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MAMMAL MOUNDS STIMULATE MICROBIAL ACTIVITY IN A SEMIARID SHRUBLAND.

THOMAS L. KIEFT [1]

Abstract. This study was conducted to determine the influence of animal disturbance, in the form of banner-tailed kangaroo rat (Dipodomys spectabilis) mounds, on soil microbial abundance and activities in a Chihuahuan Desert shrubland. Total organic carbon (TOG), microbial biomass C ([C.sub.mic]), and basal respiration were quantified in soils from beneath and between creosote bush (Larrea tridentata) in three zones: directly on the mounds, immediately surrounding the mounds, and between mounds. TOC, [C.sub.mic], and respiration were enhanced both in soils beneath the canopies of the shrubs and on the mammal mounds. Thus, mammals as well as shrubs contribute to spatial heterogeneity. Ratios of respiration to [C.sub.mic] (metabolic quotient) were highest on the mammal mounds; however, the ratio of [C.sub.mic] : TOG was not affected by shrub canopy cover or location relative to mammal mounds. The higher metabolic quotients in the vicinities of the mounds reflect physical disturbance by mammals and suggest high er proportions of relatively easily metabolized organic carbon than in soils more distant from mounds.

Key words: animal disturbance; Chihuahuan Desert; Dipodomys spectabilis; Long-Term Ecological Research (LTER) site; mammal mounds; microbial activity, effects of mammals and shrubs; microbial biomass; soil respiration; spatial heterogeneity, desert shrubland; spatial variability.

INTRODUCTION

Desert and semiarid shrubland ecosystems are known for spatial heterogeneity of resources (Schlesinger et al. 1990, 1996). Desert shrubs in particular have been shown to form the centers of fertile islands within which the majority of the nutrients and biological activities occur (Garcia-Moya and McKell 1970, Charley and West 1977). Patterns of soil microbial biomass and activities reflect the availability of organic carbon and nutrients; thus microorganisms occur in greater abundance in the soils beneath the canopies of these desert shrubs (Bolton et al. 1993, Kieft 1994, Herman et al. 1995, Kieft et al. 1998). Mammals such as banner-tailed kangaroo rats (Dipodomys spectabilis) and pack rats (Neotoma albigula) also alter the landscape of desert ecosystems and redistribute nutrients through their activities. They disturb the landscape by burrowing and creating extensive mammal mounds (Green and Murphy 1932, Best 1972, Moroka et al. 1982); they concentrate nutrients in the vicinity of the mounds by foraging f or and caching food, and by urination and defecation in the vicinity of the mounds (Green and Reynard 1932, Moorhead et al. 1988, Mun and Whitford 1990). Soil disturbance by mammals can also decrease moisture contents on the mounds (Moorhead et al. 1988, Mun and Whitford 1990). Concentration of nutrients appears to stimulate the growth of creosote bush shrubs in rings immediately surrounding the mounds (Chew and Whitford 1992).

Because the behavior of kangaroo rats (Dipodomys spp.) profoundly influences plant species composition and abundance, as well as the spatial heterogeneity of soil resources, they have been recognized as a keystone guild based on their influence on desert plant communities (Brown and Heske 1990). They also influence other animals: abundance and activities of lizards and ground-dwelling invertebrates are enhanced in the areas of kangaroo rat mounds (Hawkins and Nicoletto 1992). Kangaroo rat mounds require years to build and are occupied by successive generations, and thus are relatively permanent landscape features (Best 1972, Mun and Whitford 1990). Mounds are scattered among the dominant shrubs of the area, thus creating a second pattern of spatial heterogeneity.

This study was undertaken to determine whether microbial abundance and activity are stimulated in the vicinity of banner-tailed kangaroo rat mounds in a creosote bush (Larrea tridentata) shrubland. Components of the "soil organic carbon triangle" (Anderson and Domsch 1986)-total organic carbon (TOC), microbial biomass carbon ([C.sub.mic]), and basal respiration-as well as ratios of these components, [C.sub.mic] : TOC (Insam and Domsch 1988) and basal respiration:[C.sub.mic] (metabolic quotient) (Anderson and Domsch 1985, Insam and Domsch 1988, Insam and Haselwandter 1989), were used to evaluate the status of the soil microbiota.

