Behavioral Ecology Vol. 8 No. 2: 126-154
The evolution of parental care in shorebirds:
life histories, ecology, and sexual selection
John D. Reynolds* and Tam&s Sz6kelj*
•School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK, and bBehavioural
Ecology Research Group, Department of Zoology, Kossuth University, Debrecen, H-4010, Hungary
Parental care is expected to evolve according to a trade-off between the benefits of increased survival of offspring and costs of
reduced survival and future reproduction of adults. Here we investigate the components of this life-history trade-off in shorebirds
(Charadriides, excluding Laroidea), an avian infraorder displaying an unusual diversity in extent of care by each sex. We show
that evolutionary increases in the duration of care in one sex are associated with decreased care by the other. We found no
evidence that various hypothesised benefits of care provide a general explanation for the duration of care by either or both
sexes, although parental feeding of the young was too conservative for comparisons. Sexual dimorphism in body size had a
similar relationship to parental care in both sexes: reductions in duration of care by either sex were matched by increases in
the size of that sex relative to the other. Whereas this pattern could be explained by sexual selection in males, it was retained
within socially monogamous females. Reduced care in males (but not in females) appears to have facilitated the evolution of
greater migration distances. These results suggest that parental care has had different causes and consequences in each sex.
Benefits of desertion due to sexual selection are more clearly demonstrable for males, whereas correlates of care are less clear
for females. Key words: Aves, body size, Charadrii, desertion, life history, migration, parental care, sexual selection, shorebirds.
[Behav Ecoi 8:126-134 (1997)]
P
arental care, defined as behavior that improves the fitness
of offspring, is a key component of life histories and
breeding systems (Chitton-Brock, 1991; Reynolds, 1996; Roff,
1992). Selection for parental care arises when die benefit of
increased survival of the young exceeds the benefits to the
parent from deserting die brood and breeding again, either
during the same reproductive bout or in subsequent seasons
(Gross and Sargent, 1985; Maynard Smith, 1977; Szekely et
al., 1996). Thus, die trade-off between benefits and costs of
care for the parent can affect adult growth, survival, and sexual selection. It should therefore be possible to understand
selection for parental care and its correlates with other aspects
of animal breeding systems by comparing taxa that differ in
parental care and other components of life history and ecologyShorebirds (infraorder Charadriides, excluding gulls and allies, Laroidea) are ideal for such comparisons. The 203 species of shorebirds such as sandpipers, plovers, jacanas, and
their allies have an unusually high diversity of parental care
and mating behavior (Erckmann, 1983; Oring, 1986; Pitelka
et al., 1974; Szekely and Reynolds, 1995). This diversity occurs
at several taxonomic levels within the infraorder, including
care by both parents or by either the male or die female
alone, all within a single genus. Recent advances in molecular
phytogenies and comparative statistics (Harvey and Pagel,
1991) make it possible to test for ecological and life history
correlates of diis diversity. Previously, we have shown that diversity in care has resulted from several independent evolutionary transitions in die duration of care in either sex, with
a bias toward reductions in die relative care provided by males
in one of die major dades, the Scoloparida, which includes
sandpipers and allies (Szekely and Reynolds, 1995).
In diis study we make evolutionarily independent comparT. Szekely is now at the School of Biological Sciences, University of
Bristol, Woodland Road, Bristol, BS8 1UG, UK
Received 3 August 1995; reviled 28 March 1996; accepted 8 April
1996.
1045-2249/97/J5.00 O 1997 International Society for Behavioral Ecology
isons of aspects of ecology and life histories that may select
for and against parental care in shorebirds. These independent comparisons are used to test hypotheses described in die
following two subsections. These hypotheses were eidler proposed specifically for shorebirds (reviewed in Erckmann,
1983; Jdnsson and Alerstam, 1990; Oring, 1986; Saether et al.,
1986) or have been adapted for shorebirds from general theory for die evolution of parental care (reviewed in CluttonBrock, 1991; Sargent and Gross, 1993).
Benefit! of care
In all shorebirds, at least one parent incubates die eggs and
broods and guards die young (Johnsgard, 1981; Szekely and
Reynolds, 1995). Selection favors biparental care if a single
parent cannot rear die young alone (Lack, 1968; Lazarus,
1990; Maynard Smith, 1977). A parent might help its mate
with incubation and brooding if die clutch mass is large relative to die mate's body size (Erckmann, 1983). It has also
been suggested diat species living in cold environments may
require die attention of both adults to keep die eggs and
young warm (Erckmann, 1983; Pitelka et a]., 1974). Species
living in habitats with high rates of nest predation may also
be selected to have biparental care for two reasons: (1) better
ability to defend die offspring, especially if the adults are large
and thus able to mob die predator (Erckmann, 1983; Larsen,
1991), and (2) better ability to retain the mate for further
breeding attempts in the event of clutch failure (e.g., Emlen
and Oring, 1977; Martin and Cooke, 1987). Bodi of diese
hypotheses have been used to predict that biparental care will
be correlated positively widi rates of nest predation. However,
diis is a weak test for the antipredator function because it
assumes that predation avoidance is not sufficiently effective
to remove correlations among taxa between biparental care
and rates of nest loss.
