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Ecology |
Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6018 USA
Received for publication August 2, 2001. Accepted for publication April 26, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSTUDY SITE AND SPECIESMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: arbuscular mycorrhizae • belowground competition • belowground neighborhoods • Eryngium cuneifolium • Hypericum cumulicola • Paronychia chartacea • Polygonella basiramia • Rb • roots
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSTUDY SITE AND SPECIESMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Gurevitch et al., 1990
; Casper and Jackson, 1997
; Casper, Cahill, and Jackson, 2000
).
In many models of plant competition, neighborhood sizes are based on overlap in zones of influence, the area over which plants reduce available resources, or are determined by the space available to each plant. Some models determine the zone of influence by considering the distribution of aboveground plant parts and evaluating the numbers and locations of neighbors that impact a particular plant (e.g., Weiner, 1984
; Silander and Pacala, 1990
). Another approach divides available space among plants based on the spatial arrangement of the aboveground parts of immediate neighbors (Mead, 1966
; Mithen, Harper, and Weiner, 1984
; Daniels, Burkhart, and Clason, 1986
). These widely used approaches ignore the spatial distribution of belowground plant parts and the possibility that aboveground neighborhoods and belowground neighborhoods may differ in size.
The lateral spread of whole-plant belowground root systems is often studied by excavation of entire root systems (e.g., Cole and Holch, 1941
; Coupland and Johnson, 1965
; Brisson and Reynolds, 1994
; Mou et al., 1995
). Such studies have revealed little overlap of root systems, although the smallest roots and mycorrhizal hyphae, which are clearly important in resource uptake, are often ignored (Casper and Jackson, 1997
). Fine roots and mycorrhizal hyphae are difficult to study in situ due to the ease with which they are severed from the plant and the inability to identify individual ownership. Studies that do measure fine roots accurately often use methods that are both difficult and laborious, such as freezing and slicing techniques (e.g., Caldwell, Manwaring, and Durham, 1996
) or hand sorting of roots visually identifiable to species (e.g., Bauhas, Khanna, and Menden, 2000
).
To circumvent these problems, stable and radioactive tracers have been used to measure root activity both spatially and temporally (Ferrill and Woods, 1966
; Brown and Woods, 1968
; Currie and Hammer, 1979
; Veresoglou and Fitter, 1984
; Gibson, 1988
; Abbott, Fraley, and Reynolds, 1991
; Casper, Cahill, and Jackson, 2000
). This technique is effective for describing both the reach and function of roots belowground and can do so even for very fine roots that are missed with other methods. Indeed, Currie and Hammer (1979)
found the horizontal spread of lateral root function in a grassland was three times greater when measured with radioactive phosphorus uptake compared to excavation.
In this study, we used the nutrient analog rubidium (Rb), which is taken up along the same pathways as potassium (K) and typically occurs at very low levels in soils and plant tissues (Larcher, 1995
; Marschner, 1995
). The Rb tracer was injected into soil in localized patches and subsequently harvested plants that contained the tracer are assumed to have had active roots or mycorrhizae in the tracer patch, allowing us to estimate the extent of lateral root function and spatial overlap of herbaceous root systems in a natural setting. We used this technique to address lateral root activity for the herbaceous component of a Florida rosemary scrub community where light levels are high, soil nutrients scarce, and little aboveground overlap of herbs is observed. Most plant interactions in this system are likely occurring belowground (Tilman, 1982
, 1988
). Establishing the lateral extension and function of fine roots in rosemary scrub will help determine whether plants are competing for or partitioning resources belowground and to assess differences between mycorrhizal and nonmycorrhizal root systems.
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STUDY SITE AND SPECIES |
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TOPABSTRACTINTRODUCTIONSTUDY SITE AND SPECIESMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The climate is one of hot, wet summers and mild, dry winters. Mean (±1 SE) annual precipitation is 1331.8 ± 28.6 mm with almost half this amount falling between June and August (Archbold Biological Station weather records, 1932–2000). Soils in rosemary scrub are what make the habitat xeric, being sandy and excessively well drained. Soils are also extremely nutrient poor, with low levels of K (3.11 ± 0.93 µg/g soil), P (0.089 ± 0.035 µg/g soil), Mg (5.67 ± 2.87 µg/g soil), Ca (65.33 ± 40.71 µg/g soil), and N (3.59 ± 4.11 µg NH4/g soil and 0.38 ± 0.19 µg NO3/g soil) (C. V. Hawkes, unpublished data).
