Ephemeroptera genera as bioindicators of agricultural impact on Atlantic Forest streams

Gêneros de Ephemeroptera como biodindicadores de impactos agrícolas em córregos da Mata Atlântica

ABSTRACT

Insects of the Ephemeroptera order have been used as bioindicators of water quality as they respond to countless anthropic impacts. In this study, we assessed the use of Ephemeroptera as bioindicators of streams impacted by agricultural activities. We collected Ephemeroptera nymphs in six streams with different uses and soil cover in their drainage areas located in the northern region of the Brazilian state of Rio Grande do Sul. Based on soil use and cover analysis, we categorized the streams as ‘natural’ (drainage area with >42% native arboreal vegetation) and ‘agricultural’ (drainage area with >72% agricultural use). We collected a total of 2,767 organisms, distributed into four families and eleven genera. We observed greater abundance (68%) and taxonomic richness (11 genera) of Ephemeroptera in the agricultural streams. The natural streams comprise 32% of the fauna collected, with eight genera. That pattern was especially determined by the Baetidae and Leptohyphidae families. The genera Caenis, Cloeodes, and Tricorythopsis were abundant in the agricultural streams. In this study, we observed that genera of Ephemeroptera are tolerant to environmental changes, particularly those caused by agricultural activities. Therefore, the use of the order in studies to assess water quality must be carried out with caution.

KEYWORDS:
Aquatic insects; anthropogenic influence; taxonomic resolution; environmental quality

RESUMO

Insetos da ordem Ephemeroptera tem sido utilizado como bioindicadores de qualidade de água por responderem a inúmeros impactos antrópicos. Neste estudo avaliamos o uso dos Ephemeroptera como bioindicadores de riachos influenciados por atividades agrícolas. Coletamos ninfas de Ephemeroptera em seis riachos com diferentes usos e cobertura do solo em sua área de drenagem localizados na região norte do Rio Grande do Sul. A partir da análise do uso e cobertura do solo, categorizamos os riachos em ‘naturais’ (área de drenagem com >42% de vegetação arbórea nativa) e ‘agrícolas’ (área de drenagem com >72% de uso agrícola na área de drenagem). Coletamos um total de 2767 organismos, distribuídos em quatro famílias e 11 gêneros. Observamos maior abundância (68%) e riqueza taxonômica (11 gêneros) de Ephemeroptera nos riachos agrícolas. Os riachos naturais perfazem um total de 32% da fauna coletada com oito gêneros. Este padrão foi determinado, especialmente, pelas famílias Baetidae e Leptohyphidae. Os gêneros Cloeodes e Tricorytopsis foram abundantes nos riachos agrícolas. Neste estudo, observamos que gêneros de Ephemeroptera são tolerantes a alterações ambientais, sobretudo aquelas causadas por atividades agrícolas. Assim, o uso da ordem em estudos de avaliação da qualidade da água deve ser considerado com cautela.

PALAVRAS-CHAVE:
Insetos aquáticos; influência antrópica; resolução taxonômica; qualidade ambiental

The constant expansion of livestock and agriculture has been responsible for transforming areas with natural vegetation into fields of pasture and crops (Deegan et al., 2011). The increased release of pollutants associated with the use of fertilizers and pesticides (Xiaojing et al., 2021) and the changes in landscape constitute a major environmental issue for the integrity of aquatic ecosystems (Allan, 2004). In streams, for example, riparian zones play a fundamental role in the maintenance of the ecological status of those environments (Burdon et al., 2020; Huiñocana et al., 2020). Fully or partially removing riparian vegetation has negative consequences for the functioning of limnic ecosystems and impact the quality of aquatic environments (Siegloch et al., 2014; Tonello et al., 2021), altering physical and chemical variables of the water.

Among the physical and chemical variables of water, temperature and dissolved oxygen. Sites surrounded by vegetation tend to have lower temperature (Carvalho et al., 2000) and higher dissolved oxygen values (Bueno et al., 2005), besides an impact on the concentration of solids in suspension and turbidity (Silveira, 2004; Palharini & Pagoto, 2015).

On way of assessing aquatic environments is using biological communities. Benthonic macroinvertebrates exhibit broad diversity and are formed by countless taxonomic groups (Serna-López et al., 2020; Kumari & Maiti, 2020; Restello & Hepp, 2020), especially insects belonging to Ephemeroptera. Overall, this order is considered sensitive to anthropic changes, however, studies on Ephemeroptera assemblages show they are sensitive mainly to point-source impacts such as urbanization (Hepp et al., 2013, Buss & Salles, 2007, Rojas-Peña et al., 2021). A study carried out in Costa Rica reported that Ephemeroptera abundance is greater in impacted areas, however, diversity is higher in forest areas (Duschek et al., 2019).