Benefit! of desertion
Many benefits of brood desertion have been proposed for
shorebirds. Some explanations appear more compelling than
117
Reynolds and Szekely * Shorebird parental care
others, but most make testable predictions about correlations
between desertion and life histories or ecology. Hypotheses
concern either sexual selection or enhanced adult survival.
Sexual selection may favor brood desertion through enhanced opportunities to find a new mate (Maynard Smith,
1977; Oring, 1986; Pitelka et aL, 1974; Szekely and Williams,
1995). This could apply equally well to either sex in shorebirds, as evidenced by reversed courtship roles in species such
as dotterel {Eudromias mormtOus), jacanas, and phalaropes
(Cohvell and Oring, 1988; Jenni, 1974; Owens et aL, 1994;
Reynolds, 1987; Reynolds et aL, 1986). Species that breed at
high densities may be better able to find new mating partners
and hence may benefit more from deserting their offspring.
Sexual selection should also cause sexual dimorphism to be
most pronounced in species with the greatest disparity in parental care by each sex, and the deserting gender should be
larger as a result of selection for ability to compete for mates
(cf. Jdnsson and Alerstam, 1990).
The other potential benefit of brood desertion is enhanced
adult survival (Graul et aL, 1977; Gross and Sargent, 1985;
Owens and Bennett, 1994; Pitelka et al., 1974). Female shorebirds may desert if they lay large eggs or heavy clutches relative to their body size (Ashkenazie and Safriel, 1979). Females
may also desert their offspring if they produce clutches quickly, since body fat is lost during egg laying and often reaches
its lowest point during incubation (Erckmann, 1983; Maclean,
1969). A variation of this theme is that a female may forgo
incubation to replenish her reserves and lay a new clutch in
the event of failure of the first one (Jenni, 1974; Lenington,
1984). The female's emancipation from incubation might
therefore be advantageous to both parents, and uniparental
care should be commonest in species facing high clutch predation (Erckmann, 1983; Lenington, 1984). This is a weak test
because desertion may increase the risk of clutch predation,
rather than vice versa. Note also that this prediction is valid
only for the female, and it makes the opposite (testable) prediction to the mate-retention hypothesis. Finally, it has been
suggested that long-distance migrants of either sex may be
expected to desert in order to recoup their body reserves before leaving their breeding grounds or to obtain early access
to migration stop-over sites and wintering areas (Myers, 1981).
METHODS
Psrentsl care
We scored duration of parental care for each sex according
to how long the parent cared for the offspring (Table 1; Szekely and Reynolds, 1995). Length of incubation and fledging
time were divided into three periods each (scores 1-3 and 46, respectively). If a parent did not incubate, it received a
score of 0, and if it stayed until the chicks fledged, it received
a score of 7. These scores were linearly related to the percentage of development completed (days spent caring for
young divided by duration of incubation plus fledging) in
nine shorebird species for which exaa data on duration of
care by one sex (females) were available: Numenius arquata,
CaUdris pusilla, C mtnutiUa, C aipina, Phalaropus lobatus,
Harnatopus ostraUgus, Charadrius vrilsonia, C alexandrinus,
VtmtBus crassirostris (Pearson correlation, r = .9%, p '<
.0001)..
We investigated potential benefits of care by measuring the
duration of care by each sex separately or for both sexes combined, whereas benefits of desertion were investigated by measuring the duration of care in each sex separately.
Ecology and Efe histories
The raw data and corresponding references are shown in Table 1. Latitudes of breeding and wintering ranges were measured at four outermost locations on distribution maps (east,
north, west, and south), and the mean latitude of these four
measurements gave the mean breeding and wintering ranges,
respectively. We calculated migration distance (in degrees of
latitude) by taking the difference between the mean breeding
and wintering ranges. Clutch mass was based on mean dutch
size multiplied by the weight of fresh eggs. We used straightened wing length as a measure of body size because tarsus
length data were often unavailable. If only minimum and maximum wing length were given, we used the mean value of the
range. For the analyses of total care by both sexes combined,
we included wing measurements from unsexed specimens
(Table 1). Preference was given to wing measurements collected during the breeding season. Hatching success was
taken as the percentage of nests hatching at least one chick.
Egg-laying interval (in days) is the time span between laying
consecutive eggs for a dutch. Breeding density is given as
number of nests/ha. If more than one value was available for
breeding density or if a range of densities was given, we calculated their means. Annual survival rates of adults were estimated either from banding recoveries (n •» 9 spedes) or
from return rates to the breeding grounds (n " 12 spedes).
