FRONTISPIECE. Three-striped Warblers (Basileuterus tristriatus) were studied in the northern Andes of Venezuela.
Temperate and tropical parulids differ strongly in life histories. Three-striped Warblers have smaller clutches, longer
incubation periods, lower nest attentiveness, longer off-bouts, and slower nestling growth rates than most temperate species.
Water color by Don Radovich.
Published by the Wilson Ornithological Society
VOL. 121, NO. 4
December 2009
PAGES 667–914
The Wilson Journal of Ornithology 121(4):667–678, 2009
BREEDING BIOLOGY OF THE THREE-STRIPED WARBLER IN
VENEZUELA: A CONTRAST BETWEEN TROPICAL AND
TEMPERATE PARULIDS
W. ANDREW COX1,3 AND THOMAS E. MARTIN2
ABSTRACT.—We document reproductive life history traits of the Three-striped Warbler (Basileuterus tristriatus) from
146 nests in Venezuela and compare our results to data from the literature for other tropical and temperate parulid species.
Mean (6 SE) clutch size was 1.96 6 0.03 eggs (n 5 96) and fresh egg mass was 2.09 6 0.02 g. The incubation period was
15.8 6 0.2 days (n 5 23) and the nestling period was 10.5 6 0.3 days (n 5 12). Males did not incubate and rarely provided
food for females during incubation. Females had 57 6 2% (n 5 49) nest attentiveness (% of time on the nest incubating),
which caused egg temperature to commonly become cold relative to development. Both adults fed nestlings and feeding
rates increased with nestling age. The growth rate constant for nestlings based on mass was K 5 0.490, which is slower than
for north temperate warblers. Predation was the primary source of nest failure and only 22% of nests were successful based
on a Mayfield daily predation rate of 0.048 6 0.006. Our literature review indicates parulids differ strongly in life histories
between temperate and tropical/subtropical sites with species in the tropics having, on average, smaller clutches, longer
incubation periods, lower nest attentiveness, longer off-bouts, and longer nestling periods. Received 11 October 2008.
Accepted 6 June 2009.
Life history strategies often show strong
differences between north temperate versus subtropical and tropical sites (Moreau 1944; Lack
1947; Ricklefs 1976; Martin et al. 2000, 2006,
2007; Martin 2004), although the extent of
differences varies among phylogenetic groups
(Fierro-Calderón and Martin 2007, Martin and
Schwabl 2008). Wood-warblers (Parulidae) include a diversity of species across latitudes and
1
Division of Biological Sciences, University of Missouri,
105 Tucker Hall, Columbia, MO 65211, USA.
2
USGS, Montana Cooperative Wildlife Research Unit,
Avian Studies Program, 205 Natural Science, University of
Montana, Missoula, MT 59812, USA.
3
Corresponding author; e-mail: WACox@mizzou.edu
appear to show strong latitudinal patterns in life
history traits (Martin et al. 2000, Martin 2002,
Auer et al. 2007). The wood-warbler genus
Basileuterus, comprised of 20 species, is a
particularly widespread group distributed from
Argentina to Mexico with records reaching as far
north as southern Texas and Arizona (Dunn and
Garrett 1997). One species is endangered (B.
griseiceps), but most others are common throughout their range and are of low conservation
concern (IUCN 2006). Little is known about the
life histories of most species despite their broad
distribution and relative abundance. Basic information including nest descriptions and clutch size
is lacking for many species (Curson et al. 1994).
667
668
THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 121, No. 4, December 2009
Reproductive traits including incubation period,
nest attentiveness, and nestling growth are
described for even fewer members of Basileuterus
or other parulid genera (but see Skutch 1954,
Ghalambor and Martin 2001, Martin 2002, Auer
et al. 2007). The dearth of information from the
Tropics and the suggestion that Wood-warblers
may show strong latitudinal patterns make them
an important group to study for improving our
understanding of latitudinal patterns in life history
traits.
We describe the reproductive biology of the
Three-striped Warbler (B. tristriatus) in northern
Venezuela. This warbler inhabits the understory
of mature and second growth forests from 800 to
2,700 m elevation in Costa Rica, Panama, and in
the Andes from Venezuela to Bolivia (Hilty
2003). Nest and clutch sizes have been described
in both Ecuador and Costa Rica (Greeney et al.
