Variation in herbivore-mediated indirect effects of an invasive plant on a native plant

Theory predicts that damage by a shared herbivore to a secondary host plant species may either be higher or lower in the vicinity of a preferred host plant species. To evaluate the importance of ecological factors, such as host plant proximity and density, in determining the direction and strength of such herbivore-mediated indirect effects, we quantified oviposition by the exotic weevil Rhinocyllus conicus on the native wavyleaf thistle Cirsium undulatum in midgrass prairie on loam soils in the upper Great Plains, USA. Over three years (2001-2003), the number of eggs laid by R. conicus on C. undulatum always decreased significantly with distance (0-220 m) from a musk thistle (Carduus nutans L.) patch. Neither the level of R. conicus oviposition on C. undulatum nor the strength of the distance effect was predicted by local musk thistle patch density or by local C. undulatum density (<5 m). The results suggest that high R. conicus egg loads on C. undulatum near musk thistle resulted from the native thistle's co-occurrence with the coevolved preferred exotic host plant and not from the weevil's response to local host plant density. Mean egg loads on C. undulatum also were greater at sites with higher R. conicus densities. We conclude that both preferred-plant proximity and shared herbivore density strongly affected the herbivore-mediated indirect interaction, suggesting that such interactions are important pathways by which invasive exotic weeds can indirectly impact native plants.     

Insect herbivory and propagule pressure influence Cirsium vulgare invasiveness across the landscape

A current challenge in ecology is to better understand the magnitude, variation, and interaction in the factors that limit the invasiveness of exotic species. We conducted a factorial experiment involving herbivore manipulation (insecticide-in-water vs. water-only control) and seven densities of introduced nonnative Cirsium vulgare (bull thistle) seed. The experiment was repeated with two seed cohorts at eight grassland sites uninvaded by C. vulgare in the central Great Plains, USA. Herbivory by native insects significantly reduced thistle seedling density, causing the largest reductions in density at the highest propagule inputs. The magnitude of this herbivore effect varied widely among sites and between cohort years. The combination of herbivory and lower propagule pressure increased the rate at which new C. vulgare populations failed to establish during the initial stages of invasion. This experiment demonstrates that the interaction between biotic resistance by native insects, propagule pressure, and spatiotemporal variation in their effects were crucial to the initial invasion by this Eurasian plant in the western tallgrass prairie.     

Potential Interference Between a Threatened Endemic Thistle and an Invasive Nonnative Plant

Although the establishment of nonnative plants is recognized as a threat to native ecosystems, there are few documented examples of an invasive species directly influencing a rare native plant. The Eurasian biennial Dipsacus sylvestris (teasel) is invading the central New Mexico habitat of Cirsium vinaceum , an endemic thistle that is federally listed as threatened. We documented changes in teasel distribution and abundance between 1989 and 1993 that suggest the potential for direct interactions with the native thistle. We then compared habitat characteristics, germination behavior, and performance in greenhouse and field competition trials to evaluate the potential outcome of interference between these two species. There were no significant differences in measured habitat characteristics between sites supporting C. vinaceum and those with D. sylvestris. Dipsacus was better able to germinate in low light than the thistle, suggesting that D. sylvestris might invade C. vinaceum populations but that thistle recruitment would be unlikely in dense stands of the nonnative plants. In the greenhouse growth of C. vinaceum rosettes was significantly reduced by the presence of Dipsacus , but the invader was unaffected by the thistle; results of a short-term field experiment were equivocal but suggestive of interference between the two. We suggest criteria for managers to use in determining whether invading species pose problems for specific rare native taxa, and we discuss the constraints on experimental work where protected taxa are involved.     

Seed availability and insect herbivory limit recruitment and adult density of native tall thistle

