Hawkmoth Pollination Research Articles

Notes on Eriotheca longitubulosa (Bombacaceae1), a rare, putatively hawkmoth-pollinated species new to the Guianas

Eriotheca longitubulosa is a large, nocturnally flowering tree new to the Guianas. Floral morphology, daily phenological patterns, nectar concentration, and floral aroma were examined in order to infer pollinator type. The floral morphology and phenological data, while not necessarily typical in all features displayed by known hawkmoth-pollinated plants, suggest hawkmoth pollination by swing hovering. The presence of the sesquiterpenes alpha-farnesene and germacrene-D in the aroma supports this conclusion.

Use and Pollination of a Hawkmoth Plant, Nicotiana attenuata, by Migrant Hummingbirds

Nicotiana attemuata, an herbaceous annual plant of disturbed sites in cold deserts of western North America, has traits that suggest adaptation for hawkmoth (Sphingidae, e.g., Hyles lineata or Manduca spp.) pollination. The tubular flowers are white and open fully at night and twilight, often closing by midday. Nectar is produced between dusk and dawn, and if not harvested is resorbed between dawn and midday. At our study site in northern Arizona, hawkmoths were absent or scarce during September and early October 1994, but migrating female and juvenile Selasphorus hummingbirds (rufous and broad-tailed hummingbirds) visited flowers regularly during morning or evening and briefly defended territories centered on plants. Most of these hummingbirds disappeared from the patch at midday. We found only weak evidence that humming-birds have acted as agents of selection on floral traits of N. attenuata. Nectar production was low (ca. 1.15 μl/flower/night, containing 0.43 mg sugar) relative to most hummingbird flowers of the western United States, and although hummingbirds obtained a short-term profit from N. attenuata in the morning and early evening when nectar standing crop was high, most birds could not meet their daily energy requirements by foraging exclusively on its flowers. Hummingbird pollination had no impact on female fitness of N. attenuata, because seed production was not affected by provision of self or outcross pollen. Hummingbirds may have affected plant fitness through pollen export. Our results demonstrate the opportunism of migrant hummingbirds and suggest the potential for evolution of floral traits to proceed from such an opportunistic use of a plant in the absence of its syndrome pollinator.

The rise and fall of plant species: a population biologist's perspective

The rise and fall of plant species: a population biologist's perspective

Hawkmoth pollination of the African epiphytic orchid Mystacidium venosum , with special reference to flower and pollen longevity

The pollination biology of Mystacidium venosum Harv. ex Rolfe, an epiphytic orchid endemic to southern Africa, was investigated. The white flowers of this orchid have long spurs (c 4.5 cm) and contain dilute sucrose-dominated nectar which is secreted during the afternoon and early evening. Scent, dominated by Jasmine lactone and (E, E)-Farnesol, is emitted in the evening. A breeding system experiment established that self pollination results in inferior quality fruits. Field observations at three sites in Kwa-Zulu Natal, South Africa, in 1998 and 1999 showed that hawkmoths were frequent visitors to the orchid shortly after dusk, and carry pollinaria along the length of their tongues. No evidence for directional selection on spur length was found at any of the three sites. Results showed that flower longevity is strongly reduced by pollination, while pollinaria removal had only a small effect. Pollinia removed from flowers remained viable for up to 20 days under outdoor conditions.

Floral isolation betweenAquilegia formosaandAquilegia pubescens

The acquisition of floral nectar spurs is correlated with increased species diversity across multiple clades. We tested whether variation in nectar spurs influences reproductive isolation and, thus, can potentially promote species diversity using two species of Aquilegia, Aquilegia formosa and Aquilegia pubescens, which form narrow hybrid zones. Floral visitors strongly discriminated between the two species both in natural populations and at mixed-species arrays of individual flowers. Bees and hummingbirds visited flowers of A. formosa at a much greater rate than flowers of A. pubescens. Hawkmoths, however, nearly exclusively visited flowers of A. pubescens. We found that altering the orientation of A. pubescens flowers from upright to pendent, like the flowers of A. formosa, reduced hawkmoth visitation by an order of magnitude. In contrast, shortening the length of the nectar spurs of A. pubescens flowers to a length similar to A. formosa flowers did not affect hawkmoth visitation. However, pollen removal was significantly reduced in flowers with shortened nectar spurs. These data indicate that floral traits promote floral isolation between these species and that specific floral traits affect floral isolation via ethological isolation while others affect floral isolation via mechanical isolation.

