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Ecological Interactions between Plants and Hummingbirds in a Successional TropicalCommunityAuthor(s): Peter FeinsingerReviewed work(s):Source: Ecological Monographs, Vol. 48, No. 3 (Summer, 1978), pp. 269-287Published by: Ecological Society of AmericaStable URL: http://www.jstor.org/stable/2937231 .Accessed: 04/10/2012 21:27

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Ecological Monographs (1978) 48: pp. 269-287

ECOLOGICAL INTERACTIONS BETWEEN PLANTS AND HUMMINGBIRDS IN A SUCCESSIONAL

TROPICAL COMMUNITY'

PETER FEINSINGER Department of Zoology, University of Florida, Gainesville, Florida 32611 USA

Abstract. At Monteverde, Costa Rica, 10 successional plant species used 14 hummingbird species for pollination. Displacement among flowering seasons suggests that the plants competed for pollinators. There was no evidence that the flowering of one plant influenced hummingbirds to abandon another. Pollination in simultaneously flowering plants likely suffered nonetheless, since birds tended to move indiscriminately among flowers of different species and could lose much pollen between successive visits to conspecific plants. This may have led to scatter in flowering peaks by favoring the quick establishment of plant colonists with unique flowering seasons over colonists whose flowering seasons coincided with those of established species.

The continuous supply of nectar provided by staggered flowering peaks maintained a continuous supply of hummingbirds competing for nectar. Even inconspicuous plants with few flowers received sufficient hummingbird visits for moderate to high potential rates of outbreeding. At large, flower- laden trees and shrubs, hummingbirds defending feeding territories evidently effected much inbreeding, but movements of intruders between territories kept inbreeding from becoming absolute.

Nectar secretion rates varied widely among flowers of each of the 5 plant species in which nectar volume was measured. Many flowers produced little or no nectar, while a few secreted quite copious volumes. This "bonanza" pattern may benefit plants by reducing caloric expenditures on nectar while increasing the duration of hummingbirds' foraging bouts. The latter possibility was tested and verified experimentally with artificial flowers exposed to a free-living hummingbird on Trinidad, West Indies.

When pollinators are abundant, plants with "bonanza" patterns can attract consistent visitors and rare, inconspicuous plants can count on consistent service. At Monteverde, the unspecialized, opportunistic nature of both plants and birds assured abundant hummingbirds and resulted in a well- integrated complex of plants and pollinators despite the transient nature of the successional habitats.

Key words: coevolution; colonization; community structure; competition for pollinators; Costa Rica; flowering phenology; foraging patterns; gene flow; hummingbirds; nectar; pollination ecology; pollinator behavior; succession.

INTRODUCTION

The patterns in which nectar-feeding animals move among flowers influence profoundly the evolution and ecology of plants and, in return, affect the evolution and ecology of the animals themselves. (1) A pollinator's foraging pattern and energy budget set limits on a plant's nectar secretion rates: the plant must provide adequate nectar to attract and sustain the pollinator but not so much nectar that the pollinator becomes sedentary (Carpenter 1976, Heinrich 1975b, Heinrich and Raven 1972). (2) Pollinator foraging behavior, which varies with pollinator species, plant species, and flower dispersion, influences the genetic structure of plant populations (Frankie 1976, Levin and Kerster 1969a, 1969b, Linhart 1973); conversely, plants may flower in certain patterns to elicit appropriate foraging patterns from their pollinators (Frankie 1976, Janzen 1971, Stiles 1975). (3) The foraging patterns of pollinators as a group can create competition among plant species for pollination services; over evolutionary time spans this competition can affect plant and pollinator community structure (Heithaus 1974, Levin

Manuscript received 12 September 1977; accepted 29 April 1978.

and Anderson 1970). The scarcity of pollinators relative to nectar supplies affects the outcome of all 3 interactions.

Certain tropical plants may coexist with particular pollinators for sufficiently long to evolve precise cor- respondence in behavior and form between plant and pollinator, maximizing the energetic efficiency of pollination, ensuring optimum levels of gene flow among plants, and minimizing pollinator overlap between plant species (e.g., Dodson et al. 1969, Dressler 1968, Gilbert 1975, Janzen 1968). In early seres occupying disturbed sites, however, a continuous relationship between plant population and pollinator population rarely occurs. Hence species in both groups remain unspecialized. Among such populations, soon to yield to more complex communities, one would not expect plant-pollinator interactions to be an important organ- izing force. At Monteverde, Costa Rica, early successional habitats support 14 species of hummingbirds and 10 species of plants adapted for hummingbird pollination. With 1 minor exception, the plants have mor- phologically generalized flowers that are accessible to any hummingbird; with 2 minor exceptions (see Fein- singer 1976), the hummingbirds have relatively short, unspecialized bills that permit use of a wide variety of flowers. The sensitivity of these plants and humming-

270 PETER FEINSINGER Ecological Monographs Vol. 48, No. 3

birds to the interactions listed above is not immedi- ately obvious. This paper will show, however, that even in such a transient assemblage interactions between plants and hummingbirds have critical consequences to both, creating a complex and precisely pat- terned community.

HABITAT

Monteverde occupies a bench at ca. 1400 m elevation on the Pacific slope of the Cordillera de Tilardn, Costa Rica. My research centered in a vegetational formation that can be termed the "Lower Montane Moist Forest-Wet Forest Transition Zone" (Hold- ridge 1967; L. R. Holdridge, personal communication to G. V. N. Powell), a region subjected to an annual dry season lasting from November through May. The successional flora in this zone resembles that of lowland dry-forest sites not only in general appearance but also in species composition. Detailed descriptions of the climate and vegetation in the study areas are given elsewhere (Feinsinger 1976, 1977). Briefly, successional vegetation includes unplowed bean fields on dry hillsides, hand-cleared every October; successional scrub, with or without scattered secondary trees; and woodlands on somewhat older sites, along pasture edges, and in strips between pastures. Primary and secondary forests with closed canopy were not included in this study: their hummingbirds and hummingbird-exploited flora differed greatly from those in the more open habitats (Feinsinger 1976, 1977). Hum- mingbirds circulated freely, however, among the bean fields, scrub, and woodland, which also shared many plant species. Therefore, whether spatially adjacent or not the plants in all 3 successional habitats were linked through their common set of pollinators.

FIELD METHODS

Censuses.-I set up 1470 m of transects, 20 m wide. These were distributed among bean fields, scrub, and woodland according to the relative extent of each habitat at Monteverde. At the end of each month, from January 1972 through April 1973, I counted all open flowers on each hummingbird-visited plant found on the transects. To obtain the mid-month figures reported below I took 2-point rolling averages of consecutive censuses. More detailed descriptions of censuses, and of other field procedures mentioned below, occur elsewhere (Feinsinger 1976).

Observations of flowering plants. -Each month, from March 1972 through April 1973, I counted and timed the flower visits by hummingbirds to a representative plant or plant clump of each hummingbird-visited species in flower. If plants or sites with numerous flowers induced different hummingbird foraging patterns from those observed at scattered flowers, I observed both a representative high flower density and a representative low flower density of that plant species. Observation periods be-

gan at dawn and ran for 7 hours (wet season), 12 hours (dry season, plants with considerable hummingbird activity), 8 hours (plants receiving few visits), or 6 hours (plants receiving no visits). I partitioned data on hummingbird visits by time of day and, on trees and shrubs, by foliage area (top outside, top inside, lower outside, and lower inside). To obtain a measure of visits per flower per day, I counted the number of flowers on the plants observed, standardized the number of flower-probes observed to a 12-hour base, and divided the second figure by the first.

Mist-netting.-To clarify foraging patterns, I mist- netted to mark hummingbirds each month.

