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First published online April 18, 2008
Journal of Experimental Biology 211, 1475-1481 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013268
Sugars are complementary resources to ethanol in foods consumed by Egyptian fruit bats
Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 84990 Midreshet Ben-Gurion, Israel
* Author for correspondence at present address: Facultad de Ciencias Ambientales, Universidad de Ciencias Aplicadas y Ambientales, Calle 222 # 55–37, Bogotá, Colombia, South America (e-mail: fasbos{at}gmail.com)
Accepted 10 March 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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1%). However, ethanol toxicity is apparently
reduced when ingested along with some sugars; more with fructose than with
sucrose or glucose. We predicted (1) that ingested ethanol is eliminated
faster by bats eating fructose than by bats eating sucrose or glucose, (2)
that the marginal value of fructose-containing food (food+fructose) increases
with increasing [EtOH] more than the marginal value of sucrose- or
glucose-containing food (food+sucrose, food+glucose), and (3) that by
increasing [EtOH] the marginal value of food+sucose is incremented more than
that of food+glucose. Ethanol in bat breath declined faster after they ate
fructose than after eating sucrose or glucose. When food [EtOH] increased, the
marginal value of food+fructose increased relative to food+glucose. However,
the marginal value of food+sucrose increased with increasing [EtOH] more than
food+fructose or food+glucose. Although fructose enhanced the rate at which
ethanol declined in Egyptian fruit bat breath more than the other sugars, the
bats treated both fructose and sucrose as complementary to ethanol. This
suggests that in the wild, the amount of ethanol-containing fruit consumed or
rejected by Egyptian fruit bats may be related to the fruit's own sugar
content and composition, and/or the near-by availability of other sucrose- and
fructose-containing fruits.
Key words: fructose, frugivory, glucose, marginal value of food, sucrose, toxins
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Janzen, 1977). These toxins
may reduce the nutritional value of food and therefore affect food selection
(Cipollini, 2000;
Harborne, 1993). However, the
toxicity of these compounds may also be reduced by nutrients present in the
same, or in a different, food item. Indeed, the increase in palatability of
toxin-containing food brought about by certain nutrients might be one of the
explanations why herbivores function better when offered combinations of
different foods than when fed single-food diets
(Freeland and Janzen, 1974).
Thus, toxins in plants and those nutrients that reduce their toxicity should
be treated as complementary resources
(Rapport, 1980;
Tilman, 1980) by herbivores
because, by ingesting these resources together, a forager would earn more
towards its fitness than by ingesting the toxin separately.
Ethanol is a potentially toxic compound often encountered by frugivorous
bats in their food. Ethanol occurs ubiquitously in fleshy fruit as a
by-product of the alcoholic fermentation of sugars mainly by micro-organisms,
but also by the fruit itself (Battcock and
Azam-Ali, 1998; van Waarde,
1991). Ethanol content increases as fruit ripens
(Dominy, 2004;
Dudley, 2004;
Sánchez et al., 2004),
suggesting that obligate frugivores, such as fruit bats, may consume
significant amounts of this alcohol. For example, ripe fruit eaten by Egyptian
fruit bats (Rousettus aegyptiacus, E. Geoffroy 1810) may contain
0.1 to 0.7% ethanol, whereas unripe and overripe fruit may contain lower
and higher concentrations, respectively
(Sánchez et al., 2004).
Our research on the effects of the presence of ethanol in artificial food on
the foraging behaviour of captive Egyptian fruit bats indicated that at low
concentrations (<1%) ethanol does not affect food selection, whereas at
high concentrations (1%) ethanol deters the bats
(Sánchez et al., 2004;
Sánchez et al., 2006).
In addition, the ingestion of artificial food containing 1% ethanol can impair
the flight skills of the bats (F.S., unpublished observations), i.e. food
containing 1% ethanol can be considered as aversive for these bats. Thus,
micro-organisms, via the ethanol they produce, may have negative
effects on fruit bat–plant interactions due to the toxic effects of
ethanol. Nevertheless, the presence of nutrients in fruit that complement
ethanol could modify its effects on food selection by fruit bats.
For example, sugars such as fructose, glucose and sucrose, all common in
fleshy fruits (Baker et al.,
1998) and, coincidentally, in the natural diet of Egyptian fruit
bats (Biner et al., 2007;
Nazif, 2002;
Van Handel et al., 1972),
reduce the toxic effects of ethanol in rats and humans
(Berman et al., 2003;
Mascord et al., 1991;
Roberts et al., 1999).
