More on the distribution of cladoceran species: gaps and perspectives in Rio de Janeiro State, southeastern Brazil

Abstract

Our knowledge of cladoceran species composition and distribution of Neotropical taxa is incomplete, therefore misleading the basic understanding of biodiversity processes and biogeographical patterns of this ecologically relevant group. We present new records and an updated checklist of the cladocerans of Rio de Janeiro State (Brazil) based on a critical review of their known distribution throughout the different freshwater ecoregions. Nine marine species were recorded, and 80 non-marine cladocerans were counted from two of the four ecoregions of Rio de Janeiro State. We estimate species richness applying the interpolation and extrapolation method, using iNEXT function. With this approach we compute diversity estimates for rarefied and extrapolated samples up to double the reference sample size (number of studies). Four new records of rare species were included from surveys in the Paraiba do Sul ecoregion. The Fluminense ecoregion shows a higher richness with a more asymptotic curve and thus a lower expected richness in comparison to the Paraiba do Sul ecoregion. Ceriodaphnia cornuta Sars, 1886 was the most frequently found species whilst Moina macrocopa Straus, 1820 was the only non-native species encountered. Our study can contribute to developing a biogeographical understanding of this diverse group in a heterogeneous territory in terms of inland waters. Future studies are suggested to prioritize novel ecoregions and unexplored habitats e.g. littoral zones with high macrophyte and periphyton coverage, brackish waters, saline and high-altitude lakes, as more diverse and heterogeneous habitats will undoubtedly reveal additional records.

Keywords:
Brazil; Cladocera; distribution records; neotropical ecoregions; richness; water fleas

INTRODUCTION

The superorder Cladocera is represented by aquatic invertebrates inhabiting both marine and inland waters, and reproducing by cyclical parthenogenesis: alternating clone production, which constitutes a population of all females, with sexual reproduction when the environmental conditions are unfavorable (presence of predators, limited food resources, temperature variations) (Brooks and Dodson, 1965; Lynch, 1980; Pijanowska and Stolpe, 1996; Elmoor-Loureiro, 1997; Rocha et al., 2011). The class Branchiopoda of the Subphylum Crustacea is composed of thirteen orders including nine extant orders (Anostraca, Notostraca, Cyclestherida, Laevicaudata, Spinicaudata, Anomopoda, Ctenopoda, Haplopoda and Onychopoda, and also extinct taxa, only know from fossils (Lipostraca†, Kazacharthra†, Cryptopoda† and Proanomopoda†) (Van Damme and Kotov, 2016). Monophyly of the Cladocera was suggested from analyses based on morphological and molecular data (Fryer, 1987; Olesen, 2002; De Waard et al., 2006; Kotov, 2013), however, the phylogenetic relationships within the Cladocera are still a matter of debate and, from a general perspective, a continuous update of their biogeography, phylogeography and ecological attributes is urgent on a global scale (Forró et al., 2008).

Accordingly, the geographic distribution of cladocerans is largely unknown in most of the biogeographic regions (Forró et al., 2008), being a fruitful field for future studies. In the Neotropical mega-diverse region, taxonomic and distributional resolutions have been following international collaborative work of specialists, through new species descriptions (Paggi and Herrera-Martinez, 2020; Garibian et al., 2021; Sousa et al., 2021), new records (Elmoor-Loureiro et al., 2010a; Farias et al., 2017), evidence of non-native species (Zanata et al., 2003; Elmoor-Loureiro et al., 2010b) and endemic taxa (Kotov et al., 2010; Elmoor-Loureiro, 2014; Sousa et al., 2016). Moreover, several gaps in the Neotropical region have been continuously filled through revisions of species groups, e.g. Anthalona Van Damme, Sinev and Dumont, 2011 (Sousa et al., 2015a), and regional checklists such as in Chile (De los Ríos and Kotov, 2015), Colombia (Kotov and Fuentes-Reines, 2015), Ecuador (Lopéz et al., 2018), México (Elías-Gutiérrez et al., 1999; 2008), and Venezuela (Zoppi de Roa and López, 2008).

