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Energetics of the acrobatic courtship
in male golden-collared manakins
(Manacus vitellinus)
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Research
Cite this article: Barske J, Fusani L, Wikelski
M, Feng NY, Santos M, Schlinger BA. 2014
Energetics of the acrobatic courtship in male
golden-collared manakins (Manacus vitellinus).
Proc. R. Soc. B 281: 20132482.
http://dx.doi.org/10.1098/rspb.2013.2482
Received: 25 September 2013
Accepted: 25 November 2013
Subject Areas:
behaviour, physiology, ecology
Keywords:
energetics, heart rate telemetry, courtship,
tropics, manakins
Author for correspondence:
J. Barske
e-mail: [email protected]
J. Barske1, L. Fusani3, M. Wikelski4,5, N. Y. Feng2, M. Santos6,7
and B. A. Schlinger1,2
1
Department of Ecology and Evolutionary Biology, and 2Department of Integrative Biology and Physiology, and
the Laboratory of Neuroendocrinology, Brain Research Institute, University of California, Los Angeles, CA, USA
3
Department of Biology and Evolution, University of Ferrara, Ferrara, Italy
4
Max Planck Institute for Ornithology, Radolfzell, Germany
5
Konstanz University, Konstanz, Germany
6
Departamento de Entomologı́a Médica, Instituto Conmemorativo Gorgas de Estudios de la Salud y Instituto
Smithsonian de Investigaciones Tropicales, Panama
7
Instituto Smithsonian de Investigaciones Tropicales, Panama
In lek mating systems, females choose mates through indicators of quality,
which males may exhibit by their performance of courtship displays. In temperate regions, displaying seasons are brief (one to two months), whereas in
the tropics courtship seasons may be prolonged. Moreover, in temperatebreeding animals lekking behaviour can be energetically demanding, but
little is known about the energy costs of lekking in tropical animals. Daily,
over the course of a nearly seven-month-long breeding season, male goldencollared manakins (Manacus vitellinus) of Panamanian rainforests perform
acrobatic courtship displays that markedly elevate heart rates, suggesting
that they require high energy investment. Typically, animals of tropical lowland forests (such as manakins) exhibit a ‘slow pace of life’ metabolic
strategy. We investigated whether male manakin courtship is indeed metabolically costly or whether the birds retain a low daily energy expenditure (DEE),
as seen in other tropical species. To assess these questions, we calibrated manakin heart rate against metabolic rate, examined daily lek activity and, using
telemetry, obtained heart rates of individual wild, lekking male manakins.
Although metabolic rates peak during courtship displays, we found that
males actually invest minimal time (only approx. 5 min d21) performing
displays. As a consequence, the DEE of approximately 39 kJ d21 for male manakins is comparable to other lowland tropical species. The short, intense bursts
of courtship by these birds make up only approximately 1.2% of their total
DEE. Presumably, this cost is negligible, enabling them to perform daily at
their arenas for months on end.
1. Introduction
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2013.2482 or
via http://rspb.royalsocietypublishing.org.
Males of many species provide no direct benefits to their mates, nor help with parental care, but aggregate in leks to court females for purposes of copulating [1].
Under these conditions, females choose a partner among many males, presumably assessing indicators of quality, such as male ornaments, behaviour or
position in the lek [1,2]. Such intensive male–male competition and/or selective
female choice can lead to the evolution of exaggerated secondary sexual phenotypic and/or behavioural traits [3,4]. In temperate regions, lekking species may
display across a one- to two-month-long season when the males are thought to
expend considerable energy in courtship, here defined as time on the lek when
many individual ‘courtship displays’ are performed. In birds, for example,
male great snipe (Gallinago media) [5] and sage grouse (Centrocercus urophasianus)
[6] spend many hours per day at their leks. Their courtship activity increases their
metabolic rates, causing significant weight loss in some individuals (usually the
less successful males) [6]. The large investment in courtship, however, can be
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
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2. Material and methods
Studies were conducted during the dry season (February –
March) in forests around Gamboa, Panama (9870 N, 798420 W)
and in facilities maintained by the Smithsonian Tropical Research
Institute (STRI).
