Demography and interannual variability of salp swarms (Thalia democratica)

Abstract

Swarms of the pelagic tunicate, Thalia democratica, form during spring, but the causes of the large interannual variability in the magnitude of salp swarms are unclear. Changes in asexual reproduction (buds per chain) of T. democratica populations in the coastal waters of south-east Australia (32–35°S) were observed in three austral springs (October 2008–2010). T. democratica abundance was significantly higher in 2008 (1,312 individuals m−3) than 2009 and 2010 (210 and 92 individuals m−3, respectively). There was a significant negative relationship (linear regression, r 2 = 0.61, F 1,22 = 33.83, P < 0.001) between abundance and asexual reproduction. Similarly, relative growth rates declined with decreasing abundance. Generalised additive mixed modelling showed that T. democratica abundance was significantly positively related to preferred food >2 μm in size (P < 0.05) and negatively related to the proportion of non-salp zooplankton (P < 0.001). Salp swarm magnitude, growth, and asexual reproduction may depend on the abundance of larger phytoplankton (prymnesiophytes and diatoms) and competition with other zooplankton.

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References

  1. Alldredge AL, Madin LP (1982) Pelagic tunicates: unique herbivores in the marine plankton. Bioscience 32:655–663

    Article  Google Scholar 

  2. Andersen V (1998) Salp and pyrosomid blooms and their importance in biogeochemical cycles. In: Bone Q (ed) The biology of pelagic tunicates. Oxford University Press, New York, pp 125–138

    Google Scholar 

  3. Barlow RG, Mantoura RFC, Gough MA, Fileman TW (1993) Pigment signatures of the phytoplankton composition in the northeastern Atlantic during the 1990 spring bloom. Deep Sea Res Part II 40:459–477

    Article  Google Scholar 

  4. Blackburn M (1979) Thaliacea of the California current region: relations to temperature, chlorophyll, currents, and upwelling. Calif Coop Ocean Fish Investig Rep 20:184–193

    Google Scholar 

  5. Braconnot JC (1963) Study of the annual cycle of salps and doliolids in Rade de Villefranche-sur-mer. ICES/CIEM Int Counc Explor Sea 28:21–36

    Google Scholar 

  6. Brett M (2004) When is a correlation between non-independent variables “spurious”? Oikos 105:647–656

    Article  Google Scholar 

  7. Bruland KW, Silver MW (1981) Sinking rates of fecal pellets from gelatinous zooplankton (Salps, Pteropods, Doliolids). Mar Biol 63:295–300

    Article  Google Scholar 

  8. Clarke KR, Warwick RM (2001) Changes in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, Plymouth

    Google Scholar 

  9. Clarke KR, Somerfield PJ, Gorley RN (2008) Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Biol Ecol 366:56–69

    Article  Google Scholar 

  10. Cresswell GR (1994) Nutrient enrichment of the Sydney continental shelf. Mar Freshw Res 45:677–691

    Article  Google Scholar 

  11. Deibel D (1982) Laboratory determined mortality, fecundity and growth-rates of Thalia democratica Forskal and Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea). J Plankton Res 4:143–153

    Article  Google Scholar 

  12. Deibel D, Lowen B (2012) A review of the life cycles and life-history adaptations of pelagic tunicates to environmental conditions. ICES J Mar Sci 69:358–369

    Article  Google Scholar 

  13. Deibel D, Paffenhofer GA (2009) Predictability of patches of neritic salps and doliolids (Tunicata, Thaliacea). J Plankton Res 31:1571–1579

    Article  Google Scholar 

  14. Doblin MA, Petrou KL, Shelly K, Westwood K, van den Enden R, Wright S, Griffiths B, Ralph PJ (2011) Diel variation of chlorophyll-a fluorescence, phytoplankton pigments and productivity in the Sub-Antarctic and Polar Front Zones south of Tasmania, Australia. Deep Sea Res Part II 58:2189–2199

    CAS  Article  Google Scholar 

  15. Dubischar CD, Bathmann UV (1997) Grazing impact of copepods and salps on phytoplankton in the Atlantic sector of the Southern Ocean. Deep-Sea Res Part II Top Stud Oceanogr 44:415–433

