Marine Biology

, Volume 151, Issue 4, pp 1407–1415 | Cite as

Transport of brine shrimps via the digestive system of migratory waders: dispersal probabilities depend on diet and season

  • Marta I. Sánchez
  • Andy J. GreenEmail author
  • Francisco Amat
  • Eloy M. Castellanos
Research Article


Waterbirds are known to disperse invertebrate propagules that survive gut passage, but there is very little information about how the probability of dispersal changes at different times of the annual cycle when birds move in different directions, or how it is affected by changes in diet. We studied internal transport of brine shrimp Artemia cysts by migratory waders in the Odiel saltworks in south-west Spain. Viable cysts of parthenogenetic Artemia were abundant in the faeces and regurgitated pellets of redshank Tringa totanus, pellets of spotted redshank T. erythropus, and faeces of black-tailed godwit Limosa limosa during spring and/or autumn migrations in 2001–2002, but were not recorded during winter. Godwits did not produce pellets, and spotted redshank faeces were not sampled. Significant correlations between the number of cysts in a pellet or faecal sample and the proportion of that sample constituted by Artemia adults suggested that most cysts were ingested while in the ovisacs of gravid females. The proportion of cysts destroyed during digestion increased when accompanied by harder food items or grit, and when fewer cysts were ingested. The median number of intact cysts was higher in redshank faeces than in their pellets, but cysts extracted from pellets were more likely to hatch. A higher proportion of redshank pellets contained Artemia cysts in spring than in autumn, but more redshank migrated through the area in autumn. Significantly fewer cysts were recorded in redshank pellets in winter than in spring or autumn. Our results confirm that there is potential for long-distance dispersal of Artemia cysts via waders during both northwards (spring) and southwards (autumn) migrations.


Brine Shrimp Spring Migration Autumn Migration Artemia Cyst Artemia Population 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study has been partially funded by the Spanish R&D National Plan (projects BOS2003-02846 and CGL2004-03719). The first author was supported by a Ph.D. grant from the Ministerio de Ciencia y Tecnología and an I3P postgraduate grant from the Consejo Superior de Investigaciones Científicas. The Consejería de Medio Ambiente, Junta de Andalucía and Aragonesas Industrias y Energía S.A. provided permission to work in the saltworks. J.C. Rubio provided logistical support and advice. J. Figuerola and anonymous referees provided valuable comments on the manuscript.


