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Comparative Biochemistry and Physiology, Part A 161 (2012) 344–348
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Comparative Biochemistry and Physiology, Part A
j ourna l homepage: www.e lsev ie r .com/ locate /cbpa
Sugar assimilation and digestive efficiency in Wahlberg's epauletted fruit bat(Epomophorus wahlbergi)
Colleen T. Downs ⁎, Babalwa Mqokeli, Preshnee SinghSchool of Biological and Conservation Sciences, University of KwaZulu-Natal, Pietermaritzburg. Private Bag X01, Scottsville 3209, South Africa
⁎ Corresponding author. Tel.: +27 33 260 5127; fax:E-mail address: [email protected] (C.T. Downs).
1095-6433/$ – see front matter © 2011 Elsevier Inc. Alldoi:10.1016/j.cbpa.2011.12.003
a b s t r a c t
a r t i c l e i n f oArticle history:Received 22 June 2011Received in revised form 5 December 2011Accepted 5 December 2011Available online 13 December 2011
Keywords:GlucoseSucroseVolumetric intakeEnergy intakeFrugivory
Fruit- and nectar-feeding bats have high energy demands because of the cost of flight, and sugar is a good fuelbecause it is easily digested and absorbed. This study investigated the digestive efficiency of different sugars atdifferent concentrations in Wahlberg's epauletted fruit bat (Epomophorus wahlbergi). We predicted that thesugar type and concentration would affect the total amount of solution consumed, while the total energy gainedand the apparent assimilation efficiency would be high, irrespective of sugar type or concentration. Equicaloricsolutions of two sugar types, glucose and sucrose, at low (10%), medium (15%) and high (25%) concentrationswere offered in separate trials to bats. Total amount of solution consumed, total energy gained from each solution,and apparent assimilation efficiency, were measured. Bats had higher total volumetric intake of glucose and su-crose at the low concentrations than at the higher concentrations. However, bats maintained similar total energyintake on the respective glucose and sucrose concentrations. Batswere found to have high assimilation efficiencieson both glucose and sucrose irrespective of concentration. As bats used both sugars efficiently to maximize andmaintain energy gain, it is expected that they feed opportunistically on fruit in the wild depending on temporaland spatial availability to obtain their energy requirements. Furthermore, fruit with high sucrose or glucose con-tent will be consumed.
© 2011 Elsevier Inc. All rights reserved.
1. Introduction
Soluble carbohydrates are a key reward in fruits and are reported toinfluence fruit choice in awide variety of vertebrate frugivores, includingbirds, bats and primates (Riba-Hernandez et al., 2003). Specifically, thereis evidence for selective preferences of particular sugars in frugivorousvertebrates (Herrera, 1999; Riba-Hernandez et al., 2003). It has beenwidely debated that the sugar composition of nectar in flowers orfruits reflects selection by animals that feed on them as opposed tothe phylogeny of the plant (Baker et al., 1998; Brown et al., 2010a,b;2011a,b). Animal-dispersed fruits reward their dispersers by fleshy fruitpulp and this in turn provides a primary source of energy for the frugivore(Lepczyk et al., 2000). However, it is unlikely that frugivore preferenceshave driven the evolution of these traits. Phylogenetic effects influencefruit traits more strongly than plant-disperser interactions (Jordano,1995) and evolutionary chronologies indicate that vertebrate frugivoreslagged behind the evolution of the major fruiting families they feed on(Fleming and Kress, 2011).
Sugar composition and concentration in fruit pulp varies amongdifferent plant species (Baker et al., 1998; Wilson and Downs,2011). Interestingly, frugivorous bats usually do not swallow thefruit pulp and seed, but remove the fruit juices before spitting out
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the pulp as ‘spats’. Consequently they are similar to nectarivores,while their ecological role is mainly dispersion and not pollination.
