vol. 186, no. 2
the american naturalist
august 2015
Adult Mortality Probability and Nest Predation Rates Explain
Parental Effort in Warming Eggs with Consequences
for Embryonic Development Time
Thomas E. Martin,1,2,* Juan C. Oteyza,2 Andy J. Boyce,2 Penn Lloyd,3 and Riccardo Ton2
1. United States Geological Survey, Missoula, Montana 59812; 2. Montana Cooperative Wildlife Research Unit, University of Montana,
Missoula, Montana 59812; 3. Percy FitzPatrick Institute, Department of Science and Technology/National Research Foundation
Centre of Excellence, University of Cape Town, Private Bag X3, Rondebosch, 7701, South Africa
Submitted October 25, 2014; Accepted January 15, 2015; Electronically published May 12, 2015
Online enhancement: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.km646.
abstract: Parental behavior and effort vary extensively among species. Life-history theory suggests that age-specific mortality could
cause this interspecific variation, but past tests have focused on fecundity as the measure of parental effort. Fecundity can cause costs
of reproduction that confuse whether mortality is the cause or the
consequence of parental effort. We focus on a trait, parental allocation of time and effort in warming embryos, that varies widely
among species of diverse taxa and is not tied to fecundity. We conducted studies on songbirds of four continents and show that time
spent warming eggs varies widely among species and latitudes and
is not correlated with clutch size. Adult and offspring (nest) mortality explained most of the interspecific variation in time and effort
that parents spend warming eggs, measured by average egg temperatures. Parental effort in warming eggs is important because embryonic temperature can influence embryonic development period and
hence exposure time to predation risk. We show through correlative
evidence and experimental swapping of embryos between species
that parentally induced egg temperatures cause interspecific variation in embryonic development period. The strong association of
age-specific mortality with parental effort in warming eggs and the
subsequent effects on embryonic development time are unique results that can advance understanding of broad geographic patterns
of life-history variation.
Keywords: life history, parental effort, incubation period, embryonic
development, parental care, reproductive effort, adult mortality, nest
predation.
Introduction
Life-history theory predicts that age-specific mortality influences evolution of parental effort: decreased adult mortality and increased offspring mortality both favor evolu-
* Corresponding author; e-mail: tom.martin@umontana.edu.
Am. Nat. 2015. Vol. 186, pp. 223–236. q 2015 by The University of Chicago.
0003-0147/2015/18602-55845$15.00. All rights reserved.
DOI: 10.1086/681986
tion of reduced effort and increased investment in selfmaintenance (Williams 1966; Murphy 1968; Hirshfield and
Tinkle 1975; Law 1979; Michod 1979; Charlesworth 1994).
Litter or clutch size has been correlated with age-specific
mortality across species (e.g., Promislow and Harvey 1990;
Martin 1995, 2014; Ghalambor and Martin 2001). Yet fecundity and associated behaviors can create large costs of
reproduction that manifest in adult mortality (Calow 1979),
making it unclear whether adult mortality is the cause or the
consequence of evolved differences in fecundity (Reznick
1985). Examination of a parental behavior that is largely independent of fecundity and its costs of reproduction can
provide a clearer test of the ability of age-specific mortality to influence evolution of interspecific variation in parental effort versus self-maintenance.
Allocation of time and effort in caring for eggs is an
interesting parental behavior for tests because it is not necessarily tied to fecundity and does not seem to be a major
cause of annual rates of adult mortality. Nonetheless, it competes with time and resources for self-maintenance. For example, time that parents spend guarding eggs from potential
predators competes with time for self-maintenance across
taxa as diverse as fish and insects (Abrams and Eickwort
1981; Pressley 1981; Magnhagen and Vestergaard 1991;
Steinhart et al. 2005, 2008). Similarly, time and energy that
parents spend incubating eggs to regulate embryonic temperature can create difficulties in maintaining mass in birds
and snakes (birds: Vleck 1981; Moreno and Carlson 1989;
Williams and Dwinnel 1990; Hainsworth et al. 1998; Bryan
and Bryant 1999; Hanssen et al. 2003; snakes: Vinegar et al.
1970; Madsen and Shine 1999). Studies of these conflicts
between parental effort and self-maintenance have focused
on single species. Yet species can differ substantially in their
exposure to mortality and other environmental influences,
which should favor evolution of differing allocation solutions. Indeed, time and effort allocations differ dramat-
224
The American Naturalist
ically among species; for example, the percentage of time
that songbirds spend incubating eggs during the day varies extensively among species and latitudes (fig. 1A), and
this behavioral variation is independent of clutch size
(fig. 1B). Ultimately, the causes of evolved variation among
species in time and effort devoted to embryos versus selfmaintenance are untested in any taxa.
Life-history theory predicts that species with lower adult
mortality should devote less time and effort to parental
care (fig. 1C) and save more energy for self-maintenance
(Williams 1966; Murphy 1968; Hirshfield and Tinkle 1975;
Law 1979; Michod 1979; Charlesworth 1994). This theory
also predicts that time and effort should be reduced for species with greater offspring mortality, to enhance opportunities for additional future reproductive attempts (Law 1979;
Michod 1979; Charlesworth 1994). However, increased rates
of embryo predation can favor faster embryonic development, to reduce exposure time to predators (Martin 2002;
Martin et al. 2007; Remeš 2007). In the case of birds, higher
risk of embryo predation may favor increased parental effort to warm eggs as a means of shortening development
time and exposure to risk, given that avian embryos depend
on parental warming to develop (Weathers and Sullivan
1989; Fontaine and Martin 2006). Thus, the directional influence of embryo predation risk on parental incubation
effort is unclear, whereas increased adult mortality predicts
increased incubation effort (fig. 1C). Annual adult mortality probability is lower for many species in tropical and
Southern Hemisphere regions than in north-temperate regions (Rowley and Russell 1991; Sandercock et al. 2000;
Lloyd et al. 2014; Martin et al. 2015b), and hence a latitudinal gradient may be expected (fig. 1C). However, embryo
predation does not show clear latitudinal patterns (Martin
1996; Martin et al. 2006), and thus its effects on parental effort may not be spatially predictable.