    Article  Google Scholar 

  16. Everett JD, Baird ME, Suthers IM (2011) Three-dimensional structure of a swarm of the salp Thalia democratica within a cold-core eddy off southeast Australia. J Geophys Res 116:C12046

    Article  Google Scholar 

  17. Foxton P (1966) The distribution and life-history of Salpa thompsoni Foxton with observations on a related species, Salpa gerlachei Foxton. Discov Rep 34:1–116

    Google Scholar 

  18. Goericke R, Repeta DJ (1992) The pigments of Prochlorococcus marinus—the presence of divinyl chlorophyll-a and chlorophyll-b in a marine prokaryote. Limnol Oceanogr 37:425–433

    CAS  Article  Google Scholar 

  19. Hastie TJ, Tibshirani RJ (1990) Generalized additive models. Chapman & Hall, London

    Google Scholar 

  20. Hay S (2006) Marine ecology: gelatinous bells may ring change in marine ecosystems. Curr Biol 16:R679–R682

    CAS  Article  Google Scholar 

  21. Henschke N, Everett JD, Baird ME, Taylor MD, Suthers IM (2011) Distribution of life history stages of the salp Thalia democratica in shelf waters during a spring bloom. Mar Ecol Prog Ser 430:49–62

    Article  Google Scholar 

  22. Henschke N, Bowden DA, Everett JD, Holmes SP, Kloser RJ, Lee RW, Suthers IM (2013) Salp-falls in the Tasman Sea: a major food input to deep sea benthos. Mar Ecol Prog Ser. doi:10.3354/meps10450

  23. Heron AC (1972) Population ecology of a colonizing species—pelagic tunicate Thalia democratica. 1. Individual growth-rate and generation time. Oecologia 10:269–293

    Article  Google Scholar 

  24. Heron AC (1982) A vertical free fall plankton net with no mouth obstructions. Limnol Oceanogr 27:380–383

    Article  Google Scholar 

  25. Heron AC, Benham EE (1984) Individual growth rates of salps in three populations. J Plankton Res 6:811–828

    Article  Google Scholar 

  26. Heron AC, Benham EE (1985) Life history parameters as indicators of growth rate in three salp populations. J Plankton Res 7:365–379

    Article  Google Scholar 

  27. Heron AC, McWilliam PS, Dalpont G (1988) Length weight relation in the salp Thalia democratica and potential of salps as a source of food. Mar Ecol Prog Ser 42:125–132

    Article  Google Scholar 

  28. Jeffrey SW, Mantoura RFC, Wright SW (1997) Phytoplankton pigments in oceanography: guidelines to modern methods monographs on oceanographic methodology. UNESCO Publishing, Paris

  29. Kemp S, Hardy MA (1929) The ships, their equipment and the methods used in research. Discov Rep 1:181–189

    Google Scholar 

  30. Lavaniegos BE, Ohman MD (2003) Long-term changes in pelagic tunicates of the California current. Deep Sea Res Part II 50:2473–2498

    CAS  Article  Google Scholar 

  31. Le Borgne R, Moll P (1986) Growth rates of the salp Thalia democratica in Tikehau atoll (Tuamotu is.). Océanographie Tropicale 21:23–29

    Google Scholar 

  32. Lewontin RC (1965) Selection for colonizing ability. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 77–94

    Google Scholar 

  33. Licandro P, Ibanez F, Etienne M (2006) Long-term fluctuations (1974–1999) of the salps Thalia democratica and Salpa fusiformis in the northwestern Mediterranean Sea: relationships with hydroclimatic variability. Limnol Oceanogr 51:1832–1848

    Article  Google Scholar 

  34. Madin LP, Kremer P, Wiebe PH, Purcell JE, Horgan EH, Nemazie DA (2006) Periodic swarms of the salp Salpa aspera in the Slope Water off the NE United States: biovolume, vertical migration, grazing, and vertical flux. Deep Sea Res Part I 53:804–819

    Article  Google Scholar 

  35. Mantoura RFC, Llewellyn CA (1983) The rapid determination of algal chlorophyll and carotenoid pigments and their breakdown products in natural waters by reverse-phase high-performance liquid chromatography. Anal Chim Acta 151:297–314

    CAS  Article  Google Scholar 

  36. Miller RL, Cosson J (1997) Timing of sperm shedding and release of aggregates in the salp Thalia democratica (Urochordata: Thaliacea). Mar Biol 129:607–614

