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Marine free-living nematodes in semiarid inland waters

Nematoda marinho de vida livre em águas continentais no semiárido

Fábio Lucas de Oliveira Barros Maria Cristina da Silva Francisco José Victor de Castro Miodeli Nogueira JúniorAbout the authors

Abstract:

Aim

This study reports the occurrence of five Nematoda genera previously considered as exclusively marine in inland waters.

Methods

Sediment samples were taken, weekly, during nine weeks, at a small spring at the Horto Florestal Olho D’Água da Bica, Cuité, PB, ca. 130 km away from the shoreline, between March and May 2016 and fixed in 4% formalin. Nematodes were sorted by manual elutriation through sieves with 0.5 and 0.045 mm and slides were prepared.

Results

The sediment was classified as coarse sand, with organic matter content ranging between 2.73 and 13.32%, temperature between 27-28°C and constant salinity of 6. From 315 nematodes were sampled among which 18 were from five genera previously thought to be exclusively marine were found. Bolbolaimus was the most common, found in 11.1% of the samples, followed by Gomphionema (3.7%), Rynchonema (7.4%), Prorynchonema (7.4%) e Sabatieria (3.7%), representing 5.7% from total of nematofauna. These genera are widely distributed worldwide, but had never been recorded from inland environments.

Conclusions

This study contributes with the distributional knowledge of free-living nematodes. From literature data, these genera are not restricted by low salinity, and can be found in estuarine and/or brackish water environments and body water with direct connection to the sea. In any case, the presence of marine genera in this region which is >130 km away from the nearest shoreline is noteworthy, highlighting the importance of studying nematodes from these poorly known semiarid water bodies. These new occurrences raise questionings about the dispersal mechanisms that certified the colonization of these nematodes in the semiarid.

Keywords:
meiofauna; nematofauna; distribution, taxonomy and ecology

Resumo:

Objetivo

Esse trabalho relata a ocorrência de gêneros de Nematoda, que eram previamente considerados restritos a ambientes marinhos, em águas continentais.

Métodos

Amostras de sedimentos foram coletadas semanalmente, durante nove semanas, entre março e maio de 2016 no Horto Florestal Olho D’Água da Bica, Cuité, PB, cerca de 130 km da região costeira mais próxima e fixados em formol 4%. Os Nematoda foram separados por elutriação manual através de peneira de malha de 0,5 e 0,045 mm e lâminas foram confeccionadas.

Resultados

O sedimento foi classificado como areia grossa, com teor de matéria orgânica variando entre 2,73 e 13,32%, temperatura entre 27-28°C e salinidade constante de 6. Dentre 315 nematoides coletados, 18 são de cinco gêneros marinhos. Bolbolaimus foi o mais frequente, presente em 11,1% das amostras, seguido de Gomphionema (3,7%), Rynchonema (7,4%), Prorynchonema (7,4%) e Sabatieria (3,7%), representando 5,7% do total da nematofauna. Esses gêneros têm ampla distribuição no mundo, mas não possuem registros prévios em ambientes continentais, sendo a primeira ocorrência nesse estudo.

Conclusões

Este trabalho contribui com o conhecimento da distribuição de Nematoda de vida livre. De acordo com os dados de literatura, esses gêneros não possuem restrições a baixas salinidades, sendo encontrados em regiões estuarinas e/ou águas salobras e também em corpos de água doce com conexão direta com o mar. Ainda assim, é notável a presença de gêneros marinhos há ~130 km de distância da costa, enfatizando a importância de estudos em diferentes corpos d’água no semiárido, permitindo questionar sobre quais mecanismos de dispersão permitiram esses indivíduos colonizar essa região.

