Construction of Sand Shinnery Oak Communities of the Llano Estacado

Home , Llano Estacado, Paspalum, Quercus havardii

oak communities and other similar habitats must consider the effects of animal disturbances and the role of Construction of Sand plant-animal and plant-soil microbe interactions on plant community composition and the maintenance of Shinnery Oak plant species diversity.

Communities of the Llano Introduction

cological restoration attempts to reestablish the Estacado: Animal level of species diversity, species composition, and Einteractions characteristic of the native habitat to be Disturbances, Plant restored (Jordan et al. 1987). Successful restoration should be ecologically sustainable and repeatable. However, repeating successful restorations has been Community Structure, hampered in the past by lack of emphasis on collecting useful and habitat-specific data (Allen, E. B. 1988), including consideration of the roles of different groups and Restoration of organisms and their interactions. With the current rapid loss of species and the deterioration of ecosystems, successful restoration and rehabilitation require Shivcharn S. Dhillion^ collection of appropriate data, including data ftom less Mark A. McGinley^ obvious habitat components, prior to the implementa- tion of sound ecological restoration and management Carl F. Friese^ practices (Allen E. B. 1988; Aronson et al. 1993). John C. Ecologists have long considered animals to have important direct or indirect effects on several aspects of plant community structure (MacMahon 1981; Sousa Abstract 1984; Pickett & White 1985; Collins 1987; Gross 1987; In land restoration it is imperative to study the poten- Allen & MacMahon 1988; Gibson 1988). In many plant tial role of disturbances, biotic or abiotic, that may communities, animal-generated disturbances are es- provide sites for colonization by specific plants. Dis- sential to open sites for seedling establishment. Ani- turbances can alter community composition by re- mals are agents of soil disturbance in many ecosystems moving species or allowing others to become estab- when they produce discrete mounds of soil that can lished. In communities where animal-generated differ from surrounding soils in content and/or struc- disturbances open sites for seedling establishment, ture (Agnew et al. 1986; Mun & Whitford 1990; McGin- animals may have important indirect effects on sev- ley et al. 1994). If variation in either the biotic or abiotic eral aspects of plant community structure. Animal characteristics of disturbances produced by different disturbances in Quercus havardii communities of species of animals favors the successful establishment western Texas appear to open sites for colonization by of different plant species (such as Grubb's regenera- herbaceous species. These animal disturbances vary tion niche, Grubb 1977; Figure 1), then plant species in spatial distribution, density, and abiotic and biotic diversity may be influenced by the number of different characteristics. The abundance of herbaceous plant types of animals producing disturbances and by how seedlings is positively related to bare ground and the the characteristics of these disturbances vary season- number of distinct disturbances. Thus, the density ally. Moreover, if disturbances allow for successful and the spatial distribution of these disturbances may seedling establishment, then the density and spatial be expected to have an important influence on the distribution of animal disturbances should influence abundance and dispersion of plant species. There- plant abundance and dispersion (Figure 1). In commu- fore, successful restoration efforts of sand shinnery nities where this is true, successful restoration efforts must assure that the appropriate agents of disturbance are restored to the community. 1 Ecology Program, Department of Biological Sciences, Texas Tech University, Lubbock, TX 79409, U.S.A. Restoration practices have generally regarded the ^Current address: Department of Biology, University of role of animals in natural environments as detrimental Dayton, Dayton, OH 45469 U.S.A. or destructive—animals as consumers. Emphasis has been placed only on endangered animals that appear © 1994 Society for Ecological Restoration

MARCH 1994 Restoration Eeology Vol. 2 No. 1, pp. 51-60 51 Disturbanees, Plant Gommunity Structure, and Restoration

