Active and resting metabolism in birds: allometry, phylogeny and [PDF]

/. Zool., Lond. (1987) 213, 327-363

Active and resting metabolism in birds: allometry, phylogeny and ecology P. M. Bennett Institute of Zoology, Zoological Society of London, Regent's Park, London NW1 4RY and P. H. Harvey Department of Zoology, University of Oxford, South Parks Road, Oxford 0X1 3 PS (Accepted 17 February 1987) (With 6 figures in the text) Variation in resting metabolic rate is strongly correlated with differences in body weight among birds. The lowest taxonomic level at which most ofthe variance in resting metabolic rate and body weight is evident for the sample is among families within orders. The allometric exponent across family points is 0-67. This exponent accords with the surface area interpretation of metabolic scaling based on considerations of heat loss. Deviations of family points from this allometric line are used to examine how resting metabolic rates difTer among taxa. and whether variation in resting metabolic rate is correlated with broad differences in ecology and behaviour. Despite the strong correlation between resting metabolic rate and body weight, there is evidence for adaptive departures from the allometric line, and possible selective forces are discussed. The allometric scaling of active metabolic rate is compared with that of resting metabolic rate. The allometric exponents for the two levels of energy expenditure difTer, demonstrating that active small-bodied birds require proportionately more energy per unit time above resting levels than do active large-bodied birds. No consistent evidence was found to indicate that the different methods used to estimate active metabolic rate result in systematic bias. Birds require more energy relative to body size when undertaking breeding activities than at other stages ofthe annual cycle.

Contents Introduction Materials and methods Resting metabolic rate Active metabolic rate Ecological classification Nest type Development Incubating sex Nestling care Diet Habitat Stratification Locomotion

Breeding latitude Migration Mode of prey location and capture Mating system Nest dispersion Activity timing

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P. M. BENNETT AND P. II. HARVEY Analysis Results Taxonomic level of analysis Differences between families Ecological correlates Active metabolic rate Discussion References Appendices

Introduction

Basal and active metabolic rates have been measured for a number of bird species, and several authors have attempted interspecific comparisons of the relationships between measures of metabolic rate and body size (Brody & Proctor, 1932; King & Farner, 1961; Las'cwsk. & Dawson, 1967- Zar 1969- Aschoff & Pohl, 1970/.; Kendeigh, Dol'nik & Gavrilov, 1977; Walsberg 1983; Whittow & Rahn, 1984). There is no general agreement on the way metabolic rates scale with body size Moreover, few studies have attempted to test in a rigorous and comprehensive manner which species have higher or lower metabolic rates than expected for their size, or if this variation ,s associated with differences in ecology and behaviour. In this paper, we review the available data to examine four main questions as well as testing subsidiary hypotheses. First, how do metabolic rates change with body size in birds? Secondly, are there ecological correlates of metabolic rate when size and taxonomic effects are taken into account? Thirdly, do estimates of active metabolic rate vary with the method of measurement used and the time of year when the measurements are taken' Fourthly, how much greater is active than resting metabolic rate? Our analyses are more rigorous than those reported previously and our data base is more extensive.

Materials and methods Resting metabolic rate All data have been collected from the published literature. Data on variation in .^^"J^^S

i Y^i., ^h hv K .-nrfoift-h et al (1977) for 172 species. Manv studies have appeared since then, particular!) o

^X^rt^m-BZn, ml. EUi, ,984,. and our da.- se, ineiudes es.irna.es of re„a6 metabolic rate and body weight for 399 species (see Appendix 2). Estimates of what we shall term Resting Metabolic Rate (RMR) have been *...„,... term*. •standard' metabolic rate. The experimental conditions under which these . obtained difTer. The most common conditions are that basal metabolic rate is measured on unfed macUV bird in the dark at temperatures within the thermoneutral zone. Standard metabolic rates arc us 11 e h .ates taken when the thermoneutral zone has not been defined, and thus may include omc «** 1 m oretzulatioi, Both estimates have been included in Appendix 2. although the great majority a,e o. b ""rate. The reason that the term "resting metabolic rate' is preferredl*^*^** metabolic rate-is that the estimates are not all minimum estimates of oxygenconf been shown to have metabolic rates below accepted basal levels. The most Striking birds that enter torpor, such as hummingbirds Trochilidae and mouseb.rds Coh.dae.

