Homogenization of diatom assemblages is driven by eutrophication in tropical reservoirs

A homogeneização de conjuntos de diatomáceas é impulsionada pela eutrofização em reservatórios tropicais

ABSTRACT

Eutrophication is one of the most widespread causes of biotic homogenization in freshwater ecosystems. Biotic homogenization can be characterized as reductions in local diversity (alpha) and occupation of available niches by more generalist species. Beta diversity is expected to decrease in more homogeneous communities, however, there is no consensus on how it responds to eutrophication. We used a space-for-time approach to analyze the process of biotic homogenization on diatom assemblages in response to eutrophication in tropical reservoirs ranging from oligotrophic to hypereutrophic conditions. Diatom assemblages were analyzed in phytoplankton and surface sediment from 12 reservoirs with different trophic levels. We calculated total beta diversity and turnover and nestedness components and used regressions to analyze their relationships with productivity differences (without distance effects). Total beta diversity had a positive influence of the trophic gradient, whereas turnover was not related to eutrophication. However, we found that eutrophication and lower species richness (alpha diversity) led to increasing rates of the nestedness component. We also observed that the homogenization process was not characterized by invasion of new species, but, on the contrary, by filtering nutrient-rich tolerant species also present in oligo-mesotrophic reservoirs and able to occupy available niches in the eutrophic reservoirs. These findings (increase in nestedness, decrease in alpha diversity, and development of tolerant species) suggest that biotic homogenization is leading to a simplification of diatom assemblages in tropical reservoirs, making assemblages from eutrophic and hypereutrophic reservoirs a subset of assemblages from oligotrophic and mesotrophic ones. 

 Keywords:  Beta diversity, Biodiversity, Nestedness, Trophic gradient

RESUMO

A eutrofização é uma das causas mais comuns de homogeneização biótica em ecossistemas de água doce . A homogeneização biótica pode ser caracterizada como reduções na diversidade local (alfa) e ocupação de nichos disponíveis por espécies mais generalistas . Espera-se que a diversidade beta diminua em comunidades mais homogêneas, no entanto, não há consenso sobre como ela responde à eutrofização. Usamos uma abordagem espaço-tempo para analisar o processo de homogeneização biótica em assembleias de diatomáceas em resposta à eutrofização em reservatórios tropicais variando de condições oligotróficas a hipereutróficas. As assembleias de diatomáceas foram analisadas em fitoplâncton e sedimento de superfície de 12 reservatórios com diferentes níveis tróficos . Calculamos a diversidade beta total e os componentes de turnover e aninhamento e usamos regressões para analisar suas relações com diferenças de produtividade (sem efeitos de distância). A diversidade beta total teve uma influência positiva do gradiente trófico, enquanto o turnover não estava relacionado à eutrofização. No entanto, descobrimos que a eutrofização e a menor riqueza de espécies (diversidade alfa) levaram ao aumento das taxas do componente de aninhamento . Observamos também que o processo de homogeneização não foi caracterizado pela invasão de novas espécies, mas, ao contrário, pela filtragem de espécies tolerantes, ricas em nutrientes, também presentes em reservatórios oligo-mesotróficos e capazes de ocupar nichos disponíveis em reservatórios eutróficos. Esses achados (aumento da aninhamento , diminuição da diversidade alfa e desenvolvimento de espécies tolerantes) sugerem que a homogeneização biótica está levando a uma simplificação das assembleias de diatomáceas em reservatórios tropicais, tornando as assembleias de reservatórios eutróficos e hipereutróficos um subconjunto das assembleias de reservatórios oligotróficos e mesotróficos.

Palavras-chave: Beta diversity, Biodiversity, Nestedness, Trophic gradient

Introduction

Currently, biodiversity loss has been documented as one of the main consequences of anthropogenic stressors (Dudgeon et al., 2006; Reid et al., 2018). These losses are not simply characterized by reductions in local species richness (alpha diversity), but they also imply regional taxonomic simplification of the communities (Solar et al., 2015), which is demonstrated in lower beta diversity (i.e., variation in assemblage compositions among sites). Reductions in alpha and beta diversities may be followed by the spread of more generalist species and regional extinctions of rare and specialist species in response to environmental changes, a process known as biotic homogenization (Olden, 2006; Petsch, 2016), whose consequences include loss of ecosystem stability, thus reducing its resilience in coping with environmental disturbances (Hughes and Stachowicz, 2004).

Biotic homogenization in response to anthropogenic stressors has been reported for both terrestrial and freshwater ecosystems. For instance, removal of forested areas for agricultural use has led to the biotic homogenization of several animal and plant groups (Solar et al., 2015), as well as soil microbial communities (Rodrigues et al., 2012) in the Amazon region. In wetlands, the degradation and consequent habitat simplification has increased the similarity on plant, diatom, zooplankton, and macroinvertebrate communities (Lougheed et al., 2008). Urbanization can be also pointed out as one of the main causes of biotic homogenization, as it often produces a disturbed and homogeneous environment that leads to local extinction, subsequently leaving the environment more susceptible to invasion of alien species (Blair, 2001; McKinney, 2006). Schwartz et al. (2006) observed an association between higher extinction rates of rare plant species in Californian flora and human population density, suggesting urban development as a cause of biotic homogenization.

