It's human nature to dislike moths. Even though moths comprise nearly 10 percent of the 1.5 million catalogued living species, most people just cannot get very excited about these creatures, drab cousins of the dazzling butterflies. But plants are not so judgmental as we are, and numerous species of flowering plants are described as sphingophilous, i.e., loving hawkmoths. The nearly 1,300 currently recognized species of hawkmoths and sphinx moths (family Sphingidae) constitute an important class of nocturnal pollinating agents around the world.
The typical sphingid moth is a marvelous natural invention. This beautifully decorated creature starts life as a solitary egg oviposited on the lower side of a plant leaf by a female hawkmoth. The round-headed caterpillar (larva) that emerges has a sharply pointed, down-curved horn on the eight abdominal segment (its rear end), hence the term "hornworm." These leaf-eating caterpillars are often hard to find because they are so well camouflaged on plants, but after pupation the striking adults emerge. About the size of the smallest hummingbird (just three grams), the adult hawkmoth is a heavy insect with an aerodynamically formed body. Perched on its six legs at rest, the typical adult hawkmoth appears V-shaped--like a high subsonic stealth fighter in the hangar--with its two narrow forewings drawn back past the fuselage-like, streamlined abdomen. It is a strong, vigorous flyer that moves rapidly across long distances, darting skillfully and with clear purpose from target to target. During flight the long, narrow forewings are extended from the thorax to generate great speed. Hovering at the face of a flower, it uncoils a long tubular proboscis to insert into the flower center and suck the copious nectar. With a few daytime exceptions, hawkmoths typically perform these foraging acrobatics at night, in contrast to the daylight-active darting and hovering hummingbirds (Newsletter Summer 2000).
Plants that utilize hawkmoth pollination are already familiar to you. Anytime you smell the heavy, sweet, nocturnal fragrance of the white, tubular flowers of jasmine (Jasminum, Oleaceae), honeysuckle (Lonicera, Caprifoliaceae), Gardenia (Rubiaceae), Pittosporum (Pittosporaceae), or Stephanotis (Asclepiadceae), excellent candidates for hawkmoth visitation are in the neighborhood. Add to that some of the white-flowered woody Apocynaceae, such as Plumeria, oleander (Nerium oleander), star-jasmine (Trachelospermum jasminoides), or Natal plum (Carissa macrocarpa), and the standard syndrome of floral features begins to take shape. Other sterling, and stunning, examples are such garden herbs as flowering tobacco (Nicotiana sylvestris, Solanaceae) and four o'clocks (Mirabilis jalapa, Nyctaginaceae).
Classical descriptions of sphingophily include flowers are white to cream-colored with long, often narrow floral tubes or spurs; a flower opening that lacks a sturdy landing platform for a heavy pollinator; anthesis (flower opening) close to sunset or during the night, when the flower emits a pleasant, strong, sweet odor; anther dehiscence delayed until sunset or after dark, and stamen filaments generally white; and nectar copious (often greater than four grams per flower), thin, having a relatively low sugar concentration (about 20 percent), and either sucrose-dominant or sucrose-rich.
The readily observed set of floral features is easily matched with the requirements and features of the hawkmoths. Hovering hawkmoths need no landing platform but require a high-energy supply to maintain active flight. Sweet scents dispersed as odor plumes attract the fast-flying insect to the plant, often in total darkness. The copious nectar must be easily extractable as a thin liquid, and the form of the floral tube should accommodate the placement of the slender proboscis at the nectar source. A special device in the head, called the cibarial pump, has a flexible roof that is alternately raised and lowered to draw nectar up and then eject the nectar into the esophagus. When the hawkmoth withdraws its proboscis from the flower, pollen readily sticks to its surface, and pollen grains are easily entrapped on the scales of the moth's body.