We chose four herbaceous species for our experiment: the three perennials Eryngium cuneifolium Small (Apiaceae), Hypericum cumulicola (Small) P. Adams (Hypericaceae), and Polygonella basiramia (Small) Nesom & Bates (Polygonaceae), and the annual (occasional short-lived perennial; Anderson, 1991
) Paronychia chartacea Fern. ssp. chartacea L. C. Anderson (Caryophyllaceae). Much life history information is known for these species (e.g., Johnson and Abrahamson, 1990
; Hawkes and Menges, 1996
; Menges and Kimmich, 1996
; Quintana-Ascencio and Morales-Hernandez, 1997
). Aboveground plant sizes for all four herbs are small: P. basiramia has a basal leaf spread of 4.09 ± 2.33 cm (C. V. Hawkes, unpublished data); the largest species, E. cuneifolium, has a basal rosette diameter of 8.63 ± 5.92 cm (mean ± 1 SD; E. S. Menges, unpublished data); and Core (1941)
described P. chartacea as having a branch length of between 5 and 20 cm. No data are available for H. cumulicola, but we have rarely observed basal leaves spreading >5–10 cm from the center. The four species coexist in open gaps (Quintana-Ascencio and Menges, 2000
) where they co-occur with soil crusts dominated by cyanobacteria and algae (Hawkes and Flechtner, 2002
). Distributions range from the rare E. cuneifolium, found only in open, recently burned sites (Menges and Kimmich, 1996
) to the widespread P. basiramia, found even in small gaps of older sites (Hawkes and Menges, 1995
, 1996
). Roots from all four species (N = 4 plants per species) were stained (Koske and Gemma, 1989
) and examined for mycorrhizal colonization; only the roots of E. cuneifolium and H. cumulicola were infected with arbuscular mycorrhizal (AM) fungi.
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METHODS |
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TOPABSTRACTINTRODUCTIONSTUDY SITE AND SPECIESMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and may alter other plant nutrients as well (Belnap and Harper, 1995
), thereby potentially altering root characteristics and activity.
At eight stratified random points in a single rosemary scrub site (ABS west section, mitigation 40 tract) we injected 10 mL of 1 mol/L RbCl to a depth of 10 cm, by injecting 2 mL every 2 cm. We did so without nutrient enrichment and without regard for underlying variation in other soil nutrients. Injections were not made directly into or under plants and were a minimum of 10 m apart to permit assignment of plant uptake to a given Rb patch. Levels of K are low in these acid soils (C. V. Hawkes, unpublished data; Anderson and Menges, 1997
) and we expected the Rb to be readily taken up (Drobner and Tyler, 1998
). Because plants in this system grow very slowly, we exposed them to Rb over a 3-mo period (mid-July to mid-October 1998). Injections were repeated after heavy rainfall events (approximately every 2–3 wk) to compensate for leaching losses in the extremely porous, low-organic-matter sand of rosemary scrub.
To determine whether Rb spread horizontally after injection due to diffusion or to release by plants after uptake, we used both ion exchange beads and dye injections near each Rb patch. In each plot, water-soluble, blue vegetable dye was injected to examine lateral and vertical water movement. Negatively charged resin beads (Amberlite 1R-120 Plus [H], Rohm and Haas, Philadelphia, Pennsylvania, USA) were used to capture the positively charged Rb ions moving in the soil solution. Approximately 15 mL of resin beads were placed into nylon mesh bags that had been cut from nylon stockings into pieces 10 cm in length and sealed at the ends with rubber bands. These were positioned at 0.5 and 1.0 m from the point of injection in randomly selected directions. The minimum distance of 0.5 m was used to avoid interference of the bags with roots accessing the Rb patches. At the time of harvest, we also collected additional soil crust and soil samples from random locations within 1 m of the injection point to analyze for horizontal Rb spread through diffusion or microbial movement. To check for Rb movement within 0.5 m of the injection, four additional control plots were established after the harvest. In each plot, resin bags were placed at 0.05, 0.1, 0.2, 0.3, and 0.4 m from the Rb patch. No plants occurred aboveground between the Rb patch and the bags. Injections were otherwise identical to the initial trial.
To quantify Rb uptake and root overlap, we harvested all individuals of the four species occurring within a 2 x 2 m area centered on each of the eight randomly positioned Rb patches and recorded the distance and direction of each plant from the Rb patch. The entire aboveground portions of each plant and as much of the root system as possible were collected. Plant and soil samples were dried for 24 h at 80°C and ground to a fine powder in a Spex 8000 Mixer Mill. All plants with aboveground stems <1 m (N = 53) and a subset of plants with stems >1 m (N = 14) from the injection point were analyzed for Rb content. All bags of resin beads were collected and analyzed for Rb content. The volume of resin beads in each bag was measured to check for loss. Beads were then placed in flasks with 25 mL of 4 mol/L KCl, shaken at 185 rpm for 1 h, and 20 mL of the liquid collected in vials. Plant, soil, and liquid samples were sent to the Pennsylvania State University Materials Characterization Laboratory for analysis of Rb content (on a Perkin Elmer 703 spectrometer in flame-emission mode).
