Journal of Mammalogy, 84(3):1031±1043, 2003

MICROHABITAT USE AND POPULATION DECLINE IN BANNER-TAILED KANGAROO RATS

PETER M. WASER* AND JAMES M. AYERS Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA

Numbers of banner-tailed kangaroo rats, Dipodomys spectabilis, have declined sharply in Downloaded from https://academic.oup.com/jmammal/article/84/3/1031/903815 by guest on 24 September 2021 some but not all populations monitored in southeastern Arizona over the past 20 years. We describe concurrent changes in vegetation and report the results of microhabitat manipu- lation experiments in which we removed broom snakeweed, Gutierrezia sarothrae, from 1.00-ha (pilot) or 0.56-ha (replicate follow-up) plots. D. spectabilis became extinct on control plots, but populations remained stable on plots where snakeweed was removed. On a larger scale, declines in numbers of kangaroo rats coincided with increases in density of woody plants. The data substantiate the preferences of this species for structurally open microhabitats and document that survival rates are higher in areas that are more open. Large species like D. spectabilis are often regarded as keystone species, and our results indicate that they are vulnerable to grassland degradation.

Key words: scrub, Dipodomys spectabilis, grassland, heteromyids, kangaroo rats, keystone species, microhabitat use, population dynamics, snakeweed

Kangaroo rats (Dipodomys spp.) exert and the banner-tailed kangaroo rat, D. spec- strong in¯uences on other members of their tabilis. community. As competitors, they exert po- The large size of banner-tailed kangaroo tent negative effects on sympatric grani- rats makes them effective interference com- vores (Bowers 1986; Brown et al. 1986; Er- petitors (Bowers and Brown 1992; Bowers nest and Brown 2001; Harris 1984; Valone et al. 1987; Brown and Munger 1985; Frye and Brown 1996; Wondolleck 1978). Their 1983), but they have positive effects as preferential harvesting of large-seeded an- well: their larder hoards may create oppor- nuals prevents these plants from excluding tunities for smaller species to pilfer seeds other smaller-seeded species (Brown et al. (Brown and Heske 1990; Price et al. 2000), 1986; Guo et al. 1995; Heske et al. 1993; and their extensive systems create Samson et al. 1992) and thus, indirectly, fa- long-lasting impacts on soil characteristics cilitates ant populations (Davidson et al. (and thus plant communities) and shelter, 1984). Soil disturbance caused by their for- nesting, or estivation sites for species rang- aging may in¯uence composition of plant ing from beetles to burrowing owls (Brown communities (Brown and Heske 1990; Cur- et al. 1997; Chew and Whitford 1992; tin et al. 2000; Heske et al. 1993), as does Greene and Reynard 1932; Guo 1996; seed caching and vegetation clipping (Ker- Hawkins and Nicoletto 1992; Moorhead et ley et al. 1997; Schiffman 1994; Valone and al. 1988; Moroka et al. 1982; Mun and Thornhill 2001). These effects are particu- Whitford 1989; Seastedt et al. 1986). larly well documented for larger species, Species of large kangaroo rats have been such as the giant kangaroo rat, Dipodomys subject to marked population declines in ingens, the desert kangaroo rat, D. deserti, many areas (Goldingay et al. 1997; Single * Correspondent: [email protected] et al. 1996; Williams and Germano 1992).

