Approaches to Nectarivore-P Lant Interactions in the New World

Revista Chilena de Historia Natural 60: 285-319, 1987 Approaches to nectarivore-p lant interactions in the New World

Acercamientos a las interacciones nectarfvoro-planta en el Nuevo Mundo

PETER FEINSINGER

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

ABSTRACT

During the past two decades, the emphasis of research on animal-flower interactions has changed dramatically. Valuable data continue to be collected using the traditional approach of descriptive natural history: detailing pollination mechanisms, tallying animal flower-visitors, and refming or applying the concept of "pollination syndromes" (sets of floral traits associated with particular animal taxa). Most recent studies, however, utilize animal-flower interactions to make quantitative tests of general hypotheses in evolutionary ecology. Some topics of special interest in recent years are: (1) "coevolution" between plants and pollinators (in particular, the selective consequences to plants of variation in floral traits, or of variation in animal visitors); (2) the relationship between nectarivore morphology and the energetics of locomotion, and the relationship between the animal's energetic requirements (or other nutritional needs) and the food resources provided by flowers; (3) the role of animals in sexual selection among plants and the evolution of plant breeding systems; (4) the influence of animal pollinators on gene flow in plant populations; (5) the determinants of territorial behavior in nectarivorous animals; (6) nectarivore search patterns and the economics of foraging; (7) the relationship between social structure and niche width in populations of flower-visiting animals; (8) interspecific competition and the organization of nectarivore guilds; (9) interspecific competition, interspecific facilitation, and community pattern among animal-pollinated plants; and (10) changes in the ecology of animal-flower interactions among different communities. Many studies utilize techniques that were first developed to study the pollination of crop plants or horticultural cultivars, but few of the recent, conceptual approaches to natural animal- flower interactions have re-invaded applied research. Two major directions for future research, in fact, are the application of "post-revolutionary" concepts of animal- flower interactions to (a) agricultural research, especially in regions with many animal-pollinated crop plants, and to (b) conservation research, especially research on ecological effects of habitat fragmentation. Other gaps in our knowledge on animal-flower interactions include: (1) the particularly intriguing interactions between hawkmoths (Lepidoptera: Sphingidae) and moth-pollinated flowers; (2) the relationship between the foraging energetics of many flower-visitors and nectar availability in flowers; {3) the ontogeny of foraging in vertebrate {and invertebrate) nectarivores; (4) the short-term and long-term dynamics of nectarivore guilds; {5) the relationship between mechanisms of interaction and community pattern among plants that use the same animals as pollinators. Key words: Coevolution, competition, energetics, foraging, pollination.

RESUMEN

Durante las dos ultimas decadas, el enfasis de la investigaci6n sobre interacciones animal-flor ha cambiado dramatica- mente. Aún se sigue colectando valiosa informacion usando el metodo tradicional de historia natural descriptiva, es decir, describiendo mecanismos de polinizaci6n, contabilizando visitantes de flores y refinando o aplicando el con- cepto de "síndromes de polinización" {grupos de caracteristicas florales asociadas con taxa animales en particular). Estudios más recientes, sin embargo, utilizan las interacciones animal-tlor para probar cuantitativamente hip6tesis generales en ecologfa evolutiva. Algunos t6picos que han despertado especial interes en afios recientes son: {1) "coevo- lución" entre plantas y polinizadores (en particular, las consecuencias selectivas para las plantas debidas a cambios en caracterfsticas florales, o debidas a variaci6n en el tipo de visitantes); {2) la relaci6n entre la morfologfa de los nectarfvoros y la energetica de su modo de locomoci6n, y la relaci6n entre los requerimientos energeticos del animal (u otras necesidades nutritivas) y los recursos alimenticios provistos por las flores; (3) el papel de los animales en la selecci6n sexual entre plantas y en la evoluci6n de sistemas de reproducci6n en las plantas; (4) la influencia de polinizadores animales en el flujo de genes en poblaciones de plantas; (5) los factores determinantes del comportamiento territorial en animales nectarfvoros; (6) la "búsqueda optima de alimento", o sea, patrones y economfa de la busqueda de alimento en los nectarfvoros; {7) la relaci6n entre estructura social y amplitud del nicho en poblaciones de animales visitantes de flores; (8) competencia interespedfica y la organizaci6n de gremios de nectarfvoros; {9) competencia interespedfica, facilitaci6n interespedfica y patrones de la comunidad de flores polinizadas por animales; y (10) cambios en la ecología de interacciones animal-flor entre distintas comunidades. Aunque muchos de estos estudios utilizan tecnicas que fueron desarrolladas originalmente en estudios de polinizaci6n de plantas de cultivo, pocas aproxi- rnaciones conceptuales recientes a las interacqiones animal-flor han reinvadido la investigaci6n aplicada.

(Received 1 October 1986. Accepted 21 Apri11987) 286 FEIN SINGER

Dos de las principales direcciones de futura investigaci6n son, de hecho, la aplicaci6n de conceptos "postrevolucio- narios" de interacciones animal-flor a (a) investigacion en agricultura, especialmente en regiones con un gran numero de cultivos polinizados por animales y a (b) investigaci6n en conservaci6n, especialmente investigaci6n sobre los efectos ecol6gicos de Ia fragmentaci6n del habitat. Otras brechas·en el conocimiento de las interacciones animal-flor incluyen: (i) las interacciones entre polillas (Lepidoptera: Sphingidae) y las flo res que elias polinizan; (2) Ia relacion entre la energetica de Ia busqueda de alimento de muchos visitantes de flores y Ia disponibilidad de nectar en las flores; (3) la ontogenia de la búsqueda de alimento en nectarivoros vertebrados e invertebrados; (4) Ia dinámica de los gremios de nectarfvoros a corto y largo plazo y (5) Ia relaci6n entre los mecanismos de interacci6n y patron comunitario entre plantas que usan los mismos animales como polinizadores. Palabras claves: Busqueda de alimento, coevoluci6n, competencia, energetica, polinizaci6n.

INTRODUCTION to flower-visiting animals, many of them highly energy-limited, is variation in net energy intake (Heinrich & Raven 1972, Interactions between flower-visiting animals Heinrich 1983b). At the same time, the and the plants they inadvertently pollinate theory of interspecific competition came have intrigued biologists for centuries. to dominate community ecology (cf. Throughout the second half of the 19th MacArthur 1972, Cody & Diamond 1975, century and the first six decades of the Diamond 1978), and here too animal- 20th, most research on these interactions flower interactions offered many oppor- stressed a botanically oriented approach tunities for investigation (cf. Feinsinger that fitted descriptive studies into a general & Colwell 1978, Waser 1983a). evolutionary framework (Baker 1983). The 1970s saw an explosion of studies By the mid-20th century, a tremendous that tested ecological or microevolutionary body of information -and a daunting hypotheses with animal-flower systems. terminology- had been amassed on "an- Under the impact of numerous additional thecology" of North Temperate and researchers in the 1980s, pollination eco- (some) tropical plants (Proctor& Yeo 1973, logy is approaching the status of a "hard" Faegri & van der Pijl 1979). The mass of science, with an established theoretical descriptive studies and idiosyncratic data framework (which, of course, is still threatened to discourage conceptually evolving) and an established research pro- oriented, hypothesis-testing approaches. tocol. Rigorous hypothesis-testing studies Two decades ago, though, the study take place alongside studies on the natural of animal-flower interactions was revo- history of new systems. Inferences drawn lutionized by three reviews. Grant & Grant from studies on animal-flower interactions (1965) carefully examined pollination in are increasingly realistic. There is now the plant family Polemoniaceae from the widespread recognition that pollination viewpoints of both plants and animal is just one step, and often a relatively flower-visitors. Baker & Hurd (1968) unimportant step in proximate terms, used a comprehensive, modern ecological along the route from flower production framework to discuss numerous features by one generation to recruitment into the of the micro- and macro-evolution of next (e.g., Stiles 1978, Heithaus et al. plant-pollinator interactions. Heinrich & 1982, Wheelwright & Orians 1982, Rathcke Raven (1972) alerted a wide readership & Lacey 1985). Consequently, pollination to the role of energetics in animal-flower ecology is being rapidly integrated into relationships. These reviews (and others) balanced perspectives on plant life history coincided with the growth of "evolutionary phenomena, plant demography, and other ecology" as a general approach to eco- arenas of animal-plant interaction such as logical field studies. Because the under- seed predation, seed dispersal, and herbi- lying concern of evolutionary ecology vory. Likewise, the realization that animals is the fitness consequences of different need not be expected to forage "optimally" "tactics" (e.g., see Schoener 1971, Emlen at flowers (Heinrich 1983a, cf. Pyke 1972, Pyke et a/. 1977, Pianka 1983, 1984), and that interspecific competition Pyke 1984), animal-flower interactions is not a uniformly important feature of were an obvious choice for investigation: animal (or plant) assemblages (Strong et the consequence to plants of ecological al. 1984, Feinsinger et al. 1985, Diamond events at pollination is vru;:_iation in seed & Case 1986), has encouraged objectivity set or in the genetic "quality" of seeds in recent research on the ecology of flower- (Waser 1983b ), whereas the consequence visiting animals. NEW WORLD NECTARIVORY 287

This review will sort recent theory, to the selective influence of particular research approaches, and empirical results flowering plants. into a series of arbitrary categories. Given Recently, however, several studies have the breadth of the subject, I can highlight documented ( 1) geographic variation in only a few points and only a restricted floral traits within plant species, apparently geographic region (the New World, par- as a microevolutionary consequence of ticularly Central and North America). spatial changes in the pollinator milieu; For more comprehensive reviews, readers (2) the selective consequences, measured should consult Faegri & Van der Pijl by differential pollination success or (1979), Feinsinger (1983a), Jones & reproductive output, of intrapopulation Little (1983), Real (1983b), Willson variation in floral traits; and (3) the selec- (1983), Willson & Burley (1983), and tive consequences of visitation by different Rathcke & Lacey (1985). Furthermore, animal species. I will bypass the mass of literature on the (1) Many correlational studies exist. intricacies of the pollination event itself, Grant & Grant (1965) documented many including pollen-stigma interactions, the cases in the Polemoniaceae of intra- and genetics and evolution of compatibility interspecific variation in floral traits that systems, pollen biochemistry, and pollen corresponded to shifts in the pool of tube growth (e.g., Heslop-Harrison 1975, available pollinators. Miller (19 81) showed de Nettancourt 1977, Frankel & Galun that elevational shifts in traits of the co- 1977, Heslop-Harrison & Shivanna 1977, lumbineAquilegia caerulea (Ranunculaceae) Mulcahy & Ottaviano 1983). With those corresponded to a shift in the frequency disclaimers, we can now discuss the evo- of the hawk-moth Byles lineata (Sphin- lutionary ecology of animal-flower inter- gidae) relative to the frequency of longer- actions. tongued hawk-moths (primarily in low- elevation deserts) or bumblebees (primarily at high elevations). "COEVOLUTION" (2) Waser & Price (1981, 1983b, 1985) OF FLOWER-VISITORS showed that bumblebee pollinators were AND PLANTS significantly less effective at pollinating rare white-flowered plants than blue-flo- In broad terms, angiospermous plants wered plants in a population of the larkspur and flower-visiting animals undoubtedly Delphinium nelsonii (Ranunculaceae). As influence one another's evolution and a result, white-flowered plants set only have done so at least since the Cretaceous 30-45% as many seeds as blue-flowered (Baker & Hurd 1968, Regall977, Mulcahy plants, and the authors inferred that the 1979). Apparently, though, precise "coevo- white-flowered morph was maintained lution" or "reciprocating evolution" (Baker in the population only through spontaneous & Hurd 1968) between particular plants mutation. Paige & Whitham (1985) showed and particular pollinators is exceedingly that a population of Ipomopsis aggregata rare. Recent reviews (Feinsinger 1983a, (Polemoniaceae) shifted from red to Schemske 1983, Howe 1984a, Kiester whitish flowers through its flowering season, et al. 1984) point out that plant-pollinator as hummingbirds became more scarce "coevolution" is very diffuse. Most plant and hawkmoths predominated in the demes apparently experience simultaneous- local pollinator pool; through clever ly the selective pressures from several experiments the authors showed that pollinator populations, whose densities with hummingbird pollination red flowers (hence, relative selective impacts) may indeed produced more offspring than white fluctuate over time, as well as conflicting flowers, while the reverse was true late in selective pressures from seed predators, the season. Schoen & Clegg (1985) docu- seed dispersers, and neighboring plants. mented the effect of flower color on Demes of most flower-visiting animals, outcrossing rate and reproductive success free to roam widely in search of the most as a male parent in bumblebee-pollinated profitable floral resources, are even less Ipomoea purpurea (Convolvulaceae); they susceptible to selective influences of found that bees visited the pigmented particular plant species. In fact, I am morph significantly more frequently than unaware of any study clearly documenting the white morph, but that both morphs microevolution in nectarivores in response outcrossed at similar rates and the white 288 FEINSINGER

