So many of our readers have hummingbirds visiting their garden--even feeders to attract them--that California's hummingbirds hardly need a lengthy introduction. These are among the smallest of living birds, and were inhabitants here long before the original prehistoric humans immigrated here from Asia via the Bering Land Bridge. Indeed, hummingbirds have been an integral part of California plant communities for millions of years. Today there are approximately eighty species of native California plants that are pollinated primarily by the state's seven breeding hummingbird species.
The hummingbird family (Trochilidae, including 328 species) occurs exclusively in the New World, ranging from southern Canada and Alaska to Tierra del Fuego. A few regions, as in parts of the Great Plains, have no hummingbirds, and plant species relying on hummingbird pollination can occur only in habitats where there are breeding or dependable migrating hummingbird species. But at the other extreme, in the equatorial latitudes a locality may have 30 coexisting hummingbird species, and greater than half of all species occur in the northern Andes. Sixteen species have been observed breeding in the United States [see box], but only one, the ruby-throated hummingbird (Archilochus colubris), occurs in the eastern states.
Morphological, and now DNA sequence, evidence has revealed that hovering hummingbirds are most closely related to the insectivorous swifts, from which family Trochilidae was certainly a separate lineage at least 33 million years ago. Hummingbirds also eat arthropods--lots of them--to obtain proteins and lipids for their diets and to feed their young, but hummingbirds gloriously feature the utilization of sugars in floral nectar as their principal energy source.
In fact, hummingbirds are mainly regarded as nectarivorous birds. And throughout the Americas probably nearly 8,000 species, belonging to more than 60 plant families, evolved flowers whose principal pollinators are hummingbirds. Bromeliaceae, Gesneriaceae, Heliconiaceae, Loranthaceae, Rubiaceae, and Scrophulariaceae are families that are rich in flowers for which hummingbirds are the principal pollinators. Hummingbird-pollinated flowers evolved many times within the genera of the American cacti, and even for a single genus, such as Erythrina, the leguminous coral trees that are orthophilous and pollinated by either hummingbirds or perching birds, hummingbird pollination evolved several different times.
The typical hummingbird-pollinated flower is brilliantly colored red to orange-red and conspicuous during daylight, and has a relatively long floral tube or deep structure containing dilute nectar but no fragrance. It does not require a rocket scientist to realize that hummingbird features, such as daytime feeding, long slender bills, high requirement of sugar for energy, lack of smell, and hovering abilities, nicely match the features of the flower type. Long recognized by naturalists, this "syndrome" of floral characteristics was carefully described in the 1960s, especially with the publication of Hummingbirds and Their Flowers (1968) by Karen and Verne Grant. Thus was launched an avalanche of careful field and laboratory research on hummingbird biology and related topics on floral evolution.
This complex system--how flowers are designed to attract hummingbirds as pollinators in lieu of insects and how hummingbirds have evolved to utilize this high-caloric food--is now a classical example of coadaptation and coevolution commonly presented to beginning college biology students. The term mutualism is used for such a positive interspecific relationship, showing that both participants benefit: the plant flower receives pollination and the hummingbird extracts food. Moreover, the origin of nectarivorous birds is not a unique evolutionary event, because there are ecological analogs of hummingbird and hummingbird-flowers on other continents: the nectarivorous sunbirds of southern Africa and Asia, the honeyeaters of Australia, and the honeycreepers of the Hawaiian Islands. UCLA biology students therefore also learn that the nectarivorous lifestyle, with its peculiar structural and physiological adaptations, is a clear case of convergent evolution, in which totally unrelated lineages of organisms have evolved forms that now appear biologically and structurally very similar.
There are five general adaptations of flowers for regulating the potential animal pollinating agents. (1) Make the visit convenient for a particular pollinator or class of pollinators by adjusting the time that flowers open, their locations, and the sizes and shapes of flowers. (2) Make the visit inconvenient for the majority of other pollinating agents, so that the flowers of one species are visited somewhat consistently by a particular pollinator. With flower constancy there is a higher probability that a species will receive pollen of the same species from a pollinator's visit. (3) Provide some nutritional need for the primary visitor (i.e., some reward that encourages animal visitation). Rarely is deception used by plants to attract pollinators, because eventually visitors evolve ways to recognize deception. (4) Provide visual or fragrance cues to help pollinators to find the flowers and their rewards. (5) Position reproductive surfaces so that incoming pollen will contact the stigma and fresh pollen will be taken to the next flower. Knowing these generalizations helps us to analyze how the plant and animals match so well.
