The Wilson Journal of Ornithology 122(4):689–698, 2010
BREEDING BIOLOGY OF THE GOLDEN-FACED TYRANNULET
(ZIMMERIUS CHRYSOPS) IN VENEZUELA
WILLIAM GOULDING1,2,3 AND THOMAS E. MARTIN1
ABSTRACT.—We present the first detailed information on the breeding biology of the Golden-faced Tyrannulet
(Zimmerius chrysops). Information was gathered from 96 nests in Yacambú National Park, Venezuela during the 2002 to
2008 breeding seasons. The enclosed nest was similar to descriptions of nests of other species in the genus. Eggs were laid
on alternate days with mean (6 SE) clutch size of 1.98 6 0.02 (n 5 45) and fresh weight of 1.616 6 0.020 g (n 5 48). Only
the female incubated and the incubation period averaged 16.9 6 0.3 days (n 5 10). Nest attentiveness (% time on the nest)
averaged 66.0 6 1.6% (n 5 40) and increased from early to mid- and late-incubation. Incubation behavior yielded an
average 24-hr egg temperature of 34.88 6 0.45u C (n 5 7 nests, 43 days). The nestling growth rate constant for body mass
(k 5 0.285 6 0.011) was slow even for tropical tyrannids. The nestling period for nests where exact hatch and fledging days
were observed ranged from 17 to 19 days with an average of 18.0 6 0. 2 days (n 5 9). Both females and males fed nestlings
at a rate that increased over the nestling period with a mean of 4.41 6 0.65 trips/hr (n 5 10) during days 1 and 2 after
hatching, and 14.93 6 2.36 trips/hr (n 5 6) at pin-break (days 10–11). Daily predation rates were similar in egg-laying
(0.052 6 0.025; n 5 76.5 exposure days) and incubation periods (0.068 6 0.010; n 5 575.5 exposure days), but were lower
during the nestling period (0.039 6 0.010; n 5 377.0 exposure days). The total daily predation rate (0.057 6 0.007; n 5
989.0 exposure days) indicated only 12% of nests were successful. These breeding biology parameters for Z. chrysops differ
substantially from other tyrant-flycatchers and temperate species, further highlighting the diversity within the Tyrannidae.
Received 12 December 2009. Accepted 24 May 2010.
The Golden-faced Tyrannulet (Zimmerius
chrysops) is a member of the complex and large
New World Family Tyrannidae. Tyrannids are
diverse in behavior and occupy a broad range of
habitats and niches, reaching their greatest
diversity in the Neotropics (Ridgely and Tudor
1994, Hilty 2003, Fitzpatrick 2004), where they
comprise .20% of passerine species (McGowan
2004). General trends in avian life histories cannot
be clarified without studies of tropical species to
compensate for the historical bias toward temperate species (Martin 1996, 2004; Stutchbury and
Morton 2001). The paucity of information on
tropical bird species is particularly evident for
tyrannids. Information on the breeding biology of
most tropical tyrannids is sparse despite their
prominence in the neotropical avifauna, and
diversity of form and function.
Zimmerius chrysops is an example of the sparse
information on tropical tyrannids. Published
breeding biology information on Z. chrysops is
little more than a description of the enclosed,
dome-shaped nest with a side entrance, and
observed breeding dates (Hilty and Brown 1986,
Best et al. 1996). Yet, it is broadly distributed
with a range that extends from Peru, north through
1
USGS, Montana Cooperative Wildlife Research Unit,
University of Montana, Missoula, MT 59812, USA.
2
Current address: Indooroopilly, Brisbane 4068 Queensland, Australia.
3
Corresponding author; e-mail: willgoulding@yahoo.com.au
the Andes to Colombia and Venezuela, and occurs
from ,300 to 2,400 m asl (Hilty and Brown 1986,
Ridgely and Tudor 1994, Hilty 2003). The species
is associated with the middle to upper forest
layers, secondary growth, forest edges, as well as
with plantation and garden habitats (Fjeldså and
Krabbe 1990). Our objectives are to: (1) present
detailed reproductive biology information for Z.
chrysops, and (2) compare this information with
available temperate and tropical avian life history
information.
METHODS
We studied Golden-faced Tyrannulets during
the March–June breeding seasons in 2002–2008 in
Yacambú National Park, Lara State, Venezuela
(09u 429 N, 69u 429 W). Yacambú contains
premontane and montane cloud forest of the
northern Andes and encompasses a gradient from
500 to .2,300 m asl (Fierro-Calderón and Martin
2007). Peak precipitation in Yacambú occurs from
late April through July (Fierro-Calderón and
Martin 2007) with clouds and rain usually
enveloping habitats after the morning period,
producing cool wet conditions. We worked with
equal field effort in the same areas across years in
a 1,350 to 2,000 m asl research area.
Nests were located primarily by observing
parental behavior, but also by systematic searching. Dimensions of newly constructed nests were
measured before use and weather affected their
689
690
THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 122, No. 4, December 2010
shape. Eggs were described following Preston
(1953) as clarified by Palmer (1962). Eggs were
weighed for fresh egg mass between days 0 and 3
of incubation, and opportunistically later. The
incubation period was defined as the period
between the last egg laid (day 0) and the last
chick hatched (Nice 1954, Martin 2002). Nestling
period was defined as the number of days
between the last egg hatching and the last chick
leaving the nest.
