Jason D. Fridley

THE INVASION PARADOX: RECONCILING PATTERN AND PROCESS IN SPECIES INVASIONS

The invasion paradox describes the co-occurrence of independent lines of support for both a negative and a positive relationship between native biodiversity and the invasions of exotic species. The paradox leaves the implications of native-exotic species richness relationships open to debate: Are rich native communities more or less susceptible to invasion by exotic species? We reviewed the considerable observational, experimental, and theoretical evidence describing the paradox and sought generalizations concerning where and why the paradox occurs, its implications for community ecology and assembly processes, and its relevance for restoration, management, and policy associated with species invasions. The crux of the paradox concerns positive associations between native and exotic species richness at broad spatial scales, and negative associations at fine scales, especially in experiments in which diversity was directly manipulated. We identified eight processes that can generate either negative or positive native-exotic richness relationships, but none can generate both. As all eight processes have been shown to be important in some systems, a simple general theory of the paradox, and thus of the relationship between diversity and invasibility, is probably unrealistic. Nonetheless, we outline several key issues that help resolve the paradox, discuss the difficult juxtaposition of experimental and observational data (which often ask subtly different questions), and identify important themes for additional study. We conclude that natively rich ecosystems are likely to be hotspots for exotic species, but that reduction of local species richness can further accelerate the invasion of these and other vulnerable habitats.

Long-term resistance to simulated climate change in an infertile grassland

Climate shifts over this century are widely expected to alter the structure and functioning of temperate plant communities. However, long-term climate experiments in natural vegetation are rare and largely confined to systems with the capacity for rapid compositional change. In unproductive, grazed grassland at Buxton in northern England (U.K.), one of the longest running experimental manipulations of temperature and rainfall reveals vegetation highly resistant to climate shifts maintained over 13 yr. Here we document this resistance in the form of: (i) constancy in the relative abundance of growth forms and maintained dominance by long-lived, slow-growing grasses, sedges, and small forbs; (ii) immediate but minor shifts in the abundance of several species that have remained stable over the course of the experiment; (iii) no change in productivity in response to climate treatments with the exception of reduction from chronic summer drought; and (iv) only minor species losses in response to drought and winter heating. Overall, compositional changes induced by 13-yr exposure to climate regime change were less than short-term fluctuations in species abundances driven by interannual climate fluctuations. The lack of progressive compositional change, coupled with the long-term historical persistence of unproductive grasslands in northern England, suggests the community at Buxton possesses a stabilizing capacity that leads to long-term persistence of dominant species. Unproductive ecosystems provide a refuge for many threatened plants and animals and perform a diversity of ecosystem services. Our results support the view that changing land use and overexploitation rather than climate change per se constitute the primary threats to these fragile ecosystems.

Extended leaf phenology and the autumn niche in deciduous forest invasions

The phenology of growth in temperate deciduous forests, including the timing of leaf emergence and senescence, has strong control over ecosystem properties such as productivity and nutrient cycling, and has an important role in the carbon economy of understory plants. Extended leaf phenology, whereby understory species assimilate carbon in early spring before canopy closure or in late autumn after canopy fall, has been identified as a key feature of many forest species invasions, but it remains unclear whether there are systematic differences in the growth phenology of native and invasive forest species or whether invaders are more responsive to warming trends that have lengthened the duration of spring or autumn growth. Here, in a 3-year monitoring study of 43 native and 30 non-native shrub and liana species common to deciduous forests in the eastern United States, I show that extended autumn leaf phenology is a common attribute of eastern US forest invasions, where non-native species are extending the autumn growing season by an average of 4 weeks compared with natives. In contrast, there was no consistent evidence that non-natives as a group show earlier spring growth phenology, and non-natives were not better able to track interannual variation in spring temperatures. Seasonal leaf production and photosynthetic data suggest that most non-native species capture a significant proportion of their annual carbon assimilate after canopy leaf fall, a behaviour that was virtually absent in natives and consistent across five phylogenetic groups. Pronounced differences in how native and non-native understory species use pre- and post-canopy environments suggest eastern US invaders are driving a seasonal redistribution of forest productivity that may rival climate change in its impact on forest processes.

