Applications of Environmental DNA (eDNA) in Monitoring the Endangered Status and Evaluating the Stock Enhancement Effect of Tropical Sea Cucumber Holothuria Scabra.

Endangered species Environmental DNA Resource assessment Sea cucumber TaqMan

Journal

Marine biotechnology (New York, N.Y.)
ISSN: 1436-2236
Titre abrégé: Mar Biotechnol (NY)
Pays: United States
ID NLM: 100892712

Informations de publication

Date de publication:
Oct 2023
Historique:
received: 05 06 2023
accepted: 01 08 2023
medline: 23 11 2023
pubmed: 2 9 2023
entrez: 1 9 2023
Statut: ppublish

Résumé

The tropical sea cucumber Holothuria scabra is naturally found in the Indo-West Pacific. However, due to their commercial value, natural H. scabra populations have declined significantly in recent years, resulting in its status as an endangered species. Surveys of H. scabra resource pose a challenge due to its specific characteristics, such as sand-burrowing behavior. To overcome this problem, our study established a convenient and feasible method for assessing H. scabra resources using environmental DNA (eDNA) monitoring technology. First, H. scabra-specific TaqMan primers and probe were designed based on its cox1 gene, followed by the development of an eDNA monitoring method for H. scabra in two separate sea areas (Xuwen and Daya Bay). The method was subsequently employed to investigate the distribution of H. scabra and assess the effects of aquaculture stock enhancement through juvenile releasing in the Weizhou Island sea area. The H. scabra eDNA monitoring approach was found to be more appropriate and credible than traditional methods, and a positive impact of stocking on H. scabra populations was observed. In summary, this is the first report to quantify eDNA concentration in a Holothuroidea species, and it provides a convenient and accurate method for surveying H. scabra resources. This study introduces novel concepts for eDNA-based detection of endangered marine benthic animals and monitoring their population distribution and abundance.

Identifiants

pubmed: 37658250
doi: 10.1007/s10126-023-10239-y
pii: 10.1007/s10126-023-10239-y
doi:

Substances chimiques

DNA, Environmental 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

778-789

Subventions

Organisme : National Key Research and Development Program of China
ID : 2020YFD0901104
Organisme : National Key Research and Development Program of China
ID : 2018YFD0901605
Organisme : National Key Research and Development Program of China
ID : 2022YFD2401301
Organisme : Scientific Research and Technology Development Program of Guangxi
ID : AD22035965
Organisme : National Natural Science Foundation of China
ID : 41906101
Organisme : National Natural Science Foundation of China
ID : 42176132

