Ratios of hatchling and adult mass-independent metabolism: A physiological index to the altricial-precocial continuum

69

Respiration Physiology (1986) 65, 69-83

Elsevier

R A T I O S OF H A T C H L I N G A N D A D U L T M A S S - I N D E P E N D E N T METABOLISM: A PHYSIOLOGICAL INDEX TO THE ALTRICIAL-PRECOCIAL CONTINUUM

T H E R E S A L. B U C H E R Department of Biology, University of California - - Los Angeles, Los Angeles, CA 90024, U.S.A.

Abstract. Measures of metabolism which are theoretically mass-independent (MIM values = BMR + M°'67) are calculated for non-passerine species from data in the existing literature. These MIM values are, in fact as the acronym implies, essentially mass independent, with only 8.2~ of the variation in MIM values attributable to log mass. In 10 of the 12 orders for which data were analysed, the slopes of the regressions of MIM values on log body mass do not differ significantly from zero. A dimensionless index of the intensity of the energy metabolism of hatchlings relative to that of conspecific adults is derived based upon the mass-independent measures of metabolism for adults and hatchlings. This ranking of metabolic maturity at hatching, a physiologicalindex, is compared with the most commonly used classification of the avian ~tricial-precocial continuum which is based upon morphological and behavioral characteristics. Several taxonomic groups appear more precocial metabolically than indicated by their ranking based upon morphological and behavioral criteria. Adult Altricial

Bird Body mass

Energy metabolism Hatchling

Metabolism Precocial

It is well k n o w n that birds exhibit a wide range in their degree of maturity at hatching. The terms altricial and precocial describe two distinct and contrasting states of development: (1) an altricial hatchling naked or only sparsely covered with down, eyes closed, unable to support itself or locomote effectively, and totally dependent upon its parents for food; and (2) a precocial hatchling covered with down, eyes opened, and able to locomote with legs well developed, and in the extreme cases able to obtain its own food. Actually a continuum of developmental states at hatching exists between these two conditions, and the most widely used classification for identifying or characterizing hatchling types is that o f Nice (1962). Nice describes eight categories of maturity at hatching based u p o n morphological and behavioral criteria and assigns all extant avian taxa to one or another of the categories. Accepted for publication 17 March 1986

0034-5687/86/$03.50 © 1986 Elsevier Science Publishers B.V. (Biomedical Division)

70

T.L. BUCHER

Studies in avian biology have demonstrated strong correlations, though not causal relationships, between hatchling type and a variety of characteristics. The most obvious of such relationships include: (1) a positive correlation between per cent wet yolk in the egg and degree of precociality (Nice, 1962; Carey et al., 1980), (2) an inverse correlation between hatchling growth rates (k-values; see Ricklefs, 1979) and the degree of precociality (once variation in growth rates due to differences in adult body mass is accounted for), (3) a difference in the ontogeny of rates of oxygen consumption between altricial and precocial species (Hoyt et aL, 1978; Vleck et aL, 1979), and (4) quantitative differences in the total amounts and pre-pipping rates of embryonic oxygen consumption between altricial and precocial species (C.M. Vleck etaL, 1980; Bucher, 1983). Though the aforementioned traits show clear correlations with degree of precociality or demonstrate quantitative differences between altricial and precocial species, none provides a quantitative, mass-independent measure of physiological maturity or of relative physiological precociality at hatching. The timing of the establishment of thermoregulatory capabilities in hatchlings has been 'linked with the mode of development, altricial or precocial, characterizing the particular species' (Dawson, 1984). Strictly speaking this is not correct because the terms describe state at hatching and not a pattern of development. Moreover, thermogenic capacity is a complex phenomenon involving, as a minimum, degree of feathering, mass-surface area ratios, behavioral responses, environmental circumstances, as well as heat production capacity (Freeman and Vince, 1974). The abifity ofhatchlings to function as effective endothermic homeotherms is influenced by all these factors which do not necessarily vary in concert. It would be extremely useful to have a mass-independent tpeasure of metabolic maturity at hatching that could be used as a physiological index and would allow direct comparisons between species. The concept of a mass-independent measure of metabolism (MIM values) for mammalian species has been developed and extensively discussed by Heusner (1983, 1985). Theoretically, measurements of mass (M) and basal metabolic rate (BMR) for a single, 'average', adult individual of a species allow the calculation of a MIM value ( = BMR + M °'67 or ml 02" h - 1/gO.67) which represents a constant for that species. Heusner's use of the exponent 0.67 is based upon a dimensional analysis of the power function relating energy metabolism and body mass (BMR = a" M b) and considerations of biological similitude. The concept of biological similitude within species employed by Heusner includes such things as internal and external body isometry, the same density, the same body temperature, and the same RQ. Based upon his assumptions he derived a relationship for ideal animals as a model against which to test empirical data. The power function relating mass and basal metabolic rate, BMR = a" M b, is a consequence of the dimensional structure of energy metabolism (energy/time). Heusner determines the numerical 'value b must take so that the mass coefficient (a = BMR/M b) becomes a dimensionally meaningful, mass-independent parameter' (Heusner, 1985). An empirical value of b different from 2/3 indicates the existence of qualitative changes associated with changes in mass and/or metabolism, that is, a lack of biological similitude. The MIM concept can be applied to birds as well as to mammals (fig. 1, Appendix:

