Advertisement

Environmental Biology of Fishes

, Volume 101, Issue 6, pp 963–977 | Cite as

Environmental predictors for annual fish assemblages in subtropical grasslands of South America: the role of landscape and habitat characteristics

  • Luis Esteban Krause Lanés
  • Martin Reichard
  • Rafael Gomes de Moura
  • Robson S. Godoy
  • Leonardo Maltchik
Article

Abstract

Annual fishes (AF) are ecologically unique assemblage with major conservation concern. Several AF species are found in temporary waters of South American subtropical grasslands, an ecoregion largely neglected by conservation policies. We applied a broad-scale approach to understand distribution pattern of the AF and tested the effects of environmental predictors on occurrence, abundance and assemblage structure of this diverse Neotropical group of threatened endemic aquatic fauna. We recorded 23 AF species. AF assemblage was strongly spatially structured and many individual species formed discrete units. AF presence was negatively associated with altitude at the landscape scale, and negatively associated with maximum pool depth and presence of predatory fish at the local scale. We found negative association between AF abundance and water depth. Assemblage composition was spatially structured, differed among hydrographic regions and was influenced by altitude, temperature and monthly precipitation. AF inhabits highly vulnerable habitats currently located in livestock and agricultural landscapes. Habitat maintenance through wildlife-friendly practices should be considered as an alternative to promote AF conservation.

Keywords

Austrolebias Cynopoecilus Killifish Temporary waters Pampas 

Notes

Acknowledgements

This research was supported mainly by funds from CNPq - Conselho Nacional de Desenvolvimento Científico e Tecnológico - Brazil (52370695.2) and UNISINOS. The biological data were obtained as part of doctorate project of LEKL (CNPq process number 132343/2009-6). The Ph.D. course of LEKL was partially funded by PROSUP/CAPES scholarship (2011/2). Part of the manuscript was prepared during the period covered by the Doctorate Sandwich Abroad scholarship (SWE) of LEKL through Science without Borders program from CNPq (200165/2015-1). LM holds Research Productivity grant and MR Special Visiting Research (PVE) grant, both from CNPq. The AF collections complied with Brazilian current laws (IBAMA-02001.001148/2007-61).

Supplementary material

10641_2018_751_MOESM1_ESM.docx (32 kb)
ESM 1 (DOCX 31.6 kb)
10641_2018_751_MOESM2_ESM.docx (270 kb)
ESM 2 (DOCX 269 kb)
10641_2018_751_MOESM3_ESM.docx (433 kb)
ESM 3 (DOCX 432 kb)
10641_2018_751_MOESM4_ESM.docx (14 kb)
ESM 4 (DOCX 13.5 kb)
10641_2018_751_MOESM5_ESM.docx (182 kb)
ESM 5 (DOCX 181 kb)
10641_2018_751_MOESM6_ESM.docx (148 kb)
ESM 6 (DOCX 148 kb)
10641_2018_751_MOESM7_ESM.docx (12 kb)
ESM 7 (DOCX 12.2 kb)

