- Email: [email protected]
Blood chemistry values in three Pygoscelis penguins
Camp. Eiochem. Physiol. Vol. IOSA, No. 3, pp. 471473,
1993
0300-9629/93 $6.00 + 0.00 0 1993 Pergamon Press Ltd
Printed in Great Britain
BLOOD CHEMISTRY
VALUES IN THREE PENGUINS
PYGOSCELIS
EDUARDOAGUILERA,*JUAN MORENO?and MIGUELFERRER*$ *EstacGn Biolbgica de Doriana (CSIC) Avd. Maria Luisa, PabeGn de1 Peri 41013 Sevilla, Spain (Tel. 95-423-2340; Fax 95-462-l 125); tMuseo National de Ciencias Naturales (CSIC), J. Gutierrez
Abascal 2, 28006 Madrid, Spain (Received
I September
1992; accepted 16 October 1992)
Abstract-l. Analyses of 23 blood chemistry values were made in blood from 26 Antarctic penguins representing three different species Pygoscelis adeliae, Pygoscelisantarcticaand PygoscelisPapua. 2. Means, standard deviations and differences between species using multiple range test were obtained for each parameter investigated. 3. PygosceZis Papua exhibits values of total protein and LDH greater than the other two penguins and lower values of cholinesterase, amylase and glucose. Mean concentration of urea was the lowest in the blood of Pygoscelis antarctica, and alkaline phosphatase mean value was the greatest in this species. 4. Blood chemistry values in Pygoscelis penguins were essentially similar to those described in other bird groups. We have not found any apparent variation in penguins normal values that could be interpreted as an adaptation to Antarctic special environmental conditions.
identify differences among species, using free-living animals.
INTRODUCTION Hematological studies carried out on several aspects of the biochemistry and physiology of birds have been increasing, in particular those concerned with the determination of normal values of blood parameters. Hematological differences among taxonomic groups of birds (mainly domestic species) have been described (Balasch et al., 1976; Gee et al., 1981; Ferrer et al., 1987; Puerta et al., 1989a). However, studies on normal concentration of blood constituents of free-living birds are not very common (Puerta et al., 1989b; Puerta et al., 1990; Gonzalez and Hiraldo, 1991). Antarctic penguins are those species whose breeding range extends south of 60” S. They include the three species of the genus Pygoscelis; Adklie Pygoscelis udeliue, chinstrap Pygoscelis antarctica, and gentoo Pygoscelis pupuu. Numerous investigations have been carried out on the fasting capacity of the emperor and the king penguins Aptenodytes forsteri Aptenodytes putugonicu using blood chemistry values (Robin et al., 1988; Cherel and Le Maho, 1988; Cherel et al., 1988). Despite the great scientific attention given to penguins, due to the special environmental conditions where they live, as far as we know, no study on normal levels of the blood chemistry has been carried out with any member of the Pygoscelis genus. The aim of this study was to determine the normal limits of some hematological values and attempt to
$To whom all correspondence
should be addressed.
MATERIALSANDMETHODS This study was carried out on King George Island, South Shetland Islands, Antarctica (62”1O’S, 58”3O’W) during the 1989-90 Antarctic summer. Blood samples were obtained from 26 individuals; seven Ad&lies, 10 chinstraps, and nine gentoos. All the birds were captured at the proximity of the rookery and released at the same place after blood sampling. Up to 2 ml were obtained in each extraction from the brachial vein of the wing. Blood samples were collected in lithium-heparin tubes. Blood centrifugation and separation of plasma (10 min at 3000 rpm) were done within 6 hr after the sample was drawn. All the samples were collected between 12 a.m. and 8 p.m. to eliminate possible diurnal fluctuations caused by the circadian rhythms (Garcia-Rodriguez et al., 1987; Ferrer, 1990). A total of 23 blood parameter values have been determined. Analyses of 19 chemistry values were made on a computer process-controlled autoanalyzer (Hitachi 705 Multichannel Autoanalyzer) with the reagents recommended by Boehringer-Mannheim (Darmstadt, F.R.G.) Blood values of T3 and T4 were determined by radioimmunoassays. Methods for individual blood chemistries are presented in Table 1. Means and standard deviations (SD) were calculated in each parameter investigated. Statistical analyses were performed using One-way ANOVA. Multiple range tests based on 95% confidence intervals were used to determined differences between species.
