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Size, organic composition and energy content of north atlantic gannet Morus bassanus eggs
SIZE, ORGANIC COMPOSITION AND ENERGY CONTENT OF NORTH ATLANTIC GANNET MORUS BASSANUS EGGS ROBERT E. RICKLEFS Department of Biology, University of Pennsylvania, Philadelphia. PA 19104, U.S.A. and WILLIAM A. MON~EVECCH~ Department of Psychology, Memorial University of Newfoundland, Newfoundland (Received
AlC
St. Johns,
5S7, Canada
22 Notiember
1979)
1. Eggs averaged 3.6”/, adult weight. Percentage of yolk (15.5:,), lipid level of the dry matter of the yolk and albumen (25.8”;), and energy content (0.897 kcal.g-‘) are the smallest yet recorded for any avian egg. 2. Albumen, water. and nonlipid dry matter increased in direct proportion to egg weight. Yolk size and lipid content were independent of egg size. Egg size was more strongly correlated with water content than with any other component. 3. Gannet eggs resemble those of other altricial species, having low lipid and high water levels. The energy content of the egg is bery small compared to adult metabolic rate. which suggests that gannets invest little in egg production.
Abstract-
INTRODUCTION North Atlantic gannets Morus hassnntrs (Sulidae: Pelecaniformes) are large, pelagic seabirds. They lay a single, small egg and feed the chick, primarily on fish, until it is fully grown. Compared to many other birds, the gannet allocates little of its reproductive investment to egg production (Nelson. 1978). Here we report the size. chemical composition, and energy content of gannet eggs collected in Newfoundland. The chemical composition of bird eggs have been analyzed in detail primarily for gallinaceous species and waterfowl (Romanoff & Romanoff, 1949). Except for the brown pelican Prlecrrnusoccidentalis (Lawrence & Schreiber. 1974), mourning dove Zenaidu t~~mmuu, and starling Sturnus dgaris (Ricklefs, 1977). the composition of the eggs of altricial species has not been studied beyond determining energy content. Ricklefs (1977) has shown that the eggs of precocial species have larger yolks with a greater concentration of lipid and protein than those of altricial species. The differences between precocial and altricial species derive from the stage of development of the neonate. Patterns of variation within each group will not be fully understood until the eggs of more species having diverse reproductive patterns have been analyzed. The present study offers a contribution toward this end. METHODS
AND
MATERIALS
In May and June 1977. 32 eggs in the gannetry on Baccalieu Island (48 ‘07’N, 52 47’W). Newfoundland. were measured (dial calipers) and weighed (Pesola scale, 2 g gradations). Ten of these eggs, collected between 24 and 31 May, were hard boiled for about lOmin, then frozen. One egg cracked on boiling, but its weight did not change. Two of the remaining eggs gained 3-4 g and one lost 3 g during boiling: weights of the other eggs were unaffected. Frozen eggs were shipped by air freight to Philadelphia, and were
analyzed by RER. The intervals between dates of collection and replacement of eggs at the same nests were recorded. Shell. albumen, and yolk were analyzed separately. Owing to freezing. several of the eggs cracked and lost a variable amount of albumen (up to 35 g). The total weight of albumen was calculated by subtracting the weights of.the shell and yolk from the fresh egg weight. The percent of water in the albumen of each egg was not related to the amount of albumen lost. It proved difficult to remove all the albumen from the inside of the shell. As a result. much of the water in the shell component (2-4g) may have derived from adhered albumen. Consequently, the weight of albumen may have been under-estimated by a similar amount. perhaps Z-4”,, of fresh egg weight. Samples were air-dried at 65 C for 4X hr. Lipids were extracted from yolks for at least 6 hr in each of three fresh baths of a 5: I mixture of petroleum ether and chloroform. The dried albumen and extracted yolks of all eggs were combined. and four aliquots of yolk and two of albumen were combusted in a muffle furnace at 500 C for 6 hr to determine ash content. The ash was dissolved in weak HCI. filtered to remove carbon residues. and run through an atomic absorption spectrophotometer to determine concentrations of several cations. This analysis was done by the Limnology Department at the Academy of Natural Sciences of Philadelphia. Energy equivalents of egg components here calculated using the following conversion equivalents: 9.0 kcal ‘g 1 lipid and 5.5 kcal,g-’ ash-free nonlipid dry matter (Ricklefs. 1974).
RESULTS Eyy size. Eggs in our sample from Newfoundland (Table 1) were slightly larger on average than those of gannet populations in the eastern North Atlantic (100 British eggs, 78.06 x 49.1; Nelson, 1978). The ratio of average fresh egg weight to average adult body weight (3150g rt: 324 SD, n = 8) was 3.6x, which is similar to the ratio of 3.4% found in Great Britain. Fresh egg weights varied between 86.5 and
Table
I. Si7e of North
Atlantic
126 g (cl’. range
gannet eggs
egg Characterlrtic
!1
Table
x ri_ SD
2. Sire. chemical
Coetticlent of variation
composition
weight
(104.5 bet.
of British
birds.
Xl
to 130g). Alerap
that
01‘ samples
g. II = 391) and from
Hona\enture
in
exceeded
the
and energy content
Gulf
of
St
Lawrence
from
Britain
Island.
i 103.2 g:
Quc-
Pot111n.
of .Vf~~ru.\ h~r\.xrrur,segg5
A~eragc __ I. 2. 3. 4. 5. 6. 7. X. 9. IO.
