Domoic Acid in Stranded Marine Mammals in Thai Waters

Main Article Content

Thitima Niyomsilpchai
Supanoi Subsinserm
Narumol Kornkanitnan
Piyarat Khumraksa
Patcharaporn Kaewmong
Rachawadee Chantra

Abstract

The purpose of this research was to study the contamination of biotoxin domoic acid (DA) in stranded marine mammals in Thai waters between June 2019 and December 2021. DA was found in 34.8% (16/46) of marine mammals with concentrations ranging from non-detectable level to 37.29 µg/g. Notably, dugongs exhibited the highest DA contamination rate (53.8%), followed by whales (40%) and dolphins (25%). During the dry season, the percentage of DA contamination in marine mammals was higher than rainy season. Specifically, dugongs displayed the highest average DA concentration in muscle (7.79±16.50 µg/g), while dolphins exhibited that in the stomach contents (0.44±0.87 µg/g). Among whales, the highest average DA concentration was discovered in the brain (0.94±1.33 µg/g). Moreover, in this study, the DA contamination had been reported for the first time in three species of marine mammals, namely Stenella longirostris, Pseudorca crassidens, and Balaenoptera omurai. The results obtained from this study are useful for monitoring DA contamination on marine mammals which are marine endangered species at high risk of extinction.

Article Details

Section
Biological Sciences

References

Department of Marine and Coastal Resources, 2017, Report on the status of rare marine animals 2017, Bangkok, 22 p.

The working group prepares status information and plans for measures to conserve marine mammals for reporting in the system, 2022, National Action Plan for the Conservation and Management of Marine Mammals 2023 - 2027, Department of Marine and Coastal Resources. Bangkok, 33 p.

Kanchana, A., Surasak, T., Teerawat, P. and Phaothep, C., 2014, Handbook of Marine Mammal Species and Sea Turtles in Thailand, Department of Marine and Coastal Resources: Ministry of Natural Resources and Environment, National Buddhism Office Printing, 98 p.

Todd, E.C.D., 1993, Domoic Acid and Amnesic Shellfish Poisoning - A Review, Journal of food protection, 56 : 68-83

Brodie, E.C., Gulland, F.M.D., Greig, D.J., Hunter, M., Jaakola, J., St Leger, J., Leighfield, T.A. and Van Dolah F.M., 2006, Domoic acid causes reproductive failure in california sea lions (Zalophus californianus), Marine Mammal Science, 22 (3): 700-707

Silvagni, P., Lowenstine, L.J, Spraker, T., Lipscomb, T.P. and Gulland, F.M., 2005, Pathology of domoic acid toxicity in California sea lions (Zalophus californianus), Veterinary Pathology, 42: 184-191

Gulland, F., 2000, Domoic Acid Toxicity In California Sea Lions (Zalophus Californianus) Stranded Along The Central California Coast, May-October 1998, pp. 1-48, In Report to the National Marine Fisheries Service Working Group on Unusual Marine Mammal Mortality Events, NOAA Technical Memorandum, Washington, DC, USA

Kreuder, C., Miller, M.A. and Jessup, D.A., 2003, Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998-2001, Journal of Wildlife Diseases, 39: 495-509

Bates, S.S., Katherine, A. H., Nina, L., Marina, M. and Chui, P. L., 2018, Pseudo-nitzschia, Nitzschia, and domoic acid: new research since 2011, Elesevier, 79: 3-43

Kotaki Y., Koike, K., Yoshida, M., Thuoc, C.V., Huyen, N.T.M., Chu Hoi, N., Fukuyo, Y. and , Kodama, M. 2008, Domoic Acid Production in Nitzschia sp. (Bacillariophyceae) Isolated From a Shrimp-Culture Pond in Doson, Vietnam, Journal of Phycology, 36: 1057-1060

Quilliam, M.A., 2003, Chemical methods for domoic acid, the amnesic shellfish poisoning (ASP) toxin, pp.247-265, In Hallegraeff, G.M., Anderson D.M. and Cembella A.D. (Eds), Manual on Harmful Marine Microalage, Monographs on Oceanographic Methodology, Vol II. Paris: Intergovernmental Oceanographic Commission (UNESCO)

Zabaglo, K., Chrapusta, E., Bober, B., Kaminski, A., Adamski M. and Bialczyk, J., 2016, Environmental roles and biological activity of domoic acid: A review, Algal Research, 13: 94 -101

Oning, V., 2017, Domoic acid contamination process in marine organisms: case on the east coast of the Gulf of Thailand, Doctor of Philosophy (Marine Science), Kasetsart University, Thesis, 201 p.

