Environmental factors affect macrophyte diversity on Amazonian aquatic ecosystems inserted in an anthropogenic landscape

Ecological Indicators 113 (2020) 106231

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Environmental factors affect macrophyte diversity on Amazonian aquatic ecosystems inserted in an anthropogenic landscape

T

Ana Luísa B. Faresa,b, Lenize Batista Calvãoa,c, Naiara Raiol Torresa,d, Ely Simone C. Gurgelb, ⁎ Thaísa Sala Michelana,b,c, a Laboratório de Ecologia e Conservação (LABECO) e Laboratório de Ecologia de Produtores Primários (ECOPRO), Instituto de Ciências Biológicas, Universidade Federal do Pará, Rua Augusto Corrêa 1 - Guamá, 66075-110 Belém, PA, Brazil b Programa de Pós-Graduação em Ciências Biológicas – Botânica Tropical – Museu Paraense Emílio Goeldi e Universidade Federal Rural da Amazônia, Campus de Pesquisa, Coord. Botânica – COBOT, Av. Perimetral 1901, Terra Firme, 66077-530 Belém, PA, Brazil c Programa de Pós-Graduação em Ecologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Rua Augusto Corrêa 1 - Guamá, 66075-110 Belém, PA, Brazil d Programa de Pós-Graduação em Ecologia Aquática e Pesca, Instituto de Ciências Biológicas, Universidade Federal do Pará, Rua Augusto Corrêa 1 - Guamá, 66075-110 Belém, PA, Brazil

A R T I C LE I N FO

A B S T R A C T

Keywords: Aquatic plants Land use change Bioindicators Eastern Amazon Neotropical freshwaters

Land use is considered one of the most serious drivers of biodiversity change. Aquatic macrophytes are sensitive to changes occurring within their physical habitat and respond at different scales to the effects of land use. Our main objective was to evaluate the effects of multiple land uses on macrophyte diversity. For that, we surveyed aquatic macrophyte richness and cover, in addition to local (water parameters and canopy cover) and landscape (land use and land cover) environmental variables. We evaluated 30 aquatic ecosystems and the results showed canopy cover was negatively correlated with temperature and land use gradient, indicating this parameter reflects land use change within sites. Species richness was affected negatively by canopy cover. Forest cover loss could change macrophyte microhabitats, increasing light resources that favor species that otherwise would not be able to occur there. Species composition was related negatively with canopy cover and water turbidity, and positively related to pH. Three species were selected as indicators of change in canopy cover, which reflects land use change within the sites. Land use change favors mostly emergent and amphibious species, and some species belonging to other life-forms that show adaptations and niche requirements that are benefited by it. Macrophyte communities could be experiencing succession, in which the appearance of invasive species could be the onset of a reduction in diversity as land use consequences become abrasive. We recommend different aspects of macrophyte communities (e.g. species richness, composition, life-form diversity, presence of invasive species, and taxon-specific niche requirements) to be considered when creating indexes of integrity, and when making management decisions regarding the preservation of Amazonian freshwater ecosystems, due to their great potential as indicators, and in order to maintain overall aquatic biodiversity.

1. Introduction Most of the world’s natural landscapes have suffered with humaninduced changes (Foley et al., 2005; González-Abraham et al., 2015; Vitousek et al., 1997) consequent of the global demand for natural resources (Sala et al., 2000). This intense exploitation contributes to increased deforestation rates on tropical forests, such as the Amazon. Deforestation may transform the landscape into a mosaic comprised of different land uses (Malhi et al., 2014) and affect many ecosystems inserted in the landscape, especially freshwater ecosystems (Castello

et al., 2013; Castello and Macedo, 2016). Such landscape changes result in environmental degradation of both terrestrial and aquatic habitats (Dunlap and Jorgenson, 2012; Vitousek et al., 1997), which consequently causes loss of species, changes in community structure and ecosystem disturbance, affecting global biodiversity (McKinney and Lockwood, 1999; Vitousek et al., 1997). Land uses are distributed and changed in an heterogeneous and continuous manner, and are the result of overlapping factors, for example, local geography and historical, cultural and technological components of each society (González-Abraham et al., 2015). Land use

⁎ Corresponding author at: Laboratório de Ecologia e Conservação (LABECO) e Laboratório de Ecologia de Produtores Primários (ECOPRO), Instituto de Ciências Biológicas, Universidade Federal do Pará, Rua Augusto Corrêa 1 - Guamá, 66075-110 Belém, PA, Brazil. E-mail address: [email protected] (T.S. Michelan).

https://doi.org/10.1016/j.ecolind.2020.106231 Received 16 October 2019; Received in revised form 23 January 2020; Accepted 17 February 2020 1470-160X/ © 2020 Elsevier Ltd. All rights reserved.

