Sains Malaysiana 54(4)(2025): 959-974
http://doi.org/10.17576/jsm-2025-5404-01
Hematological and
Blood Biochemical Variations, and Their Correlation with Body Condition in
Wild-Foraging Sea Turtles of the Celebes Sea
(Variasi Hematologi dan Biokimia Darah serta Kaitannya dengan Keadaan Badan pada Penyu Laut yang Mencari Makanan secara Liar di Laut Sulawesi)
SYAMSYAHIDAH SAMSOL1,
MOHD UZAIR RUSLI1, KIRISHNAMOORTHIE JEETHVENDRA2,4,
HIDEAKI NISHIZAWA3, HUSSIEN MUIN5 & JUANITA JOSEPH2,6,*
1Sea Turtle
Research Unit (SEATRU), Institute of Oceanography and Environment, Universiti Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia
2Borneo Marine
Research Institute, Universiti Malaysia Sabah, 88400
Kota Kinabalu, Sabah, Malaysia
3Graduate School of
Informatics, Kyoto University, Kyoto, Japan
4Tropical Research
and Conservation Centre (TRACC), Pom Pom Island,
91300 Semporna, Sabah, Malaysia
5Sabah Wildlife
Department, 88100 Kota Kinabalu, Sabah, Malaysia
6Small Islands
Research Centre (SIRC), Faculty of Science and Natural Resources, Universiti Malaysia Sabah, 88400 Kota Kinabalu, Sabah,
Malaysia
Diserahkan: 25 Jun 2024/ Diterima: 16 Disember 2024
Abstract
The Celebes Sea provides critical foraging and
migratory habitats for sea turtles in Malaysian waters, yet health status data,
including hematologic and blood biochemistry parameters, remain scarce. To
address this gap, we examined the blood profiles of green turtles and hawksbill
turtles in these foraging grounds. Physical assessments such as body condition
scores and indices suggested overall clinical health, though one green turtle
exhibited
fibropapillomatosis, and a new occurrence of the burrowing
barnacle Chelolepas cheloniae was
observed on the carapace. Blood samples from 32 green turtles and 4 hawksbill
turtles were analyzed using an iSTAT handheld blood analyzer, showing interspecific
differences in blood values. Hawksbill turtles exhibited higher blood urea
nitrogen concentrations, possibly due to their high-protein diet, while one
green turtle showed abnormal blood profiles indicative of potential acidosis. This
study provides baseline health data for foraging sea turtles in the Celebes
Sea, emphasizing the importance of hematological and
biochemical monitoring in assessing health status and informing targeted
conservation strategies to address threats in their foraging habitats. These
findings help us better understand sea turtle health and support efforts to
protect these important species and their habitats.
Keywords: Blood gas; body condition index; Celebes Sea; health assessments; Southeast
Asia
Abstrak
Laut Sulawesi merupakan habitat penting untuk pemakanan dan migrasi penyu di perairan Malaysia, namun data
status kesihatan, termasuk parameter hematologi dan biokimia darah, masih kurang. Untuk menangani jurang ini, kami mengkaji profil darah penyu hijau dan penyu karah di kawasan pemakanan ini. Penilaian fizikal seperti skor dan indeks keadaan badan menunjukkan kesihatan klinikal secara keseluruhan, walaupun terdapat seekor penyu hijau yang menunjukkan fibropapillomatosis, serta penemuan baharu teritip pengorek Chelolepas cheloniae pada karapas. Sampel darah daripada 32 penyu hijau dan 4 penyu karah dianalisis menggunakan penganalisis darah genggam iSTAT yang mendedahkan perbezaan antara spesies dalam nilai darah. Penyu karah menunjukkan kepekatan nitrogen
urea dalam darah yang lebih tinggi, kemungkinan disebabkan oleh diet protein yang tinggi, manakala seekor penyu hijau menunjukkan profil darah tidak normal yang menunjukkan kemungkinan asidosis. Kajian ini menyediakan data asas kesihatan untuk penyu di kawasan pemakanan di Laut Sulawesi, menekankan kepentingan pemantauan hematologi dan biokimia dalam menilai status kesihatan serta membentuk strategi pemuliharaan yang disasarkan untuk menangani ancaman di habitat pemakanan mereka. Penemuan ini membantu kita memahami kesihatan penyu dengan lebih baik dan menyokong usaha melindungi spesies penting ini dan habitat mereka.
