Search

Menu
Search
in Ecology

Data assimilation reveals behavioral dynamics of sea cucumbers as a model for slow-moving benthic animals

32 Views


Abstract

Understanding the movement behavior of Japanese sea cucumbers (Apostichopus japonicus) is essential for ecological research and fisheries management. However, tracking their locomotion is challenging due to their slow movement and environmental variability. In this study, we employed acoustic telemetry combined with a data assimilation approach using the Kalman filter to estimate movement trajectories with high accuracy, overcoming the limitations of traditional visual tracking methods. To characterize movement complexity, we applied fractal dimension analysis, quantifying the randomness and variability of individual locomotion across different environmental conditions. Additionally, we examined the influence of key environmental factors, including water temperature, diel cycles, and boulder presence, using Generalized Linear Models (GLM). The results indicate that during the growing stage, higher water temperatures significantly increased movement activity, while boulder zones influenced movement differently depending on the season. This study also provides long-term tracking data on released sea cucumbers, offering new insights into their settlement and dispersal patterns. By combining acoustic telemetry, data assimilation, fractal analysis, and statistical modeling, we established a framework to investigate the behavioral dynamics of slow-moving benthic organisms. These findings enhance our understanding of sea cucumber ecology and provide a quantitative framework for future studies on marine invertebrate movement.

Similar content being viewed by others

Macroalgae and interspecific alarm cues regulate behavioral interactions between sea urchins and sea cucumbers

Article
Open access
10 March 2022

Development of a method for estimating asari clam distribution by combining three-dimensional acoustic coring system and deep neural network

Article
Open access
02 November 2024

Ecological niche models for the assessment of site suitability of sea cucumbers and sea urchins in China

Article
Open access
27 July 2022

Data availability

The datasets used for the production of this paper are not publicly available but may be made available by the corresponding author upon request for reasonable reasons.

References

  1. Ministry of Agriculture, F. and F. Summary of Agricultural, Forestry and Marine Products Exports and Imports in 2020. (2021).

  2. Sano, M. et al. Stock assessment of sea cucumber Apostichopus armata in coastal areas of Northern Hokkaido estimated from dredge-net catch data. Nippon Suisan Gakkaishi. 77, 999–1007 (2011).

    Google Scholar 

  3. Sakai, Y. Mass production of artificial seed of the Japanese common sea cucumber (Apostichopus japonicus) in Hokkaido, Japan. Bull. Fish. Res. Agen. 40, 129–134 (2015).

    Google Scholar 

  4. Masaki, K. et al. Movement, dispersal and growth of Farm-Raised Apostichopus japonicus juveniles after release into artificial reef (in Japanese). Aquacult. Sci. 55, 355–366 (2007).

    Google Scholar 

  5. Sakai, Y. & Kanno, M. Enhancement program of Japanese common sea cucumber Apostichopus japonicus in Hokkaido and a trial to reveal its effectiveness using microsatellite DNA markers. Fish. Genet. Breed. Sci. 46, 95–98 (2017).

    Google Scholar 

  6. Sakai, Y. Manual of Sea Ranching by Release Artificial Juvenile of Japanese Common Sea Cucumber in Hokkaido (Hokkaido Research Organization, 2023).

  7. Soliman, T., Kanno, M., Kijima, A. & Yamazaki, Y. Population genetic structure and gene flow in the Japanese sea cucumber Apostichopus japonicus across Toyama Bay, Japan. Fish. Sci. 78, 775–783 (2012).

    Google Scholar 

  8. Furukawa, G. et al. High retention rate of single spaghetti tagging in mature size Japanese common sea cucumber Apostichopus japonicus at low temperature (in Japanese). Aquacult. Sci. 67, 179–182 (2019).

    Google Scholar 

  9. Kirshenbaum, S., Feindel, S. & Chen, Y. A study of tagging methods for the sea cucumber Cucumaria frondosa in the waters off Maine. J. Shellfish Res. 25, 995–1000 (2006).

    Google Scholar 

  10. Cieciel, K., Pyper, B. J. & Eckert, G. L. Tag retention and effects of tagging on movement of the giant red sea cucumber Parastichopus Californicus. N Am. J. Fish. Manage. 29, 288–294 (2009).

