Ornithol. Sci. 2: 49–58 (2003)
SPECIAL FEATURE Ecology of seed dispersal The role of the Velvet Asity Philepitta castanea in regenera- tion of understory shrubs in Madagascan rainforest
Hajanirina RAKOTOMANANA1,*, Teruaki HINO2,#, Mamoru KANZAKI3 and Hiroyuki MORIOKA4
1 Department of Zoology, Faculty of Science, Kyoto University, Kitashirakawa-Oiwakecho, Sakyo-ku, Kyoto 606–8502, Japan 2 Kansai Research Center, Forestry and Forest Products Research Institute, Kyoto 612–0855, Japan 3 Division of Forest and Biomaterials Science, Graduate School of Agriculture, Kyoto University, Kyoto 606–8502, Japan 4 Department of Zoology, National Science Museum, Tokyo 169–0073, Japan
Abstract In the Madagascan rainforest, the role of the Velvet Asity Philepitta cas- ORNITHOLOGICAL tanea, an endemic frugivorous bird, in the regeneration of five understory shrub SCIENCE species (Myrsinaceae and Rubiaceae) was examined during the dry season (August to © The Ornithological Society October). Effective dispersal distance was 33.3 m/h. Based on seed retention time in of Japan 2003 captivity, more than 85.7% of regurgitated seeds and all defecated seeds were esti- mated to be transported outside the crowns of mother plants. Seeds passed by the Vel- vet Asity germinated less successfully than unmanipulated (control) seeds in four out of the five species of shrubs. The reduced germination rate of processed seeds was partly due to the non-adapted morphology of the Velvet Asity as a seed disperser, in particular its voluminous, thick-walled, muscular gizzard. The narrow, slightly de- curved bill and the semi-tubular tongue with vibrissae at the tip of this bird are nor- mally features of insect- and/or nectar-eaters. Moreover, since manual removal of fruit pulp decreased the germination rate of seeds, the shrub species studied may not have developed adaptations for seed dispersal by animals. The most probable expla- nation for this situation is that the Velvet Asity has shifted relatively recently to oc- cupy the niche of a fruit-eater of the understory and as yet insufficient time has passed for a sophisticated relationship with fruiting plants to have coevolved.
Key words Coevolution, Frugivory, Madagascar, Seed dispersal, Velvet Asity
In tropical forests, many trees bear fleshy fruits eating bird species involved in mutualistic interac- adapted for animal dispersal (Howe & Smallwood tions with such plants, typically have: a wide gape for 1982; Janzen 1983), and the role played by animals, swallowing large fruits whole (Snow & Snow 1988); particularly by birds, is well documented (e.g., Howe a short intestine and a thin-walled, non-muscular giz- 1977, 1981, 1986; Howe & Estabrook 1977; Murray zard for processing seeds gently and evacuating them 1988). That is, birds provide a survival advantage to quickly (Walsberg 1975); and a large liver for detoxi- fruiting plants by allowing them to escape seed pre- fying fruits (Pulliainen et al. 1983). dation near conspecific parent plants (Janzen 1970; The island of Madagascar, because of its ancient Howe 1977; Regal 1977; Hubbel 1980; Gorchov et isolation from Africa, has a unique flora and fauna al. 1993). Most of the plants adapted to bird-dispersal with a high proportion of endemic species, many of have: red or black fruits to attract birds visually which are threatened by the rapid habitat destruction (Willson & Melampy 1983); relatively small fruits and forest fragmentation that has occurred in the last that are easily swallowed by birds (Wheelright 1985); few decades and which continues today (Green & and thin-husked fruit, which are quickly processed by Sussman 1990; Ganzhorn et al. 1997). Understanding birds (Leighton & Leighton 1983). Specialized fruit- the relationships between frugivores and fruiting plants is extremely important for the preservation of (Received 27 September 2002; Accepted 17 December 2002) these forest fragments because such interactions may # Corresponding Author, E-mail: [email protected] * Present address: Department of Animal Zoology, Faculty of Sci- influence plant distribution and floristic heterogeneity ence, University of Antananarivo, Antananarivo 101, Madagas- (Howe 1977). Belher and Böhning-Gaese (in press) car have shown that frugivorous bird species are fewer,
