Demographic variation in a desert shrub, Larrea tridentate, in response to a thinning treatment

Journal of Arid Environments (2000) 45: 315–323 doi:10.1006/jare.2000.0649, available online at http://www.idealibrary.com on

Demographic variation in a desert shrub, Larrea tridentata, in response to a thinning treatment

Richard E. Miller* & Laura F. Huenneke Department of Biology, New Mexico State University, Las Cruces, NM 88003, U.S.A. (Received 7 April 1999, accepted 31 March 2000) We performed a perturbation experiment to determine the relative importance of intra-specific competition on the demographic performance of a population of creosotebush, Larrea tridentata. From 1992 to 1995, we followed 1000 individuals, half of which were in plots subjected to a thinning treatment, and the other half were in unmanipulated plots. We found no significant response to the thinning treatment for any of the traits studied. The strict interpretation of these results is that intra-specific competition is not important in this Larrea population.  2000 Academic Press Keywords: competition; creosotebush; density-dependence; population regulation

Introduction There are contrasting views regarding the importance of competition among desert plant species (Fowler, 1986). One view suggests that competition for limited resources is overshadowed by the harshness of the environment, so that establishment and survival are difficult to the point of limiting competitive interactions (Shreve, 1942; Went, 1955; Grime, 1977). An alternative view, while recognizing the harshness of the environment, suggests that it is in this environment where resources are so scarce that competition among individuals may be both common and strong (Fowler, 1986). These notions of the strength of competition in desert communities are relevant to both intra-specific competition and inter-specific competition (Yeaton & Cody, 1976; Yeaton et al., 1977; Briones et al., 1996, 1998). Here we focus on intra-specific competition because of its relevance to understanding the relative importance of densitydependent vs. density-independent population regulation in plant populations (Antonovics & Levin, 1980; Fowler, 1988). In particular, intra-specific competition is one of the most important mechanisms of negative density-dependent regulation in natural plant populations (Antonovics & Levin, 1980). However, it is also important to recognize that competition, as a density-dependent effect, may not always contribute to the regulation of populations [where population regulation in the strict sense implies that

*Address for correspondence and present address: Rick Miller, Department of Zoology, Box 90325, Duke University, Durham, NC 27708-0325, U.S.A. E-mail: [email protected] 0140-1963/00/040315#09 $35.00/0

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there is an equilibrium population size and where regulating factors produce an increase in the number of individuals when the population size falls below the equilibrium or causes a decrease when it rises above it (Fowler, 1988)]. This is because the response to a release from competition (e.g. experimental thinning) may result in a change in the size of individuals due to phenotypic plasticity (Harper, 1977), which does not necessarily result in a return to the previous population size. Conversely, a lack of intra-specific competition may suggest that a particular population is regulated in a density-independent fashion with the population at a density where individuals do not compete for limited resources. However, not detecting intra-specific competition does not rule out that a population is in some way regulated by density-dependent factors. Two approaches have generally been used to examine the relative strength of intraspecific competition, especially among desert plant species (Fowler, 1986). One is to determine the spacing pattern among neighbouring individuals within existing populations, where regular or over-dispersed spacing is interpreted as evidence for competition (e.g. Barbour, 1969; Woodell et al., 1969) or where a positive correlation between the distance between neighbouring plants and their size is interpreted as the result of past competition (e.g. Gulmon et al., 1979; Phillips & MacMahon, 1981; Briones et al., 1996). A more direct approach is to use experimental manipulations of density (either removals, thinning, or additions) to determine whether changes in density result in demographic responses consistent with density-dependence effects (Antonovics & Levin, 1980; Smith, 1983a, 1983b, 1983c; Shaw & Antonovics, 1986; Shaw, 1987; Fowler, 1995). Here we apply a perturbation to an existing population, which overcomes some of the confounding effects of natural variation in density and microenvironmental variation in resources (Fowler, 1990). The empirical basis of the debate regarding the relative importance of intra-specific competition and density-dependent population regulation in desert plant species comes, in a large part, from results of studies on the long-lived desert shrub Larrea tridentata (hereafter referred to as Larrea). This species has been characterized as a slow growing stress-tolerant plant (Reynolds, 1986). Investigations of the spacing between Larrea individuals show random and aggregated distributions, and occasionally regular spacing, which suggests that competition and density-dependent mortality may occur, but is infrequent (Woodell et al., 1969; Barbour, 1969; Fonteyn & Mahall, 1981; Phillips & MacMahon, 1981; also reviewed in Barbour, 1973; Fowler, 1986). The results from Larrea studies examining the relationship between size and distance between neighbours generally show positive correlations, suggesting that competition is relatively important in these populations (Yeaton et al., 1977; Fonteyn & Mahall, 1981; Phillips & MacMahan, 1981; Briones et al., 1996). However, the results of these descriptive studies should be viewed with caution because effects of competition may be confounded with micro-environmental differences (Antonovics & Levin, 1980; Mitchell-Olds, 1987; Fowler, 1988). Furthermore, the recognition of individuals for multi-stemmed shrubs is difficult and may lead to biases favouring the detection of regular patterns of dispersion (Ebert & McMaster, 1981). Very few perturbation studies have been employed to study competition in Larrea. Fonteyn & Mahall (1978, 1981) used both an analysis of neighbouring individuals and a removal experiment to examine competition both within Larrea and Ambrosia and between these species. Their results specific to Larrea indicate that spacing was regular, suggesting intra-specific competition is important. However, Larrea removals resulted in a significant effect on xylem pressure potentials of target individuals only during one of three wetting and drying cycles. A similar removal experiment by Briones et al. (1998) showed a similar lack of experimental evidence for competition affecting physiological performance, as well as little effect on short-term measures of growth and reproduction. Only when supplied with water did isolated Larrea exhibit greater twig, node, and leaf growth in comparison to individuals in unmanipulated areas. Taken together, these experimental results suggest that intra-specific competition as indicated