(a) Heart rate telemetry
Heart rates were recorded via telemetry using miniature transmitters as described previously for small birds [47,49–51], including
GC manakins [24]. Using mistnets, eight adult male GC manakins
were captured from five leks. Birds were given coloured leg-bands
for individual identification. Out of eight birds, four were transferred to a laboratory facility within 10 km of their capture (and
release) site, where transmitters were attached and respirometry
calibration was performed. On the remaining four birds, transmitters were attached in the field and birds were released within
approximately 10 min at the site of capture. Each transmitter
(approx. 1 g; Sparrow Systems, Fisher, USA) has a 9 cm flexible
2
Proc. R. Soc. B 281: 20132482
This involves a high joule cost but less power [34,35]; ‘joule
cost’ is not to be confused with the evolutionary ‘cost of a
trait’ [3,4,36]. Both types of behaviour might require the
animal to develop specialized physiological and morphological adaptations, one for bouts of PMR and one for extended
metabolic demands (reviewed in [37,38]). Such distinctions
are especially valuable for understanding energy expenditure
of discrete behaviours such as courtship.
Gathering accurate data on energy utilization of natural
animal behaviours can be difficult, so captive animals are
often studied, as was the case for cheetahs described above (by
measuring O2 consumption on captive cats breathing into ventilated masks while running on treadmills [33]). Using telemetry
and miniature transmitters, heart rate measures can be obtained
from wild animals. They provide excellent temporal resolution,
such that estimates of metabolic rate can be obtained in the order
of seconds to minutes. This contrasts with more traditional techniques (e.g. the doubly labelled water method) that provide
estimates across days [39–42]. Heart rate stands as a proxy for
energy expenditure [42], so the application of heart rate telemetry can be a valuable technique to identify moment-to-moment
energy expenditure [3,4,36].
Previous studies of GC manakins obtained estimates of
BMR that suggested that they maintain metabolic rates comparable to other tropical species that lack vigorous courtship
displays [12,43,44]. As the relationship between BMR and
DEE is not clearly defined [45,46], we sought to obtain diurnal and nocturnal measures of energy expenditure of wild
lekking males during their peak months of courtship. Heart
rate telemetry, in combination with respirometry to estimate
energy expenditure, enabled us for the first time to obtain
estimates of energy expenditure during various hours of the
day, as well as during specific courtship behaviours in freeliving birds, something not previously possible (cf. [47,48]).
Energy expenditure was estimated in relation to measures
of daily lek activity as well as focal observations of individual
males (this study and [24]). In addition, we compared these
estimates to comparable data obtained previously from a
similar, though non-lekking, tropical bird, the spotted antbird (Hylophylax naevioides) [49]. Our work shows that male
manakins exhibit a tropical slow pace of life despite the performance of energetically costly displays. These data offer
new insight into the energetics of tropical courtship.
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rewarded by high reproductive success, as a few males
monopolize most matings [1,7].
Many species of lekking birds live in the tropics [1], but
studies of their energy investment in courtship are scarce. Compared with birds breeding at high latitudes, lowland tropical
birds tend to develop slowly, invest less in reproduction each
year, and display slow senescence and extended longevity,
as well as a low metabolic rate; a series of life-history traits
that collectively reflect a tropical ‘slow pace of life’ [8–17]. By
tropical, we refer to the wet, lowland forest environment, as
different metabolic life-history strategies appear to apply to
tropical animals living at high elevations or in deserts [18].
Golden-collared (GC) manakins (18.1 g; Manacus vitellinus)
are tropical passerine birds that are known for their elaborate
courtship displays. GC manakins live in lowland forests of
Panama. During a lengthy breeding season (up to seven
months in duration), adult males spend much of the day at
their leks engaged in male–male and male–female interactions that include performance of courtship displays.
