Journal of Animal Ecology 2010, 79, 1086–1092
doi: 10.1111/j.1365-2656.2010.01720.x
Can selection on nest size from nest predation explain
the latitudinal gradient in clutch size?
Luis Biancucci* and Thomas E. Martin
USGS Montana Cooperative Wildlife Research Unit, 205 Natural Sciences Building, University of Montana, Missoula, MT
59812, USA
Summary
1. Latitudinal variation in clutch sizes of birds is a well described, but poorly understood pattern.
Many hypotheses have been proposed, but few have been experimentally tested, and none have
been universally accepted by researchers.
2. The nest size hypothesis posits that higher nest predation in the tropics favours selection
for smaller nests and thereby constrains clutch size by shrinking available space for eggs and ⁄ or
nestlings in the nest. We tested this hypothesis with an experiment in a tropical forest and a
comparative study between temperate and tropical field sites.
3. Specifically, we tested if: (i) predation increased with nest size; (ii) tropical birds had smaller
nests controlled for body size; and (iii) clutch size was explained by nest size controlled for body
size.
4. Experimental swapping of nests of different sizes showed that nest predation increased with nest
size in the tropical site. Moreover, nest predation rates were higher in species with larger nests in
both sites. However, nest size, corrected for body mass and phylogeny, did not differ between sites
and was not related to clutch size between sites.
5. Hence, nest predation can exert selection on nest size as predicted by the hypothesis. Nest size
increased with adult body mass, such that adult size might indirectly influence reproductive success
through effects on nest size and nest predation risk. Ultimately, however, selection from nest predation on nest size does not explain the smaller clutch sizes typical of the tropics.
Key-words: altricial birds, body size, life histories, nest predation rate
Introduction
One of the broadest patterns of variation in clutch size is the
latitudinal gradient of increase from the equator to the poles,
and this pattern has long intrigued biologists (Moreau 1944;
Lack 1947; Pianka 1966; Martin et al. 2000; Cardillo 2002;
Martin 2004). Nest predation is a commonly invoked explanation for this latitudinal pattern that can act through differing proposed mechanisms (Skutch 1949; Slagsvold 1982a;
Lima 1987; Kulesza 1990; Martin 1992; Martin & Briskie
2009). One proposed mechanism suggests that natural selection favours smaller nest sizes in tropical environments
because of high risk of nest predation, and smaller nests constrain clutch-size (Lill 1975; Snow 1978). Those authors supported their hypothesis with examples of tropical species
such as manakins (Pipridae) that have very small nests and
small clutch sizes of two eggs. Yet, such anecdotal examples
*Correspondence author. E-mail: luis.biancucci@gmail.com
do not test the generality of the hypothesis nor provide any
information about its reliability. Subsequent tests of the nest
size hypothesis focused on north temperate species, while
tests in the tropics are completely lacking. A strong test of
this hypothesis must include tropical bird species as they
form the basis of the original formulation of the hypothesis.
The nest size hypothesis makes three key testable predictions. First, nest predation rates must increase with nest size
to create selection for smaller nests. This prediction has been
tested with equivocal results. Larger nests had higher nest
predation rates than smaller nests within some north temperate species (Møller 1982; Sieving & Willson 1998; LopézIborra et al. 2004), but not in all cases (Slagsvold 1989a;
Palomino et al. 1998; Weidinger 2004). Thus, the effect of
nest size on predation risk remains unclear, and tests across
species as well as in the tropics are lacking. A second prediction is that clutch size increases with nest size. This is exactly
the case within each of several hole-nesting bird species
(Karlsson & Nilsson 1977; Møller 1982). Clutch size can
also be positively related to nest size within some open-cup
2010 The Authors. Journal compilation 2010 British Ecological Society
Clutch size, nest size, and nest predation 1087
nesting species, although larger nests also can increase hatching failure (Slagsvold 1982b, 1989a,b). Still, these intraspecific tests do not address the interspecific pattern in clutch
size originally proposed. Tests of relationships between nest
size and clutch size across species are lacking, especially
between temperate and tropical locations. A third untested
prediction is that if small nest size explains small clutch size in
tropical birds, then nests should be smaller in the tropics,
after correcting for body size.
The nest size hypothesis has one key assumption: nest predation is assumed to be higher in the tropics. High nest predation has been documented in several tropical sites (Snow &
Snow 1963; Skutch 1966; Kulesza 1990; Gibbs 1991; Roper
1992; Robinson et al. 2000), but predation is not universally
high in the tropics (Oniki 1979; Skutch 1985; Martin 1996;
Söderström 1999). Thus, the ability of nest predation to
explain nest size and clutch size in tropical birds remains
unclear.