Kata kunci: Asia Tenggara; darah; indeks keadaan badan; Laut Sulawesi; penilaian kesihatan
RUJUKAN
Aguirre, A.A. & Balazs,
G.H. 2000. Plasma biochemistry values of Green Turtles (Chelonia mydas) with and without fibropapillomas in the Hawaiian Islands. Comparative
Haematology International 10:
132-137.
Aguirre, A.A. & Lutz, P.L. 2004.
Marine turtles as sentinel species: A role for studying environmental health. EcoHealth 1(3): 236-245.
Anderson, E.T., Harms, C.A., Stringer,
E.M. & Cluse, W.M. 2011. Evaluation of hematology and serum biochemistry of cold-stunned Green Sea
Turtles (Chelonia mydas) in North
Carolina, USA. Journal of Zoo and Wildlife Medicine 42(2): 247-255.
Arthur, K.E., Limpus, C.J. & Whittier, J.M. 2008. Baseline blood
biochemistry of Australian Green Turtles (Chelonia
mydas) and effects of exposure to the toxic cyanobacterium Lyngbya majuscule. Australian Journal of
Zoology 56: 23-32.
Balfour, D., Macdonald, D.W. & Catto, C.M. 2007. Assessing the impact of
conservation interventions: A case study of Black Rhinoceros. Journal of Applied Ecology 44(3): 424-431.
Bjorndal, K.A. & Jackson,
J. 2003. Role of sea turtles in marine ecosystems: Reconstructing the past. In The
Biology of Sea Turtles, edited by Lutz, P.L., Musick,
J.A. & Wyneken, J. Boca Raton: CRC Press. pp. 259-273.
Bjorndal, K.A., Bolten,
A.B. & Chaloupka, M.Y. 2000. Green Turtle somatic
growth model: Evidence for density dependence. Ecological Applications 10(1): 269-282.
Burns, T.J., McCafferty, D.J. &
Kennedy, M.W. 2015. Core and body surface temperatures of nesting Leatherback
Turtles (Dermochelys coriacea). Journal of Thermal Biology 51:
15-22.
Casal, A.B. & Oros,
J. 2007. Morphologic and cytochemical characteristics of blood cells of
juvenile Loggerhead Sea Turtles (Caretta caretta). Research in Veterinary Science 82: 158-165.
Chan, B.K.K., Prabowo, R.E. & Lee,
K.S. 2009. Crustacean fauna of Taiwan: Barnacles, Volume 1: Cirripedia: Thoracica excluding the Pyrgomatidae and Acastinae. Taiwan: National Taiwan Ocean University.
Chaves, L.B., Berrocal,
A., Meneses, A.I., Jiménez, C. & Vásquez, C.M.O.
2013. Study on the etiology of fibropapillomatosis of Olive Ridley Sea Turtles (Lepidochelys olivacea) nesting in the National Wildlife Refuge at
Ostional, Guanacaste, Costa Rica. Revista Ciencias Marinas y Costeras 5(1): 119-134.
Flint, M., Patterson-Kane, J.C., Limpus, C.J., Work, T.M., Blair, D. & Mills, P.C. 2009. Postmortem diagnostic investigation of disease in
free-ranging marine turtle populations: A review of common pathologic findings
and protocols. Journal of Veterinary
Diagnostic Investigation 21(6): 733-759.
Haziq Harith, A.H. 2018. Marine Turtle Status in the
Northeast Semporna Priority Conservation Area (PCA) (2014-2017).
WWF-Malaysia.
