Environmental Biology of Fishes

, Volume 100, Issue 8, pp 995–1006 | Cite as

Life history strategies of annual killifish Millerichthys robustus (Cyprinodontiformes:Cynolebiidae) in a seasonally ephemeral water body in Veracruz, México

  • Omar Domínguez-Castanedo
  • Mari Carmen Uribe
  • Ana María Rosales-TorresEmail author


The annual life cycle of Millerichthys robustus is described from an ephemeral pool in Veracruz, Mexico. The state of the pool can be divided into three periods: a flood period lasting from September to March when the pool was filled with water, a drought period from April to June when the pool was dry, and a humid period in July and August when the pool was intermittently filled. Soil substrate was examined in each of these three periods (flood, drought and humid), embryos were found, and the stage of embryonic diapause was determined. During the flood period embryos were in diapause I; during the drought period in diapause II; and during the humid period mainly in diapause III with a small subset in diapause II (an example of a bet-hedging strategy). Two hatching periods (separated by two weeks) were documented during the beginning of the flood period. Fish growth was analyzed in both males and females, with females showing an overall slower growth rate and smaller adult size. In females, ovarian maturity was characterized histologically to understand the reproductive cycle. The onset of sexual maturity began during the third week after hatching (21 days) with the presence of secondary sexual characteristics in females and the beginning of Secondary Growth Stage in some ovarian follicles. All stages of oogenesis, postovulatory follicles and ovulated oocytes were observed from the fourth week post hatching (28 days) until death. M. robustus appears to exhibit similar patterns of embryonic diapause compared to other annual killifish living in seasonal water bodies closer to the equator. This study characterizes (for the first time) the adaptations and life cycle of M. robustus. This information could be useful to evaluate the potential risk of these populations and, if necessary, to develop plans for their conservation.


Reproductive cycle Growth Diapause Oogenesis Life cycle Annualism 



We appreciate the help and support of Victor Rosales Perez and Miguel Mosqueda with the collection of specimens in the field. To Stefano Valdesalici, Bela Nagy, Richard Martino (AKA) and Robert Meyer (AKA) for the valuable information suggested and provided, and to Comisión Nacional de Ciencia y Tecnología for scholarship No. 375928. We thank the academic counseling of Bruno A. Marichal Cancino and Liliana García-Calva in this project. (Sampling, management and procedures performed in this research were authorized by SGPA/DGVS/02404/14, /2015 of the Subsecretaría de Gestión para la Protección Ambiental, Dirección General de Vida Silvestre, SEMARNAT). We also sincerely appreciate the thorough and detailed comments by the reviewers that allowed for improvement of this work.


