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Spring Ephemerals) 1 Sex Lives of Woodland Herbs Spring in the forest begins with a smorgasbord of flowering herbs. Hillsides become carpeted in white, pink, and maroon as trillium flowers open. The yellow bell-shaped flowers and mottled leaves of trout lily blaze in the April sunlight. Yellow, white, and blue violets flower in profusion along trails and creeks. Squirrel corn (Dicentra canadensis) flowers flavor the air with a sweet aroma (Figure Spring Ephemerals). The early woodland herbs, or spring ephemerals, spring forth quickly with leaves, flowers, and fruits and then wither just as summer heats up. Their strategy is to perform energy demanding activities quickly while sunlight abounds under the bare forest trees. In a few short weeks, many of these perennials will shift from a cryptic underground phase to a robust plant with conspicuous flowers only to return to hiding by July. The above ground growth phase is never prolonged. April trillium flowers progress to fruits and seeds in late July. Trout lily (Erythronium americanum), on the other hand, has one of the shortest above ground periods. They send both leaves and flowers to the surface in early April, then six weeks later the plant senesces as the fruit capsule lies quietly on forest soil. Special contractile roots, common among lily members, pull the expanding trout lily corm further beneath the soil. The large, colorful spring ephemeral flowers advertise their pollen and nectar rewards to early flies and bees in the forest. Insects are efficient and abundant pollinators on warm sunny days in the spring forest. Insect pollinators feed intensively with deliberate flights between flowers. Individual insects remain faithful to specific flowers for extended times on their foraging bouts, but occasionally sample nectar from other flowers. A bee working a patch of spring beauty will likely skip over dozens of violets, trilliums, and trout lilies just to find the next spring beauty. Different flower species are easily recognized by color, nectar guides, shape, and odor to provide insects with the means for quick identification on their forays. Migrating hummingbirds also participate in the act of pollination on the hanging red flowers of columbine (Aquilegia canadensis) that colonizes light gaps within the forest. Many spring ephemeral flowers are designed for cross-pollination. Physical separation of anthers and stigmas is commonly employed as a means to reduce self-pollination in hermaphroditic (i.e., flowers with both stamens that produce pollen and ovaries that produce ovules producing) flowers. Some woodland herbs utilize a chemical interaction between pollen and stigmas to inhibit “self-pollen” from germinating on styles of the same plant (i.e., self incompatible pollen). Wild sarsaparilla (Aralia nudicaulis), white trillium (Trillium grandiflorum), trout lily and bunchberry (Cornus canadensis) are a few woodland herbs with a self-incompatibility mechanism. An out-crossing breeding system shuffles and maintains genetic variation within populations of a species. Genetic variation can manifest itself in subtle differences in characteristics such as flower color, nectar guides, pubescence and petal size and shape in many woodland flowers. Flowers on the same plant should be nearly identical and but differences likely exist on flowers of neighboring plants of the same species. A careful observer in the forest can easily see distinct differences in flowers of trillium, spring beauty, and liverleaf within a population. Much of this floral variation has a genetic basis just as hair and eye color on humans. Like humans, maintenance of variation in the population is due to a mating system where sexual encounters between different individuals of the same species are the norm. 2 Self-pollination and self-compatibility have evolved in a few woodland herbs. This means of sexual reproduction minimizes genetic variation, but guarantees reproductive success when pollinator numbers are low. Spotted touch-me-not (Impatiens capensis) grows along streams and moist areas of the forest. The large orange flowers of this handsome plant are designed for cross-pollination (chasmogamous flowers), but individual plants also produce closed flowers lower on the plant body. These cleistogamous flowers promote self-pollination by forcing anthers to contact the stigma in the closed flower bud. Many species of violets have chasmogamous and cleistogamous flowers similar to spotted touch-me-not. Insects also learn to discriminate between closely related flowers (Figure Reproductive Isolation). At least a dozen species of violet live in eastern deciduous forests. A few species are reproductively isolated by flowering very early like round-leaf violet (Viola rotundifolia) or by flowering very late