Nectar secretion measurements.-During 1971- 1973 I measured nectar secretion in 5 hummingbird- pollinated plant species described below (Inga brenesii, Malvaviscus arboreus, Hamelia patens, Lobelia laxiflora, and Cuphea sp.). On the evening prior to measurement, I bagged selected inflorescences with paper sacks after removing nectar from flowers already open. At dawn I used 10 ttl or 25 ttl measuring capillary tubes to measure accumulated nectar volumes in all selected flowers. I measured accumulated nectar in 1 subsample of flowers each hour thereafter, in a second subsample at 2-hour intervals, and in the third subsample at dusk only. The paper sacks shield- ed flowers in between measurements; later compari- sons with flowers bagged in mosquito netting revealed no noticeable effect of paper sacks on nectar flow. In Hamnelia, whose flowers open about 30 min before dawn and last a single day only, I selected inflorescences on 2 shrubs. In the herb Lobelia, whose pro- tandrous flowers open at ca. 0500 h (dawn) and last 4 days, on each of 4 consecutive evenings I had marked 18 buds about to open; on the measurement day I checked 6 flowers in each of the 4 age classes on each of the 3 removal schedules. In Inga, anthesis occurs around mid-day and flowers remain white the following day, turning yellow (but still secreting some nectar) by the third day. I recorded flower age on the 2 trees I investigated. I did not determine ages of the Mal- vaviscus and Cuphea flowers I investigated. During 1971-1973 I did not measure sugar concentration in nectar and so was unable to obtain data on caloric output of flowers, a statistic more relevant than nectar volume to the energetics of plants and hummingbirds. During summer 1975, however, I repeated nectar measurements on Hamnelia, and obtained sugar concentration with an American Optical hand refractometer. These measurements and measurements on plant species at other neotropical sites suggested that sugar concentration in nectar varied much less than volume, and that there was no noticeable inverse relation between the 2 in any particular plant population. There- fore, nectar volume affords at least a rough index to the caloric output of flowers.

Nectar availability.-While measuring base-line secretion in protected flowers, I also measured nectar

Summer 1978 PLANT-HUMMINGBIRD INTERACTIONS 271

volume in open flowers located some distance from bagged plants and exposed to foraging hummingbirds. I checked 10-15 different flowers each hour (Inga, Halnelia, Cuphea) or twice during the day (Malvavis- Cus, Lobelia). On 12 July 1975 a field assistant and I obtained more refined data for Hainelia: beginning at 0500 and continuing hourly, we measured available nectar volumes in 15-randomly chosen flowers (different flowers each hour) on plants exploited by nonterritorial Chlorostilbon canivetii, the Fork-tailed Em- erald (described below), and in 15 flowers on plants exploited by territorial male Lamnpornis calolae1na, the Purple-throated Mountain-gem.

Nectar v*ariability experiment.-During August 1975. at the Simla Research Station in the Arima Val- ley of Trinidad, I tested the prediction that hummingbirds would visit more flowers per foraging bout if nectar volumes varied than if flowers held consistently large nectar volumes (see below). The test involved a free-living AInazilia tobaci (Copper-rumped Hum- mingbird) that defended a territory at a nearby Ha- Inelia patens. From tuberculin syringes and plastic flower petals I fashioned 20 artificial flowers. Ten flowers each were attached to 2 wooden posts, and for several days flowers were kept filled with a 20% sucrose solution until the bird learned to visit them regularly. Next, on 4 consecutive mornings I maintained 50 ttl of sucrose solution in each flower on I post; I chose this volume as a standard near the lower end of nectar volumes reported in a common forest-edge plant genus pollinated by hummingbirds, Heliconia (Stiles 1975). On the second post I maintained 25 ttl in each of two flowers, 2 ttl in each of 5 flowers, and 0 ttl in each of 3 flowers. After each hummingbird foraging bout, I refilled the flowers visited to original levels, and I switched the posts' positions at half-hour intervals. Each time the hummingbird visited either post, I counted the number of flowers it probed.

HUMMINGBIRDS

Hummingbird foraging at Monteverde varied with bird species and sex, behavior of other hummingbirds present, and flower dispersion (Feinsinger 1976, Fein- singer and Chaplin 1975). Scattered flowers typically received visits from traplining"9 hummingbirds that followed repeated foraging circuits among successive plants. Flowers in dense clumps attracted aggressive birds that defended static feeding territories. Each territorial resident chased any hummingbird intruder, but often intruders could probe several flowers before being ejected or could feed briefly while the resident chased other individuals. Other aggressive birds sometimes defended several less rich flower clumps in succession, spent from a few minutes to several hours at each clump, and, like holders of static territories, occasionally visited flowers scattered among Malva- iviscus arboreus shrubs or other conspicuous plants. These shifting territories differed from traplines in that

they included far fewer plants, each of which was defended by the aggressive bird when present. Finally, many hummingbird species or individuals foraged haphazardly among dispersed flowers or robbed from territories.

The 5 most consistently noted hummingbird species displayed a range of foraging patterns. Both sexes of Aniazilia saucerottei, the Blue-vented Hummingbird, typically defended static or shifting territories against all intruders, or robbed from one another's territories. The most abundant hummingbird at Monteverde, Aniazilia acted as the "organizer species" among hummingbirds as a group (Feinsinger 1976). Philodice brvantae, the Magenta-throated Wood-star, defended intraspecific territories that often included plants also defended by Aniazilia. Chlorostilbon canliietii, the Fork-tailed Emerald, usually excluded from dense flowers, traplined scattered flowers of many plant species. Colibri thalassinuis, the Green Violet-ear, often visited scattered flowers in an irregular fashion or filched from Aniazilia territories, but Colibri also foraged in traplining fashion on occasion. An abundant forest species, Eiupheriusa eximlia, the Stripe-tailed Hummingbird, also entered the open habitats to de- fend any dense flowers neglected by AInazilia or to exploit scattered flowers, occasionally through traplines. All 5 species and most of the 9 other species had relatively short, straight bills that enabled them to visit nearly any plant species mentioned below. Historical- ly, many of the hummingbirds probably derived from the avifauna of similar habitats in tropical dry forest, while others are typical of canopy, clearings, or less often understory in the lower montane wet forests (Feinsinger 1976, 1977).

FLOWERS

Hummingbirds were the principal visitors to flowers of 10 plant species at Monteverde. Except at Malwa- viscus arboreus (see below), probing birds consistently touched the anthers and stigma, carrying pollen on bills or feathers. I did not obtain complete data on reproductive biology and cannot dismiss the possibility that some species were apomictic or autogamous. Protandry in at least I species, herkogamy (spatial separation of anthers and stigma) in nearly all argue against self-fertilizing flowers, while parthenogensis in large, vertebrate-visited flowers is rare enough to be dismissed as a possibility (see Faegri and van der Pijl 1971). While recognizing the lack of conclusive data, following the lead of other researchers (e.g., Heithaus 1974, Linhart 1973, Stiles 1975), I shall assume throughout this paper that these 10 species rely on hummingbirds for pollination and subsequent seed-set.

The widespread successional shrub Hainelia patesls

(Rubiaceae) flowered heavily in rainy season (Fig. 1), when large plants held as many as 310 flowers each and any plant with over about 70 flowers supported a static territory. Elsewhere in the tropics, insects as


500- dry w E I dry 20 a. Hamelia E

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FIG. 1. Flowering phenology of Hamelia patens and Inga brenesii at Monteverde. Two-month rolling averages of total flowers counted and number of plants in flower, on study plots at each month's end.

well as hummingbirds visit Hamelia flowers (Heithaus 1974). Large Hamelia shrubs at Monteverde also attracted insects, notably butterflies. It is probable, however, that hummingbirds (which repeatedly visited flowers in early morning) had effected most pollination before the butterflies' mid-morning arrival. Humming- birds in Hamelia patches invariably carried heavy loads of pollen on their bills.

The tree Inga brenesii (Leguminosae), recorded rarely at other lower montane sites in Costa Rica (W. C. Burger, personal communication), occurred abun- dantly in Monteverde study sites. Trees with ca. 600 flowers or more supported static territories. Whereas Inga's whitish brush blossoms appear to be candidates for bat or insect pollination, I believe that they are primarily hummingbird-pollinated. (1) Hummingbirds carried Inga pollen on chin, throat, forehead, and bill; birds netted near Inga trees were nearly covered with pollen. (2) Hummingbirds made many more visits to Inga flowers than did other flower visitors I observed (mostly hymenopterans). Perhaps the long, enclosed corolla (16-23 mm) was responsible: another Inga species, growing in the same habitats, had 7-8 mm corollas and attracted many insects but few hummingbirds. (3) Although I made no nocturnal observations and could not preclude possible bat or moth visits, the mid-day anthesis, diurnal nectar production (cf. Fein- singer 1976), and lack of a noticeable odor argued against frequent pollination by nocturnal or crepus-

cular visitors. (4) Most insect-pollinated tree species in lowland Costa Rican forests exhibit mass synchro- nized flowering (Frankie 1975, Frankie et al. 1974). For example, all trees of the other, insect-visited Inga species at Monteverde burst into flower in November- December 1971 and 1972 but produced no flowers at other times. In contrast, I. brenesii's phenology resembled Hamelia's, showing a definite peak but with some flower production throughout the year (Fig. 1).

