Interplay between the energetics of foraging

and
thermoregulatory costs in the green-backed fire
crown
hummingbird Sephanoides sephaniodes

Abstract

In response to the interplay between variation in food quality and energetic demands, the
foraging
Behavior of captive green-backed fire crown hummingbirds Sephanoides sephaniodes was
studied.
Hummingbirds were exposed to two temperatures (25 Grados Celsius vs. 15grados Celsius),
two food qualities (0.5 vs. 0.75 m sucrose solutions), and two costs of feeding (birds were
provided with feeders with and without a perch). Food selection and consumption were
measured, as well as time budgets and metabolic rate while feeding. We predicted that
when given a choice, birds would minimize the cost of feeding by selecting feeders with a
perch and with a high sugar concentration. However, rather than increasing energy
consumption when energy availability was low and thermoregulatory demands were high,
hummingbirds remained perched.
They reduced feeding and spent most of their time perching. Our results identify a novel
behavioural and
Physiological strategy in hummingbirds. These birds seem to shift their foraging behavior
depending on
Thermoregulatory and feeding costs. When these costs are high, rather than matching them
with increased energy consumption, hummingbirds reduce energy costs by reducing
activity. They seemed to adopt the following strategy: when food quality was high and
thermoregulatory demands were low, they adopted a high-expense lifestyle. In contrast,
when thermoregulatory costs were high, they adopted an energy conserving strategy even
when food quality was high. We hypothesize that limitations imposed by
Physiological processes may explain why animals do not forage during all available time
and why under
Some circumstances they choose foraging behaviours with lower rates of net energy gain.

INTRODUCTION

Animals can face unpredictability in food availability and quality. In addition, daily
energy demands may change unpredictably. For example, in endotherms, a sudden
cold spell can lead to greatly increased thermoregulatory expenses (Dawson &
O'Connor, 1996). To match supply to demands, animals must show behavioural and
physiological flexibility. Because hummingbirds are small and have an expensive
foraging mode, they are good models to investigate how animals respond to variation
in food quality and energetic demands (P. J. Miller, 1996). The small size of
hummingbirds
Makes them sensitive to variation in energy availability and demands (Hainsworth,
1981; L. L. Wolf
& Hainsworth, 1983; Calder, 1984;Mc Nab, 1988). In the wild, hummingbirds often face
short-term fluctuations in environmental temperature and energy availability (Cornet et
al., 1979; Pyke & Waser, 1981; Tamm, 1989). The challenge posed by these fluctuations
is accompanied by extremely high feeding costs. The cost of hovering in feeding
hummingbirds can reach the upper metabolic limits of vertebrates (Bartholomew &
Lighton, 1986; Suarez et al., 1990; Suarez, 1998; Winter, 1998; Chai & Dudley, 1999).
To satisfy their energetic demands while feeding on nectar, a relatively dilute sugar
solution (Baker & Baker, 1973; Baker, 1975), hummingbirds must consume relatively
enormous amounts of food. Hummingbirds feeding on dilute nectar can ingest nearly
three times their body mass in nectar per day (Powers & Nagy, 1988; Gass, Romich &
Suarez, 1999; Mc Worther & Martinez del Rio, 1999). When modelling the dynamic
energy and mass
Budgets in biological systems, Kooijman (2000) identified the main factors that
determine energy acquisition as body mass, food availability and food type, and
temperature. Following Kooijman (2000), we investigated the interplay between
foraging energetic, the costs of thermoregulation, and the feeding decisions of captive
green-backed fire crown hummingbirds Sephanoides
sephaniodes (Trochilidae).

The cost of feeding was varied by providing hummingbirds with feeders with and
without a perch.
Sucrose concentration was varied to manipulate food quality. To probe the effect of
thermoregulatory costs on feeding, environmental temperature was varied. To provide
a mechanistic foundation for the behavioural responses of the hummingbirds in our
study, their time
budgets while feeding were also monitored. Because the maintenance of high and
constant body temperature is costly for small endotherms (Johnston & Bennett, 1996),
we predicted that in the cold, the increased thermoregulatory demands would lead to
increased energy consumption. Concomitantly, because thermoregulatory costs and
basal rates of energy expenditure in small birds typically account for nearly 40-60% of
total daily energy expenditure (B. A. Wolf, Wooden &
Walsberg, 2000), we also predicted that increased energetic feeding costs would lead
to increased feeding rates, supporting the compensatory feeding hypothesis
(Mc Worther & Martinez del Rio, 1999). In fact, R. S. Miller (1985) pointed out that
hovering is not necessarily the preferred mode of feeding in hummingbirds.
Because oxygen consumption increased 2.7- fold when S. sephaniodes fed while
perched, and 6.8-fold when they fed hovering (M. J. Fernandez, M. V. Lopez- Calleja & F.
Bozinovic, pers. comm.) consequently, we expected that when given a choice,
hummingbirds would select feeders with perches and with a high sugar concentration.
We also anticipated that at high temperatures
the benefits conferred by selecting a low cost, high return strategy would be reduced.
Thus, we expected harsh conditions to intensify the need to make wise feeding choices.

