Flowers are ubiquitous in primate environments, yet their nutritional advantages are underexamined. Symphonia globulifera is a widely distributed tree exploited by a variety of animals in Africa and the Americas. We collected S. globulifera flower samples consumed by red-tailed monkeys (Cercopithecus ascanius) and compared them nutritionally to flower samples from other plant species in Kibale National Park, Uganda. Flowers were assayed for three fiber fractions (NDF, ADF, lignin), fat, crude protein, acid detergent insoluble nitrogen (ADIN), ash, and soluble sugars. We estimated available protein, total nonstructural carbohydrates (TNC), and metabolizable energy (ME). We calculated the mean and standard deviation for all nutrient categories and applied nutritional geometry to illustrate the balance among the energetic gains from available protein, fat, fiber, and TNC across flower species. Our results suggest that S. globulifera flowers provide an unusually high fat resource (14.82% ± 1.41%) relative to other flowers (1.38% ± 5.79%) and other foods exploited in the same habitat.
Florivory occurs ubiquitously among primates, having been documented in 165 primate species, yet comprises less than 10% of the annual food intake in most taxa (Heymann, 2011) contributing to why its nutritional benefits are poorly understood. Coevolutionary interactions between flowering plants and primates contributed to the adaptive radiation of primates (Sussman, 1991) and are facilitated by their high frequencies of arboreal locomotion (Heymann, 2011). Indeed, it has been proposed that protein acquisition via red leaves in Afro-Eurasian primates and red figs in Central and South American primates was a driving feature in the evolution of trichromatic vision (Valenta and Melin, 2012). Food resource (hereafter resource) selection models have been applied to investigate why primates select certain foods for consumption and are primarily based on acquiring certain nutrients while minimizing others (see Felton et al., 2009). Animal foraging is often adjusted to meet specific nutritional goals based on fluctuating nutritional needs in tandem with food nutrient content and food availability (Lambert and Rothman, 2015). Liebig’s Law of the Minimum posits growth is determined by the scarcest resource even when other essential nutrients are abundant, known as limiting factors (Salisbury, 1991). Specific macronutrients are known to be limiting factors in environments depending on the nutritional variability of that environment; for example, protein has been shown to be a limiting factor for frugivorous primates (Ganzhorn et al., 2009). Detecting nutritionally limiting factors can reveal mechanisms of resource limitation and has implications for primate conservation and health (Hanya and Chapman, 2013). Evaluating macronutrient balance in foods helps characterize specific constraints influencing food selectivity.
Symphonia globulifera (Clusiaceae) is a medium to tall sized (∼30 m) evergreen tree and aerial roots associated with wetter environments (Bittrich and Amaral, 1996; Dick et al., 2003). S. globulifera is used by people to treat a variety of medical conditions (reviewed in Fromentin et al., 2015) including coughs, fever, jaundice, and intestinal parasites in Uganda (Ssegawa and Kasenene, 2007); scabies in Gabon (Akendengué and Louis, 1994); parasites in Cameroon (Lenta et al., 2007); skin disease, diabetes, and malaria in Nigeria (Ajibesin et al., 2008); body pain and skin conditions in Panama (Gupta et al., 2005); and is ranked among the most important medicinal plants by indigenous peoples of Brazil (Prance et al., 1987). The root bark displays strong antiplasmodial properties that may aid in the development of new antimalarial drugs (Marti et al., 2010). The ethnopharmacological significance of S. globulifera has been substantiated by the phytochemical identification of various secondary metabolites validating its antiparasitic and antimicrobial uses (Fromentin et al., 2015).
Monkeys are attracted to flowering S. globulifera by its vibrant red floral displays (Gautier-Hion et al., 1985). Madagascar is the geographic origin of the genus and the island is home to 16 endemic Symphonia species (Germeraad et al., 1968). However, only S. globulifera is found outside of Madagascar, with a wide distribution throughout tropical Africa and the neotropics (Bittrich and Amaral, 1996; Dick et al., 2003). Flower morphology and physiology are consistent with a “bird pollination syndrome” in that trees exhibit diurnal flowering, produce relatively large quantities of dilute nectar, are odorless, and pollinated primarily by hummingbirds (Bittrich and Amaral, 1996) and perching birds (Gill Jr et al., 1998). Axillary inflorescences contain between 1-17 flowers, with 1-3 flowers at anthesis at a time (Gill Jr et al., 1998). Flowers stay fully open for one day and petals begin to wither thereafter. A large tree generates between 100 to 200 new blooms every day during peak flowering (Bittrich and Amaral, 1996). Previous nutritional analyses of S. globulifera have found that flowers and nectar are high in hexose sugars (i.e., glucose plus fructose) (Gill Jr et al., 1998), thus offering a plentiful albeit patchy high-energy resource when seasonally available (Porter, 2001).
