New records of two cladoceran species (Branchiopoda: Anomopoda) from Northeastern Brazil: the importance of studies in temporary ponds

Abstract

Temporary ponds are heterogeneous aquatic environments, in which hydrodynamics and richness of macrophytes may increase the diversity of zooplankton and other invertebrate communities. Cladocerans are common residents of these ecosystems, showing great variability of forms. During a faunistic survey in temporary ponds under the influence of riparian vegetation, in the Camucim Forest Protected Area, Pernambuco Endemism Center, Brazil, the cladocerans Moina dumonti Kotov, Elías-Gutiérrez and Granado-Ramírez, 2005 and Chydorus nitidulus (Sars, 1901) were found. These are their first records in the Oriental Northeast Atlantic hydrographic region, and the second record of M. dumonti in Brazil. The present study raises Cladocera species richness in Pernambuco State to 73 and also 16 in the Pernambuco Endemism Center.

Keywords
Chydoridae; Moinidae; Neotropical; Pernambuco Endemism Center; zooplankton

INTRODUCTION

Temporary pond ecosystems are abundant and occur around most of the globe, frequently threatened by human impacts and periodically exposed to water stress during the dry seasons (Williams and Hynes, 1977; De Meester et al., 2005; Williams, 2005; Medeiros et al., 2019). In such periods, evaporation processes reduce the volume of water bodies, affecting the availability of resources and the aquatic population dynamics (Junk, 2002; Lake, 2003). Even so, they host particularly diverse communities, sometimes exclusively, and they play an important role in the distribution of aquatic species and provide essential ecosystem services (Blaustein and Schwartz, 2001; Diniz et al., 2013; Fuentes-Reinés et al., 2019). The presence of riparian vegetation and macrophytes in temporary aquatic environments enhances local heterogeneity and preserves its biotic/abiotic integrity. It also promotes thermal stability, shade, shelter, and food sources for a number of animal groups, especially zooplanktonic organisms (Arcova and Cicco 1999; Thomaz and Cunha, 2010; Medeiros et al., 2019).

Cladocerans are common planktonic and/or phytophilous microcrustaceans in continental aquatic ecosystems and are highly diversified in the Neotropical region. Moinidae Goulden, 1968 and Chydoridae Dybowski and Grochowski, 1894 emend. Frey, 1967 are prominent families in this region, with high endemism rates (50 % and 57.3 %, respectively) (Forró et al., 2008). The Moinidae, particularly the genus MoinaBaird, 1850, are opportunistic, thermal stress-tolerant, and typical pelagic components in temporary water bodies (Petrusek, 2002; Farias et al., 2017). On the other hand, the Chydoridae are very specialized organisms, with limited ability for dispersion, which results in high endemism rates (Fryer, 1968). Herein, we report two new records of the cladocerans Moina dumontiKotov, Elías-Gutiérrez and Granado-Ramírez, 2005 and Chydorus nitidulus (Sars, 1901) for Northeastern Brazil, briefly discuss some of their morphological traits and the environmental context in which they were found.

MATERIAL AND METHODS

The specimens were sampled in May 2018 during zooplankton biodiversity assessments in temporary ponds under the influence of riparian vegetation. The surveys were carried out in the Camucim Forest Protected Area, near Tapacurá Ecological Station, in São Lourenço da Mata municipality, part of the Oriental Northeastern Atlantic Basin (Fig. 1, Tab. 1). This area is located within the Atlantic Forest Biome, and precisely in the Pernambuco Endemism Center (Silva and Casteleti, 2003). The climate is categorized as Tropical with dry summer (Köppen’s classification criteria: “As”), with annual average temperature varying from 24 to 26 °C, and annual rainfall at about 1200 mm, from March to July (Alvares et al., 2013).

Figure 1.
Distribution records of Moina dumontiKotov, Elías-Gutiérrez and Granado-Ramírez, 2005 and Chydorus nitidulus (Sars, 1901) in Neotropical regions.

Table 1.
New and previous records of Moina dumontiKotov, Elías-Gutiérrez and Granado-Ramírez, 2005 and Chydorus nitidulus (Sars, 1901) in Neotropical regions. Abbreviations for Brazilian States: BA = Bahia; GO = Goiás; MG = Minas Gerais; MS = Mato Grosso do Sul; MT = Mato Grosso; PA = Pará; PE = Pernambuco; PR = Paraná; RJ = Rio de Janeiro; SC = Santa Catarina; SP = São Paulo.