In this paper we tested the nest size hypothesis in tropical
and temperate sites. We started by experimentally testing the
prediction that nest predation risk increases with nest size in
a tropical Venezuelan cloud forest. We followed by conducting a comparative field study of nest size, nest predation
rates, adult body mass, and clutch sizes of birds from tropical
(i.e. Venezuela) and north temperate (i.e. Arizona) sites. We
conducted this comparative study to test the three key predictions that: (i) nest predation increases with nest size; (ii) nests
are smaller in the tropics after controlling for body mass; and
(iii) nest size constrains clutch size.
Material and methods
STUDY SYSTEMS
Experimental and comparative data were collected in Yacambú
National Park, Venezuela, a tropical cloud forest (1350–2000 m elevation) at the northern end of the Andes (9 N latitude) (Martin et al.
2006, 2007). Comparative data on north temperate species were collected in Coconino National forest, Arizona, from high elevation forest drainages (2300 m elevation) of mixed coniferous and deciduous
canopy tree species (34 N latitude) (Martin 2007).
gradient of nest sizes (Table 1). Myrmotherula has a nest of black
rootlets that is very thin-walled to the extent that you can see through
parts of the nest. Dysithamnus has a very similar nest, slightly bigger,
and with variable amounts of hanging mosses on the outside. Catharus has a more substantial nest with thick walls of mosses on the outside and leaves and thin grasses on the inside. Turdus had very solid
nests made of sticks, moss and thick grasses on the outside; and black
rootlets on the inside. Arremon had a large messy nest of sticks, and
dry leaves on the outside and dry leaves and grasses on the inside.
Old nests of the experimental species were first located. Then the
exact sites were marked and nests removed for later use. After the old
nests were removed, each marked nest site was used to run one control and one experimental trial of the experiment. At each nest site
two different nests were placed alternately: (i) a nest belonging to the
same species as the original at the site (control trial); and (ii) a nest of
a different species and a different size than the original (experimental
trial). The order of presentation of control and experimental trials at
each site was random to control possible time effects. Effects of nest
site and habitat were controlled by pairing control and experimental
nests at the same site. Both human biases and the effects of parental
behaviour on predation risk were minimized by using real nests and
sites chosen by birds. Each nest was tied to the substrate with green
floral wire and baited with one quail Coturnix coturnix egg. Quail
eggs can introduce some experimental bias in systems where snakes
are the main predators (Marini & Melo 1998), but snakes were not
important in our system. Birds are the main nest predators based on
seven seasons of videotaping nests and from data logger data showing that the vast majority of predation events occurred during the
day (Martin, unpublished data). The distance between different nest
sites was always >10 m, but generally >40 m, and spread over
5 km. The nests where checked daily until they were depredated, or
until day 14, when the egg was removed and the trial ended. Trials at
a single nest site were separated by 10 day periods to avoid learning
by predators.
The nests were considered a half sphere to calculate total surface
area and surface area of the top of the nest (Table 1). These estimates
were based on external height and diameter of every nest obtained
with a ruler or metric tape immediately after the nest was placed.
Cover was measured as the percent of the nest that was visible from
1 m away at the level of the nest from four directions (N, S, E, and