In Brazil, specialists have revised the distribution of Cladocera, mainly from inland waters while marine taxa information is restricted. Since the critical analysis of the state of the art of Brazilian Cladocera by Elmoor-Loureiro (2000), the geographic gaps and sampling bias became clear, as well as the greater importance of non-planktonic taxa. Since then, the increasing sampling effort in shallow water bodies and the littoral zone has been evident, however, a geographical hiatus persists at national and regional scales (e.g., Forró et al., 2008; Macêdo et al., 2021). Increasing efforts have shown to support potentially higher richness of cladocerans (Santos- Wisniewski et al., 2001; 2002; Zanata et al., 2003; Lopes et al., 2006; Elmoor-Loureiro et al., 2010a; 2010b; Sousa and Elmoor-Loureiro, 2011) along with local faunistic surveys that have considerably improved our biogeographic perception of this group (e.g.Santos-Wisniewski et al., 2008; Elmoor-Loureiro, 2007; Ghidini and Santos-Silva, 2011; Sousa and Elmoor-Loureiro, 2013; Sousa et al., 2014; Maia-Barbosa et al., 2014).

Another approach found in the literature is based on updates in geographic distribution of cladocerans using published data, plus new records from additional samplings to summarize regional knowledge on their composition and distribution. Such studies deal with large geographic ranges, generally with a focus on artificial geographic boundaries (e.g.Santos-Wisniewski et al., 2011; Zanata et al., 2017; Santos et al., 2021; Santos et al., 2022). These studies have been presented as checklists (Rocha et al., 2011), short faunistic updates (Sousa et al., 2009), and contextualized composition with biogeographic features considering hydrographic basins (Sousa and Elmoor-Loureiro, 2012; Diniz et al., 2020; Brito et al., 2020; Macêdo et al., 2021). This approach seems to be a good strategy to consolidate reports of species occurring in Brazil, indicating the actual use of correct nomenclature and taxonomy, suggesting new perspectives for future studies and monitoring-support materials (Forró et al., 2008; Gazulha, 2012).

Here, we present a critical updated inventory of cladocerans from the Neotropical inland waters of Rio de Janeiro State. We also examine biodiversity from studied freshwater ecoregions by computing richness estimates for extrapolated samples up to double the reference sample size. We briefly comment on records of marine taxa. We provide new records of freshwater species, as well as comments on biogeography, endemism and recommendations for future studies in the State.

MATERIAL AND METHODS

Environmental Background

We define Neotropical freshwater ecoregions after Abell et al. (2008). Considering this ecogeographic arrangement, the localities were - a priori - restricted to Paraiba do Sul (PBS), Fluminense (FLU), Ribeira do Iguape (RIG) and Northwestern Mata Atlântica (NMA) (Tab. 1, Fig. 1). The PBS ecoregion encompasses the greatest portions of Rio de Janeiro State’s territory and includes the drainage basin of the Paraíba do Sul River, which starts at the confluence of the Paraitinga and Paraibuna rivers. The upper-middle and lower stretches of Paraíba do Sul River have an economic regional relevancy due to the presence of multiple-use reservoirs, diversion of waters into another river basin (Guandu River), and a navigable low course flowing to the Atlantic Ocean. The FLU is the only ecoregion entirely contained within Rio de Janeiro territory and includes all of the coastal drainages in the state of Rio de Janeiro, mainly following into Guanabara Bay, coastal lagoons (freshwater or brackish) and marshes. Furthermore, it is where the majority of urban inland waters occurs but unraveling some great opportunities for novel records of native and invasive cladocerans from urban ponds and hypereutrophic lakes. The RIG and NMA ecoregions are restricted to its southeastern and northeastern portions, respectively. RIG has coastal environments extending across Sepetiba Bay in Rio de Janeiro State, although its major areas are in São Paulo State. Conversely, NMA is formed by coastal drainage basins in eastern Brazil from Sergipe, Bahia and Espírito Santo to Rio de Janeiro following the Itabapoana drainage in the south (Abell et al., 2008; FEOW, 2019 - http://www.feow.org).

Table 1.
Sampling localities with geographical coordinates of the records gathered from literature and from our surveys.

