Giles C. Thelen

Soil biota and exotic plant invasion

Invasive plants are an economic problem and a threat to the conservation of natural systems. Escape from natural enemies might contribute to successful invasion, with most work emphasizing the role of insect herbivores; however, microbial pathogens are attracting increased attention. Soil biota in some invaded ecosystems may promote ‘exotic’ invasion, and plant–soil feedback processes are also important. Thus, relatively rare species native to North America consistently demonstrate negative feedbacks with soil microbes that promote biological diversity, whereas abundant exotic and native species demonstrate positive feedbacks that reduce biological diversity. Here we report that soil microbes from the home range of the invasive exotic plant Centaurea maculosa L. have stronger inhibitory effects on its growth than soil microbes from where the weed has invaded in North America. Centaurea and soil microbes participate in different plant–soil feedback processes at home compared with outside Centaureas home range. In native European soils, Centaurea cultivates soil biota with increasingly negative effects on the weeds growth, possibly leading to its control. But in soils from North America, Centaurea cultivates soil biota with increasingly positive effects on itself, which may contribute to the success of this exotic species in North America.

Invasive Plant Suppresses the Growth of Native Tree Seedlings by Disrupting Belowground Mutualisms

The impact of exotic species on native organisms is widely acknowledged, but poorly understood. Very few studies have empirically investigated how invading plants may alter delicate ecological interactions among resident species in the invaded range. We present novel evidence that antifungal phytochemistry of the invasive plant, Alliaria petiolata, a European invader of North American forests, suppresses native plant growth by disrupting mutualistic associations between native canopy tree seedlings and belowground arbuscular mycorrhizal fungi. Our results elucidate an indirect mechanism by which invasive plants can impact native flora, and may help explain how this plant successfully invades relatively undisturbed forest habitat.

NOVEL WEAPONS: INVASIVE PLANT SUPPRESSES FUNGAL MUTUALISTS IN AMERICA BUT NOT IN ITS NATIVE EUROPE

Why some invasive plant species transmogrify from weak competitors at home to strong competitors abroad remains one of the most elusive questions in ecology. Some evidence suggests that disproportionately high densities of some invaders are due to the release of biochemicals that are novel, and therefore harmful, to naive organisms in their new range. So far, such evidence has been restricted to the direct phytotoxic effects of plants on other plants. Here we found that one of North Americas most aggressive invaders of undisturbed forest understories, Alliaria petiolata (garlic mustard) and a plant that inhibits mycorrhizal fungal mutualists of North American native plants, has far stronger inhibitory effects on mycorrhizas in invaded North American soils than on mycorrhizas in European soils where A. petiolata is native. This antifungal effect appears to be due to specific flavonoid fractions in A. petiolata extracts. Furthermore, we found that suppression of North American mycorrhizal fungi by A. petiolata corresponds with severe inhibition of North American plant species that rely on these fungi, whereas congeneric European plants are weakly affected. These results indicate that phytochemicals, benign to resistant mycorrhizal symbionts in the home range, may be lethal to naïve native mutualists in the introduced range and indirectly suppress the plants that rely on them.

SOIL FUNGI ALTER INTERACTIONS BETWEEN THE INVADER CENTAUREA MACULOSA AND NORTH AMERICAN NATIVES

Soil microbes may affect the way exotic invasive plants interact with native neighbors. We investigated the effects of soil fungi on interactions between the invasive weed Centaurea maculosa (spotted knapweed) and six species native to the intermountain prairies of the northwestern United States. We also compared the effect of C. maculosa on the composition of the soil microbial community to that of the native species. In the field, fungicide (Benomyl) reduced AM mycorrhizal colonization of C. maculosa roots by >80%. Fungicide did not significantly reduce non-AM fungi. When grown alone, the biomass of C. maculosa was not affected by the fungicide application. However, depending on the combination of native competitor and fungicide, C. maculosa biomass varied from 10-fold decreases to 1.9-fold increases. In untreated soils, C. maculosa grew larger in the presence of Festuca idahoensis or Koeleria cristata than when alone. When fungicide was applied these positive effects of Festuca and Koeleria on C. maculosa did not occur. A third native grass, Pseudoroegneria spicata, had much stronger competitive effects on C. maculosa than Festuca or Koeleria, and fungicide reduced the competitive effects of Pseudoroegneria. Fungicide increased Centaurea biomass when competing with the forb Gallardia aristata. However, fungicide did not affect the way two other forbs; Achillea millefolium and Linum lewisii, interacted with C. maculosa. Rhizosphere microbial communities in the root zones of the three native bunchgrass species differed from that of C. maculosa. However, despite the strong effects of soil fungi in field interactions and differences in microbial community composition, soil biota from different plant rhizospheres did not affect the growth of C. maculosa in the absence of native competitors in greenhouse experiments. Our results suggest that successful invasions by exotic plant species can be affected by complex and often beneficial effects of local soil microbial communities. These effects were not manifest as simple direct effects, but become apparent only when native plants, invasive plants, and soil microbial communities were interacting at the same time.