When a hawkmoth, during its long, continuous flights, is attracted to a flower, the nectar-drinking creature certainly must be tracking fragrance plumes. How the insect is able to assess distance and determine the best path along a scent trail to an emitting flower, using just olfactory cues, is not entirely clear, but concentrations of wind-borne odors are detected on the antennae of hawkmoths, as on other insects. Perhaps surprisingly, much of the careful research done on insect odor recognition has been performed on the tobacco hookworm or tomato cutworm, Manduca sexta, a hawkmoth species that is an agricultural pest. Minute sensory structures (55,000 of them!), termed sensilla, are present at high densities on the antennae; these are places where the cuticle of the animal is very thin or absent, hence the surface is very porous. When plant volatiles (e.g., alcohols and esters) in the air strike the antenna, they are adsorbed there and enter the lymph within the sensillum, where volatiles bind with special water-soluble proteins (called OBPs, odorant binding proteins). The volatiles appear to be transported via the OBPs to the nerve endings (dendrites), where the message is sent to the brain for processing.
Once at the face of the flower, hawkmoths apparently use visual cues to verify the correct flower. Then the strawlike proboscis uncoils and is inserted into the well from which nectar is drawn. Although it may seem that the white of the flower is a cue, especially on moonlit nights, researchers have a slightly different set of data to consider. The compound eyes of hawkmoths appear to have photoreceptivity to only three wavelengths, green (0.530 micrometers), violet (0.450 micrometers), and much shorter ultraviolet (0.350 micrometers). The white petals of hawkmoth flowers do not appear to reflect any ultraviolet light, so the hawkmoth commences to feed. Other pigmented flowers, such as the closely similar hummingbird flowers, reflect longer wavelengths and hence are generally rejected by hawkmoths. Flowers having no UV reflectance are generally not receptive to the birds, which also do not detect strong fragrances. Hawkmoths tend to use hummingbird flowers more commonly than birds use hawkmoth flowers.
Rapid wing movement to achieve liftoff, to create great speed, and to maintain hovering is energetically very expensive, to be sure, but rigorous exercise makes these creatures into heat-generating dynamos. On a cool night, thoracic body temperature of a hawkmoth in flight can rise to 46 degrees C--so hot that Bernd Heinrich, who earned his Ph.D. in zoology at UCLA (1970, dissertation titled "Flight energetics and temperature regulation by blood circulation in the sphinx moth, Manduca sexta"), called his 1993 book The Hot-Blooded Insects and started with a chapter on hawkmoths. Heinrich and coworkers discovered that the aorta of the hawkmoth loops by the flight muscles, accepting excess heat and transporting it to the abdomen, which has become a major heat sink. The manner in which increased blood circulated is shunted to the abdomen is quite a story in itself, but not for today, except to add that this is an ingenious pathway to prevent overheating by transferring the generated heat to safer quarters. Professor Heinrich and others also discovered that hawkmoths shiver in a very subtle way to generate heat and thereby raise body temperature sufficiently high (near human body temperature) to start their wings and take off. Once the moth is in flight, cooling, not heating, is the crucial process, when wing movement is so rapid that it generates a sound of more than 55 Hz!
Little in evolutionary biology is as simple as it originally seems. Although the standard syndrome of hawkmoth flowers is easy to diagnose, actually only about half of the genera pollinated by Sphingidae, and only a third of the known species, have narrow tubes. Two other designs exist: trumpet and brush. The trumpet form has white flowers with the same sweet fragrance and deeply placed nectar, but the throat is much wider and spreading. Examples would be daturas (Datura), the various species of Devil's trumpets and angel's trumpets (Brugmansia and Solandra, Solanaceae), Herald's trumper or Nepal's trumpet flower (Beaumontia grandiflora, Apocynaceae), and many night-opening amaryllids (Amaryllidaceae). Many cacti clearly fall into the trumpet design (e.g., Echinopsis multiplex, Acanthocereus tetragonus, and Hylocereus costaricensis) whereas others are more tubular (species of Selenicereus and Stenocereus eruca). Hawkmoths entering trumpet flowers are often thickly covered with pollen.