These estimates diH not differ from each other (Mann-Whitney I/test,z= .89, p> .3). Separate estimates of adult survival
rates for each sex were available for only 9 out of 21 spedes.
Therefore, we used the mean survival of males and females
(n =» 9 spedes) and survival of unsexed individuals (n = 12
spedes). If data from several locations were available, we used
data nearest the geographic range where the data on parental
care were collected.
Companrtre analyso
We used Felsenstein's (1985) test for correlated evolution of
continuous traits, as described by Harvey and Pagel (1991)
and implemented by Purvis and Rambaut (1994). Phylogenetically independent differences ("contrasts") were calculated between pairs of species or higher taxa in extent of parental care. These contrasts were then correlated with contrasts
in aspects of life history or ecology of that sex. Because the
analyses compare differences between taxa, rather than using
each spedes as a separate data point, the contrasts yield data
that are phylogeneticaUy and statistically independent (Harvey and Pagel, 1991). When more than one spedes was available in a genus, we used the spedes pairs having the greatest
difference between duration of care. Branch lengths were set
to unity because lengths are not yet available for many of the
taxa. Contrasts were standardized by dividing each contrast by
its standard deviation (Purvis and Rambaut, 1994).
The phytogeny was compiled from molecular and morphological evidence for die two major clades that encompass the
shorebirds: Scolopadda and Charadriida (Figure 1; see rationale in Szekely and Reynolds, 1995). There is conflicting
evidence about whether shorebirds are paraphyletic (e.g.,
Monroe and Sibley, 1993), but a recent reanahysis of skeletal
data by Bjorkhind (1994) suggests that they may be monophyletic, with the exception of thick-knees (Burhinidae),
which do not appear in our analyses.
Body size may confound relationships between duration of
care, ecology, and life-history variables. For example, evoh> tionary increases in female body size (wing length) were associated with increases in male wing length (r = .980, n ° 4 4
contrasts, p < .0001), clutch mass (r = .90S, n = 44 contrasts,
p < .0001), egg-laying intervals (r •> .399, n = 28 contrasts, p
Behavioral Ecology VoL 8 No. 2
128
Tkbiel
Parental care and ecological and Hfe-history
riablea of aborebinb
Referenced
Specie*
Pterodidae
Pterodtt oruntatis
Thinocoridae
Thmoeona rumxduona
Pedionomidae
Ptdumomus torquatus
Scolopaddae
Scoiopax rusticola
Scolopax manor
GalBnago wttdia
GaOmago gaUmago
Cotnocorjpha aueklandiai
Uwuaa Bmosa
LJmosaftdoa
Numenha arquata
Nummius awurieanus
Tringa rrythrvpus
Tringa stagnatitis
Tringa kypolrucos
Tringa wtacularia
Catoptrophonu srmtpahnatus
Arvnaria mttrprts
Artnaria wuUmoaphala
Ltrnnodrtmus gristus
CaUdris conutus
CaUdris alba
CaUdris pusUla
CaUdris maun
CaUdris rufieoOu
CaUdris mmtttiUa
CaUdris fusdcoOis
CaUdris bairdii
CaUdris wulanotos
CaUdris acuminaXa
CaUdris marittma
CaUdris ahpinn
CaUdris fimtgbua
Micropalama himumlopus
TryngUts subruficoUxs
Phalaropus lobatus
Rostratulidae
Rostmtula btnghaUnsis
Rostmtula sttmcoOaris
Jacanidae
ActophUomis afruanus
Micwparra captnsis
Jacana jacana
Charadriidae
Haematopus ostmUgus
PtuviaHs dominica
Ptuviatis squataroio
Charadrius wilsonia
Charadrius sanctarhtimat
Charadrius aUxandrinus
Eudrowdat morintUxu
Anarhjnchus fivntaSs
VantBus vantOus
WxneBus erassxrostris
EL
Par- Ecology
ental and life
care history
MC
FC
BR
7
7
39
0
0.03
84
237
228
1
1
0
7
26
3
05
32
113
112
2
2,3,4
7
0
S3
0
0.1
36
5
4,6
0
2
0
7
7
7
6
7
7
7
49
41
62
53
53
59
49
56
45
66
54
57
54
40
73
60
56
8
8
61
45
0
37
16
40
IS
45
55
44
47
12
65
20
40
0.4
7
7
7
7
7
7
6
4
3
7
5
0
5
4
7
3
93
66
81
64
47
152
182
296
292
98
56
49
36
158
63
69
72
4
V)
6
7
5
4
4
5
7
4
7
7
3
4
7
4
7
0
76
73
61
67
70
57
69
72
65
71
74
65
72
65
69
66
v\
44
109
95
90
98
13
30
78
64
99
48
7
7
0
7
16
31
2
0
7
7
7
0
7
0
1
1
13
0
0
0
7
7
7
7
7
7
7
7
7
7
7
7
57
66
68
19
16
33
60
44
54
7
19
87
53
8
0
11
27
8
16
0
7
7
7
7
7
7
7
7
7
7
7
6
7
7
7
0
7
0
0
7
6
0
7
0
7
4
2
7
4
0
7
6
7
MD
117
75
59
46
BD
0.09