METHODS

The study site was a creosote bush shrubland area within the Sevilleta Wildlife Refuge in central New Mexico, USA. The refuge is located near the northernmost extent of the Chihuahuan Desert. The area is immediately north of Palo Duro Canyon and in an area locally known as "Five Points." Soils in the area are sandy clay loams (60% sand, 30% silt, 10% clay) with pH [sim]7.9. Density of banner-tailed kangaroo rat mounds is [sim]6 mounds/ha in the area (Robert Parmenter [University of New Mexico], personal communication). Five mounds were randomly selected from an area within 1.0 km of Five Points. Heights of the shrubs directly on the mounds averaged [sim]1 m; shrubs in rings surrounding the mound were taller (average: 1.3 m), and shrubs that were [greater than]20 m from the mounds averaged 0.8 m. These three areas were termed "mound," "enriched," and "intermound" zones, respectively. The diameters of the enriched zones with greatest shrub heights averaged 3.3 m. The mound zones feature extensive [CaCO.sub.3] caliche at the soil surface as a result of mammal burrowing.

Soil samples were collected from beneath the canopies of creosote bush shrubs and from areas between shrubs in each of the three zones: mound, enriched, and intermound. For each of five mounds and for each of the six sample types, soil cores (0-10 cm depth, 1-cm diameter) were collected at 10 randomly selected locations and pooled in the field. Pooled samples were sieved (2-mm mesh sieve), mixed, and stored at 5[degrees]C. Three mounds were sampled in late January 1997; two more mounds were sampled in late February 1997. Microbial measures were completed within 3 wk of collection.

Soil analyses were performed as previously described (Kieft 1994, Kieft et al. 1998). Soil moisture was measured gravimetrically after 24 h desiccation at 105[degrees]C. Total organic carbon (TOC) was quantified in triplicate by the Walkley-Black method (Nelson and Sommers 1982). Basal respiration was measured as the change in [CO.sub.2] concentration, measured by gas chromatography, in the headspace gas of sealed containers containing soil samples. Soil samples (10 g wet mass) were moistened to field capacity with distilled water. Respiration was measured in four replicate subsamples during 24-h incubation at 22[degrees]C, beginning 24 h after the vials were sealed. Biomass carbon ([C.sub.mic]) was measured using the substrate induced-respiration method (Anderson and Domsch 1978). Soil samples (10 g wet mass) were moistened to field capacity, amended with 5-mg glucose solution, and incubated at 22[degrees]C. Headspace gas was sampled in four replicate vials at intervals during the period of 0.5 h to 2.5 h a fter sealing the vials. Respiration rates were converted to [C.sub.mic] using the equation of Anderson and Don1sch (1978). TOC, [C.sub.mic], and respiration were expressed per gram dry mass (gdm).

The effects of the mammal mounds (mound, enriched, and intermound areas) and plant canopy cover (canopy and non-canopy soils) on TOC and microbiological parameters were tested using two-way analysis of variance (ANOVA). Statistical analyses were performed using SYSTAT, version 5.2 (Wilkinson et al. 1992).

RESULTS

TOC (total organic carbon), [C.sub.mic] (microbial biomass C), basal respiration, and the metabolic quotient (basal respiration: [C.sub.mic]) all showed patterns of increased values in the vicinity of the mounds compared to the intermound soils and higher values beneath shrub canopies than in intermound soils (Fig. 1). In general, the rankings of TOC, biomass, respiratory activity, and metabolic quotient for the three areas were as follows: mound [greater than] enriched (ring around mound) [greater than] intermound ([greater than]20 m from mounds). The significance of these trends was confirmed by ANOVA, which showed that both factors, animal mounds and plant canopy, had significant effects (P [less than] 0.05) on nearly all of these parameters, the only exception being the effect of animal mounds on TOC (P = 0.085) (Table 1). The ratio of [C.sub.mic] to TOC appeared not to be affected by proximity to mammal mounds or plant canopies (Fig. 1; Table 1).

DISCUSSION

Spatial heterogeneity in TOC (total organic C) as well as microbial biomass and activity appear to be linked to the actions of burrowing animals as well as to plant distribution. Islands of fertility surrounding desert shrubs have been well characterized (Garcia-Moya and McKell 1970, Charley and West 1977, Bolton et al. 1993) and have been shown to have higher microbial abundance and activities (Gallardo and Schlesinger 1992, Bolton et al. 1993, Kieft 1994, Herman et al. 1995, Kieft et al. 1998). The concentration of nutrients in mammal mounds (Green and Reynard 1932, Moorhead et al. 1988, Mun and Whitford 1990) evidently leads to increased microbial activities. The positive relationship between TOC and [C.sub.mic] (microbial biomass C) reflects the usual condition of soil microorganisms being limited by organic carbon (Dommergues et al. 1978). Gallardo and Schlesinger (1992, 1995) have suggested that microbes in soils beneath shrub canopies become C limited (as opposed to N limited) during desertification. Reichman et al. (1985) and Hererra et al. (1997) have shown that kangaroo rats influence abundance and diversity of fungi colonizing the seeds stored in caches in their burrows. These fungi may contribute to the [C.sub.mic] quantified here; however, the majority of the burrows and caches lie below the 0-10 cm sampling depth of this study. The higher metabolic quotients in the mound zone may reflect soil disturbance and a high proportion of relatively easily metabolized soil carbon (Anderson and Domsch 1985, 1986, Insam and Domsch 1988, Insam and Haselwandter 1989). Wardle and Ghani (1995) warn that the metabolic quotient may be inadequate for distinguishing disturbance from environmental stress; however, the burrowing and foraging activities of mammals are well recognized causes of small-scale disturbance (Coffin and Lauenroth 1989, 1994). The low value of the metabolic quotient away from both the mounds and shrubs indicates relatively stable conditions and a high proportion of stable organic matter that is r efractory to microbial metabolism. The lack of significant plant-canopy effects on the microbial [C.sub.mic]-to-TOC ratio differs from previous studies (Kieft 1994, Kieft et al. 1998); however, seasonal variability of this ratio (Kieft et al. 1998) could explain the lack of effect at the time of the present study.

