Skip to main content

Advertisement

Log in

Trends and seasonality of the occurrence of hatched egg capsules of Rioraja agassizi (Müller & Henle 1841) (Chondrichthyes: Rajiformes) in a South Brazilian beach, Southwestern Atlantic Ocean

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

The Rio skate Rioraja agassizi is endemic to coastal waters of the Western South Atlantic. The species is common in the coasts of Argentina, Uruguay and Brazil. Previous studies performed in South Brazil, demonstrated that its hatched egg capsules are the most abundant among the co-occurring species. The aim of this study was to assess seasonality in the monthly frequency of egg capsules of R. agassizi at Praia do Cassino (33°07′34″S 52°38′22″W/ 33.126080°S 52.639327°W), southernmost coast of Brazil, over a two-year sampling. The egg capsules were manually collected from the edge of the beach in a belt transect of 1 km long and ca. 0.1 km width, on a weekly basis. After the collections, the capsules were taken to the laboratory for identification at the species level and morphometric measurements. To study the seasonality in the oviposition in R agassizi, data were analyzed monthly, seasonally and annually; accordingly, the data were expressed as non-parametric and heterogeneous, thus, statistical tests were applied to verify trends, significant differences, and descriptive parameters within each scale. In the annual and interannual data, there were statistically significant differences and trends between the sampling periods. Thus, these series of data collected are in fact random and the values demonstrated a randomness in the study site. As for the seasonal data, at least one of the seasons has a significantly different distribution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The data used in this work belong to the research project ‘‘Phylogenetic relationships, morphological, diversity and seasonal occurrence of skate egg cases (Chondrichthyes: Batoidea) from Southern Brazil’’, with registration under code PESQ 862 at FURG and are available under reasonable request to the corresponding author.

References

  • Bradley JV (1968) Distribution Free Statistical Tests. Prentice Hall, Englewood Cliffs

    Google Scholar 

  • Castro JI (2009) Observations on the reproductive cycles of some viviparous North American sharks. Aqua Int J Ichthyol 15:205–222

    Google Scholar 

  • Colonello JH (2009) Ecología reproductiva de tres batoideos (Chondrichthyes): Atlantoraja castelnaui (Rajidae), Rioraja agassizii (Rajidae) y Zapteryx brevirostris (Rhinobatidae). Implicancias de distintas estrategias adaptativas en un escenario de explotación intensiva. PhD Thesis, Universidad Nacional de La Plata, Argentina

  • Colonello JH, García ML, Lasta CA (2007) Reproductive biology of Rioraja agassizi from the coastal southwestern Atlantic ecosystem between northern Uruguay (34° S) and northern Argentina (42° S). In: Ebert DA, Sulikowski JA (eds) Biology of Skates. Springer, Dordrecht, pp 171–178

    Google Scholar 

  • Compagno LJV (2005) Checklist of living Chondrichthyes. In: Hamlett WC (ed) Reproductive biology and phylogeny of Chondrichthyes, Sharks, Batoids and Chimaeras. Science Publishers, Inc., Enfield (NH), pp 503–548

    Google Scholar 

  • Concha F, Hernández S, Oddone MC (2009) Egg capsules of the Raspthorn Sandskate, Psammobatis scobina (Philippi, 1857) (Rajiformes, Rajidae). Rev Biol Mar Oceanogr 44:253–256 (https://www.redalyc.org/articulo.oa?id=47911450026)

    Article  Google Scholar 

  • Concha F, Morales N, Larraguibel J (2013) Egg capsules of the filetail fanskate Sympterygia lima (Poeppig 1835) (Rajiformes, Arhynchobatidae) from the southeastern Pacific Ocean, with observations on captive egg-laying. Ichthyol Res 60:203–208. https://doi.org/10.1007/s10228-012-0333-8