morph was actually favored as a pollen TABLE 1 donor. Effectiveness of different visitors as pollinators & (3) Results of Schoen Clegg (1985) of Calathea ovandensis flowers (Schemske & show clearly that counts of animal visitors Horvitz 1984). Hymenoptera included Euglossa to flowers may have little relevance to heterosticta, Eulaema cingulata, Exaerete the importance or effectiveness of different smaragdina, Bombus medius, and Rathymus pollinators (also see Kalin-Arroyo et sp. Lepidoptera included several species of al. 1985). This fact was recognized in Hesperiidae plus Eurybia elvina and the 19th century but has been stubbornly ignored ever since, particularly in applied Heliconius ismenius. pollination studies, where most studies Efectividad de distintos visitantes como polinizadores determine the "important pollinators" de flores de Calathea ovandensis (Schemske & Horvitz of crop plants through tallies of visit 1984 ). Los Hymenoptera incluyen Euglossa heterosticta, frequencies alone. Primack & Silander Eulaema cingulata, Exaerete smaragdina, Bombus medius, (1975) provide an objective index for y Rathymus sp. Los Lepidoptera incluyen varias especies estimating pollinator effectiveness, but de Hesperiidae, Eurybia elvina, y Heliconius ismenius. it is better yet to measure effectiveness directly by monitoring the reproductive Number of Total fruits set consequences of single pollinator visits visits from observed Fruit-set (Motten et al. 1981, Tepedino 1981, Visitors observed visits per visit Price & Waser 1982, Handel 1983, Spears Hymenoptera 1,817 140 7.7"1o 1983). Schemske & Horvitz (1984) used Lepidoptera 757 1 O.l"'o the last method to demonstrate that Calathea ovandensis (Marantaceae) flowers visited by euglossine bees had much greater have been re-reviewed recently enough reproductive outputs than flowers visited that only brief mention needs to be made by butterflies (Table 1). Many more such here. Kevan (1983) and Scogin (1983) studies are needed to document the selec- discuss the visual cues that attract many tive forces leading to the evolution of animals to flowers and sometimes serve particular floral traits. to guide them into contact with the reproductive parts. Both authors stress that different taxa of visually oriented animals BEYOND perceive the electromagnetic spectrum in a "POLLINATION SYNDROMES" variety of ways, such as bees' well-known ability to perceive ultraviolet reflectance General Considerations and absorbance patterns. Williams ( 1983) discusses olfactory cues that attract some Because each taxon of flower-visiting animals, in particular the odors that attract animal has a unique combination of neotropical euglossine bees to certain sensory perceptions, energetic needs, be- species of orchids; research on odors charac- havioral traits, flight capabilities, social terizing other pollination syndromes, and systems, capacities for learning, and on behavioral responses by other animals, nutrient constraints, individuals of each has progressed little since Faegri & Van will use somewhat different criteria in der Pijl's (1979) review. choosing flowers at which to forage. If Considerable research (some of it re- each taxon exerts selective effects on viewed in following sections) has been per- the plant demes it exploits, such as the formed on variation among pollination effects documented by Schemske & syndromes in the quantity and constit- Horvitz (1984), then widely different uents of nectar, the usual "primary plant species sharing a common taxon attractant" (sensu Faegri & Van der as "most effective pollinator" (Stebbins Pijl 1979) that lures animals to flowers. 1970) will tend to converge, over evo- Simpson & Neff (1983) describe not lutionary time, on a broadly similar set only the variation in nectar, but also the of phenotypic features, or a "syndrome" occurrence of two much more unusual (Faegri & van der Pijl 1979). floral secretions that attract particular The floral features that vary among bee groups: lipids and resins (see also pollination syndromes, thoroughly reviewed Armbruster 1984). Simpson & Neff (1983) earlier by Faegri & Van der Pijl (1979), also review briefly the many cases where NEW WORLD NECTARIVORY 289 pollen, not nectar, is the food resource (2) Hawk-moths (Lepidoptera: Sphin- collected by animals; Buchmann (1983) gidae) are large, usually nocturnal or reviews the phenomenon of "buzz pol- crepuscular, fast-flying nectarivores that lination", in which bees induce the release imbibe nectar through long proboscides. of pollen by clinging to dehiscent anthers Most flowers they visit have long tubes, and shivering their indirect flight muscles. are pale in color, and secrete moderate Finally, the well-known cases where to copious volumes of quite dilute nectar~ animals use flowers for protection or Hawk-moths and moth-pollinated plants brood places (see Feinsinger 1983a) have are quite frequent in warm temperate, experienced a flurry of recent research. subtropical, and tropical biota (Gregory With every new study, interactions between 1963-64, Cruden 1970, Cruden et al. figs (Ficus, Moraceae) and the tiny agaonid 1976, Miller 1981, Grant & Grant 1983, wasps that pollinate them are revealing Martinez del Rio & Burquez 1986). Moth greater and greater complexity in such species vary widely in body mass, body features as phenologies, extent of pa- and wing shape, and proboscis length rasitism, and wasp sex ratios (Janzen (Casey 1976, Bullock & Pescador 1983, 1979, Wiebes 1979, Bronstein 1986). Heinrich 1983b, W.A. Haber, personal Recent investigations show that the sup- communication, 1982). Likewise, moth- posedly tight ecological relationship be- pollinated plants vary widely in spatial tween North American Yucca (Agavaceae) dispersion of flowers, tube length, and and Tegeticula moths is actually quite un- nectar production. Consequences and predictable from site to site and season to correlates of such phenotypic variation season (Aker & Udovic 1981; J. Addicott, in terms of microevolution of moths personal communication, 1985). These and plants, ecology, foraging behavior, examples point out the value of long- community dynamics, and energetics (see term, detailed studies on purportedly section below) have scarcely been inves- coevolved systems. tigated other than in the studies cited above and in ongoing work by W.A. Haber (in Costa Rica) and S.H. Bullock (in Mexico). A Few Examples of Syndromes (3) In Central and South America, large bees pollinate a great diversity of (1) Many orchids of the lowland Nee- plant species with large, brightly colored tropics are pollinated exclusively by flowers (reviewed by Frankie et al. 1983). male euglossine bees that land on the flower An equally diverse set of plants, usually but extract neither nectar nor pollen. having numerous small flowers, is pol- Although some bees visit many orchid linated by small solitary, semisocial, and species and some orchids attract many social bees (Janzen 1967, Heithaus 1979a, bee species (Ackerman 1983), in general 1979b, 1979c, Wille 1983). Much research the fragrances emitted by a particular remains to be done on these two "syn- orchid attract only a subset of the pool dromes", for example in terms of floral of euglossine species in the area. Bees characters, patterns of nectar production, apparently extract either the fragrance bee foraging behavior, the influence of bee compounds or other compounds; it is behavior and sociality on pollen movement, possible that these are used as precursors flowering phenologies, and community to pheromones used in mating (Williams dynamics of bees. 1983, Williams & Whitten 1983). Current ( 4) Butterflies are frequent visitors to research involves careful characterizations tropical and temperate flowers, for exam- of the chemical constituents of fragrance ple many flowers in the Chilean Andes spectra; intrapopulation variability in fra- (Kalin-Arroyo et al. 1983, in press). grance spectra; the biochemical pathway Although some plants appear to be between fragrances (or other compounds) adapted specifically for butterfly pol- produced by the orchids and the mating lination (Cruden & Hermann-Parker 1979, pheromones of the bees; and the role Murawski & Gilbert 1986), the diversity of those pheromones in bee behavior (N.H. of flower forms that butterflies actually Williams, personal communication, 1985; visit is quite extensive, ranging from cf. Williams 1983, Williams & Whitten brush-like blossoms on many Compositae 1983). and Mimosoideae to tiny flowers of some 290 FEIN SINGER

Labiatae to the "typical" tubular yellow- 1984, Dobat 1985), but the body of data, on-orange blossoms. Butterflies are critical like that on hawkmoth pollination, is to pollination among the Andean flora still less extensive than that on diurnal, (Kalin-Arroyo et al. 1983, in press), but more easily quantified interactions. e!sewhere the ability of butterflies to (7) Other than a possible case of rodent carry large pollen loads and transfer them pollination in Costa Rica (Lumer 1980), effectively is debated (Murphy 1984). pollination by non-flying mammals has Butterfly pollination remains somewhat rarely been investigated in North and of an enigma. Central America. Evidence from un- (5) Pollination by hummingbirds (Tro- disturbed South American habitats (Jan- chilidae) has been extensively studied son et al. 1981) suggests that pollination in North and Central America. Most by arboreal mammals may have been more hummingbirds that migrate to North widespread before human hunters arrived America have short, straight bills (Brown on the scene, and it is possible that some & Bowers 1985) and forage at plants neotropical trees and lianas currently having tubular, red corollas of moderate assigned to bird-, bat-, or even bee-pol- length (Grant & Grant 1968, Brown & lination syndromes actually evolved in Kodric-Brown 1979). In Central and response to pollination by primates or South America and the West Indies, though, other arboreal mammals. hummingbirds have a variety of bill shapes (Feinsinger & Colwell 1978, Stiles 1978, How Useful is the "Syndrome" Approach? 1981, Snow & Snow 1980, Feinsinger 1983a, Kodric-Brown et al. 1984). Most Of course, many other pollination syn- fall into two basic categories, short straight dromes can be identified among New bills (like those of the migrants to North World plants (Baker & Hurd 1968, Faegri America) and long, often curved bills & Van der Pijl 1979). In my opinion, how- (suchs as those of the hermit hummingbirds, ever, continued emphasis on "pollination Phaethominae). Flowers adapted for pol- syndromes" is unproductive. Such emphasis lination by short-billed species tend to re- leads one to expect animals to use the same semble their North American counterparts set of cues in choosing flowers as pollination in shape and in rate of nectar secretion, ecologists use in assigning plants to syndro- but sport a great diversity of colors. Short- mes, whereas in reality a foraging animal billed hummingbirds also visit a variety chooses among potential food items on the of flowers in other "syndromes", such as basis of perceived benefits and costs. Per- bee-, moth-, bat-, and passerine-pollinated ceived benefits and costs are determined by species. Some short-billed hummingbirds many proximate criteria that do not fit also rob the flowers normally pollinated easily into "syndromes", such as the by their longer-billed relatives (McDade dispersion and density of flowers, previous & Kinsman 1980). Long flowers, which activity by other foragers of the same or include most species of Heliconia and different species, and the extent of food representatives of numerous other plant limitation. Thus, any one animal may families, come in a great variety of shapes actually forage at a much greater variety and colors. Most secrete copious volumes of flowers than a "field guide to syndro- of sugar-rich nectar. Several detailed, long- mes" would indicate. Emphasis on syn- term studies have taken place on particular dromes diverts attention from the very hummingbird-plant interactions in the real ecological (and evolutionary) role of West Indies (e.g., Snow and Snow 1972, nectar robbery by animals in the same Feinsinger & Swarm 1982, Feinsinger taxon as, or different taxa from, the et al. 1982, 1985, Kodric-Brown et al. "legitimate" pollinator (Baker et a!. 1971, 1984) and Central America (e.g., Lyon & Chadek 1971, McDade & Kinsman Stiles 1975, 1978, 1981, 1985, Fein- 1980, Roubik et a!. 1985). Likewise, to singer et a/. 19 86), but detailed long- classify plants into one or another syndro- term studies from South America have me the ecologist must ignore the many not been published. flowers pollinated by two or more distinct (6) Research on bat pollination, re- taxa, and the different selective effects viewed earlier by Baker (1961, 1973), has these may have (e.g., Baker et a!. 1971, increased in recent years (e.g., Heithaus Waser 1982, Schemske & Horvitz 1984). et al. 1974, 1975, Marshall 1983, Hopkins Finally, emphasis on syndromes diverts NEW WORLD NECTARNORY 291 attention from the unifying concepts pounds; and, of course, carbohydrates. that prevail in animal-flower interactions Floral nectaries can secrete any or all regardless of the taxa iiwolved. The first of these; at present, the limits to what such concept to discuss is the relation- can be secreted are largely unknown. ship between metabolic demands of the Because carbohydrates seem to be the pollinator and food available in the flowers major "currency" in animal-flower inter- visited. actions, they have received the most attention from researchers.