Palavras-chave:
meiofauna; nematofauna; distribuição; taxonomia e ecologia

Free-living Nematoda are abundant in marine, freshwater and terrestrial environments (Bongers & Bongers, 1998BONGERS, T. and BONGERS, M. Functional diversity of nematodes. Applied Soil Ecology, 1998, 10(3), 239-251. http://dx.doi.org/10.1016/S0929-1393(98)00123-1.
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; Bhadury et al. 2006BHADURY, P., AUSTEN, M.C., BILTON, D.T., LAMBSHEAD, P.D., ROGERS, A.D. and SMERDON, G.R. Development and evaluation of a DNA-barcoding approach for the rapid identification of nematodes. Marine Ecology Progress Series, 2006, 320, 1-9. http://dx.doi.org/10.3354/meps320001.
http://dx.doi.org/10.3354/meps320001...
; Leduc & Rowden, 2018LEDUC, D. and ROWDEN, A.A. Nematode communities in sediments of the Kermadec trench, Southwest Pacific Ocean. Deep-sea Research. Part I, Oceanographic Research Papers, 2018, 134, 23-31. http://dx.doi.org/10.1016/j.dsr.2018.03.003.
http://dx.doi.org/10.1016/j.dsr.2018.03....
). There are around 30,000 free-living nematode species currently described, with appraisals suggesting from 1 to 100 million species to be described (Lambshead, 2003LAMBSHEAD, P.J.D. Marine nematode biodiversity. In: Z.X. CHEN, S.Y. CHEN and D.W. DICKSON, eds. Nematology: advances and perspectives. Nematode morphology, physiology and ecology. Wallingford: CABI Publishing, 2003, pp. 438-468.; Blaxter, 2011BLAXTER, M. Nematodes: the worm and its relatives. PLoS Biology, 2011, 9(4), 10. https://doi.org/10.1371/journal.pbio.1001050.
https://doi.org/10.1371/journal.pbio.100...
; Zhang, 2013ZHANG, Z.Q. Animal biodiversity: an update of classification and diversity in 2013. In: ZHANG, Z.Q., ed. Animal Biodiversity: An Outline of Higher-level Classification and Survey of Taxonomic Richness (Addenda). Zootaxa, 2013, 3703(1), 5-11. https://doi.org/10.11646/zootaxa.3703.1.3.
https://doi.org/10.11646/zootaxa.3703.1....
; Smythe et al., 2019SMYTHE, A.B., HOLOVACHOV, O. and KOCOT, K.M. Improved phylogenomic sampling of free-living nematodes enhances resolution of higher-level nematode phylogeny. BMC Evolutionary Biology, 2019, 19(1), 1-15.). Until de beginning of the last decade ~2270 genera from 256 families had been described worldwide (Hodda, 2011HODDA, M. Phylum Nematoda Cobb, 1932. In: ZHANG, Z.Q., ed. Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa, 2011, 3148, 63-95.), with 78 genera and ~220 species recorded from Brazil (Venekey, 2017VENEKEY, V. Updates on information about free-living marine nematodes in Brazil: new records and comments on problems in taxonomic studies. Zootaxa, 2017, 4337(1), 38-72. http://dx.doi.org/10.11646/zootaxa.4337.1.2. PMid:29242430.
http://dx.doi.org/10.11646/zootaxa.4337....
). Most of the studies dealing on aquatic free-living nematodes were performed on marine environments and inland ecosystems have been mostly neglected (Traunspurger et al., 2020TRAUNSPURGER, W., WILDEN, B. and MAJDI, N. An overview of meiofaunal and nematode distribution patterns in lake ecosystems differing in their trophic state. Hydrobiologia, 2020, 847, 2665–2679. http://dx.doi.org/ 10.1007/s10750-019-04092-1.
http://dx.doi.org/ 10.1007/s10750-019-04...
). Although the number of studies on continental nematodes is growing, they are concentrated on the northern hemisphere, mostly in Europe (Abebe et al., 2008ABEBE, E., DECRAEMER, W. and DE LEY, P. Global diversity of nematodes (Nematoda) in freshwater. Hidrobiologia, 2008, 595(1), 67-78. http://dx.doi.org/10.1007/s10750-007-9005-5.
http://dx.doi.org/10.1007/s10750-007-900...
; Traunspurger et al., 2020TRAUNSPURGER, W., WILDEN, B. and MAJDI, N. An overview of meiofaunal and nematode distribution patterns in lake ecosystems differing in their trophic state. Hydrobiologia, 2020, 847, 2665–2679. http://dx.doi.org/ 10.1007/s10750-019-04092-1.
http://dx.doi.org/ 10.1007/s10750-019-04...
). Studies dealing on inland water nematodes from Brazil are still very sparse, mostly available in grey literature with a few published papers (e.g., Lucena et al., 2015LUCENA, B.K.P., SILVA, M.C. and CASTRO, F.J.V. Nematode community of continental lakes with different concentrations of salts. Revista Nordestina de Zoologia, 2015, 9(1), 2-15.; Barros et al., 2020BARROS, F.L.O., SILVA, M.C., VIEIRA, A.A. and CASTRO, F.J.V. Freshwater nematofauna (Nematoda) in a semi-arid region. Revista Nordestina de Zoologia, 2020, 12(2), 1-14.; Pinto et al., 2021PINTO, T. K. O., NETTO, S. A., ESTEVES, A. M., CASTRO, F. J. V., NERES, P. F. and DA SILVA, M. C. Free-living freshwater nematodes from Brazil: checklist of genera and regional patterns of diversity. Nematology, 2021, 1-14. https://doi.org/10.1163/15685411-bja10100.
https://doi.org/10.1163/15685411-bja1010...
). Currently, there are 132 genera of freshwater nematodes record on Brazil (Pinto et al., 2021PINTO, T. K. O., NETTO, S. A., ESTEVES, A. M., CASTRO, F. J. V., NERES, P. F. and DA SILVA, M. C. Free-living freshwater nematodes from Brazil: checklist of genera and regional patterns of diversity. Nematology, 2021, 1-14. https://doi.org/10.1163/15685411-bja10100.
https://doi.org/10.1163/15685411-bja1010...
), but this number is certainly underestimated considering both the high nematode diversity (e.g., Zhang, 2013ZHANG, Z.Q. Animal biodiversity: an update of classification and diversity in 2013. In: ZHANG, Z.Q., ed. Animal Biodiversity: An Outline of Higher-level Classification and Survey of Taxonomic Richness (Addenda). Zootaxa, 2013, 3703(1), 5-11. https://doi.org/10.11646/zootaxa.3703.1.3.
https://doi.org/10.11646/zootaxa.3703.1....
) and the lack of studies. In the current study we report five nematode genera from inland waters which were previously known as exclusive from marine environments. These findings highlight the need of increasing the knowledge of the diversity of free-living nematodes from inland water bodies worldwide and particularly at Brazil.

