Plasma alkaline phosphatase as a sensitive indicator of age and skeletal development in wild coscoroba swans
Cecilia P. Calabuig A C , Miguel Ferrer A , Roberto Muriel A and Vallo Tilgar B
+ Author Affiliations
- Author Affiliations
A Department of Ethology and Biodiversity Conservation, Estación Biológica de Doñana, CSIC, Avenida Americo Vespucio s/n, 41092 Sevilla, Spain.
B Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, Tartu 51014, Estonia.
C Corresponding author. Email: cecicalabuig@ebd.csic.es
Wildlife Research 37(6) 504-511 https://doi.org/10.1071/WR09160
Submitted: 19 November 2009 Accepted: 16 September 2010 Published: 18 October 2010
Abstract
Context.: Recent studies have suggested that plasma alkaline phosphatase (ALP) can be used to assess skeletal development as well as health status in wild animals.
Aims.: However, the information about age-related dynamics of ALP in birds, especially in precocial species, is very scarce. Therefore, before ALP measurements can be effectively interpreted, it is necessary to determine its normal variation for each species, age group and sex.
Methods.: Here, we report total-ALP levels of free-living coscoroba swans (Coscoroba coscoroba) from the most important breeding and moulting population in Brazil. Data were gathered during the moulting period and categorised according to sex and the following three different age classes: chick (n = 11), young (n = 14) and mature (n = 29).
Key results.: ALP levels were related to the longitudinal measure of the bones, gradually diminishing with age and showing significant differences among birds of different age classes. In all age groups, no effect of sex on T-ALP concentration was detected.
Conclusions.: We conclude that measuring ALP facilitates the discrimination among different-aged individuals with similar plumage characteristics and body size.
References
Albertsen, J. O., Abe, Y., Kashikawa, S., Ookawara, A., and Tamada, K. (2002). Age and sex differences in biometrics data recorded for whooper swans wintering in Japan. Waterbirds 25, 334–339.Allen, L. C. V., Allen, M. J., Breur, G. J., Hoffmann, W. E., and Richardson, D. C. (2000). A comparison of two techniques for the determination of serum bone-specific alkaline phosphatase activity in dogs. Research in Veterinary Science 68, 231–235.
| A comparison of two techniques for the determination of serum bone-specific alkaline phosphatase activity in dogs.Crossref | GoogleScholarGoogle Scholar | 10877968PubMed |
Alonso-Alvarez, C. (2005). Age-dependent changes in plasma biochemistry of yellow-legged gulls (Larus cachinnans). Comparative Biochemistry and Physiology. A. Comparative Physiology 140, 512–518.
Anderson, H. C. (1976). Matrix vesicles of cartilage and bone. In ‘The biochemistry and physiology of bone’. (Ed. G. H. Bourne.) pp. 135–157. (Academic Press: New York.)
Badzinski, S. S., Ankney, C. D., Leafloor, J. O., and Abraham, K. F. (2002). Growth and development of Canada geese and lesser snow geese: ecological adaptation or physiological constraint? The Auk 119, 221–227.
| Growth and development of Canada geese and lesser snow geese: ecological adaptation or physiological constraint?Crossref | GoogleScholarGoogle Scholar |
Bernardes, A. T., Machado, A. B. M., and Rylands, A. B. (1990). ‘Fauna Brasileira Ameacada de Extincao.’ (Fundação Biodiversitas, Belo Horizonte: Minas Gerais, Brazil.)
Boettcher, A. A. (2004). Valores bioquímicos sanguíneos del cisne de cuello negro (Cygnus melanocoryphus, Molina 1782), en una población silvestre de Valdivia, Chile. Degree Dissertation, University Austral de Chile, Valdivia, Chile.
Bourgeois, K., Curé, C., Legrand, J., Gómez-Díaz, E., Vidal, E., Aubin, T., and Mathevon, N. (2007). Morphological versus acoustic analysis: what is the most efficient method for sexing yelkouan shearwaters Puffinus yelkouan? Journal fur Ornithologie 148, 261–269.
| Morphological versus acoustic analysis: what is the most efficient method for sexing yelkouan shearwaters Puffinus yelkouan?Crossref | GoogleScholarGoogle Scholar |
Brown, R. D., Chao, C. C., and Faulkner, L. W. (1983). Hormone levels and antler development in white-tailed and sika fawns. Comparative Biochemistry and Physiology 75, 385–390.
| Hormone levels and antler development in white-tailed and sika fawns.Crossref | GoogleScholarGoogle Scholar | 6136372PubMed |
Calabuig, P. C., Ferrer, M., and Muriel, R. (2010a). Blood chemistry of wild Brazilian coscoroba swans during molt. Journal of Wildlife Diseases 46, 591–595.
| 20688656PubMed |
Calabuig, P. C., Green, J. A., Muriel, R., and Patino, J. (2010b). Fenología del coscoroba (Coscoroba coscoroba) en el sur de Brasil y sus movimientos hacia Argentina. Ornitología Neotropical , .