Biogeography and floral evolution of baobabs (Adansonia, Bombacaceae) as inferred from multiple data sets.

The phylogeny of baobab trees was analyzed using four data sets: chloroplast DNA restriction sites, sequences of the chloroplast rpl16 intron, sequences of the internal transcribed spacer (ITS) region of nuclear ribosomal DNA, and morphology. We sampled each of the eight species of Adansonia plus three outgroup taxa from tribe Adansonieae. These data were analyzed singly and in combination using parsimony. ITS and morphology provided the greatest resolution and were largely concordant. The two chloroplast data sets showed concordance with one another but showed significant conflict with ITS and morphology. A possible explanation for the conflict is genealogical discordance within the Malagasy Longitubae, perhaps due to introgression events. A maximum-likelihood analysis of branching times shows that the dispersal between Africa and Australia occurred well after the fragmentation of Gondwana and therefore involved overwater dispersal. The phylogeny does not permit unambiguous reconstruction of floral evolution but suggests the plausible hypothesis that hawkmoth pollination was ancestral in Adansonia and that there were two parallel switches to pollination by mammals in the genus.

Species‐independent, geographical structuring of chloroplast DNA haplotypes in a montane herb Ipomopsis (Polemoniaceae)

Two hypotheses have been proposed to explain the occurrence of hybrid zones between red‐flowered Ipomopsis aggregata and white‐flowered I. tenuituba. Either local adaptation to hummingbird and hawkmoth pollinators has given rise to sympatric (or parapatric) divergence of flower colour and morphology (primary intergradation at hybrid zones), or alternatively two previously allopatric species are coming into contact at several geographical areas of secondary intergradation. We examined restriction site patterns in nuclear DNA (nrDNA), chloroplast DNA (cpDNA) and mitochondrial DNA (mtDNA) from populations of I. aggregata and I. tenuituba representing seven zones of sympatry. No variation was detected in a 350‐bp fragment of mtDNA and uninformative levels of variation were observed for nrDNA. We detected 22 potentially informative restriction site polymorphisms in cpDNA, all of which united geographical areas containing populations of both species. We detected no informative species‐specific markers. Studies of other species (e.g. oaks) have detected similar species‐independent geographical structure of cpDNA. However, in these cases secondary interegradation could be inferred from species‐specific nuclear alleles. The pattern in Ipomopsis is consistent with both primary intergradation (independent speciation in each area of sympatry) or secondary intergradation involving complete cytoplasmic replacement. Thus, additional data are needed to explain the origin of hybrid zones in Ipomopsis.

Hawkmoth pollination in Cereus peruvianus, a columnar cactus from southeastern Brazil

Summary Pollination by hawkmoths (Sphingidae) is described for Cereus peruvianus (Cactaceae) in southeastern Brazil. The flower presents a dish to bowl-shaped perianth with whitish tepals and a long floral tube. The stamens, arranged like a brush, produce abundant pollen and the long, tube-like style ends in a multi-lobed stigma. Start of anthesis is crepuscular. Anthesis lasts one night. Only little nectar is produced, with ca. 27 % sugar concentration. Odour is weak, sweetish and persists throughout the night. Handpollination tests indicate that seed production is dependent on cross-pollination. Honeybees, scarabid beetles, and hawkmoths were observed visiting the flowers, but only the latter seem to be effective pollinators. The sphingids, Agrius cingulatus and Manduca rustica, showed similar visiting behavior, which consisted of hovering, alighting on the perianth, and partially introducing the body into the nectar chamber. Both floral attributes and the morphological/behavioral characteristics of sphingids point to an adaptive trend toward sphingophily in C. peruvianus. This trend is also reflected in the flowering season, which matches the main peak of activity for sphingids at the study areas, and in the steady state flowering pattern, which promotes cross-pollination visits by these insects.