Courtship is dominated by the ‘jump–snap’ display, which
involves vigorous and rapid jumping between young saplings
interspersed with loud snaps [19–21]. Individual ‘wingsnaps’
as well as high frequency ‘rollsnaps’ are produced as the wings
strike one another after being lifted rapidly over the birds’ back
[22,23]. When displaying, heart rates are profoundly elevated
in males, even briefly exceeding 1300 beats min21 [24], one
of the highest heart rates recorded for any avian/mammalian
species [25,26]. This elevated heart rate suggests that male
manakins expend considerable energy in the performance of
courtship activities. Outside of courtship, however, GC manakins exhibit life-history traits typical of the ‘slow pace’ of
tropical life, producing small clutches (one to two eggs
[10,27]) and living as long as 14 years [9,28,29]. Thus, it is
unclear whether, during the breeding season, male GC manakins are able to sustain a tropical slow pace of life in the face of
the putative high energy demands of courtship or whether GC
manakins are an exception to the general rule that tropical
birds have a lower energy expenditure than temperate birds.
Efforts to assess organismal energy metabolism have used
various measures that describe overlapping and distinct states
of metabolism, including basal (BMR) and resting metabolic
rate (RMR), as well as peak metabolic rate (PMR), which are
determined under controlled conditions in the laboratory
[11,30,31]. Field metabolic rate (FMR), or daily energy expenditure (DEE) is used to assess the average metabolic rate of
an animal under natural conditions. Whereas the tropical
‘slow pace of life’ is associated with a relatively low BMR
and PMR [11–17], there are insufficient data to assign a definitive FMR measure for lowland tropical birds, though a trend
towards decreased FMR has been described [18].
Although these measures describe average energy expenditure, they are less useful for assessing energy demands of
discrete behaviours. One can determine the absolute amount
of energy required for a given behaviour by accounting for
the duration of the behaviour (‘joule cost’) or as the increase
in energy expenditure per unit time with an emphasis on the
peak demand required ( joules per sec; ‘power’ [32]). The
latter measure is usually applied to behaviours involving
rapid bursts of high energy. During a chase, for example, cheetahs are thought to display a brief 50-fold increase in their RMR
[33]. This behaviour requires high power but low joule cost.
By contrast, while running, a marathoner displays a minimal
increase in metabolic rate, but for an extended time period.
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Energy metabolism is assumed to be equivalent to O2 consumption, as aerobic respiration restocks depleted ATP. Fick’s equation
relates heart rate to O2 consumption using stroke volume and the
arterio-venous difference in O2 content, the product of which is
defined as O2 pulse (OP) [53]. If OP is constant or varies in a predictable manner, a calibration between O2 consumption and
heart rate can define this relationship [42,54]. If CO2 production
is known, the respiratory exchange ratio (RER) of O2 consumption and CO2 production can be calculated in order to estimate
metabolic rate [55]. Heart rate is not a measure of absolute
energy expenditure as a potential error is associated with the
metabolic rate estimates based on the RER obtained in the calibration equation [42,54]. Heart rate was calibrated against O2
consumption in four male GC manakins. Once fitted with a
transmitter, the male was placed in an open flow respirometer
consisting of an airtight plastic 2 l volume chamber that enabled
simultaneous measurement of O2 inflow and CO2 outflow. Flow
rate was adjusted to 1400 ml min21, allowing for 95% equilibrium within 1.26 min or 99% equilibrium within 3.3 min, and
ambient temperatures were 28+18C. Heart rate was averaged
across the 5 s preceding the respirometry measurement, after
ensuring that heart rate was stable in the 60 s preceding the
measurements. Birds could freely move around in the chamber,
but when placed in a dark location, they were generally quiescent in the chambers. If individuals did not move vigorously to
achieve high heart rates, we approached the chambers and
birds were enticed to move. For each bird, RER was determined
at seven to eight different heart rates. Instantaneous O2 consumption was calculated using the equation of Bartholomew et al. [56],
after empirically determining its denominator. Following Withers [57], we obtained the rate of O2 consumption (for detailed
methodological description, see [47,57]). These measurements
were then used to obtain an equation relating heart rate to
metabolic rate as described below.
