Sugar preferences, absorption efficiency and water influx in a Neotropical nectarivorous passerine,...

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Comparative Biochemistry and Physiol

Sugar preferences, absorption efficiency and water influx in a Neotropical

nectarivorous passerine, the Bananaquit (Coereba flaveola)

Astolfo Mataa,*, Carlos Bosqueb

aCentro de Ecologıa, Instituto Venezolano de Investigaciones Cientıficas, Apartado 21827, Caracas 1020-A, VenezuelabUniversidad Simon Bolıvar, Departamento de Biologıa de Organismos, Apartado 89000, Caracas 1080, Venezuela

Received 16 June 2004; received in revised form 11 October 2004; accepted 13 October 2004

Abstract

Nectarivory has evolved repeatedly in a number of unrelated bird taxa throughout the world and nectar feeding birds, regardless of their

taxonomic affiliation, display convergent foraging and food processing adaptations that allow them to subsist on weak sugar solutions.

However, phylogeny influences sugar type preferences of nectarivores. We investigated sugar preferences, assimilation efficiency and water

flux in a Neotropical honeycreeper, the Bananaquit (Coereba flaveola; Coerebidae), a member of a radiation of tanagers and finches.

Bananaquits showed no preference for nearly equicaloric (25% w/v) sucrose, glucose, fructose or glucose–fructose mixtures in pair-wise

choice tests. In agreement with this lack of preference, they were equally efficient at absorbing sucrose and both hexoses. Apparent

assimilation efficiency of these sugars was around 97.5%. In pair-wise tests, Bananaquits displayed a strong preference for the most

concentrated sucrose solution when the lowest concentration ranged from 276 to 522 mM. Between 522 and 1120 mM sucrose solution

concentrations, Bananaquits were able to adjust their volumetric food intake in order to maintain a constant energy intake. At solution

concentration of 276 mM, birds could not maintain their rate of energy intake by increasing food consumption enough. We consider that at

low sugar concentrations, Bananaquits faced a physiological constraint; they were unable to process food at a fast enough rate to meet their

energy needs. We also explored the possibility that dilute nectars might be essential to sustain high water needs of Bananaquits by allowing

them to control osmolarity of the food. Between 276 and 1120 mM sucrose solution concentrations, average amount of free water drunk by

Bananaquits was independent of food concentration. They drank very little supplementary water and did not effectively dilute concentrated

nectars. The evidence suggests that water bulk of dilute nectars is a burden to Bananaquits.

D 2004 Elsevier Inc. All rights reserved.

Keywords: Nectarivory; Nectar; Sugar assimilation; Energy balance; Sugar concentration; Physiological constraints; Bananaquit; Coereba

1. Introduction

Nectar is the main brewardQ for nectarivorous birds, andbird-pollinated plants, regardless of phylogenetic or geo-

graphic origin, secrete nectars that are dilute solutions of

simple sugars containing trace amounts of salts and amino

acids (Baker et al., 1998). In turn, nectarivores, such as

hummingbirds (Trochilidae) in the New World, many

sunbirds (Nectariniidae) in the Old World, and honeyeaters

1095-6433/$ - see front matter D 2004 Elsevier Inc. All rights reserved.

doi:10.1016/j.cbpb.2004.10.012

* Corresponding author. c/o Biblioteca Marcel Roche-IVIC, 8424

NW56 Street Suite Ccs 00206, Miami, FL 33166, USA.

E-mail address: [email protected] (A. Mata).

(Meliphagidae) in Australasia, which have independent

taxonomic affiliations and biogeographic origins, display

convergent behavioral and physiological adaptations that

allow them to process nectars efficiently. Typically, nectar-

ivorous birds can handle large volumes of food, sustain high

water influx rates and display preference for sugars that they

are more proficient at digesting and absorbing (Collins,

1981; Martınez del Rıo, 1990). In the New World,

hummingbirds are the main avian pollinators, particularly

in tropical regions, but there are a number of other flower

visitors belonging to Thraupidae (tanagers), Icteridae

(blackbirds), Emberizidae (flowerpiercers) and Coerebidae

(honeycreepers) seemingly well adapted to a nectar diet

also. However, we know little about their ability to subsist

ogy, Part A 139 (2004) 395–404

A. Mata, C. Bosque / Comparative Biochemistry and Physiology, Part A 139 (2004) 395–404396

on nectar. In this work, we study food selection and

processing adaptations of a common neotropical passerine

nectar feeder, the Bananaquit (Coereba flaveola; Coerebi-

dae—A.O.U., 1998).

