Flowering and Their Pollinators at the Arnold Arboretum

David Giblin any visitors to the Arboretum 1Arnold know it as a world- renowned garden with an unpar- alleled collection of woody plants. For others, it is a park affordmg respite from urban pressures. For still others, it is an important resource for studying a wide range of topics, from exploration to arboriculture, from plant to the history of landscape design. Speaking for myself, as a floral biologist I view the Arboretum as one of the world’s finest muse- ums of pollination biology. The plant collections of the The are to all, and Arnold Arboretum are living of magnohas open pollmators nonpollmators illustrations of the remarkable ahke In this photograph of Magnolia acummata var subcordata, the msitor, a bee, happens to be a pollmator, but it could lust as well be a beetle or fly floral over diversity engendered en7oymg a free meal. evolutionary time by the partici- pation of pollinators in plant reproduction. The ited on the female reproductive structures of vas- variety of floral sizes, shapes, colors, and fra- cular seed plants, typically with the aid of ani- grances on display demonstrate the range of mals, wind, or water. For pollination to result in adaptations evolved by the flowering plants in fertilization, the sperm cell of a pollen grain must response to the predilections and idiosyncrasies unite with the egg cell of an ovule, after which of their pollinators. the fertilized ovule develops mto a seed. For example, some flowers in the collections Basic biology teaches that the living vascular are open to all potential pollinators; others have seed plants are divided into the gymnosperms evolved complex morphologies that allow entry (the conifers, cycads, gnetophytes, and ginkgo) to only the most reliable visitors. Each morphol- and the angiosperms (flowering plants) on the ogy reflects a strategy that has proven success- basis of their reproductive characters. The ful in ensuring that these winged vectors primary distinction is that gymnosperms (liter- transport pollen between flowers. Among the ally, "naked seeds") lack flowers-the ovules more astonishing strategies are the use of petal are borne openly in cones-whereas in angio- color and pattern as signals, both honest and sperms ("vesseled seeds") the ovules are deceptive, and of male floral parts that are enclosed within the carpel of the . The spring-loaded or acoustically sensitive. fossil record has shown that flowers evolved By definition pollination is the process after the gymnosperms, making the latter the whereby pollen grains (male gametes) are depos- more ancestral lineage. 14 .

The course of floral evolution in angiosperms pollen grains. In the course of foraging among involved several major trends. These include a plants, the insects deposit pollen on the female reduction m overall complexity (for instance, a cones, allowing fertilization to begin. reduced number of stamens or petals), a transi- The evolutionary pathway from the gymno- tion from radial to bilateral floral symmetry, the sperms to the angiosperms has not yet been fusion of petal and/or sepal parts, and a transi- completely mapped. We do know that gymno- tion from a superior ovary (that is, the ovary sits sperms are almost exclusively wind-pollinated, above the attachment of the other floral whorls) whereas the majority of angiosperms evolved a to an inferior one. It is important to remember dependence on insects, birds, or mammals for that these are trends; evolution is not a linear pollination. Interestingly, recent systematics process. Ancestral morphologies such as radi- studies have shown that speciation in plants has ally symmetrical flowers with separate petals been greater in those lineages that are animal- and superior ovaries can be found in angiosperm pollinated (Dodd et al. 1999). Those studies families that are regarded as having originated support the theory that diffuse coevolution more recently. between angiosperms and their pollinators con- Most biologists agree that insects, probably tributed to today’s diversity of beetles, were the first pollinators, and that (Takhtajan 1991).~. gymnosperms were the first seed plants to rely Diffuse coevolution occurs when two groups on pollinators for reproduction (Leppik 1960). of organisms-in this case, flowering plants and Gymnosperm taxa, including members of pollinators-interact in such a way that evolu- Cycadaceae and Gnetaceae (Welwitschia tionary change in one group leads to evolution- mirabilis and species of Ephedra), all show evi- ary change in the other. Evidence for diffuse dence of being insect-pollinated (Norstog 1987; coevolution in the plant-pollinator relationship Cooper-Driver 1994; Proctor and Yeo 1996). Pre- is suggested by the fossil record, which shows sumably insects feed on the protein-rich pollen rapid diversification within both angiosperm of the male cones and on a sticky, sugar-rich and insect lineages between 75 and 50 million feature of the female cone that catches airborne years ago (Proctor and Yeo 1996). For example, the length of bee mouthparts increased during the time that tubular flowers arose; longer mouthparts presumably allowed access to nectar found at the base of many tubular-flowered species. Nevertheless, pollination biologists dispute the degree of specialization in the coevolu- tionary association between plants and pollinators. Several leading researchers believe that the evolution of floral morpholo- gies that attract specific pollina- tors are the exception. Their evidence is the observation that flowers of many plant species are visited often by a diversity of insect types (Waser et al. 1996). of this In the bilaterally symmetncal flowers of yellowwoods, the pistil and stamens Opponents view argue are tightly enclosed mthm the petals, permittmg access only to bees, which that visitation does not always are both discmmmatmg and rehable pollmators. result in pollination, and it is 15