AN INDEX OF RELATIVE PHYSIOLOGICALPRECOCIALITY

71

see, fig. 8; Heusner, 1985 for mammals). For simplicity I ignore variability in metabolic rate introduced by daily (Aschoff and Pohl, 1970) and seasonal cycles (Pinowski and Kendeigh, 1977) and population differences (Hudson and Kimzey, 1966) and pool data from different times of day or seasons if reported by a single investigator. The values plotted in fig. 1 are calculated from means of the masses and BMR values for each species of non-passerine bird that I found in the literature. A critical evaluation and comparison of values indicates that some of the reported values are probably not truly representative of basal levels of metabolism (for discussion see Calder and Dawson, 1978; Withers, 1983). At least several recent studies have indicated that apparently quiet, resting birds may in fact have levels of physiological functions highly elevated from minimal resting levels (Jungius and Hirsch, 1979; Bucher, 1985). Restraints on experimental animals, invasive instrumentation, and even the presence of the investigator can have subtle but significant effects. To avoid subjective bias I have used all values reported as BMR (and any resting metabolic rates that were lower than reported BMR's for a given species) to calculate the means listed in the appendix. Consequently, any individual value should be used in data analysis by other authors only after critical evaluation of the original references. There is a weak correlation between MIM values and log body mass for the entire data set (r 2 --- 0.082, t = 4.12, n = 192). Only 8.2Yo of the variation in the MIM ratio can be attributed to changes in log mass so the MIM values for non-passerine birds are, in fact as the acronym implies, essentially mass independent. The variability in the values reflects the diversity of form and function (lack of biological similitude) between and within the various orders (fig. 1). For the 12 orders with data from nine or more species the means of the MIM values are not the same (ANOVA for unequal samples; F[11,154] = 6.36, e < 0.001). Based upon the presently available data, analysis of covariance indicates that the slopes of the allometric equations relating BMR to mass are not all the same in various non-passerine orders (those orders with nine or more species values reported: see Appendix - F = 2.46; df = 11,142; P < 0.01). Therefore, use of the established nonpasserine allometric equations (Lasiewski and Dawson, 1967; Aschoff and Pohl, 1970) and extrapolation from them to predict metabolic rates for a particular species or for different sized individuals within a species are unwarranted if any data exists for the appropriate order or for some lower taxonomic level within it. Instead either one of two alternative options is more reasonable. One may take an empirical approach and use an allometric equation based upon data for the lowest and most closely allied taxonomic level for which there is an adequate data base; or one may use Heusner's theoretical approach and calculate the mean MIM value for the species in question or for the most closely allied taxonomic group. Based upon either of these expressions, one can predict metabolic rates. Either of the two choices seems to be a reasonable way to estimate the B MR, or resting metabolic rate, of individuals of different sizes. The use of MIM values has the additional advantage of allowing direct comparisons of metabolic intensity between species of different sizes.