The concentration of Rb that was considered elevated or enriched was calculated as the 99% upper confidence limit of the Rb levels found in background plant samples taken before Rb was injected. Throughout the results, we also present the 99% upper confidence limit of the Rb content of the resin bags. Though their meaning is less clear, they represent an extremely conservative cutoff for enrichment. No plants >1 m from the Rb column took up Rb and were therefore excluded from all analyses.
Whether the Rb content or the distance to the Rb patch of enriched plants varied by injection point (patch) or species was first tested with separate two-way ANOVAs. Post hoc 
idák comparisons were made for species when it was a significant main factor (P < 0.05). Rubidium concentrations and distances were natural log transformed to achieve normality and homogeneity of variance. We then used regression analysis to describe how the Rb content (ln transformed) of enriched plants of each species depended on distance (ln transformed) to the injection point and plant biomass.
We estimated potential root system overlap using the lateral root distances we measured for plants within a 4-m2 plot (2 x 2 m) centered on each point of tracer injection, assuming that root systems were radially symmetric in a horizontal plane. The circular areas occupied by root systems of enriched plants were calculated using their observed distances to the Rb injection point as radii; we estimated the radial area occupied by unenriched plants based on the average lateral root spread found in enriched plants. We then calculated the proportion of each 4-m2 plot that would be occupied by zero through greater than six root systems, given the actual spacing of plants aboveground.
All statistical procedures were completed with SPSS version 10.0.0 (SPSS, 1999
). Unless stated otherwise, untransformed data are reported as means ±1 SD and backtransformed data are reported as averages ± asymmetric 95% confidence intervals.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSTUDY SITE AND SPECIESMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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Elevated Rb concentrations (>10.99 ppm) occurred in all four species at distances of up to 97 cm from the point of injection, with an average distance of 51.4 ± 24.9 cm for enriched plants. The concentration of Rb differed significantly among species, but not patches (Table 1). More concentrated and variable amounts of Rb were found in E. cuneifolium compared to P. basiramia or P. chartacea; intermediate Rb concentrations occurred in H. cumulicola (Fig. 1). The distance of enriched plants to the Rb injection point did not differ among species or Rb patches (Table 1, Fig. 1), indicating that plants of all four species were capable of lateral root activity at comparable distances and that this was not altered by local microsite conditions.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSTUDY SITE AND SPECIESMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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Compared to other studies using nutrient analogs as tracers, the maximum distances over which plants took up Rb in this experiment were far greater than those found in fertilized monocultures of Abutilon theophrasti (32 cm; Casper, Cahill, and Jackson, 2000
). Field studies using tracers have found roots functioning over more comparable maximum lateral distances: 90 cm for the grass Leymus cinereus in a natural, cold-desert system (Abbott, Fraley, and Reynolds, 1991
), 60 cm for three grasses, Festuca arizonica, Muhlenbergia montana, and Bouteloua gracilis, and one shrub, Artemisia frigida, in a grassland habitat (Currie and Hammer, 1979
), and 45 cm for two grasses, Arrenatherum elatius and Poa pratensis, in a dune grassland (Gibson, 1988
). Though patterns of lateral root growth are undoubtedly species specific and habitat dependent, roots may be more likely to forage over greater distances in sandy, nutrient-poor, or dry soils (Grime, 1994
; Hutchings and de Kroon, 1994
; Schenk, Callaway, and Mahall, 1999
). Indeed, Coupland and Johnson (1965)
found that of 56 grassland species, most had more extensive root systems when growing in sandy soils than when growing in fine textured loam.
Either there is no direct relationship between aboveground plant sizes and rooting area or the root systems of these species are not radially symmetric. In some cases, plants that took up Rb were immediately adjacent to neighbors that did not access Rb patches; in five instances, plants closer to the Rb patch did not take up Rb while neighboring plants at greater distances did. Casper, Cahill, and Jackson (2000)
found irregularly shaped, discontinuous root systems in a study using two tracers. Such root geometry would result in a decreasing probability of a root hitting a tracer patch with increasing distance of the plant from the point of injection and could contribute to the observed lack of enrichment for plants >1 m from the point of Rb injection. Regardless of the shape of their root systems, plants in rosemary scrub are clearly capable of interacting with more than just their nearest neighbors.