    Google Scholar 

  11. Fujino, T. et al. Single spaghetti tagging as a high-retention marking method for Japanese common sea cucumber Apostichopus japonicus. Fish. Sci. 83, 367–372 (2017).

    Google Scholar 

  12. Purcell, S. W., Agudo, N. S. & Gossuin, H. Poor retention of passive induced transponder (PIT) tags for mark-recapture studies on tropical sea cucumbers. 28, 53–55 (2008).

  13. Gianasi, B. L., Verkaik, K., Hamel, J. F. & Mercier, A. Novel use of PIT tags in sea cucumbers: promising results with the commercial species Cucumaria frondosa. PLoS One. 10, e0127884 (2015).

    Google Scholar 

  14. Chantal Conand, M. B. A review of recent developments in the world sea cucumber fisheries. Mar. Fish. Rev. 55, 1–13 (1993).

    Google Scholar 

  15. Eriksson, H. & Byrne, M. The sea cucumber fishery in australia’s great barrier reef marine park follows global patterns of serial exploitation. Fish. Fish. 16, 329–341 (2015).

    Google Scholar 

  16. Hamaguchi, M. Development of technologies for promoting the early life ecological studies of marine benthos. Nippon Suisan Gakkaishi. 75, 771–774 (2009).

    Google Scholar 

  17. Masaki, K., Yamamura, K., Aoto, I. & Okuma, H. Factors decreasing the discovery rates of Farm-Raised juveniles of sea cucumber Apostichopus japonicus after release into artificial reef (in Japanese). Aquacult. Sci. 55, 347–354 (2007).

    Google Scholar 

  18. Yamana, Y., Hamano, T. & Goshima, S. Individual tracking to specify the aestivation site of adult sea cucumber Apostichopus japonicus on a jetty in Yoshimi Bay, Western Yamaguchi Prefecture, Japan. Plankton Benthos Res. 3, 235–239 (2008).

    Google Scholar 

  19. Pan, Y. et al. Influence of flow velocity on motor behavior of sea cucumber Apostichopus japonicus. Physiol. Behav. 144, 52–59 (2015).

    Google Scholar 

  20. Sun, J. et al. Effect of water temperature on diel feeding, locomotion behaviour and digestive physiology in the sea cucumber Apostichopus japonicus. J. Exp. Biol. 221, (2018).

  21. Barkai, A. The effect of water movement on the distribution and interaction of three holothurian species on the South African West Coast. J. Exp. Mar. Biol. 153, 241–254 (1991).

    Google Scholar 

  22. Hamel, J. F. et al. Active buoyancy adjustment increases dispersal potential in benthic marine animals. J. Anim. Ecol. 88, 820–832 (2019).

    Google Scholar 

  23. Purcell, S. W., Piddocke, T. P., Dalton, S. J. & Wang, Y. G. Movement and growth of the coral reef holothuroids Bohadschia Argus and Thelenota Ananas. Mar. Ecol. Prog Ser. 551, 201–214 (2016).

    Google Scholar 

  24. Tanaka, Y. Feeding and digestive processes of Stichopus japonicus. Bull. Fac. Fish. Hokkaido Univ. 9, 14–28 (1958).

    Google Scholar 

  25. Dong, G., Dong, S., Tian, X. & Wang, F. Effects of photoperiod on daily activity rhythm of juvenile sea cucumber, Apostichopus japonicus (Selenka). Chin. J. Oceanol. Limnol. 29, 1015 (2011).

    Google Scholar 

  26. Espinoza, M., Farrugia, T. J., Webber, D. M., Smith, F. & Lowe, C. G. Testing a new acoustic telemetry technique to quantify long-term, fine-scale movements of aquatic animals. Fish. Res. 108, 364–371 (2011).

    Google Scholar 

  27. Nanami, A. et al. Diel variation in home range size and precise returning ability after spawning migration of coral reef grouper Epinephelus ongus: implications for effective marine protected area design. Mar. Ecol. Prog Ser. 606, 119–132 (2018).

    Google Scholar 

  28. Sakai, Y. Project on Demonstration of Resource Enhancement for Export-Important Species (Open Call Research), Sect. 13.1: Japanese Sea Cucumber. FY2017 Annu. Rep. of Hakodate Fish. Exp. Stn.. (2017).

  29. Sibert, J. R., Musyl, M. K. & Brill, R. W. Horizontal movements of Bigeye tuna (Thunnus obesus) near Hawaii determined by Kalman filter analysis of archival tagging data. Fish. Oceanogr. 12, 141–151 (2003).

