Assessing Bottlenose Dolphins’ (Tursiops truncatus) Health Status Through Functional Muscle Analysis, and Oxidative and Metabolic Stress Evaluation: A Preliminary Study
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Animals and Sample Collection
2.2. Biochemical Analyses
2.3. Measurement of Oxidative Status
2.4. Statistical Analysis
3. Results
3.1. Correlations Between Sex and Oxidative Stress Markers
3.2. Correlation Between Age and Oxidative Stress Markers
3.3. Correlations Between Biochemical Parameters and Oxidative Stress Markers
3.4. Multiple Linear Regression Analysis
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Sies, H.; Berndt, C.; Jones, D.P. Oxidative stress. Annu. Rev. Biochem. 2017, 86, 715–748. [Google Scholar] [CrossRef]
- Finkel, T.; Holbrook, N.J. Oxidants, oxidative stress and the biology of ageing. Nature 2000, 408, 239–247. [Google Scholar] [CrossRef] [PubMed]
- Dröge, W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82, 47–95. [Google Scholar] [CrossRef]
- Sánchez-Rodríguez, M.A.; Mendoza-Núñez, V.M. Oxidative stress indexes for diagnosis of health or disease in humans. Oxid. Med. Cell. Longev. 2019, 2019, 4128152. [Google Scholar] [CrossRef] [PubMed]
- Vezzoli, A.; Mrakic-Sposta, S.; Brizzolari, A.; Balestra, C.; Camporesi, E.M.; Bosco, G. Oxy-inflammation in humans during underwater activities: A review. Int. J. Mol. Sci. 2024, 25, 3060. [Google Scholar] [CrossRef]
- Butler, P.J.; Jones, D.R. Physiology of diving of birds and mammals. Physiol. Rev. 1997, 77, 837–899. [Google Scholar] [CrossRef] [PubMed]
- McKnight, J.C.; Patrician, A.; Dujic, Z.; Hooker, S.K.; Fahlman, A. Diving physiology in dolphins and humans. In The Physiology of Dolphins; Academic Press: London, UK; Elsevier: London, UK, 2023; pp. 135–149. [Google Scholar]
- Kooyman, G.L.; Ponganis, P.J. The physiological basis of diving to depth: Birds and mammals. Annu. Rev. Physiol. 1998, 60, 19–32. [Google Scholar] [CrossRef]
- Ponganis, P.J. Diving mammals. Compr. Physiol. 2011, 1, 447–465. [Google Scholar] [CrossRef]
- Vázquez-Medina, J.P.; Zenteno-Savín, T.; Elsner, R.; Ortiz, R.M. Coping with physiological oxidative stress: A review of antioxidant strategies in seals. J. Comp. Physiol. B 2012, 182, 741–750. [Google Scholar] [CrossRef]
- Martinovic, J.; Dopsaj, V.; Kotur-Stevuljević, J.; Dopsaj, M.; Vujović, A.; Stefanović, A.; Nešić, G. Oxidative Stress Biomarker Monitoring in Elite Women Volleyball Athletes During a 6-Week Training Period. J. Strength Cond. Res. 2011, 25, 1360–1367. [Google Scholar] [CrossRef]
- Tafuri, S.; Cocchia, N.; Carotenuto, D.; Vassetti, A.; Staropoli, A.; Mastellone, V.; Peretti, V.; Ciotola, F.; Albarella, S.; Del Prete, C.; et al. Chemical Analysis of Lepidium meyenii (Maca) and Its Effects on Redox Status and on Reproductive Biology in Stallions. Molecules 2019, 24, 1981. [Google Scholar] [CrossRef] [PubMed]
- Esposito, L.; Tafuri, S.; Cocchia, N.; Fasanelli, R.; Piscopo, N.; Lamagna, B.; Eguren, V.; Amici, A.; Iorio, E.; Ciani, F. Assessment of living conditions in wild boars by analysis of oxidative stress markers. J. Appl. Anim. Welf. Sci. 2021, 24, 64–71. [Google Scholar] [CrossRef]
