Fruit Phenology of Tree Species and Chimpanzees’ Choice of Consumption in Kalinzu Forest Reserve, Uganda

One hundred and eighteen (118) tree species were identified, among which 58 species produced fruit within the two-year study. Fruit of only 26.3% of the latter is eaten by chimpanzees. The consumption of each of these fruits was generally low, with only two species constituting more than 25% consumption. Only about 1.7% of woody biomass is relied upon by chimpanzees in Kalinzu for food. The major tree species in chimpanzee diet monitored showed that fruit production varies monthly and seasonally. Apart from Musanga leo-errerae and Ficus spp. whose fruiting was consistent throughout the year, general fruit phenology was positively correlated with rainfall. Only three species namely: Craterispermum laurinum, Aframomum angustifolium and Beilschmiedia ugandensis produced fruit in the dry seasons. Correlation between fruit availability and consumption was significantly positive for only one species, Landlophia dawei. This indicated that frugivory of chimpanzees in Kalinzu was not opportunistic; they search for what they like to eat. Chimpanzees would have to range furthest in periods of scarcity and asynchronous fruiting hence a lot of energy expenditure in the food search alone. Therefore, diversity in fruit phenology is important for chimpanzees’ energy conservation, health and survival. Selective logging and other selective human activities that involve cutting down trees that are palatable would in future affect the food diversity and consequently the health of frugivores if not done sustainably. Since patterns of fruit phenology are also linked to patterns of rainfall, changes in the former can assist in predicting the influence of climate change on food availability for big frugivores like chimpanzees.

• Chimpanzees
• Consumption
• Fruit
• Kalinzu
• Phenology

1. Introduction

Knowing the dynamics of fruit production is important for understanding great apes’ (chimpanzees, gorillas, and bonobos) ecology, as fruit provides a nutritious resource for most of them in tropical African regions. Plant species composition, density, distribution and temporal fluctuation affect apes’ ecological features such as diet [1] -[5] , ranging patterns [6] -[8] , group size [9] [10] , reproductive parameters [11] , patterns of social interaction [12] and tool-using behavior [13] . Comparison of fruit phenology is also important for understanding the ecological differences in great apes among different study sites. The patterns of fluctuation in party size of chimpanzees are different among four chimpanzee study sites and it was suggested that the differences in dynamics of fruit production among sites were the cause [9] . The annual and seasonal fluctuations in fruit production are distinct, and a period of fruit scarcity exists at all study sites [14] . In Central Africa, fruits are more abundant in the rainy season than in the dry season. In Lopé National Park (Gabon), fruit abundance peaks in the early rainy season and fruits are scarce during the long dry seasons. Fruit abundance peaks may also occur during the mid-rainy season and become scarce during the dry season [2] [6] [15] . In East Africa, climatic factors influencing fruit phenology are varied among sites. In Mahale Mountains National Park (Tanzania), the number of plant species in fruit declines in December, January and February during the rainy season [16] . In Kibale Forest (Uganda) and Kahuzi-Biega (DRC) National Parks, fruit abundance is negatively correlated with monthly rainfall, and more fruits are available during the dry season [8] [17] . In contrast, peaks in fruit abundance occur during the rainy season in Budongo [18] . In the two sites of West Africa, Taï National Park (Cotê d’Ivore) and Bossou (Guinea), fruits tend to be abundant during the dry season [13] [19] . Even within the same habitat, patterns of fruit production differ among species, plant life forms, and vegetation types, and therefore periods of fruit scarcity also vary.

Frugivorous animals respond to periods of fruit scarcity by changing their dietary composition and/or ranging patterns [6] [8] [14] [20] . Several primate populations like vervet monkeys (Cercopithecus aethiops) [21] and baboons (Papio anubis) in Amboselli, Kenya, and Toque macaques in Sri Lanka [22] have been documented to decline in number with a natural decline in their food resources. In Kalinzu forest, selective commercial logging and pit sawing continue to occur, especially in the eastern part [23] [24] . The former Nkombe saw mill, a logging company, had been mechanically logging in the north eastern part of the forest and exclusively harvested Parinari excelsa. Local people have been harvesting/logging some useful trees, such as Carapa grandiflora and Funtumia africana, in some areas. These logging activities created some patches of secondary vegetation.

Phenological patterns are linked to factors that govern forest health such as population biology of pollinators, seed dispersers and predators, herbivores, interspecific competition among trees and other processes of primary production [25] and assist conservation scientists in predicting consequences of adverse climatic events. In this paper, overall fruit abundance and patterns of fruiting of major species are analyzed in relation to rainfall and chimpanzee feeding patterns. This will provide baseline data for management options occurring in Kalinzu Forest Reserve especially during periods of tree harvests and habitat-wide fruit scarcity since this has a dietary implication on population dynamics of frugivores like chimpanzees.

