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First published online July 20, 2006
Journal of Experimental Biology 209, 2880-2887 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02326
Short-term energy regulation of whitebellied sunbirds (Nectarinia talatala): effects of food concentration on feeding frequency and duration
Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa
* Author for correspondence (e-mail: akoehler{at}zoology.up.ac.za)
Accepted 13 May 2006
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Summary |
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Key words: compensatory feeding, feeding duration, feeding frequency, sugar concentration, sunbird, Nectarinia talatala
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), and avian nectarivores adjust the volume that they consume
according to nectar concentration. The compensatory feeding hypothesis
predicts that food intake is varied in order to maintain a constant energy
intake, and this has been demonstrated in a variety of nectar-feeding birds
(for a review, see Martínez del Rio
et al., 2001). Whitebellied sunbirds (Nectarinia
talatala), for instance, show perfect compensatory feeding over a tenfold
range of nectar concentration. Their average daily intake of 0.31 g sugar
g-1 body mass is maintained on diets from 0.25-2.5 mol
l-1 sucrose by adjusting the volumetric intake from 30.3 to 3.3 ml
per day, a ninefold difference (Nicolson
and Fleming, 2003b).
These dramatic differences in volumetric intake require alterations in meal
frequency and/or meal size as food concentration varies. Several hummingbird
species increase the number of feeding bouts as sugar concentration decreases,
but maintain a nearly constant feeding bout length
(Wolf and Hainsworth, 1977).
Other hummingbirds, and honeyeaters, have also been shown to increase their
feeding frequency when sugar concentration is decreased
(Gass, 1978;
Collins and Clow, 1978;
López-Calleja et al.,
1997). Energy gained from the nectar is not only required for the
time between feeding bouts but must also be accumulated for overnight
requirements. In a more prolonged experiment using hummingbirds with depleted
energy reserves due to food deprivation, Eugenes fulgens used
increased meal frequency to increase their energy storage rates, whereas
Lampornis clemenciae used increased meal size, and both species
reduced energy expenditure between meals
(Hainsworth et al., 1981). No
comparable information is available for sunbirds.
In this study, the effect of various sugar concentrations on short-term
feeding patterns of whitebellied sunbirds was determined. Sucrose solutions
were used, since sucrose and hexoses are equally well assimilated by sunbirds
(Lotz and Nicolson, 1996).
Sucrose concentrations of 10, 20 and 30% w/w were fed to each bird and the
effects on short-term feeding patterns were investigated by measuring the time
and duration of each feeding event, and by recording body mass constantly
throughout the day. We hypothesized that feeding frequency varies with the
concentration of the food source in order to maintain constant energy intake
on the different diets. Feeding duration, on the other hand, was not expected
to increase with decreasing sucrose concentration because of volumetric
constraints or increased metabolism resulting from the weight of the meal. We
used feeding duration as an estimate of meal size, on the assumption that
intake rates should be constant for birds feeding on a single sugar
concentration in a high volume artificial feeder. In previous studies
investigating feeding patterns of sunbirds (e.g.
Nicolson and Fleming, 2003b;
Fleming et al., 2004), the
volumetric intake was recorded on a daily or hourly basis. With continuous
recording of feeding events and their frequency, this study provides
information on a much shorter time scale.
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Materials and methods |
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).
The diet and supplementary water were provided ad libitum in
inverted, stoppered syringes attached to the cage sides.
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), the experimental diets were also supplemented
with Ensure, with the amount adjusted to allow for compensatory feeding. The
carbohydrate content of the added Ensure, even if completely digested, would
increase the sugar concentration by only 0.58%. For each bird the experimental procedure lasted 4 days. The sunbird was moved in the morning of the first day to the experimental cage (50x40x45 cm) and allowed an acclimation period with the maintenance diet for the remainder of the first day and the first night. Ambient temperature, humidity and light cycle were the same as before, but the dawn and dusk periods were omitted to synchronize start and end times of feeding. Measurements commenced at 07:00 h on the following day (day 2) and continued for 72 h, with the diets being changed every morning before lights on.