471
472
EDUARW AGUILERA et al. Table 1. Methods used for individual blood chemistries Chemistrv
Units
Laboratorv
Glucose Urea Uric acid Cholesterol Triglyceride Total protein Creatinine Amylase Calcium Phosphorus Magnesium GOT GPT GGT
mg/dl mg/dl mg/dl mg/dl mg/dl g/d1 mgldl UP mg/dl mgidl mg/dl U/l UP UP
GOD-PAP method Unease reaction Uricase reaction CHOH-PAP Enzymatic method Biuret reaction Kinetic Jaffe reaction Maltotetraose reaction Cresolphtalein complexone reaction Molybdenum blue reaction Xylidyl blue reaction I.F.C.C. technique I.F.C.C. technique L-Gamma-glutamyl-p-nitroanalide UV NAC activated uv Paranitrophenyl-phosphate Butyryl-thiocholin reaction Ion-selective-electrode Ion-selective-electrode Ion-selective-electrode Fluoroimmunoanalysis Fluoroimmunoanalysis
CPK
U/l
LDH Alkaline phosphatase Cholinesterase Sodium Potassium Chlorine T3 Thyroxine
UP U/l U/l mM/l mM/l mM/I ng/ml g/d1
RESULTS
Table 2 shows the values obtained for Adelie, chinstrap, and gentoo penguins. Differences between species, as revealed by multiple range tests (P
method
The results of the blood analyses for the rest of parameters showed a great uniformity, except for the plasma concentrations of T3, sodium and triglyceride, although no statistically significant differences between species were found.
DISCUSSION
The main objective of this study was to establish normal values for several hematological parameters of three species of the genus Pygoscelis, and to determine their mean values using free-living birds. Factors, such as age or sex, that could have influenced these ranges and could have deflected the
Table 2. Means and standard deviations of plasmatic levels of 23 blood parameters in three penguin species: seven Pycoscelis adeliae, 10 Pygosceh antarctica, and nine Pygoscelis papua
GlUCOS.2 Urea Uric acid Cholesterol Triglyceride Total protein Creatinine Amylase Calcium Phosphorus Magnesium GOT GPT GGT CPK LDH Alkaline phosphatase Cholinesterase Sodium Potassium Chlorine T3 Thyroxine
P. adeliae
P. antarctica
P. papua
mean f SD
mean f SD
mean + SD
F
277.3 f 27.2’ 3.7 + 1.6b 7.2 + 2.9 214.6 + 27.8 75.9 f 17.0 4.1 f 0.2’ 0.33 + 0.03 2440 k 665b 10.0 * 1.2 3.8 f 1.2 1.9+_0.1 141.9 + 64.0 52.7 + 26.2 2.8 Il.1 688 f 997 374.2 & 159’b 356.6 + 10Sb 4467 + 852’ 156.5 + 1.2 3.46 + 0.45 116.6 + 2.6 1.95 rt 0.55 2.97 + 0.94
236.5 f 27.2b 7.9 + 4.2”b 12.1 + 4.8 236.9 f 41.8 102.3 i_ 26.0 4.7 + 0.3b 0.30 f 0.04 1251 + 523’ 10.4 ?r 0.7 3.9 + 1.2 2.1 f 0.1 139.2 + 66.8 64.8 f 20.2 2.7 f I .9 514k87 514 f 126b 128 f 74.2” 2981 + 484’ 155.8 +_2.4 4.14 f 1.21 116.8 f 3.1 1.29 5 0.56 2.83 + 0.78
II.19 7.06 5.41 2.13 3.89 14.52 0.82 21.49 0.37 I .83 2.02 0.11 I .97 I .48 0.46 11.41 30.02 5.29 2.65 1.52 0.06 3.46 0.56
286.7 k 24.4’ 10.4 + 5.1s 12.8 f 4.5 244.6 + 19.0 81.4 f 20.4 4.1 * 0.3” 0.31 f 0.05 3694 + 1038” 10.1 f 1.3 2.9 + 1.0 2.0 + 0.2 151.9f21.4 42.3 + 19.6 3.9 + 1.3 394 * 200 201.0 f 73.4a 86.1 + 22.4’ 3669 f 1318ab 158.2 + 2.5 3.79 + 0.71 117.2k3.7 I .48 f 0.56 2.56 C 0.42
P
0.011 0.144 0.034
Multiple range tests were used to determined differences between species. In each parameter, means not marked by the same letter are significantly different (P c: 0.05).