72

T.L. BUCHER

XProcellariiformes, 7.06±0.77 ASphenisciformes, 7.19±0.80 oPelecaniformes, 8.47±2,05 14 "t~Ciconiiformes, 6.72 ± 1.10

18

O O

10

×

X

o x~

r~o~nXzx

x

6

2 I

I

I

. X Anseriformes, 8.78 ±1.02 & Folconiformes, 5.8950.57 " OGalliformes, 7.01 ± 0.98 14 aCharadriiformes, 8.58 ±1.56 ~ 13

10

O

X

×

oO

C)

o1

A

6

i-

I

tq

18

4-" £0

1

o

..c 2 I

I

1

I

F

Od

o v

E

18 14

• Phoenicopteriformes

XColumbiformes, 5.22 ~-0.74 APsittaciformes, 7.25 ~: 1.05 OApodiformes, 5.68±0.63 n Strigiformes, 4 . 9 5 ± 0 . 9 4

10 o

13

o

6

13

2 I

I

I

XStruthioniformes ZXRheiformes O Casueriiformes, 6.26-+1.97 14, aApterygiformes~ 5.67:tl.27 AGruiformes, 6.58 ± 1.22 10 #

"+m'~

•

I

oCuculiformes, 7.44±2.57 • Caprimulgiformes, 4.51-+-2.60 + Coliiformes oCoraciiforrnes, 6.15+2.41 ,IbPiciformes, 6.94±7.81

18

6

I

/,

•

•

o

o

x

2 I

101

i

I

I

10 s

MASS

I

10 5

(g)

Fig. 1. MIM values in relation to the log of body mass for non-passerine birds. Values plotted are the lowest values for each species (see Appendix). A mean + 95%CI for each order calculated from the same data is given. The usual units of measurement (ml 02 • h - 1/gO.67) are used to facilitate comparison with Heusner's plot for mammals (fig. 8; Heusner, 1985). The slopes of the regressions of MIM value on log body mass for 10 of the 12 orders for which n > 9 do not differ significantly from zero. The two exceptions are Ciconiiformes (r 2 = 0.62, t = 3.58) and Charadriiformes (r 2 = 0.39, t = 3.69).

73

AN I N D E X OF RELATIVE P H Y S I O L O G I C A L PRECOCIALITY

TABLE 1 MIM values for adults, yolk-free embryos at pre-pipping, and yolk-free hatchlings of species ranked in order of increased maturity in level of energy metabolism at hatching. Nice's rank refers to the 8 stages of maturity at hatching proposed by Nice (1962): Precocial 1, 2, 3, and 4; Semi-Preeoeial; Semi-Altricial 1 and 2; and Altricial. Adult values are from the Appendix. References for embryos and hatchlings: D. Vleck et aL, 1980; Vleek et aL, 1979; C.M. Vleck et al., 1980; Carey et aL, 1982; Bartholomew and Goldstein, 1984; Bucher, 1983; Bucher et al., 1986; Freeman, 1962; Hoyt et al., 1979; Hoyt and Rahn, 1980; Vleck and Kenagy, 1980; Pettit et aL, 1982; Ackerman et al., 1980; Booth, 1984, 1985; Vleck et aL, 1984; Bech et aL, 1984; Eppley, 1984; Pettit etal., 1981; Pettit and Whittow, 1983; Pettit etal., 1984; Dawson, 1984; Dawson and Bennett, 1981. MIM values

Poephila guttata Agelaius phoeniceus Pelecanus occidentalis Agapornis roseicollis Enicognathusferruginous Egretta ibis Coturnix coturnix Meleagris gallopavo Alectura lathami Leipoa ocellata Domestic fowl

Netta rufina Anas cylpeata Aythya ferina Anas platyrhynchos Anser anser Anas crecca Aythya fuligula Anas penelope Pygoscelis adeliae Columba livia Oceanodroma leucorhoa Oceanodromafurcata Puffinus pacificus Pterodroma hypoleuca Diomedea immutabilis Rissa tridactyla Synthliboramphus hypoleucus Gygis alba Larus argentatus Anous tenuirostrus Larus delawarensis Anous stolidus Larus atricilla Larus occidentalis Dromaius novaehollandiae Rhea americana Struthio camelus