Harms,
C.A., Mallo, K.M., Ross, P.M. & Segars, A.L. 2003. Venous blood gases and
lactates of wild Loggerhead Sea Turtles (Caretta caretta) following two capture techniques. Journal
of Wildlife Diseases 39(2): 366-374.
Hayashi, R. 2012. Atlas of the barnacles
on marine vertebrates in Japanese waters including taxonomic review of
superfamily Coronuloidea (Cirripedia: Thoracica). Journal of the Marine Biological Association
of the United Kingdom 92: 107-127.
Hayashi,
R. & Tsuji, K. 2008. Spatial
distribution of turtle barnacles on the Green Sea Turtle, Chelonia mydas. Ecological Research 23(1): 121-125.
Herbst, L.H. 1994. Fibropapillomatosis of marine turtles. Annual Review of Fish Diseases 4: 389-425.
Herbert, L.H. & Jacobson, E.R. 1995.
Diseases of marine turtles. In Biology and Conservation of Sea
Turtles, edited by Bjorndal, K.A. Washington
(DC): Smithsonian Institution Press. 6: 593.
Herbst, L., Ene,
A., Su, M., Desalle, R. & Lenz, J. 2004. Tumor outbreaks in marine turtles are not due to recent
herpesvirus mutations. Current Biology 14(17): R697-R699.
Innis, C.J., Ravich, J.B., Tlusty, M.F., Hoge,
M.S., Wunn, D.S., Boerner-Neville, L.B., Merigo, C. & Weber III, E.S. 2009. Hematologic and
plasma biochemical findings in cold-stunned Kemp’s ridley turtles: 176 cases (2001-2005). Journal of the American Veterinary Medical
Association 235: 426-432.
Innis,
C.J., Tlusty, M., Merigo,
C. & Weber, E.S. 2007. Metabolic and
respiratory status of cold-stunned Kemp’s Ridley Sea Turtles (Lepidochelys kempii). Journal of
Comparative Physiology B 177(6): 623-630.
Jeethvendra, K., Nishizawa, H., Alin, J., Muin,
H. & Joseph, J. 2023. Illegal
tortoiseshell harvest of Hawksbill Turtles (Eretmochelys imbricata) in Southeast Asia: Evidence from Baturua Reef, Semporna, Sabah, Malaysia. Journal of
Sustainable Science and Management 18(7): 54-67.
Joseph, J., Nishizawa, H., Jalimin, S.N., Othman, R., Jaaman,
S.A., Bali, J. & Xuelei, Z. 2023. Health status and genetic
compositions of Green Turtles (Chelonia
mydas) foraging in Brunei Bay. PLoS ONE 18(11): e0293979.
Joseph,
J., Jolis, G., Jeethvendra,
K., Jalimin, S.N., Nishizawa, H., Muin,
H., Isnain, I. & Saleh,
E. 2021. Chapter 7. Research and conservation of marine turtles at nesting and
foraging grounds. In The
Marine Ecosystems of Sabah, edited by Yoshida, T. & Manjaji-Matsumoto, B.M. Kota Kinabalu: Penerbit Universiti Malaysia Sabah. pp. 95-123.
Joseph, J., Nishizawa, H., Arshaad,
W.M., Kadir, S.A.S., Jaaman, S.A., Bali, J., Jamaludin, N.A. & Katoh, M. 2016. Genetic stock compositions and natal origin
of Green Turtle (Chelonia mydas)
foraging at Brunei Bay. Global Ecology and Conservation 6: 16-24.
Keller, K.A., Innis, C.J., Tlusty,
M.F., Kennedy, A.E., Bean, S.B., Cavin, J.M. & Merigo,
C. 2012. Metabolic and respiratory derangements associated with death in
cold-stunned Kemp’s ridley turtles (Lepidochelys kempii): 32 cases (2005–2009). J.
Am. Vet. Med. Assoc. 240(3): 317-323.
Kelly,
T.R., McNeill, J.B., Avens, L., Hall, A.G., Goshe, L.R., Hohn, A.A., Godfrey,
M.H., Mihnovets, A.N., Cluse,
W.M. & Harms,
C.A. 2015. Clinical pathology reference intervals for an in-water population of
juvenile Loggerhead Sea Turtles (Caretta caretta) in Core Sound, North Carolina, USA. PLoS ONE 10(3): e0115739.
