Received: 6 December 2018  |  Revised: 18 March 2019  |  Accepted: 19 March 2019 DOI: 10.1002/ece3.5150 O R I G I N A L R E S E A R C H Seasonal variation in food availability and relative importance of dietary items in the Gambian epauletted fruit bat (Epomophorus gambianus) Kofi Amponsah‐Mensah1  | Andrew A. Cunningham2  | James L. N. Wood3  | Yaa Ntiamoa‐Baidu1,4 1Centre for African Wetlands, University of Ghana, Accra, Ghana Abstract 2Institute of Zoology, Zoological Society of 1. The Gambian epauletted fruit bat (Epomophorus gambianus) is very common London, London, UK across a variety of West African habitats, but very little information is available on 3Disease Dynamics Unit, University of Cambridge, Cambridge, UK its feeding ecology or its contribution to ecosystem function. 4Department of Animal Biology and 2. We investigated seasonal variation in food availability and the relative importance Conservation Science, University of Ghana, of dietary items used by this species in a forest‐savannah transitional ecosystem. Accra, Ghana Dietary items were identified from 1,470 samples of fecal and ejecta pellets which Correspondence had been collected under day roosts or from captured bats over a 2‐year period Kofi Amponsah‐Mensah, Centre for African Wetlands, University of Ghana, Accra, (2014–2015). Ghana. 3. Plant phenology studies illustrated strong seasonal correlations between fruiting Email: mak2kofi@gmail.com and flowering and rainfall patterns: Fruits were available throughout the year but Funding information with peaks of abundance during the rainy season, while flowers were mostly Ecosystem Services for Poverty Alleviation, Grant/Award Number: NE/J001570/1; abundant during the dry season. Epomophorus gambianus bats utilized fruit and Carnegie Corporation of New York‐ flower resources from 30 plant species. Although the plant species used depended University of Ghana Next Generation of Academics in Africa Project on seasonal availability, there were clear preferences for certain species. 4. Flowers were an important food source for this fruit bat species especially during the dry season, contributing up to 79% of dietary items when fruit abundance was low. Ficus fruits were also important food item for E. gambianus, constituting over 40% of all dietary samples identified. 5. Policy implications. Our results show the importance of flowers in the diet of E. gambianus and highlight this species as an important pollinator and seed dis‐ perser, including for economically and ecologically important plant species. These findings contribute to an improved understanding of the ecological importance and potential role of this species in the forest‐savannah transition ecosystem for the development of fruit bat conservation management strategies. K E Y W O R D S dietary composition, ecosystem function, feeding ecology, fruit bat This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2019;9:5683–5693. www.ecolevol.org  |  5683 5684  |     AMPONSAH‐MENSAH Et Al. 1  | INTRODUC TION Dietary studies can increase our understanding of the interrelationships between animals and their environment and how individual species af‐ fect and contribute to their ecosystems (Stier & Mildenstein, 2005). Fruit bats (Pteropodidae) are almost exclusively phytophagous, rely‐ ing extensively on fruits, flowers, and leaves (Aziz, Olival, Bumrungsri, Richards, & Racey, 2016; Marshall, 1985). Through their feeding in‐ teractions with plants, many fruit bat species provide vital ecosystem services and are, therefore, regarded as keystone species. The biology of bats, particularly their reproduction and migration, is influenced by the distribution and timing of food availability (Marshall, 1985), which varies across landscapes and seasons (Cumming & Bernard, 1997). The timing of fruiting/flowering is often irregular across landscapes, which makes it difficult to generalize findings (such as reproductive syn‐ chrony with food abundance) obtained from one landscape to others (Cumming & Bernard, 1997). The utilization of food resources is also not uniform among fruit bats, and some studies, for example Baker and F I G U R E 1  A Gambian epauletted fruit bat (Epomophorus Harris (1957), Marshall and McWilliam (1982) and Barclay and Jacobs gambianus). Credit: Kofi Amponsah‐Mensah (2011), have shown inter‐ and intraspecific variations in food utilization in some African members of the Pteropodidae. Very few studies have explored the relative use and importance bats) that roosts in trees within the town was the focus of this study. of different food items in the diet of fruit bats (Marshall, 1985; Stier The vegetation of the area is a transition between semi‐deciduous & Mildenstein, 2005). Most studies that explored the dietary re‐ forest and Guinea savannah woodland, but it has undergone sig‐ sources of fruit bats failed to quantify the relative use of identified nificant changes mainly due to agricultural use, timber exploitation, dietary resources, primarily providing lists of food items and appar‐ and human settlement, resulting in a heterogeneous landscape with ently assuming equal use (Stier & Mildenstein, 2005). The current remnant pockets of the original forest, regenerating secondary for‐ lack of knowledge on the relative use of food items limits efforts est and farm bush. The area experiences the wet semi‐equatorial cli‐ to assign trophic roles to fruit bats (Marshall, 1985), resulting in in‐ mate where rainfall occurs in a double maxima pattern (annual range adequate characterization of the importance of their roles in the 1,016–1,210 mm),but this is changing gradually to a single extended functioning of ecosystems. This limits our understanding of how rainy season (late April–October) and a 4–5 months dry season be‐ bats impact ecosystems at local or larger scales and how changing tween November and April (Ghana Statistical Service, 2014). The land use and habitat modifications affect bat populations (Stier & mean annual temperature is 29°C, ranging between 26 and 32°C. Mildenstein, 2005; Wood et al., 2012). Epomophorus gambianus (family Pteropodidae) is a medium 2.2 | Diet identification by fecal and ejecta sized fruit bat that is widespread throughout much of West Africa sample analysis (Figure 1). The species is commonly described as a generalist and op‐ portunistic fruit feeder that thrives well in degraded forests and a The dietary components of E. gambianus were identified from variety of human modified habitats. We studied the diet of this wide‐ collections of fecal and ejecta pellets under roosting and feed‐ spread species in a West African forest‐savannah transition ecologi‐ ing trees and from captured bats. Fecal samples were collected cal zone, and here, we describe the seasonal availability and relative by placing 1.5 × 1 m plastic sheets directly under day roosts of use of food items for this species. Our findings contribute to an im‐ E. gambianus during the early hours of the day (0500–0900 hr). proved understanding of the ecological importance and potential role To avoid repeated collection of fecal samples from the same in‐ of this species in the forest‐savannah transition ecosystem for the dividuals that could arise from splatters or discontinuous depo‐ development of fruit bat conservation management strategies. sition, feces that were within 5 cm and had same characteristics (color, texture) of already collected material were ignored (Stier & Mildenstein, 2005). Fresh ejecta pellets were collected under 2  | MATERIAL S AND METHODS feeding roosts within the study area. Fecal/ejecta sample collec‐ tion was done on two to three consecutive days in each sampling 2.1 | Study area month for 21 months. Data for this study were collected in Golokuati, a town located in the Bats captured through mist‐netting for other studies also pro‐ Volta region of Ghana (N 06°59.851′ E 000°26.218′) from January vided opportunities to collect additional samples and data on di‐ 2014 to December 2015. A large E. gambianus colony (ca. 5,000 etary sources for E. gambianus; trapping was done between 1900 AMPONSAH‐MENSAH Et Al.      |  5685 and 0500 hr using ground mist nets. Any whole or remnants of fruits All dietary materials were assumed to be equal; the calorimetric or or feces or ejecta pellets expelled by E. gambianus bats during the energetic content of dietary items was not determined in this study. process were collected opportunistically for the dietary study. Bats trapped were checked also for the presence of fresh pollen on their 2.3 | Estimation of monthly food resource nostrils or wings, or for remnants of flower parts in their mouths. availability and abundance, and the timing of food The occurrence of pollen/flower parts on the body or in the mouth resource abundance in relation to rainfall of a bat was used as a proxy for feeding on flower resources by that bat and was counted as a “flower resource” sample. To estimate availability and seasonal variations in food resources, We conducted informal interviews with local farmers to help lo‐ plants identified as being utilized by E. gambianus were monitored cate plants known to be utilized by bats in West Africa (Marshall, monthly for fruiting and flowering abundance. Fruit/flower abun‐ 1985) and also to identify plants which they knew to be utilized by dance was determined through visual estimation (Chapman et al., bats. Plants identified by the local farmers were monitored for visits 1992) by a single observer (KAM) throughout the study to maintain by E. gambianus to confirm their use as a food source. Other fruiting consistency and to increase internal validity. Fruit/flower abun‐ and flowering trees in the study area were also monitored for visits dance was estimated by a modification of the method described and feeding activity by E. gambianus bats. by Devineau (1999), which entailed categorization of flowering and Each ejecta and fecal sample was collected separately into a fruiting phases into four stages (0–3) with corresponding phenol‐ clean, new plastic bag using a wooden spatula. Latex gloves were ogy scores of 0, 0.09, 0.5, and 1 (Table 1). For each plant monitored, worn during fecal and ejecta pellet collection process. Each sample the total number of fruits and flowers on the plant was estimated collected was washed through a 0.3 mm sieve using tap water in each month. Monthly fruit/flower abundance per plant was then the field before examining for seeds, flower parts, and other food estimated as: (Total number of fruits/flowers present on the plant) particles with the aid of a handheld magnifying glass. A reference × (Phenology score) for each month. To account for unequal num‐ collection based on fruits and seeds, and their characteristics (color, bers of each plant species that was monitored, monthly fruit/flower smell, texture) of fruiting plants occurring in the study area was de‐ abundance was expressed as an average of the total number of veloped and used to identify the fruits and seeds collected from the plants monitored for each plant species. fecal and ejecta samples (Djossa, Fahr, Kalko, & Sinsin, 2008; Picot, We tested for an association between food availability and di‐ Jenkins, Ramilijaona, Racey, & Carriere, 2007; Stier & Mildenstein, etary use using spearman ranked correlation coefficient (ρ). We 2005). Seeds from up to five different species of fig that occurred used the estimated percentage of fruits/flowers that are matured at the study site were very similar and could not be identified to the on each monitored plant (as