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Blood volume in domestic pigeons
BLOOD
VOLUME
IN DOMESTIC
PIGEONS
JES~~SPALOMEQUEand Jo& PLANAS Fisiologia Animal, Facultad de Biologia, Universidad de Barcelona, Barcelona-7, Spain (Received 23 May 1977)
Abstract-l. Blood volumes ranging from 16 to 21 ml blood/100 g body wt have been found in pigeons using the isotopic (59Fe) and the Blue Evans techniques. 2. A hematocrit higher than 50% and also a high hemoglobjn concentration (17.3g Hb%), gave an average of 3 g Hb,/lGQg body wt in pigeons, against 0.5g-Hb/l~g body wt in chickens. 3. The pigeon’s heart represented 1.36% of the body weight compared to only 0.75% in chickens of similar size. The breast was 26.5% and 11.60/,respectively. 4. It was observed that values in pigeons were even higher than in smaller-sized flying species.
INTRODUCl-iON
The data on blood volumes in domestic fowl is readily available (Balasch & Planas, 1971; Cohen, 1967; Hunsaker. 1968; MacCartney, 1952; Newell & Schaffner, 1950; Nirmalan & Robinson. 1972: Rodman er al., 1957; Sturkie, 1965) but it is scarcer for other species (Bond & Gilbert, 1958). In an earlier paper (Balasch et al., 1974) and in an unpublished paper on iron metabolism in pigeons, high hematological values in hemoglobin concentration (Hb), hematocrit (Hc) and erythrocyte numbers were observed, as has been reported by other authors for the same species (Bond & Gilbert, 1958; Kaplan, 1954; McGrath, 1970; Rodman et al., 1957). These observations have suggested to us that the pigeon, a species well adapted to flight with a vigorous pectoral red muscle, should have a high blood volume. However, the only data found was Bond & Gilbert (1958) and Rodman et al. (1957) which gave quantities of 9.2 and 6.1 ml blood/lOOg body wt, respectively, which do not differ greatly from other species, most of which are not good flyers (Sturkie, 1965). The special metabolism necessary for flying requires hematological and anatomical (mechanical, circulatory and respiratory) adaptations, which are possibly increased, in relatively small birds, through the inversion of the metabolism-size relationship (Schmidt-Nielsen, 1975). For this reason, in the present paper we have compared pigeons and chickens in hematological and anatomical aspects, in order to determine the actual blood volume in pigeons as related to flying habits. MATERIALS
AND METHODS
Urban domestic pigeons (Columba liuia), caught in Barcelona, and White Leghorns (Gal/us domesticus) of digerent
sizes and both sexes were used. The blood volumes were determined, by using the Blue Evans technique, according to Newell & Shaffner (1950). Blood samples were extracted immediately before and 3 min after the injection of the pigment dye (1 mg/kg body wt). The isotopic method was also used with 59Fe, which is an adaptation of the ferrokinetic technique of Bothwell & Finch (1962). Doses of 1_4$i/kg body wt were added 413
to homologous serum in amounts that did not exceed the binding capacity of the transferrin. Blood sampies (0. f-O.5 ml) were taken 5, 15,30 and 60 min after the Fe injection. Radioactivity was measured in plasma and the zero time of 59Fe concentration was calculated by extrapolation. The birds were weighed on a Ohaus balance and the organs on a Metler balance, which was accurate to 0.01 g. The hematocrit was determined in heparinized capillary tubes and spun for 6min in a clinical microhematocrit centrifuge. The hemoglobin concentration in 0.01 ml blood was measured by Drabkin’s reagent and standards obtained from Hycel. The erythrocyte number was determined by Thoma’s chamber. RESULTS
Several hematological and blood volume values, obtained in both species, are shown in Tables 1 and 2. Pigeons showed the highest relative ratios, ranging from 16.9 to 20 ml blood,/100 g body wt. Sex differences, and differences in methods of determination were not statistically significant. In chickens, however, the extreme values were 4.8 and 14.9%, and were significantly different from pigeons. The observed differences in chickens, with the two methods, could be attributed to the different body sizes of the birds. However, the comparison of small chickens with pigeons of similar size always showed a significant difference, the pigeons having a higher blood volume than chickens. The high hematocrit values of pigeon were double that in chickens, and this produced an increase in the differences between the relative erythrocyte volume in both species. In Table 3 the relative weights of assorted organs (heart, breast, spleen, liver) related to body weight are shown. It is evident that some values (heart and breast) were double in pigeons, but the liver was ap nroximatelv the same relative size. The snleen. was ihree times larger in young chi&ms (44Og) than in pigeons. DiSCUSSION
Assorted data on blood volumes in birds were collected (Table 4). Most species varied between 4 and
414
Jrsts Table
I. Blood
and erythrocyte
volumes
PALOM~QUCand
determined
Weight Species
Number
Pigeons Males
2.5
Females
22
Total (j and
47 r)
Chickms Young males
4
Young
males
3
Young
males
3
Total
10
Table
method
in prgeon
and
chickens
Hb (g/l00 ml)
Blood volume (m1/100 g body wt) _I____
Eryihrocyte volume (ml;100 g body wt) ._ ______-
49.9 +6/I 52.5 * 3.4 51.3 15.3
17.14 +3.14 17.35 10.72 17.22 k2.38
18.96 * 2.48 18.75 li: 2.56 18.93 + 2.52
9.7 * 2.0 9.X * I.6 9.15 * 1.80
370.5 + 28.4 -422.7 + 24.0 560.0 * 29.5 443.0
32.7 +2.5 29.7 -+2.3 29.0 22.6 30.7 k2.8
11.17 ri: 1.21 10.53 i_O.f4 10.41 to.82 10.73 +0.88
14.91 ^+ 1.10 12.48 + 1.36 Il.90 k2.55 13.28 +?.Oh
4.9 +O.b i.7 kO.5 3.5 * I .o 3. I 20.9
+ (r.
