Biological Journal ofthe Imnean Socirb (1989), 37: 297-310. With 4 figures
Strategies of mass change in breeding birds
J. MORENO*
Department of ~ o o l o g y Box
,
561, S-75122 Uppsala, Sweden
Received 15 Augur! 1988, accepted for publication 19 December 1988
Birds experience strikingly different patterns of mass change during breeding. In some species with
uniparental incubation, the incubating parents (mostly females) lose mass and attain their lowest
point when the chicks hatch (Incubatory mass loss strategy=IML). In species with shared
incubation, or with intense incubation feeding, the incubating parents maintain or increase in body
mass without reducing attentiveness levels (Incubatory mass constancy = I M C ) . In other species,
uniparental incubation with I M C is associated with reduced levels of attentiveness. The
mobilization of fat stores or its preservation are involved in the two strategies. I M L leads to mass
increases after hatching of the young, while the opposite is true for IMC. T h e non-incubating sex in
uniparental species does not experience significant mass changes during breeding. Fasting endurance,
predation risk and mode of development are proposed as the main selective factors determining
strategy. Latitude, climate, diet and food availability interact with the main factors. From a revision
of the literature we can deduce that IML is mainly found among large birds with prerocial
development, while I M C is typical of smaller species with altricial development. Proportional mass
losses arc positively correlated with body mass in IML-species, as well as in precocial species, where
body mass explains more than 70Yb of the variation in proportional mass change. Incubation
periods increase with body mass in uniparental IMC-species, but not in IML-species. I M L is thus
associated to fast embryonic growth in large species. Successful raising of highly-dependent young in
altricial and semialtricial species apparently depends on one of the parents retaining rcscrves until
hatching. Subsequent mass losses may be necessary to maintain the brooding parent through a
period when nestlings require heat, insulation and food. Patterns of mass change are not mere
consequences of reproductive stress but the outcome of adaptive compromises between different
selective factors and constitute an important aspect of the breeding biology and life history of birds.
KEY WORDS: -Birds
endurance
~
- strategy - incubation
mass loss - mass constancy
chick development incubation period - predation.
~
uniparcntal
~
~
lasting
~
CON'I'EN'I'S
.
Introduction .
Thr main strategies
'Ihe selective agents
General discussion .
Acknowlcdgcments
Rrferrncrs
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297
298
302
305
308
308
INTRODUCTION
Patterns of mass change in breeding birds have frequently been viewed as
evidence for the presence or absence of reproductive stress (Nice, 1938; von
*Present addrrss: Musro Nacional de Ciencias Naturales, J . Gutirrrcz Abascal 2, 28006 Madrid, Spain.
0024 4066/89/080297+ 14 $03.00/0
297
0 1989 '1 he
Linnran Society of London
298
J . MORENO
Haartmann, 1954; Winkel & Winkel, 1976; Murphy & Haukioja, 1986). Mass
loss has typically been used as an index for reproductive costs in studies of avian
life histories (Hussell, 1972; Askenmo, 1977; Bryant, 1979; De Steven, 1980; Nur,
1984). Despite evidence that birds can regulate their body mass by
spontaneously reducing energy intake (Sherry, Mrosovsky & Hogan, 1980;
Mrosovsky & Sherry, 1980), and the cautions by Freed (1981) and Norberg
(1981) that mass losses contribute to reduce flight costs of hard-working parents
and could be an adaptive response, mass losses are normally considered as
evidence of physiological exertion due to reproductive work-loads (Drent &
Daan, 1980; Yom-Tov & Hilborn, 1981).
The question arises whether we can derive any conclusion regarding
reproductive stress from patterns of mass change at the interspecific level. There
are strikingly different patterns of mass change in breeding birds, which have
rarely been discussed in studies af avian reproduction. These patterns are
characteristic of different taxa and sexes, and can be used to identify different
reproductive strategies. These strategies suggest that mass changes should not be
interpreted as mere indicators of reproductive stress in interspecific or intersexual
comparisons. They are the outcome of adaptive compromises between different
selective pressures, and thus constitute an important aspect of the breeding
biology and life history of birds. Here, I will briefly review the two main
strategies of mass change and some of the selective factors which may have
contributed to their divergence.
