, Volume 767, Issue 1, pp 51–63 | Cite as

Life history patterns are correlated with predictable fluctuations in highly seasonal environments of semi-terrestrial burrowing crayfish

  • A. V. Palaoro
  • E. del Valle
  • M. Thiel
Primary Research Paper


Animals living in extreme environments with predictable seasonality may have important life history events correlated to favourable periods. These animals pass critical life stages in protected habitats, especially during early life, often receiving parental care. It is thus hypothesized that juveniles rely on protective microhabitats provided by their parents, becoming independent only during favourable seasons. Semi-terrestrial crayfish Parastacus pugnax inhabit burrows in highly seasonal and predictable environments, thus being well suited to test this hypothesis. Following marked burrows and individual crayfish we examined the life history patterns of P. pugnax in their natural environment to test the predictions that (i) burrowing activity is higher during the wet season, (ii) reproductive events occur during favourable seasons and (iii) juveniles only disperse after reaching larger sizes. There was little or no burrowing activity during the dry season, when soil was more compact, but burrows became wider and had more openings during the wet season. After hatching, juveniles cohabited with adults for at least 4 months during the dry season. During this period juveniles grew considerably, starting independent lives during the wet season. These results suggest that the prolonged parent-offspring cohabitation evolved in response to the predictable seasonal variations in the crayfish habitat.


Behavioural adaptations Fossorial species Parastacus pugnax Parental care Seasonality 



We thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship to AVP. We also thank two anonymous reviewers for many constructive suggestions, which helped to considerably improve the manuscript.

Supplementary material

10750_2015_2475_MOESM1_ESM.docx (152 kb)
Supplementary material 1 (DOCX 152 kb)