  1. Aguilar-Morales M, Coutiño BB, Rosales SP (1996) Manual general de técnicas histológicas y citoquímicas. México, D.F. Facultad de Ciencias, UNAM, México, D.FGoogle Scholar
  2. Arenzon A, Caravalho A, Camino M (1999) Reproduction of the annual fish Cynopoecilus melanotaenia (Regan, 1912) in a temporary water body in Rio Grande do Sur, Brazil (Cyprinodontiformes, Rivulidae). Hydrobiologia 411(0):65–70CrossRefGoogle Scholar
  3. Arenzon A, Peret CA, Bohrer MB (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). Bras J Biol 61:117–123CrossRefGoogle Scholar
  4. Balaẑek R, Polačik M, Reichard M (2013) Rapid growth, early maturation and short generation time in African anual fishes. EvoDevo 4:24. doi: 10.1186/2041-9139-4-24 CrossRefGoogle Scholar
  5. Berois N, Arezo JM, Papa GN, Clivo AG (2012) Annual fish: developmenal adaptations for an extreme environment. Wiley Interdiscip Rev Dev Biol 1(4):595–602. doi: 10.1002/wdev.39 CrossRefPubMedGoogle Scholar
  6. Berois N, Arezo JM, de Sá OR (2014) The neotropical genus Austroplebias: an emerging model of annual killifishes. Cell Dev Biol 3(2):1000136. doi: 10.4172/2168-9296.1000136 Google Scholar
  7. Brown-Peterson N, Wyanski D, Saborido-Rey F, Macewicz B, Lowerre-Barbier SK (2011) A standardized terminology for describing reproductive development in fishes. Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science 3:52–70. doi: 10.1080/19425120.2011.555724 CrossRefGoogle Scholar
  8. Costa WJEM (2011) Phylogenetic position and taxonomic status of Anablepsoides, Atlantirivulus, Cynodonichthys, Laimosemion and Melanorivulus (Cyprinodontiformes: Rivulidae). Ichthyol Explor Fres 22(3):233–249Google Scholar
  9. Costa WJEM (2013) Historical biogeography of aplocheiloid killifishes (Teleostei: Cypronodontiformes). Vertebrate Zoology 63(2):139–154Google Scholar
  10. da Silva GC, Pereira SU, Volcan VM (2011) The opportunistic feeding and reproduction strategies of the annual fish Cynopoecilus melanotaenia (Cyprinodontiformes: Rivulidae) inhabiting ephimeral habitats on southern Brazil. Neotrop Ichthyol 9(1):191–200. doi: 10.1590/S1679-62252011000100019 CrossRefGoogle Scholar
  11. De Vlaming V, Grossman G, Chapman F (1982) On the use the gonadosomatic index. Comp Biochem Physiol 73A(1):31–39CrossRefGoogle Scholar
  12. Domínguez-Castanedo O, Mosqueda-Cabrera MA, Valdesalici S (2013) First observations of annualism in Millerichthys robustus (Cyprinodontiformes: Rivulidae). Ichthyol Explor Fres 24(1):15–20Google Scholar
  13. Dorn A, Musilova 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 14:210–223. doi: 10.1186/s12862-014-0210-3 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Eschmeyer WN, Fong JD (2016) Species by family/subfamily. Institute for Biodiversity Sciences and Sustainability. California Academy of Sciences. http://researcharchive.Calacademy.Org/research/ichthyology/catalog/SpeciesByFamily.Asp. Accessed 30 Sept 2016
  15. Froese R (2006) Cube law, condition factor and weight-length relationships: history, meta-analysis and recomendations. J Appl Ichthyol 22(4):241–253. doi: 10.1111/j.1439-0426.2006.00805.x CrossRefGoogle Scholar
  16. Furness IA (2015) The evolution of an annual life cycle in killifish: adaptation to ephemeral aquatic environments through embryonic diapause. Biol Rev. doi: 10.1111/brv.12194
  17. Furness IA, Lee K, Reznick ND (2015) Adaptation in a variable environment: phenotypic plasticity and bet-hedging during egg diapause and hatching in an annual killifish. Evolution 69(6):1461–1475. doi: 10.1111/evo.12669 CrossRefPubMedGoogle Scholar
  18. Grier JH, Mari U, Patiño R (2009) The ovary, Folliculogenesis, and Oogenesis in Teleosts. In: Jamieson BGM (ed) Reproductive Biology and physiology of fishes (Agnsthans and bony fishes). Science Publishers, USA, pp 25–86Google Scholar
  19. Hoaglin D, Mosteller F, Tukey J (1991) Fundamentals of exploratory analysis of variance. Wiley, New YorkCrossRefGoogle Scholar
  20. 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(1):23–33. doi: 10.1002/jez.1402150104 CrossRefPubMedGoogle Scholar
  21. Krause LLE, Wolfgang OF, 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(31–32):1971–1988. doi: 10.1080/00222933.2013.862577 Google Scholar
  22. Lorenzen ED, Heller R, Siegismund HR (2012) Comparative phylogeography of African savannah ungulates. Mol Ecol 21(15):3656–3670. doi: 10.1111/j.1365-294X.2012.05650.x CrossRefPubMedGoogle Scholar