  1. Abatzopoulos TJ, Beardmore JA, Clegg JS, Sorgeloos P (2002) Artemia: basic and applied biology. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  2. Amat F, Hontoria F, Ruiz O, Green AJ, Sánchez MI, Figuerola J, Hortas F (2005) The American brine shrimp Artemia franciscana as an exotic invasive species in the Western Mediterranean. Biol Invas 7:37–47CrossRefGoogle Scholar
  3. Baxevanis AD, Kappas I, Abatzopoulos TJ (2006) Molecular phylogenetics and asexuality in the brine shrimp Artemia. Mol Phyl Evol 40:724–738CrossRefGoogle Scholar
  4. Bohonak AJ, Jenkins DG (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecol Lett 6:783–796CrossRefGoogle Scholar
  5. Britton RH, Johnson AR (1987) An ecological account of a mediterranean salina: the Salin de Giraud, Camargue (S. France). Biol Cons 42:185–230CrossRefGoogle Scholar
  6. Browne RA, Hoopes CW (1990) Genotype diversity and selection in asexual brine shrimp (Artemia). Evol 44:1035–1051Google Scholar
  7. Castro G, Myers JP (1993) Shorebird predation on eggs of horseshoe crabs during spring stopover on Delaware Bay. The Auk 110:927–929CrossRefGoogle Scholar
  8. Charalambidou I, Santamaría L, Jansen C, Nolet B (2005) Digestive plasticity in mallard ducks modulates dispersal probabilities of aquatic plants and crustaceans. Funct Ecol 19:513–519CrossRefGoogle Scholar
  9. Clausen P, Nolet BA, Fox AD, Klaassen M (2002) Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in northern Europe-a critical review of possibilities and limitations. Acta Oecologia 23:191–203CrossRefGoogle Scholar
  10. Crawley MJ (1993) GLIM for ecologists. Blackwell, CambridgeGoogle Scholar
  11. Darwin C (1859) On the origin of species by means of natural selection. John Murray, LondonGoogle Scholar
  12. del Hoyo J, Elliott A, Sargatal J (eds) (1996) Handbook of the birds of the world, vol 3. Lynx Edicions, BarcelonaGoogle Scholar
  13. de Meester L, Gómez A, Okamura B, Schwenk K (2002) The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecologia 23:121–135CrossRefGoogle Scholar
  14. de Vlaming V, Proctor VW (1968) Dispersal of aquatic organisms: viability of seeds recovered from the droppings of captive killdeer and mallard ducks. Am J Bot 55:20–26CrossRefGoogle Scholar
  15. Dodson SI, Egger DL (1980) Selective feeding of red phalaropes on zooplankton of arctic ponds. Ecol 61:755–763CrossRefGoogle Scholar
  16. Farmer AH, Parent AH (1997) Effects of the landscape on shorebird movements at spring migration stopovers. Condor 99:698–707CrossRefGoogle Scholar
  17. Figuerola J, Green AJ (2002a) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshw Biol 47:483–494CrossRefGoogle Scholar
  18. Figuerola J, Green AJ (2002b) How frequent is external transport of seeds and invertebrate eggs by waterbirds? A study in Doñana, SW Spain. Archi Hydrobiol 155:557–565CrossRefGoogle Scholar
  19. Figuerola J, Green AJ, Santamaría L (2002) Comparative dispersal effectiveness of wigeongrass seeds by waterfowl wintering in south-west Spain: quantitative and qualitative aspects. J Ecol 90:989–1001CrossRefGoogle Scholar
  20. Figuerola J, Green AJ, Santamaria L (2003) Passive internal transport of aquatic organisms by waterfowl in Donana, south-west Spain. Glob Ecol Biogeogr 12:427–436CrossRefGoogle Scholar
  21. Green AJ, Figuerola J (2005) Recent advances in the study of long-distance dispersal of aquatic invertebrates via birds. Divers Distrib 11:149–156CrossRefGoogle Scholar
  22. Green AJ, Figuerola J, Sánchez MI (2002) Implications of waterbird ecology for the dispersal of aquatic organisms. Acta Oecologia 23:177–189CrossRefGoogle Scholar
  23. Green AJ, Sánchez MI (2006) Passive internal dispersal of insect larvae by migratory birds. Biol Lett 2:55–57CrossRefGoogle Scholar
  24. Green AJ, Sánchez MI, Amat F, Figuerola J, Hontoria F, Hortas F (2005) Dispersal of invasive and native brine shrimp Artemia (Anostraca) via waterbirds. Limnol Oceanogr 50:737–742CrossRefGoogle Scholar
  25. Havel JE, Shurin JB (2004) Mechanisms, effects, and scales of dispersal in freshwater zooplankton. Limnol Oceanogr 49:1229–1238CrossRefGoogle Scholar
