Aquatic Oligochaeta (Annelida: Clitellata) in wetlands and irrigated rice fields in the state of Rio Grande do Sul (Southern Brazil)

Oligochaeta aquáticos (Annelida: Clitellata) em áreas úmidas e arrozais irrigados no estado do Rio Grande do Sul (Sul do Brasil)

ABSTRACT

The knowledge of the diversity and distribution of aquatic Oligochaeta (Annelida: Clitellata) species is scarce in southern Brazil. This study presents a list of the species of aquatic Oligochaeta in wetlands and irrigated rice fields in the state of Rio Grande do Sul. Collections were carried out in two large wetland remnants and seven irrigated rice fields distributed in three regions across the state. We recorded eight species from two families (Alluroididae and Naididae). We expanded the distribution ranges of two species (Brinkhurstia americana and Stylaria lacustris), which represent new records for the state of Rio Grande do Sul and registered their occurrence in non-documented environments. In specific, the present study increases to 24 species the aquatic Oligochaeta diversity for the state of Rio Grande do Sul. In addition, the spatial distribution of the species recorded suggests that rice fields support a subset of the wetland fauna of aquatic Oligochaeta. The results provide important information on the ecology and distribution of limnic Oligochaeta and are useful to inform on the diversity of this fauna in agroecosystems.

KEYWORDS
Agroecosystems; freshwater biodiversity; oligochaetes; paddies; wetlands

RESUMO

Oligochaeta aquáticos (Annelida: Clitellata) em áreas úmidas e arrozais irrigados no estado do Rio Grande do Sul (Sul do Brasil). O conhecimento sobre a diversidade e distribuição das espécies aquáticas de Oligochaeta (Annelida: Clitellata) é escasso no sul do Brasil. Este estudo apresenta uma lista das espécies de Oligochaeta aquáticas em áreas úmidas e arrozais irrigados no estado do Rio Grande do Sul. As coletas foram realizadas em dois grandes remanescentes de banhados e sete arrozais irrigados distribuídos em três regiões do estado. Nós registramos oito espécies de duas famílias (Alluroididae e Naididae). Nós expandimos as áreas de distribuição de duas espécies (Brinkhurstia americana e Stylaria lacustris), que representam novos registros para o estado do Rio Grande do Sul e documentamos sua ocorrência em diferentes ambientes. Especificamente, o presente estudo aumenta para 24 a diversidade de espécies de Oligochaeta aquáticas para o estado do Rio Grande do Sul. Além disso, a distribuição espacial das espécies registradas sugere que os arrozais sustentam um subconjunto da fauna de Oligochaeta aquática. Os resultados fornecem informações importantes sobre a ecologia e distribuição de Oligochaeta límnicos e são úteis para informar sobre a diversidade desta fauna em agroecossistemas.

PALAVRAS-CHAVE
Agroecossistemas; biodiversidade aquática; lavouras de arroz; oligoquetos; banhados

Agricultural expansion promoted the conversion and degradation of freshwater ecosystems and represents a special threat to aquatic biodiversity (Dudgeon, 2019). For instance, conversion to irrigated rice fields is one the major drivers of the loss of the world’s wetland ecosystems, which is estimated to have reached approximately 70% of their original extent in the twentieth century (Davidson, 2014). However, the diversity of many wetland-dependent organisms remains undocumented in many regions of the world. Taking into account that wetlands are biodiversity hotspots and that they provide a range of ecosystem services (Davidson et al., 2019), the lack of knowledge on wetland species diversity hampers the adoption of adequate biodiversity conservation policies in these ecosystems. Nevertheless, given that agricultural land use has increasingly replaced natural ecosystems worldwide (Winkler et al., 2021), one of the main targets of Conservation Biology is therefore the study of biodiversity in agroecosystems (Altieri, 1999). On this matter, rice fields have received great attention, since earlier studies found that they can harbor an expressive fraction of the biodiversity of wetland species, leading some authors to consider them alternative sites for the wetland biota (Lawler, 2001; Bambaradeniya et al., 2004). This is because irrigated rice fields can emulate many of the environmental conditions of a typical wetland, such as low water depth, temporary hydroperiod, presence of vegetation, etc. (Lawler, 2001).