Kvitek, R., Judh D. G., G. Jason S. and Gregory J. D., 2008, Domoic acid contamination within eight representative species from the benthic food web of Monterey Bay, California, USA, Marine Ecology Progress Series, 367: 35-47

Andjelkovic, M., Vandevijvere, S., Van Klaveren, J., Van Oyen, H. and Van Loco, J., 2012, Exposure to domoic acid through shellfish consumption in Belgium, Environment International, 49: 115-119

Bejarano, A.C., VanDola. F. M., Gulland, F.M., Rowles, T.K. and Schawacke, L.H., 2008, Production and Toxicity of the Marine Biotoxin Domoic Acid and Its Effects on Wildlife: A Review, Human and Ecological Risk Assessment, 13: 544-567

Lefebvre, K.A, Bargu, S., Kieckhefer, T. and Silver, M.W., 2002, From sanddabs to blue whales: the pervasiveness of domoic acid, Toxicon 40 (7): 971–977

Scholin, C.A., Gulland, F., Doucette, G. J., Benson, S., Busman, M., Chavez, F. P. Cordaro, J., DeLong, R., Vogelaere, A, D., Harvey, J., Haulena, M., Lefebvre, K., Lipscomb, T., Loscutoff, S., Lowenstine, L. J., Marin R., Miller, P.E., McLellan, W.A., Moeller, P.D., Powell, C.L., Rowles, T., Silvagni, P., Silver, M., Spraker, T., Trainer, V. and Van Dolah, F.M., 2000, Mortality of sea lions along the central California coast linked to a toxic diatom bloom, Nature, 403 (6765): 80-84.

Thitima, N., Narumo,l K., Supanoi S. and Rachawadee C., 2019, Contamination of Biotoxin, Domoic Acid in Stranded Marine Mammals in Thai Water, Burapha Science Journal, 24 (22): 550-567

Trainer, V.L., Adams, N.G., Bill, B.D., Carla, M.S., John C.W., Peter, M., Mark, B. and Woodruff, D., 2000, Domoic acid production near California coastal upwelling zones, June 1998, Limnology and Oceanography, 45(8): 1818-1833

Oning, V., Shettapong, M. and Thaithaworn, L., 2017., Domoic acid contamination in fish from Sriracha bay, Chonburi province, Thailand, Journal of Fisheries and Environment, 41(3): 48-56

Lefebvre, K.A., Silver, M.W., Coale, S.L. and Tjeerdema, R.S., 2002. Domoic acid in planktivorous fish in relation to toxic Pseudo-nitzschia cell densities, Marine Biology, 140: 625-631

Riva, G.T., Johnson, C.K., Gulland, F.M.D, Langlois, G.W. , Heyning, J.E., Rowles, T.K. and Mazet, J.A.K., 2009, Association of an unusual marine mammal mortality event with Pseudo-nitzschia spp. Blooms along the southern California coastline, Journal of Wildlife Disease, 45(1): 109-121

Atcharaporn P., 2009, Changes in the composition and abundance of potentially harmful phytoplankton coastal area Samut Sakhon Province - Samut Songkhram, Printing House of the Agricultural Cooperatives Association of Thailand, Bangkok, 176 p.

Kongkiat, P. and Varin, T., 2556, Relationship between Dominant Red Tide Phytoplankton and Water Quality in Samutsakhon Province Coast, Technical Paper 2023, Coastal Fisheries Research and Development Bureau, Department of Fisheries, 60 p.

Ruamsub, C., 2004, Relationship between phytoplankton that causes sea water color change phenomenon and water quality along the coast of Bang Khun Thian Sea, Department of Marine and Coastal Resources, Bangkok, Technical Paper, 5: 1-32

Ruamsub, C., 2006, Phytoplankton of Red Tide Phenomenas in The Upper Gulf of Thailand, Academic Document, No. 1/2006. Phuket Marine Biological Center, Department of Marine and Coastal Resources, Ministry of Natural Resources and Environment, 96 p.