Understanding spatial and temporal variation in factors influencing plant regeneration is critical to predicting plant population growth. We experimentally evaluated seed limitation, insect herbivory, and their interaction in the regeneration and density of tall thistle (Cirsium altissimum) across a topographic ecosystem productivity gradient in tallgrass prairie over two years. On ridges and in valleys, we used a factorial experiment manipulating seed availability and insect herbivory to quantify effects of: seed input on seedling density, insect herbivory on juvenile density, and cumulative impacts of both seed input and herbivory on reproductive adult density. Seed addition increased seedling densities at three of five sites in 2006 and all five sites in 2007. Insect herbivory reduced seedling survival across all sites in both years, as well as rosette survival from the previous year's seedlings. In both years, insecticide treatment of seed addition plots led to greater adult tall thistle densities in the following year, reflecting the increase in juvenile thistle densities in the experimental year. Seedling survival was not density dependent. Our analytical projection model predicts a significant long-term increase in adult densities from seed input, with a greater increase under experimentally reduced insect herbivory. While plant community biomass and water stress varied significantly between ridges and valleys, the effects of seed addition and insect herbivory did not vary with gradient position. These results support conceptual models that predict seedling and adult densities of short-lived monocarpic perennial plants should be seed limited. Further, the experiment demonstrates that even at high juvenile plant densities, at which density dependence potentially could have overridden herbivore effects on plant survival, insect herbivory strongly affected juvenile thistle performance and adult densities of this native prairie species.     

Seed and establishment limitation contribute to long-term native forb declines in California grasslands

The effects of exotic species invasions on biodiversity vary with spatial scale, and documentation of local-scale changes in biodiversity following invasion is generally lacking. Coupling long-term observations of local community dynamics with experiments to determine the role played by exotic species in recruitment limitation of native species would inform both our understanding of exotic impacts on natives at local scales and regional-scale management efforts to promote native persistence. We used field experimentation to quantify propagule and establishment limitation in a suite of native annual forbs in a California reserve, and compared these findings to species abundance trends within the same sites over the past 48 years. Observations at 11 paired sites (inside and outside the reserve) indicated that exotic annual plants have continued to increase in abundance over the past 48 years. This trend suggests the system has not reached equilibrium > 250 years after exotic species began to spread, and 70 years after livestock grazing ceased within the reserve. Long-term monitoring observations also indicated that six native annual forb species went extinct from more local populations than were colonized. To determine the potential role of exotic species in these native plant declines, we added seed of these species into plots adjacent to monitoring sites where plant litter and live grass competition were removed. Experimental results suggest both propagule and establishment limitation have contributed to local declines observed for these native forbs. Recruitment was highest at sites that had current or historical occurrences of the seeded species, and in plots where litter was removed. Grazing history (i.e., location within or outside the reserve) interacted with exotic competition removal, such that removal of live grass competition increased recruitment in more recently grazed sites. Abundance of forbs was positively related to recruitment, while abundance of exotic forbs was negatively related. Thus, exotic competition is likely only one factor contributing to local declines of native species in invaded ecosystems, with a combination of propagule limitation, site quality, and land use history also playing important and interactive roles in native plant recruitment.     

High richness and dense seeding enhance grassland restoration establishment but have little effect on drought response

Restorations commonly utilize seed addition to formerly arable lands where the development of native plant communities is severely dispersal limited. However, variation in seed addition practices may profoundly affect restoration outcomes. Theory and observations predict that species-rich seed mixtures and seeding at high densities should enhance native plant community establishment, minimize exotic species cover, and may promote resistance and resilience to, and recovery from, environmental perturbations. We studied the post-seeding establishment of native plant communities in large grassland restoration plots, which were sown at two densities crossed with two levels of species richness on formerly arable land in Nebraska, USA, and their responses to drought. To evaluate drought resistance, recovery, and resilience of restored plant communities, we erected rainfall manipulation structures and tracked the response of seeded species cover and total plant biomass during experimental drought relative to controls and in the post-drought growing season. High seed richness and high-density seeding treatments resulted in greater richness and cover of native, seeded species per 0.5 m2 compared to low-richness and low-density treatments. Cover differences in response to seed mixture richness were driven by native forbs. Richness and cover of exotic species were lowest in high-richness and high-density treatments. We found little evidence of differential drought resistance, recovery, and resilience among seeding treatments. Increases in exotic species across years were restricted to drought subplots, and were not affected by seeding treatments. Grassland restoration was generally enhanced and exotic cover reduced both by the use of high-richness seed mixtures and high-density seeding. Given the lack of restoration treatment effects on the resistance, recovery, or resilience of seeded species exposed to drought, and the increases in exotic species following drought, other forms of active management may be needed to produce restored plant communities that are robust to climate change.     