W). Surface area was selected as the variable of key interest because
we assume it is the dimension most easily detected by visually oriented predators.
LATITUDINAL COMPARISON
NEST SWAP EXPERIMENT
To assess if nest size affects nest predation rates in a tropical forest,
an experiment was performed at the Venezuela field site. A nest swap
experiment with a crossover experimental design was performed
making use of old nests of five bird species that represented a strong
We studied 14 north temperate and 22 tropical altricial bird species
from Arizona and Venezuela, respectively (Table 2). Only species
with open-cup nests and robust estimates of nest predation rates
across many years of study (Martin et al. 2006, 2007) were considered. In particular, we used data on predation rates from 23 years of
Table 1. Species used in the nest swap experiment with the mean (±SE) surface areas of the experimental nests
Species
Latin name
Code
Surface area (cm2)
Slaty Antwren
Plain Antvireo
Slaty-backed Nightingale-Thrush
Black-hooded Thrush
Chestnut-capped Brush-finch
Myrmotherula schisticolor
Dysithamnus mentalis
Catharus fuscater
Turdus olivater
Arremon bruneinucha
SLAN
PLAN
SBNT
BHTH
CCBF
41Æ0
55Æ3
145Æ2
254Æ5
267Æ5
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 1086–1092
±
±
±
±
±
1Æ25
1Æ45
4Æ64
6Æ52
14Æ01
1088 L. Biancucci & T. E. Martin
Table 2. Species included in the comparative analysis
Species
M
ID
OD
IH
OH
N
S
Streptoprocne rutila**
Cypseloides cherriei
Coeligena coeligena
Heliodoxa leadbeateri
Sternoclyta cyanopectus
Empidonax occidentalis
Myiodynastes chrysocephalus
Masius chrysopterus
Dysithamnus mentalis
Myrmotherula schisticolor
Grallaricula ferrugineipectus
Turdus olivater
Turdus serranus
Turdus flavipes
Turdus migratorius
Catharus fuscater
Catharus aurantiirostris
Catharus guttatus
Myadestes ralloides
Arremon brunneinucha
Atlapetes semirufus
Junco hyemalis
Pipilo chlorurus
Spizella passerina
Vermivora celata
Vermivora virginiae
Dendroica coronata
Cardellina rubrifrons
Oporornis tolmiei
Piranga ludoviciana
Pheucticus melanocephalus
Saltator maximus
Thraupis episcopus
Tachyphonus rufus
Ramphocelus carbo
Vireo gilvus
20Æ00
23Æ63
6Æ59
6Æ70
6Æ67
11Æ55
41Æ0
13Æ22
15Æ05
9Æ77
16Æ46
70Æ21
66Æ00
52Æ73
76Æ65
31Æ61
26Æ96
29Æ32
29Æ45
44Æ99
28Æ76
20Æ75
29Æ48
12Æ40
9Æ12
8Æ50
12Æ55
9Æ57
10Æ95
30Æ18
44Æ52
39Æ84
30Æ35
30Æ15
24Æ14
12Æ12
5Æ58
4Æ98
4Æ31
3Æ42
3Æ27
5Æ14
7Æ30
5Æ40
5Æ42
5Æ11
5Æ79
8Æ53
8Æ41
8Æ05
9Æ47
6Æ55
6Æ14
6Æ52
7Æ08
7Æ44
6Æ79
6Æ49
7Æ04
5Æ79
5Æ40
5Æ49
5Æ24
5Æ36
5Æ19
6Æ50
6Æ20
7Æ41
6Æ15
7Æ26
5Æ94
4Æ95
8Æ00
8Æ52
7Æ25
5Æ02
4Æ92
9Æ42
11Æ30
6Æ90
7Æ49
6Æ77
12Æ71
15Æ37
14Æ03
14Æ29
13Æ62
11Æ70
11Æ47
12Æ16
12Æ30
14Æ53
12Æ59
11Æ15
12Æ44
9Æ36
9Æ15
9Æ16
8Æ94
9Æ72
11Æ49
13Æ75
13Æ17
14Æ03
12Æ05
13Æ18
9Æ65
7Æ05
2Æ47
3Æ08
3Æ24
2Æ86
1Æ96
3Æ13
4Æ55
3Æ20
4Æ44
4Æ05
2Æ29
5Æ04
5Æ58
4Æ64
5Æ96
5Æ30
4Æ51
4Æ59
4Æ11
5Æ38
4Æ94
4Æ08
4Æ78
3Æ57
3Æ73
3Æ46
3Æ31
3Æ78
4Æ47
4Æ35
4Æ18
5Æ91
3Æ45
5Æ11
4Æ90
4Æ35
7Æ67
6Æ02
10Æ65
6Æ22
5Æ84
6Æ61
7Æ90
4Æ24
6Æ19
5Æ52
4Æ74
10Æ97
11Æ41
10Æ15
10Æ07
13Æ48
9Æ68
8Æ48
9Æ86
10Æ70
9Æ24
5Æ84
7Æ73
5Æ61
5Æ45
5Æ12
5Æ10
5Æ60
7Æ45
7Æ20
8Æ69
10Æ14
6Æ20
9Æ86
8Æ11
6Æ25
10
5
32
14
40
49
2
12
90
84
34
47
8
46
60
319
62
267
46
266
29
633
98
7
383
251
8
7
17
2
7
19
2
19
11
11
V
V
V
V
V
A
V
V
V
V
V
V
V
V
A
V
V
A
V
V
V
A
A
A
A
A
A
A
A
A
A
V
V
V
V
A
Latin names of Venezuelan species follows Remsen et al. (2010);
Arizona species follows the AOU Check-List of North American
Birds (2010)
**Adult mass from Hilty (2003).
M, adult mass (g); ID, inner diameter of nest cup (cm); OD, outer
diameter (cm); IH, inner height (cm); OH, outer height (cm); N,
sample size for nest size dimensions; and S, site that species was
studied (V, Venezuela; A, Arizona).
study in Arizona and 7 years of study in Venezuela. This resulted in
predation rates based on 11 426 nests for the 14 study species in
Arizona and 2253 nests for the 22 study species in Venezuela.
