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First published online March 2, 2006
Journal of Experimental Biology 209, 1058-1063 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02122
Sex differences in food intake and digestive constraints in a nectarivorous bird
1 Department of Biology, Faculty of Science and Science Education,
University of Haifa at Oranim, Tivon, 36006, Israel
2 Department of Animal Science, Faculty of Agricultural, Food and
Environmental Quality Sciences, The Hebrew University of Jerusalem, Rehovot
76100, Israel
* Author for correspondence at present address: School of Biosciences, Main Building, Park Place, Cardiff University, Cardiff CF10 3TL, UK (e-mail: markmans{at}cardiff.ac.uk)
Accepted 24 January 2006
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We fed a diet of equicaloric solutions of sucrose and a 1:1 mixture of glucose and fructose (hexose mixture) solutions to Palestine sunbirds (Nectarinia osea). When fed sucrose solutions, males had longer transit times but similar absorption efficiencies as females. Transit times, corrected for differences in body mass and food intake, were still longer in males than in females when fed on sucrose solutions. The sex-specific differences in transit time disappeared when the birds were fed the hexose mixture.
Our results suggest that males take longer to digest than females when fed on sucrose-rich nectars as opposed to hexose-rich nectars, and therefore can allow themselves a relatively lower digestive capacity. This may suggest sex-specific co-evolution of sunbirds within mixed plant communities, which have both sucrose- and hexose-rich nectar-producing plants. Furthermore, future studies on digestion in birds may pay attention to sex-specific differences.
Key words: absorption efficiency, foraging, Palestine sunbird, Nectarinia osea, sexual dimorphism, transit time
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Clarke et al.,
1998; Markman et al.,
2002; Markman et al.,
2004) and food selection (e.g.
Forero et al., 2002). Sex
differences in digestive functions, such as nutrient extraction, should be
more easily detected when males and females do not differ in the proportion
and amount of various consumed food items, as was found in American robins
(Turdus migratorius)
(Wheelwright, 1986).
Differences in digestive functions among species are frequently explained
by differences in body size (Ricklefs,
1996). Although sexual size dimorphism is widespread among birds
(Dunn et al., 2001), there is a
lack of knowledge concerning its potential effect on the differences in
digestive attributes between sexes within a bird species. Such differences may
have implications for the foraging behaviour, and therefore on the life
history traits, of a species.
In the present study, we specifically addressed the question of whether there are differences between male and female birds in their food intake and digestive traits. If so, can these differences be fully explained by differences in body mass between the sexes? We predicted that if food intake and digestive functions are only governed by body mass, then after controlling for body mass there would be no differences between the sexes with regard to volumetric food intake, food assimilation efficiency and gut transit time.
Nectar is a simple liquid food source
(Roxburgh and Pinshow, 2002)
containing various proportions of sucrose and hexoses
(Nicolson, 2002), and no
apparent sex-specific external processing of it, for example by different bill
shapes, is known to be needed. Therefore, sex-specific digestive traits are
ideal to be studied in nectarivorous bird species. Hence, we chose Palestine
sunbirds (Nectarinia osea), which show sexual dimorphism in body
mass, to test for possible sex-specific differences in digestion.
We primarily fed the sunbirds with sucrose solution because it is a common
sugar in the nectar of many plant species that sunbirds readily feed on
(Lotz and Nicolson, 1996).
Furthermore, sunbirds will need to use their intestinal disaccharidase
sucrase, which must hydrolyze sucrose into its components glucose and fructose
before absorption can occur
(Martínez del Rio,
1990; Martínez del Rio
et al., 2001; Karasov et al.,
1986). Therefore, we further predicted that if there are
sex-specific differences in digestion of sucrose, for example due to sucrase
activity, it will be seen when feeding the birds sucrose and not when feeding
them with a 1:1 mixture of glucose and fructose of the same concentration.
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Materials and methods |
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20% w/w) sucrose solution and (2) a 2.3% protein
(Isomil formula; Promedico Ltd, Zwolle, The Netherlands) in a 0.6 mol
l–1 (20% w/w) sucrose solution, which were presented to
the birds in commercial feeders ad libitum. In addition, the birds
were offered fruit flies (Drosophila sp.) twice a week. A week prior
to the experiments, each bird was housed separately in an experimental cage
(40x30x20 cm) for acclimatization. During that time they received
maintenance solutions (see above). The experiments were carried out during the
end of winter 2003; therefore, the birds were not in a breeding state.
