ecological and behavioral determinants of pollen dispersal in hummingbird- pollinated heliconia

The University of Chicago

Ecological and Behavioral Determinants of Pollen Dispersal in Hummingbird- PollinatedHeliconiaAuthor(s): Yan B. LinhartSource: The American Naturalist, Vol. 107, No. 956 (Jul. - Aug., 1973), pp. 511-523Published by: The University of Chicago Press for The American Society of NaturalistsStable URL: http://www.jstor.org/stable/2459823 .

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Vol. 107, No. 956 The American Naturalist July-August 1973

ECOLOGICAL AND BEHAVIORAL DETERMINANTS OF POLLEN DISPERSAL IN HUMMINGBIRD-

POLLINATED HELICONIA

YAN B. LINHART

Department of Biology, University of Colorado, Boulder, Colorado 80302

Early assumptions of random mating and the consequent normal distribution of genes have proven inadequate whenever tested in the field. A number of recent studies have demonstrated that patterns of mating and gene flow in plants and animals are affected by various features of a species' biology, such as population density, territoriality, food availability, gamete vectors, dispersion, and others (Baternan 1950; Levin and Kerster 1969a, 1969b; Selander 1970).

In this context, plants pollinated by various animals offer a very inter- esting situation because of the interactions between them. Hummingbirds and the plants they feed upon and pollinate provide a good example of such an interaction. For hummingbirds, the availability of nectar has many consequences: when abundant, it can affect the onset of breeding (Stiles 1970) and elicit territorial behavior around a food source (Pitelka 1942; Ortiz-Crespo 1968; WVolf 1969; Stiles 1970; Stiles and Wolf 1970). The feeding patterns of the birds, in turn, may have an effect on pollen dispersal (Grant and Grant 1968; Schlising and Turpin 1971).

The aim of the present study was to gain precise information on plant- hummingbird interactions and on the consequences such interactions have for pollen dispersal in plants. Species of the genus Heliconia (Musaceae) and the hummingbirds feeding upon them were chosen for study because they are among the most widespread of plant-pollinator "systems" in the American tropics. First I show how the dispersion and flowering of the plants influences the feeding behavior of the birds, and then I demonstrate how this interaction affects patterns of pollen movement. These interactions were studied in Costa Rica during July-August of 1968 and 1969, mostly at Finca La Selva (Heredia Province) and Tilaran (Guanacaste Province), which sites are in the premontane wet and premontane moist life zones, respectively (Holdridge 1947).

BEHAVIORAL AND ECOLOGICAL RELATIONSHIPS

Published accounts of hummingbird feeding behavior suggest that most species exploit the nectar resource using either of two basic strategies. The first involves territorial behavior, which is characterized by perching and

511



512 THE AMERICAN NATURALIST

feeding within a fairly well circumscribed area that a bird defends against intruders and from which lie rarely travels any distance. The alternative, a wide search for food, means that a bird does not remain in one area for long, but spends much time flying between scattered flowers. Such a bird can, on occasion, intrude into a territory to feed but is soon chased away.

Territoriality around a food supply is most commonly noted in males of temperate and tropical species showing strong sexual dimorphism in colora- tion and/or size. The females of such species usually range widely in search of nectar but can show territorial behavior in some instances. (Pitelka 1942; Wagner 1945; Cody 1968; Ortiz-Crespo 1968; Wolf 1969; Stiles 1970; Stiles and Wolf 1970). Food-oriented territoriality by both sexes has been reported in species where both sexes are similarly showy in plumage and can presumably be equally effective in their displays of territorial defense (Wolf 1969; Stiles and Wolf 1970). In a third group of species, called hermits, both sexes are uniformly dull plumaged, search widely for their food, and exhibit no territorial behavior around a food source (Davis 1958; Skutch 1951, 1964). Here hermits are designated as subfamily Phaethorninae, and all other species are referred to as Trochilinae. This division was used by Ridgway (1911) and simplifies matters here.