Macroinvertebrates are fundamental to many ecological processes in freshwater ecosystems and are important components of the fauna of irrigated rice fields (Roger, 1996; Bambaradeniya et al., 2004). In southern Brazil (state of Rio Grande do Sul), the largest rice-producing region in the country, rice is an annual culture taking place between early spring (sowing) and late summer (harvest); almost the entirety of the rice production in Rio Grande do Sul is under the irrigated system (Ana & Conab, 2020). Some authors found that irrigated rice fields support a wide range of macroinvertebrate taxa (Maltchik et al., 2010, 2011, 2017; Stenert et al., 2012; Sousa et al., 2021). However, authors that simultaneously compared macroinvertebrate communities in paddies and wetlands showed that certain aspects of their structures diverge (Pires et al., 2016). In this context, species inventories are of great importance to support the formulation of management plans because they provide information on the diversity and distribution of various taxa (Christoffersen, 2010; Souza et al., 2021). In particular, inventory data from natural ecosystems act as a reference for decision making on biodiversity management and conservation policies in sites under anthropogenic impact such as agroecosystems. This is especially important taking into account that approximately 90% of the original wetlands in southern Brazil were lost, mostly due to drainage for rice plantations (Stenert & Maltchik, 2007).

Aquatic Oligochaeta are one of the main components of the macroinvertebrate fauna in wetlands (Batzer & Boix, 2016). Oligochaeta are important consumers (e.g., algal feeders), and thus play an important role in nutrient cycling and energy flow in these ecosystems; in addition, some aquatic Oligochaeta species are indicators of polluted waters and can be important tools for ecosystem health assessment (Govedich et al., 2010). Christoffersen (2007) compiled a list of 171 nominal species of aquatic Oligochaeta (except Enchytraeidae) for South America, 86 species of which occur in Brazil. However, most available inventories of Oligochaeta in Brazil focus land-dwelling species. In light of the Brazilian territory, the aquatic oligochaete fauna catalogued so far, i.e., the states of São Paulo, Minas Gerais and Mato Grosso do Sul (Rodrigues et al., 2013; Takeda et al., 2017; Girolli et al., 2021) reflects a small fraction of the diversity in the country. Therefore, more inventories are necessary to improve the knowledge of this fauna in the country (Christoffersen, 2010; Rodrigues & Alves, 2018).

Four species of aquatic Oligochaeta had been originally recorded in the state of Rio Grande do Sul (Christoffersen, 2007). Subsequent studies reported 16 species of Oligochaeta in irrigated rice fields (Maltchik et al., 2011; Stenert et al., 2012), and four species in large wetland remnants in the state (Pires et al., 2016). However, the available data for rice fields stem from small-range studies, while the knowledge of the diversity of Oligochaeta species in the largest rice-growing areas of Rio Grande do Sul remains unknown. This study presents a list of the species of aquatic Oligochaeta occurring in wetlands and irrigated rice fields in three rice-growing areas in the state of Rio Grande do Sul (southern Brazil). We aimed at updating the knowledge about the distribution of this group in the state and also at providing considerations on the diversity in such agroecosystems.

MATERIAL AND METHODS

Study area. Collections took place in three study regions covering important rice-growing areas and large wetland remnants across the state of Rio Grande do Sul (Fig. 1). In the western region of Rio Grande do Sul, the study region covered the São Donato Biological Reserve (SD; area: 4,300 ha), which consists the largest extant wetland in the region (Carvalho & Ozório, 2007). This region covers the largest rice-growing areas of Rio Grande do Sul, with over 100,000 ha of crop area and production of ~1 mi tons/year (IRGA, 2012). In the central region of Rio Grande do Sul, the study region covered a large wetland represented by a river confluence zone (Foz do Vacacaí wetlands (FV); area of ~4,600 ha; Carvalho & Ozório, 2007). The crop areas in the region cover ~35,000 ha, with production of ~250,000 tons/year (IRGA, 2012). In the southwestern region of Rio Grande do Sul (SG region), the crop areas cover ~30,000 ha, with production of ~220,000 tons/year (IRGA, 2012). Across the study regions, the climate is Cfa of Köppen (humid subtropical with hot summer), with mean annual temperature of ~18 °C and annual rainfall ranging from 1,600 and 2,200 mm (Alvares et al., 2013).