Beyond the ecological: biological invasions alter natural selection on a native plant species

Biological invasions can have strong ecological effects on native communities by altering ecosystem functions, species interactions, and community composition. Even though these ecological effects frequently impact the population dynamics and fitness of native species, the evolutionary consequences of biological invasions have received relatively little attention. Here, I show that invasions impose novel selective pressures on a native plant species. By experimentally manipulating community composition, I found that the exotic plant Medicago polymorpha and the exotic herbivore Hypera brunneipennis alter the strength and, in some instances, the direction of natural selection on the competitive ability and anti-herbivore defenses of the native plant Lotus wrangelianus. Furthermore, the community composition of exotics influenced which traits were favored. For example, high densities of the exotic herbivore Hypera selected for increased resistance to herbivores in the native Lotus; however, when Medicago also was present, selection on this defense was eliminated. In contrast, selection on tolerance, another plant defense trait, was highest when both Hypera and Medicago were present at high densities. Thus, multiple exotic species may interact to influence the evolutionary trajectories of native plant populations, and patterns of selection may change as additional exotic species invade the community.     

Multi-trophic invasion resistance in Hawaii: bioacoustics, field surveys, and airborne remote sensing

We used airborne imaging spectroscopy and scanning light detection and ranging (LiDAR), along with bioacoustic recordings, to determine how a plant species invasion affects avian abundance and community composition across a range of Hawaiian submontane ecosystems. Total avian abundance and the ratio of native to exotic avifauna were highest in habitats with the highest canopy cover and height. Comparing biophysically equivalent sites, stands dominated by native Metrosideros polymorpha trees hosted larger native avian communities than did mixed stands of Metrosideros and the invasive tree Morella faya. A multi-trophic analysis strongly suggests that native avifauna provide biotic resistance against the invasion of Morella trees and exotic birds, thus slowing invasion "meltdowns" that disrupt the functioning of native Hawaiian ecosystems.     

Human impacts, plant invasion, and imperiled plant species in California.

Invasive species are one of the fastest growing conservation problems. These species homogenize the world's flora and fauna, threaten rare and endemic species, and impose large economic costs. Here, we examine the distribution of 834 of the more than 1000 exotic plant taxa that have become established in California, USA. Total species richness increases with net primary productivity; however, the exotic flora is richest in low-lying coastal sites that harbor large numbers of imperiled species, while native diversity is highest in areas with high mean elevation. Weedy and invasive exotics are more tightly linked to the distribution of imperiled species than the overall pool of exotic species. Structural equation modeling suggests that while human activities, such as urbanization and agriculture, facilitate the initial invasion by exotic plants, exotics spread ahead of the front of human development into areas with high numbers of threatened native plants. The range sizes of exotic taxa are an order of magnitude smaller than for comparable native taxa. The current small range size of exotic species implies that California has a significant "invasion debt" that will be paid as exotic plants expand their range and spread throughout the state.     

Biotic Impoverishment and Homogenization in Unfragmented Forest Understory Communities

Abstract:  Ecological change is often hard to document because of a lack of reliable baseline data. Several recent then-versus-now surveys of temperate forest and grassland communities demonstrate losses of local plant species, but most are based on data from a single site. We resurveyed understory communities in 62 upland forest stands in northern Wisconsin (U.S.A.) for which quantitative baseline data exist from 50 years ago. These stands are within a largely unfragmented region but vary in species composition and successional stage. We collected data on changes in (1) total and native species richness, (2) the ratio of exotic to native species, (3) the relative abundance of habitat generalists, and (4) community similarity among sites. We also compared how these rates of change varied over time. Over the past 50 years, native species density declined an average of 18.5% at the 20-m² scale, whereas the ratio of exotic species to native species increased at 80% of all sites. Habitat generalists increased, and habitat specialists declined, accounting in part for an 8.7% rise in average similarity in species composition among sites. Most of these changes cannot be related to succession, habitat loss, or invasion by exotic species. Areas without deer hunting showed the greatest declines in native species density, with parks and research natural areas faring no better than unprotected stands. Animal-pollinated and animal-dispersed species also declined, particularly at unhunted sites. These results demonstrate the power of quantitative multistand data for assessing ecological change and identify overabundant deer as a key driver of community change. Because maintaining forest habitats alone fails to preserve plant diversity at local scales, local biotic simplification seems likely to continue in the region unless active efforts are taken to protect diversity.     