Causes of variation in parental effort in warming eggs
are important to understand because embryonic temperature can have important fitness consequences through effects on development time and offspring quality across
diverse taxa (Gillooly et al. 2002; Martin et al. 2007; Du
et al. 2009; Nord and Nilsson 2011; Hepp and Kennamer
2012). Yet some authors argue that intrinsic physiological processes, rather than embryonic temperatures, determine avian embryonic development time (e.g., Ricklefs
1993; Tieleman et al. 2004; Robinson et al. 2008). Thus, examination of the possible role of age-specific mortality for
evolved differences in parental incubation behavior has to
be coupled with tests of the relative importance of temperature and intrinsic causes of variation in embryonic development rates.
Here, we test these possibilities across diverse songbirds
on four continents (fig. 1). We test the ability of adult and
embryo mortality to explain variation in incubation effort.
We also report new analyses of data from a previous eggtransfer experiment (Martin et al. 2007) to test the relative
importance of intrinsic processes and parental effort in
warming eggs as the causal basis of differences in embryonic periods between species.
Material and Methods
Study Areas
We studied 110 passerine species on four continents
(fig. 1A), but we were able to obtain data on age-specific
mortality and incubation effort for only 63 species (table 1). These 63 species included 16 in north-temperate
Arizona (347N), 18 in tropical Venezuela (97N), 14 in tropical Malaysia (67N), and 15 in south-temperate South Africa (347S), representing a broad phylogenetic range of
songbirds (fig. A1, available online). Nests were studied in
north-central Arizona for 26 years (1987–2012) at about
2,350-m elevation in mixed deciduous and coniferous forest (Martin et al. 2007). Nests were studied in the tropics for 7 years (2002–2008) in primary forest in Yacambu
National Park, Venezuela, at elevations of 1,400–2,000 m
(Martin et al. 2007) and for 5 years (2009–2013) in Kinabalu Park, Malaysia, at 1,450–1,950-m elevation (Martin
et al. 2013). Nests were studied for 5 years (2000–2004) in
the south-temperate coastal dwarf shrubland near Cape
Town, South Africa, at sea level (Martin et al. 2007).
Parental Incubation Behavior
Nest attentiveness was measured as the percent of time
that parents spent on the nest incubating. Nests were videotaped during incubation for the first 6–8 h of the day,
beginning within 0.5 h of sunrise, from 1993 through 2012
in Arizona and in all study years in Venezuela, Malaysia,
and South Africa. This protocol standardized both time
of day and sampling duration (Martin et al. 2000; Martin
2002). We controlled for age of the embryo in the estimates
of nest attentiveness (see “Statistical Analyses”).
Parental Incubation Effort Measured as Egg Temperature
Parental effort is defined as the proportion of the total energy budget that is devoted to producing offspring. Energetic expenditure is higher for incubating than for nonincubating birds (Vleck 1981; Moreno and Carlson 1989;
Williams and Dwinnel 1990; Bryan and Bryant 1999;
Hanssen et al. 2003). Indeed, parental effort, as reflected
by energy expenditure, is as high during incubation as at
any stage of reproduction across diverse species (Williams
1996). Parental effort during incubation is manifested in
Mortality and Parental Effort
A
Arizona
Nest attentiveness
(% of time on nest)
100
Malaysia
Venezuela
South Africa
80
n = 110 species
60
40
20
Individual species
Nest attentiveness
(% of time on nest)
B
100
80
60
40
Arizona
South Africa
Malaysia
Venezuela
20
1
2
3
4
5
6
7
low
Incubation effort
(embryonic temperature)
C
high
Clutch Size (number of eggs)
Figure 1: Variation among species in incubation behavior, measured as percentage of time spent on the nest incubating (nest attentiveness) for the first 6–8 h of daylight. A, Mean nest attentiveness
for songbird species studied on four continents in order of increasing percentage of time spent on the nest, illustrating a geographic
gradient. Each bar represents a species, color coded by region.
B, Mean nest attentiveness was not related to average clutch size
but increased with log-transformed body mass and differed among
sites (generalized linear model: clutch size: B 5 SE p 1.24 5 1.94;
F1, 104 p 0.41, P p .52; log10 mass: B 5 SE p 12.17 5 4.52; F1, 104 p
7.26, P p .008; site: F3, 104 p 4.97, P < .001; interactions: not significant). C, Predicted relationship between adult mortality and incubation effort (measured as average embryonic temperature) within and
among geographic regions. The ellipse illustrates predictions that in-
225
part through the amount of time that parents spend on the
nest warming eggs, which varies extensively among species (fig. 1A). Incubating birds are under greater time
constraints to replenish energy than nonincubating birds
because of time spent on the nest, potentially magnifying
the costs of energy expenditure for incubation and often
creating difficulties in maintaining mass through a positive energy balance (Williams and Dwinnel 1990; Williams
1996; Hainsworth et al. 1998). As a result, energetic costs
and time constraints of incubation effort can cause mass
loss in incubating birds (Williams and Dwinnel 1990;
Hanssen et al. 2003). The time invested in warming eggs
explains much, but not all, of the variation in average egg
temperature (Martin et al. 2007). Birds also affect egg temperature through energy invested in differential regulation
of blood flow to their brood patch, a bare area on their
breast placed against eggs to warm them (White and Kinney 1974; Webb 1987). Thus, average egg temperature is a
good measure of parental effort, because it captures both
time spent incubating and the amount of energy that parents put into regulating blood flow to the brood patch
(White and Kinney 1974; Weathers and Sullivan 1989;
Martin et al. 2007). This is also true in the tropics, which
are actually cold with respect to temperatures required by
bird embryos; ambient temperatures in our midelevation
tropical sites range from 167 to 247C, which are substantially below optimal temperatures (35.57–38.57C) for avian
embryo development (Webb 1987).
