Radiographic assessment of pectoral flipper bone maturation in bottlenose dolphins (Tursiops truncatus), as a novel technique to accurately estimate chronological age
Autoři:
Ashley Barratclough aff001; Roberto Sanz-Requena aff002; Luis Marti-Bonmati aff002; Todd L. Schmitt aff003; Eric Jensen aff004; Daniel García-Párraga aff005
Působiště autorů:
National Marine Mammal Foundation, San Diego, California, United States of America
aff001; Radiology Department, Hospital Quironsalud Valencia, Blasco Ibáñez, Valencia, Spain
aff002; SeaWorld, San Diego, California, United States of America
aff003; U.S. Navy Marine Mammal Program, San Diego, California, United States of America
aff004; Fundación Oceanogràfic de la Comunidad Valenciana, Gran Vía Marqués del Turia, Valencia, Spain
aff005
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222722
Souhrn
Accurate age estimation in wildlife conservation is an important diagnostic tool in the interpretation of biological data, necropsy examination, reproductive status and population demographics. The most frequently utilized methods to age bottlenose dolphins (Tursiops truncatus) include tooth extraction; counting dental growth layer groups and dental radiography. These methods are inaccurate in dolphins > 13 years old, due to overlapping of the growth layer groups in dolphins and worn teeth. Establishing a non-invasive method of accurately aging bottlenose dolphins across the entire age range is important to long term conservation efforts to understand health status, lifespan, reproduction and survivability. A database of 126 radiographs from 94 dolphins of known chronological age was utilized to establish the stages of skeletal ossification over time. A numerical score from -1 to 8 was assigned to 16 anatomic locations on the pectoral radiograph, to create a formula to estimate age. The most informative areas to evaluate morphologically were the metaphyseal regions of the radius and ulna, and the proximal and distal epiphysis of metacarpals II and III. Third order polynomial regression calculated separate age predictor formulas for male and female dolphins, with females reaching sexual maturity earlier than males. Completion of epiphyseal closure of the long bones correlated with average sexual maturity. Managed care dolphin ages could be properly estimated with decreasing precision from within 3 months in animals < 5 years old, to within 5 years in animals > 30 years old. This diagnostic tool could also be applied to diagnose atypical ossification patterns consistent with nutritional, developmental or growth abnormalities, and identifying subclinical health issues. In conclusion, knowledge of the lifespan and the onset of sexual maturity for each species will allow this model to be applied to other cetaceans, facilitating age estimation via pectoral radiography in future research.
Klíčová slova:
Teeth – Aging – Ossification – Dolphins
Zdroje
1. Perrin WF, Myrick AC. Age determination of toothed whales and sirenians: International Whaling Commission; 1980.
2. Zweifel JR, Perrin WF. Fitting growth curves to odontocete tooth layer/length data. Age determination of toothed whales and sirenians Rep Int Whal Commn. 1980;3:216.
3. Hohn AA. Age determination and age related factors in the teeth of Western North Atlantic bottlenose dolphins. Scientific Reports of the Whales Research Institute. 1980(32):39–66.
4. Butti C, Corain L, Cozzi B, Podestà M, Pirone A, Affronte M, et al. Age estimation in the Mediterranean bottlenose dolphin Tursiops truncatus (Montagu 1821) by bone density of the thoracic limb. Journal of Anatomy. 2007;211(5):639–46. doi: 10.1111/j.1469-7580.2007.00805.x 17850286
5. Hui CA. Reliability of using dentin layers for age determination in Tursiops truncatus: Naval Ocean Systems Center Biosciences Department; 1978.
6. Kimura M. Variability in techniques of counting dentinal growth layer groups in a tooth of a known-age dolphin, Tursiops truncatus. Age Determination of Toothed Whales and Sirenians. 1980(3):161.
7. Schwarz LK, Runge MC. Hierarchical Bayesian analysis to incorporate age uncertainty in growth curve analysis and estimates of age from length: Florida manatee (Trichechus manatus) carcasses. Canadian Journal of Fisheries and Aquatic Sciences. 2009;66(10):1775–89.