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by physiological measures may be absent or infrequent in Larrea populations. In contrast, studies involving removal of Larrea individuals as part of shrub control efforts provide evidence that competition is important in Larrea populations. While the exact data do not appear to be available, the general impression from this work is that Larrea populations are extremely resilient and without constant shrub control they will return to their original densities (Beck & Tober, 1985; Herbel et al., 1985; Cox et al., 1986; Gibbens et al., 1993; Whitford et al., 1995). More generally, the demographic characteristics of Larrea are those of a desert plant with long maximum life-span, high early survival (after the first few years), high long-term survival, and episodic recruitment (Goldberg & Turner, 1986). Long-term records also suggest that population density may remain stable over relatively long periods of time (Goldberg & Turner, 1986). These observations would suggest that density-dependence may be relatively weak or act sporadically, in a manner similar to that found for the aridland grass Bouteloua rigidiseta (Fowler, 1995). To directly study the potential importance of intra-specific competition on demographic performance in a Larrea population, we undertook a perturbation experiment reducing the density of Larrea in selected areas by removing individuals (thinning treatment). We followed 1000 plants (500 in thinned plots and 500 in unmanipulated plots) over 4 years measuring growth, canopy condition, and reproduction. Our predictions were that if intra-specific competition is important then artificially reducing the density of adult individuals should result in significantly increased growth and/or reproduction of remaining individuals in comparison to plants living in unmanipulated areas. Alternatively, a lack of a response to the thinning treatment would indicate that competition is not important. Materials and methods Study organism Larrea tridentata (DC.) Cov. (Zygophyllaceae) (previously known as Larrea divaricata Cav.) is an evergreen, multi-stemmed desert shrub abundant throughout the warm deserts of North America (Shreve, 1964; Correll & Johnson, 1979). It flowers virtually throughout the year depending on environmental conditions (Oechel et al., 1972). Larrea takes advantage of favourable conditions for growth and reproduction, but can also grow during times of unfavourable conditions (Oechel et al., 1972; Cunningham et al., 1979; Schuster et al., 1992). Larrea individuals may decline in size through the death of branches or the death of shoot systems (Miller & Huenneke, 1996). There is no evidence that Larrea tridentata in the Chihuahuan desert forms clonal rings (Brisson & Reynolds, 1994; Gile et al., 1998; Miller & Huenneke, pers. obs), like those described for Larrea growing in the Mojave desert (Vasek, 1980). Furthermore, the general habit and architecture of Larrea (diploid) of the Chihuahuan desert are quite different from Larrea (polyploid) of the Sonoran and Mojave deserts (Yang, 1967; Barbour et al., 1977). Study area The Larrea population selected for study was located within an area called Big Meadows (37337N, 106336W) within the USDA Jornada Experimental Range (Agricultural Research Service; usda-ars.nmsu.ed) in southern New Mexico, in the northern Chihuahuan Desert (40 km NNE of Las Cruces, NM). The study area (elevation 1573}1597 m) is situated on a western-facing bajada (alluvial fan) at the foot of the San Andres Mountains. The vegetation of the Jornada is a mosaic of semi-arid grasslands

