Effects of sugar concentration on hummingbird feeding and energy use

Camp Riochem. Physiol. Vol. 118A, No. 4, pp. 1291-1299, 1997 Copyright 0 1997 Elsevier Science Inc. All rights reserved.

ELSEVIER

ISSN 0300-9629/97/$17.00 PII SOlOO-9629(97)00243-O

Effects of Sugar Concentration on Hummingbird Feeding and Energy Use -

M. Victoria Lhpez-Calkja,’ Francisco Bozinouic,’ and Carlos Martinez del Rio3 'DEPARTAMENTO DE CIENCIAS ECOL&ICAS, FACULTAD DE CIENCIAS, UNIVERSIDAD DE CHILE, CASILLA 653, SANTIAGO,

CHILE; ‘DEPARTAMENTO DE ECOLOG~A, FACULTAD DE CIENCIAS BIOL~GICAS, P. UNIVERSIDAD CAT~LICA IKE CHILE, CASILLA 144-D, SANTIAGO, CHILE; AND ‘DEPARTMENT OF ZOOLOGY AND PHYSIOLOGY, UNIVERSITY OF WYOMING,

LARAMIE, WY 82071, U.S.A.

ABSTRACT. We investigated the effect of sucrose concentration on the patterns of feeding, gut function, and

energy management in the nectar-eating Chilean hummingbird Sephanoides sephanoides. We interpreted these

results using a simple model of digestive function. The predictions of this model are: (a) Hummingbirds should

exhibit 100% assimilation efficiency of sugars at all sugar concentrations; (b) Daily rates of energy intake should

be positively correlated with sugar concentration; and (c) Increased sugar concentration should lead to linearly

increasing meal retention times, and, therefore, to linearly increasing time intervals between meals. In agreement

with the model, hummingbirds exhibited almost complete assimilation of sugars and increased meal retention

times and intermeal intervals with increased sugar concentration. Hummingbirds did not, however, show any significant differences in daily energy intake when fed different sugar concentrations. Birds differed in their

temporal pattern of feeding when fed solutions with sucrose solutions of contrasting concentrations. At low food sucrose concentrations (0.25 M), b’ d ir s s h owed a burst of feeding before dark. In contrast, birds feeding on higher

sucrose concentrations (0.5 M and 0.75 M) h s owed steadily declining feeding activity throughout the day. In

addition to measuring the behavior and gut function of hummingbirds, we also measured their daily patterns of energy use using respirometry. Hummingbirds showed considerable flexibility in their patterns of energy use.

The amount of energy used at night was positively correlated with the surplus of energy (intake minus diurnal expenditures) at dusk. Although birds exhibited only small variation in total daily energy budgets as a function

of sugar concentration, birds feeding at the lowest sucrose concentration (0.25 M) seemed to rely on nocturnal

torpor with more frequency than those fed on higher concentrations. We conclude that energy maximization

is probably an inappropriate assumption for birds that are not growing, storing fat, or reproducing. We present

a modification of the original model that allows assuming that birds do not maximize energy intake, but rather maintain constant rates of energy intake. We describe experiments and criteria that allow discriminating among

the two models. COMP BIOCHEM PHYSIOL 118A;4:1291-1299, 1997. 0 1997 Elsevier Science Inc.

KEY WORDS. Energetics, digestion, feeding behavior, hummingbirds, metabolic rates, sugar concentration,

respirometry

INTRODUCTION

Hummingbirds show rapid behavioral and physiological responses to manipulation of environmental energy availability in both the laboratory and the field (11,13,45). Because their small size makes them sensitive to energy stress (34,47), and because they often face marked fluctuations in energy availability and energy expenditures (35), these rapid responses are key for hummingbird day to day survival

(5). The energy content of food can have a strong influence

on the amount of energy that can be acquired by a foraging

Address reprint requests to: Carlos Martinez Del Rio, Department of Zoology and Physiology, University of Wyoming, Laramie, WY 82071-3166, U.S.A.; Tel. (307) 766-2928; Fax (307) 766.5625; E-mail: cdelrioQuwyo.edu.