THE MAIN STRATEGIES
Figure 1 depicts the two patterns of mass change of breeding females. Gonadal
growth and egg production typically lead to mass increases of 7-30% before
laying (Petersen, 1955; Haukioja, 1969; Dowsett-Lemaire & Collette, 1980;
Jakober & Stauber, 1980; Silverin, 1980; Ricklefs & Hussell, 1984; Wijnandts,
1984; Alonso, 1985; Crick & Fry, 1986). Males at this time can lose mass due to
territorial and courtship activities, which can lead to reversals in the usual sexual
dimorphism in body mass (Nice, 1938; Baldwin & Kendeigh, 1938). Laying is
always associated with a marked drop of mass in females (Fig. 1).
The two strategies (Fig. 1) diverge during the incubation phase. In some
species with uniparental incubation, females lose mass throughout this phase and
attain their lowest point when the chicks hatch. This strategy of incubatory mass
loss ( I M L ) is associated with high levels of attentiveness by females, and is
typical of galliforms and anseriforms and of penguins breeding far from the
feeding areas (Table 1). Carcass analyses have shown that the regression of
female reproductive organs represent only part of lost mass, the rest consisting of
mobilized fat stores and reduction of non-reproductive organs (Breitenbach &
Meyer, 1959; Korschgen, 1977; Krapu, 198 1 ; Drobney, 1982; Tome, 1984).
I M L is associated to the incubating sex, and not to females in particular (Le
Maho, 1977; K i l i s & Byrkjedal, 1984; Schamel & Tracy, 1987).
In some species with uniparental incubation, the male supplies the female with
food (raptors, owls, some passerines). In other species the mates cooperate in
incubating (petrels, gulls, doves, some passerines). Attentiveness in these species
is normally as high as in species with IML, but the incubating parents maintain
or increase in body mass throughout incubation (Riddle & Braucher, 1933;
MASS CHANGE IN BREEDING BIRDS
299
lncubotory
moss loss
111
0
E
Zm
73
0
m
Ew
lncubotory
moss constoncy
loyinq
”?
0
E
V
ZI
m
~
Preloying
~~~
lncubotion
Posthotchlng
Figure I . Schematic representation of the two main strategies of mass change found in breeding
birds.
Fisher, 1967; Jakober & Stauber, 1980; Prince, Ricketts & Thomas, 1981;
Croxall & Ricketts, 1983; Village, 1983; Ricklefs & Hussell, 1984; Wijnandts,
1984; Crick & Fry, 1986). When uniparental incubation is not accompanied by
I M L like in most passerines, incubation constancy decreases to 60--80% of
daylight hours (Skutch, 1962) in association with mass constancy. The strategy
of incubatory mass constancy (IMC) (Fig. 1) is thus the consequence of
cooperation between mates or reduced attentiveness.
Carcass analyses have shown that oviduct, ovaries and follicles are almost fully
atrophied at the end of incubation in some species with I M C (Petersen, 1955;
Silverin 1980; Ricklefs & Hussell, 1984; Jones, 1987a). The regression of
reproductive organs and tissues (around 5% of preincubatory mass) must thus
be compensated by a simultaneous storing of reserves in order to maintain IMC.
That fat stores are conserved or increased during incubation has been observed
in several species with I M C (MacLean in Norton, 1972; Newton, 1972; Morton,
Horstmann & Carey, 1973; Jones & Ward, 1976; Dowsett-Lemaire & Collette,
1980; Ricklefs & Hussell, 1984; Jones, 1987a, b). That I M C is linked to
incubation duties as such and not to sex is shown by cases of mass increases in
males which participate in incubation to some degree (Riddle & Braucher, 1933;
Richdale, 1947; Petersen, 1955; Fogden & Fogden, 1979; Dowsett-Lemaire &
Collete, 1980; Jones, 1987a).