The brush design is mostly represented by a cluster of flowers (an inflorescence), like mimosoid legumes (species of Calliandra, Inga, and Pithecellobium, among others), in which the floral tube is absent and the hemispherical display of stamens produced by many flowers forms "the brush" touching the pollinator. Members of the caper family (Capparaceae), such as the spider flower (Cleome spinosa), are also described as the brush type. The short proboscis of many hawkmoths (typically 20 to 60 millimeters) can be effective only for feeding from flowers with very short floral tubes or brush types, whereas a long proboscis--often exceeding 80 millimeters--can be used to reach all types of hawkmoth flowers. Only the extremely long floral tube may be limited, requiring the species with the longest proboscis.
Among his many predictions, Charles Darwin once described the waxy, ivory-white flower on an orchid of Madagascar, Angraecum sesqupedale, having a nectar-containing spur 21 to 35 centimeters in length, and speculated that for pollination this flower would require a nocturnal sphingid with an equally long proboscis. In 1903, many years after his death, an explorer there discovered the moth Xanthopan morganii ssp. praedicta, with a lengthy proboscis to perform the task! In flight cages this hawkmoth species has been able to effect pollination and cause seed set, but, contrary to popular myth, the insect has never been seen actually visiting that orchid species in the wild.
Certain plant families have evolved many different species and lineages specializing in hawkmoth pollination. The extremely large, mostly tropical family Rubiaceae contains hundreds of sweetly fragrant, long-tubular white flowers, including species of Alibertia, Bouvardia, Cosmibuena, Gardenia, Gonzalagunia, Lindenia, Psychotria, Randia, and Rondeletia, among many others. As noted earlier, there are many genera with hawkmoth flowers in the dogbane family, Apocynaceae. In nearly every country of the New World, hawkmoth-pollinated members of the cactus family can be found, including trees, shrubs, geophytes, low forms, vines, hemiepiphytes, and epiphytes. Many of the tubular flowers of the nightshade family (Solanaceae) broadcast their fragrances during summer nights, as do many monocotyledonous species of the agave family (Agavaceae) and amaryllids (Amaryllidaceae). Fully documented hawkmoth-pollinated species occur in at least 40 angiospermous families, scattered on many different branches of the phylogenetic tree, thus demonstrating another excellent example of convergent evolution.
Communities of sphingophilous species are particularly common in wet, tropical habitats, where workers have been able to find guilds of more than 100 species of Sphingidae visiting more than 30 coexisting species of sphingophilous flowers. Although most of these moth species and their plants appear in tropical latitudes, a sandy desert community with many fewer species can also be serviced by hawkmoths of a few species. For example, in certain sandy localities of the Sonoran Desert, one may find hawkmoths working dense populations of evening primroses (Oenothera, Onagraceae) with desert lily (Hesperocallis undulata), cacti such as agria (Stenocereus gummosus), senita (Lophocereus schottii), and Peniocereus greggii, and species of several other plant families. It is unlikely that only one species is pollinating only one flower species, so there will be mixed pollen grains of many species on the insect. That notwithstanding, hawkmoths are credited as fairly reliable long-distance cross-pollinators because they are able to carry even small amounts of pollen to isolated, self-incompatible plants in tropical forests to produce fruits with viable seeds.
Sphingophilous flowers are largely unused by other classes of pollinators. These nocturnal flowers are unavailable to day-active pollinators until the next morning, and, in fact, bees of various types sometimes arrive during morning hours to accomplish an even higher level of pollination success. Most hawkmoth flowers are too flimsy and have too narrow a tube to permit bat visitation, and bats almost always prefer nectar that is rich in hexose (e.g., a monosaccharide like glucose), not the disaccharide sucrose. Probably because they lack pigmentation, butterflies generally do not recognize and visit hawkmoth flowers. Hummingbirds may feed on hawkmoth flowers during daylight hours, but their visits occur usually after hawkmoths have had a nighttime opportunity for pollination. Other families of moths, such as Noctuidae and Geometridae, include many plant pollinators, but these moths utilize different groups of flowers from those specialized for the Sphingidae. Hawkmoths, unlike hummingbirds, are nonterritorial and therefore are potentially able to transport pollen to a much wider area for greater gene flow.
Criticize moths for hiding in dark places or eating holes in your wool sweater, but still recognize that thousands of plant species depend on hawkmoths for successful seed production.
Arthur C. Gibson, MEMBG Director
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