This Article Is from the July 2008 Issue of Published by the American
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This article is from the July 2008 issue of published by The American Phytopathological Society For more information on this and other topics related to plant pathology, we invite you to visit APSnet at www.apsnet.org Robert L. Mathiasen David C. Shaw Northern Arizona University, Flagstaff Oregon State University, Corvallis Daniel L. Nickrent David M. Watson Southern Illinois University, Charles Sturt University, Albury, Carbondale Australia Mistletoes are familiar to most Euro- group. Although all mistletoes are in San- toes begin forming shoots soon after they peans and North Americans because of the talales, this habit evolved five times inde- establish their connection to their host, Christmas folklore associated with these pendently therein, thus they are not mono- while the dwarf mistletoes may take 2 to 6 parasitic flowering plants (33,116). Some phyletic. Even within the Loranthaceae, years to form aerial shoots. may also know these plants are parasites of the family with the most genera of mistle- Pollination. Mistletoes are pollinated by trees but do not realize that mistletoes are toes, three genera attach only to roots and biotic agents (primarily birds and insects) widespread, ecologically important com- therefore by our definition cannot be called as well as wind. Many tropical and sub- ponents of forests worldwide. Although mistletoes. And finally, genera such as tropical mistletoes in Loranthaceae have some mistletoe species are damaging path- Tripodanthus that attach to both stems and large, colorful flowers borne in groups that ogens, most do not impact economically roots stretch the definition yet further and produce large amounts of sugar-rich nectar valuable crops and forest products but demonstrate nature’s abhorrence of human that attract avian pollinators (Fig. 1A and actually play key roles in forest ecosys- categorization. Recent molecular phyloge- B). Elaborate pollination and seed disper- tems. Particularly in Loranthaceae, coevo- netic work has greatly clarified our con- sal mechanisms involving birds have lutionary relationships with birds (involv- cepts of which members of Santalales are evolved in some of these loranth species ing pollination and seed dispersal) have mistletoes and how they are related to one (69,79,104,109,121,144,176). For exam- fueled several adaptive radiations, thus another. ple, birds pry open the fused corollas to producing one of the most diverse and reach their nectar reward, upon which the fascinating life forms on our planet. Here Mistletoe Biology pollen “explodes” onto the bird’s head we summarize mistletoe biology, pathol- Infection. The basic biology of mistle- (109,121). These mistletoes are often di- ogy, and management as well as current toes is remarkable. Host infection has been chogamous (protandrous), and after the ecological concepts and their evolution as described in detail for some groups and not birds have visited flowers in the male revealed by molecular phylogenetics. others, but is considered to be similar for phase, they eventually visit flowers in the all mistletoes (33,74,92,112,116,122). female phase, thereby effecting pollina- What Is a Mistletoe? Upon germination, seeds form a hypocotyl tion. The coevolutionary relationship be- We define a mistletoe as a parasitic that elongates until it forms a holdfast that tween mistletoes and their bird pollinators flowering plant found in the sandalwood attaches firmly to the host branch. As for is so closely linked that disruption of this order (Santalales) that attaches to the stem other flowering plants, seed germination is association could have long-term negative of another plant (primarily gymnosperms influenced by temperature, moisture, and consequences for both interacting organ- and angiosperms). Other angiosperms, light (122). The seeds of mistletoes in the isms and possibly the entire ecosystem such as Cuscuta (Convolvulaceae) and Viscaceae have a chlorophyllous en- (179,219). However, many bird-pollinated Cassytha (Lauraceae), also attach to host dosperm and embryo and so are capable of mistletoes are serviced by a broad range of stems, but these are not considered mistle- producing simple sugars as an energy species, and no bird can be considered a toes. Thus, the term mistletoe describes a source after germination (122). A penetra- mistletoe pollen specialist (219). In Mex- particular plant habit (an aerial parasite) as tion peg develops on the lower surface of ico, Central America, and South America, well as a member of a specific taxonomic the holdfast that mechanically penetrates hummingbirds are key pollinators of mis- the epidermis or bark, eventually contact- tletoes with large, showy red or yellow ing the