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Western North American Naturalist

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COMMUNITY STRUCTURE OF ELEODES BEETLES (COLEOPTERA: TENEBRIONIDAE) IN THE SHORTGRASS STEPPE: SCALE-DEPENDENT USES OF HETEROGENEITY

Nancy E. McIntyre1

ABSTRACT.—Patterns in the community structure of darkling beetle (9 Eleodes spp., Coleoptera: Tenebrionidae) assemblages in the shortgrass steppe of north central Colorado were monitored by live pitfall trapping for 4 summers. There were significant correlations among weather (temperature and precipitation), species richness, and number of individuals per species captured; effects from weather conditions also displayed 1-month and 1-yr delayed effects. Population densities of 2 eleodid species were monitored by mark-recapture methods. Densities of these species varied relatively little among years and sites, although density was correlated with temperature and precipitation. Abiotic influences on both density and richness differed between 2 macrohabitat types (shortgrass upland, shrub floodplain). The 4 largest species were most abundant in the floodplain, whereas the smallest species was most common in the upland. Affinities with cactus and shrub microhabitats (and an avoidance of bare soil) were evident, although a preference for shaded microhabitats was not detected. These results do not conform well to previous explanations of why darkling beetle assemblages are spatially and temporally heterogeneous, which primarily focused on predation and thermoregulation. Therefore, an alternative mechanism concerning scale-dependent uses of heterogeneity and mobility is proposed to account for eleodid community patterns.

Key words: Coleoptera, community diversity, darkling beetle, Eleodes, population density, precipitation, richness, shortgrass steppe, temperature, Tenebrionidae.

The shortgrass steppe of western United Upon eclosion, they may live for 2 yr as adults States is one of the least studied ecosystems in (Allsopp 1980). Adults are detritivorous, feed- North America. Disparagingly called “the Great ing mainly on grasses and forbs, and there is a American Desert” by early explorers and home- high degree of dietary overlap among species steaders because of its apparent monotony and (Yount 1971, Doyen and Tschinkel 1974, Slo- harsh climate, this biome is in fact a spatio- bodchikoff 1978, Rogers et al. 1988). Although temporally dynamic ecosystem (Knopf and flightless, the beetles are highly mobile and Samson 1997). The long-standing and persis- wander over great distances (Kramm and tent misperception of the shortgrass steppe as Kramm 1972, Calkins and Kirk 1973, Doyen homogeneous may stem from the coarse per- and Tschinkel 1974). Individuals are active ceptual scale of observers. Many of its other when temperatures permit. On the southern occupants, however, may more readily per- shortgrass steppe and in desert ecosystems, ceive the heterogeneous nature of the short- activity is usually crepuscular and nocturnal grass steppe, owing to differences in body size from spring through autumn; on the northern and mobility. In this paper I examine evidence shortgrass and mixed-grass prairies and shrub- for scale-dependent uses of heterogeneity in steppe, darkling beetles are mostly diurnal from various species of darkling beetle (Eleodes late spring through early autumn, with peaks spp., Coleoptera: Tenebrionidae) of the north- of activity in early morning and early evening ern shortgrass steppe of Colorado. (Kramm and Kramm 1972, Wise 1981b, Kenagy Darkling beetles (eleodids) are among the and Stevenson 1982, Richman et al. 1982, most abundant macroarthropods of the short- Whicker 1983, Marino 1986, Whicker and grass steppe, with as many as 9 species occur- Tracy 1987, Stapp 1997a). More detailed infor- ring in narrow sympatry (Bell 1971, Kumar et mation on darkling beetle ecology may be found al. 1976). They live most of their lives as soil- in Doyen and Tschinkel (1974), Allsopp (1980), inhabiting larvae that feed on roots and detritus. Parmenter and MacMahon (1984), Sheldon

1Department of Biology, Colorado State University, Fort Collins, CO 80523-1878. Present address: Center for Environmental Studies, Arizona State Univer- sity, Box 873211, Tempe AZ 85287-3211.

1 2 WESTERN NORTH AMERICAN NATURALIST [Volume 60 and Rogers (1984), Whicker and Tracy (1987), shaded, artificially shaded, and unshaded traps. Rogers et al. (1988), and Parmenter et al. I then tested 2 alternative hypotheses (B1 and (1989b). B2, below) regarding the relationships among The similarity of life history, diet, range, and predation risk, body size, and shrub cover. behavior among species prompts the question Although eleodids can produce unpalatable of how the darkling beetle community is quinones when threatened with predation structured in space and time. Factors that (Tschinkel 1975a), they are sometimes preyed account for spatio-temporal patterns of dark- upon by birds and rodents (Wiens et al. 1974, ling beetle community composition have been Wiens and Rotenberry 1979, Stapp 1997b). If subject to much speculation by past researchers. eleodids partition habitat according to risk of A high degree of niche overlap suggests that predation, then that partitioning may take 1 of environmental factors may play more impor- 2 forms as related to body size: tant roles in structuring eleodid assemblages and populations than do biotic factors such as (B1) Larger species, being more obvious to ver- competition and predation (Wiens and Roten- tebrate predators, should be more abundant berry 1979, Wise 1981a; but see Abrams 1980), in areas with greater shrub coverage because which may play only minor roles in determin- shrubs serve as refugia from predators; ing the abundance and distribution of darkling smaller eleodids, being less vulnerable to beetles (Wise 1981a, 1985, Parmenter and predation because of their more inconspicu- MacMahon 1988). ous size, should be widespread. Previous studies have demonstrated that (B2) Smaller species should be more abundant in darkling beetle activity and occurrence are areas with numerous refugia from predators (i.e., areas with finely textured clays with influenced by various environmental factors, cracks that serve as refugia; such soils do not including soil texture (Calkins and Kirk 1975, support high densities of shrubs); larger Krasnov and Shenbrot 1996, 1997, Stapp 1997a), species, being less vulnerable to predation abundance of food resources (McIntyre 1997), because of their size (being unmanageably shrub cover (Parmenter et al. 1989b, McIntyre large for a predatory rodent or bird), should 1997, Stapp 1997a), and thermoregulatory be widespread (Stapp 1997a, 1997b). resources (Rickard 1971, Slobodchikoff 1983, Whicker 1983, Whicker and Tracy 1987, Par- To test these hypotheses, I compared the pres- menter et al. 1989c). However, none of these ence and abundance of eleodids that differ in studies examined the interaction between abi- body size in areas differing in amount of shrub otic (weather) and environmental factors in cover. influencing eleodid communities and popu- Eleodid species exhibit different prefer- lations. In this study, I investigated habitat ences in ambient temperatures in which they occupancy at 2 spatial scales and variations in are active, perhaps reflecting species-specific eleodid density and diversity over a 4-yr period. differences in ability to conserve water (Kramm In particular, I focused on how eleodids re- and Kramm 1972, Campbell and Smith 1975, spond to temperature, precipitation, and the Slobodchikoff 1983, Whicker 1983, Whicker presence of shrubs. and Tracy 1987, Parmenter et al. 1989c). I Some eleodid species are more abundant in therefore examined 2 hypotheses of how eleo- and move to areas with greater shrub cover did richness and abundance might vary with (Parmenter and MacMahon 1988, McIntyre temperature and precipitation. Because tem- 1997), possibly because shrubs provide pro- perature and precipitation are negatively cor- tection from vertebrate predators (Parmenter related variables, these hypotheses combine and MacMahon 1988, Stapp 1997b) as well as both temperature and precipitation rather shade. I investigated both factors. than test each variable singly: Hypotheses (C1) If eleodids are heat sensitive, they should First, I tested the hypothesis (A1) that eleo- vary negatively with temperature and posi- dids prefer shrub-dominated areas because of tively with precipitation. thermoregulatory resources that shrubs pro- (C2) If eleodids are cold sensitive, they should vide. This hypothesis was addressed by com- vary positively with temperature and nega- paring pitfall-trap captures among naturally tively with precipitation. 2000] ELEODES COMMUNITY STRUCTURE 3