References

  1. Abell R, Thieme ML, Revenga C, Bryer M, Kottelat M, Bogutskaya N, Coad B, Mandrak N, Balderas SC, Bussing W, Stiassny MLJ, Skelton P, Allen GR, Unmack P, Naseka A, Rebecca NG, Sindorf N, Robertson J, Armijo E, Higgins JV, Heibel TJ, Wikramanayake E, Olson D, López HL, Reis RE, Lundberg JG, Pérez MHS Petry P (2008) Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Biomed Sci 58:403–414Google Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  3. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253CrossRefPubMedGoogle Scholar
  4. Anderson MJ, Millar RB (2004) Spatial variation and effects of habitat on temperate reef fish assemblages in northeastern New Zealand. J Exp Mar Biol Ecol 305:191–221CrossRefGoogle Scholar
  5. Azpiroz AB, Isacch JP, Dias RA, Di Giacomo AS, Fontana CS, Palarea CM (2012) Ecology and conservation of grassland birds in southeastern South America: a review. J Field Ornithol 83:217–246CrossRefGoogle Scholar
  6. Baigún CRM, Colautti D, López HL, Van Damme PA, Reis RE (2012) Application of extinction risk and conservation criteria for assessing fish species in the lower La Plata River basin, South America. Aquatic Conserv Mar Freshw Ecosyst 22:181–197CrossRefGoogle 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 42:1832–1844CrossRefGoogle Scholar
  8. Barton K (2015) MuMIn: Multi-Model Inference. R package version 1(13):4. http://cran.rproject.org/package=MuMIn Accessed: 20 August 2017
  9. Bates D, Maechler M, Bolker B, Walker S (2015) lme4: linear mixed-effects models using Eigen and S4. R package version 1:1–8 http://CRAN.R-project.org/package=lme4 Accessed: 16 March 2015
  10. Batzer DP, Palik BJ, Buech R (2004) Relationships between environmental characteristics and macroinvertebrate communities in seasonal woodland ponds of Minnesota. J N Am Benthol Soc 23:50–68CrossRefGoogle Scholar
  11. Behling H, Pillar VD (2007), Late quaternary vegetation, biodiversity and fire dynamics on the southern Brazilian highland and their implication for conservation and management of modern Araucaria forest and grassland ecosystems. Philos T Roy Soc B362: 243–251Google Scholar
  12. Berois N, Arezo MJ, Papa NG, Clivio GA (2012) Annual fish: developmental adaptations for an extreme environment. Wires: Dev Bio 1(4):595–602CrossRefGoogle Scholar
  13. Berois N, Arezo MJ, de Sá RO (2014) The Neotropical genus Austrolebias: an emerging model of annual killifishes. Annu Rev Cell Dev Bi 3: 136Google Scholar
  14. Bilenca D, Miñarro F (2004) Identificación de Areas Valiosas de Pastizal (AVP’s) en las Pampas y Campos de Argentina, Uruguay y sur de Brasil. Fundación Vida Silvestre, Buenos AiresGoogle Scholar
  15. Blažek R, Polačik M, Reichard M (2013) Rapid growth, early maturation and short generation time in African annual fishes. EvoDevo 4(1):24CrossRefPubMedPubMedCentralGoogle Scholar
  16. Bond WJ, Parr CL (2010) Beyond the forest edge: ecology, diversity and conservation of grassy biomes. Biol Conserv 143:2395–2404CrossRefGoogle Scholar
  17. Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New YorkCrossRefGoogle Scholar
  18. Cabrera AL, Willink A (1980) Biogeografia da America Latina. OEA, WashingtonGoogle Scholar
  19. 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 39:455–461CrossRefGoogle Scholar
  20. Cheffe MM, Volcan MV, Lanés LEK (2010) Pisces, Cyprinodontiformes, Rivulidae, Austrolebias vazferreirai (Berkenkamp, Etzel, Reichert and Salvia, 1994): new species record from Brazil. Check List 6:592–593CrossRefGoogle Scholar
  21. Corrêa F, Claudino MC, Bastos RF, Huckembeck S, Garcia AM (2012) Feeding ecology and prey preferences of a piscivorous fish in the Lagoa do Peixe National Park, a biosphere Reserve in Southern Brazil. Environ Biol Fish 93:1–12CrossRefGoogle Scholar
  22. Costa WJEM (2002) The annual fish genus Cynopoecilus (Cyprinodontiformes, Rivulidae): taxonomic revision, with descriptions of four new species. Ichthyo Explor Fres 13:11–24Google Scholar