Penguin blood chemistry means of the respective parameters from those of the population as a whole have not been considered. As far as we know, there is no study that deals with any functional parameter of these three penguin species, therefore no comparisons with previous data are possible. Nevertheless we can see that mean glucose values in penguins were lower than those found in raptors (Balash et af., 1976; Rehder et al., 1982; Ferrer et al., 1987), and essentially similar to those described in other bird groups (Gee et al., 1981). The mean concentration of this parameter in Pygoscelis Papua was lower than in the other two penguin species. The glucogenic mechanisms in this penguin are likely to be important, because of its feeding habits. Gentoo penguins feed inshore and are deep divers, and has both, average prey size and average body mass, greater than the other two penguin species (Trivelpiece et al., 1987). The mean concentration of urea in the blood of the chinstrap was significantly lower than those of the other two species (Table 2). These results indicate that Pygoscelis penguins, like other bird groups, have blood urea concentrations lower than those for blood uric acid (Gee et al., 1981; Puerta et al., 1989a). Nevertheless, in other groups of birds like raptors (Gee et al., 1981; Ferrer et al., 1987) or common cranes Grus grus (Puerta et al., 1990), higher concentrations for urea than for uric acid have been reported. Blood concentrations of cholesterol (Table 2) were not statistically different for the three assayed species, and similar to those described for other bird species (Gee et al., 1981; Ferrer et al., 1987; Puerta et al., 1989a). Plasma content of triglycerides was similar to those previously published for other bird species (Balash et af., 1976; Gee et al., 1981), although lower than those described for chicks of Ciconia ciconia and Ciconia nigra (Puerta et al., 1989b). The respective concentrations of calcium, phosphorus, magnesium, potassium, chlorine, T3 and thyroxine were statistically the same for the three penguin species (Table 2). We have not been able to find any ecological or physiological explanation for differences found in blood concentrations of LDH, amylase and cholinesterase (Table 2). Plasma concentration of total protein was greater in P. papua. According to Smith and Bush (1978), total protein estimation is a valuable test for evaluating the general nutritional state of a bird, a low total protein being indicative of malnutrition. Alkaline phosphatase concentration was greater in P. antarctica. This enzyme is involved in chondrogenics and osteoblastic activities and related with growth and secondary ossification of the osseous tissue (Vifiuela et al., 1991 and references therein). So, lower values in chinstraps could be indicative of a greater proportion of immature birds in the sample of this species.
473
Acknowledgements-Financial support was received from Consejo Superior de Investigaciones Cientificas. We gratefully appreciate the cooperation of F. Recio in blood analyses and the University of Chile for logistic support in Antarctica.
REFERENCES
Balasch J., Musquera S., Palacios L., Jimenez M. and Palomeque J. (1976) Comparative hematology of some falconiformes. Condor 78, 258-273. Cherel Y. and Le Maho Y. (1988) Changes in body mass and plasma metabolites during short-term fasting in the king penguin. Condor 90, 257-258. Cherel Y., Robin J. P., Walch O., Karmann H., Netchitailo P. and Le Maho Y. (1988) Fasting in king penguin: I. Hormonal and metabolic changes during breeding. Am. J. Physiol. 254, 170-177.
-
-
-
Ferrer M. (1990) Hematoloaical studies in birds. Condor 92. 1085-1086. ’ Ferrer M., Garcia-Rodriguez T., Carriho J. C. and Castroviejo J. (1987) Hematocrit and blood chemistry values in captive raptors. Comp. Biochem. Physiol. 87A, 1123-I 127. Garcia-Rodriguez T., Ferrer M., Recio F. and Castroviejo J. (1987) Circadian rhvthms of determined blood chemistry values in buzzards and eagle owls. Comp. Biochem. Physiol. @#A, 663469. Gee G. F., Carpenter J. W. and Hensler G. L. (1981) Species differences in hematological values of captive cranes, geese, raptors and quail. J. Wildl. Manage. 45, 4633483.