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In some cases, declines are related unam- tabilis spent less time near shrubs than did biguously to anthropogenic modi®cation of their smaller sympatric congeners, D. mer- habitat, but in others, causes are less clear. riami and D. ordii (Schroder 1987). For example, between summer 1983 and Mounds and burrow systems that D. spec- winter 1984 a population of D. spectabilis tabilis occupied more continuously had in the San Simon Valley in southeastern Ar- fewer shrubs within 5 m (Jones 1982). izona declined by 80%, from the 2nd most In this study, we asked whether the con- common on the site to one of the version of grassland to desert scrub caused rarest. Valone et al. (1995) summarized ev- declines in numbers of D. spectabilis.We idence that the decline was precipitated by used 2 sources of data: 1st, censuses of D. Downloaded from https://academic.oup.com/jmammal/article/84/3/1031/903815 by guest on 24 September 2021 an extreme climatic event, a tropical storm spectabilis and of woody plants on 2 long- that dropped half the average year's precip- term study sites, 1 immediately adjacent to itation on the study site during a single the Brown±Valone site and the other in a week. The negative effects of heavy rainfall nearby area in which vegetation remains could have been mediated by disease, by open grassland; and 2nd, experimental ma- premature spoilage or germination of lar- nipulations of woody vegetation, speci®cal- der-hoarded seeds, or by excessive fungal ly removal of broom snakeweed, Gutierre- growth in seed stores, resulting in the pro- zia sarothrae. Preferences for open micro- duction of lethal mycotoxins. Valone et al. habitats among kangaroo rats have been hy- (1995) favored the last of these explana- pothesized to increase survival or fecundity tions. None of these possibilities, however, by enhancing foraging ef®ciency or safety explains why D. spectabilis on the site did from predators. To determine whether mi- not recover, becoming locally extinct in crohabitat preferences have adaptive de- 1995 (Brown et al. 2001; Valone and mographic impacts, we examined the ef- Brown 1996). fects of manipulating woody vegetation on The decline of D. spectabilis at the above immigration, recruitment, and survival of siteÐhereafter the Brown±Valone siteÐco- D. spectabilis and assessed the contribu- incided with a gradual increase in the den- tions of recruitment and survival to changes sity of woody vegetation (Brown et al. in the size of D. spectabilis populations. To 1997; Valone and Kelt 1999). Many species determine whether manipulating woody of kangaroo rat are found preferentially in vegetation in¯uenced food availability as open microhabitats (Bowers et al. 1987; well as microhabitat structure, we also Germano et al. 2001; Kotler 1984; Price monitored responses of herbaceous plants. 1978a, 1978b, 1984; Price and Brown 1983; Reichman and Price 1993; Rosen- MATERIALS AND METHODS zweig and Winakur 1969). Some evidence Long-term population trends.ÐOur popula- suggests that this tendency is more pro- tion data on D. spectabilis come from mark± nounced in larger species, which also tend release±recapture studies begun in 1979. Most to be con®ned on a geographic scale to data we report in this study come from our 64- more open habitats (D. desertiÐBrown and ha ``Portal'' site, the northwest corner of which Harney 1993; Thompson 1982a; D. in- abuts the Brown±Valone site. Historical records gensÐGrinnell 1932; Williams 1987). D. suggest that this area (elevation, 1,350 m) was spectabilis, in particular, has been charac- grassland in l875 (Valone and Kelt 1999). How- ever, deterioration began in the late 1800s, and terized as a species of open grassland in 1944, the area was classi®ed as transitional (Hoffmeister 1986; Vorhies and Taylor between grassland and desert shrub (Darrow 1922). On a local scale, individuals were 1944). In 1979, it was still relatively open, with trapped more often at microsites with lower scattered shrubs (Prosopis glandulosa, Acacia percentage cover (Bowers and Brown 1992; greggi, Flourensia cernua, Ephedra trifurca, Bowers et al. 1987). Radiotracked D. spec- and especially A. constricta) and occasional August 2003 WASER AND AYERSÐPOPULATION DECLINE OF KANGAROO RATS 1033 half-shrubs (especially G. sarothraeÐwe use known alive were as high as or higher than the the term half-shrub to refer to suffrutescent pe- closed-population mark±recapture estimates. rennials, species that are smaller than most We, therefore, report minimum numbers alive. shrubs but woody at the base). The most com- Dipodomys spectabilis breeds during the win- mon grass was Tridens pulchella, but open areas ter, and nearly all individuals breed 1st in the were seasonally dominated by annuals and winter after their birth (Holdenried 1957; Rand- short-lived herbaceous perennials (Jones 1982). all 1991; Vorhies and Taylor 1922; Waser and Our 2nd site, ``Rucker,'' is about 40 km SSW Jones 1991). We