Given the above, we measured egg temperatures as the
best estimate of parental incubation effort and because of
the potential influence of temperature on embryonic periods. Egg temperatures were measured by insertion of
thermistors, during egg laying or on the first or second
day of incubation, into the center of eggs through a small
hole sealed with glue (Martin et al. 2007). The wire was
threaded through the nest and connected to a HOBO Stowaway or XTI datalogger (Onset Computer, Bourne, MA)
that recorded temperatures every 12–24 s for as long as
the nest remained active and averaged them over 24-h periods for daily estimates. We excluded nests where temperatures systematically changed across days because of failing
batteries or poorly sealed eggs. Egg temperatures were based
on extensive sampling (table 1). Because parents change
their effort with age of the embryo, we controlled for age
of embryos in estimates of average 24-h egg temperatures
across species (see “Statistical Analyses”).
cubation effort should be greater in north-temperate regions, where
adult mortality is commonly higher than that in tropical and southtemperate regions.
Table 1: Parameter estimates, standard errors, and sample sizes of daily nest predation rate, annual adult mortality probability, average
24-h egg temperature, and duration of the embryonic period
Daily nest predation
Species
Arizona species:
Empidonax occidentalis
Vireo gilvus
Sialia mexicana
Catharus guttatus
Turdus migratorius
Sitta canadensis
Sitta carolinensis
Certhia americana
Troglodytes aedon aedon
Poecile gambeli
Junco hyemalis
Pipilo chlorurus
Oreothlypis celata
Setophaga coronata
Cardellina rubrifrons
Piranga ludoviciana
South Africa species:
Telophorus zeylonus
Dessonornis caffra
Tychaedon coryphaeus
Pycnonotus capensis
Cisticola subruficapilla
Prinia maculosa
Apalis thoracica
Zosterops capensis
Sphenoeacus afer
Sylvietta rufescens
Curruca subcaeruleum
Anthobaphes chalybeus
Crithagra flaviventris
Crithagra albogularis
Emberiza capensis
Venezuela species:
Mionectes olivaceus
Zimmerius chrysops
Masius chrysopterus
Dysithamnus mentalis
Myrmotherula
schisticolor
Synallaxis cinnamomea
Myadestes ralloides
Catharus aurantiirostris
Catharus fuscater
Turdus flavipes
Turdus olivater
Troglodytes aedon
musculus
Henicorhina leucophrys
Atlapetes semirufus
Arremon brunneinucha
Annual adult mortality
Average 24-h
temperature
Mean embryo
period
Rate
SE
Nests
Rate
SE
Individualsa
T (7C)
SE
Days
Days
SE
Nests
.041
.031
.007
.089
.039
.004
.006
.010
.005
.008
.041
.053
.032
.044
.037
.036
.0016
.0019
.0011
.0028
.0016
.0005
.0009
.0011
.0005
.0006
.0014
.0031
.0014
.0033
.0016
.0033
1,336
790
330
1,505
1,376
947
310
490
1,570
1,072
1,785
594
1,453
523
1,299
421
.401
.480
.517
.482
.461
.529
.574
.452
.536
.495
.433
.445
.411
.494
.429
.435
.034
.025
.096
.023
.035
.058
.057
.072
.036
.033
.014
.088
.027
.038
.051
.035
674
857
73
1,875
655
547
164
408
1,029
709
1,885
158
976
1,008
694
728
34.82
35.90
34.98
36.20
36.36
35.56
36.01
35.09
35.68
35.29
35.93
36.14
35.68
36.12
35.68
35.92
.21
.49
.18
.18
.35
.27
2.26
.20
.17
.23
.33
.18
.23
.26
.16
.53
44
8
51
54
23
23
3
51
61
41
22
51
31
24
60
7
14.91
13.06
14.25
12.50
12.42
12.50
12.70
14.67
13.47
13.28
12.42
12.17
12.61
12.55
12.73
13.01
.05
.03
.09
.07
.03
.03
.12
.03
.03
.04
.05
.10
.05
.09
.04
.03
277
147
103
106
317
216
80
149
560
224
317
57
192
71
322
74
.124
.105
.061
.118
.080
.101
.104
.127
.102
.062
.085
.099
.113
.097
.087
.0160
.0056
.0033
.0072
.0044
.0031
.0061
.0079
.0101
.0065
.0064
.0048
.0045
.0106
.0081
69
444
491
319
451
1,350
347
293
122
73
230
509
734
102
147
.215
.097
.223
.214
.371
.294
.236
.258
.162
.212
.190
.206
.404
.330
.377
.070
.020
.020
.040
.050
.020
.020
.040
.050
.040
.030
.030
.040
.070
.070
13
83
364
45
54
212
134
41
21
41
62
55
95
24
25
34.54
33.51
34.38
35.85
35.17
35.71
35.18
36.33
34.45
34.97
34.86
35.05
36.06
35.87
35.25
1.75
.80
.41
.43
.32
.45
.37
.78
.57
.76
.54
.93
.44
2.85
1.19
4
17
34
27
34
42
25
18
26
23
36
10
24
4
10
16.25
16.44
14.03
12.31
13.79
13.18
15.21
11.00
16.71
13.75
13.76
13.57
11.90
11.92
13.58
.25
.22
.13
.19
.12
.07
.12
.17
.35
.14
.11
.09
.08
.28
.25
5
26
87
30
54
151
36
43
12
21
38
78
101
15
26
.031
.057
.033
.039
.0029
.0074
.0076
.0055
237
104
39
129
.232
.261
.108
.234
.128
.166
.183
.103
165
25
51
68
33.66
34.33
32.58
34.09
.31
.15
.20
.23
31
70
43
33
19.92
16.90
19.67
16.00
.16
.27
.33
.33
31
10
3
11
.050
.047
.039
.056
.042
.055
.044
.0057
.0094
.0060
.0071
.0025
.0072
.0064
151
40
112
102
541
93
96
.255
.180
.288
.304
.299
.396
.359
.086
.138
.157
.157
.057
.109
.098
112
43
38
63
283
39
63
34.30
33.50
35.61
34.97
34.89
35.74
36.14
.22
.24
.22
.31
.37
.20
.25
34
35
39
28
32
45
34
15.63
19.17
13.57
15.68
14.85
12.77
13.32
.21
.31
.24
.20
.09
.18
.24
14
4
10
16
95
13
13
.008
.030
.069
.054
.0020
.0024
.0127
.0032
