The Relationship between Body Weight, Egg Weight, Incubation ...

The Relationship between Body Weight, Egg Weight, Incubation Period, Nestling Period and Nest Site in the Psittaciformes, Falconiformes, Strigiformes and Columbiformes D.A. saundersA, G. T. smithA and N A. campbellB A

Division of Wildlife and Rangelands Research, CSIRO, Locked Bag No. 4, P.O. Midland, W.A. 6056. Division of Mathematics and Statistics, CSIRO, Private Bag, P.O., Wembley, W.A. 6014.

Abstract The theory that landbirds which nest in holes tend to have larger clutches, longer incubation periods and longer nestling periods than those which nest in the open was tested by comparing the Psittaciformes, Columbiformes, Falconiformes and Strigiformes. It was found that among the graminivore-frugivores, the hole-nesting Psittaciformes produce larger clutches, have longer incubation and nestling periods than the open-nesting Columbiformes. Among the carnivore-insectivores, the Strigiformes (which predominantly nest in holes) produce larger clutches and have longer nestling periods than the open-nesting Falconiformes but there is no difference in incubation periods.

Introduction Lack (1968) pointed out that, in the Passeriformes, clutch size and number ofyoung that a pair can feed in a brood depend in part on their growth rate, as the same quantity offood per day may be used to raise a small brood quickly or a larger brood more slowly. He showed that hole-nesting passerine species tend to have larger clutches and longer fledgling periods than those species which do not nest in hollows (here referred to as open-nesters). He suggested that for open-nesting species the higher rate of predation conferred a relatively greater advantage on more rapid growth, and maintained that the same trend, but less well established, may be found in the other nidicolous land birds. He concluded (p. 197) that 'most non-passerine nidicolous land birds nest in holes, and those which do so tend to have larger clutches, longer incubation periods and longer fledging periods than those with accessible nests concealed in vegetation'. Since Lack published these ideas a number of studies have been conducted on holenesting non-passerines, the Psittaciformes in particular receiving considerable attention in Australia. In order to test Lack's theories, we collected data on female body weight, egg weight, clutch size, incubation period and nestling period for as many of the Australian parrots as possible. These were compared with data from three other orders of nonpasserines, which were selected for their overlapping ranges in female body weight and differences in diet and nest site, and come from other geographical regions as well as the Australasian region (Table 1). The Australian Psittaciformes are, with one exception, all hole-nesters (the ground parrot Pezoporus wallicus nests on the ground, but under cover) and all are either graminivorous or frugivorous. The Columbiformes were selected to represent open-nesters that are also graminivores-frugivores. The Falconiformes represent opennesting carnivores-insectivores, and the Strigiformes, with a similar diet to the Falconiformes, predominantly nest in holes.

D. A. Saunders, G. T. Smith and N. A. Campbell

Methods Data on body weight, clutch size, incubation period and nestling period were obtained from a number of sources. Egg weights were calculated from egg dimensions by the method ofHoyt (1979). The data used in the following analyses are shown in Table 1, as are the sources of the data. Standard analysis of covariance technique was used to compare the relevant characteristics of the four orders on the (natural) logarithm-logarithm scale. The orders were also partitioned according to food (carnivore-insectivore versus graminivore-frugivore). Within orders it was not possible to partition according to nest site because samples were small (Psittaciformes, one open-nesting species compared with 53 hole-nesting species; Columbiformes, one hole-nesting species compared with 15 open-nesting species; Falconiformes, six hole-nesting species compared with 51 open-nesting species; Strigiformes, five open-nesting species compared with 14 hole-nesting species). To be considered, each species of an order required data for body weight, egg weight, incubation period, nestling period and clutch size. The number of data sets examined were: Psittaciformes 54; Columbiformes 16; Falconiformes 57; Strigiformes 19. The word significant is used throughout the paper in the statistical sense and is applied at the level of 5% or less.