2. Blood
and erythrocyte
volumes
Weight Species
Number
Pigeons Males
9
Females
5
Ckicken Young males
7
Adult
males
7
Adult
hens
9
Laying
by Blue Evans
X3.0* +x3 369.9 f 18.7 280.8 F36.3
*x7.3 * Mean
HC (‘I”)
(g)
Josi PLANAS
hens
10
(g)
determined by a radioisotopic chickens Hc (“0)
323.9* * 34.4 266.0 * 32.9
49.1 f 3.0 41.6 16.1
854.6 + 106.3 1863.6 f 494. I 1528.3 f 388.9 2823.0 + 846.7
30.1 t3.7 28.7 +3.7 29.4 + 1.9 33.8 + 2.6
Hb (g/lOOml)
IS.6 * 2.2 14.7 k2.8 10.3 + 1.2
10 ml, blood/lOOg body wt. At the same time, the erythrocyte volume ranged between 1.7 and 4 ml erythrocyte/lOO g body wt (Cohen, 1967; Nirmaian & Robinson, 1972; Rodman et al., 1957). However, some species, such as the duck (Balasch & Planas, f971; Bond & Gilbert, 1958), coot and loon (Bond & Gilbert, 1958). as well as the pigeon, with blood volumes higher than 16.9 ml blood/lOOg body wt. differed from the general trend. Also our data on pigeons disagree with the values of 9.2 ml blood/100 g body wt of Bond & Gilbert (1958). and the erythrocyte volume of 3.5 ml% from Rodman er al. (1957). the former being the only data available for this value until now. The blood volume variations in the same species according to size, has been explained for chickens by Newell & Shaffner (1950) and with this data, we have taken the opportunity to check this inverse relationship. In quail, Nirmalan & Robinson (1972) showed that the blood volume decreased with age. On the other hand, in female birds during the laying period,
method
Blood volume (ml/IOOg body wt)
16.9 * 3.4 20.3 f 2.9 9.2 * 2.3 6.0 + 0.9 6.3 il.8 4.9 + 1.3
(“Fe)
in pigeon
and
Erythrocyte volume (mlj1OOg body wt)
X.26 *
I.14
8.40 + 1.51 2.80 + 0.90 1.63 +0.33 1.85 +0.54 I .64 + 0.49
the blood volume showed a tendency to decrease, in the different species studied (Balasch & Planas, 1971; Nirmalan & Robinson, 1972). but in general it is not statistically significant and easily attributable to the weight increase with age. The age variation of the hematocrit values is attributable to a hormonal effect. The stimulating action of androgens on the erythropoiesis and the decreasing effect of the estrogens is well-known. Kaplan (1954) showed this in pigeons, among other vertebrates, and other authors have observed it in chickens (Balasch & Planas, 1971; Gilbert. 1969). However. the pigeon hematocrit is higher than SO%, regardless of sex (Kaplan, 1954; Bond & Gilbert, 1958; Balasch & Planas, 1971) and it is one of the highest values in birds of similar size. In small passeriform birds from 10 to 30g body wt, the hematocrit values fluctuated between 50 and 60”/:, (Carey & Morton, 1976). As a consequence of the high hematocrit, the pigeon showed (Table 4) a high erythrocyte
415
Blood volume in domestic pigeons Table 3. Relationship between some organ weights to body weight in pigeon and young chicken of similar size Organ weight referred to IOOg body wt Species
Number
Weight (g)
Heart
Breast
Liver
Spleen
1.37 kO.17
2.41 +0.56 2.32 i: 0.54 2.36 k 0.42
0.09 + 0.08 0.08 + 0.05 0.08 +0.04
2.95 ,0.45 2.99 +0.21 3.06 +0.13 3.00 +0.29
0.33 kO.10 0.23 f 0.05 0.22 10.02 0.27 f 0.08
Pigeon
Males
25
Females
22 47
Total (2 and $f
288.0* k28.3 269.9 ,187 280.8 rt26.3
20.13 1.36 +0.10
26.5 +2.3 26.6 +2.0 26.5 F1.8
370.5 f 28.4 422.7 k 24.0 560.0 k29.5 443.0 + 87.3
0.88 kO.14 0.7 1 +0.11 0.61 f 0.08 0.75 kO.16
12.2 +1.3 11.2 +1.0 11.4 to.9 11.6 +1.1
1.36
Chicken
Young males
4
Young males
3
Young males
3 IO
Total * Mean f o.