Six species that typically did not support static hummingbird territories also appeared to be adapted for hummingbird pollination. Flowers of each fit the "syn- drome of ornithophily" (Faegri and van der Pijl 1971), and I noted only sporadic visits from other nectar- feeding animals, most of which failed to touch the anthers and stigma. These plants included I geographi- cally widespread shrub of dense second-growth scrub, Malvaviscus arboreus (Malvaceae); I subcanopy par- asite, Psittacanthus lateriflorus (Loranthaceae), that grew on scattered secondary trees; 2 small 'sub- shrubs," Cuphea sp. (Lythraceae) and Justicia sp. (Acanthaceae), that grew in light shade; and 2 widespread herbs that grew in openings and on dry hillsides, Lobelia laxiflora (Lobeliaceae) and Kohleria spicata (Gesneriaceae). Bean fields at Monteverde supported extraordinarily dense stands of Lobelia; however, these presumably unusual densities, which created atypical hummingbird foraging patterns (Fein- singer 1976), will not be considered here.

Purple flowers of the uncommon vine Mandevilla veraguasensis (Apocynaceae) consistently attracted I hummingbird species, Heliomaster constantii, the Plain-capped Starthroat, but also attracted occasional bees. I could not ascertain if hummingbirds transferred much pollen in this species or in another uncommon vine, Manettia flexilis (Rubiaceae), whose rose-pink flowers appeared to be accessible to butterflies but attracted only hummingbirds in 16 h observation. Hummingbirds also visited flowers of 5 other species that appeared to be adapted for insect pollination (Feinsinger 1976) and are not considered here.

RESULTS AND DISCUSSION

Nectar secretion and hummingbird foraging

Generalizations.-Like other consumers, a nectar- ivore can be expected to maximize the ratio of energy obtained to energy expended (Feinsinger and Chaplin 1975, Gill and Wolf 1975a, 1975b, Heinrich and Raven 1972, Wolf et al. 1975, 1976), or to obtain the most nectar with the least movement between sites. The plant can be expected to maximize the ratio of successful pollination to energy expended on pollinator rewards (Baker 1975, Heinrich 1975a, 1975b, Heinrich and Raven 1972), or to obtain the most pollinator movement with the least nectar output (assuming nectar to be an energy drain and plants to be at least potentially energy limited). These opposing "strate-


gies" of plants and pollinators can have 2 vastly different consequences. (1) If flowers are sparse relative to pollinators, then flowers on any plant are visited as long as the energy they provide exceeds even slightly the energy expended by the pollinator while foraging. Within a given population, the plant whose flowers secrete that allowable minimum of nectar not only conserves the most calories but also enjoys the highest frequency of pollen transfer, since pollinators have to visit many flowers on different plants in order to sat- isfy their daily metabolic requirements (Heinrich 1975b, Heinrich and Raven 1972). (2) If flowers are abundant relative to pollinators, then individual pollinators can selectively forage from those plants whose flowers offer the most nectar, and neglect those plants offering lesser though adequate amounts. Competition ensues among conspecific plants for the pollinators' services. Thus those plants whose flowers produce large caloric rewards get pollinated, but at a double cost: not only might the caloric expense of copious nectar be significant, but also the abundant nectar might allow pollinators to become sedentary, limiting their effectiveness as outcrossing agents (for a graphic example, see Carpenter 1976, Carpenter and Mac- Millen 1975).

Hummingbird flowers might seem to fit the latter case. Hummingbirds face exorbitant energy demands (Hainsworth and Wolf 1972a, 1972b, Wolf and Hains- worth 1971), and most authors assert that the plants hummingbirds pollinate secrete copious nectar (Faegri and van der Pijl 1971, Grant and Grant 1968, Heinrich and Raven 1972, Wagner 1946). Data on certain neotropical plants confirm this generalization. For in- stance, Stiles (1975) investigated 9 species of Costa Rican Heliconia (Musaceae) and found that mean nectar secretion per flower per day ranged from 45 to 115 gl (clustering at just over 50 al), with little variation among conspecific flowers. Many Heliconia species are pollinated by hermit hummingbirds Phaethorninae (Linhart 1973, Stiles 1975). Hermits consume many arthropods (Young 1971), and there is evidence that many flowers adapted for hermit pollination go unvis- ited. Thus populations of hermit hummingbirds, at least, may be sparse relative to flowers.

If 50 gl were the typical nectar volume in hummingbird-pollinated flowers, and 4.5 g the typical hummingbird mass (the median mass of Monteverde hummingbirds was 4.45 g), the regression obtained by Hainsworth and Wolf (1972a) estimates that the bird's crop could hold at most 640 gl, or the contents of 13 flowers. Hainsworth and Wolf (1972a) state that it takes at least 30-40 min for the crop to empty. Under these conditions, then, a hummingbird could easily become satiated despite its intense energy requirements. Encountering numerous flowers (located on I large plant or several neighboring plants) each containing copious nectar, a hummingbird would visit only a few before ceasing to forage for some time in-

terval; consequently, relatively little pollen might be transferred between plants (see Heinrich 1975c for a similar discourse involving solitary bees). Some authors note that smaller, short-billed hummingbirds exploit flowers with relatively little nectar (Hainsworth and Wolf 1972b, Snow and Snow 1972), or note in passing the variable secretion rates among certain hummingbird-pollinated flowers (Hainsworth and Wolf 1972b, Wolf and Stiles 1970, Wolf et al. 1976). Nevertheless, these observations have not been related to observations on hummingbird foraging behavior nor to the energetics of plants and pollinators.

Nectar secretion at Monteverde.-The plants at Monteverde contradicted the generalization that bird- pollinated flowers invariably secrete copious nectar. Figure 2 shows that nectar secretion varied extraordinarily among flowers, more than could be attributed to random variation about a mean (in all cases, s ex- ceededx). In Lobelia (Fig. 2a), measured on 16 March 1973. some flowers produced considerable nectar volumes (up to 112 ttl in 24 h). But many flowers secreted little nectar, 15% secreted no measurable amounts, and the mean secretion per 24 h was only 16.2 ttl per flower (n = 72 flowers). Two-way analysis of variance revealed that flower age (0-3 days), measuring interval (1, 2, or 12 h), and the interaction of age and interval each had a significant effect on 24-h secretion: for age, F was significant at p < .005; for schedule, at p < .025; for interaction, at p < .01. In general, older (pis- tillate) flowers secreted less nectar than younger (sta- minate) flowers, while frequent removal stimulated secretion. Nevertheless, error variance (6 replicates per treatment) was high: some 3-day-old flowers secreted large nectar volumes, while some newly opened flowers produced almost none. When overnight production alone-most relevant to hummingbirds foraging early in the day-was analyzed, flower age had no less effect (F not significant, p > 0.05). Thus hummingbirds could not predict nectar content by sexual stage alone, at least early in the day. As detailed above, such variation in nectar volumes doubtless indicated similar variation in caloric re- ward s.

Some of the Hatnelia flowers I investigated on 20 June 1972 produced up to 50 gl of nectar (Fig. 2b). Many produced little nectar (3% produced none), however, and secretion averaged 12.5 gl per flower (n = 35). Flowers were even-aged. Measuring schedule had no significant effect on secretion (F not significant, p > .05). A second investigation (not illustrated) performed on 5 July 1975 (n = 63 flowers), during an unusually dry period, gave a lower figure ( x = 8.30 gl per flower). Some flowers produced over 20 gl of nectar, whereas many secreted none or nearly none. On this date measuring interval affected secretion (F significant at p > .01), with frequent removal inhibiting secretion. Sugar concentration varied from 9.0% to 18.3% sucrose equivalence (x = 13.6%), but


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FIG. 2. Frequency histograms of nectar secretion. Values represent total nectar volume accumulated over a 24-h period beginning at dusk.

there was no consistent relation between quantity and concentration of nectar. In neither investigation was there a significant difference in nectar secretion among plants (t values not significant. p > . 10).