Localities	Latitude	Longitude	Reference
Paraiba do Sul Ecoregion
1. Paracambi Reservoir	-22.676	-43.763	Branco et al., 2019
2. Tocos Reservoir	-22.736	-44.124	This study
3. Santana Reservoir	-22.577	-43.838	This study
4. Vigário Reservoir	-22.639	-43.895	This study
5. Ponte Coberta Reservoir	-22.685	-43.835	This study
6. Ilha dos Pombos Reservoir	-22.034	-43.000	This study
7. Ribeirão das Lajes Reservoir	-22.719	-43.896	Macêdo et al., 2018; Lopes et al., 2018
8. Funil Reservoir	-22.563	-44.603	Branco et al., 2002; Ferrão-Filho et al., 2008; Rocha et al., 2011; Picapedra et al., 2021
9. Parque Nacional do Itatiaia			Sousa et al., 2014
10. Paraiba do Sul Estuary	-21.616 -21.629	-41.000 -41.050	Sterza and Fernandes, 2006
11. Fish tanks	Several systems		Loureiro et al., 2011
12. Tijuca River, Tijuca National Park	-22.953	-43.281	Sousa et al., 2016
13.Solidão River, Tijuca National Park	-22.960	-43.288	Sousa et al., 2015a
Fluminense Ecoregion
14. Lagoinha das Tachas	-22.201	-43.493	Farias et al., 2017
15. Atoleiro pond, Restinga de Jurubatiba National Park	-22.227	-41.539	Elmoor-Loureiro et al., 2010a; Nova et al., 2021
16. Camorim Reservoir	-22.957	-43.446	Ferrão-Filho et al., 2019
17. Comprida Lagoon	-22.267	-41.650	Branco et al., 2000; Araújo et al., 2013; Nova et al., 2021
18. Carapebus Lagoon	-22.251	-41.593	Attayde and Bozelli, 1998; Santangelo et al., 2010; Araújo et al., 2013; Vargas et al., 2019
19. Cabiúnas Lagoon	-22.294	-41.691	Lopes et al., 2006; Kotov and Elmoor-Loureiro, 2008; Santangelo et al., 2008; Branco et al., 2008; Setubal et al., 2013; Araújo et al., 2013; Sousa et al., 2015; Nova et al., 2021
20. Imboassica Lagoon	-22.411	-41.826	Kozlowsky-Suzuki and Bozelli, 2002; 2004; Branco et al., 2007; Santangelo et al., 2007; Setubal et al., 2013; Araújo et al., 2013;
21. Jacarepaguá Lagoon	-22.987	-43.404	Ferrão-Filho et al., 2002
22. Urban temporary pond	-22.903	-43.172	Elmoor-Loureiro et al., 2010b
23. Paulista	-22.234	-41.544	Nova et al., 2021
24. Pitanga	-22.160	-41.299	Nova et al., 2021
25. Bezerra	-22.197	-41.449	Nova et al., 2021
26. Amarra-Boi	-22.192	-41.432	Nova et al., 2021
27. Garça lagoon	-22.217	-41.505	Araújo et al., 2015

Figure 1.
Map of the current known distribution of cladocerans in Rio de Janeiro State, Brazil. Background colors represent the four freshwater ecoregions in the state - RIG; Ribeira do Iguape, PBS; Paraiba do Sul, FLU; Fluminense and NMA for Northeastern Mata Atlantica. Distribution of non-marine taxa are described for PBS and FLU solely (red circles). Marine records are represented by red triangles.

Cladoceran surveys and collections

We searched the body of literature (mostly papers) concerning the Cladocera fauna from Rio de Janeiro State using keywords (“cladocer*” AND “Rio de Janeiro”) in Scopus and Web of Science. We also included master's dissertations and doctoral theses considering the importance of gray literature in the construction of more complete inventories of this group (e.g., Elmoor-Loureiro, 2000; Macêdo et al., 2021). We used Google maps to check the geographic records of all studies and to estimate latitude and longitude when not provided by the authors. New records were included from samples deposited in the Elmoor-Loureiro personal collection (LMAEL) and in the Museu Nacional, Universidade Federal do Rio de Janeiro (MNRJ).

Sampling localities relied on previously surveyed reservoirs with contrasting limnological and morphometric features (Klippel et al., 2020) and coastal urban and peri-urban lagoons and ponds (Branco et al., 2000, 2007; Kozlowsky-Suzuki and Bozelli, 2004; Elmoor-Loureiro et al., 2010b; Farias et al., 2017). Sampling followed different strategies according to particular features of the environment and were mostly conducted by two strategies. In the first, by filtration of 20L of water taken by bucket at sub-surface through a net of 68μm mesh size and, in the second, by vertical hauls in the euphotic zone, which was estimated through the measure of the Secchi disk depth multiplied by 2.7 (Esteves, 2011). All samples were preserved with a sugar-formalin (Haney and Hall, 1973) at 4 % final concentration. Specimens were examined for identification at × 200 and × 400 magnification under a microscope (Olympus BX51). Cladocerans were identified to the species level whenever possible using specific literature (Elmoor-Loureiro, 2007; Sousa et al., 2015b) in addition to the World checklist of freshwater Cladocera species (Kotov et al., 2013). A fraction of the species catalogued in this checklist underwent correction of nomenclature, while the others were kept in the original names found in the analyzed materials.