The experimental cage was constructed from Perspex, with ventilation holes, and contained a feeding perch and a resting perch (Fig. 1). The main perch, where the bird rested for most of the day, was suspended from an electronic balance (Mettler Toledo PB-602S, 0.01 g; Microsep Ltd, Johannesburg, South Africa). Throughout the duration of the experiment the body mass was recorded every 5 s if the bird was sitting on the main perch, using a computer interfaced with the balance. This main perch was connected to the ceiling of the cage by two slender metal rods to minimize swinging of the perch when the bird landed, which could disturb the measurements.
During a meal, the bird clung to the vertical feeding perch (Fig. 1). An infrared photo-detection system, consisting of an infrared diode light source and an array of four infrared photo-detectors interfaced to the same computer, allowed for the automated recording of the time spent feeding as well as the number of feeding events. The light source and detectors were mounted on either side of the feeder. Each time the bird inserted its bill into the sucrose solution the infrared photo-detection system recorded the feeding event, which lasted until the bird removed its bill. Prolonged resting on the feeding perch was discouraged by its smooth surface and pins inserted into the perch to reduce the space available. Since the cage was constructed from Perspex the bird was not able to cling to the sides. Furthermore, flexible plastic bristles discouraged the bird from resting on the bottom of the cage. Observation of the bird with minimal disturbance was permitted by one-way mirrors on two sides of the cage. Each sunbird was observed for 1 h (09:00 h to 10:00 h) while feeding on each sucrose concentration, in order to confirm photo-detection records as well as natural behaviour of the birds.
The measurements were repeated either partly or completely for four of the eight birds for two reasons: firstly, photo-detection malfunctions and therefore incorrect records of feeding events and secondly, insufficient use of the main perch and therefore too few mass measurements for analysis. Nevertheless, we were unable to successfully record body mass throughout the day for one of the birds since it avoided the main perch and we therefore excluded it from the analysis of mass data. Birds were released at the site of capture following termination of the study.
Definitions and analysis of feeding data
For each bird and each sucrose concentration we obtained start and end
times of all feeding events, duration of feeding events in seconds (s) and
time intervals between feeding events (s).
Separate feeding events could not be defined by return to the main perch after feeding, as occurs in hummingbirds that hover to feed. We defined a feeding event as beginning when the bill was inserted into the sucrose solution and ending when the bill was removed. The feeding event duration (hereafter referred to as FED) is defined as the time between inserting the bill into the sucrose solution and removing it. FED values of less than 0.05 s were excluded, since observations revealed that movements of the bird, particularly wing movement during flight near the feeder, caused such events. Separate feeding events were merged into a single feeding event if the interval between two consecutive feeding events was less than 0.25 s, since observation revealed that turns of the bill or its incomplete removal from the feeder were recorded as two feeding events. For three birds, larger merging intervals of 0.35, 0.50 and 0.75 s were used, owing to slight differences in the sensitivity of the photo-detectors.
The light period of the day was divided into 1 h intervals to allow for comparison with previous studies in which diet intake was recorded hourly. For each 1 h interval, mean FED and number of feeding events were calculated. Feeding event frequency (FEF) was taken as the number of feeding events per hour. Furthermore, total feeding duration during each hour was determined by summing the FED of every feeding event during the 1 h interval.
Analysis of mass data
The recording of body mass resulted in static mass values as well as
dynamic values, the latter caused by swinging of the main perch during
movements of the bird. Dynamic balance readings were filtered from static mass
data. Because of few mass data for several birds, dynamic values were included
in the analysis when the absolute difference between the focal dynamic record
and the first static record prior to the focal dynamic record was less than
0.03 g.
The mass recordings were analyzed for each bird on each diet with the same 1 h intervals as for the feeding events. For each interval, the mean mass was determined. Body mass increase of each bird on each of the different diets was expressed as the percentage change from the mean body mass during the first 1 h interval, to eliminate individual differences.
Statistical procedures
Data are expressed as mean ± s.e.m. Mean FED, FEF and total feeding
duration per 1 h interval as well as temporal changes in body mass were
analyzed by repeated-measures ANOVA. Data were arranged according to hour of
day and sucrose concentration, yielding 30 dependent variables. Sucrose
concentration and hour of day were used as within-effects. Post-hoc
comparisons were conducted with Tukey's Honest Significant Difference test for
equal sample sizes. Relationships between FED, FEF and body mass were
determined using Spearman rank correlations. Repeatability ± s.e.m. was
calculated following the method of Becker
(Becker, 1984). Mean daily FED
and FEF for each individual were subjected to Grubb's test for outliers. For
all tests the level of significance was P
0.05.