The Bananaquit is primarily a perching nectar feeder that

visits a broad variety of flowers of trees, shrubs, vines and

herbaceous plants from habitats ranging from arid scrubs to

montane evergreen forests (Hilty, 2002; Snow and Snow,

1971). Bananaquits enter most flowers from the front and

are effective pollinators of bromeliads (Sazima and Sazima,

1999); however, they are also nectar robbers and readily

poke holes in the base of long tubular corollas. This habit of

brobbingQ nectar has led some authors to considered

Bananaquits as parasites of the hummingbird–flower system

(Stiles and Freeman, 1993). Bananaquits also feed on fruits,

fruit juices, insects and, to a lesser extent, the protein

corpuscles of Cecropia (Snow and Snow, 1971, personal

observations). On the other hand, when plant food is not

readily available, Bananaquits can rely mostly on insects

and other arthropods (Bosque, 1984).

We investigated sugar preferences and assimilation

efficiencies of the Bananaquit. Sugar composition of nectars

has important consequences on bird feeding preferences

because the later may be constrained by physiological or

biochemical properties of gut function (e.g. Martinez del

Rio et al., 1992; Schondube and Martınez del Rıo, 2003).

Hence, birds of different taxonomic origin display contrast-

ing preferences for nectars varying in their proportion of

sucrose to hexoses (glucose and fructose). For instance,

among passerines, in the clade that includes thrushes

(Turdidae), starlings (Sturnidae), and mockingbirds (Mim-

idae), preference for hexoses over sucrose is related to the

fact that these birds do not express sucrase, the intestinal

enzyme that hydrolyzes sucrose (Martınez del Rıo et al.,

1988; Martınez del Rıo, 1990). In general, flowers visited

by passerines seem to produce nectars with low sucrose to

hexose ratios (Baker et al., 1998), which suggests that

passerines should display preference for hexoses. However,

we know little about sugar preferences and assimilation

efficiencies of New World passerines (but see Martınez del

Rıo, 1990; Schondube and Martınez del Rıo, 2003). We

expected that Bananaquits would be able to utilize sucrose

as well as hexoses efficiently, by virtue of their ability to

use a broad range of flower species, including those visited

by hummingbirds that are rich in sucrose (Baker and Baker,

1983).

In addition, we examined preferences and water influx of

Bananaquits in relation to sugar concentration of the food.

This aspect is of interest because flowers pollinated by

birds, particularly those visited by passerines, tend to

produce relatively dilute nectars (Baker, 1975; Baker and

Baker, 1982; Nicolson, 2002). Nectar concentration affects

the water balance of nectarivores because their water intake

is intrinsically linked to nectar concentration, and weak

nectars may place extreme water loads on birds (Fleming

and Nicolson, 2003). Why nectars of bird-pollinated plants

are so dilute is still a matter of controversy, and several non-

excluding hypotheses have been proposed (summarized by

Nicolson, 2002). In this work, we specifically consider the

possibility that nectarivorous birds need to maintain high

water influx rates, and consequently restrict the upper limits

of nectar concentrations. We considered that birds could

dilute concentrated solutions because food concentration

affects digesta retention time in nectarivores, fairly con-

centrated nectars can decrease gut emptying time and

motility (Afik and Karasov, 1995; Witmer and Soest,

1998; Witmer, 1998); and because on concentrated nectars,

free water may be an important component of the bird’s

water balance (Fleming and Nicolson, 2003). We gave birds

the opportunity to voluntarily control their water influx

rates by offering standing water in addition to sugars

solutions of increasing concentration. This condition

allowed birds to effectively dilute concentrated foods by

drinking free water, if they choose. The idea that

nectarivores may act as selective agents for weak nectars,

originally sketched by Baker (1975), has received little

attention but has also been recently examined by Nicolson

and Fleming (2003) in the African Whitebellied Sunbird

(Nectarinia talatala).

Finally, we tested the ability of Bananaquits to maintain

energy balance when fed a range of sugar concentrations. In

nature, nectar concentration varies widely (averaging from

200 to 2900 mM; Nicolson, 1998), and even small

differences in nectar concentration affect considerably the

energy balance of nectarivores (Martınez del Rıo et al.,

2001). We had interest in determining whether Bananaquits

showed compensatory feeding by decreasing their volu-

metric intake as the energy density of food increased, as has

been shown for a variety of avian nectarivores (Collins,

1981; Lloyd, 1989; Downs, 1997; Lopez-Calleja et al.,

1997; Nicolson and Fleming, 2003; Schondube and

Martınez del Rıo, 2003.

2. Materials and methods

Eight adult Bananaquits were captured with mist-nets

during October–November 2001 at the Simon Bolıvar

University campus in Caracas, Venezuela. Birds were

banded and housed individually in maintenance cages

(50�50�50) cm under a 12:12 h light/dark photoperiod at

room temperature (range 19–22 8C). At capture, averagemass was 9.31 gF0.73 SD (range: 8.20–10.47 g, n=8).