Flowers for hummingbirds are designed to attract this particular group of birds, rather than insects. Whereas the compound eyes of insects are stimulated by ultraviolet radiation, nectarivorous birds in general, and hummingbirds in particular, seek out red wavelengths of visible light, and are quickly attracted to this color as they fly over a patch of vegetation having red flowers. By and large, hummingbird flowers are brilliantly colored, especially crimson, scarlet, fuchsia, and orange-red, but the birds will also utilize flowers of many other colors, once they find them, if the flower shape and nectar rewards are right. Many types of insects would tend not to visit hummingbird flowers, even though nectar and pollen are present, because the color cues are not perceived by them and the flowers produce no fragrance.
Red coloration in plants is due to the presence of three types of pigments: carotenes, anthocyanins, and betalains. Carotenes are crystalline molecules that form within plastids and are not soluble in water; these produce many of the bright scarlet to orange flowers. Anthocyanins are water-soluble pigments stored in plant cells (within their vacuoles); these are often responsible for the fuchsia, pink, and violet hues of flowers. Betalains are a special type of vacuolar water-soluble pigments found only in one group of closely families, including cacti, bougainvillea, and portulacas; these pigments may produce vibrant magentas in these particular families. Yellow is produced by carotene-like pigments called xanthophylls, which are water-insoluble; or by water soluble pigments from certain betalains or anthocyanin-like pigments (flavonoids). The occurrence of different shades of red to yellow flowers for hummingbird pollination reflects the pigments that are available in the evolutionary repertoire of each genus and family. Clearly, red pigmentation has evolved many, many times as nectarivorous flowers evolved.
The colors that attract hummingbird pollinators are, for the most part, presented in the floral tubes that contain the nectar and which are probed by the birds. The pigmented parts often are petals (the corolla), but may be sepals (the calyx) or both (the perianth or tepals). Occasionally the colorful attractant structure is actually a brightly pigmented bract (leaf) that is associated with the flower or a group of flowers, as in the case of Indian paintbrush (Castilleja) or bromeliads.
The majority of hummingbird flowers are approximately horizontal (that is, arranged radially along the axis), permitting the hummingbird to enter from the side, but in numerous interesting cases flowers are pendant and must, therefore, be approached from below (think of a fuchsia!). A pendant flower is inconvenient for certain types of pollinators--especially any needing a landing platform--but is easily accessible to a hovering hummingbird. Also, some authors have concluded that gravity permits a faster uptake of nectar from a pendant flower than would occur in an upright flower.
In hummingbird flowers, the pollen-containing anthers and sticky stigma lobes are generally placed on the upper (dorsal) side of the floral tube, hence the pollen grains are deposited and carried on the bill's crown or on top of the bill. A smaller percentage of species have the placement of anthers and stigma on the lower (ventral) side (where pollen would be deposited on the chin) or in the center of the flower. Where the same hummingbirds are visiting flowers with different placements of anthers and stigmas, this could be a way to facilitate more effective pollination of each design.
Bill designs influence the types of flowers that are utilized by each species of hummingbird. Dilute nectar is secreted deep within the flower, so a pollinator must have a long and thin probing device to obtain this sweet reward. Not surprisingly, long bills fit comfortably into long floral tubes, and short bills cannot reach nectar at the bottoms of long tubes. Consequently, hummingbirds can be categorized as either long-billed (having an effective length of 33 millimeters or longer) or short-billed (less than 33 millimeter), and these generally correspond to use of long-tubed and short-tubed flowers, respectively. Indeed, long-billed and short-billed species can coexist in a given habitat with minimal competition for floral rewards. For example, on a typical island in the Lesser Antilles, the green-throated carib (Sericotes holosericeus), a long-billed species, extracts nectar from the long-tubed flowers while the Antillean crested hummingbird (Orthorhynchus cristatus), a short-billed species, uses the short-tubed flowers. Researchers have also found guilds of long-tubed and short-tubed flowers at many other locations. Short-billed species can visit and extract nectar from long-tubed flowers, but they leave nectar that they cannot reach. Conversely, the long bill is effective in reaching the base of short-tubed species, but these in general have substantially less sugar reward.