Species of Helticoria are important sources of nectar for hummningbirds, which can be considered as their primary pollinators for several reasons: they are the most common visitors, they come into frequent contact with anthers and stigmata while feeding, and they often carry pollen masses on their body or beak after feeding on Heliconia. Helticonia are most abundant at warmer, lower altitudes in moist to wet situations. They are most often components of second-growth vegetation, either along extensive forest edges such as cleared areas or stream banks or in small forest clearings opened by fallen trees. In Heliconia, as in other Musaceae, vegetative propagation by rhizomes appears to be common, so that several stalks, each of which bears an inflorescence at maturity, can be part of a single clone (Smith 1969). The extent of such propagation in various species does not appear to be known, and I did not determine how many flowering stalks belonged to a given clone. In this paper, all numerical counts of plants are in terms of numbers of inflorescences, since this is an important index of food available to the pollinators. Populations in forest clearings are usually small, comprising 20 or fewer inflorescences, perhaps because these small openings are relatively temporary. The stands along forest edges tend to be large, frequently containing hundreds of inflorescences, perhaps because such areas may be more permanent than forest clearings.

The species studied tend to be found either along forest edges or in clearings, but seldom in both. I have always seen Heliconia imbricata (Kuntze) Baker, Heliconia latispatha Benth., and Heliconia curtispatha Petersen along forest edges, usually in large clumps, but never inside the forest. Thus, of 33 recorded sightings of these species and a putative hybrid of the first two, 32 were along forest edges. The other was a small group of about five H. i1mbricata growing in a clear area between a stream bank and



DETERMINANTS OF POLLEN DISPERSAL 513

a wide trail. Heliconia tortuosa GCriggs and Heliconia acuminata L. Rich., on the other hand, were seen predominantly in forest clearings and only occa- sionally along forest edges. Of 23 recorded sightings of these species, 20 were small clumps within the forest while two small clumps of H. acuminata and one large clump of H. tortuosa were along a forest edge.

Twenty-six clumps of inflorescences of various species and in several locations were observed for at least 2 hours each to record the species and, when possible, the sex of the birds coming to feed and the presence or absence of territorial behavior around the plants. Eight small elunmps composed of two to 20 inflorescences were observed inside the forest. The species were either H. tortuosa or H. acumninata. Along forest edges, eight small (two to 20 inflorescences) and 10 large (over 20 inflorescences) clumps were observed. The species included H. tortuosa, H. acurninata, H. inmbricata, H. latispatha, and their hybrid. Trochilinae seen feeding included the dimorphic species Chaliybura urochrysica, Florisuga nmellivora, Thalurania furcata, and the monomorphic Antazilia tzacatl and Amazilia saucerottei. I could not determine the sex of Amazilia, so they are not included in the results; however, none were seen in the forest and some defended territories while others did not. Phaethorninae included Phaethornis superciliosus, Phaethornis longuemareus, Glaucis hirsuta, and Threnetes ruckeri.

All Heliconia clumps inside the forest were visited by Phaethorninae. Seven of them were visited by Phaethorninae exclusively, and the eighth also had one female T. ftrcata visitor. No territories were observed in the forest. The observed rarity of Troehilinae inside the forest does not hold true at all times. Slud (1964) cites F. rnellivora as an occasional visitor and T. furcata as a regular visitor inside the forest. Clumps along forest edges were visited by species of both subfamilies, but Trochilinae were predomi- nant: 21 birds were male or female Trochilinae, and nine were Phaethorni- nae. In forest-edge clumps, the amount of nectar available may determine the presence or absence of a territory. Three out of eight, or 37.5%, of small clumps supported territories and seven out of 10, or 70%, of large clumps supported territories. The number of open flowers may be more important than total number of inflorescences. Thus, territories were observed around two small clumps of H. imbricata outside the forest, one with seven and one with 12 infloreseences; each inflorescence carried an average of five open flowers every day. These clumps were within a large stand of several hundred plants which supported several territories at the time. Conversely, a stand of about 100 inflorescences of H. tortuosa, each carrying an average of one open flower a day, was never the site of a territory. These inflorescences were scattered over a linear distance of about 35 m along the edge of the forest and over 5 days of observation were only visited by three species of hermits and a T. furcata female.