Novel weapons and invasion: biogeographic differences in the competitive effects of Centaurea maculosa and its root exudate (±)-catechin

Recent studies suggest that the invasive success of Centaurea maculosa may be related to its stronger allelopathic effects on native North American species than on related European species, one component of the “novel weapons” hypothesis. Other research indicates that C. maculosa plants from the invasive range in North America have evolved to be larger and better competitors than conspecifics from the native range in Europe, a component of the “evolution of increased competitive ability” hypothesis. These hypotheses are not mutually exclusive, but this evidence sets the stage for comparing the relative importance of evolved competitive ability to inherent competitive traits. In a competition experiment with a large number of C. maculosa populations, we found no difference in the competitive effects of C. maculosa plants from North America and Europe on other species. However, both North American and European C. maculosa were much better competitors against plants native to North America than congeners native to Romania, collected in areas where C. maculosa is also native. These results are consistent with the novel weapons hypothesis. But, in a second experiment using just one population from North America and Europe, and where North American and European species were collected from a broader range of sites, competitive interactions were weaker overall, and the competitive effects of C. maculosa were slightly stronger against European species than against North American species. Also consistent with the novel weapons hypothesis, (±)-catechin had stronger effects on native North American species than on native European species in two experiments. Our results suggest that the regional composition of the plant communities being invaded by C. maculosa may be more important for invasive success than the evolution of increased size and competitive ability.

Oxalate contributes to the resistance of Gaillardia grandiflora and Lupinus sericeus to a phytotoxin produced by Centaurea maculosa

Centaurea maculosa Lam. is a noxious weed in western North America that produces a phytotoxin, (±)-catechin, which is thought to contribute to its invasiveness. Areas invaded by C. maculosa often result in monocultures of the weed, however; in some areas, North American natives stand their ground against C. maculosa and show varying degrees of resistance to its phytotoxin. Two of these resistant native species, Lupinus sericeus Pursh and Gaillardiagrandiflora Van Houtte, were found to secrete increased amounts of oxalate in response to catechin exposure. Mechanistically, we found that oxalate works exogenously by blocking generation of reactive oxygen species in susceptible plants and reducing oxidative damage generated in response to catechin. Furthermore, field experiments show that L. sericeus indirectly facilitates native grasses in grasslands invaded by C. maculosa, and this facilitation can be correlated with the presence of oxalate in soil. Addition of exogenous oxalate to native grasses and Arabidopsis thaliana (L.) Heynh grown in vitro alleviated the phytotoxic effects of catechin, supporting the field experiments and suggesting that root-secreted oxalate may also act as a chemical facilitator for plant species that do not secrete the compound.

Impact of Acroptilon repens on co-occurring native plants is greater in the invader’s non-native range

Concern over exotic invasions is fueled in part by the observation that some exotic species appear to be more abundant and have stronger impacts on other species in their non-native ranges than in their native ranges. Past studies have addressed biogeographic differences in abundance, productivity, biomass, density and demography between plants in their native and non-native ranges, but despite widespread observations of biogeographic differences in impact these have been virtually untested. In a comparison of three sites in each range, we found that the abundance of Acroptilon repens in North America where it is invasive was almost twice that in Uzbekistan where it is native. However, this difference in abundance translated to far greater differences between regions in the apparent impacts of Acroptilon on native species. The biomass of native species in Acroptilon stands was 25–30 times lower in the non-native range than in the native range. Experimental addition of native species as seeds significantly increased the abundance of natives at one North American site, but the proportion of native biomass even with seed addition remained over an order of magnitude lower than that of native species in Acroptilon stands in Uzbekistan. Experimental disturbance had no long-term effect on Acroptilon abundance or impact in North America, but Acroptilon increased slightly in abundance after disturbance in Uzbekistan. In a long-term experiment in Uzbekistan, suppression of invertebrate herbivores and pathogens did not result in either consistent increases in Acroptilon biomass across years or declines in the biomass of other native species, as one might expect if the low impact of Acroptilon in the native range was due to its strong top–down regulation by natural enemies. Our local scale measurements do not represent all patterns of Acroptilon distribution and abundance that might exist at the scale of landscapes in either range, but they do suggest the possibility of fundamental biogeographic differences in the way a highly successful invader interacts with other species, differences that are not simply related to greater biomass or reduced top–down regulation of the invader in its non-native range.

