Abstract
Background
The white teatfish, Holothuria fuscogilva, is widely distributed in coastal areas, including waters around coral reefs and seagrasses in the Indo-Pacific. In Kenya, the species is distributed in shallow reefs with higher landings reported from the Vanga-Shimoni-Gazi seascape on the Kenyan south coast. Despite its high exploitation for export and its vulnerable and endangered statuses under IUCN and CITES respectively, Kenya’s H. fuscogilva populations and how they may have been impacted by the fishing pressure have not been studied.
Methods
We estimated the genetic diversity and structure of H. fuscogilva population conveniently sampled from three sites in Kenyan south coast using the mitochondrial cytochrome oxidase subunit I (COI) gene sequences. We recorded 30 haplotypes with 43 polymorphic sites across the population. Furthermore, we estimated an overall high haplotype diversity and low nucleotide diversity of estimates of h = 0.970 ± 0.013 and π = 0.010 ± 0.001 respectively.
Conclusions
These preliminary findings suggest several population outcomes, among them a fit population, which require confirming with more comprehensive study to inform strategies for the sustainable exploitation and management of the species.
Similar content being viewed by others
Data availability
All the COI sequences used in the present study are deposited to the GenBank with accession numbers PP062748-PP062793.
References
Conand, C. (2008). Population status, fisheries and trade of sea cucumbers in Africa and the Indian Ocean. In V. Toral-Granda, A. Lovatelli and M. Vasconcellos (eds). Sea cucumbers. A global review of fisheries and trade. FAO Fisheries and Aquaculture Technical Paper. 143–193
Ochiewo J, Torre-castro MD, Muthama C, Munyi F, Nthuta JM (2010) Socio-economic features of sea cucumber fisheries in southern coast of Kenya. Ocean Coast Manag 53:192–202
Purcell SW, Williamson DH, Ngaluafe P (2018) Chinese market prices of beche-de-mer: implications for fisheries and aquaculture. Mar Policy 91:58–65
UNEP-Nairobi Convention and WIOMSA (2015). The Regional State of the Coast Report: Western Indian Ocean. UNEP and WIOMSA, 1–546
Conand C, Claereboudt M, Dissayanake C, Ebrahim A, Fernando S, Godvinden R, Lavitra T, Léopold M, Mmbaga TK, Mulochau T, Naaem S, Shea S, Vaitilingon D, Yahya S, Friedman K (2022) Review of fisheries and management of sea cucumbers in the Indian Ocean. West Indian Ocean J Mar Sci 21(1):125–148
Eriksson H, Österblom H, Crona B, Troell M, Andrew N, Wilen J, Folke D (2015) Contagious exploitation of marine resources. Front Ecol Environ 13(8):435–440
Eriksson H, de la Torre-Castro M, Olsson G (2012) Mobility, expansion and management of a multi-species scuba diving fishery in east Africa. PloS one 7(4):1–11
Eriksson H, Robinson G, Slater MJ, Troell M (2012) Sea cucumber aquaculture in the Western Indian Ocean: challenges for sustainable livelihood and stock improvement. Ambio 41(2):109–121. https://doi.org/10.1007/s13280-011-0195-8
Anderson SC, Flemming JM, Watson R, Lotze HK (2011) Serial exploitation of global sea cucumber fisheries. Fish Fish 12(3):317–339. https://doi.org/10.1111/j.1467-2979.2010.00397.x
Hasan MH (2019) Destruction of sea cucumber populations due to overfishing at Abu Ghosoun area, Red Sea. J Basic Appl Zoolo. https://doi.org/10.1186/s41936-019-0074-6
Mmbaga, T. K. (2013). The effect of fishing on the ecology of sea cucumber (Holothuroidea: Echinodermata) Holothuria scabra and Holothuria nobilis in Tanzanian sea water. International Journal of Development and Sustainability, 2(2), 1099–1126. http://isdsnet.com/ijds-v2n2-49.pdf
Friedman K, Eriksson H, Tardy E, Pakoa K (2011) Management of sea cucumber stocks: patterns of vulnerability and recovery of sea cucumber stocks impacted by fishing. Fish Fish 12(1):75–93. https://doi.org/10.1111/j.1467-2979.2010.00384.x
FAO 2016, White teatfish - Holothuria fuscogilva - Holothuriidae - HFF. Aquatic Species Distribution Map Viewer http://www.fao.org/figis/geoserver/factsheets/species.html
Ramofafia C, Battaglene SC, Bell JD, Byrne M (2000) Reproductive biology of the commercial sea cucumber Holothuria fuscogilva in the Solomon Islands. Mar Biol 136(6):1045–1056
Muthiga N, Kawaka J (2010) The breeding pattern and variations in timing and reproductive output of the commercial sea cucumber Holothuria fuscogilva in Kenya. West Indian Ocean J Mar Sci 8(2):183–192
CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora), 2019. CoP18 Prop. 45: Proposal of inclusion in Appendix II of three species belonging to the subgenus Holothuria (Microthele), Accessed 23 May 3 June 2019
Conand, C., Purcell, S. W., and Gamboa, R. U. (2013). Holothuria fuscogilva. The IUCN Red List of Threatened Species 2013, 8235
Purcell SW, Mercier A, Conand C, Hamel JF, Toral-Granda MV, Lovatelli A, Uthicke S (2013) Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish Fish 14(1):34–59
González-Wangüemert M, Valente S, Aydin M (2015) Effects of fishery protection on biometry and genetic structure of two target sea cucumber species from the Mediterranean Sea. Hydrobiologia 743:65–74
Muthiga, N., and Conand, C. (2014). Sea cucumbers in the western Indian Ocean ;WIOMSA Book Series No. 13, 1–74
Marty L, Dieckmann U, Ernande B (2014) Fisheries-induced neutral and adaptive evolution in exploited fish populations and consequences for their adaptive potential. Evolut Appl 8:47–63
Henriques R, von der Heyden S, Lipinski MR, du Toit N, Kainge P, Bloomer P, Matthee CA (2016) Spatio-temporal genetic structure and the effects of long-term fishing in two partially sympatric offshore demersal fishes. Mol Ecol 25(23):5843–5861
Horing, F. (2014). Population genetic structure of Calanoides carinatus (Copepoda, Calanoida) in the eastern Atlantic Ocean and Benguela upwelling system. MSc Thesis, University Bremen. Germany, 1- 60
Musembi P, Fulanda BM, Kairo J, Githaiga M (2019) Species composition, abundance and fishing methods of small-scale fisheries in the seagrass meadows of Gazi Bay. Kenya, J Indian Ocean Reg 15(2):139–156. https://doi.org/10.1080/19480881.2019.1603608
Fulanda BM, Munga C, Ohtomi J, Osore MK (2009) The structure and evolution of coastal migrant fishery of Kenya. Ocean Coast Manag 52(9):459–466
Li W, Chen X, Xu Q, Zhu J, Dai X, Xu L (2015) Genetic population structure of Thunnus albacores in the central pacific ocean based on mtDNA COI gene sequences. Biochem Genet 53(3):22
Ogongo BO, Chenje ME, Fulanda BM (2015) Distribution and reproductive patterns of the Epinephelus Genus Groupers off Kenyan south coast Marine Waters. J Fish Aquat Sci. https://doi.org/10.3923/jfas.2015.159.170
Ontomwa MB, Fulanda BM, Kimani EN, Okemwa GM (2019) Hook size selectivity in the artisanal handline fishery of Shimoni fishing area, south coast, Kenya. WIO J Mar Sci 19:29–46
Richmond, M. D (1997). A guide to the shores of Eastern-Africa and the Western Indian Ocean Islands. Sida/Department for Research Cooperation
Soliman T, Fernandez-silva I, Reimer JD (2016) Genetic population structure and low genetic diversity in the over-exploited sea cucumber Holothuria edulis Lesson, 1830 (Echinodermata: Holothuroidea) in Okinawa Island. Conserv Genet 17(4):811–821. https://doi.org/10.1007/s10592-016-0823-8
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452
Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of population. Bionformatics 24:2498–2504
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116
Beer, C. L. (2014). Genetic and morphometric variation of Octopus vulgaris in the Benguela Current Region. Ph.D. Thesis, Rhodes University,South Africa,1–159
Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29:2869–2876. https://doi.org/10.1093/bioinformatics/btt499
Saleky D, Setyobudiandi I, Toha HA, Takdir M, Madduppa HH (2016) Length-weight relationship and population genetic of two marine gastropods species (Turbinidae: Turbo sparverius and Turbo bruneus) in the Bird Seascape Papua. Indonesia Biodiversitas 17(1):208–217
Stewart, K. A., Draaijer, R., Kolasa, M. R., and Smallegange, I. M. (2019). The role of genetic diversity in the evolution and maintenance of environmentally-cued, male alternative reproductive tactics. BioRxiv, 1–10
Zhang BD, Li YL, Xue DX, Liu JX (2020) Population genomics reveals shallow genetic structure in a connected and ecologically important fish from the northwestern Pacific Ocean. Front Mar Sci 7:374
Maggi C, González-Wangüemert C (2015) Genetic differentiation among Parastichopus regalis populations in the Western Mediterranean Sea: potential effects from its fishery and current connectivity. Mediterr Mar Sci 16(3):489–501
Nowland SJ, Southgate PC, Basiita RK, Jerry DR (2017) Elucidation of fine-scale genetic structure of sandfish (Holothuria scabra) populations in Papua New Guinea and northern Australia. Mar Freshw Res 68(10):1901–1911