Moreover, independent experiments in rats and humans showed that, in both
species, elimination of ethanol from the blood was faster after ingestion of
fructose than after ingestion of sucrose or glucose
(Jones, 1983;
Parlesak et al., 2004).
In light of the above, we hypothesized that Egyptian fruit bats treat sugars and ethanol as complementary resources, but the degree of complementarity differs among sugars, being higher between fructose and ethanol than between either sucrose or glucose and ethanol. Since sucrose is hydrolysed into fructose and glucose, we further hypothesized that the complementarity between sucrose and ethanol would be higher than that between glucose and ethanol. Hence, we predicted that ethanol would be eliminated faster when the bats ate food containing fructose than when their food contained either sucrose or glucose.
Patch use theory can be used to determine whether a forager treats food
resources as complementary. In food patches where foragers experience
diminishing returns, the amount left in the patch after foraging, the
giving-up density (GUD), is related to the forager's quitting harvest rate
(Brown, 1988). The quitting
harvest rate is sensitive to the marginal value of the food patch, i.e. the
fitness value of an additional food item ingested by a forager
(Brown, 1992). Therefore, the
lower the GUD, the higher the marginal value of the food in the patch, and the
higher its expected contribution to fitness. Thus, GUD can be used to estimate
the marginal value of food to a forager, and also to evaluate nutritional
relationships among foods (Schmidt et al.,
1998). For example, Schmidt et al.
(Schmidt et al., 1998) showed
that when resources are perfectly substitutable, their marginal values remain
constant independent of their consumption, and they may be valued by the
forager depending only on energy content and handling time
(Pulliam, 1974). In contrast,
the marginal value of complementary food resources depends on the relative
amount of each that is consumed. Indeed, when two resources are mutually
complementary, the ingestion of one increases the marginal value of the other,
and vice versa. Nonetheless, in the case of toxin ingestion,
complementarity may not be mutual because by ingesting a toxin the nutrient
that complements it increases its marginal value, but not vice versa
(Whelan et al., 1998).
We predicted that the marginal value of fructose-containing food (food+fructose) increases with ethanol concentration, [EtOH], more than with sucrose- or glucose-containing food (food+sucrose; food+glucose). We further predicted that the marginal value of food+sucrose increases with [EtOH] more than that of food+glucose. We assumed that following changes in the marginal value of foods relative to their [EtOH] would reveal whether the bats treat sugars and ethanol as complementary resources, and used the difference between marginal values of sugar-containing foods with and without ethanol for this purpose (Table 1).
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In addition, we expected that the preference for fructose relative to sucrose or glucose would increase with [EtOH] in food, and the preference for sucrose relative to glucose would increase with [EtOH] in food.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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90% shade). Between experiments, we offered the bats
commercially produced fleshy fruit, such as melons, watermelons, bananas and
apples, ad libitum. [EtOH] in commercial fruits is highly variable,
and depends on fruit variety, conditions of storage and display at the market.
[EtOH] in these fruits is between 0.01% and 0.8%
(Ke et al., 1991;
Liu and Yang, 2002;
Senesi et al., 2005) [see also
Stevens, cited by Milton (Milton,
2004)], although higher values have been found. For example, only
2 days after optimum commercial maturity, some varieties of melon contain
4% ethanol (Senesi et al.,
2005). This research was done under permit 18150 from the Israel Nature and National Parks Protection Authority.
Ethanol in bat breath
Breath analysis has been widely used as a non-invasive technique to
estimate blood-ethanol in humans. Indeed, breath analysis provides a similar
pharmacokinetic profile of [EtOH] to that measured in venous blood. Namely,
these methods show similar patterns of ethanol elimination and their
measurements are highly correlated (Jones
and Anderson, 2003). This is because, after consumption, ethanol
distributes itself completely in body water, and well-vascularized organs,
such as brain, liver and lungs, may rapidly establish an equilibrium between
extra- and intracellular [EtOH] (Eckardt
et al., 1998). In addition, after oral ingestion of ethanol and
before equilibration among all tissue and extracellular compartments, [EtOH]
in the brain and arterial blood are higher than in less-vascularized tissues
such as muscle and peripheral veins
(Eckardt et al., 1998).
Therefore, breath [EtOH] more accurately reflects the level of central nervous
system exposure to this alcohol than [ETOH] in venous blood, particularly at
the outset of distribution of ethanol in blood and other tissues
(Eckardt et al., 1998). Thus,
we considered breath ethanol content as a relevant indicator to assess the
effects of ingested sugar on ethanol elimination in Egyptian fruit bats.