27
377
41
448
.408
.216
.272
.198
.094
.098
.237
.099
41
385
36
206
35.17
33.99
35.02
34.14
.13
.56
.18
.47
98
32
47
29
14.83
19.74
14.75
17.47
.37
.16
.26
.17
10
39
7
43
Mortality and Parental Effort
227
Table 1 (Continued )
Daily nest predation
Species
Rate
SE
Myioborus miniatus
Basileuterus tristriatus
Saltator maximus
Malaysia species:
Pachycephala hypoxantha
Rhipidura albicollis
Myophonus borneensis
Brachypteryx montana
Vauriella gularis
Ficedula hyperythra
Eumyias indigo
Enicurus leschenaulti
Alophoixus ochraceus
Phyllergates cuculatus
Seicercus montis
Pellorneum pyrrogenys
Stachyris nigriceps
Yuhina everetti
.045
.041
.069
.046
.047
.014
.044
.025
.048
.028
.047
.020
.051
.067
.045
.066
.056
a
Annual adult mortality
Individualsa
Nests
Rate
SE
.0059
.0048
.0185
126
180
20
.208
.236
.390
.082
.052
.249
.0047
.0051
.0030
.0043
.0058
.0040
.0054
.0084
.0074
.0070
.0076
.0072
.0067
.0038
175
155
77
198
59
277
119
59
26
110
182
71
169
397
.231
.426
.271
.209
.279
.248
.180
.249
.321
.342
.303
.151
.212
.338
.044
.062
.128
.103
.047
.054
.171
.139
.078
.128
.060
.064
.024
.037
Average 24-h
temperature
Mean embryo
period
T (7C)
SE
Days
Days
SE
Nests
68
172
25
34.33
34.36
36.25
.41
.21
1.52
25
45
7
15.43
15.72
13.25
.33
.18
.29
22
34
3
179
104
27
48
110
149
26
29
77
29
86
87
567
328
33.72
35.11
33.86
33.04
33.46
33.75
33.75
33.80
34.28
34.37
33.93
32.60
33.62
34.95
.15
.18
.27
.13
.36
.14
.21
.36
.43
.23
.56
.17
.23
.09
77
54
28
113
12
85
43
20
14
35
16
70
34
194
17.47
15.45
18.00
16.74
16.60
15.81
16.25
17.20
15.20
16.33
16.58
18.35
16.00
13.82
.19
.15
.24
.15
.22
.20
.27
.45
.40
.30
.23
.43
.16
.16
36
30
13
30
9
37
17
6
6
15
12
11
20
65
Effective sample size in the program MARK.
Nest Predation Rates, Embryonic Periods,
and Clutch Size
For species examined here, large numbers of nests were
monitored (table 1), following long-term protocols (Martin et al. 2000). Embryonic period was quantified as the
number of days between the last egg laid and the last
egg hatched (Martin et al. 2007). Nests were checked every
2–4 days to determine status and predation events but
were checked daily or twice daily during egg laying and
near hatch to obtain exact dates of the last eggs laid and
hatched, to accurately measure period durations. We measured clutch size as the final number of eggs laid and observed on two consecutive checks (Martin et al. 2006).
(and numbers of nests) were as follows: Apalis thoracica
into Zosterops capensis (2); A. thoracica into Crithagra flaviventris (6); Dessonornis caffra into Pycnonotus capensis
(1); Z. capensis into Cisticola subruficapilla (1); Z. capensis
into Prinia maculosa (2); C. subruficapilla into C. flaviventris (3); Sphenoeacus afer into P. capensis (2); P. maculosa
into Z. capensis (4); P. maculosa into C. flaviventris (1);
C. flaviventris into A. thoracica (2); and C. flaviventris into
C. subruficapilla (1). Here, we further analyze those data
by comparing the average change in embryonic period
against the average difference in egg temperature for each
pair of species included in swaps.
Adult Mortality
Egg-Swap Experiment
We experimentally tested the causal role of temperature
for variation in embryonic periods by using data from a
previously reported experiment where we swapped eggs
between species that differed in average egg temperature
(Martin et al. 2007). In brief, we swapped eggs during egg
laying between species with similar-sized eggs but differing
egg temperatures as a result of differing parental incubation effort. We swapped large numbers of eggs over two
field seasons at our South Africa site, but we were left with
only 25 nests that survived to hatching because of high
nest predation (see Martin et al. 2007). Identities of swaps
In Arizona, Venezuela, and Malaysia, nets were deployed
in stations of 10 or 12 nets as subplots within and across
all nest-searching plots. These netting subplots were sampled three times per breeding season, with 20–25 days
before subplots were revisited. Nets at a station were deployed for 6 h, starting at dawn. Netting methods for
the South Africa site are detailed in Lloyd et al. (2014).
All birds captured were banded with numbered metal
bands and three color bands (two bands per leg), except
for recaptures, in which case the identity was noted. Color
bands were used for resighting by nest searchers, who visited each nesting plot daily or every other day throughout
228
The American Naturalist
the season. We conducted banding/resighting studies for
21 years in Arizona (1993–2013), 7 years in Venezuela
(2002–2008), 5 years in Malaysia (2009–2013), and 7 years
(2001–2007) in South Africa. We used these capture, recapture, and resighting data in Cormack-Jolly-Seber models to
provide rigorous estimates of annual adult mortality probabilities across species (see “Statistical Analyses”).
