Chemical Ecology of the Tiger Swallowtail: Mediation of Host Use by Phenolic Glycosides

Abstract

Subspecies of the eastern tiger swallowtail butterfly exhibit striking differences in their ability to use quaking aspen (Populus tremuloides) and other members of the Salicaceae as larval host plants. Papilio glaucus canadensis survives and grows well on aspen, whereas Papilio glaucus glaucus does not. In earlier studies we isolated a crude fraction of aspen compounds that exhibited activity against P. g. glaucus and identified the components as a suite of four phenolic glycosides (salicin, salicortin, tremuloidin, and tremulacin). This study was designed to identify the specific phenolic glycosides, or interactions among glycosides, responsible for the differential abilities of Papilio subspecies to utilize quaking aspen. We bioassayed the glycosides individually and in combination against both Papilio subspecies, using neonate survival trials and fourth—instar feeding trials. None of the compounds or combinations of compounds negatively affected the survival, growth, consumption rates, or digestibility/conversion efficiencies of P. g. canadensis, or 72—h survival rates of P. g glaucus. Salicortin and tremulacin significantly increased fourth—instar duration and decreased growth rates for P. g. glaucus, primarily by reducing consumption rates. Salicin and tremuloidin showed no negative effects. Combinations of glycosides containing salicortin and tremulacin decreased larval survival and a dramatically lowered growth rates by decreasing both consumption rates and food conversion efficiencies. Observations of treated larvae indicated that these glycosides may have caused gut lesions. The active component of salicortin and tremulacin is a cyclohexeone saligenin ester, and its activity is synergized in tremulacin by the presence of a benzoyl ester on the same molecule. We propose that differences in the susceptibilities of P. g. canadensis and P. g. glacus to the active phenolic glycosides are due to differences in activity of their carboxylesterase detoxication systems.

Differences in Effects of Pyrrolizidine Alkaloids on Five Generalist Insect Herbivore Species

“…Another explanation for the diversity of plant secondary metabolites could be that related compounds act synergistically (Adams and Bernays, 1978;Lindroth et al, 1988;Berenbaum et al, 1991). However, we did not find any evidence for synergistic effects of PAs on survival of the thrips or aphids.…”

“…If the production of less effective compounds is costly, there would be selection against such compounds, although compounds that are earlier in the biosynthetic pathway can remain in the plant in small quantities as necessary precursors. Additionally, related compounds can act synergistically on herbivores (Adams and Bernays, 1978;Lindroth et al, 1988;Berenbaum et al, 1991). Furthermore, the diversity can be maintained through selection by several different herbivores and/or pathogens (Simms, 1990;Mithen et al, 1995;Juenger and Bergelson, 1998).…”

“…Although there are a few examples of differential toxic effects of structurally related compounds on specialist insect herbivores (Berenbaum et al, 1986(Berenbaum et al, , 1989Bowers and Puttick, 1988), other studies have shown that related compounds do not differ in their effects on specialist insects (Lindroth et al, 1988;Johnson et al, 1996, Macel et al, 2002. Agrawal (2000) found that induction of a diversity of glucosinolates in Lepidium virginium had no effect on a specialist but decreased feeding by a generalist herbivore.…”

Variation in Lupinus arboreus alkaloid profiles and relationships with multiple herbivores

“…Defensive compounds are not equally deterrent to all herbivores (Berenbaum et al, 1986;Lindroth et al, 1988;Berenbaum et al, 1989;Stout and Bostock, 1999), and not all herbivores have equivalent effects on plant fitness (Marquis, 1992). While one or two herbivores might have the largest effects on plant fitness, most plants suffer from herbivores representing many different guilds, including leaf feeders, gallers, stem borers, or seed predators.…”

Using hybrid and backcross larvae of Papilio canadensis and Papilio glaucus to detect induced phytochemical resistance in hybrid poplar trees experimentally defoliated by gypsy moths

“…), we have observed well-adapted herbivores (e.g., Papilio canadensis and P. rutulus) with esterase detoxification systems (Lindroth et al, 1988;Scriber et al, 1991). Other very closely related congeneric species have low esterase activities and very poor abilities to survive on any Salicaceae species (e.g., P. glaucus, P. alexiares, and P. multicaudatus; Scriber et al, 1995;Scriber, 1996).…”