    Article  Google Scholar 

  37. Oke PR, Sakov P (2012) Assessing the footprint of a regional ocean observing system. J Mar Syst 105–108:30–51

    Article  Google Scholar 

  38. Pakhomov EA, Froneman PW, Perissinotto R (2002) Salp/krill interactions in the Southern Ocean: spatial segregation and implications for the carbon flux. Deep Sea Res Part II 49:1881–1907

    CAS  Article  Google Scholar 

  39. Partridge L, Gems D, Withers DJ (2005) Sex and death: what is the connection? Cell 120:461–472

    CAS  Article  Google Scholar 

  40. Siegel V, Harm U (1996) The composition, abundance, biomass and diversity of the epipelagic zooplankton communities of the southern Bellinghausen Sea (Antarctic) with special reference to krill and salps. Arch Fish Mar Res 44:115–139

    Google Scholar 

  41. Sutherland KR, Madin LP, Stocker R (2010) Filtration of submicrometer particles by pelagic tunicates. Proc Natl Acad Sci USA 107:15129–15134

    CAS  Article  Google Scholar 

  42. Thompson H (1948) Pelagic tunicates of Australia. Commonwealth Council for Scientific and Industrial Research, Melbourne, pp 136–139

    Google Scholar 

  43. Thompson H, Kesteven GL (1942) Pelagic tunicates in the plankton of south-eastern Australian waters, and their place in oceanographic studies. Council for Scientific and Industrial Research, Melbourne 153

    Google Scholar 

  44. Tranter DJ (1962) Zooplankton abundance in Australasian waters. Mar Freshw Res 13:106–142

    Article  Google Scholar 

  45. Troedsson C, Bouquet J-M, Aksnes DL, Thompson EM (2002) Resource allocation between somatic growth and reproductive output in the pelagic chordate Oikopleura dioica allows opportunistic response to nutritional variation. Mar Ecol Prog Ser 243:83–91

    Article  Google Scholar 

  46. Tsuda A, Nemoto T (1992) Distribution and growth of salps in a Kuroshio warm-core ring during summer 1987. Deep Sea Res Part A 39(suppl 1):S219–S229

    Article  Google Scholar 

  47. Uitz J, Huot Y, Bruyant F, Babin M, Claustre H, Claustre H (2008) Relating phytoplankton photophysiological properties to community structure on large scales. Limnol Oceanogr 53:614–630

    Article  Google Scholar 

  48. Vargas CA, Madin LP (2004) Zooplankton feeding ecology: clearance and ingestion rates of the salps Thalia democratica, Cyclosalpa affinis and Salpa cylindrica on naturally occurring particles in the Mid-Atlantic Bight. J Plankton Res 26:827–833

    CAS  Article  Google Scholar 

  49. Wood SN (2006) Generalized additive models: an introduction with R. Chapman & Hall/CRC, Boca Raton

    Google Scholar 

  50. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R (statistics for biology and health). Springer, New York

    Google Scholar 

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Acknowledgments

This research was funded by ARC Discovery Grant DP0880078 held by I.M.S. and Mark E. Baird. The authors thank the captain and crew of the RV Southern Surveyor 10/2008, 05/2009, 08/2010, and 09/2010. We especially thank the 08/2010 chief scientist Dr. Matthew Taylor, CSIRO scientists, and our colleagues for their assistance during the voyages. We also thank the Plankton Ecology Laboratory, CSIRO, for Port Hacking zooplankton identifications and Dr. James Smith (UNSW) for help with statistical analyses. We would like to acknowledge the valuable reviews provided by the three anonymous reviewers that have helped to improve the clarity and focus of this manuscript. This is contribution 108 from the Sydney Institute of Marine Science.

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Correspondence to Natasha Henschke.

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Communicated by U. Sommer.

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Henschke, N., Everett, J.D., Doblin, M.A. et al. Demography and interannual variability of salp swarms (Thalia democratica). Mar Biol 161, 149–163 (2014). https://doi.org/10.1007/s00227-013-2325-2

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Keywords

  • Phytoplankton
  • Phytoplankton Community
  • Asexual Reproduction
  • Advance Very High Resolution Radiometer
  • Growth Index