Table 4. Comparative data on blood and erythrocyte volumes in avian species
Species
Method of determination
Blood volume (ml/l00 g)
Erythrocyte volume (ml/l@ g)
Blue Evans Blue Evans 5’Cr “Fe “Fe Blue Evans-59Fe 59Fe
9.2-10.5 6.3 5.4 4.9-6.2 3.9 6.s14.9 4.9
1.9 2.1 1.5-1.8 1.3 1.6-4.9 1.6
Newell & Shaffner (1950) Bond & Gilbert (1958) Rodman et al. (1957) Balasch & Planas (1971) Balasch & Planas (1971) Present study Present study
Blue Evans 59Fe “Fe
7.2 3.4-5.9 4.2
2.5 1.5-2. I 1.5
McCartney (1952) Balasch & Planas (1971) Balasch & Planas (1971)
8.3 6.8-7.4 7.1
2.4 2.5-2.7 2.4
Nirmalan & Robinson (1972) Nirmalan & Robinson (1972) Nirmalan & Robinson (1972)
References
Chicken
Males Male Male and female Laying females Male and female Laying female Turkey
Female Male and femafe Laying female Quail
Young males Male and female Laying females
“Cr “Cr “Cr
Pheasant
Blue Evans
6.7
2.2
Bond & Gilbert (1958)
Pigeon
Blue Evans $‘Cr Blue Evans “Fe
9.2 6.5-7.1 18.7-19.0 16.9-20.3
4.9 3.2-3.5 9.7-9.8 8.3-8.4
Bond & Gilbert (1958) Rodman et al. (1957) Present study Present study
Female Male and female Laying female
Blue Evans S’Cr “Fe 5”Fe
11.1-11.3 9.1 8&l 5.0 8.0
4.1-4.8 3.6 468.4 3.5
Bond & Gilbert (1958) Cohen (1967) Balasch & Planas (1971) Balasch & Planas (1971)
Goose Male and female
Blue Evans “Cr
6.8 5.8-6.7
2.6 2.4-2.6
Bond & Gilbert (1958) Hunsaker (1968)
Hawk
Blue Evans
6.2
2.7
Bond & Gilbert (1958)
Loot
Blue Evans
9.5
4.4
Bond & Gilbert (1958)
Loon
Blue Evans
13.2
7.1
Bond & Gilbert (1958)
Owl
Blue Evans
6.4
2.0
Bond SKGilbert (1958)
Adult Male and female Male and female Duck
416
JESTS PALOMH&‘~: and
volume. that was practically double that of other species. The hemoglobin concentration was also high (17.3 Hb”/,) and was similar to the values found earlier in our lab with specimens of the same origin (Balasch (‘f ul., 1974) or to data in other literature (Bond & Gilbert, 1958: Rodman or c(i.. 1957). Moreover. these values fit in well with the range variation observed by Carey & Morton (1976) in small wild passeriforms. The high hematocrit and hemoglobin concentrations in moderate sized birds such as the pigeon, were more differentiated when we calculated the amount of hemoglobin for unit of body weight. An average of 3 g Hb/lOOg body wt. against 0.5 g Hbjlmg body wt in chickens, was found. which represented a difference of six times. In several mammals, a mean of 0.9 g Hb/lOOg body wt is similar to chickens. In birds, the presence of high values of blood and erythrocyte volumes, hematocrit and hemoglobin. is usually observed in aquatic species. as a diving adaptation (Balasch et al.. 1974; Bond & Gilbert. 1958) and on account of flying activity and toleration of high altitudes (Balasch et nl.. 1974; Carey & Morton. 1976; Carpenter. 1975). The sharp differences in the hematological parameters observed between chickens and pigeons, are attributable to the flying activity. Keeping this idea in mind we also analysed some of the anatomic aspects that are related to this phenomenon, such as the size of heart and breast. The comparison of these organs was clearly significant between the two species. as values in pigeons were greater. In pigeons the heart represented I .36Oa of body wt, and in chickens of a similar size, about 4OOg. it was 0.75%; for the breast, the average values were 26.5 and I1.6g/lOOg body wt respectively (Table 3). Carey & Morton (1976) have found relative heart weights between I and 1.6Y, in smaller sized birds. with the exception of humming birds (3.-4 g whole body wt) where the heart was 2-3 g/l00 g body wt. The calculated ratio of heart wtjbody wt. determined by Berger & Hart (1974) and applied to our data, gave comparative results, but at lower levels. However. the equation of Burton rr al. (1969) obtained in chickens, gave much lower values than ones obtained by us. There were no differences between the relative weight of the liver in both species. but the spleen was greater in chickens when compared to pigeons of similar weight. In wild birds. from high mountain areas, an 1IY, increase in the heart weight and a 37”;, rise in the hematocrit has been observed. compared to similar sized birds living at low altitudes (Carey & Morton. 1976). It seems that the high hematological values (hemoglobin concentration, hematocrit and erythrocyte number) and some anatomical aspects such as the heart weight. represent an adaptation to the continuous exposure to hypoxia and a response to a greater oxygen demand for thermogenesis against the cold. as has been demonstrated in the extensive paper by Carey & Morton (1976). However. Carpenter (1975) in the comparison on two species from the Peruvian Andes, at 4100m altitude, suggested that the main difference in the hematocrit could be attributed to flying habits more than to the altitude.