Non-incubating males experience relatively slight fluctuations in mass from
J. MORENO
300
TABLE
1. Masses at the beginning of incubation, proportional mass changes and incubation periods
of different species. Only the sexes participating in incubation for each species are presented.
The mode of development is also presented according to O’Connor (1985) (A = altricial,
SA = semialtricial, SP = Semiprecocial, P = Precocial). Species of the same order are arranged
according to body mass. Only mass losses greater than 5% have been designated as IML
Incubation
mass
(9)
Species
Sex
Emperor penguin
Aptenodytes forsteri
King penguin
Aptenodytes patagonicus
Adelie penguin
Pygoscelis adeliae
Yelloweyed penguin
Megadyptes antipodes
Wandering albatross
Diomedea exulans
Black-browed albatross
Diomedea melanophris
Gray-headed albatross
Diomedea chrysostoma
Laysan albatross
Diomedea immutabilis
Western Canada goose
Branta canadensis rnofitti
Lesser Snow goose
Chen caerulescens
Emperor goose
Chen canagica
Barnacle goose
Branta leucopsis
Eider
Somateria mollisima
Cackling Canada goose
Branta canadensis minima
Brent goose
Branta bernicla
Mallard
Anas platyrrynchos
Ring-necked duck
Aythya collaris
Ruddy duck
Oxyura jamaicensis
Wood duck
Aix sponsa
Bluewinged teal
Anas discors
Sparrowhawk
Accipiter nisus
Kestrel
Falco linnunculus
Blue grouse
Dendragapus obscurus
Ring-necked pheasant
Phasianus colchicus
Red junglefowl
Gallus gallus spadiceus
Oys terca tcher
Haematopus ostralegus
Dotterel
Charadrtus mortnellus
M
34 000
M
16 000
I4 000
450&5000
F
M, F
change
Incubation
period
(d)
- 40
120
oh Mass
Dev.
mode Strategy
_ _ _ ~ SA
IML
Reference
I
- lo--20
53
SA
IML
2
-2G-32
35
SA
IML
3
+4
+8
0
0
0
0
0
43
SA
IMC
4
78
SA
IMC
5
68
SA
IMC
6
72
SA
IMC
6
7
8
F
M
F
M
F
M
F
M
F
F
450&5000
450&5000
10500
9000
4500
3500
4100
3500
3000
2600
4300
-7
+5
- 21
64
30
28
SA
P
IML
IMC
IML
F
2500
- 32
23
P
IML
9
F
2200
-21
25
P
IML
10
F
2000
- 29
20
P
IML
11
F
I900
- 32
26
P
IML
12
F
1400
-21
26
P
IML
13
F
1100
-11
24
P
IML
14
F
I050
-
14
24
P
IML
15
F
670
-
10
26
P
IML
16
F
590
-
18
24
P
IML
17
F
430
-5
30
P
IMC
18
F
330
-4
22
P
IMC
19
F
320
0
33
SA
IMC
20
F
274
0
28
SA
IMC
21
F
950
-
19
35
P
IML
22
F
850
-
19
20
P
IML
23
F
800
20
P
IML
24
M, F
540
30
P
IMC
25
M
100
25
P
IML
26
M
0
- 10--20
0
-7
30 1
MASS CHANGE IN BREEDING BIRDS
'I'ABLE I . (continued )
Species
Red phalaropr
Phalaropus fulicaria
Black guillemot
Cepphus grylle
Ring dove
Streptopella risoria
Long-eared owl
Asio otus
I engmalms owl
Aegolius funereus
Starling
Sturnus vu1,Caris
Wheatear
Oenanthe oenanthe
Song sparrow
Melosptza melodia
Barn swallow
Hirundo rustica
Sand martin
Riparia t-iparia
Pied flycatcher
Ficedula hypolcuca
Marsh warbler
Acrocephalus palustris
House wren
Troflodytes aedon
I
.