Ratio

Nice's rank

Adult (A)

Pre-IP (B)

Hatchling (C)

B/A

C/A

7.86 9.94 8.68 6.22 7.25 a 5.24 7.30 6.50 8.20 5.69 5.20 10.85 10.15 11.74 7.58 7.01 7.43 6.91 6.37 8.51 5.34 9.43 6.28 5.42 4.90 5.87 10.06 10.72 6.75 8.41 5.57 8.78 5.13 7.79 7.15 6.10 8.54 5.05

1.35 1.80 2.12 1.29 2.07 1.66 1.84 1.93 2.82 2.83 2.38 2.40 2.53 2.36 2.28 3.01 2.75 2.44 1.48 1.35 1.81 1.36 2.70 1.54 1.73 1.61 2.28 2.49

1.76 1.84 2.51 1.83 2.38 3.17 4.78 b 3.82 b 4.10 b 4.50 b 3.60 b 3.75 4.36 b 4.28 4.68 b 4.77 3.04 3.74 b 3.04 3.00 3.35 4.83 4.26 5.19 3.32 4.66 3.29 5.22 3.27 6.01 5.51 3.39 5.19 5.00

0.17 0.18 0.24 0.21 0.29 0.32 0.25 0.30 0.34 0.50 0.46 0.22 0.25 0.31 0.33 0.44 0.32 0.46 0.27 0.28 0.31 0.20 0.32 0.28 0.34 0.26 0.27 0.49

0.22 0.19 0.29 0.29 0.33 0.43 0.58 b 0.67 b 0.79 b 0.38 b 0.47 b 0.54 0.59 b 0.62 0.73 b 0.56 0.57 0.40 b 0.48 0.55 0.68 0.82 0.42 0.48 0.49 0.55 0.59 0.59 0.64 0.77 0.77 0.56 0.61 0.99

a Value is the mean for the order Psittaciformes (see fig. 1). b Calculated using hatchling mass, not yolk-free hatchling mass.

A A A A A SA1 P3 P3 P1 P1 P3 P2 P2 P2 P2 P2 P2 P2 P2 SA2 A SP SP SP SP SP SP SP SP SP SP SP SP SP SP P3 P3 P3

74

T.L. BUCHER

At hatching a bird is growing rapidly and by definition does not have a basal metabolic rate. However, a mass independent measure of its oxygen consumption at that particular stage can be calculated from its resting metabolic rate (RMR) measured at incubation temperature (MIM value = RMR - M ° 6 7 ) . This measure of energy metabolism has the same units as the adult MIM. Therefore, the ratio of hatchling MIM (based on RMR at incubation temperature) to adult MIM (based on BMR) gives a dimensionless index of the intensity of the oxygen consumption of the hatchling relative to that of the conspecific adult (table 1). The ratio of MIM values can be used as a quantitative physiological index to rank different species along an altricial-precocial continuum (the higher the value of the ratio the more precocial the species). If the ratio equals one, the two animals would have the same rate of oxygen consumption if they were the same mass, that is, the hatchling would be metabolically the same as the adult. The more the hatchling MIM differs from the adult MIM, the more the hatchling differs from the model adult in qualitative ways. In fact, we know that there are many qualitative differences between adults and hatchlings including such properties as fractional water content and body temperature. This mass-independent ranking can be determined without reference to behavioral, morphological or environmental factors. The ranking of species and of higher taxa generated by this physiological index can be compared with the ordering given by Nice's primarily behavioral and morphological classification. Similarities and differences between the rankings given by the two systems are worthy of note. Members of the Passeriformes and Psittaciformes are among the most altricial of birds by either measure, as are the Pelecanidae. Assuming that the individual species for which data exist are representative of the orders, Sphenisciformes, and especially Columbiformes, are strikingly more precocial metabolically than indicated by Nice's classification which characterizes them as semi-altricial and altricial, respectively. The MIM ratios of a penguin and a pigeon are higher than those of members of several orders classified as precocial by Nice, e.g., some GaUiformes and Anseriformes. Two groups, the Procellariiformes and the Laridae, considered semi-precocial by Nice also have MIM ratios higher than some Anseriformes and Galliformes. The metabolism of chickens increases dramatically hour by hour after hatching (Freeman, 1964), and this probably is true in other species. Therefore, the variation in the ratios calculated from MIM values (table 1) is not surprising because the values are based on data reported for hatchlings whose exact ages were not reported. Additionally, some of the values for BMR may not be truly representative of basal levels of oxygen consumption. The MIM ratios are affected by both hatchling and adult values. There is no a priori reason to assume that all characteristics of a bird will mature at the same rate. Additionally, behavior can be very plastic. Thus, in the case of the Adelie Penguin, the hatchlings face extremely harsh environmental conditions (low ambient temperatures) and intense predation by Skuas. Moreover, Adelie chicks have no possibility of feeding themselves even if they were to leave the nest immediately upon hatching because feeding in this species involves long distance travel, efficient swimming and a complex, predatory foraging behavior. Thus, there are environmental and