Carrier, D. R., and Auriemma, J. (1992). A developmental constraint on the fledging time of birds. Biological Journal of the Linnean Society. Linnean Society of London 47, 61–77.
| A developmental constraint on the fledging time of birds.Crossref | GoogleScholarGoogle Scholar |
Cubo, J., Fouces, V., Gonzales-Martin, M., Pedrocchi, V., and Ruiz, X. (2000). Nonheterochronic developmental changes underlie morphological heterochrony in the evolution of the Ardeidae. Journal of Evolutionary Biology 13, 269–276.
| Nonheterochronic developmental changes underlie morphological heterochrony in the evolution of the Ardeidae.Crossref | GoogleScholarGoogle Scholar |
de Behr, V., Daron, D., Gabriel, A., Remy, B., Dufrasne, I., Serteyn, D., and Istasse, L. (2003). The course of some bone remodelling plasma metabolites in healthy horses and in horses offered a calcium-deficient diet. Journal of Animal Physiology and Animal Nutrition 87, 149–159.
Dobado-Berrios, P., and Ferrer, M. (1997). Age-related changes of plasma alkaline phosphatase and inorganic phosphorus, and late ossification of the cranial roof in the Spanish imperial eagle (Aquila adalberti). Physiological Zoology 70, 421–427.
| Age-related changes of plasma alkaline phosphatase and inorganic phosphorus, and late ossification of the cranial roof in the Spanish imperial eagle (Aquila adalberti).Crossref | GoogleScholarGoogle Scholar |
Dobado-Berrios, P., Tella, J. L., Ceballos, O., and Donazar, J. A. (1998). Effect of age and captivity on plasma chemistry values of the Egyptian vulture. The Condor 100, 719–725.
| Effect of age and captivity on plasma chemistry values of the Egyptian vulture.Crossref | GoogleScholarGoogle Scholar |
Driver, E. A. (1981). Hematological and blood chemical values of mallard, Anas p. platyrhynchos, drakes before, during and right after remige moult. Journal of Wildlife Diseases 17, 413–421.
Dutta, C., Johnson, L. S., Larkin, D., and Mangurian, L. P. (1998). Skeletal development at the time of fledging in house wrens. The Condor 100, 568–573.
| Skeletal development at the time of fledging in house wrens.Crossref | GoogleScholarGoogle Scholar |
Fairbrother, A., Craig, M. A., Walker, K., and O’Loughlin, D. (1990). Changes in mallard (Anas platyrhynchos) serum chemistry due to age, sex, and reproductive condition. Journal of Wildlife Diseases 26, 66–67.
Ferrer, M. (1990). Haematological studies in birds. The Condor 92, 1085–1086.
| Haematological studies in birds.Crossref | GoogleScholarGoogle Scholar |
Ferrer, M., and Dobado-Berrios, P. (1998). Factors affecting plasma chemistry values of the Spanish imperial eagle, Aquila adalberti. Comparative Biochemistry and Physiology. A. Comparative Physiology 120, 209–217.
Fjeldså, J., and Krabbe, N. (1990). ‘Birds of the High Andes.’ (Zoological Museum, University of Copenhagen, and Apolo Books: Svendurg, Denmark.)
Fleisch, H., and Neuman, W. F. (1961). Mechanisms of calcification: role of collagen, polyphosphates, and phosphatase. American Journal of Physiology 200, 1296–1300.
Gambin, F., Bogé, G., and Jamet, D. (1999). Alkaline phosphatase in a littoral Mediterranean marine ecosystem: role of the main plankton size classes. Marine Environmental Research 47, 441–456.
| Alkaline phosphatase in a littoral Mediterranean marine ecosystem: role of the main plankton size classes.Crossref | GoogleScholarGoogle Scholar |
Gee, G. F., Carpenter, J. W., and Hensler, G. L. (1981). Species differences in haematological values of captive cranes, geese, raptors and quail. The Journal of Wildlife Management 45, 463–483.
| Species differences in haematological values of captive cranes, geese, raptors and quail.Crossref | GoogleScholarGoogle Scholar |
Glade, A. A. (1993). ‘Libro Rojo de los Vertebrados Terrestres de Chile.’ (Corporación Nacional Forestal (CONAF): Santiago de Chile.)