    Article  Google Scholar 

  • Cordeiro LDOA, Oddone MC (2019) Diversity and abundance of hatched skate (Chondrichthyes: Elasmobranchii: Rajoidei) egg cases at Cassino Beach, Rio Grande do Sul, Brazil. Bol Soc Zool Urug 28:38–58. https://doi.org/10.26462/28.2.1

  • Ebert DA, Davis CD (2007) Descriptions of skate egg cases (Chondrichthyes: Rajiformes: Rajoidei) from the eastern North Pacific. Zootaxa 1393:1–18

    Article  Google Scholar 

  • Figueiredo LL (1977) Manual de peixes marinhos do Sudeste do Brasil. Introdução a cações, raias e quimeras. Museu de Zoologia, Universidade de São Paulo

  • Fischer J, Licht M, Kriwet J, Schneider JW, Buchwitz M, Bartsch P (2014) Egg capsule morphology provides new information about the interrelationships of chondrichthyan fishes. J Syst Palaeontol 12:389–399. https://doi.org/10.1080/14772019.2012.762061

    Article  Google Scholar 

  • Gilbert RO (1987) Statistical methods for environmental pollution monitoring. Van Nostrand Reinhold, New York

    Google Scholar 

  • Gomes UL, Signori CN, Gadig OBF, Santos HRS (2010) Guia para identificação de tubarões e raias do Rio de Janeiro. Technical Books, Rio de Janeiro

    Google Scholar 

  • Gordon CA, Hood AR, Ellis JR (2016) Descriptions and revised key to the egg cases of the skates (Rajiformes: Rajidae) and catsharks (Carcharhiniformes: Scyliorhinidae) of the British Isles. Zootaxa 4150:255–280. https://doi.org/10.11646/zootaxa.4150.3.2

    Article  PubMed  Google Scholar 

  • Hamlett WC, Koob TJ (1999) Female reproductive system. In: Hamlett WC (ed) Sharks, Skates, and Rays. The Biology of Elasmobranch Fishes. Johns Hopkins University Press, Baltimore, pp 398–443

    Chapter  Google Scholar 

  • Hammer Ø, Harper D, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 9 pp https://palaeoelectronica.org/2001_1/past/issue1_01.htm. Accessed 18 February 2021

  • Holden MJ (1975) The fecundity of Raja clavata in British waters. ICES J Mar Sci 36:110–118. https://doi.org/10.1093/icesjms/36.2.110

    Article  Google Scholar 

  • Hubbs CL, Ishiyama R (1968) Methods for the taxonomic study and description of skates (Rajidae). Copeia 1968:483–491. https://doi.org/10.2307/1442016

    Article  Google Scholar 

  • ICMBio (2018) Livro Vermelho da Fauna Brasileira Ameaçada de Extinção: Volume VI –Peixes / 1st. ed. – Brasília, DF: ICMBio/MMA, 2018. https://www.gov.br/icmbio/pt-br/centrais-de-conteudo/publicacoes/publicacoes-diversas/livro_vermelho_2018_vol6.pdf. Accessed 28 April 2023

  • Ishihara H, Treloar M, Bor PH, Senou H, Jeong CH (2012) The comparative morphology of skate egg capsules (Chondrichthyes: Elasmobranchii: Rajiformes). Bull Kanagawa Prefect Mus Nat Sci 41:9–25

    Google Scholar 

  • Ishiyama R (1950) Studies on the rays and skates belonging to the family Rajidae, found in Japan and adjacent regions. Jap J Ichthyol 1:30–36. https://doi.org/10.11369/jji1950.1.30

  • Ishiyama R (1958) Observations on the eggs-capsules of skates of the family Rajidae, found in Japan and its adjacent waters. Bull Mus Comp Zool 118:1–24

    Google Scholar 

  • Jañez JA, Sueiro MC (2007) Size at hatching and incubation period of Sympterygia bonapartii (Müller & Henle, 1841) (Chondrichthyes, Rajidae) bred in captivity at the Temaiken Aquarium. J Fish Biol 70:648–650. https://doi.org/10.1111/j.1095-8649.2007.01332.x