Gonzalez J. L. and Hiraldo F. (1991) Some hematological data from marsh harriers (Circus aeruginosus) in central Spain. Comp. Biochem. Physiol. lOBA, 735-737. Puerta M. L., Alonso J. C., Huecas V., Alonso J. A., Abelenda M. and Muiioz-Pulido R. (19901 \ , Hematoloav and blood chemistry of wintering common cranes. Condor 92, 21%214. Puerta M. L., Huecas V. and Garcia de1 Campo A. L. (1989a) Hematology and blood chemistry of the Chilean flamingo. Comp. Biochem. Physiol. 94A, 623-625. Puerta M. L., Muxioz-Pulido R., Huecas V. and Abelenda M. (1989b) Hematology and blood chemistry of chicks of white and black storks (Ciconia ciconia and Ciconia nigra). Comp. Biochem. Physiol. 94A, 201-204. Rehder N. B., Bird D. N., Lague P. C. and Mackay C. (1982) Variation in selected hematological parameters of captive red tailed hawk. J. Wildl. Dis. 18, 105-109. Robin J. P., Frain M., Sardet C., Groscolas R. and Le Maho Y. (1988) Protein and lipid utilization during long-term fasting in emperor penguins. Am. J. Physiol. 1_
254, 6168.
Smith E. E. and Bush M. (1978) Haematological parameters on various species of Strigiformes and Falconiformes. J. Wildl. Dis. 14, 447-450.
Trivelpiece W. Z., Trivelpiece S. G. and Volkman N. J. (1987) Ecological segregation of Ad&lie, gentoo, and chinstrap penguins at King George Island, Antarctica. Ecology 68, 351-361. Viiiuela J., Ferrer M. and Recio F. (1991) Age-related variations in plasmatic levels of alkaline phosphatase, calcium and inorganic phosphorus in chicks of two species of raptors. Comp. Biochem. Physiol. !@A, 49-54.
1993
0300-9629/93 $6.00 + 0.00 0 1993 Pergamon Press Ltd
Printed in Great Britain
BLOOD CHEMISTRY
VALUES IN THREE PENGUINS
PYGOSCELIS
EDUARDOAGUILERA,*JUAN MORENO?and MIGUELFERRER*$ *EstacGn Biolbgica de Doriana (CSIC) Avd. Maria Luisa, PabeGn de1 Peri 41013 Sevilla, Spain (Tel. 95-423-2340; Fax 95-462-l 125); tMuseo National de Ciencias Naturales (CSIC), J. Gutierrez
Abascal 2, 28006 Madrid, Spain (Received
I September
1992; accepted 16 October 1992)
Abstract-l. Analyses of 23 blood chemistry values were made in blood from 26 Antarctic penguins representing three different species Pygoscelis adeliae, Pygoscelisantarcticaand PygoscelisPapua. 2. Means, standard deviations and differences between species using multiple range test were obtained for each parameter investigated. 3. PygosceZis Papua exhibits values of total protein and LDH greater than the other two penguins and lower values of cholinesterase, amylase and glucose. Mean concentration of urea was the lowest in the blood of Pygoscelis antarctica, and alkaline phosphatase mean value was the greatest in this species. 4. Blood chemistry values in Pygoscelis penguins were essentially similar to those described in other bird groups. We have not found any apparent variation in penguins normal values that could be interpreted as an adaptation to Antarctic special environmental conditions.
identify differences among species, using free-living animals.