49 H. RAKOTOMANANA et al. and their seed dispersal is far less efficient in Mada- naceae), Aphloia theaformis (Flacourtiaceae), Euge- gascar than in South Africa, while the seeds of Mada- nia spp. (Myrtaceae), Ficus spp. (Moraceae), gascan plants are less well adapted to bird-dispersal Dombeya spp. (Sterculiaceae), Tambourissa spp. than those of South Africa. (Monimiaceae), Ravensara spp. (Lauraceae), Poly- The Velvet Asity Philepitta castanea is endemic to scias spp. (Araliaceae), and Weinmannia spp. Madagascar where it is the only regularly fruit-eating (Cunoniaceae). Large areas of the forest floor are bird species occurring among rainforest understory covered with an introduced exotic plant Psidium catt- shrubs. This species consumes a wide variety of fruits leyanum. The most common epiphyte was Asplenium throughout the year, and also feeds fruits to its young nidus (Aspleniaceae) and the most common orchids as an important dietary component during the breed- were Bulbophyllum spp. and Eulophiella spp. (Orchi- ing season (Rakotomanana & Hino 1998; Rako- daceae). tomanana & René de Roland, in press). Nevertheless, this bird may not be fully adapted to frugivory as in- 2) Bird measurements dicated by its narrow, slightly decurved-bill, a bill External morphometric measurements of Velvet structure more typical of nectar- or insect-eaters Asity were obtained from museum specimens (Cor- (Langrand 1990; Yamagishi et al. 1997). nell University Museum, USA, the Peabody Mu- In this paper we describe research into the role of seum, USA, and the Tsimbazaza Botanical and Zoo- the Velvet Asity in the regeneration of five understory logical Park or PBZT, Madagascar) and from mist- shrub species (Oncostemon leprosum, Psychotria sp. net-captured birds in the field. Their bill, wing, tarsus 1, sp. 6, sp. 8 and Saldinia sp.) in a southeastern and tail lengths were measured to the nearest 0.1 mm Madagascan rainforest. We aimed to answer the fol- using callipers and birds were weighed to the nearest lowing questions: (1) Whether the internal and exter- 0.1 g using a pesola balance. Captured birds were nal morphological characteristics of the Velvet Asity marked with colored plastic bands and released un- are adapted for seed dispersal, or not; (2) How far the harmed after being measured. The tongue and diges- birds disperse seeds by regurgitation and by defeca- tive tract of one individual (taken as a specimen for tion; (3) How successfully the seeds passed by the PBZT), were observed under a light microscope. birds germinate and grow. Based on the results, we Wing areas were also measured and wing loading discuss the relationship that has coevolved between was calculated as: body weight (g)/wing area (cm2), the Velvet Asity and the fruiting plants of Madagas- according to Pennycuick (1975) and Greenwalt car. (1975).
METHODS 3) Field observations of foraging behavior A total of 96 hours of field observations were made 1) Study area between 06:00 and 12:00 or between 14:00 and 17:00 The study was carried out in the Ranomafana trop- from August to October in 1995 and 1996. Once a ical rainforest, about 365 km southeast of the capital bird was found, we followed and recorded its forag- Antananarivo, southeastern Madagascar (21°16 S– ing behavior until it was out of sight (using 10 40 47°28 E), at an altitude of 800 to 1200 m above sea binoculars and a tape recorder), using a continuous level. The study area was ca. 12.3 ha with many trails recording method (Martin & Bateson 1986). Both un- and paths. Two main seasons occur in the area: a marked and marked birds (4 males and 11 females) rainy season (November–April) and a dry season were followed. One sequence of continuous record- (May–October). The annual precipitation was 2,600 ing averaged 69.8 min (range: 30–201 min, N 40 se- mm (Nicoll & Langrand 1989) and the mean annual quences). During each observation period, the times temperature was about 21.4°C (Ranomafana-Ifanadi- when birds visited and left each plant, and the forag- ana Station). ing behavior of the focal bird, were recorded. The The vegetation was characterized by discontinuous shrubs and trees that the birds visited were tagged canopy layers composed of scattered trees 20–30 m with plastic tapes and marked on a map. For each high. Trees over 30 m tall were rare in the forest, movement, the distance in a straight line from the ini- whereas the middle-canopy layer (4–10 m) was quite tial location where the bird was encountered was dense. Trees and shrubs consisted mainly of Psycho- measured on this map. Median distances were calcu- tria spp. (Rubiaceae), Oncostemon spp. (Myrsi- lated for every five-minute interval spent in move-