Video cameras were placed at a discreet distance
($5 m) from the nest and camouflaged with
vegetation to minimize any influence on parental
behavior. Nests were filmed from 30 min after
sunrise for 6 to 8 hrs (Martin and Ghalambor 1999,
Martin 2002). Filming occurred on days 2–3 in
early incubation, during the middle of the incubation period, and ,2–3 days before expected hatch
day (early, middle, and late incubation). Nests
found after laying were filmed opportunistically on
other days (Martin 2002). Nest attentiveness at
individual nests was measured as the percent time
females were on the nest based on the number of
minutes spent incubating divided by the total
number of minutes a nest was filmed (Martin 2002).
Incubating egg temperatures (u C) were measured by inserting a thermistor into the egg center
through a small opening in the shell that was
sealed with adhesive (Weathers and Sullivan
1989, Martin et al. 2007). HOBO Stowaway
XTI dataloggers (Onset Corp., Bourne, MA,
USA) were connected to the thermistor by
discreetly inserting a fine wire through the nestwall. Thermistors were inserted within the first
2 days of incubation and dataloggers recorded
temperatures in 12–24 sec intervals for 5–7 days
per nest following Martin et al. (2007).
Nests were videotaped during the early nestling
period (days 1–3), during pin-break when flight
feathers broke their sheaths (days 10–11), and the
late nestling period preceding expected fledging
(day 15 and above). Nests were opportunistically
filmed on other days. Videotapes were analyzed
for parental brooding attentiveness (%) based on
the number of minutes brooding divided by the
total number of minutes a nest was filmed, as well
as the number of provisioning trips/hr (Martin and
Ghalambor 1999, Martin et al. 2000b). Analysis
of variance (ANOVA) was used to test for
changes in incubation and nestling attentiveness
between stages. Changes in brooding and provisioning rates with nestling age were analyzed
using correlation coefficients (r).
Chicks were measured every second day (from
day located) at the same time of day and at pinbreak. Standard measurements taken were mass,
tarsal length, wing chord, and primary feather pin
measurements. These data were used to calculate
the growth rate constant (k) following Ricklefs
(1967) and Remeš and Martin (2002). Overall
nesting success and predation rates for egg-laying,
incubation, and nestling periods were calculated
using the Mayfield method (Mayfield 1961, 1975;
Hensler and Nichols 1981; Johnson 2007). Chisquare tests of independence (X 2) were used to
test for differences in daily predation rates among
nest stages (egg laying, incubation, and nestling
periods).
Egg and nestling masses were measured using
an ACCULAB (Elk Grove, IL, USA) portable
electronic scale with a precision of 0.001 g; all
measurements were taken using Mitutoyo Digital
Calipers (Kingsport, TN, USA) with a precision of
0.01 mm. SPSS Version 15.0 (2006) was used for
statistical tests and means are given 6 one
standard error (SE).
RESULTS
Breeding Habitat.—Golden-faced Tyrannulets
nested most commonly near 1,400 m asl and were
not encountered above 1,500 m asl. This altitudinal zone contained primary and secondary growth
premontane and montane cloud forest with
patches of regenerating coffee (Coffea arabica)
plantations. Active nesting pairs were encountered
near forest edges including roads, forest trails,
water bodies, and areas of historical disturbance
inside the forest boundary. Areas where nests
were found contained suitable resources for nest
construction (moss and lichen) on tree trunks.
Nest Construction and Sites.—Pairs were observed exploring potentially suitable nest locations together prior to the nest-building process.
Only one of the pair, presumably the female,
constructed the nest (n 5 88 nest-building
observations), but the mate generally accompanied the nest-building individual. Nests were
typically constructed in a ball of moss on the
side of a tree, under a branch, or in an epiphyte
(Fig. 1). Two distinct building approaches were
observed for nest construction. The first and more
common approach involved building into an
existing lump of moss or lichen. The second
involved building the globular nest onto a bare
trunk surface. In the first approach, when a
suitable portion of moss or lichen was identified,
Goulding and Martin N GOLDEN-FACED TYRANNULET BREEDING BIOLOGY
691
FIG. 2. Seasonal distribution of nest initiation (date the
first egg is laid in a nest) for the Golden-faced Tyrannulet at
weekly (7 day) intervals.
FIG. 1. Typical nest (with eggs and nestling) of the
Golden-faced Tyrannulet with incubating female (Photographs by W. Goulding).
the adult would open a cavity first with the beak
and head and, when at the mid-body section,
would use its wings to thrust apart the moss and
widen a cavity. The adult would collect materials
to create the inside of the nest once a cavity was
established. The adult used more of the other
nesting materials for construction inside with the
moss in situ. However, in the second approach
where the nest was created on a relatively bare
surface, initial construction involved slinging the
nest material with spider webs from a point on the
bark or from a small piece of moss or lichen.
Females were observed repeatedly descending to
the ground to scour exposed banks and road
cuttings for rootlets and spider webs during
construction (e.g., 6 visits in 10 min to the same
location on a bank). They also loudly called from
beside the nest after building visits with the
nearby male usually responding. Females were
observed re-using nesting material from previous
unsuccessful nests, particularly the lining, but new
material was often used. The small size of the nest
often resulted in destruction of the nest during
predation events.
The mean height of nests above ground was
5.43 6 0.42 m (n 5 55). The external measurements were 116.14 6 4.27 mm (n 5 10) in height
by 70.83 6 2.50 mm (n 5 6) in width. Nest cups
had an external depth of 48.25 6 2.87 mm (n 5
10) with internal depth and internal diameter
being 32.85 6 2.55 mm (n 5 10) and 40.57 6
2.71 mm (n 5 7), respectively. Analysis of 11
nests showed an outer supporting structure of
moss into which spider webs, black rootlets,
lichen, and spider egg-casings of varying proportions were inserted with internal layers of finer
dark rootlets. The final internal layer was a golden
lining of soft, comose seed-arils fitting descriptions of liana seeds in the genus Odontadenia
(Apocynaceae) (Orlando Vargas Ramirez, pers.
comm.). The golden lining was characteristic of
all Z. chrysops nests that we observed.