8. Marsh H. Age determination of the dugong (Dugong dugon (Muller)) in northern Australia and its biological implications: Zoology Department, James Cook University of North Queensland; 1980.
9. Lubetkin SC, Zeh JE, Rosa C, George JC. Age estimation for young bowhead whales (Balaena mysticetus) using annual baleen growth increments. Canadian Journal of Zoology. 2008;86(6):525–38.
10. Lockyer C. The age at sexual maturity of the southern fin whale (Balaenoptera physalus) using annual layer counts in the ear plug. ICES Journal of Marine Science. 1972;34(2):276–94.
11. Benjaminsen T. Age determination and the growth and age distribution from cementum growth layers of bearded seals at Svalbard. Fiskeridirektoratets Skr. 1973;16:159–70.
12. Lockyer C, Hohn AA, Hobbs R, Stewart REA. Report of the workshop on age estimation in beluga: Beaufort, North Carolina, US 5–9 December 2011. NAMMCO Scientific Publications. 2016;10.
13. Cameriere R, Ferrante L, Cingolani M. Variations in pulp/tooth area ratio as an indicator of age: a preliminary study. Journal of Forensic Science. 2004;49(2):1–3.
14. George JC, Bada J, Zeh J, Scott L, Brown SE, O'Hara T, et al. Age and growth estimates of bowhead whales (Balaena mysticetus) via aspartic acid racemization. Canadian Journal of Zoology. 1999;77(4):571–80.
15. Bada JL, Brown S, Masters PM. Age determination of marine mammals based on aspartic acid racemization in the teeth and lens nucleus. Age Determination of Toothed Whales and Sirenians Report of the International Whaling Commission, Special. 1980(3):113–8.
16. Ferrero RC, Walker WA. Age, growth, and reproductive patterns of Dall's porpoise (Phocoenoides dalli) in the central North Pacific Ocean. Marine Mammal Science. 1999;15(2):273–313.
17. Campana SE, Stewart REA. Bomb dating, age validation and quality control of age determinations of monodontids and other marine mammals. NAMMCO Scientific Publications. 2014;10.
18. Kastelle CR, Shelden KEW, Kimura DK. Age determination of mysticete whales using 210Pb/226Ra disequilibria. Canadian journal of zoology. 2003;81(1):21–32.
19. Garde E, Frie AK, Dunshea G, Hansen SH, Kovacs KM, Lydersen C. Harp seal ageing techniques—teeth, aspartic acid racemization, and telomere sequence analysis. Journal of Mammalogy. 2010;91(6):1365–74.
20. Guglielmini C, Zotti A, Bernardini D, Pietra M, Podestá M, Cozzi B. Bone density of the arm and forearm as an age indicator in specimens of stranded striped dolphins (Stenella coeruleoalba). The Anatomical Record: An Official Publication of the American Association of Anatomists. 2002;267(3):225–30.
21. Powell JWB, Duffield DA, Kaufman JJ, McFee W. Bone density cannot accurately predict age in the common bottlenose dolphin, Tursiops truncatus. Mar Mam Sci. 2019;In Press.
22. Greulich WW, Pyle SI, Todd TW. Radiographic atlas of skeletal development of the hand and wrist: Stanford university press Stanford; 1959.
23. Loch C, Schwass DR, Kieser JA, Fordyce RE. Use of micro-computed tomography for dental studies in modern and fossil Odontocetes: Potential applications and limitations. NAMMCO Scientific Publications. 2013;10.