- Fukuda, S.; Nojima, J.; Motoki, Y.; Yamaguti, K.; Nakatomi, Y.; Watanabe, Y. A potential biomarker for fatigue: Oxidative stress and anti-oxidative activity. J. Mol. Sci. 2013, 14, 1231–1240. [Google Scholar] [CrossRef] [PubMed]
- Brancaccio, P.; Lippi, G.; Maffulli, N. Biochemical markers of muscular damage. Clin. Chem. Lab. Med. 2010, 48, 757–767. [Google Scholar] [CrossRef]
- Tafuri, S.; Marullo, A.; Ciani, F.; Della Morte, R.; Montagnaro, S.; Fiorito, F.; De Martino, L. Reactive oxygen metabolites in alpha-herpesvirus-seropositive Mediterranean buffaloes (Bubalus bubalis): A preliminary study. Pol. J. Vet. Sci. 2018, 21, 3. [Google Scholar]
- Ridgway, S.H. Homeostasis in the aquatic environment. In Mammals of the Sea: Biology and Medicine; Ridgway, S.H., Ed.; Charles C Thomas: Springfield, MA, USA, 1972; pp. 590–747. [Google Scholar]
- Medway, W.; Geraci, J.R. Clinical pathology of marine mammals. In Zoo and Wildlife Medicine; Fowler, M.E., Ed.; WB Saunders: Philadelphia, PA, USA, 1986; pp. 791–797. [Google Scholar]
- Vallyathan, N.V.; George, J.C.; Ronald, K. The harp seal, Pagophilus groenlanicus, V. Levels of haemoglobin, iron, certain metabolites and enzymes in the blood. Can. J. Zool. 1969, 47, 1193–1196. [Google Scholar] [CrossRef]
- Venn-Watson, S.K.; Ridgway, S.H. Big brains and blood glucose: Common ground for diabetes mellitus in humans and healthy dolphins. Comp. Med. 2007, 57, 390–395. [Google Scholar]
- Gatta, C.; De Felice, E.; D’Angelo, L.; Maruccio, L.; Leggieri, A.; Lucini, C.; Palladino, A.; Paolucci, M.; Scocco, P.; Varricchio, E.; et al. The case study of Nesfatin-1 in the pancreas of Tursiops truncatus. Front. Physiol. 2018, 9, 1845. [Google Scholar] [CrossRef]
- Gatta, C.; Avallone, L.; Costagliola, A.; Scocco, P.; D’Angelo, L.; de Girolamo, P.; De Felice, E. Immunolocalization of Two Neurotrophins, NGF and BDNF, in the Pancreas of the South American Sea Lion Otaria flavescens and Bottlenose Dolphin Tursiops truncatus. Animals 2024, 14, 2336. [Google Scholar] [CrossRef]
- Venn-Watson, S.; Smith, C.R.; Johnson, S.; Daniels, R.; Townsend, F. Clinical relevance of urate nephrolithiasis in bottlenose dolphins (Tursiops truncatus). Dis. Aquat. Organ. 2010, 89, 167–177. [Google Scholar] [CrossRef]
- Venn-Watson, S.; Smith, C.R.; Stevenson, S.; Parry, C.; Daniels, R.; Jensen, E.; Cendejas, V.; Balmer, B.; Janech, M.; Neely, B.A.; et al. Blood-Based Indicators of Insulin Resistance and Metabolic Syndrome in Bottlenose Dolphins (Tursiops truncatus). Front. Endocrinol. 2013, 4, 62491. [Google Scholar] [CrossRef]
- Tiganis, T. Reactive oxygen species and insulin resistance: The good, the bad and the ugly. Trends Pharmacol. Sci. 2011, 32, 82–89. [Google Scholar] [CrossRef]
- Napolitano, G.; Fasciolo, G.; Venditti, P. Mitochondrial management of reactive oxygen species. Antioxidants 2021, 10, 1824. [Google Scholar] [CrossRef] [PubMed]