Fig. 1.
Location of the study regions and study sites in Rio Grande do Sul state, Brazil. Abbreviations of the study regions: FV = ‘Foz do Vacacaí’ study region; SD = ‘São Donato’ study region; SG = ‘southwestern’ study region. Numbers indicate the study sites and follow Table I.

Site characterization and sampling period. Collections were carried out in nine study sites: one wetland and two rice fields were sampled in the FV study region; three rice fields in the SG study region; one wetland and two rice fields in the SD study region (Fig. 1; Tab. I). Rice fields had a water depth of ~10 cm, variable cultivation systems and irrigation sources. Wetlands were characterized by macrophyte stands dominated by different families. For environmental characterization purposes, we took measurements of the following water physicochemical variables: dissolved oxygen (DO), electrical conductivity (EC), water turbidity (NTU) and pH (Tab. I). Physicochemical data were taken with a multiparameter probe (HORIBA^® U-50). Collections took place in the summer of 2012 (January; austral season), during the vegetative growth phase of the rice cultivation cycle.

Tab. I.
Location and environmental description of the study sites [DO, dissolved oxygen (mg/L); EC, electrical conductivity (µS/cm); NTU, water turbidity; IS, irrigation source; CS, cultivation system)]. Site code numbers follow the codes in Fig. 1.

Region	Site code	Environment	Longitude	Latitude	pH	EC	DO	NTU	IS	CS
SD	1	Wetland	53°05’56”	29°56’22”	6.11	331	0.01	8.15
SD	2	Rice field	56°19’37”	29°08’09”	7.18	55	7.90	3.10	Reservoir	Conventional
SD	3	Rice field	56°05’05”	28°52’23”	7.92	87	10.29	7.70	River	Conventional
FV	4	Wetland	56°11’0.3”	29°00’29”	6.45	124	0.01	8.67
FV	5	Rice field	54°22’13”	30°23’53”	7.23	71	6.98	6.60	Reservoir	Conventional
FV	6	Rice field	53°12’23”	29°54’08”	6.16	10	8.33	107.00	Reservoir	Pre-germinated
SG	7	Rice field	54°53’28”	30°14’25”	6.56	130	6.45	26.8	Reservoir	Conventional
SG	8	Rice field	53°07’03”	30°15’51”	5.92	175	7.90	10.7	Reservoir	Conventional
SG	9	Rice field	54°13’11”	30°11’45”	6.35	62	3.48	7.40	River	Conventional

Sampling methods and laboratory procedures. In each study region, collections occurred simultaneously in each environment. In each study site, three samples were taken with a D-net (0.3-m diameter; 0.5-mm mesh size). Each sample consisted of three 1-m sweeps that were at least 1 m from one another. In the wetlands, samples were taken in emergent macrophyte stands, while in rice fields, samples were taken in the secondary irrigation channels (i.e., rice-growing area). The collected material was preserved in situ in 70% ethanol. Specimens were identified in the laboratory to species level whenever possible, according to specialized keys (Brinkhurst & Jamieson, 1971; Righi, 1984; Brinkhurst & Marchese, 1989). Specimens were deposited in the Zoological Collection of the Biology Laboratory of the University of Araraquara (UNIARA; Araraquara, SP, Brazil), under registration number 00265.

Compilation. Finally, we compiled the occurrence records of species of aquatic Oligochaeta in Rio Grande do Sul. For this purpose, we conducted an online literature search for primary records (e.g., published inventories of Oligochaeta species, specialist homepages, etc.) and secondary records of species of Oligochaeta (e.g., online databases and public online repositories).

RESULTS

In the study sites, we recorded 70 specimens from eight species of aquatic Oligochaeta and two families (Alluroididae and Naididae) (Tab. II). Alluroididae was represented by a single species [Brinkhurstia americana (Brinkhurst, 1964)], while Naididae was the richest family, with seven species from three subfamilies (Naidinae, Pristininae and Tubificinae). Brinkhurstia americana was the most frequent species in the study area (recorded in four out of nine study sites), followed by Allonais chelata (Marcus, 1944) (two out of nine study sites); all the other species were recorded in a single study site (Tab. II).