host’s phloem and/or xylem. Pene- flowers (15,111,204). A variety of insects Corresponding author: Robert L. Mathiasen, North- tration of host tissue is evidently purely by are the key pollinators of mistletoes in the ern Arizona University, Flagstaff, AZ; E-mail: mechanical means, as no chemical break- Viscaceae and Loranthaceae (74,116). [email protected] down of host tissue has been identified While mammals are known to visit flow- thus far. Once the mistletoe has entered ers, they have not yet been positively im- doi:10.1094/ PDIS-92-7-0988 host tissue, it develops its haustorium and plicated as mistletoe pollinators. Bats are © 2008 The American Phytopathological Society then aerial shoots. Many tropical mistle- the most likely mammal pollinators of 988 Plant Disease / Vol. 92 No. 7 mistletoes, but studies have not yet con- cept the flowerpeckers (Dicaeidae) of Asia Host distribution, size, or sex may influ- firmed their role in this process (138). (44 species) (Fig. 2A) and the euphonias ence mistletoe distribution and abundance Dispersal. The coevolution of mistle- (Carduelinae) of Latin America (33 spe- (11,12). For example, when hosts are toes with their avian vectors has resulted in cies). While most discussion of mistletoe widely scattered, their mistletoe parasites attractive and nutritious fruits that provide dispersal is typically restricted to these may be less common and widely distrib- valuable food for many bird species dietary specialists, a wide range of other uted as well. Birds that disseminate mistle- throughout the world (49,120,134,178, avian species disperse their seeds toes often perch at the tops of the larger 179,201,220). The mature fruits of mistle- (219,220), accounting for all dispersal in trees, thus depositing mistletoe seeds high toes are brightly colored (usually white, Europe and most regions of North Amer- in the canopy. For dioecious tree species, yellow, red, blue, or purple) (Fig. 1C), and ica. Within the United States, vectors of bird visitation may be biased in favor of their seeds are coated with a natural Phoradendron spp. (Viscaceae) are fairly fruiting plants, thereby influencing overall “glue,” termed viscin (116,178). Birds well known (74,89,189), but only a few mistletoe distribution (39). Furthermore, either swallow mistletoe fruits whole, peel studies have examined in any detail the the consistent availability of mistletoe off the outer exocarp and ingest the seed relationships between birds and Phoraden- fruits can attract birds which also feed on and viscin, or eat only the viscin coating dron (12,14). For many mistletoes, particu- the host’s fruits (213). This favors the around the seed (116,178,199,200,220). larly those in Central and South America, spread of seeds from infected hosts over Once the bird has eaten the seed, it is the key vectors have not been investigated noninfected hosts during years when sus- either regurgitated or defecated, but the to any large extent (but see 52,139,180). ceptible trees have not produced an abun- seed is still covered with some of its viscin The control of economically damaging dance of fruits. It has been suggested that coat, which allows it to adhere to potential mistletoes in managed areas is often con- when the seeds of infected trees are also hosts. In many instances, seeds adhering to founded by their reintroduction by birds spread by mistletoe vectors and this is a bird’s beak, legs, or feathers are rubbed (74). In South and North America, animals correlated with greater tree regeneration, off onto a branch of a potential host. other than birds have also been implicated the relationship between the mistletoe and Approximately 90 bird species from 10 in the dispersal of mistletoe seeds. In host tree approaches mutualism (213). families are considered mistletoe fruit South America, a marsupial disperses Recent studies have also suggested other specialists, exhibiting a range of behav- seeds (4), and in North America, squirrels intriguing hypotheses regarding the inter- ioral and morphological adaptations to and other mammals have been shown to actions among host morphology, bird be- their narrow diet. Most of these groups are rarely disperse dwarf mistletoe seeds ad- havior, and mistletoe dispersal in South represented by four or fewer species, ex- hering to their fur (92,136,198). America (133,139). This work suggests Fig. 1. The colorful flowers and fruits of mistletoes attract birds. A, Many tropical and subtropical mistletoes have large, colorful flow- ers that are arranged in groups and produce large amounts of sugar-rich nectar that attract pollinating birds. B, Bright red flowers of Amyema miquelli, a common mistletoe throughout the arid regions of inland Australia. C, Fruits of Psittacanthus cucularis are bright blue, which attracts birds that disperse its seeds.