report adult survival as the pro- of the Portal site. The Rucker site contains a portion of marked adults in March that survived number of small, relatively discrete populations to the next March. Fecundity was the number of of D. spectabilis; in this study, we discuss data daughters captured in August per adult female Downloaded from https://academic.oup.com/jmammal/article/84/3/1031/903815 by guest on 24 September 2021 from our longest-censused, Rucker 1, popula- in March. Recruitment was the number of new tions, which occupy approximately 24 ha. Com- adult females in March per female in March the pared with Portal, the Rucker site is slightly year before. Nearly 95% of ``new'' adults in higher in elevation (1,600 m), wetter, and on March were that were trapped as juve- richer soils. Vegetation is desert grassland, niles the year before; the remainder were adults shrubs are virtually absent, and half-shrubs are (as indicated by descended testes or elongated rare. The commonest grasses are Bouteloua spe- nipples) when initially captured, but given our cies, Hilaria mutica, and Eragrostis lehmanni- high adult capture probabilities, we believe these ana, but areas favored by kangaroo rats are char- were 1-year olds, either immigrants or late-ma- acterized by short grass and forbs interspersed turing juveniles, that we missed in the previous with patches of bare ground. census. Dipodomys spectabilis builds conspicuous Long-term trends in woody vegetation.ÐIn mounds 1±3 m in diameter and up to 0.5 m high, August of 1982, 1988, and 1993, we counted all which makes locating them straightforward shrubs and half-shrubs on 1-m2 quadrats on the (Best 1972; Vorhies and Taylor 1922). Mounds Portal site; we did the same in l982 and l993 at are often occupied for generations and can be Rucker. At Portal, counts took place on 3 plots, recognized for many years even after they are 100 by 100 m (1.00 ha). These plots were cho- abandoned (Holdenried 1957; Jones 1984, sen to contain high densities of D. spectabilis 1993). Occupied mounds are distinguishable mounds, with the presumption that such areas through fresh diggings and often by connecting are or have recently been prime habitats for this runways and sandbathing sites (Vorhies and Tay- species. We collected Rucker data on 2 plots, lor 1922). Radiotracking demonstrates that all 100 by 100 m (1.00 ha), with mound densities individuals, with rare and temporary exceptions similar to those at Portal. Quadrats were placed during dispersal, reside within such mounds at 10-m intervals in a regular grid centered with- (Jones 1982). On both sites, we censused D. in each plot. Sampling intensity was 81 quad- spectabilis at least twice yearly (March and rats/plot in l982, 64 quadrats/plot in l988, and July±August) by trapping for 2±5 nights at all 20 quadrats/plot in l993; all data were converted mounds showing fresh signs of use. In many to plants per hectare. In these samples, we en- years, additional trapping was carried out during countered 5 shrub species (A. constricta, A. April±June and October, but we suspended trap- greggi, Ephedra trifurca, F. cernua, and P. ping at the Rucker site in 1986 after removing glandulosa) and 3 half-shrubs (G. sarothrae, all animals for allozyme analyses (Elliott et al. Haplopappus tenuisectus, and Zinnia pumila). 1989). We resumed trapping in 1990 after re- Pilot woody vegetation manipulation.ÐIn colonization of the area in 1987 (Cross and Was- November 1987, we randomly chose 1 of the er 2000). three 1.00-ha Portal plots on which we had sam- We weighed, determined sex and reproductive pled plants in 1982 and manipulated microhab- status of, and tagged all individuals in both ears itat availability by hand removal of broom with uniquely numbered ®ngerling tags. Trap- snakeweed, G. sarothrae. Snakeweed was by far ping ef®ciency at mounds was extremely high, the most common woody plant on the site at the with adult capture probabilities for 3 nights es- time. The other 2 plots were left as unmanipu- timated at 96% (Cross and Waser 2000). As a lated controls. Experimental and control plots result, the minimum numbers of marked animals contained habitats of similar suitability for D. 1034 JOURNAL OF MAMMALOGY Vol. 84, No. 3 spectabilis, as judged by qualitatively similar reliably identi®able as residents of a particular vegetation, numbers of active plus inactive female's mound if they were trapped there at mounds (range, 13±14), and numbers of resident least twice and more often than at any other kangaroo rats (range, 2±4). Plots were separated mound (the latter criterion has recently been from each other by Ն150 m. We checked the con®rmed by microsatellite-based analyses of experimental plot and removed any new snake- maternityÐWinters 2001). Using these criteria, weed plants at 6-month intervals until 1996, at we used censuses and (if available) supplemen- which time snakeweed had become rare after tary trapping data to infer which individuals prolonged drought (Valone and Kelt 1999). were resident in mounds on each control or ex- To assess the impact of snakeweed removal perimental plot. This procedure also allowed us on food plants of kangaroo rats, we sampled to examine whether changes in population size Downloaded from https://academic.oup.com/jmammal/article/84/3/1031/903815 by guest on 24 September 2021 nonwoody plants on the experimental plots and on a plot were the result of death, emigration, 1 of the control plots in August 1988, using the immigration, or in situ recruitment. same sampling design described above for Statistical analyses.