Tab. II.
Species composition and number of individuals (N) of aquatic Oligochaeta recorded in wetlands and irrigated rice fields in the state of Rio Grande do Sul, Brazil. (-) = No specimen detected.

Region (according Fig. 1)				SD			FV			SG
Environment				Wetland	Rice field	Rice field	Wetland	Rice field	Rice field	Rice field	Rice field	Rice field
Site code				1	2	3	4	5	6	7	8	9
Order	Family	Subfamily	Species
Haplotaxida	Alluroididae		Brinkhurstia americana (Brinkhurst, 1964)	19	2	2	-	9	-	2	-	-
	Naididae	Naidinae	Allonais chelata (Marcus, 1944)	1	-	-	-	-	2	-	-	-
			Bratislavia dadayi (Michaelsen, 1905)	2	-	-	-	-	-	-	-	-
			Dero digitata (Müller, 1774)	-	-	-	2	-	-	-	-	-
			Slavina evelinae (Marcus, 1942)	4	-	-	-	-	-	-	-	-
			Stylaria lacustris (Linnaeus, 1758)	-	-	-	-	-	-	-	-	13
		Pristininae	Pristina proboscidea Beddard, 1896	-	-	-	1	-	-	-	-	-
		Tubificinae	Aulodrilus pigueti Kowalewski, 1914	-	-	-	-	-	-	-	11	-

Four species were recorded in the wetland of the SD region, and two species in the wetland of the FV region, while rice fields harbored one species each (Tab. II). Overall, four species were recorded in rice fields of the SG region, while six species were recorded in wetlands (Fig. 2). Brinkhurstia americana and A. chelata occurred in both environments; two species were exclusive of rice fields (Aulodrilus pigueti Kowalewski, 1914 and Stylaria lacustris Linnaeus, 1758), while four species were exclusive of wetlands (Bratislavia dadayi Michaelsen, 1905, Dero digitata Müller, 1774, Slavina evelinae Marcus, 1942 and Pristina proboscidea Beddard, 1896) (Fig. 3).

Figs 2, 3.
Aquatic Oligochaeta in wetlands and irrigated rice fields in the state of Rio Grande do Sul, Brazil: 2, taxonomic richness; 3, species composition.

The compilation of occurrence records showed that 24 species (from three families) of aquatic Oligochaeta occur in the state of Rio Grande do Sul, including the species recorded in this study. Furthermore, a comparison of the species composition between environments showed that 19 species occur in irrigated rice fields, while five species occur in wetlands. Five species were recorded in other freshwater ecosystems (e.g., lakes, lagoons) (Tab. III).

Tab. III.
Species of aquatic Oligochaeta recorded in freshwater ecosystems in the state of Rio Grande do Sul, Brazil. Codes for the ‘Reference source’ column: 1: Christoffersen, 2007; 2: Maltchik et al., 2011; 3: Stenert et al., 2012; 4: Pires et al., 2016; 5: GBIF, 2019. Grey-colored lines indicate the new records of Oligochaeta for the state.

		Reference source					Habitat
Family	Species	1	2	3	4	5	This study	Rice fields	Wetlands	Other
Alluroididae	Brinkhurstia americana (Brinkhurst, 1964)						X	X	X
Naididae	Allonais chelata (Marcus, 1944)		X	X	X			X
	Aulodrilus pigueti Kowalewski, 1914		X				X	X
	Aulodrilus limnobiusBretscher, 1899			X				X
	Aulophorus furcatus (Müller, 1774)		X					X
	Aulophorus vagus Leidy, 1880			X				X
	Bratislavia dadayi (Michaelsen, 1905)				X		X		X
	Branchiura sowerbyiBeddard, 1892					X
	Dero botrytis Marcus, 1943	X						X		X
	Dero digitata (Müller, 1774)		X	X	X			X	X
	Dero evelinae Marcus, 1943	X	X	X				X		X
	Dero multibranchiata Stieren, 1892			X				X
	Dero nivea Aiyer 1930		X	X				X
	Dero obtusa d'Udekem, 1855		X	X				X
	Dero sawayai Marcus, 1943		X	X				X
	Limnodrilus hoffmeisteri Claparède, 1862	X								X
	Pristina americana Černosvitov, 1937		X	X				X
	Pristina leidyi Smith, 1896		X	X				X
	Pristina proboscidea Beddard, 1869				X				X
	Slavina sawayai Marcus, 1944			X				X
	Slavina evelinae (Marcus, 1942)		X	X	X			X	X
	Amerigodrilus kleerekoperi (Marcus, 1944)	X								X
	Stylaria lacustris (Linnaeus, 1758)						X	X
Opistocystidae	Opistocysta funiculus Cordero, 1948		X	X				X