  23. Loureiro M, de Sá OR (2016) Diversity of Aplocheiloidei. In: Berois N, García G, de Sá OR (eds) Annual fishes: life history strategy, divesity and evolution. CRC Press, Taylor and Francis Group, USA, pp 3–31Google Scholar
  24. Markofsky J, Matias JR (1977) The effect of temperature and season of collection on the onset and duration of diapause in embryos of the annual fish Nothobranchius guentheri. J Exp Zool 202:49–56. doi: 10.1002/jez.1402020107 CrossRefPubMedGoogle Scholar
  25. Markofsky J, Matias JR, Inglima K, Vogelman JH, Orentreich N (1979) The variable effects of ambient and artificial light: dark cycles on embryonic diapause in a laboratory population of the annual fish Nothobranchius guentheri. J Exp Biol 83:203–225Google Scholar
  26. Medina M (1979) El factor de condición múltiple (KM) y su importancia en el manejo de las carpas de Israel (Cyprinus carpio); hembras en estado de madurez V (Nikolsky, 1963). Manuales Técnicos de Acuacultura. Departamento de Pesca, MéxicoGoogle Scholar
  27. Miller RR (2009) Peces dulceacuícolas de México. CONABIO, Sociedad Ictiológica Mexicana, El Colegio de la Frontera Sur y el Consejo de Peces del Desierto, México-Estados Unidos. Ciudad de México, MéxicoGoogle Scholar
  28. Murphy WJ, Collier EG (1997) A molecular phylogeny for aplocheiloid fishes (Atherinomorpha: Cyprinodontiformes): the role of vicariance and the origins of annualism. Mol Biol Evol 14(8):790–799CrossRefPubMedGoogle Scholar
  29. Passos C, Tassino B, Rosenthal GG, Reichard M (2016) Reproductive behavior and sexual selection in annual fishes. In: Berois N, García G, de Sá OR (eds) Annual fishes: life history strategy, divesity and evolution. CRC Press, Taylor and Francis Group, USA, pp 207–229Google Scholar
  30. Pinceel T, Vanschoenwinkel B, Deckers P, Grégoir A, Ver Eecke T, Brendonck L (2015) Early and late developmental arrest as complementary embryonic bet-hedging strategies in African killifish. Biol J Linn Soc 114(4):941–948. doi: 10.1111/bij.12474 CrossRefGoogle Scholar
  31. Podrabsky J, Hand C (1999) The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus. J Exp Biol 202:2567–2580PubMedGoogle Scholar
  32. Podrabsky J, Hand CS (2015) Physiological strategies during animal diapause: lessons from brine shrimp and annual killifish. J Exp Biol 218:1897–1906. doi: 10.1242/jeb.116194 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Podrabsky J, Carpenter J, Hand S (2001) Survival of water stress in annual fish embryos: dehydration avoidance and egg envelope amyloid fibers. Am J Physiol Integrative Comp Physiol 280:123–131Google Scholar
  34. Podrabsky J, Tingaud-Sequeira A, Cerdá J (2010b) Metabolic dormancy and responses to environmental desiccation in fish embryos. In: Lubzens E (ed) dormancy and resistance in harsh environments. Top Curr Genet 21:203–226CrossRefGoogle Scholar
  35. Podrabsky J, Garrett I, Kohl F (2010a) Alternative developmental pathways associated with diapause regulated by temperature and maternal influences in embryos of the annual killifish Austrofundulus limnaeus. J Exp Biol 213:3280–3288. doi: 10.1242/jeb.045906 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Polačik M, Donner TM, Reichard M (2011) Age structure of annual Nothobranchius fishes in Mozambique: is there a hatching synchrony? J Fish Biol 78:796–809. doi: 10.1111/j.1095-8649.2010.02893.x CrossRefPubMedGoogle Scholar
  37. Polačik M, Balaẑek R, Režucha R, Vrtílek M, Terzibasi-Tozzini E, Reichard M (2014) Alterntive intrapopulation life-history strategies and their trade-offs in an African annual fish. J Evol Biol 27:854–865. doi: 10.1111/jeb.12359 CrossRefPubMedGoogle Scholar
  38. Reichard M (2016) The evolutionary ecology of african annual fishes. In: Berois N, García G, de Sá OR (eds) Annual fishes: life history strategy, divesity and evolution. CRC Press, Taylor and Francis Group, USA, pp 133–158Google Scholar
  39. Ribeiro AC (2006) Tectonic history and the biogeography of the freshwater fishes from the coastal drainages of estern Brazil: an example of faunal evolution associated with a divergent continental margin. Neotrop Ichthyol 4:225–246. doi: 10.1590/1982-0224-20130228 CrossRefGoogle Scholar
  40. Ricker WE (1975) Computation and interpretation of biological statistics of fish population. Department of the Environment Fisheries and Marine Services. Ottawa Bulletin 191:203–204Google Scholar
  41. Schalk MC, Montaña GC, Libson EM (2014) Reproductive strategies of two Neotropical killifish, Austrolebias vandenbergi and Neofundulus ornatipinnis (Cyprinodontiformes: Rivulidae) in the Bolivian gran Chaco. Rev Biol Trop 62(1):109–117CrossRefPubMedGoogle Scholar