Birds were acclimated to captivity for at least 10 days before

the beginning of experiments and provided two maintenance

diets simultaneously: a 500-mM solution of equal parts of

glucose, fructose and sucrose and a mixture of the same

solution supplemented with EnsureR (Abbott Laboratories,

Holland), diluted to 6.25 g Ensure per 100 g of sugary

solution. In addition, permanently anesthetized fruit flies

(Drosophila sp.) and water were available ad libitum.

Maintenance diets, water and fruit flies were also provided

A. Mata, C. Bosque / Comparative Biochemistry and Physiology, Part A 139 (2004) 395–404 397

between experiments. Body masses, whenever indicated,

were measured with an electronic balance (Ohaus Scout II)

to the nearest 0.01 g.

2.1. Sugar type and concentration preferences

To determine possible preferences for sugar type and

concentration, we offered individual birds a choice between

two solutions placed randomly in two of four possible

positions in plastic cylindrical experimental cages (25 L).

Each feeder was a modified 10 mL pipette (graduated to 0.1

mL), with the surrounding of the drinking hole painted with

red nail varnish. Each pipette was hung on the outer side of

the cage and the bent end was introduced in an opening 5

cm above the bottom of the cage. The sugar volume

consumed hourly could be read externally with minimal

perturbation to the birds. Tests lasted 6 h and were

conducted from 0900 until 1500 h. At the end of each test,

birds were returned to maintenance cages. Food was always

provided in excess.

Preference for solution A over solution B was expressed

as a proportion; i.e. response to A/(response to A+ response

to B). Response was considered as the volume (mL) of

solution, or amount of sugar (mg) consumed when testing

for sugar type or concentration preferences, respectively.

Preference values near 1 indicate high preference; 0.5

indicates no preference and values around 0 aversion

(Martin and Bateson, 1993). Statistical tests were performed

on the arc sin transformed data.

Preference for sugar types was tested separately using a

Randomized Block Experimental Design in which individ-

ual birds were considered as blocks (e.g. Lotz and Nicolson,

1996). We presented each bird with each of six possible

pairs of nearly isocaloric (25% w/v) solutions of sucrose,

glucose, fructose and a 1:1 mixture of glucose and fructose.

Energy density of the sucrose solution should be approx-

imately 5% higher than that of hexoses (Fleming et al.,

2004). Each sugar pair was randomly allocated daily to each

bird for the 6 days that the experiment lasted. To accustom

birds to experimental sugar solutions and experimental

cages, we offered all four sugar solutions simultaneously

(randomly placed) for three consecutive days (from 0900

until 1500 h), before the beginning of the experiments. The

underlying assumption is that birds eat more of the food

type they prefer.

To determine sugar concentration preferences, we used

the same experimental design but offered pairs of sucrose

solutions of 276, 522, 743 and 943 mM. This experiment

lasted 6 days also. Each bird was tested only once for each

of the sugar type or concentration combinations.

It is well known that in addition to energetic and

nutritional values of foods, others factor such as palatability,

novelty, and positional biases affect food choice in birds

(Mason and Clark, 2000). To lessen such possible effects,

we made sure that all sugars were familiar to the birds

before experiments, and removed the effect of possible

confounding variables, such as individual positional prefer-

ences (Franke et al., 1998; Jackson et al., 1998), by

assigning sugar positions randomly each day (e.g. Lotz

and Nicolson, 1996).

Body mass of birds, recorded daily before each choice

session, remained nearly constant throughout the experi-

mental period, indicating that birds maintained their energy

balance under our laboratory conditions.

2.2. Assimilation efficiency of sugars

To determine the efficiency of Bananaquits to absorb

sucrose, glucose and fructose, we offered to four individual

birds each of these sugars for periods of 11 h during three

consecutive days, and measured the volume of the sugar

solution consumed and of excreta produced daily. Birds were

transferred from maintenance to experimental cages at 1800

h on the preceding day of the 3-day experiment. At 0700 h of

each experimental day, birds were offered a 529-mM sugar

solution and their consumption was measured hourly until

1800 h. Excreta, corresponding to 24-h periods, were

collected twice daily (to minimize contamination) in plastic

trays containing a 2-cm layer of liquid paraffin placed under

cages. The total volume was recorded to the nearest 0.1 mL

in 10-mL graduated cylinders. Birds were weighed before

and after each daily trial and returned to the experimental

cages. Sugar concentration in the excreta was measured by

the use of a hand held refractometer (Fischer; accurate to

0.2%). Apparent sugar assimilation efficiency coefficient

(AE) was estimated as the percentage of sugar ingested that

was not excreted, AE=(gSing�gSexc)/gSing�100; where

gSing and gSexc are the amounts (g) of each sugar ingested

and defecated, respectively (Karasov, 1990).