Sex
Incubation
mass
(R)
06 Mass
change
Incubation
period
(dl
Dev.
mode
__
Strategy
Reference
~
19
P
IML, I M C
27
30
SP
IMC
28
15
A
IMC
29
+ 14
27
SA
IMC
30
170
0
30
SA
IMC
31
0
-2
0
14
A
IMC
32
F
86
82
28
15
A
IMC
33
F
20
+4
12
A
IMC
34
F
22
0
16
A
IMC
35
M
14
14
14
+3
0
+4
15
A
36,37
14
A
IMC
IMC
IMC
13
13
12
0
+6
-4
13
A
39
16
A
IMC
IMC
IMC
M
55
M
M, F
375
380
300
0
0
+8
F
300
F
M
F
F
F
F
M
F
F
0--
14
IMC
38
40,41
References: I , Le Maho, 1977; 2, Stonehouse, 1960; 3, Sladen, 1958; 4, Richdale, 1947,5, Croxall & Ricketts,
1983; 6, Prince et al., 1981; 7, Fisher, 1967; 8, Aldrich & Raveling, 1983; 9, Ankney & MacInnes, 1978; 10,
Thompson & Raveling, 1987; 1 1 , Lessells et al., 1979; 12, Raveling, 1979; 13, Korschgen, 1977; 14, Ankney,
1984; 15, Krapu, 1981; 16, Hohman, 1986; 17, Tome, 1984; 18, Drobney, 1982; 19, Harris, 1970; 20, Newton,
M a r q u i s & Village, 1983; 21, Village, 1983, 22, Redfield, 1973; 23, Breitenbach & Meyer, 1959; 24, Sherry
el al., 1980; 25, Mercer, 1968; 26, K i l i s & Byrkjedal, 1984; 27, Scharnel & Tracy, 1987; 28, Asbirk, 1979; 29,
Brisbin, 1969; 30, Wijnandts, 1984; 31, Korpimaki, 1981; 32, Ricklefs & Hussell, 1984; 33, Moreno,
1989, 34, Nice, 1938; 35, Jones, 1987b; 36, Petersen, 1955; 37, Jones, 1987a; 38, Askenmo, 1982; 39, DowsettLemaire & Collette, 1980; 40 Freed, 1981; 41, Finke, Milinkovich & 'Thompson, 1987.
prelaying to hatching, and apparently do not accumulate reserves. This is the
case in both I M L (Redfield, 1973; Raveling, 1979; Ankney, 1984; Hohman,
1986) and I M C (Petersen, 1955; Haukioja, 1969; Morton el al., 1973; Silverin,
1981; Ricklefs & Hussell, 1984; Biermann & Sealy, 1985). However, there is
evidence of mass declines by males in species where they provide most of their
incubating mates' food intake (Wijnandts, 1984; Masman, 1986).
The two strategies outlined above lead to corresponding mass changes after
hatching. Parents experiencing I M L interrupt the mass decrease at hatching and
initiate a process of more or less rapid recuperation of part of their losses
(Breitenbach & Meyer, 1959; Redfield, 1973; Korschgen, 1977; Ankney &
MacInnes, 1978; Raveling, 1979). In contrast, hatching coincides in parents
which have undergone I M C with the beginning of more or less marked mass
decreases. Table 2 summarizes some of the most detailed data on mass decreases
after hatching. These mass losses are due mainly to the mobilization of fat stores
(Westerterp & Drent, 1985; Jones, 1987b), as indicated by observations of
almost complete atrophy of reproductive organs and tissues before hatching
J. MORENO
302
TABLE
2. Incubation masses, proportional mass losses during the nestling
period and duration of the nestling period for the two sexes of diffrrrnt
species. For penguins only the guard phase (C) has been considered
Inrubation
mass
Species
~.