Species / Locality	Habitat	Coordinates	Reference
Moina dumonti
Felipe Carrillo Puerto, México	Temporary pond	19◦23’37.9’’N 88◦37’12.1’’W	Kotov et al., 2005
Playa de Guanabo, Cuba	Temporary pond	23°09'40.2"N 82°07'21.3"W	Kotov et al., 2005
Rio de Janeiro, RJ, Brazil	Permanent pond	23°01ʹ24.80ʺS 43°28ʹ17.93ʺW	Farias et al., 2017
Camucim Forest Protected Area, PE, Brazil	Temporary pond	08°01'59.8"S 35°12'03.8"W	Present study
Camucim Forest Protected Area, PE, Brazil	Temporary pond	08°02'18.2''S 35°12'2.97''W	Present study
Camucim Forest Protected Area, PE, Brazil	Temporary pond	08°02'5.07''S 35°11'57.38''W	Present study
Chydorus nitidulus
Camucim Forest Protected Area, PE, Brazil	Temporary pond	08°02'24.8"S 35°11'48.5"W	Present study
Camucim Forest Protected Area, PE, Brazil	Temporary pond	08°02'18.2''S 35°12'2.97''W	Present study
Mata da Pimenteira, PE, Brazil	Temporary pond	07°53’48.96”S 38°18’14.30”W	Diniz et al., 2013
Brígida River, PE, Brazil	River	08°05.183’S 39°34.694’W	Diniz et al., 2020
Santa Rita, BA, Brazil	Reservoir	14°11’14’’S 39°42’27’’W	Macêdo et al., 2021
Bom Sucesso Farm, BA, Brazil	Reservoir	14°10’25’’S 39°44’19’’W	Macêdo et al., 2021
Pedra do Cavalo Dam, BA, Brazil	Reservoir	12°35’51.9’’S 39°00’16.4’’W	Macêdo et al., 2021
Formosa lagoon, GO, Brazil	Permanent lagoon	15°09’15.8’’S 47°28’04.7’’W	Elmoor-Loureiro, 2007
Flores do Goiás swamp, GO, Brazil	Temporary swamp	14°18’23.9’’S 46°57’34.0’’W	Elmoor-Loureiro, 2007
Baía do Castelo, MS, Brazil	Permanent pond	18°31'36.0"S 57°34'54.3"W	Hollwedel et al., 2003
Lago Buritizinho, MS, Brazil	Permanent pond	18°25'33.1"S 54°49'39.2"W	Güntzel et al., 2010
Lago Ribeirão, MS, Brazil	Permanent pond	18°25'14.7"S 54°50'31.6"W	Güntzel et al., 2010
Rio Taquari, MS, Brazil	Permanent pond	18°25’19” S 54°50’41”W	Panarelli et al., 2013
Lago Souza Lima, MT, Brazil	Permanent pond	15°43’27.3”S 56°06’52.4”W	Neves et al., 2003
Lagoa dos Patos, MS, Brazil	Permanent pond	22°49’S 53°33’W	Serafim-Júnior et al., 2003
Represa Paraibuna, SP, Brazil	Reservoir	23°26'53''S 45°33'44''W	Rocha et al., 2011
Represa Itaiquara, SP, Brazil	Reservoir	21°35'05''S 46°44'52''W	Rocha et al., 2011
Lagoa do Peixe, SP, Brazil	Permanent pond	21°37'25''S 47°48'24''W	Rocha et al., 2011
Represa Mogi, SP, Brazil	Reservoir	22°22'44.7"S 46°53'17.3"W	Rocha et al., 2011
Lago Fazenda Socorro, SP, Brazil	Permanent pond	20°57'49''S 48°40'45''W	Rocha et al., 2011
Lago Fazenda Brazil, SP, Brazil	Permanent pond	20°45'46''S 49°32'58''W	Rocha et al., 2011
Lago Marechal Rondon, SP, Brazil	Permanent pond	21º11’44’’S 50º53’52’’W	Rocha et al., 2011
Lago marginal, Rio Aguapeí, SP, Brazil	Permanent pond	21º42’24’’S 50º30’48’’W	Rocha et al., 2011
Reservatório Chavantes, SP, Brazil	Reservoir	23°08'27''S 49°42'24''W	Rocha et al., 2011; Perbiche-Neves and Nogueira, 2010
Vicentinópolis, SP, Brazil	Temporary pond	20°56’00”S 50°20’51”W	Castilho-Noll et al., 2010
Macaubal, SP, Brazil	Permanent pond	20°44’40”S 49°56’13”W	Castilho-Noll et al., 2010
Novo Horizonte, SP, Brazil	Permanent pond	21°30’10”S 49°18’29”W	Castilho-Noll et al., 2010
Represa Promissão, SP, Brazil	Reservoir	21°25’33”S 49°29 59”W	Castilho-Noll et al., 2010
Planalto, SP, Brazil	Permanent pond	21°00’54”S 49°58’41”W	Castilho-Noll et al., 2010
União Paulista, SP, Brazil	Permanent pond	20°54’28”S 49°55’17”W	Castilho-Noll et al., 2010
Magda, SP, Brazil	Permanent pond	20°32’00”S 50°11’43”W	Castilho-Noll et al., 2010
Matão, SP, Brazil	Permanent pond	21°36’18”S 48°33’12”W	Castilho-Noll et al., 2010
Matão 3, SP, Brazil	Permanent pond	21°36’25”S 48°30’33”W	Castilho-Noll et al., 2010
Represa Jurumirim, SP, Brazil	Permanent pond	23°31'40.7"S 48°38'10.5"W	Debastiani-Júnior et al., 2016
Rio Itajaí-Açu, SC, Brazil	River	26°53'27.5"S 49°14'05.4"W	Serafim-júnior et al., 2006
Represa do Iraí, PR, Brazil	Reservoir	25°23'44.8"S 49°06'10.7"W	Ghidini and Santos-Silva, 2009
Reservatório Salto Grande, PR, Brazil	Reservoir	22°56'43''S 49°57'60''W	Rocha et al. 2011
Lago dos Patos, MG, Brazil	Permanent pond	19°48'19.9''S 42°32'12.7'' W	Maia-Barbosa et al., 2014
Lago Dom Helvácio, MG, Brazil	Permanent pond	19°46'55.7''S 42°35'28.9''W	Maia-Barbosa et al., 2014
Rio Xingu, PA, Brazil	River	01°55'29.1"S 52°13'53.8"W	Matsumura-Tundise et al., 2015
Lago Batata, PA, Brazil	Permanent pond	01°30′S 56°20′W	Sodré et al., 2017
Laguna Navio Quebrado, Colombia	Saline lagoon	11°25'N 73°05'W	Fuentes-Reinés, 2014
Maicao, Colombia	Temporary pond	11°23ʹ04.63ʺN 72°16ʹ31.10ʺW	Fuentes Reinés et al., 2019
Santa Elena, México	Temporary pond	18°04'45''N 92°01'32''W	Elías-Gutiérrez et al., 2006
Chicanná, México	Temporary pond	18°30'50''N 89°28'50''W	Élias-Gutiérrez et al., 2006