Results Relationship between Egg Weight and Body Weight As found by Rahn et al. (19 7 9 , there is a significant linear relationship between In egg weight, in grams, and In body weight, in grams, within each ofthe four orders examined. The Falconiformes and Strigiformes (carnivore-insectivores) share a common slope of 0.65 (SE0.02), which is significantly less than that shared by the Psittaciformes and Columbiformes (graminivore-frugivores) of 0.74 (SE 0.02). Within both of these groupings the position of the regression lines is significantly different, which means that, over the range of body weights within the four orders, there are large differences in the weight ofeggs produced by the different orders for any given body weight. The positions ofthe regressions, expressed as a mean value adjusted to a common weight (here referred to as an adjusted mean), are: Columbiformes 2.12 (SE0.04); Psittaciformes 2.23 (SE0.02); Strigiformes, 3.74 (SE0.04); Falconiformes 3 - 9 5 (SE 0.02) (Fig. la). For any given body weight, the Columbiformes produce the lightest eggs and the Falconiformes the heaviest. For example, a bird of 400 g produces an egg of 17.8 g in the Columbiformes, 19.9 g in the Psittaciformes (1.1 times the egg of Columbiformes), 25.7 g in the Strigiformes (1.4 times) and 3 1 . 7 g in the Falconiformes (1 .8 times). The only difference possibly related in part to nest type is that among the carnivoresinsectivores, where the open-nesting order produces heavier eggs. In the graminivoresfrugivores the difference is small, with the hole-nesting order producing heavier eggs. Rahn et al. (1975) examined the relationship between egg weight and body weight, their data including the four orders studied here. From their results, a bird of 400 g produces an egg of 19.4 g in the Columbiformes, 17.9 g in the Psittaciformes (0.9 times the egg of the Columbiformes), 26.6 gin the Strigiformes (1 . 4 times) and 32.9 gin the Falconiformes (1 . 7 times). Our results are similar to theirs, although they found that the Columbiformes produce slightly heavier eggs than the Psittaciformes. Relationship between Incubation Period and Body Weight Here again there is a significant linear relationship between In incubation period (days) and In body weight within each order, without any significant difference in the slope of the regression lines. The common slope is 0.14 (SE0 . 0 1). There are, however, differences in the position of the regression lines. Falconiformes and Strigiformes share the same line (adjusted mean 3.42, SE 0 . 0 1) but the Psittaciformes (adjusted mean 3 . 2 1, SE 0.02) and the Columbiformes (adjusted mean 2.87, SE 0.03), do not (Fig. lb). The Columbiformes have the shortest incubation periods for any given body weight. Thus a species of 400 g would

Nest Site Relationships in Birds

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Fig. 1. Relationship between body weight and: ( a ) egg weight; (b) incubation period; (c) nestling period. Psittaciformes. A A . . . . . Falconiformes Strigiformes. o - - - Columbiformes. Closed symbols, hole-nesting species; open symbols, open-nesting species.. .-Joint regression line for Falconiformes and Strigiformes. =Regression line of Rahn et a/. (1974).

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Table 1. Data for each species of four orders used in this analysis Region: A, Australian: E, Ethiopian; N.4, Nearctic; NO, Neotropical: 0 , Oriental; P, Palaearctic. Usual clutch size is given as 0 . 5 of an egg when authorities give clutch size as two numbers, e.g. 2-3 becomes 2.5. Data from following sources. Psittaciforrnes: Forshaw 1981; Saunders and Smith 1981: Watters 1968; W. Boies, B. Gill, M. Gillarn, R. Green, N. Kolichis. T. Lindsey, J. Long, I. Mason, A. McEvey, J. McKean, S. Parker, I. Rowley, R. Schodde, D. Serventy, G. Smith, G. Storr, D. Vernon. Falconiformes: Newton 1979 (table 18); Brown and Amadon 1968. Strigiformes: Bent 1938; Beruldsen 1980; Dement'ev et al. 1966; Hall 1974: Harrison 1975, 1978; Roberts 1971; Schodde and Mason 1980; Schonwetter 1967; CSIRO National Collection. Columbiformes: Beruldsen 1980; Dement'ev et a/. 1968; Goodwin 1967; Hall 1974; Harrison 1975, 1978; Readers' Digest 1976; Schonwetter 1967; Serventy and Whittell 1976; CSIRO National Collection Species

Region

Body wt (g)

Egg wt (g)

Incubn period (days)

Nestl. period (days)