Table 1 shows the effect of territory establishment on the patterns and frequency of visitation by territorial male Trochilinae versus nonterritorial females and Phaethorninae. Male Trochilinae stayed in their territories. The other birds fed in both types of areas. The interaction between territory




TABLE 1 EFFECT OF TERRITORIAL BEHAVIOR ON PATTERNS OF HUMMINGBIRD VISITATION

ESTABLISHED No ESTABLISHED TERRITORY TERRITORY TOTAL (25 HR)* (17 HR)* (42 HR)*

Visits Visits Visits Total per Total per Total per Visits Hour Visits Hour Visits Hour

Territorial birds ............ 65 2.60 0 0.00 65 2.60 Nonterritorial birds .21 0.84 34 2.00 55 2.84

Total .86 3.44 34 2.00 t t

* Total hours of observation. t Interaction x2, P < .001.

condition and bird feeding behavior is highly significant statistically. The total feedings per hour were about the same for both groups of birds, but plants were fed upon at different rates depending on their suitability as territories. Plants growing within a territory were visited more often than scattered ones. Consequently, the percentages of flowers pollinated in the former may be higher than in the latter.

To get an idea of day-to-day changes in patterns of visitation, several clumps were observed intermittently for periods ranging from 2 to 9 consecutive days. In all the clumps observed, the conditions of presence of territory in H. latispatha, H. imbricata, and their putative hybrid and absence of territory in H. acurninata and H. tortuosa remained constant. This territorial constancy over several days was also reported by Pitelka (1942), Cody (1968), Grant and Grant (1968), and Wolf (1969). At La Selva, I studied several clumps of two species both in 1968 and 1969. They were at about the same stage of flowering and of a similar size in both years. The H. tortuosa in the forest did not support a territory in either year. The H. latispatha supported a territorial C. urochrysia in 1968 and a territorial T. furcata in 1969. In this context, Wagner (1945) observed a male Colibri thalassinus returning to its territory over four consecutive breeding seasons.

Thus, particular patterns of plant population size and dispersion seem to evoke patterns of hummingbird behavior which are repeatable for several days, and perhaps several years. Dense populations of plants are fed upon by territorial and nonterritorial birds, with a clear predominance of' the former. Scattered populations are fed upon solely by widely searching, nonterritorial birds. Consequences of these interactions on pollen dispersal are explored below.

DYNAMICS OF POLLEN DISPERSAL IN Heliconia

Pollen dispersal patterns were studied in two Heliconia species supporting territories and two species visited by widely searching birds. To emphasize the dispersion patterns and habitat of Heliconia species, I give this information whenever necessary and use the initials of the Latin binomial in paren-




theses. For example, Heliconia latisphatha will be referred to as "a clumped, forest-edge species (H.1.). "

One plant species of each type was chosen at Tilaran and at La Selva. The clumped forest-edge species which supported territories were H. latispath7a (Hi..) at Tilaraln and II. imbricata (Hi.) at La Selva. The highly dispersed forest species which did not support territories were H. acuminata (H.a.) at Tilaran and H. tortuosa (H.t.) at La Selva. Characteristics of the study areas are summarized in table 2.

At Tilaran, I chose a woodlot of about 1.5 hectares where both H. latispatha and H. acunminata grew. At La Selva, I chose a stand of the clumped forest-edge species (H.i.) containing about 500 infloreseences to study, since it represented the most extreme case of high plant density observed. The scattered forest species (H.t.) was common in forest clearings. However, the clearings were so widely spaced that I could not check a large enough number of clearings each day to get an idea of pollen movement over a wide area. Therefore, for H. tortuosa, I restricted my study to an almost linear array containing about 300 inflorescences and growing in varying densities along 150 m of trail.