I I. 12. 13. 14. IS 16. Il. IX. 19. 20. 71. 22. 23. 74. 2.5 76. 27. 2X. 7Y. 30 ?I. 37. 33. 34. 35. 36. 37. 3X. 39. 40. 41. 42. 43. 44. 4.5 46. 47. 4x.
Length (mm) Width (mm) Fresh weight (g) Shell weight. wet (PI “,, Fresh weight Shell weight, dry (gl “,, Fresh weight Shell weight. Hshed (gl ‘I,, Fresh weight Yolk weight. wet (g) ‘I<,l-‘rcsh weight Water (g) “,, Yolk Lipid (g) I’,, Yolk Non lipid drq (g) I’(, Yolk Ash I”,, non liptd dry)* Ash-free non lipid drq (g) ‘I,, Yolk Lipid (“,, dr!) kcal kcal,g Albumen weight. wet (g) “,, Fresh weight Water (g) “(, Albumen Non lipid dry (gl “(, Albumen Ash I”,, non lIpid dry)** Ash-free non lipId dr! (8) “() Albumen kcal kc&g Yolk lipid,ash-free non lipid dry Yolk.albumen (wet1 Yolk:albumen (dry) Yolk;albumen (kcal) Total lipid kcnl Total ash-free non llpid dr! kcal Total energq (kcal) kcal, g Fresh weight Total ash-free non lipld dry kcal Whole egg uatcr ‘I<, Total Lipid (‘I,, dry)
Measured Meahurcd Measured Meaaurcd (4) (31 Measured (6j.13) Measured (XI (3) Mcasut-ed (IO) (3) Measured (12) (I01 Measured (14) (101 Measured (16):(lOl Mcllsured (16) ~ (IX) (19).(10) (14).[(14 + (1611 14) x 9 -+ (I’)) x 5.5 (22).( IO) (3) ~ (4) ((0) (741(?) (24) x 117) Mcasuretl (241 x 1191 Mea$urcd Measured (2X) ~ (30) (311,(241 (31) x 5.5 (33):(24) (14)‘( 19) (10)‘(14) [(I41 t lIhl].(?X)
(21)(ii) (141 (4) x 9.0 (19) + 1311 _(41) x >.’ (401 + 1431 (431 (3) (41) (431 4 h+ I2 t 26 46 3 14,(14 + I6 i 2X)
Xl.630 49.705 I 17.700 14.273 0.12 I I I.321 0.096 9.771 0.0x2 IX.IX9 0. I55 IO 717 0.5XX 4.446 0.247 2.972 0.164 0.054 ?.XI I 0.155 0.599 55.4X? 3.083 X5.23X 0.725 75.390 O.XX4 9.x45 0. I I5 0.073 9.25X 0. IO7 50.195 0.5x9 I .59x 0.2 I5 0.76(l I.1 I5 3.447 40 0?11 ‘. I I.037 65.657 105.679 0.X9 7 0113 x9.1 IX 0.757
0.35x
Sample six ,I = IO, except for the ashed weight of the egg shell for which II - 7. Numbers in parentheses refer to measurements used in calculation. For example. weight of the shell divided by the fresh weight of the egg. * Average of 4 subsamples with range 4.6 h.O”,,. ** Average ol 2 subsamples. 7.1 and 7.5”,,.
3,Ji: I.315 5.657 0.967 0.009 0.767 0.00X I.141 (I.010 7.730 0.024 2.153 0.07~ 0.4X9 0.031 0.394 O.OI I (1.374 1~.010 0.032 5.530 0.3 I5 6.441 I).034 5 X5 7 O.O(l7 O.Xhh 0
007
__~__ 0.0”) 0.03 0.048 0.067 0.079 0.067 O.OXi 0. I I6 0. I26 0. I49 0. I50 0 I’)‘> 0.063 0. I IO 0.133 0. I32 (1.06X 0. 1.3.; 0.06X 0.054 0.099 0.102 0.075 0.047 0.077 o.GGi 0.0xX 0.065
0.595 0.006 -141X 0.03X
0.064 0.063 o.oxx 0.065
0.215 0.043 0.1 I4 0.167 0.464 4.404 0.x59 4.727 6.219 0.03 1 0.006 J.XX6 0.00‘1 0.027
0.IZ.F 0.19’> 0. I50 II. I so 0. I IO 0.110 0 072 0.072 0.05X 0.035 0 05.1 0.054 O.c)I 2 0.103
(4) (31 is the wet
_
163
Size, organic composition, and energy content of North Atlantic gannet Table 3. Elemental analysis of egg components Element Fe Na
Mn
Zn
CU
0.21 0.04 0.07
0.014 0.009 0.012
0.47 0.07 0.017
Wet weight (rng.g-‘) Yolk,’ Albumenh Chicken yolk’ Chicken albumen’
0.059 0.009 0.045 0.0002
0.004 0.001 0.009 0.0006
0.131 0.002 0.11 0.009
Total (mg) Yolk” Albumen’ Total
0.63 0.68 I.31
0.40 0.11 0.51
1.40 0.16 1.56
Component Dry matter (mg’g-I) Yolk (mean. n = 4) (SD) Albumen (n = 2)
K
Ca
Mg
4.15 1.91 15.3
3.71 0.84 11.8
1.55 0.40 0.26
0.58 0.07 0.54
1.16 1.99 0.70 1.61
1.03 1.54 1.12 1.67
0.432 0.034 1.44 0.12
0.162 0.070 1.28 0.09
4.62 2.55 7.17
1.73 5.29 7.02
12.4 150.0 152.4
11.1 115.7 126.8
,’ Mg.g-’ dry x 0.164. h Mg.g~’ dry x 0.115. ’ From Romanoff & Romanoff (1949). “Mg.g-’ wet x 18.19. c Mg,g-’ wet x 85.24.