METABOLIC NEEDS OF POLLINATORS Measuring the energy content of nectar VERSUS FOOD AVAILABLE IN FLOWERS The pattern of carbohydrate production Not Everything is Mutualistic among individual flowers has several aspects, each potentially subject to nat- From a nutritional standpoint, the mu- ural selection, and all of which have tualism between plants and flower-visiting ecological and evolutionary implications animals dissolves into a series of skirmishes. to animal flower-visitors. These aspects In general terms, the most fecund plant include (1) the volume of nectar a flower phenotype is that which maximizes the secretes; (2) the energy content of each ratio (effective pollen transfer/energy ex- microliter of nectar or of the total volume; pended in attracting pollinators]. The (3) the temporal pattern of secretion; numerator of the ratio is highest if the ( 4) the extent of variation among the flower produces sufficient food to attract flowers on a plant, or among plants in an effective pollinator, but not so much a deme, in each feature 1-3; and (5) food that the pollinator becomes sluggish patterning of this variation within the and sedentary (Heinrich & Raven 1972, plant according to inflorescence size, Carpenter 1976, Feinsinger 1983a). In shape, and location. some flowers, at least, the production To measure nectar volumes, my col- of "floral rewards" is costly enough to leagues and I use Drummond brand micro- exert selection for a decreased denominator pipettes. To extract nectar from curved as well (Southwick 1984). In other words, flowers or other flowers with hard-to- a famished, harried pollinator is often reach nectar chambers, we use flexible the most effective from the plant per- Intramedic brand polyethylene tubing; spective because to achieve a neutral or the nectar thereby extracted is then trans- slightly positive energy (or nutrient) ferred into a Drummond micropipette budget, the food-limited animal must for accurate measurement. Flowers of visit many flowers. many species can be repeatedly sampled; Naturally, the "optimally foraging" if this is done, cumulative measurements animal will operate quite differently from repeatedly sampled flowers should (Carpenter et al. 1983, Pyke 1984). It be compared with total nectar accumu- is often assumed that the most fit animal lated by flowers unmolested throughout phenotype is that which maximizes net the sampling period, for repeated sampling energy intake, the ratio (energy ingested/ can either stimulate or depress secretion energy expended], over a fixed time or, rates (Feinsinger 1978, Cruden & Hermann- under some conditions, that phenotype Parker 1983). In other plants, only de- which minimizes the time spent obtaining structive sampling is possible, so one must a fixed amount of energy. Thus, the begin with a very large number of flowers energetics of animal-flower interactions and then measure the accumulated nectar involve a delicate interplay between con- in a random subsample of these at regular flicting selective pressures; the balance intervals (e.g., Stiles 1975, Feinsinger et al. shifts according to the density of animals 1982). relative to flowers and according to many A clear distinction must be made other ecological variables (Heinrich & between measuring nectar secretion, and Raven 1972, Heinrich 1979a, 1983b). measuring nectar availability or standing A foraging animal requires many types crop. Secretion patterns provide the base- of nutrition: a balanced intake of different line data on food presentation by the amino acids and/or of protein; vitamins; plant, analogous to "primary productiv- trace elements or compounds; fatty com- ity" in ecosystem studies. The animal 292 FEINSINGER arriving at a flower patch encounters, flower-visitor requires a greater energy however, the standing crop, which is a intake per unit time than a small one. function not only of underlying secretion Endothermy, practiced not only by verte- patterns but also of the foraging by all brate nectarivores but also by many flower- previous visitors, as well as a function visiting insects, requires an additional of post-secretion evaporation or dilution energy input (Heinrich 1975b, 1975c, (cf. Gill & Wolf 1975, 1979, Feinsinger 1 983b ). The mode of locomotion em- 1978). Therefore, nectar available to the ployed during foraging -hovering flight, incoming animal may differ greatly from flapping flight, or landing and walking- the pattern in which nectar is secreted affects total energy expended and there- (Feinsinger et al. 1985), a fact frequently fore required. Except for a verbal argument ignored by researchers. by Heinrich (1975c, 1983b) and a disputed The energy content of nectar can be model of Pyke ( 1981; see Miller 1985), the determined by using a hand refractometer costs and benefits of these three foraging reading in dregrees Brix (percent sucrose modes have not been rigorously examined. equivalence, or weight of solute/total Continuous hovering flight allows rapid weight solution). I recommend the Reichert visits and thus high intake rates, but to (American Optical) Model 10431, a sturdy land instead and walk among flowers instrument much less expensive than obviously conserves energy. Thus, for a bee better-known models but equally accurate; that lands and walks, or a hummingbird we use clear Plexiglass chips to flatten that perches while feeding, foraging at the nectar droplet against the prism. The an inflorescence of many small flowers reading in degrees Brix is converted to consumes much more time but only grams sugar/liter of solution, or micro- slightly more energy than foraging at a grams/microliter, using Table 88 in the single large flower with the same total CRC Handbook of Chemistry and Physics nectar volume. For a hummingbird or (1978-1979). The refractometer reading hawkmoth that continues to hover while is located in Column 1 of that table, and feeding, though, the time difference the grams sugar/liter (= micrograms/ translates into a considerable energy microliter) is read from Column 4 (Bolten difference. et al. 1979). One microgram of sucrose Just how many flowers must a hawk- provides 0.01648 joules, or one microliter moth, for example, visit in order to of a sucrose solution that is 1 microgram/ strike a positive energy balance? Moth- microliter provides 0.01648 j. For example, pollinated flowers vary greatly in nectar consider a flower that secretes 15 micro- volumes and concentrations (W.A. Haber liters of a 20% sugar solution. A solution & G.W. Frankie, unpublished manuscript). of 20% sugar contains 216.2 grams/liter Let us use two examples: the herbaceous of sugar, or 216.2 micrograms/microliter Costa Rican weed Hippobroma longiflora (CRC Handbook of Chemistry and Physics (Lobeliaceae), secreting 40.1 ± 16.0 micro- 1978-1979). Thus, each microliter contains liters•flower- 1 •nighr 1 of nectar with su- 3.563 j, and the entire volume of 15 micro- crose equivalence 13.6% ± 2.1%; and the liters contains 53.45 j. The energy content vine Ipomoea alba (Convolvulaceae), se- 1 of a given percent sucrose solution is creting 8 .3± 2.1 microliters• flower-1 • nighr approximately equal to the energy content of nectar with 39.0% ± 2.2% sucrose of the same percentage monosaccharide equivalence. Using the method described solution; thus, energy value of nectar above (Bolten et al. 1979), we calculate that each microliter of Hippobroma nectar is quite independetH of the identity of 1 the sugar constituents, although other provides 2.361 j, versus 7.53 j·microliter- solutes in the nectar may bias the refracto- for Ipomoea nectar. Thus, a full flower meter reading slightly (Inouye et al. 1980). provides 94.7 j or 62.5 j, respectively. Casey (1976; also see Bartholomew & Casey 1978, Heinrich 1983b) studied Pollinator energetics and nectar patterns the energetics of hovering in various sphingids ranging from 0.12 to 6.25 g, and How much carbohydrate "fuel" is needed found that a 1 gram hovering sphingid uses 1 by a foraging animal, and what features 1154- 1593 j·h- , just to balance the influence this requirement? Body size is energy expended in hovering. Thus, a 1 g one obvious factor; all else equal, a large sphingid must visit 12 - 17 full Hippo- NEW WORLD NECTARIVORY 293 broma flowers or 18 - 26 full Ipomoea where Y is j·h-1 required for hovering and flowers per hour. Undoubtedly, forward X is mass in g. Thus, a 0.1 g hawkmoth 1 flight is less energetically costly than requires only 192.5 j·h- , whereas a 6 g hovering in place (cf. Gill 1985), but also animal (and some hawkmoths are even 1 the moth must obtain a positive, not larger) requires 5306 j·h- • How do inter- neutral, energy balance while foraging in nal diameters of proboscides, and intake order to maintain at least a neutral energy rates, vary with mass? This is unknown. balance over the entire 24-hour cycle. Clearly, though, large moths cannot effec- Such estimates of the hawkmoth- tively utilize flowers with small nectar flower energetic relationship stimulate volumes. For example, Heinrich (1983b) many speculations and questions. They calculates that a 6 g hawkmoth would imply that sphingids will only bother need to visit 580 Kalmia latifolia flowers to visit flowers that secrete quite copious each minute just to keep even. Is there a nectar. Even though the speed at which compensatory advantage for large body hawkmoths can travel long distances cuts size? Heinrich (1983b) proposes that down on their transit costs, they are large moths can fly farther, in search of expected to visit isolated plants only if nectar sources or host plants for ovi- the reward is correspondingly great; thus, position, than small moths. Furthermore, plants occurring in widely scattered popu- large moths may have access to richer lations will experience stronger selection nectar sources than small moths. Bullock for copious nectar production than plants & Pescador (1983) found a significant typically occuring in dense clumps. Hawk- positive correlation, across species, between moths are expected to choose flowers wing length and proboscis length; the having not only high secretion rates but correlation even holds within species, also high standing crops, i.e., flowers where individuals may vary more than unvisited by other sphingids and protected threefold in mass and twofold in pro- from other nectarivores; thus, hawkmoth boscis length (Casey 19 7 6; see also Miller flowers might be expected to protect their 1981 ). In general, long-tubed moth flowers nectar better (physically, and biochemically provide more nectar than short-tubed species through repellent compounds in floral (Opler 1983; Haber & Frankie, unpublished tissues) than flowers in many other syn- manuscript). At present, though, there is dromes. Like hummingbirds (Diamond little evidence from the New World that et al. 1986, Karasov et al. 1986), hawk- large, long-tongued hawkmoths specialize moths might be expected to process on long-tubed, richly rewarding flowers, nectar quickly and to extract sugars effi- although this relationship apparently does ciently, but this has not been investigated; exist on Madagascar (Nilsson et al. 1985 ). even crop capacities of hawkmoths are One other morphological feature affects unknown, although W.A. Haber (personal hawkmoth energetics: wing loading, the communication, 1986) has observed cap- ratio of body mass to total wing area. tive hawkmoths imbibing, over a 5 minute Casey (1976) examined moths of similar period, quantities of nectar equal to their mass but different wing loading and found body weight. Presumably, energetic require- that the energy expended in hovering ments differ between the sexes; this has not increased sharply with increasing wing been investigated. To cut down costs of loading or increasing wing disc loading thermoregulation and maximize the intake (ratio of body mass to the area of the of undiluted nectar, hawkmoths are ex- disc defined by the tips of the wings pected to forage only when weather during flight). Thus, moths with long conditions are ideal; hence, moth-poll- wings expend less energy in hovering than inated plants may experience very erratic moths of equivalent mass but short wings pollination success (Martinez del Rfo (Table 2). What are the costs of long wings? & Burquez 1986). Do they enforce slow flight (cf. Gi111985) Not all hawkmoths have a 1 gram mass. and thus increase transit times between In fact, body size in sphingids spans nearly far-flung flowers? How do mass, wing 2 orders of magnitude. Bartholomew & loading, and wing disc loading correlate Casey ( 197 8) present the empirical equation. with choice of flower species and flower dispersion? What is the range of hawkmoth 0 81 y = 1243 X " "foraging tactics"? The data will be 294 FEINSINGER

TABLE 2

Effect of wing length and shape on the power output required to hover, among hawkmoths (Sphingidae) of similar body mass (Casey 1976)

Efecto de Ia forma y longitud del ala en Ia potencia requierda para vuelo estacionario en polillas (Sphingidae) de masa corporal similar (Casey 1976).

