skip to main content

Title: Plant–soil interactions limit lifetime fitness outside a native plant’s geographic range margin

Plant species’ distributions are often thought to overwhelmingly reflect their climatic niches. However, climate represents only a fraction of then‐dimensional environment to which plant populations adapt, and studies are increasingly uncovering strong effects of nonclimatic factors on species’ distributions. We used a manipulative, factorial field experiment to quantify the effects of soil environment and precipitation (the putatively overriding climatic factor) on plant lifetime fitness outside the geographic range boundary of a native California annual plant. We grew plants outside the range edge in large mesocosms filled with soil from either within or outside the range, and plants were subjected to either a low (ambient) or high (supplemental) spring precipitation treatment. Soil environment had large effects on plant lifetime fitness that were similar in magnitude to the effects of precipitation. Moreover, mean fitness of plants grown with within‐range soil in the low precipitation treatment approximated that of plants grown with beyond‐range soil in the high precipitation treatment. The positive effects of within‐range soil persisted in the second, wetter year of the experiment, though the magnitude of the soil effect was smaller than in the first, drier year. These results are the first we know of to quantify the effects of edaphic variation on plant lifetime fitness outside a geographic range limit and highlight the need to include factors other than climate in models of species’ distributions.

more » « less
Award ID(s):
Author(s) / Creator(s):
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Aim

    The endophyteEpichloë alsodes, with known insecticidal properties, is found in a majority ofPoa alsodespopulations across a latitudinal gradient from North Carolina to New York. A second endophyte,E. schardliivar.pennsylvanica, with known insect‐deterring effects, is limited to a few populations in Pennsylvania. We explored whether such disparate differences in distributions could be explained by selection from biotic and abiotic environmental factors.


    Along the Appalachian Mountains from North Carolina to New York, USA.




    Studied correlations of infection frequencies with abiotic and biotic environmental factors. Checked endophyte vertical transmission rates and effects on overwintering survival. With artificial inoculations for two host populations with two isolates per endophyte species, tested endophyte–host compatibility. Studied effects of isolates on host performances in greenhouse experiment with four water‐nutrients treatments.


    Correlation analysis revealed positive associations ofE. alsodesfrequency with July Max temperatures, July precipitation, and soil nitrogen and phosphorous and negative associations with insect damage and soil magnesium and potassium. Plants infected withE. alsodeshad increased overwintering survival compared to plants infected withE. schardliior uninfected (E−) plants. Artificial inoculations indicated thatE. alsodeshad better compatibility with a variety of host genotypes than didE. schardlii. The experiment with reciprocally inoculated plants grown under different treatments revealed a complexity of interactions among hosts, endophyte species, isolate within species, host plant origin, and environmental factors. Neither of the endophyte species increased plant biomass, but some of the isolates within each species had other effects on plant growth such as increased root:shoot ratio, number of tillers, and changes in plant height that might affect host fitness.

    Main conclusion

    In the absence of clear and consistent effects of the endophytes on host growth, the differences in endophyte‐mediated protection against herbivores may be the key factor determining distribution differences of the two endophyte species.

    more » « less
  2. Abstract

    Shifts in species geographic distributions in response to climate change have spurred numerous studies to determine which abiotic (e.g. climatic) and, less commonly, biotic (e.g. competitive) processes determine range limits. However, the impact of disturbances on range limits and their interactions with climatic and biotic effects is not well understood, despite their potential to alter competitive relationships between species or override climatic effects. Disturbance might have differential effects at contrasting range limits, based on Darwin's theory that biotic interactions set abiotically benign range limits and abiotic factors set abiotically stressful range limits.

    We predicted that plants at lower elevation (abiotically benign) range limits experience a net positive effect of disturbance, whereas those at higher elevation (abiotically stressful) range limits experience a net neutral effect. We examined plant populations along elevational gradients in the Colorado Rocky Mountains, in order to quantify the effects of human trampling disturbance at lower and upper elevational range limits of the common alpine cushion plantsSilene acaulisandMinuartia obtusiloba.

    Our results are consistent with Darwin's theory. A disturbance‐mediated reduction of competitive effects increases the performance of cushion plants at lower elevations, suggesting a range limit set by biotic factors. At higher elevations, where biotic interactions are minimal, disturbance has neutral or negative effects on cushion plants.