Arbuscular mycorrhizae appear to increase uptake without extending effective root length beyond that observed in the nonmycorrhizal species. Of the mycorrhizal species, E. cuneifolium had significantly higher and H. cumulicola had higher, though not statistically significant, levels of Rb, but both had similar mean and maximum distances from Rb patches compared to the nonmycorrhizal species. Because in many respects mycorrhizae are extensions of the root system, the degree of physical overlap of roots is not a sufficient indicator of the potential degree of belowground interactions. In another sand dune system, the presence of AM fungal mycelia >8 cm from their associated plant root was demonstrated using fatty acid analyses (Olsson and Wilhelmsson, 2000
). Mycorrhizae can influence the outcome of competition between two species (e.g., Allen and Allen, 1990
; Hartnett et al., 1993
; Marler, Zabinski, and Callaway, 1999
) as well as the diversity and aboveground productivity of the plant community (van der Heijden et al., 1998
; Klironomos et al., 2000
). No doubt belowground interactions are one important mechanism behind these phenomena. By differentiating between mycorrhizal and nonmycorrhizal species, our study offers insight into the potential role of mycorrhizal fungi in defining belowground neighborhood sizes and the extent of belowground competition and suggests lines of further study in an area that has been little explored.
If individual root and mycorrhizal systems are extending almost 1 m, then herbs up to nearly 2 m apart aboveground could potentially interact belowground. Many plants did take up Rb from the same patch, indicating overlap of root or mycorrhizal function and potential competition both within and among species. Between 20 and 78% of the plants within 1 m of an Rb patch were enriched, with up to eight individual root systems obtaining Rb from the same point of tracer injection.
It is possible, however, that the overlap of roots we observed is not functional overlap in that roots or mycorrhizae may be segregated vertically within the column of tracer or may be accessing the patch at different times (Parrish and Bazzaz, 1976
). Temporal segregation of Rb uptake is less likely than spatial segregation because of the seasonal growth and nutrient limitation of the plants (Chapin, 1980
; Eissenstat and Yanai, 1996
). Root turnover would have to be much faster than aboveground tissue growth in this system for roots of different individuals to inhabit the same soil space at different times during the course of this study. Rates of root turnover for native plants in Florida scrub are unknown; roots of citrus trees in sandy Florida soils have a median lifespan of 300 d and exhibit little decline in uptake capacity during that time (Bouma et al., 2001
). Spatial segregation of roots may have occurred along the 10 cm deep column of injected Rb. Even so, indirect competition may occur as roots near the surface remove some nutrients that would otherwise filter downward through the sandy soil to deeper roots. Direct interactions are also possible as competition for water and for mobile nutrients such as nitrate can occur at proximities on the order of centimeters (Schenk, Callaway, and Mahall, 1999
).
Subsequent excavation of the herbs revealed differences among species in the shape and size of root systems and provided evidence that direct root system overlap occurs. Although following the fine roots to their ends was nearly impossible, some gross trends were observed. Most roots were found in the top 10–15 cm of soil, consistent with other studies of root depth in scrub (Hunter and Menges, in press). The nonmycorrhizal species P. basiramia and P. chartacea that had lower tissue concentrations of Rb also had smaller taproots. Several P. chartacea lateral roots were >70 cm in length. We found the roots of P. basiramia, P. chartacea, and H. cumulicola in close proximity at distances on the order of centimeters and occasionally entangled. Roots of E. cuneifolium may be spatially segregated, having few fine and lateral roots, and a deeper taproot. The ability of E. cuneifolium to take up larger quantities of Rb than the other herbs could be explained by a combination of the depth of its root system, which could place deep roots in a position to capture any tracer leaching down from the Rb columns, and its mycorrhizal association, which may cause morphological increases in surface area available for uptake or physiological increases in uptake rates. Consistent with this explanation, H. cumulicola had lower concentrations of Rb in its tissues, a shallower root system, and greater level of mycorrhizal infection than E. cuneifolium (C. V. Hawkes, unpublished data). The possibility that mycorrhizae, rather than plant biomass or distance to a resource patch, are primarily responsible for patterns of uptake activity is intriguing, though clearly more study is required to confirm the role of the mycorrhizal association in this process.
This study and others point to a balance of belowground competition and niche partitioning in the rosemary scrub ecosystem where herbaceous plant interactions aboveground are not apparent. Hawkes (2000)
, for example, suggests that changes in the supply of nitrogen from increased deposition can alter the relative abundance of the mycorrhizal and nonmycorrhizal herbs through effects on the spatial location of nitrogen sources and belowground competition. Yet no belowground models to date are sufficient to describe accurately this relationship or its ramifications for plant population or community dynamics. To address these issues, we reiterate calls for (1) inclusion of belowground interactions when studying plant competition (Cahill, 1999
; Cahill and Casper, 2000
), (2) incorporation of mycorrhizae in the study of belowground interactions, and (3) changes to neighborhood models in order to account for root and mycorrhizal belowground neighborhoods that are larger and more irregularly shaped than their aboveground counterparts (Casper and Jackson, 1997
; Casper, Cahill, and Jackson, 2000
).
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FOOTNOTES |
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2 Author for reprint requests, current address: 151 Hilgard Hall, Ecosystem Sciences, Department of Environmental Studies, Policy, and Management, University of California, Berkeley, California 94720-3110 USA (chawkes{at}nature.berkeley.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONSTUDY SITE AND SPECIESMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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