Statistical Analyses
We calculated average 24-h egg temperature for each species as our metric of parental incubation effort. Mean egg
temperature was calculated for each 24-h period after the
probe started collecting data. Parental effort and temperature generally increase in an asymptotic fashion with age
of the embryo, so we log10-transformed age (day of incubation) of the embryo. We obtained mean estimates of average 24-h egg temperature for each species from a linear
mixed model, with egg identity as a random factor nested
within species as a random factor, and with log-transformed
age fitted as random slopes within species, thereby controlling for age effects in species estimates (Martin et al. 2013).
This approach controlled for embryo age to provide an
age-standardized estimate of 24-h egg temperature for each
species (table 1) that was used in the statistical models described next. The same statistical approach was used for
nest attentiveness (i.e., fig. 1). Daily nest predation rates (table 1) were estimated with the logistic exposure method
(Shaffer 2004) based on R, version 3.0.3 for Windows (R
Development Core Team, Vienna, Austria).
The program RMark (Laake 2013) was used to estimate
annual adult survival (F) and resighting (p) probabilities
(White and Burnham 1999; Burnham and Anderson 2002).
For each species, models were built with all additive combinations of F and p assumed to be either constant or sexspecific or to include a factor to account for transients based
on the first year of capture versus all subsequent years. Thus,
the global model was F (sex 1 transient) p (sex 1 transient).
Sex in tropical sites included an unknown category because
many species do not show sexual dimorphism and many
individuals were not in breeding condition when captured.
Parameter estimates (table 1) were based on averaging across
all 16 models on the basis of model weights (Burnham and
Anderson 2002) for all species except those in the South
Africa site, where we used previous estimates (Lloyd et al.
2014). Annual adult mortality was obtained as 1 2 F.
We examined the ability of adult mortality probability,
daily nest predation rate, and log10 mass to explain variation in average 24-h egg temperature and the ability of all
four to explain variation in length of embryonic periods,
with data for these analyses deposited in the Dryad Digital
Repository: http://dx.doi.org/10.5061/dryad.km646 (Mar-
tin et al. 2015a). We included these variables as covariates
in a phylogenetic generalized least squares (PGLS) analysis, with sites treated as n 2 1 dummy variables. We used
fixed-factor models because we expected predictable differences among sites (i.e., fig. 1C). We tested whether aerial
foragers as a dummy variable (yes/no) explained additional
variation, given that aerial foragers can show lower adult
mortality and parental effort (Martin 1995). However, the
result was not close to significance in any analysis, and this
variable was dropped from the models presented. We included adult body mass as a covariate because nest predation and adult mortality may be influenced by size (Roff
2002; Biancucci and Martin 2010) and because larger birds
may also be able to stay on the nest more and keep eggs
warmer (Martin et al. 2007). We obtained mass from birds
captured in our capture-recapture efforts. We plotted the
raw data because doing so allowed us to illustrate species
by site. We corrected each covariate for the other covariates
in plotting the standardized partial regressions. We did not
correct for site effects in these partial-regression plots, to
allow illustration of any site differences.
We used an egg-transfer experiment (Martin et al. 2007)
to quantify the relative proportion of variation in embryonic periods among species that could be attributed to temperature effects. Previously, we simply showed that embryonic periods changed with swaps, but we did not examine
whether the magnitude of the change was related to the
magnitude of temperature difference (see Martin et al.
2007). We do the latter here, with data for these analyses
deposited in the Dryad Digital Repository: http://dx.doi
.org/10.5061/dryad.km646 (Martin et al. 2015a). We regressed the average change in embryonic period of transferred eggs and those from their natal nests against the average difference in egg temperatures for the pair of species
included in the swap experiment. We did not measure egg
temperature in the individual nests used in swaps, and so
we could use only differences in average egg temperatures
of species. We excluded one transfer (P. capensis into D.
caffra) included in the original report (i.e., Martin et al.
2007) because the egg was transferred on the third day after
incubation started for D. caffra. Inclusion of this transfer
did not change the significance of the results. Here, we also
estimated the relative importance of temperature as the
cause of differences in duration of embryonic periods between species. We did this by dividing the change in embryonic period of the transferred egg by the observed difference in embryonic periods between the host and natal
nests and multiplying the result by 100, and we took the
mean across all swaps. This provided the percentage of the
difference in embryonic periods between species used in
the swaps that could be attributed to temperature.
We corrected for possible phylogenetic effects (Felsenstein 1985) by using the APE (Paradis et al. 2004) and
Mortality and Parental Effort
caper (Orme 2013) packages in R, version 3.0.3 for Windows (R Development Core Team, Vienna, Austria). Phylogenetic trees were obtained from www.birdtree.org (Jetz
et al. 2012) with the Hackett et al. (2008) backbone and
were imported into the program Mesquite (Maddison and
Maddison 2011), where they were ultrametricized, and a
majority-rules consensus tree based on 500 trees was constructed (fig. A1). This consensus tree was then used in
phylogenetically controlled analyses that incorporate Pagel’s l (Pagel 1992) to transform branch lengths and reduce
overcorrection for phylogenetic effects (Symonds and Blomberg 2014). We first calculated the maximum likelihood
estimate of Pagel’s l (Pagel 1992) by using the APE package rather than caper, because caper does not provide estimates of l < 0 (Orme 2013). We conducted phylogenetic
general least squares (PGLS) analyses with the caper package because it provides overall effect sizes (R2) of the models and optimizes branch-length transformations such that
it sets a Bayesian prior for l < 0 at 0, while delta and gamma
were set to 1 in all cases.
Results
A model examining covariance of annual adult mortality
probability with nest predation rates while controlling for
adult mass among sites yielded an estimated l of 20.466.
A negative l suggests that traits are less similar among
near relatives than among more distant relatives. This is
true of our data because of the divergence between latitudes in traits of near relatives (see Martin et al. 2000; Martin 2002; Martin and Schwabl 2008). For example, northtemperate members of Parulidae (Cardellina rubrifrons)
and Passerellidae (Junco hyemalis) have similar adult mortality probabilities of 0.429 and 0.433, respectively (table 1).