  23. Costa WJEM (2006) The south American annual killifish genus Austrolebias (Teleostei: Cyprinodontiformes: Rivulidae): phylogenetic relationships, descriptive morphology and taxonomic revision. Zootaxa 1213:1–162Google Scholar
  24. Costa WJEM (2009) Aplocheiloid fishes of the Brazilian Atlantic Forest: history, diversity and conservation. Museu Nacional, Rio de JaneiroGoogle Scholar
  25. Costa WJEM (2010) Historical biogeography of Cynolebiasine annual killifishes inferred from dispersal-vicariance analysis. J Biogeogr 37:1995–2004Google Scholar
  26. Dorn A, Ng’oma E, Janko K, Reichwald K, Polačik M, Platzer M, Reichard M (2012) Phylogeny, genetic variability and colour polymorphism of an emerging animal model: the short-lived annual Nothobranchius fishes from southern Mozambique. Mol Phylogenet Evol 61:739–749CrossRefGoogle Scholar
  27. Dorn A, Musilová Z, Platzer M, Reichwald K, Cellerino A (2014) The strange case of east African annual fishes: aridification correlates with diversification for a savannah aquatic group? BMC Evol Biol 14:210CrossRefPubMedPubMedCentralGoogle Scholar
  28. Dray S, Blanchet G, Borcard D, Guenard G, Jombart T, Larocque G, Legendre P, Madi N, Wagner HH (2017) adespatial: multivariate multiscale spatial analysis. Available at: https://cran.r-project.org/package=adespatial. Acessed 12 Dec 2017
  29. Errea A, Danulat E (2001) Growth of the annual fish, Cynolebias viarius (Cyprinodontiformes), in the natural habitat compared to laboratory conditions. Environ Biol Fish 61:261–268CrossRefGoogle Scholar
  30. Escalera-Vazquez LH, Zambrano L (2010) The effect of seasonal variation in abiotic factors on fish community structure in temporary and permanent pools in a tropical wetland. Freshw Biol 55:2557–2569CrossRefGoogle Scholar
  31. Fernandes I.M., Machado Francisco A, Penha J (2010) Spatial pattern of a fish assemblage in a seasonal tropical wetland: effects of habitat, herbaceous plant biomass, water depth, and distance from species sources. Neotrop Ichthyol 8: 289–298Google Scholar
  32. Ferrer J, Malabarba LR, Costa WJEM (2008) Austrolebias paucisquama (Cyprinodontiformes: Rivulidae), a new species of annual killifish from southern Brazil. Neotrop Ichthyol 6:175–180CrossRefGoogle Scholar
  33. 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 Soc-Lond 172:846–866CrossRefGoogle Scholar
  34. Furness AI, Reznick DN, Springer MS, Meredith RW (2015) Convergent evolution of alternative developmental trajectories associated with diapause in African and south American killifish. P Roy Soc Lond B Bio 282:20142189CrossRefGoogle Scholar
  35. FZBRS (Fundação Zoobotânica do Rio Grande do Sul) (2014) Avaliação do Estado de Conservação de Espécies da Fauna do Rio Grande do Sul. Lista Vermelha da Fauna. Decreto N° 51.797/2014. http://www.liv.fzb.rs.gov.br/livlof/?id_modulo=1&id_uf=23&ano=2012. Accessed: 16 March 2015
  36. García G, Gutiérrez V, Vergara J, Calviño 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 39:1707–1719CrossRefGoogle Scholar
  37. Hair JJF, Anderson RE, Tatham RL, Black WC (2005) Análise multivariada de dados. Bookman, Porto AlegreGoogle Scholar
  38. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9Google Scholar
  39. Hasenack H, Cordeiro JLP (2006) Mapeamento da cobertura vegetal do Bioma Pampa. Relatório técnico Ministério do Meio Ambiente: Secretaria de Biodiversidade e Florestas no âmbito do mapeamento da cobertura vegetal dos biomas brasileiros. UFRGS, Porto AlegreGoogle Scholar
  40. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  41. IBGE (Instituto Brasileiro de Geografia e Estatística) (2004) Mapa de Biomas do Brasil. Primeira aproximação. http://www2.ibge.gov.br/ Accessed: 16 March 2015
  42. ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) (2013) Sumário Executivo do Plano de Ação Nacional para a Conservação dos Peixes Rivulídeos Ameaçados de Extinção. http://www.icmbio.gov.br/portal/images/stories/docs-plano-de-acao/pan-rivulideos/sumario-executivo-rivulideos.pdf. Accessed: 16 March 2015