Nest sizes of 1763 nests from Arizona and 1146 nests from Venezuela were included in the study. Daily predation rates, clutch size, and
nest dimensions for all of these species were measured. In Venezuela
the nests were measured as early in the nesting stage as possible, usually within 1–4 days of start of incubation, to avoid any effects of rain
on the size of the nest. In Arizona, where the climate is generally dry
and nests do not significantly change in size due to weather, the nests
were measured any time during the incubation or early nestling period (<day 4). In addition to surface areas, mean inner volumes were
calculated for each species considering the inner cup of the nest as a
half-sphere. Inner volume was selected because this dimension
reflects space for eggs and nestlings in the nest which ultimately may
constrain clutch size if the nest size hypothesis is true. Adult body
mass was obtained by netting and weighing adults at both field sites
except for Streptoprocne rutila, which was obtained from Hilty
(2003) (Table 2). Our study species did not differ in adult mass
between the tropical and temperate sites (anova, F1,34 = 0Æ97,
P = 0Æ33).
DATA ANALYSIS
Nest size experiment
This experiment tested the first prediction that nest predation
increases with nest size in the tropical site. At each nest site, we calculated the differences between treatments for daily predation rate
(DPR, Mayfield 1975), arc sine of average cover, and nest surface
area. DPR were calculated because they incorporate predation events
and the speed (days of exposure prior to predation) at which they
occurred. Treatment differences were calculated by subtracting the
values of experimental minus control trials. This resulted in continuous real differences in sizes of nests used for the trials. For example, if
the experimental nest was larger than the paired control nest, then
the difference was some value >0. When the experimental nest was
smaller than the control then the difference was some value <0. Similarly, if predation occurred more quickly (in fewer days of exposure)
at an experimental nest than its paired control, then the difference in
DPR was >0. Differences in DPRs were used as the dependent variable in regression analysis of differences in surface area, while controlling for possible effects of differences in average cover. Those nest
sites that were never discovered by predators (i.e. both experiment
and control trials at that site were never predated) were excluded
from the analysis assuming that lack of predation was a site-specific
effect (Martin, Scott & Menge 2000) and because they provide no
information on effects of nest size differences on nest predation. Such
effects are assumed to be random with respect to nest size differences
if they are truly site effects. We tested this assumption by testing
whether the mean difference in surface area at those sites were equal
to zero and normally distributed in order to ensure that we were not
excluding any unexpected effect of nest size.
Latitudinal comparison
We tested if nest predation rates increased with nest sizes (first prediction) across species in both the temperate and tropical field sites using
ancova with DPR as the dependent variable, field site as a factor and
surface area of the nest as a covariate. Predation effects may act on
external nest size (surface area), but external size should be related to
inner volume of the nest for nest size to act as a constraint on clutch
size. Therefore, we examined the relationship between surface area
and inner volume in both sites and tested whether inner volume was
smaller for a given surface area in the tropics. We used ancova with
inner volume as the dependent variable, field site as a factor, and surface area as a covariate. Finally, we tested if nests were smaller in the
tropical than north temperate site (second prediction) using two ancovas with inner nest volume and surface area as the dependent variables. In both cases, we used field site as a factor, and adult body
mass as a covariate. We calculated independent contrasts (Felsenstein 1985) with the residual of the linear regression between inner
volume of the nest and adult body mass, and a dummy variable for
field site to control for phylogenetic effects. The phenotypic diversity
analysis programs (PDAP) module of program Mesquite (Midford,
Garland & Maddison 2008; Maddison & Maddison 2009) that
follows Garland, Harvey & Ives (1992) was used for all calculations.
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 1086–1092
Clutch size, nest size, and nest predation 1089
0·10
Arizona
Venezuela
0·08
Daily predation rate
A phylogenetic hypothesis was developed based on Burns (1997),
Yuri & Mindell (2002), Outlaw et al. (2003), Lovette & Bermingham
(2002), Klicka, Voelker & Spellman (2005), and Jønsson & Fjeldså
(2006). To determine if clutch size was correlated with nest size across
field sites (third prediction), we conducted an ancova with clutch size
as the dependent variable, field site as a factor, and nest inner volume
and adult body mass as covariates. We also conducted independent
contrasts between adult body mass and nest inner volume as
described above. The same analyses were repeated using external volume of the nest instead of inner volume. The results were qualitatively similar, and they were not included here. In all tests we
included interactions in an initial model and then removed them if
they were not significant. Interactions were not significant in any of
the tests, so we only report main effects.