For each species, I counted the density of inflorescences and the average number of open flowers per inflorescence. From these data, I estimated the total food resource available daily in a given area; this resource is ex- pressed as number of open flowers per 10 M2. Data are summarized in table 2. Then, about five flowers from one or a small group of inflorescences, all growing within I iu of each other, were marked with a powdered dye brushed onto the dehiscing anthers. The dyes used were Evans blue, neutral red, or Bismark brown, and adhered to the sticky pollen. The powders were so concentrated that a single speck was visible because it made a bright spot when it had absorbed some of the ever-present moisture. Though I have no quantitative evidence to support this impression, birds did not seem bothered by the presence of the dye. When an inflorescence carried several open flowers, a bird often visited all the flowers on one infloreseence sequentially

TABLE 2 DESCRIPTION or AREAS WHERE POLLEN DISPERSAL WAS STUDIED

Average Location Approximate Density, Average Total

and Size of Inflorescences Flowers/ Flowers Species Area (m2) per 10 m2 Inflorescence per 10 m2

Tilaran: H. acumtnata ....... 6,300 0.17 0.5 0.08 H. latispatha ....... 200 3.40 2.8 9.52

La Selva: H. tortuosa ......... 750 4.00 1.0 4.00 H. imbricata ........ 1,000 5.00 5.0 25.00

NOTE.-For each species, the size of the area where it grew was measured by pacing. The inflorescence density was calculated from a count of the inflorescences in the study area. The average number of open flowers per infloreseence was calculated from counts made on a minimum of 20 inflorescences. The total flowers per 10 m2 is a product of inflorescence density times open flowers per inflorescence and is an estimate of the nectar resource available daily in a given area.




before going to the next infloreseenee. Observed birds did not omit dyed flowers in their sequential feeding.

Flowers at the point source were marked in the morning, usually between 7 :00 and 9:00 A.M. CST. Then, between 1:00 and 3:00 P.M., prior to the onset of the daily rains, I checked flowers at various distances from the point source to see whether they carried any dye. In the H. imbricata stand, the checking was done along three transects extending from the point source. In all other cases, all the available flowers were checked. The dyes were usually visible to the naked eye, though it was sometimes necessary to use a 14X hand lens. The dye or dyed pollen was usually seen on a petal, the stamens, or the stigma. I assumed that the dynamics of dyed-pollen dispersal were about the same as those of effective pollen dispersal. Pollen was marked, and its dispersal followed, for 2 or more days for each species to get an idea of day-to-day fluctuations, with the following results.

Tilara'n

Patterns of pollen movement in the clumped, forest-edge species (H.1.) and the scattered forest species (H.a.) are presented in figures 1 and 2, respectively. The percentages of flowers visited at a given distance represent proportions of flowers marked by dye out of all the flowers checked at that

100 I? 100 11

680 I A 80 B

>60o 60- U)

w

-J40 , 40

I A

20 60 100 14040 8 12 16 .DISTANCE, (meters)

FIG. 1.-Pollen movement in a Helicontia latispatha clump at Tilardil. The clump supported a territory of AXmazilia saiicerottei. Pollen was labeled at distance 0. The arrow marks the center of the clump. The heavy black line indicates the size and the dotted line indicates the edge of the clump around which the bird was territorial. A, Pollen dispersal pattern for July 14 (closed circles) and July 15 (opeil circles); on both days, pollen on infloreseences in the center of the territory was labeled. B, Pollen dispersal pattern on July 16; pollen on inflorescences at the edge of the clump was labeled.




-60

640 0

Z20 _. ** o w

\ o 0X

X I 1 I I I

I I

I5 1.01 Ie I

20 60 100 140 180 220 280 DISTANCE, (meters)

FIG. 2.-Pollen movement in ieliconia acit~minata at Tilardn. Individuals of this species grew scattered in the forest and supported no territories. Solid circles represent percentages of flowers visited at various distances from 0, where pollen was labeled. Crosses represent values calculated fromt the regression formula p = 56.06 - 0.309x. This regression line represents the average pollen dispersal as a function of distance.

distance. The total flowers checked at each distance varied from 10 to 50. The horizontal axis represents distance in meters of the flowers checked from the source of the dye. In the scattered forest species (fig. 2), pollen was dispersed over longer distances than in the clumped forest-edge species (fig. 1). Furthermore, in the former, where pollen flow was unimpeded by the presence of a territory and the vectors were nonterritorial Amazilia and hermits, the decrease with distance was approximately linear. In the latter, the presence of a territory of Amazilia saucerottei was associated with higher percentages of marked flowers within the confines of that territory, followed by a sharp drop-off, and then a gradual decrease.