24. Kerley ER. The microscopic determination of age in human bone. American journal of physical anthropology. 1965;23(2):149–63. 5826273
25. Ogden JA, Conlogue GJ, Rhodin AGJ. Roentgenographic indicators of skeletal maturity in marine mammals (Cetacea). Skeletal Radiology. 1981;7(2):119–23. doi: 10.1007/bf00347376 7330661
26. Galatius A, Andersen MB, Haugan B, Langhoff HE, Jespersen Å. Timing of epiphyseal development in the flipper skeleton of the harbour porpoise (Phocoena phocoena) as an indicator of paedomorphosis. Acta Zoologica. 2006;87(1):77–82.
27. Sweeny MM, Price JM, Jones GS, French TW, Early GA, Moore MJ. Spondylitic changes in long-finned pilot whales (Globicephala melas) stranded on Cape Cod, Massachusetts, USA, between 1982 and 2000. Journal of Wildlife Diseases. 2005;41(4):717–27. doi: 10.7589/0090-3558-41.4.717 16456160
28. Barratclough A, editor A Case Report Following the Repair of an Ulna Fracture in a Manatee (Trichechus manatus latirostris) Calf and the Assessment of Carpal Bone Ossification. IAAAM Conference Procedings 46th Annual IAAAM Meeting 2015; Chicago IL.
29. Colegrove KM, Venn-Watson S, Litz J, Kinsel MJ, Terio KA, Fougeres E, et al. Fetal distress and in utero pneumonia in perinatal dolphins during the Northern Gulf of Mexico unusual mortality event. Diseases of aquatic organisms. 2016;119(1):1–16. doi: 10.3354/dao02969 27068499
30. Schmeling A, Reisinger W, Geserick G, Olze A. Age estimation of unaccompanied minors: Part I. General considerations. Forensic science international. 2006;159:S61–S4. doi: 10.1016/j.forsciint.2006.02.017 16529895
31. Whitaker JM, Rousseau L, Williams T, Rowan RA, Hartwig WC. Scoring system for estimating age in the foot skeleton. American Journal of Physical Anthropology: The Official Publication of the American Association of Physical Anthropologists. 2002;118(4):385–92.
32. Gilsanz V, Ratib O. Hand bone age: a digital atlas of skeletal maturity: Springer Science & Business Media; 2005.
33. Baumann U, Schulz R, Reisinger W, Heinecke A, Schmeling A, Schmidt S. Reference study on the time frame for ossification of the distal radius and ulnar epiphyses on the hand radiograph. Forensic science international. 2009;191(1–3):15–8. doi: 10.1016/j.forsciint.2009.05.023 19577387
34. Benke H. Investigations on the osteology and the functional morphology of the flipper of whales and dolphins (Cetacea). Investigations on Cetacea. 1993;24:9–252.
35. Cooper LN, Berta A, Dawson SD, Reidenberg JS. Evolution of hyperphalangy and digit reduction in the cetacean manus. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology: Advances in Integrative Anatomy and Evolutionary Biology. 2007;290(6):654–72.
36. Mellor L, Cooper LN, Torre J, Brownell RL Jr. Paedomorphic ossification in porpoises with an emphasis on the vaquita (Phocoena sinus). 2009.
37. Calzada N, Aguilar A, Grau E, Lockyer C. Patterns of growth and physical maturity in the western Mediterranean striped dolphin, Stenella coeruleoalba (Cetacea: Odontoceti). Canadian Journal of Zoology. 1997;75(4):632–7.
38. Dawson SD. Patterns of ossification in the manus of the harbor porpoise (Phocoena phocoena): Hyperphalangy and delta‐shaped bones. Journal of Morphology. 2003;258(2):200–6. doi: 10.1002/jmor.10146 14518013
39. de Carvalho APM, Lima JY, Azevedo CT, Botta S, Queiroz FFd, Campos AS, et al. Ossification Pattern of Estuarine Dolphin (Sotalia guianensis) Forelimbs, from the Coast of the State of Espírito Santo, Brazil. PloS one. 2015;10(5):e0127435. doi: 10.1371/journal.pone.0127435 26017269
40. Calzada N, Aguilar A. Flipper development in the Mediterranean striped dolphin (Stenella coeruleoalba). The Anatomical Record: An Official Publication of the American Association of Anatomists. 1996;245(4):708–14.