The earliest nest was initiated (i.e., first egg
laid) on 13 March and the latest on 15 May with a
mean initiation date of 11 April 6 2.2 days (n 5
61) across years (Fig. 2). Nest-building activity
began in February. Two nests that fledged chicks
in early May 2006 were re-used in February 2007
with new material added.
Eggs and Clutch Size.—Eggs were elliptical in
shape and cream-white with liver-brown spots and
markings mostly concentrated in a ring toward the
obtuse end (Fig. 1). Eggs were 17.17 6 0.25 mm
in length by 13.42 6 0.11 mm in width (n 5 11).
Eggs weighed between 1.286 and 1.861 g with a
mean mass of 1.616 6 0.020 g (n 5 48). Fresh
egg weight represented 18% of mean adult body
mass of 9.0 6 0.2 g (n 5 25).
Clutch size was usually two with only one of 45
nests found prior to incubation having a single
egg, yielding a mean clutch size of 1.98 6 0.02
eggs (n 5 45). The mean number of days
observed between nest completion and laying of
692
THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 122, No. 4, December 2010
FIG. 3. Average (A) nest attentiveness, and (B) on- and
off-bout durations across three periods of incubation: early
(days 1–5), middle (days 6–11), and late (days 12–18).
Sample sizes reflect numbers of nests.
FIG. 4. The change with nestling age in (A) female
brooding behavior (% time spent brooding) and (B) rates
that parents visit the nest to provision nestlings.
the first egg was 4.71 6 0.47 (n 5 7). Eggs were
laid in the morning on alternate days.
Incubation.—Females incubated the eggs without help from males. Males were rarely observed
visiting nests during incubation, and did so at only
two of 40 nests with video observations of 6–8 hrs
each, yielding an average of 0.01 6 0.01 visits/hr
(n 5 40).
Females were not observed incubating prior to
laying the last egg and eggs hatched synchronously. Nest attentiveness averaged 66.0 6 1.6%
(n 5 40) and was lower (ANOVA, F2,37 5 6.8,
P 5 0.003) in early incubation compared with
middle and late incubation periods (Fig. 3A).
Incubation on-bouts averaged 33.35 6 1.94 min
(n 5 40) and did not change over the incubation
period (ANOVA, F2,37 5 1.1, P 5 0.3; Fig. 3B).
Length of off-bouts averaged 16.19 6 1.59 min (n
5 40) and decreased from early to later incubation
stages (ANOVA, F2,37 5 3.2, P 5 0.055;
Fig. 3B). Incubation behavior yielded an average
24-hr egg temperature of 34.88 6 0.45u C (n 5 7
nests, 43 days of sampling). The incubation period
was 16.9 6 0.3 days (n 5 10) for nests found
prior to beginning of incubation and where exact
hatch was observed.
Nestling Period.—Both adults were observed
provisioning chicks and the male was also
observed passing food to the female when she
was brooding. Adults regularly fed the nestlings
fruit that appeared to be mistletoe berries
(possibly Antidaphne viscoidea or Phoradendron
spp.), which were regularly found stuck near the
beak of chicks. Females regularly regurgitated
seeds when incubating and brooding, taking care
to eject them outside the nest. The percentage of
time females brooded decreased through the
nestling period (r 5 20.86, P , 0.001), and
stopped after the eighth primary pin feather broke
its sheath on days 10–11 (Fig. 4A). Provisioning
rates increased over the nestling period (r 5 0.80,
P , 0.001, Fig. 4B). Parents visited the nest an
average of 4.41 6 0.65 trips/hr (n 5 10) during
days 1 and 2 after hatching, and 14.93 6 2.36
trips/hr (n 5 6) at pin-break.
Chicks had gray down distributed lightly over
the head and body, and orange skin and beak at
hatching (Fig. 1). The nestling period for nests
where exact hatch and fledging days were
Goulding and Martin N GOLDEN-FACED TYRANNULET BREEDING BIOLOGY
693
tarsus length was slower at k 5 0.200 6 0.012 and
tarsus size was essentially the same length as
adults at 16.26 6 0.17 mm (n 5 22) at fledging
(Fig. 5B). Growth rate based on wing chord was k
5 0.201 6 0.010, but wing chord at fledging was
less than adult size (Fig. 5C) of 52.03 6 0.62 mm
(n 5 20).
Nesting Success and Predation.—Predation
accounted for 91.6% of failures with remaining
failures attributed to nests falling, abandonment,
and poor nest condition that allowed chicks to fall
out (re-used nest). Birds seemed to be a main
predator of nests with punctured egg remains at
times found near the nest. Nest predation often
coincided with presence of army ants (Labidus
praedator) and large mixed-bird flocks feeding
near the nest. One nest was also filmed being
predated by a capuchin monkey (Cebus olivaceus). Snakes were not recorded in video
observations and rarely observed at this elevation
in Yacambú across all years (TEM, pers. obs.).
The total daily predation rate was 0.057 6
0.007 (n 5 989 exposure days) with a total daily
mortality rate of 0.064 6 0.008. An estimated
12% of nests were successful based on a total
nesting period of 37 days. The daily nest
predation rate during egg-laying (0.052 6 0.025;
n 5 76.5 exposure days) did not differ (X 2 5 0.4,
P 5 0.6) from the incubation period (0.068 6
0.010; n 5 575.5 exposure days). However, the
daily predation rate during the nestling period
(0.039 6 0.010; n 5 377 exposure days) was
lower (X 2 5 4.2, P 5 0.029) than during
incubation.
