Abstract
Annual fishes inhabit small temporary ponds that dry up seasonally. Survival in temporary ponds requires specific physiological, morphological, and/or life cycle adaptations. Annual fishes exhibit a complex reproductive strategy with resistant eggs to survive droughts. Here, we investigate the fecundity of the annual fishes Austrolebias cyaneus and Cynopoecilus nigrovittatus individually and in interaction in situ throughout the hydroperiod (early inundation, drying, and late inundation) of a temporary pond. The monospecific treatment of Austrolebias cyaneus showed no effect on fecundity regarding body size, weight, and flooding phase. In the monospecific treatment of Cynopoecilus nigrovittatus, there was a positive effect of female body size and sampling period on the number of eggs, which was higher in the late flooding phase. In the interspecific treatment, Austrolebias laid fewer eggs in the early flooding phase when compared to the monospecific treatment, and Cynopoecilus nigrovittatus showed a reduction in the number of eggs, considering the entire hydrological cycle. These results obtained from wild populations should help to fill the knowledge gap on biological traits, which impairs the understanding of the ecology of annual killifish in small temporary wetlands.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
Code Availability
Not applicable.
References
Alvares CA, Stape JL, Sentelhas PC, de Gonçalves M, Sparovek JL G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Arenzon A, Bohrer MBC, Peret AC (1999) Reproduction of the annual fish Cynopoecilus melanotaenia (Regan, 1912) in a temporary water body in Rio Grande do sul, Brazil (Cyprinodontiformes, Rivulidae). Hydrobiologia 411:65–70. https://doi.org/10.1023/A:1003868711295
Arezo MJ, D’Alessandro S, Papa N, de Sá R, Berois N (2007) Sex differentiation pattern in the annual fish Austrolebias charrua (Cyprinodontiformes: Rivulidae). Tissue Cell 39:89–98. https://doi.org/10.1016/j.tice.2007.01.004
Avise JC, Tatarenkov A (2015) Population genetics and evolution of the mangrove rivulus Kryptolebias marmoratus, the world’s only self-fertilizing hermaphroditic vertebrate. J Fish Biol 87:519–538. https://doi.org/10.1111/jfb.12741
Barneche DR, Robertson DR, Craig RW, Marshall JD (2018) Fish reproductive-energy output increases disproportionately with body size. Science 360:642–645. https://doi.org/10.1126/science.aao6868
Bates D, Machler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Belote DF, Costa WJEM (2004) Reproductive behavior patterns in three species of the South American annual fish genus Austrolebias Costa, 1998 (Cyprinodontiformes, Rivulidae). Bol Mus Nac Rio de Janeiro 514:1–7
Berois N, Arezo MJ, Papa NG, Clivio GA (2012) Annual fish: developmental adaptations for an extreme environment. WIREs Dev Biol 1:595–602. https://doi.org/10.1002/wdev.39
Berois N, Arezo MJ, De Sá RO (2014) The neotropical genus Austrolebias: an emerging model of annual killifishes. Cell Dev Biol 3(2):136. https://doi.org/10.4172/2168-9296.1000136
Blažek R, Polačik M, Reichard M (2013) Rapid growth, early maturation and short generation time in african annual fishes. EvoDevo 4:24. https://doi.org/10.1186/2041-9139-4-24
Calviño PA (2005) Austrolebias toba (Cyprinodontiformes: Rivulidae), una especie nueva de pez anual de la Argentina. Rev Mus Argent Cienc Nat 7:183–190. https://doi.org/10.22179/REVMACN.7.335
Canavero A, Hernández D, Zarucki M, Arim M (2014) Patterns of co-occurrences in a killifish metacommunity are more related with body size than with species identity. Austral Ecol 39:455–461. https://doi.org/10.1111/aec.12103
Castro B, Wingen N, Santos S, Godoy R, Maltchik L, Lanés L, Oliveira G (2021) Biomarkers of oxidative stress in the post-embryonic characterization of the neotropical annual killifish. Biogerontology 22:507–530. https://doi.org/10.1007/s10522-021-09931-0