The material was sampled between March and May 2016 in a permanent small spring at Horto Florestal Olho D’Água da Bica, at Cuité County (6º29’06”S; 36º09’24”W), Paraíba State, in the Brazilian semiarid, located ca. 130 km from the coastline. The reservoir has an area ~230 m2, with 2 m of maximum depth, and is preserved by the Campina Grande Federal University (Universidade Federal de Campina Grande, UFCG).

Weekly samplings were performed between 24 March and 12 May 2016 in the margin of the pond. At each of the nine weeks three replicate sediment samples were taken with a 7 cm2 corer 10 cm deep. The material sampled was immediately fixed in 4% formalin. In addition, sediment samples were taken and frozen to perform standard granulometric and organic matter analyses in the laboratory (Suguio, 1973SUGUIO, K. Introdução a sedimentologia. São Paulo: Edgard Bliicher, 1973, pp. 317.; Walkley & Black, 1934WALKLEY, A. and BLACK, I. A. An examination of the Degtjareff method for determining soil organic matter, and proposed modification of the chromic acid titration method. Soil Science, 1934, 37(1), 29-38. http://dx.doi.org/10.1097/00010694-193401000-00003.
http://dx.doi.org/10.1097/00010694-19340...
). Water temperature and salinity were measured using a digital (Alfakit, AT-160, Florianopolis, Brazil) and manual field refractomer, respectively. In the laboratory, the samples were manually elutriated in sieves with meshes of 0.5 and 0.045 mm. The material retained in the finer sieve was placed in Dollfus plates and taken to the compound microscope where all nematodes were sorted and permanent slides were made (following Cobb, 1917COBB, N.A. Notes on Nemas. Contribution to the Science of Nematology, 1917, 5, 117-128.). The slides were taken to the optical microscope and the genera were identified following mostly Platt & Warwick (1983)PLATT, H.M. and WARWICK, R.M. A synopsis of the free-living marine nematodes, part I. British enoplids. Cambridge: Cambridge University Press, 1983., Warwick et al. (1998)WARWICK, R.M., PLATT, H.M. and SOMERFIELD, P.J. Free-living marine nematodes. Part III. British Monhysterids. Synopses of the British Fauna (New Series). Shrewsbury: The Linnean Society of London and The Estuarine and Coastal Science Association, 1998, 296 p. and Zullini (2010)ZULLINI, A. Identification Manual for Freshwater Nematode Genera. Italian: Università di Milano Bicocca, 2010, 112 p.. Voucher slides with the genera reported here were deposited in the Coleção de Invertebrados Paulo Young (CIPY), from Paraíba Federal University (Universidade Federal da Paraíba – UFPB) – CIPY-Nema 5-9.

The organic matter content ranged from 2.73 and 13.32%, and sediment size from 0.8 to 0.97 mm being characterized as coarse sand (Suguio, 1973SUGUIO, K. Introdução a sedimentologia. São Paulo: Edgard Bliicher, 1973, pp. 317.; Walkley & Black, 1934WALKLEY, A. and BLACK, I. A. An examination of the Degtjareff method for determining soil organic matter, and proposed modification of the chromic acid titration method. Soil Science, 1934, 37(1), 29-38. http://dx.doi.org/10.1097/00010694-193401000-00003.
http://dx.doi.org/10.1097/00010694-19340...
). Temperature was nearly constant, between 27-28°C and salinity had constant values of 6. From 315 nematodes sampled, 18 belong to five genera previously considered as exclusively marine (Table 1), and will be detailed in this study.

Table 1
Free-living Nematoda genera reported in this study, their frequency of occurrence (FO; %), number of individuals sampled (Ind.) and environmental parameters of the samples containing them. MO = organic matter content (%); G = granulometry (mm); T = temperature (°C). Environmental parameters are presented as mean ± standard deviation whenever appropriate; D.N= deposit number.

1. Bolbolaimus Cobb, 1920

Bolbolaimus has a strongly annulated cuticle, sometimes ornamented with dots. Head not set-off. Cephalic setae close to the front end. Amphideal fovea unispiral or cryptospiral. Buccal cavity strongly sclerotized, with large dorsal tooth, denticles may be present. Pharynx with anterior peribuccal bulb and posterior oval bulb. Copulatory apparatus strongly sclerotized and with gubernacular apophyses directed dorsally or dorsocaudally (Tchesunov, 2014bTCHESUNOV, A.V. Order Desmodorida De Coninck, 1969. In: A. SCHMIDT-RAESA, ed. Handbook of Zoology: Gastrotricha, Cycloneuralia and Gnathifera. 2. ed. Hamburg-Germany: De Gruyter, 2014b, pp. 399-433.; Figure 1a).

Figure 1
Free-Living Nematode genera in the Semi-Arid region. a= Bolbolaimus, b= Gomphionema, c-d=Rynchonema, e=Prorynchonema, f= Sabatieria. Amp= Amphidio; B. cav= Buccal Cavity; Bulb= Shape of pharyngeal bulb; Spic= Spicule.

