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Species co-occurrence and population dynamics in annual fish assemblages in the lower Río Uruguay basin

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Abstract

Austrolebias is a genus of annual killifishes from subtropical and temperate grasslands of South America. They coexist in assemblages of up to five species in pools with variable connection to permanent water bodies and complete their entire life cycle within 1 year, terminated by summer desiccation of their habitat. To quantify community and population characteristics of Austrolebias assemblages, we sampled a set of 18 pools in the lowlands of the confluence of Río Negro and Río Uruguay in western Uruguay, with 16 sampling trips conducted over the entire seasonal cycle in 2015. Austrolebias bellottii was a ubiquitous and generalist species, A. nigripinnis was more common in pools influenced by active floodplain, A. elongatus (a large predatory species) was rare overall, and four A. alexandri was found only in two pools. Unexpectedly, many pools desiccated in winter (mid season) and some of them supported a second cohort after their re-inundation. Fish abundance and fish density declined steadily prior to pool desiccations. There were indications that adult A. bellottii can survive a short period of habitat desiccation in wet mud, leading to coexistence of an older A. bellottii cohort with a younger A. nigripinnis cohort. Males disappeared from populations at a higher rate, especially towards the end of the season. The overall lifespan of both common species was up to 7 months in pools that did not experience mid-season desiccation. This study provides fundamental demographic parameters for the annual fish in this region.

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References

  • Alonso F, Calviño P (2018) Killis estacionales en aguas permanentes (Cyprinodontiformes; Rivulidae). BIBKCA 21:77–84

    Google Scholar 

  • Alonso F, Calviño PA, Terán GE, García I (2016) Geographical distribution of Austrolebias monstrosus (Huber, 1995), A. elongatus (Steindachner, 1881) and A. vandenbergi (Huber, 1995) (Teleostei: Cyprinodontiformes), with comments on the biogeography and ecology of Rivulidae in Pampasic and Chaco floodplains. Check List 12:1945

    Article  Google Scholar 

  • Alonso F, Terán GE, Calviño P, García I, Cardoso Y, García G (2018a) An endangered newspecies of seasonal killifish of the genus Austrolebias (Cyprinodontiformes: Aplocheiloidei) from the Bermejo river basin in the Western Chacoan region. PLoS One 13:e0196261. https://doi.org/10.1371/journal.pone.0196261

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alonso F, García I, Waldbillig M, Bozza F, Acuña T, Calviño PA, Massaro M, Ferreira EE, Solimano P (2018b) Nuevos registros de Austrolebias alexandri (Castello y López 1974) (Cyprinodontiformes, Rivulidae). BIBKA 21:50–54

    Google Scholar 

  • Arenzon A, Peret AC, Bohrer MBC (2001) Growth of the annual fish Cynopoecilus melanotaenia (Regan, 1912) based in a temporary water body population in Rio Grande do Sul state, Brazil (Cyprinodontiformes, Rivulidae). Rev Bras Biol 61:117–123

    Article  CAS  Google Scholar 

  • Arim M, Abades SB, Laufer G, Loureiro M, Marquet P (2010) Food web structure and body size trophic position and resource acquisition. Oikos 119:147–153. https://doi.org/10.1111/j.1600-0706.2009.17768.x

    Article  Google Scholar 

  • Bartáková V, Reichard M, Blažek R, Polačik M, Bryja J (2015) Terrestrial fishes: rivers are barriers to gene flow in annual fishes from the African savanna. J Biogeogr 42:1832–1844

    Article  Google Scholar 

  • Berois N, Arezo MJ, Papa NG, Clivio GA (2012) Annual fish: developmental adaptations for an extreme environment. WIREs Dev Biol 1:595–602

    Article  Google Scholar 

  • Berois N, García G, de Sá RO (2015) Annual fishes: life history strategy, diversity, and evolution. CRC Press, Boca Raton, p 343

    Book  Google Scholar 

  • Blažek R, Polačik M, Reichard M (2013) Rapid growth, early maturation and short generation time in African annual fishes. EvoDevo 4:24

    Article  PubMed Central  PubMed  Google Scholar 

  • Borthagaray AI, Berazategui M, Arim M (2015) Disentangling the effects of local and regional processes on biodiversity patterns through taxon-contingent metacommunity network analysis. Oikos 124:1383–1390

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cavallotto JL, Violante RA, Parker G (2004) Sea-level fluctuations during the last 8600 years in the de la Plata river (Argentina). Quatern Inter 114:155–165

    Article  Google Scholar 

  • Chew SF, Chan NK, LoongAM HKC, Tam WL, Ip YK (2004) Nitrogen metabolism in the African lungfish (Protopterus dolloi) aestivating in a mucus cocoon on land. J Exp Biol 207:777–786

    Article  CAS  PubMed  Google Scholar 

  • Costa WJEM (2009) Trophic radiation in the south American annual killifish genus Austrolebias (Cyprinodontiformes:Rivulidae). Ichth Exp Fresh 20:179–191