3.2
0.5
0J
0.16
23
0.008
6.1
14.8
0.03
0.01
0.02
CM
0.4
71
44
28
29
33
25
43
38
52
52
52
42
48
44
52
25
15
50
82
03
0.12
0.125
0.008
0.6
US
1.5
1.0
3.0
1.5
2.0
1.5
1.5
198
123
144
134
40
80
2.5
21
67
56
84
15
1.1
1.3
1.1
1.5
1.4
100
1.5
1.1
80
23
34
13
34
0.5
0.005
0.007
0.2
0.7
0.1
3J
3.4
131
104
137
37
22
27
49
25
99
59
169
123
93
97
104
90
122
125
144
140
127
112
132
132
136
108
8
24
25
27
28
29
30
••
JJ
35
36
37
39
41
42
45
41
47
41
8
48
49
50
44
51
129
106
140
111
52
53
8,10
3.4, 10
146
87
143
168
91
180
54
57
58
3, 10, 54, 55, 56
3, 10, 56, 57
3, 10, 58. 59
256
182
189
114
263
178
189
117
115*
111
155
117*
224
207
60
61
8
63
64
65
68
69
11
70
8, 11, 31
3. 4. 10, 32, 61
8, 10. 62
3, 10, 63
3. 4, 8. 64
8, 12, 66. 67
8. 10, 68
3, 10, 69
8
3.56
211
225
292
271
167
139
112
105
199
155
140
1.5
1.1
1.0
1.0
25
1.0
1.0
2.0
2J>
2.0
1.1
2.0
15
65
32
AS
196
61
136
146
134
42
107* 83
223
74
224
310
74
280
70
170
.142
112
75
109
56
198
157
66
155* 81
142
350*
173
68
127
56
96
49
101
54
106
92
52
125
129
131
130
132
116
74
133
67
134
50
129
114
80
lJ
1.0
1.5
WM WF
111
151
229
211
93
59
68
7
9
8
13
15
16
18
19
20
22
8
3,10
10, 11, 12
4, 8, 14
3, 15
4.8, 17
3, 10, 12
8,10
3, 4, 10, 17, 21
8, 10, 23
8, 10, 23
8, 10, 11
8, 10, 17, 26
3, 10, 27
8, 10. 14
3, 4, 10, 12, 29
3, 8, 10. 31, 32
<t 1 4
4,8
8, 10, 14
3, 8, 10, 17, 32, 38
3, 8, 10, 17, 40
3. 8, 10, 41
3, 8, 10, 17, 32, 42, 43, 44
3. 8, 10, 45
3, 8, 10. 46
3. 8, 10, 44, 46, 47
3, 8, 10, 41, 44
8.10
4, 8. 17, 32
8, 10, 14
3, 8, 10, 17, 32
3, 8, 10
8, 10, 17
Species are listed in the order given by Monroe and Sibley (1993). MC, duration of male care; FC, duration of female care; BR, breeding range
O : MD, migration distance (°): BD, breeding density (pair*ha~'); CM, clutch man (g); EL, egg-laying interval (days); HS. hatching succesi (%
nests); WM, wing length of male (mm); WF, wing length of female (mm); AS, adult survival (% year"1). Asterisks indicate measurements of
unsexed specimens.
Reynolds and Szekely • Shorebird parental care
129
tween contrasts in clutch mass (dependent variable) and contrasts in the mate's wing length. Relative survival of males and
females was calculated by taking the residuals from the contrasts in mean survival (dependent variable) regressed on the
contrasts in wing length of the investigated sex. For all sizecontrolled variables, we also provide the uncorrected statistics.
Size dimorphism was calculated by taking residuals from a regression between the contrasts in female wing length (dependent variable) against the contrasts in male wing length.
All variables were transformed before the calculations of
the contrasts. The duration of care was arcsine transformed;
the rest of the variables were transformed logarithmically
(base 10). If a variable (x) included 0, we took the log(x +
1) of that variable. The relationships between contrasts in the
dependent variable (duration of care) and the contrasts in
the independent variables were tested by linear regressions
forced through the origin, and Pearson correlation coefficients are presented (Garland et aL, 1992; Harvey and Pagel,
1991; Purvis and Rambaut, 1994). If the assumptions of these
parametric tests such as normality or homogeneity of variances were not met, we used binomial tests (Purvis and Rambaut, 1994). These tested the nun hypothesis that increases
and decreases in parental care did not correspond with
changes in the independent variable. For binomial tests, we
report the number of positive and negative contrasts and the
total number of non-zero contrasts. For some analyses the data
from one sex met the parametric test assumptions, whereas
the data for the other sex did not To facilitate comparisons
between the sexes in such cases, we therefore present binomial tests for both, and regressions for the sex where these
tests are appropriate. Because some of the alternative hypotheses made opposite predictions, we use two-tailed significance
tests throughout
RESULTS
Figure 1
Reconstructed phytogeny of shorebirds, based on molecular
evidence augmented by oncological studies (Szekely and Reynolds,
1995). Branch lengths were set to unity.
