Introduction

Both the overall packed cell volume/hematocrit (PCV/HCT) and the blood concentration of hemoglobin are reported to be identical between class Mammalia and Aves (Hawley et al., 1991). This suggests a tight level of control for these hematological parameters. However, what is not known is whether there are differences for hematological parameters for taxa within classes Mammalia and Aves. This is examined in the present study with data from a large sample size of species (357 mammalian and 323 avian species). Moreover, data from livestock, poultry and companion animals is excluded from the analyses as domestication/selective breeding may have had effects on these parameters.

In addition, negative allometric relationships for both PCV/HCT and blood concentrations of hemoglobin have been previously reported for mammals [1] and for birds [2]. This is consistent with a relationship between basal metabolic rate being proportional to the body weight to the power two thirds (reviewed: [3]). Metabolic rate, and hence a physiological parameter such as erythrocyte size, scales with body weight follow either a 2/3 or ¾ power relationship (discussed e.g. [4-6]). Erythrocyte size has been used as a proxy for somatic cell size [7] and it correlates well with the cell size of other tissues in passerine birds together with amphibians; calculated both with and without phylogenic correction [8]. In contrast, erythrocyte volume does not correlate well with the cell size of other tissues either uniformly with different tissues or to the same extent (accounting for less than 80% of the variance) in mammals [8].

What is not clear is whether the relationships between hematological parameters and log10 body weight are real reflecting an allometric relationship and the reduced needs for energy in larger animals or represents an artifact of species included in the analysis and the inclusion of domesticated animals in the analyses. The present study re-examines the relationship between hematological parameters and body weight in mammals and birds employing a large sample size of species (357 mammalian and 323 avian species) but with domestic animals excluded from the analyses.

Materials and Methods

Databases

A series of databases were assembled for hematological parameters using the published or calculated mean for the species based on rigorous and systematic series of searches of the literature. The databases for hematological parameters are shown for the following: mammals (Supplementary Table A) and birds [9]. For birds, information on body weights was from [10] while for mammals, these were was predominantly from Animal Diversity Web.

Analyses

Data were analyzed by taxonomic groups based on the following for birds [11-14] and for mammals [15,16]. However, for the latter, it should be noted that recent studies support the grouping Laurasiathera but do not support the Euarchontoglires encompassing the Glires (rodents/lagomorphs) and Euarchonta (including primates and tree shrews)[17]. Moreover, while the Cetacea (marine mammals such a whales and dolphins) are generally viewed as a branch of the Artiodactylans [14,18], the Artiodactyla and Cetacea will be considered separately in the present study due to ecological, size and other differences.

Statistics

Data were analyzed by taxa using one-way analysis of variance, with mean separated by Tukey’s range test or, when comparisons are limited to between two taxa, by Student’s t test. The relationship between hematological parameters and log10 body weights were compared by linear regression for mammals and birds.

Results

Table 1 compares hematological parameters in mammals and birds across multiple species. There were no differences between either the mean packed cell volume (PCV)/hematocrit (HCT) or hemoglobin concentrations between mammals and birds. Similarly, there were no differences PCV/HCT or hemoglobin concentrations between marsupial and placental mammals (Table 2).

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Table 1:

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Table 1. Comparison between hematological parameters between mammals and birds [Mean ± (number of species n=) S.E.M.].

Table 2 summarizes hematological parameters in mammalian taxa (where there were sufficient number of species for adequate analyses. There were marked differences between mammals and birds in erythrocyte concentration and mean erythrocyte cell or corpuscular volume (MCV). The concentration of erythrocytes was 60.2% lower in birds (p<0.001) than mammals (Table 1). In contrast, erythrocytes are much, 57.6%, smaller (p<0.001) in mammals than birds (Table 1) with a concomitant, 56.1 %, reduction (p<0.001) in hemoglobin content. Comparing placental to marsupial mammals, there was a small (18.1 %) elevation (p<0.001) in the erythrocyte concentration in the former (Table 3).

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Table 2:

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Table 2. Comparison between hematological parameters between major mammalian taxa [Mean ± (number of species n=) S.E.M.].

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Table 3:

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Table 3. Comparison between hematological parameters between marine/diving with related taxa in mammals and birds [Mean ± (number of species n=) S.E.M.].

Within placental mammals, PCV/HCT are similar in the taxa:Laurasiatheria, Primates and Glires but are 21.0 % higher than those in the Afrotheria and Xenarthra (Table 2). Moreover, the blood concentration of hemoglobin are similar in the taxa: Laurasiatheria, Primates, Glires and Xenarthra but 24.6 % lower than in the Afrotheria (Table 3). There were fewer (55.1%) (p<0.001) and larger erythrocytes (71.4%)(p<0.001) in the taxa: Afrotheria and Xenarthra than in Laurasiatheria, Primates and Glires (Table 3). Within the Laurasiatheria, PCV/HCT was highest in the Order Chiroptera and lowest in the Order Perissodactyla (Table 2). Moreover, PCV/HCT were higher the marine taxa – Cetacea and Pinnipedia than respectively the Artiodactylia and the Carnivora excluding marine taxa. The only differences in the blood hemoglobin concentration within Laurasiatherian taxa were the higher concentrations in the marine taxa – Cetacea and Pinnipedia than respectively the Artiodactylia and the Carnivora.