Our design and questions are ecologically relevant: the green-backed fire crown is a
migratory hummingbird that winters in the semi-arid and Mediterranean environments
of central Chile. In central Chile, these hummingbirds feed primarily on the nectar of
Sophora macrocarpa (Papilonaceae), Tristerix aphylus, T. tetrandrus (Lorantaceae),
Lobelia polyphylla (Lobeliaceae),
Porlieria chilensis (Zigofilaceae) and the introduced Eucalyptus globulus (Myrtaceae).
The sugar concentration in the nectar of these flowers ranges from 0.25 to 1.21 m
(Belmonte, 1988; Smith-Ramirez, 1993; Fraga, Ruffini & Grigera, 1997; Smith-Ramirez
& Armesto, 1998). Thus, birds can encounter food of varying quality while foraging.
Winters in central Chile can be cold and wet (di Castri & Hajek, 1976). Thus, birds can
be faced with cold spells in which thermoregulatory demands increase.
METHODS

Field observations, birds capture and maintenance Non-reproductive birds (mean body
mass-sd =
5.7- 0.4 g) were captured with mist nets in central Chile (33grados 17'S, 71grados
11'W) during June-July. Birds were maintained in individual 30x30x30 cm cages for 3
days, after which those birds that maintained a constant body mass (e.g. did not loss
weight) were transferred to a
60x60x60 cm cages in the aviary. Birds were maintained at 25 grados C under a 12:12
light:dark cycle and fed a 0.6 m sucrose solution, fruit-flies Drosophila melanogaster,
and water ad libitum. Between experiments, a vitamin and protein supplement was
added to the sucrose solution (Vimiprotein-L1, Rhone-Poulenc Rorer, S.A., Santiago,
Chile, 0.3 g/50 ml of solution). A total of 21 individuals were observed and studied. The
study was conducted during Austral winter-spring 1999
And autumn 2000.

Preference trials

Preference trials were conducted between 08:00 and 12:00. Variations were made to
temperature (15 Grados C and 25 Grados C), difference in sugar concentration (0.75
and 0.5 m sucrose), and the presence (P+) or absence (P7) of a perch in each of the
available feeders. Each trial consisted of 1 bird in a cage with 2 feeders. Feeders were
offered in all possible combinations of temperature,
sugar concentration and perch availability in a fully factorial design. At the 2
experimental temperatures (15 Grados C and 25 Grados C) birds spend 2.7 and 1.5
times more energy in thermoregulation, respectively, than at their thermo neutral zone
(28-33 Grados C; Lopez-Calleja & Bozinovic, 1995). Both sugar concentrations were
selected coinciding with previous feeding experiments (Lopez- Calleja, 1999).

Preference trials were determined in the 60x60X60 cm cages by providing each of 8

birds 2 feeders (with the different options). The feeders were at the same distance (c.
55 cm) from a single perch and 20 cm apart. Feeders outside the cage were used for
dripping control. Preference between feeding situation through volumetric
measurement of food consumption, was determined twice daily by measuring the
amount of food consumed from a graduated plastic feeder (. 0.1 ml). To minimize
Position effects, feeders were switched randomly between experiments. Food
consumption, body mass balance and time budget to asses the effects of sugar
concentration and ambient temperature on feeding strategy 8 birds were acclimated
for 7 days at 25 Grados C, then each bird was sequentially measured in each of 4
treatments (0.75/with-perch; 0.50/ with-perch; 0.75/without-perch; 0.50/without-perch).
Birds were then acclimated to 15 8C and the experimental
Protocol was repeated. Feeding frequency was monitored for 1 h (from 10:00 to 11:00)
using 2 video-recorders (Sony CCD-TR413 NTSC, Sony Corporation, Japan) placed in
front of the
experimental cages. These recorders were connected to a TV-VHS (Sony Corporation,
Japan) which allowed us to record the animal’s behaviour without disturbing them. To
minimize position effects, feeders were switched randomly between experiments. To
determined the mass balance, birds were weighed daily at 07:30 and mass balance
was calculated as the difference in weight between consecutive days.