Bills can also be categorized as either straight or curved downward (decurved), and this generally corresponds to effective extraction of nectar from relatively straight versus strongly curved floral tubes. Bills of many hermits (subfamily Phaethornineae) are decurved, which appropriately matches the curvature of certain long-tubed flowers in their habitat. Champions among these are the two species of sicklebills (Eutoxeres), whose bills are the only ones that properly slip into flowers of the Andean lobelioids (Centropogon) that are bent at a ninety-degree angle. The sticklebills also are very effective feeders of the curved-flowers of Heliconia. Subfamily Trochilinae includes the nonhermits, which typically have straight bills. Gary Styles, who received his Ph.D. at UCLA studying hummingbirds, used this pattern to invent the terms hermit and nonhermit flowers. All of California's hummingbird species have straight bills.
The slender bill of the hummingbird opens slightly when the tongue is protruded and then opens wider to hawk insects in the air or glean arthropods from plant surfaces. The bill tip is often sharply pointed, and the terminal edges are serrated, apparently to grasp hard-bodied arthropods and to cut open flowers for robbing nectar. Difficult to see without special photography, the hummingbird's tongue is protruded and retracted rapidly, sometimes more than ten times per second, to lick the nectar. Its tongue, which is forked at the tip, has a central trough. Dilute nectar sticks to the tongue tip and trough via capillarity. Special musculature is required to perform this rapid licking. In some hummingbirds, a tongue can be protruded as much as thirty millimeters to reach a nectar reservoir beyond the bill. The longer the distance the tongue is protruded, the slower the rate of licking, because it simply takes more time to protrude and retract the longer tongue. Experiments have shown that licking rate also slows when thicker (more viscous) nectar is presented to a hummingbird.
Hummingbirds exhibit fine daylight acrobatics, darting rapidly between flowers, attacking intruders, and courting mates by diving up to 17 meters per second. They also hover (stationary flying), some nonstop for as long as 50 minutes. On the tiniest hummingbirds, such as the bee hummingbird (Mellisuga helenae) of Cuba, which weighs only 1.9 grams and is 5.5 centimeters from tail tip to bill tip, their pointed wings may beat up to 80 times per second. Hummingbirds are capable of backward flight, which is possible because the muscles that lift the wing in the return stroke are as well-developed as those producing the downstroke. Wings are larger in proportion to body weight than for nonhovering birds of similar weights, and hummingbirds' feet are proportionately smaller. This is the way to build a hovercraft!
Rapid speeds are required to visit more flowers per unit time. Some hummingbird species are capable of visiting and sampling 20 flowers per minute, and they use the most rewarding patches of flowers. Hovering permits a hummingbird to spend a minimal quantity of time at each flower, probing each one and then moving on, rather than constantly having to land and take off. But hovering is, by all measures, the most energetically expensive form of flight, requiring ten to fourteen times more calories than would be required for the same organism to sit in one place. Optimal foraging models--which incorporate such parameters as the length of time spent at each flower, caloric reward per flower, and flying between flowers--have been used to explain the frantic activity pattern of a hummingbird.
Hummingbirds have extremely high metabolic costs. First, these tiny vertebrates have a basal metabolic rate (resting) that is among the highest of all endotherms, and they must work very hard to maintain a relatively constant body temperature, while body heat is constantly being lost to the cooler surrounding air. The small body size and high ratio of surface-to-volume make the loss of heat critical. Because the hummingbird has extremely little body fat, the metabolic machinery of this creature must be fueled by the nectar, which is rapidly used in its shortened alimentary system that is designed for efficient uptake of sugar through the gut. Add to this the cost of rapid flight and hovering. A small bird weighing only three grams can require 645 calories per hour! At nighttime, when nectar supply is often used up, a hummingbird can rapidly enter torpor, a temporary condition whereby its metabolism is slowed and body temperature drops sharply to save energy.