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and shrublands (Buffington & Herbel, 1965). The general vicinity of the Big Meadows study area is largely a Larrea dominated shrubland with scattered Flourensia cernua (tarbush) and Prosopis glandulosa (honey mesquite) [nomenclature follows Allred (1988)]. Cattle were present in the Big Meadows study area approximately every other year of the period of study. While they rarely spent time in the grasslands adjacent to the study area or within the Larrea shrublands, they occasionally moved through the study area on their way from a preferred grazing area to a nearby watering tank and in the process would occasionally damage the branches of Larrea. Gemsbok (Oryx gazella) were a more constant presence in the study area and caused more damage to the Larrea. Experimental design The study area was divided into 30;30 m grid cells (114 total, 102,600 m). A 25 m diameter circular plot was located within each grid cell. From these 114 plots, 20 plots with greater than 100 plants were randomly selected. We imposed a thinning treatment to a random selection of half of these plots immediately prior to making the first set of measurements on adult individuals. This involved removing all but the 50 target individuals (defined below). The plants were cut to the base, disturbing the soil as little as possible. New growth was continually removed thereafter. The initial densities of these plots ranged from 109 to 206 plants per plots [2221}4197 individuals ha\; mean 3076 (703 S.D.)], therefore the thinning treatment represented a 54 to 76% reduction in density. We selected this degree of perturbation to have an adequate sample of target individuals within each plot while allowing for the greatest reduction in density. In addition, the resulting density of 50 plants per plot (1019 individuals ha\) was within the range of densities observed within the Big Meadow Larrea population (Miller & Huenneke, unpublished data). The study consisted of measuring size, estimating the condition of canopies, and determining reproduction of adult plants in thinned plots and control plots. The first step involved randomly selecting 50 adult plants within each plot. We found that even the smallest Larrea individual within the study population flowered. Therefore, any plant within the plots was considered an adult plant. As mentioned above, identification of individual plants can be problematic for multi-stemmed shrubs (Ebert & McMaster, 1981). We used a definition of an individual that best represented the demographic individual (not necessarily the genetic nor physiological individual). Stems emerging from the soil surface within 7 cm of one another were considered part of a single individual. The random selection was done by temporarily numbering the plants in a plot and using a random number table to select 50 plants from the total number. Then the 50 plants in each plot (n"1000) where permanently tagged. We also made maps of shoot systems of individuals where it might be difficult to relocate those same shoot systems at the next census. The measurements of the size of the adult plants were carried out late summer/fall of each year from 1992 to 1995. Height was recorded for each plant. This measurement included both attached dead material and live material. Canopy condition was determined by estimating (to the nearest 5%) the proportion of the canopy composed of dead branches and dead shoot systems. A subsample of plants was used to obtain an estimate of the accuracy of our measurements. Height was measured to an accuracy of$1 cm and canopy condition$5%. Fruit-set can occur throughout the year. Continuously counting the number of fruits produced by all 1000 plants was not feasible. Instead we followed fruit production for a subsample of plants for 2 years (1 October 1993 to 29 September 1995). The subsample (n"40) included a random selection of five plants from each of eight plots (four thinned and four controls). These plants were visited frequently throughout the