Statistics

Statistical analyses were performed using STATISTICA (1997) statistical package for
Windows 95. The effect of treatments was tested by a multi-way ANOVA test followed
by the a posteriori Tukey test. Results are reported as mean - 1 sd,n= number of
individuals.

RESULTS

Food preferences with different ambient temperatures Comparisons involving feeders

with different sugar concentrations but with the same perch availability presumably
provide information about food preferences.
When ambient temperature was high (i.e. low thermoregulatory energy requirements),
captive green backed Fire crown hummingbirds significantly preferred the high sugar
concentration regardless of whether the feeder had a perch (F1, 44 = 38.79, P <0.0001,
see Fig. 1a) except in the case of 0.5 m/with-perch vs 0.75 m/without perch.
Comparisons involving the same sugar concentration presumably provide information
about diet selection based on perch availability. When offered food with lower sugar
concentration, hummingbirds significantly chose to feed on feeders with perch (F1,44 =
29.17, P< 0.0001; Fig. 1b). When presented with the higher
sugar concentration they showed no significant preference between feeders with or
without a perch
(F1,44 =0.166, P <0.690; Fig. 1b). The preferences of hummingbirds for feeders with
different perch availability depended on the quality of the available food. When birds
were provided with feeders containing low sugar concentration without perches and
feeders containing high sugar concentration with perches, they preferentially fed in
feeders with a perch and high sugar concentration (F1,44 =6.65, P= 0.01; Fig. 1a). When
they were offered an option between a feeder with a perch containing low sugar
concentration and a feeder without a perch containing
high sugar concentration, they did not show any significant preference (F1,44 =1.75, P=
0.18; Fig. 1a). Hummingbirds subjected to low ambient temperature significantly
preferred the high sugar concentration regardless of perch availability (F1,44 =31.65, P
< 0.001; Fig. 2a), but not for the treatment 0.5 m/with-perch vs 0.75 m/without-perch.
When offered only low sugar concentration,
birds significantly preferred the feeder with the perch, and presumably a lower
metabolic expenditure while feeding (Fig. 2b). Contrary to the results of the high
ambient temperature treatment, birds showed significant preferences for feeders with
perches when
presented with the high sugar concentration (F1,44 =6.77, P < 0.01; Fig. 2b). Mean
consumption was
higher in birds that could use a perch but this difference was not significant. As before,
the preferences of birds for feeders with different perch availability depended on the
quality of the available food. In addition, when they were offered a choice between a
feeder with a perch containing low sugar concentration and a feeder without a perch
containing high sugar concentration, they showed no significant preferences (F1,44 =
1.471, P =0.232; Fig. 2a).Food consumption, body mass balance and time budget Food
consumption (ml/min) decreased significantly with increasing sugar concentration and
ambient temperature, and was also significantly affected by the interaction between
sugar concentration and ambient temperature (Table 1a, Fig. 3a). Energy intake
(kJ/min) was not affected by sugar concentration but only by
ambient temperature (i.e. thermoregulatory energy requirements; see Table 1b, Fig.
3b). Contrary to our expectations, energy intake was lower when hummingbirds
were kept at the low ambient temperature.

Table 2. ANOVA testing for the influence of perch availability (P), sugar concentration (S), and
ambient temperature (Ta) on a) the frequency of visits to the feeder and b) resting time (min) in
Sephanoides sephaniodes.

Regarding time budgets, multi-way ANOVA indicated that the frequency of feeder visits
was higher at high ambient temperature (Fig. 4, Table 2a). Resting time was also higher
at low ambient temperature and affected by the interaction between sugar
concentration and perch availability (Fig. 4, Table 2b). In hummingbirds at low ambient
temperature resting time was 47% higher in comparison with birds at high ambient
temperature, independently of food quality or perch availability. Also, the frequency of
feeder visits was 31% lower in birds at low ambient temperature. As expected, a
negative linear relationship was observed between resting time and the frequency of
feeder visits (y= 35.05 70.40 x; r =0.44, Syx = 11.69, P = 0.0013). This behaviour may
allow hummingbirds to maintain body mass balance under different energy challenges,
as supported
by the lack of statistically significant effects of treatments (perch availability: F1,27 =
0.101, P= 0.753,
ambient temperature F1,27 =0.212, P = 0.649 and sugar concentration F1,27 = 0.126, P=
0.726) on daily mass balance (g/day).