AN INDEX OF RELATIVE PHYSIOLOGICAL PRECOCIALITY

75

behavioral constraints which make it maladaptive for the chicks to leave the nest immediately after hatching. They are constrained within an altricial behavioral mode even though they are metabolically more precocial than many species which do leave the nest and feed themselves. Two advantages to MIM values for comparing hatchling metabolism to adult metabolism or to hatchling metabolism in other species are immediately apparent. First, each species acts as its own reference in the assessment of metabolic intensity at hatching or metabolic precociality. The alternative method is to compare the hatchling's metabolism to a value predicted by a regression line (see the discussion above). This regression line, of course, represents a mean value from which each species deviates to a greater or lesser degree, and hence has questionable relevance for intraspecific comparisons. In addition, extrapolation beyond the limits of the values of mass used to compute the regression (a necessity because of the small size ofhatchlings) greatly reduces one's ability to make predictions with reasonably narrow confidence intervals. Blem (1984) comments upon some of the difficulties inherent in simply dividing metabolic rate by mass to remove the effects of size in biological analysis. Heusner (1985) rejects the pooling ofinterspecific data and points out that extrapolation from such pooled data can lead to predictions which are meaningless (see fig. 1, Heusner, 1983). Second, if comparisons of the metabolic rates of hatchlings are made with values predicted from regression lines, new values must be separately calculated for each hatchling (or embryonic) mass considered. From a practical point of view, it is easier to compare MIM values calculated for different embryonic and/or hatchling masses to a single species value than to a series of values calculated from a regression equation. The ratios of embryo and hatchling MIM to adult MIM values are directly comparable, both within a species at different stages of maturation and between species as an index of relative maturity at particular times in the ontogenetic sequence (e.g., at hatching or at pre-pipping). If an adult value for a particular species has not been and cannot be measured, then a mean value for the most closely related taxon can be used for the adult MIM value (see fig. 1). Altricial and precocial are extremely useful terms and concepts, but their use should not blind us to the variability which exists within and between various taxa and to the fact that different parameters of avian performance may have different developmental patterns and rates which may not always vary in concert. The MIM ratio offers a convenient quantitative index of metabolic maturity and is an instructive guide to the rank of a species along one physiological axis (energy metabolism) in the altricialprecocial continuum.

Acknowledgements.This study was supported in part by NSF grant # BSR 84-00387.

76

T.L. BUCHER

Appendix Mass a

(g)

MIM value a (ml 02" h - 1/M°'67)

References b

Struthioniformes

Struthio camelus

100000.0

6.86 (5.05) c

29, 41

21700.0

8.54

13

39992.0 17600.0

6.87 (6.10)c 6.41

10, 13 29

3.90 4.02 3.08

10 10 10

Rheiformes

Rhea americana Casuariiformes

Dromaius novaehollandiae Casuarius bennetti Apterygiformes

Apteryx haastii Apteryx australis Apteryx owenii

2540.0 2380.0 1095.5

Procellariiformes

Diomedea exulans Macronectes giganteus Diomedea chrysostoma Diomedea immutabilis Phoebetrt'a fusca ProceUaria aequinoctialis Procellaria cinerea Puffinus griseus Puf/'mus pacificus Pterodroma brevirostris Puffinus nativitatis Pterodroma mollis Pterodroma hypoleuca Pachyptila vittata salvini Pelecanoides georgicus Bulweria bulwerii Oceanodromafurcata Oceanodroma leucorhoa