DISCUSSION

To date, little is known about the diversity and distribution of aquatic oligochaetes in South America, especially in Brazil (Rodrigues & Alves, 2018). The few regional inventories of oligochaetes in this country (e.g., states of Amazonas, Rondônia, Mato Grosso, São Paulo, Paraná and Rio Grande do Sul) mostly refer to land species (Christoffersen, 2010). Although the compilation of Christoffersen (2007) assigned 86 species of aquatic Oligochaeta to Brazil, there have been no published inventories of limnic species, for many states, including Rio Grande do Sul (southern Brazil). According to our compilation of previous studies of aquatic Oligochaeta in Rio Grande do Sul, 22 species of aquatic oligochaetes occurred across the state (Tab. III). Our results thus updated the information on the diversity and distribution of known aquatic Oligochaeta species in the state, as they increase to 24 the number of species occurring in Rio Grande do Sul. In specific, B. americana and S. lacustris represent new records for this state.

Our study indicates that Rio Grande Sul harbors approximately one fourth (27%) of the known aquatic Oligochaeta species in Brazil. In comparison with recent inventories in other states of Brazil, the diversity of Oligochaeta recorded so far in Rio Grande do Sul is lower than other states in subtropical regions of the country. In specific, 77 species are recorded for the state of São Paulo (Gorni et al., 2015; Girolli et al., 2019; 2021), and 41 species for the state of Mato Grosso do Sul (Takeda et al., 2017). In contrast, the observed diversity of Oligochaeta in Rio Grande do Sul is higher than the states of Minas Gerais (Rodrigues et al., 2013; 19 species), Mato Grosso (Gorni et al., 2018; 22 species) and Rondônia (Gomes et al., 2017; nine species). Such contrasting pattern is a contingency associated with the fact that the latter inventories focused a single ecosystem type (lotic), while the records in Rio Grande do Sul cover different habitats (Tab. III). Thus, the diversity of Oligochaeta likely represents a subset of the known diversity in those states.

The earlier species inventories of Oligochaeta indicated the occurrence of 17 species in rice fields in Rio Grande do Sul (Maltchik et al., 2011; Stenert et al., 2012). In this study, we increased the number of species occurring in these agroecosystems to 19, since B. americana and S. lacustris had not been reported in rice fields. Brinkhurstia americana is common in other states in Brazil (Christoffersen, 2007) and was recorded in a wide array of freshwater ecosystems (from lakes and large dams to streams and high-order rivers) (Pamplin et al., 2005; Alves et al., 2006; Gorni et al., 2015; Sanches et al., 2016). Stylaria lacustris is reported as an opportunistic species with broad ranges (Timm & Erséus, 2021). This suggests a generalist habit of those species in relation to habitat type and possibly explain their establishment in a harsh environment such as rice fields.

Interestingly, a higher number of Oligochaeta species is recorded in rice fields than in wetlands in Rio Grande do Sul. This is likely the result of a combination between methodological contingencies of earlier studies and the lack of studies in other ecosystems. With respect to the former, the previous data for rice fields refer to studies that solely focused rice fields (Maltchik et al., 2011; Stenert et al., 2012); in addition, the authors in these studies covered the full cultivation cycle of the rice crop and sampled different microenvironments (i.e., primary and secondary channels). It is known that macroinvertebrate composition temporally varies over the growth phase of the rice crop and spatially across the plantation (Roger, 1996). This artifact likely contributed to increase the diversity of the Oligochaeta fauna in this agroecosystem. Conversely, species-level inventories of macroinvertebrates are rare in Rio Grande do Sul (Talhaferro et al., 2021). The study of Pires et al. (2016) recorded four species of Oligochaeta; here, we elevate to five species the known diversity of the group in wetlands in the state, as B. americana was not reported in wetlands so far.

