Range-Expanding Populations of a Globally Introduced Weed Experience Negative Plant-Soil Feedbacks

BACKGROUND: Biological invasions are fundamentally biogeographic processes that occur over large spatial scales. Interactions with soil microbes can have strong impacts on plant invasions, but how these interactions vary among areas where introduced species are highly invasive vs. naturalized is still unknown. In this study, we examined biogeographic variation in plant-soil microbe interactions of a globally invasive weed, Centaurea solstitialis (yellow starthistle). We addressed the following questions (1) Is Centaurea released from natural enemy pressure from soil microbes in introduced regions? and (2) Is variation in plant-soil feedbacks associated with variation in Centaurea's invasive success? METHODOLOGY/PRINCIPAL FINDINGS: We conducted greenhouse experiments using soils and seeds collected from native Eurasian populations and introduced populations spanning North and South America where Centaurea is highly invasive and noninvasive. Soil microbes had pervasive negative effects in all regions, although the magnitude of their effect varied among regions. These patterns were not unequivocally congruent with the enemy release hypothesis. Surprisingly, we also found that Centaurea generated strong negative feedbacks in regions where it is the most invasive, while it generated neutral plant-soil feedbacks where it is noninvasive. CONCLUSIONS/SIGNIFICANCE: Recent studies have found reduced below-ground enemy attack and more positive plant-soil feedbacks in range-expanding plant populations, but we found increased negative effects of soil microbes in range-expanding Centaurea populations. While such negative feedbacks may limit the long-term persistence of invasive plants, such feedbacks may also contribute to the success of invasions, either by having disproportionately negative impacts on competing species, or by yielding relatively better growth in uncolonized areas that would encourage lateral spread. Enemy release from soil-borne pathogens is not sufficient to explain the success of this weed in such different regions. The biogeographic variation in soil-microbe effects indicates that different mechanisms may operate on this species in different regions, thus establishing geographic mosaics of species interactions that contribute to variation in invasion success

Geographic mosaics of plant-soil microbe interactions in a global plant invasion

Aim Our aim in this study was to document the global biogeographic variation in the effects of soil microbes on the growth of Centaurea solstitialis (yellow starthistle; Asteraceae), a species that has been introduced throughout the world, but has become highly invasive only in some introduced regions. Location To assess biogeographic variation in plant-soil microbe interactions, we collected seeds and soils from native Eurasian C. solstitialis populations and introduced populations in California, Argentina and Chile. Methods To test whether escape from soil-borne natural enemies may contribute to the success of C. solstitialis, we compared the performance of plants using seeds and soils collected from each of the biogeographic regions in greenhouse inoculation/sterilization experiments. Results We found that soil microbes had pervasive negative effects on plants from all regions, but these negative effects were significantly weaker in soils from non-native ranges in Chile and California than in those from the non-native range in Argentina and the native range in Eurasia. Main conclusions The biogeographic differences in negative effects of microbes in this study conformed to the enemy-release hypothesis (ERH) overall, but the strong negative effect of soil biota in Argentina, where C. solstitialis is invasive, and weaker effects in Chile where it is not, indicated that different factors influencing invasion are likely to occur in large scale biogeographic mosaics of interaction strengths.Fil: Andonian, Krikor. University of California; Estados UnidosFil: Hierro, Jose Luis. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Ciencias de la Tierra y Ambientales de La Pampa. Universidad Nacional de La Pampa. Facultad de Ciencias Exactas y Naturales. Instituto de Ciencias de la Tierra y Ambientales de La Pampa; ArgentinaFil: Khetsuriani, Liana. Institute of Botany of the Georgian Academy of Sciences; Estados UnidosFil: Becerra, Pablo I.. Universidad Católica de Chile; ChileFil: Janoyan, Grigor. American University of Armenia; ArmeniaFil: Villareal, Diego. Universidad Nacional de La Pampa. Facultad de Ciencias Exactas y Naturales; ArgentinaFil: Cavieres, Lohengrin A.. Universidad de Concepción; ChileFil: Fox, Laurel R.. University of California; Estados UnidosFil: Callaway, Ragan M.. University of Montana; Estados Unido