,Usual clutch size

Nest site

Psittaciformes

Probosciger aterrimus Calyptorhynchus m. magn$cus C. m , samueli C. m . graptogyne C, lathami C. funereus funereus C. f: xanthanotus C. f: latirostris Callocephalon jmbriatum Cacatua r, rose~apilla C. r, kuhli C. r. assimilis C. pastinator pastinator C. p. gymnopis C. galerita galerita Glossopsitta porphyrocephala G. pusilla Alisterus scapularis Aprosmictus erythropterus Polytelis swainsonii P. anthopeplus Nymphicus hollandicus Pezoporus wallicus Melopsittacus undulatus Lathamus discolor Purpurercephalus spurius Platycercus caledonicus P. elegans elegans P, e. adelaidae P. e. jlaveolus P. eximius eximius P. e. cecilae P. e. diemenensis P. adscitus P, venustus P, icterotis icterotis P. i. xanthogenys Barnardius z. zonarius B, z. semrtorquatus B. z. barnardi Psephotus haematonotus P. varius varius P. v. orientalis P. chrysopterygius

Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole &oundA under cover Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole


Table 1. (contrnued) Region

Body wt (9)

Egg wt (g)

Northiella h. haematogaster N. h. haematorrhous N. h. narethae Neophema bourkii N. chrystoma N. elegans IYpetrophila N. chrysogaster N pulchella N splendida



Usual clutch size

Nest site

Hole Hole Hole Hole Hole Hole Hole Hole Hole Hole Falconiformes

Cathartes aura Coragyps atratus Gymnogyps californianus Pandion haliaetus Pernis apivorus Elanoides forjicatus Elanus leucurus E. caeruleus Ictinia misisippiensis Milvus migrans M. milvus Haliaeetus leucoryphus H. leucocephalus H. albicdla Neophron percnopterus Gypaetus barbatus Gyps fulvus Torgos tracheliotus Aegypius monachus Circaetus gallicus Circus aeruginosus C. cyaneus C. macrourus c . PYgargus C. melanoleucos Accipiter gentilis A. badius A, cooperii Buteogallus anthracinus Parabuteo unicinctus Buteo nitidus B. lineatus B. platypterus B. swainsonii B. jamaicensis B. buteo B. lagopus B. rufinus B. regalis Aquila pomarina A. clanga A. rapax A, heliaca A. chrysaetos Hieraaetus fasciatus Polyborus plancus Falco naumanni

Hole Hole Hole Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Open Hole


Table 1. (continued) Species

Region

Body wt (g)

Egg wt

(g)


Usual clutch size

Nest site Hole Hole/Open Open Open Open Open Open Open Open Open

F. sparverius F. tinnunculus F. vespertinus F. chicquera F. columbarius F. subbuteo F. biarmicus F. mexicanus F. rusticolus F. peregrinus

Tyto alba


Strigiformes 363 22.2

T. novaehollandiae T, tenebricosa 7. capensis Otus scops Bubo bubo Nyctea scandiaca Surnia ulula Glaucidium passerinum Ninox strenua N. connivens N. novaeseelandiae N. rufa Athene noctua Strix aluco S. uralensis Asio otus A. jlammeus Aegolius funereus

Hole Hole Hole Open Hole Open Open Hole Hole Hole Hole Hole Hole Hole Hole Hole Open Open Hole

Columbiformes

Chalcophaps indica Columba arquatrix C. guinea C. livia C. oenas C palumbus Geopelia cuneaza Goura cristata Oena capensis Phaps elegans Ptilinopus coronulazus P, insolitus Streptopelia capicola S. senegalensis S. turtur Zenaida asiatica

Open Open Open Open Hole Open Open Open Open Open Open Open Open Open Open Open

have an incubation period of about 18 days in the Columbiformes, 25 days in the Psittaciformes (1.4 times that of Columbiformes) and 31 days in the Falconiformes and Strigiformes (1 . 7 times). Within the carnivore-insectivores there is no pattern associated with nest type, but in the graminivore-frugivores, the hole-nesting Psittaciformes have longer incubation periods than the open-nesting Columbiformes (Fig. 1b).


Relationship between Incubation Period and Egg Weight The relationship between In incubation period and In egg weight also shows a significant linear relationship within each order, and all four have the same slope of 0 . 21 (SE0 . 0 1). The Falconiformes and Strigiformes have a common regression line which gives significantly longer incubation periods for any given weight of egg than in the Psittaciformes. They, in turn, have significantly longer incubation periods than the Columbiformes. Our value of the common slope of the regression lines (0.21) is comparable with that calculated by Rahn and Ar (1974) (0.22, SE 0.09) for 475 species of bird of a number of orders.