8130.0 4120.0 3753.0 3101.0 2875.0 1287.0 1014.0 740.0 337.8 315.0 307.6 274.0 173.5 165.0 127.0 87.0 46.8 43.5

8.79 10.63 (8.25) c 6.18 5.87 7.18 9.38 8.75 6.22 5.42 6.76 5.72 7.33 5.30 (4.90) c 9.14 6.91 4.61 7.45 (6.28) ¢ 9.64 (9.34) c

1 1, 17 1 22 1 1 1 17 17 1 17 1 17, 22 1 1 17 17, 39 17, 35

24085.0

9.29 (8.78) c

7

12175.0

7.83

7

Sphertisciformes

Aptenodytesforsteri Aptenodytes patagonicus Megadyptes antipodes Pygoscelis adeliae Spheniscus humboldti Eudyptes chrysolophus Eudyptes pachyrhynchus Eudyptes chrysocome Eudyptula minor

4800.0 4235.0 3870.0 3870.0 2600.0 2330.0 930.0

7.06 10.04 (8.51)c 6.71 6.12 6.39 5.80 7.93 (7.52) c

7 7 7 7 7 7 7, 37

5090.0 3274.0 2660.0 1330.0

10.66 9.20 (8.68) c 13.84 8.54

17 17 17 23

Pelecaniformes

Pelecanus conspicillatus Pelecanus occidentalis Phalacrocorax atriceps Phalacrocorax auritus

AN INDEX OF RELATIVE PHYSIOLOGICAL PRECOCIALITY

Mass ~ (g)

Sula dactylatra Fregata magnificens Anhinga anhinga Sula sula Phaethon rubricauda

MIM value• (ml 0 2 ' h - 1/M°-67)

Referencesb

1289.0 1078.0 1040.0 1017.0 593.2

8.18 4.65 5.69 7.58 8.39

17 17 23 17 32

5710.0 5470.0 2500.0 1870.0 940.0 600,0 314.0 309.9 299.2 290.4

8.10 7.39 9.23 7.14 7.52 6.69 5.23 6.59 5.24 4.03

29 29 29 29 29 29 16 16 16 16

Ciconiiformes

Leptoptilos javanicus Jabiru mycteria Mycteria americana Ardea herodias Guara alba Botaurus lentiginosus Egretta thula Egretta tricolor Egretta ibis Egretta caerulea Phoenicopteriformes

Phoenicopterus tuber

2625.0

10,87 (8.66) ¢

3, 29

8880.0 8300.0 4360.0 2620.0 1870.0 1237.0 1163.8 1149.0 904.0 816.0 791.0 721.0 660.0 574.0 554.0 467.3 440.0 289.0 250.0

8.21 12.85 8.02 (7.01) c 6.32 8.76 10.85 8.52 (7.58) c 7.81 6.69 11.74 12.79 9.57 7.03 (6.37) ~ 6.91 10.15 7.54 (6.83) ¢ 9.99 9.04 7.43

29 2 29, 33 29 29 34 29, 34 29 33 34 34 34 33, 34 34 34 28, 33 34 34 34

Anseriformes

Cygnus buccinator Cygnus olor Anser anser Chauna chavaria Domestic duck

Netta rufina Arias platyrhynchos Branta bernicla Anas rubripes Aythya ferina Anas strepera Anas acuta Anas penelope Aythya fuligula Anas clypeata Aix sponsa Aythya nyroca Anas querquedula Anas crecca Falconiformes

Vultur gryphus Gypaetus barbatus Aquila chrysaetos Geranoaetus melanoleucus Buteo buteo Falco mexicanus ~ ~ Pernis apivorus Falco mexicanus ~ ~ Falco subbuteo

10320.0 5070.0 3000.0 2860.0 1012.0 755.1 652.0 498.3 208.0

6.23 6.52 4.14 4.45 6.53 6.15 5.46 6.08 6.51

29 29 29 29 34 28 33 28 29

77

78

T.L. B U C H E R

Mass a (g)