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Références

Arnull J, Wilson AMW, Brayne K, Dexter K, Donah AG, Gough CLA, Kluckow T, Ngwenya B, Tudhope A et al (2021) Ecological co-benefits from sea cucumber farming: Holothuria scabra increases growth rate of seagrass. Aquac Environ Interact 13:301–310
doi: 10.3354/aei00409
Bohmann K, Evans A, Gilbert MTP, Carvalho GR, Creer S, Knapp M, Yu DW, De Bruyn M et al (2014) Environmental DNA for wildlife biology and biodiversity monitoring. Trends Ecol Evol 29:358–367
doi: 10.1016/j.tree.2014.04.003 pubmed: 24821515
Boothroyd M, Mandrak NE, Fox M, Wilson CC et al (2016) Environmental DNA (eDNA) detection and habitat occupancy of threatened spotted gar (Lepisosteus oculatus). Aquat Conserv-Mar Freshw Ecosyst 26:1107–1119
doi: 10.1002/aqc.2617
Boussarie G, Bakker J, Wangensteen OS, Mariani S, Bonnin L, Juhel JB, Kiszka JJ, Kulbicki M, Manel S, Robbins WD, Vigliola L, Mouillot D et al (2018) Environmental DNA illuminates the dark diversity of sharks. Sci Adv 4:eaap9661
Chaiyamoon A, Tinikul Y, Chaichotranunt S, Poomtong T, Suphamungmee W, Sobhon P, Tinikul R et al (2020) Existence of two mature sequences of cubifrin neuropeptide and their effects on spawning in the sea cucumber. Holothuria Scabra Aquaculture 519:8
doi: 10.1016/j.aquaculture.2019.734753
Cheng CH, Wu FF, Ren CH, Jiang X, Zhang X, Li XM, Luo P, Hu CQ, Chen T et al (2021) Aquaculture of the tropical sea cucumber. Stichopus monotuberculatus: induced spawning, detailed records of gonadal and embryonic development, and improvements in larval breeding by digestive enzyme supply in diet. Aquaculture 540:736690
Conand C (2018) Tropical sea cucumber fisheries: changes during the last decade. Mar Pollut Bull 133:590–594
doi: 10.1016/j.marpolbul.2018.05.014 pubmed: 30041353
Curtis AN, Tiemann JS, Douglass SA, Davis MA, Larson ER et al (2021) High stream flows dilute environmental DNA (eDNA) concentrations and reduce detectability. Divers Distrib 27:1918–1931
doi: 10.1111/ddi.13196
Djurhuus A, Closek CJ, Kelly RP, Pitz KJ, Michisaki RP, Starks HA, Walz KR, Andruszkiewicz EA, Olesin E, Hubbard K, Montes E, Otis D, Muller-Karger FE, Chavez FP, Boehm AB, Breitbart M et al (2020) Environmental DNA reveals seasonal shifts and potential interactions in a marine community. Nat Commun 11:9
doi: 10.1038/s41467-019-14105-1
Duy NDQ, Francis DS, Pirozzi I, Southgate PC et al (2016) Use of micro-algae concentrates for hatchery culture of sandfish, Holothuria scabra. Aquaculture 464:145–152
doi: 10.1016/j.aquaculture.2016.06.016
E Z, Cheng C, Wu F, Ren C, Chen R, Rao Y, Ma B. Jiang X, Luo P, Li X, Zhang X, Jiang F, Hu C, Chen T et al (2023) Nondestructive and rapid method for sex identification of the tropical sea cucumber Holothuria scabra by anal swab sampling. Aquaculture 562:738749
Eriksson H, Robinson G, Slater MJ, Troell M et al (2012) Sea cucumber aquaculture in the Western Indian Ocean: challenges for sustainable livelihood and stock improvement. Ambio 41:109–121
doi: 10.1007/s13280-011-0195-8 pubmed: 22083524
Ficetola GF, Miaud C, Pompanon F, Taberlet PJBL et al (2008) Species detection using environmental DNA from water samples. Biol Lett 4:423–425
doi: 10.1098/rsbl.2008.0118 pubmed: 18400683 pmcid: 2610135
Forootan A, Sjoback R, Bjorkman J, Sjogreen B, Linz L, Kubista M et al (2017) Methods to determine limit of detection and limit of quantification in quantitative real-time PCR (qPCR). Biomol Detect Quantif 12:1–6
doi: 10.1016/j.bdq.2017.04.001 pubmed: 28702366 pmcid: 5496743
Garlapati D, Charankumar B, Ramu K, Madeswaran P, Murthy MVR et al (2019) A review on the applications and recent advances in environmental DNA (eDNA) metagenomics. Rev Environ Sci Bio-Technol 18:389–411
doi: 10.1007/s11157-019-09501-4
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391
doi: 10.1046/j.1461-0248.2001.00230.x
Hair C, Militz TA, Daniels N, Southgate PC et al (2022) Performance of a trial sea ranch for the commercial sea cucumber, Holothuria scabra, in Papua New Guinea. Aquaculture 547:11
doi: 10.1016/j.aquaculture.2021.737500
Hamel J-F, Mercier A, Conand C, Purcell S, Toral-Granda V, Gamboa R et al (2013) Holothuria scabra. The IUCN Red List of Threatened Species. https://doi.org/10.2305/IUCN.UK.2013.RLTS.T180257A1606648.en
Hasan MH (2005) Destruction of a Holothuria scabra population by overfishing at Abu Rhamada Island in the Red Sea. Mar Environ Res 60:489–511
doi: 10.1016/j.marenvres.2004.12.007 pubmed: 15924996
Huang W, Huo D, Yu ZH, Ren CH, Jiang X, Luo P, Chen T, Hu CQ et al (2018) Spawning, larval development and juvenile growth of the tropical sea cucumber Holothuria leucospilota. Aquaculture 488:22–29
doi: 10.1016/j.aquaculture.2018.01.013
Hunter ME, Dorazio RM, Butterfield JSS, Meigs-Friend G, Nico LG, Ferrante JA et al (2017) Detection limits of quantitative and digital PCR assays and their influence in presence-absence surveys of environmental DNA. Mol Ecol Resour 17:221–229
doi: 10.1111/1755-0998.12619 pubmed: 27768244
Hunter ME, Nico LG (2015) Genetic analysis of invasive Asian Black Carp (Mylopharyngodon piceus) in the Mississippi River Basin: evidence for multiple introductions. Biol Invasions 17:99–114
doi: 10.1007/s10530-014-0708-z
Janosik AM, Johnston CE (2015) Environmental DNA as an effective tool for detection of imperiled fishes. Environ Biol Fishes 98:1889–1893