Furthermore, given that the method of analysis is non-invasive, it avoids the
trauma of serial blood sampling, which might harm the bats.
We prepared mixtures containing 1% ethanol, and fructose, sucrose or
glucose (200 g) in 1 l of distilled water. The mixtures were prepared no more
than 5 min before the beginning of each trial and were administered orally to
five adult males. We assumed that, as in humans, the likelihood of ethanol
intoxication in bats may be estimated based on blood volume
(Garriot, 2003). Therefore,
the volume of ethanol given to each bat was proportional to its total blood
volume, which is 7.2% of body mass
(Noll, 1979). Unfortunately,
to our knowledge, there is no information on ethanol metabolism in fruit bats;
thus, we also assumed that ethanol kinetics in humans and Egyptian fruit bats
was similar when estimating the intoxicating dose for each bat. For example,
for a 70 kg human with a 5 l blood volume, 9000 ml of a 1% mixture of ethanol
in water is necessary to increase blood alcohol content to a level of
intoxication, 0.15 g 100 ml–1
(Morris et al., 2006); thus a
0.14 kg fruit bat would require 18.5 ml of the same mixture to achieve a
similar blood alcohol content.
We measured ethanol levels in fruit bat breath with a gas chromatograph (GC; Scentoscreen, Sentex Systems Inc., Fairfield, NJ, USA) using argon as the carrier gas, and a column temperature of 130°C. Before the trials, we determined its retention time with ethanol standards and then measured ethanol levels in the breath of bats before administering a dose of ethanol and 5, 30, 50, 70, 90, 110 and 130 min thereafter. Between measurements, two samples of clean, dry air were run to ensure that no ethanol traces remained in the GC column. Breath samples were taken by placing the bat's snout at the end of a funnel connected to the GC sampling tube. The GC was programmed to pump samples for 10 s each time. We used the integrated area under the peak of the retention time of ethanol as a relative measurement of the ethanol content in the breath.
The marginal value of food containing ethanol and sugars
We used feeders as artificial food patches from which the bats experienced
diminishing returns (Sánchez,
2006), and measured the GUD of liquid food containing ethanol and
one of three different sugars. The liquid food contained 3 g of soy protein
infant formula (Isomil; Abbot Laboratories, Hoofddorp, The Netherlands), 0.66
g NaCl, 0.84 g KCl, and 0.584 mol sucrose (200 g) or 2x0.584 mol (210.5
g) of fructose or glucose, all dissolved in 1 l of distilled water.
The feeders were made of a cylindrical, plastic container (base diameter 6
cm; height 10 cm) with an opening big enough (diameter 6 cm) for the bats to
feed from, as described previously
(Sánchez, 2006). The
feeders were attached to the walls of the flight cages, and filled with liquid
food. To induce diminishing returns from the feeder, we placed an inedible
substrate made of 39 pieces of latex hose (each 20 mm long, 10 mm outer
diameter, 7 mm inner diameter) strung on fishing line in the feeder. The
fishing line was anchored to the bottom of the feeder to prevent removal of
the rubber pieces by the bats. The interference caused by the rubber pieces
forced the bats to work harder and harder as they removed food from the feeder
and had to push down on the rubber pieces in order to obtain more food while
going deeper into the feeder
(Sánchez, 2006). We
used this type of feeder in all experiments.
In these trials, we put five female bats at a time in one of the cages, and placed two feeders, containing different sugars, at each of three stations, i.e. a total of six feeders in the cage. At the same time, in another cage, we placed two feeders containing different sugars at each of four stations, i.e. a total of eight feeders in the cage, and introduced eight male bats at a time. In the cage of females, each feeder was filled with 75 ml of food, whereas in the males' cage each feeder contained 100 ml of food. We used different numbers of female and male bats because those were the numbers of each in the colony. The amount of food available for an individual male (8 feedersx100 ml/8 bats=100 ml per bat) was slightly greater than that for a female (6 feedersx75 ml/5 bats=90 ml per bat) to compensate for their larger size.
We offered the bats food containing fructose, sucrose or glucose, and
tested all pair-wise comparisons when the patches also contained either 0% or
1% ethanol, i.e. we did six pair-wise comparisons. The order of presentation
of each comparison was chosen randomly, and we repeated each experiment three
times. We provided the food shortly before sunset (18:30 h) and measured
the amount of food left in the feeders, i.e. the GUD, shortly after sunrise
(06:30 h). We did these experiments during the spring of 2006.