Received 14 January 1997; revised 20 May 1997; accepted 26 May 1996.

hummingbird (49), and on how much it costs to acquire it (9). Consequently, nectar sugar concentration probably has a strong effect on hummingbird foraging and energy use. Nectar sugar concentration varies both among and within plants (8,41). Interplant variation in nectar sugar concentration can influence a hummingbird’s decisions on what plants to visit (21). Temporal variation in the average sugar concentration of nectar present in a given habitat can also have an important-albeit relatively unstudied-effect on hummingbird foraging and daily energy management.

Sugar concentration influences foraging and daily energy management through both pre- and postingestional processes. Nectar viscosity increases with sugar concentration (2), and is one of the determinants of the time required by a hummingbird to extract a given volume of nectar from a flower (23,28). Research on the role of nectar sugar compo-

1292 M. V. tipez-Calleja et al.

0 2 4 6 8 10 12 14 16 18 20

Meal Retention Time (mins.)

FIG. 1. A simple mathematical model of gut function in hummingbirds (modified from 33). The figure shows the relationship between net energy obtained from a meal and the time used in processing it in the gastrointestinal tract for food containing 0.25 M, 0.5 M, and 0.75 M sucrose. Net energy intake from meal equals the difference between the energy contained in a meal minus the energy used to acquire the meal and the energy spent while assimilating it. We assumed that the intestine of a 5.7 g S. sephanoides can assimilate (i.e.

hydrolyze and transport) 26 pmoles of sucrose per minute, that the energy needed to acquire a meal equals 10.5 J, and that the energy spent while digesting the meal equals 20.4 Jlmin. We also assumed that meal sized equaled 0.21 ml, which is the optimal meal volume predicted by DeBenedictis etal. (9) for our experimental conditions. Net energy intake increases linearly with a slope equal to the rate of assimilation ([26,umole/min] X IS.64 J pmole] = 148.4 Jlmin) until all the sugar contained in a meal is assimilated. After this point, the net energy intake rate declines with a slope equal to the rate of energy use. Meal retention time that maximiie net energy intake rate (Le., net intake/meal retention time) are those in which a line passing through the origin is tan gent to the net intake curve (33). The model predicts that hummingbirds maximizing energy intake should assimilate the sugar contained in food completely. Optimal retention times for food containing 0.25 M, 0.5 M, and 0.75 M are shown by the arrows labeled A, B, and C respectively.

sition on hummingbird foraging has primarily emphasized

its effect on flower handling times (44 and references

therein). Here we approach the problem at a larger temporal

scale. We investigate the effect of experimentally varying

sugar concentration on feeding patterns and daily energy

use in hummingbirds.

This work examines the effect of sugar concentration on

the feeding behavior and daily energy management of cap-

tive Green-backed Firecrowns, Sephanoides sephanoides

[sometimes referred to as S. gderitus, (43)]. We tested the

assumptions and predictions of a simple model of humming-

bird feeding based on gut processing rates (33). This model

assumes that the time required to completely digest the vol-

ume of nectar contained in the gut is a linear function of

the sugar concentration in food. It makes several predic-

tions about how energy-maximizing hummingbirds should

respond to sugar concentration in food (Fig. 1). The predic-

tions that we examine here are the following: (a) Hum-

mingbirds should exhibit almost complete assimilation effi-

ciency of sugars independently of sugar concentration;

(b) Increasing sugar concentration should Iead to increasing

rates of energy intake; and (c) Meal retention times, and

hence intermeal intervals, should increase linearly with

sugar concentration.