2005, Jablonski et al. 2006), but no other
reproductive traits have been documented. We
provide detailed data based on 146 nests in a
montane cloud forest in Venezuela during 2002–
2006. We also present a review of the current
literature for all parulids and compare our results
to other species throughout North, Central, and
South America.
METHODS
We searched for nests from March to July,
2002–2006, in Yacambú National Park in Lara,
Venezuela (09u 429 N, 69u 429 W). This mountainous park on the northernmost edge of the
Andes is characterized by second growth and
mature tropical forest. The park ranges from 500
to 2,200 m and our field sites occurred from 1,350
to 2,000 m elevation. We located nests via
systematic and behavioral searches, and monitored them every 2–4 days, except at stagechanging events (laying, hatching, fledging) when
we monitored nests daily or twice daily (Martin
and Geupel 1993). Nest, egg, and nestling
measurements, and behavioral data were collected
following Martin et al. (2000, 2006, 2007) and
Fierro-Calderón and Martin (2007). We measured
egg mass (g) and nestling growth using ACCULAB (Elk Grove, IL, USA) portable electronic
scales with an accuracy of 60.001 g during early
incubation (days 0–2) for egg mass and every
other day (starting on day 0 or 1) for nestling
growth. Growth rates for non-experimental nests
were calculated following Remeš and Martin
(2002), and nest predation and survival rates were
calculated following Mayfield (1961, 1975) and
Hensler and Nichols (1981). Nesting season
length was estimated as the middle 90% of nest
initiations (exclusion of earliest 5% and latest
5%) following Martin (2007). We used video
cameras to measure parental behavior for 6–8 hrs
starting at dawn during incubation and nestling
phases. Nest attentiveness (% of time on the nest
incubating) was calculated for each nest as the
number of minutes on the nest/total minutes
video-monitored. We calculated the incubation
period as the number of days that lapsed between
the day the last egg was laid and when the first
egg hatched (Briskie and Sealy 1990). We
calculated the nestling period as the number of
days that lapsed from when the first egg hatched
until the first nestling fledged.
Egg temperatures (uC) were measured for B.
tristriatus by inserting thermisters on the first or
second day of incubation into the center of one
egg in each nest through a small hole sealed with
glue (Weathers and Sullivan 1989). The wire was
threaded through the nest and connected to a
HOBO Stowaway XTI datalogger (Onset Corporation, Bourne, MA, USA) that recorded temperatures every 12–24 sec for 5–7 days per nest
(Martin et al. 2007, Martin and Schwabl 2008).
Ambient temperatures were measured over the
same periods using a shaded probe near the nest.
We also measured egg temperatures for Red-faced
Warblers (Cardellina rubrifrons) in northern
Arizona using the same methodology (Martin et
al. 2007).
We searched the literature for life-history data
for all species in the Parulidae with which to
compare our results. We first consulted The Birds
of North America data base (Poole 2005) and
supplemented these data with those from other
literature. We calculated weighted means for
clutch sizes, incubation periods (days), and
nestling periods (days) when multiple mean
values and sample sizes were provided, or when
only raw data were available. We recorded a
range of values when means could not be reliably
calculated; these were excluded from analyses
when we compared temperate and tropical/
subtropical species.
Statistical Analysis.—Means are reported with
61 standard error (SE) for all data and sample
sizes reflect numbers of nests sampled. We used
SPSS Version 15.0 (2006) for all statistical tests.
We used analysis of variance (ANOVA) to test for
temporal changes in nest attentiveness (% time on
Cox and Martin N BREEDING BIOLOGY OF A TROPICAL WARBLER
669
FIG. 1. Temporal distribution of nest initiation dates (date the first egg is laid in a nest) for the Three-striped Warbler
among weekly (7 day) intervals.
the nest) and mean on- and off bouts during
incubation by separating the stage into three
categories (early, 2–3 days; middle, 5–7 days;
late, 12–14 days). We used least-significant
difference tests (LSD) to conduct post hoc tests
when ANOVA results were significant (a # 0.05).
