ORNITOLOGIA NEOTROPICAL 24: 459–468, 2013 © The Neotropical Ornithological Society FEEDING BEHAVIOR, BIRD VISITATION, AND SEED DISPERSAL IN GUAREA MACROPHYLLA AND TRICHILIA QUADRIJUGA (MELIACEAE) Federico A. Prado1 Department of Biology, Texas State University, San Marcos, TX 78666, USA. 1Current address: 1740 NE 86th St, Apt 217, Seattle, WA 98115, USA. E-mail: [email protected] Resumen. – Comportamiento alimenticio, visita de aves y dispersión de semillas en Guarea macrophylla y Trichilia quadrijuga (Meliaceae). - Estudié en el Parque Nacional Manu, Perú, el com- portamiento alimenticio, la actividad de aves y la dispersión de semillas en dos árboles simpátricos neo- tropicales de selva húmeda, Guarea macrophylla y Trichilia quadrijuga. Los números de individuos, de especies visitantes y de semillas removidas correlacionaron directamente con el tamaño de la cosecha de frutas disponibles en cada especie de planta. De 18 especies de aves que consumieron frutos de Guarea, solo cuatro (Catharus ustulatus, Myiodynastes luteiventris, Lepidothrix coronata, y Pipra fascii- cauda) la visitaron consistentemente y dispersaron sus semillas. De tres especies de aves que consu- mieron frutos de Trichilia, dos (Pipra fasciicauda y P. chloromer os) visitaron y dispersaron sus semillas regularmente. La variación en la cantidad de tiempo en los árboles frutales entre y dentro de cada espe- cie fue alta. La mayor actividad ocurrió entre las 07:00 hs y las 10:00 hs. Con pocas excepciones, todas las aves visitantes se posaron en el árbol observado y removieron frutos en vuelo o desde una percha cercana. El número de unidades de pulpa ingeridas varió de cero a seis, dependiendo del ave. Pocas semillas cayeron bajo el árbol. Abstract. – In Manu National Park, Peru, I investigated feeding behavior, bird activity on and seed dis- persal of two sympatric Neotropical rain forest trees, Guarea macrophylla and Trichilia quadrijuga. The numbers of individual visitors, visiting species, and seeds removed were directly correlated to the avail- able fruit crop for each plant species. Of 18 bird species which consumed Guarea fruits, only Swainson’s Thrush (Catharus ustulatus), Sulphur-bellied Flycatcher (Myiodynastes luteiventris), Blue-crowned Manakin (Lepidothrix coronata), and Band-tailed Manakin (Pipra fasciicauda) consistently visited and dispersed its seeds. Of three bird species which consumed Trichilia fruits, only Band-tailed and Round- tailed Manakins (P. chlor omeros ) regularly visited and dispersed its seeds. Variance in the time spent at fruiting trees across and within bird species was high. Most bird activity occurred between 07:00 h and 10:00 h. With few exceptions, all visiting birds perched in the observed tree and then removed fruit either in flight or by reaching from a nearby perch. The number of ingested pulp units per visit ranged from zero to six depending on the bird. Few seeds were dropped under the parent tree. Accepted 25 February 2014. Key words: Sulphur-bellied Flycatcher, Swainson’s Thrush, Pipridae, Guarea macrophylla, Trichilia qua- drijuga, avian seed dispersal, migrant bird visitation. INTRODUCTION whose fruits they consume. This mutualistic relationship has sparked interest in the evolu- Many frugivorous animals play an essential tionary consequences of frugivory and seed role in the reproductive biology of the plants dispersal for animals and plants (McKey 1975, 459 PRADO Howe 1981, Howe & Smallwood 1982, Her- stripped from the olive-green seeds which are rera 1985, 1986; Estrada & Fleming 1986, regurgitated or excreted. Fruits have from Fleming & Estrada 1993). In spite of the tre- zero to three seeds, although fruits with more mendous effort to understand frugivory and than three seeds have also been observed seed dispersal, however, observational data on (Foster pers. comm.). Mean food intake from many tropical tree species is sparse. A few this fruit is 0.14 g or 54% of pulp unit mass Guarea and Trichilia (Meliaceae) species have (Prado 1999). received attention: G. glabra (Howe & De Ste- Here I list the birds that visited these ven 1979, Wheelwright et al. 1984, Wenny plant species, try to differentiate seed dispers- 1999), G. kunthiana (Wenny 1999), G. tonduzii, ers from seed predators, and note avian feed- G. tuisiana, and T. havanensis (Wheelwright et ing behavior and bird activity at trees of these al. 1984), T. cuneata (Leck 1969, Foster & species. The data reported here will be useful McDiarmid 1983), and T. micrantha (Argel-de- to researchers studying plant and bird conge- Oliveira 1992). Knowledge of seed dispersal ners in other places, and will also serve as use- in G. macrophylla and T. quadrijuga is lacking. I ful baseline data for anyone carrying out a chose to study these two ornithochorous longitudinal study of plant-frugivore interac- plants because: a) they belong to the same tions at Manu National Park. family, b) they have similar