Buss & Salles (2007) pointed out that the order must be used with caution to assess environmental quality since some genera are tolerant to perturbation. Those authors found that not all genera of the Baetidae family are sensitive to anthropic impacts, such as Americabaetis, which was considered tolerant. Hepp et al. (2013) found that Americabaetis, Baetodes, Apobaetis, and Cloeodes were tolerant to limnologic characteristics related to urban impact, such as high pH and low values of dissolved oxygen. Hagenulopsis, Farrodes, and Miroculis occur in streams whose riparian vegetation has been removed for the establishment of agricultural practices, therefore, they are considered indicators of impacted sites (Brasil et al., 2014; Selvakumar et al., 2014). On the other hand, the genera of Leptophlebiidae (Shimano et al., 2010; Firmiano et al., 2017) and Leptohyphidae (Domínguez et al., 2001; Oliveira et al., 2013) are considered sensitive to environmental impact.

The northern region of the Brazilian state of Rio Grande do Sul is intensively explored for agricultural activities, resulting in significant fragmentation of remaining forests (Rovani et al., 2020). Thus, environmental evaluation and monitoring must be carried out often and, especially, employing safe approaches (Hepp et al., 2010; Restello et al., 2020). The use of insects as bioindicators has been traditionally reported in the literature, however, the responses presented by organisms may vary according to their tolerance to environmental changes. Order Ephemeroptera has ecological peculiarities that are yet to be elucidated (Buss & Salles, 2007; Flowers, 2009), particularly regarding diffuse impacts such as agriculture. In the present study, we sought to assess the responses of Ephemeroptera assemblies in streams impacted by agricultural activities taking into account taxonomic resolution.

Our hypothesis is that some genera are more representative of sites with agricultural impact and are considered tolerant to pollution. Therefore, when a more refined taxonomic resolution is employed, the response of Ephemeroptera is different than what the literature reports for the order, i.e., it is not linear and there are sensitive genera and tolerant genera.

MATERIAL AND METHODS

Area of study. The study was carried out in <3^rd order streams located in the northern region of the Brazilian state of Rio Grande do Sul (27°12’59” and 28°00’47”S; 52°48’12” and 51°49’34”W; Fig. 1). The region has humid temperate subtropical climate that belongs to types Cfa and Cfb according to the Köpen-Geiger classification (Alvares et al., 2013). Rainfall is regular and well distributed along the year, with mean annual precipitation of 1500 mm (Alvares et al., 2013). The region is located within the Atlantic Forest biome with vegetation characterized by a mix of perennifolia stationary forest with araucaria and seasonal semideciduous forest (Oliveira-Filho et al., 2015).

Six streams whose land use and cover classes have been quantified by geoprocessing techniques were selected. The quantification of ‘arboreal vegetation’ and ‘agricultural use’ was carried out in a 30 m buffer in both banks of the streams, considered the riparian zone, and in the drainage area of each stream studied, following the topographic patterns of the area. After quantification, the streams were classified into natural (R1, R2, and R3) and agricultural (R4, R5, and R6) (Fig. 1; Tab. I) according to the criteria proposed by Huñocana et al. (2020).

The water in the streams of both classifications were well oxygenated (>10 mg L^-1) and pH values were near neutral (~7). Turbidity varied from 2.03 to 9.06 NTUs and electric conductivity was between 0.11 to 0.62 mS cm^-1 in the agricultural and natural streams, respectively.

Tab. I.
Percentage of vegetation and agriculture in the drainage area and riparian zone of the streams studied, Upper Uruguay Region (Veg, vegetation; Agr, agriculture; DA, drainage area; RZ, riparian zone).

	% vegetation		% agriculture
Streams	VegDA	VegRZ	AgrDA	AgrRZ
Natural
R1	47.2	72.8	33.9	26.1
R2	43.7	76.3	24.3	9.20
R3	42.2	73.0	4.08	3.98
Agricultural
R4	5.90	7.10	87.4	83.2
R5	8.60	14.8	88.0	82.0
R6	15.6	27.2	72.6	60.3

Fig. 1.
Geographic location of the study area, northern region of the Brazilian state of Rio Grande do Sul, Brazil.