Observations of hawkmoth pollination in the South African orchid Disa cooperi

Johnson, S. D. 1995. Observations of hawkmoth pollination in the South African orchid Disa cooperi. ‐ Nord. J. Bot. 15: 121–125. Copenhagen. ISSN 0107–055X. Disa cooperi is a robust grassland orchid with long‐spud white flowers which are strongly scented in the evening. Observations at a site in Natal province, South Africa showed that hawkmoths are frequent visitors to the orchid at dusk. The hawkmoth Basiothia schenki was an effective pollinator of D. cooperi; this hawk‐moth has a medium length proboscis (x = 4.3 cm) which can be fully inserted into the nectar‐containing spur of the orchid. Pollinaria are attached ventrally to the basal portion of the proboscis where it joins the head. Another hawkmoth, Agrius convolvuli, commonly foraged on nectar from D. cooperi, but did not carry pollinaria, probably because its proboscis is too long (x = 10 cm) to allow contact between the thick basal portion of the proboscis and the orchid column. Lips in Disa are typically linear and do not produce scent, thus the autapomorphic spathulate and scent‐producing lip of D. cooperi indicates that hawkmoth pollination is derived in this species, probably from a long‐proboscid fly pollinated ancestor.

Genetic variation in central and disjunct populations of Lilium parryi

We compared levels of genetic variability in small, isolated populations of Lilium parryi in Arizona with those found in large populations in California. Arizona populations were presumably derived from California populations; they were significantly less variable and showed evidence of much higher levels of inbreeding. One California locality whose population structure is similar to those found in Arizona also had relatively low levels of genetic variability. However, the other California populations were highly variable and showed lower levels of inbreeding than Arizona populations. There was significant genetic differentiation among all populations. In Arizona, there was no relationship between current population size and genetic variability. Arizona populations may be vulnerable to extinction, given the magnitude of environmental modifications in their habitats, their small sizes, and their low levels of variability. Key words: genetic structure, rare species, hawkmoth pollination, Lilium, disjunct populations.

Pollination of Dianthus superbus L.

Pollination of Dianthus superbus L. was studied in a subalpine population in the Swiss Alps (San Bernardino Pass, 1,700m) in 1987 and 1988. Pollinators of this well known and beautiful plant are reported here for the first time. The flowers were visited exclusively by migratory nocturnal hawkmoths ( Herse convolvuli L.) in 1987, but in 1988 native noctuid moths were the most frequent flower visitors. The deeply divided and brightly coloured petals, calyx length and the strong sweet scent produced in the evening and distinctly weaker during the daytime suggest that Dianthus superbus is adapted to crepuscular and nocturnal hawkmoths rather than to noctuid moths. It is not especially adapted to diurnal hawkmoths and clearly not pollinated by butterflies as stated so far in the literature. Nectar is sucrose dominant with moderate sugar and amino acid concentrations and corresponds well with the syndrome of hawkmoth pollination. The observations are discussed with respect to both the plant and its pollinators.

The adaptedness of the floral phenotype in a relict endemic, hawkmoth-pollinated violet. 2. Patterns of variation among disjunct populations

This study examines patterns of variation in quantitative floral traits among 18 disjunct populations of Viola cazorlensis (Violaceae), a relict endemic violet of south-eastern Spain. At all sites, the species is almost exclusively pollinated by a single species of day-flying hawkmoth. Differences between populations were significant for all traits examined, and population means exhibit a broad range of variation. When all characters are considered together, each population displays a unique combination of characters. Despite interpopulation differences in character means, local populations retain most of the variability of the entire species. Floral traits do not vary in unison among flowers, and at least four different subsets of independently varying traits are identifiable. Floral similarity between populations of V. cazorlensis was largely unrelated to geographic proximity, as revealed by analyses at both large and small geographic scales. The geographic pattern of floral variation among populations represents a random patchwork, with unique combinations of character means occurring randomly across the study region. Marked population differences in quantitative floral traits in spite of spatial constancy in the identity of pollinators, a disintegrated floral phenotype, and prevailingly random geographic variation among populations, suggest low adaptedness of the floral phenotype of V. cazorlensir to its current hawkmoth pollinators.