Estimated daily energy expenditure
Because we previously found that daily energy expenditure (DEE) affects GUD
in Egyptian fruit bats kept in outdoor cages
(Sánchez et al., 2008),
we assessed the possible influence of DEE here as well. Since the cages were
protected from the sun and wind, we assumed that the effects of direct solar
radiation and of convection were negligible, and used air temperature,
Ta, to estimate the metabolic rate of resting (day) and
active (night) bats with the equations of Noll
(Noll, 1979) (see below). We
observed that our bats were active for about 11 h per night and, of that, they
were in flight for some 8 min
(Sánchez et al., 2008).
Therefore, to estimate DEE, we assumed that the bats rested for 13 h during
their daytime, inactive phase, rested for 10 h 52 min in their night-time,
active phase, and flew for 8 min at a metabolic rate 14 times the active
resting rate (Thomas,
1975).
We measured Ta in the cages to ±0.5°C using
two Thermochron iButtons (DS1921 Maxim/Dallas Semiconductor Corp., Sunnyvale,
CA, USA), hanging 20 cm from the roof of the cages. We set the iButtons to
record Ta at 10 min intervals, and averaged the
measurements. Based on each average, we estimated the oxygen consumption
(
O2, in ml
g–1 h–1) by male and female bats whose body
masses were 130 and 150 g, respectively, during each 10 min interval using
empirically derived equations for bats acclimated to 15°C at rest during
the day
(O2=2.63–0.054Ta),
and active at night
(O2=6.73–0.134Ta)
[see table 2, p. 82 of Noll
(Noll, 1979)]. To obtain an
estimate of total daily
O2, which we
converted to DEE, we summed all estimates for 10 min intervals of a diurnal
cycle and added 3 ml O2 per gram of body mass for the 8 min of
flight.
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Statistical analyses
We analysed the measurements of ethanol in bat breath by repeated-measures
analysis of variance (RM-ANOVA), using breath ethanol content as the dependent
variable, bat as a random effect, and sugar type and time as fixed effects. We
used contrasts with a Bonferroni correction in a multiple comparison procedure
(Neter et al., 1996). We used
analysis of covariance (ANCOVA) to examine the effect of [EtOH] on the
marginal value of food containing different sugars for the bats, with
GUDFrc–GUDScr,
GUDFrc–GUDGlc or
GUDScr–GUDGlc as the dependent variable, [EtOH] as
a fixed effect, food station as a blocking factor, and thermoregulatory costs
entered as a covariant. We also examined the sugar preferences of the bats
using 95% confidence intervals based on Student's one-tailed t-tests.
As an index of preference we used GUDSugar A/GUDSugar
A+GUDSugar B. 
0.05 was chosen as the minimal
acceptable level of significance.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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[EtOH] and the marginal value of sugar-containing foods
Ethanol concentration affected the marginal value of the sugar-containing
foods for both female and male bats (Table
2), i.e. GUD increased with the addition of 1% ethanol to the food
(Fig. 2). Moreover, the
marginal value of foods containing different sugars changed owing to the
increase in [EtOH]. Indeed, by increasing [EtOH] in the food, the marginal
value of food+fructose decreased relative to food+sucrose
(Fig. 2A,B) and increased
relative to food+glucose (Fig.
2C,D). The marginal value of food+sucrose was higher than that of
food+glucose when [EtOH] increased (Fig.
2E,F).
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[EtOH] and sugar preferences
In general, female and male bats appeared to prefer sucrose over fructose
and glucose, and fructose over glucose, and when food contained ethanol these
preferences were accentuated (Fig.
3). When food did not contain ethanol, the bats did not show
significant differences in their preference for fructose or sucrose (Student's
one-tailed t-test, P>0.05;
Fig. 3A). However, when ethanol
was added, they significantly preferred sucrose over fructose (Student's
one-tailed t-test, P<0.05). The bats preferred fructose
over glucose when food contained either 0% or 1% ethanol (Student's one-tailed
t-test, P<0.05; Fig.
3B), although for the females there was no significant difference
with no ethanol (Student's one-tailed t-test, P>0.05).