DISCUSSION

Classic frameworks dealing with foraging behavioural ecology, including patch use as
well as diet selection, state that these behaviours depend on the ecological context in
which foraging takes place (Stephens & Krebs, 1986; Brown, 1988, 1999).
Nevertheless, the physiological capacities of animals, in combination with the energetic
cost of feeding and the availability, structure and chemical properties of food can also
have an important, albeit relatively unstudied effect on foraging
choice (Caraco et al., 1990; Martinez del Rio, 1990; Torres-Contreras & Bozinovic, 1997;
Bautista et al., 1998; Bozinovic & Vaquez, 1999). Theoretically, when an animal
minimizes the time spent to meet its energetic/ nutritional requirements or maximizes
the energy obtained,
it is considered to be maximizing its fitness (e.g. Schoener, 1971; Hixon & Carpenter,
1988; Dukas,
1998). Here we discuss the results of our experiments which are designed to help us
better understand the interplay between foraging energetics, the costs of
thermoregulation, and the feeding decisions of captive green-backed fire crown
hummingbirds. Our study examined how the feeding preferences of hummingbirds vary
with thermoregulatory costs, feeding expenditure,
and food quality. Hummingbirds increased energy intake (kJ/min) while minimizing
feeding costs. This behaviour is emphasized when they are confronted with higher
thermoregulatory costs. When ambient temperature was low hummingbirds minimized
their feeding activity despite the availability of more concentrated food (Figs 1b & 2b).
It seems that, depending on environmental and physiological factors, S. sephaniodes
would have decreased their net energy intake by choosing the perchless feeders. This
behaviour allows hummingbirds great flexibility in the management of their energy
budgets and mass balance. The puzzling reduction in energy intake at the lower
temperature occurs even though hummingbirds were perched without feeding for a
longer time in comparison to birds under high ambient temperatures. Comparisons
involving time budgets and the use of feeders as a function of the cost of feeding and
food quality presumably provide information about how hummingbirds select and
consume food and manage their time. It was observed that hummingbirds at low
ambient temperatures did not increase energy intake, but rather reduced the frequency
of feeder visits and spent most of their time perching. A similar behaviour was
observed by Bautista et al. (1998) in starlings. Hummingbirds did not increase their
energy intake when subjected to high thermoregulatory costs, despite the opportunity
to reduce feeding costs by perching. Why do the green-backed fire crown
hummingbirds spend most of their time resting instead of increasing energy intake?
Thermoregulatory costs account for 40-60% of the total daily energy expenditure of
small birds (B. A. Wolf & Walsberg, 1996). Also, ambient temperature affects not only
thermoregulatory costs, but May also affect the viscosity of the solution and therefore
the resulting costs of nectar procurement. For example, Kingsolver & Daniel (1983)
demonstrated that thermoregulatory costs may relate not only to the necessity of
keeping the homeothermy at a particular ambient temperature, but also to the
necessity of heating cool nectar to body temperature once it is ingested. Nevertheless,
our experiments do not allow us to test if the additional cost of warming ingested food
is negligible or not. Our previous unpublished measurements of oxygen consumption
during feeding revealed a significant increase in metabolic rate during both perch and
hover feeding in comparison to resting. The rate of metabolism during resting
increased 2.7-fold during perch feeding, and 6.8-fold during hover feeding (see Suarez
et al., 1990). Lopez-Calleja & Bozinovic (1995) reported that the maximum
thermoregulatory metabolic rate of S. sephaniodes is 26.5 ml O2/g h. A comparison of
the thermoregulatory costs at 15 Grados C plus the cost of feeding
(With or without a perch) revealed the importance of adopting a perch-feeding strategy.
At 15 Grados C the thermoregulatory cost of a 5.7 g hummingbird is c. 0.99 kJ/h. The
cost of hover feeding is 3.04 kJ/h while the cost of perch feeding is 1.2 kJ/h (Fernandez
et al. unpubl. data). Consequently, everything else being equal, the total energy
expenditure (cost of thermoregulation plus the cost feeding) may decrease from c. 4.0
kJ/h to 2.2 kJ/h if hummingbirds adopt a perch-feeding strategy. Thus, given the
variability in ambient temperature, in energy content of food and in perch availability,
these hummingbirds are often approaching their metabolic ceiling when foraging,
determining their behavioural decisions about foraging and time use. Thus, both the
rates of food intake and the available feeding time must be taken into account when
interpreting potential constraints on energy budgets (see Kvist & Lindstrom, 2000).