    Google Scholar 

  • Delaney RG, Lahiri S, Fishman AP (1974) Aestivation of the African lungfish Protopterus aethiopicus: cardiovascular and respiratory functions. J Exp Biol 61:111–128

    CAS  PubMed  Google Scholar 

  • Furness AI, Lee K, Reznick DN (2015) Adaptation in a variable environment: phenotypic plasticity and bet-hedging during egg diapause and hatching in an annual killifish. Evolution 69:1461–1475

    Article  PubMed  Google Scholar 

  • García G, Gutiérrez V, Vergara J, Calvino P, Duarte A, Loureiro M (2012) Patterns of population differentiation in annual killifishes from the Paraná–Uruguay–La Plata Basin: the role of vicariance and dispersal. J Biogeogr 39:1707–1719

    Article  Google Scholar 

  • García D, Loureiro M, Machín E, Reichard M (2018) Phenology of three coexisting annual fish species: seasonal patterns in hatching dates. Hydrobiol 809:323–337

    Article  Google Scholar 

  • Haas R (1976) Sexual selection in Nothobranchius guentheri (Pisces: cyprinodontidae). Evolution 30:614–622

    Article  PubMed  Google Scholar 

  • Inglima K, Perlmutter A, Markofsky J (1981) Reversible stage-specific embryonic inhibition mediated by the presence of adults in the annual fish Nothobranchius guentheri. J Exp Zool 215:23–33

    Article  CAS  PubMed  Google Scholar 

  • Keppeler FW, Lanés LEK, Rolon AS, Stenert C, Lehmann P, Reichard M, Maltchik L (2015) The morphology-diet relationship and its role in the coexistence of two species of annual fishes. Ecol Fresh Fish 24:77–90

    Article  Google Scholar 

  • Lanés LEK, Keppeler FW, Maltchik L (2012) Abundance, sex-ratio, length-weight relation, and condition factor of non-annual killifish Atlantirivulus riograndensis (Actinopterygii: Cyprinodontiformes: Rivulidae) in Lagoa do Peixe national park, a Ramsar site of southern Brazil. Acta Ichthi Pisci 42(3)

  • Lanés LEK, Keppeler FW, Maltchik L (2014) Abundance variations and life history traits of two sympatric species of Neotropical annual fish (Cyprinodontiformes: Rivulidae) in temporary ponds of southern Brazil. J Nat Hist 48:1971–1988

    Article  Google Scholar 

  • Lanés LEK, Godoy RS, Maltchik L, Polačik M, Blažek R, Vrtílek 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

    Article  PubMed  Google Scholar 

  • Laufer G, Arim M, Loureiro M, Piñeiro-Guerra JM, Clavijo-Baquet S, Fagúndez C (2009) Diet of four annual killifishes: an intra and interspecific comparison. Neotrop Ichthyol 7:77–86

    Article  Google Scholar 

  • Loureiro M, de Sá RO (1996) External morphology of the chorion of the annual fishes Cynolebias (Cyprinodontiformes: Rivulidae). Copeia 1996(4):1016–1022

    Article  Google Scholar 

  • 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, de Sá R (eds) Annual fishes: life history strategy, diversity, and evolution. CRC Press, Boca Raton, pp 111–132

    Google Scholar 

  • Louriero M, Bessonart J (2017) Austrolebias viarius. IUCN Red List Threat Spec 2017: e.T187245A1825294. 10.2305/IUCN.UK.2017-3.RLTS.T187245A1825294.en

  • Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Geront 38:935–940

    Article  Google Scholar 

  • Nico LG, Thomerson JE (1989) Ecology, food habits and spatial interactions of Orinoco basin annual killifish. Acta Biol Ven 12:106–120

    Google Scholar 

  • Passos C, Tassino B, Reyes F, Rosenthal GG (2014) Seasonal variation in female mate choice and operational sex ratio in wild populations of an annual fish, Austrolebias reicherti. PLoS One 9:e101649

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Polačik M, Podrabsky JE (2015) Temporary environments. In: Rüdiger R, Tobler M, Plath M (eds) Extremophile fishes: ecology, evolution, and physiology of teleosts in extreme environments. Springer International Publishing, pp 217–245

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL http://www.R-project.org/

  • Reichard M, Blažek R, Polačik M, Vrtílek M (2017) Hatching date variability in wild populations of four coexisting species of African annual fishes. Dev Dyn 246:827–837

    Article  PubMed  Google Scholar 

  • Reichard M, Lanés LEK, Polačik M, Blažek R, Vrtílek M, Godoy RS, Maltchik L (2018) Avian predation mediates size-specific survival in a Neotropical annual fish: a field experiment. Biol J Linn Soc 124:56–66