FIG. 5. Relationships of (A) mass, (B) tarsus length,
and (C) wing chord length plotted against age for Goldenfaced Tyrannulets and their estimated growth rate constants
(k). The dashed lines represent mean adult sizes.
observed ranged from 17 to 19 days with an
average of 18.0 6 0.2 days (n 5 9). Nestling mass
on days 10 and 11 (i.e., pin-break) was 6.966 6
0.152 g (n 5 9). The growth rate constant (k) for
body mass was low (Fig. 5A) and nestlings were
close to mean adult weight of 9.0 6 0.2 g (n 5
25) at fledging (Fig. 5A). Growth rate based on
DISCUSSION
Golden-faced Tyrannulets in Yacambú National Park exhibited breeding biology parameters
different from most typical tyrannids (Fitzpatrick
2004). The nest appears globular, as also described for congeners (e.g., Z. acer [Beebe et al.
1917], Z. improbus [Hilty 2003], and Z. vilissimus
[Skutch 1960]), but varied in appearance depending on location of attachment and amount of
exposed nest. Nests of Z. chrysops, compared with
congeners, were slightly larger than those of Z.
vilissimus (Skutch 1960), but had a shallower
nest-cup than observed for Z. acer (Beebe et al.
1917; this was a single observation). Nest
construction and materials were virtually the same
as those observed for Z. vilissimus, including the
soft seed-aril lining (Skutch 1960), and similar to
Z. acer (Beebe et al. 1917). The use of epiphytic
694
THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 122, No. 4, December 2010
plant resources for nesting by neotropical birds is
well recognised (Nadkarni and Matelson 1989,
Fierro-Calderón and Martin 2007).
Golden-faced Tyrannulets show flexibility in
nesting height with 71% of nests in Yacambú
below the 8–12 m height range observed in
Colombia (Hilty and Brown 1986), and a nest
recorded ,45 m above ground in an emergent
Ceiba tree in Ecuador (Cisneros-Heredia 2006).
Our observations do not seem to reflect biases
towards finding low nests because we found the
majority of nests through parental behavior. We
found nests to the tops of canopies by watching
parental behavior. The lower height of nests at our
site might reflect the lower stature of the disturbed
forest areas and edges in which the species
occurred at our site. Differences between nesting
height in disturbed or regrowth areas and primary
forest have been observed in other tyrannids (e.g.,
Z. vilissimus [Skutch 1960] and Todirostrum
chrysocrotaphum [Hilty and Brown 1986]), indicating structural differences in habitat influence
nest height variation.
Nest architecture seems to be an evolutionarily
conservative character that has been used to
indicate phylogenetic relationships (Mobley and
Prum 1995, Sheldon and Winkler 1999, Zyskowski and Prum 1999). Enclosed nests are
thought to be a derived character from the more
common open nests reported for the majority of
tyrannids (Collias and Collias 1984, Fitzpatrick
2004). It is also thought to be a character that
evolved independently in different tyrannid subfamilies (Fitzpatrick 2004). The sparse available
information on nests of species of Zimmerius
indicates only subtle differences between congeners. However, nests of the majority of species in
the genus have yet to be investigated. Nest
similarity may support a close relationship between Camptostoma (Haverschmidt 1954) and
Zimmerius (unless evolved independently; Lanyon
1988). These two genera, together with the closely
related Phyllomyias virescens and others in that
genus that may be discovered to have enclosed
nests (Fitzpatrick 2004, Ohlson et al. 2008,
Rheindt et al. 2008), represent the only enclosed
nest-builders in the elaeniine clade proposed by
Ohlson et al. (2008). Despite differences in
external materials, they have similarly attached
and shaped immobile nests lined with ‘plant wool’
(not feathers) with a simple side-opening near the
top (Beebe et al. 1917, Haverschmidt 1954, Skutch
1960, this study).
The observed peak of breeding activity of Z.
chrysops is just prior to and overlapping the peak
precipitation period from late April through July
in Yacambú (Fierro-Calderón and Martin 2007).
This is a pattern in avian breeding biology
observed at other neotropical sites (Skutch 1950,
1960; Marchant 1959; Best et al. 1996; Medeiros
and Marini 2007), including some species in
lowland habitats in Venezuela (Cruz and Andrews
1989). This peak fits within the general breeding
period of January to June described for tyrantflycatchers north of Peru (Fitzpatrick 2004). The
season is relatively short compared with other
passerine species in this area (e.g., Biancucci and
Martin 2008, Niklison et al. 2008, Cox and Martin
2009). Skutch (1950) found from his observations
in Central America that, in general, avian
populations at higher altitudes exhibited a more
marked and narrow breeding season than in
lowlands. Z. chrysops is thought to breed in
Colombia from April until November at the lower
elevation of 1,000 m asl (Hilty and Brown 1986).
A record in February from Loja Province in
Ecuador also reports nesting activity by the
species at a similar altitude to Yacambú sites
(Best et al. 1996). The short season and absence of
any observations of birds re-nesting in the same
season after a successful breeding attempt indicates this species is single-brooded, typical of
tyrannids (Fitzpatrick 2004).
Eggs of Z. chrysops conform to the typical egg
coloration observed in most tyrannids (Von
Ihering 1904, Skutch 1960, Wetmore 1972). They
are slightly larger than an egg of Z. acer measured
by Beebe et al. (1917) and slightly shorter and
wider than eggs of Z. vilissimus observed by
Skutch (1960). The clutch size of two is on the
lower edge of the range of 2–6 observed in the
family and the 2–4 of most tropical tyrannids
(Fitzpatrick 2004).
