The Correlation Between Herbivory and Medicinal Activity in Thespesia Populnea, Hibiscus Tiliaceus and Hibiscus Rosa‐Sinensis on Mo’Orea, French Polynesia
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THE CORRELATION BETWEEN HERBIVORY AND MEDICINAL ACTIVITY IN THESPESIA POPULNEA, HIBISCUS TILIACEUS AND HIBISCUS ROSA‐SINENSIS ON MO’OREA, FRENCH POLYNESIA HAYLEY A. COX Integrative Biology, University of California, Berkeley, California 94720 USA Abstract. While secondary compounds are produced by plants in low abundance, these bioactive compounds are essential to human survival for their medicinal applications. These same compounds are crucial to plants, having evolved as defense mechanisms against herbivory. Chief among the theories of plant responses to herbivory, the Optimal Defense Theory (ODT) hypothesizes that plants will allocate defenses in direct proportion to the risk of a particular plant part to herbivory and the value of that part in terms of loss of fitness to the entire plant. Through insect damage assessments and antimicrobial assays, this study investigates the correlation between herbivory and medicinal activity and whether or not the within‐plant ODT is followed in three ethnobotanically useful Malvaceae species, Thespesia populnea, Hibiscus tiliaceus and Hibiscus rosa‐sinensis. All three plant species demonstrated an inverse relationship between herbivory and medicinal activity. Variation in secondary composition data from both insect damage assessment and antimicrobial tests supported the ODT. Keywords: Thespesia populnea, Hibiscus tiliaceus, Hibiscus rosa‐sinensis, coevolution, secondary compounds, herbivory, Optimal Defense Theory (ODT), antifungal INTRODUCTION (Stamp 2003), which are typically used for medicinal applications. Since the beginning of human history, The antagonistic arms race between plants plants have played an integral role in human and insects is evidenced by the diversification survival. However, while scientists have of insects and plants which occurred over the calculated that humans in their modern form same approximate time periods, and many of speciated only approximately 200,000 years these insect/ host plant relationships have ago, primitive vascular plants originated in been conserved (Farrell 1994). Today there are the Silurian period, roughly 430 million years about 240,000 species of flowering plants, ago. The oldest fossils identified definitively which greatly outnumber all other kinds of as angiosperms date from the early Cretaceous plants. As the flowering plants became more Period, around 127 million years ago (Raven diverse, so did the insects whose feeding and Johnson 1989). Thus the origin of habits were closely linked with the medicinal activity in plants must have been in characteristics of the flowering plants, response to environmental, not human, supporting the idea that insects and flowering pressures. There is a considerable amount of plants coevolved with one another (Raven and evidence that herbivory was a major selective Johnson 1989). In response to attacks by force on the evolution of plant defenses herbivores, plants have evolved a variety of mechanisms for defense. Insects have in turn countered with their own defenses (Stamp During this project I screened three 2003) because once the members of a species in the Malvaceae family (Thespesia particular group acquired the ability to feed populnea, Hibiscus tiliaceus, and Hibiscus rosa‐ on a certain bioactive plant, these herbivores sinensis), all with known bioactivity, for the gained access to a new resource which they purpose of assessing how the bioactivity of could exploit without competition from other these species correlates with damage from herbivores (Raven and Johnson 1989). The herbivores. Specifically, I ask: (1) does the defense mechanisms in plants that act as insect amount of herbivory damage on a given plant deterrents are known as “secondary” relate to the amount of insecticidal secondary compounds since they do not contribute to compound in the plant; and (2) do these any primary photosynthetic or metabolic species allocate more secondary compounds activities to the plants (Stamp 2003). While to their younger and/or reproductively active secondary compounds are produced in low parts as compared to their older parts, abundance, they are essential to human and following the predictions of the ODT? plant use. There are many possible ways plants can METHODS respond to herbivory. According to Stamp (2003), the within‐plant Optimal Defense Study Sites Theory (ODT) predicts that a plant will allocate its defenses in direct proportion to the Mo’orea (GPS location: 06K 0192036 E, risk of a particular plant part to herbivory and 8062786 N) is a volcanic, high island the value of that part in terms of loss of fitness (maximum elevation 1207 m) that is part of to the entire