In freshwater ecosystems, urbanization can promote water degradation, leading to eutrophication (Fontana et al., 2014; Zorzal-Almeida et al., 2018), which, when derived from nutrient enrichment (mainly nitrogen and phosphorus), can be a cause of biotic homogenization in these ecosystems (Donohue et al., 2009; Menezes et al., 2015; Wengrat et al., 2018). Reductions in environmental heterogeneity seem to be a key factor leading to this phenomenon, filtering species that succeed under more eutrophic conditions (Menezes et al., 2015). Contradictorily, beta diversity can be positively influenced by eutrophication at regional scales (Chase, 2010), whereas local diversity seems to be higher at intermediate levels of nutrient concentration (Svensson et al., 2007). Even though eutrophication has been suggested to both increase and decrease the turnover component (Chalcraft et al., 2008) and since the nestedness process cause species loss in response to some event that promotes disaggregation, it is reasonable to expect nestedness rates to increase with nutrient enrichment (Baselga, 2010).

Although diatom assemblages from tropical reservoirs have shown a process of biotic homogenization in response to eutrophication (Wengrat et al., 2018), it has not yet been analyzed whether the similarity among communities in eutrophic environments (1) is due to a sorting/selecting species that leads to a lower species richness, or (2) the local extinctions that generates a community composed by a subset of a richest community. Therefore, partitioning beta diversity into its components of turnover and nestedness (species substitution and species loss, respectively) could be an interesting way to solve that gap, since they help to access the processes that underly beta diversity. In addition, spatial data can be an alternative for the lack of long time series, often necessary in biotic homogenization studies. However, long time series (e.g., monitoring programs) demands greater human and financial efforts to maintain the research, which makes space-for time approach an interesting alternative. Accessing spatial patterns of biotic homogenization may give insights on how the process occur over time, which is in the core of the space-for-time approach (Blois et al., 2013). Despite its use in freshwater ecology (Thomaz et al., 2012), to our knowledge, no studies have explicitly used space-for-time approach to assess the effects of eutrophication on biotic homogenization.

We carried out samplings ranging a broad productivity gradient – from oligotrophic to hypereutrophic conditions – to investigate if the spatial biotic homogenization in a series of tropical reservoirs occurs in response to anthropogenic eutrophication. Our hypothesis is that eutrophication leads to the homogenization of diatom assemblages in tropical reservoirs. We predicted that (i) turnover rates should not increase with eutrophication, since species replacement is not expected in homogenization processes, (ii) the nestedness component should increase with higher eutrophication levels, and that (iii) homogenization leads to species loss, making diatom assemblages from more productive reservoirs a subset of those that are less productive. Finally, we made some considerations regarding using the space-to-time approach in diatom assemblage homogenization.

Section snippets

Study area

This study was conducted in 12 man-made reservoirs distributed in three watersheds of São Paulo State, southeastern Brazil (Fig. 1), encompassing an area lager than 31′000 km², located between 46°25′W – 48°22′W and 22°37′S – 23°39′S. Five of the reservoirs are components of the largest water supply system in the world (Cantareira System) and are connected via tunnels. All waters from the reservoirs flow into the Barra Bonita reservoir, located in the Tietê River, the largest river in the

Results and discussion

The reservoirs trophic state ranged from oligotrophic to hypereutrophic conditions, pH mean values ranged from slightly acidic (6.4) to alkaline (8.6), and mean conductivity ranged between 33.6 and 354.2 μS cm⁻¹ (Table 1). Using these variables, PCA analysis summarized a total of 91.9% of data variability along the first axis (and 5.2% in the axis 2), and showed strong significant Pearson correlation with the analyzed variables (pH [r = −0.92], conductivity [r = −0.96], total phosphorous

Conclusions

We conclude that eutrophication can cause homogenization of the diatom assemblages in tropical reservoirs, leading to a lower number of species and selecting more tolerant species, which are a subset of communities from less impacted environments. Despite being recognized as one of the main threats to aquatic ecosystems for decades, eutrophication remains relevant and challenging in terms of diversity loss. The space-for-time approach is a viable alternative to understand the biotic

Authors’ contributions

ECRB, SZA and DCB contributed to conceptualization, writing – review & editing. ECRB and SZA also contributed in formal analysis and roles/writing – original draft.

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.

Acknowledgments

This study was carried out within the framework of the AcquaSed project, supported by funds from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, AcquaSed Project, n° 2009/53898-9). SZA and ECRB thank their doctoral fellowship (FAPESP 2013/23703-7 and 2013/14337-7, respectively). Funding was also provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Grant 310176/2019-0 to DCB).

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