Inasmuch as the shortgrass steppe is in the creek channels. Soapweed (Yucca glauca) is cool-temperate zone, I assumed that tempera- abundant on rocky hilltops. Prickly-pear cac- ture and precipitation should have a negative tus (Opuntia polyacantha), found throughout relationship with species richness and abun- the region, is especially abundant in upland dance. Because shrubs can provide both cooler- areas with finely textured soils. There are also and warmer-than-ambient microclimates at numerous small areas of bare ground and veg- different times of day (Stapp 1997a), however, etative detritus (McIntyre 1997). There is little hypotheses C1 and C2 were modified to gen- free-standing permanent water, with the few erate the following hypothesis, which was stream channels present containing water only tested against the null hypothesis that eleo- sporadically in most locations. Topography, soils, dids are indifferent to temperature: climate, and biota of the shortgrass steppe have been described in more detail by Lauen- (D1) Eleodids in areas with lower shrub coverage roth and Milchunas (1991). should exhibit a greater number of strong Visually, the shortgrass steppe appears to correlations with weather variables than bee- be composed of 2 coarsely defined habitat types tles in areas with greater shrub coverage. that extend for dozens of square kilometers: Results from these tests are discussed with upland areas dominated by shortgrasses with respect to interactions between darkling bee- few shrubs and lowland floodplains with num- tle presence and abundance, body size, and erous shrubs. To determine whether this macro- movement capacity and mobility, producing habitat categorization was valid, 6 circular 2 new insights into how spatio-temporal varia- 638-m sites were used. Three of these sites tions in eleodid community structure may be were located in each of the 2 putative macro- an expression of the different ways in which habitat types. Within a macrohabitat, sites were different species interact with the same spatial separated by 1–3 km; a 4-km separation existed structure. between sites differing in macrohabitat type. Vegetational composition (proportion of grass/ METHODS forb, shrub, bare soil, cactus, and vegetative detritus) was measured at each site in July of Study Site each year by determining percent basal cover Research was conducted during May–August along 2 randomly located 29.25-m line-inter- 1994–1997 at the 6280-ha Central Plains cept transects (diameter of trapping-area Experimental Range (CPER) on the Pawnee circle). A hierarchical cluster analysis (using National Grassland, Colorado. Characterized average-neighbor distances and pooled covari- by gently rolling topography, the site pos- ance matrices) was then performed on the arc- sesses primarily sandy loam and loamy sand sine/square-root transformed percentages, with soils. Approximately 1630 m in elevation ASL, clustering distance correlations >0.50 accepted the area receives 322 mm average annual pre- as clusters. Cluster analysis provided a means cipitation, generally in the form of spring rains of quantifying similarities and differences in and summer convective thunderstorms. The the 6 sites rather than relying on subjective climate is semiarid, with mild summers and categorization ( Johnson and Wichern 1992). cold, dry winters. Perennial warm-season C4 Soil type and elevation at each site were also shortgrasses (primarily Bouteloua gracilis and recorded. Buchloë dactyloides) comprise most of the Community Richness vegetative biomass (Lauenroth and Milchunas 1991). Forbs (particularly Aster tanacetifolia, Darkling beetles were live-trapped in 480 Astragalus spp., Gaura coccinea, Helianthus pitfall traps in six 638-m2 trapping webs of 80 petiolaris, Leucocrinum montanum, Lomatium unbaited traps each. One trapping web was cous, Oenothera albicaulis, Oxytropis spp., situated in each of the 6 study locations. Each Plantago patagonica, Sphaeralcea coccinea, pitfall trap was a 500-mL Barber-style trap and Thelesperma filifolium) account for most (Weeks and McIntyre 1997). Traps were spaced vegetative diversity of the ecosystem. There 1.5 m apart in 8 lines along the 8 primary car- are also low shrubs (Atriplex canescens) in dinal directions to create 10 concentric rings sandy floodplains associated with ephemeral of traps (McIntyre 1995). Traps were checked 4 WESTERN NORTH AMERICAN NATURALIST [Volume 60 once daily for 7 consecutive days (6 nights) not perform well for highly mobile organisms during the 3rd wk of each month from May such as darkling beetles (Parmenter et al. through August 1994–1997 (46,080 total trap- 1989a), producing inflated density estimates, it nights). Changes in community composition has been used in a variety of field studies with month and year were noted by assessing (Anderson et al. 1983, Parmenter et al. 1989a, eleodid species richness each month from May McIntyre 1995) and performs well when cap- through August of each year for each trapping ture rates are not extremely low (<15 individ- web. uals). Low capture rates necessitate calculat- Weather data have been collected daily at ing density either from number of animals the CPER since 1961, and data for the period trapped per area (which may give inflated 1961–1990 were compiled to give 29-yr aver- density estimates) or from data pooled among ages in precipitation and temperature (com- dates or sites to calculate density for coarser piled weather data at Internet sites http://lter- spatio-temporal scales (Anderson et al. 1983). net.edu/im/climate/climdes/sgs/sgsclim.htm Numbers of E. extricata and E. hispilabris and http://sgs.cnr.colostate.edu/data/data cat/ were tallied each month from May through climateindex.html). Weather data collected dur- August of each year for each trapping web. ing the weeks I trapped were compared to Preliminary analyses revealed that capture these 29-yr averages. A Spearman rank corre- rates were highly variable. Variation in capture lation was used to detect a significant relation- rates may cause some assumptions to be vio- ship among species richness, daily minimum lated and thus can bias density estimations and maximum air temperatures, and daily made with DISTANCE, but this can be cor- amount of precipitation averaged over each rected by pooling data across time (Buckland trapping week. Rank correlations were also et al. 1993, Laake et al. 1994). Therefore, data performed on temperature and precipitation were pooled across months and density calcu- data with 1-month and 1-yr time lags to deter- lated for each year for each trapping web. mine whether eleodids exhibit a delayed re- Ninety-five percent confidence intervals (95% sponse to weather. Because many climatic CI) were constructed around the mean esti- variables are non-monotonic, making linear mated density of individuals per square meter regression susceptible to biases from data within each trapping web. Densities in trap- points at the extremes of the response distribution, outliers (defined as occurring ≥2 stan- ping webs where <15 beetles were captured were estimated as number of beetles caught dard deviations away from the mean) were 2 omitted from analyses. per trapping web area (638 m ) and have no confidence intervals associated with them. A Population Density Estimation Spearman correlation was used to detect sig- Eleodes extricata and E. hispilabris individ- nificant relationships among beetle densities, uals that were captured in the pitfall trapping daily minimum and maximum