< .04), and adult survival (r - .613, n = 18 contrasts, p <
.006). We controlled for body size by taking the residuals from
the regressions between phylogenetically independent differences. We refer to the size-corrected variables as "relative."
Thus, the relative clutch mass was calculated as the residuals
from the contrasts in clutch mass (dependent variable), regressed on the contrasts in female wing length. Similarly, the
relative egg-laying interval was calculated as the residuals from
the contrasts in egg-laying interval regressed on the contrasts
in female wing length. The incubation capacity of a parent's
mate was calculated by taking residuals from a regression be-
Duration of o r e
and females
There is a negative correlation between the duration of male
care and female care: evolutionary increases in duration of
male care were associated with evolutionary decreases in female care (binomial test, 7 positive contrasts, 19 negative contrasts, n ™ 26 contrasts, p - .031; Figure 2). (Note the important feature is the number of contrasts in care that fall
above or below the horizontal zero line.)
Benefits of o r e
We found no support for the hypothesis that the duration of
parental care in either sex would increase with the needs of
the broods when the sexes were analyzed separately (Table 2),
nor when the combined efforts by both parents were considered (total duration of care, see below). Thus, the hypothesis
• References: 1, Cramp (1985); 2. Maclean (1969); S, Hayman et aL (1986); 4. Schonwetter (1967); 5. Bennett (1983); 6, Baker-Gabb et aL
(1990); 7, Hirons (1983); 8. Cramp and Simmons (1983); 9, Mendall and Aldous (1943); 10. Johnsgard (1981); 11, Nethenole-Thompson
(1986); 12( Saether et al. (1986); 13, Tuck (1972); 14, Boyd (1962); 15, Miskelly (1990); 16, Lind (1961); 17, Oring and Lank (1984); 18.
Nowicki (1973); 19. M.C Grant (personal communication); 20. Lenington (1984); 21, Redmond and Jenni (1986); 22, Hilden (1979); 23,
Ghitz et al. (1977); 24, Yalden and Holland (1992); 25, Oring (1986); 26, Oring et aL (1983); 27, Howe (1982); 28, Nettleshlp (1973); 29,
Handel (1983); 30, Kistchinski and Flint (1973); 31, Demenu'ev and Gladkov (1969); 32, Jehl (1971); 33, JX Melnikov (personal
communication); 34, Pringie (1987); 35, Neulethlp and Maher (1973); 36. Pienkowski and Green (1976); 37, Gnuto-Trevor (1991); 38,
Ashkenazie and Safriel (1979); 39. Holmes (1973); 40. Holmes (1972); 41, Myers et aL (1982); 42. Miller (1985); 43. Miller (1983); 44.
Pitelka et aL (1974); 45, Parmelee et aL (1968); 46. Howe (1975); 47. Pitelka (1959); 48. Soikkeli (1967); 49, Holmes and Pitelka (1964); 50.
Jehl (1973); 51. Reynolds (1987); 52. Kobayashi (1955); 53, Hdhn (1975); 54. Tarboton (1976); 55. Pitman (1960); 56, Urban et aL (1986);
57. Tarboton and Fry (1986); 58, Osborne (1982); 59. Osborne and Bourne (1977); 60, Harris (1967); 61, Parmelee et aL (1967); 62. Jehl
and Murray (1986); 63, Bergstrom (1981); 64, McCuUoch (1992); 65, Szekely and Lesselb (1993); 66. Szekely (1991); 67, Szekely (1992); 68.
Pulliainen (1970); 69. Hay (1979); 70, Walters (1982).
Behavioral Ecology VoL 8 No. 2
ISO
1.0
O
M^*—*-*.
-O5<
-1.0
ao
0,2
0.4
o.8
OJ
Contrast In duration of male care
Figure 2
Relationship between phyiogenetically independent differences
between duration of male care and female care (binomial test, 7
positive contrasts, 19 negative contrasts, n *• 26 contrasts, ^> — .031).
Tkble2
Duration of parental
that incubation capacity of the mate would be correlated with
care by the opposite sex was not supported because individuals were not more likely to provide care if the dutch mass
was large relative to the size of their mate (Table 2). This was
also true when the duration of total care by both parents was
compared with clutch mass relative to mean body size of the
adults (r • -.101, n = 47 contrasts, p > A).