Animal Disturbances good water retention properties because the top 46 to , 61 cm is a very permeable sand overlying a "B" hori- zon of sandy clay loam that retains substantial quanti- ties of water (Lotspeich & Coover 1962). The climate is warm-temperature continental and semiarid, with an Biotic and Abiotic Density Spatial Distribution Characteristics of Disturbances of Disturbances average annual precipitation of 41 cm; more than 80% ! of Disturbances (Regeneration Niche) of the average precipitation occurs during the growing season of May-October. The Southern High Plains landscape is a mosaic of 1 habitats primarily dominated by agriculture. One of Piant Diversity Piant Abundance 1 1 Piant Dispersion the remaining native systems in this region is sand shinnery oak habitat, which originally occupied 2.3^ million hectares in western Texas, eastern New Mex- ico, and southern Oklahoma (Figure 2). Much of the original sand shinnery oak habitat has been disturbed Piant Community Structure or eradicated by the aggressive use of herbicides and Figure 1. Conceptual diagram illustrating the relationships of animal disturbances and plant community structure. has been converted to crop- and rangeland (Pettit The abiotic and biotic characteristics, densities, and spatial 1979). The vegetation in these communities is primar-1 distribution of animal mounds can affect plant diversity, ily sand shinnery oak, which constitutes at least 80% of abundance, dispersion and ultimately plant community the ground cover (Figure 3; Pettit 1979; personal obser-' structure. vation). Shinnery oak is a low-growing clonal shrub, seldom exceeding 1 meter in height, with extensive below-ground woody rhizomes (Figure 3); it likely re- produces exclusively through vegetative means. No- to be necessary to a system. Little notice has been seedlings were found during this study, and current ^ given to the role of less conspicuous animals in deter- work reveals no viable acorns. This system is different mining the structure of plant communities. from other oak-dominated systems in that most of the The goal of this research was to address the importance of animal disturbance on plant community structure in the highly threatened Quercus havardii Rydb. 0 100 200 300 (sand shinnery oak) communities of semi-arid western -L I Texas. We present new data and briefly review results Kilometers of our work in this poorly studied community, where indirect interactions between animals and plants appear to be particularly important. In addition, this is one of the first comprehensive reports on the status and elements to be understood and documented in the restoration and protection of sand shinnery oak communities. New Mexico

Materials and iVIethods Study Area. The Llano Estacado is that portion of the Great Plains physiographic unit south of the Canadian River that lies in eastern New Mexico and adjoining western Texas. This area is also known as the High I Texas High Plains Land Resource Area, and more recently as the I Plains Region Southern High Plains (Jones 1982; Figure 2). The Llano Sand-Shinnery Estacado has few striking topographic features except Oak Distribution for playa lakes. Elevation of the Llano Estacado ranges g] Study Site from 762 meters in the southwest to 1525 meters in the Location northwest. The parent material of the present soils is Figure 2. Location of field sites and the relative distribu- aeolian deposits, called "cover sands," that were de- tion of Quereus havardii (sand shinnery oak) plant commu- posited during the Illinoian glacial period and the in- niHes in Texas, New Mexico, and Oklahoma (modified terglacial Sangamon. This sandy-textured soil has from Jones 1982).

Restoration Eeology Disturbances, Plant Gontmunity Structure, and Restoration

habitats for a number of plant and animal species (Ta- ble 1). The specific study sites are located in central Yoakum County, 140 km southwest of Lubbock, Texas (33°22' to 33°26'N to 102°50'W, elevation. 1,065 meters). These sites are native sand shinnery oak communities belonging to the Beasly and Fitzgerald Ranches.

Field Procedures. The density and diameter of animal disturbances and soil from rabbit mounds at the Beasly ranch were sampled in May 1991. Five lOO-m^ (100 by 1 meter) subplots were established within each of two 1000-m^ plots on the Beasly ranch, and the density and size (maximum circumference) of animal disturbances in each of these subplots were determined. All disturbances were assigned to the following categories: ants, other insects, rabbit mounds, and other rodents. The characteristics of mounds documented are provided below. With a soil corer, approximately 500 g of soil were collected from rabbit mounds and adjacent (un- disturbed area within a 0.5-meter radius around the mound) off-mound areas (located on the plot) during May 15-25, 1991 {n = 29), on the Beasly ranch and during April 26 to May 1, 1992 (n = ^27), on the Fitzgerald ranch. Several characteristics of these mounds were evaluated in the laboratory as described below.