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in altered environments and could consequently be indicators of environmental alterations? Based on the findings of Akasaka et al. (2010), Alahuhta et al. (2014), Bleich et al. (2015), Mackay et al. (2010) and Mikulyuk et al. (2011) regarding the consequences of anthropogenic pressure throughout the world on different macrophyte diversity measures, we hypothesize that: i) macrophyte species richness will increase in a multiple land use gradient, due to canopy openness, especially in sites dominated by pasture and bare soil. In addition, ii) macrophyte species composition will change along a land use gradient such that sites with a higher percentage of primary and secondary forest (less altered sites) will have a higher life-form diversity than sites with more pasture and bare soil, once altered sites will favor amphibious and emergent species dominance, especially pioneer species.

effects on freshwaters follow such patterns, once water bodies are affected mainly by alterations to riparian vegetation structure (increasing canopy openness), which causes channel siltation and changes water chemistry and quality (Castello and Macedo, 2016; Johnson and Angeler, 2014; Sala et al., 2000). Such consequences harm the physical integrity of freshwaters, leading to habitat loss (Sala et al., 2000), which directly affect the local aquatic biota structure (Allan, 2004; Johnson and Angeler, 2014). Aquatic macrophytes are organisms influenced by environmental conditions created by land use. This happens because macrophyte diversity is influenced directly by physicochemical conditions of freshwaters (Alexander et al., 2008; Aoki et al., 2017; Schneider et al., 2015), making them sensitive to environmental change. Environmental factors such as light incidence, nutrient availability, and physical morphology of freshwaters, are examples of limiting factors that can affect macrophytes together or isolated (Aoki et al., 2017; Bando et al., 2015; Bornette and Puijalon, 2011; Schneider et al., 2015), and all of these factors can be affected by land use change (Johnson and Angeler, 2014; Mikulyuk et al., 2011; Sala et al., 2000). Furthermore, macrophytes respond at different scales to land use effects, especially because of their different life-forms (Akasaka et al., 2010). The response could be negative, in which land use reduces macrophyte richness (Sass et al., 2010), and causes dominance (Akasaka et al., 2010), or could be positive. A positive response would provide an increased species richness, due to canopy openness caused by the loss of riparian vegetation and nutrient availability (Bleich et al., 2015; Elo et al., 2018). In all cases, land use alters macrophyte community structure (Elo et al., 2018; Sass et al., 2010). For instance, some species can disappear when impacts cause great changes (such as increased water turbidity and channel siltation; Allan, 2004), like submerged and free-floating species (Akasaka et al., 2010; Kolada, 2010; Sass et al., 2010). However, those factors, associated with others, such as canopy openness and nutrient input can also increase growth of tolerant (e.g.: amphibious and emergent life-forms) and opportunistic species (Akasaka et al., 2010; Kolada, 2010; Quinn et al., 2011), and can facilitate invasion by exotic species (Mackay et al., 2010; Quinn et al., 2011). The substitution of submerged and free-floating species by amphibious and emergentdominated communities indicates succession in macrophyte communities (Gołdyn, 2009). Thus, macrophytes are considered bioindicators of ecological and environmental quality of freshwater ecosystems (Alahuhta et al., 2014; Bleich et al., 2015; Kassaye et al., 2016; Kolada, 2010). In addition, some can be used to rehabilitate, remediate (Jones et al., 2018; Kassaye et al., 2016) and restore ecosystems degraded by land use (Alderton et al., 2017), before such systems reach an unrecoverable state. Despite the fact that macrophytes are well-known bioindicators of water quality, and are much used in ecological assessments around the world (Akasaka et al., 2010; Mackay et al., 2010; Mikulyuk et al., 2011; Poikane et al., 2018), there is a lack of studies regarding this subject in regions with high biodiversity that are being subject to intense degradation, especially in areas suffering from stressors resulted from multiple land use. This task is even more urgent in rain forest areas like the Amazonia, where deforestation has increased in recent years (Carvalho et al., 2019; Malhi et al., 2014). Having knowledge about this subject could serve as base study to understand how macrophyte communities respond to environmental degradation in Neotropical areas, and how this can affect other freshwater communities, thus helping with environmental assessments and freshwater preservation. Thus, our objective is to evaluate the effects of land use in aquatic macrophyte diversity, using variables that can explain macrophyte distributional patterns along the sampled environments. We aimed to answer the following questions: i) Do multiple land uses affect aquatic macrophyte richness? Which environmental variables affect species richness? ii) Is there a difference between macrophyte community composition along a multiple land use gradient? If so, which local environmental variables are affecting them? iii) Which species are favored