M E TA B O L I S M

IN

BIRDS

329

Estimates of RMR that were taken during the active phase ofthe daily cycle have been excluded from the analyses (leaving data for a total of 356 species) because they have been shown to be around 25% higher in son.- -pecies (AschofT& Pohl. 1970./. /.). Many studies do not report when measurements were taken and this factor results in an unknown bias in the data. Another source of bias results from investigators using cither the lowest values obtained within the thermoneutral zone, or the average of all values within the zone, to estimate RMR. In addition, there is evidence for some species that RMR differs according to season of measurement (sec Weathers, 1979). As long as there is no systematic distribution in these potential sources of bias, then such measurement error should not affect our conclusions. In some cases, there has been more than one study on a particular species (see Appendix 2), and the estimates of RMR and the weight of animals differ between studies. In such cases, the lowest mass-specific RMR (RMR divided by body weight) was selected for analysis because RMR is the minimum value within the zone of thermoneutrality. The mass-specific RMR is only an accurate measure if the relationship between RMR and body size between individuals within species isiso .'trie. However, ranges of intraspecific variation in body size were very small compared with differences in RMR. and so the assumption of isometry is not critical. Ac tire metabolic rate Estimates of active metabolic rate (AMR) for 96 species are given in Appendix 3. The last review was by Walsberg (1983) who obtained estimates for 42 species. The methods used to estimate daily energy expenditure vary greatly and have been obtained on birds during different phases of the annual cycle. The codes used in Appendix 3 to describe the various methods refer to (after King, 1974): 1. Pellet analysis 2. "op contents 3. Single-labelled water 4. Double-labelled water 5. Time-activity combined with laboratory data on RMR 6. Extrapolations from laboratory data 7. Extrapolations from food consumption of captives 8. Observations of feeding rate and excretory rate 9. Observations of feeding rate combined with data on caloric value of food 10. Weight loss Thi ost commonly used techniques are 5 and 9. However, only 3 and 4 provide direct measurements of energv xpenditure. The indirect methods are based on many assumptions which are only beginning to be tested. For example, Wijnandts (1984) showed that Graber's (1962) estimates based on pellet analysis for 3 owl species are incorrect because the assumption that the owls void a single pellet a day is invalid. Method 5 is commonly used and is an indirect estimate of AMR using daily activity budget data combined with laboratory derived estimates ofthe energy costs ofthe various daily activities. The energy cost of activilcs are either generated by obtaining expected values from allometric equations based on small samples of species or are simply guessed as some multiple of RMR. In the latter case, the ratio of AMR to RMR has been calculated for a small number of species and is used as the multiple to estimate the energy costs of activity. This ratio is only appropriate if AM R and RMR scale to body size with the same exponent. This question and * comparison ofthe various methods for estimating AMR will be addressed below. Because ofthe relative Paucit. of data and the heterogeneous methods that have been used to estimate AMR, the ecological correlates of size-corrected values will not be examined. Ecological classification Species for which information on RMR was available were classified for a number of ecological and ^navioural variables (for sources see Bennett, 1986). As demonstrated below, the lowest taxonomic level

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METABOLISM IN BIRDS

351

Appendix 2 Table I (com.) Order

Family

Charadriiformes Charadriidae Thinocoridae Scolopacidae Stercoraiidae Laridae

Species Charadrius dubius Pluvialis dominica Thinocorus rumicivorus Tringa ochropus Scolopax rusiicola Catharacla skua C. maccormicki Gabianus pacificus Larus dcluwarensis I., canus

Columbiformes Columbidae

Anhimidae Cathartidae Falconidae

13-3

55-5

90 430 970

138-7 90-2 98-1

989 956 150 318 314 315 353 266 300 311 372 108 154 187 152 155 91-4

123

'...