Kophamel,
S., Rudd, D., Ward, L.C., Shum, E., Ariel, E., Mendez, D., Starling, J., Mellers, R., Burchell, R.K. & Munns,
S.L. 2022. Haematological and biochemical reference intervals for wild Green
Turtles (Chelonia mydas): A Bayesian
approach for small sample sizes. Conservation Physiology 10(1): coac043.
Labrada-Martagón, V., Méndez-Rodríguez, L.C., Gardner, S.C.,
López-Castro, M. & Zenteno-Savín,
T. 2010. Health indices of the Green Turtle (Chelonia mydas) along the Pacific coast of Baja California Sur,
Mexico. I. Blood biochemistry values. Chelonian Conservation and Biology 9(2): 162-172.
Laloë, J.O., Schofield, G. & Hays, G.C. 2023. Climate warming and sea turtle sex ratios
across the globe. Global Change Biology 30: e17004.
Lewbart, G.A., Hirschfeld, M., Denkinger, J., Vasco, K., Guevara, N., García, J., Munõz, J. & Lohmann, K.J. 2014. Blood gases,
biochemistry, and hematology of Galapagos Green
Turtles (Chelonia mydas). PLoS ONE 9(5): e96487.
Li, T.H., Chang, C.C., Cheng, I.J. &
Lin, S.C. 2015. Development of a Summarized Health Index (SHI) for use in
predicting survival in sea turtles. PLoS ONE 10(3): e0120796.
Lim, K.K., Hussein, M.A.S. & Palaniappan, P. 2021. Abundance, placement and sexual
identity of the epizoic barnacle Chelonibia testudinaria relative to the size and species of host
turtles in Mabul Island, Malaysia. Journal
of the Marine Biological Association of the United Kingdom 100: 1299-1309.
Liu,
R.Y. & Ren, X.Q. 2007. Fauna Sinica. Invertebrata. Volume 42 Crustacea Cirripedia Thoracica. Beijing: Science Press.
Loganathan,
A.L., Palaniappan, P. & Subbiah, V.K. 2021. First evidence of Chelonid Herpesvirus
5 (ChHV5) infection in Green Turtles (Chelonia
mydas) from Sabah, Borneo. Pathogens 10(11): 1404.
Lutcavage, M.E., Spotila, J.R. & Witherington, B.E. 2003. The importance of sea
turtles to marine ecosystems. In The biology of Sea Turtles, edited by
Lutz, P.L. & Musick, J.A. Boca Raton: CRC Press. 1: 373-384.
Manes, C., Herren, R.M.,
Page, A., Dunlap, F.D., Skibicki, C.A., Rollinson Ramia, D.R., Farrell, J.A., Capua, I., Carthy,
R.R. & Duffy, D.J. 2023. Green turtle fibropapillomatosis: Tumor morphology and growth rate in a rehabilitation
setting. Veterinary Sciences 10(7): 421.
McNally, K.L., Mott, C.R., Guertin, J.R.,
Gorham, J.C. & Innis, C.J. 2020. Venous blood gas and biochemical analysis of wild captured Green
Turtles (Chelonia mydas) and Kemp’s
Ridley Turtles (Lepidochelys kempii)
from the Gulf of Mexico. PLoS ONE 15(8): e0237596.
Mones, A.B., Gruber, E.J., Harms, C.A.,
Lohmann, C.M.F., Lohmann, K.J. & Lewbart, G.A. 2021. Lactic acidosis
induced by manual restraint for health evaluation and comparison of two
point-of-care analyzers in healthy Loggerhead Sea
Turtles (Caretta caretta). Journal of Zoo and Wildlife Medicine 52(4): 1195-1204.