    Google Scholar 

  30. Higuchi, T. Introduction To Data Assimilation (Asakura Publishing, 2011).

  31. Rauch, H. E., Tung, F. & Striebel, C. T. Maximum likelihood estimates of linear dynamic systems. AIAA J. 3, 1445–1450 (1965).

    Google Scholar 

  32. Takehara, K., Adrian, R. J., Etoh, G. T. & Christensen, K. T. A Kalman tracker for super-resolution PIV. Exp. Fluids. 29, S034–S041 (2000).

    Google Scholar 

  33. Fukaya, K. Time series analysis by state space models and its application in ecology (in Japanese). Jpn J. Ecol. 66, 375–389 (2016).

    Google Scholar 

  34. Petris, G. & An, R. Package for dynamic linear models. J. Stat. Softw. 36, 1–16 (2010).

    Google Scholar 

  35. R Development Core Team. R: A Language and Environment for Statistical Computing. (2021).

  36. Liu, D. C. & Nocedal, J. On the limited memory BFGS method for large scale optimization. Math. Program. 45, 503–528 (1989).

    Google Scholar 

  37. Sakai, Y. Study on the Enhancement of Japanese Sea Cucumber Resources III: Standardization of Artificial Seed Release Techniques. FY2020 Annu. Rep. Hakodate Fish. Exp. Stn.. (2020).

  38. Mandelbrot, B. How long is the Coast of britain? Statistical Self-Similarity and fractional dimension. Sci. (1979). 156, 636–638 (1967).

    Google Scholar 

  39. Kenneth, F. Fractal Geometry: Mathematical Foundations and Applications (Wiley, 1990).

  40. Higuchi, T. Fractal analysis of time series (in Japanese). Proc. Inst. Stat. Math. 37, 209–233 (1989).

    Google Scholar 

  41. Shishido, H., Kitahara, I., Kameda, Y. & Ohta, Y. A trajectory Estimation method for badminton shuttlecock utilizing motion blur. in Image and Video Technology (eds Klette, R., Rivera, M. & Satoh, S.) 325–336 (Springer Berlin Heidelberg, Berlin, Heidelberg, (2014).

    Google Scholar 

  42. Anderson-Sprecher, R. & Ledolter, J. State-Space analysis of wildlife telemetry data. J. Am. Stat. Assoc. 86, 596–602 (1991).

    Google Scholar 

  43. Nielsen, A., Bigelow, K. A., Musyl, M. K. & Sibert, J. R. Improving light-based geolocation by including sea surface temperature. Fish. Oceanogr. 15, 314–325 (2006).

    Google Scholar 

  44. Jonsen, I. D., Myers, R. A. & Flemming, J. M. Meta-analysis of animal movement using state-space models. Ecology 84, 3055–3063 (2003).

    Google Scholar 

  45. Jonsen, I. D., Flemming, J. M. & Myers, R. A. Robust State-Space modeling of animal movement data. Ecology 86, 2874–2880 (2005).

    Google Scholar 

  46. Hammond, L. S. Patterns of feeding and activity in Deposit-Feeding holothurians and echinoids (Echinodermata) from a shallow Back-Reef Lagoon, discovery Bay, Jamaica. Bull. Mar. Sci. 32, 549–571 (1982).

    Google Scholar 

  47. Purcell, S. W. & Kirby, D. S. Restocking the sea cucumber Holothuria scabra: sizing no-take zones through individual-based movement modelling. Fish. Res. 80, 53–61 (2006).

    Google Scholar 

  48. Mercier, A., Battaglene, S. C. & Hamel, J. F. Periodic movement, recruitment and size-related distribution of the sea cucumber Holothuria scabra in Solomon Islands. Hydrobiologia 440, 81–100 (2000).

    Google Scholar 

  49. Sun, J., Hamel, J. F. & Mercier, A. Influence of flow on locomotion, feeding behaviour and spatial distribution of a suspension-feeding sea cucumber. J. Exp. Biol. 221, (2018).

  50. Tanaka, Y., Sakai, Y., Eguchi, G. & Takagi, T. Hydrodynamics of the sea cucumber Apostichopus japonicus in flow and acceleration fields. J. Aero Aqua Bio-mechanisms. 10, 24–32 (2023).