Variation in resource availability changes the impact of invasive thistles on native bunchgrasses.

The threat posed by invasive nonnative plants to native plant populations is one of the largest challenges facing both conservation biology and restoration ecology. California has been highly impacted by invaders, although many relict stands of native plants are found on shallow, rocky soils with limited resources. The abiotic conditions of these sites may strongly influence the performance of an invasive plant and its effect on resident native species. In addition, the maturity of native plants in these sites may modulate an invader's impact; larger, well-established plants may be better able to resist invaders. In this study we examined how the impact of an invasive thistle (Centaurea solstitialis) on a native perennial bunchgrass (Nassella pulchra) changed in response to variation in soil depth, soil water availability, and bunchgrass maturity. We measured plant performance in terms of survival, growth, reproduction, and predawn water potential. We found that soil depth, water availability, and bunchgrass maturity acted in concert to influence the impact of the invasive thistle on the native bunchgrass. Both species performed better in deep soils, especially during dry years. The combination of shallow soil and low water availability reduced C. solstitialis performance and ameliorated its negative effect on N. pulchra growth and reproduction. Higher water availability resulted in a stronger negative effect of C. solstitialis on N. pulchra in both shallow and deep soils. However, as N. pulchra matured and increased in size, we saw a steady decline in C. solstitialis growth and reproductive output. Higher water availability increased the performance of C. solstitialis in shallow soils. C. solstitialis may thus have a stronger impact on N. pulchra and be more able to invade relict stands of N. pulchra in shallow soils during high-rainfall years. However, established stands of N. pulchra appear to be more resistant to invasion by C. solstitialis as N. pulchra plants grow older and larger.     

Additive effects of aboveground polyphagous herbivores and soil feedback in native and range-expanding exotic plants

Plant biomass and plant abundance can be controlled by aboveground and belowground natural enemies. However, little is known about how the aboveground and belowground enemy effects may add up. We exposed 15 plant species to aboveground polyphagous insect herbivores and feedback effects from the soil community alone, as well as in combination. We envisaged three possibilities: additive, synergistic, or antagonistic effects of the aboveground and belowground enemies on plant biomass. In our analysis, we included native and phylogenetically related range-expanding exotic plant species, because exotic plants on average are less sensitive to aboveground herbivores and soil feedback than related natives. Thus, we examined if lower sensitivity of exotic plant species to enemies also alters aboveground-belowground interactions. In a greenhouse experiment, we exposed six exotic and nine native plant species to feedback from their own soil communities, aboveground herbivory by polyphagous insects, or a combination of soil feedback and aboveground insects and compared shoot and root biomass to control plants without aboveground and belowground enemies. We observed that for both native and range-expanding exotic plant species effects of insect herbivory aboveground and soil feedback added up linearly, instead of enforcing or counteracting each other. However, there was no correlation between the strength of aboveground herbivory and soil feedback. We conclude that effects of polyphagous aboveground herbivorous insects and soil feedback add up both in the case of native and related range-expanding exotic plant species, but that aboveground herbivory effects may not necessarily predict the strengths of soil feedback effects.     

Long-term dynamics of biotic and abiotic resistance to exotic species invasion in restored vernal pool plant communities

Invasion of native ecosystems by exotic species can seriously threaten native biodiversity, alter ecosystem function, and inhibit conservation. Moreover, restoration of native plant communities is often impeded by competition from exotic species. Exotic species invasion may be limited by unfavorable abiotic conditions and by competition with native species, but the relative importance of biotic and abiotic factors remains controversial and may vary during the invasion process. We used a long-term experiment involving restored vernal pool plant communities to characterize the temporal dynamics of exotic species invasion, and to evaluate the relative support for biotic and abiotic factors affecting invasion resistance. Experimental pools (n=256) were divided among controls and several seeding treatments. In most treatments, native vernal pool species were initially more abundant than exotic species, and pools that initially received more native seeds exhibited lower frequencies of exotic species over time. However, even densely seeded pools were eventually dominated by exotic species, following extreme climatic events that reduced both native and exotic plant densities across the study site. By the sixth year of the experiment, most pools supported more exotics than native vernal pool species, regardless of seeding treatment or pool depth. Although deeper pools were less invaded by exotic species, two exotics (Hordeum marinum and Lolium multiflorum) were able to colonize deeper pools as soon as the cover of native species was reduced by climatic extremes. Based on an information-theoretic analysis, the best model of invasion resistance included a nonlinear effect of seeding treatment and both linear and nonlinear effects of pool depth. Pool depth received more support as a predictor of invasion resistance, but seeding intensity was also strongly supported in multivariate models of invasion, and was the best predictor of resistance to invasion by H. marinum and L. multilorum. We conclude that extreme climatic events can facilitate exotic species invasions by both reducing abiotic constraints and weakening biotic resistance to invasion.     