Table 1. Common plant and animal species occurring in Figure 3. Top: Landscape view of the sand shinnery oak native sand shinnery oak communities in western Texas.* community. The community overstory is dominated by Quereus havardii (sand shinnery oak). Note the dune-like Plants appearance and blowouts without shinnery oak plants. Shrubs: shinnery oak (Qtiercus havardii), sand sagebrush {Artetnisia filifolia), plains yucca {Yueea eattjpestris), and Bottom: Close-up view of dune, showing the scrubby shin- mesquite (Prosopis glandulosa). nery oak about 1 meter tall. Note the relatively deep blow- Grasses: little bluestem (Sehizaehyrium seopariutn), sand out. Photographs taken in June 1992 at the Fitzgerald bluestem {Andropogon hallii), three-awned {Aristida purpu- ranch. rea), sand dropseed {Sporobolus eryptandrus), and sand paspalum (Paspalum setaeeutti). Forbs: wild buckweed {Eriogonum annutitn), plains blackfoot (Gotmnelina ereeta), Fendler euphorb {Euphorbia fendleri), woody stem biomass is below the soil surface. The James rushpea {Gaesalpinia jamesii), and Russian thistle majority (82%) of plant species found in sand shinnery {Salsola kalt). oak communities are herbaceous (Test 1972); thus, species diversity in the community is strongly determined Anintals Ants: harvester (Pogonomyrmex barbatus), Apltaetwgaster by the number of herbaceous species growing there. eoekerelli, Pheidole erassieonis, P. dentata., Gampatiotus Animal disturbances, which abound in these commu- vieinus, Myrmeeoeystiis mimieus, and Grematogaster nities, do not appear to affect sand shinnery oak punetulata. growth. Most of the previous research in this system Birds: quail {Gallipepla squamata), mourning dove (Zenaidura has focused on ways of eradicating sand shinnery oak maeroura), and lesser prairie chicken {Tymoanuchus pallidi- (Pettit 1979). Surveys of potential rare or endangered eintus). species have not been done in this system. Currently, Mammals: kangaroo rats (Dipodomys ordii), gophers (Geomxjs sp.), ground squirrels (Gitellus sp.), western w^ith only 1% of Texas lands set aside as parks or natu- cottontail {Sxjlvilagus auduboni), small mice (Peromyscus ral areas (Texas Nature Conservancy), a major habitat manieidatus, Neotoma mieropus, and Sigmadon hispidus), type in western Texas is threatened with severe frag- antelope {Antiloearpa amerieana). mentation and eventual destruction. The remaining 'Test 1972; Jones 1982; personal observations at Beasly and Fitzgerald sand shinnery oak areas provide important refugia and ranches.