The 17-day incubation period is long relative to
the range of 12 to 16 days known for most
temperate and tropical tyrannids, and approaches
a few unusual tropical species that have suspended pendulant nests and long incubation periods
(Fitzpatrick 2004). However, the incubation
period was near the average for 33 other nontyrannid species studied in Yacambú National
Park (Martin and Schwabl 2008). The 18-day
nestling period also is in the upper range for
tyrannids, which is from 12 to 24 days with most
being 14 to 17 days (Fitzpatrick 2004). Our
observations support that mistletoe fruit in the
Goulding and Martin N GOLDEN-FACED TYRANNULET BREEDING BIOLOGY
area (e.g., Antidaphne viscoidea; Restrepo et al.
2002, Kelly et al. 2004) comprise an important
portion of the diet of nestlings, as with Z.
vilissimus (Skutch 1960), and not only for adults
for which this has already been observed with
others in the genus (Fjeldså and Krabbe 1990,
Alonso and Whitney 2001, Fitzpatrick 2004).
Slow growth has been found in other tropical
species that feed fruit to their offspring (Morton
1973). A comparison of the growth rate constant
(k) for mass with that published and summarized
for other tropical and temperate species (Ricklefs
1976, Willis et al. 1978, Oniki and Ricklefs 1981,
Starck and Ricklefs 1998, Remeš and Martin
2002) reveals it is slow even for the slowest
growing of tropical tyrannids (k , 0.3). Tropical
tyrannids from Central America and Brazil had
growth rates (k) extending from a low of 0.248 in
another species (Mionectes macconnelli) that
builds enclosed nests (Willis et al. 1978) to rates
$0.4, similar to those observed for some faster
growing tyrannids breeding in North America
such as Tyrannus tyrannus (k 5 0.438) and
Sayornis phoebe (k 5 0.425) (Murphy 1981),
Tyrannus verticalis (k 5 0.416) and T. forficatus
(k 5 0.394) (Murphy 1988), Empidonax minimus
(k 5 0.499–0.505) (Briskie and Sealy 1989), and
E. oberholseri (k 5 0.425) (Pereyra and Morton
2001). Other non-tyrannid passerines investigated
in Yacambú National Park also had much higher
growth rates (Niklison et al. 2008, Biancucci and
Martin 2008, Cox and Martin 2009).
Incubation temperature is a reflection of
parental attentiveness with cooler temperatures
(low attentiveness) associated with longer incubation period lengths (Lyon and Montgomerie
1985, Martin 2002, Hepp et al. 2006, Martin et al.
2007). The observed 24-hr incubation temperature
for Z. chrysops is below the optimal temperature
range for embryonic growth (White and Kinney
1974, Webb 1987). However, egg temperature
was close to the expected value for a tropical
species with this length of incubation period and
nest attentiveness (Martin et al. 2007: figure 2).
Skutch (1960) considered Z. vilissimus in Costa
Rica to have high nest attentiveness for a small
flycatcher. He observed mean on and off-bouts
during incubation of 32.5 and 12.5 min, respectively
with overall estimates of attentiveness of 67 and
72%. This indicated higher attentiveness (and shorter
off-bouts) for this congener than for Z. chrysops in
Yacambú National Park. Attentiveness for Z.
chrysops was in the middle of the range of 39 other
695
species studied in Yacambú (Martin and Schwabl
2008), but was lower than for most temperate
passerines (Conway and Martin 2000: appendix 1;
Martin 2002; Chalfoun and Martin 2007).
Z. vilissimus had higher provisioning rates than
those observed for Z. chrysops (Skutch 1960).
However, both had mean feeding rates at least
two-fold higher than other species studied in
Yacambú National Park (Fierro-Calderón and
Martin 2007, Biancucci and Martin 2008, Niklison et al. 2008, Cox and Martin 2009). This could
reflect compensation for lower protein levels in
fruit fed to nestlings (Morton 1973), although
flycatchers seem to feed at higher rates than other
species (Martin et al. 2000b). Consequently,
predation levels could be influenced through
greater nest detection due to increased parental
visits (Skutch 1949; Martin et al. 2000a, b).
However, predation rates were lower during the
nestling period than during earlier periods when
parents were less active.
Nesting success for Z. chrysops was among the
lowest observed for a member of the Tyrannidae
when compared with other southern hemisphere
and neotropical species. Skutch (1985) summarized data from different species in the humid
Neotropics showing that 39.7% of nests found
were successful with tyrannids exhibiting a range
of 12.1 to 50%. Mionectes oleagineus in Trinidad
had the lowest tyrannid nesting success (12.1%), a
trend observed in other small species in Trinidad
(Snow and Snow 1979). Low reproductive
estimates were observed in Suiriri islerorum
($13.6%, mean 5 20.8%) and S. affinis (19%)
in tropical savannah of Brazil (Lopes and Marini
2005, Franca and Marini 2009). In Costa Rica,
36% of nests of Zimmerius vilissimus were
successful and fledged chicks (Skutch 1985).
Other non-tyrannid neotropical species in Panama
were observed to have low nesting success similar
to Z. chrysops (e.g., some formicariids and a
thamnophilid species; Robinson et al. 2000).
However, nesting success was generally higher
(23–74%) and daily predation rates lower for other
tyrannid species in the Neotropics and southern
hemisphere; e.g., Argentina (Mezquida and Marone
2001, Auer et al. 2007), Puerto Rico (Torres Báez
and Collazo 1992), Brazil (Willis et al. 1978,
Aguilar et al. 2000, Medeiros and Marini 2007), and
Panama (Robinson et al. 2000, Dyrcz 2002).