Yelloweyed penguin
Megadyptes antipodes
Laysan albatross
Diomedea immutabilis
Sparrowhawk
Accipiter nisus
Kestrel
Falro tinnunculus
Ring dove
Sfrepfopelia risoria
Longearrd owl
Asia O ~ U J
Starling
Sturnus uulgaris
Yellow-rumped cacique
Cactcus cela
Red-backed shrikr
Lanius collurio
White-rrowned sparrow
Zonotrichia leucophys
Wheatear
Oenanthe oenanthe
Bullfinch
Pyrrhula pyrrhula
Song sparrow
Melospiza melodia
Reed bunting
Emberiza schoeniclus
Pied flycatcher
Ftcedula hypoleuca
Marsh warbler
Acrocephalus palustris
Sand martin
Riparia rtparia
House wren
Troglodytes aedon
sex
__
F
M
F, M
F
M
F
M
F, M
F
M
F
M
F
F
M
F
M
F
M
F
M
F,M
(9)
4500
4500
3000
330
I55
275
210
I50
‘lo
Mass
loss
-8
-5
- 24
Nestling
period
(d)
50 ( G )
RCkr.CllCC
I
I65
2
27
3
12
-5
- 12
-6
-8
28
4
20
5
300
270
80
85
72
- 25
22
6
15
7
25
8
32
29
29
30
28
25
25
22
21
-9
-4
13
-8
- 14
0
13
-6
-9
15
9
10
10
15
II
20
12
10
13
12
14
-
14
15
-
II
16
20
17, 18
15
19. 20
F
M
F
M
F
M
F
M
20
20
F
12
M
II
15
13
14
13
14
14
-
0
-7
-5
II
-
-
-
-9
0
20
0
19
-5
-6
0
- 13
0
References: I , Richdale, 1947; 2, Fischer, 1967; 3, Newton ef al., 1983; 4, Village,
1983; 5, Brisbin, 1969; 6, Wijnandts, 1984; 7, Ricklefs & Hussell, 1984; 8,
Robinson, 1986; 9,Jakobcr & Staubrr, 1980; 10, Morton ef a [ . , 1973; 11, Morrno,
1989; 12, Newton, 1966; 13, Nice, 1938; 14, Haukioja, 1969; 15, \Vinkel &
Winkcl, 1976; 16, Dowsett-Lemaire & Collrtte, 1980; 17, Petersrn, 1955; 18.
Jonrs, 1987a; 19, Frecd, 1981; 20, Finke el al., 1987.
(Petersen, 1955; Silverin, 1980; Ricklefs & Hussell, 1984; Jones, 1 9 8 7 4 . Nonincubating males experience much less marked mass changes in IMC-species
(Table 2), and in some cases maintain constant levels in spite of equal sharing of
feeding duties by the mates (Von Haartmann, 1954; Winkel & Winkel, 1976;
Freed, 1981 ; Ricklefs & Hussell, 1984; Wijnandts, 1984; Newton, 1986).
T H E SELECTIVE AGENTS
Three main factors were more or less explicitly proposed by Skutch (1962) to
explain the variation in incubatory constancy: fasting endurance, predation and
MASS CHANGE IN BREEDING BIRDS
303
mode of development. They can also be advanced to explain the different
strategies of mass change in combination with other factors like latitude, climate
and food.
Fasting endurance
Fasting endurance increases with body size (Calder, 1974; Peters, 1983). From
allometric relationships between body mass and egg mass (Rahn, Sotherland &
Paganelli, 1985), egg mass and length of the incubation period (Rahn & Ar,
1974), and body mass and fasting endurance (Peters, 1983), it is evident that
reliance on external food acquisition during incubation must increase with
decreasing body mass (Fig. 2). The equations derived for the thermoneutral state
and 0°C by Peters (1983) underestimate the fasting endurance observed in large
birds, probably because they do not account for increases in fat storage capacity
with body size (Lindstedt & Boyce, 1985). The equations derived by Calder
(1974) for - 1 to -9°C and 2-6°C seem more in accordance with the observed
fasting capacity of birds (Fig. 2) Complete reliance on internal stores throughout
incubation is only possible for very large birds. The smaller the species, the more
important it becomes to maximize the reduced fasting endurance imposed by
body size. Small birds should thus strive to maintain a body reserve throughout
incubation as a buffer for using during periods of reduced food availability, even
if i t implies reduced attentiveness.