0·06
0·04
0·02
0·00
0
20
40
60
80
100 120 140 160 180 200
Nest surface area (cm2)
Results
NEST SWAP EXPERIMENT
1·0
0·5
LATITUDINAL COMPARISON
Nest predation rate not only increased with nest size in the
experiment, but also increased with mean nest size across species (Fig. 2). However, only 21% of the variance was
explained (surface area: F1, 33 = 8Æ0, P = 0Æ008, r2 = 0Æ21),
and nest predation rate controlled for nest size did not differ
between sites (site: F1, 33 = 0Æ8, P = 0Æ38). Nonetheless, the
increase in predation with nest size set up the possibility that
nest predation constrains nest size in the tropics.
Nest predation may act on the external surface area, but
clutch size should be constrained by the inner volume that
holds eggs and nestlings. Birds might reduce the thickness of
the nest walls to reduce external size without compromising
internal volume, and such alterations would yield significant
site effects in the ancova. Inner volume was very strongly
related to surface area (Fig. 3) at both sites (surface area: F1,
2
33 = 58Æ2, P < 0Æ001, r = 0Æ64) but the relationship did
not differ between sites (site: F1, 33 = 0Æ2, P = 0Æ6).
0·0
120
–0·5
–1·0
–400
–300
–200
–100
BHTH-CCBF
CCBF-SBNT
BHTH-PLAN
CCBF-SLAN
BHTH-SBNT
PLAN-SBNT
BHTH-SLAN
PLAN-SLAN
CCBF-PLAN
SBNT-SLAN
0
100
200
300
Differences in nest surface area
(experiment – control)
Fig. 1. Differences in daily predation rates and differences in surface
area at 58 nest sites. Values <0 reflect experimental nests that
were smaller than paired control nests or daily predation rates that
were less than at control nests. Values >0 reflect the opposite. The
different symbol shapes indicate the pair of species that
were swapped at each site. BHTH: Black-hooded Thrush, CCBF:
Chestnut-capped Brush-finch, PLAN: Plain Antvireo, SBNT:
Slaty-backed Nightingale-Thrush, SLAN: Slaty Antwren.
Inner volume of the nest (cm3)
Differences in daily predation rate
(experiment – control)
The difference in nest size between experimental and control
nests varied substantially because nest size varied within as
well as across species. This allowed us to examine the
responses by predators to this continuous variation in nest
size differences (i.e. Fig. 1). Differences in DPRs were positively related to differences in surface area (rp = 0Æ45,
P < 0Æ001; d.f. = 55) and unrelated to differences in vegetation cover at the nest site (rp = )0Æ034; P = 0Æ80). Specifically, predation rates decreased when experimental nests
were smaller than the control and predation risk increased
when experimental nests were larger than their paired controls (Fig. 1). Thus, nest size can influence nest predation risk
in this tropical system.
Fig. 2. Nest surface area and nest predation rates for 36 altricial bird
species studied in tropical Venezuela and temperate Arizona. Nest
predation increased with nest surface area and the relationship is
similar in both field sites.
Arizona
100
Venezuela
80
60
40
20
0
0
20
40
60
80
100 120 140 160 180 200
Nest surface area (cm2)
Fig. 3. Nest inner volume was strongly related to external surface
area and the relationship was similar in both field sites.
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 1086–1092
1090 L. Biancucci & T. E. Martin
120
100
4
(a)
Arizona
Venezuela
Venezuela
Clutch size
Nest inner volume (cm3)
Arizona
80
60
3
2
40
20
1
0
0
20
40
60
80
(b)
Adult body mass (g)
We next tested whether tropical species had smaller nests,
while controlling for possible body size effects. Inner volume
of the nest increased strongly with adult mass (adult mass:
F1, 33 = 169Æ9, P < 0Æ001, r2 = 0Æ84) but did not differ
between sites (Fig. 4) for a given body mass (site: F1,
33 = 1Æ2, P = 0Æ3). Independent contrasts of the residuals of
linear regression between inner volume of the nest and adult
body mass confirmed that mass-corrected nest size was not
related to the field site (r = 0Æ07, P = 0Æ98). Surface area
also was strongly related to log-transformed adult mass
(adult mass: F1, 33 = 103Æ3, P < 0Æ001, r2 = 0Æ76), but did
not differ between sites (site: F1, 33 = 2Æ6, P = 0Æ12). Thus,
neither internal nor external nest size was smaller at the tropical site while controlling for body size, and the primary fundamental difference between latitudes expected under the
nest size hypothesis was not supported.