A Tropical Hawkmoth Community: Costa Rican Dry Forest Sphingidae

Hawkmoths (Sphingidae) constitute a major class of pollinators in the lowland dry forest of Costa Rica. In our study area, hawkmoths are the primary pollinators of about 10 percent of the tree species; they also pollinate various species of shrubs, herbs, lianas, and epiphytes. We found a total of 65 hawkmoth species and 31 native plant species that were adapted primarily for hawkmoth pollination. Abundance of both hawkmoths and hawkmoth flowers peaked in the first half of the wet season (May-July). Numbers of hawkmoths decreased through the dry season (December to April) with lowest numbers during April. Species of hawkmoth flowers also decreased through the dry season, but several species began flowering before the onset of the wet season and before the sudden increase in hawkmoth numbers that followed shortly after the first rains. Tube lengths of hawkmoth flowers ranged from 0 to 19 cm (x = 5.1 cm), matched by the range in length of hawkmoth tongues (1-20 cm, x = 4.9 cm). Hawkmoth tongue lengths were correlated with body size (wing length) (r = .70). Long flower tubes restricted access to nectar to long-tongued moths. However, long-tongued moths did not restrict their visits to long-tubed flowers. In fact, hawkmoths visited many species of flowers adapted for other pollinator types-e.g., hummingbirds, bees, and bats-along with hawkmoth flowers whose tubes were much shorter than their tongue lengths. The attractiveness of hawkmoth flower species varied greatly: some flowers were always heavily visited, other species were virtually ignored. In less attractive flowers, nectar accumulated during the night and attracted a variety of diurnal visitors the following morning. Similarly, hawkmoth flowers that opened before dark attracted diurnal and crepuscular visitors (bees, wasps, hummingbirds, butterflies) that robbed nectar and pollen, possibly decreasing flower attractiveness to hawkmoths. HAWKMOTHS (SPHINGIDAE) ARE RECOGNIZED as a major pollinator type in the tropical dry forest of Costa Rica (Frankie 1975, Haber & Frankie 1982, Frankie et al. 1983, Opler 1983), along with other animals such as large bees, butterflies, hummingbirds, and bats (Heithaus et al. 1975; Heithaus 1979a, b, c; Frankie & Haber 1983). The marked seasonality of this forest has an overriding effect on the animals that live there (Janzen 1983, 1984). The forest is largely leafless during part of the year as a result of a 6-mo dry season. Because larval hawkmoths eat leaves, the dry season strongly influences their life histories. A predictable pattern of seasonal flowering also occurs in the dry forest (Janzen 1967, Frankie et al. 1974, Opler et al. 1980), with a consequent fluctuation in availability of resources for pollinators, induding adult hawkmoths. In this paper we describe characteristics and interactions of hawkmoths and the plants they exploit for nectar. In contrast to most previous studies of hawkmoth pollination (e.g., Gregory 1963, Cruden et al. 1976), we focused on hawkmoth-plant relationships at a single site. Here we describe the members of the hawkmoth and flower communities, their seasonal patterns of abundance and floral specificity, and we discuss some key characteristics of the moths and plants as they may relate to pollination interactions. STUDY SITES AND CLIMATE STUDY SITES.-Research was centered at Cafias, Guanacaste Province, Costa Rica (Hacienda La Pacifica, Hacienda Ciruelas, and the MAG station at Taboga). The natural vegetation in the area is classified as tropical dry forest (Holdridge et al. 1971). This is a closed-canopy, broadleaf forest containing about 180 tree species that occur in two principal associations: mostly deciduous species on well-drained slopes and hills, and an evergreen forest along permanent rivers and flood plains. For detailed descriptions of the area see Holdridge et al. (1971), Frankie et al. (1974), Janzen and Liesner (1980), Opler et al. (1980), and Hartshorn (1983). CLIMATE.-Rainfall in the study area is highly seasonal (Fig. 1). The average wet season extends from mid-May to mid-November, interrupted by a 2-wk dry period in July or August (Hagnauer 1980). During dry season (November to May) precipitation is restricted to rare brief showers. Annual rainfall at Caiias ranged from 947 to 2962 mm (x = 1790) for the years 1920 to 1976 (Opler et al. 1976). I Received 14 October 1986, revision accepted 20 December 1987. 2 Corresponding author. 3 Includes Lomas Barbudal Biological Reserve and the two refuges of Palo Verde. BIOTROPICA 21(2): 155-172 1989 155 This content downloaded from 157.55.39.138 on Thu, 19 May 2016 06:27:24 UTC All use subject to http://about.jstor.org/terms