Bottom-up control of consumers leads to top-down indirect facilitation of invasive annual herbs in semiarid Chile

The abundance of exotic plants is thought to be limited by competition with resident species (including plants and generalist herbivores). In contrast, observations in semiarid Chile suggest that a native generalist rodent, the degu (Octodon degus), may be facilitating the expansion of exotic annual plants. We tested this hypothesis with a 20-year data set from a World Biosphere Reserve in mediterranean Chile. In this semiarid environment, rainfall varies annually and dramatically influences cover by both native and exotic annual plants; degu population density affects the composition and cover of exotic and native annual plants. In low-rainfall years, cover of both native and exotic herbs is extremely low. Higher levels of precipitation result in proportional increases in cover of all annual plants (exotic and native species), leading in turn to increases in degu population densities, at which point they impact native herbs in proportion to their greater cover, indirectly favoring the expansion of exotic plants. We propose that bottom-up control of consumers at our site results in top-down indirect facilitation of invasive annual herbs, and that this pattern may be general to other semiarid ecosystems.     

Invasion in a diversity hotspot: exotic cover and native richness in the Californian serpentine flora

Exotic species have been observed to be more prevalent in sites where the richness of native species is highest, possibly reflecting variation among sites in resources, propagule supply, heterogeneity, or disturbance. However, such a pattern leaves unclear whether natives at species-rich sites are subject to especially severe impacts from exotics as a result. We considered this question using path models in which relationships between exotic cover and native richness were evaluated in the presence of correlated environmental factors. At 109 sites on serpentine soils across California, USA, exotic cover was positively correlated with total native herbaceous richness and was negatively correlated with the richness of both serpentine-endemic and rare native herbs. However, in path models that accounted for the influences of soil chemistry, disturbance, overstory cover, and regional rainfall and elevation, we found no indication that exotic cover reduced any component of native herb richness. Rather, our results indicated similarities and differences in the conditions favoring exotic, native, endemic, and rare species. Our results suggest that, in spite of some localized impacts, exotic species are not exerting a detectable overall effect on the community richness of the unique native flora of Californian serpentine.     

Escape from competition: neighbors reduce Centaurea stoebe performance at home but not away

The greater abundance of some exotic plants in their nonnative ranges might be explained in part by biogeographic differences in the strength of competition, but these competitive effects have not been experimentally examined in the field. We compared the effects of neighbors on the growth and reproduction of spotted knapweed (Centaurea stoebe) in Europe, where it is native, and in Montana, where it is invasive. There were strong negative competitive effects of neighboring vegetation on C. stoebe growth and reproduction in Europe. In contrast, identical experiments in Montana resulted in insignificant impacts on C. stoebe. Although the mechanisms that produce this dramatic biogeographic difference in competitive outcome remain unknown, our results indicate that differences in net competitive interactions between ranges may contribute to the striking dominance of C. stoebe in parts of North America.     

Effects of Exotic Lonicera and Rhamnus on Songbird Nest Predation

Abstract: Habitat fragmentation and disturbance exacerbate the invasion of exotic plant species that, in turn, may attract nesting songbirds by providing a branch structure suitable for nest sites. We document that American Robin ( Turdus migratorius ) nests in two exotic plants, Lonicera maackii and Rhamnus cathartica , experienced higher predation than nests built in comparable native shrubs ( Crataegus, Viburnum ) and native tree species. This was due to a combination of lower nest height, the absence of sharp thorns on the exotic species, and perhaps a branch architecture that facilitated predator movement among the exotic species. In a more subtle interaction, nesting Wood Thrushes ( Hylocichla mustelina ) experienced apparent competition with robins for nest sites in Lonicera , and this interaction was further aggravated by an increased selectivity for Lonicera by nesting robins, possibly due to their early leaf flush and expansion. By documenting increased nest predation in songbirds nesting in exotic shrubs, our results suggest that restoring native plant communities may benefit the surrounding avian community.     