There were marked differences between mammalian taxa in erythrocyte number per unit blood volume and MCV (Table 2). Some of these such as the differences in MCV between Afrotheria plus Xenarthra and Glires plus Primates plus Laurasiatheria might be explicable by differences in body weight. However, if log10 body weight were critically, the lack of differences between MCV between Glires and Laurasiatheria would be surprising given large difference in log10 body weight [Glires - 2.49 ± S.E.M. 0.22 and Laurasiatheria 4.84 ± 0.065]. Moreover, the MCV was markedly higher (p<0.001) in the marine taxa – Cetacea and Pinnipedia than the Artiodactylia and the Carnivora by respectively 2.56 and 2.28 fold (Table 2). In view of the taxa differences in both PCV/HCT and hemoglobin concentrations, the mean corpuscular hemoglobin concentration (MCHC) was calculated. There were few differences in the MCHC between mammalian taxa except that the MCHC were lower (p < 0.01) in Primates [32.8 ± (16) 0.3 g dL-1] and Glires [31.6 ± (40) 0.6 g dL-1] than in Laurasiatheria [34.6 ± (176) 0.3 g dL-1] and higher (p < 0.001) Pinnipedia [38.5 ± (12) 1.54 g dL-1] than in non-marine Carnivora [33.3 ± (52) 0.3 g dL-1].

In contrast, the absence of differences in PCV/HCT and blood hemoglobin concentrations between mammals and birds, there were differences in PCV/HCT but not in blood hemoglobin concentrations in avian taxa (shown in Table 3). PCV/HCT was higher in the Order Anseriformes than in Order Galliformes (p<0.05), in the Order Charadriiformes together with “Landbird assemblage” than in the Gaviformes/Guiformes Waterbird radiation (p<0.05) and in the Australaves than in Afroaves (p<0.001). There were also marked differences in erythrocyte number, volume and size with, for instance, higher MCV and erythrocyte area in Gaviformes/Guiformes Waterbird radiation than in either the “Landbird assemblage” species or the Order Charadriiformes. The MCV and erythrocyte areas were respectively 32.6 and 43.8 % greater (p<0.001) in Palaeognathae than in Neognathae avian species (Table 3). There were a few differences in the MCHC between avian taxa in the Neoaves with MCHC greater in birds of the “Landbird assemblage” [35.1 ± (n=110) S.E.M 0.8 g dL-1] than in the order Charadriiformes [30.5 ± (16) 0.7] (p<0.05) and in the Afroaves [38.6 ± (50) 1.4 g dL-1] than the Australaves [32.1 ± (60) 0.5 g dL-1] (p<0.01).

There were negative (allometric) relationships between PCV/HCT, erythrocyte concentration and MCV versus log10 body weight in both birds and mammals (Table 4). In addition, there were negative relationships between hemoglobin concentrations and erythrocyte area versus log10 body weight in birds. The positive relationship between blood hemoglobin concentrations versus log10 body weight in mammals (Table 4) may reflect the taxa differences in blood hemoglobin concentrations (Table 2). While no allometric relationship for PCV/HCT was seen in marsupial mammals (adjusted R2 -0.006; p = 0.435), there is some allometric relationship in placental mammals (adjusted R2 0.057; p = 1.97E-05)(Table 5). Moreover, allometric relationships for PCV/HCT are observed in some mammalian taxa (such as the orders Chiroptera and Primates) but not others including Rodentia and Perissodactylia (Table 5). The relationship between erythrocyte size and log10 body weight was present when analyzed within taxa, for instance, in the orders Cetacea, Perissodactylia, Rodentia and Primates together the Pinnipedia (Table 6). No allometric relationship was observed in Order Carnivora excluding the Pinnipedia (marine carnivores) and both Chiroptera and Artiodactylia (Table 6).

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Table 4:

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Table 4. Comparison between hematological parameters between major avian taxa [Mean ± (number of species n=) S.E.M.].

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Table 5:

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Table 5. Relationships between erythrocyte parameters and log10 body weight.

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Table 6:

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Table 6. PCV/HCT

Strong allometric relationships were observed for erythrocyte size (area and MCV) in some avian taxa such as Columbiformes and to a less extent Galliformes (Table 7). There is no relationship between erythrocyte size and log10 body weight in some avian taxa such as the carnivorous Accipitriformes (Table 7).

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Table 7:

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Table 7. Relationships between MCV and log10 body weight in mammalian taxa.

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Table 8:

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Table 8. Relationships between MCV and erythrocyte size (area) and log10 body weight in avian taxa.