While some of the 34 Ma/lvaviscus flowers I checked on 16 January 1973 produced up to 48 gl of nectar over 24 h (Fig. 2c), 35% secreted no nectar at all. Secretion averaged 8.9 gl. Measuring interval had no effect (F not significant, p > .25). It is likely that age of flowers, which last at least 2 days, influenced their secretion. Gottsberger (1971) showed that hummingbirds are sensitive to age-specific color changes in this species. Nevertheless, my observations revealed that Monteverde hummingbirds foraged haphazardly among Malvaviscus flowers and that nearly all flowers received visits.

A few Cuphea flowers, investigated on 18 July 1972. secreted quite large volumes of nectar (Fig. 2d). But 61% (n = 96 flowers) secreted none, resulting in a low mean (1.77 al). Measuring interval had no effect (F not significant, p > .25). Secretion may have been influenced by flower age. The nectar-poor Cuphea may benefit from a mimetic relationship with Hlanelia (see Heinrich 1975c). Cuphea flowered at and after Hatne- lia's peak; it grew in the same habitat (sometimes under Hatnelia plants); and its flowers were approxi- mately the same orange-red hue as Hatnelia's. Trap- lining Chlorostilbon visited Cuphea in sequence with Hainelia shrubs.

Some of the 108 Inga brenesii flowers I measured on 26 October 1972 secreted as much as 12 gl of nectar (Fig. 2e), but 49% secreted none. Secretion per flower


averaged only 0.85 gl. There was no significant difference between the 2 trees investigated (t-test. p >.25). Neither flower age nor measuring interval had a significant effect on secretion (neither F significant. p > .05). Birds visited both older (yellow) and newer (white) flowers.

The potential significance of variable nectar vol- utnes.-I propose that the variable nectar volumes (and calories) secreted by Monteverde flowers benefit the plants concerned. Consider 2 conspecific populations, A and B. of hummingbird-pollinated plants. Each flower on an A plant secretes a large nectar volume, say the 50 gl per day proposed above. While some flowers on B plants also secrete 50 gl or more per day, most secrete little or no nectar. Not only do B plants expend fewer calories per flower and per seed than A plants (possibly a significant benefit if energy is limited for plants), but also B plants enjoy increased hummingbird movement and increased pollen dispersal. On B plants a foraging hummingbird encounters some flowers with nectar "bonanzas"' dispersed among many flowers with little or no nectar ("blanks"). In the process of locating bonanzas the bird must sample many blanks; this process requires additional energy, which in turn requires additional foraging. Rather than discouraging the bird from continuing to forage, the pattern of bonanzas scattered among numerous blanks actually reinforces continued foraging behavior. In effect, the bonanza-blank pattern is an "intermittent reinforcement schedule," which has been shown to increase the longevity of a behavior pattern (Skinner 1938). Contrast this bird's dilemma with the hummingbird foraging at A plants, which must visit only 13 sequential flowers to fill an empty crop. This reasoning follows that of Frankie and Baker (1974), Heinrich (1975a, 1975b, 1975c), Heinrich and Raven (1972), and Weaver (1956), who argue that small or variable nectar volumes stimulate increased pollinator movement.

Intensive foraging by hummingbirds can amplify a bonanza-blank dichotomy (see Heinrich 1975c). For example, Hainsworth and Wolf (1972b) reported that nectar volumes varied greatly in flowers that had been exposed to hummingbirds. Table I shows that traplining and territorial hummingbirds located more and more of the bonanzas in Monteverde Hlanelia flowers as the morning progressed, amplifying the underlying bonanza-blank pattern illustrated in Fig. 2b. In a sense, patterns of variable nectar secretion "mimic" patterns of variable nectar availability that hummingbirds would create even among flowers with uniform secretion rates.

Requirements.-For variable nectar secretion rates to increase pollination benefits, nectar must be scarce relative to hummingbird populations (see "Generali- zations" above). At Monteverde, nectar supplies ef- fectively limited hummingbird populations (Feinsinger 1976). Birds foraged at most available plants. Except

TABLE 1. Diurnal pattern of nectar volumes remaining in Hamelia patens flowers on (a) shrubs visited by traplining Chlorostilbon canivetii (Fork-tailed Emerald) and (b) shrubs visited by a territorial d Lampornis calolaema (Purple-throated Mountain-gem)

Number of flowers (out of 15) with:

Time Al of nectar

(CST) 0 0.1-2.0 2.1-5.0 5.1-10.0 > 10.0

a. Chlorostilbon canivetii traplines 0500 6 7 2 0600 10 4 1 0700 3 9 1 1 1 0800 6 9 0900 8 7 1000 11 4 1100 10 5 1200 11 4 1300 5 10

b. Lampornis calolaenia territory 0515 9 1 4 1 0615 7 4 4 0715 1 11 1 1 1 0815 5 5 2 3 0915 8 5 1 1 1015 11 3 1 1115 12 1 1 1 1215 13 1 1 1315 14 1 1415 14 1

in dense stands of Lobelia, most of the available nectar was consumed by dusk (Feinsinger 1974). Like- wise, Table I demonstrates that by 0800 h (Hlanelia

traplined by Chlorostilbon) or 1315 h (Hlanelia defended by Lainpornis calolaetna) nearly all available nectar had been consumed. Evidently Monteverde plants enjoyed the luxury of abundant pollinators competing for food supplies.

If hummingbirds could distinguish by sight flowers having or likely to have bonanzas, then regardless of pollinator density, "blanks" would receive no visits and a bonanza-blank pattern would not benefit plants. Hummingbird-pollinated flowers such as those at Monteverde are noted for relatively long corollas, which could serve in part to conceal nectar value from hummingbirds. There are often visible cues to flower sex (in plants with dichogamic flowers) or age, however. If secretion varied with sex or age, hummingbirds might learn to ignore I sex or age class of flower. But in the 2 plants where I checked the effects of age (Lobelia and Inga), at least overnight nectar secretion did not vary significantly with flower age. Evidently Monteverde plants were successful at preventing birds from locating bonanzas visually: often, while observ- ing Lobelia stands, Hlanelia bushes, and Malvaviscus

shrubs, I saw birds probe several flowers (probably blanks) in less than 0.3 sec each, then spend 2-15 sec on another flower (probably a bonanza). Rarely did I see a hummingbird hesitate before a flower, then move to a second without probing the first-the reverse behavior, expected if birds could assess nectar contents


visually. Rather than restricting visits to a few flowers (remembered bonanzas), in all 5 plant species hummingbirds foraged haphazardly or evenly over available flowers. In any event, it is unlikely that birds could memorize the pattern of bonanzas on 1 bout and restrict visits to those flowers on subsequent bouts: within some plants, secretion in different flowers peaks at different hours such that the location of bonanzas is constantly changing.