    Article  Google Scholar 

  • Reichard M, Polačik M, Blažek R, Vrtílek M (2014) Female bias in the adult sex ratio of African annual fishes: interspecific differences, seasonal trends and environmental predictors. Evol Ecol 28(6):1105–1120

  • Rosa RS, Lima FCT (2008) Peixes. In: Livro vermelho da fauna brasileira ameaçada de extinção. MMA, Brasília

    Google Scholar 

  • Thompson AW, Furness AI, Stone C, Rade CM, Ortí G (2017) Microanatomical diversification of the zonapellucida in aplochelioid killifishes. J Fish Biol 91:126–143. https://doi.org/10.1111/jfb.13332

    Article  CAS  PubMed  Google Scholar 

  • Vaz Ferreira R, Sierra de Soriano B, Soriano J (1966) Integración de la fauna de vertebrados en algunas masas de agua dulce temporales de Uruguay. Comp Trab Dep Zoo Vert, FHC 25:1–23

    Google Scholar 

  • Volcán MV, Lanés LEK, Gonçalves AC (2009) Threatened fishes of the world: Austrolebias nigrofasciatus Costa and Cheffe 2001 (Cyprinodontiformes: Rivulidae). Env Biol Fish 86:443–444. https://doi.org/10.1007/s10641-009-9544-x

    Article  Google Scholar 

  • Volcán MV, Lanés LEK, Gonçalves AC (2010) Threatened fishes of the world: Austrolebias univentripinnis Costa and Cheffe 2005 (Cyprinodontiformes, Rivulidae). Env Biol Fish 87:319–320. https://doi.org/10.1007/s10641-010-9605-1

    Article  Google Scholar 

  • Volcán MV, Sampaio LA, Bongalhardo DC, Robaldo RB (2012) Reproduction of the annual fish Austrolebias nigrofasciatus (Rivulidae) maintained at different temperatures. J App Ichth 29:648–652

    Article  Google Scholar 

  • Volcán MV, Gonçalves A, Lanés L (2017) First record of blackfin pearlfish Austrolebias nigripinnis (Regan, 1912) (Cyprinodontiformes, Cynolebiidae) from Brazil. Zootaxa 4254:387–390. https://doi.org/10.11646/zootaxa.4254.3.9

    Article  PubMed  Google Scholar 

  • Vrtílek M, Žák J, Pšenička M, Reichard M (2018a) Extremely rapid maturation of a wild African annual fish. Curr Biol 28:R822–R824. https://doi.org/10.1016/j.cub.2018.06.031

    Article  CAS  PubMed  Google Scholar 

  • Vrtílek M, Žák J, Polačik M, Blažek R, Reichard M (2018b) Longitudinal demographic study of wild populations of African annual killifish. Sci Rep 8:4774

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wourms JP (1972a) The developmental biology of annual fishes I. Stages in the normal development of Austrofundulus myersi dahl. J Exp Zool 182:143–168

    Article  CAS  PubMed  Google Scholar 

  • Wourms JP (1972b) The developmental biology of annual fishes. II. Naturally occurring dispersion and reaggregation of blastomeres during the development of annual fish eggs. J Exp Zool 182:169–200

    Article  CAS  PubMed  Google Scholar 

  • Wourms JP (1972c) 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

    Article  CAS  PubMed  Google Scholar 

  • Wourms JP, Sheldon H (1976) Annual fish oogenesis: II Formation of the secondary egg envelope. Dev Biol 50:355–366

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Financial support came from Agencia Nacional de Investigación e Innovación (ANII, FCE_2013_100380) to DG and Comisión Sectorial de Investigación Científica (CSIC I + D 2014_7) to ML. DG holds a PhD scholarship from Agencia Nacional de Investigación e Innovación (ANII, POS_NAC_2014_102280) and from CAP (Comisión Académica de Posgrado, UdelaR). DG and ML belongs to Sistema Nacional de Investigadores of Uruguay. MR was supported by Czech Science Foundation (P505/12/G112). All local and national legal and ethical guidelines were followed. The research was approved under reference number 240011-001885-13. We thank Patricia Magariños, Diego Díaz, Esteban Ortiz, Matej Polačik, Radim Blažek and Milan Vrtílek for the help in the field and Rowena Spence for English correction and comments on the ms. We thank local land owners for access on their properties, and local authorities of Villa Soriano for generous support of the project.

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  1. Departamento de Ecología y Evolución, Instituto de Biología, Facultad de Ciencias, Universidad de la República, Iguá, 4225, Montevideo, Uruguay

    Daniel García, Marcelo Loureiro & Emanuel Machín

  2. The Czech Academy of Sciences, Institute of Vertebrate Biology, Květná 8, Brno, Czech Republic

    Martin Reichard

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  1. Daniel García
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García, D., Loureiro, M., Machín, E. et al. Species co-occurrence and population dynamics in annual fish assemblages in the lower Río Uruguay basin. Environ Biol Fish 102, 569–580 (2019). https://doi.org/10.1007/s10641-019-00854-x

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