazon The counts were transformed to relative abundances of species in the total spore production and no further transformation was applied Then the invertebrate and fungi assemblages were compared by a CAP analysis and differences tested by a multivariate PERMANOVA BrayCurtis similarity coefficient In addition SIMPER similarities percentage analysis was used to analyse the most contributive species within biomes Diversity indices were also calculated to compare the number of taxa S Margalef richness index d S 1 ln N where N number of individuals and equitability J Pielous evenness between biomes 3 Results 31 Abiotic characteristics The largest differences among the studied sites of the three biomes were in precipitation lower in Cerrado 115 23 mm and higher in Amazon 24380 mm and in altitude higher in Cerrado 1005 89 m and near sea level in Amazon 79 29 m In addition Amazon sites were acidic but mostly neutral in other biomes The dominant site lithology was varied from clay to granitic The remaining characteristics were more homogenous most sites had a dense canopy cover 60 small distance to source 3 km low stream order 4 naturally constrained channels and flat or U shaped valleys The Principal Components analysis Fig 2 based on abiotic parameters except coordinates explained 686 of sites variability in the first 3 axes PC1 339 PC2 192 PC3 155 Biomes are mostly discriminated over PC1 especially by temperature eigenvector 0511 and precipitation 0485 being higher in Amazon and Atlantic Forest sites and by altitude 0444 being higher in Cerrado sites PC2 indicates a division in Cerrado sites by pH 0654 corresponding to streams located in the state of Bahia and those of Amazon and a group of Cerrado with a lower pH versus those in Atlantic Forest and remaining Cerrado sites Flat channel form also distinguished Amazon sites and a group of Cerrado sites from the Atlantic Forest and most Cerrado sites on PC2 0413 Finally PC3 is better correlated with lithology 0546 and channel form 0511 PERMANOVA confirmed that there are overall differences PseudoF 11691 p 0001 998 perm and among all biomes considering their abiotic characteristics Pairwise tests t 3152 p 0001 998 perm Atlantic Forest vs Cerrado t 2220 p 0006 278 perm Atlantic Forest vs Amazon t 4090 p 0001 996perm Cerrado vs Amazon 32 Functional parameters The overall functional variation considering all functional parameters between biomes was analysed based on data of 45 sites excluding sites with missing data for any of the functional variables PERMANOVA indicated that biomes were functionally different PseudoF 11885 p 0001 999perm The MDS plot Fig 3 and pairwise tests show that these differences mainly resulted from differences between Amazon and Atlantic Forest t 4554 p 0005 164 perm and between Amazon and Cerrado sites t 4486 p 0001 940 perm whereas the Atlantic Forest and Cerrado sites were only approached significance t 1682 p 0068 Total decomposition rates were significantly different among all biomes for the 51 sites analysed PseudoF 10898 p 0001 998 perm pairwise tests t 4022 p 0011 283 perm for Amazon vs Atlantic Forest t 4072 p 0001 951 perm for Amazon vs Cerrado t 2114 p 005 994 perm for Atlantic Forest vs Cerrado Microbial decomposition varied also among biome sites PseudoF 7277 p 0003 998 perm but was only significantly different between Amazon and Fig 2 Principal Components Analysis data transformed by log x1 and normalized based on abiotic characteristics of Cerrado grey open circles Atlantic Forest grey squares and Amazonia black triangles biome sites Atlantic Forest t 3258 p 0012 335 perm and Amazon and Cerrado t 3442 p 0001 953 perm sites whereas no significant differences were found between the Atlantic Forest and Cerrado t 1619 p 0109 994 perm Both total decomposition and microbial decomposition were lower in Cerrado sites 151 129 and 139 132 and highest in Amazon sites 470 152 mass loss in 60 days 416 101 respectively with intermediate values in the Atlantic Forest sites 237 70 and 215 93 and Fig 4A The sporulation rates of aquatic hyphomycetes differed significantly between all biomes PseudoF 38085 p 0001 999perm Pairwise tests confirm differences between Amazon and Atlantic Forest t 3407 p 0009 165 perm Amazon and Cerrado t 7988 m p 0001 937 perm and between Cerrado and Atlantic Forest t 2623 p 0017 996perm sites Lowest values were found in Cerrado 066 057 conidia mgAFDM1 d1 and Atlantic Forest 139 123 conidia mgAFDM1 d1 sites but substantially higher in Amazon sites 6319 5679 conidia mgAFDM1 d1 Fig 4B However the parameters associated with biofilms on artificial substrates were not significantly different among biomes Chla PseudoF 2119 p 0146 999 perm biofilms growth Pseudo F 0320 p 0293 996perm 51 sites analysed Fig 4C and D Yet the Chla showed a similar pattern of variation as decomposition with lower values in Cerrado 00101 00182 mg m2 d1 and Atlantic Forest 00171 00315 mg m2 d1 sites and higher values in Amazon sites 00326 00368 mg m2 d1 Fig 4C The biofilm growth rate was highly variable especially in the Cerrado where the highest values were reached Fig 4D 33 Assemblages 331 Invertebrates A total of seventy macroinvertebrate families Table S1 were identified in the three biomes with 15 min to 27 max familiessample mean 193 67 in Amazon