Test of the proposal: Trinidad.-To test the proposal that variable nectar volumes stimulate longer foraging bouts than uniformly large nectar volumes, I provided a free-living Amazilia tobaci on Trinidad with 1 set of artificial flowers each with 50 gl of nectar, another set of flowers having a Hamelia-like nectar pattern (see "Field Procedure"). The prediction held: bouts lasted an average of 4.14 flowers (21 bouts) on the "variable" post, 2.90 flowers (41 bouts) on the

uniform" post (p < .0078, Mann-Whitney U test). Origins of variable secretion rates.-Given the po-

tential advantages of variable secretion rates to a plant, it is tempting to term this feature an "adaptation" that arose through coevolution between plants and food-limited pollinators. "Adaptation" implies a genetic basis, however, and I have no proof that variable secretion rates are genetically controlled. Nectar secretion rates and concentrations among flowers on insect-pollinated plants have been shown to vary with height of flower on the plant (Percival 1965, Percival and Morgan 1965), number of leaves near the flower (Kenoyer 1917), insolation of leaves near the flower (Hocking 1968, Shuel 1952, 1955a, 1955b), air temperature or relative humidity around the flower (Fahn 1949, Free 1970, Oertel 1946, Kenoyer 1917, Shuel 1952, 1955a), exposure (Free 1970, Kenoyer 1917), or interval between visits (Percival and Morgan 1965, Raw 1953, Wykes 1950). At MOnteverde, the paper sacks controlled to some extent such variables as "exposure," temperature, and humidity; in addition, I never found a relationship between secretion and height of flower. Nevertheless, these and other prox- imate factors doubtless influenced secretion among flowers. The only intrinsic features that have been shown to influence secretion and that suggest genetic control are variable nectary size (Shuel 1961) and flower age (Fahn 1949, Free 1970, Percival 1965, Per- cival and Morgan 1965); here flower age has been dis- counted in Inga and Hamelia. A plant's genome may influence the average secretion rate among its flowers (Shuel 1961), but edaphic factors such as soil moisture (Fahn 1949, Hocking 1968, Shuel 1955a) and soil nu- trients (Raw 1953, Shuel 1955b, 1957) also affect the secretion rate of a given plant. In any case, secretion rates in Hamelia, Inga, and Malvaviscus did not vary significantly among plants. Therefore, at this point I can only guess that highly variable nectar secretion rates arise from a complex of environmental and so- matic factors, and I cannot directly ascribe their origin

to a continuous coevolutionary process between plants and pollinators. Fortuitous occurrence or evolved adaptation, variable nectar secretion can act to the advantage of plants in circumstances such as those at Monteverde.

Hummingbird foraging and the genetic structure of plant populations

Generalizations.-By transferring pollen among the flowers they visited, hummingbirds could effect gene flow among conspecific plants at Monteverde. The adaptiveness of outbreeding, particulary to weeds, is arguable (e.g., Allard 1965, Rollins 1967, Stebbins 1957), but it is generally agreed that in the presence of predictable pollinator service even a weedy, pioneer plant might benefit from some degree of gene flow (Levins 1964, Baker 1974). Levin (1975) stresses the value of outbreeding for rapid response to pressures from pathogens and herbivores. Since pathogens and herbivores may exert especially strong pressures in the tropics, he asserts, gene flow that prevents genotypes from congealing may be critical to tropical plants (see also Bawa 1974, Bawa and Opler 1975). The ur- gency of outbreeding varies among plants, however. Levins (1964) suggests that large plants such as trees, subject to a less variable lifetime environment than weeds, require less gene flow. Allard (1965), Anto- novics (1968), and Rollins (1967) propose that frequent inbreeding increases fitness in some plants by allowing specific adaptations to particular microhabitats.

When hummingbirds transfer pollen from one flower to another, they may effect outbreeding ("xenogamy") if the flowers are on different plants. But if flowers are on the same self-compatible plant, hummingbirds may effect inbreeding, here "geitonogamy," or fertilization of a flower by a pollen from another flower on the same plant (Faegri and van der Pijl 1971). Al- though some outcross pollen (pollen from another conspecific plant) remaining on the hummingbird might also be deposited, in general the chances of geitonogamy increase the longer the hummingbird remains at the plant (Kalin de Arroyo 1976, Levin et al. 1971). If plants produce few flowers each, hummingbirds cannot remain long at any one plant and must visit several in sequence (Janzen 1971), effecting considerable xenogamy (Linhart 1973, Stiles 1975). If a plant possesses many flowers, however, hummingbirds might move between plants rarely, effecting geitonogamy rather than xenogamy if flowers are self-compatible (Cruden 1972, Heinrich 1975b, Kalin de Arroyo 1976) or reducing seed set if flowers are self-incompatible. Fur- thermore, a dense flower clump might attract territorial hummingbirds. A bird defending a static territory not only restricts most of its feeding to the territory but also attempts to exclude other hummingbirds that might carry outcross pollen. The net result is reduced pollen dispersal among territories (Grant and Grant


12- t

>102 ?1Cc Ee

3 I BOTHER ]

z 1 M~~~~Oz ( E LL~~~~~~~~~~

Codd

0~~~~~~~~~

PLANT SPECIES FIG. 3. Visit frequencies to flowers of 6 plant species normally providing dispersed resources to hummingbirds. As=

Atnazilia saucerottei; Cc =Chiorostilbon canivetii; Ct =Colibri thalassinus; Ee =Eupherusa eximia; 'other'' =other hummingbird species. See text for method with which values for visits per flower day were obtained. Sample sizes: Justicia 7 days, 44 flower probes; Cuphea 6 days. 275 flower probes; Kohieria 4 days, 64 flower probes; Lobelia 9 days, 5291 flower probes; Malvaviscus 13 days, 494 flower probes; Psittacanthus 7 days, 883 flower probes.

1968, Linhart 1973, Schlising and Turpin 1971. Stiles 1975).

If intruders are sufficiently numerous, however, territoriality can actually increase outbreeding in the plant defended. A territory with many flowers attracts many intruders (e.g., Wolf and Stiles 1970) that may visit only 1 or a few flowers each before being ejected by the resident, whereas if unmolested intruders might remain within the plant for some time. Frankie and Baker (1974) note that the territorial behavior of male solitary bees reduces the length of intruders' visits. Likewise, in dense aggregations of various bee species (Butler 1945, Frankie and Baker 1974, Free 1970),

there are considerable numbers of "wandering bees,'' passively or actively displaced from flowers by sedentary individuals. These wandering bees evidently effect most outbreeding in the plants concerned. Grant and Grant (1968). among others, noted subordinate hummingbirds filching from dominants' territories and recognized the potential of filching for xenogamy.

Results: Plants with few flowers-.Figure 3 summa- rizes data on 6 Monteverde plants that produced low flower densities and chiefly attracted non-territorial hummingbird species (in Justicia, Cuphea, Kohleria, Lobelia) or aggressive species (in Malvaviscus, Psit- taclnlthus). Based on the Poisson distribution with a


mean of 0.25 visits per flower-day2, if visits were distributed randomly among flowers (a conservative bias; during any 1 visit, at least, birds tended to visit flowers evenly), only 22% of Justicia flowers would have received 1 or more Chlorostilbon visits per day. Justicia plants held few flowers (usually 1-4), however, such that if hummingbirds were carrying pollen from other Justicia plants (see next section) all flower probes could effect xenogamy. An outcrossing rate of 22% would compare favorably with rates reported in the literature (e.g., Beattie et al. 1973). With a mean of 1.98 visits/flower-day, 86% of Cuphea flowers would have received 1 or more visits per day from a randomly foraging Chlorostilbon. Since Cuphea plants held 1-4 flowers, this visit rate indicates a potentially high outbreeding rate. Kohleria and "normal" densities of Lobelia (<75 flowers/100 m2), much more conspicuous than Cuphea or Justicia, attracted numerous hummingbird species. During periods when Chloros- tilbon was absent from Monteverde (December through late January), other hummingbirds such as Colibri, Eupherusa, and females of the North Amer- ican migrant Archilochus colubris, the Ruby-throated Hummingbird, visited the flowers. Calculations using the Poisson distribution indicate that 90% (2.31 visits/ flower-day) of Kohleria flowers and essentially 100% of Lobelia flowers (5.58 visits/flower-day) received I or more visits daily even if hummingbirds foraged randomly. Since Kohleria plants rarely held over 4 open flowers and Lobelia plants seldom held over 6, rates of outbreeding if hummingbirds carried outcross pollen would have been exceptionally high.

The 2 plant species that produced few flowers yet attracted Amazilia and other aggressive birds also received many visits (Fig. 3). A Malvaviscus flower (3.47 visits/flower-day) had a 97% chance of receiving at least 1 visit a day (although around 50% of visits did not effect pollination because birds probed between petals). A Psittacanthus flower (8.67 visits/ flower-day) had a nearly 100% chance of receiving at least 1 visit. Psittacanthus plants rarely held over 20 flowers. Malvaviscus shrubs occasionally held over 90 flowers but mostly held fewer than 10. Thus potential outbreeding rates were quite high in both. Humming- bird foraging at both species resembled foraging at Lobelia or Kohleria in that plants not exploited by Amazilia always attracted other hummingbirds.