We used linear regression to test for relationships
between temporal changes in parental behavior
during the nesting stage (e.g., brooding effort,
feeding rates). We examined distributions of lifehistory trait data for temperate and subtropical/
tropical warblers using a Shapiro-Wilks test. One
or both of the distributions departed from
normality for most life-history traits, so we used
non-parametric Mann-Whitney U-tests to test for
differences in life-history traits between temperate
and subtropical/tropical warblers (Zar 2010).
RESULTS
Nest and Eggs.—We found 146 nests in 5 years
of field work. Three-striped Warblers build a
small, domed nest with a side entrance. The inside
of the cup measured 5.08 6 0.08 cm in diameter
and 3.38 6 0.10 cm in height, while the outside
diameter and height averaged 11.46 6 0.38 cm
and 7.29 6 0.35 cm, respectively. Nests were on
the ground (n 5 146) on a steep slope or bank,
built into leaf litter or under the base of saplings
and small trees. Nests were frequently placed in
the forest interior but some were built into
exposed roadside banks, culverts, and drainages.
Dates of nest initiation (i.e., first egg laid) ranged
from 8 March to 25 June across years (Fig. 1).
Nests were usually initiated after 10 April (n 5
103), although three nests were initiated in March;
two of these were from the same individual in
consecutive years based on color-banding. The
median date of nest initiations was 16 May (Fig. 1).
The nesting season lasted 68 days (Fig. 1).
Eggs were white with irregular brown spots.
Fresh egg mass (measured between day 0 and day
2 of incubation) was 2.09 6 0.02 g (n 5 90),
which represented 17.7% of adult female body
mass (11.80 6 0.18 g, n 5 33). Five of 96
clutches had one egg (5%), one had three eggs
(1%), and the rest had two eggs (94%), yielding
an average clutch size of 1.96 6 0.03 eggs.
Incubation Period.—The incubation period
averaged 15.8 6 0.2 days (n 5 23) and was
longer than for north temperate parulids, which
averaged 12.2 6 0.1 days (n 5 32 species;
Table 1). Males did not incubate and rarely
provided food for incubating females, averaging
0.03 6 0.02 trips to the nest/hr (n 5 29) during
early incubation (days 2–4) and 0.06 6 0.04 trips/
hr (n 5 14) during late incubation (days 11–16).
Nest attentiveness averaged 57 6 2% (n 5 49)
and was slightly lower than for other tropical
parulids, which averaged 64 6 1% for 15 species.
Nest attentiveness was much lower than for north
temperate parulids, which averaged 77 6 1% (n
5 31 species, Table 1). Attentiveness changed
over the incubation period for the Three-striped
Warbler (ANOVA, F2,46 5 6.4, P 5 0.004); nest
670
THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 121, No. 4, December 2009
TABLE 1. Reproductive traits of temperate and tropical parulids. Only species with data available for multiple
life-history traits are included.
Species
Temperate species
Blue-winged Warbler
(Vermivora pinus)
Golden-winged Warbler
(V. chrysoptera)
Tennessee Warbler
(V. peregrina)
Orange-crowned Warbler
(V. celata)
Nashville Warbler
(V. ruficapilla)
Virginia’s Warbler
(V. virginiae)
Northern Parula
(Parula americana)
Yellow Warbler
(Dendroica petechia)
Chestnut-sided Warbler
(D. pensylvanica)
Magnolia Warbler
(D. magnolia)
Black-throated Blue
Warbler
(D. caerulescens)
Yellow-rumped Warbler
(D. coronata)
Golden-cheeked Warbler
(D. chrysoparia)
Black-throated Green
Warbler
(D. virens)
Townsend’s Warbler
(D. townsendi)
Blackburnian Warbler
(D. fusca)
Yellow-throated Warbler
(D. dominica)
Grace’s Warbler
(D. graciae)
Kirtland’s Warbler
(D. kirtlandii)
Prairie Warbler
(D. discolor)
Palm Warbler
(D. palmarum)
Bay-breasted Warbler
(D. castanea)
Blackpoll Warbler
(D. striata)
Cerulean Warbler
(D. cerulea)
Black-and-white Warbler
(Mniotilta varia)
Mean
clutch
size
Mean
Nest
Mean
incubation attentiveness
on-bout
period (days)
(%)
duration (min)
Mean
off-bout
duration (min)
4.37
10–11
5.00
10–12
5.59
7–8
4.54
12.6
80
49
12
4.71
11–12
73
39
14
3.57
12.3
73
31
3.94
12.5
79
4.08
11.3
3.88
Mate
feed?