Similarly, tropical members of Parulidae (Myioborus miniatus) and Passerellidae (Arremon brunneinucha) have similar adult mortality probabilities of 0.208 and 0.198, respectively (table 1). Thus, species in different avian families had
more similar mortality estimates within a latitude than do
confamilial species among latitudes. The negative l, therefore, reflects that environmental conditions (i.e., latitude)
are more important than phylogeny in expression of these
traits, and l should be set to 0 to reflect this minimal phylogenetic influence.
With l set at 0, annual adult mortality probability differed among sites, being highest in the north-temperate
Arizona site, but adult mortality was not correlated with
nest predation rates or adult mass (nest predation rate:
t1, 57 p 21.12, P p .27; log10 mass: t1, 57 p 0.145, P p .89;
site (South Africa): t1, 57 p 24.13, P < .001; site (Venezuela): t1, 57 p 27.29, P < .001; site (Malaysia): t1, 57 p 26.87,
P < .001; R2 p 0.63). Thus, annual adult mortality probability and nest predation rates were not confounded in
229
analyses, but both varied extensively within and among
sites (table 1) to provide a strong basis for testing their possible influences on parental effort.
The l was also estimated as negative (20.212) in a model
for embryonic temperature with adult mortality probability, nest predation, mass, and site. The negative l again
reflects that near relatives diverged across latitudes, with
embryonic temperature often being more similar among
unrelated species in the same latitude than among near
relatives across latitudes (table 1; also Martin and Schwabl
2008). With l set at 0, adult mortality probability and nest
predation rates explained extensive variation in embryonic
temperatures, after body mass and site were accounted for
(R2 p 0.86; fig. 2; table 2A). Long-lived species with low
adult mortality exhibited lower parental effort, reflected in
cooler embryonic temperatures. Adults of long-lived species spent more time off the nest, which caused embryos
to cool to lower minimum temperatures and for longer
periods compared with shorter-lived species, even when
tropical species were compared with north-temperate species (fig. 2C). In addition, species with lower adult mortality also did not warm eggs to as high a maximum temperature as did shorter-lived species (note the highest, and
nighttime, temperatures relative to the reference line at
367C in fig. 2C). The result of longer and cooler off-bouts,
as well as cooler temperatures when on the nest, yielded
lower average temperatures in longer-lived species (see
fig. 2A, 2C).
Average embryonic temperatures differed among sites
(table 2A) and reflected a general regional pattern, with
north-temperate species generally at the high end, southtemperate species in the middle, and species from the two
tropical sites at the low end (fig. 2A). Nest predation risk
explained additional variation in parental incubation effort,
after we controlled for adult mortality effects (fig. 2B; table 2A). Ultimately, adult and offspring (nest) mortality explained most of the variation in parental effort manifested
as egg temperature (fig. 2; table 2A).
These age-specific influences on parental effort become
particularly important if embryonic temperature influences
embryonic development. The l was estimated as 20.610
for embryonic development time modeled with average egg
temperature, adult mortality, nest predation, body mass,
and site. The negative l reflects the strong divergence in
embryonic development time between latitudes for related
species (Martin 2002; Martin and Schwabl 2008), again indicating that environmental effects are more important
than phylogenetic ones for embryonic development time.
Indeed, with l set at 0, embryonic development time was
strongly related to average egg temperature across species
(fig. 3A; table 2B). Adult mortality, nest predation rates,
and adult mass did not explain any additional variation in
embryonic development time after egg temperature was ac-
The American Naturalist
1
Embryonic temperature (°C)
A
1 – Turdus migratorius
C
36
1
28
0
2
20
2 – Apalis thoracica
-1
3
36
Arizona
South Africa
-2
Malaysia
Venezuela
4
-0.2
-0.1
0.0
0.1
28
0.2
20
Adult mortality probability
3 – Synallaxis cinnamomea
36
Embryonic temperature (°C)
2
B
28
1
2
20
4 – Pellorneum pyrrogenys
36
0
3
Embryonic temperature (°C)
230
1
28
-1
20
4
-0.04
-0.02
0.00
0.02
0.04
Nest predation rate
0.06
0
6
12
18
0
6
12
18
0
Hour of the day
Figure 2: Embryonic temperature and age-specific mortality across 63 bird species from tropical and temperate sites. A, Embryonic temperature is higher in species with higher annual adult mortality probability, when corrected for daily nest predation rates and log10 mass.
B, Embryonic temperature is also higher in species with higher daily nest predation risk, when corrected for annual adult mortality probability and log10 mass. C, Examples of egg temperature variation across 48 h (0 p midnight) for days 3 and 4 of the embryonic period for a
representative species from each of the four sites. The white downward spikes occur when parents leave the nest and eggs cool. Longer-lived
tropical species commonly take longer off-bouts that cause eggs to cool more and also do not warm eggs as much as north-temperate species
(compare high temperatures to the reference line at 367C, especially at night around midnight). Numbers in A and B correspond to species in
C. Site was not taken into account for these figures to allow illustration of differences among sites.
counted for (table 2B). Moreover, the strong divergence
in embryonic periods among latitudinal sites largely disappeared once effects of the equally strong divergences in egg
temperature were taken into account (table 2B).