Jest’ PLANAS
Chickens. bred for several generations ;it a placc~ with an altitude of 38iOm. produced an increase oi 27% in the hematocrit. 36?,, in the hcmogiobin and 33”” in the erythrocyte count. compared to the values of specimens of the same race but bred at sea level (Burton c’t a/., 197 1). An experimental hypoxia in chickens caused a similar response with an increase of the heart mass and also an increased tolerance to the low oxygen concentrations (Burton rt ul.. 1969). An androgen administration. which increased the erythrocyte formation. facilitated the adaptation mechanism against the hypoxia which normally led to a polycythemia and heart hypertrophy. Likewise, in pigeons. experiments at a simulated altitude of 6700 m. during 30 days, produced a rise in the hematocrit and in the right ventricular mass of the heart (McGrath. 1970). The normal behavior and flying ability of the house sparrow in an atmosphere equivalent to 6100m altitude. compared to the collapse and quick death of the mouse. have been explained by Tucker (1968). as heart hypertrophy. The bird under these conditions showed no change in the oxygen afinity of the hemoglobin. For this. a heart output which was 3 times higher than in the mouse. caused an enlargement of 2.7 times the relative size of this organ. We must consider that both the heart hypertrophy and the polycythemia are the main adaptative mechanims for hypoxia in birds. as has been observed in nature and in experimental work (Burton ~‘t ul.. 1969; Carey & Morton. 1976; McGrath, 1970). The special anatomical patterns and effectiveness of the avian lung. with its unidirectional air flow. which is general in the whole group (Schmidt-Nielsen. 1975). must also be considered. On the other hand, the pigeon blood showed an oxygen dissociation curve similar in shape and position (P5,, = 29.4 mm Hg) to those of mammals (Lutz Yf al.. 1973). The pigeon shows these characteristics as permanent and specific adaptations. probably because of the great oxygen demand as a powerful flying bird. and for this reason comparatively high hematological and anatomical (heart, breast) values, higher than other species. were shown REFERENCES
BALASCHJ. & PLAN.U J. (1971) Hematological values in ooultrv. Rro. PSD. Fisiol. 27. 191-194. BALASCYI~ J.. PAL&EQUF: J.. PALACIOS L.. MU~QUERA S. & JIMENEZ J. (1974) Nematological values of some great flying and aquatic diving birds. Camp. Biochem. Physiol.
49A. 137.-145. BERGF.R M. &
HART J. S. (1974) Physiology and energetics of flight. In Asian Biology (Edited by FARNFR D. S. & KING J. R.), Vol. 4. pp. 415477. Academic Press. New York. BOND C. F. & GILBERT P. W. (1958) Comparative study of blood volume in representative aquatic and nonaqua-
tic birds. Am. J. Physiol. 194. 519.-521. BOTHWELLT. H. & FINCH C. A. (1962) Iron Metabolism.
Little-Brown,
Boston.
BURTON R. R.. SMITH A. H., CARLISLE J. C. & SLUKA S. J. (1969) Role of hematocrit, heart mass, and high-altitude exposure in acute hypoxia tolerance. J. appl. Physioi. 27, 49-52.
Blood volume in domestic pigeons BURTONR. R.. SAHARAR. & SMITHA. H. (1971) The hematology of domestic fowl native to high altitude. Enuiron. Physiol. 1. 155-163. CAREYC. & MORTONM. L. (1976) Aspects of circulatory physiology of mountain and lowland birds. Camp. 5i& them. Phvsiol. 54A. 61-74. CARPENTER’F.L. (1975) Bird hematocrits: effects of high altitude and strength of flight. Camp. Biochem. Physiol. ?!@A,415417. COHEN R. R. (1967) Total circulating erythrocyte and plasma volumes of ducks measured simultaneously with “Cr. Poutt. Sci. 46, 153991544. GILBERTA. B. (1969) The erythrocyte segmentation rate and packed cell volume in the domestic fowl with respect to age and sex. Br. Poult. Sci. 10, 109-l 13. HUN~AKERW. G. (1968) Blood volume of geese treated with androgen and estrogen. Poult. Sci. 47, 371-376. KAPLANH. M. (1954) Sex differences in the packed cell volume of vertebrate blood. Science E,?ft, 1044. LUTZ P. L., LONGMUIRI. S., TUTTLEJ. V. & SCHMIDTNIELSENK. (1973) Dissociation curve of bird blood and effect of red cell oxygen consumption. Rap. Physiol. 17. 269-275.