ÐData were tested for woody vegetation. We identi®ed 8 grass species normality and homogeneity of variances and (most prominently Bouteloua aristidoides, B. transformed where appropriate (Sokal and Rohlf barbata, Aristida adscensionis, and Tridens pul- 1981). For comparisons of plant densities among chella) and 28 species of annual or herbaceous plots, we used analysis of variance (ANOVA), perennials (most common was Erodium cicutar- with plots nested within treatments where appro- ium, followed by Euphorbia species, Eriogonum priate, after square-root transformation. For abertianum, Portulacca species, Baileya multi- comparisons of kangaroo rat densities between radiata, and Cassia bauhinoides). experimental and control plots, we used repeat- Follow-up woody vegetation manipulation.Ð ed-measures ANOVA. All analyses used SYS- To replicate the l987 pilot study, we selected 8 TAT (Wilkinson 1997). The criterion for statis- additional plots, 75 by 75 m (0.56 ha), on the tical signi®cance was P Ͻ 0.05. We report Portal site in October 1992. As in the pilot study, means Ϯ SE. we chose plots with qualitatively similar vege- tation characteristics and similar numbers of RESULTS mounds (range, 3±9) and resident D. spectabilis Long-term population trends.ÐPopula- (range, 1±2). We randomly chose 4 of these tions of D. spectabilis on the Portal site de- plots and hand-removed all snakeweed, treating clined by 2 orders of magnitude from a the other 4 plots as controls. The minimum dis- peak of 4.80 animals/ha in August 1982 to tance between any pair of plots was 100 m. As a low of 0.05 animals/ha in March 1994 in the pilot manipulation, we maintained our ex- perimental plots free of snakeweed until 1996, (Fig. 1). Population size dropped by 35% at which time drought had caused it to decline between August 1983 and March 1984. throughout the site. Current population density (in 2003) is still In August 1993, we sampled food plants of an order of magnitude lower than it was in kangaroo rats in 20 quadrats, 1 m2, on each of the early 1980s. the 4 experimental and 4 control plots. Rains On the Rucker site, population size also were late this year, and few plants had germi- declined after a peak in August 1982. The nated; we could identify only 7 herbaceous spe- magnitude of the decrease between August cies, most prominently Talinum auranticum and 1983 and March 1984 (36%) was similar to Eriogonum abertianum. that at Portal (Fig. 1). However, population Monitoring D. spectabilis on experimental trends at the 2 sites then diverged; the and control plots.ÐWe trapped D. spectabilis at Rucker population grew rapidly during the active mounds on all plots during the biannual censuses described above. Jones (1984) found early 1990s, even as the Portal population that some adults used Ͼ1 mound, but we estab- continued to decline. By 1994, when the lished by radiotracking that each mound's sole Portal population reached its nadir, the adult resident was reliably identi®able as the Rucker population had grown to levels sim- adult trapped there at least twice and more often ilar to those exhibited in the early 1980s. than any other adult. Similarly, juveniles were Recruitment and adult survival rates August 2003 WASER AND AYERSÐPOPULATION DECLINE OF KANGAROO RATS 1035 Downloaded from https://academic.oup.com/jmammal/article/84/3/1031/903815 by guest on 24 September 2021

FIG. 1.ÐPopulation density (animals/ha) of Dipodomys spectabilis during March censuses on the Rucker and Portal sites in southeastern Arizona, 1981±2001. Portal data are from the entire 64-ha study site, comprising 60.75 ha that was not manipulated along with 3.25 ha in the experimental plots. Because March censuses sample the population before most juveniles are old enough to enter traps, numbers primarily represent adults. Data from 1986±1989 are miss- ing for the Rucker site. were similar in the 2 populations during the early 1980s, starting high but declining in 1983±1985. By 1990, adult survival rates at FIG. 2.ÐDemographic trends on the Portal Rucker but not at Portal had returned to the and Rucker sites in southeastern Arizona, 1990± high level of the early 1980s. Adult surviv- 2000: a) annual adult survival rates, calculated al remained substantially higher at Rucker as the number of adults in year t ϩ 1 per adult than at Portal throughout most of the 1990s in year t, and b) recruitment rates, calculated as (Fig. 2a). Recruitment rates also were high- the number of 1-year-old females in year t ϩ 1 er at Rucker than at Portal during 1990± per adult female in year t. Adult survival rates 1993 but not during the late 1990s (Fig. were 0 in the Portal population from 1993 to 2b). Recruitment during the 1990s was re- 1995. lated linearly to fecundity (recruitment ϭ Ϫ0.01 ϩ 0.54 ϫ fecundity; n ϭ 22, R2 ϭ shrub species were particularly striking. 