Mean
nestling
period (days)
Nestling
growth
rate (K)
Referencesa
Y
9.3
0.559
1, 2
9–10
Y
1, 2, 4
0.654
1, 3, 5
11.3
1, 6, 7, 8
Y
9–11
1, 6, 9
11
Y
11.4
1, 7, 8
21
6
Y
10–11
1, 6, 10
78
36
10
Y
8.4
11.0
75
23
7
Y
10–11
1, 6, 11, 12
3.96
12.0
70
17
7
8–10
1, 13
3.80
13.0
72
31
12
3.86
12.8
77
25
3.90
12.1
74
37
13
3–5
12.0
78
50
15
5.70
12.5
3–5
7.4
0.579
Y
8.6
Y
12.6
15
Y
10.5
1, 16
10.0
0.647 1, 2, 6, 14
0.736
9.9
72
21
8
1, 3, 6
1, 3, 6
17
Y
1, 6
3–5
12.0
3.20
10–12
4.63
14.2
82
51
11
Y
9.4
0.547
1, 3, 6
3.92
12.0
77
55
15
Y
9.6
0.507
1, 3, 6
4.59
12.0
Y
12.0
5.43
12–13
80
18
5
Y
10.5
4.32
11.5–12
77
19
6
Y
9.5
83
50
10
Y
10.4
1, 21
Y
8–12
1
3.60
11.4
4–6
10–12
1
Y
1
1
1, 6, 18,
19, 20
0.538
1, 6
Cox and Martin N BREEDING BIOLOGY OF A TROPICAL WARBLER
671
TABLE 1. Continued.
Species
American Redstart
(Setophaga ruticilla)
Prothonotary Warbler
(Protonotaria citrea)
Worm-eating Warbler
(Helmitheros
vermivorum)
Swainson’s Warbler
(Limnothlypis
swainsonii)
Ovenbird
(Seiurus aurocapilla)
Northern Waterthrush
(S. noveboracensis)
Louisiana Waterthrush
(S. motacilla)
Kentucky Warbler
(Oporornis formosus)
Mourning Warbler
(O. philadelphia)
MacGillivray’s Warbler
(O. tolmiei)
Common Yellowthroat
(Geothlypis trichas)
Hooded Warbler
(Wilsonia citrina)
Wilson’s Warbler
(W. pusilla)
Canada Warbler
(W. canadensis)
Red-faced Warbler
(Cardellina rubrifrons)
Painted Redstart
(Myioborus pictus)
Yellow-breasted Chat
(Icteria virens)
Mean
clutch
size
Mean
Nest
Mean
on-bout
incubation attentiveness
duration (min)
(%)
period (days)
Mean
off-bout
duration (min)
Mate
feed?
Mean
nestling
period (days)
Nestling
growth
rate (K)
Referencesa
3.89
10–13
82
23
5
Y
7–9
0.613
1, 3, 6
4.55
12.5
56
18
14
Y
10.0
0.654
1, 3
4.82
13.0
Y
9.0
1
3.22
13.9
78
59
16
Y
9.9
1, 6, 22
4.31
12.2
85
110
19
Y
7.9
0.473
4.11
12.0
75
30
10
Y
9.0
5.00
12.7
79
35
9
Y
10.8
1, 3, 6, 23
1, 3, 6, 24,
0.590
25
4.12
11.0
Y
8.4–9.5
3.71
12.0
75
39
Y
8.0
1, 6, 27
4.12
12.5
77
22
Y
10.4
1, 8, 15
3.99
12.0
80
49
Y
9.8
3.61
11.0
4.11
11.9
81
22
5
Y
4.37
12.0
85
32
7
Y
4.16
12.8
75
37.4
10.5
Y
11.1
3.15
13.2
75
Y
13.0
3.68
11.6
74
Y
8.9
1
11.0
1
13.0
30, 31
Subtropical and tropical species
Colima Warbler
(Vermivora crissalis)
3–4
Flame-throated Warbler
(Parula gutturalis)
2.00
Crescent-chested Warbler
(P. superciliosa)
2–3
Tropical Parula
(P. pitiayumi)
3.14
Adelaide’s Warbler
(Dendroica adelaidae) 2–3
Masked Yellowthroat
(Geothlypis
aequinoctialis)
3.10
Grey-crowned
Yellowthroat
(G. poliocephala)
2.70
13
8.5
16
60
45
15
12.0
16.0
61
27
17
13+
68
20
10
13.3
12.8
26
61
22.5
0.537
1, 6, 26
1, 3, 6
8–9
1
10.2
1, 6
1
1, 7, 8, 28
0.557
1, 3, 29
30, 32
13.0
50
0.680
1, 3, 6
32, 33
34, 35
17.7
9.7
8, 36, 37
11.0
38
672
THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 121, No. 4, December 2009
TABLE 1.
