High mortality, fluctuation in numbers, and heavy subterranean insect herbivory in bush lupine, Lupinus arboreus

Abstract

Sporadic patchy die-off of bush lupine, Lupinus arboreus, has long been known. We describe in detail a series of these incidents on the central California coast, based upon observational and comparative evidence. Stands of thousands of plants die, while nearby mature plants live on. In some sites, repeated die-off followed by regeneration from the seed bank has led to the cover and density of this woody, perennial plant fluctuating widely over the 40 year period for which records exist. Root damage by caterpillars of the ghost moth or "swift" Hepialus californicus (Lepidoptera, Hepialidae) is a major cause of individual bush death and a probable cause of die-off of stands of lupine. Hidden from view underground, a few of these insects readily kill a juvenile or young mature plant by girdling and reaming-out roots. The mass mortality of L. arboreus that we observed involved heavy root damage by these caterpillars in evenaged stands of plants in their first (1.5-year-old) or second (2.5-year-old) flowering season. The injured plants set seed before dying. Older, larger bush lupines better withstood root damage. In plants aged 3 or more years, damage and mortality were correlated with the intensity of ghost moth caterpillars in the roots. At the highest intensity (mean = 37.5, maximum = 62 caterpillars/root), a stand of large, old L. arboreus suffered 41% mortality; 45% of root cambium (median value) was destroyed by feeding caterpillars. Mass death of mature L. arboreus was not correlated with folivory, and leaf damage ranged from nil to moderate in instances of die-off. The western tussock moth, Orgyia vetusta, accounted for the highest levels of folivory, but this insect was rare when die-offs occurred. The lowest lupine mortality rates in our study occurred where tussock caterpillar intensities were high and where plants were repeatedly defoliated by this insect. However, experimental defoliation by high, but realistic, intensities of tussock moth caterpillars resulted in some mortality of mature bushes, and the combined effects of leaf and root herbivory have yet to be assessed. In its natural range on the California coast, bush lupine has several additional species of insect herbivores that can be locally abundant and injurious to the plant, although none is associated with die-off. Subterranean natural enemies of ghost moth caterpillars may play a role in the patchy waxing and waning of this shrub. Locally, a new species of entomophagous nematode (Heterorhabditis sp.) cause high mortality in the soil, before ghost moth caterpillars have entered the root. This natural enemy may thus afford lupines protection from heavy underground herbivory.

Variation in Lupinus arboreus alkaloid profiles and relationships with multiple herbivores

“…Bayshore (BS) and Mussel Point (MP) are grassland sites. At Bayshore, cover and persistence of bush lupine is highly variable, with average lupine cover fluctuating from 0 to 60% over 10-year periods (Strong et al, 1995). Fluctuations in cover may be caused by high rates of herbivore damage; stands with little fluctuation in lupine cover had the fewest Hepialus caterpillars per root (Strong et al, 1995;Maron, 1998;.…”

“…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. The role of defensive compounds against leaf feeding herbivores has received the most attention (Rosenthal and Berenbaum, 1991), although guilds of herbivores such as root borers (Brown, 1988;Strong et al, 1995;Maron, 1998), seed predators (Louda and Potvin, 1995) and apical meristem feeders (Juenger and Bergelson, 1997) may also have strong fitness effects. For example, Strong et al (1995) found a positive correlation between the number of root boring Hepialus californicus larvae and the rate of lupine mortality, and decreases of H. californicus densities by half led to a 44% increase in lupine seed set (Preisser, 2003).…”

“…The population of L. arboreus at our study site experiences spatial and temporal variability in herbivory and damage to individual plants and among lupine stands can vary dramatically. For example, in some years lupines at some sites are almost completely defoliated by tussock moth caterpillars (Orgyia vetusta) while lupines in other sites support few caterpillars and sustain little to no damage Strong et al, 1995). L. arboreus may evolve resistance to herbivory due to the high risk of mortality and female fitness reduction due to damage on flowers, fruit and seeds (Davison and Barbour, 1977;Strong et al, 1995;Maron and Simms, 1997;Maron, 1998;Strong et al, 1999).…”

“…For example, in some years lupines at some sites are almost completely defoliated by tussock moth caterpillars (Orgyia vetusta) while lupines in other sites support few caterpillars and sustain little to no damage Strong et al, 1995). L. arboreus may evolve resistance to herbivory due to the high risk of mortality and female fitness reduction due to damage on flowers, fruit and seeds (Davison and Barbour, 1977;Strong et al, 1995;Maron and Simms, 1997;Maron, 1998;Strong et al, 1999). However, many different types of herbivores feed on L. arboreus, including insect guilds that feed on roots, leaves, flowers and seeds, as well as mammals such as deer, voles, mice and gophers (Maron and Simms, 1997;Maron, 2001).…”

Fine-Scale Genetically Based Differentiation of Life-History Traits in the Perennial Shrub Lupinus Arboreus

“…In grasslands, lupine populations often fluctuate dramatically. In some grassland sites, lupine populations oscillate from Ͻ5% to 75% cover (Strong et al 1995;pers. obs.).…”