Data analysis

From mapping the distribution records and revising updated checklists of Cladocera of Rio de Janeiro State, we provide comments on the records of alien and potentially invasive species. Additionally, analysis of endemism and a descriptive differentiation of cladocerans between the previously delimited freshwater ecoregions were conducted (Abell et al., 2008).

We also built an extrapolation curve, based on the number of studies (Rio de Janeiro State; N = 42, PBS; N= 18, FLU; N=24), using iNEXT function, focusing on species richness measures of Hill numbers (q = 0). For this, we used all gathered studies from the literature and the samplings from this study together to compare the richness between ecoregions. We assumed each of the sampled reservoirs in this study (Tocos, Santana, Vigário, Ponte Coberta and Ilha dos Pombos; Tab. 1) as a unique separate study for richness estimation analysis. This analysis was performed through the iNEXT package software R which uses Chao 2 to estimate the number of undetected species in the reference samples from a given region (Hsieh et al., 2016; R core Team, 2020). Only non-marine species were included in this analysis.

RESULTS

We listed the cladoceran fauna, followed by its frequency considering the study locations conducted in the state of Rio de Janeiro (Tab. 2, Fig. 1). The middle stretches of Paraíba do Sul and Guandu rivers as well as Rio Macaé and Rio das Ostras showed a higher sampling effort in terms of different systems and long-term investigations. No study was found considering inland waters in the portion of the RIG and NMA ecoregions. Some records of marine species followed campaigns in the offshore platform. In general, cladocerans were mainly sampled in several different inland water bodies, including nine freshwater reservoirs, several shallow lakes, ponds and brackish environments.

Table 2.
List of Cladocera species and frequency of their occurrence considering all studies. FR = first report, DI = doubtful identification.