98

59-6

148 373

Nymphicus hollandicus Ay thy a fuligula A. ferina Chauna chavaria Vultur gryphus Falco linnunculus /'. subhuteo

44-6

439 428 431

131-7

Scardafella inca Petrophassa ferruginea i.epiolila verreauxi Turlur lympanislra Eolophus roseicapillus

6-4 19 177-4

252 289 285 306

Sterna lunula S. Juscala S. maxima A nous siolidus A. tenuirostris Gygis alba Ur'ta lorn via U. aalge Columba palumhus C. unicincta C. livia

8-6

1130 1210

761

Zenaida macroura

Falconiformes

36 118

1210 275-6

Streptopelia seitegalensis S. turlur S. decaoclo

Cacatuidae

RMR

1000

/_. argenlaius /_. occidenlalis L. hyperhoreus L. atricilla /_. ridibundus

Alcidae

WT

40-5

81 131 68 271 321 85-6

574 816 2620 10320

108 208

127 48 46-6 99-2 70-2 180-1 38-7 44-8 42-8 41-4 38-4 14-5 16 4 51-9

161 131 16-8 140-5 140-5

17 35-4 34-8 35-9 38-3 33-7 30 *"" 32 9 35-5 17-5 23-5 26-3

218 18-3 13 4 15-2

5-2 8-2 18-3 12-8

29 62-9 14-2 55-8 1201

142 351 17 26-8

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P. M. BENNETT AND P. H. HARVEY

352

Appendix 2 Table I (com.) Order

1 1*.

Accipitridae

I-

1

Galliformcs

Species

Family

Phasianidae

F. sparverius Pernis apivorus A ccipiier nisus Buteo buteo Aquila chrysaetos Gypaelus barbaius Geranoaelus melanoleucus Haliaeelus leucoccphalus Meleagris gallopavo Lagopus lagopus

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L. mutus L. leucurtts Telrao urogallus

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T. tetrix Bonasa umbellus Lophortyx californica L. gambelii Colinus virginianus Excalfacloria chinensis Coturnix coturnix C. japonica Perdix perdix A lee tor is graeca

A. chukar Gallus gallus

Cracidac Gruiformes Gruidae Rallidae Psittaciformes Psittacidac

Penelope purpurescens Crax alberti C. daubenioni Grus canadensis Anlhropoides paradisea Crex crex Fulica atra Melopsitlacus undulatus Agarpornis roseicollis Myiopsitla monachus

WT 117 652 135 1012 3000 5070 2S60 4096 3700 524 567 539 590 432 326 3900 4010 1079 931 644 138 126-1 194 42-7 49 97 97 97-5 115 483 501 620 633 475 2430 2000 2000 2000 2006 2710 2040 2800 2800 3890 4030 96 412 39 25-2 33-7 48-1 81-5 83-1 83-1 80-4 80-4

RMR 17-4 48-3 19 6 77-6 102 228 106 272-4 184 64-2 59-3 78-8 70-5 77-8 48-8 246 244 144-5 157-3 49-2 15-7 15-6 23 6 13 18-4 23 21-3 20-2 49-5 44-5 58-9 52-3 40-5 160-4 97-5 137 115 130-7 124 112 136 148-4 168 220 16-3 42-1 12-8 6-2 9-9 9-6 16-2 16-3 14-1 15-5 10-6

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METABOLISM IN BIRDS

353

Appendix 2 Table I (com.) Order

Cuculiformes

Family

Cuculidae

Species Bolborhynchus lineola Loriculus galgulus Neophema pulchella N. bourkii Amazona viridigenalis Cuculus canorus Eudyramys scolopacea Cacomanlis variolosus

r;ci formes

Strieidae

Geococcyx californica Centropus senegalensis Micralhene whilneyi Nyclea scandiaca Bubo virginianus Speotyto cunicularia Of US asio O. scops O. trichopsis Glaucidium gnoma G. cuculoidcs Surnia ulula Strix aluco Aegolius acadicus

Asio Jlammeus A. oius

Caprimulgiformes

Apodiformes

Podargidac Caprimulgidae

Apodidae Trochilidac

Podargus ocellaius Chordeiles minor Caprimulgus europaeus Phalaenoptilus nutlalli Nyclidromus albicollis Euros topodtts gut tains Apus apus Calypte costae C. anna Siellula calliope Archilochus colubris A. alexandri