Materials and Methods

Adult male Sephanoides sephnoides (mean mass rfr SD =

5.76 -+ 0.46 grams, size range = 9.7 to 11.4 cm, hJ = 45)

were captured with mist nets in Central Chile. They were

maintained in individual 60 X 60 X 60 cm cages at 25°C

and 12L : 12D photoperiod. For 3 days following capture and

between experiments, birds were fed a sucrose-solution

(20% weight/volume) supplemented with vitamins and

proteins (Vimiprotin-L’, 0.3g/50 ml of solution). Between

experiments fruitflies and water were also provided ud li-

bitum.

We used three experimental sucrose solutions to assess

the role of sugar concentration on feeding patterns and gut

function: 0.25, 0.50, and 0.75 M (with caloric contents

equal to 1.43, 2.7 1, and 4.3 kJ/ml, respectively). Sugar con-

centration were selected following previously reported nec-

tar flower concentration in the field (43). Most experiments

involved comparisons among groups of three to five individ-

uals. A total of 45 individuals participated in all our experi-

ments. In our first series of experiments we investigated the

effect of sugar concentration on (a) the daily temporal pat-

tern of food intake, (b) total daily food consumption,

(c) intermeal intervals, and (d) preferences among sugar

concentrations. Volumetric food consumption was deter-

mined hourly using glass feeding tubes. These tubes (i.d. 7.8

mm) had a 33 cm vertical section and a lower 5 cm section

that was bent at a 45” angle; the tip of the lower section

was tapered into a hole (i.d. 2.5 mm). Total daily intake was

determined from hourly measurements of intake. Intermeal

intervals were monitored using a videorecorder during 2 hr

(from lO:OO-12:OO).

Preferences among sugars were determined at the mainte- nance cages by providing each of 8 birds with 3 feeders (tube glass) containing 0.25, 0.5, and 0.75 M sugar solutions for 4 hr (between 10:00 and 14:00), the feeders were at the same distance (cu. 45 cm) from a single perch and 7 cm apart from each other. Sugar digestibility was estimated from apparent assimilated mass coefficient measurements (AMC*; 24). Food intake and excreta produced in 24 hr

were measured to estimate

AMC* = 100 x (Q, - Q,)/Q,,

where Q, and Qe are dry food intake and excreta production

rates in grams/day, respectively. Birds were fed in plastic-

lined cages and volumetric intake and excreta production

were monitored hourly for 12 hr. Excreta was collected in

microcapillary tubes and its volume measured. Excreta pro-

duced overnight was collected the following morning (3 1).

Hummingbird Feeding and Energetics

All excreta samples were dried at 60°C to constant weight.

Because birds mix urinary and fecal products in the cloaca,

AMC* underestimates true assimilation efficiency. As an

indirect measurement of meal retention time, we used a

time processing index (PTI) proposed by Martinez de1 Rio

(3 1). PTI equals the reciprocal of excretion rate. If the gas-

trointestinal volume remains constant during the time of

measurement, the reciprocal of excretion time estimates the

time required to process a gut volume of digesta (39). All

the experiments (except preferences) were conducted on

hummingbirds housed on mesh cages with the following di-

mensions: front, and back measured 15 X 15 cm, bottom,

top and the sides measured 30 X 30 cm.

To assess the effect of sugar concentration on energy ex-

penditures we housed birds in metabolic chambers of similar

dimensions than experimental cages. These chambers con-

tained a perch and a feeder that provided ad libitum food.

Birds could fly freely inside of these cages and could fly from

the perch to the feeder. Oxygen consumption in these

chambers was monitored hourly for 24 hr using a computer-

ized automatic manometric respirometry system based on

the design of Morrison (36) and described in detail in (30).

Briefly, CO: and H20 were chemically absorbed with

Ba(OH): and CaCl? respectively; ambient temperature was

controlled with a water bath maintained at 25°C (-+0.5”C),

a temperature within the thermoneutrality range of S. sephanoides (30). Light was provided with a natural light 60-W

lamp. Birds were acclimated to the chambers for 48 hr be-

fore measurements were conducted. To transform oxygen

consumption to energy units, we used 20.1 J/ml Oz (37).