This genus has been recorded between 66°N and 26°S (Muthumbi & Vincx, 1999MUTHUMBI, A.W. and VINCX, M. Microlaimidae (Microlaimoidea: Nematoda) from the Indian Ocean: description of nine new and known species. Hydrobiologia, 1999, 397, 39-58. http://dx.doi.org/10.1023/A:1003686212934.
http://dx.doi.org/10.1023/A:100368621293...
; Kovalyev & Tchesunov, 2005KOVALYEV, S.V. and TCHESUNOV, A.V. Taxonomic review of microlaimids with description of five species from the White Sea (Nematoda: Chromadoria). Zoosystematica Rossica, 2005, 14(1), 1-16.; Hua et al., 2016HUA, E., MU, F., ZHANG, Z., YANG, S., ZHANG, T. and LI, J. Nematode community structure and diversity pattern in sandy beaches of Qingdao, China. Journal of Ocean University of China, 2016, 15(1), 33-40. http://dx.doi.org/10.1007/s11802-016-2686-5.
http://dx.doi.org/10.1007/s11802-016-268...
; Leduc, 2016LEDUC, D. One new genus and three new species of deep-sea nematodes (Nematoda: Microlaimidae) from the Southwest Pacific Ocean and Ross Sea. Zootaxa, 2016, 4079(2), 255-271. http://dx.doi.org/10.11646/zootaxa.4079.2.7. PMid:27396004.
http://dx.doi.org/10.11646/zootaxa.4079....
; Long et al., 2017LONG, P.K., GAGARIN, V.G., TU, N.D., PHUONG, N.T.X. and THANH, N.V. Bolbolaimus obesus sp. n. (Nematoda, Desmodorida) from Mangrove Thickets in the Tien Yen River Estuary, Vietnam. The Biological Bulletin, 2017, 44(8), 844-851. http://dx.doi.org/10.1134/S1062359017080064.
http://dx.doi.org/10.1134/S1062359017080...
). It currently has 11 valid species, all of them from marine environments (Bezerra et al., 2020BEZERRA, T.N., DECRAEMER, W., EISENDLE-FLÖCKNER, U., HODDA, M., HOLOVACHOV, O., LEDUC, D., MILJUTIN, D., MOKIEVSKY, V., PEÑA SANTIAGO, R., SHARMA, J., SMOL, N., TCHESUNOV, A., VENEKEY, V., ZHAO, Z. and VANREUSEL, A. Nemys: World Database of Nematodes [online]. 2020 [viewed 28 May 2020]. Available from: http://nemys.ugent.be
http://nemys.ugent.be...
), although it may also be found in estuarine waters in salinity between 7.0-7.5 (Long et al., 2017LONG, P.K., GAGARIN, V.G., TU, N.D., PHUONG, N.T.X. and THANH, N.V. Bolbolaimus obesus sp. n. (Nematoda, Desmodorida) from Mangrove Thickets in the Tien Yen River Estuary, Vietnam. The Biological Bulletin, 2017, 44(8), 844-851. http://dx.doi.org/10.1134/S1062359017080064.
http://dx.doi.org/10.1134/S1062359017080...
). This is the first record of Bolbolaimus from inland waters.

2. Gomphionema Wieser & Hopper, 1966

Gomphionema presents buccal cavity heavily cuticularized, consisting of an anterior concave chamber and a cylindroconoid posterior portion, and armed with a massive dorsal tooth not entering the cheilostoma; subventral teeth absent. Pharyngeal bulb large, “barrel-shaped”, occupying approximately one-third of the total pharyngeal length (Tchesunov, 2014aTCHESUNOV, A.V. Order Chromadorida Chitwood, 1933. In: A. SCHMIDT-RAESA, ed. Handbook of Zoology, Gastrotricha, Cycloneuralia and Gnathifera. 2. ed. Hamburg-Germany: De Gruyter, 2014a, pp. 467-486.; Figure 1b).