air tempera- array were marked on the elytra with colored tures, and daily amount of precipitation. Corre- enamel paint to distinguish recaptured indi- lations were also performed on temperature viduals from new captures. These 2 species and precipitation data with 1-month and 1-yr were chosen for population monitoring because time lags. they are among the most widespread and abun- Multiple-scale Habitat Analyses dant eleodids at CPER (Bell 1971, Whicker 1983, McIntyre 1997). The computer package Differences in macrohabitat use by eleo- DISTANCE was used to estimate population dids were assessed with analysis of variance densities of these species (Buckland et al. 1993). (ANOVA), using clusters from the hierarchical DISTANCE uses distance-sampling theory, cluster analysis based on vegetation as blocks whereby the spacing between captures is used of variance. Species richness and population to derive significantly fitted models of detec- density were compared among blocks. Signifi- tion probabilities to estimate population den- cant factors in ANOVA models were then com- sity (Wilson and Anderson 1985, Laake et al. pared among blocks with Tukey’s Studentized 1994). Only new captures are used in fitting Range (HSD) test for post-hoc comparisons. these models so as to eliminate bias from trap- To assess differences in microhabitat use by happy individuals. Although DISTANCE may eleodids, a 25-cm-diameter circle centered on 2000] ELEODES COMMUNITY STRUCTURE 5 each pitfall trap was characterized by the fol- RESULTS lowing microhabitat types: grass, bare ground General Community Patterns (unvegetated areas at least as large as the opening of a pitfall trap), cactus, vegetative Nine darkling beetle species were captured detritus, and shrub. Each trap was then cate- (Figs. 1, 2). ANOVA revealed that there were gorized as having caught either at least as significant differences in species richness many as or fewer than the average number of among months within 1995 but not within the eleodid individuals (obtained by taking the other years (Table 1). In 1995 the highest total number of individuals captured in a trap- diversity of species was trapped in August; ping web during a given year and dividing by trapping in May, June, and July captured simi- the 80 traps present in a web). Trap “success” lar numbers of species (HSD = 2.09, df = 20, was therefore a binary quantity comprising 2 P < 0.05). Significantly more species were mutually exclusive categories. Representing trapped in each of the 6 trapping sites in 1997 trap success as a binary quantity in this man- than in the other 3 yr (HSD = 1.99, df = 92, P ner rather than as a continuous response vari- < 0.05). able circumvents the assumption that the data For abundance, significant differences among assume a Poisson distribution, which is not months were found in 3 of 4 yr studied (1994, present in this case (mean and variance dif- 1995, and 1997; Table 1). In 1994 the greatest χ2 fered significantly, = 960.65, P = 0.0001). number of eleodid individuals was trapped in Binomial logistic regression was used to corre- May, with the remaining 3 months not signifi- late a trap’s success with the microhabitats cantly different from one another (HSD = surrounding it. Data were pooled by site and 3.96, df = 20, P < 0.05). In 1995 the reverse year; pooling is justified because calculating was true, with significantly more individuals trap success in the manner described above per species being captured in June, July, and accounts for any among-site and -year varia- August than in May (HSD = 3.96, df = 20, P tion and allows for general trends to emerge. < 0.05). In 1997 most individuals were cap- If eleodids are attracted to certain microhabi- tured in July, least in June (HSD = 3.96, df = tat types, then traps surrounded by those 20, P < 0.05). Significantly more individuals microhabitats should capture more beetles (as for each of the 9 species were trapped in 1994 determined by a Wald χ2 analysis; SAS Insti- than in the other years, and the least number tute Inc. 1996). of eleodids was captured in 1995 (HSD = Effects of Shade 1.99, df = 92, P < 0.05). on Eleodid Captures Of the 9 eleodids captured, most were One of the 3 shrub-floodplain sites (site 4) found throughout the 4-month trapping period. was selected at random for experimental Certain species, however, were more abun- manipulation of the effects of shade on eleodid dant early in the season (E. extricata and E. captures. Each of the 80 pitfall traps present fusiformis), whereas others were more com- was classified as being naturally shaded by mon in late summer (E. longicollis and E. shrubs or unshaded (following the criterion of obsoleta). E. suturalis and E. tricostata were Rickhard and Haverfield 1965). A random most abundant in midsummer. All 9 species subset of the unshaded traps was provided were captured each year. with artificial shade in the form of paper Multiple-scale Habitat Analyses “parasols” (25-cm-diameter circles supported atop 20-cm-high nails placed adjacent to a Cluster analysis quantitatively supported trap). To provide a balanced design, equal num- the visual separation of 2 macrohabitat types bers of naturally shaded, artificially shaded, within the shortgrass steppe, based upon per- and unshaded traps were selected at random cent basal vegetation coverage (basal branch- for analysis (N = 26 traps per 3 treatments). ing of sites 1–3: normalized root mean squared These traps were open for 6 consecutive days correlation = 0.61; basal branching of sites in July 1994, with eleodid captures in each 4–6: normalized root mean squared correla- trap type tallied each day. Average eleodid tion = 0.77). Three trapping webs were located captures were then compared among trap types within upland shortgrass areas (sites 1–3), using a Kruskal-Wallis test. which were characterized by extensive grass 6 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 1. Species composition (%) of pitfall-trap captures by month for shortgrass upland macrohabitat. Years (1994–1997) pooled. Species marked with an asterisk (*) comprised <1% of captures for all months. Species marked with a dagger (†) were not captured in any month. coverage (mean basal ground cover = 86.97%), = 1, P = 0.0001) as well as year (F = 7.79, df few shrubs (1.53%) and cactus (0.92%), little = 3, P = 0.0020) and month (F = 5.34, df = vegetative detritus (1.21%), and moderate 3, P = 0.0024). amounts of bare ground (7.13%). These sites More eleodid species were trapped in flood- had fine sandy loam soils and averaged 1643 plains than in uplands (F = 203.86, df = 1, m in elevation. The other 3 trapping areas P = 0.0001; HSD: 2.825, df = 64, P < 0.05). were located within shrub floodplains (sites Densities of E. extricata and E. hispilabris, 4–6) and had higher amounts of shrubs however, did not differ significantly between (14.66%), vegetative detritus (5.12%), cactus the 2 macrohabitats (Fig. 3; E. extricata: F = (1.08%), and bare ground (16.80%) but less 0.98, df = 7, P = 0.4778; E. hispilabris: F = extensive grass coverage (60.65%). These sites 1.12, df = 7, P = 0.3972) or among years (E. had loamy and loamy sand soils and averaged extricata: F = 1.78, df = 3, P = 0.1921; E. 1621 m in elevation. Significant correlates with hispilabris: F = 1.17, df = 3, P = 0.3520), eleodid species richness among the 6 trapping probably because of high variance associated areas were macrohabitat type (F = 203.86, df with the density estimates. 2000] ELEODES COMMUNITY STRUCTURE 7