In the clumped forest-edge species (HI.) pollen dispersal was studied for 3 days. The comparisons between days are presented in figures 1A and 1B. On July 14 and 15, when the flowers marked were in the center of the H. latispatha clumps, the curves are very similar (fig. 1A). On July 16, the dye was placed on flowers at the edge of the clump. The resulting curve (fig. 1B), in contrast to other curves observed, showed a peak at some distance from the source of labeled pollen. The location of the peak cor- responded to the center of the clump. This pattern may have been due to the fact that the bird fed on the labeled flowers and then flew back to the center of the clump before he resumed feeding. The result suggests that the territorial hummingbird concentrated its feeding in the center, where there were more flowers, and visited the periphery, where food was less abundant, less often. The results in figure 2 represent totals of 4 days of observation on H. acuminata. In this species, comparisons between daily patterns of dispersal are not possible because too few flowers were available on any single day.

The dyes used to mark H. latispatha were sometimes seen onlH. acumnata flowers and vice-versa, and dyed pollen of both species was found on flowers




of Costuts sp. (Zingiberaceae). This means that at times individual birds feed on several species of plants. Observations on a lack of flower specificity in hummingbirds have been reported (Grant 1949; Faegri and van der Pijl 1966). These observations on interspecific pollen deposition also suggest that introgroessive hybridization could provide a source of variability for Heliconia.

La Selva

Distances of pollen dispersal for the clumped forest-edge species (H.i.) and the scattered forest species (H.t.) are presented in figures 3 and 4, respectively. Pollen movement in the clumped forest-edge species (H.i.) was the most restricted of the four species studied (fig. 3). I studied pollen dispersal from two different clumps in a stand of 500 inflorescences. Each clump supported a territory of male Thalurania furcata. One clump was composed of seven inflorescences. The pollen dispersal from that clump was studied on August 2, 3, and 4; because the patterns were very similar, only the curve showing the 3-day total is shown (fig. 3A). On August 5, two inflorescences were cut off, leaving five, to see how the reduced food resource would affect territoriality and pollen spread. The resulting curve (fig. 3B) shows that the only effect seems to be a higher percentage of pollination within the territory, perhaps due to increased intensity of feeding at the remaining flowers. On August 6, I marked flowers in a second clump con-

ol 100 Io 1(0o

-801 80 B 801 C

60 60- 601 B

40 -1l 40 -1 401 z

20 1 201 20 *0

a. ~ ~ I

20 40 0 40 20- 40 DISTANCE (meters)

FIG. 3.-Pollen movement in two clumps of Heliconia imbricata at La Selva. Both clumps supported territories of Thalurania furcata. In all cases, pollen was labeled at distance 0, which was also the center of the clump. The heavy black line indicates the size and the dotted line indicates the edge of the clump around which a bird was territorial. A, Dispersal from clump I with seven infloreseences. B, Dispersal from clump I with five infloreseences. C, Dispersal from clump II.




0 w

>60- U)

w 3:40

D _

w 20

20 40 60 00 DISTANCE, (me ters)

FIG. 4.-Pollen movement in ieliconia tortuosa at La Selva. Individuals of this species grew in a linear array along a trail and snpportecl no territories. The line joining the solid circles represents dispersal on Angnst 2. The line joining the open circles represents dispersal on Angust 4.

sisting of 12 infloreseenses. The curve (fig. 3C) shows that the pollen did not travel much farther than in the first clump, with the bulk again remaining within the territory. Note that all three curves fall to zero very quickly, presumably because the territories were strongly defended. There were several other territories in the stand, so that nonterritorial birds seldom had a chance to feed in this area. If some pollen was carried away, it must have been much less than 1%; the zero percentages represent a total of 236 flowers checked at distances over 30 m, none of which was marked with dye.

A few H. latispatha grew scattered among the H. imbricata, and 11 out of 73 flowers checked (15.1%) were marked by dye from the latter, suggesting a potential for hybridization. Indeed, putative hybrid Heliconia with inflorescences intermediate in general appearance between the two species grew in several places at La Selva. Some of these intermediate inflorescences were sterile, but most carried flowers which were visited and presumably pollinated by hummingbirds. About 100 seeds from these intermediates were cut open in 1968 and another 100 in 1969; all were empty, strongly suggesting that these intermediates are sterile hybrids.

The patch of the scattered forest species (H.t.) in which I worked represents an unusually high density for this species, and the distances pollen was moved in this patch may be shorter than in the forest. Again, results show that feeding by nonterritorial birds was associated with extensive pollen dispersal. The differences between the 2 days are striking. The peak at 45 iu on August 2 was observed in a concentration of about 30 inflorescences growing at that distance from the labeled flowers. Consequently, a hummingbird may have overlooked the area between the two peaks, where there were fewer inflorescences, and spent more time in areas of higher food concentrations. On August 4 the distribution of open flowers was similar but




the pattern was very different. I cannot account for the difference between the two patterns, and I was not able to repeat the study again.

DISCUSSION

The data presented in the text and in table 1 suggest that the hummingbirds observed have alternative feeding strategies which result in a division of the nectar resource. This situation has a parallel among bees, which are another major group of nectar feeders (van der Pijl 1966; Janzen 1971). Whether this is a true dichotomy or whether there is a spectrum of intermediate conditions does not appear to be known. For such a dichotomy of behavior patterns to exist, there ought to be a dichotomy of flowering patterns and consequent food concentrations among the plants pollinated by such animals. Janzen (1971) pointed out that tropical flowering plants exhibit a variety of flowering and distribution patterns. My observations suggest that some ieliconia species in Costa Rica have patterns of flowering, habitat preference, and clumping which result in a dichotomy of food concentrations. For the plants, this situation seems to result in a division of the pollinator resource. Consequently, there may be a reduction of competition for food by the birds and for pollinators by the plants.

Heliconia-hunimingbird interactions also resulted in density-dependent patterns of pollen dispersal. In dense populations of inflorescences, territories were established and a large proportion of the pollen movement was restricted to the confines of territories (figs. 1 and 3). The amount of pollen moved out of the territory appeared to depend on the availability of food and competition for that food by hummingbirds. For example, at Tilaran, there were few Heliconia or other plants in flower. Consequently, competition for food may have been quite intense. The H. latispat7ha I observed, though defended by a territorial Amazilia, were fed upon by intruding birds on occasion, and in that situation pollen was transported beyond 100 in (fig. 1). At La Selva, more Heliconia, Costus, and other plants were in flower. Furthermore, the H. imbricata stand I observed was partitioned into several small territories, and I did not see a single intruding hermit or female feeding during the several hours I kept watch. In that area, labeled pollen was not moved beyond 25 in (fig. 3). In scattered populations of inflorescences, no territories were established and pollen movement was much more extensive. The pattern of pollen dispersal over distance may be relatively linear, as at Tilaran (fig. 2), where inflorescences were scattered fairly uniformly over a wide area, or irregular, as happened at La Selva (fig. 4), where the peaks may correspond to areas of higher plant density which may be visited more often than single scattered ifflorescences.

Vegetative propagation appears to be common in Heliconia, and the number of inflorescences comprising a given clone was not ascertained. Furthermore, it is not known whether Ieliconia are self-compatible or not. Consequently, the observed patterns of pollen dispersal cannot be equated




with gene flow between genetically distinct individuals. However, it seems safe to conclude that there is a pronounced potential for inbreeding in forest-edge species because of the high inflorescence density, large number of flowers per inflorescence, and territorial behavior of the pollinators. Under such conditions, a given pollen grain has a high probability of landing either on its parent inflorescence or on a neighboring inflorescence which may be of the same clone. Furthermore, a territorial bird, which feeds in a restricted area, will reduce pollen movement out of this area and also reduce pollen movement into this area by keeping other birds away. In contrast, in scattered forest species the potential for inbreeding seems much lower because inflorescences carry fewer flowers, are more scattered, and are pollinated by nonterritorial birds. Thus, for the species of Heliconia and hummingbirds studied and under the conditions described, the interactions observed lead to very different patterns of pollen dispersal and potential for gene exchange. These patterns may be relatively constant from year to year because the feeding behavior of the various bird species is also constant and seems to be closely tied to patterns of flowering in the plants.