The extremely poor nesting success of Z.
chrysops reflects high predation pressure, and
may reflect the tendency for this species to nest
696
THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 122, No. 4, December 2010
along forest edges where predation levels are high
(Söderström 1999). Multiple re-nest attempts
would be expected to occur to compensate for
high predation (Martin 1995, Fitzpatrick 2004),
but the short breeding season (i.e., Fig. 2) and our
observations suggest that only 2–3 nesting
attempts are made.
The small clutch size of Z. chrysops with a
relatively long incubation period and slow nestling growth suggest this species is at the ‘slow’
end of the slow-fast life history gradient (Martin
1996, 2004). The solely neotropical distribution,
lack of morphological specialization (Traylor
1977), and indication that only conservative
differences in nest architecture occur within the
genus, place importance on investigating reproductive parameters of the diversity of Zimmerius
species. Phenotypic similarity or dissimilarities
would be valuable for understanding the finer
scale processes influencing reproduction and
broader life history variation within tyrannids;
e.g., localized predation rates imposed upon
otherwise phylogenetically close and similar
species (Skutch 1949, 1985; Bosque and Bosque
1995; Martin 1995; Martin et al. 2000a).
ACKNOWLEDGMENTS
We thank L. A. Biancucci, Karolina Fierro-Calderón, A.
M. Niklison, M. J. Foguet, A. A. Majewska, and R. A.
Ruggera for discussions and assistance in the field. We also
thank John Kanowski, Elena Arriero, Martine Maron, and
C. A. McAlpine for help with the manuscript. This study
was made possible in part by support under NSF grants
DEB-0543178 and DEB-0841764 to T. E. Martin. Permit
numbers were DM/0000237 from FONACIT, PA-INP-0052004 from INPARQUES, and 01-03-03-1147 from Ministerio del Ambiente. Specific equipment identities are
provided to aid specific methods and do not represent an
endorsement of these companies by USGS.
LITERATURE CITED
AGUILAR, T. M., M. MALDONADO-COELHO, AND M. Â.
MARINI. 2000. Nesting biology of the Gray-hooded
Flycatcher (Mionectes rufiventris). Ornitologia Neotropical 11:223–230.
ALONSO, J. A. AND B. M. WHITNEY. 2001. A new
Zimmerius tyrannulet (Aves: Tyrannidae) from white
sand forests of northern Amazonian Peru. Wilson
Bulletin 113:1–9.
AUER, S. K., R. D. BASSAR, J. J. FONTAINE, AND T. E.
MARTIN, 2007. Breeding biology of passerines in a
subtropical montane forest in northwestern Argentina.
Condor 109:321–333.
BEEBE, W., G. I. HARTLEY, AND P. G. HOWES. 1917.
Tropical wildlife in British Guiana. Volume 1. New
York Zoological Society, New York, USA.
BEST, B. J., M. CHECKER, R. M. THEWLIS, A. L. BEST, AND
W. DUCKWORTH. 1996. New bird breeding data from
southwestern Ecuador. Ornithologia Neotropical 7:69–
73.
BIANCUCCI, L. A. AND T. E. MARTIN. 2008. First description
of the breeding biology and natural history of the Ochrebreasted Brush Finch (Atlapetes semirufus) in Venezuela. Wilson Journal of Ornithology 120:856–862.
BOSQUE, C. AND M. T. BOSQUE. 1995. Nest predation as a
selective factor in the evolution of development rates
in altricial birds. American Naturalist 145:234–260.
BRISKIE, J. V. AND S. G. SEALY. 1989. Determination of
clutch size in the Least Flycatcher. Auk 106:269–278.
CHALFOUN, A. AND T. E. MARTIN. 2007. Latitudinal
variation in avian incubation attentiveness and a test
of the food limitation hypothesis. Animal Behaviour
73:579–585.
CISNEROS-HEREDIA, D. A. 2006. Notes on breeding,
behaviour and distribution of some birds in Ecuador.
Bulletin of the British Ornithologists Club 126:153–
164.
COLLIAS, N. E. AND E. C. COLLIAS. 1984. Nest building and
bird behavior. Princeton University Press, Princeton,
New Jersey, USA.
CONWAY, C. J. AND T. E. MARTIN. 2000. Evolution of
passerine incubation behavior: influence of food,
temperature, and nest predation. Evolution 54:670–
685.
COX, W. A. AND T. E. MARTIN. 2009. Breeding biology of
the Three-Striped Warbler in Venezuela: a contrast
between tropical and temperate parulids. Wilson
Journal of Ornithology 121:667–678.
CRUZ, A. AND R. W. ANDREWS. 1989. Observations on the
breeding biology of passerines in a seasonally flooded
savanna in Venezuela. Wilson Bulletin 101:62–76.
DYRCZ, A. 2002. Breeding ecology of the Social (Myiozetetes similis) and Rusty-margined (M. cayanensis)
flycatchers at Barro Colorado Island, Republic of
Panama. Ornitologia Neotropical 13:143–151.
FIERRO-CALDERÓN, K. AND T. E. MARTIN. 2007. Reproductive biology of the Violet-chested Hummingbird in
Venezuela and comparisons with other tropical and
temperate hummingbirds. Condor 109:680–685.
FITZPATRICK, J. W. 2004. Family Tyrannidae (Tyrant
Flycatchers). Pages 170–257 in Handbook of the birds
of the world. Volume 9. Cotingas to pipits and
wagtails (J. del Hoyo, A. Elliott, and D. A. Christie,
Editors). Lynx Edicions, Barcelona, Spain.
FJELDSÅ, J. AND N. KRABBE. 1990. Birds of the High Andes.
Zoological Museum, University of Copenhagen, Denmark.