Fig. 2. Species composition (%) of pitfall-trap captures by month for shrub floodplain macrohabitat. Years (1994–1997) pooled. Species marked with an asterisk (*) comprised <1% of captures for all months.

Some significant microhabitat affinities were TABLE 1. ANOVA results for differences in number of revealed. Traps located near cactus caught an species (richness) and abundance among months for average of 1 more beetle per trap than did 1994–1997; ns = not significant. traps where cactus was absent (model good- Year F df P ness-of-fit: log-likelihood = 107.9292, P = 0.0000; χ2 = 12.2047, P = 0.0005). A similar ------Effect: richness among months ------relationship was noted for traps near shrubs, 1994 2.43 3 0.0956 ns 1995 6.03 3 0.0043 which caught an average of 3 more individuals 1996 0.55 3 0.6571 ns per trap (model goodness-of-fit: log-likelihood 1997 0.69 3 0.5709 ns = 49.1869, P = 0.0000; χ2 = 11.8918, P = 0.0006). Conversely, traps located near bare ------Effect: abundance among months ------ground caught an average of 2 fewer beetles 1994 13.96 3 0.0001 per trap (model goodness-of-fit: log-likelihood 1995 4.32 3 0.0167 = –132.3717, P = 0.0000; χ2 = 5.3276, P = 1996 1.12 3 0.0719 ns 0.0210). No significant relationships were 1997 3.35 3 0.0395 8 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Shrub Cover, Predation Risk, and Body Size Although most species were widespread, certain species attained higher numbers in one or the other macrohabitat type (Table 2; Figs. 1, 2). The larger species (E. hispilabris, E. longicollis, E. obscura, and E. suturalis) were more abundant in the shrub floodplains (body size information from Whicker 1983 and Crist et al. 1992), and one of these (E. longicollis) occurred only in the shrub-floodplain sites. The smallest species (E. extricata) was more common in the shortgrass uplands, but it over- laps considerably in size with other species that were more abundant in floodplain sites (E. fusiformis and E. tricostata), found only in floodplain sites (E. opaca), or were equally abundant in both macrohabitat types (E. obsoleta). Weather Precipitation was highly variable in timing and amount during the 4-yr study period (Table 3). While 1994 was drier than the 29-yr average, the years 1995–1997 were wetter. There was also variation among months within each year, with May receiving most precipitation in most years (except 1997, when August received the most rainfall). The years of my study were also cooler than the 29-yr average. Although maximum daily air temperatures in 1994 and 1995 fell within the 29-yr range, 1996 and 1997 were consistently cooler by Fig. 3. Average estimated population density for E. ° extricata (top) and E. hispilabris (bottom) in 2 macrohabitat 2–3 C. types (shortgrass upland and shrub floodplain) at the Cen- Some weather variables were significantly tral Plains Experimental Range, Colorado, 1994–1997. correlated with richness during some months Open bars represent shortgrass upland sites; filled bars and years in certain trapping sites. For example, represent shrub floodplain sites. Note differences in scale of y-axes. Density values are averaged across the 3 sites precipitation levels were significantly nega- within each of 2 macrohabitat types for clarity of presenta- tively correlated with eleodid species richness tion. Confidence intervals are not shown for sake of clarity only at 2 trapping sites in a single year (Table (site and year effects nonsignificant; see text for statistics). 4). The number of species trapped at sites 1, 2, and 6 in 1995 was positively correlated with maximum air temperature and negatively correlated with minimum air temperatures and noted for the presence of grass or vegetative daily air temperatures. Other relationships detritus. were not significant. Differences in captures There were also some significant effects on with shade eleodid richness from weather conditions of the previous year or month, and these effects No significant differences were found in were also mediated by site. Temperatures in average eleodid captures among naturally 1994 were significantly correlated with rich- shaded (39.8 individuals), artificially shaded ness at trapping site 1 in 1995, for example, (40.5), and unshaded (36.6) pitfall traps (χ2 = and temperatures in the summer of 1995 sig- 0.44015, df = 2, P = 0.8025). nificantly affected richness at site 4 in 1996. 2000] ELEODES COMMUNITY STRUCTURE 9

TABLE 2. Average number of individuals captured by species in each of the 2 macrohabitat types (SU = shortgrass upland, SF = shrub floodplain). Values averaged across 3 sites within each macrohabitat type, across 4 months, and across 4 yr for clarity of presentation. EXTR = E. extricata, FUSI = E. fusiformis, HISP = E. hispilabris, LONG = E. longicollis, OBSC = E. obscura, OBSO = E. obsoleta, OPAC = E. opaca, SUTU = E. suturalis, TRIC = E. tricostata. EXTR FUSI HISP LONG OBSC OBSO OPAC SUTU TRIC SU 42.61 6.52 2.64 0 2.40 20.30 0 0.04 0.27

SF 6.50 21.70 16.23 2.44 82.04 19.54 0.40 5.25 18.17

TABLE 3. Weather data, 1994–1997, compared to historical data collected 1961–1990. PPT = precipitation (mm), AIRMAX = maximum daily air temperature (°C), AIRMIN = minimum daily air temperature (°C), TEMP = average daily air temperature (°C). A dash (—) indicates no data available. Year PPT AIRMAX AIRMIN TEMP Historic 282.7 17.28 1.13 9.27 1994 135.0 17.81 –0.45 8.63 May 11.8 28.96 7.88 19.19 June 0 31.38 10.36 21.31 July 0 34.05 11.01 22.85 August 1.0 32.15 14.76 22.66 1995 302.9 17.37 –0.97 7.66 May 4.31 16.69 –6.83 7.69 June — — — — July 0 26.13 11.03 17.89 August 0 29.58 12.13 23.65 1996 423.4 16.89 –0.66 7.99 May 0.25 15.98 5.81 7.48 June 1.02 26.86 11.84 20.12 July 0.25 29.42 12.14 20.12 August 0 30.46 10.44 20.22 1997 408.8 15.36 –1.02 7.07 May — — — — June 4.32 27.02 10.83 17.99 July 0 31.56 11.71 22.44 August 13.72 29.02 13.91 20.93

Precipitation in 1996 negatively affected rich- E. hispilabris numbers were significantly cor- ness in site 5 in 1997. Precipitation levels in related with weather variables of the current May 1994 affected the number of eleodid and previous years, depending on site. For species trapped in June at sites 2, 3, and 5; and instance, density was significantly correlated maximum air temperatures in June 1996 were with the current year’s minimum and daily negatively correlated with the number of mean air temperatures at site 1 and precipita- species trapped at site 3 in July. Other relation and maximum air temperature at site 6. tionships were not significant. Densities at sites 3 and 4 were affected by Densities of E. extricata and E. hispilabris both current and prior weather conditions. populations were affected by some weather Other relationships were not significant. variables (Table 5). E. extricata densities were primarily affected by weather conditions of DISCUSSION the previous year, and this effect was mediated by site. For example, at trapping sites 1, 3, and Eleodid community composition of the 5, density was significantly correlated with northern shortgrass steppe showed as much daily mean temperature of the previous year. variation among months within a year as among At sites 2, 4, and 6, densities responded to years. Some eleodid species experienced irreg- precipitation levels and temperature maxima. ular increases and declines in abundance in 10 WESTERN NORTH AMERICAN NATURALIST [Volume 60