(d) Courtship activity
In a previous study, we found that courtship displays (in particular
the production of mechanical wing sounds) are associated with
extremely high heart rates, hence they are the most energydemanding behaviours performed on the lek [24]. Pointing to
their importance, wingsnap and rollsnap frequencies are also significant predictors of mating success [24]. We calculated average
on-lek activity across the day using audio recordings (06.30 to
17.30). During our study period, sunrise occurred between 06.03
and 06.34, with sunset occurring between 18.10 and 18.35. A
microphone attached to a digital recorder with more than 12 h of
battery life was placed in a central position within five different
leks (with 4+1 adult courting males) from which we obtained
three 1-day audio recordings (see electronic supplementary
material, table S1). To estimate daily social and courtship activity,
audio files were analysed using COOLEDIT v. 2000 software. Dividing the file into 1 h intervals, starting at 06.30, we counted the
number of wingsnaps and rollsnaps between 06.30 and 07.30,
which represented activity at 07.00, and so on. To estimate activity
of individual males on a lek, we divided the hourly sums of mechanical sounds produced by the number of males occupying that
lek. Breeding male GC manakins have very high lek attendance
and on the day of recording, all males were known to be present
on the lek. In addition, we used data from previously obtained
video recordings (n ¼ 17) and focal observations (n ¼ 31) of individual males, to estimate mating success in relation to the time
spent by males performing courtship displays [24]. High-speed
videos (n ¼ 87) of 17 courting males were used to measure the
average duration of a courtship display. With focal observations,
we measured the number of displays and rollsnaps performed
by males as well as their mating success.
(e) Statistical analyses
SPSS v. 19 (IBM Inc., USA) was used for statistical analyses.
Calibration relationships between heart rate and O2 consumption
of birds in the respirometer were determined by least-square
regressions. A generalized linear model (GLM) with metabolic
rate as the dependent variable, individual as a random factor
and heart rate as a covariate was used to determine the overall
relationship between heart rate and O2 consumption based on
the data collected for the four birds during calibration. The standard error of the estimate (SEE) and the coefficient of variation
(COV ¼ 100 SEE/estimate) were calculated after Green [54].
To investigate the pattern of courtship activity, we used a GLM
with hour of the day as the repeated measure (daytime) and leks
as the between-subject factor. The pattern of heart rate across the
day was examined using a GLM with hour of day as the repeated
measure (daytime). Heart rates were log-transformed to obtain
normality. Post hoc tests with Bonferroni corrections were used to
identify differences of activity or heart rate between different
time points. Differences between antbirds and GC manakins
were investigated using t tests. If not indicated differently, values
in the text are given as mean+s.e.m.
(c) Comparative analyses of manakin energetics
Heart rate measures and estimates of DEE were compared with
those obtained using a similar method in another lowland tropical bird of similar size, the spotted antbird (17.6 g) [49]. From six
adult male antbirds, heart rates were recorded continuously and
measurements were obtained every 5 min for 24 h (for additional
details, see [49]). Additionally, we compared GC manakin DEE
with estimates derived from several other models [18,58,59].
3. Results
(a) Patterns of daily courtship activity
Activity levels varied significantly across the day and
also between leks (daytime: F3.5,34.6 ¼ 9.159, p , 0.001; lek:
F4,10 ¼ 5.643, p ¼ 0.012; interaction: F13.8,34.6 ¼ 1.743, p ¼ 0.266;
3
Proc. R. Soc. B 281: 20132482
(b) Calibration of heart rate versus O2 consumption
GC manakin minimal MR, the best estimate of BMR or RMR in
wild birds in which environmental conditions and feeding
status cannot be controlled, was compared with RMR estimates
obtained from the equation of Aschoff & Pohl [60].
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wire antenna and two wire electrodes, and was glued to trimmed
feathers on the centre of the bird’s back. The two electrodes were
inserted beneath the skin (for details, see [49,50]). The heart rate
transmitters emitted a continuous, amplitude-modulated carrier
signal that was frequency-modulated by heart muscle potentials.
Transmitters attached in this way fall off after approximately
14 days, eliminating the need for recapture of the birds [52].
Every 10 min for 30 s, using a Yagi antenna connected to an
AR8000 receiver (AOR Ltd., Japan), heart rates were recorded as
sound files (mp3) on a digital recorder connected to the receiver
(mp3 recorder, Edirol R09, Roland Inc., Japan). In this way, heart
rate measures were obtained randomly with respect to behaviour,
providing an accurate reflection of the bird’s daily commitment to
different energetic demands. Sound files were analysed using
COOLEDIT v. 2000 software (Syntrillium Software, USA). Bandpass
filters (Fast Fourier transform filters) were applied to increase the
signal-to-noise ratio between heart rate frequency and carrier frequency. Heart rate was measured by identifying 10 consecutive
amplitude spikes, and then averaging the time intervals between
each spike pair [51]; skeletal muscle potentials were irregular
and easily distinguished from iterative potentials emanating
from the heart.