Collection and identification of Ephemeroptera. The organisms were collected in the spring of 2019 and summer of 2020 using a Surber sampler (250 µm mesh and 0.09 m² area). Three subsamples were collected from each stream, all in rocky substrate to prevent possible effects of the types of substrates in the sampling. The material was fixated in situ with 70% ethanol and stored in plastic flasks. At the laboratory, Ephemeroptera were identified down to the genus taxonomic level using the keys proposed by Salles et al. (2004) and Mugnai et al. (2010). The organisms identified were recorded and deposited at the Benthonic Invertebrate Collection of the Regional Museum of Upper Uruguay (Museu Regional do Alto Uruguai - MuRAU) of the Universidade Regional Integrada do Alto Uruguai e das Missões (URI).

Data analysis. The structure of the Ephemeroptera assembly was determined based on abundance, given by the total number of organisms collected, and richness, estimated by the number of genera identified. Data normality was verified using Shapiro-Wilk test. For each family, we carried out t tests aiming at verifying the variation between abundance and richness in the natural and agricultural streams. Richness could not be assessed for the Caenidae and Leptophlebiidae families as they exhibited only a single genus. Pearson linear correlation analysis was performed to verify whether the percentages of vegetation and agriculture in the drainage area or riparian zone are related to (i) the families in the Ephemeroptera assembly and (ii) each of the genera identified.

The statistical analyses were performed using the statistical software R (R Core Team, 2022) via the ‘vegan’ (Oksanen et al., 2022) and ‘ggplot2’ (Wickham et al., 2022) data packages.

RESULTS

We collected a total of 2,767 organisms, belonging to four families and 11 genera of the Ephemeroptera order (Tab. II). In the natural streams, we collected a total of 878 specimens (32% of the total), belonging to four families and eight genera. In the agricultural streams, we collected 1,889 specimens (68% of the total), belonging to four families and 11 genera (Tab. II). The most representative family in the natural streams was Leptophlebiidae at 517 specimens (59% of the fauna at those sites), while Baetidae was the most representative in agricultural streams, with 702 specimens collected (37% of the fauna samples in those streams). The genera Americabaetis, Apobaetis, and Traverhyphes were exclusive of agricultural streams (Tab. II).

The abundance of the Baetidae (t = -3.4; p = 0.03) and Leptohyphidae (t = -4.2; p = 0.03) families was greater in the agricultural streams (Figs 2A and 2B, respectively). On the other hand, the abundance of the Caenidae and Leptophlebiidae did not differ among streams. We observed greater richness of Baetidae (t = - 5.0; p = 0.01) and Leptohyphidae (t = -4.2; p = 0.03) in the agricultural streams (Figs 2C and 2D, respectively). Hagenulopsis and Baetodes were the most abundant genera in the natural streams, whereas Paracleodes, Caenis, and Tricorythopsis were the most abundant in the agricultural streams.

Fig. 2.
Boxplot for abundance and richness of families of the Ephemeroptera order between the natural and agricultural streams: A, abundance of Baetidae; B, abundance and Leptohyphidae; C, richness of Baetidae; and D, richness of Leptohyphidae.

Tab. II.
Ephemeroptera genera identified in natural and agricultural streams, northern Rio Grande do Sul state, Brazil.

Family/Genera	Streams
	Natural	Agricultural
Baetidae
Americabaetis Kluge, 1992	0	23
Apobaetis Day, 1955	0	9
Baetodes Needham & Murphy, 1924	200	196
Cloeodes Traver, 1938	10	190
Paracleodes Day, 1955	34	231
upiara Salles, Lugo-Ortiz,Da-Silva & Francischetti, 2003	4	53
Caenidae
Caenis Stephens, 1835	43	330
Leptophlebiidae
Hagenulopsis Ulmer, 1920	517	465
Leptohyphidae
Tricorythopsis Traver, 1958	2	305
Tricorythodes Ulmer, 1920	68	83
Traverhyphes Molineri, 2001	0	4
Abundance	878	1889
Richness of genera	8	11

Baetidae exhibited a negative correlation with vegetation in the DA and RZ (Figs 3A and 3B) and a positive correlation with agriculture in the DA and RZ (Figs 3C and 3D). For Leptohyphidae, we observed a negative correlation with vegetation in the DA and RZ (Figs 3E, 3F) and a positive correlation with agriculture in the DA and RZ (Figs 3G, 3H). We did not observe correlations between land use and cover with Caenidae abundance (p > 0.05).

Given the relationships between land uses and cover and the genera identified, we observed that only Cleodes and Tricorythopsis exhibited significant correlations (Tab. III).