The family Ethmolaimidae is divided into two subfamilies Ethmolaiminae and Neotonchinae this latter encompassing Gomphionema (Bezerra et al., 2013BEZERRA, T.N., PAPE, E., HAUQUIER, F. and INGELS, J. New genus and two new species of the family Ethmolaimidae (Nematoda: Chromadorida), found in two different cold-seep. Zootaxa, 2013, 3692(1), 7-27.). This genus has a wide distribution, between 50°N and 90°S (Boucher & Gourbault, 1990BOUCHER, G. and GOURBAULT, N. Sublittoral meiofauna and diversity of nematode assemblages off Guadeloupe Islands (French West Indies). Bulletin of Marine Science, 1990, 47(2), 448-463.; Ndaro & Ólafsson, 1999NDARO, S.G. and ÓLAFSSON, E. Soft-bottom fauna with emphasis on nematode assemblage structure in a tropical intertidal lagoon in Zanzibar, eastern Africa: I. Spatial variability. Hydrobiologia, 1999, 405, 133-148.; Netto & Gallucci, 2003NETTO, S.A. and GALLUCCI, F. Meiofauna and macrofauna communities in a mangrove from the Island of Santa Catarina, South Brazil. Hydrobiologia, 2003, 505(1), 159-170.; Fisher & Sheaves, 2003FISHER, R. and SHEAVES, M.J. Community structure and spatial variability of marine nematodes in tropical Australian pioneer seagrass meadows. Hydrobiologia, 2003, 495(1-3), 143-158. http://dx.doi.org/10.1023/A:1025406624390.
http://dx.doi.org/10.1023/A:102540662439...
; Ingole & Singh, 2010INGOLE, B. and SINGH, R. Biodiversity and community structure of free-living marine nematodes from the Larsemann Ice Shelf, East Antarctica. Current Science, 2010, 99(10), 1413-1419.; Bezerra et al., 2013BEZERRA, T.N., PAPE, E., HAUQUIER, F. and INGELS, J. New genus and two new species of the family Ethmolaimidae (Nematoda: Chromadorida), found in two different cold-seep. Zootaxa, 2013, 3692(1), 7-27.; Pastor de Ward et al., 2015PASTOR DE WARD, C., LO RUSSO, V., VILLARES, G., MILANO, V., MIYASHIRO, L. and MAZZANTI, R. Free-living marine nematodes from San Julián Bay (Santa Cruz, Argentina). ZooKeys, 2015, 489, 133-144. http://dx.doi.org/10.3897/zookeys.489.7311. PMid:25878534.
http://dx.doi.org/10.3897/zookeys.489.73...
; Venekey & Melo, 2016VENEKEY, V. and MELO, T.P.G.D. Nematodes as indicators of shrimp farm impact on an amazonian estuary (Curuçá, Pará, Brazil). Brazilian Journal of Oceanography, 2016, 64(1), 75-87. http://dx.doi.org/10.1590/S1679-87592016108206401.
http://dx.doi.org/10.1590/S1679-87592016...
; Thai et al., 2017THAI, T.T., MY YEN, N.T., THO, N. and QUANG, N.X. Meiofauna in the mangrove–shrimp farms ponds, Ca Mau province. Vietnam Journal of Science and Technology, 2017, 55(3), 271. http://dx.doi.org/10.15625/2525-2518/55/3/8410.
http://dx.doi.org/10.15625/2525-2518/55/...
). There are records of the subfamily Ethmolaiminae in estuarine and inland waters, while the subfamily Neothonchinae was previously recorded only in marine waters (Bezerra et al., 2013BEZERRA, T.N., PAPE, E., HAUQUIER, F. and INGELS, J. New genus and two new species of the family Ethmolaimidae (Nematoda: Chromadorida), found in two different cold-seep. Zootaxa, 2013, 3692(1), 7-27.).

Gomphionema is typically found on marine (Semprucci et al., 2013SEMPRUCCI, F., COLANTONI, P., BALDELLI, G., SBROCCA, C., ROCCHI, M. and BALSAMO, M. Meiofauna associated with coral sediments in the Maldivian subtidal habitats (Indian Ocean). Marine Biodiversity, 2013, 43(3), 189-198. http://dx.doi.org/10.1007/s12526-013-0146-7.
http://dx.doi.org/10.1007/s12526-013-014...
), and brackish waters from estuaries and mangroves in salinity as low as 7 (Venekey & Melo, 2016VENEKEY, V. and MELO, T.P.G.D. Nematodes as indicators of shrimp farm impact on an amazonian estuary (Curuçá, Pará, Brazil). Brazilian Journal of Oceanography, 2016, 64(1), 75-87. http://dx.doi.org/10.1590/S1679-87592016108206401.
http://dx.doi.org/10.1590/S1679-87592016...
; Thai et al., 2017THAI, T.T., MY YEN, N.T., THO, N. and QUANG, N.X. Meiofauna in the mangrove–shrimp farms ponds, Ca Mau province. Vietnam Journal of Science and Technology, 2017, 55(3), 271. http://dx.doi.org/10.15625/2525-2518/55/3/8410.
http://dx.doi.org/10.15625/2525-2518/55/...
). This genus currently has five species described and still is poorly studied (Bezerra et al., 2020BEZERRA, T.N., DECRAEMER, W., EISENDLE-FLÖCKNER, U., HODDA, M., HOLOVACHOV, O., LEDUC, D., MILJUTIN, D., MOKIEVSKY, V., PEÑA SANTIAGO, R., SHARMA, J., SMOL, N., TCHESUNOV, A., VENEKEY, V., ZHAO, Z. and VANREUSEL, A. Nemys: World Database of Nematodes [online]. 2020 [viewed 28 May 2020]. Available from: http://nemys.ugent.be
http://nemys.ugent.be...
). Both the genus Gomphionema and the subfamily Neothonchinae were not previously found in inland waters with this study being the first such record.

3. Rhynchonema Cobb, 1920

Rynchonema presents cuticle coarsely striated. Amphids placed over or very close to the end of the buccal tube. Buccal cavity in two parts; short anterior chamber, at the level of cephalic setae, narrow tubular part extending along the cervical region. Male with two testes. Spicules short and arcuate. Tail conical (Fonseca & Bezerra, 2014FONSECA, G. and BEZERRA, T.N. Order Monhysterida Filipjev, 1929. In: A. SCHMIDT-RAESA, ed. Handbook of Zoology: Gastrotricha, Cycloneuralia and Gnathifera. 2nd ed. Hamburg-Germany: De Gruyter, 2014, pp. 435-465.; Figure 1cd).