in order to meet its foraging requirements. Increased flower visitation should mcrease the likelihood of successful pollination. Conversely, pollinators would ideally visit only those flowers that provide an adequate reward relative to the time and energy invested m foraging. Assuming easy access to adequate rewards, the most efficient approach would be to forage randomly among species. In that case, however, the plants would be the losers: the pol- len from one plant species might end up in the flower of an unrelated species, and the reproduc- tive success Pnor to pollmator visitation, "sprmg-loaded" an- of each species would be reduced. thers are held by the lower petals. Pollmators disrupt The result of these conflicts m perspective the petals upon entry, releasmg the anthers, which has been the evolution of strategic compromises deposit their pollen on the msect’s underside. From between plants and their pollinators. Examples The Natural of Pollination Michael History by can be found throughout the Arboretum Proctor, Peter Yeo, and Andrew Lack, 1996. Used by grounds, us to retrace major courtesy of Timber Press. enabling develop- ments in these give-and-take relationships. pollinator preference that has driven diversifica- They have contributed substantially to the aes- tion in floral morphology. thetic appeal of the Arboretum and, indeed, of The long-standing, coevolutionary associa- gardens everywhere. tion between plants and pollinators is based on The magnolia family (Magnoliaceae), promi- a mutualism, a win-win situation for the par- nently displayed near the Hunnewell Visitor ticipants of a biological interaction. In this case, Center, is one of the most ancestral angiosperm plants benefit by getting their pollen trans- families in the living collections. Members of ported between flowers, and pollinators benefit the genus Magnolia possess a generalized floral by acquiring pollen, nectar, or oils from the morphology that does not discriminate among flowers that they visit. floral visitors: the flowers are radially sym- A mutualism often requires con- tinual adjustments by the partici- pants to ensure a parity in benefits. From the plant’s perspective, the number of fertilized ovules must be high enough to justify the invest- ment in energy required to attract and reward pollinators. This invest- ment can be measured m terms of flower size and number, duration of flowering period, and/or amounts of pollen, nectar, or oil produced. To ensure adequate return on this investment, plants typically do not provision each flower with rewards high enough to satisfy the pol- linator’s needs in a single visit. The goal is to offer a reward generous to attract and enough pollinators The reflexed anthers of Kalmia latifolia m the left photo mdicate an yet stmgy enough that the pollina- unpollmated flower. The photo at nght shows how the anthers are tor needs to visit several flowers released after pollinator visltation. 166

source for some adult beetles and flies. Consequently these floral visitors are consuming rather than transporting the pollen, which reduces the repro- ductive opportunities for the tree; such is the downside to the easy-access approach. However, in most cases, some of the pollen sticks to the insects’ bodies while they feed, to be deposited on the stigmas of flowers visited later. In some cases, certain visitors are clearly inadequate as polli- nators, a category that mcludes the indiscriminate forager. A visitor that acquires pollen from A truss of mountam laurel with some anthers still reflexed and yet to be the flowers of species A and pollmated, and some released, indicating pollination. then visits the flowers of species B makes a poor pollinator; reproductive opportunities for both plants have been lost. Pol- len from A is wasted if it ends up on B’s flowers because fertili- zation does not occur. Addition- ally, the stigmatic surface of B is clogged by A’s pollen, and this reduces B’s reproductive capacity. Some plants have evolved a two-step solution to this problem: first, they con- trive to attract pollinators capable of fidelity, and second, they develop ways to keep out all other visitors. Walking up the Arboretum’s main drive we encounter yel- Communication between flowers and pollmators is common In Catalpa lowwood (Cladrastis kentukea), the combmation dark brown seen m specioso of splotches (most easily scholar tree (Styphnolobium the rightmost flower) and yellow patches oment pollinators to the location of the nectar. japonicum, formerly Sophora japonica~, and bristly locust metrical; the petals are many and large; and a (Robinia hispida), members of the legume fam- central strobilus (cone) containing numerous ily (Fabaceae). Unlike the magnolias, these stamens and pistils rises above the petals. A plants have bilaterally symmetrical flowers glance inside the flowers on a single tree reveals with the pistil and stamens hidden inside a tight the result of this open-door policy: a diverse enclosure of petals. Only bees have the strength assemblage of flies, bees, and beetles can typi- and coordination to manipulate the petals and cally be found. Pollen is the only floral reward gain access to the flower’s interior and the nec- offered-not an ideal arrangement from the tar it holds; and unlike beetles and flies, bees tree’s viewpoint, since pollen is a primary food show a good deal of species-level constancy 177