Hawk-moth scale analysis and pollination specialization in the epilithic Malagasy endemic Aerangis ellisii (Reichenb. fil.) Schltr. (Orchidaceae)

The pollination biology of the epilithic endemic Aerangis ellisii (Reichenb. fil.) Schltr. (Orchidaceae) was studied on an inselberg in the Antananarivo region, central Madagascar. The flowers exhibit long nectariferous spurs indicative of hawk-moth pollination, the mechanism evidently involving pollinia transfer via the frons and palpi of the vectors. Analysis of hawk-moth scales on naturally pollinated stigmas showed that the principal pollinators were Agrius conuolvuli (Linnaeus) and Panogena lingens (Butler). Proboscis morphology of long-tongued Malagasy Sphingidae in relation to nectar position and spur morphology in A. ellisii also indicated that A. conuolvuli and P. lingens were best suited to interact with the plant's floral adaptation. Aerangis ellisii seems to display a relatively moderate specialization versus the Malagasy hawk-moth guild since its nectar is accessible even to those long-proboscis hawk-moth species which are not able to act as pollinators.

Angraecoid Orchids and Hawkmoths in Central Madagascar: Specialized Pollination Systems and Generalist Foragers

Angraecoid Orchids and Hawkmoths in Central Madagascar: Specialized Pollination Systems and Generalist Foragers

Additional Observations on Temperate North American Hawkmoth Flowers

Additional information on hawkmoth visits to flowers of 24 species in the continental United States is presented to enlarge the data base. We now have hawkmoth pollination records for 41 native species and visitation records for at least three naturalized species in the temperate North American flora. The total number of native sphingophilous species in this flora is 106. The most important sphingophilous plant group of supraspecific taxonomic rank in temperate North America is the tribe Onagreae (family Onagraceae). The evolution of the hawkmoth pollination system in this group is discussed.

Hawkmoth Pollination of Aquilegia chrysantha (Ranunculaceae) in Southern Arizona

ABASTRACT.-Aquilegia chrysantha occupies mesic habitats in mountainous regions of the southwestern United States and northern Mexico. The faintly scented, yellow flowers are protandrous and the spurs secrete large quantities of nectar (29% total sugars). Seed set for plants under cages was 31% compared with 55% for open-pollinated flowers. The most common pollinator of the species in the Chiricahua Mountains was the crepuscular hawkmoths Eumorpha achemon (Sphingidae), although two Sphinx species also foraged effectively for nectar. The mean tongue length (4.4 cm) of Eumorpha is relatively short compared with the length (6.7 cm) of the floral spurs of A. chrysantha. This suggests that longer-tongued hawkmoths such as the Sphinx (5.4 cm) may be more important pollen vectors for A. chrysantha than is indicated by their low frequency of visitation in this study. Diurnal visitation to A. chrysantha flowers at a very low rate by large bees and hummingbirds, or recent evolution as a moth-visited taxon, may account for the failure of this hawkmoth-pollinated species to have developed a strictly crepuscular or nocturnal anthesis. Southwestern North America is a region where hawkmoths (Sphingidae) are abundant and many plant species have flowers adapted for visitation by these insects (Gregory, 1963, 1964; Miller, 1981, and included references). Also in this area there are a number of closely related Aquilegia species with pale-colored flowers and unusually long floral spurs. Grant (1952) suggested that members of this group (the A. caerulea James complex) are probably pollinated by hawkmoths. Subsequent observations have shown that A. caerulea is indeed adapted for pollination by hawkmoths, with bumblebees and hummingbirds also visiting its flowers (Miller, 1978, 1981). However, A. micrantha Eastwood, a species that Grant placed in the A. caerulea species group, may be better adapted for pollination by nectar-foraging bumblebee queens than for pollination by hawkmoths (Miller and Willard, 1983). Aquilegia chrysantha Gray is another member of the A. caerulea species group considered to be adapted for hawkmoth pollination (Knuth, 1908; Grant, 1963), although corroborating observations in the field are few (Grant, 1952, 1976; Ritter, cited in Lott, 1979). The species occurs in mesic habitats at elevations of 910-3350 m throughout much of Arizona, New Mexico, Sonora, western Chihuahua, and into Coahuila and Texas where it intergrades with A. longissima Gray ex. Watson (Kearney and Peebles, 1960; Lott, 1979). This paper describes the floral characteristics of A. chrysantha and reports the pollinator activity on several populations of this species in southern Arizona, thus contributing to our understanding of the role pollinators have played in the floral evolution of the columbines.