Nakanishi, Y., Adulyanukosol, K., Arai, N., and Hosoya, S., 2009, Dugong grazing scars confirmed in Enhalus acoroides meadoss, Journal of Advanced Marine science and Technology Society, 14(2): 1-8

Sheppard, J. K., Lawler, I. R., and Marsh, H., 2007, Seagrass as pasture for seacows: Landscape-level dugong habitat evaluation, Estuarine, Coastal and Shelf Science, 71: 117-132

Department of Marine and Coastal Resources, 2017, National Dugong Conservation Plan Phase 1 (2020-2022), Bangkok, 27 p.

Thitima, N., 2010, Epiphytic Diatom on Seagrass Blade at Ban Pa Khlok, Phuket Province, Master of Science. Kasetsart University, Bangkok, Thesis, 327 p.

Nipaporn, C., 1994, Biology and electron microscopic structure of the diatom Nitzschia sp., Master of Science. Kasetsart University. Bangkok,Thesis

Sullivan, M.J., 1979, Epiphytic Diatom of Three Seagrass Species in Mississippi Sound, Bulletin of Marine Science, 29(4): 459-464

Sullivan, M.J., 1983, Community Structure of Epiphytic Diatom from the Gulf Coast of Florida, USA, pp. 374-384., In Proceedings of the 7th Symposium on Recent and Fossil Diatom. Otto Koeltz Press, Koengstein

Chang, M.H. and Lee, K.S., 2008, Species Composition of the Epiphytic Diatoms on the Leaf Tissues of Three Zostera Species Distributed on the Southern Coast of Korea, Algae, 23(3): 75-81

Cheng, A., 2016, Benthic algae and diatom communities in seagrass meadows under three different human impact regimes in Bocas del Toro, Panamá, SIT Graduate Institute, Carleton College, 24 p.

Vanessa, C.d.R. and Margareth, C., 2022, Diversity and Variation of Epiphytic Diatoms on Ruppia maritima L., Related to Anthropogenic Impact in an Estuary in Southern Brazil, Diversity, 14: 1-25

Patrawut, T., Chetphong, M. and Chalatip, J., 2018, Accumulation of Heavy Metals in Aquatic Environment and Impacts on Irrawady Dolphins in Trat bay, Trat Province, In Research Project in the Category of Income budget from government subsidies (national budget) For the fiscal year 2018, Burapha University, 64 p.

Department of Marine and Coastal Resources, Knowledge Mamagment, https://km.dmcr.go.th/c_1/s_ 96/d_4209, March, 2023

Kanjana, A., Surasak, T., Teerawat, P., and Poathep, C., 2014, Field Guide to Marine Mammals and Turtles of Thailand, Department of Marine and Coastal Resources, Bangkok, 96 p. (in Thai)

Fire, E.F., E. F.,Andrea, B., Robert, A.D.,Greg, E.,Tod, A. L., Keith, M.,Glenn, A. M., Kathleen, M. T. M.,Michael, M., Misty, N., Katie, P., Zhihong, W., Frederick, W. W., 2021, An assessment of temporal, spatial and taxonomic trends in harmful algal toxin exposure in stranded marine mammals from the U.S. New England coast, https://doi.org/10.1371/journal.pone.0243570, March, 2023

Lefebvre, K. A., Quakenbush, L., Frame, E., Burek Huntington, K., Sheffield, G., Stimmelmayr, R., Bryan, A., Kendrick, P., Ziel, H., Dickerson, B. and Gill, V., 2016, Prevalence of algal toxin in Alaskan marine mammals foraging in a changing arctic and subarctic environment, Harmful Algae, 55: 13 - 24.

Fire, S.E., Wang, Z., Leighfield, T.A., Morton, S.L., McFee, W.E., McLellan, W.A., Litake,r R.W., Tester, P.W., Hohn, A.A., Lovewell, G., Harms, C., Rotstein, D.S., Barco, S.G., Costidis, A., Sheppard, B., Bossart G.D., Stolen, M., Durden, W.N. and Van Dolah, F.M., 2009, Domoic acid exposure in pygmy and dwarf sperm whales (Kogia spp.) from southeastern and mid-Atlantic U.S. waters. Harmful Algae, 8, 658-664.