1994 Restoration Eeology 53 Disturbances, Plant Community Structure, and Restoration

Spatial distributions of animal-generated patch dis- 0.4-1 turbances and herbaceous seedlings v^ere sampled at the Fitzgerald Ranch in October 1991. Late October (0 0) represents the end of the fall period of seedling estab- u • Ants e 0.3- lishment. Two 40-meter transects were established, D Mammals and the line-intercept method was used to estimate the cover of plant species, litter, and bare ground in each V) 1-meter interval of both transects. The number and size (maximum circumference) of animal-generated 0.2 - disturbances were determined in 40 l.O-meter-by-0.5- c meter quadrats immediately adjacent to each line tran- o sect. To determine spatial distributions, all distur- o a. 0.1 - bances at this study site were assigned to the following o categories: ants, pocket gophers, other rodents, and unknown. Ant disturbances were characterized either by a mound of soil piled around the nest entrance or 0.0 BJl 00 CO VO VO — the large cleared area around the nest entrance charac- o en o oi o teristic of harvester ants. Pocket gopher mounds were o characterized by the large mound of soil typically dis- Disturbance Size (cm) : placed by members of this genus. Rodent disturbances Figure 4. Frequency distribution of size of disturbance [ were characterized by areas of scraping and digging (maximum diameter) produced by ants and mammals at I the Fitzgerald ranch. Note that there are peaks in the dis- often associated with the entrances of burrow systems. tribution of ants at 0-5 cm and 25-30 cm and that there In each quadrat, we counted the number of seedlings are peaks for mammals at 15-20 cm and 45-50 cm. of herbaceous species less than 20 cm tall, and we noted the number of seedlings associated with animal- generated disturbances. f Because we have not identified the agent of distur- sium, calcium, iron, and magnesium) of soils collected bance to species in every case, it is impossible to assign from the Fitzgerald ranch were processed at the Texas ^ each disturbance to a distinct species. Instead, in both A&M Soil Analysis Laboratory, Lubbock, Texas. sampling designs outlined above, disturbances were The dilution plating technique was used to detect classified in broad categories. Disturbances produced microbial colony forming units (cfu) on standard me- by ants were further divided into two categories: less dia. A 2.0-gram subsample was removed for dry- than 15 cm in diameter and greater than 15 cm in diam- weight estimation. A second 2.0-gram sample of fresh ^ eter. These two categories were chosen because the weight of soil was placed in 198 ml of sterile distilled frequency distribution of the size of ant disturbances water and mixed on a stir plate for 15 minutes. Appro- appeared to be bimodal (Figure 4). Smaller ant mounds priate dilutions of soil were made to quantify microbe were generally produced by different species of ants populations. Separate counts were made from each of than larger ant mounds (McGinley et al. 1994). Thus, it the mounds collected, with five replicates (plates) per ^ was possible to have a maximum number of four dis- sample. Total counts of bacteria and fungi were ob- - tinct disturbance types in a plot, although this could be tained by plating 1-ml dilutions onto nutrient agar and an underestimation of the actual number of distinct 2% malt extract agar, respectively (Ames et al. 1987; species producing disturbances. Dhillion & Anderson 1993). Antibiotics, 30 mg l^^ of streptomycin and 30 mg I' of chlorotetracycline, were Laboratory Procedures. Biotic constituents of soil col- added to cooled 2% malt extract agar to restrict bacte- lected from rabbit mounds and off-mound areas at the rial growth. All cultures were incubated at 20°C and; Beasly ranch were immediately evaluated. Soil sam- only dilution plates that yielded between 30 and 3O0 ples were processed for enumeration of hyphal colonies were counted (Dhillion & Anderson 1993). A lengths, mycorrhizal spores and inoculum potential, 50-gram soil subsample was used to assess hyphal root pieces, and bacterial and fungal propagules. Sub- lengths employing the membrane filter technique samples of soil were removed for each of the above (Sundman & Sivela 1978). The remaining soil samples evaluations. The number of root pieces was obtained were air dried and stored at 4°C. Arbuscular mycorrhi- i by sieving approximately 300 grams of soil through a 4 zal (AM) spores were isolated from a 20-gram sample mm sieve; only obviously living roots were oven dried with a wet-sieving density gradient procedure (Ander-' and weighed. Abiotic constituents (pH, moisture, am- son & Liberta 1989). Intact, cytoplasm-filled spores monium, nitrate, total nitrogen, organic matter, potas- were counted.

Restoration Ecology MARCH 1994 Disturbances, Plant Community Structure, and Restoration

120 -1 50 n A

40 -

30 -

a 20 - Lrt

t 10 20 40 60 80 100 120 a; '2° 1 Transect 2 Percent Cover of Oaks o o tu u 100 - •< 0009

50 -, B 80 -

40 -

30 -

Distance (m) Figure 5. The percentage cover of shinnery oak and bare ground along two 40-meter transects. The location of blowouts can be determined by regions where the percentage cover of the oak goes to zero. These transects both ran % Bare Ground (Excluding Blovouts) east-west and thus were perpendicular to the long axis of Figure 6. (A) The relationship between percentage cover of the blowouts. shinnery oak and the density of herbaceous plants. (B) The relationship between the percentage of bare ground (excluding blowouts) and the density of herbaceous plants.

Results The community overstory of the site is dominated by Table 2. Relationships between number of disturbances, sand shinnery oak (Figure 3; Figure 5). The soil surface plant cover, and number of herbaceous plants using is covered by a dense layer of leaf litter, so there is little Spearman's Rank Correlations (corrected for ties). bare ground (Figure 5). The density of the herbaceous N r, p stratum is independent of the oak cover, however, suggesting that herbaceous plant density is not limited Number of disturbances versus % 65 -0.195 0.118 by the oak cover (Figure 6; Table 2). oak cover 0.040 0.740 Numerous types of biotic and abiotic disturbances % bare ground versus % oak cover 65 Number of herbaceous plants versus 65 0.139 0.267 are found in high densities within the sand shinnery % oak cover oak communities, ranging from large blowouts to Number of herbaceous plants versus 65 0.634 0.0001 smaller disturbances produced by animals (such as % bare ground rabbit, gopher, heteromyid, ants, beetles, and hyme- Number of herbaceous plants versus 65 0.215 0.086 nopterans—Table 3; Figure 4 and Figure 7; blowouts— number of disturbances Number of herbaceous plants versus 65 0.265 0.034 Figure 5). Thus, the shinnery oak habitat has a particu- number of distinct disturbance larly diverse set of disturbances. The density of these types disturbances may be quite high (Table 3). Further-