described in Table 1) as a measure of species level. Hence, all fig seeds from ejecta/fecal samples were food abundance rather than the estimated monthly total number of pooled together as “Ficus spp.” Each dietary material identified in fruits on each plant. We chose this measure of abundance because each fecal or ejecta sample was recorded to occur just once in that early fruiting/flowering stages of plants produce high numbers of sample (i.e., as presence only without quantification within a sam‐ fruits/flowers which are immature and not readily available for use ple) as it was impossible to quantify the number or quantity of par‐ by bats, therefore, using these estimates will produce false‐negative ticular food items within each fecal/ejecta sample collected. Both correlations. fecal and ejecta samples were treated as equal and dietary items To determine the timing of flower and fruit abundance in rela‐ identified from both were treated the same and pooled together. tion to rainfall within the study area, we related mean monthly fruit Dietary materials identified from samples were expressed as relative and flower abundance to the mean monthly rainfall for the study abundance (percentage) of total monthly samples collected, with the area. Rainfall data for the study area were obtained from the Ghana assumption that each sample collected was from an individual bat. Meteorological Agency (www.meteo.gov.gh). TA B L E 1  Categorization and description of flowering and fruiting stages of plants and their corresponding phenology scores used in quantifying fruit and flower abundance Estimated % of fruits/flowers Fruiting/flowering stage Stage description matured Phenology score 0 No flower/fruit present; or, if present, all flowers and 0 0 fruit dead and desiccated 1 Flower buds with less than 10% of flowers open; early 9 0.09 fruit setting with less than 10% of fruits matured 2 Flower buds present and 10% to 50% of flowers 50 0.5 opened; 10% to 50% of fruits matured size 3 Peak flower bloom with over 50% of flowers opened 100 1 peak of fruit maturity with over 50% of fruits fully matured 5686  |     AMPONSAH‐MENSAH Et Al. 3  | RESULTS example, Mangifera indica and Azadirachta indica, had two flowering periods; a major one in December/January and a minor one in June/ 3.1 | Food composition and relative abundance July (Figure 4). Flowers lasted for short periods and most flowering of food resources based on fecal and ejecta sample plants were devoid of flowers within a month of flowering. analysis Mean monthly rainfall in the study area was high over a continu‐ ous 7‐ to 8‐month period with peaks in June and October. These two A total of 1,470 samples of fecal and ejecta pellets were collected peaks in rainfall were separated by a short period of reduced rain in over the 21‐month sampling period, comprising 401 samples col‐ August and a 5‐month‐long dry season following the October peak lected from trapped bats, 505 ejecta pellets, and 564 fecal sam‐ (Figure 5). The main period of flower abundance occurred during the ples collected under day roosts. A total of 129 trapped bats were dry season, November to February, with a peak in December. A lower observed with fresh pollen on their bodies/nostrils and 866 fecal incidence of flowering occurred from April through to August with and ejecta samples collected contained seeds. Plant material in 42 minimum flower abundance around September–October. Compared fecal samples could not be identified and did not match any of the to flowers, fruits were relatively more available throughout the year, descriptions in the reference collection. These were not included in with a major peak in fruit abundance occurring in March and a minor the analysis. peak in October. Thirty species of plant, belonging to at least 16 families, were iden‐ tified in the E. gambianus fecal and ejecta samples examined (Table 2). Six species were utilized for their flowers only, 20 for their fruits, and 4  | DISCUSSION four for both fruits and flowers. Three to eight different food items were utilized in each month. There was no significant difference in 4.1 | Dietary composition the use of specific dietary items by the different sexes of E. gambi‐ anus that were trapped. Flower resources, together with fruits from The diet of E. gambianus within our study area in Ghana, West Africa, four plant groups, Vitex doniana, Anthocleista vogelii, Ficus spp., and was found to consist of 30 plant species from at least 16 families. Polyalthia longifolia, constituted over 80% of all dietary items identi‐ These results confirm the varied diet of this species (Boulay & fied. Ficus spp. were identified in over 40% of all samples collected Robbins, 1989; Marshall, 1985; Marshall & McWilliam, 1982). We and were utilized in all sampling months (Table 3). Fruits of Solanum were unable to identify only 42 samples from 1,470 that did not sp. and Melothria sp. were recorded in 11 and seven of the sampling match our reference collection, possibly because they were eaten months, respectively, but had low frequencies of 2.4% and 1.1% of the outside our sampling area; therefore, our results provide a conserva‐ total samples collected. Vitex doniana occurred most frequently in the tive estimate of the dietary sources available to E. gambianus in this diet of E. gambianus from August to October when the variety of food forest‐savannah transition zone. sources identified was low relative to the rest of the year. Fruits of With the exception of the family Cucurbitaceae, all of the A. vogelii and P. longifolia constituted significant proportions of the di‐ plant families we identified were already known to be eaten by etary items identified during March/April and May/June, respectively. fruit bats in West Africa (Marshall, 