2. Study Area

In Uganda, chimpanzees are restricted to the western part and the total number is estimated at 4950. Of these, 230 occur in Kalinzu at a density of 1.55 km⁻² ranking third after Kibale at 2.32 km⁻² and Bugoma at 1.9 km⁻² (Table 1) [26] . Kalinzu Forest Reserve lies in south-western Uganda (0˚17'S and 30˚07'E). It covers 137 km² and borders the Maramaganbo forest and the two form part of the Queen Elizabeth National Park. Kalinzu forest is one of the richest forests in Uganda, with more tree species recorded here than anywhere else. Three important timber species from this forest are considered endangered. These include Cordia milleni, Entandrophragma angolense, and Lovoa swynnertonii [27] . It is inhabited by six species of primates including the largest population of l’hoest’s monkeys (Cercopithecus l’hoest), a species considered vulnerable to extinction. Kalinzu together with Maramagambo forests represent the largest tract of forests at this altitude in Uganda. Kalinzu covers an exceptional altitudinal range, which combined with its topographical, climatic and geological diversity, and its location in western Albertine rift valley close to the believed upper Pleistocene forest refugia, gives rise to a great variety of forest habitat. The Forest occupies a shallow saucer-shaped depression in the rift valley escarpment with its floor at about 1463 m above sea level from which rise a few grassy hills that reach up to 1845 m.

The vegetation of Kalinzu is broadly classified as medium altitude moist evergreen tropical rain forest [27] .

Table 1

Ugandan forests inhabited by chimpanzees (NP―national park; FR―forest reserve)

Forest	Size (km2)	No. of tree species (% of country total species)	Total chimpanzee population	Density of chimpanzees
Kibale NP	795	209 (49%)	1420	2.32
Bugoma FR	365	158 (36%)	630	1.90
Kalinzu FR	137	265 (57%)	230	1.55
Budongo FR	793	240 (56%)	640	1.36
Itwara FR	97	143 (33%)	130	1.35
Kasyoha-Kitomi FR	399	204 (47%)	410	0.92
Rwenzori NP	996	75 (18%)	500	0.46
Bwindi NP	321	163 (38%)	210	0.43

Generated from [26] [27] .

According to the most recent classification, Kalinzu forest vegetation can be simplified into four vegetation types: mixed mature forest, Parinari dominated mature forest (Parinari mature), Parinari dominated secondary forest (Parinari secondary), and Musanga dominated secondary forest (Musanga secondary) [28] . The rainfall pattern has two peaks―in April and October. The June-July dry season is more severe than the one in January. The temperatures of Kalinzu Forest Reserve range from the minimum of 13˚C to the maximum of 28˚C.

3. Methods

Ten parallel transects 5 km long and 5 m wide running east to west of Kalinzu forest were used to collect data. Distance between transects was 500 m. Each of these transects was divided into ten 500-m sections totalling to 100 plots. All trees above 10 cm in diameter at breast height (DBH) within 2.5 m of each side of the transect were recorded. The number of trees of each species in 5 × 500 m block was used as a variable for the analysis of Species Important Value Index (SIVI). A total of 25 km² of vegetation was sampled. SIVI values were calculated to give a comparable index incorporating measures of tree species distribution, relative density and abundance. The SIVI value is therefore, the summed value of relative density, relative frequency and relative dominance. The sum of these three values for the particular species, the species importance value index (SIVI) never exceeds 300 because each parameter is a percentage ranging from 0 to 100 [29] . Tree species were ranked on the basis of their SIVI values.

A fruit phenology census was conducted along each of these 10 transects for two years. During each census, fallen fruit was counted. Fallen fruit from one tree, 2.5 m of each side of the transect, was considered as one fruit cluster. When more than one tree of similar species contributed to the cluster of fruit on the ground, it was divided amongst the number of fruiting trees. The number of clusters thus matched with the number of fruiting trees that dropped fruit within the census belt. The tree species, the numbers of fruit in each cluster and whether the fruit would be ripe or unripe (determined by majority) was recorded. The numbers of fruit in each cluster was grouped as 1 - 4, 5 - 9, or >10, and assigned a frequency score of 1, 3, or 9 respectively, then a fruit abundance index (FAI) was determined from the total number of scores per hectare as explained in [1] . The FAI of fruits eaten by chimpanzees was calculated separately. To examine the relationship between number of fruit in the tree and number of fallen fruit, major trees whose fruit was recorded to be eaten by chimpanzees during the preliminary faecal analysis were randomly chosen on the transects and monitored for fruit production. A record of ripe and unripe fruit was taken.