41. Paul E, Sikes RS. Wildlife researchers running the permit maze. ILAR journal. 2013;54(1):14–23. doi: 10.1093/ilar/ilt013 23904528
42. García-Párraga D, Schmitt TL, Jensen E. Use of Radiographic Parameters for Age Estimation in Bottlenose Dolphins (Tursiops truncatus). IAAAM Conference. 2011.
43. Steele J. Handedness in past human populations: skeletal markers. Laterality: Asymmetries of Body, Brain and Cognition. 2000;5(3):193–220.
44. Solovieva S, Vehmas T, Riihimäki H, Luoma K, Leino-Arjas P. Hand use and patterns of joint involvement in osteoarthritis. A comparison of female dentists and teachers. Rheumatology. 2005;44(4):521–8. doi: 10.1093/rheumatology/keh534 15728421
45. Wells RS. The role of long-term study in understanding the social structure of a bottlenose dolphin community. Dolphin societies: Discoveries and puzzles. 1991:199–225.
46. Read A, Wells R, Hohn A, Scott M. Patterns of growth in wild bottlenose dolphins, Tursiops truncatus. Journal of Zoology. 1993;231(1):107–23.
47. Harrison RJ, Ridgwa SH. Gonadal activity in some bottlenose dolphins (Tursiops truncatus). Journal of Zoology. 1971;165(3):355–66.
48. Schmeling A, Olze A, Reisinger W, König M, Geserick G. Statistical analysis and verification of forensic age estimation of living persons in the Institute of Legal Medicine of the Berlin University Hospital Charité. Legal medicine. 2003;5:S367–S71. 12935635
49. Galatius A, Jespersen Å. Bilateral directional asymmetry of the appendicular skeleton of the harbor porpoise (Phocoena phocoena). Marine mammal science. 2005;21(3):401–10.
50. Cutler GB Jr. The role of estrogen in bone growth and maturation during childhood and adolescence. The Journal of steroid biochemistry and molecular biology. 1997;61(3–6):141–4. 9365183
51. Stockin KA, Wiseman N, Hartman A, Moffat N, Roe WD. Use of radiography to determine age class and assist with the post‐mortem diagnostics of a Bryde's whale (Balaenoptera brydei). New Zealand Journal of Marine and Freshwater Research. 2008;42(3):307–13.
52. Aguilar A, Lockyer CH. Growth, physical maturity, and mortality of fin whales (Balaenoptera physalus) inhabiting the temperate waters of the northeast Atlantic. Canadian Journal of Zoology. 1987;65(2):253–64.
53. Stolen MK, Barlow J. A model life table for bottlenose dolphins (Tursiops truncatus) from the Indian River Lagoon System, Florida, USA. Marine mammal science. 2003;19(4):630–49.
54. Thacher TD, Fischer PR, Pettifor JM, Lawson JO, Manaster BJ, Reading JC. Radiographic scoring method for the assessment of the severity of nutritional rickets. Journal of Tropical Pediatrics. 2000;46(3):132–9. doi: 10.1093/tropej/46.3.132 10893912
55. Choo AD, Mubarak SJ. Longitudinal epiphyseal bracket. Journal of children's orthopaedics. 2013;7(6):449–54. doi: 10.1007/s11832-013-0544-1 24432108
56. Andersen E. Comparison of Tanner‐Whitehouse and Greulich‐Pyle methods in a large scale Danish survey. American journal of physical anthropology. 1971;35(3):373–6. doi: 10.1002/ajpa.1330350312 4332702
57. Lockyer C, Mackey B, Read F, Härkönen T, Hasselmeier I. Age determination methods in harbour seals (Phoca vitulina) with a review of methods applicable to carnivores. NAMMCO Scientific Publications. 2010;8:245–63.
58. Garn SM, Lewis AB, Blizzard RM. Endocrine factors in dental development. Journal of Dental Research. 1965;44(1):243–58.