Typical nectar of a hummingbird-pollinated flower is dilute. Measured sugar concentrations mostly have been 20 to 30 percent. This is much less concentrated than that found in closely related insect-pollinated species. In addition, the nectar for hummingbirds is very rich in sucrose (a disaccharide sugar), whereas related, insect-pollinated flowers and flowers pollinated by perching birds produce nectar in which hexoses (smaller monosaccharides) dominate. Flowers for hummingbirds characteristically have maximum nectar at dawn, and by midday most of the resource has been depleted via extraction or evaporation. The long-tubed hummingbird flowers tend to have high daily nectar secretion, and also yield twice the amount of sucrose per day, hence they are a greater source of energy than short-tubed flowers, according to at least one study. Some authors have suggested that water and minerals obtained from nectar, such as phosphorus, chloride, and sodium, are critical components in the hummingbird diet.
Hummingbirds may establish territories while in a plant population, but they must include in that defended territory enough resources to meet daily caloric requirements. This is often not possible when flower densities are too low. The alternative is traplining. Traplining is a feeding strategy used by hummingbirds when their flowers are widely dispersed; the bird visits widely dispersed flowers along the same (regular) route each day, to obtain sufficient nectar. In temperate habitats during breeding time and even during migrations, hummingbirds characteristically establish and aggressively defend territories. In neotropical habitats, a dense patch of heliconias may be adequate to define a territory, but it is common to find traplining, especially among hermits, which must forage from tree to tree, epiphyte to epiphyte. How far does the pollen really travel within territories or along traplines? In the few good experiments that have been accomplished in nature, pollen movement is typically only several meters. Information is largely absent on distances of pollen flow via traplining in tropical forests.
Great patience and lots of field time are required to diagnosis a natural community of hummingbirds and their flowers. Even where there is only a single species of hummingbird, as in southern Alaska, the Carolinas, or southern Chile, there are many questions to answer about the ways which many plant species with tubular red flowers can coexist with only one bird pollinator species. Part of the answer often lies in having peak flowering times that are somewhat different, so that during a particular week one species of plant may be preferred, and thereby set more seed, than another. But this is often just hopeful thinking, because just as often species overlap in flowering times. Another complication for understanding is the arrival and departure of migratory hummingbirds into territories of resident species. In western North America, it appears that there is a wave of flowering for hummingbird species from the Mexico border northward into Canada and Alaska, providing nutrition for hummingbirds migrating northward to breed. Within a mountain range, flowering of hummingbird flowers often progresses as a wave from low elevation to high elevation, creating a shifting resource up a mountain and within a single meadow.
Hummingbird plants are especially concentrated along the north-south mountain ranges on the western side of the continent, and these are the corridors used by hummingbirds as they migrate north and south each year. At the extremes, few hummingbird-pollinated species occur (only five in southern Alaska), but along the Sierra Madre Occidentale in Mexico and proceeding through mountainous Central America and along the northern Andes, the number of hummingbird-pollinated species increases dramatically. Surely it is no coincidence that Central America and the Andes through Peru are where both the most hummingbird species and most of their plants are found.
In the Santa Monica Mountains, hummingbirds are very important pollinators of certain native perennials. Nonetheless, they are, by necessity, opportunistic and learn to use any convenient nectar source, including native species that are pollinated primary by insects, introduced plants around homes, flowering tobacco, and others. Our flora is instructive in that we see hummingbird-adapted flowers are also visited by insects, and insect-pollinated flowers are visited by hummingbirds, hence they share in the successful seeding of these species. Throughout the world, very few flowers are pollinated exclusively by one animal species. One-to-one relationships are exceedingly rare. Long-tongued bees and butterflies often share flowers with hummingbirds.
The interrelationships of flowers and hummingbirds are mostly unstudied for complex habitats where many species coexist. And in many ways, the eclectic and artificial assemblage at MEMBG is complex, like a forest habitat. In MEMBG, we have an impressive list of species that bear hummingbird-type flowers, both long-tubed and short-tubed. We have flowers from South Africa and Australia that are adapted for pollination by native bird families there; yet, in this foreign land, hummingbirds use these too, especially aloes. Some flower every day of the year, and our hummingbirds very contented creatures.
Because our newsletter is not published in color, the beauty of the hummingbird-pollinated flowers is somewhat lost in these pages. You will have to visit our garden to observe these plants in living color, or study online at the botanical garden website (http://www.lifesci.ucla.edu/botgard/). When you learn about this subject, you will know why our hummingbirds hum--and it isn't because they don't know the words. The word for them here is MEMBG.
ARTHUR C. GIBSON, MEMBG Director