Universidad Sim6n Bolivar, Departamento de Biologœa de Organismos, Apartado 89000,
Caracas 1080, Venezuela; and
2University of California, Department of Avian Sciences, Davis, California 95616, USA
In homeotherms, residual variation of mainte-
nance-energy costs around allometric curves can be
related to factors independent of body mass, such as
food habits (McNab 1986), taxonomic affiliation
(Bennett and Harvey 1987), season (Kendeigh et al.
1977), habitat type (Hubert and Dawson 1974), cli-
mate (Weathers 1979), and body composition (Daan
et al. 1990). Food habits are important because the
rate of energy acquisition might limit the rate of en-
ergy expenditure (McNab 1986, Weiner 1992). For
mammals, McNab (1978, 1986)hypothesized that the
processing of food with low metabolizable energy
content, including the leaves of woody plants, re-
quires a low basal metabolic rate (BMR). Hence, ar-
boreal mammals that meet large portions of their en-
ergy requirement from leaves have lower BMRs than
predicted from allometric equations (McNab 1978,
1980a). Some of the reduction of BMR in folivorous
mammals seems to be related to properties of leaves,
E-mail: carlosb@usb.ve
such as their low metabolizable energy owing to the
content of difficult-to-digest fiber and to the high
content of secondary compounds (McNab 1978,
1986).
Food habits also influence rates of maintenance en-
ergy expenditure in birds (McNab 1988), but the re-
lationship between folivory and avian BMR is not
fully understood. To a large extent, this is because
little is known about the energetics of folivorous spe-
cies. Here, we report on the maintenance energy
costs and thermal response to ambient temperature
of two species of passerines that regularly include
leaves and other plant tissues in their diets. Passer-
ines are of interest because of their high mass-spe-
cific energy expenditure, because their small body
size constrains the use of green tissues of plants, and
because folivory is particularly scarce among them
(Morton 1978, Parra 1978). Characteristics intrinsic
to leaves should also affect avian consumers; there-
fore, it is of interest to determine if folivory is cor-
related with reduced BMR in birds, as it is in mam-
mals.
We studied two species of cardinalids, the Grayish
Saltator (Saltator coerulescens; 47.0 + SD of 2.6 g; n =
6) and the Orinocan Saltator (S. orenocensis; 32.7 _+ 2.1
g; n = 4) from the central floodplains (llanos) of Ven-
ezuela. Both species are generalized arboreal herbi-
vores at our study site, feeding mostly on fruits,
leaves, and other plant tissues.
Grayish Saltators feed almost exclusively on plant
tissue throughout the year. Their diet is largely made
up of fruit (35.6% of feeding observations), mature
leaves of woody plants (27.7%), and flowers (16.6%).
Most of the rest of the diet (20%) is made up of a va-
riety of other plant tissues (leaf buds, flower buds,
tendrils, and the skin of seed pods). Insects account
for only 0.1% of feeding observations (Rodriguez
1994). Orinocan Saltators also consume mostly plant
tissue throughout the year but are less folivorous
than Grayish Saltators. Nevertheless, during the
rainy season mature leaves account for 19.5% of feed-
ing observations and leaf buds a further 2.3%. The
rest of the diet is made up of flowers and flower but-
tons (34.5%), fruits (28.7%), and seeds (14.9%). Li-
chens and insects are consumed occasionally (Garcfa
1994). Both species have simple guts, and given their
small body size and brief mean retention time of di-
gesta (59 min for Grayish Saltator and 80 min for Or-
inocan Saltator), it is likely that the bulk of their en-
ergy requirements is extracted from cell solubles
rather than from fiber fermentation (Garcia 1994,
Rodriguez 1994). Other species of saltators are also
known to regularly include leaves, buds, and fruits
in their diets (Jenkins 1969, Munson and Robinson
1992); however, none that has been studied in more
detail is exclusively or obligatorily folivorous.
In this work, we compare maintenance energy
costs of both species of saltator with those expected
from allometric equations. We expected, by analogy
with arboreal folivorous mammals, that BMRs
would be lower than predicted for passerines of their
size.
Methods.--We mist netted saltators at Fundo Pe-
cuario Masaguaral (Gurico State, 8ø34'N, 67ø35'W),
a cattle ranch in the seasonal savannahs of Venezue-
la, from June to August 1995. Vegetation is a mosaic
of open savanna and gallery forest. Rainfall averages
1,400 to 1,500 mm annually and is largely concen-
trated in a single rainy season that lasts from May to
November. Temperature varies only slightly during
the year; average monthly minimum and maximum
temperatures are 19.0 and 37.7øC, respectively
(Troth 1979).