Although solids other than sugars can affect refractom-

eter readings (Inouye et al., 1980), measurements of sugar

concentration in the excreta of birds feeding solely on liquid

diets should be little affected. In addition, solid matter was a

negligible component of the cloacal fluid of Bananaquits;

nonetheless, we centrifuged samples and used only the

supernatant for refractometer reading. Presence of electro-

lytes in the excreta would erroneously cause an over-

estimation of the concentration of sugar in the excreta and

hence an underestimation of AEs.

2.3. Sucrose intake and water influx in relation to solution

concentration

We measured sucrose intake and estimated water influx

in relation to the concentration of the food to determine:

First, if Bananaquits effectively diluted the more concen-

trated foods by drinking supplementary water; and second,

whether Bananaquits showed compensatory feeding by

ingesting a constant amount of sugar, independently of

food concentration. We offered to each of seven individuals

a sucrose solution in one feeder and water in the other

(randomly placed). We randomized the order in which each

Administrador

Resaltado

Fig. 1. Preference of Bananaquits, C. flaveola, between pairs of nearly

isocaloric (25% w/v) sugars solutions (S: Sucrose; G: glucose; F: fructose;

GF: 1:1 mixture of G and F), shown as the proportion of sugar solution

eaten (left in pair position). For each sugar pair, individual preferences were

calculated for each bird and the mean preference (cross hair) for the eight

birds tested against the null hypothesis of no preference (0.5; dotted line),

using one-sample paired t-tests. Birds showed no preference for any sugar

type. Each symbol denotes an individual bird.

Fig. 2. Intake of glucose (open symbols) or fructose (solid symbols) in

relation to intake of sucrose in pair-wise choice trials of nearly equicaloric

solutions ( y=1.10�0.97x, r2=0.82, Pb0.05). The slope of the linear

relationship is not significantly different from �1, indicating that all sugars

are energetically equivalent to Bananaquits. Dotted lines indicate 95%

confidence interval.


of five sucrose solutions concentrations (276, 522, 743, 943,

and 1120) was presented daily to each bird. Birds were

weighed and introduced in the cylindrical cages at 0900 h,

and their consumption of sugar solution and water was

recorded hourly until 1500 h. Those sugar concentrations

comprise the range of nectars habitually found in bird-

pollinated flowers (Baker et al., 1998). We estimated water

influx as the sum of water gained by drinking, preformed

water in food, and metabolically produced water (Schmidt-

Nielsen, 1997). Preformed and metabolic water intakes were

determined from solution intakes. Metabolic water produc-

tion was estimated from the amount of sugar consumed

during the 6-h experimental interval, assuming that 97% of

sucrose was assimilated (see Results) and that oxidation of 1

g of sugar produces 0.56 g of water (Schmidt-Nielsen,

1997).

We also recorded Bananaquit activity by means of video

cameras placed above each of six experimental cages. We

measured frequency and duration of visits to the sugar (or

water) feeders by direct inspection of the video recordings,

and report here on the relationship between sucrose

concentration and time interval between feeding bouts only.

Further details on this section of the study will be published

elsewhere.

2.4. Digesta retention time

We grossly estimated transit time of the digesta—the

time of first appearance of a marker in the excreta—by

offering for 5 minutes to each of four Bananaquits, a 529-

mM sucrose solution dyed with red Mc Cormick food

colorant (e.g. Downs, 1997). At the end of this period,

the colored solution was replaced by a similar non-dyed

solution. We monitored excreta production continuously

through a video camera and recorded by visual inspection

the time when colorant was first present in the excreta.

Birds were unfed for 12 h prior to the experiment and all

of them fed avidly during the early morning trials.

Excreta were collected under mineral oil in the exper-

imental cages.

3. Results

3.1. Sugar type preferences

Compared with the no preference value (arc sin 0.5),

Bananaquits did not show preference for any of the 529-mM

sugar solutions (Fig 1; PN0.05 for all sugar pairs; paired one

sample t-test, n=8 in each case). All sugars, glucose,

fructose, sucrose and the glucose–fructose mix, were

equally acceptable to the birds. Furthermore, there were

no significant differences between the mean volume of each

sugar type consumed by all birds during the 6-day experi-

ment (Repeated measures one-way ANOVA F(3,21)=0.203;

P=0.893).

3.2. Digestion and assimilation efficiency of sugars.

Assimilation efficiencies, of sucrose 97.2F0.1, glucose

97.5F0.1, fructose 97.4F0.2 (n=4 in all cases) were

evenly high, indicating that Bananaquits are equally able

to assimilate sugars of different chemical composition.