Non-marine taxa		FLU	PBS	LMAEL	MNRJ	%
Chydoridae
Aloninae (subfamily)
Acroperus tupinamba Sinev and Elmoor-Loureiro, 2010		X	X			1.11
Ovalona cf cambouei (Guerne and Richard, 1893) (as Alona cambouei)	DI	X	X			1.39
Coronatella cf. poppeiRichard, 1897 (as Alona poppei)	DI	X	X			1.39
Alona guttata (Sars, 1862)		X	X	X		3.06
Alona yara Sinev and Elmoor-Loureiro, 2010		X	X		X	1.11
Anthalona neotropica Sousa, Elmoor-Loureiro and Debastiani-Júnior 2015		X		X		<1
Anthalona verrucosa (Sars, 1901)		X		X		2.79
Biapertura ossiani (Sinev, 1998)		X	X	X		1.11
Bryospilus repens Frey, 1980			X	X	X	<1
Coronatella monacantha (Sars, 1901)		X				<1
Coronatella paulinae Sousa, Elmoor-Loureiro and Santos, 2015		X				<1
Coronatella rectangula (Sars, 1861)	DI	X				<1
Euryalona brasiliensis Brehm and Thomsen, 1936	DI	X		X		<1
Flavalona iheringula (Kotov and Sinev, 2004)		X	X	X	X	1.11
Graptoleberis occidentalis Sars, 1901		X		X		<1
Karualona muelleri Richard, 1897		X			X	<1
Kurzia latissima (Kurz, 1875)	DI	X				<1
Kurzia polyspina Hudec, 2000		X				<1
Leberis davidi (Richard, 1895)		X				<1
Leydigia ipojucae Brehm​, 1938			X			<1
Leydigia schubarti Brehm and Thomsen, 1936	DI		X			<1
Leydigiopsis brevirostris Brehm, 1938		X				<1
Leydigiopsis curvirostris Sars, 1901		X				<1
Leydigiopsis megalops Sars, 1901	FR			X		<1
Magnospina dentifera (Sars, 1901)		X				<1
Nicsmirnovius paggii Sousa and Elmoor-Loureiro, 2017		X				<1
Ovalona glabra (Sars, 1901)		X	X		X	<1
Oxyurella longicaudis (Birge, 1910)					X	<1
Alonella clathratula Sars, 1896		X				<1
Chydorus eurynotus Sars, 1901		X	X		X	1.67
Chydorus pubescens Sars, 1901		X			X	<1
Chydorus sphaericus (O.F. Müller, 1776)	DI	X				<1
Disparalona leptorhyncha Smirnov, 1996		X				<1
Dunhevedia colombiensis Stingelin, 1913		X		X		<1
Dunhevedia odontoplax Sars, 1901		X				<1
Ephemeroporus cf. barroisi (Richard, 1894)	DI	X				<1
Ephemeroporus hybridus (Daday, 1905)		X			X	<1
Ephemeroporus tridentatus (Bergamin, 1939)					X	<1
Pleuroxus (Picripleuroxus) similis (Vávra, 1900)	DI	X				<1
Macrothricidae						<1
Grimaldina freyi Neretina and Kotov, 2017					X	<1
Guernella raphaelis Richard 1892		X		X		<1
Macrothrix elegans Sars, 1901		X		X	X	1.11
Macrothrix laticornis (Jurine, 1820)	DI	X	X			<1
Macrothrix paulensis (Sars,1901)		X	X	X		<1
Macrothrix squamosa Sars, 1901		X	X	X		<1
Macrothrix superculeata (Smirnov, 1982)		X				<1
Macrothrix triserialis Brady, 1886	DI	X	X			1.39
Streblocerus pygmaeus Sars, 1901	FR			X		<1
Ilyocryptidae						<1
Ilyocryptus spinifer Herrick, 1882		X	X	X	X	4.46
Bosminidae						<1
Bosmina cf. tubicenBrehm, 1953		X	X			1.39
Bosmina freyi De Melo and Hebert, 1994		X				<1
Bosmina hagmanni Stingelin, 1904		X	X		X	4.18
Bosmina longirostris (O.F.Müller, 1776)		X	X			3.34
Bosminopsis deitersi Richard, 1895		X	X			4.74
Moinidae						<1
Moina dumonti Kotov, Elías-Gutiérrez and Granado-Ramírez, 2005		X		X		<1
Moina macrocopa (Straus, 1820)		X		X		<1
Moina micrura Kurz, 1875		X	X	X		3.06
Moina minuta Hansen, 1899		X	X			4.18
Moina reticulata (Daday, 1905)		X				1.11
Moinodaphnia macleayi (King, 1853)		X		X	X	<1
Daphniidae						<1
Ceriodaphnia cornuta Sars, 1885		X	X	X	X	5.85
Ceriodaphnia laticaudata P. E. Müller, 1867		X				<1
Ceriodaphnia paradoxaSpandl, 1926 (probably C. cornuta)	DI		X			1.95
Ceriodaphnia reticulata (Jurine, 1820)		X				<1
Ceriodaphnia richardi Sars, 1901		X	X	X		1.11
Ceriodaphnia silvestrii Daday, 1902		X	X	X	X	3.06
Daphnia gessneri Herbst, 1967		X	X		X	4.46
Daphnia laevis Birge, 1878			X			1.39
Scapholeberis freyi Dumont and Pensaert, 1983		X	X	X		1.11
Simocephalus serrulatus (Koch, 1841)		X	X	X	X	2.23
Simochephalus latirostris Stingelin, 1906		X	X			1.67
Simochephalus acutirostratus (King, 1853)				X	X	<1
Sididae						<1
Diaphanosoma birgei Koříneck, 1981		X	X	X		4.46
Diaphanosoma brevireme Sars, 1901		X	X			1.95
Diaphanosoma fluviatile Hansen, 1899		X	X			<1
Diaphanosoma spinulosum Herbst, 1967		X	X	X		2.79
Latonopsis australis-group Sars, 1888	FR			X		<1
Pseudosida ramosa (Daday, 1904)	FR			X		<1
Sarsilatona serricauda (Sars, 1901)				X	X	<1
Marine taxa
Podonidae
Pleopis polyphemoides (Leuckart, 1859)
Pleopis schmackeri Poppe, 1889
Podon intermedius Lilljeborg, 1853
Podon leuckarti G.O. Sars, 1862
Evadne nordmanni Lovén, 1838
Evadne spinifera P.E. Müller, 1867
Pseudoevadne tergestina (Claus, 1877)
Sididae
Penilia avirostris Dana, 1849