  26. Horne FR (1966) The effect of digestive enzymes on the hatchability of Artemia salina eggs. Trans Am Micr Soc 85:271–274CrossRefGoogle Scholar
  27. Iverson GC, Warnock SE, Butler RW, Bishop MA, Warnock N (1996) Spring migration of western sandpipers along the Pacific Coast of North America: a telemetry study. Condor 98:10–21CrossRefGoogle Scholar
  28. MacDonald GH (1980) The use of Artemia cysts as food by the flamingo (Phoenicopterus ruber roseus) and the shelduck (Tadorna tadorna). In: Persoone G, Sorgeloos P, Roels O, Jaspers E (eds) The brine shrimp Artemia. Ecology, culturing, use in aquaculture, vol 3. Universa Press, pp97–104Google Scholar
  29. Nogales M, Medina FM, Quilis V, González-Rodríguez M (2001) Ecological and biogeographical implications of Yellow-Legged Gulls (Larus cachinnans Pallas) as seed dispersers of Rubia fruticosa Ait. (Rubiaceae) in the Canary Islands. J Biogeog 28:1137–1145CrossRefGoogle Scholar
  30. Pennycuick CJ, Battley PF (2003) Burning the engine: a time-marching computation of fat and protein consumption in a 5420-km non-stop flight by great knots, Calidris tenuirostris. Oikos 103:323–332CrossRefGoogle Scholar
  31. Proctor VW (1964) Viability of crustacean eggs recovered from ducks. Ecol 45:656–658CrossRefGoogle Scholar
  32. Proctor VW, Malone CR, deVlaming VL (1967) Dispersal of aquatic organisms: viability of disseminules recovered from the intestinal tract of captive Killdeer. Ecol 48:672–676CrossRefGoogle Scholar
  33. Rice WR (1989) Analyzing tables of statistical tests. Evol 43:223–225CrossRefGoogle Scholar
  34. Sánchez MI, Green AJ, Castellanos EM (2005) Seasonal variation in the diet of the redshank Tringa totanus in the Odiel Marshes, south-west Spain: a comparison of faecal and pellet analysis. Bird Study 52:210–216CrossRefGoogle Scholar
  35. Sánchez MI, Green AJ, Castellanos EM (2006a) Spatial and temporal fluctuations in use by shorebirds and in availability of chironomid prey in the Odiel saltpans, south-west Spain. Hydrobiologia 567:329–340CrossRefGoogle Scholar
  36. Sánchez MI, Green AJ, Castellanos EM (2006b) Internal transport of seeds by migratory waders in the Odiel marshes, south-west Spain: consequences for long-distance dispersal. J Avian Biol 37:201–206CrossRefGoogle Scholar
  37. Sánchez MI, Green AJ, Castellanos EM (2006c) Temporal and spatial variation of an aquatic invertebrate community subjected to avian predation at the Odiel salt pans (SW Spain). Arch Hydrobiol 166:199–223CrossRefGoogle Scholar
  38. SAS Institute Inc (2000) SAS/STAT ® software, User’s Guide. Cary, NCGoogle Scholar
  39. StatSoft (1999) Statistica 5.5. Tusla, OK: StatSoftGoogle Scholar
  40. Stroud DA, Davidson NC, West R, Scott DA, Haanstra L, Thorup O, Ganter B, Delany S (2004) Status of migratory wader populations in Africa and Western Eurasia in the 1990s. Int Wader Stud 15:1–259Google Scholar
  41. Welham CVJ (1994) Flight speeds of migrating birds: a test of maximum range speed predictions from three aerodynamic equations. Behav Ecol 5:1–8CrossRefGoogle Scholar
  42. Wetlands International (2002) Waterbird population estimates, 3rd edn. Wetlands international global series No. 12. Wageningen, The NetherlandsGoogle Scholar
  43. Wolf N (2001) Foraging ecology and site selection in Western Sandpipers during their fall migration through southwestern British Columbia. Masters Thesis, Biological Sciences. Simon Fraser UniversityGoogle Scholar
  44. Wurtsbaugh WA, Maciej Gliwicz Z (2001) Limnological control of brine shrimp population dynamics and cyst production in the Great Salt Lake, Utah. Hydrobiologia 466:119–132CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Marta I. Sánchez
    • 1
    • 2
    • 4
  • Andy J. Green
    • 1
    Email author
  • Francisco Amat
    • 3
  • Eloy M. Castellanos
    • 2
  1. 1.Wetland Ecology GroupEstación Biológica de Doñana-CSICSevillaSpain
  2. 2.Departamento de Biología Ambiental y Salud Pública, Facultad de Ciencias ExperimentalesUniversidad de HuelvaHuelvaSpain
  3. 3.Instituto de Acuicultura de Torre de la Sal-CSICRibera de CabanesSpain
  4. 4.Génétique et Evolution des Maladies Infectieuses (GEMI), UMR CNRS/IRD 2724Montpellier Cedex 5France

Personalised recommendations