0.82), and differences in fecundity between Broom snakeweed increased more than 10- the 2 populations paralleled those in re- fold between 1982 and 1988. Although cruitment. snakeweed density declined thereafter, it Long-term trends in woody vegetation.Ð was still 7 times as high in 1993 as in 1982 On the Portal site, the proportion of quad- (0.80 stems/m2 Ϯ 0.10 compared with 0.12 rats containing shrubs and half-shrubs in- Ϯ 0.02 stems/m2; F ϭ 7.729, d.f. ϭ 1, 99, creased markedly during the study period P ϭ 0.007). Snakeweed plants commonly (Fig. 3). Increases in 2 half-shrub and 1 attain a diameter of 0.5 m, and by 1988 1036 JOURNAL OF MAMMALOGY Vol. 84, No. 3 Downloaded from https://academic.oup.com/jmammal/article/84/3/1031/903815 by guest on 24 September 2021

FIG. 3.ÐIncreases in the density of shrubs and half-shrubs (burroweed, Haplopappus tenuisec- tus, and broom snakeweed, Gutierrezia saroth- rae) on Portal plots in southeastern Arizona, 1982±1993. Error bars represent SE among FIG. 4.ÐNumbers of Dipodomys spectabilis plots. trapped on 1 pilot experimental and 2 control 1.00-ha plots on the Portal site in southeastern Arizona during March and August censuses. substantial parts of the site were covered Dashed vertical line indicates snakeweed remov- with a nearly continuous snakeweed ``can- al in November 1987. Error bars represent SE opy.'' Another half-shrub associated with among plots. overgrazing, burroweed, H. tenuisectus, was not detected on the site at all in the 1982 census but was found in 1988 and has The number of D. spectabilis trapped on the since increased rapidly (0.01 Ϯ 0.01 stems/ pilot experimental plot did not show an im- m2 in 1988, 0.50 Ϯ 0.08 stems/m2 in 1993). mediate positive response to snakeweed re- Shrub densities increased from 0.01 Ϯ moval, but by August 1988 (9 months after 0.01 stems/m2 in 1982 to 0.06 Ϯ 0.02 the manipulation), it had begun to climb stems/m2 in 1988 and 0.17 Ϯ 0.03 stems/ (Fig. 4). Meanwhile, numbers of D. spec- m2 in 1993. Increases in shrubs, together tabilis on the 2 pilot control plots slowly with the half-shrubs H. tenuisectus and Z. declined. During the 5 years before we re- pumila, were signi®cant (F ϭ 59.26, d.f. ϭ moved snakeweed, population sizes on the 1, 99, P Ͻ 0.0001). Most of the increase in experimental plot were always lower than shrub density was due to whitethorn acacia, those on 1 or both control plots, but during A. constricta. We found only a single Aca- the 5 postremoval years, rats on the exper- cia in 243 sample quadrats in 1982 but 21 imental plot were more common than they Acacia in 160 quadrats in 1993. Most Aca- were on either control plot during 7 of 10 cia specimens observed in the 1993 census censuses. were small in stature, suggesting that their Stem densities for food plants of kanga- germination occurred after 1982. roo rats in 1988 were substantially higher We detected no woody plants of any spe- on the experimental than on the control cies in quadrats on the Rucker site either in plots. Grasses were half again as common 1982 or in 1993. G. sarothrae and H. ten- on the experimental plot (58.2 plants/m2 uisectus occurred but at extremely low den- compared with 36.0 plants/m2; F ϭ 11.715, sities, and no shrubs were present on or d.f. ϭ 1, 126, P ϭ 0.0008). Differences near the site. were particularly striking for 2 annual Pilot woody vegetation manipulation.Ð grasses, B. aristidoides and Aristida ad- August 2003 WASER AND AYERSÐPOPULATION DECLINE OF KANGAROO RATS 1037

and signi®cant (F ϭ 30.857, d.f. ϭ 1, 6, P ϭ 0.001) throughout the 5 years after snakeweed removal, even after kangaroo rat populations on all plots began to increase coincident with the general decline of snakeweed in 1994±1996. Sample sizes are too small for detailed demographic analyses. However, because we know which individuals were resident