Fig. 3.
Pearson linear correlation among Baetidae richness: A, percentage of vegetation in the DA; B, vegetation in the RZ; C, percentage of agriculture in the DA; and D, agriculture in the RZ, and Leptohyphidae richness: E, percentage of vegetation in the DA; F, vegetation in the RZ; G, percentage of agriculture in the DA; and H, agriculture in the RZ (DA, drainage area; RZ, riparian zone).

Tab. III.
Pearson correlation values between Ephemeroptera genera and the percentage of vegetation and agriculture in the DA and RZ. *significant correlations (p < 0.05) (DA, drainage area; RZ, riparian zone).

Taxa	% Veg DA	% Veg RZ	% Agr DA	% Agr RZ
Baetidae
Americabaetis	- 0.64	- 0.67	0.58	0.63
Apobaetis	- 0.63	- 0.65	0.57	0.60
Baetodes	- 0.50	- 0.46	0.30	0.32
Cloeodes	- 0.82*	- 0.84*	0.76	0.82*
Paracleodes	- 0.58	- 0.56	0.49	0.47
Tupiara	- 0.70	0.70	0.65	0.63
Caenidae
Caenis	- 0.48	- 0.47	0.51	0.53
Leptophlebiidae
Hagenulopsis	-0.14	-0.24	-0.43	-0.40
Leptohyphidae
Tricorythopsis	-0.89*	-0.88*	0.88*	0.86*
Tricorythodes	-0.018	-0.05	0.09	0.07
Traverhyphes	-0.54	-0.57	0.49	0.53

DISCUSSION

We observed greater abundance and richness of genera in the streams with more intense agricultural uses. The richness of the Baetidae and Leptohyphidae genera was also higher in the agricultural streams, which does not corroborate studies that point to higher richness of Ephemeroptera genera in more preserved streams (Alves et al., 2006; Arimoro & Muller, 2010; Siegloch et al., 2014).

Buss et al. (2002) stated that Baetidae organisms are little sensitive to environmental changes and are easily found at sites with intermediate levels of degradation. On the other hand, Domínguez et al. (2006) and Buss & Salles (2007) reported that Baetidae species are demanding of sites with higher environmental integrity. Therefore, the lack of consensus among records in the literature is evident. The dietary habit of Baetidae must be taken into account in the analysis since they are scraping organisms. In that sense, streams surrounded by agriculture exhibit low levels of plant cover in their banks, which leads to greater sunlight incidence onto the stream and facilitates the establishment of periphyton (Huñocana et al., 2020), thus increasing the abundance of Baetidae.

Likewise, our results do not corroborate studies that report sensitivity by Leptohyphidae to disturbances (Peres, 1988; Callisto et al., 2002; Chagas et al., 2017). Thus, we can propose that Baetidae and Leptohyphidae adapted to the altered stretches of streams, possibly explained by the hypothesis of intermediate disturbance of anthropic origin. Some studies state that intermediate disturbances may explain the higher richness of Ephemeroptera nymphs in areas with anthropic impact (Siegloch et al., 2008; Souza et al., 2011).

Our results showed that Tricorythopsis (Leptohyphidae), Cloeodes (Baetidae), and Caenis (Caenidae) were more abundant in the agricultural streams. Such results contradict those presented by Firmiano et al. (2017), who report that Tricorythopsis is sensitive to perturbation. Impacted environments may exhibit lower habitat availability, with less input of allochthonous material into the system and predominance of fine particulate organic matter, which favors the prevalence of collecting organisms, thus justifying the presence of Tricorythopsis in the agricultural streams. The presence of opercular gills facilitate the tolerance against suspended solids and, in very turbid streams and rivers, that family becomes an important component of the benthonic community (Domínguez et al., 2006). Such result shows that we must be careful when generalizing the tolerance of families of the order Ephemeroptera since some genera may be tolerant to changes in adjacent areas.

The presence of Cloeodes in the agricultural streams also differ from the results presented by several studies that state the genus is sensitive to pollution (Buss & Salles, 2007; Chacón & Segnini, 2007; Forero-Céspedes & Reinoso-Flórez, 2013). Cloeodes was recorded in association with algae biofilm (periphyton) or rocky substrates (Souza et al., 2011), while Domínguez et al. (2006) observed that nymphs are found in a broad range of habitats, both in well-oxygenated streams and in poorly oxygenated sites. The higher presence of Cloeodes in agricultural streams shows that the genus tolerates agricultural use both in the riparian zone and in the drainage area of the basin assessed.