Birds ingested all sugars solutions at a similar rate; the

average total volume of each sugar solution consumed by

all four birds at the end of each 12-h period did not

differ between the three sugars (Repeated measures one

way ANOVA F(2,6)=1.76; P=0.25), suggesting that all

Fig. 4. Average solution (A) and sugar intake (B) rates in relation to sucrose

concentration. Mean values not sharing a common letter are significantly

different ( Pb0.05). Sugar intake is independent of concentration when


sugars are energetically similar to Bananaquits. Average

body masses recorded at 0700 or at 1800 h (n=4) did

not differ among days (repeated measures two way

ANOVA: F(2,6)=0.019; P=0.70), but the mean body mass

at 1800 h was significantly higher than the mean mass at

0700 h (F(1,3)=133,9; Pb0.001). Thus, body mass gained

during the day-time and body mass lost at night were

similar for all sugars. In addition, when Bananaquits

were given a choice between glucose or fructose and

sucrose, their rate of hexose intake was negatively

correlated with the rate of sucrose intake. The slope of

this relationship was not significantly different from �1

(t14=0.202, PN0.05; Fig 2). We conclude that Banana-

quits are able to survive on any of the sugars tested at

least for short periods of time.

3.3. Sugar concentration preferences

Bananaquits showed a strong preference for the most

concentrated sucrose solution available, when the most

diluted solution of the pair ranged from 276 to 522 mM,

but showed no preference—or did not discriminate—

between the two most concentrated solutions (743 vs.

943 mM; Fig. 3).

3.4. Volume intake rates and compensatory feeding

Sucrose concentration had a significant effect on

volumetric intake rates of Bananaquits (repeated-measures

ANOVA, F(4,24)=4.40, Pb0.05); as sucrose concentration

increased Bananaquits diminished their volumetric food

ingestion (Fig. 4A). Thus, birds compensated for low sugar

feeding on solutions above 400 mM.

Fig. 3. Sucrose concentration preferences of Bananaquits, expressed as the

proportion of the volume of sugar solution eaten (left in pair). Preference

was calculated for each bird and the mean preference (cross hair) for the

eight birds tested against the null hypothesis of no preference (0.5; dotted

line), using one-sample paired t-tests. Mean preference values significantly

different from 0.5 are indicated by an asterisk below the sugar pair. Values

clumped around zero indicate aversion for the sugar in the left of the pair. In

most cases, Bananaquits preferred the most concentrated sugar solution.

content of food by increasing consumption. This relation-

ship is described by the power function y=94.4x�0.7934

(r2=0.95), where y is the volume (mL) of solution ingested

and x is the sugar concentration (mM; following

Fig. 5. Bananaquit body mass change in relation to sucrose solution

concentration. Cross hairs indicate mean values.


McWhorter and Martınez del Rıo, 1999). The exponent of

this power function was significantly greater than �1

(slopeFse=�0.793F0.089, r2=0.708), indicating that com-

pensatory ability of Bananaquits was limited. When

concentration of the sucrose solution was decreased to

276 mM, they could not maintain their rate of sugar (and

energy) intake by increasing food consumption enough

(Fig. 4B). In contrast, average sugar intake remained

constant when concentration of the sucrose solutions varied

from 522 to 1120 mM. Inability to balance their energy

budget when fed the most diluted diet was evident by the

fact that, in contrast to all other diets, on average birds were

not able to gain mass after feeding for six hours on this diet

(Fig. 5). Nevertheless, individuals differed in their ability to

gain or lose weight.

3.5. Feeding pattern and digesta retention time

Bananaquits fed intermittently, they licked rapidly the

sugar solutions for brief feeding bouts before pausing for

varying amounts of time that depended on solution concen-

tration. Time interval between feeding bouts decreased with

decreasing sucrose concentration ( y(min)=0.96+0.004x(mM);

r=0.56, Pb0.001; n=30); forcing Bananaquits to feed more

frequently, likely attempting to maintain a constant level of

sugar intake (see Fig. 4B). Digesta transit time of four birds

fed sucrose solutions ranged from 17 to 25 min.

3.6. Water influx and consumption of standing water

Bananaquits drank very little water regardless of sucrose

concentration. The average amount of standing water

consumed per bird during the 6-h experimental period was

independent of solution concentration (F (4,16)=2.127,

P=0.125; Fig. 6). Their total water influx was largely

determined by the amount of preformed water in food, the

Fig. 6. Water influx of Bananaquits at different sucrose concentrations,

when supplementary drinking water was available. Bananaquits do not

dilute concentrated foods.

contribution of metabolic water being minor also. Banana-

quits were able to handle large water fluxes, particularly

when feeding on the most dilute sucrose solution.

4. Discussion

Our results show that Bananaquits share with specialized

nectarivores a number of traits that allow them to exploit

nectar efficiently. Indeed, they are able to subsist temporally

on sugar solutions by digesting disaccharides and absorbing

single sugars efficiently, and by sustaining high water fluxes

in order to process large volumes of dilute nectar rapidly. In

addition, they have anatomical adaptations, such as a highly

modified bifurcated, nearly tubular, tongue lined with

fringes (Bezzel and Prinzinger, 1990), a slender sharp

decurved bill, and a simple and short digestive tract

(personal observations), that facilitate nectar collection and

processing.