while foraging. Bees visit legume flowers for fused to form a cuplike structure that offers a their nectar, as this sugar-based solution fuels steady landmg surface for pollinators. Inspect their fhght. Many legumes use "spring-loaded" the flower closely and you will see that the stamens to ensure that the bees they nourish anthers are held m small depressions that ring earn their meal. As a bee makes its way into the the inner periphery of the petal tissue. This cre- flower to collect the nectar reward, the flower’s ates tension on the filaments that hold the spnng-loaded stamens are tripped, propelling its anthers, as their other end is anchored lower pollen onto the bee’s underside. When the bee down in the center of the flower. Each stamen visits the next flower, the pollen is deposited on therefore looks like a small catapult. The pres- the stigma as the bee enters, and pollination has sure of a pollinator walking on the petal surface been effectively, and efficiently, achieved. sets off one or several of these catapults, and the Legumes are not alone in using spring-loaded pollen is plastered onto the visitor’s body. stamens to affix pollen to visitors. Mountain Signals are the attraction strategy of choice laurel (Kalmia Iatlfoha), a member of the heath for several taxa in the Arboretum. Catalpa family (Ericaceae) and a New England native, speciosa (western catalpa), like other members can be found throughout the Arboretum. Over of the bignone family (Bignonaceae), can be evolutionary time, petals on the flowers have found on Bussey Hill just above the lilac collec- tion. It produces large, white, tubular flowers with a pronounced lower lip. Looking inside a flower one notices two distinctive features: one, a pair of broad yellow stripes that start near the mouth of the tube and terminate at its base, and two, some small, brownish-purple splotches scattered throughout the tube. To our eyes it is color and pattern beautifully arranged, but to bees these are guides to that highly prized reward, nectar. In some taxa, signalling to potential pollina- tors continues even after the flowers have been pollinated. Red buckeye (Aesculus paviaJ, of the horse-chestnut family (Hippocastanaceae), is found growing along the main dnve just beyond the Cornus collection. It produces red tubular flowers with yellow nectar guides that attract pollination by bees, but here, after a flower is pollinated, the guides "turn themselves off" by changing from yellow to pink (Weiss 1995). To understand the benefits of such a signal, con- sider once again the perspective of the bees. Many pollinating bees sip nectar continu- ously in order to fuel the flight muscles that carry them between the flowers they visit and the brood they provision with pollen. Like all animals, bees strive for maximum foragmg effi- ciency. After encountering several unrewarding Members of the Aesculus genus, mcludmg this horse- flowers on a single plant, a bee is likely to move chestnut, A. x plantenensis, maximize the size on to another As a the that of inflorescence display by retaining pollmated nearby. result, plant is snubbed loses flowers. Pollmators distmgmsh between vmgm and reproductive opportunities. pollmated flowers on the basis of colored patches By turmng off the nectar guides of the flowers on the petals that have already been visited, the red buckeye 18 .1