Continued.
Species
Red Warbler
(Ergaticus ruber)
Pink-headed Warbler
(E. versicolor)
Slate-throated Redstart
(Myioborus miniatus)
Brown-capped Redstart
(M. brunniceps)
Collared Redstart
(M. torquatus)
Two-banded Warbler
(Basileuterus
bivittatus)
Pale-legged Warbler
(B. signatus)
Golden-crowned Warbler
(B. culicivorus)
Rufous-capped Warbler
(B. rufifrons)
Black-cheeked Warbler
(B. melanogenys)
Three-striped Warbler
(B. tristriatus)
Buff-rumped Warbler
(Phaeothlypis fulvicauda)
Wrenthrush
(Zeledonia coronata)
Red-breasted Chat
(Granatellus venustus)
Mean
clutch
size
Mean
Nest
Mean
on-bout
incubation attentiveness
duration (min)
(%)
period (days)
Mean
off-bout
duration (min)
3.00
16.0
66
2–4
16.0
71
20.0
8.0
2.72
14.4
67
37.6
18.2
2.60
16.6
67
33.1
17.4
2.50
15.0
74
28.5
9.8
3.00
14.8
62
46.1
22.6
2.60
16.6
65
30.3
16.5
2–4
62
44.0
2–4
66
2.00
Y
Mean
nestling
period (days)
Referencesa
10–11
39
10–11
30, 31
11.8
Y
Nestling
growth
rate (K)
12.6
0.522 40, 41, 42
8, 30, 36,
37
13.0
40
Y
10.9
8, 36, 37
Y
12.5
8, 36, 37
26.0
10+
32
44.0
23.0
12.0
32
62
29.0
18.0
45.7
35.0
1.96
15.8
57
2.00
16–19
68–74
2.00
2–4
Mate
feed?
14.0
32
Y
10.5
0.490
43
Y
12–15
31
17+
30, 44
45, 46
a
1. Poole (2005), 2. Remeš (2006), 3. Remeš and Martin (2002), 4. Canterbury (1990), 5. Holmes and Nixon (2000), 6. Conway and Martin (2000), 7. Palacios
and Martin (2006), 8. Martin (2002), 9. Knapton (1984), 10. Graber and Graber (1951), 11. Lawrence (1948), 12. Tate (1970), 13. Nice (1926), 14. Holmes et al.
(1992), 15. Martin unpubl. data, 16. Jennifer Reidy (pers. comm.) 17. Matsuoka et al. (1997), 18. Harrison (1984), 19. MacArthur (1958), 20. Mendall (1937), 21.
Oliarnyk and Robertson (1996), 22. Thompson (2005), 23. Peck and James (1987), 24. Eaton (1958), 25. Robinson (1987), 26. Vicki McDonald (pers. comm.), 27.
Cox (1958), 28. Martin (1995), 29. Marshall and Balda (1974), 30. Curson et al. (1994), 31. Skutch (1954), 32. Skutch (1967), 33. Di Giacomo (2005), 34. Bond
(1930), 35. Spaulding (1937), 36. Auer et al. (2007), 37. Martin et al. (2000), 38. Martinez et al. (2004), 39. Elliott (1969), 40. Skutch (1945), 41. Ewert (1975), 42.