Considering all the data obtained from the literature and the samples collected in more than 30 inland waters of the Rio de Janeiro State (Tab. 2), we recorded 80 cladoceran taxa, distributed in eight families: Chydoridae (40), Moinidae (6), Macrothricidae (9), Sididae (7), Daphniidae (12), Bosminidae (5), Ilyocryptidae (1). When the representative species in sampling localities were considered, the most common taxa were: Ceriodaphnia cornuta Sars, 1886, Bosminopsis deitersiRichard, 1895, Diaphanosoma birgeiKorinek, 1981, Daphnia gessneriHerbst, 1967, Ilyocryptus spiniferHerrick, 1882, Moina minutaHansen, 1899, and Bosmina hagmanniStingelin, 1904. Our study further allowed us to identify species with a rare status with particular niche requirements that can be considered as new records for Rio de Janeiro State, such as Coronatella paulinaeSousa, Elmoor-Loureiro and Santos, 2015, Nicsmirnovius paggiiSousa and Elmoor-Loureiro, 2017.

The sample-size-based extrapolation curves estimated a higher richness than observed, both for each of the ecoregions (FLU and PBS), as well as for both together (Fig. 2A, B, C). However, the FLU ecoregion showed higher richness than PBS at both current and projected values. The estimated richness obtained from twice the known sampling units was 51 for PBS and 91 species for FLU (Fig. 2B, C). Yet, the PBS curve showed a linear tendency while FLU showed an asymptotic curve and stabilizing tendency from twice the analyzed studies. These different patterns may be influenced by the number of studies but also the different types of environments pertaining to each ecoregion.

Figure 2.
Observed richness (OS, full line) and extrapolated richness (ES, dashed line) using the Hill number (q = 0 species richness) of the Cladoceran fauna observed, considering the number of studies, in Rio de Janeiro State (A; OS=80, ES=90), Paraiba do Sul (B; OS=36, ES=51) and Fluminense (C; OS=66, ES=91). Confidence interval of 95 % was obtained by the bootstrap method and represented by the shaded area of the fitted curve.

Chydoridae (Aloninae and Chydorinae) showed a higher number of representatives in the FLU. Specifically, of the total richness from Aloninae, 60 % were exclusively from FLU and 7.4 % from PBS. Considering Chydorinae 69 % were exclusively from FLU while 7.6 % from PBS. Moina macrocopaStraus 1820, a stress tolerant cladoceran from Palearctic regions, was the only non-native species recorded exclusively in urban ponds from FLU. As far as we know, Cladoceran alien species are absent from other ecoregions of Rio de Janeiro State from traditional morphological studies.

Marine cladocerans were sampled in the pelagic zone of the continental shelf (Fig. 1) and accounted for 9 species: the sidid Penilia avirostrisDana, 1849 and the podonids Pleopis schmackeriPoppe, 1889, Podon intermediusLilljeborg, 1853, Pleopis polyphemoidesLeuckart, 1859, Podon leuckartiSars, 1862, Pseudevadne tergestinaClaus, 1877, Evadne nordmanni Lovén, 1836, and Evadne spinifera P.E. Müller, 1867.

DISCUSSION

Despite the increase in cladoceran surveys in the Neotropics in recent years (e.g.,Padovesi-Fonseca et al., 2016; Elmoor-Loureiro et al., 2018; Brito et al., 2020; Diniz et al., 2020; Macêdo et al., 2021; Santos et al., 2021; Santos et al., 2022), our study revealed that there are still very few studies focused on the composition and distribution of cladocerans in Rio de Janeiro State. We observed representatives of the seven cladoceran families in Rio de Janeiro State, encompassing 80 non-marine and 9 marine taxa. Nevertheless, up to thirteen taxa have not previously been identified to the species level, particularly in the genera Macrothrix, Disparalona, Alona and Diaphanosoma. The total richness found in this State, including dubious identifications, was higher than the majority of the current checklists for other Brazilian states (RS, CE, DF, PE, BA < RJ < MG, SP, MS, MT). However, these faunistic comparisons could be more adequately addressed between States by considering the differences in both temporal and spatial efforts employed.