RESULTS Daily Temporal Pattern of Intake

We noted that hummingbirds fed more actively in the

morning and steadily declined food consumption through-

out the day. To test if this decline in food consumption was

statistically significant, we calculated the correlation coef-

ficients (7) for food consumption per hour vs time for each

bird. We used two tailed t-tests to examine if the average

r was significantly different from 0. Food intake declined

significantly throughout the day for hummingbirds fed 0.5

and 0.75 M sugar solutions (average r + SD = -0.6 t 0.2

and -0.5 ?I 0.2, P < 0.02, respectively, N = 5, Fig. 2).

However, bards fed on the most dilute sugar solution (0.25

M) did not show a significant decline in food consumption

through time (average r + SD = -0.35 t 0.5, P > 0.2) and

showed a distinctive burst of intake in the last two hours of

the light period (Fig. 2).

Total Daily Food Consumption

Total daily volumetric food consumption decreased signifi-

cantly with sugar concentration (rr = -0.83, N = 15,

P < 0.00 I). The relationship between daily food intake and

concentration was adequately described by a power func-

3.0’

2.5‘

2.0’

h

3 ; 1.5

l

1.0

0.5

1293

o.o+ 09 10 11 12 13 14 15 16 17 18 19 20

Time Interval FIG. 2. Relationship between volumetric intake and time for hummingbirds feeding on food with different food concen trations. Values are means for five individuals. Regression lines were fitted to these means for descriptive purposes only. Average (*SE) slopes calculated from regressions fitted through data for individual hummingbirds for food containing 0.75 M, 0.5 M, and 0.25 M were -0.029 (*0.009), -0.080 (+0.023), and -0.010 (kO.006) mllhr, respectively. The slopes differed significantly among sugar concentrations (F,,,, = 3.9, P < 0.05).

tion, with a slope that did not differ significantly from - 1

(slope + SE = -0.95 % 0.1, r’ = 0.85, Fig. 3). This rela-

tionship indicates that daily energy intake was not corre-

lated with sugar concentration (r\ = 0.08, P > 0.5, Fig. 3),

and is contrary to the energy-maximization assumption of

Martinez de1 Rio and Karasov’s (33) model. When calcu-

lated for every hour throughout the day, energy intake rates

were not positively correlated with sugar concentration ei-

ther (r, < 0.31, P > 0.5). In captive S. sephunoides, the rate

of energy intake did not increase with sugar concentration.

Because sugar assimilation efficiency was close to 100% (see

below) and it was independent from sugar concentration in

food, net energy intake closely approximated metabolizahle

energy intake.

1294 M. V. L6pez-Calleja et al.

:

35.1 f 6.0 :

8

: i f

50 Q

zia as4 30 I$

c

35

1 Y = 6.54 (X)a0.g5

5J I I I

0.25 0.50 0.15

Sugar Concentration (M)

FIG. 3. Daily volume and energy intake in hummingbiis as a function of sugar concentration in food. The power function through the volume versus concentration data (y = ~.S(X)-“~~) was fitted using a nonlinear least squares routine (JMPB for Macintosh). Note that the exponent of this function is not significantly different from - 1, and consequently daily energy intake is independent of sugar concentration. Daily energy intake averaged 35.7 kJ/day (SD = 6.0) and is represented by the horizontal line in the upper panel.

Intermeal Intervals and Meal Frequencies

The interval between meals of individuals monitored between 10:00 to 12:OO increased significantly with sugar concentration (rr = 0.88, P < 0.01, N = 11). Although the relationship between sugar concentration depicted in Fig. 4 appears to be accelerating and, hence, nonlinear, a test for departure from linearity (50, pp. 278) failed to reject the null hypothesis of linearity (F1,* = 1.7, P > 0.1). Meal frequency decreased significantly with increased sugar concentration (rs = -0.77, P < 0.05, N = 11, Fig. 4).