Collins and Ryan (1994), 43. This study, 44. Hunt (1971), 45. Vega Rivera et al. (2004), 46. Grant (1964).
attentiveness during early incubation was similar
(LSD, P 5 0.70) to the middle period, and both
were less (LSD, P 5 0.026) than during late
incubation (Fig. 2A). This change was caused by
a dramatic reduction in length of off-bouts over
the incubation period (ANOVA, F2,46 5 7.1, P 5
0.002; Fig. 2B). On-bout duration showed a
marginal decline in late incubation (ANOVA,
F2,46 5 2.7, P 5 0.081, Fig. 2B).
Both on- and off-bouts were relatively long for
the Three-striped Warbler. On-bouts averaged
45.7 6 2.5 min (n 5 49) (Fig. 2B), but averaged
37.2 6 3.4 min (n 5 31 species) and 31.4 6
2.5 min (n 5 13 species) for temperate and
tropical species, respectively. Off-bouts averaged
35.0 6 3.1 min (n 5 49) (Fig. 2B), and 10.6 6
0.7 min (n 5 30 species) and 17.0 6 1.6 min (n 5
12 species) for temperate and tropical species,
respectively. These long off-bouts caused egg
temperatures of Three-striped Warblers to reach
cold levels relative to development (Fig. 3). In
contrast, the Red-faced Warbler, a north temperate relative, kept egg temperatures higher despite
much colder ambient temperatures (Fig. 3). Egg
temperature of the Three-striped Warbler averaged 33.93 6 0.47u C over 24-hr periods from
27 days of sampling across seven nests (with an
overall mean taken from means of each nest),
while the mean temperature for the Red-faced
Warbler was 35.75 6 0.18u C (n 5 3 nests,
7 days).
Nestling Period.—The nestling period was 10.5
6 0.3 days (n 5 12). This period length was
similar to north temperate relatives, which
Cox and Martin N BREEDING BIOLOGY OF A TROPICAL WARBLER
FIG. 2. Average (A) nest attentiveness, and (B) on- and
off-bout durations across three periods of incubation for the
Three-striped Warbler: early (days 2–4), middle (days 5–9),
and late (days 11–16). Sample sizes reflect numbers of nests.
averaged 10.0 6 0.2 days (n 5 28 species), but
less than for other tropical species which averaged
11.9 6 0.3 days (n 5 11 species; Table 1). The
amount of time that females spent brooding
nestlings declined (r 5 20.91, P , 0.001) with
age of nestlings (Fig. 4A). Both males and
females provisioned nestlings, and rate of visits
to the nest to feed young increased with nestling
age (r 5 0.87, P , 0.001; Fig. 4B). Nestlings
weighed 1.70 6 0.07 g (n 5 8) on hatch day and
11.50 6 1.01 g (n 5 9) when the eighth primary
feather broke its sheath (i.e., pin break) between
days 6 and 8. Growth rate constant (K) for the
nestling period based on nestling mass (Fig. 5A)
was greater than when based on tarsus (Fig. 5B),
and resulted in an estimated asymptote of 13.50 6
0.47 g, which was higher than mean mass for
adult females (11.80 6 0.18 g, n 5 33). The
growth rate based on mass (K 5 0.490 6 0.030)
was slower than for north temperate parulids,
which averaged K 5 0.591 6 0.018 (n 5 15
species; Table 1).
673
Nest Survival.—Twenty of 146 nests were
abandoned before the nest was finished being
built or an egg was laid and did not contribute to
nest survival analyses. Another 18 nests were
excluded because of effects by researcher activities. Twenty-four of the remaining 108 nests
fledged young, 18 were still active when monitoring was discontinued at the end of the season,
and 66 failed yielding a total of 1,258.5 days of
exposure. Predation was the source of failure for
60 of the 66 failed nests with the remaining six
nests failing due to weather, abandonment, or
unknown reasons. The overall daily predation rate
was 0.048 6 0.006, and the total daily survival
rate was 0.948 6 0.006. Daily predation rates
were 0.027 6 0.019, 0.042 6 0.007, and 0.070 6
0.015 during egg-laying, incubation, and nestling
stages, respectively. The overall nest success
based on a total nesting period of 28 days was
22%.