plant. Further, there will be the Society Islands archipelago in French within‐plant variation in the distribution of Polynesia. Three species in the Malvaceae these bioactive compounds for defense; the family were selected for study for two reasons: plant will invest the greatest amount of first, each species has documented medicinal defensive secondary compounds in its most activity (Whistler 1992) and second, reproductively active parts (flowers, fruits and Anderson’s (2005) study on the model young leaves) (Anderson, 2005). Anderson Malvaceae species, cotton, found evidence for (2005) found support for this idea in a study the presence of anti‐herbivore defensive focused on a model system using cotton compounds. Thespesia populnea, Hibiscus (Gossypium hirsutum: Malvaceae) in which tiliaceus, and Hibiscus rosa‐sinensis, were damage resulted in higher concentrations of collected from two sites on Mo’orea– site A secondary compounds in the young and/or along the coastline just south of Gump Station reproductive tissue. This type of defense is (06K 0199841 E, 8063792 N) and site B along known as an induced defense reaction because the coastline on Mari Mari Kellum’s property it involves new production or the (06K 0197422 E, 8061475 N) (Figure 1). All translocation of secondary compounds within plant species collected were deposited into the the plant in response to tissue damage University of California Herbarium, Berkeley. (Anderson 2005). Anderson’s study further revealed that an induced response occurs after Sample Species insect damage throughout the entire plant regardless of where plant damage originally Thespesia populnea, Soland ex. Correa 1807, occurred. Another major type of plant defense of the Malvaceae family (Tahitian name is constitutive defense, a defense always “Miro”) is a native tree that is widespread present in a plant. Anderson’s (2005) study from East Africa to Eastern Polynesia and is documented the presence of both constitutive common both along beaches (Medicinal Plants and induced defenses in cotton plants. in the South Pacific, 1998), and in the valleys Site A. Gump 500 m elevation. H. rosa‐sinensis, widely Station introduced throughout the South Pacific (Medicinal Plants in the South Pacific 1998) has been reported to have antioestrogentic, Site B. Mari Mari anti‐cancer, analgesic, anti‐inflammatory and Kellum’s Property antifungal properties (Medicinal Plants in the South Pacific 1998). Traditionally, H. rosa‐ sinensis has been used by Tahitians to induce abortion, ease menstrual cramps, assist in childbirth and to treat boils, sores and FIG. 1. Site locations on Mo’orea. inflammations (Medicinal Plants in the South Pacific, 1998). of Mo’orea (Chabouis, 1970). It is known to contain antibacterial, antifungal, anti‐yeast, Plant Material Collection antiimplantation and antispasmotic properties (Medicinal Plants in the South Pacific 1998) At each site, plant material was collected and has a wide range of traditional uses from three individuals of each species (n=18). throughout the South Pacific. These include In order to asses if the amount of herbivory the use of an infusion of the crushed seeds to damage on a given plant correlated to the soothe headaches and the use of sap from the amount of insecticidal secondary compound fruit stalk to topically treat skin ailments such in the plant, samples were collected from each as centipede bites (Whistler, 1992), jellyfish individual, separating each tree into four stings and cuts (Tom Carlson, personal quadrants: water‐side left (A), water‐side right communication). (B), mountain‐side left (C), and mountain‐side Hibiscus tiliaceus, Linnaeus 1753 (common right (D) (Figure 2). Each quadrant was name yellow or beach hibiscus or Tahitian separated into the highest and lowest four name “Purau”) is a native, medium‐sized tree branches that could be reached. To determine abundantly distributed throughout the if these species allocated more secondary tropics. It is found along coastlines worldwide compounds to their younger and/or and is common on beaches and thickets reproductively active parts as compared to (Medicinal Plants in the South Pacific 1998), their older parts, four “young” and four “old” yet can spread up to the highest points on leaves were collected from each height within Mo’orea (Murdock, 2008). H. tiliaceus has each quadrant from each individual (n=1152). traditionally been used by the Polynesians to “Young” leaves were categorized as the first treat a wide range of ailments including sizable leaf at the tip of each branch and “old” fractured bones, sprained muscles, gonorrhea, leaves as the tenth leaf down on the same menstrual cramps, abrasions, and fever branch. Additionally, five haphazardly (Medicinal Plants in the South Pacific 1998). A collected fruit samples for T. populnea and five student paper (Achrekar 1995) additionally flowers