  43. Klein AHF (1998) Clima regional. In: Seeliger U, Odebrecht C, Castello JP (eds) Os ecossistemas costeiro e marinho do extremo sul do Brasil. Ecoscentia, Rio Grande, pp 5–7Google Scholar
  44. Lanés LEK, Keppeler FW, Maltchik L (2014a) 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 48:1971–1988CrossRefGoogle Scholar
  45. Lanés LEK, Gonçalves ÂC, Volcan MV (2014b) Discovery of endangered annual killifish Austrolebias cheradophilus (Aplocheiloidei: Rivulidae) in Brazil, with comments on habitat, population structure and conservation status. Neotrop Ichthyol 12:117–124CrossRefGoogle Scholar
  46. Lanés LEK, Rolon AS, Stenert C, Maltchik L (2015) Effects of an artificial and annual opening of a natural sandbar on the fish community in a coastal lagoon system: a case study in Lagoa do Peixe floodplains, southern Brazil. J Appl Ichthyol 31:321–327CrossRefGoogle Scholar
  47. 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 89:2345–2364CrossRefPubMedGoogle Scholar
  48. Loureiro M, Duarte A, Zarucki M (2011) A new species of Austrolebias Costa (Cyprinodontiformes: Rivulidae) from northeastern Uruguay, with comments on distribution patterns. Neotrop Ichthyol 9:335–342CrossRefGoogle Scholar
  49. Loureiro M, Zarucki M, González I, Vidal N, Fabiano G (2013) Peces continentales. In: Soutullo A, Clavijo C, Martínez-Lanfranco JA (eds) Especies prioritarias para la conservación en Uruguay. Vertebrados, moluscos continentales y plantas vasculares, 1st edn. DINAMA, Montevideo, pp 91–112Google Scholar
  50. Loureiro M, Borthagaray A, Hernández D, Duarte A, Pinelli V, Arim M (2015) 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 111–132CrossRefGoogle Scholar
  51. Lowe-Mcconnel RH (1999) Estudos ecológicos de comunidades de peixes tropicais. EdUSP, São PauloGoogle Scholar
  52. Machado IF, Maltchik L (2010) Can management practices in rice fields contribute to amphibian conservation in southern Brazilian wetlands? Aquat Conserv 20:39–46Google Scholar
  53. Maltchik L, Lanés LEK, Stenert C, Medeiros ESF (2010) Species-area relationship and environmental predictors of fish communities in coastal freshwater wetlands of southern Brazil. Environ Biol Fish 88:25–35CrossRefGoogle Scholar
  54. Maltchik L, Lanés LEK, Keppeler FW, Rolon AS, Stenert C (2014) Landscape and habitat characteristics associated with fish occurrence and richness in southern Brazil palustrine wetland systems. Environ Biol Fish 9:297–308CrossRefGoogle Scholar
  55. Matthews WJ (1998) Patterns in freshwater fish ecology. Chapmann & Hall, New YorkCrossRefGoogle Scholar
  56. McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software, Gleneden BeachGoogle Scholar
  57. Morán-López R, Da Silva E, Pérez-Bote JL, Corbacho Amado C (2006) Associations between fish assemblages and environmental factors for Mediterranean-type rivers during summer. J Fish Biol 69:1552–1569CrossRefGoogle Scholar
  58. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  59. Nico LG, Taphorn DC (1984) Limnology of Orinoco basin - annual killifish pools. Journal of American Killifish Association 19:59–72Google Scholar
  60. Nico LG, Thomerson JE (1989) Ecology, food habits and spatial interactions of Orinoco Basin annual killifish. Acta Bio Venez 12:106–112Google Scholar
  61. Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Stevens MHH, Wagner H (2009) Vegan: community ecology package. R package version 1.15-2. R Project for Statistical Computing, Vienna, AustriaGoogle Scholar
  62. Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson GL, Solymos P, Stevens MHH Wagner H (2015) Vegan: Community Ecology Package. http://CRAN.R-project.org/package=vegan. Accessed: 16 March 2015
  63. Oliveira JM, Pillar VD (2004) Vegetation dynamics on mosaics of Campos and Araucaria forest between 1974 and 1999 in southern Brazil. Community Ecol 5:197–202CrossRefGoogle Scholar
  64. Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D'Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on earth. Biomed Sci 51:933–938Google Scholar