Downscaling Climate over Complex Terrain: High Finescale (<1000 m) Spatial Variation of Near-Ground Temperatures in a Montane Forested Landscape (Great Smoky Mountains)*

Landscape-driven microclimates in mountainous terrain pose significant obstacles to predicting the response of organisms to atmospheric warming, but few if any studies have documented the extent of such finescale variation over large regions. This paper demonstrates that ground-level temperature regimes in Great Smoky Mountains National Park (Tennessee and North Carolina) vary considerably over fine spatial scales and are only partially linked to synoptic weather patterns and environmental lapse rates. A 120-sensor network deployed across two watersheds in 2005‐06 exhibited finescale (,1000-m extent) temperature differences of over 28C for daily minima and over 48C for daily maxima. Landscape controls over minimum temperatures were associated with finescale patterns of soil moisture content, and maximum temperatures were associated with finescale insolation differences caused by topographic exposure and vegetation cover. By linking the sensor array data to 10 regional weather stations and topographic variables describing site radiation load and moisture content, multilevel spatial models of 30-m resolution were constructed to map daily temperatures across the 2090-km 2 park, validated with an independent 50-sensor network. Maps reveal that different landscape positions do not maintain relative differences in temperature regimes across seasons. Near-stream locations are warmer in the winter and cooler in the summer, and sites of low elevation more closely track synoptic weather patterns than do wetter high-elevation sites. This study suggests a strong interplay between near-ground heat and water balances and indicates that the influence of past and future shifts in regional temperatures on the park’s biota may be buffered by soil moisture surfeits from high regional rainfall.

NULL MODELS OF EXOTIC INVASION AND SCALE-DEPENDENT PATTERNS OF NATIVE AND EXOTIC SPECIES RICHNESS

Surveys of natural habitats often indicate that native and exotic species richness are positively correlated at large scales and negatively correlated at small scales. The small-scale relationship is often presented as evidence that native richness can repel invasion or conversely that exotic invasions can reduce native diversity. The larger scale pattern has been interpreted as evidence of the importance of facilitation, variable habitat quality, propagule supply, and other ecological phenomena. However, these explanations fail to consider expected native-exotic richness relationships under a null model assuming no species interactions. We show via simulation that the null expectation for a randomly assembled community is a negative relationship between native and exotic species richness at the smallest scales and, when plots vary in total richness, a positive relationship at larger scales. We outline a procedure to compare observational data to this null expectation using a permutation test of labels of species origin (native or exotic). Our use of this technique on plant community data indicates that patterns of native and exotic richness are remarkably similar to those generated by a null model. We argue that a null model approach is needed to evaluate whether observed native-exotic richness data deviate significantly from expected patterns generated by sampling and statistical artifacts.

Worldwide evidence of a unimodal relationship between productivity and plant species richness

Grassland diversity and ecosystem productivity The relationship between plant species diversity and ecosystem productivity is controversial. The debate concerns whether diversity peaks at intermediate levels of productivity—the so-called humped-back model—or whether there is no clear predictable relationship. Fraser et al. used a large, standardized, and geographically diverse sample of grasslands from six continents to confirm the validity and generality of the humped-back model. Their findings pave the way for a more mechanistic understanding of the factors controlling species diversity. Science, this issue p. 302 The humped-back model of plant species diversity is confirmed by a global grassland survey. The search for predictions of species diversity across environmental gradients has challenged ecologists for decades. The humped-back model (HBM) suggests that plant diversity peaks at intermediate productivity; at low productivity few species can tolerate the environmental stresses, and at high productivity a few highly competitive species dominate. Over time the HBM has become increasingly controversial, and recent studies claim to have refuted it. Here, by using data from coordinated surveys conducted throughout grasslands worldwide and comprising a wide range of site productivities, we provide evidence in support of the HBM pattern at both global and regional extents. The relationships described here provide a foundation for further research into the local, landscape, and historical factors that maintain biodiversity.

Community and ecosystem effects of intraspecific genetic diversity in grassland microcosms of varying species diversity

Studies of whether plant community structure and ecosystem properties depend on the genetic diversity of component populations have been largely restricted to species monocultures and have involved levels of genetic differentiation that do not necessarily correspond to that exhibited by neighboring mature individuals in the field. We established experimental communities of varying intraspecific genetic diversity, using genotypes of eight species propagated from clonal material of individuals derived from a small (100-m2) limestone grassland community, and tested whether genetic diversity (one, four, and eight genotypes per species) influenced community composition and annual aboveground productivity across communities of one, four, and eight species. Eight-species communities were represented by common grass, sedge, and forb species, and four- and one-species communities were represented by four graminoids and the dominant grass Festuca ovina, respectively. After three years of community development, there was a marginal increase of species diversity with increased genetic diversity in four- and eight-species communities, and genetic diversity altered the performance of genotypes in monospecific communities of F. ovina. However, shifts in composition from genetic diversity were not sufficient to alter patterns of community productivity. Neighborhood models describing pairwise interactions between species indicated that genetic diversity decreased the intensity of competition between species in four-species mixtures, thereby promoting competitive equivalency and enhancing species equitability. In F. ovina monocultures, neighborhood models revealed both synergistic and antagonistic interactions between genotypes that were reduced in intensity on more stressful shallow soils. Although the dependence of F. ovina genotype performance on neighborhood genetic composition did not influence total productivity, such dependence was sufficient to uncouple genotype performance in genetic mixtures and monocultures. Our results point to an important connection between local genetic diversity and species diversity in this species-rich ecosystem but suggest that such community-level dependence on genetic diversity may not feedback to ecosystem productivity.