Alternatively, the rate of digestion and/or nutrient transport across gut membranes
may constrain the rate of energy intake at a maximal level as hypothesized by
Diamond et al. (1986) and Karasov et al. (1986). These authors suggested that
hummingbirds are energy maximizers, but that their digestive processing time
determines feeding behaviour, explaining why hummingbirds spend most of their time
perching. Although our experiments do not allow us to directly test the digestive
constraint hypothesis; Lopez-Calleja, Bozinovic & Martinez del Rio (1997) documented
that S. sephaniodes consumed significantly higher volumes of nectar early in the
morning than later in the afternoon without compromising digestive efficiency.
McWhorter & Martinez del Rio (1999) suggested that the rate of water processing by
the kidneys of hummingbirds might impose a constraint on energy intake. These
authors hypothesized that because hummingbirds feed on diets
that are dilute aqueous solutions, their feeding time as well as energy assimilation may
be constrained by excess water elimination. In addition, at low ambient temperature
there is an additional water excess as a result of decreased evaporative water loss
(Calder, 1984). These
physiological mechanisms may also explain why hummingbirds spend a long time
resting when feeding on diets with low sugar concentrations.
One major goal in physiological ecology is to understand the factors that might impose
a metabolic ceiling to the energy and time budgets of an animal. As pointed out by
Hammond & Diamond (1997), the energy budget of an organism may be limited by the
amount of food available in the environment and/or by its own design. Changes in time
budgets and in the expression of physiological and behavioural mechanisms of energy
conservation indicate the existence of a metabolic ceiling in hummingbirds. Recently,
McWhorter & Martinez del Rio (2000), McWhorter & Lopez-Calleja (2000) examined the
factors that might impose a constraint or might affect the energy and time budgets.
McWhorter & Martinez del Rio (2000) asked if gut function limits hummingbird food
intake and therefore influences their energy budgets. These authors found that when
hummingbirds were faced with higher energetic demands acutely, they were unable to
increase energy assimilation to meet these demands, suggesting a central limitation to
their energy budgets. On the other hand, Lopez-Calleja (1999) suggested that the
peripheral organs (muscles) of S. sephaniodes could not transform energy into work
and heat quickly enough to meet demands when birds were chronically exposed to low
temperatures (and thus higher energetic demands). That hummingbirds limit foraging
activity regardless of food availability, suggests that the concomitant energetic
demands of thermoregulation and flight costs may exceed the energetic capacity of the
muscle. Physiological capacities therefore influence food consumption and thus the
energy budgets of hummingbirds. Finally, McWhorter & Lopez-Calleja (2000) proposed
that the relative importance of central vs peripheral limitations changes based on the
temporal and spatial conditions experienced by the animal. That is, both central and
peripheral limitations are important influences on the energy budget of hummingbirds
and therefore affect their foraging ecology. In addition, our previous laboratory studies
of torpor in Chilean green-backed fire crown hummingbirds (Lopez-Calleja et al., 1997)
demonstrated that body temperature is lowered only when the hummingbird is
energetically stressed. Thus, they can reduce energy expenditure to compensate for
low food availability and/or quality and for high thermoregulatory and feeding costs
(see also Tiebout, 1991, 1992, 1993).

Our results identify a novel behavioural and physiological strategy in hummingbirds;

these animals seem to shift their foraging strategy depending on thermoregulatory and
feeding costs. When these are high, rather than matching them with increased energy
consumption, they reduce energy costs by reducing activity. Hummingbirds seemed to
adopt the following strategy: when food quality was high and thermoregulatory
demands were low, they adopted a high-expense lifestyle. In contrast,
when thermoregulatory costs were high, they adopted an energy-conserving strategy
even when food quality was high. We hypothesize that limitations imposed by
physiological processes may explain why animals are not capable of foraging during all
the time available, and why under some circumstances they choose foraging
behaviours with lower rates of net energy gain (Bozinovic & Martinez del Rio, 1996;
Bozinovic & Vasquez, 1999; Bozinovic et al., 2000). In addition, Sandlin (2000)
demonstrated that intraspecific interactions such as competition may also determine
foraging decision, i.e. selection of high or low food quality. All these factors indicate
that any particular behaviour represents an integrated response to the biotic and
abiotic environment and the physiological state of the animal. The physiological
constraints to the foraging ecology of animals are probably extremely important in
determining when and how a food patch should be used and a diet selected (Tamm,
1989), which in addition to inter- and intraspecific interactions
(Sandlin, 2000) would seem to be major components of the energy budget of free-living
hummingbirds.
Acknowledgements

This work was funded by a FONDAP 1051-0001 grant to F. Bozinovic. We are extremely
grateful to Lee Gass, Fabian Jaksic, Carlos Martinez del Rio, and Todd McWhorter,
Roberto Nespolo and Alvaro Palma for useful comments and their generous help. All
experiments reported in this article were conducted according to the Chilean current
law and under permit SAG-1485 of Servicio Agricola y Ganadero, Chile.