The Bananaquit is a member of a large radiation of

tanagers (Thraupidae) and finches (Fringillidae) among

which nectar-feeding seemed to have evolved independently

multiple times. Its precise phylogenetic affinities are still a

matter of controversy, but its sister genera are rather of the

bfinche typeQ (Burns et al., 2003; Remsen, 2003). Nectar-

feeding adaptations of Bananaquits are similar to those of

other unrelated taxa such as New World hummingbirds

(Martınez del Rıo, 1990) and flowerpiercers (Schondube

and Martınez del Rıo, 2003), Old World sunbirds (Nectar-

iniidae; Lloyd, 1989; Downs and Perrin, 1996; Lotz and

Nicolson, 1996), and Australasian honeyeaters (Mellipha-

gidae; Collins, 1981), lories and lorikeets (Loriidae;

Karasov and Cork, 1996, see also Klasing, 1998).

4.1. Sugar type preference and assimilation efficiencies

Bananaquits showed no preference for sucrose, glucose

or fructose in pair-wise choice tests. In agreement with

this lack of preference, birds were equally efficient at

absorbing sucrose and both hexoses; apparent assimilation

efficiency of any of these sugars was above 97%. High

assimilation efficiency is typical of nectarivorous birds

(Karasov, 1990); thus, Bananaquit assimilation efficiencies

are comparable to those of hummingbirds (97–99%;

Castro et al., 1989; Karasov, 1990), sunbirds (99%;

Downs, 1997; Jackson et al., 1998), and Australian

lorikeets (98%; Karasov and Cork, 1996). It is noteworthy

that Bananaquits did not show preference for sucrose

solutions, which are about 5% energetically richer than

hexose solutions (see above). High variability of the data

in Fig. 1 suggests that lack of preference could have been

the result of individual birds making opposite choices

during specific trials, not necessarily the result of all

animals ingesting similar amounts of both solutions being

tested (see Fig. 1). Some of this individual variation could

have also been due to positional preferences; however, as


explained above, these confounding effects should not

affect the conclusion that as a group Bananaquits showed

no preference for any of the sugars tested. Contrasting

results of the concentration preference experiment, show-

ing that Bananaquits have strong preference for the most

concentrated sugar solution available (Fig. 3), reveal that

sugar preferences prevail when taking side biases into

account by randomizing sugar positions (see also Lotz and

Nicolson, 1996).

Bananaquits assimilate sucrose efficiently, indicating that

they express sucrase, the intestinal enzyme required to

hydrolyze sucrose before absorption of its hexose compo-

nents. The ability of Bananaquits to process sucrose

efficiently was manifested by several lines of evidence.

First, the slope of the linear relationship between the rates of

hexose and sucrose intake in pair-wise trials was not

statistically different from �1 (Fig. 2). Second, Bananaquits

ingested nearly equicaloric hexose and sucrose solutions at

similar rates during 12-h trials, and the assimilation

efficiency of each of those sugars was similar. Third, daily

changes in body mass were similar when consuming

hexoses or sucrose. Taken together, these results indicate

that hexoses and sucrose were energetically equivalent to

birds. Hence, Bananaquits not only must express sucrase,

but most likely, its activity was high enough that the rate of

hydrolysis of sucrose did not hinder assimilation of its

monomer components, although Bananaquits had high

passage rates (see Afik and Karasov, 1995).

In general, passerines prefer glucose and fructose over

sucrose (Martinez del Rio et al., 1992; Baker et al., 1998),

while hummingbirds prefer sucrose over glucose or fructose

only solutions (Martınez del Rıo, 1990; Stiles, 1976).

However, it is now known that preference for sugar types

is not an invariable trait of nectarivores. Recently, Nicolson

(2002) revealed that in floral nectars of southern African

plants, composition and concentration are related; more

concentrated nectars are sucrose-rich while hexose nectars

are dilute. Concomitantly, it has been shown that in the

Neotropical Cinnamon-bellied Flowerpiercer (Diglossa bar-

itula) and the Magnificent Hummingbird (Eugenes fulgens)

sugar preference depends on nectar concentration. Both

species prefer sucrose at higher concentrations, but their

preference switches to hexoses at lower concentrations

(Schondube and Martınez del Rıo, 2003).

Our type preference experiments were performed at

intermediate concentrations only (25% w/v), and Banana-

quits, like other specialized nectar-feeding birds, including

the Cinnamon-bellied Flowerpiercer and the Magnificent

Hummingbird, were indifferent at this concentration. We

have no basis to hint at possible concentration-dependent

sugar preference in Bananaquits; nonetheless, our results

strongly suggest that they are sugar generalists. This

conclusion is in agreement with the broad range of flowers

regularly visited by Bananaquits in Trinidad, where they

feed from at least 50 flower species (Snow and Snow,

1971).