Wing disc Wing span Wing loading loading Required power Species Mass (g) (em) (g cm-2) (g cm-2) (cal h-1 g-1)

Protambulyx strigilis 1.20 12.8 0.057 0.009 5.7 Manduca sexta 1.21 11.0 0.082 0.016 7.7 Agrius convolvuli 1.20 8.7 0.195 0.020 8.7

difficult to collect, but the results are sure hovering (Epting & Casey 1973). Hum- to be intriguing. mingbirds with high wing disc loading Likewise, what is the relationship (heavy for their wing length) expend more between sugar concentration and flower energy than hummingbirds with equivalent choice by hawkmoth? Sugar concentration masses but longer wings. The most efficient varies greatly among the nectars of hawk- flight speeds of the former, however, may moth flowers (Haber & Frankie, un- be much higher than those of the latter, published manuscript). Undoubtedly, in- so that even if they expend more energy ternal tongue widths and nectar extraction per unit flight time birds with high wing rates vary greatly among hawkmoths. disc loading may cover a long distance Perhaps, then, there are parallels between with less total energy expenditure (Gill hawkmoth feeding energetics and the 1985). much better studied feeding energetics At one time it appeared that wing disc of butterflies. Kingsolver & Daniel (1969) loading (and required energy output for proposed a biophysical model for the hovering) was clearly related to a simple mechanics of nectar extraction by but- dichotomy in hummingbird foraging behav- terflies, and after making a number of ior: hummingbirds with high wing disc assumptions proposed that maximum net loading defend territories at dense clumps energy intake would occur at a sugar of flowers that yield abundant energy, concentration of 20-25% sucrose equival- whereas behaviorally subordinate species ence regardless of the butterfly considered. or sexes that are excluded from these Recently, more sophisticated studies in rich nectar pockets, foraging instead on biophysics and bioenergetics (May 1985b, dispersed, nectar-poor flowers, have low c, Pivnick & McNeil 1985) have shown wing disc loading and low foraging costs that many of the earlier assumptions were (Feinsinger & Chaplin 1975, Feinsinger unrealistic, and that optimum sugar con- et a!. 1979b). Continued investigation has centrations varied among butterfly species revealed a more complex picture. The and even between sexes. Through con- relationship we originally proposed seems trolled laboratory experiments in which to be restricted to hummingbirds having butterflies' proboscides were inserted into moderately short, straight bills and foraging capillary tubes with predetermined flow primarily at ornithophilous flowers. Small, rates and "nectar" constituents, May behaviorally subordinate (in encounters (1985a, b) has even determined the fitness with larger territory-holders), bee-like consequences of flower choice in but- hummingbirds frequently forage at small terflies. insect-pollinated flowers and also tend Likewise, wing disc loading has been to have high wing disc loading (P. Feinsin- investigated much more thoroughly in ger, unpublished data). Here, high loading another taxon than in hawkmoths. In may permit exceedingly precise probes hummingbirds, wing disc loading clearly into numerous closely packed flowers in relates to the energy expended while rapid succession. Many hermit humming- NEW WORLD NECTARNORY 295 birds (Phaethominae) and other long moths have more dilute nectar, not more billed hummingbirds also have high wing concentrated nectar, than short-tubed ones disc loadings but are rarely bellicose; (Haber & Frankie, unpublished manuscript). for them, the relationship between wing disc loading and most efficient flight Pollinator physiology and nectar speed (Gill 1985) may be most important, constituents for these birds often fly many hundreds of meters between isolated flowers each The chemical composition of sugar in holding a copious supply of concentrated nectar varies widely, and to some extent nectar (Stiles & Wolf 1979, Feinsinger is associated with pollinator taxon (Baker & 1983a). Baker, 1983a, 1983b, 1983c). For example, Copious, concentrated nectar aver- most flowers adapted for hummingbird, aging around 35% sucrose equivalence hawkmoth, or butterfly pollination are at sea level) in fact characterizes most rich in sucrose, whereas those adapted for flowers adapted for pollination by long- pollination by bats, passerine birds, or billed hummingbirds. Until recently this bees are hexose-rich. The distinction fact (Stiles 1975, Bolten & Feinsinger between nectars of hummingbird- and 1978, Feinsinger et al. 1982, unpublished passerine-pollinated flowers is especially data) was unreconciled with other assertions intriguing: it occurs even among closely that most hummingbird flowers secreted related species, such as those in the genus quite dilute nectar, averaging around 20- Erythrina (Baker & Baker 1983b, 1983c). 25% sucrose equivalence at sea level (Baker Current research addresses the physio- 1975, Pyke & Waser 1981) or with biological basis and behavioral consequences physical models showing that the net of sugar preferences in nectar-feeding energy hummingbirds gained from nectar birds (C. Martinez del Rfo, personal actually declined with increasing sugar communication, 1986). concentrations (e.g., Heynemann 1983). Baker & Baker (1975, 1983b) have also In 1982, however, Ewald & Williams performed the definitive studies on the showed that at least one hummingbird distribution of other organic compounds species fed by extremely rapid licking among floral nectars. In particular, amino (ca. 0.06 seconds per lick), squeezing the acid concentrations and constituents vary nectar from the tongue each time the widely among nectars, and, like sugars, tongue was exserted through the tightly appear to correlate with expected prefer- closed mandibles. For the hummingbird ences, of pollinators, considering meta- examined, each lick meant an intake of bolic needs, requirements of nutrients about 1 microliter of nectar. Kingsolver for reproduction, and the availability of & Daniel (1983) showed that, if the nectar alternate protein sources in the normal volume in a flower was sufficiently small diet. For detailed information, readers to be extracted with one or a few licks, should consult the Bakers' thorough net energy intake would indeed be maxi- reviews. mized (at sea level) at 20-25% sucrose equivalence; but if the nectar volume was Pollen and animal metabolism sufficiently large to require multiple licks, net energy intake at sea level would be Many animals visit flowers to extract maximized at 35-40% sucrose equivalence! pollen, not nectar (Simpson & Neff 1983). Secretion rates and standing crops in The role of pollen in diets of the bee family long-tubed hummingbird-pollinated flowers, Apidae is well known (Vivino & Palmer which also have high sugar concentrations, 1944, Haydack & Tanquarry 1963, Hein- greatly exceed those in short-tubed hum- rich 1979a). Gilbert ( 1972) describes the mingbird-pollinated flowers (Feinsinger & means by which Heliconius butterflies Colwell 1978; Feinsinger et al. 1982, extract nutrients from pollen, and des- 1985, unpublished data, Beach et al., cribes the consequences of this procedure unpublished manuscript). Thus, the model to the fecundity and longevity of the fits very well the data on nectar in hum- insects. Through complex laboratory experi- mingbird-visited flowers. Apparently the ments, Howell (1974) detailed the impor- Kingsolver-Daniel (1983) explanation does tance of pollen in the diet of female (and not extend to hawkmoths, however, for male) bats (see also Simpson & Neff 1983). long-tubed flowers pollinated by hawk- Foraging on pollen is more difficult to 296 FEIN SINGER observe and quantify than foraging for all flowers secreting at equal rates, con- nectar, which may explain the paucity sidering haphazard visits from previous of research on pollen consumption by foragers. Thus, individuals in a food- animals other than honeybees. limited animal population would be unlikely to discriminate against plants with Do plants ''manipulate'' pollinator foraging? "sloppy" secretion patterns. Bonanza-blank patterns have also been discovered in plants Let us examine more closely the conflict visited by those bees that are often food- between patterns of nectar production limited at the population level (e.g., Brink that maximize effective pollination for 1982, Frankie & Haber 1983, Herrera & plants, and patterns that maximize net Soriguer 1983). energy intake by pollinators. At times, The "bonanza-blank" model extends to flower-visiting animals, individually or interspecific mumcry. Many examples collectively, can "manipulate" plants by occur of nectarless plants that resemble choosing the most rewarding food sources nectar-producing species flowering nearby and virtually ignoring others, but at other (see reviews by Heinrich 1975c, Wiens times, when nectar is limiting to pollinator 1978, Feinsinger 1983a, Dafni 1984). populations, plants can "manipulate" pol- As long as mimic plants are rare relative linators because at least some pollinator to rewarding ones, pollinators may fail individuals will be forced to forage at to distinguish the different species, and plants that secrete just enough nectar to the mimic plants could achieve pollination Provide a positive energy balance. with no energy expended on feeding ani- An interesting pattern occurs in flowers mals. At this time, there is little evidence adapted for hummingbird pollination. Long- that these situations are truly model- billed hummingbirds are only sporadically mimic phenomena (Bierzychudek 1981 a). food-limited (Stiles 1975, 1978, 1981, It is clear, though, that pollinators exert Feinsinger 1983a, unpublished data). Indi- strong selective pressures on patterns of viduals are very selective among species nectar secretion (and, presumably, on of long-tubed flowers adapted for pol- production of pollen as food) by plants, lination by them. Most species of long- and that these selective pressures vary tubed flowers secrete high mean nectar with the relative numbers of pollinators volumes with low variance. Short-tubed and plants even as this ratio changes flowers pollinated by short-billed humming- through a single flowering season. birds, however, in habitats where these birds are often food-limited as a group, secrete low mean nectar volumes with THE ROLE OF ANIMALS IN SEXUAL exceedingly high variance (Fein singer 197 8, SELECTION AND BREEDING SYSTEM Feinsinger 1983a, 1983b). Previously I EVOLUTION IN PLANTS interpreted these "bonanza-blank" patterns of nectar secretion as features that created The pollinator:flower ratio, the predicta- intermittent reinforcement schedules for bility of pollinator visitation, and the hungry foragers, prolonging hummingbird foraging behavior of individual flower- attention to flower species having such visiting animals may also play a role in patterns and maximizing pollen movement the evolution of plant breeding systems. while minimizing energy expended on Recent papers propose schemes for animals' nectar (Feinsinger 1978, 1983a, 1983b, influence on the evolution of particular Ott et al. 1985; see also Sober6n & Marti- breeding systems (e.g., Beach & Bawa nez del Rio 1985). It is likely, however, 1980, Givnish 1980, 1982, Beach 1981, that plants visited by numerous food- Kress 1983, Baker 1984) or, more generally, limited foragers simply experience a the evolution of the great diversity of relaxation in selective pressure to mini- breeding systems that exist among angio- mize variation, such as the pressure sperms (Bawa & Beach 1981, Wyatt 1983). that long-flowered plants presumably Recently, the possible influence of experience. To the short-billed humming- pollinators on sexual selection in plants bird the standing crop resulting from has drawn considerable attention (Janzen a bonanza-blank pattern in underlying 1977, Willson 1979, 1983, Stephenson & nectar secretion would be indistinguishable Bertin 1983, Willson and Burley 1983, from the pattern of standing crop were Bell 1985). Underlying the theories and NEW WORLD NECTARIVORY 297