Doublefile (Viburnum plicatum f. tomentosum) is in ; it grows in the viburnum collection located near the Dana Greenhouses. Snow-white flowers are produced in flashy, flat-topped cymes that few human visitors fail to notice. However, close inspection of an individual cyme reveals that its showiness resides in the ring of large (0.75 to 1.5 inches wide) sterile flowers that surround an interior cluster of unenticing fertile flowers. The pri- mary role of the sterile flowers is to attract pollinators-rather deceptively, since they offer no reward. Much like restaurant customers who find that the special of the day is no longer being served, pollinators will nevertheless indulge themselves in whatever rewards the fertile flowers do offer before leaving. A final example brings us back to the Hunnewell Visitor Center. In my view, Actinidia arguta (bower actimdia), a vine in Actinidiaceae, boasts the most mnovative polli- nation mechanism found at the Arboretum. It grows along the fence just south of the main entrance. This species is primarily dioecious, meaning that there are separate male and female plants. Pollen is extracted from the male flow- The famtly darker patch on the petals of this Weigela ers an known as "buzz middendorffiana mdicate that the flowers have been through amazing process pollinated. pollination" (Buchmann 1983, Proctor et al. 1996). A visiting bee grabs the anthers with its directs pollinators to profitable flowers, thereby legs and then vibrates its wings while remaining enhancing their efficiency while improving stationary. This generates an acoustic resonance its own reproductive opportunities. Other taxa that causes pollen grains to pour out of the in the Arboretum that employ post-pollination anthers and onto the bee’s body. When the bee signaling either through color or morphologi- forages for nectar in a female A. arguta flower, cal changes in floral parts include flowering pollination is achieved. weigela in Caprifoliaceae, Scots broom (Cytisus This has by no means been an exhaustive scoparius) in Fabaceae, and goldenrain tree account of pollination mechanisms on display (Koelreutena pamculata) in Sapindaceae at the Arnold Arboretum. Examples can easily (Weiss 1995).~. be found to illustrate the adaptive significance Flowering plants are certainly not above prac- of many other pollination-related flower charac- ticing deception in order to attract pollinators. teristics ; the positioning of the ovary with Like restaurant owners, they live in a competi- respect to the petals and sepals, inflorescence tive world where the biggest challenge is per- architecture, and floral fragrance all have adap- suading the desired clientele to stop in and tive value in the context of pollination. Clearly, where advertising may be a useful tool. Within successful pollination, a challenge faced by all some taxa there is a positive correlation vascular seed plants, has been solved in many between flower size and the amount of reward: ways. The Arnold Arboretum provides in a the bigger the flower, the more pollen or nectar single location an unusually comprehensive to be found. However, some plants don’t always taxonomic collection that allows visitors to back up their advertising. observe the remarkable innovations that have 19

resulted from the mutualistic relationship between plants and their pollinators. Viewing the living collections at the Arnold Arboretum as a pollination biol- ogy museum reminds us that the diversity of flower shapes, colors, and sizes that brighten our gardens, entertain our minds, and touch our spirits have their origins in a relation- ship that was initiated over 100 million years ago.

Literature Cited Buchmann, S.L 1983. Buzz pol- lination m angiosperms Handbook of expenmental pollination biology, ed. Deception can reduce metabolic costs associated with pollmator attraction. C.E. Jones & RJ. Little sterile draw toward the diminutive ones of New York: Van Nostrand Large flowers pollmators fertile Viburnum tomentosum. Remhold, 73-113. plicatum f Cooper-Driver, G. 1994. Welmtchia mmabihs A Dream Waser, N.M., L. Chittka, M.V. Price, N.M Williams, True. Amoldia 2-10 Ollerton 1996. Generalization in Come 54(2) : J. pollina-~,41 tion systems, and why it matters. Ecology 77: ~ and M.W Chase. 1999. ’ Dodd, M E., J Silvertown, 1043-1060. Phylogenetic analysis of trait evolution and species diversity variation among angiosperm Weiss, M.R 1995. Floral color change: a widespread families Evolution 53: 732-744. functional convergence American Journal of

Leppik, E.E 1960. Early evolution of flower types. . Botany 82(2) 167-185 Lloydia 3: 72-92 Norstog, K. 1987. Cycads and the origin of msect Amencan Sclentist 75. pollination. 270-278. David Giblin was an intern and curatorial associate in Proctor, M., P. Yeo, and A. Lack. 1996 The natural the Arboretum’s plant records department. Since then, history of polhnation Portland, OR Timber he has earned a master’s degree m conservation biology Press, 179-180. from the University of Washington and is currently a Takhta~an, A 1991. Evolutionary trends m flowering doctoral candidate at the University of Missouri where plants. New York: Columbia University Press, he is studying the relationship between pollinators and 171-184. floral longevity.