MARCH 1994 Restoration Ecology 55 Disturbances, Plant Community Structure, and Restoration

Table 3. Assessment of the density and diameter (mean) of Disturbance Types animal disturbances within a sand shinnery oak site in Transect 1 —•— Ant western Texas (Beasly Ranch). o Rodent —K— Unknown Ant Other Rabbit Other Mounds Insects Mounds Rodents Site 1 (100 m^) 143 13 2 46 Site 2 (100 m2) 153 24 27 41 Mound Size (cm) 4-20 2-5 30-70 10-15 If) u c ID more, disturbances produced by animals tend to be n clumped in the habitat (Figure 7; Figure 8). 3 The cover of the dominant plant species at the site is CO 5 not related to the density of animal disturbances or Disturbance Types bare ground (Table 2). Instead, the one characteristic —•— Ant that each of the disturbances shares is that they expose n —O-- Heteromyid K Gopher £ 3 Z

Distance (m) Figure 8. The density of disturbances produced by differ- \ ent disturbance agents along two 40-meter transects. Note that the disturbances are not evenly spaced along the transect. i««L, «-. *' .• ^r bare ground by the removal of the leaf litter layer. Disturbances produced by different species of animals vary in a number of abiotic and biotic conditions. First, they can differ greatly in size (Table 3; Figure 4). Sec- ond, abiotic characteristics such as organic content and nutrient content (ammonium, nitrate, total nitrogen, iron, and magnesium) of disturbances have been observed to vary (Table 4). Finally, biotic characteristics such as the amount of root material, mycorrhizal spore density, number of microorganisms, and fungal hyphal length differ significantly among disturbances produced by rabbits (Table 5). ; The density of herbaceous plants is positively correlated with the amount of bare ground in the plot (Table Figure 7. Top: Gopher disturbances (mounds indicated by 2; Figure 6; see also Figure 7). Herbaceous plants were arrows) are abundant in sand shinnery oak communities associated with disturbances more often than would and frequently occur among vegetation. Photograph taken be expected by chance. For example, 71.1% of the her- in September 1991 at the Beasly ranch. Bottom: Seedlings baceous plants (n = 288) were associated with dis- of three herbaceous plants were associated with a rabbit turbed sites even though the cover of bare ground was mound. The opening of the rabbit burrow is indicated by only 18.7% (x^ test, p < 0.05). an arrow. Photograph taken in May 1992 at the Fitzgerald Overall, the density of seedlings in a plot is indepen- ranch. dent of the number of disturbed patches found in a

Restoration Ecology MARCH 1994 Disturbances, Plant Community Structure, a,nd Restoration

Table 4. Comparisons of selected abiotic characteristics of mound and off-mound soils of Sylvilagus auduboni (western 50 n cottontail) burrows from a sand shinnery oak site in western Texas. 40 - Mound Characteristics Mound Off-Mound P Organic Matter (%) 3.8 1.67 0.001 pH 7.0 7.0 0.220 Total Nitrogen (mg kg ') 722 424 0.001 20 - Ammonium (mg kg"') 10.5 2.7 0.004 Nitrate (mg kg"') 2.1 1.0 0.001 Potassium (mg kg"') 2.1 2.2 0.628 10 Calcium (mg kg"') 951 907 0.617 5.1 3.0 0.001 Iron (mg kg"') 0 —I Magnesium (mg kg ') 146.7 54.7 0.001 10 Density of Disturbances (no./0.5 o plot (Figure 9a; Table 2). However, the density of her- 50-1 B baceous plants in a plot is positively correlated with a> the number of distinct types of disturbed patches 40 - found in the plot (Figure 9b; Table 2). Thus, it appears that a variety of types of disturbed patches is necessary but not sufficient to produce high herbaceous plant 1 densities. Q