  42. Shidlovskiy KM (2010) Collecting Notobranchius in south-western Tanzania. Nothobranchius Archives 1:18–27Google Scholar
  43. Tanizaki K (1988) Ecología de peixes anuaisraros do Estado de Rio de Janeiro – género Cynolebias Stridachner, 1876 (Cyprinodontiformes, Rivulidae). In congreso Brasileiro de Zoología, Brazil 15:318Google Scholar
  44. Terzibasi TE, Valenzano M, Benedetti M, Roncaglia P, Cattaneo A, Domenici L, Cellerino A (2008) Large differences in aging phenotype between strains of the short-lived annual fish Nothobranchius furzeri. PLoS One 12(3):e3866. doi: 10.1371/journal.pone.0003866 CrossRefGoogle Scholar
  45. Terzibasi TE, Dorn A, Ng’oma E, Polačik M, Balaẑek R, Reichwald K, Petzold A, Watters B, Reichard M, Cellerino A (2013) Parallel evolution of senescence in annual fishes in response to extrinsic mortality. BMC Evol Biol 13:77–89. doi: 10.1186/1471-2148-13-77 CrossRefGoogle Scholar
  46. Valdesalici S (2013, 2013) Pronothobranchius chirioi n. sp. A new annual killifish species from the Niger River drainage, with redescription of P. kiyawensis, P. gambiensis and P. seymouri (Cyprinodontiformes: Nothobranchiidae). Killi-Data Seres:21–41Google Scholar
  47. Valdesalici S, Cellerino A (2003) Extremely short lifespan in the annual fish Nothobranchius furzeri. P Roy Soc Lond B Bio 270:189–191. doi: 10.1098/rsbl.2003.0048 CrossRefGoogle Scholar
  48. Vaz-Ferreira R, Sierra de Soriano, Scagila B (1964) Ecología de la reproducción de los peces del genero Cynolebias Stridachner. Arch Soc Biol Montevideo 161–171Google Scholar
  49. Volcan MV, Fonseca PA, Figueiredo MR, Sampaio AL, Robaldo BR (2012) Effect of temperature on growth of the threatened annual fish Austrolebias nigrofasciatus Costa y Cheffe 2001. Biota Neotrop 12(4):1–6CrossRefGoogle Scholar
  50. Volcan MV, Gonҫalves CA, Guadagnin LD (2013) Length-weight relationship of three annual fishes (Rivulidae) from temporary freshwater wetlands of southern Brazil. J Appl Ichthyol 29:1188–1190. doi: 10.1111/jai.12214 CrossRefGoogle Scholar
  51. Wallace AR, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am Zool 21(2):325–343CrossRefGoogle Scholar
  52. Watters BR (2009) The ecology and distribution of Nothobranchius fishes. J Am Killifish Assoc 42:37–76Google Scholar
  53. Wildekamp RH, Romand R, Scheel JJ (1986) Cyprinodontidae. In: Daget J, Gosse PJ, Thys van den Audenaerde FD (eds) Check-list of the freshwater fishes of Africa (CLOFFA). Brussels, MRAC; Tervuren; and ORSTOM, Paris, pp 165-276Google Scholar
  54. Wilderkamp RH (2004) A world of killies. Atlas of the oviparous Cyprinodontiform fishes of the world. American Killifish Association, MishawakaGoogle Scholar
  55. Williams DD (2006) The biology of temporary waters. Oxford University Press, New YorkGoogle Scholar
  56. Winemiller KO (2005) Life history strategies, population regulation, and implications for fisheries management. Can J Fish Aquat Sci 62(4):872–885. doi: 10.1139/f05-040 CrossRefGoogle Scholar
  57. Wootton RF (1991) Ecology of teleost fishes. Fish and fisheries. Sereies. Chapman & Hall, 2-6 Bodanz Row, LondonGoogle Scholar
  58. Wourms JP (1972a) Developmental biology of annual fishes. I. Stages in the normal development of Austrofundulus myersi. Dahl J Exp Zool 182:143–168CrossRefPubMedGoogle Scholar
  59. Wourms JP (1972b) Developmental biology of annual fishes. II. Naturally occurring dispersion and reaggregation of blastomers during the development of annual fish eggs. J Exp Zool 182:169–200CrossRefPubMedGoogle Scholar
  60. Wourms JP (1972c) Developmental biology of annual fishes. III. Pre-embryonic and embryonic diapause of variable duration in eggs of annual fishes. J Exp Zool 182:389–414CrossRefPubMedGoogle Scholar
  61. Young LJ, Bornik BZ, Marcotte LM, Charlie NK, Wagner NG, Hinch GS, Cooke JS (2006) Integrating physiology and life history to improve fisheries management and conservation. Fish Fish 7:262–283. doi: 10.1111/j.1467-2979.2006.00225.x CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  1. 1.Programa de Doctorado en Ciencias Biológicas y de la SaludUniversidad Autónoma MetropolitanaCoyoacanMexico
  2. 2.Laboratorio de Biología de la Reproducción, Departamento de Biología Comparada, Facultad de CienciasUniversidad Nacional Autónoma de MéxicoCoyoacanMéxico
  3. 3.Laboratorio Bioquímica de la Reproducción, Departamento de Producción Agrícola y AnimalUniversidad Autónoma Metropolitana-XochimilcoCoyoacánMéxico

Personalised recommendations