4.2. Sugar concentration preferences and compensatory

feeding

In pair-wise choice tests, Bananaquits consistently chose

the highest sucrose concentration, although they were

indifferent to the two more concentrated solutions (Fig. 3).

Preference trials examine the hypothesis that individuals are

able to discriminate between alternative foods and select the

most profitable one. The underlying assumption is that the

rate of energy (or nutrient) acquisition should be maxi-

mized. Although preference trials do not specifically

examine this supposition, it can be assumed that max-

imization of energy intake can be achieved by maximizing

benefits and/or minimizing foraging and food processing

costs. In our choice trials, Bananaquits always preferred the

richest solution when concentration ranged from 276 to 522

mM. The advantage of selecting the more concentrated food

when offered dilute solutions is clear; when feeding on the

weakest solution, they were unable to maintain their energy

balance and lost mass (Fig. 4A and B). When given a choice

between foods of intermediate concentration, Bananaquits

also preferred the most concentrated one, but benefits

associated to such selection are not as readily apparent.

Above 522 mM, their energy gains remained constant

regardless of sugar concentration (Fig. 4B). Hence, at

intermediate concentrations, benefits of rejecting the weak-

est solutions are likely related to the reduction of time and

(or) energy costs of foraging and food processing. In

agreement with this proposition, time between feeding

bouts increased with nectar concentration, consequently,

resting time decreased as concentration of the food became

weaker. In addition, excess water intake poses energetic and

physiological challenges associated with thermoregulation,

renal function and electrolyte balance. Cost of food

warming, energy expenditure in recovering solutes, and

electrolyte losses increase with food dilution (Fleming and

Nicolson, 2003; Lotz et al., 2003; Lotz and Nicolson, 2002).

Interestingly, when Bananaquits were offered the two

most concentrated sucrose solutions (743 vs. 943 mM), their

preference for the richest food vanished. Why this is so is a

question of interest, but the answer is unclear to us. It is

unlikely that Bananaquits were unable to discriminate

between both solutions, our results show that they have

sharp discriminatory abilities. It is more likely that when

feeding on solutions above approximately 700 mM, no

further reduction of foraging and food processing costs can

be accrued under our experimental conditions. Likewise, in

Rufous Hummingbirds (Selasphorus rufus) preference for

concentrated sucrose solutions disappears above 50% (w/v);

their discriminatory ability is more precise in the range of

flowers, they most often exploit for nectar (near 20%; Blem

et al., 2000).

Nectar-feeding birds increase their volumetric food

intake as sugar concentration decreases (Lopez-Calleja et

al., 1997; Collins, 1981; Lotz and Nicolson, 1999). The

relationship between both variables has been described as a


power function whose exponent, when equal to �1,

indicates that compensation is complete. Under such

circumstances, sugar intake is independent of food concen-

tration (McWhorter and Martınez del Rıo, 1999; McWhorter

and Martınez del Rıo, 2000). Within the range of sugar

concentrations used in our experiments, the exponent of the

intake–concentration curve was significantly greater than

�1, indicating that sugar intake was dependent of sugar

concentration. Bananaquits did not display perfect compen-

satory feeding. However, if the lowest concentration (276

mM) is excluded, they showed perfect compensation. In

effect, between 522 and 1120 mM solution concentrations,

sucrose intake was independent of concentration. Compen-

satory feeding is a widespread capacity of birds in general

(Klasing, 1998), and of nectarivores in particular

(McWhorter and Lopez-Calleja, 2000; Martınez del Rıo et

al., 2001; Nicolson and Fleming, 2003).

When feeding on the weakest solution (276 mM),

Bananaquits could not maintain their rate of sugar intake

by increasing food consumption (Fig. 4A,B). At low sugar

concentrations, Bananaquits faced a physiological con-

straint; they were unable to process food at a fast enough

rate to meet their energy needs. Reduced energy intake and

increased energy costs when processing dilute foods caused

birds to loose mass (Fig. 5). Such constraint on energy

acquisition could be the consequence of limits on the

digestion and absorption of sucrose and (or) on the

processing of preformed water (Martınez del Rıo et al.,

2001; Nicolson and Fleming, 2003). At low nectar concen-

trations, assimilation of sugars may be reduced because

sucrose hydrolysis becomes the limiting step, or because

absorption may be limited by low luminal concentrations

(Levey and Martınez del Rıo, 1999). An alternative, non-

exclusive hypothesis is that the rate of plasma processing by

the kidneys could limit food ingestion, if water absorption

from the digesta was essentially complete (Beuchat et al.,

1990). Under either of these circumstances, a high water

load would place an upper limit to the rate of food

processing, and consequently compromise the rate of energy

acquisition.