sites 527 mean 217 55 in the Atlantic Forest and 236 132 91 in Cerrado sites The SIMPER analysis Table 2 indicates that Cerrado and the Atlantic rainforest had a comparable withinbiome similarity ie similarity between assemblages found in sites of the same biome regarding the invertebrates 32 and 29 respectively while the Amazonian samples were more alike 72 Yet the most representative families of the invertebrate assemblages were similar for the three biomes eg Chironomidae Elmidae Ceratopogonidae Leptoceridae Hydropsychidae Eight families were only representative of Cerrado sites but had a low contribution to the within biome similarity eg Calopterygidae Coenagriodinae Polycentropodidae and Pyralidae seven families were representative of the Atlantic rainforest eg Megapodagrionidae Palaemonidae and Hyalellidae and four representative of the Amazon rainforest Palaemonidae Dytiscidae Glossossomatidae Gerridae and Scirtidae Macroinvertebrate assemblages were significantly different among biomes PseudoF 22328 p perm 0002 997 perm Pairwise tests showed that differences were significant between Cerrado and Amazon sites t 1488 p 0025 952 perm and Cerrado and the Atlantic Forest t 1533 p 0018 998 perm but only nearly significant between Amazon and Atlantic Forest sites t 1342 p 0078 275 perm The CAP plot confirms these patterns Fig 5 In addition it is clear that among biomes the geographic proximity given by the state is not necessarily associated with assemblages similarity 332 Fungi Fourteen species of aquatic hyphomycetes were identified in this study Table S2 The total number of species found in biomes varied between 4 in Amazon rainforest and 12 in Cerrado with an intermediate value in Atlantic rainforest 9 The SIMPER analysis Table 3 indicates that Cerrado and the Atlantic rainforest had again a comparable withinbiome similarity Fig 3 Canonical analysis of principal coordinates CAP based on decomposition rates total and microbial primary productivity and growth rate of biofilms and sporulation rates log x1 transformation from 45 stream sites located in Cerrado grey open circles Atlantic Forest grey squares and Amazonia black triangles biomes States where the sites are located are given by the codes AM Amazon BA Bahia Minas Gerais MG DF Distrito Federal ES Espírito Santo RJ Rio de Janeiro PA Paraná Santa Catarina SC Abiotic differences were reflected in the global patterns in processes and assemblages of the aquatic ecosystems These findings are in accordance with the early study on functional ecosystem parameters of Minshall et al 1983 in temperate North American streams which found that although the gradual change proposed by the RCC was verified there variations between biomes due to different regional climate geomorphological and riparian conditions Our results are also in accor dance with the Stream Biome Gradient Concept Dodds et al 2015 This concept proposes that the same factors controlling terrestrial communities temperature and precipitation can be assumed to influence stream ecosystems because of their direct influence on hydrology geomorphology and interactions with terrestrial vegetation However the similarity patterns observed among biomes differed depending on the structural and functional components considered no significant differences in parameters associated with biofilms growth rate and primary production sig nificant differences among all biomes for total decomposition and sporulation rates and partial and partial for invertebrate and fungi assemblages These results partially confirm our hypothesis of aquatic differences among terrestrially defined biomes Some authors have found different patterns between aquatic and terrestrial ecosystems among biomes for example in litter decomposition which may be due to the longitudinal character of rivers not present in land where water and nutrients move continually downstream Gessner et al 2010 GarcíaPalacios et al 2015 The fact that water travels in watercourses across large areas may contribute to explain these lower differences among aquatic ecosystems In addition the transitional character of the riparian vegetation between biomes may be at the same time a consequence and a contribute to the higher similarity in aquatic systems dependent on terrestrial organic matter and energy inputs Gonçalves et al 2014 Rezende et al 2016 Bambi et al 2017 This is however an unexplored hypothesis in the literature The fact that total decomposition varied among all biomes may be related to the strong association of this aquatic process to the terrestrial systems as most organic material decomposed in streams is originated from the riparian vegetation Rezende et al 2016 Bambi et al 2017 However the invertebrate assemblages that take part in the decomposition process differed only between the Cerrado and the two rainforests but not among the later This could indicate also a small contribution of invertebrates to the decomposition process of leaf litter in these tropical biomes as proposed by other authors Graça et al 2015 Leite et al 2016 Likewise a study in the terrestrial environment of the Atlantic Forest biome found no relationship between invertebrate species richness and litter decomposition rates Sobrinho et al 2014 However it could also be a response of litterfall