INTRODUCTION Hematological studies carried out on several aspects of the biochemistry and physiology of birds have been increasing, in particular those concerned with the determination of normal values of blood parameters. Hematological differences among taxonomic groups of birds (mainly domestic species) have been described (Balasch et al., 1976; Gee et al., 1981; Ferrer et al., 1987; Puerta et al., 1989a). However, studies on normal concentration of blood constituents of free-living birds are not very common (Puerta et al., 1989b; Puerta et al., 1990; Gonzalez and Hiraldo, 1991). Antarctic penguins are those species whose breeding range extends south of 60” S. They include the three species of the genus Pygoscelis; Adklie Pygoscelis udeliue, chinstrap Pygoscelis antarctica, and gentoo Pygoscelis pupuu. Numerous investigations have been carried out on the fasting capacity of the emperor and the king penguins Aptenodytes forsteri Aptenodytes putugonicu using blood chemistry values (Robin et al., 1988; Cherel and Le Maho, 1988; Cherel et al., 1988). Despite the great scientific attention given to penguins, due to the special environmental conditions where they live, as far as we know, no study on normal levels of the blood chemistry has been carried out with any member of the Pygoscelis genus. The aim of this study was to determine the normal limits of some hematological values and attempt to
$To whom all correspondence
should be addressed.
MATERIALSANDMETHODS This study was carried out on King George Island, South Shetland Islands, Antarctica (62”1O’S, 58”3O’W) during the 1989-90 Antarctic summer. Blood samples were obtained from 26 individuals; seven Ad&lies, 10 chinstraps, and nine gentoos. All the birds were captured at the proximity of the rookery and released at the same place after blood sampling. Up to 2 ml were obtained in each extraction from the brachial vein of the wing. Blood samples were collected in lithium-heparin tubes. Blood centrifugation and separation of plasma (10 min at 3000 rpm) were done within 6 hr after the sample was drawn. All the samples were collected between 12 a.m. and 8 p.m. to eliminate possible diurnal fluctuations caused by the circadian rhythms (Garcia-Rodriguez et al., 1987; Ferrer, 1990). A total of 23 blood parameter values have been determined. Analyses of 19 chemistry values were made on a computer process-controlled autoanalyzer (Hitachi 705 Multichannel Autoanalyzer) with the reagents recommended by Boehringer-Mannheim (Darmstadt, F.R.G.) Blood values of T3 and T4 were determined by radioimmunoassays. Methods for individual blood chemistries are presented in Table 1. Means and standard deviations (SD) were calculated in each parameter investigated. Statistical analyses were performed using One-way ANOVA. Multiple range tests based on 95% confidence intervals were used to determined differences between species.
471
472
EDUARW AGUILERA et al. Table 1. Methods used for individual blood chemistries Chemistrv
Units
Laboratorv
Glucose Urea Uric acid Cholesterol Triglyceride Total protein Creatinine Amylase Calcium Phosphorus Magnesium GOT GPT GGT
mg/dl mg/dl mg/dl mg/dl mg/dl g/d1 mgldl UP mg/dl mgidl mg/dl U/l UP UP
GOD-PAP method Unease reaction Uricase reaction CHOH-PAP Enzymatic method Biuret reaction Kinetic Jaffe reaction Maltotetraose reaction Cresolphtalein complexone reaction Molybdenum blue reaction Xylidyl blue reaction I.F.C.C. technique I.F.C.C. technique L-Gamma-glutamyl-p-nitroanalide UV NAC activated uv Paranitrophenyl-phosphate Butyryl-thiocholin reaction Ion-selective-electrode Ion-selective-electrode Ion-selective-electrode Fluoroimmunoanalysis Fluoroimmunoanalysis
CPK
U/l
LDH Alkaline phosphatase Cholinesterase Sodium Potassium Chlorine T3 Thyroxine
UP U/l U/l mM/l mM/l mM/I ng/ml g/d1
RESULTS
Table 2 shows the values obtained for Adelie, chinstrap, and gentoo penguins. Differences between species, as revealed by multiple range tests (P
method
The results of the blood analyses for the rest of parameters showed a great uniformity, except for the plasma concentrations of T3, sodium and triglyceride, although no statistically significant differences between species were found.