Discussion Environmental heterogeneity may be an important fac- tor influencing plant community structure. It is reason- able to expect that the spatial and temporal dispersion of disturbances caused by different disturbance agents Number of Distinct Disturbance Types influences patterns of plant community composition Figure 9. (a) The relationship between the density of dis- and species diversity (Figure 1; Pickett & White 1985; turbances and the density of herbaceous plants. (/;) The Huntly & Inouye 1988; Hobbs & Hunneke 1991). The relationship between the number of types of disturbances idea of the dependence of certain species on the pres- (ant, rabbit, gopher, other insects, other rodents, and ence of disturbances is not new. The heterogeneity blowouts) produced by different agents and the density of created by the nature of patchiness directly affects the herbaceous plants. level of resource availability within a community for establishing organisms. Disturbances can thus alter community composition by removing species or allow- dows through which species may enter and survive in ing others to become established (see Sousa 1984; a community (Pickett & White 1985; Gross 1987). Gross 1987). Disturbances may thus be viewed as win- Several studies in other systems have shown that variation in biotic and abiotic characterisdcs can influence seedling germination and establishment (see Table 5. Comparisons of selected biotic characteristics of Chapin 1983; Vitousek 1985; Allen M. F. 1988; Cham- mound and off-mound soils of Sylvilagus auduboni (western bers et al. 1990), and they may play an important role cottontail) burrows from a sand shinnery oak site in in maintaining alternate strategies for species in such western Texas. communities (see Loucks et al. 1985; Gross 1987). Mound Characteristics Mound Off-Mound P Through burrowing, rodents can expose circles of bare ground in grassland by destroying perennial plants on Root Pieces (g/100 g soil) 5.8 2.6 0.001 Arbuscular mycorrhizal spores 43 27 0.052 and around their nests or warrens. But by enhancing (numbers/100 g soil) nutrient and moisture availability they can also create Hyphal lengths (cm/100 g soil) 1669 1035 0.01 congenial patches for annual herbaceous plant coloni- Total Bacteda (cfuVlO g soil) 16 X 10^ 12 X lO'' 0.01 zation (Collins 1987; Dean & Milton 1991). Abandoned Total Fungi (cfu/10 g of soil) 21 X 103 14 X 103 0.001 harvester ant mounds in Wyoming provide nutrient- *cfu = colony forming units. and microbial-rich areas for native species to become

MARCH 1994 Restoration Ecology Disturbances, Plant Community Structure, and Restoration