Energy balance, food intake rates, and digestive efficiency of sugarshave been widely studied in birds (Levey, 1987; Witmer, 1998;McWhorter and Martínez del Rio, 2000; Brown and Downs, 2003;Brown et al., 2010a,b, 2011a,b; Odendaal et al., 2010; and referencestherein), but relatively little in bats with only a few species studied(Roces et al., 1993; Herrera, 1999; Tracy et al., 2007; Voigt andSpeakman, 2007; Ayala-Berdon et al., 2008; Herrera and Mancina,2008; Welch et al., 2008; Amitai et al., 2010; Ayala-Berdon et al.,2011). Because of flight, bats have high energy needs compared withsimilar sized non-flying mammals (Roces et al., 1993; Voigt andWinter, 1999; Tracy et al., 2007; Voigt and Speakman, 2007; Amitaiet al., 2010). To sustain this need, nectarivorous and frugivorous batsregulate their intake of sugars in response to nectar sugar concentra-tion, and these sugars are relatively easily digested and absorbed andso a good fuel for flight (Suarez et al., 1990; Ayala-Berdon et al., 2008;Voigt and Speakman, 2007; Ayala-Berdon et al., 2011). Floral nectarsof New World plants consumed by bats vary in sugar concentrationfrom dilute (3%) to concentrated (33%), but average 20% (Roces et al.,1993; Baker et al., 1998; Rodriguez-Peña et al., 2007). Bats and birdsthat have a high sugar intake show similar digestive adaptations andconstraints (Welch et al., 2008).
To ingest hexose sugars (glucose and fructose) saves the delay ofhydrolyzing sucrose. However, intake of dilute solutions is more of alimiting factor with increased water intake that also results in
345C.T. Downs et al. / Comparative Biochemistry and Physiology, Part A 161 (2012) 344–348
decreased absorption rates of hexoses and decreased affinity of su-crase for its substrate sucrose (Ramírez et al., 2005; Herrera andMancina, 2008; Ayala-Berdon et al., 2008). Furthermore, with diluteconcentrations bats have to feed regularly and increase their volu-metric intake to compensate for the low sugar intake and to meettheir energy requirements (Herrera and Mancina, 2008; Ayala-Berdon et al., 2008, 2011).
Optimal foraging theory attempts to model the most efficient foodchoices an animal is most likely to make to gain the most energy fromfood at the lowest energy cost (Hixon, 1980; Worthington, 1989;Giraldeau, 2008). Generally, the assimilation efficiencies of bats arehigh and similar for the different sugar types as bats are able to me-tabolize all sugars efficiently (Herrera, 1999; Rodriguez-Peña et al.,2007; Tracy et al., 2007; Welch et al., 2008; Amitai et al., 2010).There is a rapid and efficient rate of digestion, in relation tocarbohydrate-rich meals, in frugivorous and nectarivorous bats(Tracy et al., 2007). It appears that most nectarivorous and frugivo-rous bats mostly consume a diet low in both fat and protein, butrich in simple carbohydrates that they catabolize directly (Roceset al., 1993; Amitai et al., 2010).
Wahlberg's epauletted fruit bat (Epomophorus wahlbergi; bodymass males 68.0–165.0 g; females 64.0–124.7 g; Monadjem et al.,2010) occurs in many parts of Africa including the eastern part ofSouth Africa and is known to feed on a variety of fleshy fruits and nec-tar of flowers (Skinner and Chimimba, 2005; Monadjem et al., 2010).Fruits of figs (Ficus sp.) are preferred in the wild (Fenton et al., 1985).These bats are found in savanna, woodland and forest margins wherethere are trees with fleshy fruits on them. They are also found in peri-urban areas with many trees (Monadjem et al., 2010). The bats ex-tract the juices and nutrients from fruit pulp in the buccal cavityand then generally discard the pulp, skin and seeds as “spats”(Skinner and Chimimba, 2005; Monadjem et al., 2010). This practiceof discarding fruit parts has been used by other mammalian frugi-vores to reduce the intake of fiber and tannins in fruit (Kendricket al., 2009).
The aim of the study was to investigate the effect of sugar type andconcentration on sugar intake and assimilation efficiency of E.wahlbergi.We predicted that the sugar type and concentration would affect thetotal amount of solution consumed, while the total energy gained andthe apparent assimilation efficiency would be high, irrespective ofsugar type or concentration. In addition E. wahlbergi intake rates of therespective solutions were determined.
2. Methods
E. wahlbergi were caught in mist-nets in Pietermaritzburg, SouthAfrica in late September and November 2009 under a permit fromEzemvelo KZN Wildlife. They were housed in outdoor aviaries(4.1×2.4×2m) at the animal house of the University of KwaZulu-Natal,with males and females in separate aviaries. Bats were individuallymarked with light-weight color-coded necklaces. Each evening batswere provided a maintenance diet of nectar (20% glucose, sucrose andfructose) and a selection of chopped fruit (mainly pear, banana andapple) and a supplement (Lory Life, CA, USA). Bats (n=6; 5 males, 1 fe-male) were transferred to a 25 °C constant environment room with a12L:12D and placed individually in cages (77×52×81 cm). Bats contin-ued to be fed as before, prior to each experiment.