TABLE 4. Spearman rank correlation matrix for number of species captured and weather variables, 1994–1997. Values are rs(P). “Current year” indicates correlations performed on data within a year, whereas “1-yr lag” indicates weather data from year prior to the one listed and “1-month lag” indicates correlations performed with weather data from the month prior to the one listed within a year. PPT = precipitation, AIRMAX = maximum daily air temperature, AIRMIN = minimum daily air temperature, TEMP = average daily air temperature. Only significant correlations are shown for sake of clarity. Time Site PPT AIRMAX AIRMIN TEMP ------Current year ------1995 1 0.96(0.0005) –0.92(0.0014) –0.99(0.0001) 1995 2 –0.93(0.0011) 0.96(0.0004) –0.90(0.0012) –0.97(0.0003) 1995 5 –0.99(0.0001) 1995 6 0.97(0.0003) –0.90(0.0009) –0.97(0.0003) ------1-yr lag ------1995 1 0.83(0.0026) 1996 4 0.86(0.0028) 1997 5 –0.90(0.0019) ------1-month lag ------6/1994 2 –0.97(0.0003) 3 –0.97(0.0003) 5 –0.97(0.0003) 7/1994 3 –0.90(0.0019)

response to weather (primarily precipitation species were present every year, suggesting and minimum air temperatures), although that I sampled the entire local eleodid species population densities of the 2 focal species pool (see also Kumar et al. 1976). remained relatively stable across years and Shrubs and Shade sites. Most of the 9 eleodid species present at No significant shrub-shade effects (hypoth- CPER were widespread, occurring in both esis A1) were found, probably because beetles macrohabitat types (shortgrass uplands and were captured during a thermally favorable shrub floodplains), although certain species “window” of time (Whicker 1983), a daily were more abundant in one or the other period when beetles can be active (and thus macrohabitat (Figs. 1, 2). The 4 largest species trapped). During most of this window, beetles (E. hispilabris, E. longicollis, E. obscura, and do not need to seek out thermoregulatory sites E. suturalis) were more abundant in shrub associated with shrubs. Therefore, it is not floodplains. Most smaller species were more surprising that beetle captures were similar abundant in floodplain sites (E. fusiformis, E. between shaded and unshaded traps. Parmenter opaca, and E. tricostata), although 1 species and MacMahon (1984) reported similar nega- (E. obsoleta) was equally abundant in both tive results from a shrub-removal experiment macrohabitat types. The smallest species (E. in the shrub-steppe of Wyoming (~40% shrub extricata) was more common in shortgrass coverage), which suggests that shade may not uplands. These results are consistent with be an important resource provided by shrubs Whicker (1983), Parmenter and MacMahon when eleodids are active (although it may be (1984), and Stapp (1997a). Beetles were cap- important during other portions of the day or tured more often in traps located near cactus at night; Stapp 1997a). and shrub microhabitats in both macrohabi- As a word of caution, however, the short- tats, and significantly lower capture rates were grass steppe has a relatively low amount of noted for traps associated with bare soil (see shrub coverage (≤14%), and so any favorable also Stapp 1997a). microhabitats created by shrubs would be rel- Most eleodids were widespread over time, atively rare. In habitats with shrub canopy being present throughout most of the summer, coverage ≥90%, however, microclimate differ- although there was some phenological turn- ences associated with shrubs may be more over in species abundance and community pronounced, and some microhabitat partition- composition (Figs. 1, 2). In addition, most ing by eleodids has been revealed under such 2000] ELEODES COMMUNITY STRUCTURE 11

TABLE 5. Spearman rank correlation matrix for population density of E. extricata (EXTR) and E. hispilabris (HISP) and weather variables. Values are rs(P). “Current year” indicates correlations performed on data within a year, whereas “1-yr lag” indicates weather data from the previous year. PPT = precipitation, AIRMAX = maximum daily air temperature, AIRMIN = minimum daily air temperature, TEMP = average daily air temperature. Only significant correlations are shown for sake of clarity. Species Year Site PPT AIRMAX AIRMIN TEMP ------Current year ------HISP 1996 1 –0.90(0.0031) 0.97(0.0003) HISP 1996 2 HISP 1996 3 –0.99(0.0001) HISP 1996 4 –0.96(0.0005) HISP 1996 5 HISP 1996 6 –0.99(0.0001) 0.90(0.0001) ------1-yr lag ------EXTR 1995 1 0.99(0.0001) EXTR 1995 2 –0.99(0.0001) –0.92(0.0008) EXTR 1995 3 0.99(0.0001) EXTR 1995 4 –0.99(0.0001) –0.92(0.0008) EXTR 1995 5 0.99(0.0001) EXTR 1995 6 –0.99(0.0001) –0.92(0.0008) HISP 1997 3 –0.99(0.0001) HISP 1997 4 –0.99(0.0001)