Pollination by Deceit in a Mass-Flowering Tropical Tree Plumeria rubra L. (Apocynaceae)

Flowers of Plumeria rubra, a mass-flowering tropical tree, share many traits with hawkmoth-pollinated flowers, and Plumeria pollen was recovered from the tongues of 17 hawkmoth species in Costa Rica. Rates of visitation and fruit set were exceptionally low compared with other hawkmoth flowers sympatric with Plumeria, apparently because Plumeria flowers produce no nectar reward. Hawkmoths in a flight cage quickly learned to avoid nectarless Plumeria flowers, but readily fed from these flowers after artificial nectar was added. Although no specific model for Plumeria was found in Costa Rica, the presentation of generalized odor and visual cues that mimic typical hawkmoth flowers may facilitate deceitful pollination of Plumeria. FLORAL MIMICRY ENCOMPASSES a diversity of reproductive strategies used by plants to achieve pollination by animals (see reviews of Wiens 1978, Little 1983). Because of experience with a model, pollinators visit a floral mimic expecting a reward. However, the mimic provides no reward and pollination occurs through deceit. Despite the importance of floral mimicry as a reproductive strategy, little detailed information about such systems exists (Wiens 1978, Williamson 1982, Little 1983). Williamson (1982) stressed that floral mimicry should be defined in terms of reproductive fitness. However, showing that fitness of a floral mimic is increased by its interaction with a model has rarely been successful in floral mimicy systems (Boyden 1980, Bierzychudek 1981, Williamson, pers. comm.). The essential difference in selection pressure on floral and insect mimics suggests that floral mimics may be less dependent upon resemblance to a model than insect mimics. Failure of an insect mimic to deceive a predator usually leads to the mimic's death, but failure of a floral mimic to deceive a pollinatory only results in the loss of potential pollination event. Deceitful plants may also attract pollinators by presenting cues that the pollinators innately recognize, rather than relying on strong resemblance to a model. In some instances a specific model may be absent (Dafni and Ivri 1981a, b; Ackerman 1981, 1983). In addition, convergence within floral syndromes may further complicate analysis of floral mimicry systems (Brown and Kodrik-Brown 1979, Williamson and Black 1981, Little 1983). In this paper I describe the floral biology of Plumeria rubra L. (Apocynaceae), a tropical tree apparently adapted for hawkmoth pollination. Plumeria produces no floral nectar and may be a generalized mimic of other hawkmoth-pollinated flowers. The reproductive biology of this species differs from typical examples of floral mimicry in that Plumeria lacks a specific model, is a massively flowering tree with an extended blooming period, and may be the most abundant hawkmoth flower in tropical deciduous forest of Costa Rica during much of its blooming period. STUDY SITES AND METHODS From 1976-1982 I studied Plumeria in northwestern Costa Rica (Guanacaste Province) at Hacienda La Pacifica, 10 km north of Canias, and at the Comelco ranch, centered 10 km north of Bagaces. The lowland deciduous and evergreen riparian forests at these sites (50-100 m elevation) are described by Frankie et al. (1974, 1983), Opler et al. (1980), and Opler (1983). I also made observations near the community of Monteverde (northern Puntarenas Province) from 1979-1982 where Plumeria grows in semi-deciduous, moist forest on the Pacific slopes at 800-1200 m elevation. FLORAL BIOLOGY.-Flowering phenology is based on Frankie et al. (1974) and my observations from 19761982. I studied the floral behavior of Plumeria using the methods of Haber and Frankie (1982) and Frankie et al. (1983). I monitored nectar secretion intensively on bagged flowers of two trees over several days and checked for possible nectar production on about 20 additional trees by probing flowers with microcapillary tubes and inspecting dissected flowers. I counted ovules in dissected flowers and seeds in mature fruits from the lowland site. Fruit numbers were easily observed on leafless trees during the dry season at