Relationship between Nestling Period from Hatching to Leaving the Nest) and Body Weight There is a significant linear relationship between In nestling period (days) and In body weight in each of the four orders, without any significant difference in the slope of the regression lines. The common slope is 0 . 3 2 (SE0.02). There are, however, significant differences in the positions of the regression lines, that ofthe Psittaciformes (adjusted mean 4.03, SE 0.04) being significantly higher than that shared by the Falconiformes and Strigiformes (adjusted mean 3.55, SE 0.03) which is, again, significantly higher than that of the Columbiformes (adjusted mean 3.18, SE 0.06) (Fig. lc). The shortest nestling periods are in the Columbiformes, where a species of 400 g has an average nestling period of about 25 days compared with 36 days for the Falconiformes and Strigiformes (1.4 times that of Columbiformes) and 58 days for the Psittaciformes (2.3 times). Within the carnivore-insectivores there is no apparent difference in nestling period, but the data from the Strigiformes are much more widely scattered than those from the other orders. In the Falconiformes, the young remain in the nest until they are able to fly well and are almost fully grown. Although many species of Strigiformes nest in holes, the young often leave the nest before they are fully grown and sometimes before they are able to fly. While actual time in the nest is being compared, the fact that the nestlings leave at different physiological stages in development clouds this issue. However, three species of Strigiformes do have nestling periods similar to those of an equivalent weight of Psittaciformes (Table 1; Fig. lc): Tyto alba, T. novaehollandiae and T. tenebricosa (Schodde and Mason 1980). All remain in the nest hollow until the nestlings are almost fully grown and are able to fly strongly. If there were more complete data for the Strigiformes they might show that the Strigiformes take longer to fledge than the Falconiformes.

Relationship between Clutch Size and Body Weight Despite the large variations in the number of eggs in the clutches of some species, particularly the Strigiformes [e.g. the Snowy Owl Nyctea scandiaca may lay anything from 4 to 10 eggs depending on season (Harrison 1975)], there is an inverse relationship between usual clutch size and body weight in the Psittaciformes, Falconiformes and Strigiformes. The Columbiformes have been excluded from this analysis because they are determinate layers producing either one or two eggs. In general, the Strigiformes produce more eggs for a given body weight than do the Falconiformes which, in turn, produce more than the Psittaciformes. Within these three orders, the larger the species, the smaller the clutch size.

Discussion That there is a connection between egg weight and body weight has been known for some time, Rahn et al. (1975) presenting the most recent review from 809 species in 17 orders. Our results for the four orders that we examined are essentially the same as theirs (Table l), each order having a regression line which differs from those of the others. Our data confirm that the relationship is definable mathematically and, therefore, either egg weight or body weight


may be used to compare the incubation and nestling periods between the four orders. We consider that body weight is more suitable for this purpose, because it is a convenient index of the size of the adult which carries out the incubation and brooding. The relationship between incubation period and body weight is the same for the two orders of carnivore-insectivores, and appears to be unaffected by nest type. Within the graminivore-frugivores, there are quite marked differences (Fig. lb), the hole-nesting Psittaciformes having longer incubation periods than the open-nesting Columbiformes. Rahn et al. (1975) produced an equation for the relationship between incubation periods and body weight, based on data from 475 species of a number of orders. This relationship is shown in Fig. 1band is little different from that within the Psittaciformes. This suggests that the Psittaciformes have probably had little pressure to alter the length of incubation, but the Columbiformes, with their more vulnerable nest sites, have probably evolved very much shorter incubation periods. The carnivore-insectivores produce larger clutches for any given body weight than the graminivore-frugivores. This may be influenced in part by diet, the former group being able to take advantage quickly of an increase in the abundance of prey. Within both dietary groupings, the large clutches are generally produced among the hole-nesting orders and, with the exception of the Columbiformes, the heavier species tend to lay fewer eggs than the lighter species. Within the graminivore-frugivores, nestling periods also show very definite differences between orders (Fig. lc), and these may be related to nest type. The hole-nesting Psittaciformes have very much longer nestling periods for any given body weight than do the Columbiformes. It appears that, as suggested by Lack (1968), the Columbiformes have evolved shorter nestling periods because of their more vulnerable nest sites, and the Psittaciformes have evolved longer nestling periods. Examination of Fig. lc, in which hole-nesting Falconiformes and Strigiformes are distinguished from the open-nesting members of each order, shows that the same may be true in the carnivore-insectivores. Within the Falconiformes, the three largest hole-nesting species have longer nestling periods than similar-sized open-nesting species, yet have incubation periods which are the same (Fig. 1b). The three smallest hole-nesting species have nestling periods which are the same as similar-sized open-nesting species. Within the Strigiformes, the only three species which nest in holes and retain the nestlings in the hollow until they are able to fly strongly, all have nestling periods much longer than equivalent-sized species which nest in the open, or which nest in holes with the young leaving before they are able to fly well. This indicates that, within these two orders, some of the species nesting in holes may have evolved longer nestling periods than those which nest in the open. Acknowledgments