- Bossard, G.B.; Reidarson, T.H.; Dierauf, L.A.; Duffield, D.A. Clinical patology. In CRC Hanbook of Marine Mammals Medicine, 2nd ed.; Dierauf, L.A., Gullard, F.M.D., Eds.; CRC Press: Boca Raton, FL, USA, 2001; Chapter 19; pp. 383–436. [Google Scholar]
- Khan, A.A.; Allemailem, K.S.; Alhumaydhi, F.A.; Gowder, S.J.T.; Rahmani, H. The biochemical and clinical perspectives of lactate dehydrogenase: An enzyme of active metabolism. Endocr. Metab. Immune Disord. 2020, 20, 855–868. [Google Scholar] [CrossRef] [PubMed]
- Xiaolu, L.; Yanyan, Y.; Bei, Z.; Xiaotong, L.; Xiuxiu, F.; Yi, A.; Yulin, J.; Jian-Xun, W.; Zhibin, W.; Tao, Y. Lactate metabolism in human health and disease. Signal Transduct. Target. Ther. 2022, 7, 305. [Google Scholar]
- Powers, S.K.; Jackson, M.J. Exercise-induced oxidative stress: Cellular mechanisms and impact on muscle force production. Physiol. Rev. 2008, 88, 1243–1276. [Google Scholar] [CrossRef] [PubMed]
- McCord, J.M. The evolution of free radicals and oxidative stress. Am. J. Med. 2000, 108, 652–659. [Google Scholar] [CrossRef]
- Geraci, J.R.; Lounsbury, V.J. Marine Mammals Ashore: A Field Guide for Strandings, 2nd ed.; National Aquarium: Baltimore, MD, USA, 2005. [Google Scholar]
- Alberti, A.; Bolognini, L.; Macciantelli, D.; Carratelli, M. The radical cation of N,N-diethyl-para-phenylendiamine: A possible indicator of oxidative stress in biological samples. Res. Chem. Intermed. 2000, 26, 253–267. [Google Scholar] [CrossRef]
- Vázquez-Medina, J.; Zenteno-Savín, T.; Elsner, R. Antioxidant enzymes in ringed seal tissues: Potential protection against dive-associated ischemia/reperfusion. Comp. Biochem. Physiol. C 2006, 142, 198–204. [Google Scholar] [CrossRef]
- Beaulieu, M.; Costantini, D. Biomarkers of oxidative status: Missing tools in conservation physiology. Conserv. Physiol. 2014, 2, cou014. [Google Scholar] [CrossRef]
- Agarwal, A.; Prabakaran, S.A. Mechanisms of oxidative stress in male infertility and the role of antioxidants: A review. Reprod. Biomed. Online 2005, 11, 641–650. [Google Scholar] [CrossRef] [PubMed]
- Vina, J.; Gambini, J.; Lopez-Grueso, R.; Abdelaziz, K.M.; Jove, M.; Borras, C. Females Live Longer than Males: Role of Oxidative Stress. Curr. Pharm. Des. 2011, 17, 3959–3965. [Google Scholar] [CrossRef] [PubMed]
- Metcalfe, N.B.; Alonso-Alvarez, C. Oxidative stress as a life-history constraint: The role of reactive oxygen species in shaping phenotypes from conception to death. Funct. Ecol. 2010, 24, 984–996. [Google Scholar] [CrossRef]
- Ortiz, R.M.; Wade, C.E.; Ortiz, C.L. Effects of prolonged fasting on plasma cortisol and TH in postweaned northern elephant seal pups. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 208, R790–R795. [Google Scholar] [CrossRef]
- Alonso-Álvarez, C.; Pérez-Rodríguez, L.; García, J.T.; Viñuela, J.; Mateo, R. Age and breeding effort as sources of individual variability in oxidative stress markers in a bird species. Physiol. Biochem. Zool. 2007, 83, 110–118. [Google Scholar] [CrossRef] [PubMed]
- Giorgi, C.; Marchi, S.; Simoes, I.C.M.; Ren, Z.; Morciano, G.; Perrone, M.; Patalas-Krawczyk, P.; Borchard, S.; Jedrak, P.; Pierzynowska, K.; et al. Mitochondria and Reactive Oxygen Species in Aging and AgeRelated Diseases. Int. Rev. Cell Mol. Biol. 2018, 340, 209–344. [Google Scholar] [CrossRef]