Finally, it is important to notice in this study that the majority of the species found in wetlands were not found in rice fields. In addition, 50% of the species recorded in rice fields occurred in wetlands (Fig. 3) and the species so far recorded in wetlands in the state are not yet recorded in rice fields (Tab. III). These results reinforce the hypothesis that rice fields represent an alternative habitat for the wetland biota (Lawler, 2001; Maltchik et al., 2017); however, only part of the species of Oligochaeta in wetlands were capable of occupying rice fields, namely habitat generalist species such as B. americana, S. lacustris and A. chelata. Earlier studies of the spatial distribution of Oligochaeta species have shown that these invertebrates respond to variation in the local environmental conditions of a given site, e.g., water quality and habitat structure (Alves et al., 2006). Our study thus suggests that rice fields are suitable habitats only for a subset of the wetland fauna of Oligochaeta, in accordance with findings of previous studies with macroinvertebrates (Pires et al., 2016; Maltchik et al., 2017).

Our study provided the first inventory of aquatic Oligochaeta species in the state of Rio Grande do Sul. Our results include two new species records for the state and show that 24 species occur in Rio Grande do Sul, suggesting that approximately one fourth (27%) of the known aquatic Oligochaeta species in Brazil is found in the state. This study also contributed to increase the knowledge of the diversity and distribution of aquatic Oligochaeta in wetlands and irrigated rice fields. In specific, we documented the occurrence of additional species in each environment and indicated that rice fields tend to harbor generalist species. In this context, species inventories in natural and man-made ecosystems are of great importance to support the formulation of policies on biodiversity management in threatened ecosystems, such as wetlands and conservation policies in sites under anthropogenic impact such as rice crops. This is particularly important taking into account that approximately 90% of the wetlands in Rio Grande do Sul were mostly lost to rice plantations and that agricultural expansion is concentrated in South American countries.

Acknowledgments

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. The authors thank the team of the former Laboratory of Aquatic Macroinvertebrates from UFSM for their aid in field sampling. This research was part of the master dissertations of MMP and ES at the Animal Biodiversity Graduate Program from UFSM. MMP and ES were granted scholarships from CAPES (Finance Code 001).