Results: Inga and Hamelia.-Hamelia shrubs with few flowers attracted primarily Chlorostilbon and attracted Colibri during months when Chlorostilbon was absent (Fig. 4). Aggressive birds such as Amazilia ef- fectively defended flower-laden shrubs, however, and allowed few other hummingbirds to approach. I cal-

2 Values for visits/flower-day reported here and in Figs. 3 and 4, which are averages over all days observed, differ from values in Feinsinger (1976), which were averages over all flowers observed.

culated the mean number of flowers visited between a hummingbird's known entrance to a shrub and its known exit. This "bout length" increased dramatical- ly with flower number (Fig. 5 and Table 2). The inverse of bout length, or the proportion of all flower-probes that were probes made by hummingbirds just entering the shrub ("firsts"), was therefore much lower on plants defended as territories than on traplined plants. Hamelia flowers are self-compatible (Y. B. Linhart, personal communication). Therefore, the proportion of "firsts" is an index to the ratio of xenogamic to geitonogamic pollinations: some carryover of outcross pollen to the 2nd flower, the 3rd flower, or further would doubtless occur, but the proportion of outcross pollen deposited on stigmas would be expected to decline with bout length (Kalin de Arroyo 1976, Levin et al. 1971). The actual mean number of firsts received per flower per day, obtained through multiplying the proportion of firsts by the mean number of visits per flower per day (Fig. 4), differed by nearly a factor of 4 between low and high densities (Table 2) even though high densities held only 70-310 flowers. The Poisson distribution, used with these figures, indicates that a flower within a static territory had a 20% chance of receiving I or more firsts in a day, while a flower on a traplined shrub had a 62% chance. This contrast implies that offspring of large, flower-laden shrubs were considerably more inbred than offspring of shrubs with few flowers-a possibility now under investigation (Y. B. Linhart, J. Mitton, and P. Feinsin- ger, personal communication).

In Inga, lengths of foraging bouts also increased with flower density (Fig. 6). But flower-laden Inga, each defended by a single Amazilia or at most 1 Amazilia and 1 Philodice, attracted numerous intruders. Often intruders could probe a few flowers before being displaced to adjacent trees. Since the number of potential intruders increased with a tree's attractive- ness, among trees with over 600 flowers (the minimum number to support a static territory) the relationship between bout length and flower density ceased (Fig. 6). In consequence, bout lengths at flower-laden trees were not significantly greater than at flower-sparse trees (Table 2), and were scarcely longer than bout lengths at high-density Hamelia shrubs despite the fact that flower-laden Inga trees held as many as 5000 flowers. Multiplying the proportion of firsts by the frequency of visits per flower gives the mean number of firsts per flower per day (Table 2); Poisson values calculated from the last value demonstrate that a given flower in a static territory had a 4% chance of receiving 1 or more firsts, whereas a flower in a flower-sparse tree had a 13% chance. Doubtless this 3-fold difference would have been much greater except for the activities of territorial birds, which kept nectar filchers in constant motion between trees. Data on the breeding system of this species are not available. The closely related dry-forest species Inga spuria is probably


12

lo :PEvb g Ee

o i

-~other JJ!IfIIJZ 106

-J /NGAX

PLANT SPECIES, FLOWER DENSITY FIG. 4. Visit frequencies to different flower densities on the shrub Hamelia patens and the tree Inga brenesii (see text),

where high flower densities were concentrations of over 70 flowers (Hainelia) or over 600 flowers (Inga). Legend as in Fig. 3, with the addition of Philodice bryantae (Pb). Sample sizes in Table 2.

self-compatible (T. S. Elias, personal communication), suggesting that 1. brenesii is at least partly so. But the possibility that I. brenesii is self-incompatible must also be considered (e.g., Bawa 1974, Kalin de Arroyo 1976). While the frequency of firsts may indicate the ratio of outbred to inbred seeds, as in Ha- melia, the number of firsts may instead indicate the frequency with which flower-visits result in fertilization at all.

The ecology of outbreeding at Monteverde. -The 6 flower-sparse, relatively short-lived plants illustrated in Fig. 3 exploit fluctuating environments unpredict-

able in space and time. Thus they fit Case II of Levins (1964). in which gene flow (here promoted by the foraging of a variety of hummingbird species) is shown to be of adaptive value. In contrast, Hainelia and Inga are capable of reaching large size in suitable microhabitats. Assume for the moment that Inga is at least partly self-compatible. Presumably an individual that reaches large size at a particular site and has the resources to produce many flowers (and seeds) at that site possesses a genotype well adapted to local conditions. Swamping by other genotypes might lower fitness (see Allard 1965, Levins 1964). Thus a genetic


100 -

i HAMELIA PA TENS| I 0.924 (p<.001) |

80-

F is H

0 -

z I E -I E

L 0

to

> 40-

LAJ to I

-J

U_~~I 20-

0 I_

| 600 200 300

FLOWERS / PLANT

FIG. 5. Mean length of foraging bouts at Hamelia shrubs, expressed as number of flowers visited between a hummingbird's known entrance to and exit from a plant. Average value for each observation day versus the number of flowers on the shrub observed. Vertical dashed line at 70 flowers separates shrubs supporting static territories from shrubs exploited by non-territorial individuals.

system combining considerable inbreeding with a small amount of outbreeding would seem (admittedly in retrospect) to confer maximum genetic flexibility on such individuals (Allard 1965, Levins 1964, Rollins 1967). At Monteverde, only those Inga and Hamelia that were large, presumably long-lived, disease-free and free from over-shading or strangling-i.e., individuals successful in particular, relatively stable microhabitats-produced high flower densities. Thus territorial hummingbirds may have inadvertently created an optimal balance between xenogamy and geitonogamy. In the less likely event that Inga is self-incompatible, by decreasing the mean bout length and increasing intertree movement territorial hummingbirds may have inadvertently promoted seed set.

Of course; the chain of factors leading to the flexible genetic system of large Hamelia (and Inga?) is circumstantial: large plants are physiologically capable of producing many flowers, which attract territorial hummingbirds, whose behavior creates low but not insignificant frequencies of xenogamy. Also circumstantial are the considerably higher rates of xenogamy in flower-sparse Hamelia, and probably Inga (Table

100 l

0

I,4NGA BRENESH r * = 0.810 (p <.001)

80 - [> 600 flowers:rs'] -

I 0

C I 0 z

60

LL

a .1 a0

F l > 40-

0) I

o

& 0

*3. | I

201 -

40 I

0 2000 4000 6000

FLOWERS / PLANT

FIG. 6. As Fig. 5 but for Inga trees. Line at 600 flowers separates trees supporting static hummingbird territories from trees in traplines or supporting shifting territories.

2). Small, young, or overshaded plants produced low flower densities, primarily during the flowering peaks of the larger individuals. I speculate that outbreeding might confer greater fitness on these plants than inbreeding, particularly if pollen is exchanged with flower-laden "successful" individuals. The "successful" plants themselves also produced low flower densities at other times of the year (Fig. 1). Seeds produced by these flowers must face a less certain environment than the large seed crops produced by the plants' pulsed, dense flower crops. Following Levins' (1964) discussion, I propose that gene flow among these flowers is also adaptive. Do seeds produced by these low flower densities disperse farther (thus encountering less predictable environments) than the seeds set by the high flower densities on the same plants? Seeds of Hamelia are bird-dispersed, while seeds of Inga are mammal-dispersed. If seed dispersers act like pollinators and become more sedentary at high fruit densities, then the answer is "yes" and the adaptive significance of gene flow among low flower densities is even more clearcut. The hypothesis remains to be tested.