in which mounds, we can infer that 1 effect Downloaded from https://academic.oup.com/jmammal/article/84/3/1031/903815 by guest on 24 September 2021 of snakeweed removal was to attract ani- mals from beyond the boundaries of the ex- perimental plots. Before the manipulations, percentages of animals trapped that were ``visitors'' (animals not resident in mounds within the plot) were small (10%) on both control and experimental plots. During the FIG. 5.ÐNumbers of Dipodomys spectabilis 2 years after snakeweed removal, percent- trapped on 4 follow-up experimental and 4 con- age of visitors remained low (10%) on the trol 0.56-ha plots on the Portal site in south- control plots but increased to 30% where eastern Arizona during March and August cen- we removed snakeweed. suses. Dashed vertical line indicates snakeweed removal in October 1992. Error bars represent Most of the difference in numbers of res- SE among plots. idents trapped on control and experimental plots was due to the larger numbers of ju- veniles found on plots without snakeweed scensionis. Annuals and herbaceous peren- (14 versus 5). We cannot determine how nials were more than 3 times as common many of these 14 juveniles were born on where we had removed snakeweed (17.1 the plots, but because 6 were found on plots versus 5.6 plants/m2; F ϭ 15.404, d.f. ϭ 1, without resident females, local immigration 126, P ϭ 0.0001). Erodium cicutarium was was clearly important. Recruitment of new the strongest contributor to this trend, but adults was higher on experimental plots (7 Baileya multiradiata, C. bauhinoides, Eu- versus 2); the majority of these animals im- phorbia species, Pectis longipes, and Sida migrated from elsewhere on the Portal ®licauda also were found at least twice as study site. In addition, the proportion of often on the experimental plot. adults surviving per year was higher on ex- Follow-up woody vegetation manipula- perimental plots (0.3) than on control plots tion.ÐResponses of kangaroo rats to snake- (0.2). weed removal in the additional 4 experi- Our ability to detect an effect of snake- mental and 4 control plots paralleled those weed removal on herbaceous plants in in the pilot study. Before manipulation, summer 1993 was compromised by low numbers of D. spectabilis captured on ex- summer rainfall. The few herbaceous perimental and control plots were similar plants that were present in August 1993 and slowly declining. After manipulation, did not differ in density between experi- populations on the control plots continued mental and control plots (F ϭ 0.001, d.f. to decline, decreasing to zero on all 4 rep- ϭ 1, 6, P ϭ 0.98). licates within 1 year. In contrast, popula- tions on the experimental plots remained DISCUSSION stable (Fig. 5). Differences between control Three types of data indicate a negative and experimental plots remained consistent effect of woody vegetation on numbers of 1038 JOURNAL OF MAMMALOGY Vol. 84, No. 3

D. spectabilis: the temporal relationship soils or overgrazing (Cole et al. 1977; of population declines with increases in James et al. 1991). It is an aggressive com- shrubs and half-shrubs on the Portal site, petitor on degraded rangelands, and grasses the lack of a population decline on the are known to increase after its removal shrub-free Rucker site, and the clear pos- (McDaniel et al. 1982). D. spectabilis is itive effects of snakeweed removal. In known to cache seeds of most of the grass fact, the primary effect of our woody veg- and large-seeded herbaceous species that etation manipulation was to halt the de- increased in density after our 1988 manip- cline in D. spectabilis that was occurring ulation (Monson and Kessler 1940; Reich- on the Portal study site. During the mid- man et al. 1985; Vorhies and Taylor 1922). Downloaded from https://academic.oup.com/jmammal/article/84/3/1031/903815 by guest on 24 September 2021 1990s, our experimental plots were almost Erodium cicutarium, a large-seeded inva- the only patches of relatively open habitat sive annual that responded particularly remaining on the Portal site, and most strongly to the absence of snakeweed (or to members of the Portal population lived on the physical disturbance we caused by or adjacent to them. The partial recovery hand-weeding), is used heavily by several of the Portal population in the late 1990s, species of kangaroo rats including D. spec- after a general die-off of snakeweed in tabilis (Fitch 1948; Monson and Kessler 1993±1995, is also consistent with this in- 1940; Reichman 1975; Schiffman 1994; terpretation. Shaw 1934). On the other hand, D. spec- Valone et al. (1995) suggested that pop- tabilis also caches seeds of snakeweed ulations of D. spectabilis can respond (Monson and Kessler 1940; Reichman et al. negatively in the short term to periods of 1985). Some species that it commonly uses extremely heavy rainfall. Populations on (e.g., Eriogonum abertianum and Talinum the Portal and Rucker sites, the Brown± auranticum) did not show a clear response Valone site, and another study site about to snakeweed removal. The removal itself 3 km W of it (J. Randall, in litt.) declined had no demonstrable effect on densities of during the mid-1980s after a wet El NinÄo herbaceous plants in the dry summer of year. However, the precise timing of the 1993. declines differed. Most of the decline on We interpret our results as a response to our Portal site occurred between August the increased representation of open micro- and October 1983, slightly before the habitat produced by our manipulation rather population crash on the Brown±Valone than to any speci®c effect of snakeweed. site; the decline on our site was much Although snakeweed removal halted the de- more gradual and did not result in extinc- cline