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

  • Daniel García
  • Marcelo Loureiro
  • Emanuel Machín
  • Martin ReichardEmail author
Article

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.

Keywords

Annual fish Community assembly Cyprinodontiformes Seasonal dynamics Sex ratio 

Notes

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.

Supplementary material

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10641_2019_854_MOESM2_ESM.pdf (1.4 mb)
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References

  1. Alonso F, Calviño P (2018) Killis estacionales en aguas permanentes (Cyprinodontiformes; Rivulidae). BIBKCA 21:77–84Google Scholar
  2. 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 12:1945Google Scholar
  3. 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 Google Scholar
  4. 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 21:50–54Google Scholar
  5. 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 61:117–123Google Scholar
  6. 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 Google Scholar
  7. 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 42:1832–1844Google Scholar
  8. Berois N, Arezo MJ, Papa NG, Clivio GA (2012) Annual fish: developmental adaptations for an extreme environment. WIREs Dev Biol 1:595–602Google Scholar
  9. Berois N, García G, de Sá RO (2015) Annual fishes: life history strategy, diversity, and evolution. CRC Press, Boca Raton, p 343Google Scholar
  10. Blažek R, Polačik M, Reichard M (2013) Rapid growth, early maturation and short generation time in African annual fishes. EvoDevo 4:24Google Scholar
  11. 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 124:1383–1390Google Scholar
  12. 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 Google Scholar
  13. Cavallotto JL, Violante RA, Parker G (2004) Sea-level fluctuations during the last 8600 years in the de la Plata river (Argentina). Quatern Inter 114:155–165Google Scholar
  14. 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 207:777–786Google Scholar
  15. Costa WJEM (2009) Trophic radiation in the south American annual killifish genus Austrolebias (Cyprinodontiformes:Rivulidae). Ichth Exp Fresh 20:179–191Google Scholar
  16. Delaney RG, Lahiri S, Fishman AP (1974) Aestivation of the African lungfish Protopterus aethiopicus: cardiovascular and respiratory functions. J Exp Biol 61:111–128Google Scholar
  17. 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 69:1461–1475Google Scholar
  18. 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 39:1707–1719Google Scholar
  19. García D, Loureiro M, Machín E, Reichard M (2018) Phenology of three coexisting annual fish species: seasonal patterns in hatching dates. Hydrobiol 809:323–337Google Scholar
  20. Haas R (1976) Sexual selection in Nothobranchius guentheri (Pisces: cyprinodontidae). Evolution 30:614–622Google Scholar
  21. 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 215:23–33Google Scholar
  22. 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 24:77–90Google Scholar
  23. 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)Google Scholar
  24. 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 48:1971–1988Google Scholar
  25. 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 89:2345–2364Google Scholar
  26. 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 7:77–86Google Scholar
  27. Loureiro M, de Sá RO (1996) External morphology of the chorion of the annual fishes Cynolebias (Cyprinodontiformes: Rivulidae). Copeia 1996(4):1016–1022Google Scholar
  28. 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 111–132Google Scholar
  29. Louriero M, Bessonart J (2017) Austrolebias viarius. IUCN Red List Threat Spec 2017: e.T187245A1825294. 10.2305/IUCN.UK.2017-3.RLTS.T187245A1825294.enGoogle Scholar
  30. Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Geront 38:935–940Google Scholar
  31. Nico LG, Thomerson JE (1989) Ecology, food habits and spatial interactions of Orinoco basin annual killifish. Acta Biol Ven 12:106–120Google Scholar
  32. 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:e101649Google Scholar
  33. 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 217–245Google Scholar
  34. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL http://www.R-project.org/
  35. 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 246:827–837Google Scholar
  36. 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 124:56–66Google Scholar
  37. 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):1105–1120Google Scholar
  38. Rosa RS, Lima FCT (2008) Peixes. In: Livro vermelho da fauna brasileira ameaçada de extinção. MMA, BrasíliaGoogle Scholar
  39. 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 Google Scholar
  40. 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 25:1–23Google Scholar
  41. 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 Google Scholar
  42. 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 Google Scholar
  43. Volcán MV, Sampaio LA, Bongalhardo DC, Robaldo RB (2012) Reproduction of the annual fish Austrolebias nigrofasciatus (Rivulidae) maintained at different temperatures. J App Ichth 29:648–652Google Scholar
  44. 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 Google Scholar
  45. 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 Google Scholar
  46. Vrtílek M, Žák J, Polačik M, Blažek R, Reichard M (2018b) Longitudinal demographic study of wild populations of African annual killifish. Sci Rep 8:4774Google Scholar
  47. Wourms JP (1972a) The developmental biology of annual fishes I. Stages in the normal development of Austrofundulus myersi dahl. J Exp Zool 182:143–168Google Scholar
  48. 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 182:169–200Google Scholar
  49. 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 182:389–414Google Scholar
  50. Wourms JP, Sheldon H (1976) Annual fish oogenesis: II Formation of the secondary egg envelope. Dev Biol 50:355–366Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Departamento de Ecología y Evolución, Instituto de Biología, Facultad de CienciasUniversidad de la RepúblicaMontevideoUruguay
  2. 2.The Czech Academy of Sciences, Institute of Vertebrate BiologyBrnoCzech Republic

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