TABLE 2. Hummingbird movement between plants with many flowers (static territories) and with few flowers (shifting territories or traplines). Calculated from the mean number of flowers, for each observation day, visited by each observed hummingbird between its known entrance to a plant (potentially carrying outcross pollen) and known departure from the plant, or the inverse of this figure ("firsts"). See text for details

Hamelia Inga

shrubs with shrubs with trees with trees with Parameter many flowers few flowers many flowers few flowers

Number of observation days 8 13 8 15 Total number of flower visits 10 218 2 612 23 389 9 404 Visits/flower-day 9.96 9.41 1.85 3.61 Mean number of flowers probed per bout 45.5 9.8 46.7 25.2

t-statistic -4.855 (p < .001) 2.080 (p > .05)

Mean proportion of total flower-probes that are "firsts" 0.022 0.102 0.021 0.040 Mean number of "firsts" per flower per day 0.219 0.959 0.039 0.144

Competition among plants and hummingbird foraging

Generalizations. -Simultaneously flowering plant populations may affect one anothers' reproductive success by competing for pollinators in 1 of 2 ways (Levin and Anderson 1970). (1) If pollinators are scarce relative to flowers, pollinators may forage pref- erentially at the more common, conspicuous, or re- warding species, leading to a decline in the frequency of visits to the other species (Bobisud and Neuhaus 1975, Levin and Anderson 1970, Straw 1972). (2) Even when flowers are scarce relative to pollinators, if pollinators simply visit plants of the 2 species in the order encountered (formally, if pollinators are not constant), each pollinator may visit several plants of the more common species between visits to successive plants of the rarer species. The resulting mixed pollen loads reduce the rate of effective pollination in the rare species (Faegri and van der Pijl 1971, Levin 1970, 1972, Levin and Anderson 1970).

Competition in sense (1) above, termed the "dominating flowering phenomenon" (Faegri and van der Pijl 1971), may lead to eventual exclusion of the rarer species from sites or seasons where more abundant species flower (Levin and Anderson 1970, Straw 1972). Consequently, when plants exploiting a common set of pollinators reveal distinct flowering seasons, the ultimate cause may be ascribed to this type of competition. Coexisting insect-pollinated plants often have flowering peaks staggered throughout the growing season or (in the tropics) throughout the year (Frankie 1975, Frankie et al. 1974, Gentry 1974, Hein- rich 1975a, Heithaus 1974, Hocking 1968, Mosquin 1971, Reader 1975). Previous studies have also revealed displaced flowering peaks among plant species pollinated by temperate (Stiles 1973, Austin 1975) and tropical (Heithaus 1974, Stiles 1975, Wolf 1970) hummingbirds. Some investigators (e.g., Free 1963, Gil- bert 1975, Linsley et al. 1963) have found plant species that do flower simultaneously to produce attractants

at different times of the day; presumably, this behavior is another result of competition for pollinators.

Temporal differences amtong Montev erde plants.-

Figure 7 shows that flowering peaks of the hummingbird-pollinated plants at Monteverde were staggered through the year. In no month were fewer than 3 nor more than 5 species at peak flowering. If Mandevilla and Manettia (perhaps not primarily hummingbird- pollinated) are excluded, the range was 2 to 5 peaks per month. Plants whose flowering seasons overlapped sometimes showed diel differences in nectar secretion and visitor activity. For example, in April 1973 Ha- mnelia and Lobelia attracted the same hummingbird species, but at different times of the day (Fig. 8). Can phenological and diel divergence among Monteverde plants be ascribed to either type of competition for pollinators?

Did dominating flowering'' affect Monteverde plants?-During the 14 months at Monteverde, there were several instances where a hummingbird population exploiting 2 plant species visited the first plant less frequently when the second plant approached its flowering peak. For example, in 1972 Amazilia visits to flower-laden Hamnelia shrubs declined from over 12 per flower per day in August to 6 in September, to 0.5 in October; many Inga trees were then coming into flower (Fig. 1) and attracting numerous Amazilia. Chlorostilbon filled the void at Hamnelia, however, such that total visits by both bird species averaged 6.7 per flower per day in September, 8.8 in October. Near- ly every such vacancy, left by 1 hummingbird population abandoning 1 plant species in favor of another, was quickly filled by other hummingbirds. Even when Lobelia peaked and its nectar became superabundant (Feinsinger 1976), hummingbirds as a group continued to visit other plant species regularly. During this study, then, the dominating flowering phenomenon did not affect plants; therefore, it cannot be invoked to explain their flowering phenologies.

The role of competition among birds.-At Monte-


Number of Peaks 3 3 3 3 3 3 4 5 4 4 3 3 4 3

100,000

0~~~~~~~~~ 3 10,? 000

0 LL

1000

o J

, 10 < Mv

A

M AMJ J A S O N D J F M A 1972 1973

FIG. 7. Flowering peaks of all hummingbird-pollinated plant species at Monteverde. Numbers of flowers censused on study plots illustrated for peak months only, where a peak month is one where flower count is 25% or more of maximum ever reached (see Heithaus 1974). Two-month rolling averages, as in Fig. 1. L = Lobelia; I = Inga; J = Justicia; H = Hamelia; C = Cuphea; Ma = Malvaviscus; P = Psittacanthus; K = Kohleria; Mv = Mandevilla; Mf = Manettia.

verde, incessant competition among the hummingbirds (Feinsinger 1976) overrode the dominating flowering phenomenon. Aggressive species such as Amazilia, defending flower-rich areas, forced less belligerent birds to forage among more widely dispersed flowers. In July 1972, for example, territorial species concen- trated on flower-laden plants while nonterritorial species visited scattered flowers (Table 3), with the net result that all plants depending on hummingbird pollination received at least 1.3 visits per flower per

day. Resource partitioning among birds also acted to disperse foraging within individual plants (Feinsinger 1976; see also Colwell et al. 1974). Table 4 details a day's activity at an Inga tree. Whereas Amazilia pre- ferred inner flowers and Philodice fed exclusively on outer flowers, the sum of these and other species' foraging patterns distributed visits quite evenly among flowers regardless of their location. Thus competition among hummingbirds maintained the absolute frequency with which they visited flowers.

TABLE 3. Visits to all hummingbird-pollinated plants in flower during July 1972

Visits/Flower-Day at:

Inga Hamelia

low density high density low density high density Cuphea Mandevilla Malvaviscus

by: Amazilia 0.38 1.71 8.93 1.71 Chlorostilbon 4.00 8.23 0.38 1.71 Eupherusa 0.20 Lampornis calolaema 0.77 Heliomaster constantii 2.14

All species 4.00 1.35 9.94 9.31 1.71 2.14 1.71


1.0 4 April H m la1111Cc 0

1973 ~A s 3 t a lAP-r1 B s

K~~t 0.6 2

1gi *-.=.]. -4MEe

0. 05 .Lobelia 1

0. 124

0.2 - -ul2

0 m0

FIG. 8. Temporal divergence of nectar secretion and hummingbird foraging in Harnelia and Lobelia. Legend as in Figs. 3, 4. but height of bar indicates visits per flower per hour rather than per day. Dashed line: Nectar secretion per hour in flowers measured each hour (but 0 is total overnight secretion between dusk and dawn).

Did competition for constant pollinators affect plants at Monteverde -Resource partitioning among hummingbirds did not necessarily maintain constancy to particular flower species, however. At Monteverde, Chlorostilbon and other wandering foragers often visited different species of plants in mixed order (e.g., Lobelia and Kohleria; Hamelia, Cuphea, and Inga; Haamelia and Justicia). Most of these plants distributed pollen over the same sites: the bird's forehead, its bill, or less often its chin. Since pollen loads drop readily from hummingbird feathers and bills, birds probably lost considerable pollen between successive

visits to conspecific plants when these were dispersed among flowers of other species. Except for Mande- villa, which received the undivided attention of Helio- master constantii, traplined plant populations that flowered at different times from each other may have experienced relatively greater constancy and fecundity than plant populations that bloomed synchronously.

