Search

Menu
Search
in Ecology

Egg mass gelatinous envelopes of yellow goosefish Lophius litulon protect the internal eggs and larvae from salinity stress and desiccation

32 Views


Abstract

Some teleosts, including yellow goosefish Lophius litulon, spawn gelatinous egg masses, but the biological function of the gelatinous matrix remains poorly understood due to limited experimental access. This study tested whether the gelatinous membrane of L. litulon egg masses, which naturally float just below the sea surface in coastal areas, protects eggs and larvae from abiotic stress. Salinity stress experiments using 782 and 605 eggs were conducted. Embryos retained within gelatinous membranes maintained high survival and normal growth after 45 and 90 h of exposure to 50% diluted salinity, whereas those removed showed significant reductions (two-way ANOVA; p < 0.001 and = 0.015, respectively). Additionally, experiments using 449 and 599 larvae examined responses to 24-hour exposure under desiccation and elevated temperature conditions (2–3 °C above the appropriate temperature). The gelatinous matrix retained moisture, showing stable survival and growth (two-way ANOVA; p = 0.838 and 0.804, respectively), although heat stress reduced survival (two-way ANOVA; p < 0.001). These results indicate that the gelatinous matrix offers physical protection from some types of environmental stress, likely an adaptive trait for survival in variable coastal habitats. This study provides the first experimental evidence of such protective functions in gelatinous egg masses of marine fishes.

Similar content being viewed by others

Multistressor global change drivers reduce hatch and viability of Lingcod embryos, a benthic egg layer in the California Current System

Article
Open access
20 December 2022

Multigenerational laboratory culture of pelagic ctenophores and CRISPR–Cas9 genome editing in the lobate Mnemiopsis leidyi

Article

13 June 2022

In situ recordings of large gelatinous spheres from NE Atlantic, and the first genetic confirmation of egg mass of Illex coindetii (Vérany, 1839) (Cephalopoda, Mollusca)

Article
Open access
30 March 2021

Data availability

The data that support the findings of this study are openly available in *Figshare* at https://doi.org/10.6084/m9.figshare.30071737.v2.

References

  1. Sequeira, V. et al. The gelatinous matrix of the teleost Helicolenus Dactylopterus Dactylopterus (Delaroche, 1809) in the context of its reproductive strategy. Mar. Biol. Res. 7, 478–487. https://doi.org/10.1080/17451000.2010.528769 (2011).

    Google Scholar 

  2. Vega, R. et al. Evaluation and comparison of the efficiency of two incubation systems for Genypterus Chilensis (Guichenot, 1848) eggs. Lat Am. J. Aquat. Res. 40, 187–200. https://doi.org/10.3856/vol40-issue1-fulltext-18 (2012). (Spanish with English abstract).

    Google Scholar 

  3. Ikeda, T., Hirai, A., Tabata, S., Onishi, Y. & Mito, S. Key to fish eggs in Japan. In An atlas of early stage fishes in Japan (2nd ed.) (ed. Okiyama, M.) (Tokai University Press, 2014).

  4. Pietsch, T. W. & Arnold, R. J. Frogfishes: Biodiversity, Zoogeography and Behavioral Ecology (Johns Hopkins Univ., 2020).

  5. Armstrong, M. P., Musick, J. & Colvocoresses, J. A. Age, growth, and reproduction of the goosefish Lophius Americanus (Pisces, Lophiiformes). Fish. Bull. 90, 217–230 (1992).

    Google Scholar 

  6. Morris, J. J. A., Sullivan, C. V. & Govoni, J. J. Oogenesis and spawn formation in the invasive lionfish, Pterois Miles and Pterois volitans. Sci. Mar. 75, 147–154 (2011).

    Google Scholar 

  7. Greer, A. T., Chiaverano, L. M., Ditty, J. G. & Hernandez, F. J. In situ observations of fish larvae encased within a pelagic gelatinous matrix. Mar. Ecol. Prog Ser. 614, 209–214. https://doi.org/10.3354/meps12916 (2019).

    Google Scholar 

  8. Pernet, B. Benthic egg masses and larval development of Amblyosyllis speciosa (Polychaeta: Syllidae). J. Mar. Biol. Assoc. U K. 78, 1369–1372. https://doi.org/10.1017/S0025315400044568 (1998).

    Google Scholar 

  9. Collin, R. & Giribet, G. Report of a cohesive gelatinous egg mass produced by a tropical marine bivalve. Invert. Biol. 129, 165–171. https://doi.org/10.1111/j.1744-7410.2010.00188.x (2010).