In the natural streams, Hagenulopsis (Leptoplhebiidae) was the most abundant. Habitat heterogeneity is one of the main factors of distribution of that family (Goulart & Callisto, 2005). The structure of a community of aquatic insects may be influenced by the existing resources, substrate variety, and environmental heterogeneity, thus justifying the abundance of that family in the natural streams (Abelho, 2001; Boyero, 2003; Taniguchi & Tokeshi, 2004; Burdett & Watts, 2009). To Flowers & de la Rosa (2010), the family Leptoplhbiidae is widely tolerant to temperature and certain levels of pollution. However, Hagenulopsis tolerates different environmental conditions and may be found in waters with better conditions (Flowers & de la Rosa, 2010).

Americabaetis (Baetidae) nymphs were exclusively found in agricultural streams and are considered less sensitive to environmental impacts (Callisto et al., 2001; Buss & Salles, 2007; Souza et al., 2011). Americabaetis occur in several types of habitats, including sites with some level of perturbation (Siegloch et al., 2008), which may explain in this case the exclusivity in agricultural streams.

Caenis was another abundant genus in the agricultural streams. Those are sturdy and little demanding organisms that may tolerate a broad range of environmental conditions and may live in polluted and eutrophic waters, where many other members of the Ephemeroptera order are unable to survive, which justifies the abundance of that group in the agricultural streams (Flowers & de la Rosa, 2010; Oliveira et al., 2017).

Many works with aquatic insects as bioindicators analyze the fauna of Ephemeroptera, Trichoptera, and Plecoptera jointly, with Ephemeroptera responding as sensitive organisms to anthropic impact (Junqueira et al., 2010; Chang et al., 2014; Valente-Neto et al., 2018; Huiñocana et al., 2020). However, there are gaps regarding the patterns of different genera. We observed such fact in this study when analyzing Ephemeroptera genera, finding that some are tolerant to agricultural impact as they were more abundant in that type of stream.

Our results suggest the genera of the Ephemeroptera order are sensitive to agricultural impact. The so-called agricultural streams had greater abundance and richness of organisms. Caenis, Cloeodes, and Tricorythopsis were the most abundant in the agricultural streams, contradicting some studies as previously mentioned. Works only at the order level may not be sufficient to indicate the sensitivity of the group to agricultural impact. We observed that, in order to determine the agricultural impact on Ephemeroptera, the organisms must be identified down to the taxonomic level of genus, corroborating our hypothesis.

Acknowledgements

RMR thanks the financial support of the Research Fostering Foundation of the State of Rio Grande do Sul (Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul - FAPERGS - 19/2551-0002062-7) and the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq, Brazil) under process #409685/2016-0. LAE is grateful for the graduate studies scholarship (CAPES/Modality II) linked to the Ecology Graduate Program at URI Erechim. LUH is a recipient of a productivity scholarship from the CNPq, process #310394/2023-6. SVM is a recipient of a Junior Post-Doctorate scholarship from the CNPq, process #150477/2021-0, Post-Doctorate Program at UFMS and Foundation to Support the Development of Education, Science and Technology of Mato Grosso do Sul (Fundação de Apoio ao Desenvolvimento de Ensino, Ciência e Tecnologia do Mato Grosso do Sul) (process # 83/050.593/2023).