2. Material and methods 2.1. Study area Sampling took place in 30 sites encompassing streams (20), lakes (6) and ponds (4), located in Paragominas, Pará, Brazil (Lat: 02°59′45″ S; Long: 47°21′10″ W), and inserted within the Capim River Basin (see details in Supplementary Materials – Fig. S1). The climate is characterized as humid and hot, with a mean annual temperature of 26 °C, mean air humidity of 81%, and mean annual precipitation of 1.800 mm (Pinto et al., 2009). The type of vegetation at Paragominas consists of a tropical rainforest formation, once the municipality is located within the world’s largest remaining tropical forest, the Amazon. In addition, a range of human activities are carried out along its territory (e.g., agriculture, pasture, logging and mining activities; Gardner et al., 2013; Pinto et al., 2009). 2.2. Sampling design We sampled macrophyte abundance-based composition data, in July 2017, with a 1 m2 (1 m × 1 m) quadrat, placing it in one place within each sampling site. A percentage of cover (%) was assigned to each species inside the quadrat, and used as a surrogate for macrophyte composition. For that measure, each quadrat was considered an independent sample and the sampling was established on places with well-developed macrophyte mats and with better access, so we could make the most precise cover estimation. Species richness data were sampled by taking notes of all macrophyte species occurring in a 150 m transect of each aquatic ecosystem. All sampling sites were located at least 1 km apart from each other. Macrophytes were identified in the field, and the non-identified material was collected, identified using specialized literature (i.e., Amaral et al., 2008; Lorenzi, 2008; Pott and Pott, 2000), consulting specialists, and comparing with herbarium material and was later deposited in the João Murça Pires (MG) Herbarium, located in the Museu Paraense Emílio Goeldi (State of Pará, Brazil). Life-forms were categorized following de Esteves (2011), Amaral et al. (2008), Pott and Pott (2000) and Abe et al. (2015) in addition to field observations. Limnological data (local environmental variables) were measured using a multiparameter probe (Horiba U-50) and comprised pH, temperature (°C), water turbidity (NTU), conductivity (µS/cm), dissolved oxygen (mg/L) and total dissolved solids (ppm). We also measured canopy cover above the quadrats using a densitometer, which we later converted to percentage, according to the index proposed by Peck et al. (2006). 2.3. Obtention of remote sensing data for land use and land cover characterization Landscape variables consisted of land use and land cover classes present on the 30 sampling sites, which were characterized using different geoprocessing software: ArcGIS 10.1 (ESRI, 2014), PCI 2

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changes along a land use gradient, and see which environmental variables affected species composition, we used a distance-based redundancy analysis (dbRDA), a model that accepts different types of distance matrices (Legendre and Anderson, 1999), and enables us to control the influence of one or more variables in the analysis using the “condition” function. Therefore, it allowed us to use a Bray-Curtis matrix for abundance-based composition data, a set of environmental predictors, and to control the effects of ecosystem type. The species matrix was log-transformed, while the environmental matrix was standardized. We validated this model using a permutation test at 999 permutations. To answer question (iii), of which life forms are favored in altered environments and therefore could be indicators of such state?, we performed a Threshold Indicator Taxa Analysis (TITAN) for each environmental variable (Baker and King, 2010). TITAN combines and extends Change-point Analysis (King and Richardson, 2003; Qian et al., 2003) and Indicator Species Analysis (IndVal; Dufrêne and Legendre, 1997), aiming to identify taxon-specific responses to anthropogenic changes to assess in which point the community as a whole exhibits a tipping point as a response to continuous environmental gradients (Baker and King, 2010). In this study, we ran the analysis using 500 iterations and excluded all taxa that had < 3 occurrences from our community matrix, following Baker and King (2010). For more details on the TITAN analysis see Baker and King (2010). We performed all analyses in software R 3.5.1 (R Core Team, 2018). We Performed PCA using the function ‘prcomp’ in R core package. For the GLMM, we used the ‘glmer.nb’ function of the package lme4 version 4.1-1 (Bates et al., 2015). For dbRDA, we used the function ‘capscale’ on the package vegan version 2.5-3 (Oksanen et al., 2018). We ran TITAN in the package TITAN2 version 2.1 (Baker et al., 2015).

Geomatica V10.1 (Hill, 2007) and Ecognition 9 (Definiens, 2009). We identified land use and land cover classes using Image Digital Processing (PDI) from the RapidEye Earth Imaging System (REIS) optic sensor. Images were obtained from the Brazilian Ministry of Environment website (http://geocatalogo.mma.gov.br/). Images were selected from 2015, the most recent year available in the database. REIS images were obtained and orthorectified in a geographic coordinates system projected in the geodesic DATUM WGS 84. The images underwent an atmospheric correction, i.e., a process that attenuates effects of the atmosphere in the spectral response of a target and converts pixel values from digital numbers to reflectance values. Atmospheric correction was conducted using PCI Geomatics 2015 software and ATCOR Ground Reflectance module. Then, we built the mosaic in PCI Geomatica OrtoEngine module. The REIS mosaic was submitted to a guided object classification using Ecognition 9. We validated the classes using TerraClass 2014 images provided by the Brazilian National Institute for Space Research – INPE (Almeida et al., 2016). We then calculated the Kappa Index (0.72), which reflects the supervised classification quality, and ranked it according to Landis and Koch (1977). Thus, we considered it acceptable for the results obtained. Land use/land cover classes of the sites were established according to De Almeida et al. (2016). We identified: (a) Primary vegetation, which comprises areas occupied by tropical rainforest; (b) Secondary vegetation, a vegetation resulted from a natural succession process after total or partial primary vegetation suppression after natural or anthropogenic processes; (c) Pastures, areas occupied by intensive and/or extensive livestock breeding, and (d) bare soil, areas of unprotected soil, especially those containing road systems such as dirt roads, highways, and mining areas. Each land use/land cover class dimension was quantified in km2 with a 300 m circular buffer around each sampling site using ArcGIS 10.1 software and were later converted to cover percentage (%).