established (Friese & Allen 1993). Research on Mount different disturbances. Interestingly, the density of I St. Helens showed that rodent mounds had a higher seedlings per plot was positively correlated with the number of mycorrhizal propagules, brought up to the number of distinct disturbance types in that plot. tephra surface, which facilitated the formation of mu- Thus, it is possible that the greater seedling density tualistic mycorrhizal associations with new seedlings was due to an increase in the number of different plant (Allen M. F. 1988; Allen & MacMahon 1988; Allen et al. species that could germinate in the site. 1992). In contrast, in a study of annual grasslands on The influence of animal disturbance on plant com- serpentine soil in California, gopher soils had lower munity structure may be further complicated by the mycorrhizal propagules due to the inoculum-poor sub- effect that the animal community has on the microbial surface soil brought to the surface (Koide & Mooney community, and how the microbial community influ- 1987). Thus, by knowing and understanding the role ences the plant community. In semiarid to arid re- in an area of vectors such as animals, one might pre- gions, a large number of plants form associations with dict patterns of seedling establishment and, subse- arbuscular mycorrhizae (Dhillion & Zak 1993). Animal- quently, plant community structure (MacMahon 1981; mediated patch disturbances with higher levels of my- Warner et al. 1987). corrhizal propagules are potentially important to sub- Animal disturbances may also be particularly impor- sequent plant establishment because various tant in determining the plant community structure of mycorrhizal fungi can have different physiological ef- the sand shinnery oak community (Figure 1). This fects (such as enhanced photosynthetic rates) on their community differs from many others because distur- hosts, can increase biomass production and uptake of bance does not necessarily affect its established vegeta- nutrients (such as P, N, Zn, Mn) and water, and can j tion. Disturbances in this community appear to open create differential host survival in infected seedlings! sites for colonization by herbaceous species. This (see Allen E. B. 1989; Allen M. F. 1991; McGinley et al. j study and related studies (McGinley et al. 1994) show 1994). Within a community, different mycorrhizal that different animal disturbances can have varied fungi can also show preferential infection of roots of characteristics within a community, thus adding to the different plant species, thus differentially affecting, level of heterogeneity of the site. We have also ob- plant growth and physiology (McGonigle & Fitter served that both animal disturbances and herbaceous 1990; Dhillion 1992; Dhillion & Friese 1994). Our green- plants are patchily dispersed in the habitat (McGinley house studies with Schizachyriwn scoparium (little blue- ^ & Dhillion, unpublished data). Thus, we would expect stem grass) have shown that the effect of mycorrhizal that the density and spatial distribution of these ani- fungi on seedling establishment differs according to mal disturbances may have an important influence on the nitrogen content of the soil (McGinley et al. 1994). ^ the abundance and the dispersion of plant species (Fig- This variation in abundance of organisms, such as my- ure 1). corrhizal fungi, in discrete patches in any habitat; The maintenance of a diverse community of herba- should provide sites for colonization by both myco- ceous species in sand shinnery oak communities may trophic (obligate and facultatively mycorrhizal) and very well be related to the presence of different types nonmycotrophic plants (see Allen M. F. 1991; Allen and frequencies of disturbance if different plant spe- E. B. 1982fl, 1982b). Differential colonizadon by plants, ^ cies are able to establish seedlings more successfully in a result of environmental heterogeneity, results in the different disturbances (Grubb 1977). We have ob- overall increase in and maintenance of species diver- served that both the biotic and abiotic characteristics of sity. disturbances vary among different disturbance agents and seasonally within the same disturbance agent (such as ants, rabbits, and gophers; Dhillion, unpub- Restoration Considerations lished data; Figure 1). Furthermore, our greenhouse In land restoration processes it is imperative to study experiments have shown that sufficient variation in the potential role of disturbances, biotic or abiotic, that abiotic and biotic characteristics exists to influence may provide sites for colonization by specific plants. plant performance (McGinley et al. 1994; Dhillion, un- The importance of animals should be related not only published data). Thus, we have experimental evidence to their conservation status or apparently destructive • showing that the growth of a single plant species dif- and consuming nature, but also to their role in increas- fers among different soils produced by different ani- ing and maintaining diversity by influencing patch mal disturbances. Before we can conclude that envi- structure. Thus, successful restoration efforts of sandl ronmental heterogeneity produced by different species shinnery oak communities and other similar habitats of animals maintains a high diversity of plant species must take into account the effects of plant-animal and in the community, we must first show that seedlings of plant-soil microbe interactions on plant community different species establish most effectively in soils from species diversity and composition. Perhaps the best,

58 Restoration Ecology MARCH 19« Disturbances, Plant Community Structure,'and Restoration

mechanism for proper restoration of such a commu- ungrazed mixed-grass prairie in western South Dakota. nity would be initially to attempt to reestablish the Journal of Range Management 39:135-139. dominant vegetation and later to add necessary animal Allen, E. B. 1982fl. Germination and competition of Salsola kali with native C3 and C4 species under three temperature re- species to the community. Because the addition of gimes. Bulletin of the Torrey Botanical Club 109:39-46. seeds can provide only a limited increase in the rich- Allen, E. B. 1982b. Water and nutrient competition between ness of species in communities, it may be important Salsola kali and two native grass species (Agropyron smithii not only to add animal species but also to assure their and Bouteloua gracilis). Ecology 63:732-741. maintenance. The overall impact of adding and main- Allen, E. B., editor. 1988. The reconstruction of disturbed arid ecosystems. Westview Press, Boulder, Colorado. taining animals would enhance landscape-level patchi- Allen, E. B. 1989. The restoration of disturbed arid landscapes ness, thereby increasing and maintaining the biologi- with special reference to mycorrhizal fungi. Journal of Arid cal diversity of a community. Environments 17:279-286. Successful restoration efforts require that the re- Allen, M. F. 1988. Re-establishment of VA mycorrhizae follow- stored area be large enough to contain viable popula- ing severe disturbance: Comparative patch dynamics of a shrub desert and a subalpine volcano. Proceedings of the tion sizes of all important species. Individual members Royal Society of Edinburgh 94:63-71. of species such as pocket gophers, heteromyid ro- Allen, M. F. 1991. The ecology of mycorrhizae. Cambridge Stud- dents, or rabbits, and individual colonies of different ies in Ecology, Cambridge University Press, Cambridge, ant species may generally require larger areas than will England. Allen, M. F., and J. A. MacMahon. 1988. Direct VA mycorrhizal an individual plant. Thus, the minimum area neces- inoculation of colonizing plants by pocket gophers sary to contain enough individuals or colonies to main- {Tliomomys talpoides) on Mount St. Helens. Mycologia tain viable populations of animal species may be larger 80:754-756. than the minimum area needed to maintain stable pop- Allen, M. F., C. CrisafuUi, C. F. Friese, and S. L. Jeakins. 1992. ulations of the more common plant species. Before ini- Re-formation of mycorrhizal symbioses on Mount St. Helens, 1980-1990: Interactions of rodents and mycorrhizal tiating a successful restoration effort, it may be neces- fungi. Mycological Research 96:447-453. sary to consider the area needed for successful Ames, R. N., K. L. Mihara, and G. J. Bethlenfalvay. 1987. The restoration of animal populations, in cases where ani- establishment of microorganisms in vesicular-arbuscular mals are particularly important in determining plant mycorrhizal and control treatments. Biology and Fertility of community structure. Soils 3:217-223. Anderson, R. C, and A. E. Liberta. 1989. Growth of little blue- In systems dominated by a single species, it is im- stem {Schizachyriwn scoparium) in fumigated and nonfumiga- portant to evaluate the possible mechanisms operating ted soil under various inorganic nutrient conditions. Ameri- to sustain species diversity in an otherwise apparently can Journal of Botany 76:95-104. monotypic stand. Furthermore, the existence of the Aronson, J., C. Floret, E. Le Floc'h, C. Ovalle, and R. Pontanier. 1993. Restoration and rehabilitation of degraded ecosystems dominant vegetation may not be determined by animal in arid and semi-arid lands. I. A view from the south. Resto- or other disturbances or by the availability of open ration Ecology 1:8-17. patches, but the existence of herbaceous plants may Chambers, J. C, J. A. MacMahon, and R. W. Brown. 1990. well be. For example, Platt (1975) and Collins (1987) Alpine seedling establishment: The influence of disturbance showed that the structure of grasslands consists of per- type. Ecology 71:1323-1341. Chapin, F. S. 1983. Patterns of nutrient absorption and use by ennial species that consume the majority of the re- plants from natural and man-modified environments. Pages sources and annual forbs that are highly dependent on 175-187 in H. A. Mooney and M. Godron, editors. Distur- the presence of disturbance. Therefore, in systems bance and ecosystems. Ecological Studies 44, Springer- where restoration attempts have failed, it may be im- Verlag, Mew York. perative to explore the specific characteristics of distur- Collins, S. L. 1987. Interactions of disturbances in tallgrass prairie: A field experiment. Ecology 68:1243-1250. bances that may be creating congenial patches for spe- Dean, W. R. J., and S. J. Milton. 1991. Patch disturbances in arid cies establishment much like those observed in this grassy dunes: Antelope, rodents and annual plants. Journal study. of Arid Environments 20:231-237. Dhillion, S. S. 1992. Evidence for host-mycorrhizal preference in Acknowledgments native grassland species. Mycological Research 96:356-362. Dhillion, S. S., and R. C. Anderson. 1993. Root growth, and We thank Johnnie L. Fitzgerald for generously allowing us to microorganisms associated with the rhizoplane and root work on his ranch, and Brian Croyle, Mary Croyle, Joan zone soil of a native C4 grass on burned and unburned sand Neumann, and Pamela Yeh for help with data collection. We prairies. Soil Biology and Fertility 17:115-120. also wish to thank Joan Neumann for her help in manuscript preparation. Comments and reviews by Edie Allen, Mike Allen, Dhillion, S. S., and C. F. Friese. 1994. The occurrence of mycor- and Bill Niering improved this manuscript considerably. rhizas in prairies: Application to ecological restoration. In press. 13th North American Prairie Conference Proceed- ings. University of Windsor Press, Windsor, Canada. LITERATURE CITED Dhillion, S. S., and J. C. Zak. 1993. Microbial dynamics in arid Agnew, W., D. W. Uresk, and R. M. Hansen. 1986. Flora and ecosystems: Desertification and the potential role of mycor- fauna associated with prairie dog colonies and adjacent rhizas. Proceedings of the USA-NSF symposium on Deserti-

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