    Google Scholar 

  51. Kato, A. & Hirata, H. Effects of water temperature on the circadian rhythm of the Sea-cucumber, Stichopus japonicus (in Japanese). Aquacult. Sci. 38, 75–80 (1990).

    Google Scholar 

  52. Ru, X., Zhang, L., Liu, S. & Yang, H. Reproduction affects locomotor behaviour and muscle physiology in the sea cucumber, Apostichopus japonicus. Anim. Behav. 133, 223–228 (2017).

    Google Scholar 

  53. Lillacci, G. & Khammash, M. Parameter Estimation and model selection in computational biology. PLoS Comput. Biol. 6, e1000696 (2010).

    Google Scholar 

Download references

Acknowledgements

We would like to express our sincere gratitude to Mr. Manabu Shimono, Mr. Toru Miyagawa, and Itaru Araki from the Fisheries Technology Extension Office for their invaluable support during the diving surveys. We also appreciate the assistance of Ms. Yuki Nitta in the preparation of this manuscript. This study was made possible through the use of research equipment purchased under the Demonstration Project for the Enhancement of Resources of Important Export Species, funded by the Fisheries Agency of Japan. We extend our deepest thanks to all those involved. This study highlights that even species with limited mobility, such as sea cucumbers, can yield valuable insights into animal behavior.

Funding

This research was partially supported by a research grant from The South Hokkaido Science Promotion Foundation for the project “Development of Behavioral Information Acquisition Technology for Sea Cucumbers Using State Estimation Techniques and Understanding Individual Movement Characteristics.” Additionally, funding was provided by the Hokkaido Research Organization under two separate projects: (1) a project on marine ranching of Japanese common sea cucumber, and (2) a commissioned project aimed at demonstrating the enhancement of fisheries resources important for export. We sincerely appreciate the support of all those involved.

Author information

Author notes

  1. Erica Sasano

    Present address: Kansai Electric Power Co., Inc., Osaka, 530-8270, Japan

  2. Kouki Kanda

    Present address: Organo Co., Inc., Tokyo, 136-8631, Japan

Authors and Affiliations

  1. Faculty of Fisheries Sciences, Hokkaido University, Sapporo, 060-0810, Japan

    Tsutomu Takagi, Erica Sasano & Kouki Kanda

  2. Graduate School of Environmental Science, Hokkaido University, Sapporo, 060-0810, Japan

    Yuto Tanaka

  3. Hakodate Fisheries Research Institute, Hakodate, 040-0051, Japan

    Yuichi Sakai

Authors

  1. Tsutomu Takagi
    View author publications

    Search author on:PubMed Google Scholar

  2. Yuto Tanaka
    View author publications

    Search author on:PubMed Google Scholar

  3. Erica Sasano
    View author publications

    Search author on:PubMed Google Scholar

  4. Kouki Kanda
    View author publications

    Search author on:PubMed Google Scholar

  5. Yuichi Sakai
    View author publications

    Search author on:PubMed Google Scholar

Contributions

The manuscript was written by T.T. The experimental design was conceived by Y.S. and T.T. The diving surveys and measurements were conducted by Y.S., Y.T., E.S., and K.K. The analyses, including statistical analysis, were performed by T.T. and Y.T. Figures in the manuscript were created by T.T. and Y.T. Y.S. and T.T. secured the funding for this study. All the authors reviewed the manuscript.

Corresponding author

Correspondence to
Tsutomu Takagi.

Ethics declarations

Competing interests

The authors declare no competing interests.

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 4.0 International License, which permits use, sharing, adaptation, 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 changes were made. 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/4.0/.

Reprints and permissions

About this article

Cite this article

Takagi, T., Tanaka, Y., Sasano, E. et al. Data assimilation reveals behavioral dynamics of sea cucumbers as a model for slow-moving benthic animals.
Sci Rep (2025). https://doi.org/10.1038/s41598-025-29171-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41598-025-29171-3

Keywords

  • Data assimilation
  • Sea cucumber
  • Fractal dimension
  • Movement ecology
  • Acoustic telemetry
  • Benthic organism tracking

Source: Ecology - nature.com

Mechanisms of light harvesting complex proteins in photoprotection of the brown tide alga

Satisfying multidimensional human well-being efficiently and equitably through dynamic urban planning

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