50 The Velvet Asity and regeneration of shrubs ment from the initial locations. A quadratic equation into two groups; in one group (manipulated seeds) was devised to express the relationship between dis- the pulp was manually removed, in the other group tance traveled and time elapsed during foraging (control seeds) the pulp remained intact. Processed movements. and non-processed seeds (excluding insect-damaged seeds) were used for germination experiments. Be- 4) Experimental determination of seed retention cause all of the seeds of O. leprosum went rotten after times defecation by the Velvet Asity, and because very few From August to October 1996, five Velvet Asity (2 Psychotria sp. 8 seeds were defecated, defecated males and 3 females) were mist-netted, and kept for seeds could not be investigated in these two species. experimental determination of seed retention time Forty to two hundred seeds were used in germina- (SRT) of five common fruiting species: O. leprosum, tion experiments of each seed treatment of each shrub Psychotria sp. 1, sp. 6, sp. 8 and Saldinia sp. (Psy- species. Seeds were planted in sand in small contain- chotria species were identified by number, as their ers (28.5 cm length 24.5 cm width 5 cm height). species names are not known; see Appendix 1). In the The experiments were carried out in a glasshouse field, each captured individual was temporarily under constant luminosity and at a constant tempera- housed in a small cage (1 m 1m 1 m) for a maxi- ture of 24°C. Watering was twice a week. The germi- mum of five hours, and supplied with ripe fruits of nation of seeds, seedling survival, and seedling stem the target plant. One trial was conducted for each in- lengths, were all monitored at weekly intervals for dividual, and water was available during each trial. 100 days after sowing. The number of fruits consumed was counted and the time from consumption to evacuation of seeds by re- RESULTS gurgitation and defecation was measured using a stopwatch. Since uneaten fruits were removed five 1) Morphological characteristics minutes after the first fruit was consumed, the num- The average body weight and external morpho- ber of ingested seeds differed among species (Appen- metric measurements (accompanied with standard dix 2). Since we did not know exactly when the seeds deviation and sample size in parentheses) of the evacuated were ingested, we used, as the time of in- adults were: body weight 8.9 3.2 g (19); bill gestion, the midpoint of the interval during which length 18.1 1.9 mm (55), bill width 6.0 0.9 mm fruits was consumed. Unclear data were removed (55); bill depth 5.1 0.4 mm (55); tarsus length from the analysis because determination of SRT is 24.3 2.4 mm (53); wing length 82.1 0.3 mm (55); critical to the estimation of effective seed dispersal. tail length 42.5 0.5 mm (55). The bill was narrow After each trial, the bird was released unharmed. (width/length 0.33 0.05 and depth/length 0.28 Processed seeds were classified as regurgitated 0.04), and slightly decurved. (clean) and defecated (mixed with feces). Some SRT The wing loading averaged 0.53 g/cm2 (2), and the followed by regurgitation data were also obtained wing tip has poorly developed slots (Rakotomanana through direct observation in the field. unpublished data). The tongue was semi-tubular with The distribution of the seeds dispersed (i.e. the a deep cleft (5 mm in length) anteriorly with vibrissae seed shadow) by the Velvet Asity was estimated at the tip (Fig. 1). The intestine was about 20 cm long based on SRT followed by regurgitation or by defeca- and there was a muscular thick-walled (ca. 4 mm), tion, for each shrub species, using the movement dis- voluminous gizzard (averaging 3% of body weight). tance-time equation. Data relating to Psychotria sp. 1 and sp. 6, which have similar-sized seeds (Appendix 2) Foraging movements and behavior 2), were combined owing to the small SRT sample Among foraging observations of the Velvet Asity sizes for each species. 