REFERENCES

• Abelho, M. 2001. From litterfall to breakdown in streams: a review. The Scientific World 1:656-680.
• Allan, J. D. 2004. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annual Review of Ecology, Evolution, and Systematics 35:257-284.
• Alvares, C. A.; Stape, L. L.; Sentelhas, P. C.; Gonçalves, J. D. M. & Sparovek, G. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22:711-728.
• Alves, M. V.; Baretta, D. & Cardoso, E. J. B. N. 2006. Fauna edáfica em diferentes sistemas de cultivo no estado de São Paulo. Revista de Ciências Agroveterinárias 5:33-43.
• Arimoro, F. O. & Muller, W. J. 2010. Mayfly (Insecta: Ephemeroptera) community structure as an indicator of the ecological status of a stream in the Niger Delta area of Nigeria. Environmental Monitoring Assessment 166:581-594.
• Boyero, L. 2003. Padrões multiescala de variação espacial de comunidades de macroinvertebrados de fluxo. Ecological Research 18:365-379.
• Brasil, L. S.; Juen, L.; Batista, J. D.; Pavani, M. G. & Cabette, H. S. R. 2014. Longitudinal Distribution of the Functional Feeding Groups of Aquatic Insects in Streams of the Brazilian Cerrado Savanna. Neotropical Entomology 43:421-428.
• Bueno, L. F.; Galbiatti, J. A. & Borges, M. J. 2005. Monitoramento de Variáveis de Qualidade da Água do Horto Ouro Verde - Conchal - SP. Engenharia Agrícola 25(3):742-748.
• Burdett, A. S. & Watts, R. J. 2009. Modifying living space: an experimental study of the influences of vegetation on aquatic invertebrate community structure. Hydrobiologia 618(1):161-173.
• Burdon, F. J.; Ramberg, E.; Sargac, J.; Forio, M. A. E.; Saeyer, N. de; Multinova, P. T.; Moe, T. F.; Pavelescu, M. O.; Dinu, V.; Cazacu, C.; Witing, F.; Kupilas, B.; Grandin, U.; Volk, M.; Rîsnoveanu, G.; Gethals, P.; Friberg, N.; Johnson, R. K. & McKie, B. G. 2020. Assessing the benefits of forested riparian zones: a qualitative index of riparian integrity is positively associated with ecological status in European streams. Water 12(4).
• Buss, D. F.; Baptista, D. F.; Nessimian, J. L.; Dorvillé, L. F. & Silveira, M. P. 2002. Influence of water chemistry and environmental degradation on macroinvertebrate assemblage in a river basin in South-East Brazil. Hydrobiologia 481(1-3):125-136.
• Buss, D. F. & Salles, F. F. 2007. Using Baetidae as biological indicators of environmental degradation in a Brazilian river basin. Environmental Monitoring and Assessment 130:365-372.
• Callisto, M.; Moreno, P. & Barbosa, F. 2001. Habitat diversity and benthic functional trophic groups at Serra do Cipó, Southeast Brazil. Brazilian Journal of Biology 61(2):259-266.
• Callisto, M.; Moreno, P.; Gonçalves, J. F. Jr.; Leal, J. J. F. & Esteves, F. A. 2002. Diversity and biomass of Chironomidae (Diptera) larvae in an impacted coastal lagoon in Rio de Janeiro, Brazil. Brazilian Journal of Biology 62(1):77-84.
• Carvalho, A. R.; Schlittler, F. H. M. & Tornisielo, V. L. 2000. Relações da atividade agropecuária com parâmetros físicos químicos da água. Química Nova 23(5):618-622.
• Chacón, M. M. & Segnini, S. 2007. Óptimos y tolerancias ambientales para las ninfas de Ephemeroptera en un gradiente atititudinal en la cordillera de Mérida, Venezuela. Entomología Mexicana 6:225-230.
• Chagas, F. B.; Rutkoski, C. F.; Bieniek, G. B.; Vargas, G. D. L. P.; Hartmann, P. A. & Hartmann, M. T. 2017. Utilização da estrutura de comunidades de macroinvertebrados bentônicos como indicador de qualidade da água em rios no sul do Brasil. Ambiente e Água 12(3):416-426.
• Chang, F. H.; Lawrence, J. E.; Rios-Touma, B. & Resh, V. H. 2014. Tolerance values of benthic macroinvertebrates for stream biomonitoring: assessment of assumptions underlying scoring systems worldwide. Environmental monitoring and assessment 186(4):2135-2149.
• Deegan, L. A.; Neill, C.; Haupert, C. L.; Ballester, M. V. R.; Krusche, A. V.; Victoria, R. L.; Thomas, S. M. & Momoor, de E. 2011. Amazon deforestation alters small stream structure, nitrogen biogeochemistry and connectivity to larger rivers. Biogeochemistry 105(1-3):53-74.
• Domínguez, E.; Hubbard, M. D.; Pescador, M. L. & Molineri, C. 2001. Capítulo 1: Ephemeroptera. In: Fernández, H. & Domínguez, E. eds. Guía para la determinación de los artrópodos bentónicos sudamericanos. San Miguel de Tucumán, Universidad Nacional de Tucumán.