Food intake and gut transit time
Hexose solutions have twice the total molarity of the sucrose solutions,
but values of experimental solutions are given throughout for the sucrose
equivalent (SE) solution to emphasise that the concentrations of hexoses and
sucrose were equicaloric (see Fleming et
al., 2004). Birds were fed diets, one diet at a time, of 0.3 mol
l–1 SE (10% w/w), 0.6 mol l–1 SE
(20% w/w), 1 mol l–1 SE (35% w/w) and 1.5 mol
l–1 SE (50% w/w) sucrose or 1:1 equivalent
glucose:fructose (hexose) solutions. The birds did not receive any
protein-sucrose solution or free water during this period. In order to allow
the birds to adjust to a given sugar solution, birds were offered the solution
for two days before the experiment started. To quantify the food intake by the
birds, two 5 ml syringes were offered as an ad libitum solution every
morning at the same time. The syringes were weighed before being placed in the
cages, and again one hour later. Later, at noon, the two syringes were removed
and another two 5 ml syringes were weighed before being offered to the birds,
and again one hour later. The order of the diets was randomised and all birds
were fed all diets. Body mass of each bird was recorded at the beginning of
the experiments.
Immediately after measuring the food intake of each bird on any given sugar
solution in the morning session, the birds were deprived of food for 30 min.
At the end of the food deprivation period, a 5 ml syringe with a red dye
solution (0.001 g E122 Carmoisine dye powder, a synthetic red azo dye, per ml
of sugar solution) was placed in the cages for 10 min, after which the clear
sugar solution was resumed. The transit time was measured as the time passed
from the beginning of drinking the dye solution to the first appearance of
red-coloured excreta on a piece of white paper placed at the bottom of the
cage. These time points were determined while observing the birds through
eye-size openings in a curtain, without apparent disturbance to the birds, and
timing each event with a stopwatch. Transit time was repeated again at noon of
the same day (following Downs,
1997) immediately after the noon food intake session. As there
were no significant differences in the transit times between morning and noon
sessions (for sucrose, males F1,48=0.95, females
F1,32=0.67; for hexose, males
F1,40=0.57, females F1,32=1.68; all
P>0.05), we used an average transit time per bird for further
analysis.
Apparent sugar absorption efficiency
While feeding the birds each of the four sucrose solutions, excreta were
collected over a period of two hours into trays filled with mineral oil, which
were placed beneath the cages. The trays were emptied and the excreta were
separated from the oil using centrifugation (Sorvall RC 5B plus, Wilmington,
DE, USA; 4068 g, 3 min). Sugar concentration in the nectar and
the excreta was measured by using a temperature-compensated refractometer
(Atago ATC-1E, Tokyo, Japan, 0–32%). The apparent sugar absorption
efficiency (AE*) was calculated as follows:
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).
Statistical analysis
The unit for analysis was always a data point for each bird, namely its:
(1) food intake per hour, (2) food transit time and (3) apparent sugar
absorption efficiency. Prior to analysis, apparent absorption efficiencies,
which are given as percentages, were normalized using an arcsine-square-root
transformation.
A two-sample t-test was performed to test for differences between
male and female body mass. We used Spearman correlations to test the effect of
sucrose and hexose mixture concentration on the volumetric food intake and
transit time for each sex. As birds were repeatedly fed on all the
concentrations, repeated-measures ANOVAs were applied to test for the effects
of sex and sugar concentration (of sucrose or hexose mixture solutions) on the
volumetric food intake and absorption efficiency
(Sokal and Rohlf, 1997).
However, in order to compare the non-linear curves of volumetric food intake
between the sexes we used the method offered by Motulsky and Ransnas
(1987). Repeated-measures
ANCOVAs were used to control for the effect of body mass (i.e. log body mass
used as a covariate) when testing for the effect of sex and sugar
concentration on the volumetric food intake and transit time.
Repeated-measures ANCOVAs were also used to control for the effect of
allometric body mass [log body mass0.25 (see
Karasov, 1990); used as a
covariate] when testing for the effect of sex and sugar concentration on
transit time.