REFERENCES

• Altieri, M. A. 1999. The ecological role of biodiversity in agroecosystems. Agriculture, Ecosystems & Environment 74:19-31.
• Alvares, C. A.; Stape, J. L.; Sentelhas, P. C.; De Moraes Gonçalves, J. L. & Sparovek, G. 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22:711‑728.
• Alves, R. G.; Marchese, M. R. & Escarpinati, S. C. 2006. Oligochaeta (Annelida, Clitellata) in lotic environments in the State of São Paulo, Brazil. Iheringia, Série Zoologia 96(4):431-435.
• ANA - Agência Nacional de Águas e Saneamento Básico & CONAB - Companhia Nacional de Abastecimento. 2020. Mapeamento do Arroz Irrigado no Brasil. Brasília, ANA. 40p.
• Bambaradeniya, C. N. B.; Edirisinghe, J. P.; De Silva, D. N.; Gunatilleke, C. V. S.; Ranawana, K. B. & Wijekoon, S. 2004. Biodiversity associated with an irrigated rice agro-ecosystem in Sri Lanka. Biodiversity and Conservation 13:1715-1753.
• Batzer, D. & Boix, D. 2016. An Introduction to Freshwater Wetlands and Their Invertebrates. In: Batzer, D. & Boix, D. eds. Invertebrates in Freshwater Wetlands: An Internation Perspective on their Ecology. Cham, Springer International Publishing, p. 1-23.
• Brinkhurst, R. O. & Jamieson, B. G. M. 1971. Aquatic Oligochaeta of the world. Toronto, University of Toronto Press. 860p.
• Brinkhurst, R. O. & Marchese, M. R. 1989. Guia para la identificación de oligoquetos acuáticos continentales de Sud y Centroamerica. Santa Fé, Asociación de Ciencias Naturales del Litoral. 207p.
• Carvalho, A. B. P. & Ozório, C. P. 2007. Avaliação sobre os banhados do Rio Grande do Sul, Brasil. Revista de Ciências Ambientais 1:83-95.
• Christoffersen, M. L. 2007. A catalogue of aquatic microdrile oligochaetes (Annelida: Clitellata) from South America. Acta Hydrobiologica Sinica 31:59-86.
• Christoffersen, M. L. 2010. Continental biodiversity of South American Oligochaetes: the importance of Inventories. Acta Zoológica Mexicana 2:35-46.
• Davidson, N. C. 2014. How much wetland has the world lost? Long-term and recent trends in global wetland area. Marine and Freshwater Research 65:934-941.
• Davidson, N. C.; van Dam, A. A.; Finlayson, C. M. & McInnes, R. J. 2019. Worth of wetlands: revised global monetary values of coastal and inland wetland ecosystem services. Marine and Freshwater Research 70(8):1189-1194.
• Dudgeon, D. 2019. Multiple threats imperil freshwater biodiversity in the Anthropocene. Current Biology 29:960-967.
• GBIF - Global Biodiversity Facility. 2019. GBIF Occurrence Download. Available at <Available at https://doi.org/10.15468/dl.kzsjn7 >. Accessed on 2019.11.09.
  » https://doi.org/10.15468/dl.kzsjn7
• Girolli, D. A.; Gorni, G. R.; Colombo-Corbi, V. & Corbi, J. J. 2019. First record of Nais schubarti Marcus, 1944 (Oligochaeta: Naididae) in the State of São Paulo. Brazilian Journal of Biology 79:552-553.
• Girolli, D. A.; Lima, M. F.; Sanches, N. A. O.; Colombo-Corbi, V.; Corbi, J. J. & Gorni, G. R. 2021. Aquatic oligochaetes (Annelida: Clitellata) in reservoirs in São Paulo State: list of occurrence and ecological observations on the species. Biota Neotropica 21(3):e2021.
• Gomes, D. F.; Sanches, N. A. O.; Sahm, L. H. & Gorni, G. 2017. Aquatic Oligochaeta (Annelida: Clitellata) in extractive reserve Lake Cuniã, Western Brazilian Amazon. Biota Neotropica 17(1):e20160232.
• Gorni, G.; Peiró, D. F. & Sanches, N. 2015. Aquatic Oligochaeta (Annelida: Clitellata) from State of São Paulo, Brazil: Diversity and Occurrence review. Biota Neotropica 15(1):e20140063.
• Gorni, G.; Sanches, N. A. O.; Colombo-Corbi, V. & Corbi, J. J. 2018. Oligochaeta (Annelida: Clitellata) in the Juruena River, MT, Brazil: species indicators of substrate types. Biota Neotropica 18(4):e20180566.
• Govedich, F.; Bain, B.; Moser, W.; Gelder, S.; Davies, R. & Brinkhurst, R. 2010. Annelida (Clitellata). In: Thorp, J. H. & Covich, A. P., eds. Ecology and Classification of North American Freshwater Invertebrates. Amsterdam, Elsevier, p. 385-436.
• IRGA - Instituto Riograndense do Arroz. 2012. Acompanhamento da Semeadura do Arroz Irrigado no Rio Grande do Sul: Safra 2011/2012. Instituto Riograndense do Arroz. Available at <Available at http://www.irga.rs.gov.br >. Accessed on 2012.06.30.