Breeding latitude (a hypothesised correlate of harshness of
incubation conditions) was not correlated with duration of
care by either sex (Table 2), nor by both sexes combined (r
«• —.051, n • 49 contrasts, p > .7). The idea that birds remain
with their mates to nest again after dutch failure was also not
supported for care by females (the only sex for which a comparison was possible; Table 2), nor for the total duration of
care by both sexes (binomial test, four positive contrasts, six
negative contrasts, n •* 10 contrasts, p = .754). These results
are also not consistent with the hypothesis that females forgo
incubation to produce replacement clutches rapidly in the
event of nest failure.
Finally, our results do not support the hypothesised advantage of large body size in defense against predators, because
the duration of total care provided by both parents was not
correlated with the average body size of the parents (r =
-.094, n =» 48 contrasts, p > .5).
Benefits of desertion
One prediction from sexual selection theory was not supported: the duration of parental care in either sex did not
in relation to hypothesized benefits of care and desertion In snorebirds
Benefits of care
Incubation requirements
Incubation capacity of mate*
Breeding latitude*
Mate-retention
Hatching success1
Benefits of desertion
Sexual selection
Breeding density"1
Sexual dimorphism in wing length (fnn)
Adult survival
Clutch mass*
"
Relative clutch mass'
Egg-laying interval*
Relative egg-laying interval
Annual survival11
Relative annual survival
Migration distance
Increase in duration of male care .
Increase in duration of female care
No. of contrasts
No. of contrasts
Positrw:
Negative
P
Positive
Negative
P
14
16
15
15
1.0
1.0
14
22
26
22
.082
1.0
—
—
—
4
6
.754
9
22
12
7
.664
.009
12
8
15
32
.700
.0003
14
14
8
8
9
5
9
17
.719
1.0
.286
.383
.607
.424
.031
28
21
14
12
11
9
25
15
19
11
14
6
7
19
.067
.874
15
14
13
6
9
22
.690
.845
.332
.804
.451
Phyiogenetically independent differences between taxa (contrasts) were calculated for duration of care for each sex separately. Binomial tests
are given for each sex throughout, and where data meet parametric assumptions (females only), correlation coefficients and regression
coefficients are in footnotes. The phylogeny in Figure 1 was used to extract contrasts. Relative measures have been controlled for body size
(see Methods).
• r - -.179, b - -1.134, n - 44, p > .2.
• T - -.013, b - -.038, n - 49, p > .9.
• No variation in duration of male care in species where data cm hatching success were available.
• r•r'r•r"r-
-.129, b - -.081, n - 30, p > .4.
-.047, b - -.136, n - 48. p > .7.
.074, b - .456, n - 44, p > .6.
.332, b - 1.265, n - 29, p - .07.
.419, b - 1.983, n - 20, p - .06.
1S1
Reynolds and Szekely * Shorebird parental care
1.0
2
, A
3
OJS
c
0.0 • •
o
75
a
I
-O6
o
o
-1.0
-0.03
-O02
-0.01
B
1.0 •
0.00
0.01
0.02
0.03
•
2
S
03 •
#
o
0.0 -
o
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• • •
•
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« .
-1.0 -0.03
-0.02
-0.01
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0.00
0.01
•
0.02
0X3
Contrast In female:male wing length
Figures
Relationships between standardized linear contrasts in wing-length
dimorphism and duration of parental care in shorebirds. (A) Males
(r = .454, » - 44 contrast!, p < .002), (B) females (r - -.582, n
— 44 contrasts, p < .001). Wing-length dimorphism was calculated
by using residuals from a linear regression between wing length of
female (dependent variable) and wing length of male.
would be subject to the most intense sexual selection. To test
this hypothesis for males, we reanalyzed the data using new
contrasts by excluding the following socially polygynous species: Scolopax rusticola, S. minor, GalHnago media, Cotnocorypha aucklandica, CaHdris fusdcoUis, C mdanotos, C acuminata, C. ftrrughua, Trjngitts subruficoOis, and Charadrius attxandrinus. A* predicted by sexual selection, the correlation
between duration of male parental care and female: male size
dimorphism does not occur within socially monogamous species (binomial test, 10 positive contrasts, 11 negative contrasts,
n " 21 contrasts, p m 1.0). The relationship shown in Figure
3A was primarily due to differences between socially monogamous and polygynous taxa.
A similar test was performed for females by excluding the
following socially polyandrous species: Ptdieniomus torquatus,
Trtnga macularia, Phalaropus lobatus, Rostratuta bmghalmsis,
AetophUamis qfricanus, Jacana jacana, Charadrius alexandrinus, and Eudromias morhuQus. Interestingly, the relationship
between duration of female care and femalennale size dimorphism remains negative and significant even when these multidutching species are excluded (binomial test: 11 positive
contrasts, 21 negative contrasts, n » 32 contrasts, p > .1; r =
—.375, n •• 36 contrasts, p < .03). Thus, unlike males, increases in duration of female care are correlated with decreases in
the size of the female relative to the male, even when die
females form pair bonds with only one male per season.