We used three-way ANCOVA to control for the effect of food intake (i.e. as a covariate) when testing for the effects of sex, type of sugar (i.e. sucrose and 1:1 hexose mixture solutions) and sugar concentration on transit time.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Food intake
The relationships between food intake and sugar concentration were well
described by similar power functions for both sexes
(Fig. 1A,B). Sucrose
concentration had a significant effect on food intake (repeated-measures
ANOVA: F3,30=92.96, P<0.001), with volumetric
food intake decreasing significantly with sucrose concentration in both sexes
(Fig. 1A; for males
rs=–0.84, N=28, P<0.001; for
females rs=–0.80, N=23,
P<0.001). There were no significant differences in the volumetric
intake of sucrose solutions per hour between males and females, as detected by
comparing the two curves (Fig.
1A; F=0.86, P>0.05) following Motulsky and
Ransnas (1987).
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Transit time
The transit time for digesta was not affected by intake rate
(Table 1), when applied as a
covariate. There was a significant effect of sex on transit time
(Table 1), with males having
longer transit times than females on sucrose (58% longer when averaged across
the four sucrose concentrations; Fig.
2A; repeated-measures ANOVA, F1,10=73.175,
P<0.001) but having similar transit times to females when feeding
on the hexose mixture (Fig. 2B;
repeated-measures ANOVA: F1,9=0.05, P=0.82). Type
of sugar (i.e. sucrose or hexose mixture) had a significant effect on transit
time (Table 1). There was a
significant interaction term between sex and type of sugar
(Table 1), reflecting the fact
that although the females had shorter transit times when feeding on sucrose as
compared with the hexose mixture, in males it was the other way around with
shorter transit times on the hexose mixture, except for the 1.5 mol
l–1 SE where their transit time was shorter on the sucrose
solution (Fig. 2A,B).
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Both sexes significantly increased their transit time with increasing concentrations of both sugars (Table 1; once feeding on sucrose solution – males rs=0.89, N=28, P<0.001, for females rs=0.90, N=23, P<0.001; once feeding on hexose mixture solution – males rs=0.88, N=24, P<0.001, for females rs=0.85, N=20, P<0.001) in a similar way, as reflected by the non-significant interaction term between sex, sugar type and sugar concentration. There was a significant interaction term between type of sugar and sugar concentration, probably because while feeding on sucrose the increase in transit time was steady, as opposed to the hexose mixture, where at low concentrations (0.3 mol l–1 SE and 0.6 mol l–1 SE) transit time was almost constant but at higher concentrations (1 mol l–1 SE and 1.5 mol l–1 SE) it remarkably increased.
The transit times in males, while feeding on sucrose solutions, were significantly longer than in females even after using body mass as a covariate (repeated-measures ANCOVA, F1,9=103.3, P<0.0001) or allometric body mass (body mass0.25) as a covariate (repeated-measures ANCOVA, F1,9=103.8, P<0.0001). The transit time in males was not significantly different from that of females while feeding on the hexose mixture solutions, once we used either body mass (repeated-measures ANCOVA, F1,8=0.335, P=0.579) or allometric body mass as a covariate (repeated-measures ANCOVA, F1,8=0.305, P=0.596).
Absorption efficiency
Sunbirds of both sexes absorbed 98% of the sucrose, irrespective of the
concentration of the four solutions. There were no significant differences in
absorption efficiency between the males and females (repeated-measures ANOVA,
F1,12=1.63, P=0.226) or while the birds consumed
different sucrose concentrations (repeated-measures ANOVA,
F3,36=2.25, P=0.099). Previous work by Roxburgh
and Pinshow (2002) using
Palestine sunbirds as a model showed that their digestion efficiency on both
10% w/w (0.3 mol l–1 SE) and 50% w/w (1.5 mol
l–1 SE) of the hexose mixture was 99.2%; therefore, we did
not find a justification to test the digestive efficiency of our birds while
feeding on the hexose mixture.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), which tested his
predictions using greater double-collared sunbirds (Nectarinia afra).
Similar apparent patterns of food regulation by nectarivorous birds were
previously reported (e.g. Downs,
1997; Martinez del Rio et al.,
2001; Nicolson and Fleming,
2003), most recently in Palestine sunbirds
(McWhorter et al., 2003).
Both sexes seemed to be limited by digestion processes, as transit time
increased with increasing sugar concentration (see
Downs, 1997). The fact that
both sexes consumed the same amounts of sucrose solutions, contrary to the
fact that the males were significantly heavier and therefore expected to have
higher energy intake, may suggest that males were limited in their ability to
digest sucrose as compared with females. Indeed, males had longer transit
times on sucrose compared with females, even after correcting for food intake
and body mass. This means that the difference between transit times of males
and females cannot be explained fully by either allometry or food intake
rates, demonstrating sex-specific digestive responses.
