The Role of the Velvet Asity Philepitta Castanea in Regeneration Of
Total Page：16
File Type：pdf, Size：1020Kb
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°16ЈS– ing behavior until it was out of sight (using 10ϫ40 47°28ЈE), 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, Nϭ40 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.