If competition for constant pollinators affects a plant's fecundity, then, which process results in community patterns like Fig. 7: natural selection that acts to separate the flowering seasons of those species al-

TABLE 4. Visits to a flower-laden Inga brenesii tree with 4980 flowers, observed for 12 h in November 1972, with flowers apportioned by eye into 4 foliage regions

Total number of Vists/Flower-Day In:

Hummingbird flowers visited Top Outside Top Inside Lower Outside Lower Inside

Amazilia 2550 0.545 0.782 0.390 0.469 Colibri 579 0.036 0.041 0.193 0.221 Philodice 1250 0.561 0 0.122 0 Eupherusa 37 0 0 0.019 0 Archilochus colubris 447 0.206 0.011 0.030 0.021 Eli'ira cupreiceps 166 0.010 0.057 0.048 0.025

All species 5029 1.358 0.891 0.802 0.736


6-

0

cn4 w

01 La..

LiL 0

2-

z

o~~~~~~~~-- M A M J J A S 0 N D J F M A 1972 1973

MONTH

FIG. 9. Total numbers of hummingbird-pollinated flowers (2-month rolling averages) counted on study plots. Solid line: All such flowers. Dashed line: Flowers not in sufficient densities to support static hummingbird territories.

ready established on a site, or community-level selection that affects the success of prospective colonists according to their pre-existing phenologies? I suspect that the former has less influence at a particular successional site. The flowering phenology of a plant population is not subject simply to the whim of pollinators; it may be more or less fixed by the optimal season for seed dispersal and the length of time re- quired for seed maturation (cf. Beattie et al. 1973, Jan- zen 1969, Snow 1966). Furthermore, early successional plants rely on speed invasion, rapid population buildup, seed production, and dispersal to other lo- calities before the physical and biological attributes of the site are altered such that other plant species are favored (see Baker 1974, MacArthur and Wilson 1967). Rarely would they go through sufficient generations at a particular site for natural selection, no mat- ter how strong, to alter drastically their flowering seasons. At Monteverde, I inferred from local records and observations of variously-aged plant assemblages that sites not continuously disturbed supported at most 5 or 6 generations of Lobelia, Kohleria, Cuphea, or Justicia before dense shrubbery extinguished their populations. The more dispersed populations of Ha- melia, Inga, Malvaviscus, and Psittacanthus may technically have lasted many generations at Monte- verde, but at least Hamelia's flowering phenology there was no different from its phenology throughout Central America and the Caribbean. It is possible that Inga and Hamelia set the phenological framework into which other species fit. Therefore, while natural selection is expected to mold a plant species' flowering phenology over the long run, it may not be immedi- ately responsible for divergent phenologies among co- occurring species.

I propose that selection operated at the community rather than the individual level at Monteverde. The

plants in the study sites represented only a fraction of the species of early successional, hummingbird-visited plants growing on the western slope of the Cordillera de Tilardn, many at sites with physical characteristics similar to those at the study plots. Most species in this pool have flowers adapted for the generalized, short- billed hummingbirds typical of Monteverde, and relatively invariable flowering seasons at any 1 elevation. While I have no direct evidence for differential colonization success among these species, the following reasoning seems plausible. A plant species from this pool invading the study habitats would at first be rare relative to species already present. If the invader flowered synchronously with established species that re- lied on the same pollinators, pollinator constancy to its flowers could be very low. Consequently, if it were allogamous the invader's seed set would be low, its invasion retarded, and its successful establishment jeopardized. In contrast, an invader that flowered when few established species bloomed, or that by chance attracted pollinators at a unique time of day, could receive relatively uninterrupted pollination and could become established rapidly (Frankie 1975 and Heithaus 1974 use similar reasoning). In short, at least in early successional communities the ability to maintain constancy in generalized pollinators may hasten the establishment of some plant species relative to others, resulting in an assemblage of species with different flowering seasons such as those in Fig. 7. This process has implications to limits set on the species diversity of the plants concerned (Heithaus (1974).

The consequence of displaced flowering peaks.- Whatever its origin, the displacement of flowering phenologies ensured a year-around resource base for Monteverde hummingbirds (Fig. 9). At all times of the year some flowers were available; in particular, the number of flowers in low-density arrays remained nearly constant. Since long-lived vertebrates in the tropics require food the year around, the supply provided by staggered flowering peaks (Faegri and van der Pijl 1971, Heithaus et al. 1975, van der Pijl 1956) or fruiting peaks (Snow 1966) acts to sustain vertebrate populations exploited by plants and to retain these populations within the community. Yet this mainte- nance function is an inevitable consequence of competition among plants for the vertebrates' services.

CONCLUSIONS

Unless the disturbance creating them is chronic, openings in the wet tropics return rapidly to forest (Budowski 1963). The plants and hummingbirds that exploit disturbed sites are quick to invade openings as they occur and quick to disperse to other sites before the forest regenerates. Highly mobile, hummingbirds respond especially quickly to openings containing new food sources (Feinsinger 1976). Successional plants depending on hummingbirds for pollination can count on visits at whichever site they colonize. But plants


cannot expect 1 particular hummingbird species to be present in all openings they invade. Therefore, these plants have corollas that are short enough to invite probes from most hummingbirds likely to be encountered, while sufficiently long to exclude most insects (and peeping hummingbirds). Likewise, hummingbirds circulating among openings cannot depend on the consistent presence of plants with particular corolla shapes, and must have general-purpose bills adequate to probe a range of hummingbird-pollinated flowers as well as various insect-pollinated ones. Thus most species of hummingbirds have access to, and forage among, a number of flower species (Feinsinger 1976, Snow and Snow 1972, Wolf 1970, Wolf et al. 1976).

In the presence of several suitable plant species with corollas of similar shape, then, successional hummingbirds rarely restrict their foraging to 1. Therefore, allogamous plants that bloom synchronously may lower each other's reproductive success and retard each other's establishment more than plants with unique flowering seasons or other features enhancing constancy in pollinators. The result, sequential flowering seasons among the successful colonists, assures hummingbirds of a continuous food supply and encourages their commitment to nectar resources. This commitment, opportunistic foraging behavior, and the lack of interspecific distinctions in feeding apparatus lead to severe competition among the birds for nectar supplies. Food-limited hummingbirds cannot be fastidious in their foraging. In contrast to communities such as mature forest, where many plants with morphologi- cally specialized flowers exert themselves to attract large, similarly specialized hummingbirds, successional plants with variable secretion rates enjoy certain advantages that would be denied to plants secreting copious nectar. Variable secretion rhythms further ex- acerbate nectar shortages and competition among hummingbirds. The resultant partitioning of all ex- ploitable nectar sources among hummingbirds main- tains flexibility in plant genetic systems: no plant, regardless of rarity or size, is ignored by potential pollen vectors.

Thus the hummingbirds and plants at a successional site display coevolved features only in general terms. The relationship between plants and birds can better be described as "co-immigration." At any 1 site, those hummingbirds most able (due to habitat preference, competitive abilities, morphology, and so forth) to exploit the typical flowers are the successful invaders (see Feinsinger 1976), arriving in synchrony with those plant species best able to exploit promiscuous hummingbirds and to tolerate the site's peculiar edaphic and biological features. Although consequences of the plants' nectar secretion, gene flow, and phenology may be circumstantial rather than coevolved, the complex at Monteverde, like any natural community, is more than just a haphazard assortment of species. Opportunism among plants and birds, and birds' ten-

dency to exhaust nectar sources through various foraging methods, result in a robust though transient community whose plants offer food to hummingbirds in prescribed patterns and appear to obtain necessary amounts of gene flow in return.

ACKNOWLEDGMENTS

I am grateful to R. B. Root and members of the Compar- ative Ecology Guild at Cornell University for encouraging me to write this paper and for commenting on its embryonic stages. V. Adams, P. Bierzychudek, H. J. Brockman, S. M. Chambers, R. K. Colwell, M. Crump, B. A. Drummond III, G. W. Frankie, D. G. Griffin III, P. G. Kevan, Y. B. Linhart, G. F. McCracken, R. Montgomerie, N. Pearson, B. J. Rathcke, and R. B. Root provided numerous helpful comments on later drafts. I thank the people of Monteverde for their kindness and my wife Claudia for her patience. W. H. and R. E. Buskirk, R. K. Colwell, L. E. Gilbert, P. A. Opler, G. V. N. Powell, F. G. Stiles, and R. H. Whittaker provided advice during field work. W. C. Burger of the Field Museum, L. Diego-G6mez of the Museo National de Costa Rica, and Luis Poveda of the Universidad de Costa Rica identified plant specimens. J. A. Wolfe ably assisted me at Monteverde during summer 1975, while G. Angehr and M. Wissink were of great help on Trinidad. Field work during 1972-1973 was supported by an Andrew D. White Fellowship, a Cornell Graduate Fellowship, funds from a National Science Foun- dation (NSF) training grant to the Section of Ecology and Systematics at Cornell University, and a gift from Mr. J. S. Dunning. Field work during summer 1975 was supported by a Faculty Research Grant and a Venture Grant from the Uni- versity of Denver and by funds from the Department of Bi- ological Sciences at the University of Denver. Preparation of the manuscript was underwritten by NSF grant DEB 76- 2037 1.

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