Like Bananaquits, other nectarivores typically suffer a

shift from compensatory feeding to physiological constraint

when feeding on very dilute diets, but their ability to subsist

on weak nectar solutions seems superior to that of the

Bananaquit. Gurney’s Sugarbird (Promerops gurneyi;

Promeropidae), and most sunbirds (Nectariniidae) tested to

date (Whitebellied, Malachite [Nectarinia famosa], Black

[Nectarinia amethystina], and Palestine [Nectarinia osea]),

are able to balance energy losses by adjusting volumetric

intake of sucrose solutions ranging from 250 to 292 mM

(Downs, 1997, Nicolson and Fleming, 2003, McWhorter et

al., 2003). Likewise, Cinnamon-bellied Flowerpiercers

(Thraupidae) and all hummingbirds (Trochilidae) tested to

date (Broad tailed [Selasphorus platycercus], and Magnif-

icent Hummingbirds and Green-backed Firecrowns [Sepha-

noides sephaniodes]), compensate energetically at sugar

concentrations of 250–292 mM (Lopez-Calleja et al., 1997,

McWhorter and Martınez del Rıo, 1999, Schondube and

Martınez del Rıo, 2003). Lesser Double-collared Sunbirds

(Nectarinia chalybea), and the Australian Meliphagidae,

Western Spinebill (Acanthorhynchus superciliosis) and

Brown Honeyeater (Lichmera indistincta), have been

reported to compensate on 400 mM solutions, but they

were not tested on lower concentrations (Collins, 1981, Lotz

and Nicolson, 1999).

4.3. Water influx in relation to food concentration

Bananaquits were able to process water at high rates,

especially when feeding on dilute sugar solutions. The

average water influx rate of 6.8 mL in just 6 h (when

feeding on 276 mM sucrose solutions) was higher than

allometric predictions (6.5 mL/24 h; Williams et al., 1993)

for an 8-g bird. We explored the possibility that weak

nectars might be essential to sustain high water needs of

Bananaquits by allowing birds to control osmolarity of the

food. Bananaquits always minimized their water intake,

indicating that it is not essential to them to sustain high

water influx rates, and that on the contrary, large volumetric

food intakes pose a burden to them (see above). Nonethe-

less, evaporative water losses of nectarivorous birds increase

significantly with ambient temperature (Collins et al., 1990),

and decreasing water vapor density (Powers, 1992). Under

hotter and dryer conditions than those of our mild laboratory

environment, physiological water needs should be greater,

and preference for dilute nectars or drinking of free water

might become a necessity under wild conditions. In fact,

nectarivorous honeyeaters (Meliphagidae) are dependent on

drinking water in arid regions of Australia (Fisher et al.,

1972).

In another study that also provided supplementary water,

in addition to sucrose solutions, Whitebellied Sunbirds

significantly diluted the more concentrated foods (Nicolson

and Fleming, 2003; Fleming and Nicolson, 2003). In that

study, the range of sugar concentrations offered (70–2500

mM) was considerably broader than in ours, and White-

bellied Sunbirds drank large volumes of free water when

food concentration was above 1500 mM. Ingestion of

supplementary drinking water allowed to estimate a

bpreferred food concentrationQ of 1050 mM for Whitebellied

Sunbirds (Nicolson and Fleming, 2003). The range of sugar

concentrations used in our experiments was chosen to match

the range of nectars likely to be encountered by passerines

and hummingbirds in nature (12–30%; Baker, 1975), while

solutions offered to Whitebellied Sunbirds include extremes

normally beyond the range of natural nectars.

In conclusion, Bananaquits independently evolved a

number of functional traits convergent to those of other

specialized nectarivorous birds that allow them to subsist on

nectars from a broad array of flowers. They show a strong

preference for concentrated nectars but are able to use weak

solutions by processing large volumes quickly. Nonetheless,


on very dilute foods, their intake is limited by physiological

constraints related to water loading. The evidence suggests

that water bulk of dilute solutions is a burden to

Bananaquits, hence it is unlikely that they act as a selective

force for weak nectars of flowers.

Acknowledgments

Early stage of Bananaquit research was funded by a

postdoctoral fellowship to AM from FONACIT (No.

2001001306). CB was supported by the Decanato de

Investigacion y Desarrollo (S-CB-7) from Universidad

Simon Bolıvar. Thanks are due to R. Jaffe and L. Perera

who provided assistance with bird maintenance and data

collection. Tom Martin kindly provided the video cameras.

We gratefully acknowledge extensive comments and con-

structive criticisms by three anonymous referees. Birds were

handled under permit #41-0301 to AM by Oficina Nacional

de Diversidad Biologica (MARNR).

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