Skip to main content
Log in

Integrating field and laboratory evidence for environmental sex determination in the amphipod, Echinogammarus marinus

  • Short Communication
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The causes of sex determination in amphipods are believed to be multi-factorial. Sex determination in Echinogammarus marinus (Leach, 1815) has been reported to be linked with feminising parasites. To date, however, no such studies have linked this species with environmental sex determination (ESD). A field study and laboratory breeding experiments were conducted to determine the influence of photoperiod on sex determination. Over the two-year field study, males dominated during August to November, whilst female-biased populations were observed during April to July. A significant linear relationship was observed between photoperiods and sex ratios from the field data. Under laboratory conditions, photoperiod was also shown to be an influential factor in sex determination, with a male bias over a long-day photo regime (61.5 % male broods) and a female biased over a short-day photoperiod regime (43.5 % male broods). Findings suggest that there is some level of ESD present within the species, suggesting considerable plasticity in the sex differentiation pathway.

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

References

  • Adams J, Greenwood P, Naylor C (1987) Evolutionary aspects of environmental sex determination. Rep Int Dev Res Cent Can 11:123–135

    Google Scholar 

  • Appadoo C, Myers AA (2004) Reproductive bionomics and life history traits of three gammaridean amphipods, Cymadusa filosa Savigny, Ampithoe laxipodus Appadoo and Myers and Mallacoota schellenbergi Ledoyer from the tropical Indian Ocean (Mauritius). Acta Oecol 26:227–238

    Article  Google Scholar 

  • Baron B, Buckle F, Espina S (2002) Environmental factors and sexual differentiation in Poecilia sphenops Valenciennes (Pisces: Poeciliidae). Aquac Res 33:615–619

    Article  Google Scholar 

  • Bull JJ (1980) Sex determination in reptiles. Q Rev Biol 55:3–21

    Article  Google Scholar 

  • Bulnheim H (1978) Interaction between genetic, external and parasitic factors in sex determination of the crustacean amphipod, Gammarus duebeni. Helgoland Mar Res 31:1–33

    Google Scholar 

  • Castiglioni DS, Buckup GB (2008) Ecological traits of two sympatric species of Hyalella Smith, 1874 (Crustacea, Amphipoda, Dogielinotidae) from southern Brazil. Acta Oecol 33:36–48

    Article  Google Scholar 

  • Conover DO, Kynard BE (1981) Environmental sex determination—Interaction of temperature and genotype in a fish. Science 213:577–579

    Article  CAS  Google Scholar 

  • Doi W, Yokota M, Struessmann CA, Watanabe S (2008) Growth and reproduction of the portunid crab Charybdis bimaculata (Decapoda: Brachyura) in Tokyo Bay. J Crustacean Biol 28:641–651

    Article  Google Scholar 

  • Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263

    Article  Google Scholar 

  • Dunn AM, Adams J, Smith JE (1993) Is intersexuality a cost of environmental sex determination in Gammarus duebeni? J Zool 231:383–389

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Dunn AM, Hogg JC, Kelly A, Hatcher MJ (2005) Two cues for sex determination in Gammarus duebeni: adaptive variation in environmental sex determination? Limnol Oceanogr 50:346–353

    Article  Google Scholar 

  • Fisher RA (1958) The genetical theory of natural selection. Dover, New York

    Google Scholar 

  • Ford AT, Glazier DS (2008) Persistently high levels of intersexuality in male-biased amphipod populations. Zoology 111:401–409

    Article  Google Scholar 

  • Ford AT, Rodgers-Gray TP, Davies IM, Dunn AM, Read PA, Robinson CD, Smith JE, Fernandes TF (2005) Abnormal gonadal morphology in intersex, Echinogammarus marinus (Amphipoda): a possible cause of reduced fecundity? Mar Biol 147:913–918

    Article  Google Scholar 

  • Ford AT, Fernandes TF, Robinson CD, Davies IM, Read PA (2006) Can industrial pollution cause intersexuality in the amphipod, Echinogammarus marinus? Mar Pollut Bull 53:100–106

    Article  CAS  Google Scholar 

  • Janzen FJ, Paukstis GL (1991) Environmental Sex Determination in Reptiles: ecology, evolution and experimental design. Q Rev Biol 66:149–179

    Article  CAS  Google Scholar 

  • Kato Y, Kobayashi K, Watanabe H, Iguchi T (2011) Environmental sex determination in the branchiopod crustacean Daphnia magna: deep Conservation of a doublesex gene in the sex-determining pathway. PLoS Genet 7:3

    Article  Google Scholar 

  • Kelly A, Hatcher MJ, Dunn AM (2004) Intersexuality in the amphipod Gammarus duebeni results from incomplete feminisation by the vertically transmitted parasitic sex ratio distorter Nosema granulosis. Evol Ecol 18:121–132

    Article  Google Scholar 

  • Korpelainen H (1990) Sex-ratios and conditions required for environmental sex determination in animals. Biol Rev 65:147–184

    Article  CAS  Google Scholar 

  • Lasker R, Wells JBJ, McIntyre AD (1970) Growth, reproduction, respiration and carbon utilisation of sand-dwelling harpacticoid copepod, Asellopsis intermedia. J Mar Biol Assoc UK 50:147–160

    Article  Google Scholar 

  • Legrand JJ, Legrand-Hamelin E, Juchault P (1987) Sex determination in Crustacea. Biol Rev 62:439–470