Clutch size was smaller in Venezuela than Arizona (Martin
et al. 2006) even though nest size was not. The general lack of
difference in nest size between latitudes (i.e. Fig. 4) suggested
that nest size did not explain clutch size differences. Indeed,
clutch size differed between sites, but was not related to inner
volume of the nest after controlling for adult body mass
(Fig. 5a; site: F1, 32 = 196Æ9, P < 0Æ001; inner volume: F1,
32 = 1Æ4, P = 0Æ2; adult mass: F1, 32 = 2Æ2, P = 0Æ15). The
result was the same even when we analyzed only families with
members in both field sites (Fig. 5b). For example, Turdus
olivater from Venezuela and the congeneric Turdus migratorius in Arizona have similar masses and nest sizes, but clutch
sizes show the classic latitudinal differences. Analysis of independent contrasts between clutch size and inner volume of
the nest also was not significant (r = 0Æ005. P = 0Æ45). Thus,
nest size did not explain clutch size variation within or
between latitudes.
Discussion
We report the first experimental test in the tropics and the
first comparative test within and across latitudes of the nest
size hypothesis. Some, but not all, previous studies have dem-
Clutch size
Fig. 4. Nest inner volume was strongly related to adult body mass in
both field sites.
4
3
2
1
–30
Cardinalidae
Emberizidae
Thraupidae
Turdidae
Tyrannidae
–20
–10
0
10
20
30
Nest size controlled for adult body mass
Fig. 5. (a) Clutch size plotted against the residuals from the regression of inner nest volume on adult body mass; and (b) when only
including the families with members in both field sites, showing that
species with similar body and nest sizes have larger clutch sizes in the
north temperate than tropical site.
onstrated that nest predation risk increases with nest size
(Lopéz-Iborra et al. 2004; Møller 1990; Sieving & Willson
1998; Willson & Gende 2000; but see Palomino et al.; Weidinger 2004). Yet those studies were only based on a few
north temperate species, leaving the effect of nest size on predation risk in the tropics unknown, and the relationship
across species untested. Our study suggests that predation
risk generally increases with nest size based on both experiments and tests across species and latitudes (Figs. 1 and 2).
This finding supported the prediction that nest predation
may exert selection on nest size as proposed by the nest size
hypothesis. Nest size may constrain clutch size in some north
temperate species (Slagsvold 1982b, 1989a, 1989b), but we
showed that bird species with similar nest sizes and body
masses still differed in clutch sizes across latitudes (Fig. 5).
This opposes the prediction that nest size constrains clutch
size in the tropics. Moreover, we demonstrated that after controlling for body mass, nest sizes were not smaller in the tropical site compared with the temperate site (Figs. 3 and 4) and
phylogeny does not account for the lack of difference. Thus,
our results clearly reject the hypothesis that nest size constrains clutch size in our tropical site.
The positive relationships between nest size and nest
predation risk (Figs. 1 and 2) and between nest size and
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 1086–1092
Clutch size, nest size, and nest predation 1091
body size (Fig. 4) suggest an interesting pattern: nest predation risk increases with body size. A positive relationship between nest predation risk and body size was
reported for 10 species of Mimidae from the temperatezone regions (Murphy & Fleischer 1986). Our results suggest a more general pattern of increasing nest predation
with body size for open-cup nesting birds. Given that
body size also can be related to other life-history traits
(Lindstedt & Calder 1981; Sæther 1989), then consideration of the costs and benefits of body size, including
possible nest predation costs, may enhance understanding
of the evolution of life history strategies. Ultimately, nest
predation risk does not lead to latitudinal differences in
nest size, as we showed here, and thereby does not
explain smaller tropical clutch sizes. Nonetheless, nest
predation can favour smaller clutch sizes through other
mechanisms (Slagsvold 1982a) that have not been tested.
Nest predation can also be a strong selective force that
may interact with other proposed mechanisms such as
food limitation, parental feeding rates, or adult survival
(Martin 1992, 2004; Martin et al. 2000). Those possible
interactions are predicted to be sometimes synergistic and
sometimes antagonistic (Martin 1996, 2004). Since none
of the proposed hypotheses alone seem to explain
latitudinal variation in clutch size (see Martin 1996;
Martin et al. 2000, 2006), and tests of the interactions
among hypothesized selective forces are still lacking,
future research could benefit from examination of such
interactions.
Acknowledgements
We are grateful to D. Barton for his help in the statistical analysis and his
comments, M. J. Alvarez and J. C. Oteyza, for their valuable help in the
field and many people who helped in collecting the data reported here. This
study was made possible in part by support under NSF grants DEB0543178 and DEB-0841764 to T. E. Martin. Permit numbers are
DM ⁄ 0000237 from FONACIT; PA-INP-005-2004 from INPARQUES; and
01-03-03-1147 from Ministerio del Ambiente. We thank C. Bosque for substantial aid in facilitating this work. Specific equipment identities are simply
provided to aid specific methods and do not represent an endorsement of
these companies by USGS.
References
AOU Check-List of North American Birds (2010) Available at: http://
www.aou.org/checklist/north/full.php, accessed 6 January 2010.