Plant foragers can positively or negatively influence plant reproductive success through florivory (Chapman et al., 2013). Frugivorous-faunivorous primates often consume nectar and other flower parts more frequently than whole flowers (Heymann, 2011). Several neotropical primate species have been documented feeding specifically on the nectar of S. globulifera including spider monkeys (Ateles geoffroyi) (Riba-Hernández and Stoner, 2005), brown capuchins (Cebus apella), woolly monkeys (Lagothrix lagotricha) (Peres, 1994), tamarins (Saguinus fuscicollis, Saguinus mystax) (Garber, 1988), and squirrel monkeys (Saimiri sciureus) (Lima and Ferrari, 2003). S. globulifera flowers and nectar are also consumed by red-tailed monkeys (Cercopithecus ascanius) (Struhsaker, 2017; Bryer, 2020), red colobus (Piliocolobus badius) (Dominy and Lucas, 2001), grey-cheeked mangabeys (Lophocebus albigena) (Rothman, unpubl. data), and blue monkeys (Cercopithecus mitis) (Kaplin et al., 1998; Bryer, 2020) in East Africa.
Exploring the nutritive advantages of flowers and their parts (buds, stalks, nectar, oil) offers insight into the nutritional choices made by primates. Our study examines the benefits of florivory by addressing the following questions: what is the nutritional significance of S. globulifera flowers in the diet of primates, and how does the nutrient composition of this flower compare to other flowers and major food categories?
Material and methods
Study site and species
This study was conducted at the Kanyawara site, in Kibale National Park, western Uganda (0°13-0°41N and 30°19-30°32E), a 795 km2 mid-altitude (1500 m) evergreen forest, with bimodal rains and high interannual rainfall variability (Chapman et al., 2018). Red-tailed monkeys (C. ascanius) are common at this site, with a mean group size of 19.18-23.30 and primarily occupy old-growth forests and areas experiencing mild anthropogenic disturbance (i.e., lightly logged), with their abundance decreasing in heavily logged areas (Chapman et al., 2021) S. globulifera flowers (N = 63) were collected from May-July, 2017 coinciding with the dry period of longest duration annually.
MAHB and three field assistants estimated nutritional intake of adult female redtail monkeys (Bryer, 2020) by conducting continuous focal follows (aiming for full-day focal follows from 7:00 to 19:00) of adult females in three groups (N = 8 focal females per group) from May 2015 to January 2017 (20 months). Feeding was defined as beginning with ingestion of a food item into the mouth and ending when the female stopped chewing and switched to another activity. Plant species and part were recorded along with a count of the number of items eaten.
Plant collection and handling
We collected whole, freshly fallen flowers of S. globulifera (N = 63 samples; N = 7 trees) from the base of focal trees in spring 2017 (fig. 1). We placed flowers into inert plastic bags and immediately transported them to the field station for desiccation using methods described in Rothman et al. (2012). Each individual sample comprised multiple flowers weighing 20 g dry weight, each from a single focal tree.
Additionally, S. globulifera flower part samples (N = 1 flower; N = 1 flower stalk) and samples (N = 36) from twelve other flower species consumed by red-tailed monkeys in 2015-2017 were collected by MAHB and a field team; these included: Erythrina abyssinica, Funtumia africana, Hoslundia opposita, Lantana camara, Maesa lanceolata, Millettia dura, Piper capense, Psychotria sp., Randia sp., Strychnos mitis, Tabernaemontana pachysiphon, and Urera cameroonensis (see Bryer 2020 for details). Samples were dried in the field. Dried samples were ground in a Wiley Mill with 1 mm screen (Thomas Scientific) and then exported to Hunter College of the City University of New York’s Nutritional Ecology Laboratory where a portion of the field dried samples were re-dried at 105°C to calculate % dry matter.
Chemical analyses, nutrient calculations, and statistical analysis
The right-angled mixture triangle
Fat composition was highest in S. globulifera flowers and flower stalks in comparison to flowers, flower stalks, and flower buds from all twelve other plant species consumed by red-tailed monkeys (table 1). Flowers of any species accounted for 5.0% of daily kcal intake and represent 3.6% of the time spent feeding over the 20 months and two flowering events, which demonstrates flowers are a relatively rare though potentially energetically valuable resource (fig. 2).
Right-angled mixture triangles indicate that S. globulifera flower nutritional composition is uniquely high in fat content compared to samples (N = 36) from the other flower species consumed by redtail monkeys (fig. 3) and other principal resources (ripe fruit N = 89; unripe fruit N = 104; insects N = 6; young leaves N = 308) that are low fat (fig. 4). A minority of fruit parts consumed by red-tailed monkeys contain more fat than S. globulifera flowers: these species of fruits include Celtis gomphophylla (referred to in previous literature as Celtis durandii) ripe fruit and unripe fruit, which is known to be a fatty fruit species in primate diets in Kibale (Worman and Chapman, 2005); Erythrococca sp. ripe fruit; Macaranga sp. seeds of ripe fruit; Lindackeria sp. seeds of ripe fruit; and Maesa lanceolata unripe fruit. The sum of TNC + fat is more dispersed along the y-axis with less distinction between S. globulifera and other flower species (fig. 5) than when fat is considered independently (fig. 3). The flower portion of the plant is unique in this fat content, as indicated by the lower fat content of the S. globulifera flower stalks compared to flowers (table 1). Collectively, our results suggest S. globulifera is an infrequently exploited resource yet provides an unusually high source of fat and thus energetic payoff.
We determined the macronutrient concentrations of S. globulifera, a resource exploited irregularly by red-tailed monkeys (fig. 2) and found these flowers had a high fat composition compared to all other flower species (fig. 3). The high fat content resembled some insects (specifically caterpillars) and was heavily clustered in high fat compared to other food categories with more variable fat content (e.g., ripe, and unripe fruit) (fig. 4). We found S. globulifera was lower in sugars than expected (fig. 5, table 1) in contrast to high hexoses reported by Gill Jr et al. (1998). This suggests that primates could be targeting S. globulifera more for its fat content opposed to TNC or other nutrient combinations. Fat serves as an available energy store for primates (Thompson, 2013), with the caloric value of high fat foods surpassing that of protein, carbohydrates, and energetic returns from fiber (NRC, 2003). Flowers were exploited less often than other food categories (fig. 2) yet provided more energy in the form of fat than anticipated for an intermittent resource. Fatty acids are composed of long-chain hydrocarbons acting as essential dietary components for primates since no biochemical pathways produce these molecules (White, 2009). Essential fatty acids prevent and mitigate common diseases, notably coronary heart disease, and aid in critical cellular functions by serving as the structural components in the phospholipid membranes of tissues, particularly the brain and eyes (Connor, 2000).
Fruits can contain higher lipid content than other plant tissues and have been shown to provide the majority of essential fatty acids intake (44.8%). The diet of red-tailed monkeys is low in fat, with the average daily fat intake 10% of metabolizable energy, though daily intake of fat varies widely (Bryer, 2020). Red-tailed monkeys obtain the most fat from resources such as Celtis gomphophylla unripe and ripe fruit, and some insects (Bryer, 2020). Sympatric grey-cheeked mangabeys were observed feeding on S. globulifera flowers on one day out of >100 full day follows, likely indicating this species does not serve any sustainable nutritional importance in their diet (Rothman, unpubl. data).
The anthers of S. globulifera flowers contain a unique oily fluid originating from the tapetum composed exclusively of an unsaturated fatty acid, ester methyl nervonate (15-Tetracosenoic acid methyl ester), in which pollen grains are suspended (Bittrich et al., 2013). The presence of methyl nervonate as a naturally occurring plant substance is highly unusual, with identification occurring only in several other species and its chemical properties unknown (see Bittrich et al., 2013). The quantity of nectar secreted by a single flower under normal conditions averages 775 μl during one day (Bittrich and Amaral, 1996). Though the oil is adapted to carry pollen grain, this oil-pollen mixture does not attract pollinators, such as bees or birds for reasons that remain unclear (Bittrich et al., 2013). C. ascanius consume flower anthers in general, which comprise up to 2.3% of their diet (Struhsaker, 2017) and engage in the behaviour of drinking and licking the inside of the flower while holding the flower cupped in their hands, followed by discarding/dropping the flower that may indicate S. globulifera anther oil exploitation as well as nectar consumption (Bryer, 2020), yet its dietary importance is unknown. Female red-tailed monkeys spent 1.55-7.65% of their daily feeding time exploiting S. globulifera liquid (nectar and/or anther oil) exclusively, which contributed 0.11-1.08% of daily dry matter intake (Bryer, 2020). If C. ascanius were consuming S. globulifera anther oil, and not nectar, it contributed based on the assumption of majority fat content and minority pollen content, an average of 18% daily fat intake during only 4% daily feeding time (Bryer, 2020). These distinctions may indicate differences in the nutritive benefits derived from liquid versus the flower.
The exploitation of fatty S. globulifera flowers by monkeys likely represents the interruption of a pollination mutualism with birds. Several studies have shown that birds, in preparation for migration, preferentially accumulate different macronutrient reserves, namely adipose fat, in some cases increasing their fat reserves by 50% in preparation for migration (Pierce and McWilliams, 2005). Because the timing of annual flowering of S. globulifera in Kibale (Valenta, unpubl. data) coincides with the spring migration (late April through early June) (Saino et al., 2007), and floral morphology and tree focal observations indicate the importance of birds as pollinators (Valenta, unpub. data; Bittrich and Amaral, 1996), it is likely that the high fat content in S. globulifera flowers represents a nutritious reward for birds in exchange for pollination services. While the vibrant pink, red, and yellow floral displays of S. globulifera likely evolved to signal nutrient availability to avian mutualists; catarrhine primates, possess trichromatic color vision – thus, these floral displays would appear as vibrantly to Afro-Eurasian monkeys as they appear to humans (Jacobs and Deegan, 1999) (fig. 6). It may be that catarrhine primates are consuming fat-rich flowers, without in turn providing beneficial pollination services.
In sum, S. globulifera is a high-fat resource exploited by red-tailed monkeys in an otherwise fat scarce diet. This is noteworthy since flowers are not characteristically considered a substantial fat resource for primates and highlights the potential nutritional importance of florivory as an intrinsic foraging strategy.
Thank you to the Uganda Wildlife Authority and the Uganda National Council for Science and Technology for permission to conduct this research. We thank Hillary Musinguzi, Richard Sabiiti, Richard Kaseregenyu, and Patrick Ahabyoona for assistance with behavioural data collection. Thank you to Jenny Paltan for assistance in the lab. Thank you to Robert Lund and two anonymous reviewers for their suggestions and insights that substantially improved this paper.
Statement of ethics
This study protocol was reviewed and approved by the Uganda Wildlife Authority and the Uganda National Council for Science and Technology.
Conflict of interest statement
The authors have no conflicts of interest to declare.
This research was funded by NSF BCS 1540369 to MAHB and NSF BCS 1521528 to JMR as well as National Geographic, and CAC was supported by the Wilson Center during the writing phase of this project.
ACR wrote the manuscript and assisted with analysis. MAHB contributed data, assisted with analysis, and writing of the manuscript. JMR conducted assays and contributed reagents and materials. CAC, JMR, ON, and KV contributed to project design, data collection, and write-up.
Data availability statement
Resource intake data supporting fig. 2 and macronutrient content of flower species supporting figs 3-5 and table 1 are publicly available in MAHB’s dissertation. Raw data available on request.
Ajibesin KK, Ekpo BA, Bala DN, Essien EE, Adesanya SA (2008). Ethnobotanical survey of Akwa Ibom state of Nigeria. Journal of Ethnopharmacology 115: 387–408.
Akendengué B, Louis AM (1994). Medicinal plants used by the Masango people in Gabon. Journal of Ethnopharmacology 41: 193–200.
Bittrich V, Amaral M (1996). Pollination biology of Symphonia globulifera (Clusiaceae). Plant Systematics and Evolution 200: 101–110.
Bittrich V, Nascimento-Junior JE, Amaral MdCE, de Lima Nogueira PC (2013). The anther oil of Symphonia globulifera L.f. (Clusiaceae). Biochemical Systematics and Ecology 49: 131–134.
Bryer M (2020). Nutritional strategy and social environment in redtail monkeys (Cercopithecus ascanius). p. 324. City Univeristy of New York (CUNY).
Chapman C, Bonnell T, Sengupta R, Goldberg T, Rothman J (2013). Is Markhamia lutea’s abundance determined by animal foraging? Forest Ecology and Management 308: 62–66.
Chapman C, Galán-Acedo C, Gogarten JF, Hou R, Lawes MJ, Omeja PA, Sarkar D, Sugiyama A, Kalbitzer U (2021). A 40-year evaluation of drivers of African rainforest change. Forest Ecosystems 8: 66.
Chapman C, Valenta K, Bonnell TR, Brown KA, Chapman LJ (2018). Solar radiation and ENSO predict fruiting phenology patterns in a 15-year record from Kibale National Park, Uganda. Biotropica 50: 384–395.
Conklin-Brittain N, Knott C, Wrangham R (2006). Energy intake by wild chimpanzees and orangutans: methodological considerations and a preliminary comparison. In Feeding Ecology in Apes and Other Primates (Boesch CGH, Robbins MM, eds.), p. 523. Cambridge University Press.
- Search Google Scholar
- Export Citation
( , Conklin-Brittain N , Knott C Wrangham R ). 2006 Energy intake by wild chimpanzees and orangutans: methodological considerations and a preliminary comparison. In Feeding Ecology in Apes and Other Primates ( , eds.), p. , Boesch CGH Robbins MM 523. Cambridge University Press.
Conklin N, Wrangham R (1994). The value of figs to a hind-gut fermenting frugivores: a nutritional analysis. Biochemical Systematics and Ecology 22: 137–151.
Connor WE (2000). Importance of n-3 fatty acids in health and disease. American Journal of Clinical Nutrition 71: 171s–175s.
Dick CW, Abdul-Salim K, Bermingham E (2003). Molecular systematic analysis reveals cryptic tertiary diversification of a widespread tropical rain forest tree. The American Naturalist 162: 691–703.
Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28: 350–356.
Fromentin Y, Cottet K, Kritsanida M, Michel S, Gaboriaud-Kolar N, Lallemand M-C (2015). Symphonia globulifera, a widespread source of complex metabolites with potent biological activities. Planta Medica 81: 95–107.
Ganzhorn JU, Arrigo-Nelson S, Boinski S, Bollen A, Carrai V, Derby A, Donati G, Koenig A, Kowalewski M, Lahann P (2009). Possible fruit protein effects on primate communities in Madagascar and the Neotropics. PloS One 4: e8253.
Garber PA (1988). Foraging decisions during nectar feeding by tamarin monkeys (Saguinus mystax and Saguinus fuscicollis, Callitrichidae, primates) in Amazonian Peru. Biotropica 20: 100–106.
Gautier-Hion A, Duplantier JM, Quris R, Feer F, Sourd C, Decoux JP, Dubost G, Emmons L, Erard C, Hecketsweiler P, Moungazi A, Roussilhon C, Thiollay JM (1985). Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65: 324–337.
- Search Google Scholar
- Export Citation
( , Gautier-Hion A , Duplantier JM , Quris R , Feer F , Sourd C , Decoux JP , Dubost G , Emmons L , Erard C , Hecketsweiler P , Moungazi A , Roussilhon C Thiollay JM ). 1985 Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65: 324– 337.
Germeraad JH, Hopping CA, Muller J (1968). Palynology of tertiary sediments from tropical areas. Review of Palaeobotany and Palynology 6: 189–348.
Gill Jr GE, Fowler RT, Mori SA (1998). Pollination biology of Symphonia globulifera (Clusiaceae) in central French Guiana. Biotropica: 139–144.
Goering HK, Van Soest PJ (1970). Forage fiber analyses (apparatus, reagents, procedures, and some applications), US Agricultural Research Service.
Gupta MP, Solís PN, Calderón AI, Guionneau-Sinclair F, Correa M, Galdames C, Guerra C, Espinosa A, Alvenda GI, Robles G, Ocampo R (2005). Medical ethnobotany of the Teribes of Bocas del Toro, Panama. Journal of Ethnopharmacology 96: 389–401.
Hall MB, Hoover WH, Jennings JP, Webster TKM (1999). A method for partitioning neutral detergent-soluble carbohydrates. Journal of the Science of Food and Agriculture 79: 2079–2086.
Hanya G, Chapman CA (2013). Linking feeding ecology and population abundance: a review of food resource limitation on primates. Ecological Research 28: 183–190.
Jacobs GH, Deegan JF (1999). Uniformity of colour vision in Old World monkeys. Proceedings of the Royal Society of London. Series B: Biological Sciences 266: 2023–2028.
Kaplin BA, Munyaligoga V, Moermond TC (1998). The influence of temporal changes in fruit availability on diet composition and seed handling in blue monkeys (Cercopithecus mitis doggetti). Biotropica 30: 56–71.
