Skip to main content
Log in

Occurence of intersexuality in a laboratory culture of the copepod Eurytemora affinis from the Seine estuary (France)

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

We show in this study that intersexuality can occur in the estuarine copepod Eurytemora affinis, and we reported the presence of three intersexual copepod individuals from a laboratory culture of this species from the Seine estuary conducted at low temperature (7°C). These individuals presented both female and male characteristics. The prosome size and antennules of intersex individuals were similar to those of normal females, but all the other morphological details were more similar to normal males. The appearance of the three intersex individuals in the culture at low temperature coincided with a decrease in food quality due to a feeding with Rhodomonas marina at its stationary phase. This induced a significant decrease in the mean clutch size and skewed sex-ratio in favor of males. The reduction in food quality in addition to low temperature of 7°C (which induced slow development) is suspected to be responsible of the appearance of intersex individuals. This stressful situation seems to propagate to the following two generations at low temperature in contrast to the case of the experiment at higher temperature 20°C where no intersex individual was observed. These results confirmed the role of food quality in sex determination of copepods. Moreover, the role of early developmental stages and also the consequences of stressful conditions throughout different generations were discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Allsop DJ, West SA (2003) Changing sex at the same relative body size. Nature 425:783–784

    Article  CAS  PubMed  Google Scholar 

  • Allsop DJ, West SA (2004) Sex ratio evolution in sex changing animals. Evolution 58:1019–1027

    PubMed  Google Scholar 

  • Atz JW (1964) Intersexuality in fishes. In: Armstrong CN, Marshall AJ (eds) Intersexuality in vertebrates including man. Academic Press, New York, pp 145–232

    Google Scholar 

  • Bayly IAE, Shiel RJ (2008) Intersexuality in Boeckella triarticulata (Thomson, 1883) (Copepoda, Calanoida): a trap for unwary taxonomists. Crustaceana 81:299–304

    Article  Google Scholar 

  • Berenike A, Diekmann S, Peck MA, Holste L, St Jean MA, Campbell RW (2009) Variation in diatom biochemical composition during a simulated bloom and its effect on copepod production. J Plankton Res 31:1391–1405

    Article  CAS  Google Scholar 

  • Buston PM, Munday PL, Warner RR (2004) Sex change and relative body size in animals. Nature. 02512 doi: 10.1038

  • Cailleaud K, Forget-Leray J, Souissi S, Hilde D, LeMenach K, Budzinski H (2007) Seasonal variations of hydrophobic organic contaminant concentrations in the water-column of the Seine Estuary and their transfer on a planktonic species Eurytemora affinis (Calanoïda, copepoda). Part1: PCBSs and PAHs. Chemosphere 70:270–280

    Article  CAS  PubMed  Google Scholar 

  • Cailleaud K, Forget-Leray J, Pehulet L, LeMenach K, Souissi S, Budzinski H (2009) Tidal influence on the distribution of hydrophobic organic contaminants in the Seine Estuary and on their biological effects on the copepod Eurytemora affinis. Environ Pollut 157:64–71

    Article  CAS  PubMed  Google Scholar 

  • Charnov EL (1982) The theory of sex allocation. Monogr Popul Biol 18:1–355

    CAS  PubMed  Google Scholar 

  • Devreker D (2007) Etude de la dynamique de population du copépode Eurytemora affinis dans l’estuaire de la Seine: une approche combinée in situ et expérimentale. PhD thesis, Université du Havre, France. 150 pp

  • Devreker D, Souissi S, Seuront L (2004) Effects of individual variability on the development and mortality of the first naupliar stages of Eurytemora affinis (Copepoda, Calanoida) under different conditions of salinity and temperature. J Exp Mar Biol Ecol 303:31–46

    Article  Google Scholar 

  • Devreker D, Souissi S, Forget-Leray J, Leboulenger F (2007) Effects of salinity and temperature on the post embryonic development of Eurytemora affinis (Copepoda; Calanoida) of the Seine estuary: a laboratory study. J Plankton Res 29:i117–i133

    Article  Google Scholar 

  • Devreker D, Souissi S, Molinero JC, Nkibuto F (2008) Trade-offs of the copepod Eurytemora affinis in mega-tidal estuaries. Insights from high frequency sampling in the Seine Estuary. J Plankton Res 30:1329–1342

    Article  Google Scholar 

  • Devreker D, Souissi S, Winkler G, Forget-Leray J, Leboulenger F (2009) Effects of salinity and temperature on the reproduction of Eurytemora affinis (Copepoda; Calanoida) from the Seine estuary: a laboratory study. J Exp Mar Biol Ecol 368:113–123

    Article  Google Scholar 

  • Dharani G, Altaff K (2002) Facultative sex reversal in the freshwater plankton Sinodiaptomus (Rhinediaptomus) indicus Calanoida: copepoda. Curr Sci 82:794–795

    Google Scholar 

  • Dunn AM, Adams J, Smith JE (1990) Intersexs in shrimp: a possible disadvantage of environmental sex determination. Evolution 44:1875–1878

    Article  Google Scholar 

  • Dunn AM, McCabe J, Adams J (1996) Intersexuality in Gammarus duebenii (Amphipoda), a cost incurred in population with environmental sex determination ? Crustaceana 69:313–320