DISCUSSION
The main objective of this study was to establish normal values for several hematological parameters of three species of the genus Pygoscelis, and to determine their mean values using free-living birds. Factors, such as age or sex, that could have influenced these ranges and could have deflected the
Table 2. Means and standard deviations of plasmatic levels of 23 blood parameters in three penguin species: seven Pycoscelis adeliae, 10 Pygosceh antarctica, and nine Pygoscelis papua
GlUCOS.2 Urea Uric acid Cholesterol Triglyceride Total protein Creatinine Amylase Calcium Phosphorus Magnesium GOT GPT GGT CPK LDH Alkaline phosphatase Cholinesterase Sodium Potassium Chlorine T3 Thyroxine
P. adeliae
P. antarctica
P. papua
mean f SD
mean f SD
mean + SD
F
277.3 f 27.2’ 3.7 + 1.6b 7.2 + 2.9 214.6 + 27.8 75.9 f 17.0 4.1 f 0.2’ 0.33 + 0.03 2440 k 665b 10.0 * 1.2 3.8 f 1.2 1.9+_0.1 141.9 + 64.0 52.7 + 26.2 2.8 Il.1 688 f 997 374.2 & 159’b 356.6 + 10Sb 4467 + 852’ 156.5 + 1.2 3.46 + 0.45 116.6 + 2.6 1.95 rt 0.55 2.97 + 0.94
236.5 f 27.2b 7.9 + 4.2”b 12.1 + 4.8 236.9 f 41.8 102.3 i_ 26.0 4.7 + 0.3b 0.30 f 0.04 1251 + 523’ 10.4 ?r 0.7 3.9 + 1.2 2.1 f 0.1 139.2 + 66.8 64.8 f 20.2 2.7 f I .9 514k87 514 f 126b 128 f 74.2” 2981 + 484’ 155.8 +_2.4 4.14 f 1.21 116.8 f 3.1 1.29 5 0.56 2.83 + 0.78
II.19 7.06 5.41 2.13 3.89 14.52 0.82 21.49 0.37 I .83 2.02 0.11 I .97 I .48 0.46 11.41 30.02 5.29 2.65 1.52 0.06 3.46 0.56
286.7 k 24.4’ 10.4 + 5.1s 12.8 f 4.5 244.6 + 19.0 81.4 f 20.4 4.1 * 0.3” 0.31 f 0.05 3694 + 1038” 10.1 f 1.3 2.9 + 1.0 2.0 + 0.2 151.9f21.4 42.3 + 19.6 3.9 + 1.3 394 * 200 201.0 f 73.4a 86.1 + 22.4’ 3669 f 1318ab 158.2 + 2.5 3.79 + 0.71 117.2k3.7 I .48 f 0.56 2.56 C 0.42
P
0.011 0.144 0.034
Multiple range tests were used to determined differences between species. In each parameter, means not marked by the same letter are significantly different (P c: 0.05).
Penguin blood chemistry means of the respective parameters from those of the population as a whole have not been considered. As far as we know, there is no study that deals with any functional parameter of these three penguin species, therefore no comparisons with previous data are possible. Nevertheless we can see that mean glucose values in penguins were lower than those found in raptors (Balash et af., 1976; Rehder et al., 1982; Ferrer et al., 1987), and essentially similar to those described in other bird groups (Gee et al., 1981). The mean concentration of this parameter in Pygoscelis Papua was lower than in the other two penguin species. The glucogenic mechanisms in this penguin are likely to be important, because of its feeding habits. Gentoo penguins feed inshore and are deep divers, and has both, average prey size and average body mass, greater than the other two penguin species (Trivelpiece et al., 1987). The mean concentration of urea in the blood of the chinstrap was significantly lower than those of the other two species (Table 2). These results indicate that Pygoscelis penguins, like other bird groups, have blood urea concentrations lower than those for blood uric acid (Gee et al., 1981; Puerta et al., 1989a). Nevertheless, in other groups of birds like raptors (Gee et al., 1981; Ferrer et al., 1987) or common cranes Grus grus (Puerta et al., 1990), higher concentrations for urea than for uric acid have been reported. Blood concentrations of cholesterol (Table 2) were not statistically different for the three assayed species, and similar to those described for other bird species (Gee et al., 1981; Ferrer et al., 1987; Puerta et al., 1989a). Plasma content of triglycerides was similar to those previously published for other bird species (Balash et af., 1976; Gee et al., 1981), although lower than those described for chicks of Ciconia ciconia and Ciconia nigra (Puerta et al., 1989b). The respective concentrations of calcium, phosphorus, magnesium, potassium, chlorine, T3 and thyroxine were statistically the same for the three penguin species (Table 2). We have not been able to find any ecological or physiological explanation for differences found in blood concentrations of LDH, amylase and cholinesterase (Table 2). Plasma concentration of total protein was greater in P. papua. According to Smith and Bush (1978), total protein estimation is a valuable test for evaluating the general nutritional state of a bird, a low total protein being indicative of malnutrition. Alkaline phosphatase concentration was greater in P. antarctica. This enzyme is involved in chondrogenics and osteoblastic activities and related with growth and secondary ossification of the osseous tissue (Vifiuela et al., 1991 and references therein). So, lower values in chinstraps could be indicative of a greater proportion of immature birds in the sample of this species.