Subtropical/Tropical vs. Temperate Species.—
Differences between the Three-striped Warbler
and temperate species paralleled trends observed
from available data for other tropical/subtropical
and temperate parulids (Table 1). Clutch size for
tropical parulids averaged 2.53 6 0.12 eggs (n 5
14), which was lower than the mean clutch size of
4.20 6 0.10 eggs (n 5 38) for temperate species
(U 5 0, P , 0.001). Mean incubation period for
tropical warblers was 14.9 6 0.4 days (n 5 13),
which was longer than the mean period of 12.2 6
0.1 days (n 5 32) for temperate species (U 5 29,
P , 0.001). Females of tropical species had lower
nest attentiveness during incubation (64 6 1%, n
5 15) than temperate species (77 6 1%, n 5 31)
(U 5 21, P , 0.001). This was a result of offbouts that averaged 18.4 6 2.0 min (n 5 13),
which was longer than the mean value of 10.6 6
0.7 min (n 5 30) for temperate species (U 5 61,
P , 0.001). Mean on-bouts averaged 32.4 6
2.5 min (n 5 14) for subtropical/tropical species,
similar to the mean value of 37.2 6 3.4 min (n 5
31) for temperate species (U 5 192, P 5 0.54).
The mean nestling period for subtropical/tropical
species was 11.8 6 0.3 days (n 5 12), which was
longer than the mean value of 10.1 6 0.2 days (n
5 28) for temperate species (U 5 53.5, P 5
0.001). The mean growth rate based on mass (K 5
0.506 6 0.016, n 5 2) for tropical species was
marginally different from the mean value (K 5
0.591 6 0.018, n 5 15) for temperate species (U
5 3, P 5 0.073).
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THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 121, No. 4, December 2009
FIG. 3. Representative examples of egg temperature fluctuations over days 3 and 4 of incubation in comparisons of the
Three-striped Warbler with a north temperate relative, the Red-faced Warbler. The two dashed lines at the top of each cell
represent the optimum temperature zone for development (White and Kinney 1974, Webb 1987). The ambient temperature
range over the sampling period is shown in each cell.
DISCUSSION
The domed ground nests of the Three-striped
Warbler we found in Venezuela were structurally
similar to those reported in other locations
(Greeney et al. 2005, Jablonski et al. 2006) and
those built by other members of the genus (Marini
and Cavalcanti 1994, Auer et al. 2007). The dome
can reduce predation risk by making its contents
less visible (Collias and Collias 1984, Auer et al.
2007). Domes may also protect nests from
weather in the tropics where heavy rains are
common throughout most of the breeding season
(Skutch 1967, Snow 1978, Collias and Collias
1984).
Three-striped Warblers had low variation in
clutch size with 94% of all nests containing two
eggs and no nest containing more than three eggs.
The only nest from Costa Rica that has been
described contained three nestlings (Jablonski et
al. 2006), which may indicate geographic variation in clutch size. Warblers at our site had a
smaller clutch size than reported for congeners
and other parulids in the Tropics and subtropics,
and a much smaller clutch size than north
temperate relatives (Table 1, also see Martin
1988), reflecting the well-known latitudinal gradient (Moreau 1944; Martin et al. 2000, 2006).
The mean incubation period for the Threestriped Warbler was typical of tropical parulids
and longer than temperate breeding species, as has
been generally observed (Ricklefs 1969, Martin
2002, Martin et al. 2007, Martin and Schwabl
2008). The longer incubation period of the Threestriped Warbler compared to temperate species
was associated with lower nest attentiveness and
longer off-bouts that yielded cooler incubation
temperatures, as seen for other tropical birds
(Chalfoun and Martin 2007, Martin et al. 2007,
Martin and Schwabl 2008). Temperatures decreased to levels sufficiently low to slow development (White and Kinney 1974, Webb 1987),
which explains part of this latitudinal trend
(Martin 2002, Martin et al. 2007, Martin and
Schwabl 2008). Nest attentiveness during incubation for the Three-striped Warbler was typical of
other tropical warblers but on- and off-bouts were
considerably longer than for other species. This
might reflect a response to high nest predation
risk; daily predation rate at our site in Venezuela
was higher than for related species in Argentina
(Martin et al. 2000, Auer et al. 2007) or Arizona
(Martin 2002). Higher predation risk can favor
longer bouts to reduce the numbers of trips to the
nest (Weathers and Sullivan 1989, Conway and
Cox and Martin N BREEDING BIOLOGY OF A TROPICAL WARBLER
675
FIG. 4. Scatter plots of change with nestling age in (A) female Three-striped Warbler brooding behavior (% time spent
brooding) and (B) rates that parents visit the nest to provision nestlings (n 5 14 nests).