Influence of a Large Herbivore Reintroduction on Plant Invasions and Community Composition in a California Grassland

Abstract:  Despite many successful reintroductions of large mammalian herbivores throughout the world, remarkably little attention has focused on how these actions affect native and exotic vegetation at reintroduction sites. One such herbivore is tule elk ( Cervus elaphus nannodes ), which was on the brink of extinction in the mid 1800s, but now has numerous stable populations due to intensive reintroduction efforts. Here, we summarize results from a 5-year exclosure experiment that explored the effects of tule elk on a coastal grassland in northern California. Elk significantly altered the species composition of this community; the response of annual species (dominated heavily by exotic taxa) was dramatically different from perennial species. Elk herbivory increased the abundance and aboveground biomass of native and exotic annuals, whereas it either had no effect on or caused significant decreases in perennials. Elk also decreased the cover of native shrubs, suggesting that these herbivores play an important role in maintaining open grasslands. In addition, elk significantly reduced the abundance and biomass of a highly invasive exotic grass , Holcus lanatus, which is a major problem in mesic perennial grasslands. Our results demonstrate that the successful reintroduction of a charismatic and long-extirpated mammal had extremely complex effects on the plant community, giving rise to both desirable and undesirable outcomes from a management perspective. We suspect that these kinds of opposing effects are not unique to tule elk and that land managers will frequently encounter them when dealing with reintroduced mammals.     

Mitigating exotic impacts: restoring deer mouse populations elevated by an exotic food subsidy.

The threat posed by exotic organisms to native systems has led to extensive research on exotic invaders, yet management of invasives has progressed relatively slowly. This is partly due to poor understanding of how exotic species management influences native organisms. To address this shortfall, we experimentally evaluated the efficacy of an invasives management tool for restoring native deer mouse (Peromyscus maniculatus) populations elevated by exotic species. The exotic insects, Urophora spp., were introduced in North America for biological control of the Eurasian invader, spotted knapweed (Centaurea maculosa), but instead of controlling C. maculosa, Urophora have become an important food resource that doubles P. maniculatus populations, with substantial indirect effects on other organisms. We hypothesized that herbicide suppression of Urophora's host plant would reduce the Urophora food resource and restore P. maniculatus populations to natural levels. Prior to treatment, mouse populations did not differ between controls and treatments, but following treatment, P. maniculatus were half as abundant where treatment reduced Urophora. Peromyscus maniculatus is insensitive to direct herbicide effects, and herbicide-induced habitat changes could not explain the P. maniculatus response. Treatment-induced reductions of the Urophora food resource offered the most parsimonious explanation for the mouse response: Multistate mark-recapture models indicated that P. maniculatus survival declined where Urophora were removed, and survival rates were more correlated with variation in population size than movement rates. Other demographic and reproductive parameters (sex ratios, reproductive status, pregnancy rates, and juvenile recruitment) were unaffected by treatment. These results suggest the Urophora biocontrol elevated P. maniculatus survival, and the herbicide treatment restored mouse populations by removing the exotic food and reducing survival. This work illustrates the importance of mechanistic understandings of community and population ecology for improving invasive species management.     

Effect of Invasive Plant Species on Temperate Wetland Plant Diversity

Abstract:  Invasive species are a major threat to global biodiversity and an important cause of biotic homogenization of ecosystems. Exotic plants have been identified as a particular concern because of the widely held belief that they competitively exclude native plant species. We examined the correlation between native and invasive species richness in 58 Ontario inland wetlands. The relationship between exotic and native species richness was positive even when we controlled for important covarying factors. In addition, we examined the relationship between the abundance of four native species (  Typha latifolia, T. angustifolia, Salix petiolaris, Nuphar variegatum ) and four invasive species (  Lythrum salicaria, Hydrocharis morsus-ranae, Phalaris arundinacea, Rhamnus frangula ) that often dominate temperate wetlands and native and rare native species richness. Exotic species were no more likely to dominate a wetland than native species, and the proportion of dominant exotic species that had a significant negative effect on the native plant community was the same as the proportion of native species with a significant negative effect. We conclude that the key to conservation of inland wetland biodiversity is to discourage the spread of community dominants, regardless of geographical origin.