The fact that the sex differences in transit time disappeared when fed on
the hexose mixture may suggest that the differences between the sexes while
feeding on sucrose are related to processes associated with the breakdown of
sucrose to monosaccharide, such as sucrase enzymatic activity. In light of
this, it might be that females possess more sucrase per cm2
intestine than do males and/or differ in any conditions that affect sucrase
activity, such as pH or temperature in the gut, or gut surface area. Such a
conclusion must be supported by further investigation of the sex-specific
sucrase activity. However, the combination of the supposedly lower enzyme
capacity of males and their longer gut transit time seem to be enough to
satisfy sugar digestion rates at normal levels, but if males were pressed to
increase their intake for some reason (e.g. higher needs for activity,
thermoregulation, etc.) they would have relatively lower capacity to digest
their food, as implied by the longer time that they had to keep the food in
their digestive system compared with females. Alternatively, it might be that
females are simply designed with relatively higher digestive capacity because
it is they, and not males, that must increase intake during egg production
(Pendlebury et al., 2004).
Females had shorter transit times while feeding on sucrose compared with when feeding on the hexose mixture, and males had shorter gut transit times when feeding on hexose mixture. As this can affect the capacity of the digestive system, it may mean different abilities to consume food. This can result in a possible difference in the use of sucrose-rich versus hexose-rich nectar-producing flowers by males and females. Such a difference between the sexes hints that there might be less competition between males and females if they feed on different types of nectar-producing flowers. This may be selected for in a situation where there are mixed plant communities that comprise both sucrose-rich and hexose-rich nectar-producing plants.
Assimilation efficiency (the proportion of the food or nutrient consumed
that is actually digested and absorbed) of nectarivorous birds as a function
of sugar concentration was previously studied
(Downs, 1997;
Jackson et al., 1998;
Roxburgh and Pinshow, 2002).
Our findings that both male and female Palestine sunbirds assimilated the
sugars in their food almost completely, regardless of sugar concentration, fit
the results of McWhorter et al.
(2003) and Roxburgh and
Pinshow (2002), which were
obtained from male Palestine sunbirds. The independency of assimilation
efficiency from sugar concentration was reported for other nectarivorous birds
as well (Karasov et al., 1986;
Martínez del Rio, 1990;
Jackson et al., 1998).
Assimilation efficiency is dependent on the nutrient content of the food,
gut surface area and volume, gut transit time, enzyme activity and the density
of transport proteins (Worthington,
1989; Karasov,
1990; Robbins,
1993). In our experiments, the nutrient content of the diet was
similar for both sexes. Further, gut transit time should be affected by gut
surface and volume. The last two traits are an allometric function of body
mass (Worthington, 1989;
Karasov, 1990). However, gut
transit time of males when fed on sucrose solutions was much longer than that
of females even after we controlled for body mass and food intake (see
Karasov, 1990). Hence, the much
longer food processing in the gastro-intestinal tract of males in order to
achieve the same assimilation efficiency as females might be beyond the sexual
differences in gut volume or surface area.
As a consequence of these high food intake rates relative to their body
mass, high extraction efficiencies and short transit times for digesta, both
sexes in Palestine sunbirds probably maximize their net energy gain on diets
of low and high sugar concentration solutions, as has also been shown in
malachite sunbirds (Nectarinia famosa), black sunbirds
(Nectarinia amethystina) and Gurney's sugarbirds (Promerops
gurneyi) (Downs, 1997).
However, the shorter gut transit time of females while feeding on sucrose
solutions, compared with males, raises the question of whether females, which
probably have relatively higher digestive capacity when feeding on sucrose,
are better in maximizing their net energy gain while feeding on sucrose-rich
nectars. To answer this question, further investigation is needed.
To conclude, the differences between males and females in transit times when fed on sucrose as opposed to when fed on hexose mixture call for: (1) more detailed description of the gastro-intestinal system of both sexes, especially because body mass-independent differences appear between the sexes, and (2) further studies looking into the ecological implications of possible diet segregation between sexes, while feeding on different nectar composition, and their effect on plant pollination. Therefore, we suggest that future studies might use sex as a factor in their analysis of digestive traits in birds.
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Acknowledgments |
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