Six ponds were chosen for sampling in this area (see Medeiros et al., 2019). Environmental data were obtained through a multiparameter water-quality meter, Horiba-U50. For each station, a minimum of 10 liters of water were filtered using a 20 µm net, and the organisms retained were fixed in 4 % neutral formalin. Specimens were identified under a light microscope, according to literature (e.g., Elmoor-Loureiro, 1997; Farias et al., 2017), and deposited in the Zooplankton Collection of the Federal Rural University of Pernambuco (vouchers CZ-UFRPE: 18008, 18010, 18011, 18019, 18029, 18034).

SYSTEMATICS

Class Branchiopoda Latreille, 1817

Order Anomopoda Sars, 1865

Suborder Aradopoda Kotov, 2013

Family Moinidae Goulden, 1968

Genus Moina Baird, 1850

Moina dumonti Kotov, Elías-Gutiérrez and Granado-Ramírez, 2005

(Fig. 2)

Figure 2.
Specimens of female (a, c, e, g) and male (b, d, f, h) of Moina dumontiKotov, Elías-Gutiérrez and Granado-Ramírez, 2005 from Camucim Forest Protected Area, Pernambuco, Brazil. a, Parthenogenetic female; b, male; c, antenna I, aesthetasc of similar size (Arrow-2 setae); d, antenna I, Arrow-1 points to four hook-like setae; e, postabdomen (Arrow-3: set of teeth - n: 5); f, postabdomen (Arrow-4: set of teeth - n: 4); g, h, back of the dorsal valve of female and male, respectively.