Concentration Preferences

Sephanoides sephanoides significantly, and very strongly, pre- ferred the most concentrated solution (0.75 M) over the two other more dilute ones (Randomized Block ANOVA with individual birds as blocks, Fz,lz = 190.6, P < 0.001). They consumed roughly ten and a hundred times more of the 0.75 M than of the 0.5 and 0.25 M sugar solutions, respectively (mean intake ? SD of 0.75, 0.5, and 0.25 M solutions was 10.4 + 1.6, 1.5 + 1.2, and 0.1 2 0.3 ml/ 4 hr, respectively).

Digestive Correlates of Sugar Concentration

Assimilated mass coefficients were exceedingly high and did not differ significantly among concentrations (AMC* 2

0.0 1 0.00

r I

0.25 0.50 0.75


FIG. 4. Meal frequency in hummingbiis (upper panel) decreased significantly with sugar concentration in food ( y = 48.5 -43.8x, r2 = 0.81), whereas the interval between meals increased significantly with sugar concentration ( y = 0.05 + 0.36x, (r’ = 0.56).

SD = 98.7 5 0.7, N = 12, Fz,s = 2.2 P > 0.15, one-way ANOVA). The time used to process each volume of in- gested food as estimated by PTI increased linearly with sugar concentration in food (Fig. 5).

Sugar Concentration and Daily Energy Use Patterns

Figure 6 illustrates the time course of energy expenditures for hummingbirds fed on the three experimental sugar con-

045 0.;0 0.h


FIG. 5. The time required to process nectar increased linearly with sugar concentration in food. The regression equa- tion is y = 0.04 + 0.34x (3 = 0.89, P < 0.001).

Hummingbird Feeding and Energetics 1295

0.6 4 0.25 M

1 I , I I I I , I , , , ,

oom 04:OO 0830 12:aO 1690 20:0+3 24m

Time (EST)

FIG. 6. Time course of energy expenditures in Sephanoides

sephanoides fed on nectar containing 0.75 M, 0.5 M, and 0.25 M sucrose. Bars in top panel indicate dark and light periods of measurement. BMR is the basal metabolism docu- mented for this species (BMR f SD = 0.01 kJ/hr g), (30). Note that 3 individuals fed 0.25 M sucrose solutions entered torpor and lowered their metabolic rate below BMR during the dark period.

centrations. Although birds showed no significant differ-

ences in 24 hr energy expenditures among sugar concentra-

tions (mean + SD = 5.02 -+ 1.2 kJ/day g, N = 12, F!,‘) =

1.9, P > 0.2, one-way ANOVA), they showed differences

in the probability of entering torpor. Three out of four birds

fed on 0.25 M sugar solutions entered torpor at night,

whereas all of the birds fed on the 0.5 M or 0.75 M solutions

maintained metabolic rates at or above basal levels (Fig. 6).

We defined torpor operationally as a lowering in metabolic

rate helow basal levels (30).

In S. sephanoidq the amount of energy spent at night

was linearly correlated with the net amount of energy accu-

mulated during the day (Fig. 7). However, the slope of this

relationship was significantly lower than 1 (slope t SE =

0.35 -C 0.06, t = 11.55, P < 0.05), suggesting that birds with

higher accumulation of energy at the end of the day had

0 0.75 M 0 0.50 M

0 0.25 M

I I I

0 IO 20 30

Energy intake - Daytime Energy Expenditures

@J/day)

FIG. 7. Relationship between diurnal energy surplus (intake- expenditures during the day) anl energy spent at night. Hummingbirds fed on 0.75 M, 0.5 M, and 0.25 M sucrose solutions are shown as closed, shaded, and open circles, respectively. A common regression line was fitted through all individual data points (y = 2.15 + 0.35x, rz = 0.80, P < 0.001).

higher reserves at the beginning of the next day. Note that

two birds feeding at the low concentration diet (0.25 M)

used more energy during the night than they accumulated

during the previous day. These birds were in negative energy

balance and entered torpor at night. The amount of energy

used during the night depended on diurnal energy accumu-

lation. Daily energy accumulation depended on both daily

energy intake and diurnal energy expenditures (Fig. 7). To

determine the independent effect of diurnal energy intake

and energy expenses on the amount of energy used at night

we used multiple regression. Both daily energy intake and

daytime expenditure had significant effects on the amount

of energy spent at night (F,,q = 18.1, R’ = 0.82, P < 0.001).