During the experimental period, birds were kept
for one to four days in individual cages in a room
exposed to natural photoperiod. During this period,
birds were offered cultivated (papaya and guava)
and wild fruits that are regularly included in their
natural diet (i.e. Annona jahni and Momordica char-
antia). Saltators readily adapt to cages and maintain
their body mass on a diet of fruit, which they prefer
to leaves under caged conditions (Garcfa 1994, Rod-
rfguez 1994). Birds were fasted for 4 to 6 h before the
experiments. Because enough time elapsed between
the last feeding and the experimental measurements
for birds to have emptied their guts several times, we
concluded that birds were under postabsorptive con-
ditions. Sex of the birds was unknown, and no in-
dividual was molting during the experiments.
We measured oxygen consumption (902) of six
Grayish Saltators and four Orinocan Saltators in re-
lation to ambient temperature (Ta) during the non-
active phase with an open-flow Applied Electro-
chemistry model S-3A analyzer as described in
Weathers et al. (1980). Birds were weighed to the
nearest 0.01 g before being placed in a dark, 15.2-L
metabolic chamber through which air was drawn
with a flow rate of approximately 0.762 L. min for
Grayish Saltators and 0.658 L - min - for Orinocan
Saltators. The chamber was placed in a thermostati-
cally controlled temperature cabinet that allowed us
to regulate ambient temperature. The system was al-
lowed to equilibrate for at least 1 h before the begin-
ning of measurements. Effluent air was run through
tubes containing silica gel and soda lime granules to
remove H20 and CO2 before measuring oxygen con-
centration. We recorded only the lowest stabilized
readings of the presumably inactive individuals. At
the end of each run, we opened the metabolic cham-
ber and measured cloacal body temperature (Tb)
with a thermocouple accurate to 0.1øC and re-
weighed the bird. We used the average of the initial
and final body masses of each bird to calculate its
specific metabolic rate. Ambient temperature in the
chamber was continuously monitored with Cu-Cn
thermocouples connected to a Campbell Scientific
CR21 data logger. Not every bird was run over the
whole ambient temperature range. Rates of oxygen
consumption were calculated according to Hill
(1972) and expressed under STP conditions.
For each species, the relationship between 902 and
To was examined by the method of Yaeger and Ultsch
(1989). This method fits two straight segments to the
data and determines the point where they intercept.
This point can be considered the lower critical tem-
perature where the shift from metabolic regulation
of oxygen consumption to metabolic conformation
occurs. We estimated "wet" thermal conductance by
calculating a mean conductance from individual
conductances obtained by applying C = 902 / (T -
To) to each measurement of oxygen consumption and
body temperature below thermoneutrality (McNab
1980b). We considered BMR as the average of O2
values within the thermoneutral zone. To compare
measured oxygen consumption rates with expecta-
tions from allometric equations, we used an energy
equivalent of I watt (W) to 0.05 mL O 2 . s-L All birds
were released unharmed .at the end of the experi-
ments.
Results for Grayish Saltators.--Based on the method
.
o
41
4O
39
38
37
38
10
2 3 4
5O
A 3.5
o_ 2.0
I-.
1.5
O 1.0
U,I
>- 0.5
x
o.o
lO
FIG. 1.
20 30 40 50
AMBIENT TEMPERATURE (øC)
Body temperature (A) and oxygen con-
sumption (B) in relation to ambient temperature of
six postabsorptive Grayish Saltators during their
nonactive phase. The two lines in the lower figure
were fitted by the method of Yeager and Ultsch (1989;
see text for equations). Each symbol represents one
individual bird.
of Yeager and Ultsch (1989), we fitted two lines to the
data set (Fig. lB). The line to the left (402 = 3.657 -
0.078T; n = 22, r = 0.790, P < 0.001) and the line to
the right (902 = 1.941 - 0.015Ta; n = 18, r = 0.296,
P = 0.233) intersected at 27.1øC. This point marks the
shift from metabolic conformation to metabolic reg-
ulation and can be considered to be the lower limit
of thermoneutrality. Average nightly body temper-
ature of individuals within the thermoneutral zone
was 39.4 _+ SE of 0.141øC (n = 14). Grayish Saltators
maintained a high but variable body temperature
(Fig. 1A). Although birds clearly could thermoreg-
ulate, their body temperature was not controlled pre-
cisely, and it varied significantly with ambient tem-
perature (T b = 36.4 + 0.091T; n = 40, r = 0.617, P
< 0.001). Not even within the thermoneutral zone
was there a clear indication that birds maintained a
constant body temperature. Average body tempera-
ture at night fell within the range recorded for other
passerines (see Prinzinger et al. 1991).
