SpringerLink
Log in

Photoperiod controls egg laying and caudodorsal cell hormone expression but not gonadal development in the pond snail Lymnaea stagnalis

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Photoperiod is a reliable cue to regulate growth and reproduction for seasonal adaptation. Although photoperiodism has been well studied in Chordata and Arthropoda, less is known about Mollusca. We examined photoperiodic effects on egg laying, body size, gonad-somatic index, oocyte size and relative amounts of caudodorsal cell hormone mRNA in individual rearing conditions in the pond snail Lymnaea stagnalis. Twenty-five weeks after hatching, the percentages of egg-laying snails under a photoperiod of 12 h light and 12 h darkness (12L:12D) were significantly smaller than those under longer days. The total numbers of eggs and egg masses under 12L:12D were significantly smaller than those under longer days. Significant differences between 16L:8D and 12L:12D were not observed in the soft body and ovotestis weight, and the gonad-somatic index. Photoperiodic effects were also not observed in oocyte diameters twenty-two weeks after hatching. Twenty-seven weeks after hatching amounts of caudodorsal cell hormone mRNA were significantly lower in the cerebral ganglia with commissure under 12L:12D than 16L:8D. L. stagnalis exhibited a clear photoperiodic response in egg laying and the amount of caudodorsal cell hormone mRNA, but not in gonadal development. Under 12L:12D suppression of caudodorsal cell hormone expression might suppress egg laying.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Code availability

For statistical analysis, R “R” was downloaded from “https://cran.ism.ac.jp/”, “http://aoki2.si.gunmau-u.ac.jp/R/src/Steel-Dwass.R”, encoding = ”euc-jp”.

References

  • Bailey SE (1981) Circannual and circadian rhythms in the snail Helix aspersa Müller and the photoperiodic control of annual activity and reproduction. J Comp Physiol A 142:89–94

    Article  Google Scholar 

  • Bernheim SM, Mayeri E (1995) Complex behavior induced by egg-laying hormone in Aplysia. J Comp Physiol A 176:131–136

    Article  CAS  Google Scholar 

  • Berry RW (1982) Seasonal modulation of synthesis of the neurosecretory egg-laying hormone of Aplysia. Dev Neurobiol 13:327–335

    Article  CAS  Google Scholar 

  • Bohlken S, Joosse J (1982) The effects of photoperiod on female reproductive activity and growth of the freshwater plumonate snail Lymnaea stagnalis kept under laboratory breeding conditions. Int J Inver Rep 4:213–222

    Article  Google Scholar 

  • Bohlkena S, Joossea J, Geraerts WPM (1987) Interaction of photoperiod, grou** and isolation in female reproduction of Lymnaea stagnalis. Int J Inver Rep Dev 11:45–57

    Article  Google Scholar 

  • Cain GL (1956) Studies on cross-fertilization and self-fertilization in Lymnaea stagnalis. Biol Bull 111:45–52

    Article  Google Scholar 

  • Chase R (2002) Behavior and its neural control in gastropod molluscs. Oxford, New York

  • Denlinger D, Yocum GD, Rinehart JP (2012) Hormonal control of diapause. In: Gilbert LI (ed) Insect endocrinology. Academic Press, Cambridge, pp 430–463

    Chapter  Google Scholar 

  • Egonmwan RI (1991) The effects of temperature and photoperiod on growth and maturation rate of Limicolaria flammea Müller (Gastropoda: Pulmonata: Achatinidae). J Afr Zool 105:69–75

    Google Scholar 

  • Fodor I, Hussein AAA, Benjamin PR, Koene JM, Pirger Z (2020) The unlimited potential of the great pond snail Lymnaea stagnalis. elife 9:e56962. 

    Article  PubMed  PubMed Central  Google Scholar 

  • Geraerts WPM, Bohlken S (1976) The control of ovulation in the hermaphroditic freshwater snail Lymnaea stagnalis by the neurohormone of the caudodorsal cells. Gen Comp Endocr 28:350–357

    Article  CAS  Google Scholar 

  • Gomot P, Gomot L, Griffond B (1989) Evidence for a light compensation of the inhibition of reproduction by low temperatures in the snail Helix asperse. Ovotestis and albumen gland responsiveness to different conditions of photoperiods and temperatures. Biol Reprod 40:1237–1245. 