750
heart rate (beats min–1)
150
125
100
75
50
25
500
250
0
7
8
9
10 11 12 13
time of day (h)
14 15
16 17
Figure 1. Diurnal pattern of courtship activity of male GC manakins.
Mechanically produced sounds (wingsnaps and rollsnaps), measures of manakin social and courtship behaviour at the lek, were recorded for five different
leks in three 1-day recordings. Hourly means were calculated including
30 min before and after the time point. Values were then divided by the
number of males (4+1) on the corresponding lek, which was determined
with direct behavioural observations. Mean values of sounds produced
male21 h21 on each of the five leks are shown.
heart rate
7
8
9
10 11 12 13 14 15 16 17
7
8
9
10
11
12
13
14
15
16
17
Figure 2. Hourly differences in activity and heart rate levels. Results of
Bonferroni-corrected post hoc tests comparing activity and heart rate levels
between different hours of the day (07.00 to 17.00). Arrows indicate significant differences. The shaded area shows values for heart rates and arrows
refer to the hours on the top. For example, heart rate is lower at 13.00 compared with 08.00. The non-shaded area of the table refers to activity and
arrows refer to hours on the left. An example is the significantly lower activity
at 17.00 compared with 07.00 and 08.00.
figure 1). Thus, despite differences between leks in the magnitude of activity, leks were similar with respect to their patterns
of daily courtship. Activity was generally elevated in the
morning, declining to a nadir at 12.00, after which activity
levels increased significantly to a peak at 14.00, and then
declined significantly by 17.00 (figure 2).
(b) Patterns of daily heart rate
Telemetry transmitters added approximately 5.5% of a bird’s
body mass (18.1 g) and appeared to have minimal impact on
the birds: males with transmitters were regularly observed
06.00
12.00
time (h)
18.00
Figure 3. Daily heart rate pattern. The thick line represents the hourly mean
heart rates of eight male GC manakins. Hourly averages were calculated for
the 30 min before and after the time point. During the night, we obtained
heart rate measurements of only six manakins. No measure was taken at 3.00
in the morning, thus we averaged values of 2.00 and 4.00 to complete the
graph. Thin lines represent the 95% CIs (1 s.d.). Shaded areas indicate night
time (18.12 until 06.15).
courting and sometimes even copulating with females (see the
electronic supplementary material, video S1, of [24]). Nevertheless, we cannot rule out the possibility that they have
some impact on the birds, including increasing energy expenditure, leading to an overestimation of natural energy expenditure
(reviewed in [61]).
For six birds, we measured heart rates across a complete 24 h
span; heart rates during daylight hours were measured on two
additional birds (61+12 diurnal recordings versus 17+4 nocturnal recordings; electronic supplementary material, table S2).
When comparing hourly individual averages between 07.00
and 17.00, we found a significant effect of daytime on heart
rate (F10,40 ¼ 6.180, p , 0.001; figure 3). Heart rates rose steeply
after 05.00, reaching a significant peak of 596+37 beats min21
at 07.00, where they remained for another hour (figure 2).
Following this early morning peak, heart rates significantly
decreased to 394+14 beats min21 at 13.00. For the remainder
of the afternoon, heart rates were slightly elevated, reaching a
peak at 18.00 (500+16 beats min21), a time that corresponded
with decreased activity on the lek (figure 2).
At sunset, heart rates markedly declined, with nocturnal rates
generally low, decreasing to a min of 290+8 beats min21 at
04.00. This result corresponds with previous findings of low nocturnal metabolic activity in GC manakins such that the birds
appear to exhibit heterothermia, achieving a minimum nocturnal
body temperature of 26.88C [44]. Nevertheless, GC manakins
retain the capacity to be responsive at night [44] as we observed
discrete surges in nocturnal heart rate (approx. 700 beats min21)
in one bird, likely to indicate reactions to disturbance.