1985; Marshall & McWilliam, Flower resources were recorded in 10% of all samples collected and 1982; Mickleburgh, Hutson, & Racey, 1992; Rosevear, 1965). were most common from November to February. Fruits of Melothria sp. (family Cucurbitaceae) were identified in The use of most dietary items correlated strongly and positively about 1% of the total samples and in samples from seven months with their abundance (Figure 2) with fruits and flowers being used of the study. Although there is no record of this plant family as when they were available and abundant. The use of both Ficus spp. a food source of fruit bats in West Africa, Marshall (1985) lists and Solanum sp. however was weakly and negatively correlated to the fruits and leaves of Sechium sp., another member of the fam‐ their abundance. The use of Ficus spp. was mostly relatively higher ily Cucurbitaceae, as a food source for the bat genus Cynopterus than that of other food items with similar monthly abundances. in parts of Asia. Our observation of Melothria sp. in the diet of E. gambianus provides an addition to the extensive range of plant 3.2 | Timing of food resource abundance in relation species and families recorded as being utilized by fruit bats in to rainfall West Africa. Most food items identified as part of the diet for E. gambianus Twenty‐two plant species were monitored for the timing and abun‐ appeared generally to be linked to the seasonal availability of these dance of fruits and/or flowers. Fruits of many species, for example, food items within the study area, thus supporting the description Psidium guajava, Solanum sp., A. vogelii, and Ficus spp., were available of this bat species as an opportunistic feeder (Boulay & Robbins, throughout the sampling period but with varying fruit abundances 1989; Marshall, 1985; Marshall & McWilliam, 1982). Although sea‐ (Figure 3). The fruits of Sterculia rhinopetala, Antiaris toxicaria, and sonal availability may dictate the use of food resources in fruit bats, Milicia excelsa were not consistently available throughout the year. some species can also exhibit preferential diet selection. For ex‐ Flowering in most of the plants exploited by E. gambianus oc‐ ample, Baker and Harris (1957) described Eidolon helvum as prefer‐ curred once per year around December/January. A few species, for entially eating the flowers of Ceiba pentandra over those of Parkia AMPONSAH‐MENSAH Et Al.      |  5687 TA B L E 2  Plant species and their food resource identified as being consumed by Plant family Species Common name Food resource Source Epomophorus gambianus Anacardiaceae Spondias mombin Yellow mombin FR a,b,c Anacardium occidentale Cashew FR b,c Mangifera indica Mango FR a,b,c Annonaceae Polyalthia longifolia Indian mast tree FR a,b,c Annona muricata Soursop FR b,c Bignoniaceae Spathodea campanulata African tulip FL a,b tree Bombacaceae Bombax buonopozense Red silk‐cotton FL b Ceiba pentandra Silk Cotton FL a,b Caricaceae Carica papaya Pawpaw FR a,b,c Combretaceae Terminalia catappa Indian almond FR a,b,c Cucurbitaceae Melothria sp. Mouse melon FR a Fabaceae Daniellia oliveri African copaiba FL a,b balsam Parkia biglobosa African locust FL a,b bean Gentianaceae Anthocleista vogelii Cabbage tree FR, FL a,b Malvaceae Adansonia digitata Baobab FL b Sterculia rhinopetala Brown sterculia FR a Meliaceae Azadirachta indica Neem FR, FL a,b,c Moraceae Antiaris toxicaria False iroko, FR a,b Antiaris Ficus spp. (five species) Figs FR a,b,c Milicia excelsa Iroko, Odum FR a,b,c Musaceae Musa sp. Banana FR, FL a,c Myrtaceae Psidium guajava Guava FR a,b,c Syzygium sp. woodland FR a,b waterberry Solanaceae Solanum sp. Potato tree FR a,b Verbenaceae Vitex doniana Black plum FR a,b,c *  Unidentified FR, FL a Note. FL: flower; FR: fruit; source refers the origin(s) of information presented: a: current study; b: literature Marshall (1985); Marshall and McWilliam (1982); c: indigenous knowledge; *Unidentified trees. clappertoniana, when both were in flower. In the current study, 4.2 | Relative importance of food of different plant fruits of Solanum sp. and Melothria sp. were identified in the diet items in the diet of Epomophorus gambianus of E. gambianus during several months, but their overall relative abundance was less than 4% of samples. Fruits of Ficus spp. had Ficus spp. were represented in over a third of all samples and were a relatively high frequency of occurrence in dietary samples of up eaten in all months of this study, indicating that fruits from Ficus spp. to 52% in June–July when fig fruits were at the lowest abundance constitute an important component of the E. gambianus diet. The and as many as nine other food items were available. Thus, fruits genus Ficus is an important source of food in the diet of other frugiv‐ of Ficus spp. may be preferred over other food items and searched orous animals, including over 20 genera of fruit bat (Mickleburgh et for during the period of low fig fruit abundance. This implies the al., 1992), so it is not surprising that it featured in the diet of E. gam‐ preference for some dietary items over others or use in hierarchi‐ bianus in the current study. Ficus fruits might be an important source cal manner, where some food items may only be supplementary to of food because multiple species occur with an asynchronous fruit‐ more preferred ones. This would support Marshall's suggestion that ing phenology, resulting in fruits being widely available throughout E. gambianus and most other fruit bats could be spatio‐temporal “se‐ the year (Barclay & Jacobs, 2011; Shanahan, So, Compton, & Corlett, quential specialists,” with a preference for some food items among 2001). Our observations are consistent with this; Ficus spp. fruits those available, rather than true generalists (Marshall, 1985). were available throughout the study period. Ficus fruits contain high 5688  |     AMPONSAH‐MENSAH Et Al. TA B L E 3  Monthly relative use (%) of dietary items identified from Epomophorus gambianus fecal and ejecta pellets over a 21‐month period. No data were collected in September and October 2014 and January 2015 Month/frequency of occurrence (%) Jan Feb Mar Apr May Jun Jul Aug Nov Dec Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Dietary Item 2014 2015 Anthocleista 49 64 15 1 2.9 17 1.6 18 24 3.2 vogelii Antiaris 5.7 toxicaria Azadirachta 23 1.9 1.6 1.3 3.6 16 3.2 1.9 indica Carica papaya 6.3 2.8 Ficus spp. 31 2.7 26 32 8.3 4 29 24 45 51 6 64 75 6.3 18 52 35 12 39 47 22 Flower 41 79 5.8 33 4.3 26 13 62 resources Insect parts 3.3 Mangifera 2.8 3 14 4.3 3 indica Melothria sp. 6.9 1.5 3.1 1.4 6.7 7.6 6.7 Milicia excelsa 1.1 4.5 2.6 Musa sp. 3.8 Polyalthia 69 27 6.3 25 47 6.5 longifolia Psidium 12 19 2.9 2 16 4.7 guajava Solanum sp. 4.2 1.5 4.7 4.2 2.9 3.2 6.6 3.5 4.8 2 14 Spondias 7.6 mombin Sterculia 1.3 rhinopetala Vitex doniana 3.3 46 6.3 6.5 47 78 52 13 1.6 others 2.7 12 17 7.6 3.8 4.4 9.7 4.7 4.8 Number of 4 2 5 3 5 5 8 6 7 5 6 6 5 7 5 8 6 4 4 5 4 dietary resources AMPONSAH‐MENSAH Et Al.      |  5689 F I G U R E 2  Correlations between the abundance and use of dietary items of Epomophorus gambianus. Spearman ranked correlation coefficient (ρ) values are indicated beside species/food items. Abundance is expressed as the percentage of the estimated fruits/flowers that are matured per tree. The use of dietary items is expressed as the number of times that dietary item is recorded in total monthly fecal collections. Only dietary items that were detected in the diet of the bats in three or more sampling months were used. One outlier value for Ficus spp. (use = 288, abundance = 37.5) not shown on graph levels of calcium relative to other fruits (O'Brien et al., 1998), so late pregnancy (March and September) and parturition (April/May their year‐round availability could be important for the maintenance and October/November) reported for E. gambianus in West Africa of the bats' health, including for pregnant and lactating females (Thomas & Marshall, 1984). Thus, these two plant species together (Barclay & Jacobs, 2011). with Ficus spp. could be important dietary items during such vital Other fruits that may play vital roles in the diet of E. gambianus stages in the reproduction of E. gambianus. include those of V. doniana and A. vogelii. These fruits accounted for While fruit bats usually feed mostly on fruits, flowers also con‐ significant proportions of the diet of E. gambianus, which suggests stitute important dietary items (Marshall, 1985). However, very few preferential selection of these fruits over other food items when studies have assessed the extent of flowers in the diet of fruit bats. available. Fruits of V. doniana have a higher protein content (72.8– In our study, flower resources contributed over 9% of the dietary 82.4 g/kg) (Agbede & Ibitoye, 2007; Vunchi et al., 2011), compared items identified. In the dry (“lean” fruiting) seasons, flowers contrib‐ to P. guajava and Ficus spp. (22.2 and 24.6 g/kg, respectively; Ruby, uted up to 79% of dietary items, although our analyses did not allow Nathan, Balasingh, & Kunz, 2000) and, thus, V. doniana fruits may us to estimate the proportion of calorific intake in different months. be preferred over other available fruits. The availability and use of We identified the flowers of at least 10 plant species as being utilized the fruits of V. doniana and A. vogelii coincides with the periods of by E. gambianus, all of which have been reported previously as food F I G U R E 3  Estimated mean monthly fruiting abundance of plant species whose fruits were identified to be consumed by Epomophorus gambianus. Abundance is estimated as the total number of fruits × monthly phenology score per tree 5690  |     AMPONSAH‐MENSAH Et Al. F I G U R E 4  Estimated mean monthly flowering abundance of plants whose flowers were identified to be utilized by Epomophorus gambianus. Abundance is estimated as total number of flowers × monthly phenology score per tree sources for other fruit bat species in West Africa (Baker & Harris, plays an important subsistence rather than a supplementary role in 1957; Marshall, 1985; Marshall & McWilliam, 1982; Mickleburgh et the diet of E. gambianus. The flowers of C. pentandra for instance al., 1992). are reported to be an important food source for bats in Madagascar Because flowering and fruiting periods for most of the monitored during the dry season (Andriafidison et al., 2006), where flowers plants were asynchronous, we assumed that bats observed with from a single tree could sustain a large chiropteran community over a fresh pollen on their nostrils and/or wings had visited these plants short period (Gribel, Gibbs, & Queiroz, 1999). Flowers can contribute purposely to feed on nectar and/or pollen from their flowers. Some considerable amounts of dietary protein (Law, 1992a; Long & Racey, trapped bats had both pollen and fruit items collected from them 2007; Nelson, Miller, Heske, & Fahey, 2000; Ruby et al., 2000), sup‐ (n = 18 bats), but in majority of these cases (n = 17) the identified plementing the low protein content of most fruits (Barclay & Jacobs, fruits were from plants which were not flowering at that time, hence 2011; Marshall, 1985; Ruby et al., 2000; Stier & Mildenstein, 2005). supporting our assumption. Peaks in flower abundance and the use Although E. gambianus was observed to visit flowering trees of flower resources occurred mostly during the dry season when and several trapped bats were covered in pollen, we could not fruit abundance was lowest. This suggests that the use of flowers confirm