59. Keller EE, Sather AH, Hayles AB. Dental and skeletal development in various endocrine and metabolic diseases. The Journal of the American Dental Association. 1970;81(2):415–9. doi: 10.14219/jada.archive.1970.0173 4316671
60. Schwacke LH, Zolman ES, Balmer BC, De Guise S, George RC, Hoguet J, et al. Anaemia, hypothyroidism and immune suppression associated with polychlorinated biphenyl exposure in bottlenose dolphins (Tursiops truncatus). Proceedings Biological sciences / The Royal Society. 2012;279(1726):48–57.
61. Schwacke LH, Smith CR, Townsend FI, Wells RS, Hart LB, Balmer BC, et al. Health of common bottlenose dolphins (Tursiops truncatus) in Barataria Bay, Louisiana, following the deepwater horizon oil spill. Environ Sci Technol. 2014;48(1):93–103. doi: 10.1021/es403610f 24350796
62. Lewall EF, Cowan IM. Age determination in black-tail deer by degree of ossification of the epiphyseal plate in the long bones. Canadian Journal of Zoology. 1963;41(4):629–36.
63. McMillan CJ, Griffon DJ, Marks SL, Mauldin GE. Dietary-related skeletal changes in a Shetland Sheepdog puppy. Journal of the American Animal Hospital Association. 2006;42(1):57–64. doi: 10.5326/0420057 16397196
64. Oginni LM, Sharp CA, Badru OS, Risteli J, Davie MWJ, Worsfold M. Radiological and biochemical resolution of nutritional rickets with calcium. Archives of disease in childhood. 2003;88(9):812–7. doi: 10.1136/adc.88.9.812 12937108
65. Lanham SA, Bertram C, Cooper C, Oreffo RO. Animal models of maternal nutrition and altered offspring bone structure–bone development across the lifecourse. Eur Cell Mater. 2011;22:321–32. 22116650
66. Holick MF. Resurrection of vitamin D deficiency and rickets. The Journal of clinical investigation. 2006;116(8):2062–72. doi: 10.1172/JCI29449 16886050
67. Lewis M, Roberts C. Growing pains: the interpretation of stress indicators. International Journal of Osteoarchaeology. 1997;7(6):581–6.
68. Byers S. Calculation of age at formation of radiopaque transverse lines. American journal of physical anthropology. 1991;85(3):339–43. doi: 10.1002/ajpa.1330850314 1897606
69. Smith CR, Rowles TK, Hart LB, Townsend FI, Wells RS, Zolman ES, et al. Slow recovery of Barataria Bay dolphin health following the Deepwater Horizon oil spill (2013–2014), with evidence of persistent lung disease and impaired stress response. Endangered Species Research. 2017;33:127–42.
70. Schaefer F, Seidel C, Binding A, Gasser T, Largo RH, Prader A, et al. Pubertal growth in chronic renal failure. Pediatric Research. 1990;28(1):5. doi: 10.1203/00006450-199007000-00002 2377395
71. Cole AL, Webb L, Cole TJ. Bone age estimation: a comparison of methods. The British journal of radiology. 1988;61(728):683–6. doi: 10.1259/0007-1285-61-728-683 3416108
72. Kim JR, Shim WH, Yoon HM, Hong SH, Lee JS, Cho YA, et al. Computerized Bone Age Estimation Using Deep Learning Based Program: Evaluation of the Accuracy and Efficiency. American Journal of Roentgenology. 2017;209(6):1374–80. doi: 10.2214/AJR.17.18224 28898126
73. George J, Nagendran J, Azmi K. Comparison study of growth plate fusion using MRI versus plain radiographs as used in age determination for exclusion of overaged football players. Br J Sports Med. 2012;46(4):273–8. doi: 10.1136/bjsm.2010.074948 21173009
Článok vyšiel v časopise
PLOS One
2019 Číslo 9
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania