The dominant woody plant in the coastal prairie habitat at the Bodega Marine Lab (BMR) is the nitrogen-fixing bush lupine (Lupinus arboreus). Die-backs of large patches of bush lupine have been linked to herbivory by root-feeding larvae of the ghost moth Hepialus californicus. At low densities, these larvae depress lupine growth, seed set, and slightly increase mortality (Maron 1998); at high densities, they dramatically reduce lupine survival (Strong et al. 1995). Bush lupines, ghost moths, and the primary predator of ghost moth larvae at BMR, the entomopathogenic nematode (EPN) Heterorhabditis marelatus, (“nematode”) are native.
Entomopathogenic nematodes are widespread, important natural enemies of insects in soil and litter (Hominick 2002). Adults, reproduction, and feeding are restricted to the interior of insect hosts. The non-feeding "infective juveniles," (IJs) or third-instar, dauer larvae are the dispersing propagules of EPNs. Species in the family Heterorhabditidae are hermaphroditic, and a single IJ often kills the host. IJs enter a host through a spiracle or other orifice, and then regurgitate a mutualistic bacterium that quickly kills the host. The nematodes feed and reproduce for multiple generations inside the cadaver; after the resources of the host cadaver are depleted, the resulting IJs emerge into the soil en masse and disperse in search of hosts (Gaugler 2002).
Heterorhabditis marelatus' distribution is patchy on the BMR landscape; they are often abundant in one location but absent from areas 5–10 m away. This patchy distribution is similar to that found in the few other EPNs that have been studied in nature (Stuart and Gaugler 1994). In a field experiment with lupine seedlings, seedling mortality increased with increasing ghost moth density; however, even low nematode densities prevented plant death over a wide range of realistic herbivore densities (Strong et al. 1999). Presence of the nematode similarly halved densities of large larvae in mature bush lupine, increasing trunk growth and seed set within a single growing season by 44% and 67%, respectively (Preisser 2003). Although H. marelatus may have hosts other than ghost moth larvae, field surveys over nearly ten years have found no other nematode-killed organisms at BMR (D. Strong, unpublished data).
The interactions between H. marelatus, ghost moth larvae, and the bush lupine occur in the context of a Mediterranean-type climate characterized by large seasonal changes in rainfall (Barbour et al. 1973). Virtually all rain occurs during the winter (November–March); only 5.3% of the total recorded rainfall at BMR between 1969–2002 fell during May through September (data courtesy of BMR archives). Ghost moths are univoltine, mate during the winter, and lay eggs on or around lupine bushes. The larvae burrow into lupine roots, feed and grow through the dry summer season, pupate, and emerge as adults in the middle of the next wet season.
Ghost moth larvae are most vulnerable to nematode predation in wet, winter soil because H. marelatus travels through the thin film of water surrounding soil particles. Dry conditions prevent them from moving or finding prey (Grant and Villani 2003). As a result, nematode cohorts produced by hosts at the end of the wet season must persist until the following wet season, when the next generation of ghost moth larvae appears. Although H. marelatus can survive short dry periods in the relatively moist core of soil aggregates (D. Strong, unpublished data), Heterorhabditid nematodes cannot tolerate extended drying (Liu and Glazer 2000). Other studies have found that Heterorhabditid infective juveniles are often extremely desiccation-intolerant (reviewed in Glazer 2002); even populations from relatively dry regions were capable of entering only a shallow anyhdrobiotic state rather than a true ‘resting phase’ (Liu and Glazer 2000). Above-average summer soil moisture following wet El Niño – Southern Oscillation (ENSO) winters was correlated with increased persistence of H. marelatus under lupines, decreased herbivore density, and increased lupine growth and seed set. Additionally, the two years during and immediately prior to each of the large-scale lupine die-backs at BMR linked to ghost moth herbivory were significantly drier than average (Preisser and Strong 2004).
LITERATURE CITED
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