research on sexual selection is the "Bate- only has this variation been shown to man Principle" (Bateman 1948, Charnov have a basis in the gametophyte (pollen 1979), which proposes an asymmetry in tube) genome, but also strong correlations the costs of producing male and female have been shown between the speed gametes. The principle holds that female with which tubes of a particular gametes are more costly to produce than donor grow down a particular plant's male gametes; thus, fewer female gametes style and the vigor of the resulting off- are produced. Consequently, maternal spring (Mulcahy 1979, 1983, Mulcahy fitness is unlikely to be limited by the et al. 1983). Fifth, intense competition number of male gametes available; rather, among growing pollen tubes for access to given an overabundance of male gametes, a flower's ovules (Mulcahy 1979, Marshall maternal fitness is likely to vary with & Ellstrand 1985, 1986) is exacerbated the genetic quality of the male gametes by various maternal mechanisms, such as successful in fertilization, and selection long styles (Mulcahy 1983, Mulcahy et al. should act on females to discriminate 1983), or stigma receptivity delayed among these gametes or, on the basis until many grains from diverse donors of phenotype, among the males providing have been deposited (Kress 1983, Galen them. Conversely, paternal fitness is et al. 1986). Sixth, mixtures of pollen from likely to be severely limited by the scarcity several donors have been shown experi- of female gametes; hence, intense com- mentally to increase seed set and seed petition for access to female gametes is "quality" in recipient plants compared likely to occur among male gametes or to the results of single-donor pollinations among males. (Schemske & Fenster 1983, Schemske & At first glance the Bateman Principle Pautler 1984, Marshall & Ellstrand 1985, appears to be a panacea capable of ex- 1986). plaining numerous phenomena in angio- In short, most current thought on sexual sperms. First, in many native and cul- selection supports the Bateman Principle, tivated plant populations the number of and suggests that maternal reproduction fruits matured appears to be limited by can be highly selective: either male gameto- resources available to the maternal plant, phytes (pollen tubes) compete intensely not the number of pollen grains received for access to ovules, ensuring that only (Willson 1979, Stephenson 1981, 1984, the fastest growing tubes -which may Motten 1986, Stephenson & Winsor 1986). produce the most vigorous offspring- end Second, many hermaphroditic plants pro- up contributing to zygotes; or, unable to duce far more flowers than the number mature all embryos in any event, plants · of fruits that are matured even when selectively mature only the potentially all flowers are doused with compatible most vigorous offspring after zygote pollen (Stephenson 1981); this result formation has occurred. Thus, animal is interpreted either in terms of selective pollinators are relegated to a minor role fruit abortion on the part of females, in maternal reproductive function among selection to maximize male reproductive plants, other than effects of the diversity function by dispersing pollen to as many of pollen loads they deliver (Mulcahy other plants as possible (Janzen 1977, 1979, Ellstrand 1984, Marshall & Ellstrand Bell 1985), or both (Bawa & Webb 1984, 1985, 1986), although of course they Sutherland & Delph 1984, Sutherland still are given a leading role in reproduction 1986a, b). Third, careful hand pollinations through paternity (e.g., Janzen 1977, have shown that some plants selectively Belll985). mature fruit based on the genotype of Field evidence for the Bateman Prin- the pollen source (e.g., Bertin 1982, ciple, though, is not nearly so conclusive. 1985, Lee & Bazzaz 1982, Bookman Bierzychudek (1981 b) pointed out that 1983, 1984), whereas pollen grains germany studies document plants that receive minate and produce pollen tubes wherever inadequate pollination for full seed- or possible. Fourth, there is tremendous fruit-set, and other studies (e.g., Snow variation in the rates with which pollen 1982, McDade 1983, McDade & Davidar tubes from different paternal donors, or 1984, Zimmerman 1984, Hainsworth et al. even the same donor, grow down a style 1985) also demonstrate that maternal (e.g., Mulcahy 1983, Mulcahy et al. 1983, reproduction of plants is frequently Marshall & Ellstrand 1985, 1986); not limited by pollen loads brought by ani- 298 FEINSINGER mals. For example, most hummingbird- flow· thus, I will deal with a few aspects pollinated flowers in cloud forest at Monte- only: verde, Costa Rica receive fewer compatible Accurate means exist for monitoring pollen grains [as indicated by the number the dispersal of individual pollen grains of pollen tubes reaching the base of the from particular source flowers to recipient style, assessed with Martin's (1959) techni- stigmas. These are often so costly and que] than the number of ovules available time-consuming that sample sizes of for fertilization (Feinsinger et al. 1986; recipient flowers are severely limited. W. H. Busby & S. Kinsman, unpublished At the other extreme, many studies, such data). as most of those reviewed by Levin & Enticing though it is, then, the Bateman Kerster (1974), use large samples of Principle should be applied with caution: pollinator flight distances to estimate real plant populations experience spatial, roughly the distance that pollen moves. temporal, and interspecific variation in the Because pollen is often carried for several relative importance of pollen and female successive flights, because the extent of resources as limits to maternal reproduc- such pollen carryover varies greatly among tive output. In my opinion, recognizing pollinators, and because the number of the interplay of pollen versus resource grains carried also varies greatly among pol- limitation that natural plant populations linators, pollinator flight distances may experience opens up many more oppor- often be very poor indices to actual pollen tunities for theory and research than does flow (Schaal 1980. Handell983, Lertzman passively accepting the popular paradigm & Gass 1983). Recently, many researchers of the Bateman Principle. have compromised on a technique that yields large sample sizes yet is less biased than tallies of pollinator flight distances: tracing the movement of a pollen analog, THE INFLUENCE OF ANIMAL POLLINATORS fluorescent dye. ON GENE FLOW AMONG PLANTS Powdererl dyes whitish in visible light The extent of gene flow among plants but highly colored under fluorescent determines deme size and obviously light are available from various North affects microevolution of plant pop- American manufacturers. Small amounts ulations (Levin & Kerster 1974). The of dye can be applied to newly dehisced terms "neighborhood area" and "neigh- anthers with, for example, a flat toothpick; borhood size" have more precise de- after foraging has taken place, possible finitions than "deme size", and are in recipient stigmas can be collected and general use. Neighborhood size is an examined under a fluorescent light for index to the number of individuals among the presence of dye. Ideally, stigmas are which gene flow occurs over the course examined under a compound microscope of a generation, whereas neighborhood equipped with an epifluorescence system area is simply the area occupied by those [the same microscope used to count individuals (Levin & Kerster 1974). Each pollen tubes (Martin 1959)], which allows concept, neighborhood size and neighbor- the detection of single grains of dye; but hood area, has different implications a dissecting microscope, or even just to local adaptation and microevolution a hand-held ultraviolet light source, is of plants. sufficient for relative estimates to be Breeding systems of plants, and dispersal made. The fluorescent-dye technique has patterns of seeds, obviously influence gene flaws. Handel (1983) points out that flow. The foraging behavior of flower dye dispersal is only an index to actual visitors, and the number of successive pollen flow and cannot be used to estimate recipients to which they carry pollen true pollen dispersal distances without from a single donor ("pollen carryover"), exhaustive testing (see also Waser & Price obviously have a major impact as well 1982). Even pollen flow itself is at best (Handel 1983, Lertzman & Gass 1983). only an index, and perhaps not a very Handel (1983) details techniques for good one, to actual gene flow, because tracing pollen movement from source to the success of pollen at fertilization may recipient flowers, and thoroughly reviews vary with distance from the donor plant the literature on pollinators and gene (Waser & Price 1983a). Still, for com- NEW WORLD NECTARNORY 299

parative studies fluorescent dyes, used may move pollen in different ways (Linhart properly, provide reasonable relative in- 1973, Linhart & Feinsinger 1980). dices to pollen movement by animals, indices certainly preferable to those de- rived from pollinator flight distances "FORAGING STRATEGIES" (Thomson et al. 1986). OF FLOWER-VISITING ANIMALS What are some aspects of pollinator foraging (and flowers) that affect pollen We tum to the ecological determinants dispersal and gene flow? ( 1) Pollinators of foraging choices made by flower-visiting do not move in random directions after animals, choices whose consequence is leaving a particular flower. Levin et al. pollen movement among flowers. Animal- (1971) and Hodges & Miller (1981) dis- flower systems are nearly ideal for testing covered marked directionality in the general theories in foraging behavior. flight paths of pollinators and, conse- Foraging choices made by nectarivores have quently, in gene flow (see also Handel consequences not only to their own food 1983, Handel & Mishkin 1984). (2) Varia- intake, but also to the plants involved; as tion in the extent of pollen carryover has discussed above, this feedback loop leads been investigated thoroughly by a few over time to the patterning of rewards researchers only (e.g., Thomson & Plowrigh t by plants. In many cases the rewards 1980, Price & Waser 1982, Waser & Price themselves are easily quantified by the 1982, 1984, Lertzman & Gass 1983). Appa- ecologist; costs and benefits of different rently, deposition of pollen from a particular foraging choices are estimated with re- donor flower does not always follow a lative confidence; many nectarivores are smooth decay curve; instead, some may exceedingly easy to observe and even to be retained through visits to several manipulate while foraging; patterns of succeeding flowers, to be deposited by rewards are easy to mimic experimentally; chance much later in the animal's foraging and the risk of predation, which confounds bout. (3) By influencing the movement foraging studies on other trophic groups, patterns of pollinators, average nectar is not a significant factor at least for volumes and the pattern of nectar variation some nectarivores. Thus, in recent years among flowers will affect pollen dispersal "foraging tactics" of nectarivores have distances and neighborhood size (Wadd- attracted more research interest than has ington 1981, Zimmerman 1982, Ott any other aspect of animal-flower inter- et al. 1985). (4) The spacing between plants actions, and some of these studies have can influence both neighborhood size contributed substantially to the growth and area. Area changes because pollinators of foraging theory in general (Pyke et al. must move farther among more widely 1977, Pyke 1984). spaced plants to obtain the same amount of food (Levin & Kerster 1974, Beattie Territoriality: Why, When, and How 1976). Both neighborhood size and neighborhood area change if the identity Many nectarivores defend territories at of the pollinators themselves changes dense clumps of flowers. Unlike those with altered flower dispersion (Linhart of many other animals, nectar-centered 1973, Feinsinger 1978, Linhart & Fein- territories are often very responsive to singer 1980). (5) Different pollinator rapid temporal shifts in resource density, species visiting the same flowers will move intruder pressure, and the energetic needs pollen different distances, so that the of the resident. This flexibility facilitates relative frequencies of different visitors research on the ecological determinants, will have marked effects on neighborhood behavioral correlates, and consequences of size (Schmitt 1980, Waser 1982). For territoriality. example, flight distances of butterflies Territoriality has both benefits (potential tend to have higher means and much increases in gross energy intake) and costs higher variances than flight distances (excluding intruders through displays or of bees (Schmitt 1980); hummingbirds chases). Like other animals, nectarivores may move pollen much longer (Webb are expected to be territorial (a) when & Bawa 1983) or much shorter (Murawski energy is limiting; (b) when territoriality, & Gilbert 1986) distances than butterflies; here defined as defense of an area within and different species of hummingbirds which the resident controls or restricts 300 FEINSINGER the use of resources, results in a greater net North American meadows through which energy gain than non-territorial foraging; these hummingbirds migrate, flower den- and (c) when other aspects of daily life, sity varies on a daily time scale, yet hum- or of fitness, do not suffer as a con- mingbirds respond extremely qUlckly to sequence of territorial behavior. this variation (Carpenter et a/. 1983). Carpenter & MacMillen (1976), Kodric- On most days the meadows are fully Brown & Brown (1978), Gass & Mont- occupied by territories each of which gomerie (1981), Ewald & Orians (1983), provides its resident with just enough and Hixon et al. (1983), among others, nectar to equal or exceed slightly the discuss various models for changes in the daily energetic requirements. cost: benefit ratio with variation in floral density or intruder pressure. At low flower Do other foraging modes maximize net densities, territorial behavior is disad- energy intake? vantageous because resources are inde- fensible. At high flower densities, territorial Some non-territorial hummingbirds, and behavior becomes disadvantageous because other nectar-feeders, visit scattered flowers either (a) nectar becomes so abundant in a quite regular, repeated sequence. that the increment in gross energy intake "Traplining" behavior was first described provided through flower defense vanishes; in female euglossine bees (Janzen 1971) (b) intruder pressure rises to the point and has since been reported for male where costs exceed benefits; or both. euglossines (Ackerman et a/. 1982) and These researchers tested the models on two very different functional groups of Hawaiian honeycreepers (Carpenter & hummingbirds: the long-billed species that MacMillen 1976) or hummingbirds (Kodric- exploit nectar-rich but scattered flowers Brown 1978, Ewald & Orians 1983, Hixon (Linhart 1973, Feinsinger & Colwell 1978, et al. 1983), and in general found a good Gill 1978, Stiles 1978, 1981), and those fit: birds abandon territorial behavior short-billed individuals that are habitually when flowers become either sparse or excluded from territories (Feinsinger & exceedingly dense. Gill & Wolf (1975, Chaplin 1975, Feinsinger 1976). Often, 1979) performed parallel studies on long-billed "high-reward trapliners" allow African sunbirds (Nectariniidae); their plentiful nectar to accumulate in flowers detailed results show a clear energetic basis between revisits (Feinsinger, unpublished for rapid changes in territorial behavior. data; see Feinsinger et a/. 1985), but Nectar-feeding birds also show re- "low-reward trapliners" appear to keep markable flexibility in the mechanisms nectar levels exceedingly low by attuning employed in the defense and exploitation revisit frequencies to rates of nectar se- of territories. Ewald & Orians (1983) cretion (Feinsinger 1976, Gill 1978), showed that Anna hummingbirds ( Calyp te thus passively excluding other foragers anna) made predictable shifts in the fre- from their traplines. To my knowledge, quency of passive displays relative to F. B. Gill's ongoing research on Costa active chases as intruder pressure and Rican hermit hummingbirds is the only quality of territories changed (see also rigorous investigation of the economic Frost & Frost 1980). Lyon et al. costs and benefits of traplining behavior. ( 1977) showed that territorial hum- In contrast to the solitary foraging mingbirds discriminated among the species modes discussed above, some nectar-feeders of hummingbird intruder, expending the apparently forage in groups. Passerine most effort on those species most likely birds in Trinidad (Feinsinger et al. 1979a) to lower the nectar supply drastically. and bees in Costa Rica (Frankie 1976) Paton & Carpenter (1984) showed that appear at flowering trees in distinct rufous hummingbirds (Selasphorus rufus) "waves"; at least the passerines may form foraged heavily at the periphery of their reasonably cohesive single- or mixed-species territories early in the day, preserving the flocks. Some bats, too, appear at rich re- territories' core for later in the day. Gass source concentrations in "waves" (Heithaus et al. (1976; also Gass 1978, 1979, Gass & et al. 1974, 1975, Sazima & Sazima 1977, Lertzman 1980) have documented a Howell 1979, Howell & Roth 1981). remarkably close fit of size and number of Whether or not these reflect cohesive rufous hummingbird territories to the bat flocks using a common roost is not nectar resources available. In the montane conclusively determined. In a detailed NEW WORLD NECTARIVORY 301 energetic analysis, Howell ( 1979) showed (and energy) spent in sampling from that the energetic benefits of group various patches. Nectarivores live in a foraging outweighed those the bats would world of especially rapid changes in the obtain were they solitary foragers. The nectar value of patches ( cf. Pleasants & consensus is that group foraging may be Zimmerman 1979). Up-to-date knowledge advantageous for animals encountering of the local region's possible patches is discrete, massive crops of nectar-rich therefore essential, and many foragers flowers, such as large Puya and Agave may sample widely after their daily energy plants or large Erythrina trees, where the requirements are met. For example, many flower crop is far too large for territo- territorial hummingbirds spend increasing riality (cf. Carpenter & MacMillen 1976) amounts of time off the territory late but where some energy may be saved, in in the day, and non-territorial species as comparison to haphazard solitary foraging, well appear to spend some afternoon by avoiding areas where others in the hours assessing possible foraging sites flock are seen to forage. for the crucial early morning hours of the following day (Feinsinger 1976, Gass & Search patterns and the economics of Sutherland 1985; F. G. Stiles, personal foraging communication, 1986). In fact, data an observer obtains during a nectarivore's An animal undertaking a foraging bout sampling period, if taken out of context, makes a series of choices that affect its could easily be misinterpreted as "non- diet and its energy intake (Pyke et al. optimal foraging". 1977, Pyke 1984). In order, these choices In a sense, social nectarivores pool are: (1) upon choosing the habitat, which sampling effort and thus decrease the "patch types" to visit; (2) which foraging total sampling effort of the "individual", path to employ within the patch while or colony. For example, in a colony searching for potential food items; (3) of bumblebees (which do not recruit), which of the items encountered to utilize; as each forager goes through a trial and and (4) when to abandon the patch and error process the distribution of bees move on to another. adjusts slowly to the distribution of good At each step, the choice that yields the and poor patches on a particular day highest net energy gain depends on char- (Heinrich 1976b, 1979a, 1979b, Pyke acteristics of the forager and of the 1980). A colony of eusocial bees having resource. Often, theory and research are "scouts" that recruit foragers to rich couched in terms of "optimal foraging", patches, such as meliponine bees (Johnson but as Heinrich (1983a) points out opti- & Hubbell 1974, 1975, Hubbell & John- mality arguments may be misleading and son 1978, Wille 1983) or honeybees tautological; there are too many possible (Visscher & Seeley 1982), may be as close ways of defining "optima". A more ob- to an "omniscient forager" as possible: jective way to approach foraging decisions streams of nectar and pollen harvesters may be to ask, do the choices that foraging are dispatched to good patches almost animals make provide them with a higher as soon as these become available. net energy gain than if they were foraging ( 2) The foraging path. After choosing in a stereotyped or a haphazard pattern? a patch, the nectarivore is expected to In colloquial terms, do animals forage in choose the path that (a) minimizes the ways that get them "good deals" in terms distance, or energy expended, between of energetic costs and benefits (see also successive food sources and (b) mini- Waddington 1983)? mizes the chances for revisiting the same ( 1) Patch choice. In general terms, flower in a single foraging bout. Kamil foraging nectarivores are expected to (1978) showed that Hawaiian honey- choose the patch providing the highest creepers appeared to minimize revisitation, expectation of energy yield per unit spreading their foraging evenly over the time (Pyke et al. 1977, Pyke 1980, 1984, inflorescences in their territories. Attempts Carpenter et al. 1983). How does a forager to duplicate these results with territorial obtain information on expected yield? hummingbirds have failed (Miller et al. Some early models of foraging assumed 1985; P. Feinsinger, unpublished data, that foragers were omniscient, but more C. Murcia, unpublished data), but "trap- sophisticated models incorporate time lining" behavior, where it occurs, may 302 FEINSINGER meet both the distance- and the revisi- by the forager. Net energy return is a tation-minimizing criteria. function of actual nectar volumes and Most studies on choice of foraging of handling time, which for a given bee path have involved bumblebees. Pyke is a function of flower morphology and (1978a, b) investigated bees foraging previous experience. Likewise, Lewis (1986) at Delphinium nelsonii flowers, which demonstrated the importance of learning are arranged spirally on the spike. First, in flower choice by the butterfly Pieris he showed that the angle at which bees rapae. turned as they went from one inflorescence Another criterion affecting flower choice to the next was one that reduced the by bees is variance in nectar rewards. Ca- chances for revisitation (Pyke 1978b). raco (1980, see also Caraco et al. 1980) Second, he showed that the path a bee proposed that foraging animals operating took among the flowers on a given spike on neutral or positive energy budgets was one that increased nectar intake and would tend to be "risk averse", choosing reduced movement costs. Pyke interpreted patches or food types with low variance these foraging movements in terms of in the rate of return, whereas foragers "optimal choice" of foraging path. operating on a negative energy budget, Recent investigations (e.g., Heinrich given some possibility of encountering an 1979c) have produced less clearcut results unusually rich reward quickly, would and have thrown some doubt on Pyke's switch to "risk prone" foraging in patches "optimal choice" interpretation. For exam- or at resources yielding high variance in ple, some bumblebees may forage in the rate of intake. Waddington & Holden stereotyped patterns regardless of the (1979), Real (1981 ), Waddington et al. vertical distribution of nectar in a flower (1981 ), and Real et al. (1982) showed spike (Corbet et al. 1981). Still, in a experimentally that various hymenopteran careful study Waddington and Heinrich foragers (wasps, bumblebees, or honey- (1979) showed that Bombus edwardsii bees) tended towards "risk aversion", were capable of modifying their foraging usually choosing artificial flowers with path in response to the distribution of low variance in nectar volumes over differ- nectar on artificial inflorescences. When ently colored flowers having the same rewards were concentrated among the mean but high variance. These results lowest flowers, bees quickly learned may explain the scarcity of bonanza-blank to start from the bottom of each "in- patterns of nectar secretion in plants whose florescence" and to depart before reaching pollinators are not often food-limited as the empty topmost flowers. When instead a group. Conversely, when food is scarce the rewards were concentrated among the for pollinators, the theory of risk-sensitive topmost flowers, bees quickly learned to foraging predicts a switch to risk-prone begin each inflorescence in the middle behavior (Caraco 1980, Caraco et al. 1980), and to depart from the top. When rewards such as that provided by a bonanza-blank were evenly distributed among flowers, nectar secretion pattern. Certainly, more bees switched to foraging throughout research is crucial to understanding the each "inflorecence", beginning near the relationship between risk-sensitive foraging bottom and departing only when the top and food limitation. was reached. Thus, foraging paths appear ( 4) When to leave the patch. Foragers to involve both stereotyped and learned may make this decision based on their behaviors. perception of the rate of return from the (3) Food choice. The criteria influencing current patch versus the expected rates food choice and diet breadth are more of return in alternative patches, modified clearcut, and more widely investigated, by the costs of transit. Some foragers' per- for other animals than for nectarivores ceptions can apparently be quite accurate. (see reviews by Schoener 1971, Mac- For example, Hartling & Plowright ( 1979) Arthur 1972, Pulliam 1974, Charnov showed that bumblebees stayed foraging 1976, Pyke et al. 1977, Pyke 1984). longer at one artificial inflorescence as Heinrich (1976b, 1979b) and others (La- distance to the next inflorescence was verty 1980, Harder 1983, 1985) have increased. shown clearly, however, the determinant When costs and benefits of alternative of flower choice by individual bumblebee patches are not so well known, nectarivores foragers: net energy return as perceived may use standard "stopping rules", leaving NEW WORLD NECTARIVORY 303 after encountering a given number of Laverty 1980, Harder 1983, 1985, Plow- empty flowers in sequence. Stopping rules right & Laverty 1984), a naive bumblebee may be flexible, though. For example, forager learns to forage at a "major" plant Best & Bierzychudek (1982) found that species and one or more "minors" (see bumblebees switched from a "stopping review in Feinsinger 1983a). Perceived rule" of 4- 5 flowers in early morning rewards are affected by species-specific to 1 flower in late afternoon. A few of flower complexity, rate of nectar secretion, the many other studies dealing with the flower dispersion, and, most importantly, decision of when to leave a patch include the extent to which existing foragers Howell & Hartl(l980), Waddington (1981), already visit the flowers. Thus, all else Marden & Waddington (1981), Schluter being equal, a naive forager will tend to ( 1982), Hodges ( 1985), and Wolf & Hains- choose flowers of species underu tilized by worth (1986). other bees. The net result is that foragers Finally, at least one study has dealt from any one bumblebee population are not with flexible "stopping rules" for distributed broadly over most flower entire patches, but rather with flexible species available (Johnson 1986), even stopping rules for the effort spent at though each bee makes quite specialized individual flowers. Whitham (1977) showed choices and each plant population ex- that bees foraging on flowers of Chilopsis periences quite constant pollinators. linearis (Bignoniaceae), early in the day In contrast, some bees remain specialized when most flowers held large nectar on particular plant species regardless of volumes, achieved a higher net energy conditions, and the population maintains a intake by leaving the last drops of nectar very narrow niche. Strickler (1979) showed in the flowers than by spending the time that Hoplitis anthocopoides collected necessary to extract these dregs. Later in pollen from one plant species only, and the day, however, when nectar levels was more effective at doing so than less were low overall, bees stayed longer and stereotyped bee foragers. extracted the dregs. This result parallels Coexisting meliponine bee species in cases of "partial prey consumption" by Costa Rica have a variety of niches (John- predators, in which animals cease feeding son & Hubbell 1974, 1975, Hubbell & on one prey and begin searching for others Johnson 1978, Wille 1983). Foragers long before extracting all possible energy from non-recruiting species visit a wide and nutrients from the first (Sih 1980). variety of flower species and dispersions; thus, the population has a broad niche. At any one time, though, a population NICHE WIDTH AND SOCIAL STRUCTURE of a species that recruits foragers has a OF NECTARIVORE POPULATIONS narrow niche, as all foragers are concentrated at especially rewarding resources, The collective result of decisions made by where they overwhelm other bees. Visscher individual foragers is a characteristic pattern & Seeley (1982) showed that healthy of resource use by the species population wild colonies of honeybees (Apis mellifera) to which they belong, one aspect of the resembled recruiting meliponine species, population's "niche" (Whittakeretal. 1973, with numerous scouts sampling from Feinsinger et al. 1981 ). A population of various patches but recruiting in such a specialists all having similar specialties will way that foragers were pooled in patches have a narrow niche; a population of of the plant species that were most re- generalists will have a broad niche, but so warding at any one time; energy-stressed will a population of specialists each having colonies engaged in much less sampling and a somewhat different specialty. Obviously, remained with particular plant species a broad-niched population composed of for long times; but, because different generalist flower-visitors will have a quite colonies experienced different degrees of different impact on flower pollination than energy stress, the net result was that a population with an equally broad niche honeybees as a whole were dispersed but containing a diversity of specialists. over all appropriate flower species. Thus, Bumblebees studied by Heinrich (1976b, the niche of feral honeybees might be as 1979a, 1979b) exemplify populations with broad as the niche of a bumblebee po- specialized individuals but broad niches. pulation, but very different foraging On the basis of perceived rewards (see techniques are responsible. 304 FEIN SINGER