    Article  Google Scholar 

  • Dur G, Souissi S, Devreker D, Ginot V, Schmitt FG, Hwang J-S (2009) Effect of temperature and individual variability on the reproduction of the estuarine copepod Eurytemora affinis Individual-based experimental and modelling approach. Ecol Model 220:1073–1089

    Article  Google Scholar 

  • Fleminger A (1985) Dimorphism and possible sex change in copepods of the family Calanidae. Mar Biol 28:273–294

    Article  Google Scholar 

  • Ford AT, Fernandes TF, Riders SA, Read PA, Robinson CD, Davies IM (2003) Reproduction in theamphipod, Echinogammarus marinus a comparison between normal and intersex specimens. J Mar Biol Ass UK 83:937–940

    Article  Google Scholar 

  • Ford AT, Fernandes TF, Riders SA, Read PA, Robinson CD, Davies IM (2004) The coasts of intersexuality: a crustacean perspective. Mar Biol 145:951–957

    Article  Google Scholar 

  • Forget-Leray J, Landriau I, Minier C, Leboulenger F (2005) Impact of endocrine toxicants on survival, development, and reproduction of the estuarine copepod Eurytemora affinis (Poppe). Ecotox Environ Safety 60:288–294

    Article  CAS  Google Scholar 

  • Gusmão LFM, McKinnon AD (2009) Sex ratios, intersexuality and sex change in copepods. J Plankton Res 31:1101–1117

    Article  Google Scholar 

  • Hartwell SI, Wright DA, Savitz JD (1993) Relative sensitivity of survival, growth and reproduction of Eurytemora affinis (Copepoda) to assessing polluted estuaries. Water Air Soil Pollut 71:281–291

    Article  CAS  Google Scholar 

  • Ianora A, Mazzochi MG, Scotto Di Carlo B (1987) Impact of parasitism and intersexuality on Mediterranean populations of Paracalanus parvus (Copepoda; Calanoida). Dis Aqua Org 3:29–36

    Article  Google Scholar 

  • Katona SK (1973) Evidence for sex pheromones in planktonic copepods. Limnol Oceanogr 18:574–583

    Article  Google Scholar 

  • Koski M, Engström J, Viitasalo M (1999) Reproduction and survival of the calanoid copepod Eurytemora affinis fed with toxic and non-toxic cyanobacteria. Mar Ecol Prog Ser 186:187–197

    Article  Google Scholar 

  • LeBlanc GA (2007) Crustacean endocrine toxicology: a review. Ecotoxicology 16:61–81

    Article  CAS  PubMed  Google Scholar 

  • Minier C, Levy F, Rabel D, Bocquené G, Godefroy D, Burgeot T, Leboulenger F (2000) Flounder health status in the Seine Bay. A multibiomarker study. Mar Environ Res 50:373–377

    Article  CAS  PubMed  Google Scholar 

  • Ohtsuka S, Huys R (2001) Sexual dimorphism in calanoid copepods: morphology and function. Hydrobiologia 453(454):441–466

    Article  Google Scholar 

  • Olmstead AW, LeBlanc GA (2007) The environmental–endocrine basis of gynandromorphism (intersex) in a crustacean. Int J Biol 3:77–84

    CAS  Google Scholar 

  • Rasband WS (1997–2008) ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA. http://rsb.info.nih.gov/ij/

  • Schminke HK (2007) Entomology for the copepodologist. J Plankton Res 29:i49–i62

    Google Scholar 

  • Sillett KB, Stemberger S (1998) Masculinized female in a population of Leptodiaptomus minitus (copepoda, calanoida). Can J Zool 76:596–600

    Article  Google Scholar 

  • Souissi S, Ginot V, Seuront L, Uye S-I (2004) Using multi-agent systems to develop individual based models for copepods: consequences of individual behaviour and spatial heterogeneity on the emerging properties at the population scale. In: Seuront L, Strutton P (eds) Handbook of scaling methods in aquatic ecology: measurement, analysis, simulation. CRC Press, Boca Raton, pp 527–546

    Google Scholar 

  • Souissi S, Daly Yahia MN, Hwang J-S (2007) Foreword (copepod special issue). J Plankton Res 29:i1–i2

    Article  Google Scholar 

  • Swell RBS (1951) The epibionts and parasites of the planktonic copepoda of the Arabian Sea. John Murray expedition. Sci Rep BM (NH) 9:253–394

    Google Scholar 

  • Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92

    Article  CAS  PubMed  Google Scholar 

  • West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295:1685–1688

    Article  CAS  PubMed  Google Scholar 

  • West SA, Reece SE, Sheldon BC (2002) Sex ratios. Heridity 88:117–124

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Financial support was provided by the program Seine Aval. This work is a contribution to ZOOSEINE project funded by Seine-Aval IV program. This paper is a contribution to the bilateral project between the National Science Council (NSC) of Taiwan and the National Centre for Scientific Research (CNRS) of France. This paper is part of A. Souissi PhD project. We are grateful to James J. Pierson for his comments and improvements of the English. We also thank A. Simiand and D. Ballenghien for their help with algal and copepod cultures. We thank both anonymous reviewers for their valuable comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sami Souissi.

Additional information

Communicated by X. Irigoien.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Souissi, A., Souissi, S., Devreker, D. et al. Occurence of intersexuality in a laboratory culture of the copepod Eurytemora affinis from the Seine estuary (France). Mar Biol 157, 851–861 (2010). https://doi.org/10.1007/s00227-009-1368-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1368-x

Keywords

Navigation