The other main benefit of deserting broods may be unproved adult survival. Thus, females may be selected to desert
after the energetic expense of laying a large mass of eggs relative to their own weight, or after laying eggs rapidly (Ashkenazie and Safriel, 1979). The clutch-mass prediction was not
supported: there was no correlation with parental care, regardless of whether female body size was controlled (Table 2).
The relationship between egg-laying interval and female desertion seems to support the initial prediction: females tend
to remain with the brood longer when the period between
the laying of consecutive eggs per clutch is longer (Table 2).
However, this relationship may be due to body size-dependent
laving intervals (see "Comparative analyses"), as the relationship disappeared when female size was controlled (Table 2).
Evolutionary increases in annual adult survival (sexes combined due to lack of separate data) were accompanied by increases in duration of care by the female, but not by the male
(Table 2). Again, this relationship disappeared when we controlled for female size (Table 2).
Contrasts among taxa in parental care by males were correlated with contrasts in migration distance: long migration
distances (data from both sexes combined) were associated
with short male-care (Table 2; Figure 4A). This relationship
did not occur in females (Table 2; Figure 4B).
DISCUSSION
change with increasing breeding density (one measure of ease
of attracting a second mate; Table 2). However, a key prediction of sexual selection theory was supported: evolutionary
increases in female: male size dimorphism were matched by
decrease* in female care and increases in male care, respectively (Figure 3). Thus, the evolution of smaller relative size
in one sex has been correlated with an increase in parental
care by that sex. Evolutionary changes in duration of care in
either sex had no relationship to changes in the absolute size
of that sex (binomial test: males, 14 positive contrasts, 15 negative contrasts, n •= 29 contrasts, p «= 1.0; females, 23 positive
contrasts, 17 negative contrasts, n » 40 contrasts, p > .4; r
females •» -.036, n = 44 contrasts, p > .8).
One might expect that males of socially potygynous species
and females of socially potyandrous (muldchitching) species
Benefits of care
Many reviews have attempted to explain the unusual diversity
among shorebird species in uniparental or biparental care according to differing needs of the offspring (eg., Erckmann,
1983; Lenington, 1984; Oring, 1986; Pitelka et aL, 1974; Saether et aL, 1986). Predictions from three of these hypotheses
have not been supported by our analyses: there was no correlation between biparental care and offspring requirements
as reflected by (1) breeding in high latitudes (hence the need
for both parents to incubate and brood the young in harsh
conditions; Erckmann, 1983; Pitelka et al.. 1974), (2) producing large dutch-masses relative to adult body size (Ashkenazie
and SafrieV1989), or (3) the need for both parents to defend
die young against strong brood predation (Erckmann, 1983;
13J
Behavioral Ecology VoL 8 No. 2
1.0, A
(Ibidorhjncha), thick-knees (Burhinus), Magellanic plover
(Phtviandhu), and sheathbiUs (Quonis) (Johnsgard, 1981;
Kelso, 1972; Walters, 1984). This finding is consistent with the
demonstration that short-duration pair bonds were more likely to evolve in taxa where the young are self-feeding and nidifugous across nonpasserine birds (Sillen-Tullberg and Temrin, 1994).
0.5.
of desertion
•OS-
-1.0
0.0
0.2
0.4
0.6
0.8
, B
2
S
o
I
£
o.o <-
c
o
o
-1.0
0.0
0.2
0.4
0.6
0.8
Contrast In migration distance
Figure 4
Relationships between standardized linear contrasts in duration of
care and migration distance in shorebirds (sexes combined). (A)
Males (binomial test, 9 positive contrasts, 22 negative contrasts, n 31 contrasts, p ~ .031), (B) females (binomial test, 25 positive
contrasts, 19 negative contrasts, n - 44, p » .451).
Larsen, 1991; Lenington, 1984). Each test has limitations,
some of which are rather severe. For example, if brood predadon has selected for biparental care, and biparental care
has been effective, then it may be futile to expect to see correlations between current patterns of care and predadon. The
use of latitude as a surrogate for environmental harshness also
seems rather crude, as hot or wet riimatM may also select for
the combined efforts of both parents. Finally, it should be
borne in mind that both ecological variables and aspects of
life histories often vary among populations, which would be
missed by species-wide comparisons.