91.1% of items were ripe or partially-ripe fruits taken from understory shrubs ( 7.5 m in height) belonging 5) Seed-germination experiment to the Rubiaceae and Myrsinaceae. The size and Processed seeds (regurgitated and defecated by the shape of fruits and the size and number of seeds var- Velvet Asity) and non-processed seeds (naturally- ied among shrub species (Appendix 1). During field fallen fruits) of the five shrub species were collected observations, birds were observed to take from 1 to from the forest floor and dried in a cool place over 16 fruits from one shrub, depending on the size or several weeks. Non-processed seeds were divided abundance of fruits. The seeds were either regurgi-
51 H. RAKOTOMANANA et al. tated or defecated away from the parent plants. The swallow them whole without manipulating them with seeds of almost all of the larger fruits, such as Psy- its bill. All the seeds appeared to be voided intact chotria sp. 8, were regurgitated, not defecated. through regurgitation and defecation. More than 60% The median distances of movement, measured in a of regurgitation of all five shrub species’ seeds, was straight line from the initial encounter point, in- observed within 5–10 min after ingestion (Fig. 3). creased almost linearly with increasing time and to SRT data were obtained for O. leprosum in the field 33.3 m in one hour (Fig. 2). The maximum distance and experimentally, but there was no significant dif- was 58.4 m. ference between them (c 2 test 2.5, df 4, P 0.05). No seeds of Psychotria sp. 8 were observed to be 3) Seed retention time and seed-shadow defecated either in the field or in captivity (Appendix The Velvet Asity was observed to pluck fruit and 2). SRT followed by defecation was more variable than SRT followed by regurgitation, with the excep- tion of Saldinia sp. SRTs of the seeds of Psychotria sp. 1 and sp. 6 were longer than those of O. leprosum and Saldinia sp. (Fig. 4; Mann Whitney’s U test, Psy- chotria sp. 1, sp. 6/O. leprosum, z 4.7, P 0.001, Psychotria sp. 1, sp. 6/Saldinia sp., z 5.7, P 0.001 and O. leprosum/Saldinia sp., z 1.7, NS). The estimated maximum distances of dispersal by regurgitation were 18.2 m in O. leprosum, 5.4 m in Saldinia sp, 6.7 m in Psychotria sp. 1, 18.7 m in Psy- chotria sp. 6, and 13.8 m in Psychotria sp. 8 (Fig. 5). Defecated seeds were transported farther than regur- gitated seeds (Fig. 4). The dispersal distances by defecation were estimated to range from 8.5 m to 18.7 m in O. leprosum, from 9.1 m to 15.4 m in Sal- dinia sp, and from 14.4 m to 29.0 m in Psychotria sp. 1 and sp. 6. The average crown diameters of the un- derstory shrubs were 1.6 0.8 m in O. leprosum, 1.9 m 0.6 m in Psychotria sp. 1, 1.6 0.5 m in Psycho- Fig. 1. (a) The whole tongue and (b) tongue tip of P. cas- tria sp. 6, 2.8 0.9 m in Psychotria sp. 8, and tanea.
Fig. 2. Relationship between time and median distance of movement in a straight line from the initial encounter point.
52 The Velvet Asity and regeneration of shrubs
Fig. 3. SRT of seeds regurgitated by P. castanea for each of five shrub species.
Fig. 4. SRT of seeds defecated by P. castanea for each of five shrub species. Arrows correspond to median pas- sage times.
1.7 0.6 m in Saldinia sp. (N 20 for each species). Velvet Asity has a negative effect on the germination Thus for all of the five shrub species more than of the seeds of four of the five shrub species (Psycho- 85.7% of the regurgitated seeds and all of the defe- tria sp. 8 was the exception) (Table 1). The processed cated seeds were estimated to be transported beyond and manipulated seeds of Saldinia sp., Psychotria sp. the crown of the mother plant. 1 and Psychotria sp. 6 germinated less successfully than their control seeds. The processed seeds of O. 4) Germination ratios and growth rates of processed leprosum all went rotten before germination, although and non-processed seeds the germination ratio of manipulated seeds was Seed-germination experiments revealed that the higher than the control seeds. No differences in ger-
53 H. RAKOTOMANANA et al.
Fig. 5. Estimated seed shadow produced by regurgitation and defecation for each of five shrub species.