Taken together, these data allow us to calculate mean
diurnal (active) heart rate of 450+15 beats min21, calculated from 06.00 to 18.30, and a mean nocturnal heart rate of
332+23 beats min21. Overall, the mean daily heart rate
(24 h period) was 398+13 beats min21.
(c) Calibration of heart rate versus O2 consumption
Heart rate calibration measurements spanned 382–943 beats
min21 (see electronic supplementary material, table S3),
coinciding roughly with the range of heart rates recorded in
the field (195–979 beats min21). During courtship displays,
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activity
4
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wing- and rollsnaps male–1 h–1
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120
100
80
E
60
G
40
H
I
20
450
750
850
550
650
heart rate (beats min–1)
950
Figure 4. Relationship between heart rates and metabolic rates. Least-square
regressions of heart rates against metabolic rates for four birds determined by
calibration measurements: bird E ( p , 0.001), bird G ( p ¼ 0.013), bird H
( p , 0.001) and bird I ( p , 0.001). See table 1 for statistical details.
average heart rates exceeded these ranges by 38 beats min21
[24], so there may be some error in estimating metabolic rate
at those elevated heart rates, as calibration of such high
energy levels cannot be obtained in the laboratory. The RER
was on average 0.88+0.01, which lies within the predicted
range of 0.7–1 [30].
A linear relationship between O2 consumption and heart
rate of captive birds is required to estimate energy expenditure
from heart rates recorded in the wild. We found such a relationship in GC manakins (figure 4 and table 1), confirming what
had been observed previously in other small birds [47,49,51].
When comparing the regressions obtained from the four
birds, we found that intercepts were significantly different
between individual regressions (F4,28 ¼ 11.77, p , 0.001), but
the slopes were the same (table 1). Following Green et al. [41],
we obtained a final regression equation using the slope
from the pooled data with an average of the individual intercepts to predict energy expenditure in the wild: MR ¼ ( f H 0.148) 2 19.796, where MR is the metabolic rate in kJ day21
and f H is the heart rate in beats min21. Eqn (11) from [41]
was used to calculate the standard error of the estimated
MR. The error associated with the variation between GC
manakins (d 2) was 48.5 (kJ2)(beats min21)22 and the error
associated with the scatter around the regression lines (e 2)
was 8.1 1025 (beats min21)2.
(d) Daily energy metabolism and comparative analyses
From the average daily heart rate, we estimated DEE to be
39.1+2.5 kJ day21 (table 2). We are confident of these estimates given the relatively low 4–6% COV we obtained for each
estimate. The lowest recorded nocturnal heart rate was used to
estimate minimal MR, calculated to be 14.1+4.7 kJ day21.
Manakins had significantly lower day (t12 ¼ 25.534,
p , 0.001) and 24 h (t10 ¼ 24.525, p ¼ 0.001) heart rates
than those of spotted antbirds but no difference was found
in DEE between the two species (t10 ¼ 0.609, p ¼ 0.556;
table 2). Similar oxygen consumption combined with a
lower heart rate suggests that manakins have an increased
cardiac output, that is they eject a greater volume of blood
with each heartbeat. This conclusion is supported by the limited available data on heart weight in these species. A higher
cardiac output is typically associated with a larger heart mass;
bird
n
a
b
r2
p
E
7
213.8
0.15
0.97
, 0.001
G
H
7
7
24.76
222.55
0.14
0.15
0.71
0.93
0.017
,0.001
I
8
235.18
0.15
0.94
,0.001
when heart weight to body weight ratios are calculated for
these two species (dry heart weights over wet body weights
from [62]), that of manakins (0.046/15 g ¼ 3.1 1023) exceeds
that of antbirds (0.044/16.1 g ¼ 2.7 1023).
Our estimates of DEE in manakins obtained from heart
rate measures compare favourably with those based on a general model for tropical birds [18], whereas estimates obtained
from models for passeriformes in general [59] or songbirds
from arid and mesic climates [58] were almost twice that of
the GC manakins (table 3). Moreover, applying the equation
of Aschoff & Pohl [60] that estimates BMR of temperate zone
birds, a manakin-sized bird is predicted to have a BMR of
26 kJ day21, a value twice the minimal MR of 14 kJ day21
that we estimated in this study.