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Continuous measurements of feeding events and body mass resulted in detailed information about short-term feeding patterns and body mass over the course of the day. Fig. 2 shows feeding duration and body mass of one bird (individual 7) feeding on the 10% w/w sucrose diet. From this figure, it can be seen that feeding events lead to an increase in body mass. Between feeding events, birds lose mass as a result of evaporative water loss and excretion of cloacal fluid. Large amounts of data necessitated the use of mean values of FED, FEF and body mass over hourly intervals for statistical analysis and graphical representation.
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Total feeding duration, i.e. the total time that birds spent feeding per hour, differed significantly between diets (F2,14=46.60, P<0.001; Fig. 5). Birds had a higher total feeding duration on the dilute diet than on the other two diets, due to the demonstrated increase in FEF on the 10% diet (P<0.001). Total feeding durations on the 20% and 30% sucrose concentrations did not differ (P=0.89). The total time that the birds spent feeding was very short, approximately 144 s h-1 on the dilute diet and 96 s h-1 on the other diets.
Body mass gains on the different diets
The body mass increase during the light period for seven of the birds is
presented in Fig. 6. There was
a trend for body mass increase to be positively correlated with diet
concentration, but this was not significant (F2,12=1.47,
P=0.27). Mass gains were similar on all three diets. Birds showed a
linear increase in their body mass over the day on all sucrose concentrations
(linear regressions: 10%: R2=0.96; 20%:
R2=0.95; 30%: R2=0.85). All birds
maintained their body mass during the four experimental days
(F2,12=0.32, P=0.73).
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Individual differences in feeding patterns
Irrespective of diet concentration and time of day, large
between-individual differences in feeding patterns were observed in terms of
FED and FEF. Fig. 7
demonstrates these differences for the 20% diet, which is equivalent to the
bird's maintenance diet. Individual birds employed different feeding
strategies. Whereas most birds had long FED combined with a low FEF, others
showed short FED and fed more often. One female bird in particular showed a
much higher FEF and lower FED than all other birds
(Fig. 7A,B, individual 3). We
calculated the repeatability of individual feeding behaviour on the 20% diet
over four half-hour intervals between 9:00-11:00, where feeding was not
influenced by morning deficits or energy savings in the evening (see below).
Both FED and FEF were highly repeatable (repeatability ± s.e.m. for
FED: 0.75±0.13; FEF: 0.91±0.05). Individual differences in FEF
and FED were not related to body mass (Spearman R: FED:
R7=0.54, P=0.22; FEF:
R6=0.26, P=0.62) but this might be due to our
small sample size. One bird had to be excluded from both of the above analyses
because of insufficient mass data. Individual 3 was shown to be a statistical
outlier (Grubb's T=2.22, P<0.05) and was excluded from
the correlation between FEF and body mass.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Volumetric intake during a meal could be limited by crop size. Diamond et
al. (Diamond et al., 1986)
proposed that cropemptying time limits feeding frequency in hummingbirds, thus
explaining the large amount of time spent perching. However, hummingbirds
usually fill their crops to only 10-30% of capacity
(Carpenter et al., 1991), and
neither honeyeaters nor sunbirds possess crops
(Collins et al., 1980;
Mbatha et al., 2002).
Hummingbirds are also capable of processing food much faster than indicated by
their rates of ad libitum intake
(Tiebout, 1989).