417
MCCARTNEYM. G. (1952) Total blood and corpuscular volume in turkey hens. Poult. Sci. 31, 184-185. MCGRATH J. J. (1970) Effect of chronic hypoxia on hematocrit ratios and heart size in the pigeon. Lifp Sci. 9, 451455. NEWELLG. W. & SHAFFNERC. S. (1950) Blood volume determination in chickens. Pot&. Sci. 29, 78-87. NIRMALAN G. P. & ROBINSONG. A. (1972) Effect of ane. sex, and egg laying on the total erythrocyte volume (“CrO, label) and the plasma volume (“‘I-serum albumin label) of Japanese quail. Can. f. Pension. Pharmac. 50, 610. RODKAN G. P., EBAUGH F.
G. & SPIVEY-FOXM. R. (1957) The life span of the red blood cell and the red blood cell voiume in the chicken, pigeon and duck as estimated by the use of NaZ5’CrO+ Blood 12. 355-366. SCHMIDT-NIELSMK. (1975) Animal Physiology. Cambridge University Press, London. STURKIEP. D. (1965) Avian Physiology. 2nd edn. Cornell University Press, Ithaca, New York. TUCKERV. A. (1968) Respiratory physiology of house sparrows in relation to high-altitude flight. J. exp. Biol. 48, 55566.
VOLUME
IN DOMESTIC
PIGEONS
JES~~SPALOMEQUEand Jo& PLANAS Fisiologia Animal, Facultad de Biologia, Universidad de Barcelona, Barcelona-7, Spain (Received 23 May 1977)
Abstract-l. Blood volumes ranging from 16 to 21 ml blood/100 g body wt have been found in pigeons using the isotopic (59Fe) and the Blue Evans techniques. 2. A hematocrit higher than 50% and also a high hemoglobjn concentration (17.3g Hb%), gave an average of 3 g Hb,/lGQg body wt in pigeons, against 0.5g-Hb/l~g body wt in chickens. 3. The pigeon’s heart represented 1.36% of the body weight compared to only 0.75% in chickens of similar size. The breast was 26.5% and 11.60/,respectively. 4. It was observed that values in pigeons were even higher than in smaller-sized flying species.
INTRODUCl-iON
The data on blood volumes in domestic fowl is readily available (Balasch & Planas, 1971; Cohen, 1967; Hunsaker. 1968; MacCartney, 1952; Newell & Schaffner, 1950; Nirmalan & Robinson. 1972: Rodman er al., 1957; Sturkie, 1965) but it is scarcer for other species (Bond & Gilbert, 1958). In an earlier paper (Balasch et al., 1974) and in an unpublished paper on iron metabolism in pigeons, high hematological values in hemoglobin concentration (Hb), hematocrit (Hc) and erythrocyte numbers were observed, as has been reported by other authors for the same species (Bond & Gilbert, 1958; Kaplan, 1954; McGrath, 1970; Rodman et al., 1957). These observations have suggested to us that the pigeon, a species well adapted to flight with a vigorous pectoral red muscle, should have a high blood volume. However, the only data found was Bond & Gilbert (1958) and Rodman et al. (1957) which gave quantities of 9.2 and 6.1 ml blood/lOOg body wt, respectively, which do not differ greatly from other species, most of which are not good flyers (Sturkie, 1965). The special metabolism necessary for flying requires hematological and anatomical (mechanical, circulatory and respiratory) adaptations, which are possibly increased, in relatively small birds, through the inversion of the metabolism-size relationship (Schmidt-Nielsen, 1975). For this reason, in the present paper we have compared pigeons and chickens in hematological and anatomical aspects, in order to determine the actual blood volume in pigeons as related to flying habits. MATERIALS
AND METHODS
Urban domestic pigeons (Columba liuia), caught in Barcelona, and White Leghorns (Gal/us domesticus) of digerent
sizes and both sexes were used. The blood volumes were determined, by using the Blue Evans technique, according to Newell & Shaffner (1950). Blood samples were extracted immediately before and 3 min after the injection of the pigment dye (1 mg/kg body wt). The isotopic method was also used with 59Fe, which is an adaptation of the ferrokinetic technique of Bothwell & Finch (1962). Doses of 1_4$i/kg body wt were added 413
to homologous serum in amounts that did not exceed the binding capacity of the transferrin. Blood sampies (0. f-O.5 ml) were taken 5, 15,30 and 60 min after the Fe injection. Radioactivity was measured in plasma and the zero time of 59Fe concentration was calculated by extrapolation. The birds were weighed on a Ohaus balance and the organs on a Metler balance, which was accurate to 0.01 g. The hematocrit was determined in heparinized capillary tubes and spun for 6min in a clinical microhematocrit centrifuge. The hemoglobin concentration in 0.01 ml blood was measured by Drabkin’s reagent and standards obtained from Hycel. The erythrocyte number was determined by Thoma’s chamber. RESULTS