(e) Energy requirements for the courtship display
Male GC manakin heart rates rose during the performance of
courtship displays and rollsnaps to 1017+28 and 1062+
102 beats min21, respectively [24]. For courtship displays, this
rate corresponded to 131 kJ day21 (5.5 kJ h21) with a COV of
3% (corrected from [24]), which is equivalent to the PMR
of manakins induced by exercise measured by Wiersma et al.
[11]. Although overall lek activity lasted for many hours per
day, males varied greatly in the total number of displays they
performed, ranging from 1.6 to 140 displays day21, producing
an average of 32+5 displays day21 (n ¼ 31). Importantly, each display lasts on average 9.5+0.5 s (n ¼ 17), thus
males engage in courtship displays for only 5+1 min day21
(0.25–22.2 min day21; data from [24]). Consequently, they
spent on average 0.46 kJ in courtship displays, which corresponds to 1.2% of their DEE. On average, males also
produce 10.8+ 1.5 rollsnaps h21, expending an additional
0.04 kJ day21 on rollsnaps. Thus, the performance of the two
most demanding courtship behaviours requires on average
0.5 kJ day21. If we assume that the power required for a courtship display is similar across males, then the least active males
would spend approximately 0.1% of their DEE in courtship
displays compared with approximately 5.2% of the most
active ones (see electronic supplementary material, figure S1).
Although we have not measured energy investment in courtship in relation to mating success in GC manakins, it is likely
that from least active to most active and successful males, GC
manakins expend a minimal amount of energy in their courtship displays including the production of mechanical sounds.
5
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0
350
Table 1. Parameters of least-square regressions for heart rate against
metabolic rate of four male golden-collared manakins. Birds equipped with
a heart rate transmitter were placed in a respirometer, and heart rate was
measured simultaneously with O2 consumption and CO2 production. The
RER is used to estimate metabolic rate, following Walsberg & Hoffman
[55]. bird, birds used for calibrations; n, number of measurements that
have been taken at different heart rates; a, intercept; b, slope.
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metabolic rate (kJ day–1)
140
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variable
antbird
t (d.f.)
p
450+15 (8)
601+24 (6)
25.534(12)
0.000
night (b min )
24 h (b min21)
332+23 (6)
397+12 (6)
384+15 (6)
492+17 (6)
21.896(10)
24.525(10)
0.087
0.001
DEE (kJ day21)
39.1+2.5 (6)
37.4+2.4 (6)
0.609(10)
0.556
day (b min21)
21
Table 3. Estimates of DEE based on the heart rate method from this study
and three different models based on birds living in the tropics,
passeriformes, and passerines from arid and mesic climates. All model
estimates are based on the body weight of manakins (18.1 g).
method
DEE (kJ day21)
animals
heart rate method
39.1
GC manakins
Anderson & Jetz [18]
Nagy et al. [59]
38.8
74.5
tropical birds
passeriformes
Garamszegi et al.
[58]
79.0
passerine from arid
and mesic climates
4. Discussion
Despite their high-power-demanding courtship displays,
heart rate measures of free-living birds indicate that GC
manakins maintain a low DEE typical for tropical birds. Similar results are obtained by several independent analytic
approaches. First, using data collected via similar techniques, we found no difference between DEE of GC
manakins and the spotted antbird, a non-lekking sympatric
bird with a low DEE [49]. Second, when we apply several
models designed to provide general estimates of avian
energy expenditure, manakins’ energy expenditure is
approximately 50% of what is expected [58,59]. Only the
model by Anderson & Jetz [18] that is designed for tropical
birds provides an estimate that is similar to what we obtained
(table 3). In addition, compared with temperate-breeding
birds, BMR is lower in tropical birds, including the GC manakin [12,43,44]. Our data confirm the measurements of BMR
obtained by Vleck & Vleck [43] (21 kJ day21) and Bartholomew
et al. [44] (20 kJ day21), which are both lower than what
would be estimated by the equation of Aschoff & Pohl [60]
for birds of the temperate zone (26 kJ day21). Thus, our estimates of DEE as well as minimal MR together with previous
estimates of BMR strongly suggest that GC manakins with
their high-power-demanding courtship displays fall in the life
history strategy classification of ‘slow pace of life’, typical for
tropical birds [10,12,17,49].