Grewal, R., and Mahmood, A. (2004). Coordinated secretion of alkaline phosphatase into serum and intestine in fat-fed rats. Indian Journal of Gastroenterology 23, 175–177.
He, P.-J., Yu, J.-Q., and Fang, S.-G. (2005). Sex identification of black swan (Cygnus atratus) using the locus/specific and implications for this reproduction. Reproduction in Domestic Animals 40, 196–198.
| Sex identification of black swan (Cygnus atratus) using the locus/specific and implications for this reproduction.Crossref | GoogleScholarGoogle Scholar |
Hoffmann, W. E., Solter, P. F., and Wilson, B. W. (1999). Clinical enzymology. In ‘The Clinical Chemistry of Laboratory Animals’. (Eds W. F. Loeb and F. W. Quimby.) pp. 399–454. (Taylor and Francis: Philadelphia, PA.)
Johnsgard, P. (1978). ‘Ducks, Geese, and Swans of the World.’ (University of Nebraska Press: Lincoln, NE.)
Kan, K. W., and Cress, R. L. (1987). Temporal relationship between fetal bovine skeletal growth and circulating hormone levels. Calcified Tissue International 40, 137–148.
| Temporal relationship between fetal bovine skeletal growth and circulating hormone levels.Crossref | GoogleScholarGoogle Scholar |
Kirkwood, J. K., Duignan, P. J., Kember, N. F., Bennett, P. M., and Price, D. J. (1989). The growth rate of the tarsometatarsus bone in birds. Journal of Zoology 217, 403–416.
| The growth rate of the tarsometatarsus bone in birds.Crossref | GoogleScholarGoogle Scholar |
Kuz’mina, V., Glatman, L., Drabkin, V., and Gelman, A. (2003). Amylolytic activity in fish intestinal mucosa: temperature effects. Comparative Biochemistry and Physiology. B, Comparative Biochemistry 134, 529–534.
| Amylolytic activity in fish intestinal mucosa: temperature effects.Crossref | GoogleScholarGoogle Scholar |
Lahiri, D. K., and Nurnberger, J. I. (1991). A rapid non-enzymatic method for the preparation of HMW DNA from blood for RFLP studies. Nucleic Acids Research 19, 5444.
| A rapid non-enzymatic method for the preparation of HMW DNA from blood for RFLP studies.Crossref | GoogleScholarGoogle Scholar |
Lewandowski, A. H., Campbell, T. W., and Harrison, G. J. (1986). Clinical chemistries. In ‘Clinical Avian Medicine and Surgery’. (Eds G. H. Harrison and L. R. Harrison.) pp. 192–200. (Saunders: Philadelphia, PA.)
Mänd, R., Tilgar, V., and Leivits, A. (2000). Reproductive response of great tits, Parus major, in a naturally base-poor forest habitat to calcium supplementation. Canadian Journal of Zoology 78, 689–695.
| Reproductive response of great tits, Parus major, in a naturally base-poor forest habitat to calcium supplementation.Crossref | GoogleScholarGoogle Scholar |
Mathiasson, S. (1980). Weight and growth rates of morphological characters of Cygnus olor. In ‘Proceedings, 2nd International Swan Symposium’. (Eds G. V. T. Matthews and M. Smart.) pp. 379–389. (IWRB: Sapporo, Japan.)
Mathiasson, S. (2005). Biometrics and structures of the mute swan, Cygnus olor – parameters and technique used in a Swedish project. Göteborgs Naturhistoriska Museum Årstryck 2005, 77–86.
Menegheti, J. O., and Dotto, J. C. (2006). Status of the black-necked swan Cygnus melanocorypha and coscoroba swan Coscoroba coscoroba in the south of Brazil. In ‘Waterbirds around the World’. (Eds G. C. Boere and D. A. Stroud.) pp. 183–184. (The Stationery Office: Edinburgh, UK.)