  1. Angers, D. A. & J. Caron, 1998. Plant-induced changes in soil structure: processes and feedbacks. Biogeochemistry 42: 55–72.CrossRefGoogle Scholar
  2. Arias, P. & D. Muñoz, 1991. Antecedentes bioecologicos del camarón de vega (Parastacus pugnax Poeppig, 1835) en el área del Chillán. Agro-Ciencias 7: 167–172.Google Scholar
  3. Bennett, N. C. & C. G. Faulkes, 2000. African Mole-Rats: ecology and Eusociality. Cambridge University Press, Cambridge.Google Scholar
  4. Bonilla, C. A., C. Bonomelli & G. Urrutia, 2002. Spatial and temporal distribution of precipitation and soil water content at three forest sites of the VIII Region of Chile. Agricultura Técnica 62: 541–554.CrossRefGoogle Scholar
  5. Bovbjerg, R. V., 1956. Some factors affecting aggressive behaviour in crayfish. Physiological Zoology 29: 127–136.CrossRefGoogle Scholar
  6. Brett, R. A., 1991. The ecology of naked mole-rat colonies: burrowing, food and limiting factors. In Sherman, P. W., J. U. Jarvis & R. D. Alexander (eds), The Biology of the Naked Mole-Rat. Princeton Univesity Press, New Jersey: 97–136.Google Scholar
  7. Cardoso, R. S. & V. G. Veloso, 1996. Population biology and secondary production of the sandhopper Pseudorchestoidea brasiliensis (Amphipoda: Talitridae) at Prainha Beach, Brazil. Marine Ecology Progress Series 142: 111–119.CrossRefGoogle Scholar
  8. Dalosto, M. M., A. V. Palaoro & S. Santos, 2012. Mother-offspring relationship in the Neotropical burrowing crayfish Parastacus pilimanus (Von Martens, 1869) (Decapoda, Parastacidae). Crustaceana 85: 1305–1315.CrossRefGoogle Scholar
  9. Danks, H. V., 2002. Modification of adverse conditions by insects. Oikos 99: 10–24.CrossRefGoogle Scholar
  10. Danks, H. V., 2007. The elements of seasonal adaptations in insects. The Canadian Entomologist 139: 1–44.CrossRefGoogle Scholar
  11. Egan, R. S. & P. W. C. Paton, 2004. Within-pond parameters affecting oviposition by wood frogs and spotted salamanders. Wetlands 24: 1–13.CrossRefGoogle Scholar
  12. Eversole, A. G. & S. M. Welch, 2013. Ecology of the primary burrowing crayfish Distocambarus crockeri. Journal of Crustacean Biology 33: 660–666.CrossRefGoogle Scholar
  13. Fontoura, N. F. & L. Buckup, 1989. O crescimento de Parastacus brasiliensis (von Martens, 1869) (Crustacea, Decapoda, Parastacidae). Revista Brasileira de Biologia 49: 897–909.Google Scholar
  14. Gasith, A. & V. H. Resh, 1999. Streams in Mediterranean climate regions: abiotic influences and biotic responses to predictable seasonal events. Annual Review of Ecology and Systematics 30: 51–81.CrossRefGoogle Scholar
  15. Gómez, C. L., J. R. Maldonado & M. R. G. Rojas, 2015. Soil permeability in the Chillán river Basin, between Estero Peladillas and the Ñuble river, Chile. Revista Colombiana de Geografía 24: 73–86.CrossRefGoogle Scholar
  16. Gonzalez-Voyer, A. & N. Kolm, 2010. Parental care and investment. In Encyclopedia of Life Sciences. Wiley, Chichester. Doi: 10.1002/9780470015902.a0021907.
  17. Grow, L., 1981. Burrowing behaviour in the crayfish, Cambarus diogenes diogenes Girard. Animal Behaviour 29: 351–356.CrossRefGoogle Scholar
  18. Hamr, P. & A. M. M. Richardson, 1994. Life history of Parastacoides tasmanicus tasmanicus Clark, a burrowing freshwater crayfish from South-western Tasmania. Australian Journal of Marine and Freshwater Research 45: 455–470.CrossRefGoogle Scholar
  19. Helms, B. S., C. Figiel, J. Rivera, J. Stoeckel, G. Stanton & T. A. Keller, 2013. Life-history observations, environmental associations, and soil preferences of the Piedmont blue burrower (Cambarus [Depressicambarus] harti) Hobbs. Southeastern Naturalist 12: 143–160.CrossRefGoogle Scholar
  20. Herbst, M. & N. C. Bennett, 2006. Burrow architecture and burrowing dynamics of the endangered Namaqua dune mole rat (Bathyergus janetta) (Rodentia: Bathyergidae). Journal of Zoology 270: 420–428.CrossRefGoogle Scholar
  21. Herbst, M., J. U. M. Jarvis & N. C. Bennett, 2004. Non-invasive assessment of reproductive seasonality in the Red data listed wild Namaqua dune mole-rat Bathyergus janetta. Journal of Zoology 263: 259–268.CrossRefGoogle Scholar
  22. Hobbs Jr, H. H. & M. Whiteman, 1991. Notes on the burrows, behavior, and color of the crayfish Fallicambarus (F.) devastator (Decapoda: Cambaridae). The Southwestern Naturalist 6: 127–135.CrossRefGoogle Scholar
  23. Horwitz, P. H. J., A. M. M. Richardson & P. M. Cramp, 1985. Aspects of the life history of the burrowing freshwater crayfish Engaeus leptorhyncus at Rattrays marsh, North East Tasmania. Tasmanian Naturalist 82: 1–5.Google Scholar
  24. Ibarra, M. A. & P. M. Arana, 2011. Growth of burrowing crayfish Parastacus pugnax (Poeppig, 1835) determined by marking technique. Latin American Journal of Aquatic Research 39: 378–384.CrossRefGoogle Scholar
  25. Ibarra, M. A. & P. M. Arana, 2012. Biological parameters of the burrowing crayfish, Parastacus pugnax (Poeppig, 1835), in Tiuquilemu, Bío-Bío Region, Chile. Latin American Journal of Aquatic Research 40: 418–427.CrossRefGoogle Scholar
  26. Johnston, K. & B. J. Robson, 2009. Commensalism used by freshwater crayfish species to survive drying in seasonal habitats. Invertebrate Biology 128: 269–275.CrossRefGoogle Scholar
  27. Katandukila, J. V., C. T. Chimimba, N. C. Bennett, R. H. Makundi, S. C. Le Comber & C. G. Faulkes, 2014. Sweeping the house clean: burrow architecture and seasonal digging activity in the East African root rat from Tanzania. Journal of Zoology 293: 271–280.CrossRefGoogle Scholar
  28. Linsenmair, K. E., 2007. Sociobiology of terrestrial isopods. In Duffy, J. E. & M. Thiel (eds), Evolutionary Ecology of Social and Sexual Systems—Crustaceans as Model Organisms. Oxford University Press, New York: 339–364.CrossRefGoogle Scholar