We were surprised to discover that overall daily courtship
activity in GC manakins lacks high joule costs. Although individual courtship displays per se have high power demands,
reaching PMRs ninefold higher than minimal MR and threefold higher than DEE [11,24], males actually spend minimal
time per day in courtship performance, using on average
only 1.2% of their DEE on courtship dances. Short, highly
intensive exercise bouts are thought to rely on anaerobic
energy production, though there is good evidence that anaerobic metabolism plays a limited role in fuelling manakin
courtship. First, heart rates decrease the moment the courtship
display ends [24], evidence that the birds have not accumulated
an O2 deficit. Second, one can estimate aerobic scope, the maximum O2 consumption of an animal during exercise over the
animal’s BMR, which for birds of 18.1 g such as manakins is
estimated to be 36 [63]. We find that manakins reach only
about nine times BMR during courtship, which is well within
the animal’s aerobic scope, hence courtship is likely to be
sustained by aerobic metabolism. Thus, we are confident that
our measures are valid estimates of energy expenditure
during GC manakin courtship.
Collectively, males on a lek produce considerable noise in
order to attract females and engage in courtship bouts in
hopes of mating. Yet each individual invests minimal energy
in the lekking enterprise. Even the most active male, performing as many as 140 courtship displays per day, invests only 5%
of his DEE, because each display only lasts approximately 9.5 s.
This strategy of low joule costs could explain why manakins are
able to display for up to seven months of the year and retain a
lengthy life span.
In contrast to GC manakins, other lekking species engage in
courtship involving high joule costs [5,62,64,65]. For example,
sage grouse males perform on average 1680 displays during
one or two bouts per day [63,66]. Thus, each bout of displaying
(totalling about 1.4 h day21) probably functions as an endurance exercise [6]. These energy demands may impose limits
on the duration of the season of courtship, which lasts only
one to two months.
Courtship enables females to assess male quality for
purposes of mating [67]. Presumably, males that engage in
courtship that exacts high joule cost do so, at least partly, to
demonstrate their capacity to withstand the behaviouradded energy demands [2– 4]. The females might then
choose males based on their behavioural and/or physiological adaptations to accumulate and efficiently metabolize
the energy reserves required for courtship activity. Rather
than being limited by total energy, male GC manakins
appear to be performance-limited; that is, the courtship display may be designed to demonstrate physiological and
morphological qualities associated with their rapid, acrobatic
performances. For example, male manakins have hypertrophied skeletal muscles and fibres modified for increased
Proc. R. Soc. B 281: 20132482
manakin
6
rspb.royalsocietypublishing.org
Table 2. Heart rate measures and estimates of DEE of two tropical birds. DEE obtained with heart rate telemetry was compared between the golden-collared
manakin (18.1 g) and the spotted antbird (17.6 g). Columns 2 and 3 are mean values for manakins and antbirds for the following variables: average diurnal
heart rate (day), average minimal heart rate (night), average daily heart rate (24 h) and average DEE. Measures are reported as mean+s.e. (sample size).
Columns 4 and 5 show the results of t-tests comparing the different variables between the two species. Manakins have lower heart rates for two of the three
measures, but no difference is found in DEE. Also when comparing mass corrected DEE, we did not find a significant difference. Data on antbirds are taken
from [49].
Downloaded from http://rspb.royalsocietypublishing.org/ on June 16, 2017
All procedures for animal use were approved by UCLA Chancellor’s
Animal Research Committee, STRI and the Panamanian Autoridad
Nacional del Ambiente.
Acknowledgements. We thank the Smithsonian Tropical Research Institute for support in Panama. The Princeton University 2008 tropical
biology field course, G. Terranova and E. Choi contributed to data
collection and processing. We thank J. Green for his advice on
data analysis, and D. Altshuler and K. Nagy as well as anonymous
referees for valuable comments.
Funding statement. This research was supported by NSF-IBN-021319 to
B.A.S.
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