FRANCA, L. F. AND M. Â. MARINI. 2009. Low and
variable reproductive success of a neotropical tyrantflycatcher, Chapada Flycatcher (Suiriri islerorum).
Emu 109:265–269.
HAVERSCHMIDT, F. 1954. The nesting of the Ridgway
Tyrannulet in Surinam. Condor 56:139–141.
HENSLER, G. L. AND J. D. NICHOLS. 1981. The Mayfield
method of estimating nesting success: a model,
estimators and simulation results. Wilson Bulletin
93:42–53.
Goulding and Martin N GOLDEN-FACED TYRANNULET BREEDING BIOLOGY
HEPP, G. R., R. A. KENNAMER, AND M. H. JOHNSON. 2006.
Maternal effects in Wood Ducks: incubation temperature influences incubation period and neonate phenotype. Functional Ecology 20:307–314.
HILTY, S. J. 2003. Birds of Venezuela. Second Edition.
Princeton University Press, Princeton, New Jersey,
USA.
HILTY, S. J. AND W. L. BROWN. 1986. A guide to the birds
of Colombia. Princeton University Press, Princeton,
New Jersey, USA.
JOHNSON, D. H. 2007. Estimating nest success: a guide to
the methods. Studies in Avian Biology 34:65–72.
KELLY, D. L., G. O’DONOVAN, J. FEEHAN, S. MURPHY, S.
O. DRANGEID, AND L. MARCANO-BERTI. 2004. The
epiphyte communities of a montane rain forest in the
Andes of Venezuela: patterns in the distribution of the
flora. Journal of Tropical Ecology 20:643–666.
LANYON, W. E. 1988. A phylogeny of the thirty-two genera
in the Elaenia assemblage of tyrant flycatchers.
American Museum Novitates 2914:1–57.
LOPES, L. E. AND M. Â. MARINI. 2005. Low reproductive success of Campo Suiriri (Suiriri affinis) and
Chapada Flycatcher (S. islerorum) in the central
Brazilian Cerrado. Bird Conservation International
15:337–346.
LYON, B. E. AND R. D. MONTGOMERIE. 1985. Incubation
feeding in Snow Buntings: female manipulation or
indirect male parental care? Behavioral Ecology and
Sociobiology 17:279–284.
MARCHANT, S. 1959. The breeding season in S.W. Ecuador.
Ibis 101:137–152.
MARTIN, T. E. 1995. Avian life history evolution in relation
to nest sites, nest predation and food. Ecological
Monographs 65:101–127.
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. 2002. A new view for avian life history
evolution tested on an incubation paradox. Proceedings of the Royal Society of London, Series B
269:309–316.
MARTIN, T. E. 2004. Avian life-history evolution has an
eminent past: does it have a bright future? Auk
121:289–301.
MARTIN, T. E. AND C. K. GHALAMBOR. 1999. Males feeding
females during incubation. I. Required by microclimate or constrained by nest predation? American
Naturalist 153:131–139.
MARTIN, T. E. AND H. SCHWABL. 2008. Variation in maternal
effects and embryonic development rates among
passerine species. Philosophical Transactions of the
Royal Society of London, Series B 363:1663–1674.
MARTIN, T. E., J. SCOTT, AND C. MENGE. 2000a. Nest
predation increases with parental activity: separating
nest site and parental activity effects. Proceedings of
the Royal Society of London, Series B 267:2287–
2293.
MARTIN, T. E., P. R. MARTIN, C. R. OLSON, B. J.
HEIDINGER, AND J. J. FONTAINE. 2000b. Parental care
and clutch sizes in North and South American birds.
Science 287:1482–1485.
697
MARTIN, T. E., S. K. AUER, R. D. BASSAR, A. M. NIKLISON,
AND P. LLOYD. 2007. Geographic variation in avian
incubation periods and parental influences on embryonic temperature. Evolution 61:2558–2569.
MAYFIELD, H. 1961. Nesting success calculated from
exposure. Wilson Bulletin 73:255–261.
MAYFIELD, H. F. 1975. Suggestions for calculating nest
success. Wilson Bulletin 87:456–466.
MCGOWAN, K. J. 2004. Introduction: the world of birds.
Pages 1.1–1.114 in Handbook of bird biology (S.
Podulka, R. Rohrbaugh Jr., and R. Bonney, Editors).
Cornell Laboratory of Ornithology, Ithaca, New York,
USA.
MEDEIROS, R. C. S. AND M. Â. MARINI. 2007. Biologia
reprodutiva de Elaenia chiriquensis (Lawrence) (Aves,
Tyrannidae) em Cerrado do Brasil Central. Revista
Brasileira de Zoologia 24:12–20.
MEZQUIDA, E. T. AND L. MARONE. 2001. Factors affecting
nesting success of a bird assembly in the central Monte
Desert, Argentina. Journal of Avian Biology 32:287–296.
MOBLEY, J. A. AND R. O. PRUM. 1995. Phylogenetic
relationships of the Cinnamon Tyrant, Neopipo
cinnamomea, to the tyrant flycatchers. Condor
97:650–662.
MORTON, E. S. 1973. On the evolutionary advantages and
disadvantages of fruit eating in tropical birds.
American Naturalist 107:8–22.
MURPHY, M. T. 1981. Growth and aging of nestling Eastern
Kingbirds and Eastern Phoebes. Journal of Field
Ornithology 52:309–316.
MURPHY, M. T. 1988. Comparative reproductive biology of
kingbirds (Tyrannus spp.) in eastern Kansas. Wilson
Bulletin 100:357–376.
NADKARNI, N. M. AND T. J. MATELSON. 1989. Bird use of
epiphyte resources in neotropical trees. Condor
91:891–907.