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2 years (weekly during times of peak fruit-set). Each fruit (five-seeded mericarp) was counted and collected. Seeds were dissected from mericarps, noting the number of mericarps filled. Seeds were also tested for viability by germinating them in petri dishes on moist filter paper in the dark. Together these data provided an estimate of the number of viable seeds produced by each individual in the subsample. Statistical analyses A nested analysis of variance (ANOVA) was used to compare changes in height, changes in canopy condition, and fecundity in response to the thinning treatment (thinned vs. controls), with plot (treated as a random effect) nested within treatment. Appropriate F-tests were constructed with the TEST statement of the GLM procedure of SAS (SAS Institute, 1990). Data were slightly unbalanced so type III sums of squares were used. The values for changes in height were the difference between the measurements made in 1992 and 1995. The values for changes in canopy condition were differences in the estimates of the proportion of the canopies composed of dead branches and dead shoot systems in 1992 and the same estimates made in 1995. Changes in height and canopy condition for the intervening years were not included in the analysis because the magnitude of the year to year changes were similar to our estimate of measurement error. Four reproductive characters were examined: (1) total number of fruits produced by the plants included in the reproduction subsample over the 2 year collection period; (2) proportion of mericarps that contained seeds; (3) proportion of seeds that were viable; and (4) number of viable seeds produced by each individual [calculated from the preceding value: number of viable seeds"number of mericarps collected (total number of fruits;5;percentage of mericarps filled with seeds;percentage of seeds that were viable]. Because fruit-set is generally correlated with plant size (r"0)508, p"0)0008), analysis of covariance (with plant height in 1992 as the covariate) was used to determine the response of total fruit-set and estimated number of viable seeds to the thinning treatment. Fruit-set and number of viable seeds were log transformed to meet the assumptions of normality, while the proportion of mericarps filled and proportion of seeds viable were arcsine transformed (Sokal & Rohlf, 1981). Results The change in height from 1992 to 1995 was negative on average for plants in both the thinned plots and control plots (Table 1). Changes in plant height result from three different processes. Increases in height are due to growth, whereas decreases in height may be due to either deterioration of dead portions of the canopy, or to branches being broken by gemsbok or cattle (Miller, pers. obs.). The overall negative values result from growth usually being in small increments [mean (S.D.) changes in height greater than or equal to zero: control, 2)98 cm (3)56); thinned, 3)39 cm (2)94)], while a decline in size may be large increments of change, such as when a branch is broken [mean (S.D.) changes in height, less than zero: control, !7)71 cm (8)28); thinned, !6)96 cm (7)43)]. No significant response to the thinning treatment was observed for changes in height (Table 1). Furthermore, separate analyses indicated that neither growth (changes*0) nor declines in size (changes(0) were significantly different between the thinned plots and control plots (F"0)808, p"0)380; F"1)59; p"0)219, respectively). In contrast, the plot to plot variation was significant (Table 1). It is important to restate that the treatment effect was tested over the plot effect in the analysis of variance. In other words, the extent of the plot to plot variation influences the ability to detect treatment differences. The pattern of response, while non-significant, showed that

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Table 1. Demographic performance of a Larrea tridentata population in response to a thinning treatment. Values shown are means of plot means for each treatment (S.E. given in parentheses). Changes in height and canopy condition obtained by comparing measurements made in 1992 to the same measurements made in 1995. Fecundity was determined over a 2-year period. Specifically, the measures are: (a) number of fruits ( five-seeded mericarp) produced by individual plants; ( b) proportion of mericarps filled with seeds; (c) proportion of seeds that were viable; and (d) number of viable seeds produced (calculated from the preceding values). Results of F-tests from analysis of variance are also given for the treatment effect and the plot effect

Treatment Control

Thinned

Change in height (cm) !2)14 (1)36) !0)83 (2)34) Change in canopy condition (%) 1)45 (4)26) 1)39 (2)82) Number of fruits 46)4 (60)9) 241)2 (300)5) Proportion of mericarps filled (%) 15)3 (11)1) 14)6 (4)8) Proportion of seeds viable (%) 45)4 (11)7) 42)4 (21)7) Number of viable seeds 11)49 (29)45) 129)07 (241)31)