Material examined. 1 ind. (CZ-UFRPE 18010), Camucim Forest Protected Area, São Lourenço da Mata, Pernambuco, 8°02'18.2''S 35°12'2.97''W (WGS84), 09 May 2018, colls. R.F. de Oliveira and F.A. Santos; 7 ind. (CZ-UFRPE 18011), 4 ind. (CZ-UFRPE 18029), Camucim Forest Protected Area, São Lourenço da Mata, Pernambuco, 8°02'14''S 35°12'01''W, 09-10 May 2018, colls. R.F. de Oliveira and F.A. Santos; 1 ind. (CZ-UFRPE 18019), Camucim Forest Protected Area, São Lourenço da Mata, Pernambuco, 8°01'59.8"S 35°12'03.8"W, 10 May 2018, colls. R.F. de Oliveira and F.A. Santos.

Specimens. All M. dumonti specimens have morphological characters corresponding to the original description (Kotov et al., 2005) (Fig. 2); with body structures of parthenogenetic females (Fig. 2a) and males (Fig. 2b), although it was not possible to observe the presence of ocellae at the base of the first antenna. Females show short and practically cylindrical antennae, with an aesthetasc tip of similar size (Fig. 2c); whereas males showed long and slightly curved antennae, distally with four similar hook-like setae (Fig. 2d). Postabdomen with terminal claw showing basal pecten with five spines in females (Fig. 2e) and four in males (Fig. 2f). All males showed the same set of spines on the basal pecten. This morphological character easily distinguishes this species from its congeners. The setulated hook in the dorsal portion of the posterior valve observed by Farias et al. (2017) does not exist in females (Fig. 2g) or males (Fig. 2h) sampled in the present study.

Ecology and habitat. Parthenogenetic females, ephippials and males were collected in two distinct environments: two ponds with riparian vegetation and a predominance of the macrophyte Lemna on the waterline; and one pond without riparian vegetation and a predominance of the macrophyte Azolla. These environments showed population densities of 27,208 ind/m³ and 833 ind/m³, respectively. The influence of riparian vegetation on the zooplanktonic communities of these ponds was described by Medeiros et al. (2019), who associated the occurrence of M. dumonti with low water turbidity (45.81 ± 27.84 NTU), high oxygenation (5.17 ± 2.10 mg L^-1), and variable a-chlorophyll concentrations (23.31 ± 28.07 µg L^-1).

Distribution. Since its description, M. dumonti has been recorded in three environments in the world: two temporary habitats in Mexico and Cuba (Kotov et al., 2005) and one perennial lagoon in Rio de Janeiro, Brazil (Farias et al., 2017). In this study, the specimens were recorded in a habitat similar to its type-locality, temporary ponds, for the first time in the Brazilian Northeast region (Fig. 1). Thus, this species is now recorded in Southeast Atlantic (SE) and Oriental Northeast Atlantic (NOr) hydrographic regions of Brazil.

Suborder Radopoda Dumont and Silva-Briano, 1998

Family Chydoridae Dybowski and Grochowski, 1894 emend. Frey, 1967

Subfamily Chydorinae Dybowski and Grochowski, 1894 emend. Frey, 1967

Genus Chydorus Leach, 1816

Chydorus nitidulus ( Sars, 1901 )

(Fig. 3)

Figure 3.
Specimen of Chydorus nitidulus (Sars, 1901) from Camucim Forest Protected Area, Pernambuco, Brazil. a, Habitus of a female (Arrow-1: labral keel); b, postabdomen; c, valves (Arrow-2: denticle in the posteroventral corner).

Material examined. 1 ind. (CZ-UFRPE 18008), Camucim Forest Protected Area, São Lourenço da Mata, Pernambuco, 8°02'24.8"S 35°11'48.5"W (WGS84), 09 May 2018, colls. R.F. de Oliveira and F.A. Santos; 12 ind. (CZ-UFRPE 18010), 2 ind. (CZ-UFRPE 18034), Camucim Forest Protected Area, São Lourenço da Mata, Pernambuco, 8°02'18.2''S 35°12'2.97''W (WGS84), 09 and 11 May 2018, colls. R.F. de Oliveira and F.A. Santos.

Specimens. The specimens of C. nitidulus show characters similar to their latest descriptions (Elmoor-Loureiro, 1997). In Fig. 3a, the body structure of a parthenogenetic female is represented, with oval body and postabdomen exposed. Arrow indicates the naked and elongated labral keel, which is diagnostic for this species. Details of postabdomen are typical, showing terminal claw chitinized and curved, with two basal spines of different sizes (Fig. 3b). Valves have one denticle in the posteroventral corner (Fig. 3c).