Several hematological and blood volume values, obtained in both species, are shown in Tables 1 and 2. Pigeons showed the highest relative ratios, ranging from 16.9 to 20 ml blood,/100 g body wt. Sex differences, and differences in methods of determination were not statistically significant. In chickens, however, the extreme values were 4.8 and 14.9%, and were significantly different from pigeons. The observed differences in chickens, with the two methods, could be attributed to the different body sizes of the birds. However, the comparison of small chickens with pigeons of similar size always showed a significant difference, the pigeons having a higher blood volume than chickens. The high hematocrit values of pigeon were double that in chickens, and this produced an increase in the differences between the relative erythrocyte volume in both species. In Table 3 the relative weights of assorted organs (heart, breast, spleen, liver) related to body weight are shown. It is evident that some values (heart and breast) were double in pigeons, but the liver was ap nroximatelv the same relative size. The snleen. was ihree times larger in young chi&ms (44Og) than in pigeons. DiSCUSSION
Assorted data on blood volumes in birds were collected (Table 4). Most species varied between 4 and
414
Jrsts Table
I. Blood
and erythrocyte
volumes
PALOM~QUCand
determined
Weight Species
Number
Pigeons Males
2.5
Females
22
Total (j and
47 r)
Chickms Young males
4
Young
males
3
Young
males
3
Total
10
Table
method
in prgeon
and
chickens
Hb (g/l00 ml)
Blood volume (m1/100 g body wt) _I____
Eryihrocyte volume (ml;100 g body wt) ._ ______-
49.9 +6/I 52.5 * 3.4 51.3 15.3
17.14 +3.14 17.35 10.72 17.22 k2.38
18.96 * 2.48 18.75 li: 2.56 18.93 + 2.52
9.7 * 2.0 9.X * I.6 9.15 * 1.80
370.5 + 28.4 -422.7 + 24.0 560.0 * 29.5 443.0
32.7 +2.5 29.7 -+2.3 29.0 22.6 30.7 k2.8
11.17 ri: 1.21 10.53 i_O.f4 10.41 to.82 10.73 +0.88
14.91 ^+ 1.10 12.48 + 1.36 Il.90 k2.55 13.28 +?.Oh
4.9 +O.b i.7 kO.5 3.5 * I .o 3. I 20.9
+ (r.
2. Blood
and erythrocyte
volumes
Weight Species
Number
Pigeons Males
9
Females
5
Ckicken Young males
7
Adult
males
7
Adult
hens
9
Laying
by Blue Evans
X3.0* +x3 369.9 f 18.7 280.8 F36.3
*x7.3 * Mean
HC (‘I”)
(g)
Josi PLANAS
hens
10
(g)
determined by a radioisotopic chickens Hc (“0)
323.9* * 34.4 266.0 * 32.9
49.1 f 3.0 41.6 16.1
854.6 + 106.3 1863.6 f 494. I 1528.3 f 388.9 2823.0 + 846.7
30.1 t3.7 28.7 +3.7 29.4 + 1.9 33.8 + 2.6
Hb (g/lOOml)
IS.6 * 2.2 14.7 k2.8 10.3 + 1.2
10 ml, blood/lOOg body wt. At the same time, the erythrocyte volume ranged between 1.7 and 4 ml erythrocyte/lOO g body wt (Cohen, 1967; Nirmaian & Robinson, 1972; Rodman et al., 1957). However, some species, such as the duck (Balasch & Planas, f971; Bond & Gilbert, 1958), coot and loon (Bond & Gilbert, 1958). as well as the pigeon, with blood volumes higher than 16.9 ml blood/lOOg body wt. differed from the general trend. Also our data on pigeons disagree with the values of 9.2 ml blood/100 g body wt of Bond & Gilbert (1958). and the erythrocyte volume of 3.5 ml% from Rodman er al. (1957). the former being the only data available for this value until now. The blood volume variations in the same species according to size, has been explained for chickens by Newell & Shaffner (1950) and with this data, we have taken the opportunity to check this inverse relationship. In quail, Nirmalan & Robinson (1972) showed that the blood volume decreased with age. On the other hand, in female birds during the laying period,
method
Blood volume (ml/IOOg body wt)
16.9 * 3.4 20.3 f 2.9 9.2 * 2.3 6.0 + 0.9 6.3 il.8 4.9 + 1.3
(“Fe)
in pigeon
and
Erythrocyte volume (mlj1OOg body wt)
X.26 *
I.14
8.40 + 1.51 2.80 + 0.90 1.63 +0.33 1.85 +0.54 I .64 + 0.49