    Article  CAS  PubMed  Google Scholar 

  • Hermann PM, de Lange RPJ, Pieneman AW, Ter Maat A, Jansen RF (1997) Role of neuropeptides encoded on CDCH-1 gene in the organization of egg-laying behavior in the pond snail, Lymnaea stagnalis. J Neurophysiol 78:2859–2869

    Article  CAS  Google Scholar 

  • Hubendick B (1951) Recent Lymnaeidae Their variation, morphology, taxonomy, nomenclature, and distribution. Kungl Svenska Vetensk Akad Handl 3:1–223

    Google Scholar 

  • Hussein AAA, Baz ES, Mariën J, Tadros MM, El-Shenawy NS, Koene JM (2020) Effect of photoperiod and light intensity on learning ability and memory formation of the pond snail Lymnaea stagnalis. Invertebr Neurosci 20:18

    Article  CAS  Google Scholar 

  • Joosse J (1984) Photoperiodicity, rhythmicity and endocrinology of reproduction in the snail Lymnaea stagnalis. In: Porter R, Collins GM (eds) Photoperiodic regulation of insect and molluscan hormones. Pitman, London, pp 204–220

    Google Scholar 

  • Kits KS, Bos NPA (1981) Pacemaking mechanism of the afterdischarge of the ovulation hormone-producing caudo-dorsal cells in the gastropod mollusc Lymnaea stagnalis. J Neurobiol 12:425–439

    Article  CAS  Google Scholar 

  • Koene JM, Montagne-Wajer K, Ter Maat A (2006) Effects of frequent mating on sex allocation in the simultaneously hermaphroditic great pond snail. Behav Ecol Sociobiol 60:332–338

    Article  Google Scholar 

  • Kupfermann I (1970) Stimulation of egg laying by extracts of neuroendocrine cells (bag cells) of abdominal ganglion of Aplysia. J Neurophysiol 33(6):877–881

    Article  CAS  Google Scholar 

  • Kuroda R, Abe M (2020) The Pond Snail Lymnaea stagnalis. EvoDevo 11:24

    Article  Google Scholar 

  • Li KW, Geraerts WPM, Joosse J (1992) Purification and chemical characterization of caudodorsal cell hormone-II from the egg-laying controlling caudodorsal cells of Lymnaea stagnalis. Peptides 13:215–220

    Article  CAS  Google Scholar 

  • Nakadera Y, Blom C, Koene JM (2014) Duration of sperm storage in the simultaneous hermaphrodite Lymnaea stagnalis. J Molluscan Stud 80:1–7

    Article  Google Scholar 

  • Nelson RJ, Denlinger DL, Somers DE (2010) Photoperiodism, the biological calendar. Oxford University Press, New York

    Google Scholar 

  • Numata H, Udaka H (2010) Photoperiodism in Mollusks. In: Nelson RJ, Denlinger DL, Somers DE (eds) Photoperiodism, the biological calendar. Oxford University Press, New York, pp 173–192

    Google Scholar 

  • Piggott H, Dussart G (1995) Egg-laying and associated behavioural response of Lymnaea peregra (Muller) and Lymnaea stagnalis (L) to calcium in their environment. Malacologia 37:13–21

    Google Scholar 

  • Pinsker HM, Dudek FE (1977) Bag cell control of egg laying in freely behaving Aplysia. Science 197:490–493

    Article  CAS  Google Scholar 

  • Plesch B, de Jong-Brink M, Boer HH (1971) Histological and histochemical observations on the reproductive tract of the hermaphrodite pond snail Lymnaea stagnalis (L.). Neth J Zool 21:180–210

    Google Scholar 

  • Scheller RH, Jackson JF, McAllister LB, Rothman BS, Mayeri E, Axel R (1983) A single gene encodes multiple neuropeptides mediating a stereotyped behavior. Cell 32:7–22

    Article  CAS  Google Scholar 

  • Sokolove PG, McCrone EJ (1978) Reproductive maturation in the slug, Limax maximus, and the effects of artificial photoperiod. J Comp Physiol 125:317–325

    Article  Google Scholar 

  • Stephens GJ, Stephens GC (1966) Photoperiodic stimulation of egg laying in the land snail Helix aspersa. Nature 212:1582

    Article  Google Scholar 

  • Ter Maat A, Lodder JC, Wilbrink M (1983) Induction of egg-laying in the pond snail Lymnaea stagnalis by environmental stimulation of the release of ovulation hormone from the caudo-dorsal cells. Int J Inver Rep 6:239–247

    Article  Google Scholar 

  • Ter Maat A, Dijcks FA, Bos NPA (1986) In vivo recordings of neuroendocrine cells (caudo-dorsal cells) in the pond snail. J Comp Physiol A 158:853–859