Table 1. Cumulative germination ratios (%) of seeds at 100 days in four treatments for five shrub species. Sample sizes are shown in parentheses. The same letters indicate significant differences between treatments for each species, with Fisher’s exact test (Bonferroni’s method, P 0.05).
Oncostemon Psychotria sp. 1 Psychotria sp. 6 Psychotria sp. 8 Saldinia sp. leprosum
Control 11.7 (60)a 37.5 (200)abc 55.0 (200)abc 14.5 (200)ab 66.5 (200)abc Manipulated 35.0 (60)ab 17.0 (100)ad 25.0 (100)a 39.0 (100)a 30.5 (200)a Regurgitated 0.0 (24)b 6.0 (200)bd 11.0 (50)b 39.0 (100)b 40.0 (80)b Defecated – 7.0 (100)c 8.0 (50)c – 32.0 (50)c c 2 17.4 77.5 148.7 65.9 58.3 d.f. 2 3 3 2 3 P .001 .0001 .0001 .0001 .0001
–: Not investigated. mination rates were found between regurgitated and the seedlings that germinated from defecated seeds defecated seeds in four species. For Psychotria sp. 8, were significantly taller than, or not different from, however, regurgitated and manipulated seeds germi- those from other treatments, although those from re- nated more successfully than the control seeds. gurgitated seeds were shorter than their control seeds. On the other hand, the Velvet Asity had a positive In O. leprosum and Psychotria sp. 8, for which defe- effect on the growth rates of seedlings after germina- cated seeds were not investigated, the seedlings that tion. In Psychotria sp. 1 and sp. 6 and Saldinia sp., germinated from manipulated or regurgitated seeds
54 The Velvet Asity and regeneration of shrubs
Table 2. Stem lengths (mean SD) of seedlings at 100 days after sowing in four treatments for five shrub species. Sample sizes are shown in parentheses. The same letters indicate significant differences between treatments for each species, with post-hoc F- test (Bonferroni’s method, P 0.05).
Oncostemon Psychotria sp. 1 Psychotria sp. 6 Psychotria sp. 8 Saldinia sp. leprosum
Control 20.0 1.2 (7)a 29.0 0.7 (70)abc 25.0 0.8 (105)ab 15.0 0.8 (26)ab 31.0 1.1 (130)abc Manipulated 30.0 0.9 (14)a 23.0 0.6 (12)ade 26.0 1.0 (12)ac 35.0 0.8 (39)ac 27.0 0.8 (51)ade Regurgitated – 24.0 0.7 (12)bdf 21.0 1.3 (6)bcd 40.0 1.1 (33)bc 28.0 0.8 (30)bdf Defecated – 30.0 0.8 (7)cef 25.0 0.8 (4)d – 35.0 0.8 (14)cef F 492.6 358.6 5746.1 357.6 357.6 d.f. 1 3 3 2 3 P .0001 .0001 .0001 .0001 .0001
–: Not investigated. were significantly taller than those from the control partially a seed predator. Although the Velvet Asity’s seeds (Table 2). narrow, slightly decurved bill, and its semi-tubular tongue with vibrissae at the tip, may help it obtain in- DISCUSSION sects (Gardner 1925) and/or nectar, these characteris- tics are unlikely to be useful for seed-eating (Amadon The seed shadow produced by the Velvet Asity in- 1950; Richard & Bock 1973). dicates some contribution of this bird to the seed dis- Only Psychotria sp. 8 which produces seeds with a persal of shrubs in the Madagascan rainforest, al- thick, hard seed coat, benefited from processing in though the maximum dispersal distance (58.4 m) was the Velvet Asity’s gut, and from artificial manipula- much shorter than that of Neotropical frugivorous tion. This species of shrub may have adapted to seed birds (ca. 220–510 m, Murray 1988). The short dis- dispersal by the Velvet Asity, although its foraging persal distances recorded in Madagascar might be preference was not high when compared with other due to the Velvet Asity’s aerodynamically non-ad- species owing to the large size of its fruits (Rako- vanced wing features, such as its short wings, high tomanana & Hino 1998). Since the control seeds, wing loading, and poorly slotted wing, which would with pulp, germinated more successfully than manip- produce poor lift and acceleration during flight (Sav- ulated seeds, without pulp, however, the shrub ile 1957; Pennycuick 1969, 1975; Norberg 1981; species other than Psychotria sp. 8 may not have de- Rayner 