same females, as no nest disturbances were noted. The average dimensions of first and second eggs were similar: first eggs, length = 78.97 f 4.66mm, breadth = 49.33 + 1.56mm, shape index = 1.60 + 0.85, weight = 112.06 + 11.54 g; second eggs, length = 80.49 + 3.83 mm, breadth = 49.54 + 1.08 mm, shape index = 1.62 _t 0.85, weight = 114.62 + 6.62 g (all comparisons nonsignificant, Ps > 0.05). The productmoment correlation coefficient between the weights of first and second eggs of each female (r = 0.86, P < 0.01) indicate a characteristic egg size for each female. Relaying intervals at these nests and 2 others averaged 12.6 k 2.27 days (range, 9-17 days). Egg composition. Averages and indices of dispersion for measured and calculated egg parameters are presented in Table 2. Comprising only 15.5% of fresh egg weight, the yolk is at the low end of the range for altricial species (15-30x) and well below the range for precocial species (22-50x, excluding megapodes) (Nice, 1962; Collins & LeCroy, 1972). The level of water in the yolk (59%) is similar to that of other altricial birds (57-66%) but is above the range of precocial species (4350%) (Ricklefs, 1977). The percentage of water in the albumen (88.4%) is within the range for all species (85-90%); there is no systematic relationship between water level and mode of development. Similarly, the percentage of lipid in the dry matter of the yolk (59.9%) lies within the range for all species (5669%). The gannet’s egg resembles those of other altricial species in having a relatively small yolk with a high water content. The lipid level in the dry matter of the albumen and yolk (25.8%) is lower than that reported for any other species (precocial, 39950%; altricial, 3&37%). The ratio of lipid to fresh egg weight (4”,,) is lower than any so far reported, except for the blue-footed booby, Sula nebuxii, which has a similar lipid level (Nelson, 1978). The energy per gram fresh weight of a gannet egg (0.90 kcal.g-‘) is also the lowest yet reported, and the yolk-albumen energy ratio (1.115) is virtually identical to that of
the brown pelican, the only other pelecaniform egg analyzed (Lawrence & Schreiber, 1974). Levels of eight elements in the yolk and albumen are presented in Table 3. Compared to the domestic fowl, the gannet egg has slightly greater concentrations of sodium and much lower concentrations of calcium and magnesium. Because calcium and magnesium are restricted primarily to the yolk in the chicken, and because the gannet’s egg has such a small yolk, the total reserves of these elements for the developing embryo are much smaller in the gannet than in the chicken. This difference presumably reflects the different degrees of development of altricial and precocial neonates. Relationship of egg components to fresh egg weight. Product-moment coefficients of correlation and regression between the logarithm of a component weight and the logarithm of fresh egg weight were calculated to determine allometric relationships among the parts of eggs (Table 4). The weights of the shell and yolk were independent of variation in fresh egg weight. Albumen increased in direct proportion to egg weight (b = 1.36 & 0.30, r = 0.85) but the amount of water in the egg was even more closely related to egg weight (b = 1.12 f 0.08, r = 0.98). Egg size was related to its water content more than to any other component, and it was more highly correlated with total water content than with the separate water contents of either the albumen or the yolk. It appeared, therefore, that the amount of albumen may have been inversely related to the size or water content of the yolk. We found that the amount of water in albumen was significantly negatively correlated with the percentage of water in the yolk and similarly but less strongly correlated with the total weight, water content, and nonlipid dry matter content of the yolk (Table 5). DISCUSSION
A one-egg clutch equal to about 3.6% of adult body weight and having a low energy density constitutes
I64
Dependent Log Log Log Log Log Log Log Log Log
cartable
dry shell (61 yolk (101 albumen (73) ‘I<>albumen (25) albumen hater (26) yolk water (12) water (461 lipid (39) ash-free non lipid dry (41) Numbers in parentheses * P < 0.05, ** P < 0.01
0.0x
1).3X are keyed to components in Table 1: logarithms statistics calculated only for significant
: regresston
a relatively small investment among species of birds (see King, 1973; Ricklefs, 1974. 1977). According to Aschoff & Pohl’s (1970) equation relating standard metabolic rate (SMR) to body weight in nonpasserine birds, the gannet’s SMR (weight = 3150 g) would be about 171 kcal.day-‘. The single egg contains an average of 106 kcal, or 62”” SMR for 1 day. In this study. the minimum interval between egg loss and relaying was 9 days, but even if the yolk were formed in 5 days (11 kcal’day- ‘) and the albumen secreted in one day (50 kcal ,day- ‘) the daily energy cost of forming the egg, including energy metabolized for biosynthesis, probably would not exceed 50”,, SMR. For comparison, daily costs of egg formation calculated by Ricklefs (1974) varied from 394, SMR for hawks and owls, to 45”;, SMR for passerines (altricials), 1267, SMR for galliformes, and between 149 and 180”;, SMR for various groups of precocious waterbirds. The egg of the North Atlantic gannet is like those of other altricial species in having high water and low lipid levels. Ricklefs (1977) showed that the differences between the eggs of altricial and precocial birds parallel differences in the composition of chicks, But without more detailed studies. we cannot interpret finer variation among species having similar modes of development. Variation in the size of North Atlantic gannet eggs is accompanied by proportional variation in water and nonlipid dry matter. but not in lipid. Variation in egg size derives primarily from vsariation in amount of albumen secreted. Yolk size bore no relation to Table