Cellerino A, Valenzano DR, Reichard M (2015) From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology. Biol Rev 91:511–533. https://doi.org/10.1111/brv.12183
Costa WJEM (1995) Phylogeny and classification of Rivulidae revisited: origin and evolution of annualism and miniaturization in rivulid fishes (Cyprinodontiformes: Aplocheiloidei). J Comp Biol 3:220–225
Costa WJM (2002) The annual fish genus Cynopoecilus (Cyprinodontiformes: Rivulidae): taxonomic revision, with descriptions of four new species. Ichthyol Explor Freshw 13:11–24
Costa WJEM (2006) The south American annual killifish genus Austrolebias (Teleostei: Cyprinodontiformes: Rivulidae): phylogenetic relationships, descriptive morphology and taxonomic revision. Zootaxa 1213:1–162. https://doi.org/10.11646/zootaxa.1213.1.1
Costa WJEM (2009) Trophic radiation in the south American annual killifish genus Austrolebias (Cyprinodontiformes: Rivulidae). Ichthyol Explor Freshw 20:179–191
Costa WJEM (2010) Historical biogeography of Cynolebiasine annual killifishes inferred from dispersal-vicariance analysis. J Biogeogr 37:1995–2004. https://doi.org/10.1111/j.1365-2699.2010.02339.x
Costa WJEM, Amorim PF, Mattos JLO (2017) Molecular phylogeny and timing of diversification in South American Cynolebiini seasonal killifishes. Mol Phylogenet Evol 116:61–68. https://doi.org/10.1016/j.ympev.2017.07.020
D’Anatro A, Loureiro M (2005) Geographic variation in Austrolebias luteoflamulatus Vaz-Ferreira, Sierra & Scaglia (Cyprinodontiformes, Rivulidae). J Fish Biol 67:849–865. https://doi.org/10.1111/j.0022-1112.2005.00791.x
Ferrer J, Wingert JM, Malabarba LR (2014) Description of a new species and phylogenetic analysis of the subtribe Cynopoecilina, including continuous characters without discretization (Cyprinodontiformes: Rivulidae). Zool J Linn 172:846–866. https://doi.org/10.1111/zoj.12190
Fonseca AP, Volcan MV, Robaldo RB (2018) Incubation media affect the survival, pathway and time of embryo development in neotropical annual fish Austrolebias nigrofasciatus (Rivulidae). J Fish Biol 92:165–176. https://doi.org/10.1111/jfb.13504
Fox J, Weisberg S (2019) An R companion to applied regression. Sage, Thousand Oaks, CA, USA. https://socialsciences.mcmaster.ca/jfox/Books/Companion/
García D, Loureiro M, Tassino B (2008) Reproductive behavior in the annual fish Austrolebias reicherti Loureiro & García 2004 (Cyprinodontiformes: Rivulidae). Neotrop Ichthyol 6:243–248. https://doi.org/10.1590/S1679-62252008000200012
Godoy RS, Lanés LEK, Weber V, Stenert C, Noblega HG, Oliveira GT, Maltchik L (2019) Age-associated liver alterations in wild populations of Austrolebias minuano, a short-lived neotropical annual killifish. Biogerontology 20:687–698. https://doi.org/10.1007/s10522-019-09822-5
Godoy R, Lanés L, Weber V, Wingen N, Pires MM, Oliveira G, Maltchik L (2020) Oxidative stress resistance in a short-lived neotropical annual killifish. Biogerontology 21:217–229. https://doi.org/10.1007/s10522-019-09855-w
Godoy RS, Weber V, Lanés LEK, Reichard M, Gemelli T, Hohendorff RV, Maltchik L (2021) Recognizing the enemy: do predator cues influence hatching in neotropical annual killifish? J Fish Biol 99:1476–1484. https://doi.org/10.1111/jfb.14856
Gonçalves CS, Souza UP, Volcan MV (2011) The opportunistic feeding and reproduction strategies of the annual fish Cynopoecilus melanotaenia (Cyprinodontiformes: Rivulidae) inhabiting ephemeral habitats on southern Brazil. Neotrop Ichthyol 9:191–200. https://doi.org/10.1590/S1679-62252011000100019
Lanés LEK, Keppeler FW, Maltchik L (2014) Abundance variations and life history traits of two sympatric species of annual fish (Cyprinodontiformes: Rivulidae) in temporary ponds of southern Brazil. J Nat Hist 48:1971–1988. https://doi.org/10.1080/00222933.2013.862577
