Condor, 82:3142 @ The Cooper Ornithological society 1980 ARILS AS FOOD OF TROPICAL AMERICAN BIRDS ALEXANDER F. SKUTCH ABSTRACT.-In Costa Rica, 16 kinds of trees, lianas, and shrubs produce arillate seeds which are eaten by 95 species of birds. These are listed and compared with the birds that feed on the fruiting spikes of Cecropia trees and berries of the melastome Miconia trinervia. In the Valley of El General, on the Pacific slope of southern Costa Rica, arillate seeds and berries are most abundant early in the rainy season, from March to June or July, when most resident birds are nesting and northbound migrants are leaving or passing through. The oil-rich arils are a valuable resource for nesting birds, especially honeycreepers and certain woodpeck- ers, and they sustain the migrants. Vireos are especially fond of arils, and Sulphur-bellied Flycatchers were most numerous when certain arillate seeds were most abundant. Many species of birds take arils from the same tree or vine without serious competition. However, at certain trees with slowly opening pods, birds vie for the contents while largely neglecting other foods that are readily available. Although many kinds of fruits eaten by during the short time that the seed remains birds may be distinguished morphological- in the alimentary tract of a small bird. ly, functionally they fall into two main Wallace (1872) described how the Blue- types, exemplified by the berry and the pod tailed Imperial Pigeon (Duculu concinnu) containing arillate seeds. Berries and ber- swallows the seed of the nutmeg (Myristicu rylike fruits are generally indehiscent; no frugruns) and, after digesting the aril or hard or tough integument keeps animals mace, casts up the seed uninjured. Several away from the edible tissue. In contrast to species of large fruit pigeons (Duculu my- a berry, which develops from the ovary, an risticivoru, D. luctuosu, D. bicolor, and D. aril is an outgrowth of the ovule, or of the spilorrhou) are sometimes known as “nut- funicle which attaches it to the placenta. An meg pigeons,” and the last two are reported aril may partly or completely cover the to eat wild nutmegs (Goodwin 1967). The seed. Accordingly, each seed has its own Many-colored Fruit Dove (Ptilinopus per- aril, although, when seeds are many and ousii) of Samoa and neighboring islands is small, their arils may be massed together. also known as the “nutmeg dove.” Pijl Arillate seeds are commonly enclosed in (1952) recognized the role of arils in the dis- tough or woody pods or capsules, which persal of seeds of tropical plants by birds, protect them until mature, at which time the and gave several examples, including pods split open to expose the seeds promi- species of New World origin. In a long list nently. Arils and pods are often of contrast- of fruits eaten by tanagers and honeycreep- ing colors: an aril may be white in a red or ers on Trinidad, Snow and Snow (1971) in- yellow pod, or red between yellow valves, cluded many species with arillate seeds, the whole conspicuous amid green foliage, belonging to the genera Clusiu, Sloaneu, easily found by hungry animals, who may Pro&m, Alchorneu, Supium, Duvillu, and disperse the seeds. Lucistemu, but they did not give special at- Rarely, as in granadillas or maypops (Pas- tention to arils. sifloru spp.), arillate seeds are enclosed in I present here my own observations on a thin, indehiscent pod. Arils of certain pas- arils and the birds that eat them, amplifying sion flowers are also exceptional in being my earlier account (Skutch 1971). Unless sweetish, although most others that I have otherwise stated, my observations were tasted have no evident sugar but are often made at “Los Cusingos,” which is situated slightly bitter. Many arils are poor in starch between Santa Elena and Quizarra in the but rich in lipids and proteins (McDiarmid Valley of El General, on the Pacific slope of et al. 1977). Oils or fats are the chief non- southern Costa Rica, at about 750 m above nitrogenous reserves of many seeds, and ar- sea level. These records have been gath- ils develop from the seeds themselves. ered over many years, but more intensively Within the soft aril is a seedcoat that is often during the last four. For comparison, I list hard, or somehow able to resist digestion the birds that I have seen eat two other at- 32 ALEXANDER F. SKUTCH , lcm, FIGURE 1. Compsoneuru Sprucei. Above: A seed enclosed in its bright red aril hangs between the two pale yellow valves of the open pod. Below: A seed removed from its aril. It is pale brown, mottled with deep brown. i -; % z tractive plant foods, the berries of a mela- .c -5 stome and the pistillate spikes of Cecropia : trees. Lacking means to make quantitative % analyses of arils, I tested for starch by the B iodine reaction and looked for globules or g c larger flows of oil in microscopic prepara- $ tions. Scientific names of birds not given in 5 the text will be found in Table 2. ; z 9 THE ARILLATE SEEDS AND THE * 3 BIRDS THEY ATTRACT Virola spp. (Myristicaceae). These big trees of humid forests at low altitudes bear ellip- soid capsules that, while still attached to the twigs, split into two valves, between which hangs a single, large arillate seed. The bright red aril divides near the base into narrow or broad, strap-shaped branches, be- tween which the shiny, brown seed is partly ARILS AS FOOD 33 visible (Table 1). The aril contains much oil but little or no starch. To me, it is pleasantly spicy when ripe but painfully hot and pep- pery when not quite mature. I have seen only fairly large birds swallow these big seeds. In El General, those of V. Koschnyi are taken by Blue-diademed Motmots, Ru- fous Pihas, Masked Tityras, Grays’ Thrush- es, and White-throated Thrushes. The thrushes try strenuously to eat the whole, lcm ) , lcm , +2mm, aril-covered seed, sometimes failing to do so. FIGURE 2. Siparuna nicuraguensis. Left: A pale red In the Panama Canal Zone, I have seen ripe receptable. Center: A receptacle that has opened Collared Aracaris (Pteroglossus torquatus) exposing nine seeds attached to the rough, pale red inner surface. Right: A single shiny gray seed, with a and Massena Trogons (Trogon massena) eat bright red aril covering half its surface, and a small red the slightly smaller seeds of V. panumensis; caruncle at its lower left. Chapman (1929) reported their consump- tion by the Rufous Motmot (Baryphthengus ruficupillus) and Chestnut-mandibled Tou- can, and Van Tyne (1929) included them spicy taste and is rich in oil but contains among the fruits eaten by the Keel-billed little or no starch. Ochre-bellied Pipromor- Toucan. Seeds of V. surinumensis are eaten phas, Blue Honeycreepers, and Blue-black by the Red-billed Toucan (Rumphastos tu- Grosbeaks (Cyunocompsu cyunoides) cunus) (Bourne 1975), Capuchinbird or pluck the seeds one by one from the pale Calfhird (Perissocephulus tricolor; Snow red inner surface of the receptacle. 1972) and Bearded Bellbird (Procnius uv- Zunthoxylum spp. (Rutaceae). These eruno; Snow 1970). trees with thorny trunks bear large panicles Compsoneuru Sprucei (Myristicaceae). of small capsules, which in some species are This small, slender tree, up to 12 m high, is so covered by projecting oil glands that they widely scattered through the rain forest at resemble miniature strawberries. At maturi- Los Cusingos. Its pale yellow pods open by ty each pod splits into two valves, permit- two valves, exposing a single, bright red, ting the single black, shiny seed to slip out arillate seed (Fig. 1). Unlike the aril of the and stand above it upon the short, thread- related Virolu, this aril, about 0.5 mm thick, like funiculus (Table 1). The thin, oil-rich, is almost entire, covering like a sleeve the black aril, nearly tasteless to me, covers a pale brown seed, mottled with deeper hard, indigestible seed coat. In October brown (Table 1). The open fruits, hanging 1936, on the northern side of the Valley of beneath slender leafy twigs, are conspicu- El General at an altitude of about 890 m, I ous. Of all the arils that I have examined, watched a tree as its seeds (3 mm in diam- only these contain much starch, as well as eter) were sought by Blue Honeycreepers, a fair amount of oil. They would appear to who came in groups of three to six or seven be most attractive to birds; yet, I have never individuals. Other birds that ate these seeds seen any bird pluck them, probably because included the Scarlet-thighed Dacnis (Duc- each tree bears too few to draw many visi- nis venustu), Golden-masked Tanager, and tors, and to watch it in dense forest one must Ochre-bellied Pipromorpha. stand too near. I have seen Blue-diademed At a Zanthoxylum tree of another species, Motmots carry many of the seeds to nest- growing at about 1,700 m in the Costa Rican lings, who left some uneaten in their bur- mountains, in March 1938, the tiny black row. Placed on a feeder, these nutritious ar- seeds were eaten by Gray-capped Flycatch- ils were neglected by the birds; and ers, Vermilion-crowned Flycatchers, Sul- domestic chickens disdained them. phur-bellied Flycatchers, Ochre-bellied Pi- Sipurunu nicuruguensis (Monimiaceae). promorphas, Mountain Thrushes (Turdus This straggling shrub of lush second-growth plebejus), and, above all, by Mountain thickets bears pale red, strongly lemon- Elaenias (Elueniu fruntzii). In November scented globes 17-24 mm in diameter (Fig. 1964, in the vicinity of San Jose, Costa Rica, 2).