  29. Lovegrove, B. G., 1989. The cost of burrowing by the social mole-rate (Bathyergidae) Cryptomys damarensis and Heterocephalus glaber: the role of soil moisture. Physiological Zoology 62: 449–469.CrossRefGoogle Scholar
  30. Martínez, A. W. & E. H. Rudolph, 2011. Records of intersexuality in the burrowing crayfish, Parastacus pugnax (Poeppig, 1835) (Decapoda, Parastacidae) with comments on the sexuality of the species of Parastacus. Crustaceana 84: 221–241.CrossRefGoogle Scholar
  31. Noro, C. K. & L. Buckup, 2008. Estrutura populacional e biologia reprodutiva de Parastacus defossus (Crustacea: Decapoda: Parastacidae). Zoologia 25: 624–629.Google Scholar
  32. Noro, C. K. & L. Buckup, 2009. O crescimento de Parastacus defossus (Crustacea: Decapoda: Parastacidae). Zoologia 26: 54–60.CrossRefGoogle Scholar
  33. Noro, C. K. & L. Buckup, 2010. The burrows of Parastacus defossus (Decapoda: Parastacidae), a fossorial freshwater crayfish from Southern Brazil. Zoologia 27: 341–346.CrossRefGoogle Scholar
  34. Nowak, M. A., C. A. Tarnita & E. O. Wilson, 2010. The evolution of eusociality. Nature 466: 1057–1062.PubMedCentralCrossRefPubMedGoogle Scholar
  35. Osawa, N., 2000. Population field studies on the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): resource tracking and population characteristics. Population Ecology 42: 115–127.CrossRefGoogle Scholar
  36. Palaoro, A. V., M. M. Dalosto, C. Coutinho & S. Santos, 2013. Assessing the importance of burrows through behavioral observations of Parastacus brasiliensis, a neotropical burrowing crayfish (Crustacea), in laboratory conditions. Zoological Studies 52: 4.CrossRefGoogle Scholar
  37. R Core Team, 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing (ed.). Vienna, Austria.Google Scholar
  38. Rasa, O. A. E., 1995. Ecological factors influencing burrow location, group size and mortality in a nocturnal fossorial Kalahari detritivore, Parastizopus armaticeps Peringuey (Coleoptera: Tenebrionidae). Journal of Arid Environments 29: 353–365.CrossRefGoogle Scholar
  39. Rasa, O. A. E., 1999. Division of labor and extended parenting in a desert tenebrionid beetle. Ethology 105: 37–56.CrossRefGoogle Scholar
  40. Reynolds, S. J., K. A. Christian, C. R. Tracy & L. B. Hutley, 2011. Changes in body fluids of the cocooning fossorial frog Cyclorana australis in a seasonally dry environment. Comparative Biochemistry and Physiology part A: Molecular & Integrative Physiology 160: 348–354.CrossRefGoogle Scholar
  41. Richardson, A. M. M., 2007. Behavioral ecology of semiterrestrial crayfish. In Duffy, J. E. & M. Thiel (eds), Evolutionary Ecology of Social and Sexual Systems—Crustaceans As Model Organisms. Oxford University Press, New York: 320–338.Google Scholar
  42. Rotherham, D. & R. J. West, 2003. Comparison of methods for sampling poopulations of ghost shrimp, Trypaea australiensis (Decapoda: Thalassinidea: Calassinidae). Fisheries Research 60: 585–591.CrossRefGoogle Scholar
  43. Rudolph, E. H., 1997. Intersexualidad en el camarón excavador Parastacus pugnax (Poeppig, 1835) (Decapoda, Parastacidae). Investigaciones Marinas 25: 7–18.CrossRefGoogle Scholar
  44. Rudolph, E. H., 2013. Parastacus pugnax (Poeppig, 1835) (Crustacea, Decapoda, Parastacidae): conocimiento biológico, presión extractiva y perspectivas de cultivo. Latin American Journal of Aquatic Research 41: 611–632.CrossRefGoogle Scholar
  45. Segev, O., M. Mangel, N. Wolf, A. Sadeh, A. Kershenbaum & L. Blaustein, 2011. Spatiotemporal reproductive strategies in the fire salamander. Behavioral Ecology 22: 670–678.CrossRefGoogle Scholar
  46. Stieglitz, T., P. Ridd & P. Müller, 2000. Passive irrigation and functional morphology of crustacean burrows in a tropical mangrove swamp. Hydrobiologia 421: 69–76.CrossRefGoogle Scholar
  47. Šumbera, R., J. Šklíba, M. Elichová, W. N. Chitaukali & H. Burda, 2008. Natural history and burrow system architecture of the silvery mole-rat from Brachystegia woodland. Journal of Zoology 274: 77–84.Google Scholar
  48. Suter, P. J. & A. M. M. Richardson, 1977. The biology of two species of Engaeus (Decapoda: Parastacidae) in Tasmania III—habitat, food, associated fauna and distribution. Australian Journal of Marine and Freshwater Research 28: 95–103.CrossRefGoogle Scholar
  49. Trivers, R., 1972. Parental investment and sexual selection. In Campbell, B. (ed.), Sexual Selection and the Descent of Man. Aldine Publishing Company, Chicago: 136–179.Google Scholar
  50. Trumbo, S. T., 2012. Patterns of parental care in invertebrates. In Royle, N. J., P. T. Smiseth & M. Kölliker (eds), The Evolution of Parental Care. Oxford University Press, New York: 81–100.CrossRefGoogle Scholar
  51. Williams, D. D., N. E. Williams & H. B. N. Hynes, 1974. Observations on the life history and burrow construction of the crayfish Cambarus fodiens (Cottle) in a temporary stream in southern Ontario. Canadian Journal of Zoology 52: 365–370.CrossRefGoogle Scholar
  52. Zagal, E., N. Rodríguez, I. Vidal & L. Quezada, 2002. Microbial activity in a volcanic ash soil under different agricultural management. Agricultura Técnica 62: 297–309.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Programa de Pós-Graduação em Biodiversidade AnimalUniversidade Federal de Santa MariaSanta MariaBrazil
  2. 2.Facultad de Ciencias del MarUniversidad Católica del NorteCoquimboChile
  3. 3.Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI)CoquimboChile
  4. 4.Centro de Estudios Avanzados en Zonas Áridas (CEAZA)CoquimboChile

Personalised recommendations