    Google Scholar 

  10. Puneeta, P., Vijai, D., Yoo, H. K., Matsui, H. & Sakurai, Y. Observations on the spawning behavior, egg masses and paralarval development of the ommastrephid squid Todarodes Pacificus in a laboratory mesocosm. J. Exp. Biol. 213, 3825–3835. https://doi.org/10.1242/jeb.127670 (2015).

    Google Scholar 

  11. Przeslawski, R. A review of the effects of environmental stress on embryonic development within intertidal gastropod egg masses. Molluscan Res. 24, 43–63. https://doi.org/10.1071/MR04001 (2004).

    Google Scholar 

  12. Yoneda, M. et al. Reproductive cycle, fecundity, and seasonal distribution of the anglerfish Lophius Litulon in the East China and yellow seas. Fish. Bull. 99, 356–370 (2001).

    Google Scholar 

  13. Yamada, U., Tokimura, M., Horikawa, H. & Nakabo, T. Fishes and Fisheries of the East China and Yellow Seas (Tokai Univ., 2007) (in Japanese).

  14. Takeya, Y., Nara, K. & Kosaka, Y. Behavioral analysis of the yellow goosefish Lophius Litulon using bio-logging techniques. J. Fish. Tech. 6, 1–15 (2013). (in Japanese with English abstract).

    Google Scholar 

  15. Hoshino, N., Ichige, S., Suzuki, M., Yamaguchi, Y. & Toyoshima, S. Breeding experiment of anglerfish, Lophius litulon, and examination as an object species farming. Ibaraki Pref Fish. Exp. Rep. 40, 11–28 (2006). (in Japanese with English abstract).

    Google Scholar 

  16. Ishikawa, T., Nakaya, M., Eno, Y. & Takatsu, T. Macroscopic and microscopic morphological characteristics of gelatinous egg masses (egg veils) of yellow goosefish Lophius Litulon (Lophiiformes; Lophiidae). J. Fish. Biol. 105, 1338–1342. https://doi.org/10.1111/jfb.15867 (2024).

    Google Scholar 

  17. Ishikawa, T. et al. Changes in morphology and specific gravity in larvae of Lophius Litulon (Lophiiformes; Lophiidae) before and after emergence from egg veil. Environ. Biol. Fishes. 105, 303–312. https://doi.org/10.1007/s10641-022-01222-y (2022b).

    Google Scholar 

  18. Nakaya, M. et al. The effect of temperature on the early development and starvation tolerance of yellow goosefish Lophius Litulon. Aquacult. Sci. 65, 251–254. https://doi.org/10.11233/aquaculturesci.65.251 (2017).

    Google Scholar 

  19. Ishikawa, T., Nakaya, M. & Takatsu, T. Embryonic development and effect of water temperature on hatching of Lophius Litulon. Environ. Biol. Fishes. 105, 77–86. https://doi.org/10.1007/s10641-021-01195-4 (2022a).

    Google Scholar 

  20. Mito, S. Pelagic fish eggs from Japanese waters–X. Gadida and lophiida. Jpn J. Ichthyol. 11, 103–113. https://doi.org/10.11369/jji1950.11.103 (1963). (in Japanese with English abstract).

    Google Scholar 

  21. Gao, W. et al. Validation of otolith daily increments formation and growth analysis of yellow goosefish Lophius Litulon. Fish. Sci. 87, 541–548. https://doi.org/10.1007/s12562-021-01529-2 (2021).

    Google Scholar 

  22. Kim, U. Y. On the morphology of larval stage of Lophius Litulon (Jordan). Bull. Korean Fish. Soc. 9, 273–280 (1976). (in Korean with English abstract).

    Google Scholar 

  23. Spencer, M. L., Vestfals, C. D., Mueter, F. J. & Laurel, B. J. Ontogenetic changes in the buoyancy and salinity tolerance of eggs and larvae of Polar Cod (Boreogadus saida) and other Gadids. Polar Biol. 43, 1141–1158. https://doi.org/10.1007/s00300-020-02620-7 (2020).

    Google Scholar 

  24. Amida, A., Washitake, H., Kimura, T., Umino, T. & Ikeda, Y. Survival of squid, aka-ika, Sepioteuthis sp. 1, hatched from egg cases exposed to stressful conditions during the early-middle embryonic stage of development. Aquacult. Sci. 67, 241–248. https://doi.org/10.11233/aquaculturesci.67.241 (2019).

    Google Scholar 

  25. Woods, H. A. & DeSilets, A. R. Jr. Egg-mass gel of Melanochlamys Diomedea (Bergh) protects embryos from low salinity. Biol. Bull. 193, 341–349. https://doi.org/10.2307/1542936 (1997).