- Castellini, M. Physiology of marine mammals: An overview. Mar. Mamm. Sci. 2018, 34, 523–535. [Google Scholar]
- Harman, D. Free radical theory of aging: An update. Ann. N. Y. Acad. Sci. 2006, 1067, 10–21. [Google Scholar] [CrossRef]
- Lesser, M.P. Oxidative stress in marine environments: Biochemistry and physiological ecology. Annu. Rev. Physiol. 2006, 68, 253–278. [Google Scholar] [CrossRef]
- Fridovich, I. Oxygen toxicity: A radical explanation. J. Exp. Biol. 1998, 201, 1203–1209. [Google Scholar] [CrossRef]
- Cantú-Medellín, N.; Byrd, B.; Hohn, A.; Vázquez-Medina, J.P.; Zenteno-Savín, T. Differential antioxidant protection in tissues from marine mammals with distinct diving capacities. Shallow/short vs. deep/long divers. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2011, 158, 438–443. [Google Scholar] [CrossRef]
- Selleghin-Veiga, G.; Magpali, L.; Picorelli, A.; Felipe, A.S.; Ramos, E.; Nery, M.F. Breathing Air and Living Underwater: Molecular Evolution of Genes Related to Antioxidant Response in Cetaceans and Pinnipeds. J. Mol. Evol. 2024, 92, 300–316. [Google Scholar] [CrossRef] [PubMed]
- Wilhelm-Filho, D.; Sell, F.; Ribeiro, L.; Ghislandi, M.; Carrasquedo, F.; Fraga, C.G.; Wallauer, J.P.; Simoes-Lopesa, P.C.; Uhart, M.M. Comparison between the antioxidant status of terrestrial and diving mammals. Comp. Biochem. Physiol. A 2002, 133, 885–892. [Google Scholar] [CrossRef] [PubMed]
- García-Castañeda, O.; Gaxiola-Robles, R.; Kanatous, S.; Zenteno-Savín, T. Circulating glutathione concentrations in marine, semiaquatic, and terrestrial mammals. Mar. Mamm. Sci. 2007, 33, 738–747. [Google Scholar] [CrossRef]
- Russo, F.; Gatta, C.; De Girolamo, P.; Cozzi, B.; Giurisato, M.; Lucini, C.; Varricchio, E. Expression and immunohistochemical detection of leptin-like peptide in the gastrointestinal tract of the South American sea lion (Otaria flavescens) and the bottlenose dolphin (Tursiops truncatus). Anat. Rec. 2012, 295, 1482–1493. [Google Scholar] [CrossRef]
- Gatta, C.; Russo, F.; Russolillo, M.G.; Varricchio, E.; Paolucci, M.; Castaldo, L.; Lucini, C.; de Girolamo, P.; Cozzi, B.; Maruccio, L. The orexin system in the enteric nervous system of the bottlenose dolphin (Tursiops truncatus). PLoS ONE 2014, 9, e105009. [Google Scholar] [CrossRef]
- De Felice, E.; Gatta, C.; Giaquinto, D.; Fioretto, F.; Maruccio, L.; D’Angelo, D.; Scocco, P.; de Girolamo, P.; D’Angelo, L. Immunolocalization of Nesfatin-1 in the gastrointestinal tract of the common bottlenose dolphin (Tursiops truncatus). Animals 2022, 12, 2148. [Google Scholar] [CrossRef]
Animals | Age | Sex | d-ROMs (U. Carr) | OXY (μmol HClO/L) | OSi (d-ROMs/OXY) |
---|---|---|---|---|---|
1 | 42 | M | 80 | 1332.5 | 6 |
2 | 32 | M | 75 | 1259.5 | 5.9 |
3 | 5 | F | 81 | 1251.0 | 6.5 |
4 | 19 | F | 61 | 1264.6 | 4.8 |
5 | 9 | M | 82 | 1145.4 | 7.1 |
6 | 26 | M | 91 | 1255.6 | 7.2 |
7 | 25 | M | 78 | 1280.2 | 6.1 |
8 | 19 | F | 84 | 1268.4 | 6.6 |