of D. spectabilis at Portal and a gen- tion. The lowest adult survival rates ob- eral snakeweed die-off in the mid-1990s co- served on our Rucker site did not occur incided with a modest recovery of kangaroo until a year after the decline on the rats there, densities at Portal remain far be- Brown±Valone site. It is possible that low those on the Rucker (grassland) site or short-term ¯uctuations in numbers of D. on the Portal site in the early 1980s, at spectabilis re¯ect some consequence of which time shrubs and half-shrubs in gen- rainfall, but these ¯uctuations appear to eral were much less common. be superimposed on those caused by lon- Our results are qualitatively similar to ger-term changes in woody vegetation. those of habitat manipulations in other Are the positive consequences of our ex- communities of heteromyid . Den- periments on numbers of kangaroo rats a sities of D. merriami decreased when cover speci®c effect of snakeweed? One possibil- was added (Rosenzweig 1973; Thompson ity is that snakeweed (or its removal) in¯u- 1982b). Numbers of D. merriami (Price ences food availability. Gutierrezia is wide- 1978a), D. ordii (Whitford et al. 1978), and ly considered to be an indicator of poor D. stephensi (Price et al. 1994) increased August 2003 WASER AND AYERSÐPOPULATION DECLINE OF KANGAROO RATS 1039 after reduction in shrub density. Numbers tional support for the idea that preferences of D. agilis (Price and Waser 1984) and D. for open microhabitat increase survival. stephensi (Price et al. 1995) increased after Adult survival rates at Portal were highest destruction of vegetation by ®re. These par- in the early 1980s, when woody plant cov- allels led us to infer that D. spectabilis is er was lowest, and during the 1990s, they responding negatively to some aspect of were nearly always higher at Rucker, the ``lack of openness'' rather than to snake- more open site, than at Portal. weed per se. Our results also support the idea that Numerous authors have presented hy- preferences for open microhabitat, al- potheses on why kangaroo rats avoid closed though probably present in all kangaroo Downloaded from https://academic.oup.com/jmammal/article/84/3/1031/903815 by guest on 24 September 2021 microhabitats. Open microhabitats may fa- rats, are stronger in larger species. Num- vor plants producing preferred, larger seeds bers of smaller species trapped on our ex- (Hutto 1978; M'Closkey 1980), concentrate perimental plots, primarily D. merriami, seeds in larger, more widely scattered did not differ between treatments (Ayers clumps (Price 1978b, 1986; Reichman and 1994), and populations of D. merriami or Price 1993), be associated with soil types D. ordii have not declined on the Brown± from which kangaroo rats extract seeds Valone site even though it has become more ef®ciently (Price and Waser 1985; brushier (Brown et al. 2001; Valone et al. Price et al. 2000), or allow more unimpeded 1995). On the open site, Rucker, D. mer- mobility, thereby increasing their ef®ciency riami and D. ordii have never represented in gathering food or reducing their vulner- more than 2% of the kangaroo rats cap- ability to raptors (Bowers 1982; Brown et tured during our censuses (P. M. Waser, in al. 1988; Kotler 1984; Kotler and Brown litt.). Several investigators of kangaroo rat 1988; Thompson 1982b; but see Longland populations in decline have commented and Price 1991). Our data cannot separate on the apparent negative effect of shrubs these possibilities, but we can address a re- or dense exotic grasses (Congdon and lated question (Price 1986): what ®tness Roest 1975; Goldingay et al. 1997; Price components (if any) do these preferences et al. 1994; Williams and Germano 1992). affect? Germano et al. (2001) showed that several As in most of the microhabitat manip- species of kangaroo rat have been affected ulation studies cited above, ``visits'' and adversely by the spread of alien grasses immigration were major contributors to that impede movement. Our results are the increase in kangaroo rat numbers on consistent with these speculations in that our experimental plots. Thus, such exper- they imply a negative effect of structur- iments clearly demonstrate the existence ally closed microhabitat on survival of of microhabitat preferences, but evidence kangaroo rats. that these preferences increase survival is During the last century, woody vegeta- less de®nite. However, that numbers of tion has increased at the expense of native kangaroo rats remained stable on our ex- grassland throughout much of the south- perimental plots while they were declin- west United States, responding to some ing to extinction on the adjacent Brown± combination of grazing pressure, lack of Valone site and on most of the rest of our ®re, and (recently) wetter winters (Bahre Portal site implies that preference for and Shelton 1993; Brown and Archer 1999; open microhabitat has positive conse- Brown et al. 1997; Chew 1982; Cole et al. quences for ®tness. Although our experi- 