Burns, K.J. (1997) Molecular systematics of tanagers (Thraupinae): evolution
and biogeography of a diverse radiation of neotropical birds. Molecular
Phylogenetics and Evolution, 8, 334–348.
Cardillo, M. (2002) The life-history basis of latitudinal diversity gradients: how
do species traits vary from the poles to the equator? Journal of Animal Ecology, 71, 79–87.
Felsenstein, J. (1985) Phylogenies and the comparative method. American
Naturalist, 125, 1–15.
Garland, T., Harvey, P.H. & Ives, A.R. (1992) Procedures for the analysis of
comparative data using phylogenetically independent contrasts. Systematic
Biology, 41, 18–32.
Gibbs, J.P. (1991) Avian nest predation in tropical wet forest: an experimental
study. Oikos, 60, 155–161.
Hilty, S.L. (2003) Birds of Venezuela. Princeton University Press, Princeton,
New Jersey, USA.
Jønsson, K.A. & Fjeldså, J. (2006) A phylogenetic supertree of oscine passerine
birds (Aves: Passeri). Zoologica Scripta, 35, 149–186.
Karlsson, J. & Nilsson, S.G. (1977) The influence of nest-box area on clutch size
in some hole-nesting passerines. Ibis, 119, 207–211.
Klicka, J., Voelker, G. & Spellman, G.M. (2005) A molecular phylogenetic
analysis of the ‘‘true thrushes’’ (Aves: Turdinae). Molecular Phylogenetics
and Evolution, 34, 486–500.
Kulesza, G. (1990) An analysis of clutch-size in New World passerine birds.
Ibis, 132, 407–422.
Lack, D. (1947) The significance of clutch-size. Ibis, 89, 302–352.
Lill, A. (1975) The evolution of clutch size and male ‘‘chauvinism’’ in the white
bearded manakin. Living Birds, 13, 211–231.
Lima, S.L. (1987) Clutch size in birds: a predation perspective. Ecology, 68,
1062–1070.
Lindstedt, S.L. & Calder, W.A. (1981) Body size, physiological time, and longevity of homeothermic animals. Quarterly Review of Biology, 56, 1–16.
Lopéz-Iborra, G.M., Pinheiro, R.T., Sancho, C. & Martinez, A. (2004) Nest
size influences nest predation risk in two coexisting Acrocephalus warblers.
Ardea, 92, 85–91.
Lovette, I.J. & Bermingham, E. (2002) What is a wood-warbler? Molecular
characterization of a monophyletic parulidae. The Auk, 119, 695–714.
Maddison, W.P. & Maddison, D. (2009) Mesquite: a modular system for evolutionary analysis. Version 2.72 Available at: http://mesquiteproject.org.
Marini, M.A. & Melo, C. (1998) Predators of quail eggs, and the evidence
of the remains: implications for nest predation studies. Condor, 100, 395–
399.
Martin, T.E. (1992) Interaction of nest predation and food limitation in reproductive strategies. Current Ornithology, 9, 163–197.
Martin, T.E. (1996) Life history evolution in tropical and south temperate
birds: what do we really know? Journal of Avian Biology, 27, 263–272.
Martin, T.E. (2004) Avian life-history evolution has an eminent past: does it
have a bright future? The Auk, 121, 289–301.
Martin, T.E. (2007) Climate correlates of 20 years of trophic changes in a highelevation riparian system. Ecology, 88, 367–380.
Martin, T.E. & Briskie, J.V. (2009) Predation on dependent offspring: a review
of the consequences for mean expression and phenotypic plasticity in avian
life history traits. Annals of the New York Academy of Sciences, 1168, 201–
217.
Martin, T.E., Scott, J. & Menge, C. (2000) Nest predation increases with parental activity: separating nest site and parental activity effects. Proceedings of
the Royal Society B: Biological Sciences, 267, 2287–2293.
Martin, T.E., Martin, P.R., Olson, C.R., Heidinger, B.J. & Fontaine, J.J.
(2000) Parental care and clutch sizes in north and South American birds. Science, 287, 1482–1485.
Martin, T.E., Bassar, R.D., Bassar, S.K., Fontaine, J.J., Lloyd, P., Mathewson,
H.A., Niklison, A.M. & Chalfoun, A. (2006) Life-history and ecological correlates of geographic variation in egg and clutch mass among passerine species. Evolution, 60, 390–398.
Martin, T.E., Auer, S.K., Bassar, R.D., Niklison, A.M. & Lloyd, P. (2007)
Geographic variation in avian incubation periods and parental influences on
embryonic temperature. Evolution, 61, 2558–2569.
Mayfield, H.F. (1975) Suggestions for calculating nest success. The Wilson Bulletin, 87, 456–466.