Independent Yolk Yolk Yolk Yolk Yolk
5. Correlations
variable
(10) water (121 “,, water (13) non lipid dry (16) lipid (14)
and regresston
fresh egg weight, even though variation in yolk size (2.7g SD. 14.5”, CV) was of similar magnitude to that in albumen (6.4g SD. 7.5”; CV). The weight of the albumen was inversely related to the size and, particularly, the percent of water in the yolk. The origin of this relationship may be either systemic. involving the differential response of developing follicles and the oviduct to physical condition or hormonal status of the female, or local, involving a direct response by the oviduct to the size of yolk. In the starling, egg size is directly related to the size of the oviduct (Ricklefs, 1976). The relationship also may have a genetic basis. It is well known that variation in egg size within a population has a large genetic component (see Marble, 1943). The relationship of egg composition to egg size has been mvcstigated in several species of precocial birds and one altricial species. the starling (see Schreiber & Lawrence, 1976: Ricklefs. 1977; Ricklefs u ul.. 1978: Nisbet, 1978). In precocial species. yolk size tends to vary in direct proportion to egg size and large eggs produce large chicks. although the allocation of materials between the chick and its yolk sac and among lipid. water. and nonlipid dry matter seems to vary from one species to the next. In the starling and gannet. yolk size is independent of egg size. Apparently. for the altricial chick, large size and. perhaps, high water content are more important than increased energy stores at hatching. cl&now/rdgemrnrs- -. G. C‘oombes and helped collect and measure
constants of the relationshtps albumen and othct- components
Correlation coethcient 0.52 ~ 0.50 ~ o.hs* _ 0 47 0.I I
are base 10. relationships
Intercept
I.35 5
Numbers in parentheses arc keyed to components tn Table 2. * P < 0.05: regression \tattstics are calculated only f(>r \tgniticant
between
J. M. Porter
eggs. Dr L M. Tuck thr
amount
of hater
provided tn
Slope 01 regresston
Standard error of slope
~ 102.2
47.0
relattonshtps
Size, organic composition. and energy content of North Atlantic gannet inspiration and encouragement. The Canadian Guard allowed us access to housing facilities on Baccalieu Island, and the light station personnel, E. Blundon, R. Hyde, F. Noonan, P. Rice, C. Riggs and L. Walsh. provided warm hospitality. Arrangements for the elemental analysis were made through Dr S. Friant. Research was supported by grants from the National Research Council of Canada (No. A0687 to WAM) and from the US. National Science Foundation (No. DEB 77 27071 to RER). REFERENCES ASCHOFF J. & POHL H. (1970)
Der Ruheumsatz von Vijgeln als Funktion der Tageszeit und der Korpergrosse. J. Om. Lpz. 111, 3847. COLLINS C. T. & LECROVM. (1972) Analysis of measurements, weights and composition of common and roseate tern eggs. Wilson Bull. 84, 187-192. KING J. R. (1973) Eneraetics of reproduction in birds. In Breeding &olo& ofBirds(Editedby FARNERD. L.). Nat. Acad. Sci.. Washineton. D.C. LAWRENCE J. M. & S&R&R R. W. (1974) Organic material and calories in the eggs of the brown pelecan, PelePhysiol. MA, canus occidentalis. Comp. Biochem. 435-440.
MARBLED. R. (1943) Genetics of egg shape. P&r. 22, 2442.
Sci.
165
NELSONJ. B. (1978) The Sulidae: Gannets and Boobies. Oxford University Press, Oxford. NICE M. M. (1962) Development of behavior in precocial birds. Trans. Linn. Sot. 8, l-211. NSBET I. C. T. (1978) Dependence of fledgling success on egg-size, parental performance and egg-composition among common and roseate terns. Sternn hirundo and S. dougallii. Ibis 120, 207-215. POULINJ. M. (1968) Reproduction du dou de bassan (Stifu bu.~u~n[~)Be Bonaventure (Quebec) (Perspective ecologique). M.Sc. Thesis, Lava1 University, Quebec. RICKLEFSR. E. (1974) The energetics of reproduction in birds. In Auian Energetics (Edited by PAYNIXRR. A., JR). Publ. Nuttall Ornithol. Club, No. 15. RICKLEFSR. E. (1976) The chemical composition of the ovary, oviduct, and follicles of the starling. Auk 93, 184187. RICKLEFSR. E. (1977) Composition of eggs of several bird species. Auk 94, 350-356. RICKLEFSR. E., HAHN D. C. & MONTE~ECCHIW. A. (1978) The relationship between egg size and chick size in the laughing gull and Japanese quail. Auk 95, 135-144. ROMANOFF A. L. & ROMANOFF A. J. (1949) The Auian Egg. Wiley, New York. SCHREIBER R. W. & LAWRENCE J. M. (1976) Organic material and calories in laughing gull eggs. Auk 93, 4652.