It should also be noted that biparental care always occurs
in, but is not restricted to, species that feed their young for
long periods after hatching. This trend was too conservative
for independent comparisons, occurring in the Charadriida
clade, which includes oystercatchers (Haematopus), ibiabill
This study shows that the duration of parental care is related
to sexual dimorphism in body size. Evolutionary reductions
in care by either sex are correlated with increases in body size
of that sex relative to the other (Fig. S). This result supports
Jdnsson and Alerstam's (1990) study, in which they investigated sandpipers and allies (Scolopaddae) without taking the
pbyiogenetic relatedness among the species into account Our
results are consistent with sexual selection in males because
the relationship disappears when socially polygynous species
are excluded. Sexual selection may therefore have caused a
general trend toward evolutionary reductions in male care in
scolopacids through time (Szekely and Reynolds, 1995),
though the direction of causation cannot be inferred from
comparative studies such as this. But sexual selection on females does not explain why, in most contemporary species,
females still tend to desert broods earlier than males, especially since female brood desertion often occurs late in the nesting period (Szfkety and Reynolds, 1995). Furthermore, the
strong pattern of increases in femalermale size being correlated with reduced female care remains even when socially
poh/androus species are excluded. This result appears to support the suggestion ofJdnsson and Alerstam (1990) that small
body size may be more efficient during incubation than large
body size. However, enthusiasm for this consistency should be
tempered by the fact that Jdnsson and Alerstam's calculations
assumed that food intake rates are independent of body size,
which may not be realistic.
The benefit of reducing care may include more than enhanced mating opportunities. Sexual selection in males and
egg-laying by females may select for reduced care to compensate for survival costs. Cause and effect are difficult to disentangle, but in the case of migration, most parental care patterns must have evolved first, since most of the bifurcations
in care in our phytogeny are far older than contemporary
migratory routes, most of which have evolved within the last
5,000 years, following the retreat of the glaciers after the last
ice age 12,000 years ago (Alerstam, 1990). Thus, changes in
male (but not female) care may have affected future options
for migration, with species where males provide little care being able to afford to migrate farther due to their energetic
savings. It remains an enigma why females do not show the
same pattern. It is also noteworthy that in ruffs, PhUomachus
pugnax, males do not participate in incubation, yet they migrate shorter distances than females do (Gill et al., 1995).
Studies of sex differences in migration in relation to energetics and body size are vital for understanding the correlation
between male desertion and migration distance of taxa shown
here.
Myers (1981) has shown a relationship between timing of
desertion and migration distance, using a study restricted to
calidrine sandpipers. That study did not take phylogenetic relationships into account, and it combined the parental care
of both sexes in die analyses. The raw data used here match
Myers's data closely, and when we restrict our phyiogenetically
independent analyses to calidrines only, our results are the
same as for our full data set, with only males showing the
relationship. Thus, the main discovery of Myers, that parental
care and migration are inversely related, is corroborated here.
Reynolds and Szikety • Shoretard parental care
We extend his observations to encompass shorebirds generally, but restrict the pattern to males.
The analyses presented here have searched for broad correlations among many taxa between parental care and other
aspects of life histories. It is, of course, possible for uniparental care to have evolved for different reasons in different
taxa. It remains plausible, for example, that most species of
tropical jacanas have evolved male care because of selection
on females to be free to produce replacement clutches in
high-predadon environments (Erckmann, 1983; Jenni, 1974),
whereas die temperate and arctic-breeding phalaropes have
evolved female care to enable females to be capitalize on
ephemeral food resources (Emlen and Oring, 1977; Erckmann, 1983). Indeed, sexual selection operates differently in
these groups. In most jacana species there is strong sexual
dimorphism in body size, vigorous territoriality, and females
often form simultaneous pair bonds with multiple males,
whereas phalaropes are less dimorphic in size, are not territorial, and, except for small populations, exhibit low levels of
social polyandry (Reynolds, 1987).
In conclusion, benefits of desertion through sexual selection appear to have operated differently on each sex of shorebirds, and there may also be different causes in different species. Whereas offspring desertion may have opened the way
toward increased migration distance for males, females show
no such correlation. Relationships between sexual dimorphism and parental care appear to be more consistent'between the sexes and across taxa, with evolutionary reductions
in care by either sex being correlated with increases in body
size of that sex relative to the other. Again, however, closer
examination shows a sex difference, with the pattern disappearing among males when socially polygynous species are
excluded, whereas the relationship remains strong in females
when socially polyandrous species are excluded. These results
suggest that the causes and correlates of parental care are
different in each sex. To understand these differences requires detailed studies of energetic costs of incubation and
migration in relation to parental care and sexual selection.
We thank CM. Perrins and L. Birch for accets to the Alexander library at Oxford. M.G. Wilson helped us by translating Russian and
German references. R.B. Lanctot, P. Fleming, M.C Grant, JJ. Melnikov, and PS. Tomkovich kindly provided unpublished information,
and I.M. C6te, J.NCN. Smith, W.j. Sutherland, and two anonymous
reviewen made helpful comments on the manuscript. A. Purvis kindly
provided advice on some analyses. TS. was supported by the British
Ecological Society (Research Travel Grant no. 9S/4) for a visit to the
University of East AngUa during the preparation of this paper, by the
Hungarian OTKA Foundation (no. T5492), and by a Leverhulme
Trust Grant to AX Houston, L Cuthill and J.M. McNamara (F/182/
AP).
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