• Domínguez, E.; Molineri, C.; Pescador, M. L.; Hubbard, M. & Nieto, C. 2006. Ephemeroptera of South America. Moscow, Pensoft. 646p.
• Duschek, V. G.; Springer, M.; Niedrist, G. H. & Füreder, L. 2019. Macroinvertebrates as indicators in tropical streams with different land use in southern Costa Rica. Acta ZooBot Austria 156:99-113.
• Firmiano, K. R.; Ligeiro, R.; Macedo, D. R.; Juen, L.; Hughes, R. M. & Callisto, M. 2017. Mayfly bioindicator thresholds for several anthropogenic disturbances in neotropical savanna streams. Ecological Indicators 74:276-284.
• Forero-Céspedes, A. M. & Reinoso-Flórez, G. 2013. Estudio de la familia Baetidae (Ephemeroptera: Insecta) en una cuenca con influência de la urbanización y agricultura: río Alvarado - Tolima. Revista de La Asociación Colombiana de Ciencias Biológicas 25:12-21.
• Flowers, R. W. & de la Rosa, C. 2010. Ephemeroptera (Capítulo 4). Revista de Biologia Tropical 58:63-93.
• Goulart, M. & Callisto, M. 2005. Mayfly diversity in the Brazilian tropical headwaters of Serra do Cipó. Brazilian Archives of Biology and Technology 4:983-996.
• Hepp, L. U.; Milesi, S. V.; Biasi, C. & Restello, R. M. 2010. Effects agricultural and urban impacts on macroinvertebrates assemblages in streams (Rio Grande do Sul, Brazil). Revista Brasileira de Zoologia 27:106-113.
• Hepp, L. U.; Milesi, S. V.; Biasi, C.; Restello, R. M. & Molozzi, J. 2013. Distribution of aquatic insects in urban headwater streams. Acta Limnologica Brasiliensia 25:1-10.
• Huiñocana, J. C. S.; Albertoni, E.; Picolotto, R. C.; Milesi, S. V. & Hepp, L. U. 2020. Nestedness of insect assemblages in agriculture-impacted Atlantic forest streams. Annales de Limnologie - International Journal of Limnology 56:1-9.
• Junqueira, M. V.; Friedrich, G. & Pereira de Araujo, P. R. 2010. A saprobic index for biological assessment of river water quality in Brazil (Minas Gerais and Rio de Janeiro states). Environmental monitoring and assessment 163(1):545-554.
• Kumari, P. & Maiti, S. K. 2020. Bioassessment in the aquatic ecosystems of highly urbanized agglomeration in India: An application of physicochemical and macroinvertebrate-based indices. Ecological Indicators 111:106053.
• Mugnai, R.; Nessimian, J. L. & Baptista, D. L. 2010. Manual de identificação de macroinvertebrados aquáticos do Estado do Rio de Janeiro. Rio de Janeiro, Technical Books. 173p.
• Oksanen, J.; Blanchet, F. G.; Friendly, M.; Kindt, R.; Legendre, P.; McGlinn, D. & Stevens, M. H. H. 2022. Vegan: Community Ecology Package. i: R package version 2.6- 2.
• Oliveira, A. V. S.; Araujo, C. C.; Pereira, T. P. B.; Ferreira, A. N.; Viana- Júnior, A. B. & Dantas, J. O. 2013. Diversidade de Insetos Aquáticos e sua Relação com a Qualidade da Água no Rio Poxim Açu, São Cristóvão, SE. Cadernos de Agroecologia 8(2):1-5.
• Oliveira- Filho, A. T.; Budke, J. C.; Jarenkow, J. A.; Eisenlohr, P. V. & Neves, D. R. M. 2015. Delving into the variations in tree species composition and richness across South American subtropical Atlantic and Pampean forests. Journal of Plant Ecology 8:242-260.
• Oliveira, M. B.; Lazari, P. L.; Hepp, L. U. & Restello, R. M. 2017. Distribuição de Ephemeroptera, Plecoptera e Trichoptera em riachos do Alto Uruguai gaúcho. Distribuição de Ephemeroptera, Plecoptera e Trichoptera em riachos do Alto Uruguai gaúcho. Perspectiva 41(153):135-146.
• Palharini, W. S. & Pagotto, J. P. A. 2015. A importância da vegetação ripária para ambientes aquáticos continentais. SaBios: Revista de Saúde e Biologia 10(2):66-74.
• Peres, G. R. 1988. Guia para el studio de los amcroinvertebrados acuáticos del Departamento de Antioquia. Fondo para la Protección del Medio Ambiente “José Celestino Mutis”, Bogotá. 217p.
• R Core Team. 2022. R: A language and environment for statistical computing [online]. Vienna: R Foundation for Statistical Computing [viewed 14 Apr. 2022]. Available at <https://www.R-project.org/>.
  » https://www.R-project.org/