AlC
St. Johns,
5S7, Canada
22 Notiember
1979)
1. Eggs averaged 3.6”/, adult weight. Percentage of yolk (15.5:,), lipid level of the dry matter of the yolk and albumen (25.8”;), and energy content (0.897 kcal.g-‘) are the smallest yet recorded for any avian egg. 2. Albumen, water. and nonlipid dry matter increased in direct proportion to egg weight. Yolk size and lipid content were independent of egg size. Egg size was more strongly correlated with water content than with any other component. 3. Gannet eggs resemble those of other altricial species, having low lipid and high water levels. The energy content of the egg is bery small compared to adult metabolic rate. which suggests that gannets invest little in egg production.
Abstract-
INTRODUCTION North Atlantic gannets Morus hassnntrs (Sulidae: Pelecaniformes) are large, pelagic seabirds. They lay a single, small egg and feed the chick, primarily on fish, until it is fully grown. Compared to many other birds, the gannet allocates little of its reproductive investment to egg production (Nelson. 1978). Here we report the size. chemical composition, and energy content of gannet eggs collected in Newfoundland. The chemical composition of bird eggs have been analyzed in detail primarily for gallinaceous species and waterfowl (Romanoff & Romanoff, 1949). Except for the brown pelican Prlecrrnusoccidentalis (Lawrence & Schreiber. 1974), mourning dove Zenaidu t~~mmuu, and starling Sturnus dgaris (Ricklefs, 1977). the composition of the eggs of altricial species has not been studied beyond determining energy content. Ricklefs (1977) has shown that the eggs of precocial species have larger yolks with a greater concentration of lipid and protein than those of altricial species. The differences between precocial and altricial species derive from the stage of development of the neonate. Patterns of variation within each group will not be fully understood until the eggs of more species having diverse reproductive patterns have been analyzed. The present study offers a contribution toward this end. METHODS
AND
MATERIALS
In May and June 1977. 32 eggs in the gannetry on Baccalieu Island (48 ‘07’N, 52 47’W). Newfoundland. were measured (dial calipers) and weighed (Pesola scale, 2 g gradations). Ten of these eggs, collected between 24 and 31 May, were hard boiled for about lOmin, then frozen. One egg cracked on boiling, but its weight did not change. Two of the remaining eggs gained 3-4 g and one lost 3 g during boiling: weights of the other eggs were unaffected. Frozen eggs were shipped by air freight to Philadelphia, and were
analyzed by RER. The intervals between dates of collection and replacement of eggs at the same nests were recorded. Shell. albumen, and yolk were analyzed separately. Owing to freezing. several of the eggs cracked and lost a variable amount of albumen (up to 35 g). The total weight of albumen was calculated by subtracting the weights of.the shell and yolk from the fresh egg weight. The percent of water in the albumen of each egg was not related to the amount of albumen lost. It proved difficult to remove all the albumen from the inside of the shell. As a result. much of the water in the shell component (2-4g) may have derived from adhered albumen. Consequently, the weight of albumen may have been under-estimated by a similar amount. perhaps Z-4”,, of fresh egg weight. Samples were air-dried at 65 C for 4X hr. Lipids were extracted from yolks for at least 6 hr in each of three fresh baths of a 5: I mixture of petroleum ether and chloroform. The dried albumen and extracted yolks of all eggs were combined. and four aliquots of yolk and two of albumen were combusted in a muffle furnace at 500 C for 6 hr to determine ash content. The ash was dissolved in weak HCI. filtered to remove carbon residues. and run through an atomic absorption spectrophotometer to determine concentrations of several cations. This analysis was done by the Limnology Department at the Academy of Natural Sciences of Philadelphia. Energy equivalents of egg components here calculated using the following conversion equivalents: 9.0 kcal ‘g 1 lipid and 5.5 kcal,g-’ ash-free nonlipid dry matter (Ricklefs. 1974).
RESULTS Eyy size. Eggs in our sample from Newfoundland (Table 1) were slightly larger on average than those of gannet populations in the eastern North Atlantic (100 British eggs, 78.06 x 49.1; Nelson, 1978). The ratio of average fresh egg weight to average adult body weight (3150g rt: 324 SD, n = 8) was 3.6x, which is similar to the ratio of 3.4% found in Great Britain. Fresh egg weights varied between 86.5 and
Table
I. Si7e of North
Atlantic
126 g (cl’. range
gannet eggs
egg Characterlrtic
!1
Table
x ri_ SD
2. Sire. chemical
Coetticlent of variation
composition
weight
(104.5 bet.
of British
birds.
Xl
to 130g). Alerap
that
01‘ samples
g. II = 391) and from
Hona\enture
in
exceeded
the
and energy content
Gulf
of
St
Lawrence
from
Britain
Island.
i 103.2 g:
Quc-
Pot111n.
of .Vf~~ru.\ h~r\.xrrur,segg5
A~eragc __ I. 2. 3. 4. 5. 6. 7. X. 9. IO.