9 | 12 | F | 67 | 1268.2 | 5.3 |
10 | 7 | F | 58 | 1238.5 | 4.7 |
11 | 14 | M | 69 | 1348.6 | 5.1 |
Variable | Sex Pearson’s Coefficient (r) |
---|---|
d-ROMs (U.Carr) | 0.459 |
OXY (µmol/L) | 0.122 |
OSi (d-ROMs/OXY) | 0.390 |
Variable | Age Pearson’s Coefficient (r) |
---|---|
d-ROMs (U.Carr) | 0.328 |
OXY (µmol/L) | 0.468 |
OSi (d-ROMs/OXY) | 0.148 |
Animals | GLU (mg/dL) | AST (U/L) | LDH (U/L) | CK (U/L) |
---|---|---|---|---|
1 | 135.9 | 354.4 | 798 | 99 |
2 | 91.3 | 174.5 | 479 | 122 |
3 | 114.4 | 154.1 | 2395 | 58 |
4 | 111.5 | 163.4 | 319 | 104 |
5 | 124.3 | 240.1 | 160 | 151 |
6 | 106.1 | 218.1 | 479 | 86 |
7 | 142.4 | 221.4 | 798 | 140 |
8 | 108.9 | 157.6 | 319 | 31 |
9 | 111.9 | 370.8 | 160 | 68 |
10 | 107.8 | 153.6 | 479 | 188 |
11 | 108.6 | 199.6 | 319 | 80 |
Biochemical Parameter | Correlation with d-ROMs (r) | Correlation with OXY (r) | Correlation with OSi (r) |
---|---|---|---|
GLU | 0.195 | 0.075 | 0.175 |
AST | 0.081 | 0.193 | 0.030 |
CK | −0.390 | −0.394 | −0.248 |
LDH | 0.143 | 0.458 | −0.012 |
Biochemical Parameter | Coefficient (d-ROMs) | p-Value (d-ROMs) | Coefficient (OXY) | p-Value (OXY) | Coefficient (OSi) | p-Value (OSi) |
---|---|---|---|---|---|---|
GLU | 0.1608 | 0.632 | −0.9205 | 0.484 | 0.0190 | 0.546 |
AST | −0.0127 | 0.820 | 0.1009 | 0.645 | −0.0015 | 0.779 |
CK | −0.1136 | 0.228 | −0.6523 | 0.094 | −0.0058 | 0.491 |
LDH | 0.0094 | 0.646 | 0.1754 | 0.058 | −0.0002 | 0.908 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gatta, C.; Iorio, E.L.; Genovese, C.; Biancani, B.; Mores, A.; La Monaca, D.; Caterino, C.; Avallone, L.; Sanchez-Contreras, G.J.; De Vivo, I.; et al. Assessing Bottlenose Dolphins’ (Tursiops truncatus) Health Status Through Functional Muscle Analysis, and Oxidative and Metabolic Stress Evaluation: A Preliminary Study. Animals 2025, 15, 1215. https://doi.org/10.3390/ani15091215
Gatta C, Iorio EL, Genovese C, Biancani B, Mores A, La Monaca D, Caterino C, Avallone L, Sanchez-Contreras GJ, De Vivo I, et al. Assessing Bottlenose Dolphins’ (Tursiops truncatus) Health Status Through Functional Muscle Analysis, and Oxidative and Metabolic Stress Evaluation: A Preliminary Study. Animals. 2025; 15(9):1215. https://doi.org/10.3390/ani15091215
Chicago/Turabian StyleGatta, Claudia, Eugenio Luigi Iorio, Carla Genovese, Barbara Biancani, Alessandro Mores, Daniele La Monaca, Chiara Caterino, Luigi Avallone, Guillermo J. Sanchez-Contreras, Immaculata De Vivo, and et al. 2025. "Assessing Bottlenose Dolphins’ (Tursiops truncatus) Health Status Through Functional Muscle Analysis, and Oxidative and Metabolic Stress Evaluation: A Preliminary Study" Animals 15, no. 9: 1215. https://doi.org/10.3390/ani15091215
APA StyleGatta, C., Iorio, E. L., Genovese, C., Biancani, B., Mores, A., La Monaca, D., Caterino, C., Avallone, L., Sanchez-Contreras, G. J., De Vivo, I., Ciani, F., & Tafuri, S. (2025). Assessing Bottlenose Dolphins’ (Tursiops truncatus) Health Status Through Functional Muscle Analysis, and Oxidative and Metabolic Stress Evaluation: A Preliminary Study. Animals, 15(9), 1215. https://doi.org/10.3390/ani15091215