3. Results

2.4. Data analysis

3.1. Community structure and environmental variables

Before performing hypothesis testing, we tested for multicollinearity among environmental predictors using a Spearman Correlation Matrix. We considered the correlation coefficient value of r ≥ 0.6 as significant. Whenever two variables were correlated we selected one to be retained based on the literature (i.e., Akasaka et al., 2010; Aoki et al., 2017; Bando et al., 2015; Bornette and Puijalon, 2011; Mackay et al., 2010). Consequently, we maintained variables that were most important for the biological group, avoiding multicollinearity. Most land use variables were correlated among themselves and were of the same unit. Therefore, we chose to summarize them using a Principal Component Analysis (PCA), for which variables were arcsine-transformed, since they are proportions. We used the Broken-Stick criterion (Jackson, 1993) as a model of axis selection. The axis retained represents land use contribution in one dimension, or the land use gradient, and was used as the land use variable in the correlation analysis. A visual analysis revealed the relationship between species richness and environmental variables was non-normal. Therefore, we used a Generalized Linear Mixed Model (GLMM) to test hypothesis (i) that macrophyte species richness will increase in a multiple land use gradient. We used environmental variables as predictors and species richness as the response variable. GLMMs are suited for data with nonnormal distributions and they can incorporate random effects to account for nested observations (Bolker et al., 2009; Zuur et al., 2009). In this case, we chose to include ecosystem type (stream, pond and lake) as the random effect that was spatially structuring the variables to the model. All environmental variables were standardized. We also tested for overdispersion in the response variable, which was significant. Therefore, the family that best suited the data was the negative binomial (Zuur et al., 2009). Model validation was based on visual analyses of residuals (Zuur et al., 2009). To test hypothesis (ii), that macrophyte species composition

We recorded 49 species, divided among 23 families of vascular plants, ferns and lycophytes, which encompass 5 life-forms: amphibious, emergent, floating-leaved and rooted and free-submerged (see Table S1 in Supplementary Materials for all species recorded in this study). Canopy cover varied greatly among ecosystems (0% to 100% cover) and had the largest standard deviation (Table 1). Turbidity also varied greatly among the sampling sites, from 0.600 NTU to 32.167 NTU. Water temperature varied mildly (22.870 °C to 31.110 °C), along with conductivity, dissolved oxygen and total dissolved solids. Landscape variables also varied among sites (Table 1). Primary forest had the highest cover in a site (89.013%) and the highest standard deviation (27.851), followed by bare soil (maximum: 79.676%, Table 1 Environmental variables investigated in the 30 sampling sites collected and their range (minimum and maximum), mean values and standard deviations (SD). Variable Local Canopy cover Temperature pH Conductivity Turbidity Dissolved oxygen Total dissolved solids Landscape Primary vegetation Secondary vegetation Pasture Bare soil

3

Unit

Range (Max–Min)

Mean ± SD

% °C mS/s ntu mg/L ppm

100.000–0.000 31.110–22.870 6.157–3.927 0.160–0.021 32.167–0.600 9.590–3.420 0.104–0.014

43.021 ± 39.615 25.773 ± 1.883 4.934 ± 0.428 0.036 ± 0.010 6.781 ± 6.344 7.018 ± 1.275 0.024 ± 0.007

% % % %

89.013–0.000 72.360–0.000 74.568–0.000 79.676–0.000

36.459 20.485 18.599 22.248

± ± ± ±

27.851 15.740 16.152 17.605

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Table 2 Spearman Correlation Matrix built with the environmental predictors. Bold values indicate correlation coefficient values of r ≥ 0.6. Variables

Temperature

pH

Conductivity

Turbidity

Dissolved oxygen

Canopy cover

Total dissolved solids

pH Conductivity Turbidity Dissolved oxygen Canopy cover Total dissolved solids Land use gradient (PCA axis)

0.140 −0.125 0.106 0.035 −0.657 −0.137 0.604

−0.297 0.033 0.521 −0.099 −0.329 0.091

0.119 −0.128 0.097 0.959 −0.051

−0.136 0.068 0.085 0.037

−0.019 −0.115 −0.252

0.101 −0.618

−0.090

is negatively correlated with canopy cover (−0.767) while the second axis explained 16.18% of fitted variation, and is negatively related with turbidity (−0.679) and positively with pH (0.410). The triplot shows Urochloa arrecta, Utricularia sp., Eleocharis interstincta, E. plicharhachis, Cyperus haspan, and Cabomba aquatica were associated positively with the first axis, which is correlated negatively with canopy cover, meaning the cover of those species increased in sites with decreased canopy cover. Apalanthe granatensis and Xyris jupicai were associated positively with the second axis, which is positively correlated with pH and negatively correlated with turbidity, while Fuirena umbellata was negatively correlated with it. The cover of A. granatensis and X. jupica increased in sites with increased pH and decreased turbidity, while the cover of F. umbellata decreased on those conditions. Calyptrocarya glomerulata, Diplacrum capitatum, Homolepis aturensis, Spermacoce verticillata and Cyclosorus interruptus occurred in sites with increased turbidity. Tonina fluviatilis, Nymphaea rudgeana, E. confervoides, Ludwigia lepdocarpa, Sauvagesia erecta, Leersia hexandra, Ceratopteris thalictroides and Cyperus odoratus occurred in sites with increased pH (Fig. 1).