1977; Valone and Kelt 1999). Whatever the mental plots or our sample sizes were too cause, our results make it clear that the in- small to detect signi®cant effects of mi- vasion of woody vegetation is detrimental crohabitat on demography, our long-term to D. spectabilis. However, when popula- demographic data provide strong correla- tion densities are not too low, our data also 1040 JOURNAL OF MAMMALOGY Vol. 84, No. 3 imply that even relatively small patches of LITERATURE CITED open habitat can have positive consequenc- AYERS, J. M. 1994. Population decline in banner-tailed es for the persistence of kangaroo rat pop- kangaroo rats (Dipodomys spectabilis) in southeast- ulations. ern Arizona. M.S. thesis, Purdue University, West Lafayette, Indiana. BAHRE,C.J.,AND M. L. SHELTON. 1993. Historic veg- RESUMEN etation change, mesquite increases, and climate in El nuÂmero de ratas canguro de cola southeastern Arizona. Journal of Biogeography 20: 489±504. abanderada Dipodomys spectabilis,ha BEST, T. L. 1972. Mound development by a pioneer disminuido dramaÂticamente en casi todas population of the banner-tailed kangaroo rat, Dipo- las poblaciones seguidas en los uÂltimos 20 domys spectabilis. American Midland Naturalist 87: Downloaded from https://academic.oup.com/jmammal/article/84/3/1031/903815 by guest on 24 September 2021 anÄos en el SE de Arizona. En este aÂrticulo 201±206. BOWERS, M. A. 1982. Foraging behavior of heteromyid aprovechamos de describir los cambios rodents: ®eld evidence of resource partitioning. Jour- vegetacionales y presentamos los resulta- nal of Mammalogy 63:361±367. dos de la manipulacioÂn experimental en la BOWERS, M. A. 1986. Geographic comparison of mi- crohabitats used by three heteromyids in response to cual se corto la hierba-culebra (Gutierre- rarefaction. Journal of Mammalogy 67:46±52. zia sarothrae) en cuadrantes de 1.00-ha BOWERS,M.A.,AND J. H. BROWN. 1992. Structure in (piloto) o 0.56-ha (replicas de seguimien- a desert rodent community: use of space around Di- podomys spectabilis mounds. Oecologia 92:242± to). D. spectabilis se extinguio en los 249. cuadrates control, en tanto que se mantu- BOWERS, M. A., D. B. THOMPSON, AND J. H. BROWN. vo estable en los cuadrantes donde se 1987. Spatial organization of a desert rodent com- munity: food addition and species removal. Oeco- mantuvo la hierba-culebra. La disminu- logia 72:77±82. cioÂn del nuÂmero de ratas canguro coinci- BROWN, J. H., D. W. DAVIDSON,J.C.MUNGER, AND R. dio con el aumento, en escalas de mayor S. INOUYE. 1986. Experimental community ecology: the desert granivore system. Pp. 41±61 in Commu- tamanÄo, de las especies arbustivas. Los nity ecology (J. Diamond and T. J. Case, eds.). Harp- datos apoyan la preferencia de esta espe- er & Row, New York. cie por micro-haÂbitats estructuralmente BROWN, J. H., AND B. A. HARNEY. 1993. Population abiertos y ademas documentan que las tas- and community ecology of heteromyid rodents in temperate habitats. Pp. 618±651 in Biology of the as de sobrevivencia son mas altas en las (H. H. Genoways and J. H. Brown, areas mas abiertas. Ratas canguro grandes eds.). Special Publication, American Society of como D. spectabilis son a menudo consi- Mammalogists 10:1±719. BROWN,J.H.,AND E. J. HESKE. 1990. Control of a deras como especies clave y nuestros re- desert-grassland transition by a keystone rodent sultados indican que esta especie es vul- guild. Science 250:1705±1708. nerable a la degradacioÂn de la pradera. BROWN,J.H.,AND J. C. MUNGER. 1985. Experimental manipulation of a desert rodent community: food addition and species removal. Ecology 66:1545± CKNOWLEDGMENTS A 1563. We thank L. Elliott, N. Link, and B. Keane BROWN, J. H., T. J. VALONE, AND C. G. CURTIN. 1997. for their unstinting assistance in plant sam- Reorganization of an arid ecosystem in response to recent climate change. Proceedings of the National pling, kangaroo rat trapping, and weeding Academy of Sciences 94:9729±9733. thousands of snakeweed plants. We bene®ted BROWN, J. H., T. G. WHITHAM,S.K.M.ERNEST, AND greatly from discussions with, and comments C. A. GEHRING. 2001. Complex species interactions from, J. Brown, R. Chew, M. Price, G. Rath- and the dynamics of ecological systems: long-term bun, T. Valone, N. Waser, J. Winters, and 2 experiments. Science 293:643±650. BROWN,J.R.,AND S. ARCHER. 1999. Shrub invasion anonymous reviewers. We thank 2 generations of grassland: recruitment is continuous and not reg- of the Krentz family for their willingness to ulated by herbaceous biomass or density. Ecology let us work on their ranch and the Piedras 80:2385±2396. Blancas Field Station for housing during man- BROWN, J. S., B. P. KOTLER,R.J.SMITH, AND W. O. uscript preparation. We thank I. M. Ortega for WIRTZ II. 1988. The effects of owl predation on the foraging behavior of heteromyid rodents. Oecologia the Spanish translation. Work was funded in 76:408±415. part by the National Science Foundation (DEB CHEW, R. M. 1982. 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