circumstances (Parmenter et al. 1989b, 1989c). there. Predacious rodents, for example, attain In particular, Eleodes extricata is usually asso- densities 8–16 times higher in shrub-domi- ciated with open, shrub-free areas (this study, nated areas of the shortgrass steppe, and more Whicker and Tracy 1987, Parmenter et al. species of rodents that prey upon eleodids are 1989b, 1989c). found in areas with shrubs (Stapp 1996). Parmenter and MacMahon (1988) found Shrubs, Predation Risk, that most larger-bodied tenebrionids showed and Body Size little response to predator removal, which they Regarding the hypotheses about body-size attributed to better chemical (quinone) defenses. differences in predation risk by macrohabitat/ Although most Eleodes species are assumed to degree of shrub cover, my data do not com- possess chemical defenses (Tschinkel 1975a, pletely support either alternative. With alter- 1975b, Allsopp 1980), not all species have native B1, for example, although some smaller been tested to determine whether this is true. eleodid species were more abundant in upland In this study I observed such chemicals in sites, others were more abundant in shrub only 4 species: E. extricata (small species, most floodplains with coarsely textured soils that do abundant in uplands; defensive chemical also not provide refugia, and larger species were found in this species by Parmenter and Mac- not widespread. With alternative B2, smaller Mahon [1988]), E. fusiformis (small species, species were not widespread, with some being most abundant in shrub floodplains), E. hispi- more abundant in uplands and others achiev- labris (large species, most abundant in shrub ing higher numbers in floodplains (Figs. 1, 2). floodplains), and E. obsoleta (small species, In other words, neither hypothesis explains found in both macrohabitats). Therefore, no why there were fewer individuals of only some clear patterns of habitat occupation with of the smaller eleodid species in shrub flood- defensive capabilities emerged, and no con- plains and simultaneously why there were lower clusions can be drawn about potential differ- numbers of the larger species in uplands. ences in predation risk among the different Rodent-removal experiments have shown species (and different body sizes) in the short- that eleodid populations may increase by as grass steppe without further study. much as 63% in the absence of predators (Par- Given this information as well as the paucity menter and MacMahon 1988). Even so, some of empirical data on differential rates of species- eleodid species may prefer shrub-dominated specific eleodid predation, these hypotheses areas although predators are more numerous of why eleodid communities are structured as 12 WESTERN NORTH AMERICAN NATURALIST [Volume 60 they are must be viewed with skepticism. than sedentary species; Southwood 1966). Eleo- Instead, eleodids may prefer areas with shrubs dids are active only during a thermally favor- because of resources that shrubs provide or able window of time each day (Whicker 1983). because of environmental (particularly edaphic) Beetles are trapped only when they are active, factors that are correlated with, but indepen- with the daily timing and duration of their dent of, shrub presence (Parmenter and Mac- activity window determined by the weather. Mahon 1984, Parmenter et al. 1989b, McIntyre Therefore, beetles may in fact respond strongly 1997, Stapp 1997a). to temperature and precipitation, insofar as these variables determine when beetles can be Shrubs and Weather active, but not density or diversity. Species-specific differences in physiologi- In general, larger ectotherms are less cal tolerance of weather variables may account affected by weather conditions than are for phenological turnovers in species richness smaller ones because of the negative relation- and abundance I observed each year, but ship between body size and convective heat there is a high degree of overlap in physiologi- loss. Larger beetles may be exposed to greater cal tolerances among the different species I heat gain than are smaller species by virtue of studied (Whicker 1983, Whicker and Tracy their smaller surface-area-to-volume ratio. 1987). Thus, it is perhaps not surprising that I Thus, larger species may require shrub micro- observed overlap in community composition climates more so than smaller species, which and population density among weather condi- may explain why the 4 largest eleodid species tions and years (Figs. 1, 2). were consistently more abundant in shrub Species-specific physiological differences floodplains. This relationship does not explain may be compromised by habitat effects. For the more complicated community-habitat pat- example, the avoidance of bare-soil microhabi- terns of the smaller species, however. tats may reflect an avoidance of areas in which An Alternative Explanation thermoregulation is difficult (cf. McIntyre in for Patterns Observed press) or where food resources are absent. In addition, because insectivorous rodents create Various forms of habitat partitioning seem to offer only partial explanations for the spatio- areas of bare soil during burrow excavations temporal characteristics of the eleodid com- (Stapp 1997b), eleodids may be more exposed munity of the shortgrass steppe. Can other to predation in bare-ground areas and hence mechanisms provide a more comprehensive avoid such areas. This microhabitat avoidance explanation of the abundance and distribution was not reflected in macrohabitat occupation, of eleodids on the shortgrass steppe? however, because shrub-floodplain sites pos- Because all eleodid species are highly vagile, sessed more bare soil. Different mechanisms they are presumably not excluded from one or of habitat selection may be operating at differ- another macrohabitat type because of an in- ent scales, creating this apparent paradox of ability to reach it. The presence of at least a habitat occupancy (see also McIntyre 1997). few individuals of nearly all species in both Hypothesis D1 received only partial sup- macrohabitat types indicates this is true, and port, suggesting that the eleodid community is the macrohabitats themselves are interspersed somewhat insensitive to weather. Because dark- throughout the shortgrass steppe, being sepa- ling beetles are ectotherms, it comes as no rated by no more than a few kilometers. surprise that they responded to some weather Because macrohabitats are defined by differ- variables (see also Hinds and Rickard 1973), ences in vegetative structure (e.g., presence vs. but it is surprising that they did not respond absence of shrubs), differences in this struc- more strongly and consistently to weather ture may be driving the eleodid community variables. This weak relationship may be arti- patterns by acting as filters to movement, the factual, however, because the test of hypothe- process by which animals achieve habitat ses C1 and C2 included a hidden bias. Pitfall selection. This idea was first hinted at by trapping is influenced by both insect abun- Roughgarden (1974) with respect to how dif- dance (with more abundant species exhibiting ferent scales of environmental heterogeneity higher capture rates) and insect activity (with affect population dynamics by affecting dis- more mobile species being captured more often persal distances; it was further modified by 2000] ELEODES COMMUNITY STRUCTURE 13

Wiens and Milne (1989), Crist et al. (1992), Scale-dependent uses of heterogeneity may Crist and Wiens (1995), Keitt et al. (1997), and also explain how an individualistic behavior Wiens et al. (1997). such as movement can translate into popula- Different macrohabitats, by virtue of their tion- and community-scale patterns (Crist and differences in physiognomic structure, possess Wiens 1995). For example, adult eleodids may different “viscosities.” Species that differ in move to areas with favorable oviposition and their movement behaviors (capacity and mobil- larval-development sites, resulting in higher ity, defined below) would therefore respond eleodid abundances there the following year. differently to different portions of a landscape Very little is known about egg and larval (Roughgarden 1974, Rolstad 1991). Overall requirements, however, and nothing is known movement capacity (distance traveled in a about larval movements. More studies are given time period) is affected by body size, needed about other life stages of eleodids if with larger species able to cover greater dis- we are to understand fully their community tances than smaller species (With 1994, Keitt organization. et al. 1997). An animal’s mobility (ease of The shortgrass steppe has an abundant, movement) is also affected by its body size diverse, and understudied arthropod fauna. Its because animals interact with environmental darkling beetle community possesses some features according to the scale of those fea- spatio-temporal dynamics that resist straight- tures. For example, large, mobile animals are forward explanations. Continued long-term able to disregard fine-grained features such as monitoring of eleodids and weather in both small variations in topography or vegetative shortgrass-upland and shrub-floodplain macro- physiognomy. Small species, on the other habitat types may reveal how abiotic and envi- hand, are affected by these small features, ronmental factors interact to influence dark- which are (relative to themselves) not small at ling beetle community structure. Particular all. Large eleodids do indeed move over fea- attention should be paid to how environmen- tures that smaller beetles circumambulate tal heterogeneity may be perceived at differ- (Crist et al. 1992). Thus, large, mobile species ent scales to create dynamic community pat- perceive landscapes as more connected because terns. they interact with spatial features at a broader (coarser) scale (Levins 1968, Kotliar and Wiens ACKNOWLEDGMENTS 1990). If a structure is very large relative to the size of an animal, the structure in its en- I thank Phil Chapman for statistical advice, tirety may be disregarded and interactions made Chris Wasser for weather-data compilations, only with its component parts (Rolstad 1991). and Jeff Cordulack, Dan Hopkins, Scott Malt- To a large eleodid beetle, then, shortgrass zahn, John Sovell, and Ron Weeks for field poses no obstructions to movement; to a small assistance. Tom Crist, Tom Hobbs, Boris Kon- beetle, however, shortgrass may represent a dratieff, Robert Parmenter, John Wiens, and veritable thicket. Large beetles would be forced Tom Wilson made helpful comments on manu- to interact with shrubs, however, but small script drafts. Funding was provided by the beetles may be able simply to move through National Science Foundation Shortgrass Steppe small gaps in aboveground roots and leaf litter. Long-Term Ecological Research project (grant Therefore, larger species should accumulate BSR-9011659, principal investigators I.C. in areas with coarse physical structure (i.e., Burke and W.K. Lauenroth) and 2 Sigma Xi shrub macrohabitats), whereas smaller species Grants-in-Aid of Research. should be found more often in areas with finer-textured vegetation that is sufficiently large to detain them (i.e., shortgrass uplands). LITERATURE CITED This scale-dependent mobility explains why ABRAMS, P. 1980. Some comments on measuring niche there were more individuals of the large eleo- overlap. Ecology 61:44–49. did species in the shrub floodplains, why some ALLSOPP, P.G. 1980. The biology of false wireworms and small species were more abundant in the shrub their adults (soil-inhabiting Tenebrionidae) (Coleop- floodplains than in the shortgrass uplands, and tera): a review. Bulletin of Entomological Research 70:343–379. why the smallest species was most abundant ANDERSON, D.R., K.P. BURNHAM, G.C. WHITE, AND D.L. in the uplands. OTIS. 1983. Density estimation of small-mammal 14 WESTERN NORTH AMERICAN NATURALIST [Volume 60