The causal importance of temperature for embryonic periods was clearly demonstrated by the transfer experiment:
the average change in embryonic period of transferred eggs
was highly predicted by the average change in temperature
between natal and host species (fig. 3B). Moreover, the average change in embryonic period due to temperature across
all swaps accounted for 60.4% 5 4.5% of the difference in
embryonic periods between natal and host nests, leaving
Mortality and Parental Effort
231
Table 2: Overall model effect size (R2) and coefficients (B) and their standard errors, t values, degrees of
freedom, and significance for 63 songbird species from Arizona, South Africa, Venezuela, and Malaysia
Variable
A. Average 24-h egg temperature as dependent variable:
Adult mortality probability
Nest predation rate
Log10 body mass
Site (South Africa)
Site (Venezuela)
Site (Malaysia)
Error
B. Embryonic period as dependent variable:
Average 24-h egg temperature
Adult mortality probability
Nest predation rate
Log10 body mass
Site (South Africa)
Site (Venezuela)
Site (Malaysia)
Error
B (SE)
t
df
P
7.23 (.634)
15.37 (2.77)
.421 (.179)
.178 (.266)
.234 (.194)
2.456 (.200)
11.40
5.55
2.35
.67
1.21
22.28
1
1
1
1
1
1
56
!.001
!.001
.022
.51
.23
.027
22.17 (.29)
1.79 (2.53)
4.77 (7.53)
.54 (.410)
2.400 (.584)
.853 (.429)
2.368 (.458)
27.44
.71
.63
1.32
2.68
1.99
2.80
1
1
1
1
1
1
1
55
!.001
.48
.53
.19
.50
.052
.43
Note: R2 p 0.86 for both A and B. Significance is from phylogenetic generalized least squares analysis using the caper package (Orme 2013).
39.6% 5 4.5% due to intrinsic and other unmeasured influences on development rates.
Discussion
The consistently negative l’s estimated in the phylogenetic
analyses indicated that the traits explored here were labile and more strongly influenced by environmental than
by phylogenetic effects. Indeed, age-specific mortality explained an extensive amount of variation in songbird parental care strategies across the world (fig. 2; table 2A). The
increase in parental incubation effort in species with greater
adult mortality (i.e., fig. 2A) follows from life-history theory and empirical evidence of other parental traits, such
as fecundity (e.g., Williams 1966; Crowl and Covich 1990;
Reznick et al. 1990, 1996; Barbraud and Weimerskirch
2001; Martin 2002, 2014). In contrast, the increase in parental effort in species with greater nest predation risk
(i.e., fig. 2B) is opposite to this theory. Instead, the results
follow from expectations for reducing risk via shortened
embryonic periods and shortened exposure to predators
(Weathers and Sullivan 1989; Martin 2002; Fontaine and
Martin 2006). Early theory considered the effects of juvenile
mortality on energy expenditure versus self-maintenance
within the context of increased self-maintenance allowing
increased within-season or between-season iteroparity (e.g.,
Williams 1966; Murphy 1968; Hirshfield and Tinkle 1975;
Law 1979; Michod 1979; Charlesworth 1994). This theory
did not take into account the possibility that parental effort
could reduce the risk of the current effort, via shortening
of the period of risk. Thus, theory concerning the effects
of age-specific mortality for parental effort has to consider
not only the costs to the parents, in terms of residual reproductive value, but also the potential benefits of reduced
current offspring mortality risk.
The benefits of increased parental effort for reducing
exposure time to nest predation risk depend on a causal
influence of parentally induced temperature on development time. Our swapping experiments, as well as other
experiments, demonstrate that parental effort in warming
eggs is a clear causal influence on embryonic development
time (fig. 3; also see Martin et al. 2007; Du et al. 2009;
Nord and Nilsson 2011; Hepp and Kennamer 2012). Indeed, temperature accounted for a strong proportion (i.e.,
60%) of the difference in development time between species (see “Results”; fig. 3B). The relative influence of temperature on development time is important to understand
because temperature effects on development time have opposing effects on offspring quality, compared with intrinsic effects. Longer (i.e., slower) development time that is
caused by intrinsic mechanisms can yield benefits to offspring quality and adult longevity (McCay 1933; Ricklefs
1993, 2006; Arendt 1997; Rollo 2002; Metcalfe and Monaghan 2003; Kim et al. 2011; Lee et al. 2013). In contrast,
longer development periods that are primarily caused by
cooler temperatures do not yield higher-quality offspring
or lower mortality within species (Hare et al. 2004; Ardia
et al. 2010; Nord and Nilsson 2011; DuRant et al. 2012;
Hepp and Kennamer 2012). Instead, these extrinsic temperature effects can mask physiological benefits of slower
232
The American Naturalist
Embryonic period (d)
20
A
18
embryonic period
of transferred egg
in host nest
natal nest
16
tra
ns
14
12
10
32.5
fer
Arizona
South Africa
Malaysia
Venezuela
33.0
33.5
}
}
34.0
34.5
35.0
35.5
36.0
temperature
effect
intrinsic
effect
host nest
36.5
Change in embryonic period (d)
Embryonic temperature (°C)
B
1
0
-1
-2
-3
r = -0.94, P < 0.001
-1
0
1
2
Egg temperature difference
(mean host spp − mean natal spp)
Figure 3: Effects of temperature on embryonic periods of 63 bird species from tropical and temperate sites. A, Embryonic period is strongly
correlated with average 24-h egg temperature. The open triangle is hypothetical to illustrate the egg-transfer experiment. An egg from the
natal nest is transferred to the host nest, and the change in embryonic period is reflected by the hypothetical triangle, where the embryonic
period is shorter than that for eggs in the natal nest but still longer than that for eggs in the nest of the host species. Site was not taken into
account to allow illustration of differences among sites. B, Change in embryonic period of a transferred egg relative to that in its natal nest
versus the difference between the average egg temperatures of the natal and host species. The change in embryonic period is an average for
each pair of species, as is the temperature difference.
intrinsic development (Martin and Schwabl 2008; Martin
et al. 2013). Indeed, variation in embryonic periods was
not explained by physiological processes such as metabolic
rates of embryos (Martin et al. 2013), nor did it explain
variation in offspring quality as measured by immune
function (Palacios and Martin 2006; Martin et al. 2011)
when embryonic temperature was not considered (also
see Ardia et al. 2010; DuRant et al. 2012; Arriero et al.
2013).