1981; Rakotomanana 1998). veloped adaptations for seed dispersal by animals in- The Velvet Asity has some of the general features cluding birds. of specialized fruit-eaters, including, for example, a How do we explain the current relationship be- diet consisting mostly of fruits (Snow 1980; Morton tween the Velvet Asity and the understory shrub 1973), great attentiveness and faithfulness to fruiting species, in which the asity appears to be a partial seed plants, the habit of regurgitating seeds, rapid passage predator, but one that carries seeds some distance of seeds through the gut (McKey 1975), and posses- from the mother plant? The most probable explana- sion of a short digestive tract (Desselberger 1931; tion is that the Velvet Asity has shifted relatively re- Docters Van Leeuwen 1954; Walsberg 1975). The de- cently from being an insect- and/or nectar-eater to creased germination ratios of seeds regurgitated or being a frugivore in the understory and as yet insuffi- defecated by the Velvet Asity demonstrate, however, cient time has passed for a sophisticated relationship that this species may not be adapted for dispersing with fruiting plants to have coevolved. That a niche seeds of fruiting plants. The rough chemical and shift may have occurred, is indicated by the morpho- physical treatment experienced inside the bird’s mus- logical structure of the Velvet Asity’s bill and tongue, cular, thick-walled, voluminous gizzard, which is and by observations that show that it takes arthropods twice the size of that of a specialized frugivorous bird and nectar on rare occasions (Prum & Razafindratsita such as Phainopepla nitens (Walsberg 1975), may 1997; Rakotomanana et al. in press). In addition, two cause seed damage, indicating that the Velvet Asity is species of Sunbird-Asity Neodrepanis coruscans and
55 H. RAKOTOMANANA et al.
N. hypoxantha, which are classified in the same en- tion also goes to the following institutions: Direction demic family, Philepittidae, as the Velvet Asity, and Générale des Eaux et Forêts, Ranomafana National Park considered to have the same ancestral origins as the Project, Silo National des Graines Forestiéres, Velvet Asity, both feed mainly on nectar and insects Douroucouli Foundation, Yale University, Cornell Uni- and have long, thin, decurved bills (Langrand 1990; versity and World Wide Fund for Nature, the Laboratory Morris & Hawkins 1998) and tubular tongues of Animal Sociology and Laboratory of Plant Ecology (Morioka, unpublished). (Osaka City University) and Laboratory of Animal Be- In Madagascar, lemurs are also important seed-dis- haviour (Kyoto University) for their cooperation in the persers. In the same forest in which our study site realization of the present study. This study was sup- was located, Dew and Wright (1998) have shown that ported by the Japanese Government and a Grant under seeds passed by lemurs germinate more successfully, the Monbusho International Scientific Research Pro- gram (Field Research No. 06041093). and grow faster than those not passed by lemurs, in- dicating mutualistic adaptations between lemurs and fruiting plants. Dew and Wright (1998) also sug- REFERENCES gested that fruits more than 10 mm in diameter are Amadon D (1950) The Hawaiian honeycreepers (Aves: most likely to be dispersed by lemurs, while those Drepaniidae). Bull Am Mus Nat Hist 95: 151–262. less than 10 mm in diameter are most likely to be dis- Belher B & Böhning-Gaese K (in press) The role of persed by birds. The fruits of four of the five shrub birds in seed dispersal and its consequences for forest species we studied were less than 10 mm in diameter, ecosystem. Acta Zool Sinica (Suppl). only Psychotria sp. 8 fruits were larger. Evidently, Desselberger H (1931) Der Verdauungskanal der Dicae- based on fruit size, seed dispersal of these fruiting den nach Gestalt und Funktion. J