As expected, we found higher estimated richness than the actual values for the State and for both the FLU and PBS ecoregions. In general, these results were influenced by the lack of sampling in the RIG and NMA (Fig. 1) and several studies with sampling throughout similar or nearby environments e.g., coastal lakes and lagoons located in Macaé plain in the FLU ecoregion or connected reservoirs in the PBS ecoregion. In the PBS ecoregion, sampling localities were mainly from artificial environments such as freshwater reservoirs (e.g., Branco et al., 2002; Macêdo et al., 2018; Branco et al., 2019) and fish tanks (Loureiro et al., 2011). Conversely, in the FLU, cladocerans were sampled in natural coastal lagoons (e.g., Branco et al., 2000; 2007; Kozlowsky-Suzuki and Bozelli, 2004; Araújo et al., 2015; Vargas et al., 2019), shallow ponds (Elmoor-Loureiro, 2010a; 2010b; Araújo et al., 2013), and estuaries (Sterza and Fernandes, 2006). These habitats are distinguished by several morphometric and environmental differences (water depth, water volume, habitat complexity), which in part explains the higher number of representatives of the subfamilies Aloninae (representing the most speciose Cladoceran family; Smirnov, 1996a) and Macrothricidae in the FLU since most species are benthic or phytophilous (Smirnov, 1974). Despite this, we did not closely examine the microhabitats from where samples were collected in the literature, and the redundancy and spatial homogeneity of artificial reservoirs and fish tanks are a concern in many studies regarding the assessment of cladoceran diversity (Meschiatti et al., 2000; Elmoor-Loureiro, 2007; Chatterjee et al., 2013; Debastiani-Júnior et al., 2016). In addition, as suggested by other annotated checklists (Zanata et al., 2017; Macêdo et al., 2021), assessing heterogeneous habitats proved to enhance diversity of cladocerans in inland water ecosystems by adding specialized species e.g., Bryospilus repens Smirnov, 1980, reported by Sousa et al. (2014).

Moreover, the composition of microcrustaceans can be significantly underestimated considering the choice of the sampling strategies in these ecosystems, which are often non-standardized and dependent on the habitat type and on the aims of the studies (Macêdo et al., 2018). It is also possible that the underestimated richness of cladoceran species was influenced by the lack of sampling in central and northward portions of the PBS ecoregion, which encompasses several less-studied aquatic ecosystems such as rivers and small ponds surrounded by tropical forests, and shallow lakes of the lower course of the Paraíba do Sul River.

In the specific case of the FLU ecoregion, the estimation curve approaches an asymptote as the number of studies increases. Also, the observed richness represented more than 50 % of the estimated value, thus showing a higher adequacy and usefulness in estimating richness than in PBS (Toti et al., 2000; Williams et al., 2007). The more rapid stabilization in the FLU is comparable to the curve for the entire State of Rio de Janeiro (Fig. 2a) and Bahia (Macêdo et al., 2021), as well as the findings in the Brazilian semi-arid, despite both groups of microcrustaceans (Cladocera and Copepoda) being considered by Diniz et al. (2020). Although seasonal variation is of great importance for zooplankton structure (e.g.,Branco et al., 2007; Santangelo et al., 2007) with consequences for a more realistic assessment of the community composition, aquatic ecosystems are still overlooked in terms of temporal efforts in the FLU ecoregion (Elmoor-Loureiro et al., 2010a; 2010b; Farias et al., 2017; Nova et al., 2021).

Considering the PBS, areas with higher sampling efforts were at the middle reaches of the Paraíba do Sul River and its connectivity through water diversion with Guandu basin. This is due to several cascading reservoirs along the Piraí, Guandu and Paraíba do Sul rivers that have been the target of monitoring programs for domestic water supply and hydroelectric power generation (e.g., Branco et al., 2002; Rocha et al., 2002; Lopes et al., 2018). Even with the increase in new records from the sampling performed in the PBS in this study, the rarefaction curve showed no asymptotic tendency for this ecoregion (Fig. 2B), possibly attributable to the great temporal effort in contrast to the narrow spatial diversity of systems. In other words, these studies were not enough to cover all aquatic habitats within reservoirs, which have spatial and temporal heterogeneity regarding abiotic variables and biological communities. These sampling campaigns were predominantly carried out in the limnetic zone, neglecting the more diverse areas such as littoral zones and macrophytic banks that increase environmental complexity (Villabona-González et al., 2011; Choi et al., 2014).