Lambert J, Rothman J (2015). Fallback foods, optimal diets, and nutritional targets: primate responses to varying food availability and quality. Annual Review Of Anthropology 44: 493–512.
Lenta BN, Vonthron-Sénécheau C, Weniger B, Devkota KP, Ngoupayo J, Kaiser M, Naz Q, Choudhary MI, Tsamo E, Sewald N (2007). Leishmanicidal and cholinesterase inhibiting activities of phenolic compounds from Allanblackia monticola and Symphonia globulifera. Molecules 12: 1548–1557.
- Search Google Scholar
- Export Citation
( , Lenta BN , Vonthron-Sénécheau C , Weniger B , Devkota KP , Ngoupayo J , Kaiser M , Naz Q , Choudhary MI , Tsamo E Sewald N ). 2007 Leishmanicidal and cholinesterase inhibiting activities of phenolic compounds from. Molecules Allanblackia monticolaand Symphonia globulifera 12: 1548– 1557. 17960072
Licitra G, Hernandez T, Van Soest P (1996). Standardization of procedures for nitrogen fractionation of ruminant feeds. Animal Feed Science and Technology 57: 347–358.
Lima E, Ferrari S (2003). Diet of a free-ranging group of squirrel monkeys (Saimiri sciureus) in eastern Brazilian Amazonia. Folia Primatologica 74: 150–158.
Marti G, Eparvier V, Moretti C, Prado S, Grellier P, Hue N, Thoison O, Delpech B, Guéritte F, Litaudon M (2010). Antiplasmodial benzophenone derivatives from the root barks of Symphonia globulifera (Clusiaceae). Phytochemistry 71: 964–974.
Pierce BJ, McWilliams SR (2005). Seasonal changes in composition of lipid stores in migratory birds: causes and consequences. The Condor 107: 269–279.
Porter LM (2001). Dietary differences among sympatric Callitrichinae in northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. International Journal of Primatology 22: 961–992.
Prance GT, Balée W, Boom B, Carneiro RL (1987). Quantitative ethnobotany and the case for conservation in Ammonia. Conservation Biology 1: 296–310.
Raubenheimer D (2011). Toward a quantitative nutritional ecology: the right-angled mixture triangle. Ecological Monographs 81: 407–427.
Raubenheimer D, Machovsky-Capuska G, Chapman C, Rothman J (2015). Geometry of nutrition in field studies: an illustration using wild primates. Oecologia 177: 223–234.
Riba-Hernández P, Stoner KE (2005). Massive destruction of Symphonia globulifera (Clusiaceae) flowers by central American spider monkeys (Ateles geoffroyi). Biotropica 37: 274–278.
Rothman J, Chapman C, Pell A (2008). Fiber-bound nitrogen in gorilla diets: implications for estimating dietary protein intake of primates. American Journal of Primatology 70: 690–694.
Rothman J, Chapman C, Van Soest P (2012). Methods in primate nutritional ecology: a user’s guide. International Journal of Primatology 33: 542–566.
Saino N, Rubolini D, Jonzén N, Ergon T, Montemaggiori A, Stenseth NC, Spina F (2007). Temperature and rainfall anomalies in Africa predict timing of spring migration in trans-Saharan migratory birds. Climate Research 35: 123–134.
Ssegawa P, Kasenene JM (2007). Medicinal plant diversity and uses in the Sango bay area, southern Uganda. Journal of Ethnopharmacology 113: 521–540.
Struhsaker T (2017). Dietary variability in redtail monkeys (Cercopithecus ascanius schmidti) of Kibale National Park, Uganda: the role of time, space, and hybridization. International Journal of Primatology 38: 914–941.
Thompson ME (2013). Comparative reproductive energetics of human and nonhuman primates. Annual Review Of Anthropology 42: 287–304.
Valenta K, Melin A (2012). Protein limitation explains variation in primate colour vision phenotypes: a unified model for the evolution of primate trichromatic vision. In Zoology, pp. 29–46. Rijeka, InTech.
Van Soest P (1963). Use of detergents in the analysis of fibrous feeds. II. A rapid method for the determination of fiber and lignin. Journal of the Association of official Agricultural Chemists 46: 829–835.
Van Soest P, Robertson J, Lewis B (1991). Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74: 3583–3597.
Worman COD, Chapman C (2005). Seasonal variation in the quality of a tropical ripe fruit and the response of three frugivores. International Journal of Primatology 63: 689–697.