doi: 10.1007/s10641-015-0405-5
Klymus KE, Merkes CM, Allison MJ, Goldberg CS, Helbing CC, Hunter ME, Jackson CA, Lance RF, Mangan AM, Monroe EM, Piaggio AJ, Stokdyk JP, Wilson CC, Richter CA et al (2020) Reporting the limits of detection and quantification for environmental DNA assays. Environmental DNA 2:271–282
doi: 10.1002/edn3.29
Klymus KE, Richter CA, Chapman DC, Paukert C et al (2015) Quantification of eDNA shedding rates from invasive bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix. Biol Conserv 183:77–84
doi: 10.1016/j.biocon.2014.11.020
Li M, Shan X, Wang W, Ding X, Dai F, Lv D, Wu H et al (2020) Qualitative and quantitative detection using eDNA technology: a case study of Fenneropenaeus chinensis in the Bohai Sea. Aquaculture and Fisheries 5:148–155
doi: 10.1016/j.aaf.2020.03.012
Liao YL (1997) Phylum Echinodermata Class Holothuroidea. In: Editorial Committee of Fauna Sincia, Academia Sinica (ed) Fauna Sincia. Science Press, Beijing
Matejusova I, Graham J, Bland F, Lacaze JP, Herman G, Brown L, Dalgarno E, Bishop JD, Kakkonen JE, Smith KF, Douglas A et al (2021) Environmental DNA based surveillance for the highly invasive carpet sea squirt Didemnum vexillum: a targeted single-species approach. Front Mar Sci 8:16
doi: 10.3389/fmars.2021.728456
Minamoto T, Yamanaka H, Takahara T, Honjo MN, Kawabata Z et al (2012) Surveillance of fish species composition using environmental DNA. Limnology 13:193–197
doi: 10.1007/s10201-011-0362-4
Nontunha N, Chaiyamoon A, Chaichotranunt S, Tinikul R, Poomtong T, Sobhon P, Tinikul Y et al (2021) Neurotransmitters induce larval settlement and juvenile growth of the sea cucumber, Holothuria scabra. Aquaculture 535. https://doi.org/10.1016/j.aquaculture.2021.736427
Ogram A, Sayler GS, Barkay TJJOMM et al (1987) The extraction and purification of microbial DNA from sediments. 7:57–66
Osaki R, Imaeda H, Ban H, Aomatsu T, Bamba S, Tsujikawa T, Sasaki M, Fujiyama Y, Andoh A et al (2011) Accuracy of genotyping using the TaqMan PCR assay for single nucleotide polymorphisms responsible for thiopurine sensitivity in Japanese patients with inflammatory bowel disease. Exp Ther Med 2:783–786
doi: 10.3892/etm.2011.287 pubmed: 22977575 pmcid: 3440725
Purcell S, Samyn Y, Conand C et al (2012) Commercially important sea cucumbers of the world. Rome. In: FAO species catalogue for fishery purposes
Purcell SW, Conand C, Uthicke S, Byrne M et al (2016) Ecological roles of exploited sea cucumbers. In: Hughes RN, Hughes DJ, Smith IP, Dale AC (eds) Oceanography and marine biology: an annual review. 54. Crc Press-Taylor & Francis Group, Boca Raton
Rees HC, Bishop K, Middleditch DJ, Patmore JRM, Maddison BC, Gough KC et al (2014) The application of eDNA for monitoring of the Great Crested Newt in the UK. Ecol Evol 4:4023–4032
doi: 10.1002/ece3.1272 pubmed: 25505530 pmcid: 4242556
Rondon MR, August PR, Bettermann AD, Brady SF, Grossman TH, Liles MR, Loiacono KA, Lynch BA, Macneil IA, Minor C, Tiong CL, Gilman M, Osburne MS, Clardy J, Handelsman J, Goodman RM et al (2000) Cloning the soil metagenome: a strategy for accessing the genetic and functional diversity of uncultured microorganisms. Appl Environ Microbiol 66:2541–2547
doi: 10.1128/AEM.66.6.2541-2547.2000 pubmed: 10831436 pmcid: 110579
Solinas A, Thelwell N, Brown T et al (2002) Intramolecular TaqMan probes for genetic analysis. Chem Commun 2272–2273
Strickler KM, Fremier AK, Goldberg CSJBC (2015) Quantifying effects of UV-B, temperature, and pH on eDNA degradation in aquatic microcosms. 183:85–92
Thomsen PF, Willerslev E (2015) Environmental DNA - an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv 183:4–18
doi: 10.1016/j.biocon.2014.11.019
Uthicke S, Robson B, Doyle JR, Logan M, Pratchett MS, Lamare M et al (2022) Developing an effective marine eDNA monitoring: eDNA detection at pre-outbreak densities of corallivorous seastar (Acanthaster cf. solaris). Sci Total Environ 851. https://doi.org/10.1016/j.scitotenv.2022.158143
Wang L, Xu J, Liu H, Wang S, Ou W, Zhang M, Wei F, Luo S, Chen B, Zhang S, Yu K et al (2023) Ultrasensitive and on-site eDNA detection for the monitoring of crown-of-thorns starfish densities at the pre-outbreak stage using an electrochemical biosensor. Biosens Bioelectron 230:115265
Wang XY, Lu GQ, Zhao LL, Du XQ, Gao TX et al (2021) Assessment of fishery resources using environmental DNA: the large yellow croaker (Larimichthys crocea) in the East China Sea. Fish Res 235:10
doi: 10.1016/j.fishres.2020.105813
Wang XY, Zhang HB, Lu GQ, Gao TX et al (2022) Detection of an invasive species through an environmental DNA approach: the example of the red drum Sciaenops ocellatus in the East China Sea. Sci Total Environ 815:9
doi: 10.1016/j.scitotenv.2021.152865
Wu LS, Li JL, Tong F, Zhang JJ, Li MM, Ding SX et al (2022) Resource assessment of Larimichthys crocea in the East China Sea based on eDNA Analysis. Front Mar Sci 9:12
doi: 10.3389/fmars.2022.890756
Yang X, Wu M, Zhang L, Li J, Chen F, Pan Y et al (2015) Annual change of gonadal development in Holothuria scabra from Hainan island. Journal of Southern Argiculture 46:1117–1122
Yoccoz NG (2012) The future of environmental DNA in ecology. Mol Ecol 21:2031–2038
doi: 10.1111/j.1365-294X.2012.05505.x pubmed: 22486823