Discussion

There was no difference between the overall PCV/HCT between the Classes Mammalia and Aves (Table 1). This is identical to a previous report [19]. The mean PCV/HCT in birds was 44.7% (Table 1). This broadly agrees with a previous mega-analysis in birds [2] that reported a PCV/HCT of 46.3 % across about 100 avian species, principally passeriform species of birds. In contrast to the lack of differences between PCV/HCT in birds and mammals, there were differences between taxa within both the Classes Mammalia and Aves. For instance, PCV/HCT was lower in the Afrotheria and Xenarthra than in the other major taxa of placental mammals, namely Glires, Euarchontoglires or Supraprimates (Primates) plus Laurasiatheria. Within the Laurasiatheria, PCV/HCT was highest in the order Chiroptera and lowest in the order Perissodactylia. The oxygen needs for flight by bats might account for the high PCV/HCT. However, if the high HCT in bats (Table 2) is related to the oxygen requirements of flight, a differences between PCV/HCT in birds and mammals would be expected. No such difference for PCV/HCT is observed (Table 1). The PCV/HCT was greater in marine mammals, order Cetacea (whales and dolphins) and clade Pinnipedia (seals, sea-lions and walruses) than in related taxa respectively Artiodactylia [18] and non-marine Carnivora. This elevated PCV/HCT in marine mammals may again be accounted for by the energetic/oxygen needs of these large marine mammals. However, there was no such difference between the marine/diving birds. The magnitude of the differences in PCV/HCT in mammalian taxa [35.5 % (Afrotheria) to 55.6 % (Chiroptera)] was greater than that for avian taxa [39.1 % (Galliformes) to 47.9 % (Australaves)].

The blood concentrations of hemoglobin reported in the present communication (Table 1)(mammals - 14.9 g dL-1 and birds - 15.1 g dL-1) were somewhat higher than those reported previously [20]; viz. mammals 12.9 g dL-1 and birds 13.1 g dL-1. There are not difference between the overall blood concentrations of hemoglobin between the Classes Mammalia and Aves (Table 1) as has been previously observed [19]. Similarly, no differences in blood concentrations of hemoglobin were observed between avian taxa and for predominantly for mammalian taxa (Tables 2 and 4). The exceptions were the low blood concentrations of hemoglobin in Afrotheria and the higher blood concentrations of hemoglobin in in marine mammals, viz. order Cetacea and clade Pinnipedia (Table 3). Elevated blood concentrations of hemoglobin have been noted in diving animals [21] but they were no observed in avian marine birds in the Order Sphenisciformes (penguins). It is interesting that there were more difference between taxa for PCV/HCT than for blood concentrations of hemoglobin. For instance, while the PCV/HCT was 21.1 % higher in the Order Chiroptera than in the Super-order Laurasiatheria in general, there was no difference in the blood concentrations of hemoglobin (Table 2). In contrast comparing marine mammals with related taxa, the changes in PCV/HCT and blood concentrations of hemoglobin are broadly similar (Table 3). Similarly, artic species of mammals have elevated blood concentrations of hemoglobin size [22].

Both HCT/PCV and blood hemoglobin are related to log body weight in birds and mammals (Table 6). This is similar to the relationship reported by Bishop and Butler [2] who established a relationship between HCT and log body weight in birds [Hct=61Mb20.07±0.01, R2=0.31, P<0.001]. While it has been argued that hematocrit and blood concentration of hemoglobin or “oxygen-carrying capacity of the blood is highly conserved in birds and mammals” [19], the present analyses lend support the conservation of the same specific set-point for hematocrit and blood concentration of hemoglobin in birds and mammals.

Erythrocytes are larger and less numerous in birds than in mammals (Table 1). This is similar to previous reports [19]. Moreover, erythrocyte size is related to log body weight (Table 5, 7, 8). Although erythrocyte size has been used as a proxy for somatic cell size [7], the difference in erythrocyte size between birds and mammals might be assumed to reflect at least in part the volume of a nucleus in avian erythrocytes. In fish, the log nucleus area was strongly linearly related to log erythrocyte area [7]. The present strong link between erythrocyte size and log body weight in birds are consistent with previous reports. There is a strong positive correlation between log erythrocyte size (area) and log genome size in birds as in mammals, amphibians and reptiles [23-26]. Moreover, genome size is positively correlated with log body weight in birds [27].

It might be argued that differences in PCV/HCT and other hematological parameters in mammalian and avian taxa reflect an artifact of sampling of large versus small animals and the allometic relationship for PCV/HCT and MCV (Tables 5-8). It is argued that not only are there some taxonomic differences in PCV/HCT and other hematological parameters in the Classes Mammalia and Aves but also in the relationship between PCV/HCT with log10 body weight. For instance while there is an overall allometric relationship PCV/HCT in mammals (Table 5), it is only seen in some mammalian taxa (Chiroptera and Primates) but not others (Perissodactylia, Pinnipedia and Rodentia) (Table 6). Conversely there is an overall allometric relationship for MCV in both mammals and birds (Table 5), it is only seen in some mammalian taxa (Chiroptera and Primates) but not others (Perissodactylia, Pinnipedia and Rodentia) (Table 6).