Parker, A., Corinne, G., Raphael, K., Megan, M., Christine, K.J. and Melissa M., Distribution of the neurotoxin domoic acid (DA) among various tissues and bodily fluids of naturally-exposed, DA-positive southern sea otter (Enhydra lutris nereis), https://www.vetmed.ucdavis.edu/sites/g/files/ dgvnsk 491/files/inline-files/Parker.pdf, March, 2023

De la Riva, G.T., Christine, K. J., Jonna, A.K. M., Frances, M.D.G., Gregg, L., John, H. and Teri, R., 2006, Marine Mammal Strandings Along the Southern California Coast Associated With Domoic Acid Producing Algal Blooms, In IAAAM Conference Proceeding, Retrieved September 15, 2018, from https://www.vin.com/ apputil/content/defaultadv1.aspx?pId=11215&meta=Generic&catId=31320&id= 3981151&ind =117&objTypeID=17

De la Riva, G.T., Johnson, C.K., Gulland, F.M.D., Langlois, G.W., Heyning, J.E., Rowles,T.K. and Mazet, J.A.K., 2009, Association of an unusual marine mammal mortality event with Pseudo-nitzschia spp. blooms along the Southern California coastline, Journal of Wildlife Diseases, 45:109-121.

Bargu, S., Mary S., Tracey, G., Kathryn, R. and Frances, G., 2010, Complexity of domoic acid-related sea lion strandings in Monterey Bay, California: foraging patterns, climate events, and toxic blooms,Marine Ecology Progress Series, 418: 213-222.

Fire, S.E., Wang, Z., Byrd, M., Whitehead, H.R., Paternoster, J. and Morton, S.L., 2011, Co-occurrence of multiple classes of harmful algal toxins in bottlenose dolphins (Tursiops truncatus) stranding during an unusual mortality event in Texas, USA. Harmful Algae, 10, 330-336.

Silvagni, P., Lowenstine, L.J, Spraker, T., Lipscomb, T.P. and Gulland, F.M., 2005, Pathology of domoic acid toxicityin California sea lions (Zalophus californianus), Vet. Pathology Journal, 42: 184-191

Ramsdell, J.S. and Zabka, T.S., 2008, In utero domoic acid toxicity: a fetal basis to adult disease in the California sea lion (Zalophus californianus). Mar Drugs, 6(2), 262–290. Royal Thai Government Gazette. (2018). Criteria for Toxins and Bacteria in Bivalve, 161ง: (pp. 47-48).

Gulland, F.M.D., Leslie, A.D. and Kary,l L.W., 2018, CRC Handbook of Marine Mammal Medicine, Boca Raton: Taylor & Francis Group. P. 319-327

Gulland, F.M.D., Haulena, M., Fauquier, D., LangLois, G., Lander, M.E., Zabka, T., and Duerr, R., 2002, acid toxicity in Californian sea lions (Zalophus califiornianus): clinical signs, treatment and survival, Veterrinary Record, 150(15): 475-480

Nash, S.B., Baddock, M.C., Takahashi, E., Dawson, A,. Cropp, R., 2017, Domoic acid poisoning as a possible cause of seasonal cetacean mass stranding events in Tasmania, Australia. Bulletin of Environmental Contamination and Toxicology 98, 8-13

Fire, S.E., Wang, Z., Leighfield, T.A., Morton, S.L., McFee, W.E., McLellan, W.A., Litake,r R.W., Tester, P.W., Hohn, A.A., Lovewell, G., Harms, C., Rotstein, D.S., Barco, S.G., Costidis, A., Sheppard, B., Bossart G.D., Stolen, M., Durden, W.N. and Van Dolah, F.M., 2009, Domoic acid exposure in pygmy and dwarf sperm whales (Kogia spp.) from southeastern and mid-Atlantic U.S. waters Harmful Algae, 8:658-664.