    Article  Google Scholar 

  • Lincoln JL (1979) British marine Amphipoda: Gammaridea. British Natural History Museum, London

    Google Scholar 

  • Litulo C (2005) Life history of the crab, Macrophthalmus boscii (Audouin, 1826) (Decapoda, Brachyura, Ocypodidae). Crustaceana 78:665–676

    Article  Google Scholar 

  • MacArthur RH (1965) Ecological consequences of natural selection. Blaisdell, New York

    Google Scholar 

  • Maly EJ (1970) Influence of predation on adult sex ratios of 2 copepod species. Limnol Oceanogr 15:566–573

    Article  Google Scholar 

  • Maranhao P, Bengala N, Pardal M, Marques J (2001) The influence of environmental factors on the population dynamics, reproductive biology and productivity of Echinogammarus marinus Leach (Amphipoda, Gammaridae) in the Mondego estuary (Portugal). Acta Oecol 22:139–152

    Article  Google Scholar 

  • Martins I, Ford AT, Fernandes TF (2009) Intersexuality incidence, sex ratio fluctuations and intersex reproductive output as factors affecting the temporal variation of intersexed populations of the marine amphipod Echinogammarus marinus. Mar Environ Res 68:163–169

    Article  CAS  Google Scholar 

  • Mautner SI, Cook KA, Forbes MR, McCurdy DG, Dunn AM (2007) Evidence for sex ratio distortion by a new microsporidian parasite of a Corophiid amphipod. Parasitology 134:1567–1573

    Article  CAS  Google Scholar 

  • May RM (1983) Sexual systems—when to be which sex. Nature 301:16–17

    Article  CAS  Google Scholar 

  • Múrias T, Cabral JA, Marques JC, Goss-Custard JD (1996) Short-term effects of intertidal macroalgal blooms on the macrohabitat selection and feeding behaviour of wading birds in the Mondego estuary (West Portugal). Estuar Coast Shelf S 43:677–688

    Article  Google Scholar 

  • Naylor C, Adams J (1987) Sexual dimorphism, drag constraints and male performance in Gammarus duebeni (Amphipoda). Oikos 48:23–27

    Article  Google Scholar 

  • Naylor C, Adams J, Greenwood PJ (1988a) Population dynamics and adaptive sexual strategies in a brackish water crustacean, Gammarus duebeni. J Anim Ecol 57:493–507

    Article  Google Scholar 

  • Naylor C, Adams J, Greenwood PJ (1988b) Variation in sex determination in natural populations of a shrimp. J Evol Biol 1:355–368

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  CAS  Google Scholar 

  • Petersen JJ (1972) Factor affecting sex-ratios of a mermithid parasite of mosquitos. J Nematol 4:83–87

    CAS  Google Scholar 

  • Prato E, Trono A, Biandolino F (2009) Life History of Talorchestia deshayesii (Amphipoda, Talitridae) in the Ionian Sandy Beach (Southern Italy). Braz Arch Biol Technol 52:911–922

    Article  Google Scholar 

  • Saher NU, Qureshi NA (2011) Density, distribution and population structure of Opusia indica (Ocypodoidae: Camptandriidae) in a coastal mangrove creek in Pakistan. Biologia 66:138–145

    Article  Google Scholar 

  • Sanchez L (2008) Sex-determining mechanisms in insects. Int J Dev Biol 52:837–856

    Article  CAS  Google Scholar 

  • Short S, Guler Y, Kille P, Ford AT (2012) Paramyxean-microsporidian co-infection in amphipods: is the consensus that Microsporidia can feminise their hosts presumptive? Int J paristol 42:683–691

    Article  Google Scholar 

  • Tyler EHM, Somerfield PJ, Berghe EV, Bremner J, Jackson E, Langmead O, Palomares MLD, Webb TJ (2012) Extensive gaps and biases in our knowledge of a well-known fauna: implications for integrating biological traits into macroecology. Global Ecol Biogeogr. doi:10.1111/j.1466-8238.2011.00726.x

    Google Scholar 

  • Visser ME, Both C, Lambrechts MM (2004) Global climate change leads to mistimed avian reproduction. Adv Ecol Res 35:89–110

    Article  Google Scholar 

  • Vlasblom AG (1969) A study of a population of Marinogammarus marinus (leach) in the oosterschelde. Neth J Sea Res 4:317–338

    Article  Google Scholar 

  • Watt PJ, Adams J (1994) Adaptive variation in sex determination in a crustacean, Gammarus duebeni. J Zool 232:109–116

    Article  Google Scholar 

  • Yang G, Short S, Kille P, Ford AT (2011) Microsporidia infections in the amphipod, Echinogammarus marinus (Leach): suggestions of varying causal mechanisms to intersexuality. Mar Biol 158:461–470

    Article  Google Scholar 

Download references

Acknowledgments

YG and SS are supported by the Natural Environment Research Council (UK) grant (NE/G004587/1) awarded to PK and ATF. We are appreciative to Amaia Etxabe Green and Joanna Murry for their assistance with field work and figure preparation, respectively.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alex T. Ford.

Additional information

Communicated by S. A. Poulet.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guler, Y., Short, S., Kile, P. et al. Integrating field and laboratory evidence for environmental sex determination in the amphipod, Echinogammarus marinus . Mar Biol 159, 2885–2890 (2012). https://doi.org/10.1007/s00227-012-2042-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-012-2042-2

Keywords

Navigation