Basal metabolic rate was 1.489 _+ 0.04 mL O2 ß g-
ß h (n = 14), or 0.3887 W ß ind for a 47.0-g bird.
This value is 64.4% of that expected from body mass
for passerines during the night period as predicted
by Aschoff and Pohl (1970) and 63.6% of that ex-
pected for passerines during summer nights (calcu-
lated from Kendeigh et al. 1977). BMR measured for
the Grayish Saltator fell below the 95% confidence in-
terval of the standard regression of BMR and body
mass for birds (Reynolds and Lee 1996).
Thermal conductance was 0.116 _+ 0.002 mL O2
ß g- ß h - ß øC-, which is 18.9% higher than expected
from body mass for passerines during the rest phase
(i.e. 0.098 mL O 2 ß g ß h ß øC ; Aschoff 1981). Ex-
trapolated body (= ambient) temperature at a rate of
metabolism equal to zero (i.e. 46.9øC; Fig. lB) was
considerably higher than recorded body tempera-
tures.
Results for Orinocan Saltators.--The two lines fitted
by Yaeger and Ultsch's (1989) method, ''O 2 = 1.83 +
0.06T, and 902 = 2.91 - 0.04T,, intercepted at Ta =
10.9øC, which is not biologically meaningful. There-
fore, on the basis of visual inspection we divided the
data set in points above and below 25øC and fitted by
least squares a line to each subset (Fig. 2B). The line
to the left ('O = 3.925 - 0.080T; n = 11, r = 0.74,
P = 0.009) and the line to the right ('O: = 1.540 +
0.006T; n = 9, r = 0.102, P = 0.794) intersected at
27.7øC, which we considered to be the lower limit of
thermoneutrality. Average nightly body temperature
of individuals within the thermoneutral zone was
38.8øC _+ 0.269 (n = 6). As in the former species, body
temperature of Orinocan Saltators varied signifi-
cantly with ambient temperature, even within the
thermoneutral zone (Tb = 32.4 + 0.198T,; n = 20, r =
0.774, P < 0.001; Fig. 2A). Average body temperature
at night also fell within the range recorded for other
passerines (see Prinzinger et al. 1991).
Basal metabolic rate was 1.715 -+ 0.064 mL O: ß g
ß h (n = 6), or 0.3136 W. ind for a 32.7-g bird. This
value is 67.9% of that expected from body mass for
passerines during the night period as predicted by
Aschoff and Pohl (1970) and 65.4% of that expected
for passerines during summer nights as calculated
from Kendeigh et al. (1977). BMR of the Orinocan
Saltator also fell below the 95% confidence interval
of the standard regression of BMR and body mass for
birds (Reynolds and Lee 1996).
Thermal conductance of Orinocan Saltators was
0.143 _+ 0.004 mL O ß g ß h ß øC , which is 23.9%
higher than expected from body mass for passerines
during the rest phase (i.e. 0.115 mL O 2 ß g- ß h
ß øC-; Aschoff 1981). As for Grayish Saltators, ex-
trapolated body (= ambient) temperature at a rate of
metabolism equal to zero (i.e. 49.1øC; Fig. 2B) was
considerably higher than recorded body tempera-
tures.
m
0
4'1
4O
39
38
37
38
35
34
33 I ......... , .......
10 20
30 40 50
3.5
0 2.0
I--
Q.
'-' 1.5
O 1.0
- 0.5
o.o
lO
B
20 30 40 50
AMBIENT TEMPERATURE (øC)
FIG. 2. Body temperature (A) and oxygen con-
sumption (B) in relation to ambient temperature of
four postabsorptive Orinocan Saltators during their
nonactive phase. The two lines of the lower figure
were fitted by dividing the data set into points below
and above 25øC (see text for equations). Each symbol
represents one individual bird.