POLLINATOR FORAGING BEHAVIOR AND GENE DISPERSAL IN SENECIO (COMPOSITAE).

Wright (1943, 1946) showed that in a continuous population of organisms, the pattern of genetic differentiation is largely determined by the number of individuals in a local random breeding unit, or neighborhood. When neighborhoods are small, populations are subject to greater differentiation, both randomly and in response to natural selection. Neighborhood size is a function of population density and gene dispersal. The breeding systems and stationary spatial distributions of animal-pollinated flowering plants are consistent with the assumptions of Wright's models; such systems have proved excellent for the study of neighborhood size, because gene dispersal can be estimated directly by measuring pollinator movements and seed dispersal distances (Kerster and Levin, 1968; Levin and Kerster, 1968, 1969a, 1969b, 1974; Schaal and Levin, 1978; Beattie, 1979). The foraging behavior of pollinators has major importance for patterns of gene dispersal in plant populations (Levin, 1979a, 1979b). Foraging behavior in turn may be affected by the quality and distribution of the nectar sugar rewards offered by flowers (Heinrich and Raven, 1972; Heinrich, 1975). Pollinators can utilize only flower resources which provide sufficient caloric reward to make foraging energetically profitable (Heinrich and Raven, 1972; Heinrich, 1975). Types of pollinators may differ by several orders of magnitude in the metabolic energy costs they incur during foraging and thermoregulation (Heinrich and Raven, 1972; Heinrich, 1975). For example, butterflies, which thermoregulate by basking (Watt, 1968) and have relatively low foraging costs, can profitably utilize flowers with relatively small nectar rewards (Watt et al., 1974), while bumblebees and hawkmoths, which thermoregulate metabolically and expend more energy in foraging (Heinrich, 1975), would operate at a loss on the same resource. Many flower species have specialized features of nectar presentation adapting them to a particular pollinator type (Heinrich and Raven, 1972; Faegri and van der Pijl, 1979). For example, plant species specialized for bumblebee or hawkmoth pollinators often provide rich nectar rewards in deep-spurred nectaries that are inaccessible to low-energy pollinators. On the other hand, many plants provide minute quantities of nectar that are profitable only to animals with low metabolic costs. If pollinator types with different energy requirements differ in their foraging behavior, then the neighborhood structures of plants specialized for those pollinators can be expected to differ also. Linhart (1973) has shown that pollen dispersal patterns in tropical Heliconia differ dramatically depending on whether territorial or traplining hummingbirds are the pollinators. Moreover, for plants which are generalists, pollinated by several types of animals, neighborhood structure may be significantly affected by the proportion of pollen transferred by different pollinator types. Two aspects of pollinator foraging behavior have particular importance for patterns of plant gene dispersal. First, flight distances between plants will determine the distance over which pollen is transferred. Second, in self-compatible plants the number of flowers visited per plant will determine the proportion of seeds set that are selfed or outcrossed, and thus will affect levels of inbreeding. Moreover, if pollen from a given flower is carried over to more than one of the flowers subse-

Hawkmoth Pollination in the Genus Oenothera

Hawkmoth Pollination in the Genus Oenothera