fruit types, i.e., capsules that dehisce to expose seeds covered METHODS with bright red-orange or red arils, c) they have an equal average arilloid (seed with aril) Study site. Observations were made in the mass of 0.27 g, and d) they fruit in the study mature floodplain forest around Cocha Cashu site at roughly the same time. These plant Biological Station in Manu National Park, species, however, differ in average aril mass Peru (11°53’17”S, 71°24’27”W, approximately (see below), and apparent nutritional value of 400 m a.s.l.). Located on the fringes of the the aril (Guarea oily, Trichilia watery). equatorial zone, the climate at the station has Fruits of G. macrophylla are borne on a well-defined wet season from mid October racemes on the terminal ends of branches. to April, followed by a dry season from May They have a thick, woody, bumpy, dull purple- through September. The mean annual tem- brown exocarp. When the fruit is ripe, the perature is between 23° C and 24° C, and capsule dehisces longitudinally forming four rainfall exceeds 2000 mm (Terborgh et al. sections and exposing from 4 to 10 bright 1990). A thorough description of the study red-orange arillate seeds. These are plucked site, including climate, vegetation, habitat and ingested whole by birds, the oily red arils types, and fruiting phenology can be found in stripped off, and the yellow-white seeds Terborgh (1983). regurgitated or defecated intact. The average food intake is 0.034 g or 12.6% of the pulp Study species. Two Neotropical plants, Guarea unit (Prado 1999). macrophylla Vahl ssp. pachycarpa and Trichilia The exocarp of a T. quadrijuga fruit is rela- quadrijuga Kunth in HBK ssp. quadrijuga, tively thin, soft, smooth, bright orange in family Meliaceae, were observed. The species color and is borne singly at the tips of small reach heights of 25 m and 30 m, respectively branches. When ripe, the three-part capsule (Roosmalen 1985). I collected data at the end dehisces to expose a single juicy, bright red of the dry season and beginning of the rains, pulp unit. As in Guarea, these are plucked and between 14 October and 16 November, 1998. swallowed by birds, and the juicy red flesh is During this period, both Guarea and Trichilia 460 AVIAN SEED DISPERSAL IN MELIACEAE SPP. came into fruit. Further information on the ing periods, I identified birds that visited each natural history and distributions of these two tree, recorded the length of their stay in sec- genera can be found in Pennington (1981) onds with a stopwatch, and recorded time of and Gentry (1993). day. Observations were not made equally across all hours, due to rain or lack of avail- Study trees. I selected three large fruiting trees able fruit. To estimate bird activity throughout of G. macrophylla (trees # 1, 2, and 3) and three the day, I divided the total number of individuals of T. quadrijuga (trees # 4, 5, and recorded visits during each hour by the num- 6). The plants were identified by their fruits ber of hours for which observations were and leaves (Roosmalen 1985) and by compari- made during that hour. sons to photocopies of herbarium sheets. I noted whether each bird perched in the From two additional trees of T. quadrijuga, I tree, its feeding behavior (in air or sallying, collected fruit for aril and seed measurements. perching and reaching up or down), number The number of hours each tree was observed, of pulp units ingested per visit (if any), along with approximate height and forest type method of ingestion (swallow whole, bite or are as follows: tree # 1(30 h, 10 m, mature mash), whether seeds were dropped under the high-ground), tree # 2 (30 h, 7 m, flood-dis- tree or carried away (i.e., beyond the tree turbed), tree # 3 (33 h, 7 m, mature high- crown). When more than one bird visited the ground), tree # 4 (28 h, 4 m, late succes- tree, I kept the stopwatch running and sional), tree # 5 (23 h, 3 m, flood-disturbed), stopped it after the last bird had flown away. and tree # 6 (20 h, 3 m, late successional). During these occasions, I simply recorded the Observations were made at a distance of 10 to bird species present, any ingested fruits that I 15 m from each tree to minimize disturbance determined with certainty, and estimated the to visiting birds, and for a time proportional length of visit in seconds for each bird as fol- to tree size and quantity of fruits available. I lows: If the first bird to arrive was not the last did not observe trees from which I collected to leave, I divided the total recorded time for fruit. I covered five terminal racemes on each all visitors by the total number of birds in that of two trees of G. macrophylla with thin cotton period. Otherwise, if the first bird to arrive netting and counted the number of dehisced was also the last one to leave, I used the total fruits in each mesh bag at the beginning of time recorded as the length of the visit for each observation day.