At any one time the niche of a terri- interactions are highly visible as well; torial hummingbird population is apt and because, for some groups at least, to be quite narrow, as only a few plant there is a clearcut and easily tested relation- species are likely to provide resources ship between morphology and resource use. worth defending (Feinsinger 1976, 1983a). "Tongue" length of bumblebees varies Over time, though, the niche becomes among and within species (Heinrich 1976a, quite broad as plant species going out of, Morse 1977, Harder 1983, 1985). Tongue or corning into, flower are respectively length strongly affects efficiencies of discarded from, or added to, the list of nectar extraction from flowers with differ- defensible resources. Subordinate, short- ent corolla lengths (Inouye 1980, Harder billed hummingbirds have access only to 1985), and thus constrains foraging choices. scattered flowers of many species; thus, Often, nectar from flowers with different populations of low-reward trapliners, for corolla lengths is fed on by different bee example, are broad-niched at any one species. Thus, some bumblebee assemblages time. Likewise, long-billed high-reward may be structured by competition (Inouye trapliners often forage at numerous species 1977). Many recent studies have been per- having long-tubed flowers. We have found formed in Scandinavia and Finland (e.g., by individuals carrying as many as 16 pollen I. Hanski, H. Lundberg, A. Pekkarinen, species simultaneously (Feinsinger et al. E. Ranta). One of the most convincing 1987). Relative to long-tubed flowers, studies, however, was performed in North then, populations of high-reward trapliners America by Inouye (1978). Inouye in- have broad niches; but considering all vestigated meadows where long-tongued hummingbird-pollinated flowers they could Bombus appositus coexisted with short- potentially visit, these species have quite tongued B. flavifrons. Normally, B. narrow niches, as they rarely visit the appositus workers majored on long-flo- less rewarding short-tubed flowers (Fein- wered Delphinium barbeyi, and ignored singer 1983a). short-flowered Aconitum columbianum; B. flavifrons majored on Aconitum and ignored Delphinium. When one bee species INTERSPECIFIC COMPETITION AND or the other was experimentally removed, GUILD ORGANIZATION IN NECTARIVORES however, nectar welled up in the unutilized flower species, and the remaining bee In recent years the field of community species began utilizing those flowers even ecology has been racked by dissension though they were less efficient at ex- over the importance of competition among tracting nectar than the "normal" visitor natural populations, and its role in struc- (Inouye 1978, 1980). Thus, exploitative turing communities (e.g., Lewin 1983a, competition certainly occurs among bum- 1983b, Schoener 1983, Strong et al. 1984, blebees (see also Heinrich 1976a). Even Diamond & Case 1986). Many critics of though such competition may play a competition theory point out that evidence minor role in the evolution of the tongue for resource limitation, the precondition length of a particular bee species, it may for ecologically (and evolutionarily) im- play a larger role in assembling, from a portant competition, is difficult to collect; pool of potential colonists, groups of that the extent of resource limitation coexisting bumblebee species (Bowers is likely to vary widely in space and time; 1985a, b). that the relationship between resource Meliponine bees in Central America limitation, even when it occurs, and "cha- compete intensely for access to rich nectar racter displacement" among coexisting sources. Using artificial nectar sources, species is very complex and tenuous. Hubbell & Johnson (1977, 1978) and Animal-flower interactions provide ex- Johnson (1981) showed that behaviorally cellent systems for examining the role subordinate species were often the first of competition, because production, availa- to discover new food and exploit it, but bility, and use of resources are easily when larger, recruiting species discovered monitored; because interactions are extre- rich resources they overwhelmed and mely dynamic, as plant populations go displaced the smaller, non-recruiting bees. into or out of flower over quite short Interactions among meliponine species time spans; because many nectarivores at natural nectar sources undoubtedly are highly visible, and their competitive are more complex, but apparently inter- NEW WORLD NECTARIVORY 305 specific competition among meliponines, or much more constant, however, in the between meliponines and other bees, cha- understory of these forests, as well as racterizes densely flowering trees (Roubik in natural gaps such as those caused by 1978, 1980, 1983, Frankie & Haber 1983, treefalls (Stiles 1975, 1985, Feinsinger Wille 1983) and may affect bee community et al. in press; but see Stiles 1977). As structure (cf. Hubbell & Johnson 1977). a result, most of the nectar available The year-around dynamics of meliponine- (at least to short-billed hummingbirds) flower associations have not yet been in flowers of the understory or gaps is investigated thoroughly. utilized on a daily basis throughout the Guild structure and seasonal dynamics year. Hummingbirds of tropical forest in nectar-feeding birds, however, have been understory appear to be quite sedentary, investigated at several Central American and there are few transient populations. sites and on Trinidad and Tobago. Fein- Such habitats tend to have one or a few singer & Colwell (1978) reviewed earlier species of short-billed hummingbirds ex- studies and distinguished five "roles" ploiting short-tubed hummingbird-pol- that nectar-feeding birds appeared to fill: linated flowers, and one or a few species territorialists, high-reward trapliners, low- of hermit hummingbirds or other long- reward trapliners, and two roles not billed species exploiting long flowers. mentioned previously: generalists (who Thus, structure and dynamics of hum- fit in between territorialists and low- mingbird assemblages vary with the nature reward trapliners) and "territory-parasites". of the habitat and resources involved. We pointed out that a hummingbird's The extraordinarily dynamic assemblages morphological and behavioral phenotype of tropical old-fields exemplify commu- guided it towards one or another role, nities where the intensity of competition, but that some birds might change behav- and community structure, vary seasonally ioral roles with changes in resources or (Feinsinger 1976, Feinsinger et al. 1985). in the local array of other nectar-feeding The distinction between those old-fields birds. (and some forest canopies), with their In general, studies performed in large hordes of migrant nectarivores, and the tropical "old fields", or patches of an- relatively stable resource regimes (and thropogenic successional vegetation, have nectarivore assemblages) of forest under- revealed extremely dynamic interactions stories points out that the "organizing among hummingbirds (Colwell 1973, Fein- principles" of superficially similar species singer 1976, 1980, Wolf et a/. 1976, assemblages may in fact differ greatly. Feinsinger & Swarm 1982, Feinsinger Monitoring the entire annual cycles of et a/. 1985). The density of flowers may other tropical nectarivore taxa or guilds vary by two orders of magnitude over will surely reveal even more about the the year. During seasons of nectar scarcity, variable role of competition in community a small number of bird species, filling structure. widely different roles, coexists. During flowering peaks, however, numerous addi- SPECIES INTERACTIONS AND COMMUNITY tional species enter from nearby and distant PATTERN AMONG PLANTS habitats (see also Feinsinger 1980). By monitoring throughout an annual cycle the Plants belonging to different species but nectar available within flowers, Feinsinger using the same animal pollinators may et al. (1985) documented the extreme influence one another's pollination through resource limitation that led to intense several different mechanisms: competition and forced "secondary" species (1) Neighbors may influence the fre- to emigrate during times of flower scarcity, quency with each other's flowers receive versus the superabundant nectar that visits from animals, (a) either by drawing allowed the coexistence of many species animals away from each other (resulting at other times. in competition) or (b) by collectively Canopies of some tropical forests may luring animals into a patch (resulting in likewise provide seasonal bursts of re- facilitation) (Schemske 1981, Thomson sources that support extremely dynamic 1982, 1983, Rathcke 1983, Real 1983a, hummingbird assemblages (Feinsinger & Waser 1983a, 1983b). Colwell 1978, W. H. Busby, unpublished (2) If animals visit plants of different data). Nectar availability appears to be species in succession, "interspecific pollen 306 FEINSINGER transfer" may occur (Rathcke 1983, Waser If, through competition for pollina- 1983a). (a) If pollen rubs off on flowers tion, flowering peaks become dispersed of other species, paternal reproductive throughout the growing season or (in success declines as the number of grains tropical climates) throughout the year, dispersed to conspecific flowers, and the then the animals that visit these flowers number of conspecific plants reached, are provided with a constant supply of declines (Waser 1978b, 1983a, Rathcke food. Thus, the animals can develop 1983, Campbell 1985a). (b) Interspecific sedentary life styles and can specialize pollen transfer may lower maternal re- on nectar or pollen. From the plants' productive success if: (i) heterospecific perspective, this means that animals that grains occupy scarce space on the stigma, can pollinate them are constantly available. or induce it to close, thereby limiting Thus, a causal chain could link the mech- access by conspecific grains (Waser 1978a, anisms of interaction among plants, b, Waser & Fugate 1986); (ii) heterospecific 1- 2biv above, to the existence of pheno- grains have allelopathic effects on con- logical pattern among coexisting plants, specific grains (Sukhada & Jayachandra the existence of stable nectarivore assem- 1980, Thomson et al. 1981 ); (iii) hetero- blages, even to an accelerating interspecific grains result in hybridization dependence and coevolution between and gamete wastage (Stiles 1975, Waser flowers and flower-visitors (Heinrich & 1983b); or (iv) the cumulative number of Raven 1972, Stiles 1977, 1981, Waser conspecific grains received by stigmas & Real 1979, Feinsinger 1983a). declines (Campbell 1985b, Campbell & Alternatively, the competitive mecha- Motten 1985, Feinsinger et al. 1986, nisms proposed above could lead to mor- Motten 1986). phological displacement in location of The collective results of mechanisms the reproductive parts, among plants 1 through 2biv may be quite complex, simultaneously using the same pollinators especially at extremes in flower density (Waser 1983a). Morphological displace- (Rathcke 1983, Thomson 1983). Unless ment would minimize the amount of sudden flowering bursts overwhelm the interspecific pollen transfer (mechanism pollinator pool, however, effects on visit 2), such that rare species might actually frequencies (mechanism 1) may be minor benefit from using the foragers that come compared to effects on pollen transfer to more common, popular neighbors (Waser 1983b ). Furthermore, at least some (mechanism 1b). Thus, a causal chain studies suggest that stigma packing (2bi) could lead from mechanism 1b above and allelopathy (2bii) by the hetero- towards a pattern of convergence in specific pollen grains that stigmas receive flowering seasons among some coexisting are inconsequential compared to the plants, rather than towards the diver- impact of conspecific grains lost (me- gence expected among morphologically chanisms 2a and 2biv) (Campbell 1985a, similar flowers (reviewed in Feinsinger 1985b, Campbell & Motten 1985, Kahn 1983a). & Waser 1985, Feinsinger et al. 1986). Unfortunately for the speculation out- The possible effects just listed suggest lined in the preceding two paragraphs, that plants of different species flowering patterns in the flowering of coexisting simultaneously are likely to suffer re- plant species have proven to be somewhat productive depression relative to plants illusory (Poole & Rathcke 1979, Gleeson flowering at different times from one 1981, Rathcke 1983, 1984, Fleming & another. Natural selection or selective Partridge 1984, Rathcke & Lacey 1985, immigration could, then, lead to divergent Wheelwright 1985). Observed distributions flowering times among the species in a of the flowering seasons of "competing" pollination guild. Thus, competition could plant species should always be tested be responsible for apparently regular against the distributions to be expected dispersion among the flowering seasons of were flowering seasons random with co-occurring plant species (e.g.. Heithaus respect to one another, i.e., those dis- 1974, Heinrich 1975a, Stiles 1975, 1977, tributions generated by a "null model" 1981, 1985, Feinsinger 1978, 1983a, Plea- (Harvey et al. 1983) of flowering pheno- sants 1980, 1983; see reviews by Rathcke logies. When performed properly, these & Lacey 1985, Wheelwright 1985, Arm- tests usually reveal that purportedly bruster 1986). "regularly dispersed" flowering seasons NEW WORLD NECTARIVORY 307 are displaced no farther from one another expected from the process of competition than would be expected by chance alone in a stable environment (Murray et al. (Fleming & Partridge 1984). 198 7). In a "null model" analysis of As in the remainder of community data collected between July 1981 and ecology, most discussions of species inter- June 1983, none of the 12 short-tubed actions and phenotypic patterns within species we examined, and only 2 of the 19 "pollination guilds" (coexisting plants long-tubed species of flowers we examined, using a common set of pollinators) rely had blooming seasons that overlapped with on data either on the ecological inter- the remainder of their guild significantly actions or on the patterns but not both. less than expected by chance alone. On the Recently, my colleagues (J. H. Beach, other hand, 3 of 19 long-flowered species W. H. Busby, S. Kinsman, Y. B. Linhart, actually experienced greater phenological K. G. Murray, W. Z. Pounds, J. A. Wolfe) overlap from other species than expected and I have spent several years studying by chance. Furthermore, in neither guild both species interactions and community did species flowering simultaneously ex- patterns in two guilds of plants in cloud hibit significantly greater morphological forest at Monteverde, Costa Rica. One displacement than expected by chance guild consists of plants pollinated by the (Murray et al. 1987). short-billed hummingbird Lampornis calo- A number of explanations exist for the laema; the other guild contains plants absence of community-level pattern we pollinated by long-billed hummingbirds, discovered. For example, (1) the variable primarily Phaethornis guy. We documented environment of the Monteverde cloud flowering phenologies, monitored flower- forest, like most other habitats, produces visitation patterns, examined floral mor- considerable year-to-year variation in phologies of the ca. 40 plant species flowering phenologies and interspecific concerned, and noted the patterns with overlaps, thus permitting the coexistence which pollen grains were deposited on of species (or phenotypes) having traits the beaks and feathers of hummingbirds. that would be maladaptive in a stable We evaluated interactions among plant environment (cf. Chesson 1986, Chesson species by detailing the effects of neigh- & Case 1986, Hubbell & Foster 1986). boring flowers on the pollen loads a plant's (2) The cloud-forest community, like stigmas receive. other communities, is in long-term climatic Results have revealed tremendous com- disequilibrium (cf. Davis 1986); plant plexity in plant-pollinator and plant- species may be migrating independently, plant relationships. Neighboring plants and at different speeds, over the landscape. of different species sometimes have ad- (3) Other selective forces that affect verse affects on one another's pollination flowering phenology and flower mor- (as measured by the number of conspecific, phology, such as those related to fruit compatible pollen grains that stigmas production, may override the forces receive), but only in the guild with short- generated by interspecific pollen loss tubed flowers, and even there only during (Rathcke & Lacey 1985); the conse- certain seasons (Feinsinger et al. 1986). quences of flowering at the "wrong" Long-tubed flowers of different species time may have little consistent effect on actually enhance one another's pollination eventual reproductive output. on occasion. The species composition of The complexity we discovered is un- neighboring plants does not have consistent doubtedly not unique to the Monteverde effects on the number of heterospecific cloud forest. This complexity suggests pollen grains a stigma receives; further- that it may be far too simplistic to expect more, S. Kinsman (unpublished manu- plants sharing pollinators always to compete script) has failed to find any significant intensely or to flower in patterns that detrimental effects of heterospecific grains minimize overlap, just as analogous ex- even when they do arrive on stigmas (see pectations for other "competing" species also Kohn & Waser 1985). Thus, com- have often been shown to be unrealistic petition sometimes occurs, but only (Wiens 1977, Simberloff & Boecklen through mechanism 2b.iv above and only 1981, Strong 1983, Strong et a!. 1984, in one of the two guilds examined. Diamond & Case 1986). Convergence Even short-tubed flower species at among plants to utilize the same effective Monteverde do not exhibit the pattern pollinators seems to be much more likely 308 FEINSINGER than divergence to avoid competition et al. 1980b). Most studies taking this (Brown & Kodric-Brown 1979). Further- approach utilize anthropogenic distur- more, the complexity of interactions in bances. Recently, we completed a study the Monteverde cloud forest suggests comparing natural disturbances (treefall that simultaneous investigation into pro- gaps and larger, landslide-like gaps) with cesses of species interactions and into the intact understory of the Monteverde phenotypic patterns of those species are (Costa Rica) cloud forest, but found only more valuable than investigation into subtle differences in species identities one or the other in isolation. We hope and species interactions among these that other investigators, whether primarily habitats (Feinsinger et al. 1987, in press, "pollination ecologists" or primarily com- Linhart et al. in press). munity ecologists, will undertake similar investigations. APPLIED POLLINATION ECOLOGY