Ornithol 79: plants should depend primarily on birds. If they are 353–370. indeed dependent on the Velvet Asity for seed disper- Dew JL & Wright P (1998) Frugivory and seed disper- sal, how have these fruiting plants maintained their sal by four species of primates in Madagascar’s East- populations in spite of their low germination success ern rain forest. Biotropica 30: 425–437. rate? In order to understand the dynamics of under- Docters van Leeuwen WM (1954) On the biology of story shrub survival it is necessary to examine plant some Javanese Loranthaceae and the role birds play seed dispersal in more detail, examining not only the in their life histories. Beaufortia 4: 105–205. contribution of the Velvet Asity, but also that of occa- Gardner LL (1925) The adaptive modifications and tax- sional frugivorous visitors such as the Madagascar onomic value of the tongue in birds. Proc US Nat Bulbul Hypsipetes madagascariensis, the Red- Mus 67: 1–49. fronted Brown Lemur Eulemur fulvus rufus and the Ganzhorn JU, Langrand O, Wright PC, O’Connor S, Red-bellied Lemur Eulemur rubriventer, and bats Rakotosamimanana B, Feistner ATC & Rumpler Y such as Pteropus rufus and Rousettus madagas- (1997) The state of Lemur conservation in Madagas- cariensis. car. Prim Conser 8: 1–12. Green G & Sussman RW (1990) Deforestation history of the eastern rain forest of Madagascar from satellite ACKNOWLEDGMENTS images. Science 248: 212–215. Greenwalt CH (1975) The flight of birds. Trans Am Phil We are grateful to S. Yamagishi, M. Imafuku and A. Soc New Ser 65:1–67. Mori for their critical reading and comments on the pre- Gorchov DL, Cornejo F, Ascorra C & Jaramillo M liminary draft of this paper and to M. Brazil for lan- (1993) The role of seed dispersal in the natural regen- guage editing. We are also indebted to A. Randrianjafy eration of rain forest after strip-cutting in the Peru- and other staff of the PBZT, R. Rakotonindrina and vian Amazon. Vegetatio 107/108: 337–349. other staff of Association Nationale pour la Gestion des Howe HF (1977) Bird activity and seed dispersal of a Aires Protégées for facilitating the administration, P. tropical wet forest tree. Ecology 58: 539–550. Wright and J. Rakotomalala for arranging the use of pre- Howe HF (1981) Dispersal of a neotropical nutmeg (Vi- liminary research facilities, and R. L. Ramamonjisoa rola sebifera) by birds. Auk 98: 88–98. and H. Razafiarisoa for collaborating in the germination Howe HF (1986) Seed dispersal by fruit-eating birds experiments. This study would have not been possible and mammals. In: Murray DR (eds) Seed Dispersal. without the essential help of S. Rakotomanana, D. Ran- pp 123–189. Academic Press, Sydney. drianantenaina and P. Rasabo in the field. Our apprecia- Howe HF & Estabrook GF (1977) On intraspecific com-
56 The Velvet Asity and regeneration of shrubs
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57 H. RAKOTOMANANA et al.
Appendix 1. Fruit characteristics of five srub species.
Oncostemon Psychotria Psychotria Psychotria Saldinia leprosum sp. 1 sp. 6 sp. 8 sp.
Plant family Myrsinaceae Rubiaceae Rubiaceae Rubiaceae Rubiaceae Fruit colour red red blue red blue Fruit type berry berry berry berry berry Fruit shape round ovoid ovoid ovoid round Seeds number 1 1 or 2 1 or 2 1 or 2 1 or 2 Average fruit size (mm)a 7.1 5.9 7.3 11.9 8.2 Average seed size (mm)b 4.9 4.7 4.8 9.6 2.8 a: Number of sample is 60 for each species. b: Samples were 122, 30, 84, 42 and 185 in the order of species from the left.
Appendix 2. The number of fruits ingested and seeds processed by the Velvet Asity for each shrub species in the cage experi- ment.
Oncostemon Psychotria Psychotria Psychotria Saldinia leprosum sp. 1 sp. 6 sp. 8 sp.
Ingested fruits 139 35 50 7 52 Regurgitated seeds 125 24 42 14 2 Defecated seeds 14 18 2 0 50
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