    Article  Google Scholar 

  • Jañez JA, Meijide FJ, Lucifora LO, Abraham C, Argemi F (2018). Growth and reproduction in captivity unveils remarkable life-history plasticity in the smallnose fanskate, Sympterygia bonapartii (Chondrichthyes: Rajiformes). Neotrop Ichthyol 16 (4). https://doi.org/10.1590/1982-0224-20180013

  • Kang HW, Jo YR, Kang DY, Jeong GS, Jo HS (2013) Spawning characteristics and artificial hatching of female mottled skate, Beringraja pulchra in the west coast of Korea. Dev Reprod 17:247–255. https://doi.org/10.12717/DR.2013.17.3.247

    Article  PubMed  PubMed Central  Google Scholar 

  • Kendall MG (1975) Rank correlation methods. Charles Griffin, London

    Google Scholar 

  • Levene H (1960) Robust tests for equality of variances. In: Olkin I (ed) Contributions to Probability and Statistics. Stanford University Press, Palo Alto, pp 278–292

    Google Scholar 

  • Love MS, Schroeder DM, Snook L, York A, Cochrane G (2008) All their eggs in one basket: a rocky reef nursery for the longnose skate (Raja rhina Jordan & Gilbert, 1880) in the Southern California Bight. Fish Bull 106:471–475

    Google Scholar 

  • Mabragaña E, Cousseau MB (2004) Reproductive biology of two sympatric skates in the south-west Atlantic: Psammobatis rudis and Psammobatis normani. J Fish Biol 65:559–573. https://doi.org/10.1111/j.0022-1112.2004.00473.x

    Article  Google Scholar 

  • Mabragaña E, Lucifora LO, Massan AM (2002) The reproductive ecology and abundance of Symptevygia bonapartii endemic to the south-west Atlantic. J Fish Biol 60:951–967. https://doi.org/10.1111/j.1095-8649.2002.tb02420.x

    Article  Google Scholar 

  • Mabragaña E, Lucifora LO, Corbo MDL, Astarloa JMD (2015) Seasonal reproductive biology of the bignose fanskate Sympterygia acuta (Chondrichthyes, Rajidae). Estuar Coasts 38:1466–1476. https://doi.org/10.1007/s12237-014-9888-0

    Article  CAS  Google Scholar 

  • Méndez-Abarca F, Méndez CF, Reyes RA, Vargas HA, Aragón GA (2013) Fish species involved in mass washed up eggs in Chinchorro beach, Arica-Chile during the period of one year. Rev Zool 24:27–29

    Google Scholar 

  • Musick JA, Ellis JK (2005) Reproductive evolution of Chondrichthyans. In: Hamlett WC (ed) Reproductive biology and phylogeny of Chondrichthyes: Sharks, Batoids and Chimaeras. CRC Press, Endfield, pp 45–80

    Google Scholar 

  • Oddone MC, Vooren CM (2002) Egg-cases and size at hatching of Sympterygia acuta in the south-western Atlantic. J Fish Biol 61:858–861. https://doi.org/10.1111/j.1095-8649.2002.tb00919.x

    Article  Google Scholar 

  • Oddone MC, Vooren CM (2008) Comparative morphology and identification of egg capsules of skate species of the genera Atlantoraja Menni, 1972, Rioraja Whitley, 1939 and Sympterygia Müller & Henle, 1837. Arq Ciênc Mar 41:5–13. DOI: https://doi.org/10.32360/acmar.v41i2.6056

  • Oddone MC, Amorim AF, Mancini PL, Norbis W, Velasco G (2007) The reproductive biology and cycle of Rioraja agassizi (Müller and Henle, 1841) (Chondrichthyes: Rajidae) in southeastern Brazil, SW Atlantic Ocean. Sci Mar 71:593–604

  • Oddone MC, Marçal AS, Vooren CM (2004) Egg capsules of Atlantoraja cyclophora (Regan, 1903) and A. platana (Günther, 1880) (Pisces, Elasmobranchii, Rajidae). Zootaxa 426:1–4

    Article  Google Scholar 

  • Pollom R, Barreto R, Charvet P, Cuevas JM, Faria V, Herman K, Marcante F, Montealegre-Quijano S, Motta F, Paesch L, Rincon G (2020) Rioraja agassizii. The IUCN Red List of Threatened Species 2020: e.T63109A3118640. https://doi.org/10.2305/IUCN.UK.2020-3.RLTS.T63109A3118640.en. Accessed 05 April 2023.