Plot

F

p

2)40

0)139

3)03 0)0001

0)025 0)877 1)91 0)218

3)86 0)0001 4)41 0)003

0)201 0)668

1)70 0)172

0)172 0)689

1)17 0)368

2)71

3)15 0)016

0)152

F

p

plants in thinned plots decreased less in height from 1992 to 1995 than plants in control plots (Table 1). Improvement in canopy condition occurs through growth, through the loss of dead material, or both processes simultaneously. Decline in canopy condition results from the death of shoots and branches, or both processes simultaneously. There was no significant response to the thinning treatment with respect to changes in canopy condition and the difference in mean values was only slightly more than 0)05% (Table 1). However, there was significant plot to plot variation in changes in canopy condition (Table 1). Number of fruits produced, or fruit-set, was not significantly different in response to the thinning treatment (Table 1). Again, while the trend is not significant, the pattern of response was greater fruit production in the thinned plots. There was significant plot to plot variation for this character (Table 1). A similar result was observed for the estimate of number of viable seeds with a greater but non-significant difference between seed production in thinned plots and control plots (Table 1). Proportion of mericarps filled with seeds and the proportion of seeds that were viable were essentially invariant between treatments and across plots (Table 1). While following the 1000 individual Larrea plants from 1992 to 1995 we observed seven deaths, with three deaths in the control plots and four in the thinned plots. This indicates that, on average, there were 2)3 deaths per 1000 individuals, which suggests a life-span of approximately 430 years for Larrea in this population. Discussion The consistent result from this study was a lack of response by the Big Meadow Larrea tridentata population to the thinning treatment with respect to both growth and reproduction. Strictly interpreted, these findings suggest that intra-specific competition is not

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important in this Larrea population. Furthermore, they suggest that negative densitydependence was not acting within this population through competitive interactions, or at least not at a level that was detectable in our study. The apparent lack of intra-specific competition in this desert shrub population is consistent with the notions of early desert ecologists reflecting on the harshness of the environment and suggesting competition is infrequent or generally absent in desert plant communities (Shreve, 1942; Went, 1955), as well as being consistent with many of the empirical results obtained from other perturbation experiments (Fonteyn & Mahall, 1978, 1981; Briones et al., 1998). While the strict interpretation of these results supports a lack of intra-specific competition, it is informative to examine the pattern of response to the thinning treatment. The mean values for changes in height were less negative for plants in the thinned plots and mean fruit production was more than four times greater for plants in the thinned plots. While these were not statistically significant results, the trends are consistent with the expectations of intra-specific competition being important. Moreover, given the long life-span of approximately 430 years for the plants in this Larrea population and the slow growth of Larrea, it is quite possible that our results indicate the general importance of density-dependent population regulation. However, it may be acting on a time-scale in Larrea that is much longer or more infrequent than other life forms, such as short-lived perennial herbs (e.g. Salvia lyrata: Shaw & Antonovics, 1986; Shaw, 1987; Bouteloua rigidiseta: Fowler, 1995). The significant plot to plot variation for almost all traits studied suggests a high degree of spatial heterogeneity in the environment. It is likely that plastic responses by the Larrea plants to micro-environmental variation in soil resources resulted in much of the observed variation in growth and reproductive characters (Cunningham et al., 1979; Lajtha & Whitford, 1989). This spatial heterogeneity could have two consequences for our study. First, the high degree of spatial heterogeneity may make detecting a response to the thinning treatment more difficult. For example, while we observed changes in growth and reproduction to the thinning treatment, the magnitude of these responses were small in comparison to the magnitude of plot to plot variation. In addition, the spatial heterogeneity may mean that the intensity of intra-specific competition varies in relationship to variation in soil resources. This could also translate into density-dependence acting in a patchy manner within the population. It has been shown that the action of density-dependence in plant populations living in arid environments may be weak and sporadic (Fowler, 1995). This is consistent with the general demographic characteristics of Larrea populations (Goldberg & Turner, 1986), as well as being consistent with the results from perturbation experiments where the effects of competition were detected either infrequently (Fonteyn & Mahall, 1981) or only under specific environmental conditions (Briones et al., 1998). Therefore, to definitively determine the relative importance of intra-specific competition and densitydependent population regulation for this long-lived desert shrub will probably require following a perturbation experiment over decades. Hopefully this study provides a step towards that goal. The authors thank K. Havstad for permission to work on the Jornada Experimental Range; and R. Dunn, J. Veech, C. McGlone, J. Thompson, J. Baggs, J. Trojan, S. Wood, R. Little, O. Jimenez-Moreno, O. Telgarska, J. Osowski, G. Akin, J. Schwarz, J. Gurrola, and V. Peywa for field assistance. Special thanks to J. Anderson for invaluable logistic support. We thank M. Rausher for helpful discussions. We appreciate the comments of L. Kohorn and P. Tiffin on an earlier version of the manuscript. We thank R. Gibbens and T. Ward for sharing their unpublished data with us. Funding was provided by the USDA/Bureau of Land Management, Grant G910"A1-002, awarded to L. Huenneke and a continuation from the U.S. National Biological Service, and by the Jornada Long Term Ecological Research program, NSF DEB-9240216. R. Miller also would like to thank Duke University for additional support through a postdoctoral fellowship.

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