However, energy intake had a significant positive effect

(partial regression coefficient % SE = 0.36 ? 0.07, P <

0.001) whereas daytime expenditures had a significant nega-

tive effect (partial regression coefficient -+ SE = -0.38 ?

0.14, P < 0.03). The amount of energy spent at night by

hummingbirds increased with increased energy intake, but

decreased with the amount of energy spent during the day.

Although hummingbirds were able to compensate for differ-

ences in energy intake and diurnal expenditures by varying

night energy use, their energy balance (i.e., the difference

between total daily intake and total daily expenditures) var-

ied with concentration. The energy balance of birds fed on

low (0.25 M) and high (0.75 M) sugar solutions was not

significantly different from 0. On average these birds were

not accumulating energy. The balance of birds fed on solu-

tions with intermediate sugar concentrations (0.5 M), in

contrast, was significantly positive (Fig. 8).

1296 M. V. Lbpez-Calleja rt al.

1200 1

8-

6-

ns

! 0.75


FIG. 8. Daily energy balance (energy intake minus energy expenditures) in Sephanoides sephanoides fed on sucrose solutions of varying in concentration. Histograms are means and error bars are standard errors (N = 4 hummingbirds per sucrose concentration).

DISCUSSION

Sugar Concentration and a Model of Hummingbird C&t Function: How Well Does it Perform?

Several predictions of Martinez de1 Rio and Karasov’s (33)

model were supported by the results of our experiments.

Hummingbirds exhibited almost complete assimilation ef-

ficiency of sugars, independently of sugar concentration.

The thorough assimilation of the sugars found in nectar

seems to be characteristic of hummingbirds (16,25,31). Our

results suggest that assimilation efficiency does not depend

on the sugar concentration of nectar. Also, as predicted by

the model, meal retention times and intermeal intervals in-

creased linearly with sugar concentration. The most impor-

tant prediction of the model, however, was falsified. Hum-

mingbirds did not increase their rate of energy intake when

fed on more concentrated sugar solutions. They maintained

remarkably constant daily energy intakes that were inde-

pendent of concentration.

A constant rate of daily energy intake can be interpreted

in two alternative ways: (a) At the scale of a day, humming-

birds did not act as “energy maximizers” (sensu Schoener,

42); or (b) gut processing rates “constrained” the rate of

energy intake at a maximal possible level as hypothesized

by Karasov et al. (25). Although our experiments do not

allow us to directly distinguish between these two hypothe-

ses, our observations support the first alternative. Birds con-

sumed significantly higher volumes of nectar early in the

morning than later in the afternoon, without compromising

digestive efficiency. Hummingbirds could completely assim-

ilate the sugar in food at higher rates than those shown on

‘v; 4 loo0 4

0 2 4 6 8 10 12 14 16 18 20

Meal Retention Time @ins.)