  • Schmöle S, Brown M, Witteveen M (2020) All washed up: Spatial and temporal variation in the wash-up and fate of Chondrichthyan egg cases along a section of the Garden Route, South Africa. Afr J Mar Sci 42:141–149. https://doi.org/10.2989/1814232X.2020.1760936

    Article  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611. https://doi.org/10.2307/2333709

    Article  Google Scholar 

  • Smith C, Griffiths C (1997) Shark and skate egg-cases cast up on two South African beaches and their rates of hatching success, or causes of death. Afr Zool 32:112–117

    CAS  Google Scholar 

  • Van der Laan R, Fricke R, Eschmeyer WN (2023). Eschmeyer's Catalog Of Fishes: Classification. https://www.calacademy.org/scientists/catalog-of-fishes-classification/ Accessed 05 April 2023

  • Vooren CM (1998) Ambientes costeiros e marinhos e sua biota, elasmobrânquios demersais. In: Seeliger U, Odebrecht C, Castello JP (eds) Os ecossistemas costeiro e marinho do extremo sul do Brasil. Rio Grande, Ecoscientia, pp 157–162

    Google Scholar 

  • Walker TI (2005) Reproduction in fishery science. In: Hamlet WC (ed) Reproductive biology and phylogeny of Chondrichthyans, Sharks, Batoids and Chimaeras. Science Publishers, Inc., Enfield, pp 81–127

    Google Scholar 

  • Wilson E (1925) The cell in development and heredity. New York

  • Wourms JP (1977) Reproduction and development in Chondrichthyan fishes. Am Zool 17:379–410. https://doi.org/10.1093/icb/17.2.379

    Article  Google Scholar 

  • Wourms JP (1981) Viviparity: The maternal-fetal relationship in fishes. Am Zool 21:473–515. https://doi.org/10.1093/icb/21.2.473

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall

Download references

Acknowledgements

The present work constituted the Undergraduate Thesis of Natalia Silveira Gularte (Biological Sciences Course, FURG). Comments by Dr. Augusto Ferrari (Instituto de Ciências Biológicas, FURG) and Dr. Luis Gustavo Cardoso (Instituto de Oceanografia, FURG) on the first draft considerably improved the paper. Dr. Carolus Maria Vooren (IO-FURG) was the encourager of the development of a quantitative and continue monitoring program of the occurring of egg capsules by species over an extended time period at Cassino beach. This is the first paper on the subject and we dedicate it to his memory.

Funding

This study was granted by the Institutional Program of Scholarships of Scientific Initiation of the Brazilian National Council of Scientific and Technological Development of the Universidade Federal do Rio Grande (PIBIC/CNPq/FURG) during 2018–2021.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Natalia Silveira Gularte.

Ethics declarations

Animal ethics statement

The present work did not include any kind of animal sampling or experimentation. The egg capsules used were exclusively collected from the beach, already hatched.

Conflict of interest

The authors declare that there are no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gularte, N.S., Norbis, W. & Oddone, M.C. Trends and seasonality of the occurrence of hatched egg capsules of Rioraja agassizi (Müller & Henle 1841) (Chondrichthyes: Rajiformes) in a South Brazilian beach, Southwestern Atlantic Ocean. Environ Biol Fish 106, 1569–1577 (2023). https://doi.org/10.1007/s10641-023-01435-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-023-01435-9

Keywords

Navigation