Abstract
This study evaluated how the plasma steroid hormones testosterone (T) and 17β-estradiol (E2) are related to follicular development in regenerating females of the cururu stingray, Potamotrygon wallacei, during the rising water season of the middle Rio Negro basin. The relative weight of hepatic and ovarian tissues, as well as the morphological changes in the vitellogenic follicles, were related to the increase in the water level. Correlations between the maximum follicular diameter (MFD) and E2 and T levels suggest a concomitant action of these steroids in controlling follicular growth. These associations support the idea that the reproduction of this species is synchronous with the local hydrological cycle of the middle Rio Negro basin.
References
ANA (2021) Sistema de cota online. Cota online ANA. http://cotaonline.ana.gov.br/ConsultarDados.aspx. Accessed 05 June 2021.
Araújo MLG (1998) Biologia reprodutiva e pesca de Potamotrygon sp. C (Chondrichthyes, Potamotrygonidae), no médio rio Negro, Amazonas. Dissertation, Instituto Nacional de Pesquisas da Amazonia.
Araújo MLG, Charvet-Almeida P, Almeida MP, Pereira H (2004) Freshwater stingrays (Potamotrygonidae): status, conservation and challenges. CITES. https://cites.org/sites/default/files/common/com/ac/20/E20-inf-08.pdf. Accessed 05 June 2021.
Awruch CA (2013) Reproductive endocrinology in chondrichthyans: The present and the future. Gen Comp Endocrinol 192:60–70. https://doi.org/10.1016/j.ygcen.2013.05.021
Callard IP, Fileti LA, Koob TJ (1993) Ovarian steroid synthesis and the hormonal control of the elasmobranch reproductive tract. Environ Biol Fishes 38:175–185. https://doi.org/10.1007/BF00842914
Carvalho MR, Loboda TS, Silva JP (2016a) A new subfamily, Styracurinae, and new genus, Styracura, for Himantura schmardae (Werner, 1904) and Himantura pacifica (Beebe & Tee-Van, 1941) (Chondrichthyes: Myliobatiformes). Zootaxa 4175:201–221. https://doi.org/10.11646/zootaxa.4175.3.1
Carvalho MR, Rosa RS, Araújo MLG (2016b) A new species of Neotropical freshwater stingray (Chondrichthyes: Potamotrygonidae) from the Rio Negro, Amazonas, Brazil: The smallest species of Potamotrygon. Zootaxa 4107:566–586. https://doi.org/10.11646/zootaxa.4107.4.5
Charvet-Almeida P, Araújo MLG, Almeida MP (2005) Reproductive aspects of freshwater stingrays (Chondrichthyes: Potamotrygonidae) in the Brazilian Amazon Basin. J Northwest Atl Fish Sci 35:165–171. https://doi.org/10.2960/J.v35.m502
CPRM (2017) Monitoramento hidrológico, Boletim Nº. 49–08/12/2017. Serviço Geológico do Brasil. https://www.cprm.gov.br/sace/boletins/Amazonas/20171208_16-20171211%20-%20160537.pdf. Accessed 23 September 2021.
Dodd JM (1983) Reproduction in cartilaginous fishes (Chondrichthyes). In: Hoar WA, Randall DJ, Donaldson EM (eds) Fish Physiology Vol. IX A. Academic Press, New York, pp. 31–95.
Duncan WP, Shibuya A, Araújo MLG, Zuanon J (2016) Biologia e história natural de Potamotrygon wallacei (Carvalho, Rosa e Araújo, 2016) na bacia do Rio Negro, Amazônia Central, Brasil. In: Lasso CA, Rosa RS, Morales-Betancourt MA, Garrone-Neto D, Carvalho M (eds) XV. Rayas de agua dulce (Potamotrygonidae) de Suramérica. Parte II: Colombia, Brasil, Perú, Bolivia, Paraguay, Uruguay y Argentina. Serie Editorial Recursos Hidrobiológicos y Pesqueros Continentales de Colombia. Bogotá DC, pp. 289–302.