Rhynchonema has been found between 18-36°N and 0-40°S (Jesús-Navarrete, 2003JESÚS-NAVARRETE, A. Diversity of nematoda in a Caribbean atoll: Banco Chinchorro, Mexico. Bulletin of Marine Science, 2003, 73(1), 47-56.; Leduc et al., 2012LEDUC, D., ROWDEN, A.A., BOWDEN, D.A., NODDER, S.D., PROBERT, P.K., PILDITCH, C.A., DUINEVELD, G.C.A. and WITBAARD, R. Nematode beta diversity on the continental slope of New Zealand: spatial patterns and environmental drivers. Marine Ecology Progress Series, 2012, 454, 37-52. http://dx.doi.org/10.3354/meps09690.
http://dx.doi.org/10.3354/meps09690...
; Sandulli et al., 2015SANDULLI, R., MILJUTIN, D., ANGELETTI, L. and TAVIANI, M. Meiobenthos and nematode assemblages from different deep-sea habitats of the Strait of Sicily (Central Mediterranean Sea). Mediterranean Marine Science, 2015, 16(2), 402-412. http://dx.doi.org/10.12681/mms.1145.
http://dx.doi.org/10.12681/mms.1145...
; Bezerra et al., 2014BEZERRA, T.N., SMOL, N. and VINCX, M. Two new species of Rhynchonema Cobb, 1920 from a Brazilian sandy beach. Marine Biodiversity, 2014, 44(3), 343-365. http://dx.doi.org/10.1007/s12526-014-0223-6.
http://dx.doi.org/10.1007/s12526-014-022...
; Tu & Gagarin, 2017TU, N.D. and GAGARIN, V.G. Free-living nematodes from mangrove forest in the Yên River estuary (Vietnam). Inland Water Biology, 2017, 10(3), 266-274. http://dx.doi.org/10.1134/S1995082917030129.
http://dx.doi.org/10.1134/S1995082917030...
), and was reported from deep seawaters between 750 and 6300 m depth (Vanhove et al., 2004VANHOVE, S., VERMEEREN, H. and VANREUSEL, A. Meiofauna towards the South Sandwich Trench (750–6300 m), focus on nematodes. Deep-sea Research. Part II, Topical Studies in Oceanography, 2004, 51(14-16), 1665-1687. http://dx.doi.org/10.1016/j.dsr2.2004.06.029.
http://dx.doi.org/10.1016/j.dsr2.2004.06...
). Rynchonema was also reported from estuarine brackish waters with low salinity between 4.5-6.0 (Tu & Gagarin, 2017TU, N.D. and GAGARIN, V.G. Free-living nematodes from mangrove forest in the Yên River estuary (Vietnam). Inland Water Biology, 2017, 10(3), 266-274. http://dx.doi.org/10.1134/S1995082917030129.
http://dx.doi.org/10.1134/S1995082917030...
).

4. Prorhynchonema Gourbault, 1982

Prorhynchonema possess buccal cavity in two parts; anterior short, at level of cephalic setae, posterior tubular, restricted to the anterior part of the cervical region. Amphids circular, placed well posterior to the end of buccal tube. Spicules short and arcuate. Tail conical (Gourbault, 1982GOURBAULT, N. Nematodes marins de Guadeloupe. I. Xyalidae nouveaux des genres Rhynchonema Cobb et Prorhynchonema nov. gen. Bulletin du Muséum National d’Histoire Naturelle, 1982, 4, 1-2.; Figure 1e).

Prorhynchonema has been recorded at 16°N (Gourbault, 1982GOURBAULT, N. Nematodes marins de Guadeloupe. I. Xyalidae nouveaux des genres Rhynchonema Cobb et Prorhynchonema nov. gen. Bulletin du Muséum National d’Histoire Naturelle, 1982, 4, 1-2.) and 0-80ºS (De Broyer et al., 2007DE BROYER, C., BOUQUEGNEAU, J. M., DAUBY, P., DE RIDDER, C. and VANREUSEL, A. Biodiversity of three representative groups of the Antarctic Zoobenthos: Comparative structure, distribution and function (BIANZO), Brussels: Belgian Science Policy, 2007.; Venekey et al., 2010VENEKEY, V., FONSECA-GENEVOIS, V. and SANTOS, P.J. Biodiversity of free-living marine nematodes on the coast of Brazil: a review. Zootaxa, 2010, 2568(1), 39-66. http://dx.doi.org/10.11646/zootaxa.2568.1.2.
http://dx.doi.org/10.11646/zootaxa.2568....
) and was reported from deep waters between 750 and 6300 m depth (Vanhove et al., 2004VANHOVE, S., VERMEEREN, H. and VANREUSEL, A. Meiofauna towards the South Sandwich Trench (750–6300 m), focus on nematodes. Deep-sea Research. Part II, Topical Studies in Oceanography, 2004, 51(14-16), 1665-1687. http://dx.doi.org/10.1016/j.dsr2.2004.06.029.
http://dx.doi.org/10.1016/j.dsr2.2004.06...
). Prorhynchonema in estuarine waters with salinity as low as 10 (Tilbert, 2017TILBERT, S. Diversidade e estrutura da nematofauna em regiões estuarinas tropicais (~7ºS) [Dissertação de Mestrado. Mestrado em Ciências Biológicas]. João Pessoa: Universidade Federal da Paraíba, 2017.). None of these genera had been previously recorded in inland waters with this study representing the first record.