    Article  Google Scholar 

  • Ter Maat A, Zonneveld C, De Visser JAGM, Jansen RF, Montagne-Wajer K, Koene JM (2007) Food intake, growth, and reproduction as affected by day length and food availability in the pond snail Lymnaea stagnalis. Am Malacol Bull 23:113–120

    Article  Google Scholar 

  • Ter Maat A, Pieneman AW, Koene JM (2012) The effect of light on induced egg laying in the simultaneous hermaphrodite Lymnaea stagnalis. J Molluscan Stud 78:262–267

    Article  Google Scholar 

  • Udaka H, Numata H (2008) Short-day and low temperature conditions promote reproductive maturation in the terrestrial; slug, Lehmannia valentiana. Comp Biochem Physiol A 150:80–83

    Article  Google Scholar 

  • Udaka H, Mori M, Goto SG, Numata H (2007) Seasonal reproductive cycle in relation to tolerance to high temperatures in the terrestrial slug Lehmannia valentiana. Invertebr Biol 126:154–162

    Article  Google Scholar 

  • Vreugdenhil E, Jackson JF, Bouwmeester T, Smit AB, MinnenJ V, Van Heerikhuizen H, Klootwijk J, Joosse J (1988) Isolation, characterization, and evolutionary aspects of a cDNA clone encoding multiple neuropeptides involved in the stereotyped egg-laying behavior of the freshwater snail Lymnaea stagnalis. J Neurosci 8:4184–4191

    Article  CAS  Google Scholar 

  • Wayne NL (2001) Regulation of seasonal reproduction in mollusks. J Biol Rhythm 16:319–402

    Article  Google Scholar 

  • Wayne NL, Lee W, Michel S, Dyer J, Sossin WS (2004) Activity-dependent regulation of neurohormone synthesis and its impact on reproductive behavior in Aplysia. Biol Reprod 70:277–281

    Article  CAS  Google Scholar 

  • Yvonne A (1983) Transfer of semen accelerates the onset of egg-laying in female copulants of the hermaphrodite freshwater snail, Lymnaea stagnalis. Inter J Invertebr Reprod 6:249–257

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, fifth edition. Pearson Prentice Hall, Upper Saddle River

Download references

Acknowledgements

We thank Professor Etsuro Ito at Waseda University for kindly providing Lymnaea stagnalis and their guidance and advice for rearing. We also thank Dr. Yoshitaka Hamanaka for sharing data of cdch mRNA amount in the whole central nervous system and for critical reading of the manuscript.

Funding

No funding was received for conducting this study.

Author information

Author notes

  1. Hitomi Kitai and Umi Kakuda have equally contributed to this work.

Authors and Affiliations

  1. Graduate School of Science, Osaka City University, Osaka, Osaka, 558-8585, Japan

    Hitomi Kitai, Umi Kakuda, Shin G. Goto & Sakiko Shiga

  2. Graduate School of Science, Osaka University, Machikaneyama cho, Toyonaka, Osaka, 560-0043, Japan

    Sakiko Shiga

Authors
  1. Hitomi Kitai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Umi Kakuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shin G. Goto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sakiko Shiga
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. HK conducted the experiments for Fig. 1 and Fig. 3a. UK conducted experiments for Fig. 2, Fig. 3b, and Fig. 4. HK and UK wrote the first draft of the manuscript. SS and SGG performed the data analysis. SS and SGG made the experimental design and wrote the manuscript. All authors read, and approved the final manuscript.

Corresponding author

Correspondence to Sakiko Shiga.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethics approval

This article does not contain any studies with vertebrate animals performed by any of the authors.

Animal care declaration

All experiments were carried out in accordance with the guide for the care and use of laboratory animals of the university.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 44 KB)

359_2021_1494_MOESM2_ESM.pptx

Comparison of relative amounts (a) and the summary of two-way ANOVA (b) of ß-tubulin mRNA in the cerebral ganglia and commissure of Lymnaea stagnalis reared under different photoperiod (12L:12D and 16L:8D) and different age (22 and 27 weeks after hatching). Columns and bars in a show average and S.D., respectively. N = 5 (all samples), N.S., not significant (PPTX 48 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kitai, H., Kakuda, U., Goto, S.G. et al. Photoperiod controls egg laying and caudodorsal cell hormone expression but not gonadal development in the pond snail Lymnaea stagnalis. J Comp Physiol A 207, 523–532 (2021). https://doi.org/10.1007/s00359-021-01494-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-021-01494-2

Keywords

Search

Navigation