How to better predict long-term benefits and risks in weed biocontrol: an evolutionary perspective.

Classical biological control (also called importation biological control) of weeds has a remarkable track record for efficiency and safety, but further improvement is still needed, particularly to account for potential evolutionary changes after release. Here, we discuss the increasing yet limited evidence of post-introduction evolution and describe approaches to predict evolutionary change. Recent advances include using experimental evolution studies over several generations that combine -omics tools with behavioral bioassays. This novel approach in weed biocontrol is well suited to explore the potential for rapid evolutionary change in real-time and thus can be used to estimate more accurately potential benefits and risks of agents before their importation. We outline this approach with a chrysomelid beetle used to control invasive common ragweed.

Evolving while invading: rapid adaptive evolution in juvenile development time for a biological control organism colonizing a high-elevation environment.

We report evidence of adaptive evolution in juvenile development time on a decadal timescale for the cinnabar moth Tyria jacobaeae (Lepidoptera: Arctiidae) colonizing new habitats and hosts from the Willamette Valley to the Coast Range and Cascades Mountains in Oregon. Four lines of evidence reveal shorter egg to pupa juvenile development times evolved in the mountains, where cooler temperatures shorten the growing season: (i) field observations showed that the mountain populations have shorter phenological development; (ii) a common garden experiment revealed genetic determination of phenotypic differences in juvenile development time between Willamette Valley and mountain populations correlated with the growing season; (iii) a laboratory experiment rearing offspring from parental crosses within and between Willamette Valley and Cascades populations demonstrated polygenic inheritance, high heritability, and genetic determination of phenotypic differences in development times; and (iv) statistical tests that exclude random processes (founder effect, genetic drift) in favor of natural selection as explanations for observed differences in phenology. These results support the hypothesis that rapid adaptation to the cooler mountain climate occurred in populations established from populations in the warmer valley climate. Our findings should motivate regulators to require evaluation of evolutionary potential of candidate biological control organisms prior to release.

The statistical analysis of insect phenology.

We introduce two simple methods for the statistical comparison of the temporal pattern of life-cycle events between two populations. The methods are based on a translation of stage-frequency data into individual 'times in stage'. For example, if the stage-k individuals in a set of samples consist of three individuals counted at time t(1) and two counted at time t(2), the observed times in stage k would be (t(1), t(1), t(1), t(2), t(2)). Times in stage then can be compared between two populations by performing stage-specific t-tests or by testing for equality of regression lines of time versus stage between the two populations. Simulations show that our methods perform at close to the nominal level, have good power against a range of alternatives, and have much better operating characteristics than a widely-used phenology model from the literature.

Effects of Vegetation Disturbances on Insect Biological Control of Tansy Ragwort, Senecio Jacobaea.

Our study had two major objectives: (1) to clarify the roles of buried seed and different types of localized disturbance in activating outbreaks of a pasture weed (tansy ragwort, Senecio jacobaea), and (2) to measure the effectiveness of two natural enemies (the cinnabar moth Tyria jacobaeae and a ragwort flea beetle, Longitarsus jacobaeae) in inhibiting weed population increase and spread. We conducted a 5-yr field experiment on the coast of Oregon using a randomized-block design with four blocks x three levels of disturbance (background vegetation was Tilled, Clipped, Unaltered) x two levels of cinnabar moth (Exposed, Protected) x two levels of flea beetle (Exposed, Protected) = 48 plots (each plot was 0.25 m^2). Disturbance consistently increased ragwort abundance (measured as density of juveniles, adults, and their offspring; cover; and biomass); the effect was generally greater in Tilled compared to Clipped disturbance treatments. We also found striking differences in the contribution of each natural enemy to ragwort control. The flea beetle quickly reduced ragwort survival, and this led to a strong and rapid reduction in ragwort abundance. The cinnabar moth reduced ragwort fecundity, but this did not translate into reductions in ragwort cover (measured in 1986 and 1987) or biomass (measured annually from 1986 through 1990). These results establish that (1) ragwort populations were limited more by availability of microsites for germination and establishment than by availability of seed, (2) the ragwort flea beetle was the key factor regulating ragwort abundance, and (3) reduction in ragwort fecundity by the cinnabar moth had little effect on the dynamics of ragwort populations on local scales of space and time. These findings underscore the value of field experiments for investigating the dynamics of biological control systems, the manner in which they are regulated, and their response to perturbation. They further establish how colonization and invasion by ragwort depend on attributes of the disturbance and of natural enemy regimes.

Wind Dispersal Distances in Dimorphic Achenes of Ragwort, Senecio Jacobaea.

A mark-recapture study of wind-dispersed achenes of Senecio jacobaeo conducted in western Oregon showed that the proportion of achenes dispersing a given distance varied significantly with changes in site (inland vs. coastal), surroundings (mown vs. unmown), height of release (0-50, 50-100, 100-150, 150-200 cm), time of release (early vs late in the season), direction of dispersal, and achene type (disk vs. ray achenes). Influences of height of release, direction, achene type, and time of release were strongly conditioned by site and surroundings. The majority of achenes dispersed very short distances. Of 53 301 achenes falling in the recapture area, 31% travelled only 1 m, 89% travelled 5 m or less, and none were collected > 14 m from the source. Thus, while it is theoretically possible for these wind-dispersed achenes to travel long distances, actual dispersal distances are short due to local conditions of humidity, wind, and vegetation structure.

Dormancy and dispersal in dimorphic achenes of tansy ragwort, Senecio jacobaea L. (Compositae).

Marginal and central florets of the capitula of tansy ragwort Senecio jacobaea yield different kinds of fruit. The central ("disk") achenes are lighter (x±SE=199±5µg), more numerous (x±SE=58±0.6 achenes per head), and are equipped with a pappus aiding wind transport and rows of trichomes aiding animal transport. The marginal ("ray") achenes are heavier (x±SE=286±7µg), less numerous (virtually invariant at 13 achenes per head), and lack dispersal structures. Whereas disk achenes are relased shortly after they mature, ray achenes are retained by the parent for a period of months following maturity.Germination at constant temperature (20°C) and with alternating light (12 h light: 12 h dark) demonstrated that disk and ray achenes exhibit different germination syndromes. Germination percentage increases linearly with achene fresh weight in both types; for a given weight, disk achenes have a higher germination percentage than ray achenes. Germination time decreases with increasing achene weight in disk achenes, but increases with achene weight in ray achenes.The germination percentages and germination times for disk and ray achenes diverge progressively with increasing achene weight. The divergence in behavior is a result of diverging patterns of dry matter allocation in the two achene types. Increase in the size of disk achenes favors the embryo fraction, thereby speeding germination while reducing protection. Increase in the size of the ray achenes favors the pericarp fraction, thereby increasing protection while delaying germination.Reduced germination percentage and germination speed of the ray achenes were shown by experimental manipulation to be caused by physical inhibition by their thicker pericarps.Dimorphism in ragwort likely speards germination out in space and time, thereby increasing the number of safe sites an individual parent can exploit in disseminating offspring. The syndrome in other heteromorphic composites resembles that of ragwort, generally combining reduced dispersal-delayed germination in the outer achenes and distance dispersal-quick germination in the central achenes. The outer achenes are generally less numerous and larger. Dispersal traits (large numbers, early release and light wieght) are the direct opposite of dormancy traits (small numbers, delayed release and heavier weight). Thus conflicts between the properties determining dormancy and dispersal appear to require separate dormancy and dispersal phenotypes.