5. Sabatieria Rouville, 1903

The three individuals belonging to the genus Sabatieria were identified by the cuticle striated or with transverse punctuation, lateral differentiation as larger regular or irregular punctuations may occur. Anterior sensilla arranged in three crowns. Cephalic setae longer than the outer labial. Anterior portion of buccal cavity globular to cup-shaped, posterior portion narrow as a collapsed tube, weakly sclerotized; sometimes with small projections of the wall at the border between the two portions. Male excretory system with two additional uninucleate subventral gland cells far behind the cardia. Spicules usually enlarged proximally, apophyses usually directed dorsocaudally or caudally (Figure 1f). All these characteristics are consistent with those described in the review of Platt (1985)PLATT, H.M. The free-living marine nematodes genus Sabatieria (Nematoda: Comesomatidae). Taxonomic revision and pictorial keys. Zoological Journal of the Linnean Society, 1985, 83(1), 27-28. http://dx.doi.org/10.1111/j.1096-3642.1985.tb00872.x.
http://dx.doi.org/10.1111/j.1096-3642.19...
.

This genus is widely distributed worldwide, between 50ºN and 50ºS (Chen & Vincx, 1999CHEN, G. and VINCX, M. Nematodes from the Strait of Magellan and the Beagle Channel (Chile): the genus Sabatieria (Comesomatidae: Nematoda) with the description of Sabatieria coomansi n. sp. Hydrobiologia, 1999, 405, 95-115. http://dx.doi.org/10.1023/A:1003752619953.
http://dx.doi.org/10.1023/A:100375261995...
; Pastor De Ward, 2003PASTOR DE WARD, C.T. Two new species of Sabatieria (Nematoda, Comesomatidae) from Golfo Nuevo, Chubut (Argentina). Zootaxa, 2003, 172(1), 1-12. http://dx.doi.org/10.11646/zootaxa.172.1.1.
http://dx.doi.org/10.11646/zootaxa.172.1...
; Botelho et al., 2007BOTELHO, A.P., DA SILVA, M.C., ESTEVES, A.M. and FONSÊCA-GENEVOIS, V. Four new species of Sabatieria Rouville, 1903 (Nematoda, Comesomatidae) from the Continental Slope of Atlantic Southeast. Zootaxa, 2007, 1402(1), 39-57. http://dx.doi.org/10.11646/zootaxa.1402.3.
http://dx.doi.org/10.11646/zootaxa.1402....
; Gagarin & Nguyen, 2008GAGARIN, V.G. and NGUYEN, V.T. A new genus and three new species of free-living Nematodes from mangroves of the Red river estuary, Vietnam. Journal of Biology, 2008, 30, 3-11.; Ansari et al., 2012ANSARI, K.G.M.T., LYLA, P.S. and AJMAL KHAN, S. New records of free-living marine nematodes (Nematoda: Enoplida) from Indian waters. Journal of the Marine Biological Association of India, 2012, 54(2), 5-11.; Leduc et al., 2012LEDUC, D., ROWDEN, A.A., BOWDEN, D.A., NODDER, S.D., PROBERT, P.K., PILDITCH, C.A., DUINEVELD, G.C.A. and WITBAARD, R. Nematode beta diversity on the continental slope of New Zealand: spatial patterns and environmental drivers. Marine Ecology Progress Series, 2012, 454, 37-52. http://dx.doi.org/10.3354/meps09690.
http://dx.doi.org/10.3354/meps09690...
). It has been commonly found on marine muddy sediments where it is frequently abundant (Yang et al., 2019YANG, P., GUO, Y., CHEN, Y. and LIN, R. Four new free-living marine nematode species (Sabatieria) from the Chukchi Sea. Zootaxa, 2019, 4646(1), zootaxa.4646.1.2. http://dx.doi.org/10.11646/zootaxa.4646.1.2. PMid:31717025.
http://dx.doi.org/10.11646/zootaxa.4646....
). Sabatieria is commonly amongst the dominant nematode genera on marine environments such as deep water (Ott et al., 1991OTT, J.A., NOVAK, R., SCHIEMER, F. HENTSCHEL, U., NEBELSICK, M. and POLZ, M. Tackling the Sulfide Gradient: A Novel Strategy Involving Marine Nematodes and Chemoautotrophic Ectosymbionts. Marine Ecology (Berlin), 1991, 12(3), 261-279. http://dx.doi.org/10.1111/j.1439-0485.1991.tb00258.x.
http://dx.doi.org/10.1111/j.1439-0485.19...
), oceanic islands, estuaries, sand beaches and continental shelf (Vanreusel et al., 2010VANREUSEL, A., FONSECA, G., DANOVARO, R., DA SILVA, M.C., ESTEVES, A.M., FERRERO, T., GAD, G., GALTSOVA, V., GAMBI, C., DA FONSÊCA GENEVOIS, V., INGELS, J., INGOLE, B., LAMPADARIOU, N., MERCKX, B., MILJUTIN, D., MILJUTINA, M., MUTHUMBI, A., NETTO, S., PORTNOVA, D., RADZIEJEWSKA, T., RAES, M., TCHESUNOV, A., VANAVERBEKE, J., VAN GAEVER, S., VENEKEY, V., BEZERRA, T.N., FLINT, H., COPLEY, J., PAPE, E., ZEPPILLI, D., MARTINEZ, P.A. and GALERON, J. The contribution of deep-sea macrohabitat heterogeneity to global nematode diversity. Marine Ecology (Berlin), 2010, 31(1), 6-20. http://dx.doi.org/10.1111/j.1439-0485.2009.00352.x.
http://dx.doi.org/10.1111/j.1439-0485.20...
; Venekey et al., 2010VENEKEY, V., FONSECA-GENEVOIS, V. and SANTOS, P.J. Biodiversity of free-living marine nematodes on the coast of Brazil: a review. Zootaxa, 2010, 2568(1), 39-66. http://dx.doi.org/10.11646/zootaxa.2568.1.2.
http://dx.doi.org/10.11646/zootaxa.2568....
). This genus has been found with salinity down to 1 (Adão et al., 2009ADÃO, H., ALVES, A.S., PATRÍCIO, J., NETO, J.M., COSTA, M.J. and MARQUES, J.C. Spatial distribution of subtidal Nematoda communities along the salinity gradient in southern European estuaries. Acta Oecologica, 2009, 35(2), 287-300. http://dx.doi.org/10.1016/j.actao.2008.11.007.
http://dx.doi.org/10.1016/j.actao.2008.1...
), and recently recorded inside the São Francisco River (NE Brazil) relatively close (<20 km) and with direct connection to the sea (Pinto et al., 2021PINTO, T. K. O., NETTO, S. A., ESTEVES, A. M., CASTRO, F. J. V., NERES, P. F. and DA SILVA, M. C. Free-living freshwater nematodes from Brazil: checklist of genera and regional patterns of diversity. Nematology, 2021, 1-14. https://doi.org/10.1163/15685411-bja10100.
https://doi.org/10.1163/15685411-bja1010...
). The current record emphasizes its presence on freshwater >100 km away from the coast in a body of water completely independent from the sea.