Although individuals of the dominant plant species, creosote bush, were the largest and appeared to be the most robust in the enriched areas surrounding the mounds compared to the mound and intermound zones, the TOC, [C.sub.mic], and microbial respiration values did not reflect this pattern. Instead, the mound soils had values of these parameters that were as high as or higher than those in the enriched and intermound zones, suggesting that the activities of the animals have at least as great an effect as the plants in concentrating microbial substrates within resource islands. Schlesinger et al. (1990) hypothesized that spatial heterogeneity of resources is increased during the transition of semiarid and desert grasslands into shrublands. Mammals appear to be a source of this spatial heterogeneity, in addition to the shrubs themselves. These mammal-generated resource islands may facilitate the invasion of shrubs into grassland areas (Chew and Whitford 1992, Schlesinger and Pilmanis 1998). Further concentrat ion of nutrients beneath the shrubs is thought to occur via feedback mechanisms (Schlesinger et al. 1990).

Previous studies have shown that the burrowing activities of mammals influence plant community structure (Brown and Heske 1990, Heske et al. 1993, Guo 1996, Fields et al. 1999) and also soil nutrient concentrations (Moorhead et al. 1988, Mun and Whitford 1990). Since soil microbes are dependent on plant-derived organic carbon, it is not surprising to find that microbial communities are influenced quantitatively by changes in plant community structure. Microbial communities may also be influenced qualitatively, i.e., microbial species composition may be different in the vicinity of the mounds, but this was not tested in the present study.

Clearly, burrowing mammals have a significant effect on soil microbial biomass and activity. With an average density of 6 mounds/ha and average size of the mound plus enriched zone of [sim]40 [m.sup.2], the mammal disturbance enhances microbial activity in [sim]2% of the total area. Creosote bush canopies cover 8% of the area at this site (Kieft et al. 1998). Thus, overlapping plant and animal patterns contribute significantly to spatial heterogeneity. Mammal mounds deserve further study, particularly to elucidate temporal dynamics as well as spatial patterns and to quantify biogeochemical cycling of nitrogen and other elements in these mammal-induced fertile islands.

ACKNOWLEDGMENTS

This research was supported by the National Science Foundation (BSR88-11906). This is Sevilleta Long-Term Ecological Research Program Publication number 143. We thank Wenona Ayarbe and Mary McHale for technical assistance and Kevin Kirk for helpful discussions.

(1.) Corresponding author. E-mail: tkieft@nmt.edu

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                   Results of two-way ANOVA for each of
                  the measured soil parameters tested for
                   the effects of mammal mounds (mound,
                  enriched, and intermound areas), plant
                  canopy (beneath canopy and open soils),
                          and their interactions.
                   Factors
                   Mounds                      Canopy
Parameter [+]         F    df         P          F     df        P
TOC                 2.73   2             0.085   4.52  1             0.044
[C.sub.mic]         4.20   2             0.027  18.8   1  [less than]0.001
Basal respiration   3.32   2             0.001  11.4   1  [less than]0.001
[C.sub.mic]:TOC     0.252  2             0.779   0.038 1             0.847
Metabolic quotient 11.7    2  [less than]0.001  36.5   1  [less than]0.001
                   Mounds X Canopy
Parameter [+]             F        df   P
TOC                     0.435      2  0.652
[C.sub.mic]             1.28       2  0.297
Basal respiration       0.185      2  0.607
[C.sub.mic]:TOC         1.03       2  0.372
Metabolic quotient      0.692      2  0.510
(+.)TOC = total organic C, [C.sub.mic] = microbial biomass C,
metabolic quotient = basal respiration: [C.sub.mic].
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Author:AYARBE, JOHN P.; KIEFT, THOMAS L.
Publication:Ecology
Date:Apr 1, 2000
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