Auteurs

Zixuan E (Z)

CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, People's Republic of China.
University of Chinese Academy of Sciences, Beijing, 100049, People's Republic of China.

Peng Luo (P)

CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, People's Republic of China.
Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458, People's Republic of China.

Chunhua Ren (C)

CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, People's Republic of China.
Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458, People's Republic of China.

Chuhang Cheng (C)

Guangxi Key Laboratory of Marine Environmental Science, Guangxi Beibu Gulf Marine Research Center, Guangxi Academy of Sciences, Nanning, 530007, People's Republic of China.

Wenjie Pan (W)

CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, People's Republic of China.
University of Chinese Academy of Sciences, Beijing, 100049, People's Republic of China.

Xiao Jiang (X)

CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, People's Republic of China.
Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458, People's Republic of China.

Fajun Jiang (F)

Guangxi Key Laboratory of Marine Environmental Science, Guangxi Beibu Gulf Marine Research Center, Guangxi Academy of Sciences, Nanning, 530007, People's Republic of China.

Bo Ma (B)

CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, People's Republic of China.
University of Chinese Academy of Sciences, Beijing, 100049, People's Republic of China.

Suzhong Yu (S)

CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, People's Republic of China.
University of Chinese Academy of Sciences, Beijing, 100049, People's Republic of China.

Xin Zhang (X)

CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, People's Republic of China.
Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458, People's Republic of China.

Ting Chen (T)

CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, People's Republic of China. chan1010@scsio.ac.cn.
Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 511458, People's Republic of China. chan1010@scsio.ac.cn.

Chaoqun Hu (C)

CAS Key Laboratory of Tropical Marine Bio-resources and Ecology (LMB), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, People's Republic of China. hucq@scsio.ac.cn.
Guangxi Key Laboratory of Marine Environmental Science, Guangxi Beibu Gulf Marine Research Center, Guangxi Academy of Sciences, Nanning, 530007, People's Republic of China. hucq@scsio.ac.cn.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH