Fruit Preference in the Velvet Asity Philepitta Castanea in a Rain Forest of Madagascar

Jpn. J. Ornithol. 47: 11-19, 1998

Fruit Preference in the Velvet Asity Philepitta castanea in a Rain Forest of Madagascar

Hajanirina RAKOTOMANANA1 and Teruaki HINO2

1 Department of Zoology, Faculty of Science, Kyoto University, Kitashirakawa- Oiwakecho, Sakyo-Ku, Kyoto 606-8502 Kansai Research Center, Forestry 2 and ForestProducts Research Institute, Momoyama, Fushimi, Kyoto 612-0855

Feeding preference of the Velvet Asity Philepitta castanea was examined in relation to fruiting phenology and a variety of fruit characteristics (nutritive and energy contents, colour, size, weight, seed load, handling time and seed passage time) in Ranomafana rain forest, southeastern Madagascar, during the dry season (August-October). In the period when total fruit supply exceeded birds' energy requirement, fruit preference was obvious and stable, that is, fruits of Oncostemon leprosum were preferred, those of all Psychotria spp. were taken at random without preference, and those of Saldinia sp. were avoided. But we did not find a preference among fruits, as predicted in optimal foraging theory, when total fruit supply was in short. There was no direct correspondence between the asity preference and any fruit characteristics. Assuming that frugivorous birds have a fixed criterion of fruit characteristics for selection, the fruits of Saldinia sp. might be avoided because the criteria on nutrition and/or energy were not filled (suggested by lowest values in percent of the nutrition assimilated, energy/handling time, and energy/pulp weight). Forag- ing the large-sized fruits of Psychotria sp.8 with some favourable properties was perhaps limited by gape size. The fruits of O. leprosum may have been preferred due to the higher pulp-to-seed ratio and the shorter seed passage time resulting in higher food processing rate than Psychotria spp. Key Words: Food preference, Fruit characteristics, Phenology, Philepitta castanea

Optimal foraging theory has predicted diet choice in birds based on maximization of energy gain per unit foraging time (reviews in Pyke 1984, Stephens and Krebs 1986). In fruit-eating birds, however, diet choice has been complicated because many different fruit characteristics affect the fruit preference by birds, such as energy gain per time (Snow 1962a, 1962b, Foster 1978), nutritive contents (Morton 1973, Sorensen 1981,1983, Herrera 1982), size (Wheelwright 1985), seed load (Howe & Van de Kerchove 1980, Herrera 1981), seed passage rate (Sorensen 1984), colour (Stiles 1982, Willson & Melampy 1983, Willson & Whelan 1990), taste (Sorensen 1983) and accessibility (Denslow and Moermond 1982). Forests in Madagascar have unique flora and fauna with many endemic species, but they are endangered by rapid deforestation. In order to preserve these forests, we need to understand relationship between frugivorous birds and fruiting plants,

1 Present address: Cite 67 ha sud Logt 315, Antananarivo 101, Madagascar 12 Hajanirina RAKOTOMANANA and Teruaki HIND [Jpn.J.Ornithol.Vol.47 No.1 because their interactions are important in the maintenance and regeneration of the flora (Janzen 1970). In special, the Velvet Asity Philepitta castanea (Philepittidae), which is an endemic and the only fruit-eating bird species in the understory shrubs, is of great value in research. We investigated the asity's preference of fruits in relation to fruiting phenology and several characteristics of fruits (nutrition, energy, colour, size, seed load, handling time and seed passage time) during the dry season.

STUDY AREA This study was carried out at Ranomafana National Park, Madagascar. This locality represents the montane tropical rain forest situated in the southeastern part of the island (21*16'S-47*28'E), about 365 km South East from the capital, Antananarivo, at the altitude 800-1200 m. Many small streams come out of the mountains and they empty into the Namorona River which crosses the forest. Basically, two seasons are discriminated: the rainy season (November-April) and the dry season (May-October). The annual precipitation is 2,600 mm (Nicoll and Langrand 1989) and the annual mean temperature is about 21.4°C (Ifanadiana station). The understory of Ranomafana rain forest is very diverse with many small trees and shrubs. Common fleshy-fruiting species include Psychotria spp. (Rubiaceae), Oncostemon spp. (Myrsinaceae), Eugenia spp. (Myrtaceae), Ficus spp. (Moraceae), Tambourissa spp. (Monimiaceae), Polyscias spp. (Araliaceae), Aphloia theaeformis (Flacourtiaceae) and Weinmannia spp. (Cunoniaceae). The most common epiphytes were Asplenium nidus (Aspleniaceae) and orchids Bulbophyllum and Eulophiella. A vast area of the rain forest is occupied by an introduced species Psidium cattleianum. The detailed descriptions of the Ranomafana vegetation can be found in Hooper (1991).

METHODS 1) Estimation of fruit production In our study site (12.25 ha), the ripe fruit productions were examined in five species of understory shrubs exploited by the Velvet Asity during the study (August - November) in 1995 and 1996. Those species were Oncostemon leprosum, Psychotria sp.1, sp.6, sp.8 and Saldinia sp., where Psychotria was identified by species number due to lack of species names. The ripeness of fruits was judged according to the colour. To assess the weekly fruit production of each species, big branches with enough fruits were netted not to be visited by animals. Seventeen exclosures were made for each shrub species and the numbers of unripe and ripe fruits in each branch were counted every week. For each species, total fruit production per shrub was estimated as an average of the number of ripe fruits in each exclosure multiplied by the number of branches in the same shrub. Then, total fruit production in our study area was calculated by multiplying the total fruit production estimated per shrub by the number of adult shrubs estimated from belt transect method. In order to analyse a seasonal change of fruit production in relation to bird foraging, the study period was divided into the three periods: A (20 August-7 September), B (8-27 September ) and C (28 September-16 October). July 1998] Fruit Preference in the Velvet Asity 13

2) Bird survey and preference index In our study site, we observed fruit consumption behaviour by birds with a continuous recording method (Martin & Bateson 1986) between 06:00 and18:00 h (96 hours in total). We could usually follow a focal bird for a maximum of two and half hours. Species and the number of the fruits taken or regurgitated, time of observation, and sex, age and location of the bird were continuously recorded. Handling time per fruit was, measured with a stopwatch, defined as the time from touching fruit to swallowing at the back of the throat. We used Strauss's linear index L=r-p (r and p are the proportions of fruit species in the diet and in the environment, respectively) to evaluate preference for each fruit species in different periods. This index ranges from -1 (maximum avoidance) to +1 (maximum preference) centred on zero (random feeding). We chose this index among several preference indices (Lechowicz 1982), because the index gave the most stable results for samples from different periods that differed in relative abundance of available fruits. The daily energy requirement of a free-living bird can be calculated by 4.2W0.61 where W is the body weight of the bird (Walsberg 1983). The daily energy requirement for one individual was 38.9 KJ with an average body weight 38.5 g (Rakotomanana, 1998). Then, the total daily energy requirements in our study site was 933.6 KJ for 24 adult birds, which were counted with territory mapping and mistnetting during the study.

3) Analysis of nutritive contents of fruit Fruit diameter was measured to 0.1 mm using a dial caliper (60 fruits for each species). Wet mass of pulp and seed were also weighed to nearest 0.1 g using a small electronic portable balance (at least 20 fruits for each species). Dried pulp samples from 100g - fresh fruits were used for nutritional analyses. Total sugars were obtained using the Phenol-H2SO4method after extracting with 80% ethanol. Total starches were obtained using the Phenol-H2SO4method after extracting with 1N- HCl. Total lipids were extracted in a soxhlet apparatus and total proteins were extracted using the Weatherburn method (Weatherburn 1967). Total ash was obtained using 600°C drying method at a normal air pressure, and then fiber was remained. Total energy contents of pulp were determined using a Phillipson microbomb calorimeter.