patterns and the adaptation of invertebrate assemblages to them Leite et al 2016 In fact a recent study showed a greater and more similar litterfall in the Amazon and Atlantic Forest compared to the Cerrado corresponding to the precipitation patterns Tonin et al 2017 In spite of this the literature is not as consensual as for terrestrial envi ronments White et al 2013 found a relationship between precipitation and litterfall but not with decomposition rates Another possibility is the influence of the parameter measured a recent study showed that it is shredders biomass and not individuals abundance that is positively correlated with decomposition Aguiar et al 2018 This aspect was not assessed here but should be further investigated in acrossbiome studies On the other hand in our study microbial decomposition differed between the two rainforests Amazon and Atlantic Forest which might have compensated for the reduced contribution of invertebrates to decomposition Nevertheless no differences were found among biomes in the aquatic hyphomycete assemblages associated with the balsa wood and the most representative species was the same Yet sporulation rates of aquatic hyphomycete which are associated with microor ganisms metabolism Suberkropp and Chauvet 2001 Medeiros et al 2009 Graça et al 2015 differed among biomes This Table 2 Taxa contributing most to the within biome BrayCurtis similarity up to 90 cumulative contribution SIMPER analyses based on macroinvertebrate assemblage contributive presenceabsence data Cerrado Atlantic Forest Amazon Aeshnidae 5 Baetidae 2 Calamoceratidae 2 Calamoceratidae 7 Calamoceratidae 3 Ceratopogonidade 4 Ceratopogonidade 4 Ceratopogonidade 12 Chironomidae 41 Chironomidae 15 Chironomidae 22 Elmidae 15 Elmidae 28 Elmidae 10 Dytiscidae 2 Gomphidae 1 Helicopsychidae 3 Helicopsychidae 5 Hydropsychidae 6 Hydropsychidae 3 Hydropsychidae 3 Leptoceridae 3 Leptoceridae 15 Leptoceridae 7 Leptohyphidae 1 Leptohyphidae 6 Leptophlebiidae 4 Leptophlebiidae 3 Leptophlebiidae 8 Libellulidae 1 Megapodagrionidae 3 Odontoceridae 5 Perlidae 5 Perlidae 3 Polycentropodidae 1 Palaemonidae 9 Simuliidae 4 Tipulidae 2 MJ Feio et al Global Ecology and Conservation 16 2018 e00498 9 Fig 5 Canonical analysis of principal coordinates CAP of macroinvertebrate assemblages log x1 transformation in 53 stream sites located in Cerrado grey open circles Atlantic Forest grey squares and Amazonia black triangles biomes States where the sites are located are given by the codes AM Amazon BA Bahia Minas Gerais MG DF Distrito Federal ES Espírito Santo RJ Rio de Janeiro PA Paraná Santa Catarina SC Fig 6 Canonical analysis of principal coordinates CAP of aquatic hyphomycetes assemblages log x1 transformation in 36 stream sites located in Cerrado grey open circles Atlantic Forest grey squares and Amazon black triangles biomes States where the sites are located are given by the codes AM Amazon BA Bahia Minas Gerais MG DF Distrito Federal ES Espírito Santo RJ Rio de Janeiro PA Paraná Santa Catarina SC on the functionalstructural variable used Two further steps should include testing the effect of disturbance and temporal variability on each of these potential indicators The reduced number of studies on tropical stream biofilms specially related with the influence of light and on their potential as bioindicators also show the necessity of investigating more patterns of variation at large and small scales but see BurgosCaraballo et al 2014 Burns and Ryder 2001 NeresLima et al 2016 Finally future studies should test the patterns evidenced here with sites from other areas of the three biomes and especially with more Amazon sites which was the least represented biome Acknowledgements The authors acknowledge the support of MARE strategic program UIDMAR042922013 CAPESBrasil for the program Atração de Jovens Talentos 88881062146201401 and fellowships attributed to RTM 88882306486201801 and to ALLS AUXPEPNPD31382010 FAPESB RED 00222013 FAPES for the fellowship granted to MM TO 02642016 CNPq for the research productivity grant awarded to MC CNPq 30338020152 the financial support from PD AneelCemig GT599 in Minas Gerais INCT ADAPTAll CNPqFAPEAM for supporting field sampling in Amazon ALLS and MMP are grateful to the staff of Laboratory of Freshwater Ecology Federal University of Santa Catarina Brasil for the field support YM are grateful to the logistic support of the Univ Federal do Paraná JSF and IM are PhD students of Programa de Pósgraduação em Ecologia Conservação e Manejo da Vida Silvestre in UFMG Appendix A Supplementary data Supplementary data to this article can be found online at httpsdoiorg101016jgecco2018e00498 References AbdelRaheem A Shearer CA 2002 Extracellular enzyme production by freshwater ascomycetes Fungal Divers 11 119 Aguiar AC NeresLima V Moulton TP 2018 Relationships of shredders leaf processing and organic matter along a canopy cover gradient in tropical streams J Limnol 77 109120 Alvim EACC Medeiros AOM Rezende RS Gonçalves JFJr 2014a Leaf breakdown in a natural open tropical stream J Limnol 73 248260 Alvim EACC Medeiros AOM Rezende RS Gonçalves JFJr 2014b Small leaf breakdown in a savannah headwater stream Limnologica 51 131138 Anderson MJ 2001 A new method for 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