The processing of nectar meals requires hydrolysis of the sucrose component
to glucose and fructose, then absorption of the latter. Birds must also deal
with large volumes of preformed water. Gut transit time decreases with
increasing volume of a sucrose meal
(Tiebout, 1989) and with
increasing concentration
(López-Calleja et al.,
1997; Markman et al.,
2006). The decrease in transit time on dilute diets accounts for
the increased meal frequency that we measured. It has also been suggested that
delivery of nectar meals to the intestine should be faster for sucrose than
hexose nectars of equivalent energy content, because of the lower osmotic
concentration (Beuchat et al.,
1990). Sucrose hydrolysis rates may be limiting in birds feeding
on low nectar concentrations (McWhorter
and Martínez del Rio, 2000), and the passive component of
hexose absorption may also be affected, because it depends on contact time
with the absorptive surfaces (McWhorter et
al., 2005). However, if water is absorbed rapidly down the length
of the intestine, dilute meals will not remain dilute. This especially applies
to hummingbirds which, unlike sunbirds, do not modulate their intestinal water
absorption in response to food dilution
(McWhorter and Martínez del Rio,
1999; McWhorter et al.,
2003). In the latter study, Palestine sunbirds (N. osea)
decreased the fraction of absorbed water by 60% on a diet of 0.29 mol
l-1 sucrose: under these conditions, the load on the kidneys is
correspondingly reduced but nutrients may have to be extracted from low
luminal concentrations. Unfortunately we have no information on the gradients
of sugar concentration along the intestine in nectar-feeding birds.
Energetic considerations may explain why FED did not increase on the dilute
diet. For hummingbirds with access to unlimited food supplies, a model of
optimal meal size (DeBenedictis et al.,
1978) suggests constraints due to the weight of the meal (although
the water in dilute meals is eliminated quickly). Large meal sizes would lead
to increased body mass and increased energy expenditure between meals.
European starlings (Sturnus vulgaris), when exposed to different
amounts of work required to obtain food, save energy during a hard treatment
by reducing body mass (Bautista et al.,
1998). This is expected to reduce flight costs, although the
implications of body mass for flight performance of hummingbirds remain
mechanistically unclear (Altshuler and
Dudley, 2002). Ruby-throated hummingbirds (Archilochus
colubris) on restricted diets showed effects of body mass on hovering
ability in low-density air, but not on maximum flight speed in a wind tunnel
(Chai et al., 1999). When the
metabolic costs of flight are measured directly, the short flights of sunbirds
have been shown to be relatively inexpensive compared to those of starlings
(Hambly et al., 2004).
Concentration effects
The increase in total feeding duration of sunbirds on the dilute diet of
10% sucrose can be attributed to compensatory feeding
(Martínez del Rio et al.,
2001). Adjustment of food intake according to diet concentration
is exhibited by many nectar-feeding birds, including honeyeaters
(Collins and Clow, 1978;
Collins et al., 1980), several
hummingbird species (López-Calleja
et al., 1997; McWhorter and
Martínez del Rio, 1999;
Fernández et al.,
2002), and three sunbird species
(Lotz and Nicolson, 1999;
McWhorter et al., 2003;
Nicolson and Fleming,
2003b).
Unexpectedly, there was no difference in total feeding duration between the
20% and 30% sucrose diets. The inverse exponential relationship between
volumetric intake of whitebellied sunbirds and diet concentration provides a
proximate explanation. For sucrose concentrations between 0.25 and 2.5 mol
l-1, this relationship is described by the function:
 |
where V = volumetric intake (ml), C = sucrose
concentration (mol l-1) and a and b are
empirically derived constants (Nicolson
and Fleming, 2003b). Applied to the sucrose concentrations used in
the present study (10%=0.30 mol l-1, 20%=0.63 mol l-1,
30%=0.99 mol l-1), this function shows that, over a 12 h light
period, birds have to consume 25.70 ml of the most dilute diet of 10%, 12.53
ml of the 20% diet and 8.10 ml of the 30% diet. Hence, the volume consumed
daily differs far more between the 10 and 20% diets than between 20 and 30%,
explaining the increase in total feeding duration on the most dilute diet. The
small expected difference between the 20% and 30% diets will be obscured by
large between-individual differences. With larger sample sizes and more
concentrated diets, it might be possible to demonstrate decreases in total
feeding duration with increasing sugar concentration. Support for our findings
also comes from a study on lesser double-collared sunbirds (N.
chalybea) (Lotz and Nicolson,
1996), which preferred 20% over 10% sucrose solutions, but were
indifferent to 20% and 30% sucrose. Feeding frequencies of hummingbirds have
been measured on sucrose concentrations similar to those in the present study:
in Archilochus colubris and Lampornis clemenciae, feeding
frequencies were similar on 0.5 and 1.0 mol l-1 sucrose solutions,
but much higher on 0.25 mol l-1 sucrose
(Wolf and Hainsworth, 1977),
again showing effects only on the most dilute diets. Studies of feeding
behaviour in small honeyeaters also show significant changes in feeding
frequency only on dilute solutions such as 0.2 mol l-1 sucrose
(Collins and Clow, 1978;
Collins et al., 1980).