the blood volume showed a tendency to decrease, in the different species studied (Balasch & Planas, 1971; Nirmalan & Robinson, 1972). but in general it is not statistically significant and easily attributable to the weight increase with age. The age variation of the hematocrit values is attributable to a hormonal effect. The stimulating action of androgens on the erythropoiesis and the decreasing effect of the estrogens is well-known. Kaplan (1954) showed this in pigeons, among other vertebrates, and other authors have observed it in chickens (Balasch & Planas, 1971; Gilbert. 1969). However. the pigeon hematocrit is higher than SO%, regardless of sex (Kaplan, 1954; Bond & Gilbert, 1958; Balasch & Planas, 1971) and it is one of the highest values in birds of similar size. In small passeriform birds from 10 to 30g body wt, the hematocrit values fluctuated between 50 and 60”/:, (Carey & Morton, 1976). As a consequence of the high hematocrit, the pigeon showed (Table 4) a high erythrocyte
415
Blood volume in domestic pigeons Table 3. Relationship between some organ weights to body weight in pigeon and young chicken of similar size Organ weight referred to IOOg body wt Species
Number
Weight (g)
Heart
Breast
Liver
Spleen
1.37 kO.17
2.41 +0.56 2.32 i: 0.54 2.36 k 0.42
0.09 + 0.08 0.08 + 0.05 0.08 +0.04
2.95 ,0.45 2.99 +0.21 3.06 +0.13 3.00 +0.29
0.33 kO.10 0.23 f 0.05 0.22 10.02 0.27 f 0.08
Pigeon
Males
25
Females
22 47
Total (2 and $f
288.0* k28.3 269.9 ,187 280.8 rt26.3
20.13 1.36 +0.10
26.5 +2.3 26.6 +2.0 26.5 F1.8
370.5 f 28.4 422.7 k 24.0 560.0 k29.5 443.0 + 87.3
0.88 kO.14 0.7 1 +0.11 0.61 f 0.08 0.75 kO.16
12.2 +1.3 11.2 +1.0 11.4 to.9 11.6 +1.1
1.36
Chicken
Young males
4
Young males
3
Young males
3 IO
Total * Mean f o.
Table 4. Comparative data on blood and erythrocyte volumes in avian species
Species
Method of determination
Blood volume (ml/l00 g)
Erythrocyte volume (ml/l@ g)
Blue Evans Blue Evans 5’Cr “Fe “Fe Blue Evans-59Fe 59Fe
9.2-10.5 6.3 5.4 4.9-6.2 3.9 6.s14.9 4.9
1.9 2.1 1.5-1.8 1.3 1.6-4.9 1.6
Newell & Shaffner (1950) Bond & Gilbert (1958) Rodman et al. (1957) Balasch & Planas (1971) Balasch & Planas (1971) Present study Present study
Blue Evans 59Fe “Fe
7.2 3.4-5.9 4.2
2.5 1.5-2. I 1.5
McCartney (1952) Balasch & Planas (1971) Balasch & Planas (1971)
8.3 6.8-7.4 7.1
2.4 2.5-2.7 2.4
Nirmalan & Robinson (1972) Nirmalan & Robinson (1972) Nirmalan & Robinson (1972)
References
Chicken
Males Male Male and female Laying females Male and female Laying female Turkey
Female Male and femafe Laying female Quail
Young males Male and female Laying females
“Cr “Cr “Cr
Pheasant
Blue Evans
6.7
2.2
Bond & Gilbert (1958)
Pigeon
Blue Evans $‘Cr Blue Evans “Fe
9.2 6.5-7.1 18.7-19.0 16.9-20.3
4.9 3.2-3.5 9.7-9.8 8.3-8.4
Bond & Gilbert (1958) Rodman et al. (1957) Present study Present study
Female Male and female Laying female
Blue Evans S’Cr “Fe 5”Fe
11.1-11.3 9.1 8&l 5.0 8.0
4.1-4.8 3.6 468.4 3.5
Bond & Gilbert (1958) Cohen (1967) Balasch & Planas (1971) Balasch & Planas (1971)
Goose Male and female
Blue Evans “Cr
6.8 5.8-6.7
2.6 2.4-2.6
Bond & Gilbert (1958) Hunsaker (1968)
Hawk
Blue Evans
6.2
2.7
Bond & Gilbert (1958)
Loot
Blue Evans
9.5
4.4
Bond & Gilbert (1958)
Loon
Blue Evans
13.2
7.1
Bond & Gilbert (1958)
Owl
Blue Evans
6.4
2.0
Bond SKGilbert (1958)
Adult Male and female Male and female Duck
416
JESTS PALOMH&‘~: and
volume. that was practically double that of other species. The hemoglobin concentration was also high (17.3 Hb”/,) and was similar to the values found earlier in our lab with specimens of the same origin (Balasch (‘f ul., 1974) or to data in other literature (Bond & Gilbert, 1958: Rodman or c(i.. 1957). Moreover. these values fit in well with the range variation observed by Carey & Morton (1976) in small wild passeriforms. The high hematocrit and hemoglobin concentrations in moderate sized birds such as the pigeon, were more differentiated when we calculated the amount of hemoglobin for unit of body weight. An average of 3 g Hb/lOOg body wt. against 0.5 g Hbjlmg body wt in chickens, was found. which represented a difference of six times. In several mammals, a mean of 0.9 g Hb/lOOg body wt is similar to chickens. In birds, the presence of high values of blood and erythrocyte volumes, hematocrit and hemoglobin. is usually observed in aquatic species. as a diving adaptation (Balasch et al.. 1974; Bond & Gilbert. 1958) and on account of flying activity and toleration of high altitudes (Balasch et nl.. 1974; Carey & Morton. 1976; Carpenter. 