When embryonic temperature is taken into account,
physiological processes such as metabolism explained residual variation in embryonic periods (Martin et al. 2013)
and accounted for variation in offspring immune response
(Martin et al. 2011). These residual intrinsic effects make
sense, given that the egg-transfer experiment demonstrated
that intrinsic and other unmeasured effects accounted for
∼40% of the difference in development times between species (see “Results”). In short, physiological processes explained some of the variation in length of embryonic period
and offspring quality, but only once larger temperature effects were taken into account. Yet adult mortality was not
related to embryonic time after embryonic temperature
was accounted for (table 2B), suggesting that residual intrinsic effects on embryonic development time do not account for the broad variation in adult mortality among species. Similarly, development rates of postnatal offspring (i.e.,
Mortality and Parental Effort
after hatching) explained no variation in adult mortality
during a stage when temperature is much less important
(Martin et al. 2015b).
The inability to explain variation in adult mortality by
intrinsic influences on development may result from selection acting on several potential trade-offs (fig. 4). The probability of the nest being discovered by a predator increases
with each day the eggs remain in the nest, which can favor the faster embryonic development observed across species with higher nest predation risk (e.g., Martin 2002; Martin et al. 2007; Remeš 2007). Faster development may be
accomplished through physiological processes that can affect offspring quality and adult mortality (e.g., Arendt 1997;
Billerbeck et al. 2001; Metcalfe and Monaghan 2003; Ricklefs 2006; Lee et al. 2013). Yet adult mortality may be influenced more strongly by environmental influences, such
as predation, migration, or non–breeding season stressors
(e.g., Rowley and Russell 1991; Sillett and Holmes 2002;
Evans et al. 2006; Turbill et al. 2011), than by physiological
costs of growth and development (see Martin et al. 2015b).
Indeed, shortening development time through warmer temperatures, rather than physiological processes, may reduce
impacts of faster intrinsic development on offspring quality
(e.g., Martin and Schwabl 2008; Martin et al. 2011). Still, the
effort in warming eggs to achieve this faster development
represents an energetic cost to parents (e.g., Vleck 1981;
Moreno and Carlson 1989; Williams 1996) that can create
a cost of reproduction (Visser and Lessells 2001). Increased
incubation effort may also expose parents to increased risk
of predation on themselves (Magrath 1988; Arnold et al.
2012). Ultimately, increased parental effort to warm eggs
and reduce exposure time of embryos to nest predators must
be balanced against the risks to adult mortality. Life-history
theory predicts that longer-lived species should reduce these
potential costs through reduced incubation time and effort,
as we found here (fig. 2). The clear interaction of both nest
predation and annual adult mortality in explaining paren-
Adult
mortality
233
tal effort in warming eggs (fig. 2), despite their lack of covariance (see “Results”), and the influence of both temperature (fig. 3) and intrinsic processes (see “Results”) on
embryonic time suggest interaction of all of these effects
(fig. 4).
The extensive variation in parental time warming eggs
within and across diverse geographic regions (fig. 1) also
can have unrecognized consequences with respect to climate change. Species with low adult mortality spend the
least amount of time on the nest and expose their embryos
to ambient temperature much more than species with high
adult mortality (fig. 2A, 2C). As a result, embryos of these
species experience the largest consequences of changes in
ambient temperature. Given that tropical birds commonly
have the lowest adult mortality, associated with the lowest
parental effort and greatest exposure of embryos to ambient temperature (fig. 2A, 2C), they are the most exposed to
the potential impacts of increased ambient temperatures
during this life stage. This exposure could yield benefits
under global warming, given that warmer temperatures
during off-bouts may provide physiological benefits and
cause shorter embryonic periods that reduce exposure time
to predation.
Ultimately, parental incubation effort exhibited broad
geographic patterns that covaried with age-specific mortality across diverse songbird taxa (figs. 1, 2). The ability
of age-specific mortality to explain extensive variation in
parental effort in warming eggs (fig. 2) is a unique result
that follows from life-history theory (e.g., Williams 1966;
Michod 1979; Charlesworth 1994; Martin 2002, 2014). It
also provides evidence of a possible causal mechanism for
explaining broad geographic patterns in life-history variation. At the same time, the trade-offs between costs of parental effort to residual reproductive value and benefits of
greater parental effort for reduced nest predation and increased offspring quality (fig. 4) could use further exploration and modeling.
Parental
Effort
Embryonic
period length
Nest
predation
Physiological
processes
Figure 4: Adult and offspring (nest predation) mortalities interact to influence both parental effort in warming eggs and intrinsic physiological processes, both of which influence embryonic period length. As a result, embryonic period length can influence adult mortality because of physiological trade-offs and can influence nest predation risk because of the length of time exposed to predators.
234
The American Naturalist
Acknowledgments
We are grateful to S. Ducatez, L. Kruuk, J. LaManna,
M. Symonds, H. A. Woods, and our lab for helpful comments on the manuscript. We are also grateful to M. Lakim,
Sabah Parks, and the Sabah Biodiversity Centre for their
help in Malaysia; G. Greeff, Eskom, and the Western Cape
Nature Conservation Board in South Africa; and C. Bosque,
the Instituto Nacional de Parques, and the Fondo Nacional
de Ciencia, Tecnología y Innovación (Fonacit) in Venezuela. This work was supported by the National Science
Foundation (grants DEB-0841764, DEB-1241041, and IOS1349178), and the US Geological Survey Climate Change
Research Program. This work was conducted under the auspices of University of Montana Institutional Animal Care
and Use Committee protocol 059-10TMMCWRU. Any
use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US
Government.
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Associate Editor: Michael Kearney
Editor: Judith L. Bronstein
A Temminck’s babbler (Pellorneum pyrrogenys) from Malaysian Borneo on its nest. This tropical species is long-lived, with 90% of individuals surviving each year. It incubates for only 40% of daylight hours, causing egg temperatures that are relatively cold compared with the
temperatures that embryos need for development. Photograph by Thomas E. Martin.