Accipter n/sus Falco tinnunculus

135.0 108.0

M I M value ~ (ml O~" h - 1/M°67) 6.36 6.41

References b

29 29

Galliformes

Tetrao urogallus Meleagris gallopavo Crax alberti Gallus gallus Domestic fowl

Penelope purpurescens Alectura lathami Leipoa ocellata Lyrurus tetrix Bonasa umbellus Alectoris graeca Lagopus lagopus Perdix perdix Lagopus mutus Lagopus leucurus Colinus virginianus Callipepla californicus Callipepla gambelii Coturnix coturnix Coturnix chinensis Excalfactoria chinensis

3955.0 3700.0 2800.0 2430.0 2143.2 2040.0 1910.0 1390.0 1005.0 644.0 626.5 555.0 492.0 432.0 326.0 194.0 138.0 136.0 101.6 49.0 42.7

8.27 6.50 5.79 7.51 6.20 (5.20) c 5.89 8.20 5.69 12.85 5.60 6.46 8.60 (7.36) ¢ 6.42 11.58 8.77 5.85 5.02 4.54 8.17 (7.30) c 8.29 4.21

4030.0 3890.0 556.0 96.0

7.34 5.74 7.31 (5.77) c 6.65

33 29 29 29 29 29 Booth unpubl. Booth unpubl. 36 33 33 33 33 33 33 29 33 20 29, 33, 34, 40 34 29

Gruiformes

Anthropoides paradisea Grus canadensis Fulica atra Crex crex

29 29 5, 33, 34 33

Charadriiformes

Larus hyperboreus Gabianus pacificus Catharcta maccormicki Larus argentatus Uria lomvia arra Catharcta skua Uria aalge inornata Larus oecidentalis Larus delawarensis Seolopax rusticola Larus canus Sterna maxima Rissa tridactyla Larus ridibundus Larus atricilla Sterna fuscata Synthliboramphus hypoleucus Anous stolidus

1600.0 1210.0 1130.0

1000.0 989.2 970.0 878.2 761.0 439.0 430.0 429.5 373.0 350.5 283.0 275.6 148.0 146.0 138.7

18.82 9.48 13.10

8.41 12.70 8.48 11.20 (9.86) c 7.15 8.78 6.66 7.05 8.53 10.06 8.32 (7,67) ~ 7.79 5,01 10.72 5.13

29 29 17

17 25 29 25 17 17 33 33 17 6 17, 33 17 17 18 17

A N I N D E X O F RELATIVE P H Y S I O L O G I C A L P R E C O C I A L I T Y

Mass" (g)

Sterna lunata Gygis alba Anous tenuirostris Tringa ochropus Charadrius dubius

M I M value a

References b

(ml 0 2 • h- I/M°'67)

131.7 98.1 90.2 90.0 36.0

4.79 6.75 5.57 8.11 6.77

17 17 17 34 33

335.4 166.0 164.6 154.0 150.0 147.0 108.0 107.0 81.0 41.2

6.18 (5.34) c 4.48 6.27 (5.41) ¢ 6.98 5.14 5.21 6.60 5.46 (5.25) c 3,75 3.88 (3.78) c

14, 29, 33 14 29, 33 33 29 14 33 29, 33 14 14, 29

341.9 271.0 85.6 81.7 55.7 48.1 40.0 40.0 32.9 27.0

7.22 5.91 6.26 6.66 (6.06) ¢ 7.35 6.22 8.84 8.20 7.56 (6.19) c 10.24

9 15 33 33 8 8 34 34 8, 34 34

284.7 188.0 175.0 119.8

5.94 8.88 8.54 7.57 (6.38) c

33 34 34 33, 34

2024.0 1216.2 520.0 484.5 406.0 333.0 244.0 162.7 159.0 137.6 120.6 101.7 54.2 46.2

4.60 8.04 (7.14) ¢ 5.65 / 4.95 (4.57) c 5.50 6.20 5.85 (5.66) c 5.15 4.46 (3.17) ¢ 4.82 4.11 5.97 (4.17) ¢ 5.33 3.28 (3.18) ~