Discussion.--In accordance with expectations,
both species of saltator had substantially lower
BMRs than predicted from their body size. This re-
duction of resting metabolism should contribute to
an economy of daily energy expenditure. Other ar-
boreal folivores also have low BMRs. Speckled Mouse-
birds (Colius striatus; 50 to 55 g) and Blue-naped
Mousebirds (Urocolius macrourus; 51.3 g), two par-
tially folivorous species of tropical and temperate
Africa, feed on leaves, buds, and fruit and have
BMRs that are 75 and 63%, respectively, of expected
(Bartholomew and Trost 1970, Prinzinger 1988). Fur-
thermore, mousebirds are able to enter torpor, an im-
portant energy-saving mechanism (Bartholomew
and Trost 1970, Prinzinger et al. 1981). Likewise, the
obligate folivorous, fiber-fermenting Hoatzin (Op-
isthocomus hoazin; 598 g) of the Neotropics has a BMR
that is 69.8% of expected (Grajal 1991). In mammals,
reduction of BMR is highest in medium-sized arbo-
real species, particularly those that rely extensively
on fiber fermentation (McNab 1978). Microtine ro-
dents of small body mass that feed heavily on leaves
of woody plants, and that probably digest cell solu-
bles only, have high basal rates (McNab 1986). Fur-
thermore, in mammals it appears that BMR is re-
duced only in species whose diets consist of at least
20 to 30% leaves (McNab 1978: figure 6). In contrast,
BMRs are considerably reduced in small birds (e.g.
saltators and mousebirds) that are incapable of fiber
fermentation and that incorporate leaves in their diet
to a moderate extent only.
The interaction between food quality and diges-
tive physiology might influence metabolic rates of
homeotherms because digestive and absorptive pro-
cesses might limit rates of energy acquisition, thus
setting an upper ceiling to the energy budget of or-
ganisms (e.g. Weiner 1992, Veloso and Bozinovic
1993). In particular, McNab (1978, 1986) proposed
that the use of a poor food source by mammalian ar-
boreal folivores might require them to have a low
basal rate of metabolism. He posed three nonexclu-
sive explanations to interpret the correlation be-
tween folivory and reduced BMR in mammals. First,
leaves might have a low metabolizable energy con-
tent because they are rich in fiber, which is difficult
to digest. Limitations on the maximum bulk of en-
ergy-dilute food that can be processed daily by the
digestive tract might limit energy intake in folivores.
Second, the low basal rates of folivorous mammals
may be an adaptation to reduce the intake of toxic
secondary compounds present in the green tissues of
plants. Reduced intake of secondary compounds
may reduce dose-related negative effects and the
costs of detoxification. Third, arboreal mammalian
folivores, particularly larger species, are rather sed-
entary and have a low proportion of muscle mass rel-
ative to body mass. In mammals, low basal rates of
metabolism are correlated with reduced muscle
mass.
Explanations proposed by McNab in relation to
mammals might also apply to folivorous birds. First,
difficulties associated with the digestion of fiber (and
of soluble cell contents contained within fibrous cell
walls) determine that metabolizable energy of fo-
liage ranks lowest among bird foods (Karasov 1990).
Likewise, limitations of tract volume and processing
rate of energy-dilute foliage are known to limit in-
take rates in folivorous birds (Kenward and Sibly
1977). Second, folivorous birds are known to limit in-
take in order to reduce ingestion of toxic plant sec-
ondary metabolites (Jakubas et al. 1993), and detox-
ification costs might be a substantial portion of their
energy and nutrient budget (Guglielmo et al. 1996).
Third, in birds small muscle mass in association with
sedentary habits might also be correlated with a low
basal rate of metabolism (McNab 1988, 1994). Few
data exist on time budgets of arboreal folivorous
birds, but it is of interest that the obligatorily foli-
vorous Hoatzin has a thickened callus of skin on the
tip of the sternum that helps it to maintain a sitting
posture for 70 to 80% of the day (Strahl 1988). In our
study site, nonbreeding individuals of both species
of saltator remain motionless for major portions of
their time budget. Grayish Saltators and Orinocan
Saltator spend about 50 and 42% of daylight hours,
respectively, sitting and a further 30 and 35% en-
gaged in low-cost static activities such as preening
and singing (Garcfa 1994, Rodriguez 1994).