Otwoma, L. M. (2018). Connectivity and exploitation of Acanthurus triostegus and Acanthurus leucosternon in the Indian Ocean: Application of genetics and single stock assessment to aid coral reef management. PhD Thesis, University of Bremen. Germany,1–147
Triest LV, der Stocken T, Sierens T, Deus EK, Mangora MM, Koedam N (2021) Connectivity of Avicennia marina populations within a proposed marine transboundary conservation area between Kenya and Tanzania. Biol Cons 256:109040
van der Ven RM, Ratsimbazafy HA, Kochzius M (2022) Large-scale biogeographic patterns are reflected in the genetic structure of a broadcast spawning stony coral. Coral Reefs 41:611–624. https://doi.org/10.1007/s00338-022-02220-3
Mkare, T. K. (2013). Genetic population structure of fenaeid prawns Fenaeus monodon Fabricius 1798, Penneropenaeus indicus H. Milne Wards 1837 and Metapenaeus monoceros Fabricius 1798 in the Malindi–Ungwana Bay, Kenya. M.Sc. Thesis, Stellenbosch University, South Africa
Rodrigues F, Valente S, González-wanguemert M (2015) Genetic diversity across geographical scales in marine coastal ecosystems : Holothuria arguinensis a model species. J Exp Mar Biol Ecol 463:158–167
Gardner MG, Fitch AJ (2012) Population genetic structure of sea cucumber (bêche-de-mer) in northern Australia. Seafood CRC Final Rep Proj 2008:1–40
Hamamoto K, Soliman T, Poliseno A, Fernandez-silva I (2021) Higher genetic diversity of the common sea cucumber Holothuria atra in marine protected areas of the central and southern Ryukyu Islands. Front Conserv Sci 2:1–16
Vergara-Chen C, González-Wangüemert M, Marcos C, Pérez-Ruzafa Á (2010) Genetic diversity and connectivity remain high in Holothuria polii (Delle Chiaje 1823) across a coastal lagoon-open sea environmental gradient. Genetica 138(8):895–906. https://doi.org/10.1007/s10709-010-9472-x
Fang DA, Luo H, He M, Mao C, Kuang Z, Qi H, Xu D, Tan L, Li Y (2022) Genetic diversity and population differentiation of naked carp (Gymnocypris przewalskii) revealed by cytochrome oxidase subunit I and D-Loop. Front Ecol Evol. https://doi.org/10.3389/fevo.2022.827654
Uthicke S, Conand C, Benzie JAH (2001) Population genetics of the fissiparous holothurians Stichopus chloronotus and Holothuria atra (Aspidochirotida): a comparison between the Torres Strait and La Réunion. Mar Biol 139(2):257–265
Acknowledgements
We thank Kenya Marine and Fisheries Research Institute (KMFRI) fisheries officers, sea cucumber traders, fishermen and BMU officials of Shimoni, Gazi and Vanga who assisted in acquiring sea cucumber samples. We would also like to appreciate all working groups of the Pwani University Biosciences Research Center (PUBReC) and KMFRI molecular lab staff for assisting on molecular work in the lab.
Funding
This work was supported by Western Indian Ocean Marine Association (WIOMSA) under MARG I (Grant number MARGI-2020-C09).
Author information
Authors and Affiliations
Contributions
The research plan was conceived by Diana Karan. Field sampling was done by Diana Karan with help from Thomas Mkare and Bernerd Fulanda. Diana Karan conducted all lab experiments with supervision from Thomas Mkare and Sammy Wambua. Data analyses was performed by Diana Karan with guidance from Thomas Mkare and Sammy Wambua. Diana Karan drafted the manuscript. Bernerd Fulanda, Thomas Mkare and Sammy Wambua supervised the preparation of the draft. Bernerd Fulanda, Thomas Mkare and Sammy Wambua helped with writing, proofreading, and editing the final version of the manuscript. All authors contributed to the article and approved the submitted version.
Corresponding author
Ethics declarations
Competing Interest
The authors declare that they have no competing interests.
Ethical approval
This study involved sampling sea cucumber and was reviewed and approved by the Ethics Review Committee Board from Pwani University with sampling carried out under Kenya Wildlife Service permit. The samples used in this study were acquired from the fishermen and were part of their catch about to be processed thus were mostly dead or semi-dead. All procedures performed in this study were in accordance with the ethical standards as guided by the institutional research committee and accorded permit.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Karan, D., Fulanda, B., Mkare, T. et al. A peek into the population genetics of white teatfish (Holothuria fuscogilva) of Kenya’s south coast. Mol Biol Rep 51, 397 (2024). https://doi.org/10.1007/s11033-024-09310-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11033-024-09310-1