if these bats were actively eating pollen, nectar, or both. The importance of pollen in the diet of E. gambianus is unclear. Boulay and Robbins (1989) stated that there was no evidence to support E. gambianus feeding on pollen, based on the absence of pollen in analyzed gut contents (Baker and Harris (1957). Happold (2013) also suggests that this species visits flowers for their nectar but not the pollen. However, Pteropodidae bats may lick pollen directly from anthers during feeding (Marshall, 1985) or ingest it during grooming of fur dusted with pollen after visiting plants to feed on nectar (Law, 1992b). Pteropus spp. may actually feed and depend on pollen as an important food source (Long & Racey, 2007; Marshall, 1985; Mickleburgh et al., 1992). Andriafidison et al. (2006) report that in Madagascar, over 40 percent of the 118 plant taxa that have been identified as part of the diet of Pteropus rufus and Eidolon dupreanum were identified from pollen in feces. They suggested that the contribution of pollen and nectar to the diet of fruit bats may be largely underestimated and the low re‐ porting of pollen in the diet of bats could be due to a surveillance bias or methodological constraints. We were not equipped to carry F I G U R E 5  Abundance and the timing of flowering and fruiting out microscopic analysis of pollen; therefore, further studies of the in relation to mean monthly rainfall. Combined mean monthly fruit pollen content of feces are needed to confirm its importance as a and flower abundance over 2 years were used dietary material in fruit bats. AMPONSAH‐MENSAH Et Al.      |  5691 4.3 | Timing of food resources during this period likely makes this bat species an important pollina‐ tor of forest and fruit trees, such as C. pentandra, D. olivieri, P. biglo‐ Food availability for African fruit bats is constrained by rainfall as bosa, A. vogelii, and B. buonopozense. fluctuations in fruit abundance are tied to rainfall patterns (Cumming Several food plants utilized by E. gambianus, including M. excelsa, & Bernard, 1997; Happold & Happold, 1990; Rautenbach, Kemp, & B. buonopozense, Ficus spp., S. campanulata, and C. pentandra, are im‐ Scholtz, 1988). Fruit phenology studies show an abundance of fruits portant pioneer species of the forest‐savannah transition ecological during the rainy season, while flowering occurs in the preceding dry zone (Hawthorne & Gyakari, 2006). These plants contribute sub‐ season (Frankie, Baker, & Opler, 1974; Janzen, 1967). Our findings stantially to ecosystem biomass, and fruits of plants like Ficus spp. are consistent with this pattern; however, our findings demonstrate provide food for birds and mammals (Kunz, Braun de Torrez, Bauer, that fruits are available throughout the year, but with peaks in fruit Lobova, & Fleming, 2011; Shanahan et al., 2001). Other plants, such abundance occurring at the onset of, or during, the rainy season. Each as Solanum sp., Ficus capensis, and A. vogelii, are important species fruiting period occurred a month or two after the flowering period. during early succession stages of forestation (Swaine & Hall, 1983). In drier areas of Africa, with stronger seasonal variations in rainfall, By spreading the seeds of these species, therefore, E. gambianus seasonality in fruiting and flowering may be more pronounced, caus‐ likely plays an important role in the maintenance and regeneration ing fruits to be less available throughout much of the year (Cumming of forest vegetation, and the persistence of original forest plant spe‐ & Bernard, 1997). In such areas, peaks in flower abundance might cies. This role could be especially important when considering cur‐ play an even more important role in the diet of frugivorous bats dur‐ rent levels of forest degradation and loss. ing periods of low fruit abundance. In addition to helping to maintain forest ecosystem function, the The timing and seasonality of food abundance are particularly feeding activities of E. gambianus appear to provide several direct important to the timing of reproduction in fruit bats (Cumming & and indirect benefits to people. Some of the plants that are likely to Bernard, 1997; Happold & Happold, 1990), where birthing is timed be pollinated and dispersed by E. gambianus have high economic im‐ such that food is available for juveniles after they are weaned portance. Tree species, such as M. excelsa, B. buonopozense, S. rhino‐ (Cumming & Bernard, 1997; Fleming, Hooper, & Wilson, 1972). In petala, and C. pentandra, have economic importance in Ghana, being West Africa, annual bimodal peaks in parturition for E. gambianus exploited for timber and other uses (Hawthorne & Gyakari, 2006). In occur in April/May and in October/November (Thomas & Marshall, particular, M. excelsa is heavily exploited to the extent that it is now 1984). Lactation lasts about 7–13 weeks (Nowak, 1999; Thomas & threatened by overexploitation in Ghana (Hawthorne & Gyakari, Marshall, 1984), implying that the first annual postweaning period 2006; Taylor, Kankam, & Wagner, 2000). for E. gambianus occurs around June/July, coinciding with a period Fruits of plants, such as V. doniana, S. mombin, Syzygium sp., and of availability of both flowers and fruits. The second postweaning P. guajava, are sold and consumed locally and contribute to the diet period occurs around December/January, which coincides with the and income of people, especially rural dwellers across West Africa. observed major peak in flower abundance. These observations sug‐ Even though plants like M. indica, P. guajava, and Anacardium occi‐ gest that flowers might have an important role in supporting the dentale are cultivated on large scales and may no longer rely on bats maintenance and growth of newly weaned bats. for their dispersal or