standard deviation: 17.605), pasture (max: 74.568; SD: 16.152), and secondary forest (Max: 72.360; SD: 15.740). All land use classes failed to occur in at least one site (see Fig. S2 for visual exploration of the variables). 3.2. Summarization of landscape variables The Broken-stick criterion retained the first PCA axis to summarize the landscape variables, which represented 61.24% of total variance. Primary vegetation was the variable that most contributed to the formation of this axis, and was negatively correlated to it, along with bare soil and pasture activities, which were also highly correlated with the first axis, but positively (see Table S2 for PCA results in Supplementary Materials). Canopy cover was negatively correlated with temperature and land use, while conductivity was positively correlated with total dissolved solids (Table 2). Consequently, canopy measurements may be interpreted as a surrogate of land use in the studied systems. In addition, temperature, total dissolved solids and land use gradient were excluded from the other models. Further interpretation of model results will follow as such: sites with reduced canopy cover have high water temperature, reduced primary forest and increased bare soil and pasture cover, while sites with increased conductivity have increased total dissolved solids (Table 2).

3.4. Indicator species of environmental change The TITAN analysis detected three indicator species of changes on canopy cover. The species Eleocharis interstincta (emergent) and Utricularia sp. (free submerged) had a negative response (z−) and were recorded as indicators of reduced Canopy cover, while Triplophyllum dicksonioides (amphibious) had a positive response (z + ) and was selected as an indicator of increased canopy cover (Fig. 2). The change points of canopy cover present in the sampling sites were observed between 71.658% for Utricularia sp. (z score: 3.860) and E. interstincta (z score: 5.480), and 79.546% for Triplophyllum dicksonioides (z score: 6.410) (For additional information, see Table S3 in the Supplementary Materials). No species were selected as indicators of the other environmental factors (conductivity, pH, turbidity and dissolved oxygen).

3.3. Effects of environmental variables on macrophyte species richness and composition To test the effects of environmental variables on macrophyte species richness, we performed a GLMM. The results showed that, among all local environmental variables, species richness is associated negatively with canopy cover (Estimate = −0.374, P < 0.001), increasing with riparian vegetation loss (Table 3). To detect which environmental variables best explained macrophyte community composition structure along the sites, we performed dbRDA. This model showed environmental variables explained 19.840% of community structure, while type of ecosystem (constrained variable) explained 16.090% of variance (F = 1.362; P = 0.016; Df = 5). The first dbRDA axis explained 58.860% of fitted variance and

4. Discussion According to the results, hypothesis (i) and (ii) were corroborated, as aquatic macrophyte species richness was affected negatively by canopy cover, and species composition changed along a canopy cover gradient (which reflects land use change among the sites). Variation in land use can be represented by the proportion of canopy cover among the sites, since the land use gradient was taken out of the models due to correlation with canopy cover. Sites with lower canopy cover have reduced primary forest cover and increased bare soil and pasture covers (more altered), while sites with increased canopy cover exhibited the opposite pattern (less altered).

Table 3 Results of Generalized Linear Mixed Model (GLMM) testing the contribution of environmental variables to explain macrophyte species richness. Bold values indicate signifcant values of p < 0.01. Explanatory variable

Estimate

Std. error

z

P

Intercept Canopy cover pH Conductivity Turbidity Dissolved Oxygen Random effects

1.980 −0.374 0.046 −0.109 −0.051 −0.065

0.074 0.078 0.090 0.085 0.078 0.093

26.702 −4.811 0.513 −1.279 −0.661 −0.692

< 0.001*** < 0.001*** 0.608 0.201 0.509 0.489

Variance < 0.001

Std. Dev. < 0.001

Intercept

4.1. Effects of environmental variables on macrophyte species richness and composition Canopy cover affected macrophyte species richness negatively, meaning richness increased in sites with reduced canopy cover (more altered). Light incidence is considered one of the most important 4

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Fig. 1. Distance-based Redundancy Analysis performed between macrophyte species composition and environmental variables Canopy cover (cano), Conductivity (cond), Dissolved Oxygen (DO), pH (pH) and Turbidity (turb). A) Triplot showing the correlation among species and environmental variables. B) Triplot sowing the correlation among sites and environmental variables. The color scale of the points is according to the percent of Primary Forest cover present in each sampling site.