Lanés LEK, Godoy RS, Maltchik L, Polacik M, Blazek R, Vrtilek M, Reichard M (2016) Seasonal dynamics in community structure, abundance, body size and sex ratio in two species of neotropical annual fishes. J Fish Biol 89:2345–2364. https://doi.org/10.1111/jfb.13122
Lanés L, Reichard M, Moura R, Godoy R, Maltchik L (2018) Environmental predictors for annual fish assemblages in subtropical grasslands of South America: the role of landscape and habitat characteristics. Environ Biol Fishes 101:127–139. https://doi.org/10.1007/s10641-018-0751-1
Legendre P, Legendre LFJ (2012) Numerical Ecology. Elsevier, Amsterdam, Netherlands
Loureiro M, Borthagaray A, Hernández D, Duarte A, Pinelli V, Arim M (2016) Austrolebias in space: scaling from ponds to biogeographical regions. In: Berois N, García G, Sá RO (eds) Annual fishes: life history strategy, diversity, and evolution. CRC Press, Boca Raton, pp 111–132. https://doi.org/10.1201/b19016-11
Loureiro M, Sá RO, Serra SW, Alonso F, Lanés LEK, Volcan MV, Calviño PA, Nielsen D, Duarte A, García G (2018) Review of the family Rivulidae (Cyprinodontiformes, Aplocheiloidei) and a molecular and morphological phylogeny of the annual fish genus Austrolebias Costa 1998. Neotrop Ichthyol 16:e170074. https://doi.org/10.1590/1982-0224-20180007
Maluf JRT (2000) Nova classificação climática do Estado do Rio Grande do sul. Rev Bras Agrometeorol 8:141–150
Nico LG, Thomerson JE (1989) The south American annual fish genus Cynopoecilus (Cyprinodontiformes: Rivulidae): new species, geographic distribution, and notes on biology. Copeia 1989:925–939
Podrabsky J, Riggs C, Wagner J (2016) Tolerance of environmental stress. In: Berois N, García G, Sá RO (eds) Annual fishes: life history strategy, diversity, and evolution. CRC Press, Boca Raton, pp 159–184. https://doi.org/10.1201/b19016-13
R Development Core Team (2020) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. http://www.R-project.org
Reis RE, Lucena ZMS, Lucena CAS, Malabarba LR (2003) Peixes. In: Fontana CS, Bencke GA, Reis RE (eds) Livro Vermelho da fauna ameaçada de extinção no Rio Grande do sul. Edipucrs, Porto Alegre, pp 117–145
Rosa RS, Lima FCT (2008) Peixes. In: Machado ABM, Drummond GM, Paglia AP (eds) Livro Vermelho da fauna brasileira ameaçada de extinção. Ministério do Meio Ambiente, Brasília, pp 9–285
Schalk CM, Montaña CG, Libson ME (2014) Reproductive strategies of two neotropical killifish, Austrolebias vandenbergi and Neofundulus ornatipinnis (Cyprinodontiformes: Rivulidae) in the bolivian Gran Chaco. Rev Biol Trop 62:102–111. https://doi.org/10.15517/RBT.V62I1.6567
Shibatta O (2005) Reprodução do pirá-brasília, Simpsonichthys boitonei Carvalho (Cyprinodontiformes, Rivulidae), e caracterização de seu habitat na Reserva Ecológica do Instituto Brasileiro de Geografia e Estatística, Brasília, Distrito Federal. Brasil Rev B Zool 22:1146–1151. https://doi.org/10.1590/S0101-81752005000400048
Thibault RE, Schultz RJ (1978) Reproductive adaptations among viviparous fishes (Cyprinodontiformes: Poeciliidae). Evolution 32:320–333. https://doi.org/10.1111/j.1558-5646.1978.tb00648.x
Vaz-Ferreira R, Sierra B, Scaglia S (1964) Eco-etología de la reproducción en los peces del género Cynolebias Steindachner, 1876. Arch Soc Biol Montevideo 26:44–49
Volcan MV, Guadagnin DL (2020) Annual and non-annual fish assemblages respond differently to environmental and spatiotemporal variations of temporary wetlands from southern Brazil. Freshw Biol 65:639–649. https://doi.org/10.1111/fwb.13589
Volcan MV, Lanés LEK (2018) Brazilian killifishes risk extinction. Science 361:340–341. https://doi.org/10.1126/science.aau5930
