The Natural Enemies Hypothesis (i.e., introduced species experience release from their natural enemies) is a common explanation for why invasive species are so successful. We tested this hypothesis for Ammophila arenaria (Poaceae: European beachgrass), an aggressive plant invading the coastal dunes of California, USA, by comparing the demographic effects of belowground pathogens on A. arenaria in its introduced range to those reported in its native range. European research on A. arenaria in its native range has established that soil-borne pathogens, primarily nematodes and fungi, reduce A. arenaria's growth. In a greenhouse experiment designed to parallel European studies, seeds and 2-wk-old seedlings were planted in sterilized and nonsterilized soil collected from the A. arenaria root zone in its introduced range of California. We assessed the effects of pathogens via soil sterilization on three early performance traits: seed germination, seedling survival, and plant growth. We found that seed germination was reduced by 12-16% in nonsterilized soil compared with sterilized soil; similarly, seedling survival was reduced by 7-13%. Both root and shoot biomass decreased in the nonsterilized soil treatments compared with sterilized soil, by as much as 81% after 6 wk of growth. A comparison of the introduced and native ranges failed to show a demographic release from natural enemies; biomass effects of pathogens after 6 and 12 wk of growth were nearly equal between studies in California and The Netherlands. Identification of pathogens and inoculation experiments with fungi from the nonsterilized soil revealed several common fungal pathogens, whereas virtually no pathogenic nematodes were found. Therefore, we found a partial escape from enemies (i.e., pathogenic nematodes were absent in the introduced range), although there was no demographic release. These findings suggest that to fully understand the success and impact of A. arenaria in North America, one must look beyond escape from natural enemies.
Summary 1.Pathogen spillover occurs when disease levels for a given population are driven by transmission from a reservoir species that carries a high pathogen load. Pathogen spillover is widely documented in crop systems, but has been little studied in natural plant communities. 2. The abundant seed production of weedy species may create a scenario where spillover of a generalist seed pathogen onto less abundant seeds of native hosts is possible. The invasive annual weed cheatgrass (Bromus tectorum) is a potential reservoir species for Pyrenophora semeniperda, a multiple-host fungal seed pathogen that naturally occurs in the semi-arid western United States. 3. To investigate potential community-level consequences of spillover by this pathogen in plant communities invaded by cheatgrass, we first used artificial inoculation studies to determine the relative susceptibility of seeds of cheatgrass and five co-occurring native grasses to P. semeniperda. Secondly, we quantified the pathogen reservoir (density of pathogen-killed seeds) in the spring seed bank for cheatgrass monoculture, cheatgrass-invaded native grass, and uninvaded native grass patches. Thirdly, potential pathogen spillover onto co-occurring native grasses was quantified by planting native grass seeds into field-collected seed-zone samples from each vegetation patch type and scoring subsequent seed mortality. 4. All species tested were susceptible to infection by P. semeniperda, but their vulnerability to seed death varied as a function of germination time and degree of susceptibility. 5. Seed bank samples from cheatgrass-dominated patches contained seed densities over four times higher than samples from uninvaded native grass patches, and P. semeniperda-killed seeds were also present at much higher densities, indicating that cheatgrass can function as a reservoir for P. semeniperda. Native seeds planted into seed-zone samples from cheatgrass-dominated patches were more likely to be killed by P. semeniperda than those planted into samples from uninvaded native patches. Seed mortality also varied across years, sites and host species. 6. Synthesis. Pathogen spillover onto native seeds is likely to operate within seed banks of semi-arid communities invaded by cheatgrass, and perhaps other weeds, and may have broad consequences for community structure. Our findings also demonstrate the ecological significance of multiple-host pathosystems that operate at the seed stage.
Given the dramatic levels of seed death and the ability of this pathogen to reduce seed carry-over, it is intriguing to consider whether P. semeniperda could be used to control B. tectorum through direct reduction of its seed bank.
Cheatgrass (Bromus tectorum L., Poaceae), an introduced winter annual, has invaded a variety of habitats in western North America. This study examines variation in cheatgrass germination response and after-ripening patterns that are related to differences in habitat and to yearly differences in weather conditions during seed maturation. Seeds collected from five contrasting populations in 1992 and 1993 were subjected to controlled dry storage and then incubated across a range of temperatures. Recently harvested seeds were dormant and germinated slowly, while fully after-ripened seeds were nondormant and germinated rapidly. The optimal incubation temperature for mean germination time shifted from 5:15 to 20:30 °C as a result of after-ripening. Between-population differences in germination response appear to be related to the potential risk of precocious summer germination. The results from this 2-year study suggest that the more extreme yet predictable environments select for seed germination and after-ripening patterns that are genetically fixed, while populations from more favorable environments tended to show more between-year variations, suggesting more phenotypic plasticity. Germination percentage showed greater between-year variation than mean germination time. Between-year differences could not be explained simply by differences in maximum temperature or total precipitation during maturation. Adaptive germination responses in cheatgrass populations from contrasting habitats may have both genetic and environmental components, thus explaining why this species can become established in such a variety of habitats. Keywords: after-ripening, invading species, dormancy, mean germination time, cheatgrass, downy brome.
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