Miller, S. L., Gregg, M. A., Kuritsubo, A. R., Combs, S. M., Murdock, M. K., Nilsson, J. A., Noon, B. R., and Botzler, R. G. (1988). Morphometric variation in tundra swans: relationships among sex and age classes. The Condor 90, 802–815.
| Morphometric variation in tundra swans: relationships among sex and age classes.Crossref | GoogleScholarGoogle Scholar |
Nascimento, J. L. X., Flores, J. M., Ataguile, B. S., Koch, M., Barbosa, S., and Parreira dos Santos, P. J. (2001). Biological aspects of the black-necked swan (Cygnus melancoryphus) and coscoroba swan (Coscoroba coscoroba) in Rio Grande do Sul state, Brazil. Melopsittacus 4, 31–38.
Newbrey, J. W., and Banks, W. J. (1975). Characterization of developing antler cartilage matrix. 11. An ultrastructural study. Calcified Tissue Research 17, 289–302.
| Characterization of developing antler cartilage matrix. 11. An ultrastructural study.Crossref | GoogleScholarGoogle Scholar |
Olayemi, F. O., Arowolo, R. O. A., Saba, A. B., and Famakinde, S. A. (2002). Effect of sex on the blood profiles of the Nigerian local duck. Bulletin of Animal Health and Production in Africa 50, 67–71.
Olsen, G., Rininger, D., Ets, M., and Sladen, W. (2002). Baseline haematology and clinical chemistry results from captive-raised trumpeter swans. Waterbirds 25, 375–379.
Perry, M., Obrecht, H., Williams, B., and Kuenzel, W. (1986). Blood chemistry and hematocrit of captive and wild canvasbacks. The Journal of Wildlife Management 50, 435–441.
| Blood chemistry and hematocrit of captive and wild canvasbacks.Crossref | GoogleScholarGoogle Scholar |
Polo, F. J. (1995). Estudio bioquımico y enzimatico del plasma de aves en cautividad. Ph.D. Thesis. Universidad de Barcelona, Spain.
Price, C. P. (1993). Multiple forms of human serum alkaline phosphatase: detection and quantification. Annals of Clinical Biochemistry 30, 355–372.
Proctor, N. S., and Lynch, P. J. (1993). ‘Manual of Ornithology: Avian Structure and Function.’ (Yale University Press: New Haven, CT.)
Puerta, M. L., Garcia del Campo, A. L., Abendela, M., Fernandez, A., Huecas, V., and Nava, M. P. (1992). Hematological trends in flamingos, Phoenicopterus tuber. Comparative Biochemistry and Physiology. A. Comparative Physiology 102, 683–686.
| Hematological trends in flamingos, Phoenicopterus tuber.Crossref | GoogleScholarGoogle Scholar |
Romagnoli, E., Minisola, G., Carnevale, V., Scillitani, A., Frusciante, V., Aliberti, G., and Minisola, S. (1998). Assessment of serum total and bone alkaline phosphatase measurement in clinical practice. Clinical Chemistry and Laboratory Medicine 36, 163–168.
| Assessment of serum total and bone alkaline phosphatase measurement in clinical practice.Crossref | GoogleScholarGoogle Scholar |
Salo, L. A., Yliniemi, T., Larmas, M., and Nieminen, M. (1986). Phosphatase and peptidase activities in reindeer antler throughout the growth cycle. Journal of Interdisciplinary Cycle Research 17, 1–6.
Seijas, S. M. (2001). ‘Censo Neotropical de Cisnes, Período 1998–2000.’ (LOLA: Buenos Aires, Argentina.)
Seiser, P. E., Duffy, L. K., McGuires, A. D., Roby, D. D., Golet, G. H., and Litzow, M. A. (2000). Comparison of pigeon guillemot, Cepphus columba, blood parameters from oiled and unoiled areas of Alaska eight years after the Exxon Valdez oil spill. Marine Pollution Bulletin 40, 152–164.
| Comparison of pigeon guillemot, Cepphus columba, blood parameters from oiled and unoiled areas of Alaska eight years after the Exxon Valdez oil spill.Crossref | GoogleScholarGoogle Scholar |
Silva-Garcia, C. M., and Brewer, G. L. (2007). Breeding behavior of the coscoroba swan (Coscoroba coscoroba) in El Yali wetland, central Chile. Ornitologia Neotropical 18, 573–585.
Solberg, H. E. (1987). International Federation of Clinical Chemistry (IFCC) Scientific Committee, Clinical Section. Expert Panel on Theory of Reference Values (EPTRV) and International Committee for Standardization in Haematology (ICSH) Standing Committee on Reference Values. Approved recommendation (1987) on the theory of reference values. Part 5. Statistical treatment of collected reference values. Determination of reference limits. Clinica Chimica Acta 170, S13–S32.