  65. Overbeck GE, Müller SC, Fidelis A, Pfadenhauer J, Pillar VDP, Blanco CC, Boldrini II, Both R, Forneck ED (2007) Brazil’s neglected biome: the south Brazilian Campos. Perspect Plant Ecol 9:101–116CrossRefGoogle Scholar
  66. Pazin VFV, Magnusson WE, Zuanon J, Mendonça FP (2006) Fish assemblages in temporary ponds adjacent to ‘terra-firme’ streams in Central Amazonia. Freshw Biol 51:1025–1037CrossRefGoogle Scholar
  67. Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sc 11:1633–1644CrossRefGoogle Scholar
  68. Peres-Neto PR, Legendre P (2010) Estimating and controlling for spatial structure in the study of ecological communities. Glob Ecol Biogeogr 19:174–184CrossRefGoogle Scholar
  69. Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87(10):2614–2625CrossRefPubMedGoogle Scholar
  70. Pillar VD, Vélez E (2010) Extinção dos Campos Sulinos em unidades de conservação: um fenômeno natural ou um problema ético? Nat Conservação 8:84–86CrossRefGoogle Scholar
  71. 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
  72. Polačik M, Reichard M (2010) Diet overlap among three sympatric African annual killifish species Nothobranchius spp. from Mozambique. J Fish Biol 77:754–768PubMedGoogle Scholar
  73. Polačik M, Donner MT, Reichard M (2011) Age structure of annual Nothobranchius fishes in Mozambique: is there a hatching synchrony? J Fish Biol 78:796–809CrossRefPubMedGoogle Scholar
  74. R Development Core Team (2015) R: a language and environment for statistical computing-version 3.2.1. R foundation for statistical computing, Austria. http://www.r-project.org. Accessed: 16 March 2015
  75. Reichard M (2015) The evolutionary ecology of African annual fishes. In: Berois N, García G, de Sá R (eds) Annual fishes: life history strategy, diversity, and evolution. CRC Press, Boca Raton, pp 133–158CrossRefGoogle Scholar
  76. Reichard M, Polačik M, Sedláček O (2009) Distribution, colour polymorphism and habitat use of the African killifish, Nothobranchius furzeri, the vertebrate with the shortest lifespan. J Fish Biol 74:198–212CrossRefPubMedGoogle Scholar
  77. 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 28:1105–1120CrossRefGoogle Scholar
  78. Reichard M, Janáč M, Polačik M, Blažek R, Vrtílek M (2017) Community assembly in Nothobranchius annual fishes: nested patterns, environmental niche and biogeographic history. Ecol Evol 7:2294–2306CrossRefPubMedPubMedCentralGoogle Scholar
  79. Ribeiro AC (2006) Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of eastern Brazil: an example of faunal evolution associated with a divergent continental margin. Neotrop Ichthyol 4:225–246CrossRefGoogle Scholar
  80. Rolon AS, Maltchik L (2010) Does flooding of rice fields after cultivation contribute to wetland plant conservation in southern Brazil? Appl Veg Sci 13:26–35CrossRefGoogle Scholar
  81. Saraiva DD, Souza AF (2012) Effects of environmental factors and plantation forests on endangered cactus diversity and composition in subtropical south American grasslands. Perspect Plant Ecol 14(4):267–274CrossRefGoogle Scholar
  82. Saraiva DD, de Sousa KDS, Overbeck GE (2014) Multiscale partitioning of cactus species diversity in the south Brazilian grasslands: implications for conservation. J Nat Conserv 24:117–122CrossRefGoogle Scholar
  83. Schwartz SS, Jenkins DG (2000) Temporary aquatic habitats: constraints and opportunities. Aquat Ecol 34:3–8CrossRefGoogle Scholar
  84. SEMA (Secretaria do Ambiente e Desenvolvimento Sustentável do Rio Grande do Sul) (1994) Regiões hidrográficas do estado do Rio Grande do Sul. http://www.sema.rs.gov.br/conteudo.asp?cod_menu=54. Accessed: 16 March 2015
  85. Soininen J (2015) Spatial structure in ecological communities – a quantitative analysis. Oikos 125:160–166CrossRefGoogle Scholar
  86. Stenert C, Maltchik L (2007) Influence of area, altitude and hydroperiod on macroinvertebrate communities in southern Brazil wetlands. Mar Freshw Res 58:993–1001CrossRefGoogle Scholar