Data were obtained from many sources and these are noted in the caption to Table 1. TO all of these people we are extremely grateful. The figure was drawn by Mr C. P. de Rebeira (Division of Wildlife and Rangelands Research, CSIRO) and an earlier draft of the manuscript was constructively criticised by Mr I. Rowley (Division of Wildlife and Rangelands Research, CSIRO). References Bent, A. C. (1932). Life histories of North American gallinaecous birds. U.S. Natl Mus. Bull. No. 162. Bent, A. C. (1938). Life histories of North American birds: birds of prey. Pt. 2. U.S. Natl Mus. Bull. No.. 170. Beruldsen, G . (1980). 'A Field Guide to Nests and Eggs of Australian Birds.' (Rigby: Adelaide.) Brown, L., and Amadon, D. (1968). 'Eagles, Hawks and Falcons of the World.' (Country Life Books, Hamlyn Publishing Group Ltd: Middlesex, England.)


Dement'ev, G. P., Gladkov, N. A., Ptushenko, E. S., Spangenberg, E. P., and Sudilovskaya, A.M. (1966). 'Birds of the Soviet Union.' Vol. 1. [Israel Program for Scientific Translations: Jerusalem.] Dement'ev, G. P., Meklenburtsev, R. N., Sudilovskaya, A. M., and Spangenberg,E. P. (1968). 'Birds of the Soviet Union.' Vol. 2. [Israel Program for Scientific Translations: Jerusalem.] Forshaw, J. M. (1981). 'Australian Parrots.' 2nd (rev.) Ed. (Lansdowne Editions: Melbourne.) Goodwin, D. (1967). 'Pigeons and Doves of the World.' (British Museum (Natural History): London.) Hall, B. P. (1974). 'Birds of the Harold Hall Australian Expeditions (1962-70)' (British Museum (Natural History): London.) Harrison, C. (1975). 'A Field Guide to the Nests, Eggs and Nestlings of European Birds.' (Collins: London.) Harrison, C. (1978). 'A Field Guide to the Nests, Eggs and Nestlings of North American Birds.' (Collins: Glasgow.) H O ~ D. { F. (1979). Practical methods of estimating volume and fresh weight of birds eggs. Auk 96, 73-7. Lack, D. (1968). 'Ecological Adaptations for Breeding in Birds.' (Methuen and Co.: London.) Newton, I. (1979). 'Population Ecology of Raptors.' (T. and A. D. Poyser: Berkhamsted.) Rahn, H., and Ar, A. (1974). The avian egg: incubation time and water loss. Condor 76, 147-52. Rahn, H., Paganelli, C. V., and Ar, A. (1975). Relation of avian egg weight to body weight. Auk 92, 750-65. Readers' Digest (1976). 'Complete Book of Australian Birds.' (Readers' Digest Services Pty Ltd: Suny Hills, N.S.W.) Roberts, A. (1971). 'Birds of South Africa.' 3rd Ed., revised by G. R. McLachlan and R. Liversidge. (John Voelcker Bird Book Fund: Cape Town.) Saunders, D. A., and Smith, G. T. (1981). Egg dimensions and egg weight loss during incubation in five species of cockatoo, and the use of measurements to determine the stage of incubation of birds' eggs. Aust. Wildl. Res. 8, 41 1-19. Schodde, R., and Mason, I. J. (1980). 'Nocturnal Birds of Australia.' (Lansdowne Editions: Melbourne.) Schonwetter, M. (1967). 'Handbuch der Oologie.' Vol. 1. (Akademie-Verlag: Berlin.) Serventy, D. L., and Whittell, H. M. (1976). 'Birds of Western Australia.' 5th Ed. (University ofwestern Australia Press: Perth.) Watters, P. A. (1968). An integrated numerical and orthodox approach to the taxonomy of the order Psittaciformes. Ph.D. Thesis, University of New England, Armidale, N.S.W.

Manuscript received 2 March 1983; accepted 27 June 1983