Muñoz-Pérez,
J.P., Lewbart, G.A., Hirschfeld, M., Alarcón-Ruales, D., Denkinger,
J., Castañeda, J.G. & Lohmann, K.J. 2017. Blood gases, biochemistry and
haematology of Galápagos Hawksbill Turtles (Eretmochelys imbricata). Conservation Physiology 5(1): cox028.
Nishizawa,
H. & Joseph, J. 2022. Differences in
the morphological body condition index of sea turtles between species and size
classes. Journal of the Marine Biological Association of the United
Kingdom 102: 479-485.
Nishizawa,
H., Joseph, J., Jolis, G., Isnain,
I., Muin, H., Johari, S. & Saleh, E. 2024.
Variations in body condition of Green Turtles (Chelonia mydas) in two nearby foraging grounds indicate their
sensitivity to foraging habitats. Aquatic Conservation: Marine and
Freshwater Ecosystems 34(1):
e4038.
Nishizawa,
H., Joseph, J., Chong, Y.K., Syed Kadir, S.A., Isnain,
I., Ganyai, T.A., Jaaman,
S. & Zhang, X. 2018. Comparison of the rookery connectivity and migratory
connectivity: Insight into movement and colonization of the Green Turtle (Chelonia mydas) in Pacific-Southeast
Asia. Marine Biology 165: 77.
Oksanen, J., Guilaume Blanchet, F., Friendly, M., Kindt, R., Legendre, P.,
McGlinn, D., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Peter Solymos, M., Stevens, H.H., Szoecs,
E. & Wagner, H. 2022. Vegan:
Community Ecology Package. R package version 2.6-4.
https://CRAN.R-project.org/package=vegan (Accessed on 19th February
2024).
Perrault,
J.R., Levin, M., Mott, C.R., Bovery, C.M., Bresette, M.J., Chabot, R.M., Gregory, C.R., Guertin, J.R.,
Hirsch, S.E., Ritchie, B.W. & Weege, S.T. 2021. Insights on immune function
in free-ranging Green Sea Turtles (Chelonia
mydas) with and without fibropapillomatosis. Animals 11(3): 861.
Phu, J.L. & Palaniappan,
P. 2019. Recaptured wild green sea turtles (Chelonia mydas) with newly
documented boat strike injuries in Mabul Island,
Sabah, Malaysia. Chelonian Conservation and Biology 18(2): 265-272.
Pilcher, N. 2010. Population structure and
growth of immature Green Turtles at Mantanani, Sabah, Malaysia. Journal
of Herpetology44(1): 168-171.
R
Core Team. 2022. R: A Language and
Environment for Statistical Computing. R Foundation for Statistical
Computing, Vienna, Austria. https://www.R-project.org/ (Accessed on 19th
February 2024).
Reséndiz, E., Fernández-Sanz, H.,
Barrientos-Torres, D.S. & Lara-Uc, M.M. 2019. Clinical pathology and health reference
values for Loggerhead Sea Turtles (Caretta caretta) and Olive Ridley Turtles (Lepidochelys olivacea) in
the Gulf of Ulloa, Baja California Sur, Mexico. Comparative Clinical
Pathology 28: 1637-1650.
Samsol, S., Abd Wahid, M.E., Li, T.H. & Rusli, M.U. 2020. Hematology,
blood gases and biochemistry profiles of wild-nesting sea turtles in
Terengganu, Malaysia. Malaysian Applied Biology 49(4): 25-31.
Santoro, M. & Meneses,
A. 2007. Haematology and plasma chemistry of breeding Olive Ridley SeaTurtles (Lepidochelys olivacea). The Veterinary Record 161(24): 818-819.
Stabenau, E.K., Heming, T.A. & Mitchell, J.F. 1991. Respiratory, acid-base and ionic
status of Kemp's Ridley Sea Turtles (Lepidochelys kempi) subjected to trawling. Comparative
Biochemistry and Physiology Part A: Physiology 99(1-2): 107-111.
Stacy, N.I. & Innis, C.J. 2017.
Clinical pathology. In Sea Turtle Health and Rehabilitation, edited by Manire, C.A., Norton, T.M., Stacy, B.A., Innis, C.J. &
Harms, C.A. Plantation, Florida: J. Ross Publishing 28: 147-207.
