CONSERVATION OF PHEROMONE CHEMISTRY WITHIN THE CERAMBYCIDAE ON A GLOBAL SCALE , AND IMPLICATIONS FOR INVASION BIOLOGY

Beetles in the large family Cerambycidae are important pests worldwide because the larvae of most species bore within the woody tissues of trees and shrubs, as well as products constructed of wood. The endophytic lifestyle of these species results in their being readily and broadly transported in wood and wooden products by international commerce. Moreover, the polyphagous nature of the larvae of many species assures that host plants will be available in natural and managed habitats where they have been newly introduced. For these reasons, cerambycids are among the most important exotic species intercepted in international quarantine, and some species have proven to be devastating pests as exotic and invasive species, such as the Asian longhorned beetle, Anoplophora glabripennis (Motschulsky), and Aromia bungii (Faldermann). Federal regulatory agencies have long been limited in the methods available to them for blocking the introduction and establishment of exotic cerambycids, due primarily to the great numbers of insects that are brought into the country, the difficulty of detecting infestations, and the lack of efficient methods of monitoring for the adult beetles. In particular, scant information about the chemical ecology of cerambycids has hindered the development of sensitive methods of quarantine monitoring. For example, as of 14 years ago, pheromones had been identified for only five species of cerambycids, of the ~35,000 described species. Since that time, however, much has been learned about the volatile pheromones of cerambycids, with pheromone components at least tentatively identified for nearly 300 species worldwide. One important outcome of these recent advances in pheromone research is the discovery that the pheromone chemistry of more closely related cerambycid species (i.e., in the same subfamily, or in some cases, tribes) is often highly conserved. Research to date suggests that pheromone chemistry breaks out along subfamily lines. That is, a common pheromone component of species in the subfamily Cerambycinae is (R)-3-hydroxyhexan-2-one, its chain-length analogs, and the related 2,3-alkanediols. The compound 2-(undecyloxy)ethanol is now known to serve as the likely pheromone for many species of Monochamus, the timber beetles, of the subfamily Lamiinae native to both the Old and New Worlds. Similarly, (E)-6,10-dimethylundeca-5,9-dien2-ol (known as fuscumol) is a pheromone of a number of species in the subfamily Spondylidinae native to Europe and North America. The same compound and its acetate have been identified as pheromones of species in some tribes of the Lamiinae in both North and South America. All of the pheromones described above are produced by males and attract both sexes, and thus are considered aggregation-sex pheromones. However, it appears that pheromones of species in the subfamilies Prioninae and Lepturinae are produced by females and attract only males. Consistent with the global conservation of pheromone chemistry, many species of prionines native to Asia, Europe, and North America are now known to use as a pheromone the same chemical, 3,5dimethyldodecanoic acid, known as prionic acid. Sympatric species of cerambycids may share dominant pheromone components, or even have pheromones of identical composition. Likewise, species native to different continents may have similar or identical pheromones, despite their having been isolated from one another for many thousands of years. As a result of this global similarity in pheromone composition, traps baited with a compound that is a common pheromone component will capture a multitude of species over the course of the season in any particular part of the world, and unique complexes of species in different parts of the world. Our research with collaborators in Asia, Europe, Africa, Australia, and South America has confirmed that traps baited with the common pheromones attract a diversity of native species in field screening bioassays. In fact, such screening studies have confirmed attraction of species in every part of the world where they have been tested. This, despite the fact that only tiny fractions of the various continents have been sampled to date, in each case less than 0.0001% of the land mass. The positive results from such preliminary field studies suggest that a huge number of species could be attracted on a global scale, testifying to the ubiquity of these chemicals as pheromones. It is important to note, however, that there is growing evidence that certain species of cerambycines and lamiines have pheromones of very different chemistry, which may be shared among few species, or may even be species specific. Detailed study of the pheromone chemistry of sympatric species native to the eastern USA, including multiple species in the subfamilies Cerambycinae and Lamiinae, has demonstrated that unproductive interspecific attraction may be averted by variation among species in seasonal and/or daily flight period, or by the action of minor pheromone components that serve to antagonize attraction of heterospecifics, while synergizing attraction of conspecifics. These mechanisms that serve to prevent interspecific attraction obviously are a product of coevolution, and the community represents a tightly coevolved system in which each species occupies a unique pheromone “niche” based on phenology and pheromone chemistry. Among the cerambycines native to our most common study area, east-central Illinois, about half of the estimated 40 species have pheromones of the hydroxyketone/alkanediol class. This complex of species, segregated by seasonal and/or diel activity period, or by minor pheromone component, may represent a substantial barrier to the introduction of exotic species that use the same compounds as pheromones. That is, the sharing of pheromone components among cerambycid species around the world has profound implications for the establishment and invasion by exotic species. It is important to note that colonies of newly introduced species are founded by quite small numbers of individuals. Specifically, infested materials that have been transported into a new region will yield few adult beetles when compared to population densities of native species in the area, the adults likely will not emerge synchronously, and will disperse to find hosts after emerging. Adults of the exotic species will encounter the native community with which it has not coevolved, and therefore may experience conflict with native species with which it overlaps in pheromone chemistry and phenology. In this scenario, signals from calling males of the exotic species will be obscured by the signals of much more abundant males of the native species, and the miniscule population of exotics will go extinct. We hypothesize that this type of interference in the pheromone communication of the exotic species will strongly enhance Allee effects. By this reasoning, the probability of an exotic species establishing in the eastern USA will be strongly influenced by its pheromone chemistry. An example is the cerambycine Xylotrechus atronotatus Pic, native to Asia, with a pheromone comprised solely of the very common (R)-3hydroxyhexan-2-one. Establishment of this species in the eastern USA is likely to be strongly hindered by the great number of native species that produce the same chemical as their dominant or sole pheromone component, hence creating a natural form of mating disruption of the exotic species. In contrast, establishment of the Asian cerambycine species Trichoferus campestris (Faldermann) may have been favored by its having a pheromone chemistry that is unusual in North America. Males of this species produce the aromatic compound (2R,4R)-2-hydroxy-4methyl-1-phenylhexan-2-one. Trapping studies conducted in Utah, Illinois, Ohio, New York, and Pennsylvania have demonstrated that no native species are attracted by this compound, providing strong evidence that this chemical is not used as a pheromone by any of our native species. Thus, adults of T. campestris apparently have a unique pheromone channel which is not subject to interference from any native species, and even at very low population densities the adults can find one another and mate, unhindered by the native cerambycid community. The result is that North America represents “pheromone free space” for this species, and a few introduced adults will be enough for successful invasion and establishment. The pheromone free space hypothesis also may account for the facility with which Asian longhorned beetle has colonized North America, with apparently independent introductions resulting in established populations in New York, New Jersey, Illinois, Ohio, and Massachusetts, as well as Toronto, Canada. The pheromone of this species has yet to be fully characterized, but two likely components are 4-(heptyloxy)butanol and its corresponding aldehyde, 4(heptyloxy)butanal. Extensive trapping studies conducted in various areas of the eastern USA have shown that no native species are attracted by these compounds, suggesting that establishment of A. glabripennis also has been favored by its having a pheromone that is unique