Parasitic plants: Important components of biodiversity

From Plant Press, Vol. 22, No. 4, October 2019.

By Marcos A. Caraballo-Ortiz

Parasitic organisms are generally viewed in a negative way because of their ability to “steal” resources. However, they are biologically interesting because their dependency on hosts for survival have influenced their behavior, morphology, and genomes. Parasites vary in their degree of necessity from a host, ranging from being partially independent (hemiparasitic) to being complete dependent (holoparasitic). Some parasites can live independently, but if they find potential hosts, they can use them to supplement their nutritional needs (facultative parasitism).

Laurel dodder (Cassytha filiformis, Lauraceae) twining around the stems of its host (Croton sp., Euphorbiaceae) on Providenciales Island, Turks and Caicos. (photo by M. Caraballo)

Parasitism is not a phenomenon unique to animals, as there are plants parasitic to other plants. Current biodiversity estimates indicate that approximately 4,700 species of flowering plants are parasitic, which account for about 1.2% of the total inferred number of plant species in the world. About half of the known species of parasitic plants belong to a single order, Santalales, which is diverse and mainly composed of hemiparasites. However, parasitism has evolved independently in 11 lineages of angiosperms comprising 27 families, some of them small and consisting of only one species. Parasitic plants have been able to colonize almost every corner of the world (except the polar regions), and many are common in lowlands and disturbed habitats. Only a few parasitic plants yield economically important products such as the sandalwood, obtained from the tropical shrub Santalum album (order Santalales). Other products are local and include traditional medicines, food, and crafts like “wood roses”. Many parasites are also considered agricultural pests as they can impact crops and timber plantations.

Aerial shrubby habit of a mistletoe (Dendropemon purpureus, Loranthaceae) on the branches of a calabash tree (Crescentia cujete) in Gonave Island, Haiti. (photo by M. Caraballo)

It is difficult to describe a typical parasitic plant because they possess a wide diversity of growth habits such as trees, terrestrial or aerial shrubs, vines, and herbs. The largest known parasitic plant is the tree Okoubaka aubrevielli (order Santalales) from tropical Africa, which can reach up to 40 m tall and parasitize many species of trees, apparently killing the closest neighbors to minimize competition for light. The smallest parasite is likely the miniature mistletoe Viscum minimum (also in order Santalales), whose tiny stems and inflorescences measure up to 3 mm long and in nature, only grows on two species of spurges (Euphorbia horrida and E. polygona, Euphorbiaceae) from South Africa. It is notable that the largest flower in the world, the corpse lily (Rafflesia arnoldii, Rafflesiaceae), is a parasite that grows embedded into the stems of a woody vine (Tetrastigma spp., Vitaceae) in the rainforests of Sumatra. Many other parasitic plants grow as vines such as dodders (Cuscuta spp., Convolvulaceae) and the laurel dodder (Cassytha spp., Lauraceae), which form dense masses of twining yellowish stems wrapping their hosts. Terrestrial parasites like broomrapes (Striga spp., Orobanchaceae) are known for their capacity to affect or even destroy agricultural crops such as rice, maize, sugarcane, and sorghum. Some parasitic herbs are not aggressive and are used as ornamentals in gardens such as the Indian paintbrush (Castilleja coccinea, Orobanchaceae) and some species of louseworts (Pedicularis spp., Orobanchaceae).

The most recognized parasitic plants are probably mistletoes which are aerial hemiparasitic shrubs. Mistletoes are part of the folklore from many countries and are still included in modern traditions such as the Christmas custom of kissing under the mistletoe for enduring love. The Christmas mistletoe involves two species: the European Viscum album and its American counterpart Phoradendron leucarpum. However, mistletoes are a diverse group comprising about 1,663 species in 90 genera distributed around the globe, especially in the tropics. All mistletoes belong to order Santalales where they are classified in five families: “Amphorogynaceae”, Loranthaceae, Misodendraceae, Santalaceae, and “Viscaceae”.

Table 1. Orders and families containing parasitic flowering plants, with estimated numbers of genera and species. Names within quotes include taxa not properly recognized yet by the Angiosperm Phylogeny Group IV (APG Bot. J. Linn. Soc. 181:1–20; 2016). Estimates obtained and adapted from “The Parasitic Plant Connection” website by Daniel Nickrent (2019; https://parasiticplants.siu.edu).