  87. Streck EV, Kämpf N, Dalmolin RSD, Klamt E, Nascimento PC, Schneider P, Giasson E, Pinto LFS (2008) Solos do Rio Grande do Sul. EMATER/RS-ASCAR, Porto AlegreGoogle Scholar
  88. Teresa FB, Souza Luzia S, Silva DMA, Barbosa HO, Lima JD, Nabout JC (2016) Environmental constraints structuring fish assemblages in riffles: evidences from a tropical stream. Neotrop Ichthyol 14:e150185CrossRefGoogle Scholar
  89. Valeriano MM, Rossetti DF (2011) Topodata: Brazilian full coverage refinement of SRTM data. Appl Geogr 32:300–309CrossRefGoogle Scholar
  90. Vasconcelos RP, Henriques S, França S, Pasquaud S, Cardoso I, Laborde M, Cabral HN (2015) Global patterns and predictors of fish species richness in estuaries. J Anim Ecol 84:1331–1341CrossRefPubMedGoogle Scholar
  91. Vaz-Ferreira R, Sierra de Soriano B, Soriano Señorans J (1966) Integración de la fauna de vertebrados en algunas masas de agua dulce temporales del Uruguay. Compendios de Trabajo del Departamento de Zoología Vertebrados de la Facultad de Humanidades y Ciencias. Universidad de la República, MontevideoGoogle Scholar
  92. Vega E, Baldi G, Jobbagy EG, Paruelo J (2009) Land use change patterns in the Río de la Plata grasslands: the influence of phytogeographic and political boundaries. Agric Ecosyst Environ 134:287–292CrossRefGoogle Scholar
  93. Volcan MV, Gonçalves ÂC, Lanés LEK (2011a) Distribution, habitat and conservation status of two threatened annual fishes (Rivulidae) from southern Brazil. Endanger Species Res 13:79–85CrossRefGoogle Scholar
  94. Volcan MV, Lanés LEK, Gonçalves ÂC, Cheffe MM (2011b) First record of annual killifish Austrolebias melanoorus (Amato, 1986) (Cyprinodontiformes: Rivulidae) from Brazil, with data on habitat and conservation. J Appl Ichthyol 27:1120–1122CrossRefGoogle Scholar
  95. Volcan MV, Gonçalves ÂC, Lanés LEK (2014a) Austrolebias quirogai (Actinopterygii: Cyprinodontiformes: Rivulidae) in Brazil: Occurence, population parameters, habitat characteristics, and conservation status. Acta Ichthyol Piscat 44:37–44CrossRefGoogle Scholar
  96. Volcan MV, Lanés LEK, Gonçalves ÂC (2014b) Austrolebias bagual, a new species of anual fish (Cyprinodontiformes: Rivulidae) from southern Brazil. Aqua 20:3–14Google Scholar
  97. Volcan MV, Gonçalves ÂC, Lanés LEK, Guadagnin DL (2015) Annual fishes (Rivulidae) from southern Brazil: a broad-scale assessment of their diversity and conservation. In: Berois N, García G, de Sá RO (eds) Annual fishes: life history strategy, diversity and evolution. CRC Press, Boca Raton, pp 185–204CrossRefGoogle Scholar
  98. Watters BR (2009) The ecology and distribution of Nothobranchius fishes. J Am Killifish Ass 42:58–61Google Scholar
  99. Weber E, Hasenack H (org.) (2007) Base cartográfica digital do Rio Grande do Sul - escala 1: 250.000. UFRGS, Porto AlegreGoogle Scholar
  100. Williams DD (2006) The biology of temporary waters. New York, OxfordGoogle Scholar
  101. Winemiller KO, Jepsen DB (1998) Effects of seasonality and fish movement on tropical river food webs. J Fish Biol 53:267–296CrossRefGoogle Scholar
  102. 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 182:389–414CrossRefPubMedGoogle Scholar
  103. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith G (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar
  104. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Luis Esteban Krause Lanés
    • 1
    • 2
    • 3
  • Martin Reichard
    • 4
  • Rafael Gomes de Moura
    • 1
  • Robson S. Godoy
    • 1
  • Leonardo Maltchik
    • 1
  1. 1.Laboratório de Ecologia e Conservação de Ecossistemas AquáticosUniversidade do Vale do Rio dos Sinos (UNISINOS)São LeopoldoBrazil
  2. 2.Instituto Pró-Pampa, Laboratório de IctiologiaPelotasBrazil
  3. 3.Programa de Pós-Graduação em Zoologia, Laboratório de Fisiologia da Conservação, Faculdade de BiociênciasPontifícia Universidade Católica do Rio Grande do Sul (PUCRS)Porto AlegreBrazil
  4. 4.Institute of Vertebrate BiologyAcademy of Sciences of the Czech RepublicBrnoCzech Republic

Personalised recommendations