pollination, fruit bats such as E. gambianus re‐ main relevant for the maintenance of the genetic diversity of their 4.4 | Importance of Epomophorus gambianus to wild types (Kunz et al., 2011). The services provided by E. gambianus ecosystem services through its foraging highlight the importance of this species (and fruit bats in general) to the ecosystems in which they occur. Evidence Seeds from several of the fruits identified as part of diet of E. gam‐ of these services, such as those presented in this study, therefore, bianus were small enough to be easily swallowed undamaged during should be used to inform the public and policymakers to promote the feeding, retained in the gut of the bats and identified in the fecal conservation of E. gambianus and other fruit bat species. samples collected. Even larger seeds that are not swallowed can be carried and dropped some distance from the parent plants. Over ACKNOWLEDG MENTS 58% of fecal samples collected contained seeds of Ficus spp., M. ex‐ celsa, A. vogelii, Solanum sp., P. guajava, and Melothria sp. These seeds This work was part‐funded by the Carnegie Corporation of New identified in the samples collected did not appear different in size, York‐University of Ghana Next Generation of Academics in shape, and morphology from those collected from whole fruits as Africa Project and the Ecosystem Services for Poverty Alleviation part of the reference collection. By feeding on these fruits, E. gam‐ grant number NE/J001570/1. James Wood is supported by the bianus plays a vital ecological role in the successful dispersion of ALBORADA Trust. Ethical approval was granted by The Institutional seeds of these plants. Fruit bats are reported to be responsible for Review Board of the Nogouchi Memorial Institute of Medical the dispersion of seeds from at least 156 species of plants (Fujita Research (CPN:002/13‐14). We would like to express our gratitude & Tuttle, 1991). During the dry season, when flowers are relatively to Mr. Alfred Ali of the Centre for African wetlands, University of more abundant, the increased utilization of flowers by E. gambianus Ghana for his assistance in the field. 5692  |     AMPONSAH‐MENSAH Et Al. CONFLIC T OF INTERE S TS Djossa, B. A., Fahr, J., Kalko, E. K., & Sinsin, B. A. (2008). Fruit selection and effects of seed handling by flying foxes on germination rates of The authors declare that there are no conflict of interests. Shea trees, a key resource in northern Benin, West Africa. Ecotropica, 14, 37–48. Fleming, T. H., Hooper, E. T., & Wilson, D. E. (1972). Three Central AUTHORS’ CONTRIBUTIONS American bat communities: Structure, reproductive cycles and movement patterns. Ecology, 53, 555–569. YNB conceived the ideas; YNB and KAM designed methodology; Frankie, G. W., Baker, H. G., & Opler, P. A. (1974). Comparative pheno‐ KAM collected the data, analyzed the data, and led the writing of logical studies of trees in tropical wet and dry forests in the low‐ the manuscript; YNB, AAC, and JLNW obtained the funding; AAC, lands of Costa Rica. Journal of Ecology, 62, 881–913. https://doi. org/10.2307/2258961 JLNW, and YNB supervised the research, reviewed and edited the Fujita, M. S., & Tuttle, M. D. (1991). Flying foxes (Chiroptera: manuscript. All authors contributed critically to the drafts and gave Pteropodidae): threatened animals of key ecological and eco‐ final approval for publication. nomic importance. Conservation Biology, 5, 455–463. https://doi. org/10.1111/j.1523‐1739.1991.tb00352.x Ghana Statistical Service (2014). 2000 Population and housing census, dis‐ DATA ACCE SSIBILIT Y trict analytical report: Techiman North District assembly. www.stats‐ ghana.gov.gh. Accra, Ghana: Ghana Statistical Service. Dryad https://doi.org/10.5061/dryad.8sk41pc. Gribel, R., Gibbs, P. E., & Queiroz, A. L. (1999). Flowering phenology and pollination biology of Ceiba pentandra (Bombacaceae) in Central Amazonia. Journal of Tropical Ecology, 15, 247–263. https://doi. ORCID org/10.1017/S0266467499000796 Happold, D. C., & Happold, M. (1990). Reproductive strategies of Kofi Amponsah‐Mensah https://orcid. bats in Africa. Journal of Zoology, 222, 557–583. https://doi. org/0000‐0002‐8625‐1681 org/10.1111/j.1469‐7998.1990.tb06014.x Happold, M. (2013). Epomophorus gambianus Gambian epauletted fruit Andrew A. Cunningham https://orcid. bat. In D. Happold, & M. Happold (Eds.), Mammals of Africa (pp. 242– org/0000‐0002‐3543‐6504 243). London, UK: Bloomsbury Publishing. James L. N. Wood https://orcid.org/0000‐0002‐0258‐3188 Hawthorne, W., & Gyakari, N. (2006). Photoguide for the forest trees of Ghana: A tree‐spotter's field guide for identifying the largest trees. Yaa Ntiamoa‐Baidu https://orcid.org/0000‐0002‐3915‐3341 Oxford, UK: Oxford Forestry Institute, Department of Plant Sciences. Janzen, D. H. (1967). Synchronization of sexual reproduction of trees within the dry season in Central America. Evolution, 21, 620–637. R E FE R E N C E S https://doi.org/10.1111/j.1558‐5646.1967.tb03416.x Kunz, T. H., Braun de Torrez, E., Bauer, D., Lobova, T., & Fleming, Agbede, J. O., & Ibitoye, A. A. (2007). Chemical composition of black plum T. H. (2011). Ecosystem services provided by bats. Annals of (Vitex doniana): an under‐utilized fruit. Journal of Food, Agriculture & the New York Academy of Sciences, 1223, 1–38. https://doi. Environment, 5, 95–96. org/10.1111/j.1749‐6632.2011.06004.x Andriafidison, D., Andrianaivoarivelo, R. A., Ramilijaona, O. R., Law, B. S. (1992a). The maintenance nitrogen requirements of the Razanahoera, M. R., MacKinnon, J., Jenkins, R. K. B., & Racey, P. A. Queensland blossom bat (Syconycteris australis) on a sugar/pol‐ (2006). Nectarivory by endemic malagasy fruit bats during the dry len diet: is nitrogen a limiting resource? Physiological Zoology, 65, season. Biotropica, 38, 85–90. 