    Synthesis and applications. Human trampling disturbance exerts differential effects on alpine cushion plant populations at contrasting range limits, emphasizing the need to account for the effects of climate change into the management and conservation of disturbed areas. Disturbance can diminish plant–plant competitive interactions at lower elevational range limits, and thus possibly stabilize alpine species populations susceptible to climate change‐mediated encroachment by lower elevation species. Conservation and management approaches should therefore particularly account for the differential effects of disturbance across climatic gradients.

    more » « less
  3. Abstract

    Temporal variation is a powerful source of selection on life history strategies and functional traits in natural populations. Theory predicts that the rate and predictability of fluctuations should favor distinct strategies, ranging from phenotypic plasticity to bet-hedging, which are likely to have important consequences for species distribution patterns and their responses to environmental change. To date, we have few empirical studies that test those predictions in natural systems, and little is known about how genetic, environmental, and developmental factors interact to define the “fluctuation niche” of species in temporally variable environments. In this study, we evaluated the effects of hydrological variability on fitness and functional trait variation in three closely related plant species in the genus Lasthenia that occupy different microhabitats within vernal pool landscapes. Using a controlled greenhouse experiment, we manipulated the mean and variability in hydrological conditions by growing plants at different depths with respect to a shared water table and manipulating the magnitude of stochastic fluctuations in the water table over time. We found that all species had similarly high relative fitness above the water table, but differed in their sensitivities to water table fluctuations. Specifically, the two species from vernal pools basins, where soil moisture is controlled by a perched water table, were negatively affected by the stochasticity treatments. In contrast, a species from the upland habitat surrounding vernal pools, where stochastic precipitation events control soil moisture variation, was insensitive to experimental fluctuations in the water table. We found strong signatures of genetic, environmental (plastic), and developmental variation in four traits that can influence plant hydrological responses. Three of these traits varied across plant development and among experimental treatments in directions that aligned with constitutive differences among species, suggesting that multiple sources of variation align to facilitate phenotypic matching with the hydrological environment in Lasthenia. We found little evidence for predicted patterns of phenotypic plasticity and bet-hedging in species and traits from predictable and stochastic environments, respectively. We propose that selection for developmental shifts in the hydrological traits of Lasthenia species has reduced or modified selection for plasticity at any given stage of development. Collectively, these results suggest that variation in species’ sensitivities to hydrological stochasticity may explain why vernal pool Lasthenia species do not occur in upland habitat, and that all three species integrate genetic, environmental, and developmental information to manage the unique patterns of temporal hydrological variation in their respective microhabitats.

    more » « less
  4. Abstract

    As organisms shift their geographic distributions in response to climate change, biotic interactions have emerged as an important factor driving the rate and success of range expansions. Plant–microbe interactions are an understudied but potentially important factor governing plant range shifts. We studied the distribution and function of microbes present in high‐elevation unvegetated soils, areas that plants are colonizing as climate warms, snow melts earlier, and the summer growing season lengthens. Using a manipulative snowpack and microbial inoculation transplant experiment, we tested the hypothesis that growing‐season length and microbial community composition interact to control plant elevational range shifts. We predicted that a lengthening growing season combined with dispersal to patches of soils with more mutualistic microbes and fewer pathogenic microbes would facilitate plant survival and growth in previously unvegetated areas. We identified negative effects on survival of the common alpine bunchgrassDeschampsia cespitosain both short and long growing seasons, suggesting an optimal growing‐season length for plant survival in this system that balances time for growth with soil moisture levels. Importantly, growing‐season length and microbes interacted to affect plant survival and growth, such that microbial community composition increased in importance in suboptimal growing‐season lengths. Further, plants grown with microbes from unvegetated soils grew as well or better than plants grown with microbes from vegetated soils. These results suggest that the rate and spatial extent of plant colonization of unvegetated soils in mountainous areas experiencing climate change could depend on both growing‐season length and soil microbial community composition, with microbes potentially playing more important roles as growing seasons lengthen.

    more » « less
  5. Abstract

    While microorganisms are recognized for driving belowground processes that influence the productivity and fitness of plant populations, the vast majority of bacteria and fungi in soil belong to a seed bank consisting of dormant individuals. However, plant performance may be affected by microbial dormancy through its effects on the activity, abundance, and diversity of soil microorganisms. To test how microbial seed banks influence plant‐soil interactions, we purified recombinant resuscitation promoting factor (Rpf), a bacterial protein that terminates dormancy. In a factorially designed experiment, we then applied the Rpf to soil containing field mustard (Brassicarapa), an agronomically important plant species. Plant biomass was ~33% lower in the Rpf treatment compared to plants grown with an unmanipulated microbial seed bank. In addition, Rpf reduced soil respiration, decreased bacterial abundance, and increased fungal abundance. These effects of Rpf on plant performance were accompanied by shifts in bacterial community composition, which may have diluted mutualists or resuscitated pathogens. Our findings suggest that changes in microbial seed banks may influence the magnitude and direction of plant‐soil feedbacks in ways that affect above‐ and belowground biodiversity and function.

    more » « less