Martin 2000, Martin et al. 2000). Alternatively,
longer bouts might reflect greater food limitation
and females may require long off-bouts for selfmaintenance (Conway and Martin 2000, Chalfoun
and Martin 2007).
The nestling period for all tropical parulids
spans from as few as 9 days for Masked
Yellowthroat (Geothlypis aequinoctialis) to at
least 17 days for Wrenthrush (Zeledonia coronata) with the Three-striped Warbler’s nestling
period ,1.4 days shorter than the mean nestling
period for other tropical species. This may be
related to high nest predation rates; nestling
periods and mortality rates are often negatively
correlated (Lack 1968, Remeš and Martin 2002).
Alternatively, the short nestling period may be a
proximate response to greater food availability
relative to brood size. Adults with one of the
smallest average clutch sizes among tropical
parulids may more easily be able to feed young
at rates adequate for faster growth and earlier
maturity. Young fledged at a mass that exceeded
adults. The generality of this result is difficult to
assess because growth rates and fledging size for
other tropical parulid species are almost entirely
lacking. The growth rate for the Three-striped
Warbler was slower than that of all temperate
warblers for which data are available except the
Ovenbird (Seiurus aurocapilla). The slower
growth of tropical than temperate birds was noted
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THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 121, No. 4, December 2009
FIG. 5. Relationships of (A) mass, and (B) tarsus length
plotted against age for Three-striped Warblers and their
estimated growth rates (K) and asymptotes (A). The dashed
lines represent the (A) mean mass and (B) mean tarsus
lengths of adults (n 5 135).
by Ricklefs (1976) long ago, although comparisons of related species in both areas have
remained rare.
Only two other studies we found provided data
on nest predation rates for tropical parulids. The
overall daily predation rate was relatively high for
Three-striped Warblers at our field site with an
estimated nest success rate of only 22%. This was
higher than for any parulid at the Argentina site
(Auer et al. 2007) and for the Buff-rumped
Warbler (Phaeothlypis fulvicauda) in Costa Rica
(Skutch 1985). A high predation rate may make it
difficult for adults to breed successfully in a given
year in addition to its potential to influence clutch
size, nest attentiveness, and nestling periods. A
species with low nest success could compensate
by increasing the length of its breeding season.
The breeding season of the Three-striped Warbler
was about twice the length of seasons for parulids
in Arizona (Martin 2007), but it only nested about
10 days longer than related species in Argentina
that had much lower nest predation rates (Auer et
al. 2007). The lengthy breeding season did not
result in substantially more breeding attempts than
in other parulids. Some breeding pairs renested
four times following nest failure (WAC, pers.
obs.), but north temperate parulids may also renest
four times or more (Grzybowski and Pease 2005,
Murray and Nolan 2007). More detailed observations on individual pairs of tropical parulid
species throughout the breeding season are needed
to improve our understanding of how high
predation rates and breeding season length affect
annual fecundity.
The Parulidae include 115 species (AOU 1998).
Much attention has been placed on the ecology
and evolution of species in North America, but
strikingly few data are available for species in
Central and South America where the majority of
parulid species reside (48 tropical and subtropical
species are not included in Table 1 due to lack of
available information). The Three-striped Warbler
had a smaller clutch, longer incubation period,
lower nest attentiveness, longer off-bouts, and a
slower growth rate than its temperate relatives.
Improving data collection efforts outside of North
America will lead to a better understanding of
tropical strategies and allow for more robust
comparisons of latitudinal patterns.
ACKNOWLEDGMENTS
This study was made possible in part by support under
NSF grants DEB-9981527, DEB-0543178, and DEB0841764 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 Carlos Bosque for substantial aid in obtaining
permits for this work, Karie Decker for statistical help, and
Allison Cox and Robin Hirsch-Jacobson for their comments
on earlier drafts of this manuscript.
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