33 4, 38 24 26, Johnson unpubl. 21 27 21, 33 27 19, 31 12 31 11, 19, 21, 31 31 30, 31

Columbiformes

Columba livia Ocyphaps lophotes Streptopelia decaocto Streptopelia turtur Columba palumbus Streptopelia risoria Streptopelia senegalensis Zenaida macroura Petrophassa ferruginea Columbina inca Psittaciformes

Amazona viridigenalis Cacatua roseicapilla Nymphicus hollandicus Myiopsitta monachus Bolborhynchus lineola Agapornis roseicollis Neophema pulchella Neophema bourkii Melopsittacus undulatus Loriculus galgulus Cueuliformes

Geococcyx californianus Eudynamys scolopacea Centropus senegalensis Cuculus canorus Strigiformes

Nyctea scandiaca Bubo virginianus Strix aluco Tyto alba Asioflammeus Sumia ulula Asio otus Glaucidium cuculoides Otus asio Athene cunicularia Otus trichopsis Aegolius acadicus Glaucidium gnoma Micrathene whitneyi

79

80

T.L. BUCHER

Mass a (g) Caprimulgiformes Podargus ocellatus Caprimulgus europaeus Chordeiles minor Nyctidromus albicollis Phalaenoptilus nuttallii Apodiformes Apus apus Patagona gigas Eulampis jugularis Lampornis clemenciae Eugenes fulgens Calypte anna Selasphorus rufus Selasphorus sasin Archilochus alexandri Archilochus colubris Calypte costae Stellula calliope Coliiformes Colius striatus Coraciiformes Upupa epops Alcedo atthis Piciformes Dendrocopus major Jynx torquilla

MIM value~ (ml 0 2 . h 1/M°'67)

References b

145.0 77.4 75.0 43.0 40.0

3.62 6.27 4.57 5.38 2.71

33 33 29 29 33

44.9 19.1 8.4 7.9 6.6 4.8 3.8 3.7 3.3 3.2 3.2 3.0

6.11 7.10 6.68 4.56 5.15 7.28 4.97 5.06 5.07 6.37 4.38 5.40

33 33 33 33 33 33 33 29 29 29 29 29

52.5

4.46

33

67.0 34.3

5.96 6.34

34 33

107.5 31.8

7.56 6.33

33 33

a Mean of values calculated for the species from data in the references cited. b To minimize the size of the bibliography I cited review papers which contain values for numerous species unless inconsistent values for the same species from the same references were noted in different reviews. In such cases, I cited original references. (1) Adams and Brown, 1984; (2) Bech, 1980; (3) Bech et al., 1979; (4) Benedict and Fox, 1927; (5) Brent et al., 1984; (6) Brent et aL, 1983; (7) Brown, 1984; (8) Bucher, 1983; (9) Bucher, 1985; (10) Calder and Dawson, 1978; (11) Collins, 1963; (12) Coulombe, 1970; (13) Crawford and Lasiewski, 1968; (14) Dawson and Bennett, 1973; (15) Dawson and Fisher, 1982; (16) Ellis, 1980; (17) Ellis, 1984; (18) Eppley, 1984; (19) Gatehouse and Markham, 1970; (20) Goldstein and Nagy, 1985; (21) Graber, 1962; (22) Grant and Whittow, 1983; (23) Hennemann, 1983; (24) Herzog, 1930; (25) Johnson and West, 1975; (26) Johnson, 1974; (27) Johnson and Collins, 1975; (28) Kaiser and Bucher, 1985; (29) Lasiewski and Dawson, 1967; (30) Ligon, 1968; (31) Ligon, 1969; (32) Pettit et aL, 1985; (33) Pinowski and Kendeigh, 1977; (34) Prinzinger and Hanssler, 1980; (35) Ricklefs et al., 1980; (36) Rintamaki et al., 1983; (37) Stahel et al., 1984; (38) Turner, 1969; (39) Vleck and Kenagy, 1980; (40) Weathers, 1981 ; (41) Withers, 1983. c Numbers in parentheses are the lowest values calculated for the species from the data in the references cited.

AN INDEX OF RELATIVE PHYSIOLOGICAL PRECOCIALITY

81

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