Finally, the bats preferred sucrose over glucose when food contained either 0%
or 1% ethanol (Student's one-tailed t-test, P<0.05;
Fig. 3C).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In general, sugars affect ethanol kinetics by reducing gastric emptying,
which slows ethanol absorption (Schwartz
et al., 1996), and in doing so reduces the speed at which ethanol
reaches the bloodstream (Kricka and Clark,
1979). The `fructose effect', i.e. faster elimination of ethanol
in the presence of fructose than in presence of other sugars, has been
recognized for more than 50 years [Stuhlfauth and Neumaier, 1951, cited in
Tygstrup et al. (Tygstrup et al.,
1965)]; nonetheless, the underlying mechanism is not clearly
understood. During ethanol catabolism NAD is reduced to NADH, and the supply
of NAD might limit ethanol oxidation. It has been proposed that during
fructose metabolism NADH is transformed into NAD, and thus fructose increases
ethanol oxidation (Scholz and Nohl,
1976; Thieden et al.,
1972; Tygstrup et al.,
1965). However, this idea is not fully accepted yet
(Mascord et al., 1991).
Egyptian fruit bats assimilate fructose faster than glucose
(Keegan, 1977), and although
there is no information on sucrose assimilation in these bats, it is possible
that differences in the rate of assimilation of sugars may help explain their
effect on ethanol elimination.
The results of the present study suggest that Egyptian fruit bats are less
efficient at metabolizing ethanol than wild, frugivorous birds. For instance,
European starlings, Sturnus vulgaris, administered oral doses of
ethanol of 3 g kg–1 eliminated 100% of the alcohol within 130
min (Prinzinger and Hakimi,
1996). Waxwings, Bombycilla garrulous, administered
intravenous doses of ethanol of 2 g kg–1 eliminated almost
all the alcohol in 120 min (Eriksson and
Nummi, 1982). In contrast, the breath of Egyptian fruit bats that
had been given a relatively small oral dose of ethanol (0.13 g
kg–1) still contained three orders of magnitude more ethanol
than before administration after 130 min [before, 152681±85032, mean
± s.d.; after 130 min, 2.495(x106)±918123].
Even though there is little information in the literature on the ethanol
content of fruits consumed by birds and bats, at least in Israel, it seems
that birds and bats consume fruits that have a similar [EtOH]
(Sánchez et al., 2004).
So, there does not appear to be an a priori reason to expect that
frugivorous birds should metabolize ethanol more efficiently than frugivorous
bats. The fact that birds apparently do so suggests that they have an
advantage over bats when high quality, ripe fruit is scarce. This may be
because when ripe fruit is hard to find, frugivores may be in relatively poor
body condition and are, therefore, more likely to take the risk of ingesting
ethanol-rich fruit (Sánchez et al.,
2008).
In support of our predictions, the increase of [EtOH] in food raised the
marginal value of food+fructose and food+sucrose relative to food+glucose,
indicating that Egyptian fruit bats treated ethanol and sucrose, and ethanol
and fructose as complementary resources
(Schmidt et al., 1998).
However, contrary to our predictions, incrementing [EtOH] increased the
marginal value of food containing sucrose relative to food containing
fructose. These results suggest that, when confronted with ethanol-rich food,
the amount ingested by the bats depends, at least in part, on the sugar
content of the food item.
Although the increase in [EtOH] did not modify the rank order of sugar
preferences by Egyptian fruit bats, it augmented their preference for the
sugar with a higher marginal value when food did not contain ethanol. The
Egyptian fruit bats' preference for sucrose over fructose, and for fructose
over glucose, is similar to that of other Old World fruit bats, and this
pattern has been explained by the lower threshold for tasting sucrose than
fructose or glucose in these bats (Herrera
et al., 2000). The pattern of sugar preferences shown by female
and male bats was very similar; however, females did not appear to find
differences between fructose and glucose in ethanol-free mixtures, whereas
males did. The power of this particular comparative test for females was close
to 0.5, suggesting that to ascertain whether female and male bats really do
have different preferences for fructose and glucose requires that the sample
size be increased.
Another apparent difference between male and female bats was related to the
effect of DEE on the marginal value of sugar-containing foods. In females the
effect of DEE was significant for sucrose vs glucose, whereas for
males it was also significant for fructose vs glucose, but in
interaction with [EtOH]. No other comparison for either sex was significant.
Thus, it is unclear whether there are differences between the sexes for the
effect of DEE on the marginal value of sugar-containing foods in the presence
of ethanol. In addition, in a previous experiment, designed to determine the
effect of [EtOH] on the marginal value of artificial food in male Egyptian
fruit bats, the effect of DEE was also significant
(Sánchez et al., 2008).