species are associated with different ranges of light incidence, as some species thrive in shaded habitats, whereas others occur only in lightsaturated habitats (Bornette and Puijalon, 2011). Thus, it is not surprising that, in this study, macrophyte community composition changed along a gradient of light availability. Moreover, Mackay et al. (2010) studied the use of macrophytes as indicators of tropical stream conditions in Queensland (Australia), and suggested the riparian vegetation condition could be used to assess the condition of the macrophyte community in advance. They reported macrophytes responded more strongly to canopy and riparian vegetation metrics than to land use metrics (Mackay et al., 2010). On our study, we recorded a similar pattern, where canopy cover affected species richness as well as macrophyte community structure. The percent cover of amphibious (Cyperus haspan) and emergent (Urochloa arrecta, Eleocharis interstincta, E. plicharhachis) species increased with reduced canopy cover but were not the only favored lifeforms. Those life-forms, considered more tolerant (Akasaka et al., 2010; Kolada, 2010; Quinn et al., 2011), dominated more altered sites, especially those presenting a shift towards shallower and more nutrient-

limiting factors for macrophyte occurrence in freshwaters (Bando et al., 2015; Bornette and Puijalon, 2011; Lacoul and Freedman, 2006). Species richness increases with light availability (Bando et al., 2015; Bleich et al., 2015; Wood et al., 2012). This result is also associated with land use change. Studies have shown intensive land use could increase macrophyte species richness due to several factors, for example sediment and nutrient input, changes in channel morphology (Elo et al., 2018; Mikulyuk et al., 2011), and especially increase in light incidence due to canopy cover loss (Bleich et al., 2015; Mackay et al., 2010). The loss of forest cover, especially of the riparian vegetation, increases light availability on more altered sites (Allan, 2004; Heartsill-Scalley and Aide, 2003). This could change macrophyte microhabitats, increasing availability of light resource, which in turn could favor species that otherwise would not be able to occur there, explaining the increased species richness. Canopy cover, turbidity and pH were the main drivers of macrophyte community structure on this study. The shade created by the riparian vegetation can be considered an environmental filter for macrophyte occurrence (Bando et al., 2015; Wood et al., 2012). Different

Fig. 2. Results of the TITAN on individual species abundance in response to a Canopy Cover gradient. Black circles indicate the species that presented a reduced occurrence (z−) as the environmental gradient increased, and white circles indicate species with increased (z+) occurrence. The size of the circles is proportional to the magnitude of the response (z score). The horizontal lines represent the upper and lower quantiles of the Canopy cover values.

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those species are adapted to more acidic waters, typical of the Amazon River basin (Junk and Howard-Williams, 1984). Rooted-submerged (A. granatensis, E. confervoides and Tonina fluviatilis) and floating-leaved species (Nymphaea rudgeana), could be tolerant to a wide range of alkalinity values, thus occurring in sites where pH increases and approaches neutral values. This does not affect carbon uptake by emergent and amphibious species, which mostly rely on atmospheric carbon (Bornette and Puijalon, 2011), reason why such species were also favored by increasing pH. Studies with macrophytes and human-induced disturbances show an increased species diversity, despite environmental alterations. However, such diversity reduces in time, as impact increases, due to competition with algae (Moore et al., 2010; Theissen et al., 2012), invasive species (Gołdyn, 2009) or simply due to habitat loss caused by channel siltation and drought, as systems become inhospitable for plant life (Gołdyn, 2009; Mikulyuk et al., 2011; Moore et al., 2010). Umetsu et al. (2018) found an excessive growth of emergent species on degraded sites, which they attributed to high nutrient contents on the river substrate, while the occurrence of submerged species richness declined under nutrient-rich conditions. Bleich et al. (2015) also pointed out that emergent species dominate the riparian zone of altered streams draining cattle ranching areas in the Southern Brazilian Amazon and selected some of those emergent species as indicators of altered conditions. The consequences of land use (e.g., loss of canopy cover previously provided by the riparian vegetation and change in water chemistry) favor mostly emergent and amphibious species, along with other lifeforms that show adaptations and niche requirements benefited by land use change. It seems the communities in this area could be experiencing succession, such that the community is starting to shift to another successional stage, i.e., from communities dominated by shade-tolerant amphibious species, to the establishment of submerged species and dominance of open-areas emergent and amphibious species (Gołdyn, 2009; Moore et al., 2010). The appearance of invasive species could indicate the onset of a diversity reduction as the consequences of landuse become more abrasive (excessive nutrients, water turbidity, algae bloom, etc.).