Stacy, N.I., Perrault, J.R. & Wood, L.D. 2023. Blood analytes of
Hawksbill Sea Turtles (Eretmochelys imbricata) from Florida waters: Reference intervals and
size-relevant correlations. Frontiers in Ecology and Evolution 11:
1199688.
Stacy, N.I.,
Innis, C.J. & Hernandez, J.A. 2013. Development and evaluation of three
mortality prediction indices for cold-stunned Kemp’s Ridley sea turtles (Lepidochelys kempii). Conservation
Physiology 1: cot003.
Stamper, M.A., Harms, C., Epperly, S.P., Braun-McNeill, J. & Stoskopf,
M.K. 2005. Relationship between barnacle epibiotic load and hematologic
parameters in Loggerhead Sea Turtles (Caretta caretta), a comparison between migratory and
residential animals in Pamlico Sound, North Carolina. Journal of Zoo and Wildlife Medicine 36: 635-641.
Teas, W.G. 1993. Species composition and
size class distribution of marine turtle strandings on the Gulf of Mexico and southeast United States coasts, 1985-1991. NOAA
Technical Memorandum NMFS-SEFSC-315.
Thomson, J.A., Burkholder, D., Heithaus, M.R. & Dill, L.M. 2009. Validation of a rapid
visual-assessment technique for categorizing the body condition of Green
Turtles (Chelonia mydas) in the
field. Copeia 2009(2): 251-255.
Tristan, T. & Norton, T. 2017. Physical
examination. In Sea Turtle Health and Rehabilitation, edited by Manire, C.A., Norton, T.M., Stacy, B.A., Innis, C.J. & Harms,
C.A. Plantation, FL: J. Ross Publishing. pp. 99-121.
Trocini, S., Warren, K., O’Hara, A., Bradley, S.
& Robertson, I. 2013. Health and hatching success of two Western Australian
Loggerhead Turtle (Caretta caretta) nesting populations. PhD Thesis. Murdoch University (Unpublished).
Uphyrkina, O., Johnson, W.E., Quigley, H., Miquelle,
D., Marker, L., Bush, M. & O'Brien, S.J.
2001. Phylogenetics, genome diversity and origin of modern Leopard, Panthera pardus. Molecular
Ecology 10(11): 2617-2633.
Van Houtan, K.S., Hargrove,
S.K. & Balazs, G.H. 2010. Land use, macroalgae,
and a tumor-forming disease in marine turtles. PLoS ONE 5(9): e12900.
Wolf, K.N., Harms, C.A. & Beasley, J.F. 2008.
Evaluation of five clinical chemistry analyzers for
use in health assessment in sea turtles. Journal of the American Veterinary
Medical Association 233: 470-475.
Work, T.M. & Balazs,
G.H. 1999. Relating tumor score to hematology in green turtles with fibropapillomatosis in Hawaii. Journal of Wildlife Diseases 35(4): 804-807.
Work, T.M., Raskin,
R.E., Balazs, G.H. & Whittaker, S.D. 1998.
Morphologic and cytochemical characteristics of blood cells from Hawaiian Green
Turtles. American Journal of Veterinary Research 59: 1252-1257.
Wyneken, J. 2001. The Anatomy of Sea Turtles.
NMFS Tech. Publication. NOAA Tech., Memo NMFS-SEFSC 470, 172.
Yang, T., Haas, H.L., Patel, S., Smolowitz, R., James, M.C. & Williard,
A.S. 2019. Blood biochemistry and haematology of migrating Loggerhead Turtles (Caretta caretta)
in the Northwest Atlantic: Reference intervals and intra-population
comparisons. Conservation Physiology 7(1): coy079.
Zardus, J.D. 2021. A global synthesis of the
correspondence between epizoic barnacles and their sea turtle hosts. Integrative Organismal Biology 3(1): obab002.
*Pengarang untuk surat-menyurat; email: juanita@ums.edu.my