6. Final remarks

Apart from the five genera reported here, Pseudosteneria and Odontophoroides also were previously thought to be exclusive from marine environments but have been reported in the Brazilian semiarid (Lucena et al., 2015LUCENA, B.K.P., SILVA, M.C. and CASTRO, F.J.V. Nematode community of continental lakes with different concentrations of salts. Revista Nordestina de Zoologia, 2015, 9(1), 2-15.). It is noteworthy the presence of many marine genera in closed body of waters of this region which is >130 km away from the nearest shoreline. All these genera are frequently found in estuarine brackish waters with low salinity (Adão et al., 2009ADÃO, H., ALVES, A.S., PATRÍCIO, J., NETO, J.M., COSTA, M.J. and MARQUES, J.C. Spatial distribution of subtidal Nematoda communities along the salinity gradient in southern European estuaries. Acta Oecologica, 2009, 35(2), 287-300. http://dx.doi.org/10.1016/j.actao.2008.11.007.
http://dx.doi.org/10.1016/j.actao.2008.1...
; Long et al., 2017LONG, P.K., GAGARIN, V.G., TU, N.D., PHUONG, N.T.X. and THANH, N.V. Bolbolaimus obesus sp. n. (Nematoda, Desmodorida) from Mangrove Thickets in the Tien Yen River Estuary, Vietnam. The Biological Bulletin, 2017, 44(8), 844-851. http://dx.doi.org/10.1134/S1062359017080064.
http://dx.doi.org/10.1134/S1062359017080...
; Tu & Gagarin, 2017TU, N.D. and GAGARIN, V.G. Free-living nematodes from mangrove forest in the Yên River estuary (Vietnam). Inland Water Biology, 2017, 10(3), 266-274. http://dx.doi.org/10.1134/S1995082917030129.
http://dx.doi.org/10.1134/S1995082917030...
). Consequently, the saline condition in many of the semiarid water bodies and inland freshwater closer seawater (6 in this study; 19 in Lucena et al., 2015LUCENA, B.K.P., SILVA, M.C. and CASTRO, F.J.V. Nematode community of continental lakes with different concentrations of salts. Revista Nordestina de Zoologia, 2015, 9(1), 2-15.; and <0.5 in Pinto et al., 2021PINTO, T. K. O., NETTO, S. A., ESTEVES, A. M., CASTRO, F. J. V., NERES, P. F. and DA SILVA, M. C. Free-living freshwater nematodes from Brazil: checklist of genera and regional patterns of diversity. Nematology, 2021, 1-14. https://doi.org/10.1163/15685411-bja10100.
https://doi.org/10.1163/15685411-bja1010...
) may not be a restrictive factor to the survival of these nematode genera. These observations raise questionings about the dispersal mechanisms of these tiny organisms and highlight the importance of studying nematodes from different semiarid water bodies. Further taxonomic studies with identification down to the species level will be important to test for endemism of these Nematoda from the Brazilian semiarid water bodies.

Acknowledgements

This study was part of the bachelorship dissertation of the first author which received support from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) 88887.475400/2020-00. Also, the authors thank Dr. Márcio Frazão Chaves for helping with the photographs, and to Dra. Jessica Prata for the help with depositing the voucher slides.

  • Cite as: Barros, F. L. O., Silva, M. C., Castro, F. J. V. and Nogueira Júnior, M. N. Marine free-living nematodes in semiarid inland waters. Acta Limnologica Brasiliensia, 2021, vol. 33, e15.

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Edited by

Associate Editors: Irineu Bianchini Junior, Antonio Fernando Monteiro Camargo.

Publication Dates

  • Publication in this collection
    14 June 2021
  • Date of issue
    2021

History

  • Received
    25 June 2020
  • Accepted
    21 May 2021
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