rich environments. However, the percent cover of two submerged species (Utricularia sp. and Cabomba aquatica) also increased under altered conditions. Those species (which co-occurred on many sites) could have niche requirements that are favored in altered environments. C. aquatica is a rooted-submerged species that occurs in freshwaters with elevated light incidence and nutrient input (Ørgaard, 1991; Pott and Pott, 2000), while Utricularia sp. is a carnivorous free-submerged macrophyte that occurs in sites with low light incidence and nutrients, using plankton as a food resource (Pott and Pott, 2000; Raynal-Roques and Jérémie, 2005). It may be that altered sites, with higher light availability, also provided environmental conditions required by those species, and increased habitat heterogeneity (e.g., low water flow, nutrient input and presence of plankton). Low water flow and light incidence benefits C. aquatica, and increases the presence of planktonic organisms, favoring the occurrence of Utricularia sp. Another result is that an invasive species (Urochloa arrecta) was negatively associated with increase in canopy cover, and thus positively associated with land use change. The shade created by the riparian vegetation can limit this species from spreading (Evangelista et al., 2017), which is concerning, once it indicates that the main consequence of land use changes (i.e., riparian vegetation loss) is favoring ecosystem invasion. In addition, several studies have showed land use pressure increases the cover of invasive species (Gołdyn, 2009; Lougheed et al., 2008; Mackay et al., 2010; Quinn et al., 2011; Sass et al., 2010). Disturbances reduce competitive advantages of native species, which added to propagule pressure and eutrophication, facilitates invasion (Shea and Chesson, 2002). Furthermore, the presence of an invasive macrophyte harms native macrophyte communities (Michelan et al., 2010), resulting in loss of several native taxa that provide ecosystem services. Therefore, an invasive macrophyte affects not only macrophyte diversity, but also the diversity of other organisms (e.g., fish, insects and periphyton) depending on them (Lougheed et al., 2008). Water turbidity is a measure of light availability on the water column (Lacoul and Freedman, 2006) and is a metric often used to assess freshwater quality. It is also a limiting factor especially for submerged macrophytes (Akasaka et al., 2010; Lacoul and Freedman, 2006). The species Calyptrocarya glomerulata, Diplacrum capitatum, Homolepis aturensis, Spermacoce verticillata, Cyclosorus interruptus and Fuirena umbellata (emergent and amphibious) occurred at sites with increased water turbidity, while Apalanthe granatensis (submerged) and Xyris jupicai (amphibious) occurred at sites with lower water turbidity. An increase in water turbidity is harmful to most submerged species. Therefore, the absence of submerged species could have given a competitive advantage to emergent and amphibious species. The parameter pH is associated with alkalinity, which affects carbon (both organic and inorganic) availability in the water (de Esteves, 2011). Carbon is important for primary production (Toivonen and Huttunen, 1995) and therefore affects community composition, as macrophytes can use different carbon sources available in both water and air. As such, macrophytes may occur on different pH ranges, but that varies among taxonomic groups and species belonging to the same life form (Alexander et al., 2008; Bornette and Puijalon, 2011; Vestergaard and Sand-Jensen, 2000). The species Apalanthe granatensis, Xyris jupicai, Tonina fluviatilis, Nymphaea rudgeana, E. confervoides, Ludwigia lepdocarpa, Sauvagesia erecta, Leersia hexandra, Ceratopteris thalictroides and Cyperus odoratus were positively associated with increased pH values, while Fuirena umbellata was associated negatively with increased pH. These species belong to several life forms (amphibious, emergent, submerged and floating-leaved), but most are emergent and amphibious species. In this study, pH values varied but remained more acidic towards neutral (Min: 3.927; Max: 6.157; Table 2), which is common for tropical freshwaters (Ríos-Villamizar et al., 2013). On this pH range, carbonic acid (and dissolved CO2) is the most dominant source of inorganic carbon in the water (de Esteves, 2011), and could limit submerged and floating-leaved species as pH approaches neutral values, since most of

4.2. Indicator species Our results pointed to three species as indicators of canopy cover change: two indicated canopy cover loss, and one indicated increase in canopy cover. The emergent species E. interstincta requires a high light availability, often indicates an intermediate stage of plant succession in freshwater ecosystems after the free-floating stage (Pott and Pott, 2000), and occurs in altered sites (Bleich et al., 2015). This species increases its cover mostly by vegetative growth, becoming dominant in the margins of water bodies (Pott and Pott, 2000). E. interstincta could indicate early succession, following primary vegetation loss. Utricularia sp. was also selected as an indicator of decreased canopy cover. Utricularia sp. is a free-submerged species that occurs in places with low light incidence, low nutrient availability and low water flow, and is a carnivorous plant (Pott and Pott, 2000; Raynal-Roques and Jérémie, 2005). Carnivorous species are poor competitors for resources (e.g., light and nutrients), and often need some sort of disturbance to reduce competition intensity (Jennings and Rohr, 2011). Moreover, aquatic carnivorous plants are mostly rootless, obtaining nutrients from the water column by diffusion through leaves and stems; they rarely have specialized structures for long-term nutrient storage (Ellison and Adamec, 2011). Thus, aquatic carnivorous plants rely strongly on the ability of absorbing nutrients from their prey. Our results differ from others, which reported pollution and eutrophication reduced the population of some Utricularia species (Jennings and Rohr, 2011). Maybe this species can thrive in more altered sites, with increased light incidence, because of their carnivorous habit, as they do not depend on nutrients in water to obtain resources 6

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requirements) should be considered when creating indexes of integrity, and when making management decisions regarding the preservation of Amazonian freshwater ecosystems, due to their great potential as indicators, and in order to maintain overall aquatic biodiversity.