Midford, P.E., Garland T. Jr. & Maddison, W.P. (2008) PDAD: PDTREE
package for Mesquite. Available at: http://mesquiteproject.org/pdap_
mesquite.
Møller, A.P. (1982) Clutch size in relation to nest size in the swallow Hirundo
rustica. Ibis, 124, 339–343.
Møller, A.P. (1990) Nest predation selects for small nest size in the blackbird.
Oikos, 57, 237–240.
Moreau, R.E. (1944) Clutch-size: a comparative study, with special reference to
African birds. Ibis, 86, 286–347.
Murphy, M.T. & Fleischer, R.C. (1986) Body size, nest predation, and
reproductive patterns in brown thrashers and other mimids. Condor, 88,
446–455.
Oniki, Y. (1979) Is nesting success of birds low in the tropics? Biotropica, 11,
60–69.
Outlaw, D.C., Voelker, G., Mila, B. & Girman, D.J. (2003) Evolution of longdistance migration in and historical biogeography of Catharus thrushes: a
molecular phylogenetic approach. The Auk, 120, 299–310.
Palomino, J.J., Martı́n-Vivaldi, M., Soler, M. & Soler, J.J. (1998) Functional
significance of nest size variation in the rufous bush robin Cercotrichas galactotes. Ardea, 86, 177–185.
Pianka, E.R. (1966) Latitudinal gradients in species diversity: a review of
concepts. American Naturalist, 100, 33–46.
Remsen, J.V., Cadena, C.D., Jaramillo, A., Nores, M., Pacheco, J.F., Robbins,
T.S., Schulenberg, T.S., Stiles, F.G., Stotz, D.F. & Zimmer, K.J. (2010) A
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 1086–1092
1092 L. Biancucci & T. E. Martin
classification of birds of South America. Available at: http://www.museum.
lsu.edu/~Remsen/SACCBaseline.html, accessed 4 January 2010.
Robinson, W.D., Robinson, T.R., Robinson, S.K. & Brawn, J.D. (2000) Nesting success of understory forest birds in central Panama. Journal of Avian
Biology, 31, 151–164.
Roper, J.J. (1992) Nest predation experiments with quail eggs: too much to
swallow? Oikos, 65, 528–530.
Sæther, B. (1989) Survival rates in relation to body weight in European birds.
Ornis Scandinavica, 20, 13–21.
Sieving, K.E. & Willson, M.F. (1998) Nest predation and avian species diversity in northwestern forest understory. Ecology, 79, 2391–2402.
Skutch, A.F. (1949) Do tropical birds rear as many young as they can nourish?
Ibis, 91, 430–455.
Skutch, A.F. (1966) A breeding bird census and nesting success in Central
America. Ibis, 108, 1–16.
Skutch, A.F. (1985) Clutch size, nesting success, and predation on nests of
neotropical birds, reviewed. Ornithological Monographs, 36, 575–594.
Slagsvold, T. (1982a) Clutch size variation in passerine birds: the nest predation
hypothesis. Oecologia, 54, 159–169.
Slagsvold, T. (1982b) Clutch size, nest size, and hatching asynchrony in birds:
experiments with the fieldfare (Turdus pilaris). Ecology, 63, 1389–1399.
Slagsvold, T. (1989a) Experiments on clutch size and nest size in passerine
birds. Oecologia, 80, 297–302.
Slagsvold, T. (1989b) On the evolution of clutch size and nest size in passerine
birds. Oecologia, 79, 300–305.
Snow, D.W. (1978) The nest as a factor determining clutch-size in tropical
birds. Journal of Ornithology, 119, 227–230.
Snow, D.W. & Snow, B.K. (1963) Breeding and the annual cycle in three Trinidad thrushes. The Wilson Bulletin, 75, 27–41.
Söderström, B. (1999) Artificial nest predation rates in tropical and
temperate forests: a review of the effects of edge and nest site. Ecography, 22,
455–463.
Weidinger, K. (2004) Relative effects of nest size and site on the risk of predation in open nesting passerines. Journal of Avian Biology, 35, 515–523.
Willson, M.F. & Gende, S.M. (2000) Nesting success of forest birds in southeast Alaska and adjacent Canada. Condor, 102, 314–324.
Yuri, T. & Mindell, D.P. (2002) Molecular phylogenetic analysis of Fringillidae, ‘‘New World nine-primaried oscines’’ (Aves: Passeriformes). Molecular
Phylogenetics and Evolution, 23, 229–243.
Received 30 March 2010; accepted 1 June 2010
Handling Editor: Jonathan Wright
2010 The Authors. Journal compilation 2010 British Ecological Society, Journal of Animal Ecology, 79, 1086–1092