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HOME-RANGE FIDELITY AND USE OF HISTORIC HABITAT BY ADULT COLORADO PIKEMINNOW (PTYCHOCHEILUS LUCIUS) IN THE WHITE RIVER, COLORADO AND UTAH

David B. Irving1 and Timothy Modde2

ABSTRACT.—Twelve wild adult Colorado pikeminnow (Ptychocheilus lucius), captured in the tailwaters of Taylor Draw Dam on the White River, Colorado, were implanted with radio transmitters and their movement patterns monitored from 1992 to 1994. The spawning migration of these fish was extensive. In 1993, the only full year of the study, the fish migrated an average of 658 km from the White River to spawning sites in the Yampa or Green rivers and back to the White River. Eight of these fish were translocated in the river upstream of the dam in April 1993. These fish and the 4 others below the dam remained in the river until May 1993. All 12 had migrated down the White River to spawning sites in the Green and Yampa rivers by July 1993. The fish that were located above the dam successfully passed over the dam during their downstream migration. Seven fish migrated upstream toward the Yampa River Canyon spawning site and 5 migrated downstream toward the Green River Desolation/Gray Canyon spawning site. Five of 7 Yampa River fish were found at the spawning site. The other 2 were found 5–8 km downstream of the site. One of 5 Green River fish was found at the spawning site, the other 4 between 16 and 62 km upstream of the site. All fish migrated back to the White River by August 1993 and were found near the dam by October 1993. Two fish were recaptured and translocated above the dam in September 1993. Five fish were located below the dam and 2 above the dam in April 1994. By July 1994 seven of the same fish that had migrated toward the Yampa River in 1993 were found at the Yampa Canyon spawning site. At the same time, 3 of 5 fish that migrated toward the Green River in 1993 were found at the Desolation/Gray Canyon spawning site. This included 2 fish that had been found upstream of the site in 1993. The 12 fish traveled an average of 6 km d–1 (range: 4–10 km d–1) during the migration period from May through Octo- ber 1993. Generally, fish moved faster to the spawning site than back from the site to the White River. These fish moved very little within their home ranges in the White River. Six fish tagged in 1992 moved only 0.1–2.3 km in the tailwater reach below Taylor Draw Dam from September 1992 through April 1993. All fish, after their spawning runs, had moved up to or near the dam by October 1993. These fish were not tracked again until April 1994. Their movement patterns in April 1994 were similar to those observed in April 1993. The greatest amount of fish movement in the White River was displayed by the 8 fish placed above Taylor Draw Dam in April 1993 and the 2 placed in Kenney Reser- voir in September 1993. They moved 1.1–40.6 km in the river before and after their spawning migration in spring and autumn 1993. These spawning migrations suggest that adult Colorado pikeminnow in the White River were recruited from both Green and Yampa river spawning populations and were presumably imprinted to these respective spawning sites. Those fish placed above Taylor Draw Dam established home ranges in habitats previously occupied by Colorado pikeminnow before the dam was completed. They remained there until they migrated downstream during the spawning period. Although we did not study fish passage, our study demonstrates that adult Colorado pikeminnow will use habitat if access is provided. Translocation of wild adult fish into historic but unoccupied habitats may be a valuable recovery option.

Key words: Colorado pikeminnow, Ptychocheilus lucius, migration, telemetry, home-range fidelity.

Colorado pikeminnow, Ptychocheilus lucius, pikeminnow was listed as endangered by the is a large, warmwater cyprinid endemic to the U.S. Fish and Wildlife Service in 1967 and given Colorado River basin of western United States protection under the Endangered Species Act and Mexico (Jordan and Everman 1896, Minck- in 1974 (Federal Register 39[3]:1175). Self- ley 1973). Once widely distributed in the main sustaining populations exist only in the upper channel and major tributaries, the long-lived Colorado River basin, with greatest numbers species has been extirpated from 80% of its in the Green River subbasin (Tyus 1991). historic range following the construction of As with several other large-river fishes in the mainstem impoundments and establishment American Southwest, the Colorado pikeminnow of nonnative predators (Tyus 1991). Colorado is potamodromous, with spawning migrations

1U.S. Fish and Wildlife Service, Fish and Wildlife Management Assistance Office, 855 East 200 North (112–13), Roosevelt, UT 84066. 2U.S. Fish and Wildlife Service, Colorado River Fishery Project, 266 West 100 North Suite 2, Vernal, UT 84078.