I50
Complete reliance on
50 -
25 -
10 I
I
5
10
I
I
50 100
I
I
500 1000
I
I
I
5 0 0 0 10000 50000
Body mass ( g )
Figurr 2. Proportion of incubaticm pt-riod which could bc covcrcd by body rescrvrs in rclation to
body mass. T h e following equations havr been used to calculate the relationships shown: Passrrincs:
egg mass ( g )=0.258 x W""' ( W = b o d y mass in g) (R ahn el al., 1985); Nonpassrrines: cgg mass
(kg)=0.075 x W"m ( W i n kg) (Cabana el al., 1982); Incubation time (days) =54 x (egg mass in
kg)"" ( R a h n & Ar, 1974); Fasting endurance (days) at O"C=6.9x ( W i n kg)"" (I'rters 1983);
Fasting riiduranre at thrrmoneutrality= 10.6 x b""h
(Prtcrs, 1983); Fasting cndurancr at - I
-9"C= 1 2 . 4 W"'"
~
[Calder, 1974); Fasting mdurance at 2-6"C= 15 X W""'
(Caldcr, 1974).
~
304
J . MORENO
Predation
Large birds can defend their nests from predators by their mere presence.
Therefore, it pays for them to incubate continuously (Thompson & Raveling,
1987). The absence of this advantage has released small birds from the need to
maintain constant attentiveness for protective reasons. The defensive capacity of
birds with predatory habits may have led to high incubatory constancy and
selected for stronger sexual size dimorphism in raptors and owls (Andersson &
Norberg, 198 1).
The question is whether the level of constancy is an adaptation to predation
pressure or to risks of thermal exposure. The reduced attentiveness in
uniparental incubators with I M C must imply that nest structure and insulative
properties and/or egg resistance to temperature fluctuations must compensate to
some degree for the longer absence of the parent, if it is not going to result in
lower egg hatchability. Morton & Pereyra (1985) found that embryos of the
Dusky Flycatcher Empidonax oberholseri breeding at high altitudes, frequently
experienced large fluctuations in temperature. They suggested that tolerance of
such oscillations might be a key adaptation of birds breeding in cold regions.
Such an adaptation might have enabled the evolution of intermittent
uniparental incubation from the ancestral biparental pattern (Kendeigh, 1952;
Skutch, 1957). Lill (1979) found very low incubatory constancies in females of
the Superb Lyrebird Menura novaeholliae Latham, protracted embryonic cooling
each day and an incubation period twice as long as predicted from body mass.
This is an example of the adaptation of embryo tolerance to uniparental
incubation in a situation of presumable energy limitation on females (Lill, 1986).
A comparison of egg tolerances to neglect and of the insulative properties of nests
of uniparental IML- and IMC-species would clarify this issue.
Mode of development
In the altricial and semialtricial modes of development, a strenuous phase of
parental care follows hatching of the young, involving intense brooding as well
as feeding duties. The incubating parent is typically the one mainly responsible
for brooding the chicks, which may imply strong conflicts between the different
activities (Moreno, 1987). Precocial chicks in 'non-feeders' (Winkler & Walters,
1983) can find their own food, and precociality in general implies reduced
brooding needs. It is thus more important for parents of altricial and
semialtricial species to maintain body reserves throughout incubation in order to
cope with parental care duties. Without these reserves, the capacity to care for
the young could be significantly reduced. Females of some altricial species desert
the clutch if body mass during incubation drops to levels later attained while
feeding young (Newton, 1986; Jones, 1987b).
Latitude and climate interact with the other factors to determine the mass
change pattern. Male red phalaropes Phalaropus fulicaria L. show I M C at 66"N in
Alaska but experience I M L further north (Schamel & Tracy, 1987). This
difference is related to higher incubatory constancy in the north, probably to
reduce exposure of the clutch in the colder climate. Incubatory constancy
appears tuned to climatic conditions in these small waders, leading to sacrifices
in fasting capacity to ensure efficient incubation. Diet and food availablity
probably also affect the pattern of mass change. Birds depending on hard-tocatch prey and/or living in poor environments should have problems in
MASS CHANGE IN BREEDING BIRDS
305
maintaining I M C without cooperation between mates or reduced levels of
attentiveness. Most raptors, owls and seabirds travelling long distances to feed
typically have biparental incubation or considerable incubation feeding by
males (Kendeigh, 1952).