1975). The sharp differences in the hematological parameters observed between chickens and pigeons, are attributable to the flying activity. Keeping this idea in mind we also analysed some of the anatomic aspects that are related to this phenomenon, such as the size of heart and breast. The comparison of these organs was clearly significant between the two species. as values in pigeons were greater. In pigeons the heart represented I .36Oa of body wt, and in chickens of a similar size, about 4OOg. it was 0.75%; for the breast, the average values were 26.5 and I1.6g/lOOg body wt respectively (Table 3). Carey & Morton (1976) have found relative heart weights between I and 1.6Y, in smaller sized birds. with the exception of humming birds (3.-4 g whole body wt) where the heart was 2-3 g/l00 g body wt. The calculated ratio of heart wtjbody wt. determined by Berger & Hart (1974) and applied to our data, gave comparative results, but at lower levels. However. the equation of Burton rr al. (1969) obtained in chickens, gave much lower values than ones obtained by us. There were no differences between the relative weight of the liver in both species. but the spleen was greater in chickens when compared to pigeons of similar weight. In wild birds. from high mountain areas, an 1IY, increase in the heart weight and a 37”;, rise in the hematocrit has been observed. compared to similar sized birds living at low altitudes (Carey & Morton. 1976). It seems that the high hematological values (hemoglobin concentration, hematocrit and erythrocyte number) and some anatomical aspects such as the heart weight. represent an adaptation to the continuous exposure to hypoxia and a response to a greater oxygen demand for thermogenesis against the cold. as has been demonstrated in the extensive paper by Carey & Morton (1976). However. Carpenter (1975) in the comparison on two species from the Peruvian Andes, at 4100m altitude, suggested that the main difference in the hematocrit could be attributed to flying habits more than to the altitude.
Jest’ PLANAS
Chickens. bred for several generations ;it a placc~ with an altitude of 38iOm. produced an increase oi 27% in the hematocrit. 36?,, in the hcmogiobin and 33”” in the erythrocyte count. compared to the values of specimens of the same race but bred at sea level (Burton c’t a/., 197 1). An experimental hypoxia in chickens caused a similar response with an increase of the heart mass and also an increased tolerance to the low oxygen concentrations (Burton rt ul.. 1969). An androgen administration. which increased the erythrocyte formation. facilitated the adaptation mechanism against the hypoxia which normally led to a polycythemia and heart hypertrophy. Likewise, in pigeons. experiments at a simulated altitude of 6700 m. during 30 days, produced a rise in the hematocrit and in the right ventricular mass of the heart (McGrath. 1970). The normal behavior and flying ability of the house sparrow in an atmosphere equivalent to 6100m altitude. compared to the collapse and quick death of the mouse. have been explained by Tucker (1968). as heart hypertrophy. The bird under these conditions showed no change in the oxygen afinity of the hemoglobin. For this. a heart output which was 3 times higher than in the mouse. caused an enlargement of 2.7 times the relative size of this organ. We must consider that both the heart hypertrophy and the polycythemia are the main adaptative mechanims for hypoxia in birds. as has been observed in nature and in experimental work (Burton ~‘t ul.. 1969; Carey & Morton. 1976; McGrath, 1970). The special anatomical patterns and effectiveness of the avian lung. with its unidirectional air flow. which is general in the whole group (Schmidt-Nielsen. 1975). must also be considered. On the other hand, the pigeon blood showed an oxygen dissociation curve similar in shape and position (P5,, = 29.4 mm Hg) to those of mammals (Lutz Yf al.. 1973). The pigeon shows these characteristics as permanent and specific adaptations. probably because of the great oxygen demand as a powerful flying bird. and for this reason comparatively high hematological and anatomical (heart, breast) values, higher than other species. were shown REFERENCES
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G. & SPIVEY-FOXM. R. (1957) The life span of the red blood cell and the red blood cell voiume in the chicken, pigeon and duck as estimated by the use of NaZ5’CrO+ Blood 12. 355-366. SCHMIDT-NIELSMK. (1975) Animal Physiology. Cambridge University Press, London. STURKIEP. D. (1965) Avian Physiology. 2nd edn. Cornell University Press, Ithaca, New York. TUCKERV. A. (1968) Respiratory physiology of house sparrows in relation to high-altitude flight. J. exp. Biol. 48, 55566.