Ecology and habitat. Parthenogenetic females of C. nitidulus were recorded in environments limnologically distinct from those of M. dumonti, although both species were collected in stations dominated by Lemna. The specimens sampled in the present study occurred in ponds with both degraded and preserved riparian vegetation, which show high turbidity (132 ± 96.55 NTU), low oxygenation (3.57 ± 2.73 mg L^-1) and low a-chlorophyll concentration (14.24 ± 13.76 µg L^-1).

Distribution. Chydorus nitidulus is a Neotropical species, previously recorded in Venezuela (Rey and Vásquez, 1886; Vásquez and Rey, 1989), Argentina (Paggi, 1972), Brazil (Elmoor-Loureiro, 1997), Mexico (Elías-Gutiérrez et al., 2006), and Colombia (Fuentes-Reinés, 2014; Fuentes-Reinés et al., 2019). In Brazil, this species was mainly recorded in the hydrographic regions of Amazonia (AM), Paraguay (PG), Paraná (PR), São Francisco (SF), East (AL), South (SA) and Southeast Atlantic (SE), and Tocantins/Araguaia (TA) (see Fig. 1 and Tab. 1, for references). Thus, this study expands the distribution of C. nitidulus to the Oriental Northeast Atlantic hydrographic region (NOr) and to Atlantic forest ponds in Northeastern Brazil.

DISCUSSION

In Northeastern Brazil, most studies on Cladocera were performed in large water bodies, such as reservoirs, rivers, and shallow lakes (Sousa et al., 2009; Soares and Elmoor-Loureiro, 2011; Medeiros and Melo Júnior, 2016; Cabral et al., 2020). This is in contrast with studies on smaller and temporary aquatic environments (e.g., ponds and pools), which are rare (Diniz et al., 2013; Melo and Medeiros, 2013). These latter ecosystems are numerous, heterogeneous, and important to conservation, because they are highly dynamic and hold highly specialized species (De Meester et al., 2005). Cladoceran species are very diversified in these habitats, because their structure and dynamics are affected by fluctuations in biotic and abiotic conditions (Crispim and Freitas, 2005; Diniz et al., 2013). However, this aquatic community is often threatened because temporary habitats are more susceptible to human impacts. Pollution, trampling by cattle, eutrophication, the introduction of exotic species, and deepening to a permanent state are the most common impacts (Wiliams and Hynes, 1977; De Meester et al., 2005).

This study fills a latitudinal gap in the distribution of M. dumonti between the tropical north and the subtropical southern hemispheres (Kotov et al., 2005; Farias et al., 2017). The previously disjointed distribution is attributed to its early description (Kotov et al., 2005) but also reveals how poorly studied the habitats are that this species inhabits (e.g., temporary ponds). This study records for the second time the occurrence of this cladoceran species in Brazil. On the other hand, although C. nitidulus has been recorded in a wide variety of aquatic habitats in Northeastern Brazil (Tab. 1), a similar situation occurs with this species, which has hitherto only had two records in temporary ponds (Diniz et al., 2013). With the inclusion of M. dumonti¸ this study expands to 73 the list of Cladocera species registered in Pernambuco State. The region now features four species of Moinidae and 43 of Chydoridae (Soares and Elmoor-Loureiro, 2011; Diniz et al., 2013; Sousa et al., 2015a; 2015b; Medeiros and Melo-Júnior, 2016; Medeiros et al., 2019; Diniz et al., 2020). Our results also reinforce the importance of performing further research and inventories in temporary environments to expand the knowledge about associated aquatic diversity, especially in the remnants of the Brazilian Atlantic Forest.

ACKNOWLEDGEMENTS

We thank the staff of the Tapacurá Ecological Station (UFRPE) for their support. We are grateful to Alan Pedro de Araújo (MSc.) and Rogério Ferreira de Oliveira (MSc.) (PPGE/UFRPE), for their support in the field. ILSM and FAS are supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

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• Zoobank:

  http://zoobank.org/urn:lsid:zoobank.org:pub:94F2CE9A-F77C-4A5A-BC90-E0CE7206545C

Publication Dates

• Publication in this collection
  06 Sept 2021
• Date of issue
  2021

History

• Received
  08 Feb 2021
• Accepted
  20 May 2021