These results provide evidence for the impact of the distribution of the nectar resource on pollen dispersal and on the potential breeding structure of plant populations. This phenomenon has been discussed recently by Heinrich and Raven (1972). However, their review emphasizes the various evolutionary mechanisms which contribute to a dispersion of the nectar resource so as to maximize cross-pollination. In hummingbird-Heliconia interactions, maximal cross-pollination occurs only in species consisting of scattered populations growing in small forest openings of apparently short duration. In contrast, species growing in dense stands along forest edges- which appear to have greater temporal stability-have much more restricted pollen movement. This apparent association between extent of outcrossing and environmental stability may have adaptive significance, as discussed by Levins (1964) and Levin and Kerster (1969b).

Finally, patterns of pollen movement may be applicable to the abundant fauna of Heliconia inflorescences. Such inflorescences frequently contain protozoa and dipteran larvae (Maguire, Belk, and Wells 1968) that can be dispersed by birds (Maguire 1963). The interactions between Heliconia and birds may have a particular impact on the dispersal and population structure of animals that are specific to their plant hosts, as some of the Heliconia- dwelling Drosophila seem to be (Pipkin, Rodriguez, and Leon 1966).

SUMMARY

Hummingbirds in Costa Rica exploit nectar resources using alternative strategies: some defend a feeding territory while others range widely for their food. In Amazilia spp., both sexes are territorial. In Thalurania futrcata, Chalybura strochrysia, and Florisuga nmeliivora, males are territorial, but not females. In Phaethornis spp., Threnetes ruckeri, and Glaucis hirsuta,




both sexes range widely. One of the primary nectar sources for hummingbirds in Costa Rica are species of the genus Heliconia (Musaceae). The birds appear to be the primary pollinators of Heticonia.

Heliconia species differ in their daily flower output, habitat preferences, and dispersion patterns. Heliconia tortuosa and H. aculminata usually have one flower per inflorescence per day, are forest species, and grow very dispersed in small groups of less than 20 inflorescences. Thus, the nectar they provide is very scattered. Heliconia imbricata, H. latispatha, and H. curtispatha have several flowers per inflorescence per day, are forest-edge species, and grow in large clumps or stands which can number several hundred inflorescences. Consequently, the nectar they provide is concentrated in large quantities in small areas.

The dispersed forest species of Heliconia were fed upon by nonterritorial birds, whereas the clumped forest-edge species were fed upon primarily by territorial birds. This interaction may be advantageous to both organisms by lowering the competition for food among birds and the competition for pollinators among the plants.

Movement of labeled pollen was extensive in the dispersed populations of forest species and much more restricted in the dense populations of forest- edge species. Possible consequences of these patterns of pollen dispersal for population structure are discussed.

Interspecific pollen movement was observed. Heliconia latispatha pollen was found on H. acuminata flowers, and vice-versa. Heliconia imbricata pollen was found on H. latispatha, and putative hybrids of these two species were common in one area.

ACKNOWLEDGMENTS

I thank F. G. Stiles, who taught me many facts of hummingbird life, helped me to develop some of the ideas presented here, and reviewed early versions of this manuscript. I also benefited greatly from suggestions made by H. G. Baker, M. C. Clark, A. Gill, J. L. Hamrick, J. Harding, J. H. Hunt, Y. Kiang, K. Keeler, and W. J. Libby in the course of discussions and reviews of the manuscript. Many fellow participants in two Organization for Tropical Studies courses also contributed helpful ideas and observations. The opportunity to carry out this study was provided by participation in two courses offered by the OTS. A portion of the study was supported by PHS training grant 2-Tl-GM367 from Research Training Grants Branch, National Institute of General Medical Sciences.

LITERATURE CITED

Bateman, A. J. 1950. Is gene dispersion normal? Heredity 4:353-363. Cody, M. L. 1968. Interspecific territoriality among hummingbird species. Condor 70:270-

274. Davis, T. A. 1958. The displays and nests of three forest hummingbirds in British Guiana.

Ibis 100:31-39.




Faegri, K., and L. van der Pijl. 1966. The principles of pollination ecology. Pergamon, London. 248 p.

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ecological and behavioral determinants of pollen dispersal in hummingbird- pollinated heliconia

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