Equicaloric solutions of two sugar types (sucrose and glucose) atthree concentrations, high (25%), medium (15%) and low (10%)(Brown et al., 2008) were offered to the bats (n=6) on differentnights respectively. Indigenous South African fleshy fruits are mostlyhexose dominant with a few being sucrose dominant (Wilson andDowns, 2011). Only one solution was available per night. Trialswere conducted every second night. At 15:30 h, prior to each eveningtrial, bats were weighed and transferred to smaller cages(38×41×38 cm) with trays containing liquid paraffin (±1 cm
deep) underneath each cage to collect excreta. They were providedwith a particular solution in a calibrated burette per cage at 18:00 hwith the onset of the scotophase. The initial amount of sugar solutionin each burette was recorded and thereafter recorded hourly until06:00 h, the onset of the photophase. Bats were then weighed andreturned to their bigger cages after 07:00 h. Total volume consumedwas converted to energy to determine energy intake with 1 mL of10% glucose=1.650 kJ, 1 mL of 15% glucose=2.475 kJ, 1 mL of 25%glucose=4.125 kJ, 1 mL of 10% sucrose=1.650 kJ, 1 mL of 15% sucro-se=2.475 kJ, and 1 mL of 25% sucrose=4.125 kJ as per Brown et al.(2008).
It was not possible to separate urine from feces as the output wasgenerally a clear fluid. Consequently after each trial, respective bat ex-creta were collected using a 0.5 mL syringe and volume determined,and then placed in Eppendorf vials and frozen at −18 °C until furtheranalyses. Sugar content of control samples of the different diets and ofexcreta were analyzed using an isocratic high performance liquid chro-matography (HPLC) system (LC-20AT; Shimadzu Corp., Kyoto, Japan)equipped with a refractive index detector (RID-10A; Shimadzu Corp.)and a 300 mm–7.8 mm Rezex RCM-Monosaccharide column (8 μmpore size; Phenomenex®, Torrance, CA, USA) according to Liu et al.(1999). Thereafter apparent assimilation efficiency (AE) was deter-mined correcting for volume consumed and excreted where AE=100×((mgmL−1 sugarin×volume ingested)−(mg mL−1 sugarout×volume of excreta))/(mg mL−1 sugarin×volume ingested) (Jacksonet al., 1998). As amount of sugar in excreta was low (see Results), itwas assumed that sugar excreted in the urine was negligible so excretasugar content reflected fecal output.
As the same six bats were used in all trials, comparisons betweeninitial and final body mass, volume intake rates, total volumetric in-take, total energy intake, and apparent assimilation efficiencies onthe respective diets were done using Generalised linear ModelRepeated-Measures Analysis of Variance (RMANOVA) with STATIS-TICA (Statsoft, version 7, Tulsa, OK, USA). RMANOVA was also usedto determine the total sugar volume ingested by each individual.Post-hoc Tukey HSD tests were conducted for total volumetric intakeand total energy intake.
3. Results
There was no significant difference in body mass when initial andfinal body mass comparisons were compared for the different diettreatments (RMANOVA: F(5, 25)=2.23, P=0.0834). The range inbody mass varied with initial of 101.7–109.9 g while final from101.2 to 109.8 g. Change in body mass (final–initial) showed nosignificant difference for the different diet treatments (RMANOVA:F(2, 10)=2.95, P=0.098, Fig. 1).
E. wahlbergi intake rates of the respective solutions varied withtime. Initial intake was high at 10% glucose and later decreased,while initial intake was low at 25% sucrose, increased over time, andlater decreased (Fig. 2). Although volumetric intake of bats changed,there was no significant difference in the volumetric intake ratewith time between the sugar concentrations when combined(RMANOVA: F(55,330)=1.09, P=0.315; Fig. 2).
Total volumetric intake of different sugar concentrations andsugar type of E. wahlbergi showed no significant difference (RMA-NOVA: F(2,10)=0.896, P=0.439). However, post-hoc Tukey testsshowed significant differences when comparing 10% glucose with25% glucose (P=0.039), 15% sucrose (P=0.025), and 25% sucrose(P=0.020) diets. Glucose and sucrose total volumetric intake de-creased with increased concentration, with greatest total volumetricintake at 10% for both glucose and sucrose (Fig. 3).