GENERAL DISCUSSION
Can we predict mass change strategies in different avian taxa? A glance at
Table 1 allows some preliminary conclusions. First, I M L is mainly found among
large birds (55-34 000 g, mean=4617 g, Table l ) , while I M C is characteristic of
smaller species ( 1 2 10 500 g, mean = 1653 g, Table 1 ) . Second, I M L is mainly
represented among precocial species and I M C among altricial ones (G = 20.52,
d.f.=2, P=0.005, Table 1). Third, a majority of uniparental incubators lose
mass, while most biparental species show constancy (G = 6.90, P= 0.05,
Table 1). Both body size and developmental mode apparently bear some
relationship to mass changes. This conclusion is however confounded by the fact
that precocial birds are generally larger than altricial ones (55 4300gvs.
12-300 g, Table 1).
Skutch (1962) and Afton (1980) presented evidence showing that body size
and incubatory constancy are positively correlated. The regression between logtransformed body mass and proportional I M L is significant for all IML-species
=2.6-6.9 log (mass), P=0.017, r 2=0.26) and highly significant
(change ("lo)
for precocial species (change (yo)=24.4- 13.9 log (mass), P=0.0007, r 2=0.48).
There is also a significant negative correlation between proportional mass
change and mass for semialtricial species (change(%) = 38.9-12.5 log (mass),
P=O.O188, r 2=0.30), mainly due to three specialized Antarctic penguins in the
sample (Table I ) . If we remove from the relationship for precocials the four
points for incubating males (all are waders), body mass of precocial birds
explains more than 70';/, of the variation in proportional mass change (Fig. 3).
Thus, mass loss in precocial species seems to be determined by body-sizedependent fasting endurance.
MOSS(9)
Figurr 3 . Rrlationship betwrrn proportional mass changr during incubation and initial body mass
in prrcocial specks. 'l'hr regrrssion for females is plotted.
J. MORENO
40
log y = 0.89
U
P
+ 0.22
log x
= 0.0003
0
U
0
L
al
a
.0 = IMC
0 =IML
0
10
I
I
1000
I00
10 00
MOSS( g )
Figurr 4. Relationship hetwern length of incubation periods and body mass in uniparrntally
incubating IML- and IMC-sprcirs. 'I'hr rrgrrssion for IMC-sprcirs is shown. 'l'hr rcgrrssion for
IML-species was not significant.
T h e increase in proportional mass losses with body size i n IML-species may
bear some relationship to the lack of a positive relationship between length of
incubation periods and body mass found (Fig.4). As would be expected from
general allometric relationships (Peters, 1983), there is such a relationship for
uniparental IMC-species (Fig. 4 ) . Large proportional mass losses are apparently
associated with faster embryonic growth in IML-species. Reducing the length of
incubation periods appears to be one of the main advantages of the I M L strategy. If I M L contributes to speeding u p embryonic growth, with its
consequences of reduced predation exposure of the clutch and earlier hatching, i t
should be advantageous for all large birds capable of losing mass without risking
failure. In some large raptors and owls, mass losses of incubating females are
normally postponed until hatching of the chicks by intensive male feeding
(Newton, 1979). T h e mass levels attained by deserting females during incubation
are not lethal nor d o they lead to desertion when nestlings require most food
(Newton, 1986). Successful parental care appears to be highly dependent on
females keeping their fat stores until hatching of the young (Wi,jnandts, 1984).
What are the consequences for the brooding sex of diminished fat stores at
hatching in altricial and semialtricial species? Lifjeld & Slagsvold (1986) have
shown that female pied flycatchers Ficedula hypoleuca Pallas with large incubation
masses produce fledglings that are both larger and in better condition than light
females. In another study of the same species, experimental clutch enlargements
led to mass losses instead of the normal IMC-pattern (Moreno & Carlson, 1989).