A considerable portion of the diet of saltators is
made up of fruits and other plant tissues. Data on the
energetics of frugivores is scant, but it appears that
frugivory in birds is also associated with low BMR
(McNab 1988). However, this is not well established
because three species of highly frugivorous Neotrop-
ical manakins (Pipridae) have BMRs that correspond
to their body size (Vleck and Vleck 1979). Neverthe-
less, several of the conditions that apply to folivory
might also apply to frugivory. Fruit has a high water
content and a considerable portion of indigestible
seeds; hence, metabolizable energy of whole fruits
per unit of fresh mass is quite low (Karasov 1990),
and processing by the digestive tract might limit in-
take in highly frugivorous species (Levey and Grajal
1991). Similarly, secondary metabolites of fruit pulp
can limit intake in frugivores (Izhaki and Safriel
1989, Cipollini and Stiles 1993). Perhaps the low bas-
al rates in saltators are associated with folivory in
combination with frugivory.
Neither species of saltator fully balanced heat loss-
es through an increase in metabolism as ambient
temperature decreased (their body temperatures
dropped in a seemingly controlled manner). The de-
crease in T b between 34 and 13øC T a that we estimat-
ed from the regression equations was 1.9øC in the
Grayish Saltator (from 39.5 to 37.6øC) and 4.1øC in
the Orinocan Saltator (from 39.1 to 35.0øC). This con-
trolled decrease in Tb, although moderate, should
contribute to an economy of energy expenditure and
also could be considered an adaptation to save en-
ergy. A moderate decrease in T b with falling Ta, con-
trolled hypothermia, is known for approximately 40
other species of birds, including mousebirds (Prin-
zinger et al. 1991). Failure to increase heat produc-
tion enough to balance heat loss also has the effect of
lowering the slope of the line to the left of the lower
critical temperature (Figs. lB and 2B), which coupled
with a combination of physical and chemical ther-
moregulation (McNab 1980b), should account for the
high extrapolated body temperatures at an estimated
rate of metabolism equal to zero for both species.
Tropical birds seem to have reduced BMRs for
their body size, particularly species that regularly
forage in the sun (Weathers 1979, 1997). Latitude, or
factors associated with it (e.g. lower mass of meta-
bolically active tissue; Rensch and Rensch 1956 in
Daan et al. 1990), might be a confounding factor in
the interpretation of our finding that saltators have
reduced metabolic rates. At this point, we cannot
discern the effects of diet and latitude on our results.
However, the fact that saltators spend 77 to 80% of
their time sitting, singing, and preening suggests
that, under such a relaxed time budget, it is unlikely
that they would be forced to forage or to spend con-
siderable portions of time exposed to unfavorable ra-
diative environments. The fact that BMR is reduced
in other arboreal folivores, including temperate spe-
cies, suggests that diet is important.
Among folivorous birds, it appears that only the
more arboreal species have reduced metabolic rates.
The ground-dwelling folivorous grouse and ptar-
migan (Tetraoninae) of temperate latitudes have
metabolic rates that are similar to or higher than
those expected from considerations of body mass
alone (see Weathers 1979, McNab 1988). Likewise,
flightless, forb-eating ratites and largely terrestrial,
grass-feeding anseriforms do not have reduced
BMRs (see McNab 1988). To some extent, this pattern
is similar to that found in mammals in which only
the more sedentary arboreal species have low basal
rates. In contrast, the consumption of grass and forbs
by terrestrial herbivorous mammals is associated
with high basal rates (McNab 1978, 1986). Further re-
search is needed to unravel the effects of latitude, fo-
livory, and arboreal habits on the metabolic rates of
birds.
Acknowledgments.--We are grateful to Sr. Toms
Blohm for permission to work at Hato Masaguaral
and for his unrestricted support of our activities.
Kako provided logistical support in many ways.
MAP was partially supported by ECONATURA
while at Hato Masaguaral. Travel expenses of RBS to
Venezuela were covered by a Jastro-Shields Graduate
Research Fellowship from the University of Califor-
nia. Wes Weathers kindly allowed the use of the ox-
ygen analyzer. Research on saltators at Hato Masa-
guaral was initiated by M. A. Garcia and A. Rodri-
guez. Suggestions by reviewers greatly improved the
manuscript. All birds were captured and handled
under permissions from PROFAUNA (Ministerio del
Ambiente y Recursos Naturales Renovables) issued
to M. A. Garcia and A. Rodriguez.
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Received 11 November 1997, Accepted 22 April 1998.
Associate Editor: M.E. Murphy