4) Cage experiment for seed passage time From August to October 1996, five individuals were mistnetted and used in the cage experiment to measure seed passage time for each fruiting species. We made one trial by one bird for each fruiting species. In the field, each bird was housed temporally in a 1 m3cage for a maximum of 5 hours and supplied with ripe fruits of a target plant. Uneaten fruits were removed five minutes after the first amount of fruits was eaten. We recorded the number of fruits ingested and the time to evacuation of seeds by regurgitation or defecation. Since we did not exactly know when most of the seeds evacuated were ingested, we used a median value between the shortest and longest times in common for an ingestion time of those unidenti- fied seeds. Unclear data were removed from the analysis. We could not get sufficient data on Psychotria sp.6 and sp.8, because the captured birds had to be released after a certain time not to be weakened physiologically. Seed passage time mature

14 Hajanirina RAKOTOMANANAand Teruaki HINO [Jpn.J.Ornithol.Vol.47 No.1 by regurgitation were also obtained with the continuous recording method in the

RESULTS 1) Fruit preference The Velvet Asity regularly took fruits of Jasminum sp. by 10-25% of diets, although all of them remained unripe during the study (Table 1). Since we had no data on abundance of the unripe fruits for Jasminum sp., we calculated preference indices for five fruiting species with the foraging data except for the species (Table 1). The results showed that the fruit preference was distinct and did not change between the periods A and B. In both periods, that is, the fruits of O. leprosum were preferred, those of all the Psychotria spp. were taken at random without preference, and those of Saldinia sp. was avoided. However, the asity did not show any fruit preferences for O. leprosum and the two species of Psychotria in the period C.

Table 1. Seasonal changes in the average abundance and proportion of ripe fruits in each species, proportion of fruits eaten and fruit preference by the Velvet Asity

1: A: 27 August-7 September, B: 8-27 September, C: 28 September-16 October 2: Toal numbers of observations for fruit eating by birds were 1,014, 829 and 330 in the periods A, B and C, respectively. July 1998] Fruit Preference in the Velvet Asity 15

2) Fruit abundance Abundance of ripe fruits of each species temporally changed in different patterns (Table 1). The fruits of O. leprosum gradually increased and had a peak in the period C. This shrub had a longer fruiting season (ca. five months) due to asyn- chronous ripening. On the other hand, the fruits of the other species perhaps synchronously ripened before or at the start of the study and then decreased to zero in Psychotria sp.8 in the period A, in Saldinia sp. in the period B, and in Psychotria sp.l and sp.6. in the period C. According to the different fruiting phenology between species, the composition and total abundance of ripe fruits varied between periods. Fruit abundance was not the factor explaining different fruit preference between species, because fruit preference was stable between the periods A and B irrespective of different compositions of ripe fruits in the habitat. In order to examine if the asity obtained sufficient amounts of energy from fruits in the habitat in each period, we compared total energy supplies of fruits and total energy requirements of birds (Table 2). The results showed that fruits were oversupplied in the period A and B, but were in short supply in the period C. Thus, the fruit abundance relative to energy requirements may explain the seasonal change in whether fruits were eaten selectively or randomly.

Table 2. Comparisons between the total energy supply by fruits and the total energy requirement by the Velvet Asity in different periods in our study site

1: A: 27 August-7 September, B: 8-27 September, C: 28 September-16 October 2: Total energy supply = sum of [fruit abundance of each species (Table 1) * energy per fruit of each species (Table 3)] 3: Total energy requirement = the total daily energy requirement by birds (933.6 KJ for 24 birds) * No. of days

3) Fruit characteristics The physical, nutritive, and energetic characteristics of the fruits were compared between species to find the factors explaining the fruit preference in the periods A and B (Table 3). The colour of fruits was red in the preferred O.leprosum and blue in the avoided Saldinia sp., not contradicting with one of hypotheses that conspicuously-coloured fruits were selected by frugivores (Willson and Whelan 1990). Psychotria sp.8 was largest in size and heaviest in the weight of both pulp and seeds. The pulp was lightest in Psychotria sp.6 and the seeds were lightest in Saldinia. Pulp-to-seed ratio was highest in the avoided Saldinia sp. and the second in the preferred O. leprosum. The fruits with rich nutrition or energy may be selected by birds. Nutritive contents in the pulp largely varied among fruits. The proportion of carbohydrates was highest in Psychotria sp.1 and lowest in Saldinia sp., that of lipid was highest in Psychotria sp.8 and lowest in Saldinia sp., and that of fiber was highest in 16 Hajanirina RAKOTOMANANAand Teruaki HINO [Jpn.J.Ornithol.Vol.47 No.1

Table 3. Comparisons of physical characteristics, nutritive contents and energetic values of fruits eaten by the Velvet Asity.

1,2: Numbers of samples were 60 in the diameter and 20 in the weights for each species 3: Dried pulp samples from 100g-fresh fruits were used for analysis of nutrients and energy 4: Numbers of observations for handling time of fruits by birds were 34, 24, 48, 10 and 40 in the order of species from the left.

Saldinia sp. and lowest in Psychotria sp.l. For simplicity, if carbohydrates, lipid and protein are lumped as the nutrients assimilated, its proportion was highest in Psychotria sp.1 and lowest in Saldinia sp. Both total amount of energy and the energy per pulp weight were highest in Psychotria sp.8 due to its large size, but lowest in Saldinia sp. and the second in Oncostemon perhaps due to low amount of the nutrition assimilated. Handling time taken from pluck to swallow of fruits was outstandingly long in Psychotria sp.8 due to its large size, which was as large as gape width of the asity (ca. 12 mm in unpublished data). Nevertheless, this fruit had the highest energy intake per handling time. In contrast, the energy intake rate was similar and lowest in Saldinia sp. and O. leprosum. In frugivorous birds, food passage rate may be more important than food intake rate (Sorensen 1984). The average seed passage time was shorter in Saldinia sp. and O. leprosum than Psychotria sp.1 due to short passage by defecation (Table 4). July1998] Fruit Preference in the Velvet Asity 17

Table 4. Comparisons in seed passage time (sample size in parentheses) of fruits eaten by the Velvet Asity.

1: Data from cage experiments 2: Data from both cage experiments and field observations 3: -Not available data due to sample size <5

On the whole, there was no direct correspondence between the asity's preference and any fruit characteristics, because the most preferred O. leprosum were more similar to the most avoided Saldinia sp. than to Psychotria spp. .in many fruit characteristics. DISCUSSION Based on maximization of food intake per foraging time, optimal foraging theory predicts that foragers should have a broader diet in a productive environment than in an unproductive environment (Charnov 1976). In the present study, this prediction was supported by the seasonal change in fruit preference by the Velvet Asity, that is, the bird was selective in diet only when fruit supply exceeded birds' requirement in the habitat (i.e., in the periods A and B). When fruit abundance was not sufficient even if eating unripe fruits of Jasminum sp. (i.e., in the period C), not only took the asity fruits at random, but also took insects in mixed-species flocks (pers. obs.). The optimal foraging theory have also succeeded in predicting diet choice in birds, such as insect- (Krebs et al. 1977) and seed-eaters (Pulliam 1985). However, fruit-eaters have two major problems for this theory to be applied. The one is that foraging time (searching time + handling time) was difficult to be defined and to be measured. What is searching time for frugivores ? Fruits will be easily found because they are usually in sight not like insects or seeds hidden in some cover. If fruits are more abundant, birds may decrease searching time. In this study, however, fruit abundance did not explain the different preference between fruits. Neither did an energy gain per handling time (defined as the time from pluck to swallow of fruits). The other problem is that many factors other than energy intake rate affect diet choice in frugivorous birds. This study examined nutrition, colour, size, pulp-to- seed ratio and seed passage time, in addition to abundance, energy and handling time described above. However, there was no direct correspondence between the asity's preference and any fruit characteristics. In fact, the most preferred O. .

18 Hajanirina RAKOTOMANANAand Teruaki HINO [Jnp.J.Ornithol. Vol.47 No.1 leprosum were more similar to the most avoided Saldinia sp. than to Psychotria spp. in many characteristics. We may have to assume that Velvet Asity had some criteria of fruit characteristics to determine whether eating it or not. If so, the criterion should be given by the properties which were worst in fruits of Saldinia sp. The possible factors are the lowest proportion of nutrients assimilated, the lowest energy per weight and the lowest energy per handling time, all of which are related to energetic and /or nutritional quality of fruits. The inconspicuous colour, blue of the fruits of Saldinia sp. may have been a secondary factor of avoidance (Willson & Whelan 1990). If Saldinia sp. is excluded, we can give the possible factors explaining why the fruits of O. leprosum were preferred. Those are the high pulp-to-seed ratio and the short seed passage time, both of which will result in high food processing rate (Sorensen 1984). Although the largest-sized fruits of Psychotria sp.8 had some favourable properties such as the highest energy per handling time and the highest energy per weight, the foraging on those fruits was perhaps limited by gape size (Wheelwright 1985). Despite inspecting many characteristics of fruits, we could not give a clear explanation on the fruit selection by the Velvet Asity. We only conclude that frugivore's diet choice is very complicated in dependence on a variety of factors. We need more intensive observations and well-designed experiments on fruit preference, and also need more information on internal mechanisms of assimilation and digestion in fruit-eating birds.

We are grateful to Professor. S. Yamagishi for his support and valuable advice. We thank Ms Y. Okauchi for her collaboration on the analysis of fruit samples. We would like also to thank Messrs A. Rakotozafy, P. Rasabo and D. L. Randrianantenaina for their assistance in the field and to the staff of Ranomafana National Park Project and DEF (Direction des Eaux et Forets) for giving us permission for exportation of fruit samples. This study was partly supported by a grant under the Monbusho International Scientific Research Program (No.06041093).

LITERATURE CITED Charnov, E. L., 1976. Optimal foraging: the marginal value theorem. Theor. Popul. Biol. 9: 129-136. Denslow, J. S. and Moermond, T. C., 1982. The effect of accessibility on rates of fruit removal from tropical shrubs: an experimental study. Oecologia 54: 170-176. Foster, M. S., 1978. Total frugivory in tropical passerines: A reappraisal. Trop. Ecol. 19: 131-151. Herrera, C. M., 1981. Fruit vegetation and competition for dispersers in natural popu- lations of Smilax aspera. Oikos 36: 51-58. Herrera, C. M., 1982. Defense of ripe fruits from pests: its significance in relation to plant-disperser interactions. Am. Nat. 120: 218-241. Hooper, C., 1991. Man and the Malagasy rain forest. Forestry preliminary report for MAB (the Man and the Biosphere) grant. Ranomafana National Park Office, Antananarivo. Howe, H. F. & Van de Kerchove, G. A., 1980. Nutmeg dispersal by tropical birds. Science 210: 925-927. Janzen, D. H., 1970. Herbivores and the number of tree species in tropical forests. Am. Nat. 104: 502-528. July1998] Fruit Preference in the Velvet Asity 19