Total energy intake of E. wahlbergi between the respective diettreatments did not differ significantly for glucose nor sucrose (RMA-NOVA: F(2,10)=0.77, P=0.488, Fig. 4). Bats maintained total energyintake on the respective glucose and sucrose concentrations.
Vertical bars denote +/- standard errors
25%15%10%
Diets
-4
-3
-2
-1
0
1
2
3
Bod
y m
ass
chan
ge (
g da
y-1)
GlucoseSucrose
Fig. 1. Mean change (final–initial) in bodymass (±SE, n=6) (g) ofWahlberg's epaulettedfruit bat (Epomophorus wahlbergi) fed the different solutions of the respective sugartreatments.
10% 15% 25%Diet trials
0
10
20
30
40
50
60
70
80
Tota
l vol
umet
ric in
take
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l day
-1)
GlucoseSucrose
Fig. 3. Total volumetric intake (±SE, n=6) (mL day−1) of Wahlberg's epauletted fruitbat (Epomophorus wahlbergi) fed different types and concentrations of sugartreatments.
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Similarly, there was no significant difference in E. wahlbergi apparentassimilation efficiency between the sugar types at different concen-trations (RMANOVA: F(2,6)=0.122, P=0.887) (Fig. 5). Mean valuesranged 95.8–98.7% using the HPLC method correcting for volume in-take and in excreta.
4. Discussion
Body mass of E. wahlbergi did not change significantly with thedifferent sugar diets and this was further shown when change inbody mass was compared with sugar concentration and type. In ad-ditionwhen offeredwith both hexose and sucrose solutions in preferencetrials they maintained body mass above 5% (Coleman and Downs, inpreparation). Similarly, nectar-feeding phyllostomid bats body massremained constant despite feeding on a range of nectar concentrations,suggesting a behavioral compensation (Ayala-Berdon et al., 2008; 2009)as demonstrated by Ayala-Berdon et al. (2011). Several fruit- andblossom-eating chiropterans exhibit torpor or heterothermy as an energysaving mechanism during their inactive phase, or during periods of foodshortages (Bartholomew et al., 1964; Geiser et al., 2005; Riek et al.,2010). Similarly E. wahlbergi show heterothermy during their day-time inactive phase (Downs et al., in press). Storage of energy as
19h00 20h00 21h00 22h00 23h00 00h00 01h00 02h00 03h00 04h00 05h0006h00
Time (Hours)
-4
-2
0
2
4
6
8
10
12
14
16
Vol
umet
ric in
take
(m
l h-1
)
10%G15%G25%G10%S15%S25%S
Fig. 2. Volumetric intake rate (±SE, n=6) (mL h−1) of Wahlberg's epauletted fruitbat (Epomophorus wahlbergi) fed different sugar types and concentrations from18:00 h–06:00 h (Note G = glucose, S = sucrose).
fat is not optimal for a flying animal because converting energy toand from fat is energetically expensive, and more mass equals theneed for more energy to fly (Voigt and Speakman, 2007; Amitaiet al., 2010). Metabolizing exogenous carbohydrates directly topower their highmass-specific metabolic rate would save the energeticcosts involved in breaking down lipids if the energywas stored as fat forthe bats (Voigt and Speakman, 2007; Welch et al., 2008; Amitai et al.,2010).
E. wahlbergi volumetric intake rate was generally high in the firstfew hours of feeding and later decreased. Volumetric intake rate ofsome birds is also high in the first few hours of feeding and similarlydecreases with time particularly at higher concentrations (Downs,2000; McWhorter and Martínez del Rio, 2000; Brown et al., 2010b).
Animals' behavioral response caused by changes in nutritionalcontent in food has been named intake response (i.e. increases infood intake caused by reduction in nectar concentration). The intakeresponse has two possible scenarios: compensatory feeding andphysiological constraints (McWhorter and Martínez del Rio, 2000;Ayala-Berdon and Schondube, 2011). Compensatory feeding impliesanimals obtaining the same amount of energy when they consume
10% 15% 25%
Sugar concentration
20
30
40
50
60
70
80
90
100
110
120
130
140
Tot
al e
nerg
y in
take
(kJ
day
-1)
GlucoseSucrose
Fig. 4. Total energy intake (kJ day−1) (±SE, n=6) of Wahlberg's epauletted fruit bat(Epomophorus wahlbergi) on respective sugar nectar treatments.