Is there a risk to living large? Large size correlates with reduced growth when stressed for knapweed populations

A central hypothesis in ecology is that plant life history evolution is constrained by fundamental “compromises between the conflicting selection pressures resulting from particular combinations of competition, stress, and disturbance”, with stress being defined as abiotic conditions that restrict production. Biogeographic differences among native and non-native ranges of invasive plants may provide unique opportunities for tests of this theory. We conducted a greenhouse experiment with Centaurea stoebe plants from North American and European populations. We compared the total biomass and phenotypic plasticity indices for plants from the native and non-native ranges under stressed and non-stressed conditions. The average size of Centaurea stoebe plants from 13 North American populations was greater than that of plants from 18 European populations regardless of stress treatment. However, when plants from the same populations were exposed to lower resources the differences in biomass between plants from North American and European populations were significantly less, suggesting that large plants were poorer stress tolerators. For all 31 populations the regression slope for the relationship between mean mass for populations in non-stressful conditions and mean mass in stressful conditions was less than 1.0, indicating that populations that produced large plants in good conditions also produced plants that grew disproportionately less in stressful conditions. These findings suggest that Centaurea stoebe may be evolving towards being a good “competitor” (sensu Grime, 1977) in its invasive range, but at the cost of being a good “stress tolerator”.

Growth and competitive effects of Centaurea stoebe populations in response to simulated nitrogen deposition.

Increased resource availability can promote invasion by exotic plants, raising concerns over the potential effects of global increases in the deposition of nitrogen (N). It is poorly understood why increased N favors exotics over natives. Fast growth may be a general trait of good invaders and these species may have exceptional abilities to increase growth rates in response to N deposition. Additionally, invaders commonly displace locals, and thus may have inherently greater competitive abilities. The mean growth response of Centaurea stoebe to two N levels was significantly greater than that of North American (NA) species. Growth responses to N did not vary among C. stoebe populations or NA species. Without supplemental N, NA species were better competitors than C. stoebe, and C. stoebe populations varied in competitive effects. The competitive effects of C. stoebe populations increased with N whereas the competitive effects of NA species decreased, eliminating the overall competitive advantage demonstrated by NA species in soil without N added. These results suggest that simulated N deposition may enhance C. stoebe invasion through increasing its growth and relative competitive advantage, and also indicate the possibility of local adaptation in competitive effects across the introduced range of an invader.

Native Sod Rescue— A Viable Business Model (Montana)

A Texas, is a city known nationwide for its live music, environmental awareness, and high standard of living. Now the city can also boast an improved quality of life for its feathered and furred residents by becoming the thirtieth community to receive the National Wildlife Federation’s (NWF) Community Wildlife Habitat certification. It is the first Texas community, also the largest city and first state capitol in the country, to earn this special wildlife habitat designation. To date, over 113,000 individual habitats and 31 communities have been certified by the national environmental conservation organization. The desire to make Austin wildlife friendly stemmed from the fact that the region is one of the fastest growing metropolitan areas in the country. Austin’s current population of 774,000 is expected to reach over one million people by 2025 (Robinson 2009). The city wanted a plan to help wildlife and maintain the region’s biodiversity and unique ecosystems, and NWF’s Community Wildlife Habitat project gave the city a template to help meet several environmental conservation goals under one umbrella program. These goals include minimizing climate change, conserving water, enhancing the quality of wildlife habitat within the city, and improving air and water quality. In March 2007, Mayor Will Wynn and the City Council passed a resolution to obtain NWF certification and demonstrate the city’s long-term commitment to creating new wildlife habitat within the city by educating citizens and encouraging natural, native landscapes community-wide and on city-owned sites. Alpine, California, became the first-ever certified community in May 1998. The community-wide certification grew out of NWF’s Certified Wildlife Habitat program that began in 1973 as a way to help habitat enthusiasts turn their yards and other garden spaces into enticing wildlife refuges. To qualify, a site needs the basic elements that allow wildlife to flourish: food, water, cover, and places to raise young. Creating habitat is as simple as planting native plants that offer nectar, seeds, and berries year-round, including a reliable water source, and providing places for protection and rearing young such as evergreen shrubs or a birdhouse. Applicants must also practice sustainable gardening techniques, such as reducing or eliminating chemical fertilizers and pesticides, conserving water, planting native plants, removing invasive plants, harvesting rainwater, and composting. The Community Wildlife Habitat certification is based on a point system determined by population size. Points are acquired by completing habitat, education, and community project goals. Austin needed to accumulate 1,000 total points. The most challenging goal was habitat certification, which required that a minimum of 600 homes, six schools and ten businesses, places of worship, or other locations in Austin be certified through NWF’s Certified Wildlife Habitat program. When the city originally announced its plans to become a certified community, there were approximately 340 NWF-certified habitats in Austin, including 15 schools and 12 businesses, places of worship, and other common areas. A new Parks and Recreation Department program, Wildlife Austin, was created in February 2008 with a budget that included the salary of one staff person to lead the certification effort and approximately