634–648. Aziz, S. A., Olival, K. J., Bumrungsri, S., Richards, G. C., & Racey, P. A. Law, B. S. (1992b). Physiological factors affecting pollen use by (2016). The conflict between pteropodid bats and fruit growers: Queensland blossom bats (Syconycteris australis). Functional Ecology, Species, legislation and mitigation. In C. C. Voigt, & T. Kingston 6, 257–264. (Eds.), Bats in the anthropocene: Conservation of bats in a changing Long, E., & Racey, P. A. (2007). An exotic plantation crop as a key‐ world (pp. 377–426). Cham, Switzerland: Springer International stone resource for an endemic megachiropteran, Pteropus rufus, in Publishing. Madagascar. Journal of Tropical Ecology, 23, 397–407. https://doi. Baker, H., & Harris, B. (1957). The pollination of Parkia by bats and its org/10.1017/S0266467407004178 attendant evolutionary problems. Evolution, 449–460. Marshall, A. G. (1985). Old World phytophagous bats (Megachiroptera) Barclay, R. M., & Jacobs, D. (2011). Differences in the foraging behaviour and their food plants: a survey. Zoological Journal of the Linnean of male and female Egyptian fruit bats (Rousettus aegyptiacus). Society, 83, 351–369. https://doi.org/10.1111/j.1096‐3642.1985. Canadian Journal of Zoology, 89, 466–473. tb01181.x Boulay, M. C., & Robbins, C. B. (1989). Epomophorus gambianus. Marshall, A. G., & McWilliam, A. N. (1982). Ecological observations Mammalian Species, 1–5. https://doi.org/10.2307/3504318 on epomorphorine fruit bats (Megachiroptera) in West African Chapman, C. A., Chapman, L. J., Wangham, R., Hunt, K., Gebo, D., & savanna woodland. Journal of Zoology, 198, 53–67. https://doi. Gardner, L. (1992). Estimators of fruit abundance of tropical trees. org/10.1111/j.1469‐7998.1982.tb02060.x Biotropica, 24, 527–531. https://doi.org/10.2307/2389015 Mickleburgh, S. P., Hutson, A. M., & Racey, P. A. (1992). Old World fruit Cumming, G., & Bernard, R. (1997). Rainfall, food abundance and timing bats. An action plan for their conservation. Gland, Switzerland: IUCN. of parturition in African bats. Oecologia, 111, 309–317. https://doi. Nelson, S. L., Miller, M. A., Heske, E. J., & Fahey, J. G. C. (2000). org/10.1007/s004420050240 Nutritional consequences of a change in diet from native to agricul‐ Devineau, J.‐L. (1999). Seasonal rhythms and phenological plasticity tural fruits for the Samoan fruit bat. Ecography, 23, 393–401. https:// of savanna woody species in a fallow farming system (South‐west doi.org/10.1111/j.1600‐0587.2000.tb00296.x Burkina Faso). Journal of Tropical Ecology, 15, 497–513. https://doi. Nowak, R. M. (1999). Walker's mammals of the world. Baltimore, MD: org/10.1017/S0266467499000978 John Hopkins University Press. 1936. AMPONSAH‐MENSAH Et Al.      |  5693 O'Brien, T. G., Kinnaird, M. F., Dierenfeld, E. S., Conklin‐Brittain, N. L., in Milicia excelsa, a threatened West African hardwood. In J. R. Wrangham, R. W., & Silver, S. C. (1998). What's so special about figs? Cobbinah, & M. R. Wagner (Eds.), Research advances in restoration Nature, 392, 668. of Iroko as a commercial species in West Africa (pp. 29–39). Kumasi, Picot, M., Jenkins, R. K., Ramilijaona, O., Racey, P. A., & Carriere, S. M. Ghana: Forestry Research Institute of Ghana (FORIG). (2007). The feeding ecology of Eidolon dupreanum (Pteropodidae) in Thomas, D., & Marshall, A. (1984). Reproduction and growth in three eastern Madagascar. African Journal of Ecology, 45, 645–650. https:// species of West African fruit bats. Journal of Zoology, 202, 265–281. doi.org/10.1111/j.1365‐2028.2007.00788.x https://doi.org/10.1111/j.1469‐7998.1984.tb05954.x Rautenbach, I. L., Kemp, A. C., & Scholtz, C. H. (1988). Fluctuations in Vunchi, M. A., Umar, A. N., King, M. A., Liman, A. A., Jeremiah, G., & availability of arthropods correlated with microchiropteran and avian Aigbe, C. O. (2011). Proximate, vitamins and mineral composition predator activities. Koedoe, 31, 77–90. https://doi.org/10.4102/koe‐ of Vitex doniana (black plum) fruit pulp. Nigerian Journal of Basic and doe.v31i1.486 Applied Science, 19, 97–101. Rosevear, D. R. (1965). The bats of West Africa. London, UK: Trustees of Wood, J. L., Leach, M., Waldman, L., MacGregor, H., Fooks, A. R., Jones, the British Museum (Natural History). xvii, +, 418. K. E., … Cunningham, A. A. (2012). A framework for the study of zoo‐ Ruby, J., Nathan, P. T., Balasingh, J., & Kunz, T. H. (2000). Chemical notic disease emergence and its drivers: spillover of bat pathogens as composition of fruits and leaves eaten by short‐nosed fruit bat, a case study. Philosophical Transactions of the Royal Society of London Cynopterus sphinx. Journal of Chemical Ecology, 26, 2825–2841. B: Biological Sciences, 367, 2881–2892. Shanahan, M., So, S., Compton, S. G., & Corlett, R. (2001). Fig‐eating by vertebrate frugivores: a global review. Biological Reviews, 76, 529– 572. https://doi.org/10.1017/S1464793101005760 How to cite this article: Amponsah‐Mensah K, Cunningham Stier, S. C., & Mildenstein, T. L. (2005). Dietary habits of the world's larg‐ est bats: the Philippine flying foxes, Acerodon jubatus and Pteropus AA, Wood JLN, Ntiamoa‐Baidu Y. Seasonal variation in food vampyrus lanensis. Journal of Mammalogy, 86, 719–728. https://doi. availability and relative importance of dietary items in the org/10.1644/1545‐1542(2005)086[0719:DHOTWL]2.0.CO;2 Gambian epauletted fruit bat (Epomophorus gambianus). Ecol Swaine, M. D., & Hall, J. B. (1983). Early Succession on cleared for‐ Evol. 2019;9:5683–5693. https://doi.org/10.1002/ece3.5150 est land in Ghana. Journal of Ecology, 71, 601–627. https://doi. org/10.2307/2259737 Taylor, D. A. R., Kankam, B. O., & Wagner, M. R. (2000). The role of the fruit bat, Eidolon helvum, in seed dispersal, survival, and germination