I I. 12. 13. 14. IS 16. Il. IX. 19. 20. 71. 22. 23. 74. 2.5 76. 27. 2X. 7Y. 30 ?I. 37. 33. 34. 35. 36. 37. 3X. 39. 40. 41. 42. 43. 44. 4.5 46. 47. 4x.
Length (mm) Width (mm) Fresh weight (g) Shell weight. wet (PI “,, Fresh weight Shell weight, dry (gl “,, Fresh weight Shell weight. Hshed (gl ‘I,, Fresh weight Yolk weight. wet (g) ‘I<,l-‘rcsh weight Water (g) “,, Yolk Lipid (g) I’,, Yolk Non lipid drq (g) I’(, Yolk Ash I”,, non liptd dry)* Ash-free non lipid drq (g) ‘I,, Yolk Lipid (“,, dr!) kcal kcal,g Albumen weight. wet (g) “,, Fresh weight Water (g) “(, Albumen Non lipid dry (gl “(, Albumen Ash I”,, non lIpid dry)** Ash-free non lipId dr! (8) “() Albumen kcal kc&g Yolk lipid,ash-free non lipid dry Yolk.albumen (wet1 Yolk:albumen (dry) Yolk;albumen (kcal) Total lipid kcnl Total ash-free non llpid dr! kcal Total energq (kcal) kcal, g Fresh weight Total ash-free non lipld dry kcal Whole egg uatcr ‘I<, Total Lipid (‘I,, dry)
Measured Meahurcd Measured Meaaurcd (4) (31 Measured (6j.13) Measured (XI (3) Mcasut-ed (IO) (3) Measured (12) (I01 Measured (14) (101 Measured (16):(lOl Mcllsured (16) ~ (IX) (19).(10) (14).[(14 + (1611 14) x 9 -+ (I’)) x 5.5 (22).( IO) (3) ~ (4) ((0) (741(?) (24) x 117) Mcasuretl (241 x 1191 Mea$urcd Measured (2X) ~ (30) (311,(241 (31) x 5.5 (33):(24) (14)‘( 19) (10)‘(14) [(I41 t lIhl].(?X)
(21)(ii) (141 (4) x 9.0 (19) + 1311 _(41) x >.’ (401 + 1431 (431 (3) (41) (431 4 h+ I2 t 26 46 3 14,(14 + I6 i 2X)
Xl.630 49.705 I 17.700 14.273 0.12 I I I.321 0.096 9.771 0.0x2 IX.IX9 0. I55 IO 717 0.5XX 4.446 0.247 2.972 0.164 0.054 ?.XI I 0.155 0.599 55.4X? 3.083 X5.23X 0.725 75.390 O.XX4 9.x45 0. I I5 0.073 9.25X 0. IO7 50.195 0.5x9 I .59x 0.2 I5 0.76(l I.1 I5 3.447 40 0?11 ‘. I I.037 65.657 105.679 0.X9 7 0113 x9.1 IX 0.757
0.35x
Sample six ,I = IO, except for the ashed weight of the egg shell for which II - 7. Numbers in parentheses refer to measurements used in calculation. For example. weight of the shell divided by the fresh weight of the egg. * Average of 4 subsamples with range 4.6 h.O”,,. ** Average ol 2 subsamples. 7.1 and 7.5”,,.
3,Ji: I.315 5.657 0.967 0.009 0.767 0.00X I.141 (I.010 7.730 0.024 2.153 0.07~ 0.4X9 0.031 0.394 O.OI I (1.374 1~.010 0.032 5.530 0.3 I5 6.441 I).034 5 X5 7 O.O(l7 O.Xhh 0
007
__~__ 0.0”) 0.03 0.048 0.067 0.079 0.067 O.OXi 0. I I6 0. I26 0. I49 0. I50 0 I’)‘> 0.063 0. I IO 0.133 0. I32 (1.06X 0. 1.3.; 0.06X 0.054 0.099 0.102 0.075 0.047 0.077 o.GGi 0.0xX 0.065
0.595 0.006 -141X 0.03X
0.064 0.063 o.oxx 0.065
0.215 0.043 0.1 I4 0.167 0.464 4.404 0.x59 4.727 6.219 0.03 1 0.006 J.XX6 0.00‘1 0.027
0.IZ.F 0.19’> 0. I50 II. I so 0. I IO 0.110 0 072 0.072 0.05X 0.035 0 05.1 0.054 O.c)I 2 0.103
(4) (31 is the wet
_
163
Size, organic composition, and energy content of North Atlantic gannet Table 3. Elemental analysis of egg components Element Fe Na
Mn
Zn
CU
0.21 0.04 0.07
0.014 0.009 0.012
0.47 0.07 0.017
Wet weight (rng.g-‘) Yolk,’ Albumenh Chicken yolk’ Chicken albumen’
0.059 0.009 0.045 0.0002
0.004 0.001 0.009 0.0006
0.131 0.002 0.11 0.009
Total (mg) Yolk” Albumen’ Total
0.63 0.68 I.31
0.40 0.11 0.51
1.40 0.16 1.56
Component Dry matter (mg’g-I) Yolk (mean. n = 4) (SD) Albumen (n = 2)
K
Ca
Mg
4.15 1.91 15.3
3.71 0.84 11.8
1.55 0.40 0.26
0.58 0.07 0.54
1.16 1.99 0.70 1.61
1.03 1.54 1.12 1.67
0.432 0.034 1.44 0.12
0.162 0.070 1.28 0.09
4.62 2.55 7.17
1.73 5.29 7.02
12.4 150.0 152.4
11.1 115.7 126.8
,’ Mg.g-’ dry x 0.164. h Mg.g~’ dry x 0.115. ’ From Romanoff & Romanoff (1949). “Mg.g-’ wet x 18.19. c Mg,g-’ wet x 85.24.