    Google Scholar 

  26. Eyster, L. The embryonic capsules of nudibranch molluscs: literature review and new studies on albumen and capsule wall ultrastructure. Am. Malac Bull. 4, 205–216 (1986).

    Google Scholar 

  27. Krishnamoorthi, B. Studies on the osmotic properties of the eggs and larvae of a brackish-water polychaete, marphysa gravelyi Southern. Proc. Indian Acad. Sci. 34, 199–209 (1951).

    Google Scholar 

  28. Krishnamoorthi, B. Volume regulation in eggs, larvae and adults of a brackish-water polychaete, diopatra variabilis (Southern). Proc. Indian Acad. Sci. 57, 275–289 (1963).

    Google Scholar 

  29. Gassen, L., Esters, L., Ribas-Ribas, M. & Wurl, O. The impact of rainfall on the sea surface salinity: a mesocosm study. Sci. Rep. 14, 6353 (2024).

    Google Scholar 

  30. Lie, H. J., Cho, C. H., Lee, J. H. & Lee, S. Structure and Eastward extension of the Changjiang river plume in the East China sea. J. Geophys. Res. 108, 3077. https://doi.org/10.1029/2001JC001194 (2003).

    Google Scholar 

  31. Sampaio, L. A. & Bianchini, A. Salinity effects on osmoregulation and growth of the Euryhaline flounder Paralichthys orbignyanus. J. Exp. Mar. Biol. Ecol. 269, 187–196. https://doi.org/10.1016/S0022-0981(01)00395-1 (2002).

    Google Scholar 

  32. Ern, R., Huong, D. T. T., Cong, N. V., Bayley, M. & Wang, T. Effect of salinity on oxygen consumption in fishes: a review. J. Fish. Biol. 84, 1210–1220. https://doi.org/10.1111/jfb.12330 (2014).

    Google Scholar 

  33. Evans, T. G. & Kültz, D. The cellular stress response in fish exposed to salinity fluctuations. J. Exp. Zool. A. 333, 421–435. https://doi.org/10.1002/jez.2350 (2020).

    Google Scholar 

  34. Varsamos, S., Nebel, C. & Charmantier, G. Ontogeny of osmoregulation in postembryonic fish: a review. Comp. Biochem. Physiol. A. 141, 401–429. https://doi.org/10.1016/j.cbpb.2005.01.013 (2005).

    Google Scholar 

  35. Fariña, A. C. et al. Lophius in the world: a synthesis on the common features and life strategies. ICES J. Mar. Sci. 65, 1272–1280. https://doi.org/10.1093/icesjms/fsn140 (2008).

    Google Scholar 

  36. Christie, B. L., Montoya, P. Z., Torres, L. A. & Foster, J. W. The natural history and husbandry of the walking batfishes (Lophiiformes: Ogcocephalidae). Drum Croak. 47, 7–40 (2016).

    Google Scholar 

  37. Gao, W., Nakaya, M., Takatsu, T., Takeya, Y. & Noro, K. Feeding habits of larval yellow goosefish Lophius Litulon around the Shimokita Peninsula and in Funka Bay, Japan. Aquacult. Sci. 68, 275–277. https://doi.org/10.11233/aquaculturesci.68.275 (2020).

    Google Scholar 

  38. Bakker, C. Phytoplankton/zooplankton relationships during spring in the brackish lake Grevelingen 1976–1978 (III). Hydrobiol. Bull. 13, 78–79 (1979).

    Google Scholar 

  39. de Ridder, M. Some considerations on the geographical distribution of rotifers. Hydrobiologia 85, 209–225 (1981).

    Google Scholar 

  40. Kourkoutmani, P. et al. Synchaeta’s community in the urban coastal area of the Thessaloniki Bay. Hydrobiologia 851, 3025–3037 (2024).

    Google Scholar 

  41. Paxton, C. G. M. & Willoughby, L. G. Resistance of perch eggs to attack by aquatic fungi. J. Fish. Biol. 57, 562–570. https://doi.org/10.1111/j.1095-8649.2000.tb00260.x (2005).

    Google Scholar 

  42. Cameron, P. & Von Westernhagen, H. Malformation rates in embryos of North sea fishes in 1991 and 1992. Mar. Pollut Bull. 34, 129–134. https://doi.org/10.1016/S0025-326X(96)00069-0 (1997).

    Google Scholar 

  43. Finn, R. N., Widdows, J. & Fyhn, H. J. Calorespirometry of developing embryos and yolk-sac larvae of turbot (Scophthalmus maximus). Mar. Biol. 122, 157–163 (1995).