for survival, relying on their traps to obtain nutrients by consuming plankton. Studies have shown Utricularia sp. and phytoplankton have a synergistic relationship. Traps of different Utricularia species usually exhibit high amounts of algae, which are possibly consumed, used to attract zooplankton for consumption, or both (Alkhalaf et al., 2009; Díaz-Olarte et al., 2007; Koller-Peroutka et al., 2015). Competition for nutrients favors algae over submerged species in altered sites (with high water turbidity and low water flow; Lacoul and Freedman, 2006), which can increase zooplankton populations, thus increasing resource availability for carnivorous plants (Koller-Peroutka et al., 2015). The species Triplophyllum dicksonioides was selected as an indicator of increased canopy cover. This species is an amphibious fern commonly found in riparian habitats, occurring mostly in shaded and humid sites (Drucker et al., 2008; Paixão et al., 2013), and was recorded on the margins of waterbodies with a surrounding riparian vegetation. A great riparian condition could provide a microclimate (shading and moisture) that is suitable for ferns (Mackay et al., 2010). Thus, as a shade-tolerant amphibious fern, this species could be an indicator of highly shaded (less altered) habitats. The results presented reinforce that macrophyte species are indicators of altered conditions. Moreover, emergent and amphibious species are important as land use indicators, as they can be strong indicators of altered conditions (Alahuhta et al., 2014, 2012; Bleich et al., 2015), and stand out indicating ecological succession in freshwaters. However, we also show that species of similar life forms have different resource requirements when it comes to light availability. There are shade-tolerant amphibious species and light-tolerant emergent species. Finally, another important point to emphasize is that the percent cover of Utricularia sp. increased in response to reduced canopy cover, which is associated with the land use gradient, bringing to light the possible role of its carnivorous habit as an efficient survival strategy in Amazonian freshwater ecosystems affected by land use changes. Carnivorous-prey interactions in impacted areas can be more deeply understood through experimental approaches.

CRediT authorship contribution statement Ana Luísa B. Fares: Conceptualization, Methodology, Investigation, Formal analysis, Validation, Writing - review & editing. Lenize Batista Calvão: Conceptualization, Formal analysis, Writing original draft. Naiara Raiol Torres: Formal analysis, Investigation, Writing - original draft. Ely Simone C. Gurgel: Conceptualization, Writing - original draft. Thaísa Sala Michelan: Conceptualization, Methodology, Investigation, Supervision, Writing - review & editing. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements AL Fares and NR Torres are thankful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001 for their scholarships. LB Calvão is thankful to CNPq (process 154761/2018-4) and BRC (Brazilian Research Consortium) for her postdoctoral scholarship. We thank the Aquatic Biota field crew (Ana Luiza Andrade, Calebe Maia, Carina Paiva, Gilberto Salvador, Leandro Juen, and Thiago Barbosa) for helping with field sampling. We thank André B. Gil for helping with plant identification, and Carina Paiva for her critique on the manuscript, which helped improve the final version of our paper. Funding

5. Conclusions This work was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001 and Hydro Paragominas Company for supporting the research projects “Effects of soil use on diversity and ecophysiology on the riparian vegetation, aquatic macrophytes and plankton in streams and lagoons in mining areas of Paragominas, Pará, Brazil” and “Monitoring Aquatic Biota of Streams on Areas of Paragominas Mining SA, Pará, Brazil” through the Biodiversity Research Consortium Brazil-Norway (BRC). This paper is number 0007 in the publication series of the BRC.

Our results indicate macrophyte community response to freshwater environmental parameters (and consequently to land use) are taxonspecific and vary greatly, and thus they are important indicators of environmental change in Amazonian aquatic ecosystems. For instance, canopy cover loss increases overall species richness, but emergent and amphibious species are dominant under such conditions. However, some submerged species have beneficial adaptations and niche requirements that enable coexistence with dominant species within altered habitats. However, those conditions allow for establishment and spread of invasive species, such as Urochloa arrecta, which can be harmful for native macrophyte diversity on a long-term basis. This study brings information on macrophyte communities inserted in an anthropogenic landscape. Our results show that, with simple diversity measures, such as species richness and composition, we are already able to see the effects of environmental change on macrophyte communities of Amazonian ecosystems, indicating how sensitive this group is, but also how other bioassessment approaches could bring further information regarding freshwater quality and preservation. In addition, some macrophyte species (e.g. Utricularia sp., E. interstincta and Triplophyllum dicksonioides) can be used as indicators of change in environmental conditions affected by land use. We also emphasize on the role of canopy cover provided by the riparian vegetation in structuring macrophyte communities on Amazonian freshwaters. Another step on biological assessment on this area would be incorporating longterm macrophyte monitoring, along with functional and phylogenetic approaches, and integrity index development considering macrophytes as a target biological group. Thus, we conclude that the aspects of macrophyte communities (e.g. species richness, composition, life-form diversity, presence of invasive species, and taxon-specific niche

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