473
Acknowledgements-Financial support was received from Consejo Superior de Investigaciones Cientificas. We gratefully appreciate the cooperation of F. Recio in blood analyses and the University of Chile for logistic support in Antarctica.
REFERENCES
Balasch J., Musquera S., Palacios L., Jimenez M. and Palomeque J. (1976) Comparative hematology of some falconiformes. Condor 78, 258-273. Cherel Y. and Le Maho Y. (1988) Changes in body mass and plasma metabolites during short-term fasting in the king penguin. Condor 90, 257-258. Cherel Y., Robin J. P., Walch O., Karmann H., Netchitailo P. and Le Maho Y. (1988) Fasting in king penguin: I. Hormonal and metabolic changes during breeding. Am. J. Physiol. 254, 170-177.
-
-
-
Ferrer M. (1990) Hematoloaical studies in birds. Condor 92. 1085-1086. ’ Ferrer M., Garcia-Rodriguez T., Carriho J. C. and Castroviejo J. (1987) Hematocrit and blood chemistry values in captive raptors. Comp. Biochem. Physiol. 87A, 1123-I 127. Garcia-Rodriguez T., Ferrer M., Recio F. and Castroviejo J. (1987) Circadian rhvthms of determined blood chemistry values in buzzards and eagle owls. Comp. Biochem. Physiol. @#A, 663469. Gee G. F., Carpenter J. W. and Hensler G. L. (1981) Species differences in hematological values of captive cranes, geese, raptors and quail. J. Wildl. Manage. 45, 4633483.
Gonzalez J. L. and Hiraldo F. (1991) Some hematological data from marsh harriers (Circus aeruginosus) in central Spain. Comp. Biochem. Physiol. lOBA, 735-737. Puerta M. L., Alonso J. C., Huecas V., Alonso J. A., Abelenda M. and Muiioz-Pulido R. (19901 \ , Hematoloav and blood chemistry of wintering common cranes. Condor 92, 21%214. Puerta M. L., Huecas V. and Garcia de1 Campo A. L. (1989a) Hematology and blood chemistry of the Chilean flamingo. Comp. Biochem. Physiol. 94A, 623-625. Puerta M. L., Muxioz-Pulido R., Huecas V. and Abelenda M. (1989b) Hematology and blood chemistry of chicks of white and black storks (Ciconia ciconia and Ciconia nigra). Comp. Biochem. Physiol. 94A, 201-204. Rehder N. B., Bird D. N., Lague P. C. and Mackay C. (1982) Variation in selected hematological parameters of captive red tailed hawk. J. Wildl. Dis. 18, 105-109. Robin J. P., Frain M., Sardet C., Groscolas R. and Le Maho Y. (1988) Protein and lipid utilization during long-term fasting in emperor penguins. Am. J. Physiol. 1_
254, 6168.
Smith E. E. and Bush M. (1978) Haematological parameters on various species of Strigiformes and Falconiformes. J. Wildl. Dis. 14, 447-450.
Trivelpiece W. Z., Trivelpiece S. G. and Volkman N. J. (1987) Ecological segregation of Ad&lie, gentoo, and chinstrap penguins at King George Island, Antarctica. Ecology 68, 351-361. Viiiuela J., Ferrer M. and Recio F. (1991) Age-related variations in plasmatic levels of alkaline phosphatase, calcium and inorganic phosphorus in chicks of two species of raptors. Comp. Biochem. Physiol. !@A, 49-54.