The pattern of fruit consumption by chimpanzees reported in this study was determined by faecal analysis [2] . It was supplemented by direct observations of feeding where possible, to confirm the consumption of foods that were seen in faecal sample remains. Fresh chimpanzee faecal samples were collected but those that scattered on the ground or among branches were ignored due to the difficulty in picking a representative sample of such. After a day’s collection, the faecal samples were preserved in plastic bags with 100% ethanol and the following noted: date of collection, location, time of collection, and the visible contents of the faecal sample by majority constituent.

A total of 2635 faecal samples were collected in 26 months (monthly range 24 - 206; mean = 101). Each month, the faecal samples were placed in a metal sieve with 1mm mesh and washed in running water. Once the soluble solution had gone, the seeds were sorted. The samples were then sun dried and divided into categories: seed, skin, and pulp of fruit, leaf matter, pith, ant, mammal, entire leaf, or others. We evaluated the percent volume of each food category in each sample, where the smallest unit would be 5%. We recorded species names except where more than one species in the same genus could have indistinguishable seeds e.g. Ficus spp. Indistinguishable seeds in this genus were treated as a single fruit “species group”. One identifiable fruit species meant one fruit species group.

4. Results

4.1. Kalinzu Forest Tree Composition

A total of 16,778 trees belonging to 118 species (6 of which remained unidentified) and 44 families were recorded. The identified tree species and their Species Importance Value Indices are as shown in Table 2. Of these

Table 2

Species important value indices, fruit availability index and consumption of fruit of tree species by chimpanzees in Kalinzu forest reserve

NAME	FAMILY	DORMINANCE	DENSITY	FREQ OF TREES	SIVI	FAI	% of FAECAL SAMPLES WITH SEED
		Basal area/ha	Tree/ha
*Craterispermum laurinum	Rubiaceae	18,337.6	398.9	3750	46.0	462.9	8.3
Funtumia Africana	Apocynaceae	32,744.9	289.7	2723.0	35.5
Strombosia scheffleri	Alocaceae	94,377.3	133.5	1255.0	24.9	568.1
Parinari excelsa	Chrysobalanaceae	134,656.5	26.9	253.0	17.4	108.7
*Celtis durandii	Ulmaceae	48,255.9	88.3	830	14.9	757.0	2.7
*Ficus spp.	Moraceae	91,451.0	31.6	297.0	13.3	140.2	67.3
*Musanga leo-errerae	Urticaceae	43,269.6	44.4	417.0	9.5	349.3	78.7
Carapa grandiflora	Meliaceae	26,119.4	50.2	472	8.4	97.2
Sapium ellepticum	Euphobiaceae	33,625.6	39.3	369	7.9	178.3
Carapa Procera	Meliaceae	23,193.2	38.2	359.0	6.7	83.3
*Drypetes bipidensis	Euphorbiaceae	28,470.2	30.2	284	6.4	102.0	3.1
Cassipourea sp.	Rhizophoraceae	11,386.7	38.6	363	5.5	0.7
Xymalos monospora	Monimiaceae	9344.2	34.3	322	4.8	18.2
Macaranga schweinfurthii	Euphobiaceae	9916.5	34.3	322	4.8	-
Oxyanthus speciosus	Rubiaceae	3322.4	39.7	373.0	4.7	89.7
*Alchonea hitera	Euphorbiaceae	1718.1	39.7	373	4.6	118.9	0.1
Markhamia platycalyx	Bignoniaceae	10,206.8	30.5	287.0	4.5	-
*Beilschmiedia ugandensis	Luauraceae	11,847.3	28.7	270	4.4	10.1	1.5
Trema orientalis	Ulmaceae	8246.2	29.7	279	4.2	80.0
*Syzigium guinense	Myrtaceae	11,129.8	26.9	253	4.2	130.2	0.2
Trichoscypha submontana	Anacardiaceae	18,597.1	16.6	156	3.8	131.8
Newtonia buchananii	Leguminoceae	17,644.5	17.3	163.0	3.8	45.9
*Linociera johnsonii	Caprifoliacea	7511.2	24.3	228	3.5	43	-
Mitragyna stipulosa	Rubiaceae	19,046.2	10.7	101	3.2	-
*Prunus africana	Rosaceae	16,599.2	11.7	110	3.1	62.6	0.6
*Pseudospondias microcarpa	Anacardiaceae	19,065.1	4.0	38	2.5	32.1	9.0
Dictyandla sp.	Rubiaceae	3031.5	18.8	177	2.4	71.7
*Myrianthus holstii	Moraceae	1078.9	20.0	188	2.3	32.8	2.1
Diospyros abyssinica	Ebenaceae	6540.1	10.4	98.0	1.9	90.6
Pleiocarpa pycnantha	Apocynaceae	1681.8	14.8	139	1.8	8.4

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