Order	Families	Parasitic Genera	Parasitic Species
Boraginales	Lennoaceae	2	4
Cucurbitales	Apodanthaceae	2	10
Ericales	Mitrastemonaceae	1 (Mitrastemon)	2
Lamiales	Orobanchaceae	100	2,100
Laurales	Lauraceae	1 (Cassytha)	20
Malpighiales	Rafflesiaceae	3	35
Malvales	Cytinaceae	2	12
Piperales	“Hydnoraceae”	2	12
Santalales	16 “Families”	166	2,284
Saxifragales	Cynomoriaceae	1 (Cynomorium)	1
Solanales	Convolvulaceae	1 (Cuscuta)	215
Zygophyllales	Krameriaceae	1 (Krameria)	23
Total Number of Parasitic Plants	27	282	4,718

The largest flower in the world, Rafflesia arnoldi (Rafflesiaceae), from West Sumatra, Indonesia. (photo by Lentera Merah; CC BY-SA 3.0, https://creativecommons.org/licenses/by-sa/3.0)

All mistletoes have the capacity to create their own food through photosynthesis, hence the term “hemiparasites”. However, since mistletoes depend on hosts to obtain water and some mineral nutrients, they are also considered obligate parasites. The relationships between mistletoes and hosts is complex and involves compatibility at the physical, physiological, and most likely genetic levels. Mistletoes, as well as other parasitic plants, can have unusual chloroplast genomes with major alteration or losses of genes and rearrangements of their genomes due to their dependence on hosts.

Inflorescence of the American cancer-root (Conopholis americana, Orobanchaceae) parasitizing the roots of a red oak tree (Quercus rubra, Fagaceae) at the Shenandoah National Park, Virginia. Note the yellowish color of the plant which reflects its holoparasitic nature. (photo by M. Caraballo)

Most mistletoes also have intimate interactions with birds, depending on them for seed dispersal and sometimes pollination services. In fact, studies have shown that there are lineages of birds and mistletoes that have coevolved, where birds specialize in feeding on mistletoe fruits and track them across the landscape. In a similar way, some mistletoes have evolved specialization to grow only in one or a few species of trees. For example, the dwarf mistletoe (Arceuthobium, Viscaceae) parasitizes pines (Pinaceae), junipers and cypresses (Cupressaceae) exclusively. In spite of being parasites, mistletoes are important components of ecosystems and are even considered keystone species because of their capacity to attract and maintain biodiversity.

My current research project at the National Museum of Natural History is focused on the genetics and taxonomy of mistletoes from tropical America. With a concentration on the Loranthaceous mistletoes, I am exploring the structure of their chloroplast genomes and building a phylogeny that will include almost all known Neotropical genera. The results from this work will help clarify the generic delimitations of mistletoes and I will propose taxonomic changes if needed. As tropical mistletoes are very diverse but still poorly known, and herbaria often house many unidentified or misidentified specimens, my contribution of updated mistletoe identification keys will assist in the curation of herbarium specimens.

Another aspect of my research project is the study of mistletoes from island systems. Many tropical islands worldwide harbor a rich endemic flora, and the Caribbean Islands are not an exception. The Caribbean island archipelago is one of the world’s top five hotspots of biodiversity, containing one the highest concentrations of endemic plant and animal species on the planet, but much of the endemic diversity remains little studied. An outstanding component of these island-endemic floras are mistletoes in the genus Dendropemon (Loranthaceae), which is one of the most species-rich of the 180 island-endemic plant genera of the Caribbean.

Morphological diversity of the Caribbean mistletoes Dendropemon (Loranthaceae). Variable characters include the color and shape of flowers and stamens (top), the color and shape of fruits (center), and the indumenta of inflorescences and branches (bottom). (photo by M. Caraballo & T. Carlo)

Dendropemon and its close relatives form an ancestral clade of small-flowered mistletoes, and is among the seven most diverse genera (out of 76) of Loranthaceae worldwide. The flowers of Dendropemon are among the smallest in the family and are easily distinguished by an extreme dimorphism of stamens, by the presence of staminodia, and by monads in the inflorescences. Dendropemon is also the most widely distributed island-endemic plant genus in the Caribbean, and presents a showcase for the study of biogeography and diversification in the region.

During an integrative taxonomic revision in preparation, I have discovered several new species of Dendropemon and a series of nomenclatural and taxonomic changes in the genus, highlighting the importance of combining herbarium specimens, fieldwork, and modern molecular techniques to revise the taxonomy of this poorly known and diverse group. My work also incorporates the conservation of endangered parasitic plants, especially when they are island-endemic and depend on rare host trees for their survival.

In summary, parasitic plants such as mistletoes offer an excellent opportunity to study the evolution of interactions between plants from the genomic and ecological perspectives. My research emphasizes the need to conduct integrative taxonomic studies of poorly known groups of organisms using traditional herbarium studies and modern molecular techniques to assess their global diversity.