CONNECTING FINE- AND BROAD-SCALE SPECIES-AREA RELATIONSHIPS OF SOUTHEASTERN U.S. FLORA

Although the rate that species accumulate with area has long been regarded as an important component of fine-scale community structure and several studies have examined this rate in meta-analyses, few if any studies have systematically examined fine- scale species-area relationships using a consistent survey protocol over a large region. We examined fine-scale species-area relationships using the extensive database of the Carolina Vegetation Survey (North Carolina, South Carolina, Georgia, and Tennessee, USA), in- cluding 1472 plots wherein vascular plant richness was recorded for each of six subplot sizes regularly spaced on a log10 scale, from 0.01 to 1000 m 2 . Contrary to prevailing theory, our data closely and consistently fit an Arrhenius (power law) species-area model, echoing broader-scale patterns. Species accumulation rate (Z) values fell within a narrow range (95% between 0.2 and 0.5) despite a 30-fold range in 1000-m 2 richness. When we added regional- and global-scale richness estimates to our results, a Preston-type triphasic curve emerged. We suggest that (1) fine-scale species-area relationships are remarkably consistent and (2) full-scale species-area curves reveal scale dependencies in diversity data that are not accounted for by current species-area theory.

Grassland root communities: species distributions and how they are linked to aboveground abundance

There is little comprehensive information on the distribution of root systems among coexisting species, despite the expected importance of those distributions in determining the composition and diversity of plant communities. This gap in knowledge is particularly acute for grasslands, which possess large numbers of species with morphologically indistinguishable roots. In this study we adapted a molecular method, fluorescent fragment length polymorphism, to identify root fragments and determine species root distributions in two grasslands in Yellowstone National Park (YNP). Aboveground biomass was measured, and soil cores (2 cm in diameter) were collected to depths of 40 cm and 90 cm in an upland, dry grassland and a mesic, slope-bottom grassland, respectively, at peak foliar expansion. Cores were subdivided, and species that occurred in each 10-cm interval were identified. The results indicated that the average number of species in 10-cm intervals (31 cm3) throughout the sampled soil profile was 3.9 and 2.8 species at a dry grassland and a mesic grassland, respectively. By contrast, there was an average of 6.7 and 14.1 species per 0.5 m2, determined by the presence of shoot material, at dry and mesic sites, respectively. There was no relationship between soil depth and number of species per 10-cm interval in either grassland, despite the exponential decline of root biomass with soil depth at both sites. There also was no relationship between root frequency (i.e., the percentage of samples in which a species occurred) and soil depth for the vast majority of species at both sites. The preponderance of species were distributed throughout the soil profile at both sites. Assembly analyses indicated that species root occurrences were randomly assorted in all soil intervals at both sites, with the exception that Festuca idahoensis segregated from Artemisia tridentata and Pseudoroegnaria spicata in 10-20 cm soil at the dry grassland. Root frequency throughout the entire sampled soil profile was positively associated with shoot biomass among species. Together these results indicated the importance of large, well-proliferated root systems in establishing aboveground dominance. The findings suggest that spatial belowground segregation of species probably plays a minor role in fostering resource partitioning and species coexistence in these YNP grasslands.

Integration of local and regional species-area relationships from space-time species accumulation

A long‐standing observation in community ecology is that the scaling of species richness, as exemplified by species‐area curves, differs on local and regional scales. This decoupling of scales may be largely due to sampling processes (the increasing constraint imposed by sampling fewer individuals at fine scales), as distinct from ecological processes, such as environmental heterogeneity, that operate across scales. Removal of the sampling constraint from fine‐scale richness estimates should yield species‐area curves that behave like those of the regions in which they are embedded, but an effective method for this removal has not been available. We suggest an approach that incorporates the manner in which small areas accumulate species over time as a way to remove the signature of sampling processes from fine‐scale species‐area curves. We report for three species‐rich grasslands from two continents how local plant species richness is distributed through time at multiple, nested spatial scales, and we ask whether sampling‐corrected curves reflect the spatial scaling of richness of each larger floristic province. Our analysis suggests that fine‐scale values of richness are highly constrained by sampling processes, but once these constraints are removed, the spatial scaling of species richness is consistent from the scale of individuals to that of an entire province.