same females, as no nest disturbances were noted. The average dimensions of first and second eggs were similar: first eggs, length = 78.97 f 4.66mm, breadth = 49.33 + 1.56mm, shape index = 1.60 + 0.85, weight = 112.06 + 11.54 g; second eggs, length = 80.49 + 3.83 mm, breadth = 49.54 + 1.08 mm, shape index = 1.62 _t 0.85, weight = 114.62 + 6.62 g (all comparisons nonsignificant, Ps > 0.05). The productmoment correlation coefficient between the weights of first and second eggs of each female (r = 0.86, P < 0.01) indicate a characteristic egg size for each female. Relaying intervals at these nests and 2 others averaged 12.6 k 2.27 days (range, 9-17 days). Egg composition. Averages and indices of dispersion for measured and calculated egg parameters are presented in Table 2. Comprising only 15.5% of fresh egg weight, the yolk is at the low end of the range for altricial species (15-30x) and well below the range for precocial species (22-50x, excluding megapodes) (Nice, 1962; Collins & LeCroy, 1972). The level of water in the yolk (59%) is similar to that of other altricial birds (57-66%) but is above the range of precocial species (4350%) (Ricklefs, 1977). The percentage of water in the albumen (88.4%) is within the range for all species (85-90%); there is no systematic relationship between water level and mode of development. Similarly, the percentage of lipid in the dry matter of the yolk (59.9%) lies within the range for all species (5669%). The gannet’s egg resembles those of other altricial species in having a relatively small yolk with a high water content. The lipid level in the dry matter of the albumen and yolk (25.8%) is lower than that reported for any other species (precocial, 39950%; altricial, 3&37%). The ratio of lipid to fresh egg weight (4”,,) is lower than any so far reported, except for the blue-footed booby, Sula nebuxii, which has a similar lipid level (Nelson, 1978). The energy per gram fresh weight of a gannet egg (0.90 kcal.g-‘) is also the lowest yet reported, and the yolk-albumen energy ratio (1.115) is virtually identical to that of
the brown pelican, the only other pelecaniform egg analyzed (Lawrence & Schreiber, 1974). Levels of eight elements in the yolk and albumen are presented in Table 3. Compared to the domestic fowl, the gannet egg has slightly greater concentrations of sodium and much lower concentrations of calcium and magnesium. Because calcium and magnesium are restricted primarily to the yolk in the chicken, and because the gannet’s egg has such a small yolk, the total reserves of these elements for the developing embryo are much smaller in the gannet than in the chicken. This difference presumably reflects the different degrees of development of altricial and precocial neonates. Relationship of egg components to fresh egg weight. Product-moment coefficients of correlation and regression between the logarithm of a component weight and the logarithm of fresh egg weight were calculated to determine allometric relationships among the parts of eggs (Table 4). The weights of the shell and yolk were independent of variation in fresh egg weight. Albumen increased in direct proportion to egg weight (b = 1.36 & 0.30, r = 0.85) but the amount of water in the egg was even more closely related to egg weight (b = 1.12 f 0.08, r = 0.98). Egg size was related to its water content more than to any other component, and it was more highly correlated with total water content than with the separate water contents of either the albumen or the yolk. It appeared, therefore, that the amount of albumen may have been inversely related to the size or water content of the yolk. We found that the amount of water in albumen was significantly negatively correlated with the percentage of water in the yolk and similarly but less strongly correlated with the total weight, water content, and nonlipid dry matter content of the yolk (Table 5). DISCUSSION
A one-egg clutch equal to about 3.6% of adult body weight and having a low energy density constitutes
I64
Dependent Log Log Log Log Log Log Log Log Log
cartable
dry shell (61 yolk (101 albumen (73) ‘I<>albumen (25) albumen hater (26) yolk water (12) water (461 lipid (39) ash-free non lipid dry (41) Numbers in parentheses * P < 0.05, ** P < 0.01
0.0x
1).3X are keyed to components in Table 1: logarithms statistics calculated only for significant
: regresston
a relatively small investment among species of birds (see King, 1973; Ricklefs, 1974. 1977). According to Aschoff & Pohl’s (1970) equation relating standard metabolic rate (SMR) to body weight in nonpasserine birds, the gannet’s SMR (weight = 3150 g) would be about 171 kcal.day-‘. The single egg contains an average of 106 kcal, or 62”” SMR for 1 day. In this study. the minimum interval between egg loss and relaying was 9 days, but even if the yolk were formed in 5 days (11 kcal’day- ‘) and the albumen secreted in one day (50 kcal ,day- ‘) the daily energy cost of forming the egg, including energy metabolized for biosynthesis, probably would not exceed 50”,, SMR. For comparison, daily costs of egg formation calculated by Ricklefs (1974) varied from 394, SMR for hawks and owls, to 45”;, SMR for passerines (altricials), 1267, SMR for galliformes, and between 149 and 180”;, SMR for various groups of precocious waterbirds. The egg of the North Atlantic gannet is like those of other altricial species in having high water and low lipid levels. Ricklefs (1977) showed that the differences between the eggs of altricial and precocial birds parallel differences in the composition of chicks, But without more detailed studies. we cannot interpret finer variation among species having similar modes of development. Variation in the size of North Atlantic gannet eggs is accompanied by proportional variation in water and nonlipid dry matter. but not in lipid. Variation in egg size derives primarily from vsariation in amount of albumen secreted. Yolk size bore no relation to Table