FIG. 9. A modified version of the figure depicted in Fig. 1. All parameters are identical to those used to construct Fig. 1, but we assumed that hummingbirds modulated inter-meal intervals to achieve a constant rate of energy intake rather than to maximize the rate of energy intake. The time that each meal should be processes can be found from the inter- section of the net rate of intake curve and the dashed line. The slope of this line equals 49.6 Jfmin (Le., 35.7 kJ/day). Note that under this assumption, the length of time spend between meals also increases as a function of sugar concentration in nectar. The predicted times spent processing meals containing 0.25 M, 0.50 M, and 0.75 M sucrose are indicated by arrows A, B, and C, respectively. Note that this model also predicts complete sugar assimilation. The model shown in Fig. 1 assumes that the gut functions continuously at maximal capacity. In contrast, this new model shows that as sugar concentration in food increases, the gut spends in. creasing periods of time idling. Idling times, defined as pee riods after which all sugar in the gut has been assimilated, are shown as horizontal bars a, b, and c for meals containing 0.25 M, 0.5 M, and 0.75 M sucrose, respectively.

average throughout the day. An energy-maximizing hum-

mingbirds could maintain those high intake rates and in-

crease its daily energy intake. As observed by Hainsworth

(17), Hainsworth et al. (18), and Hainsworth and Wolf (22)

in other hummingbird species, at the temporal scale of a

day hummingbirds appeared to regulate energy intake at a

constant level. They appeared to be “satisficers” [sensu

Ward, (48)] rather than maximizers.

How can we reconcile the lack of energy maximization

apparently shown by S. sephanoides with the verification of

several of the predictions of Martinez de1 Rio and Karasov’s

(33) model? F‘g I ure 9 shows the predicted relationship be-

tween meal retention time and sugar concentration in nec-

tar for a hummingbird attempting to maintain a constant

rate of energy intake. The predictions of the model under

this assumption are very similar to those predicted by an

energy maximization assumption: Hummingbirds should ex-

hibit almost complete assimilation efficiency of sugars inde-

pendently of sugar concentration and meal retention times,

and hence intermeal intervals, should increase linearly with

sugar concentration.

If these two assumptions yield similar predictions, how


can we differentiate among them? The energy maximization

assumption predicts that hummingbirds will be processing

food in the gut at the maximal possible rate allowed by sugar

hydrolysis and uptake in the gut (33), whereas the constant

energy intake model predicts that hummingbirds will not

use their guts at maximal capacity. Rather they will have

“idle” time during which the gut is empty and not actively

processing food (Fig. 9). Indeed, the model predicts that the

time that the gut spends “idle,” i.e., empty of food, will

increase as a function of sugar concentration. To test the

“constant” energy intake rate assumption, hummingbirds

must be exposed to environmental conditions that force

them to increase their rate of energy expenditure, such as

low temperature (27), unpredictable variation in environ-

mental temperature or food supplies (6,10), and long dis-

tances between the perch and the nectar source (45). We

predict that these experiments will show that humming-

birds will be able to match their energy intake to energy

expenditures and to show much higher rates of energy in-

takes than those shown in the benign conditions almost

always used to study hummingbird feeding behavior [(25);

this study]. It would be interesting to know if, and under

what experimental conditions, hummingbirds shift from

maintaining a constant rate of energy intake to energy in-

take maximization.

Karaso\. and Cork (26) examined the predictions of Mar-

tinez de1 Rio and Karasov’s (33) model in nectar-eating

Rainbow lorikeets (Trichoglossus haematodzls). The re-

sponses of lorikeets to variation of glucose concentration in

food were, in some respects, similar to those exhibited by

hummingbirds: Lorikeets showed no differences in assimila-

tion efficiency among sugar as a function of sugar concentra-

tion and did not show higher energy intake rates with in-

creased food sugar concentration. In contrast with

hummingbirds, however, sugar assimilation efficiency was

relatively low (90.5%) and meal retention times did not

differ among sugar concentrations. Karasov and Cork (26)

concluded that energy maximization was probably an inap-

propriate assumption for animals that are not growing, stor-

ing fat, or reproducing. The physiological mechanisms un-

derlying the differences in the responses of hummingbirds

and Iorikcets to food sugar concentration remain to be de-

termined.