COMPARISONS OF ANIMAL-FLOWER Pollination ecology and agriculture INTERACTIONS AMONG COMMUNITIES A vast literature exists on pollination of Two sites that differ in a major ecological crop plants (see reviews by Free 1970, feature may exhibit pronounced differ- McGregor 1976, Caron 1979, Crane & ences in animal-flower interactions as well Walker 1983, Erickson 1983, Estes et al. as in other community components. For 1983). Many techniques used to assess example, a change in elevation can alter the pollination event itself, and its con- the relative effectiveness of different sequences in terms of seed or fruit output pollinator taxa, leading to a shift in the of the plant, are very sophisticated (except frequency of plants relying on these taxa for the practice of determining effective and profoundly affecting the dynamics of pollinators simply by tallying insect flower- each plant or flower-visitor guild (Cruden visitors). Yet surprisingly few "post- 1972, Kalin-Arroyo et al. 1983, 1985, revolutionary" concepts of animal-flower in press). Community-level patterns in interactions have filtered back into the flowering phenology may also vary with applied literature. The fact that many elevation (Kalin-Arroyo et al. 1981 ). temperate-zone crop plants are wind Likewise, comparisons between wet and pollinated may partly explain this paradox, seasonally dry forest sites in Costa Rica but neither have most concepts dealt have revealed profound differences in with in this review been applied to the community phenology of plants (Frankie many animal-pollinated tropical crops. et al. 197 4, Opler et al. 1980a). Nectar- feeding birds on different continents Pollination ecology and conservation may be resource-limited to very different extents, affecting greatly the ecology and Although Kevan (1975) proposed that evolution of their relations with bird- pollination be examined in the context pollinated flowers (Carpenter 1978). of environmental conservation, I know of Islands typically have fewer species of only two papers that clearly relate con- flower-visiting animals (and plants) than servation and animal-flower interactions: equivalent sites on the mainland; this a popular article (Janzen 19 7 4) and a decline in species richness can affect the short speculative essay (McClanahan 1986; ecology of the nectarivore species that although see Howe 1984b concerning remain (as compared with their con- plant-frugivore interactions and conser- specifics on the species-rich mainland) vation). Fragmentation of natural habitats and the pollination of the plants they and the spread not only of sterile lands visit (Feinsinger et al. 1979a, 1982, 1985, (such as pastures) but also of species- Linhart & Feinsinger 1980, Feinsinger & rich successional vegetation must have Swarm 1982, Spears 1987. profound effects on nearly every aspect Finally, species identities of plants and of animal-flower interactions mentioned pollinators, and the nature of species inter- in this review. Habitat fragmentation actions, may change as a disturbed patch cannot help but affect population struc- of landscape goes through secondary ture and, eventually, microevolution of succession (Parrish & Bazzaz 1979, Opler the surviving plant populations. Direct or NEW WORLD NECTARNORY 309 indirect effects of habitat fragrnention ty's (1980) work on bumblebees, though, on the pollinator milieu may act as a we know next to nothing about the on- broad community-level "selective filter" togeny of foraging. How does a humming- on recruitment in plant populations: bird fledgling, leaving the nest for the recruitment in some plant populations, first time, learn to forage? learn which because of their breeding systems and flowers are rewarding, which unrewarding? pollinators, may be affected scarcely at all learn the spatial locations of flowers by habitat fragmentation, but recruitment before starving to death? set up a trap- in others may decline dramatically or line, a territory, or even a haphazard cease altogether as a result of inadequate foraging route in a community where all pollination. Habitat fragmentation un- resources are apt to be consumed by older doubtedly has profound effects on guilds individuals? of nectarivores that normally migrate ( 4) With the exception of studies men- among several different patches, distri- tioned above and a few others, very little buted broadly over the landscape. Such is known about the short-term (an annual long-term effects on the community cycle or less) and long-term (over several ecology of conserved habitat fragments, years) dynamics of nectarivore guilds. As is effects more subtle but perhaps more true for the remainder of community ecol- profound than the loss of conspicuous ogy long-term studies are tremendously carnivore species from these fragments, more valuable than short-term studies that need to be investigated carefully. might, unbeknownst to the investigator, be taking place under unrepresentative conditions or, just as serious, might miss the unusual events crucial to shaping the SUGGESTIONS FOR FUTURE RESEARCH animal and plant assemblages under study. (5) Likewise, instead of fragmentary Although a continuation of "pre-revo- studies concerning interspecific pattern lutionary" pollination ecology is certainly alone, or concerning competitive inter- valuable, other areas of research may be actions alone, integrated studies are needed more productive. For example: that deal simultaneously with pattern ( 1) A few particular pollination syn- and process in plant species interactions dromes are virtually uninvestigated from as mediated by pollinators. a "post-revolutionary", quantitative standpoint, and offer many intriguing possibi- ( 6) Comparisons of animal-flower systems lities for future research. Chief among between the subalpine/alpine meadows these, despite problems associated with of temperate North America and those its crepuscular or nocturnal nature and the of the southern Andes have begun and fabled unpredictability of its animal hopefully will expand. The large body participants (see Martinez del Rio & of research performed at Rocky Mountain Burquez 1986), is the interaction between Biological Laboratories provides an ex- hawkmoths and moth-pollinated flowers. cellent comparison for Andean inves- (2) Research on the relationship between tigations. the foraging energetics of flower-visitors (7) Perhaps most crucial, considering and nectar availability in flowers has only the recent awakening of the world's been rigorously examined by a relatively conscience in regard to tropical defo- few researchers and in a very few groups. restation, is the infusion of new ideas (and Techniques are available for quantifying new researchers) into applied pollination precisely the energetic expenditures of ecology. The scarcity of up-to-date, quan- small animals, and for quantifying precisely titative, carefully designed and inter- the nectar output of plants. preted research on the role of pollination (3) Other than gaps in knowledge ecology in agriculture, or in the con- pointed out earlier, the determinants of servation of fragmented habitats, is foraging choices in nectarivores have been inexcusable. Good studies can yield in- investigated quite exhaustively. Further formation useful in an applied sense details on, for example, the movement while testing general hypotheses in ri- of bees within or between inflorescences gorous enough fashion to provide the may not add much to extant knowledge. requisite publications in non-applied scien- Aside from Heinrich's ( 1979b) and Laver- tific journals. 310 FEIN SINGER

ACKNOWLEDGMENTS 171. University of Chicago Press, Chicago, Illinois. Ideas in this paper reflect the collective influence of BAKER HG & I BAKER (1983c) Floral nectar sugar many friends, exerted over many years. I am especially constituents in relation to pollinator type. grateful to the following persons: J.J. Armesto, H.G. In: Jones CE & RJ Little (eds) Handbook Baker, I. Baker, J.H. Beach, W.H. Busby, R.K. Colwell, of experimental pollination biology: 117-141. M.L. Crump, W.A. Haber, M.T. Kalin-Arroyo, S. Kins- Van Nostrand Reinhold, New York, New York. man, Y.B. Linhart, C. Martinez del Rio, C. Murcia, BAKER HG & PD HURD (1968) Intrafloral ecology. K.G. Murray, P.A. Opler, M.V. Price, B.J. Rathcke, Annual Review of Entomology 13: 385-415. A.G. Stephenson, F.G. Stiles, D.R. Strong Jr., J.D. BAKER HG, RW CRUDEN & I BAKER (1971) Minor Thomson, K.D. Waddington, N.M. Waser, and J.A. Wolfe. parasitism in pollination biology and its The National Science Foundation of the U.S.A., most community function: the case of Ceiba acu- recently through grants DEB 80-11008 and BSR 86-05043, minata. BioScience 21: 1127-1129. and the University of Florida have generously supported BARTHOLOMEW GA & TM CASEY (1978) Oxygen my research. consumption of moths during rest, preflight warmup and flight in relation to body size and wing morphology. Journal of Experimental UTERATURE CITED Biology. 76: 11-25. BATEMAN AJ (1948) Intra-sexual selection in Dro- ACKERMAN JD (1983) Diversity and seasonality of sophila. Heredity 2: 349-368. male euglossine bees (Hymenoptera: Apidae) BAWA KS & JH BEACH (1981) Evolution of sexual in central Panama. Ecology 64: 274-283. systems in flowering plants. Annals of the ACKERMAN JD, MR MESLER, KL LU & AM MON- Missouri Botanical Garden 68: 254-274. 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