    Google Scholar 

  44. Ishibashi, Y. et al. Ontogeny of tolerance to hypoxia and oxygen consumption of larval and juvenile red sea bream, Pagrus major. Aquaculture 244, 331–340. https://doi.org/10.1016/j.aquaculture.2004.11.019 (2005).

    Google Scholar 

  45. Eme, J. et al. Critical windows in embryonic development: shifting incubation temperatures alter heart rate and oxygen consumption of lake Whitefish (Coregonus clupeaformis) embryos and hatchlings. Comp. Biochem. Physiol. Part. A: Mol. Integr. Physiol. 179, 71–80. https://doi.org/10.1016/j.cbpa.2014.09.005 (2015).

    Google Scholar 

  46. Singh, N. R., Love, B., Murray, C. S., Sobocinski, K. L. & Cooper, W. J. The combined effects of acidification and acute warming on the embryos of Pacific herring (Clupea pallasii). Front. Mar. Sci. 10, 1307617 (2023).

    Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Y. Takeya (Aomori Prefectural government), Dr. K. Noro and Mr. R. Suzuki (Aomori Prefectural Industrial Technology Research Center Fisheries Institute) for their support and valuable suggestions. We thank to Mr. Y. Kindaichi (Kazamaura Fisheries Cooperative Association), Mr. G. Komamine (Komamine Corporation) the staff of Kazamaura Village Government and Laboratory of Marine Bioresources Ecology of Hokkaido University Faculty of Fisheries for their kind assistance in collection of specimens. This work was conducted under permits from Hokkaido University Manual for Implementing Animal Experimentation. This work was supported by JSPS KAKENHI Grant Number JP23KJ0049.

Funding

This work was supported by JSPS KAKENHI Grant Number JP23KJ0049.

Author information

Authors and Affiliations

  1. Graduate School of Fisheries Sciences, Hokkaido University, 3–1–1, Minato, Hakodate, 041–8611, Hokkaido, Japan

    Tomoya Ishikawa & Yuta Eno

  2. Faculty of Fisheries Sciences, Hokkaido University, 3–1–1, Minato, Hakodate, 041–8611, Hokkaido, Japan

    Mitsuhiro Nakaya & Tetsuya Takatsu

Authors

  1. Tomoya Ishikawa
    View author publications

    Search author on:PubMed Google Scholar

  2. Mitsuhiro Nakaya
    View author publications

    Search author on:PubMed Google Scholar

  3. Yuta Eno
    View author publications

    Search author on:PubMed Google Scholar

  4. Tetsuya Takatsu
    View author publications

    Search author on:PubMed Google Scholar

Contributions

**Tomoya Ishikawa: ** Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Validation, Visualization, Writing – original draft, Writing – review & editing, Resources.**Mitsuhiro Nakaya: ** Conceptualization, Funding acquisition, Supervision, Investigation, Methodology, Project administration, Writing – review & editing, Resources.**Yuta Eno: ** Conceptualization, Data curation, Methodology, Resources, Validation, Writing – review & editing.**Tetsuya Takatsu: ** Conceptualization, Formal analysis, Funding acquisition, Supervision, Writing – review & editing.

Corresponding author

Correspondence to
Tomoya Ishikawa.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval

All procedures and experiments were carried out in accordance with the experimental guidelines set by Hokkaido University.

Consent to participate

All of the authors have approved the contents of this paper and have agreed to the submission policies.

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 Material 1

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Cite this article

Ishikawa, T., Nakaya, M., Eno, Y. et al. Egg mass gelatinous envelopes of yellow goosefish Lophius litulon protect the internal eggs and larvae from salinity stress and desiccation.
Sci Rep (2025). https://doi.org/10.1038/s41598-025-32075-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41598-025-32075-x

Keywords

  • Anglerfish
  • Early life history
  • Environmental stress
  • Gelatinous egg mass
  • Hydrogel
  • Larvae

Source: Ecology - nature.com

Aeolian sand migration induced land degradation and desertification hotspots identification in the semi-arid rain shadow regions of Anantapur, India

Global species delimitation of smooth-shelled blue mussels in the Mytilus edulis complex

This portal is not a newspaper as it is updated without periodicity. It cannot be considered an editorial product pursuant to law n. 62 of 7.03.2001. The author of the portal is not responsible for the content of comments to posts, the content of the linked sites. Some texts or images included in this portal are taken from the internet and, therefore, considered to be in the public domain; if their publication is violated, the copyright will be promptly communicated via e-mail. They will be immediately removed.

Back to Top
Close