Takenaka, A., Gotoh, S., Watanabe, T., and Takenaka, O. (1988). Developmental changes of plasma alkaline phosphatase, calcium and inorganic phosphorus in relation to the growth of bones in the Japanese macaque (Macaca fuscata). Primates 29, 395–404.
| Developmental changes of plasma alkaline phosphatase, calcium and inorganic phosphorus in relation to the growth of bones in the Japanese macaque (Macaca fuscata).Crossref | GoogleScholarGoogle Scholar |
Tilgar, V., Mänd, R., Ots, I., Mägi, M., Kilgas, P., and Reynolds, S. J. (2004a). Calcium availability affects bone growth in nestlings of free-living great tits (Parus major), as detected by plasma alkaline phosphatase. Journal of Zoology 263, 269–274.
| Calcium availability affects bone growth in nestlings of free-living great tits (Parus major), as detected by plasma alkaline phosphatase.Crossref | GoogleScholarGoogle Scholar |
Tilgar, V., Ots, I., and Mänd, R. (2004b). Bone alkaline phosphatise as a sensitive indicator of skeletal development in birds: a study of great tit nestlings. Physiological and Biochemical Zoology 77, 530–535.
| Bone alkaline phosphatise as a sensitive indicator of skeletal development in birds: a study of great tit nestlings.Crossref | GoogleScholarGoogle Scholar |
Tilgar, V., Kilgas, P., Viitak, A., and Reynolds, S. J. (2008a). The rate of bone mineralization in birds is directly related to alkaline phosphatase activity. Physiological and Biochemical Zoology 81, 106–111.
| The rate of bone mineralization in birds is directly related to alkaline phosphatase activity.Crossref | GoogleScholarGoogle Scholar |
Tilgar, V., Kilgas, P., Mägi, M., and Mänd, R. (2008b). Age-related changes in the activity of bone alkaline phosphatase and its application as a marker of prefledging maturity of nestlings in wild passerines. The Auk 125, 456–460.
| Age-related changes in the activity of bone alkaline phosphatase and its application as a marker of prefledging maturity of nestlings in wild passerines.Crossref | GoogleScholarGoogle Scholar |
Villegas, A., Sanchez, J. M., Costillo, E., and Corbacho, C. (2002). Blood chemistry and haematocrit of the black vulture (Aegypius monachus). Comparative Biochemistry and Physiology. A. Comparative Physiology 132, 489–497.
Viñuela, J., and Ferrer, M. (1997). Regulation of growth in red kites and imperial eagles. The Wilson Bulletin 109, 92–101.
Viñuela, J., Ferrer, M., and Recio, F. (1991). Age-related variations in plasma levels of alkaline phosphatase, calcium and inorganic phosphorus in chicks of two species of raptors. Comparative Biochemistry and Physiology. A. Comparative Physiology 99, 49–54.
| Age-related variations in plasma levels of alkaline phosphatase, calcium and inorganic phosphorus in chicks of two species of raptors.Crossref | GoogleScholarGoogle Scholar |
Warner, G. P., Hubbard, H. L., Lloyd, G. C., and Wuthier, R. E. (1983). Pi and Ca metabolism by matrix vesicles prepared from chicken epiphyseal cartilage microsomes by isosmotic Percoll density-gradient fractionation. Calcified Tissue International 35, 327–338.
| Pi and Ca metabolism by matrix vesicles prepared from chicken epiphyseal cartilage microsomes by isosmotic Percoll density-gradient fractionation.Crossref | GoogleScholarGoogle Scholar |
Watkins, B. A., Li, Y., Allen, K. G. D., Hoffmann, W. E., and Seifert, M. F. (2000). Dietary ratio of (n-6)/(n-3) polyunsaturated fatty acids alters the fatty acid composition of bone compartments and biomarkers of bone formation in rats. Journal of Nutrition 130, 2274–2284.
Whitehead, P. J., and Tschirner, T. (1990). Magpie goose, Anseranas semipalmata, nesting on the Mary River floodplain, Northern Territory, Australia: extent and frequency of flooding losses. Australian Wildlife Research 17, 147–157.
| Magpie goose, Anseranas semipalmata, nesting on the Mary River floodplain, Northern Territory, Australia: extent and frequency of flooding losses.Crossref | GoogleScholarGoogle Scholar |