Volcan MV, Severo-Neto F (2019) Austrolebias ephemerus (Cyprinodontiformes: Rivulidae), a new annual fish from the upper Rio Paraguai basin, brazilian Chaco. Zootaxa 4560:541–553. https://doi.org/10.11646/zootaxa.4560.3.6
Volcan M, Fonseca AP, Robaldo R (2011) Reproduction of the threatened annual killifish Austrolebias nigrofasciatus (Cyprinodontiformes: Rivulidae), confined in a natural environment. JoTT 3:1864–1867. https://doi.org/10.11609/JoTT.o2575.1864-7
Volcan MV, Fonseca AP, Figueiredo MRC, Sampaio LA, Robaldo RB (2012) Effect of temperature on growth of the threatened annual fish Austrolebias nigrofasciatus Costa & Cheffe 2001. Biota Neotrop 12:68–73. https://doi.org/10.1590/S1676-06032012000400007
Volcan MV, Gonçalves AC, Guadagnin DL (2013) Length-weight relationship of three annual fishes (Rivulidae) from temporary freshwater wetlands of southern Brazil. J Appl Ichthyol 29:1188–1190. https://doi.org/10.1111/jai.12214
Volcan MV, Gonçalves AC, Guadagnin DL (2018) Body size and population dynamics of annual fishes from temporary wetlands in Southern Brazil. Hydrobiologia 811:367–378. https://doi.org/10.1007/s10750-018-3789-3
Vrtílek M, Reichard M (2015) Highly plastic resource allocation to growth and reproduction in females of an african annual fish. Ecol Fresh Fish 24:364–373. https://doi.org/10.1111/eff.12175
Vrtílek MZ, ZAK J, Polacik M, Blazek R, Reichard M (2018) Longitudinal demographic study of wild populations of african annual killifish. Sci Rep 8:4774. https://doi.org/10.1038/s41598-018-22878-6
Wiggins GB, MacKay RJ, Smith IM (1980) Evolutionary and ecological strategies of animals in annual temporary pools. Arch Hydrob 58:97–206
Wootton RJ, Smith C (2015) Reproductive biology of teleost fishes. Wiley-Blackwell, Hoboken
Wourms JP (1972) The developmental biology of annual fishes. III. Pre-embryonic and embryonic diapause of variable duration in the eggs of annual fishes. J Exp Zool 182:389–414. https://doi.org/10.1002/jez.1401820310
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x
Acknowledgements
This research was authorized by IBAMA/ICMBio (SISBIO process number 83141-1) and UNISINOS Ethic Committee (PPECEUA 12.2019).
Funding
This research was supported by CNPq - Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grant numbers 165529/2020-2, 305475/2018-5). LM and CS hold Research Productivity Grants from CNPq.
Author information
Authors and Affiliations
Contributions
Vinicius Weber and Leonardo Maltchik: assisted with conceptualization, formal analysis, data curation, methodology, visualization, writing – original draft, writing – review & editing. Vinicius Weber, Robson Souza Godoy, Luis Esteban Krause Lanés and Pedro Henrique de Oliveira Hoffmann: assisted with experimental design, field and laboratory work and manuscript preparation and editing. Cristina Stenert: performed statistical analyses and prepared the manuscript. Leonardo Maltchik: assisted with funding acquisition, project administration and supervision. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no conflict of interest regarding this publication. The authors have no relevant financial or non-financial interests to disclose.
Ethics Approval
We declare that data collection complied with the current Brazilian environmental laws (SISBIO 83141-1) and UNISINOS Ethic Committee (PPECEUA 12.2019).
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
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.
About this article
Cite this article
Weber, V., Godoy, R.S., Lanés, L.E.K. et al. Egg Production of Annual Fish Austrolebias cyaneus and Cynopoecilus nigrovittatus Occurs Throughout Their Entire Life Cycle to Survive in a Temporary Wetland. Wetlands 43, 97 (2023). https://doi.org/10.1007/s13157-023-01745-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13157-023-01745-9