like purple forest violet (Viola adjunca). For those species that flower simultaneously and in close proximity to one another, the challenge is to attract faithful bumble bees to encourage pollen movement only between flowers of the same species. Forest violets rarely hybridize, and any pollen movement between violet species will result in the waste of pollen and perhaps lower reproduction. The pale violet (Viola striata) produces cream- colored flowers with violet nectar guides and a short nectar spur. The long-spurred violet (Viola rostrata) has violet colored flowers with dark blue blotches towards the inside of petals and a very long nectar spur. Canada violet (Viola canadensis) has pure white flowers with purple lines and a yellow center. The downy yellow violet (Viola pubescens) produce bright yellow flowers with reddish nectar guides. All bloom profusely along our trails and maintain a high degree of pollinator fidelity, and maintain their unique species identity. Bumble bees foraging in a mixed violet population use the differences in visual, tactile, and olfactory cues to move between flowers of the same species. As long as the foraging bout remains profitable, bumbles will stick to flowers of the same species and change flowers only when nectar rewards decline below some threshold. Floral traits can also serve as guideposts or reminders of caloric rewards when a bumble flies to new patches of flowers much like the golden arches have become icons for high calorie hamburgers when visiting a new town. Dutchman’s breeches (Dicentra cucullaria) and squirrel corn (Dicentra canadensis) provide another story of pollination and insect discrimination. Native bumble bees pollinate both species. Pollination mistakes are seldom made and even if cross-pollination between the species results, hybrid seed would not be produced. Squirrel corn flowers are fragrant and the petals have rounded bases. Dutchman’s breeches have sharply-angled petal bases and no odor. These powerful recognition signals allow discriminating bumble bees to concentrate on one species of flower at any given time. Not all spring ephemerals value insect pollination (Figure Wind Pollinated Forest Herbs). The forest sedges (Carex) and early meadow rue (Thalictrum dioicum) produce less conspicuous flowers and larger and more numerous stamens higher off the ground than insect-pollinated flowers. Anthers 3 of these two plants rock back and forth in gentle spring breezes broadcasting pollen to the surrounding forest floor. Large feathery stigmas capture pollen on the wind. Much of the pollen is lost to the forest floor which is why these plants must produce many stamens, large anthers, and more pollen. Even though evolution has lead to a waste of pollen grains, these species are less exuberant in their advertisement and save energy by not attracting and rewarding insects with colorful, energetically costly nectar-bearing flowers. The lack of color in the flowers may also prevent insects from being attracted and then stealing pollen. Natural selection has acted along different paths to meet the same requirements for reproduction. Flowering does continue in the herbaceous zone of forests well into June and July, although less profusely. The early, colorful flowers are gradually replaced with those of white (Figure Summer Woodland Flowers). In the darkened forest, white stands out more strongly against green leaves on the forest floor rather than red or pink. Forest bees and flies continue to pollinate that late flowering species such as foam flower (Tiarella canadensis), Canada mayflower (Maianthemum canadensis), bunchberry, starflower (Trientalis borealis), teaberry (Gaultheria procumbens), false solomon’s seal (Smilicina racemosa), baneberry (Actaea alba), wild sarsaparilla, and partridgeberry (Mitchella repens). The pollination system of partridgeberry is unique among the forest herbs (Figure Partridgeberry Flowers). Individual plants produce one of two flower types and both flowers have tubular corolla with pubescent petals. The “pin” type flower has a four-pronged stigma that unfolds beyond the open petals. The four anthers are located on top of shortened stamens within the corolla tube in pin flowers. The “thrum” type flower has the reverse morphology. The four-lobed stigma opens within the corolla tube and the stamens protrude beyond the petals to expose the anthers. Legitimate pollination occurs in specific directions: thrum pollen to pin stigmas and pin pollen to thrum stigmas. The physical separation of stigmas and anthers ensures that pollen deposition and retrieval on insects occurs on different regions of their body for the appropriate pollination pathway. When mistakes are made, the plant has a built-in biochemical pollen recognition system to reject
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