This experiment was done in summer, thus the effect of DEE, and its
interaction with [EtOH], on the marginal value of food for the bats may also
be related to season.
How does ethanol modify the marginal value of sugar-containing foods for
Egyptian fruit bats? In humans, the perception of sweet, bitter and irritant
taste in mixtures containing different concentrations of sucrose varies with
[EtOH] (Nurgel and Pickering,
2006). Also, the perception of sweet and sour by humans in
mixtures with different [EtOH] changes with fructose concentration
(Zamora et al., 2006). In
light of this, since Egyptian fruit bats use flavour, i.e. taste and odour, to
assess food quality (Korine et al.,
1996; Sánchez et al.,
2006), it is likely that the changes in the marginal value of the
foods containing fructose, sucrose and glucose with the increase in [EtOH] for
the bats were a result of ethanol interacting differently with each of the
sugars and affecting the flavour of the foods in which they occurred.
The odour and taste of ethanol may be used by Egyptian fruit bats to
identify overripe, unpalatable fruit
(Sánchez et al., 2008;
Sánchez et al., 2006).
Thus, another explanation for our results is that the bats might perceive
fruit rich in ethanol and sucrose as food with lower levels of toxins than
fruit rich in ethanol and fructose or glucose. It is also possible that
sucrose-rich fruit contain other compounds that improve ethanol elimination,
that are not associated with fructose or glucose content. For example,
Lisander et al. (Lisander et al.,
2006) showed that in humans, infused amino acid mixtures improved
ethanol elimination better than infused equicaloric mixtures of glucose.
Our results on ethanol in bat breath, and on the marginal value of food
containing ethanol and sugars, intimate a contradiction between physiology and
behaviour. Specifically, although fructose enhanced ethanol elimination in
Egyptian fruit bat breath more than the other sugars, the bats treated sucrose
and ethanol as being `more' complementary than fructose and ethanol. This
discord implies that the bats did not identify the potentially beneficial
effects of ingesting fructose when food contained ethanol. Nonetheless, the
notable preference for sucrose-rich fruit by Egyptian fruit bats may be
advantageous with regard to ethanol consumption, since many wild fruits
consumed by pteropodid bats are rich in sucrose, and also have a higher
content of fructose than glucose (Baker et
al., 1998). In Israel, Egyptian fruit bats consume domestic (e.g.
persimmon Diospyros kaki, loquat Eriobotrya japonica) and
wild (e.g. date Phoenix dactylifera, carob Ceratonia
silicua) fruits (Korine et al.,
1998), which may have a high sucrose and fructose content
(Baker et al., 1998;
Biner et al., 2007;
Clark and MacFall, 2003;
Van Handel et al., 1972).
Thus, the preference for food+sucrose by Egyptian fruit bats could still be
beneficial for these bats when they eat ethanol-rich food.
Diet mixing in herbivores may have its roots in non-additive interactions,
e.g. complementarity, between the resources they consume
(Bjorndal, 1991). Fruits are
chemically complex resources (Cipollini,
2000), and this complexity is increased by the activity of
frugivorous micro-organisms, which may explain why some fruits are treated as
complementary by frugivorous vertebrates. Since the basis of nutritional
complementarity between resources, such as fruit, lies in the non-additive
interactions of particular compounds, examining these interactions may help to
explain patterns of food selection observed in herbivores. One of the possible
consequences of frugivores perceiving fruits as complementary resources is the
occurrence of `neighbourhood effects'
(Whelan et al., 1998). This
may be because food selection by a frugivorous forager, and the time spent
exploiting a patch, may depend on the diversity of fruiting plants occurring
in an area and their nutritional relationships. Thus, one might expect that
the amount of an ethanol-rich fruit ingested, or its rejection, by Egyptian
fruit bats could be related to the proximity of sucrose- and
fructose-containing fruits.
In summary, previous studies have recognized that micro-organisms can
reduce food quality and deter frugivores, and thus affect seed dispersal
(Borowicz, 1988;
Buchholz and Levey, 1990). We
have gone a step further to show that ethanol, a potential toxin produced by
fermentative micro-organisms, and sugars produced in fleshy fruit can interact
and affect food selection by Egyptian fruit bats. Our research suggests that
the influence of micro-organisms on the interactions between fruit-bearing
plants and frugivores is complex, and may depend on the individual effects of
compounds produced by micro-organisms on frugivorous animals and on the
interaction between these compounds and nutrients in the fruits.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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