  » http://www.irga.rs.gov.br
• Lawler, S. P. 2001. Rice fields as temporary wetlands: A review. Israel Journal of Zoology 47:513-528.
• Maltchik, L.; Rolon, A. S.; Stenert, C.; Machado, I. F. & Rocha, O. 2011. Can rice field channels contribute to biodiversity conservation in southern Brazilian wetlands? Revista de Biologia Tropical 59:1895-1914.
• Maltchik, L.; Stenert, C. & Batzer, D. P. 2017. Can rice field management practices contribute to the conservation of species from natural wetlands? Lessons from Brazil. Basic and Applied Ecology 18:50-56.
• Pamplin, P. A. Z.; Rocha, O. & Marchese, M. 2005. Riqueza de espécies de Oligochaeta (Annelida, Clitellata) em duas represas do rio Tietê (São Paulo). Biota Neotropica 5:63-70.
• Pires, M. M.; Kotzian, C. B.; Spies, M. R. & Baptista, V. A. 2016. Comparative assessment of aquatic macroinvertebrate diversity in irrigated rice fields and wetlands through different spatial scales: An additive partitioning approach. Marine and Freshwater Research 67:368-379.
• Righi, G. 1984. Oligochaeta. In: Schaden, R. ed. Manual de identificação de invertebrados límnicos do Brasil. Brasília, CNPq. 48p.
• Rodrigues, L. F. T. & Alves, R. D. G. 2018. Global panorama of studies about freshwater oligochaetes: main trends and gaps. Papéis Avulsos de Zoologia 58:e20185838.
• Rodrigues, L. F. T.; Leite, F. S. & Alves, R. G. 2013. Inventory and distribution of Oligochaeta (Annelida, Clitellata) in first-order streams in preserved areas of the state of Minas Gerais, Brazil. Biota Neotropica 13:245-254.
• Roger, P. A. 1996. Biology and management of the floodwater ecosystems in ricefields. Manila, International Rice Research Institute. 250p.
• Sanches, N. A. O.; Sahm, L. H.; Gomes, D. F.; Corbi, J. J.; Ribeiro, M. L. & Gorni, G. R. 2016. Inventário de Oligochaeta (Annelida: Clitellata) em córregos urbanos de Bocaina - SP, Brasil. Revista Brasileira Multidisciplinar 19(1):27-46.
• Sousa, R.; Halabowski, D.; Labecka, A. M.; Douda, K.; Aksenova, O.; Bespalaya, Y.; Bolotov, I.; Geist, J.; Jones, H. A.; Konopleva, E.; Klunzinger, M. W.; Lasso, C. A.; Lewin, I.; Liu, X.; Lopes-Lima, M.; Mageroy, J.; Mlambo, M.; Nakamura, K.; Nakano, M.; Österling, M.; Pfeiffer, J.; Prié, V.; Paschoal, L. R. P.; Riccardi, N.; Santos, R.; Shumka, S.; Smith, A. K.; Son, M. O.; Teixeira, A.; Thielen, F.; Torres, S.; Varandas, S.; Vikhrev, I. V.; Wu, X.; Zieritz, A. & Nogueira, J. G. 2021. The role of anthropogenic habitats in freshwater mussel conservation. Global Change Biology 27:2298-2314.
• Stenert, C. & Maltchik, L. 2007. Influence of area, altitude and hydroperiod on macroinvertebrate communities in southern Brazil wetlands. Marine and Freshwater Research 58:993-1001.
• Stenert, C.; Maltchik, L. & Rocha, O. 2012. Diversidade de invertebrados aquáticos em arrozais no Sul do Brasil. Neotropical Biology and Conservation 7:67-77.
• Takeda, A. M.; Fujita, D. S.; Ragonha, F. H.; Petsch, D. K. & Montanholi-Martins, M. C. 2017. Oligochaeta (Annelida) de ambientes aquáticos continentais do Estado do Mato Grosso do Sul (Brasil). Iheringia, Série Zoologia 107:e2017107.
• Talhaferro, J. T.; Bueno, A. A. P.; Pires, M. M.; Stenert, C.; Maltchik, L. & Kotzian, C. B. 2021. Three new species of Hyalella (Crustacea: Amphipoda: Hyalellidae) from the Southern Brazilian Coastal Plain. Zootaxa 4970:257-292.
• Timm, T. & Erséus, C. 2021. World List of Marine Oligochaeta. Stylaria lacustris (Linnaeus, 1758). World Register of Marine Species. Available at <Available at http://www.marinespecies.org/aphia.php?p=taxdetails&id=137486 >. Accessed on 2021.07.22.
  » http://www.marinespecies.org/aphia.php?p=taxdetails&id=137486
• Winkler, K.; Fuchs, R.; Rounsevell, M. & Herold, M. 2021. Global land use changes are four times greater than previously estimated. Nature Communications 12:1-10.

Publication Dates

• Publication in this collection
  08 Dec 2021
• Date of issue
  2021

History

• Received
  02 Aug 2021
• Accepted
  27 Oct 2021