This pattern is apparently finely tuned to the energetic costs of incubation and
resource availability to the females. IML-patterns can also be adjusted to clutch
size. Clutch enlargements in the Dotterel Charadrius morznellus I,. lead to greater
mass losses than normal ( K i l i s & Lofaldli, 1987).
Regarding predation, Skutch ( 1949, 1962) considered constant incubation t o
be advantageous also for small species by reducing the level of activity near the
nest and thus the risk of attracting predators. Also, cryptic females of some small
species on the nest may be less conspicuous than an uncovered clutch (Skutch,
M A S S C H A N C E IN BREEDING BIRDS
307
1957; Westmoreland & Best, 1986). Thus it is not obvious that only large birds
should be constant in order to avoid predation. If predation is the main selective
factor favouring constancy and thus I M L in large species, we should expect
body-mass-independent constancy and IML in predator-free environments.
Higher predation rates would lead to larger effects of body size on incubation
and IML.
The traditional interpretation of posthatching mass losses as expressions of
parental stress (reviewed by Ricklefs, 1974) has been challenged by Freed (1 98 1)
and Norberg (1981). They propose that mass losses are adaptive by permitting
reductions in the energetic costs of flight before the most demanding period of
parental care. T h e timing of mass losses and the lack of relationship between
feeding intensity by both parents and current mass loss support this notion
(Freed, 1981). An alternative explanation is that females are probably using
their fat stores for self-maintenance in order to have time for brooding and
finding food for nestlings, while males have not accumulated reserves previously
and are not restricted in their use of time by brooding duties. Why is i t only
females that use body reserves after hatching of the chicks? The answer resides
probably in the accumulation of reserves prior to laying. Once reserve
accumulation has been initiated for the purpose of egg production, it may be
advantageous to maintain stores for later use. Males which have become
liberated from the presumably ancestral condition of joint incubation
(Kendeigh, 1952; Skutch, 1957), need to be lean to minimize flight costs
(Pennycuick, 1975; Norberg, 1981; Lima, 1986). In species where males
incubate and brood, we should expect fat storage also by males, which seems to
be the case in some species (Riddle & Braucher, 1933; Petersen, 1955; Fogden &
Fogden, 1979; Dowsett-Lemaire & Collette, 1980; Jones, 1987a).
To conclude, the advanced developmental state of the chicks at hatching in
precocial species is proposed as having allowed a strategy of speeding up
embryonic growth by continuous attendance of the clutch with the consequent
mass losses. This strategy has been followed to different degrees, depending on
the body mass and thus the fasting endurance of the incubating parents. In
nidicolous birds, the necessity by one of the parents of maintaining reserves for
the period when young require heat, food and protection in the nest, has led to
shared incubation, intense incubation feeding by mates or reduced attentiveness
in uniparental species. T h e loss of these reserves after hatching is not evidence of
stress in these species, but the expected use for which they were preserved
throughout incubation. However, mass loss may exceed the normal range in
some individuals due to specially unfavourable conditions or experimental
manipulations (Westerterp, Gortmaker & Wijngaarden, 1982; Nur, 1984). Only
these excesses should be considered as true indicators of nutritional stress. Body
size, mode of development, predation pressure, climate, diet and food
availability probably interact to determine the exact pattern of mass changes
observed in males and females of different species. T h e importance of the
different factors can be ascertained by controlled field experiments and
interspecific or intersexual comparisons. Patterns of mass change should not be
interpreted as simple consequences of reproductive stress, but as the outcome of
adaptive compromises between an array of selective pressures.
Their study can contribute to a better understanding of the selective factors
which have shaped avian reproductive strategies.
308
J MORENO
ACKNOLYLEDGEMEN'I S
A. Carlson, A. Lundberg, A. P. Moller, S . G. Nilsson, J. N. M . Smith and S .
Ulfstrand read and made helpful comments on earlier versions of thc
manuscript. I have been supported financially by a grant from the Swedish
Natural Sciences Research Council.
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