Selasphorus rufus S. sassin Eugenes fulgens Lampornis clemenciae

WT

RMR

C

55-7 27 40 40 337-8 111-6 128 188 23-8 23-8 284-7 175 45-9 2026 1450 132-4 142-7 151 166 63-9 120 54 163 333 520 124 105-9 83 85-5 406 252 236 243 240-5 145 72 77-4 40 35 43 88 44-9 3-2 4 4-8

12-5 10 7 12 111 43-9 17-3 25-9 34 3-9 2-5 30-2 311 5-3 87 108 16 14 14-6 121 7-3 9-2 91 17-9 35-1 43 13-5 16 2 10 5 14 5 26-6 19-7 27 29-2 26-4 11-7 9-1

A'

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1-4 1-4

2-1 12-9 5-3 21

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P. M. BENNETT AND P. H. HARVEY

354

Appendix 2 Table I (com.) Order

Family

Species

Eulampis jugularis Patagona gigas

Oreotrochilus estella Ocrealus underwoodii Chlorostilbon mcllisugus Orlhorhynchus crislalus Aceslrura mulsani Urosticle henjumini Chrysuronia oenone Florisuga mellivora Agleaclis cupripennis Boissonneaua mallhewsii Amhracolhorax nigricollis Trochilus scilulus

Coliiformes

Coliidae

T. polyimus Coitus sirialus C. custanoius

Trogoniformes Coraciiformes

Trogonidae A Iced in id ae Upupidae Mcropidac

Piciformes

Picidae

Passeriformes

C. macrourus Colitis indicus Trogon rufus Alcedo at this Upupa epops Merops viridis Jynx torquilla Picoides major

Dendrocolaptidae Xiphorhynchus guliatus Formicariidae Thamnophilus punclalus Pipridae Pipra mentalis

WT SI 5 815 8-4 9-5 9-5 191 17-5 17-5 8-4 8-7 8-7 2-7 2-7 2-9 2-9 2-9 2-9 3-3 3-3 3-9 3-9 5 5 6-9 6-9 7-2 7-2 7-2 7-2 7-7 7-7 4 4 4-9 6-3 52-5 51 2 69 69 57-7 48-5 53-5 53 34-3 67 33-8 33-8 318 98 117 45-2 21 12 12-3 12 4 14 5

RMR 13

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METABOLISM IN BIRDS

355

Appendix 2 Table I (com.) Order

Family-

Species Manacus vilellinus

Tyrannidac

Alaudidae

Hirundinidae

Molacillidae

Pycnonotidac

Sayornis phoebe Empidonax virescens E. minimus Myiarchus criniius Contopus virens Tyrannus tyrannus Eremophila alpestris Lullula arborea Alauda arvensis Riparia riparia Hiriindo rustica H. labitica Delichon tirbica Motacilla /lava At. alba Anthus pratensis A. irivialis A. campeslris Pycnonotus goiavier P. Jinlaysoni

Criniger bres

irenidae Laniidae

Chloropsis sonnerali Lanius coliurio L. excubiior L. crisialus

Bombycillidae Cinclidae Troglodytidae

Bomhycilla garrulus Cinctus mexicanus Troglodytes troglodytes

Prunellidae Muscicapidae

T. aedon Prunella maduluris Erithacus rubecula

E. cyane E. luscinia E. svecicus Saxicola rubelra Phoenicurus phoenicurus P. ochruros

WT

15-8 15 5 15 6 21-6 12 3 10

RMR 4-9 4-8

5-7 71 3-7 4-9

33-9 13-9 35-7 26

7-9 5-3 9

26 33-2 461 13-6

6-8 101 11-6 4-8 6-5 3-7 4-8 7-3 5-3 6-2 5-8 6-2 7 7-9 51 7 4-6 6-5 7-3 9-6 7-8 7-9 16-8 5-2 6-3 19-7 9-5 4-4 5 6 6-7 6-2, 5-8 10 10 5', 9-2' 5-5" 3-6 8-4 7-4 5 4-8 6-7 6-9 5

18 141 141 20-5 14-7 18 18-2 IS-9 19 7 21-8 28-6 28-6 26-3

26-3 35 35 39-7 27 72-4 26-9 26-9 72-5 50-2 9 9-2

9-7 16-8 17 6 17 6 16-7 14 15 4 13-4 13-4 30 20-8 14-3 13 141 181 13-9

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