NICE, M. M. 1954. Problems of incubation periods in North
American birds. Condor 56:173–197.
NIKLISON, A. M., J. I. ARETA, R. A. RUGGERA, K. L.
DECKER, C. BOSQUE, AND T. E. MARTIN. 2008. Natural
history and breeding biology of the Rusty-breasted
Antpitta (Grallaricula ferrugineipectus). Wilson Journal of Ornithology 120:345–352.
OHLSON, J., J. FJELDSÅ, AND P. G. P. ERICSON. 2008. Tyrant
flycatchers coming out in the open: phylogeny and
ecological radiation of Tyrannidae (Aves, Passeriformes). Zoologica Scripta 37:315–335.
ONIKI, Y. AND R. E. RICKLEFS. 1981. More growth rates of
birds in the humid New World tropics. Ibis 123:349–
353.
PALMER, R. S. (Editor). 1962. Handbook of North
American birds. Yale University Press, New Haven,
Connecticut, USA.
PEREYRA, M. E. AND M. L. MORTON. 2001. Nestling growth
and thermoregulatory development in subalpine Dusky
Flycatchers. Auk 118:116–136.
PRESTON, F. W. 1953. The shapes of bird eggs. Auk
70:160–182.
REMEŠ, V. AND T. E. MARTIN. 2002. Environmental
influences on the evolution of growth and development rates in passerines. Evolution 56:2505–2518.
698
THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 122, No. 4, December 2010
RESTREPO, C., S. SARGENT, D. J. LEVEY, AND D. M.
WATSON. 2002. The role of vertebrates in the
diversification of New World mistletoes. Pages 83–
98 in Seed dispersal and frugivory: ecology, evolution,
and conservation (D. J. Levey, W. R. Silva, and M.
Galetti, Editors). CAB International, Wallingford,
United Kingdom.
RHEINDT, F. E., J. A. NORMAN, AND L. CHRISTIDIS. 2008.
Phylogenetic relationships of tyrant-flycatchers (Aves:
Tyrannidae), with an emphasis on the elaeniine
assemblage. Molecular Phylogenetics and Evolution
46:88–101.
RICKLEFS, R. E. 1967. A graphical method of fitting
equations to growth curves. Ecology 48:978–983.
RICKLEFS, R. E. 1976. Growth rates of birds in the humid
New World tropics. Ibis 118:179–207.
RIDGELY, R. S. AND G. TUDOR. 1994. The birds of South
America, Volume 2. The suboscine passerines.
University of Texas Press, Austin, USA.
ROBINSON, W. D., T. R. ROBINSON, S. K. ROBINSON, AND J.
D. BRAWN. 2000. Nesting success of understory forest
birds in central Panama. Journal of Avian Biology
31:151–164.
SHELDON, F. H. AND D. W. WINKLER. 1999. Nest
architecture and avian systematics. Auk 116:875–877.
SKUTCH, A. F. 1949. Do tropical birds rear as many young
as they can nourish? Ibis 91:430–455.
SKUTCH, A. F. 1950. The nesting seasons of Central
American birds in relation to climate and food supply.
Ibis 92:185–222.
SKUTCH, A. F. 1960. Life histories of Central American
birds. Volume 2. Pacific Coast Avifauna Number 34.
SKUTCH, A. F. 1985. Clutch size, nesting success, and
predation on nests of neotropical birds, reviewed.
Ornithological Monographs 36:575–594.
SNOW, B. K. AND D. W. SNOW. 1979. The Ochre-bellied
Flycatcher and the evolution of lek behavior. Condor
81:286–292.
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.
SPSS. 2006. Version 15.0.0. SPSS Inc., Chicago, Illinois,
USA.
STARCK, J. M. AND R. E. RICKLEFS. 1998. Data set of avian
growth parameters. Pages 381–423 in Avian growth
and development (J. M. Starck and R. E. Ricklefs,
Editors). Oxford University Press, New York, USA.
STUTCHBURY, B. J. M. AND E. S. MORTON. 2001.
Behavioral ecology of tropical birds. Academic Press,
San Diego, California, USA.
TORRES BÁEZ, P. AND J. A. COLLAZO. 1992. Biologı́a
reproductiva y datos preliminares sobre patrones de
crecimiento del Juı́ de Puerico (Myiarchus antillarum)
en Cabo Rojo, Puerto Rico. Caribbean Journal of
Science 28:30–37.
TRAYLOR JR., M. A. 1977. A classification of the tyrant
flycatchers (Tyrannidae). Bulletin of the Museum of
Comparative Zoology 148:129–184.
VON IHERING, H. 1904. The biology of the Tyrannidae with
respect to their systematic arrangement. Auk 21:313–322.
WEATHERS, W. W. AND K. A. SULLIVAN. 1989. Nest
attentiveness and egg temperature in the Yellow-eyed
Junco. Condor 91:628–633.
WEBB, D. R. 1987. Thermal tolerance of avian embryos: a
review. Condor 89:874–898.
WETMORE, A. 1972. Birds of the Republic of Panama. Part 3.
Smithsonian Institution Press, Washington, D.C., USA.
WHITE, F. N. AND J. L. KINNEY. 1974. Avian incubation.
Science 186:107–115.
WILLIS, E. O., D. WECHSLER, AND Y. ONIKI. 1978. On
behavior and nesting of McConnell’s Flycatcher
(Pipromorpha macconnelli): does female rejection
lead to male promiscuity? Auk 95:1–8.
ZYSKOWSKI, K. AND R. O. PRUM. 1999. Phylogenetic
analysis of the nest architecture of neotropical
Ovenbirds (Furnariidae). Auk 116:891–911.