Twiner, M.J., Flewelling, L.J., Fire S.E., Bowen-Stevens, S.R., Gaydos, J.K., Johnson, C.K., Landsberg,

J.H., Leighfield, T.A., Mase-Guthrie, B., Schwacke, L., Van Dolah, F.M., Wang, Z. and Rowles, T.K., 2012, Comparative Analysis of Three Brevetoxin-Associated Bottlenose Dolphin (Tursiops truncatus)

Mortality Events in the Florida Panhandle Region (USA), PLOS ONE, 7:1-19

Lefebvre, K. A., Alison, R., Elizabeth, R. F., Kathleen, M. C., Shelly, N., Keri, A. B., Heathe,r W. and Frances, M.D.G., 2010, Clinical signs and histopathology associated with domoic acid poisoning in northern furseals (Callorhinus ursinus) and comparison of toxin detection methods, Harmful Algae, 9:374-383.

Fire, S.E., Wang, Z., Berman, M., Langlois, G.W., Morton, S.L., Sekula-Wood, E. and Benitez-Nelson, C.R., 2010, Trophic Transfer of the Harmful Algal Toxin Domoic Acid as a Cause of Death in a Minke Whale Balaenoptera acutorostrata) Stranding in Southern California. Aquatic Mammals, 36(4):342-350.

Twiner, M. J., Spencer, F., Lori, S., Leigh, D., Zhihong, W., Steve, M., Stephen, R., Brian, B., Teresa, K. R. and Randall, S. W., 2011, Concurrent Exposure of Bottlenose Dolphins (Tursiops truncatus) to Multiple Algal Toxins in Sarasota Bay, Florida, USA, PLOS ONE, 7:1-15.

Busse, L.B., Venrick, E.L., Antrobus R., Miller, P.E., Vigilant, V., Silver, M.W., Mengelt, C., Mydlarz L. and Prezelin, B.B., 2006, Domoic acid in phytoplankton and fish in San Diego, CA, USA. Harmful Algae, 5: 91–101.

Bates, S.S., 1998, Ecophysiology and Metabolism of ASP Toxin Production, Physiological ecology of harmful algal blooms, 405-426.

Fehling, J., Green, D.H., Davidson, K., Bolch, C.J. and Bates, S.S., 2004, Domoic acid production by Pseudo-nitzschia seriata (Bacillariophyceae) in Scottish water, Journal Phycology, 40: 622-630

Liefer, J.D., Robertson, A., MacIntyre, H.L., Smith W.L. and Dorsey, C.P., 2013, Characterization of a toxic Pseudo-nitzschia spp. bloom in the Northern Gulf of Mexico associated with domoic acid accumulation in fish, Harmful Algae, 26: 20-32.

Bates, S.S. and Richard, J., 1995, Domoic acid production and cell division by P. multiseries in relation to a light: dark cycle in silicate-limited chemostat culture, Harmful Marine Algae Blooms, 140-143

Bates, S.S., Garrison, D. and Horner, R., 1998, Bloom Dynamics and Physiology of Domoic Acid Producing Pseudo-nitzschia Species, Physiological ecology of harmful algal blooms, 267-292

Fehling, J., Davidson, K., Bolch, C.J. and Bates, S.S., 2004, Growth and domoic acid production by Pseudo-nitzschia seriata (Bacillariophyceae) under phosphate and silicate limitation, Journal Phycology, 40: 674-683

FAO. 2004. Marine biotoxins. FAO FOOD AND NUTRITION PAPER 80. Agriculture and Consumer Protection. 133-134 pp., https://books.google.co.th/books?hl=th&lr=&id=9fEfCzh5DXwC&oi=fnd &pg= PA2&dq= FAO+ 2004++Marine+biotoxins++FOOD+AND+NUTRITION+PAPER+80&ots=sMGVGPEon U& sig=bjo6nH6_tAJS9ei1t8AgEuYjvm4&redir_esc=y#v=onepage&q=FAO%202004%20%20Marine%20biotoxins%20%20FOOD%20AND%20NUTRITION%20PAPER%2080&f=false, March, 2023

Royal Thai Government Gazette, 2018, Criteria for Toxins and Bacteria in Bivalve, 161ง: 47-48 (in Thai)