Fasano S, D’Antonio M, Pierantoni R, Chieffi G (1992) Plasma and follicular tissue steroid levels in the elasmobranch fish, Torpedo marmorata. Gen Comp Endocrinol 85:327–333. https://doi.org/10.1016/0016-6480(92)90017-E
Fujinami Y, Semba Y (2020) Non-lethal assessment of reproductive stage for female blue sharks Prionace glauca using sex steroid hormones. J Fish Biol 96:1501–1504. https://doi.org/10.1111/jfb.14312
Goergen G, Tatsch JD, Mendoza FRT, Valdés RH, Kannemberg C, Parcianello A, Valente F, Boiaski NT (2016) Hydroclimatic variability on the Rio Negro Watershed: a case study at Brazilian area. Ciênc Nat 38:376–382. https://doi.org/10.5902/2179460X20270
Goulding M, Carvalho ML, Ferreira EG (1988) Rio Negro, rich life in poor water. Amazonian diversity and foodchain ecology as seen through fish communities. SPB Academic Publishing. The Hague. 200p.
Hamlett WC, Koob TJ (1999) Female reproductive system. In: Hamlett WC (ed) Sharks, Skates and Rays: The Biology of Elasmobranch Fishes. Hopkins University Press London, Skates and Rays, pp 398–443
Hamlett WC, Ferri AG, Miglino MA (1992) Modes of Reproduction in the Elasmobranchs of Brazil. In: Hamlett WC (ed) Reproductive Biology of South American Vertebrates. Springer-Verlag, New York, pp 3–18
Hamlett WC, Jezior M, Spieler R (1999) Ultrastructural analysis of folliculogenesis in the ovary of the yellow spotted stingray, Urolophus jamaicensis. Ann Anat 181:159–172. https://doi.org/10.1016/S0940-9602(99)80003-X
ICES (2013) Report of the workshop on Sexual Maturity Staging of Elasmobranchs (WKMSEL). ICES CIEM. http://www.ices.dk/sites/pub/Publication%20Reports/Expert%20Group%20Report/acom/2012/WKMSEL/WKMSEL%202012.pdf. Accessed 05 June 2021.
Junk WJ, Bayley PB, Sparks RE (1989) The flood pulse concept in river-floodplain systems. Can J Fish Aquat Sci 106:110–127
Latrubesse EM, Franzinelli E (2005) The late Quaternary evolution of the Negro River, Amazon, Brazil: Implications for island and floodplain formation in large anabranching tropical systems. Geomorphology 70:372–397. https://doi.org/10.1016/j.geomorph.2005.02.014
Leenheer JA (1980) Origin and nature of humic substances in the waters of the Amazon River Basin. Acta Amaz 10(3):513–526. https://doi.org/10.1590/1809-43921980103513
Manire CA, Rasmussen LEL, Hess DL, Hueter RE (1995) Serum steroid hormones and the reproductive cycle of the female bonnethead shark, Sphyrna tiburo. Gen Comp Endocrinol 97:366–376. https://doi.org/10.1006/gcen.1995.1036
Marcon JL, Morales-Gamba RD, Barcellos JFM, Araujo MLG (2021) Sex steroid hormones and the associated morphological changes in the reproductive tract of free-living males of the cururu stingray Potamotrygon wallacei. Gen Comp Endocrinol 309:113786. https://doi.org/10.1016/j.ygcen.2021.113786
Moya AC, Wehitt A, Díaz-Andrade MC, Di-Giacomo EE, Galíndez EJ (2017) Female reproductive traits of a commercially exploited skate: Atlantoraja platana (Günther, 1880) (Chondrichthyes, Rajidae). Ovarian morphology, gametogenesis and microscopic verification of maturity criteria. Micron 101:232–240. https://doi.org/10.1016/j.micron.2017.08.001
Oliveira AT, Araújo MLG, Lemos JRG, Santos MQC, Pantoja-Lima J, Aride PHR, Tavares-Dias M, Marcon JL (2017) Ecophysiological interactions and water-related physicochemical parameters among freshwater stingrays. Braz J Biol 77:616–621. https://doi.org/10.1590/1519-6984.01816
Pratt JHL (1988) Elasmobranch gonad structure: A description and survey. Copeia 3:719–729. https://doi.org/10.2307/1445394
Pedreros-Sierra TM, Arrieta-Prieto DM, Mejía-Falla PA (2016) Reproductive system of females of the Magdalena river endemic stingray Potamotrygon magdalenae: Anatomical and functional aspects. J Morphol 277:680–697. https://doi.org/10.1002/jmor.20527
Prisco M, Romano R, Ricchiari L, Limatola E, Andreuccetti P (2002) An ultrastructural study on the vitellogenesis in the spotted ray Torpedo marmorata. Gen Comp Endocrinol 128:171–179. https://doi.org/10.1016/s0016-6480(02)00542-7