Krebs, J. R., Erichsen, J. T., Webber, M. I. & Charnov, E.L., 1977. Optimal prey selection by the great tit (Parus major). Anim. Behav. 25: 30-38. Lechowicz, M. J., 1982. The sampling characteristics of electivity indices. Oecologia 52: 22-30. Martin, P. & Bateson, P., 1986. Measuring behaviour: an introductory guide. Cambridge University Press, Cambridge. Morton, E. S., 1973. On the evolutionary advantages: disadvantages of the fruit eating habit in tropical birds. Am. Nat. 107: 8-22. Nicoll, M. & Langrand, O., 1989. Madagascar: revue de la conservation et des aires protege'es. World Wide Fund for Nature, Gland, Switzerland. Pulliam, H. R., 1985. Foraging efficiency, resource partitioning and the coexistence of sparrow species. Ecology 66: 1829-1836. Pyke, G. H., 1984. Optimal foraging theory: a critical review. Ann. Rev. Ecol. Syst. 15: 523-575. Rakotomanana, H., 1998. Negative relationship between relative tarsus and wing lengths in Malagasy rain forest birds. Jpn. J. Ornithol 47: 1-9. Snow, D. W., 1962a. A field study of the Black and White Manakin, Manacus manacus, in Trinidad. W.I. Zoologica 47: 67-104. Snow, D. W., 1962b. A field study of the Golden-headed Manakin, Pipra erythrocephala, in Trinidad, W.I. Zoologica 47: 183-198. Sorensen, A. E., 1981. Interactions between birds and fruits in a temperate woodland. Oecologia 50: 442-450. Sorensen, A. E., 1983. Taste aversion and frugivore preference. Oecologia 56: 117-120. Sorensen, A. E., 1984. Nutrition, energy and passage time: experiments with fruit preference in European Blackbirds (Turdus merula). J. Anim. Ecol. 53: 545-557. Stephens, D. W. & Krebs, J. R., 1986. Foraging theory. Princeton Univ. Press, Princeton. Stiles, E. W., 1982. Fruit flags: two hypotheses. Am. Nat.120: 500-509. Walsberg, G.E., 1983. Avian ecological energetics. Farner, D. S., King, J. R. & Parkes, K. C. (eds.) Avian Biology 7: 161-220. Academic Press, London. Weatherburn, M. W., 1967. Phenol-hypochlorite reaction for determination of ammo- nia. Anal. Chem. 39: 971-974. Wheelwright, N. T., 1985. Fruit size, gape width, and the diets of fruit eating birds. Ecology 66: 808-818. Willson, M. F. & Melampy, M. N., 1983. The effect of bicolored fruit displays on fruit removal by avian frugivores. Oikos 41: 27-31. Willson, M. F. & Whelan, C.. J., 1990. The evolution of fruit color in fleshy- fruited plants. Am. Nat. 136: 790-809.

(Received 27 October 1997; Accepted 18 June 1998) July 1998］ 29

マダガスカル降雨林におけるビロードマミヤイロチョウの果実に対する選好性

(Fruit Preference in the Velvet Asity Philepitta castanea in a rain forest of Madagascar. 47:11-19)

Hajanirina RAKOTOMANANA1・日野輝明2

1京都大学理学部動物学教室，〒606－8502 京都市左京区北白川追分町 2森林総合研究所関西支所鳥獣研究室，〒612－0855 京都市伏見区桃山町

ビロードマミヤイロチョウ Philepitta castanea は，マダガスカル固有の果実食の鳥である．マダガスカル南東部のラノマファナ降雨林の下層部で唯一の果実食者である本種について，乾期（8月－ 10月）における果実の選好性を調べ，それを果実の結実量の季節変化やさまざまな形質的な特徴（栄養素，エネルギー量，色，大きさ，重量，種子の負荷量，処理時間，種子の体内通過時間）との関係［J pn．J．Ornithol． 30 和文抄録 Vol．47 No．1

から解析した．果実の供給量が鳥のエネルギー要求量を越えている期間においては，明確でかつ安定な選好性が示された，すなわち，Oncostemon の果実は好まれたのに対し，Psychotria 3 種の果実に対しては果実量に比例したランダムな採食が行われ，Saldinia の果実は忌避された．しかし，果実の供給量が不足している期間には，果実に対する特別な選好性は示されなかった．このような果実量に対する選好性の季節変化は，最適採食理論による予測と一致した，ところが，選好されたOncostemon と忌避された Saldinia の果実は Psychotria の果実よりも多くの形質において類似しており，ビロードマミヤイロチョウによる果実の選好性の順序は果実のどのような形質の順序とも一致しなかった．そこで，本種はある一定の規準を満たす果実のみを採食すると仮定すると，Saldirzia の果実が選好されなかったのは，この果実は栄養価あるいはエネルギーに関する規準（同化される栄養素の割合，エネルギー獲得量／処理時間，エネルギー量／果肉重）を満たさなかったためであると考えることができるかもしれない．また，果実食の鳥にとって好ましいいくつかの形質をもつ Psychotria sp．8 の果実が選好されなかったのは，その果実サイズが脂の開口幅とほぼ同じであることによって採食が制約されたのであろう．一方，Oncostemon の果実が選好されたのは，Psychotria の果実に比べて大きな果肉／種子の重量比と短い体内通過時間をもつことから，果実の体内処理速度がすぐれているためであると推測された．

1現住所：Cite 67 ha sud Logt 315 ，Antananarivo 101，Madagascar