Temporal Feeding Patterns

Several studies have reported that captive hummingbirds

maintain relatively constant rates of energy accumulation

during the day (22,47). With the exception of birds feeding

at low sugar concentrations, S. se&no&s individuals

showed highly significant declines in feeding rates, and en-

ergy accumulation, throughout the day (Fig. 2). Harrison

(14) reported similar patterns of decreased feeding through-

out the day in captive trap-lining [sensu Feinsinger and Col-

well, (12)] hummingbirds (Phaetornis superciliosus) fed ad li-

bitum. They hypothesized that the difference between trap-

liners and other hummingbird species is a result of variation

in the natural temporal availability of nectar. According to

Harrison (14) trap-liners feed on a shared nectar resource

that declines in availability throughout the day, whereas

other hummingbird species often maintain feeding territo-

ries where nectar availability can be defended at relatively

constant levels ( 11,15). Although Sephanoides sephanoides

males aggressively defend feeding territories (32), in captiv-

ity they show a declining rate of energy intake throughout

the day.

This decline has been shown in other hummingbirds.

Tiebout (46) has shown that in captivity, both the territori-

alist Anazilia saucerotii and the trap-lining Chlorostilbon can-

ivetii show declining intake rates of feeding throughout the

day (46). A declining pattern of feeding through the day

with a short burst of late afternoon feeding seems to be

widespread among passerines ( 1) and has been predicted un-

der fairly general assumptions by a dynamic optimization

model (3). A short burst of afternoon feeding was exhibited

by a wild broad-tailed hummingbird (5) and by S. sepha-

noides in captivity when fed on low sugar concentration

food (Fig. 2). Clearly, a constant pattern of feeding is not

common to all hummingbirds and may not even be com-

mon to all territorial species. The factors that explain the

variation shown by different hummingbird species in their

temporal pattern of feeding in captivity and in the wild re-

main to be established.

Sugar Concentration and Energy Management

Individual birds showed considerable flexibility in energy

management when faced with a food supply varying in qual-

ity (Figs 6 and 7). This flexibility led to relatively small

variation in daily energy budgets among diets (Fig. 8). One

of the factors that allowed hummingbirds to manage their

energy in a flexible fashion was the modulation of night

energy expenditures. The amount of energy spent at night

seemed to be regulated in a linear fashion hy the amount

of energy accumulated during the previous day (Fig. 7). Bed-

nekoff et al. (4) have shown a similar pattern in Great Tits

(Parus major). Given that hummingbirds can save energy by

lowering their nighttime metabolism (19,29,38), why don’t

they do it every night? Entering hypothermia must have a

cost, such as the reduction in the ability to detect and avoid

nocturnal predators (3,19), and must he used either when

energy availability is limited or when maintaining high fat

reserves is required, such as during pre-migratory fattening

(7). It must be emphasized, however, that our results and

those of Bednekoff et al. (3) suggest that energy conserva-

tion at night in small birds is not an ali or none phenome-

non. Rather the amount of energy used at night seemed to

be a continuous function of the amount of energy gathered

during the day. Furthermore, in our experiments, birds with

1298 M. V. L6pezCalleja et al.

the highest diurnal energy surpluses at nightfall seemed to

have higher energy reserves early in the morning. Because

in captivity hummingbirds tend to maintain relatively con-

stant body masses [(40), Mpez-Calleja and Bozinovic un-

publ. data], it is likely that birds with high morning energy

reserves will show lower energy intake rates (20). Even in

small animals, such as hummingbirds, all the intricacies of

the regulation of energy reserves may not be apparent in 24

hr measurements (22).

This matluscript benefited from the critical comments of C. L. Gass,

D. _I. Levey, T. McWhorter, D. O’Brien, M. Rosenmann, and D.

Wagner. Our work was supported by FONDECYT (Chile, grant J950394), Depto. Postgmdo y Postit&, LJ. de Chile (grant PG-

J4.96), and NSF (US, grant IBN: 9258505). This research was con-

ducted during the graduate program of M. V. L$ez-Calkja as part of her doctoral thesis.

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