Independent Yolk Yolk Yolk Yolk Yolk
5. Correlations
variable
(10) water (121 “,, water (13) non lipid dry (16) lipid (14)
and regresston
fresh egg weight, even though variation in yolk size (2.7g SD. 14.5”, CV) was of similar magnitude to that in albumen (6.4g SD. 7.5”; CV). The weight of the albumen was inversely related to the size and, particularly, the percent of water in the yolk. The origin of this relationship may be either systemic. involving the differential response of developing follicles and the oviduct to physical condition or hormonal status of the female, or local, involving a direct response by the oviduct to the size of yolk. In the starling, egg size is directly related to the size of the oviduct (Ricklefs, 1976). The relationship also may have a genetic basis. It is well known that variation in egg size within a population has a large genetic component (see Marble, 1943). The relationship of egg composition to egg size has been mvcstigated in several species of precocial birds and one altricial species. the starling (see Schreiber & Lawrence, 1976: Ricklefs. 1977; Ricklefs u ul.. 1978: Nisbet, 1978). In precocial species. yolk size tends to vary in direct proportion to egg size and large eggs produce large chicks. although the allocation of materials between the chick and its yolk sac and among lipid. water. and nonlipid dry matter seems to vary from one species to the next. In the starling and gannet. yolk size is independent of egg size. Apparently. for the altricial chick, large size and. perhaps, high water content are more important than increased energy stores at hatching. cl&now/rdgemrnrs- -. G. C‘oombes and helped collect and measure
constants of the relationshtps albumen and othct- components
Correlation coethcient 0.52 ~ 0.50 ~ o.hs* _ 0 47 0.I I
are base 10. relationships
Intercept
I.35 5
Numbers in parentheses arc keyed to components tn Table 2. * P < 0.05: regression \tattstics are calculated only f(>r \tgniticant
between
J. M. Porter
eggs. Dr L M. Tuck thr
amount
of hater
provided tn
Slope 01 regresston
Standard error of slope
~ 102.2
47.0
relattonshtps
Size, organic composition. and energy content of North Atlantic gannet inspiration and encouragement. The Canadian Guard allowed us access to housing facilities on Baccalieu Island, and the light station personnel, E. Blundon, R. Hyde, F. Noonan, P. Rice, C. Riggs and L. Walsh. provided warm hospitality. Arrangements for the elemental analysis were made through Dr S. Friant. Research was supported by grants from the National Research Council of Canada (No. A0687 to WAM) and from the US. National Science Foundation (No. DEB 77 27071 to RER). REFERENCES ASCHOFF J. & POHL H. (1970)
Der Ruheumsatz von Vijgeln als Funktion der Tageszeit und der Korpergrosse. J. Om. Lpz. 111, 3847. COLLINS C. T. & LECROVM. (1972) Analysis of measurements, weights and composition of common and roseate tern eggs. Wilson Bull. 84, 187-192. KING J. R. (1973) Eneraetics of reproduction in birds. In Breeding &olo& ofBirds(Editedby FARNERD. L.). Nat. Acad. Sci.. Washineton. D.C. LAWRENCE J. M. & S&R&R R. W. (1974) Organic material and calories in the eggs of the brown pelecan, PelePhysiol. MA, canus occidentalis. Comp. Biochem. 435-440.
MARBLED. R. (1943) Genetics of egg shape. P&r. 22, 2442.
Sci.
165
NELSONJ. B. (1978) The Sulidae: Gannets and Boobies. Oxford University Press, Oxford. NICE M. M. (1962) Development of behavior in precocial birds. Trans. Linn. Sot. 8, l-211. NSBET I. C. T. (1978) Dependence of fledgling success on egg-size, parental performance and egg-composition among common and roseate terns. Sternn hirundo and S. dougallii. Ibis 120, 207-215. POULINJ. M. (1968) Reproduction du dou de bassan (Stifu bu.~u~n[~)Be Bonaventure (Quebec) (Perspective ecologique). M.Sc. Thesis, Lava1 University, Quebec. RICKLEFSR. E. (1974) The energetics of reproduction in birds. In Auian Energetics (Edited by PAYNIXRR. A., JR). Publ. Nuttall Ornithol. Club, No. 15. RICKLEFSR. E. (1976) The chemical composition of the ovary, oviduct, and follicles of the starling. Auk 93, 184187. RICKLEFSR. E. (1977) Composition of eggs of several bird species. Auk 94, 350-356. RICKLEFSR. E., HAHN D. C. & MONTE~ECCHIW. A. (1978) The relationship between egg size and chick size in the laughing gull and Japanese quail. Auk 95, 135-144. ROMANOFF A. L. & ROMANOFF A. J. (1949) The Auian Egg. Wiley, New York. SCHREIBER R. W. & LAWRENCE J. M. (1976) Organic material and calories in laughing gull eggs. Auk 93, 4652.