Body mass gains on the different diets
The increase in body mass over the course of the day is necessary to
provide energy for the night, when birds do not feed. Similar increase in body
mass during the day on all three diets confirms the occurrence of compensatory
feeding by the sunbirds. Lesser double-collared sunbirds also achieve the same
daily mass gain irrespective of diet concentration
(Lotz and Nicolson, 1996). In
a variety of nectar-feeding birds the pattern of energy accumulation is
commonly linear through the day, sometimes slowing in the afternoon
(Wolf and Hainsworth, 1977;
Collins and Morellini, 1979;
Nicolson et al., 2005).
In previous studies, whitebellied sunbirds fed sucrose-only diets at
20°C lost approximately 3% of body mass per day, since sucrose solutions
can not meet all their dietary requirements
(Nicolson and Fleming, 2003b).
Experimental diets in the present study were supplemented with Ensure and
birds maintained their body mass throughout the experimental procedure.
Daily rhythms in feeding patterns
Whitebellied sunbirds feed steadily during the morning and early afternoon,
followed by reduced intake during mid-afternoon and then an increase at the
end of the day to provide energy stores for the night
(Fleming et al., 2004). The
high rate of feeding in the early morning compensates for overnight mass loss
and rehydrates the birds after the overnight fast. A rather different pattern
is evident when feeding is examined on a short-term basis. FED and FEF were
found to vary greatly during the course of the day on all diet concentrations.
In the early morning and in the evening, birds fed less often and therefore
had longer FED. During the rest of the day, birds showed a higher FEF coupled
with a shorter FED. This observed daily pattern in feeding behaviour is
unlikely to be related to ambient temperature normally experienced by wild
birds since birds used in our study were kept under constant temperature for
11 months prior to the experiment. Despite the inverse relationship between
FEF and FED, total feeding duration also showed a daily rhythm, being higher
in the late morning than during the afternoon.
However, this reduction in feeding rate in mid-afternoon was much less
obvious than in previous studies where food intake of whitebellied sunbirds
was measured on an hourly basis (Fleming
et al., 2004; Nicolson et al.,
2005). The different pattern may be due to disturbance of the
birds during hourly weighing of feeders, or may reflect the fact that intake
rates and total feeding duration are not directly comparable. Collins and Clow
(Collins and Clow, 1978) also
recorded varying ingestion rates in honeyeaters, with nectar extraction being
least efficient in the early morning. The relationship between meal size and
meal duration in nectar-feeding birds needs further investigation.
Individual differences in feeding patterns
We have examined sunbird feeding patterns in much more detail than previous
studies. Measurements over a short time scale have highlighted unexpectedly
large between-individual variation in feeding patterns. Individual birds
differed greatly in terms of their FED and FEF, irrespective of diet
concentration and time of day. Recently, sex-specific differences in transit
time were demonstrated in Palestine sunbirds, which might affect their
foraging behaviour (Markman et al.,
2006). However, only two females were used in our study and we
were unable to test whether the sexes differ in their feeding patterns.
Observations on another group of whitebellied sunbirds feeding in an outdoor
aviary (A. Köhler, unpublished data) showed similar high variation
between individuals in both feeding frequency and feeding duration.
Although they have received limited attention, inter-individual differences
are also apparent in the responses of hummingbirds and starlings to imposed
energetic constraints (Tooze and Gass,
1985; Bautista et al.,
1998), and in the sugar preferences of sugarbirds and sunbirds
(Jackson et al., 1998). In
whitebellied sunbirds fed diets ranging from 0.25-2.5 mol l-1
sucrose, greater variation in sucrose intake was found between individuals on
a particular diet than between diets
(Nicolson and Fleming, 2003b).
The variation in physiology and behaviour seen under constant laboratory
conditions is likely to be accentuated as circumstances vary in the natural
environment. Perhaps individual differences in feeding behaviour of sunbirds
may translate into varying proficiencies in handling flowers of different
morphology and nectar characteristics.
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Acknowledgments |
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