Prisco M, Valiante S, Romano M, Ricchiari L, Liguoro A, Laforgia V, Limatola E, Andreuccetti P (2004) Ovarian follicle cells in Torpedo marmorata synthesize vitellogenin. Mol Reprod Dev 67:424–429. https://doi.org/10.1002/mrd.20036
Prisco M, Valiante S, Di-Fiore MM, Raucci F, Del-Giudice G, Romano M, Laforgia V, Limatola E, Andreuccetti P (2008) Effect of 17β-estradiol and progesterone on vitellogenesis in the spotted ray Torpedo marmorata Risso 1810 (Elasmobranchii: Torpediniformes): Studies on females and on estrogen-treated males. Gen Comp Endocrinol 159:116–116. https://doi.org/10.1016/j.ygcen.2008.04.011
Rasmussen LEL, Gruber SH (1993) Serum concentrations of reproductively-related circulating steroid hormones in the free-ranging lemon shark, Negaprion brevirostris. Environ Biol Fishes 38:167–174. https://doi.org/10.1007/BF00842913
Snelson JFF, Rasmussen LEL, Johnson MR, Hess DL (1997) Serum concentrations of steroid hormones during reproduction in the Atlantic stingray, Dasyatis sabina. Gen Comp Endocrinol 108:67–79. https://doi.org/10.1006/gcen.1997.6949
Tricas TC, Maruska KP, Rasmussen LEL (2000) Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray. Gen Comp Endocrinol 118:209–225. https://doi.org/10.1006/gcen.2000.7466
Tsang PCW, Callard IP (1992) Regulation of ovarian steroidogenesis in vitro in the viviparous shark, Squalus Acanthias. J Exp Zool 261:97–104. https://doi.org/10.1002/jez.1402610111
Waltrick DS, Simpfendorfer CA, Awruch CA (2017) A review on the morphology of ovarian follicles in Elasmobranchs: a case study in Rhizoprionodon taylori. J Morphol 278:486–499. https://doi.org/10.1002/jmor.20644
Wourms JP (1977) Reproduction and development in Chondrichthyan. Am Zool 17:379–410. https://doi.org/10.1093/icb/17.2.379
Acknowledgements
Authors thank the professional fishers from Barcelos, Amazonas, for their support in collecting the wild P. wallacei females. To the Biomolecule Purification Laboratory, BIOTEC Multidisciplinary Support Center and Aya Sadahiro Ph.D. at the Federal University of Amazonas (UFAM) for their support in the immunoassay analyses. This investigation had prior authorization (SISBIO No. 18285–1) from the Chico Mendes Institute for Biodiversity Conservation (ICMBio) – Ministry of the Environment, and was conducted in accordance with the guidelines of the Ethics Committee for the Use of Animals in Research from the Federal University of Amazonas (Protocol CEUA/UFAM # 002/2017).
Funding
This work was financed by a grant from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) to JLM (process #48566/2013–0). A doctoral grant was provided to RDMG by the Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM, process # 003/2019 POSGREP).
Author information
Authors and Affiliations
Contributions
Ruben Dario Morales-Gamba conceptualized, conducted the fieldwork, conducted the morphological and hormonal analysis, analyzed the data, and wrote the draft manuscript. Maria Lúcia Góes de Araújo conceptualized and supervised the experiments, conducted the morphological analysis and interpretation of reproductive data. José Fernando Marques Barcellos conducted the morphological analysis and assisted with the data analysis. Jaydione Luiz Marcon conceptualized and supervised the experiments, provided the funding acquisition, conducted the fieldwork, and gave final approval for the version to be published. All authors contributed to reviewing and editing the manuscript.
Corresponding author
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Morales-Gamba, R.D., de Araújo, M.L.G., Barcellos, J.F. et al. Follicular growth and sex steroids in adult females of the endemic Amazonian freshwater stingray Potamotrygon wallacei (Chondrichthyes, Potamotrygonidae). Environ Biol Fish 104, 1665–1672 (2021). https://doi.org/10.1007/s10641-021-01191-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-021-01191-8