Similar to other surveys from tropical and subtropical regions, the total number of species remain underestimated regarding morphological and taxonomic difficulties and geographical and temporal restricted samplings e.g.: Thailand (99 species) (Maiphae et al., 2005; 2008), Southern India - Maharashtra (22 species) (Padhye and Victor, 2015) or in the Republic of South Africa (112 species) (Smirnov, 2008). However, without considering the possible differences in sampling methods and surveyed area, the reported number of species in this study is much higher than that reported by Coronel et al. (2007) in Bolivia (21), by Frisch et al. (2006) in Spain (21), or by Rajapaksa and Fernando (1982) in Sri Lanka (62). Therefore, we suggest some new areas to be potentially explored: São João, Piabanha, Rio Dois rivers, and estuarine systems and coastal lagoons, lower Paraiba do Sul and Itabapoana rivers and the most elevated areas of the state, such as Serra da Mantiqueira. Also, some studies in different localities did not mention species lists (Gonçalves Jr. et al., 2004), which may include taxonomic surprises and new records (e.g.,Sousa et al., 2015b; Farias et al., 2017).

Ceriodaphnia cornuta G.O. Sars, 1886 was the most commonly found species considering all studies (Tab. 2). This can be explained by its wide distribution in other tropical and Neotropical environments as well as its high feeding adaptability (Dumont and Tundisi, 1984; Korinek, 2002; Sampaio et al., 2002; Villalobos and González, 2006; Rocha et al., 2011). Except for Moina macrocopa, which was found in an intermittent urban pond in the Rio de Janeiro vicinity (Elmoor-Loureiro et al., 2010b), all species were considered native. This raises a concern on the lack of investigations in urban areas, where new occurrences were added to the State (Elmoor-Loureiro et al., 2010b) and to South America; as in the case of Moina dumonti, first reported by Farias et al. (2017) in a perennial hypereutrophic lagoon in Rio de Janeiro.

All marine species herein described occur on the Brazilian coast (Marazzo and Valentin, 2004; Miyashita et al., 2011; Rosa et al., 2021), and were accordingly less diverse than inland water cladocerans (Egloff et al., 1997; Onbé, 1999). However, Pleopis schmackeri is a Palearctic species and, as well as Moina macrocopa, and Podon intermedius is a species typically described from Nearctic regions (Egloff et al., 1997).

In summary, this work provides: i) technical material for supporting environmental monitoring analysis and ecological investigations in the area, ii) makes future studies possible to compare diversity parameters at local and regional scales, and iii) indicates areas where sampling efforts should be intensified, such as small waterbodies, semi-terrestrial ecosystems and protected areas such as the Parque Nacional do Itatiaia, strategically important for housing a large part of the Mata Atlântica biome. This study was entirely based on morphological data, which in part could explain some of the misidentifications (see Tab. 2 for all suggested doubtful identifications). Looking at current taxonomic knowledge about Cladocera, some dubious reports emerge from the literature, especially regarding the chydorines. Therefore, close taxonomic attention should be given to studies in the region using an integrative approach to assist in refining taxonomic resolution. Such procedures are useful in the identification of cryptic invasions and early detections from genetic material obtained directly from environmental samples. This first overview on the distribution of cladocerans in Rio de Janeiro may have implications for the conservation of the fauna and environments as well as for the understanding of their biogeography in Brazil and South America.

ACKNOWLEDGMENTS

Rafael L Macêdo would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES) for the PhD scholarship in Ecology and Natural Resources at Federal University of São Carlos. The authors also thank the Neotropical Limnology Group (NEL/UNIRIO) for laboratory facilities. Elmoor-Loureiro is grateful to Paulo C. Young, in memoriam, who made access to the Cladoceran collection of the National Museum of Rio de Janeiro possible. All the authors are grateful to the anonymous reviewers for their careful and constructive reviews of our paper.

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Additional Information and Declarations

• Consent for publication

  All authors approved the manuscript and gave their consent for submission and publication in Nauplius. We also guarantee that the research findings have not been previously published.

• Funding and grant disclosures

  RLM was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brazil (CAPES, doctorate scholarship). VV was funded by the National Council for Scientific and Technological Development (Bolsista do CNPq - Brazil).

Erratum

• In the article “More on the distribution of cladoceran species: gaps and perspectives in Rio de Janeiro State, southeastern Brazil”, with DOI number: 10.1590/2358-2936e2022032, published in the journal Nauplius, vol. 30, e2022032:
  In the list of authors, where it reads:
  Vinícius Veras e Silva
  It should read:
  Vinicius Veras

Edited by

Editor-in-chief:

Christopher Tudge

Associate Editor:

Jessica Covalite

Publication Dates

• Publication in this collection
  28 Nov 2022
• Date of issue
  2022

History

• Received
  17 Aug 2021
• Accepted
  09 Mar 2022