Vertical bars denote +/- standard errors
25%15%10%Diets
92
93
94
95
96
97
98
99
100
101
App
aren
t ass
imila
tion
effic
ienc
y (%
) GlucoseSucrose
Fig. 5. Apparent assimilation efficiency (%) (±SE, n=6) of Wahlberg's epauletted fruitbat (Epomophorus wahlbergi) fed different solutions and concentrations of sugar usingthe HPLC method where volume ingested and excreted is accounted for.
347C.T. Downs et al. / Comparative Biochemistry and Physiology, Part A 161 (2012) 344–348
food of different concentrations. Alternatively, animals presentingphysiological constraints (e.g. the rate of sucrose hydrolysis by sucrasein nectar-feeding animals) are not able to achieve compensatory feed-ing because they obtain less energy when fed low food quality(McWhorter andMartínez del Rio, 2000; Ayala-Berdon and Schondube,2011). Generally animals showing compensatory feeding do not pre-sent physiological constraints, however it is dependent on the sugarconcentrationwith somebird species constrained at low concentrations(Brown et al., 2010a,b; 2011a,b). Bat species studied by Herrera andMancina (2008) and Ayala-Berdon et al. (2008 and 2009) presentedphysiological constraints that prevent them from maintaining a con-stant energy intake when fed concentrations were ≤15% (wt/vol) forboth hexoses and sucrose. So far, only one bat species, Choeronycterismexicana, is known to show compensatory feeding irrespective of con-centration (Ayala-Berdon and Schondube, 2011)when fed sucrose con-centrations ranging from 5 to 35% (wt/vol). Total volumetric intake ofE. wahlbergi at low concentrations of glucose and sucrose were highercompared with more concentrated solutions of the respective sugars.Similar to E. wahlbergi, when sugar concentration increases, manyavian nectarivores decrease volumetric intake to regulate energy intakeand bodymass (Downs, 1997; Brown et al., 2010a,b; 2011a,b; Odendaalet al., 2010). Intake (and consequently energy as the solutions wereequicaloric) of glucose was generally higher than sucrose at the respec-tive concentrations. Previously other studies have suggested that theanimals showing this trend are then limited by sucrose digestion(McWhorter andMartínez del Rio, 2000; Ayala-Berdon and Schondube,2011). However, in the current study E. wahlbergimaintained bodymassand their apparent assimilation efficiencies were high irrespective ofsugar type or concentration. Further research on their digestive enzymesmay provide insight intowhether digestive processes are affecting energybudgets.
Asmentioned, apparent assimilation efficiencies of E. wahlbergiwhenfed glucose and sucrose, irrespective of concentration, were relativelyhigh. This indicated that irrespective of sugar type, bats were able to ef-ficientlymaximize their energy gainwhen feeding onnectar. Neotropicalnectarivorous and frugivorous bats show similar higher assimilation effi-ciencies for all sugar types (Herrera, 1999).
Frugivorous bats play an ecological role as they pollinate flowersand disperse fruit seeds (Herrera, 1999), but relatively little isknown about the feeding ecology of E. wahlbergi. It is apparent thatthey used both glucose and sucrose efficiently to maximize and main-tain energy gain. Wilson and Downs (2011) found that most indige-nous South African fleshy fruits are hexose dominant with a fewbeing sucrose dominant (84% hexose dominant, with 50% being
fructose and 34% being glucose dominant; only 16% were sucrosedominant). Furthermore, these fleshy fruits were generally high inwater content and low in protein and lipid content (Wilson andDowns, 2011). Bats, therefore, are expected to feed according towhat is available in terms of fruits, irrespective of sugar type/content.Consequently it is expected that they feed opportunistically on fruitin the wild depending on its temporal and spatial availability to ob-tain their energy requirements. Furthermore, fruit with higher sucroseor glucose contentmay be favored to optimize foraging/feeding behavior.However, as relatively little is known about the feeding ecology ofE. wahlbergi in the wild and more research is required.
Acknowledgments
M. Brown, J. Coleman, G. Anderson, and S. Tesfay are thanked forguidance and practical assistance. The National Research Foundation,South Africa provided an honors bursary to BM.
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