• Restello, R. M.; Batistoni, D.; Sobczak, J. R. S.; Valduga, A. T.; Zakrzevski, S. B.; Zanin, E. M.; Decian, V. S. & Hepp, L. U. 2020. Effectiveness of protected areas for the conservation of aquatic invertebrates: a study-case in southern Brazil. Acta Limnologica Brasiliensia 32:e5.
• Restello, R. M. , & Hepp L. U. 2020. Monitoramento biológico de riachos com uso de invertebrados aquáticos. In: Hepp, L. U. & Restello, R. M. org. Ecologia de riachos no Alto Uruguai Gaúcho. Erechim, EdiFapes, p. 33-51.
• Rojas-Peña, J. I.; Vásquez-Ramos, J. M.; Salinas-Jiménez, L. G.; Osorio-Ramirez, D. P. & Caro-Caro, C. I. 2021. Effects of physical and chemical factors on Ephemeroptera (Insecta) assemblages in an urban river of the eastern Colombian Llanos. Papeis Avulsos Zoologia 61:e20216107.
• Rovani, I. L.; Decian, V. S.; Zanin, E. M.; Brandalise, M.; Quadros, F. R. & Hepp, L. U. 2020. Socioeconomic changes and land use and land cover of the Northern Region of Rio Grande do Sul, Brazil. Floresta e Ambiente 27(3):e20180258.
• Salles, F. F.; da-Silva, E. R.; Serrão, J. E.; Hubbard, M. D. & Francischetti, C. N. 2004. As espécies de Ephemeroptera (Insecta) registradas para o Brasil. Biota Neotropica 4(2):1-4.
• Selvakumar, C.; Sivaramakrishnan, K. G.; Janarthanan, S.; Arumugam, M. & Arunachalam, M. 2014. Impact of riparian land-use patterns on Ephemeroptera community structure in river basins of the southern Western Ghats, India. Knowledge and Management of Aquatic Ecosystems 412:11.
• Serna-López, J. P.; Mc Cann, F. D. S.; Macías, F. D. J. V. & Ramírez, N. J. A. 2020. An image processing method for recognition of four aquatic macroinvertebrates genera in freshwater environments in the Andean region of Colombia. Environmental Monitoring and Assessment 192(10):1-11.
• Shimano, Y.; Cabette, H. S. R.; Salles, F. F. & Juen, L. 2010. Composição e distribuição da fauna de Ephemeroptera (Insecta) em área de transição Cerrado-Amazônia, Brasil. Iheringia, Série Zoologia 100(4):301-308.
• Siegloch, A. E.; Froehlich, C. G. & Kotzian, C. B. 2008. Composition and diversity of Ephemeroptera (Insecta) nymph communities in the middle section of the Jacuí River and some tributaries, southern Brazil. Iheringia, Série Zoologia 98(4):425-432.
• Siegloch, A. E.; Suriano, M.; Spies, M. & Fonseca-Gessner, A. 2014. Effect of land use on mayfly assemblages structure in Neotropical headwater streams. Anais da Academia Brasileira de Ciências 86(4):1735-1747.
• Siegloch, A. E.; Schmitt, A. C. R.; Spies, M. B.; Petrucio, M. A. & Hernández, A. M. I. M. 2016. Effects of small changes in riparian forest complexity on aquatic insect bioindicators in Brazilian subtropical streams. Marine and Freshwater Research 68(3):519-527.
• Silveira, M. P. 2004. Aplicação do biomonitoramento para avaliação da qualidade da água em rios. Embrapa Meio Ambiente-Documentos (INFOTECA-E).
• Souza, H. L.; Cabette, H. S. R. & Juen, L. 2011. Baetidae (Insecta, Ephemeroptera) em córregos do cerrado matogrossense sob diferentes níveis de preservação ambiental. Iheringia, Série Zoologia 101(3):181-190.
• Taniguchi, H. & Tokeshi, M. 2004. Effects of habitat complexity on benthic assemblages in a variable environment. Freswater Biology 49(9):1164-1178.
• Tonello, G.; Decian, V. S.; Restello, R. M. & Hepp, L. U. 2021. The conversion of natural riparian forests into agricultural land affects ecological processes in Atlantic forest streams. Limnologica 91:125927.
• Valente- , Neto F.; Rodrigues, M. E. & de Oliveira Roque, F. 2018. Selecting indicators based on biodiversity surrogacy and environmental response in a riverine network: Bringing operationality to biomonitoring. Ecological indicators 94:198-206.
• Xiaojing, N. I.; Parajuli, P. B.; Ouyang, Y.; Dash, P. & Siegert, C. 2021. Assessing land use change impact on stream discharge and stream water quality in an agricultural watershed. Catena 198:105055.
• Wickham, H.; Chang, W.; Henry, L.; Pedersen, T. L.; Takahashi, K.; Wilke, C.; Woo, K.; Yutani, H. & Dunnington, D. 2022. ggplot2: Create elegant data visualisations using the grammar of graphics. In: R package version 3.3. 6.

Edited by

Associate Editor:

Pedro Giovâni da Silva

Publication Dates

• Publication in this collection
  24 June 2024
• Date of issue
  2024

History

• Received
  21 Feb 2024
• Accepted
  24 Apr 2024