16 2000] COLORADO PIKEMINNOW IN WHITE RIVER 17 initiated by changes in discharge, temperature, This study examined migratory movements and photoperiod (Tyus 1986, 1990). Using an of 12 adult Colorado pikeminnow in the White extensive telemetry and mark-recapture data River through 2 successive spawning periods set, Tyus (1990) described factors initiating and determined where these fish spawned. It migration and spawning of Colorado pike- also tested whether some of these fish that minnow in the Green River subbasin, includ- were translocated into formerly occupied habi- ing the White River. Some fish migrated 1-way tats above Taylor Draw Dam would remain in distances >300 km to 1 of 2 known spawning that habitat, move into the reservoir, or return areas (Yampa Canyon in Yampa River or Gray/ to home ranges below the dam. Desolation Canyon in Green River), and individuals were captured on the same spawning STUDY AREA sites in multiple years. Of 153 fish implanted with radio transmitters, 41% migrated ≥1 times The White River drainage encompasses 1.3 to 1 of the 2 known spawning areas, with an million ha of arid pinion-juniper and sage- additional 11% suspected of doing so (Tyus brush desert in northwestern Colorado and 1990). Spawning migration was not detected in northeastern Utah (Fig. 1). The river drains approximately half the fishes implanted with into the Green River, a major tributary to the radio transmitters. Lack of movement was pre- Colorado River in southeastern Utah. The sumably because fish were either immature or high-gradient, cool-headwater, canyon-bound nonannual spawners (Tyus 1990). Ryden and reaches consist of riffles, runs, and rapids with Ahlm (1996) found similar behavior in Col- boulder, cobble, and gravel substrates. The orado pikeminnow radio-tracked over a 3.5-yr low-gradient warmwater reaches are charac- period on the San Juan River in New Mexico, terized by deep eddies, pools, and runs that Colorado, and Utah. Movement of 12 of 13 meander through slower, turbid waters, with vegetated shorelines and gravel, sand, and silt fish they studied averaged 17.7 km (range: substrates. Summer water temperatures often 1.8–32.8 km). The other fish moved a total of reach 20°C. Peak spring discharge ranges 93.0 km and was the only one thought to dis- between 100 and 170 m3 s–1. Taylor Draw play migratory behavior. Although factors initi- Dam is operated as a run-of-the river facility ating spawning migrations and spawning-site and provides water storage, flood control, and fidelity have been well described (Tyus 1986, hydroelectric power. Kenney Reservoir, above 1990), movement patterns of individual fish in the dam, is 275 ha and provides recreational consecutive years are not well understood. boating and fishing. Previous studies have found no early life stages and few juvenile Colorado pikeminnow MATERIALS AND METHODS in the White River; most fish in the river are adults (Tyus 1986). Taylor Draw Dam, con- We captured 12 wild adult Colorado pike- structed in 1985 on the White River, created a minnow by electrofishing and trammel-netting barrier to upstream movement, preventing in a 0.5-km reach (km 163–168) of the White access to about 32% (77.8 km) of the habitat in River below Taylor Draw Dam. Six fish (#1–6) the White River historically used by adult Colo- were caught in September 1992 and 6 more rado pikeminnow (Carlson et al. 1979, Wick et (#7–12) in April 1993. Each fish was mea- al. 1985, Trammell et al. 1993). It is assumed sured for total length (TL), tagged with a PIT that after closure of the dam those Colorado (passive integrated transponder), and surgi- pikeminnow upstream of the dam migrated cally implanted with a 24-month (16-g) radio over the dam to downstream spawning areas. transmitter. Fish were anesthetized with tri- Post-spawning fish moving back upstream were caine methanesulfonate and radio transmitters blocked from returning to their previously (internal loop antennas) placed into the body occupied home range above Taylor Draw Dam. cavity via a surgical incision as quickly as pos- As a result, fish congregated below the dam in sible following capture. Fish were released densities up to 37 adults per 0.4 km as recent- within 10 min after surgery. ly as 1993 (Irving and Modde 1994). These den- Eight fish, 2 recaptured from the 1992 group sities may also be the result of recent high re- and 6 from the 1993 group, were translocated cruitment of Colorado pikeminnow throughout 30 km upstream of the dam to determine if fish the Green River basin (McAda et al. 1998). would remain in habitats previously occupied 18 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 1. Radio telemetry study area for 12 wild adult Colorado pikeminnow (Ptychocheilus lucius) tracked on the White, Green, and Yampa rivers, upper Colorado River basin, Colorado and Utah, 1992–1994. by Colorado pikeminnow (historic habitat) Locations of all 12 fish were monitored on before dam completion. We also translocated 2 the ground using a radio search-receiver with fish recaptured in September 1993, 1 from the bidirectional paddle antennas and from the air 1992 group and 1 from the 1993 group, into with fixed-wing aircraft with omni-directional the lower reach of Kenney Reservoir (km 169) loop antennas. Fish tracked on the ground were to determine if they would remain in the triangulated to the nearest 0.25 m; fish locations reservoir, pass through the reservoir, or access tracked by air were estimated to the nearest upstream habitats. 0.4 km (based on transmitter pulse rate, signal 2000] COLORADO PIKEMINNOW IN WHITE RIVER 19 strength, and aircraft speed). From September The 8 fish (#1, 4, 7, 8, 9, 10, 11, 12) relo- 1992 to April 1993 (before placing any upstream cated in the White River (km 198.2) above of the dam), we monitored fish locations month- Kenney Reservoir in the spring of 1993 ly, and approximately weekly between 15 April remained in historic riverine habitats above and 30 September 1993. Fish locations during the reservoir until initiation of the down- 1994 were monitored in late April and on 2 stream spawning migration (Fig. 3). One fish dates during the migration and spawning (#1) moved downstream on May 15 (Table 1), period (1 and 13 July). Although radio-track- the others between mid-June and early July ing was not monitored on a continuous basis, (Fig. 2). travel rates (km d–1) were calculated for each On 9 and 14 September 1993, two fish (#4, fish for the 1993 migration period. 9, respectively) were relocated to the lower end of Kenney Reservoir (km 170.6). These RESULTS fish moved upstream of the reservoir (Fig. 3) within 8 d and were located in historical river- Twelve Colorado pikeminnow (409–743 mm ine habitats the following spring (20 April TL, 1000–3750 g) were captured in the 0.4-km 1994). tailwater reach below Taylor Draw Dam (km Five fish (#1, 3, 6, 10, 12) were located just 168.2) in 1992 and 1993 (Table 1). The 6 fish below Taylor Draw Dam (km 167.4–168.2) and (#1–6) captured and implanted with radio 2 fish (#4, 9) above the dam (km 180.2–185.1) transmitters in September 1992 remained in the following year on 20 April 1994 (Fig. 2). the White River within 1 km below Taylor The 5 fish below the dam, located 3–15 km Draw Dam through fall 1992 and spring 1993 downstream of the dam the previous October, (Fig. 2). The 6 fish (#7–12) captured in April moved back upstream to the dam in spring 1993 were located within a 0.8-km reach 1994. The 2 fish relocated into Kenney Reser- below the dam. It was assumed that all fish voir in September 1993 moved an additional survived because each transmitter remained 5–8 km further upstream. On 1 and 13 July active throughout the 2-yr monitoring period. 1994 seven fish (#1, 2, 3, 7, 8, 9, 10) located in The spawning migration of these fish was April were found within the Yampa River extensive. Colorado pikeminnow tagged in the spawning reach: three (#5, 6, 12) were found White River migrated an average of 658 km at the Green River spawning site, and two from the White River to spawning sites in the (#4, 11) were found between 43 and 105 km Yampa or Green rivers and back to the White upstream of the Green River site. All fish River (Table 1, Fig. 2). All 12 radio-tagged fish moved to or near the same spawning area they migrated downstream in the White River in used the previous year. 1993 and entered the Green River. Seven of The 12 fish traveled an average of 6 km d–1 these fish moved upstream in the Green River, (range: 4–10 km d–1) during the migration 5 fish (#1, 3, 8, 9, 10) into the Yampa River period from May through October 1993 (Table spawning area (Yampa Canyon km 0–32), and 1). Generally, fish moved faster to the spawn- 2 (#2, 7) located 11 and 16 km downstream ing site than back to the White River. of the spawning area (Fig. 2). These 7 fish Aside from their spawning migration, these migrated between 548 and 951 km from mid- fish moved very little within their home ranges May through late October 1993. During the in the White River. For example, the 6 fish same year 1 fish (#12) moved downstream in tagged in 1992 moved only 0.1–2.3 km in the the Green River and was located at the Green tailwater reach below Taylor Draw Dam from River spawning site (Gray/Desolation Canyon September 1992 through April 1993. All 12 km 232–256). Four other fish (#4, 5, 6, 11) fish, after migrating to and from their respec- were found 27–100 km upstream of the spawn- tive spawning sites, migrated back to the ing area (Fig. 2). The Green River migrants White River by late August and September traveled between 437 and 687 km from mid- 1993. Five of these fish (#1, 4, 6, 9, 11) moved May through late September 1993 (Table 1). back upstream to Taylor Draw Dam and then All fish returned to the White River between redistributed themselves downstream 2.4–10.1 mid-August and late October 1993, thus show- km by October 1993. The other 7 fish (#2, 3, ing home-range fidelity. 5, 7, 8, 10, 12) did not appear to move up to 20 WESTERN NORTH AMERICAN NATURALIST [Volume 60 ______No. days No. km ) Start End tracked traveled –1 upper Colorado River basin, and No. days No. km Rate Date monitored translocated into Kenney Reservoir 4 km upstream of Taylor Draw Dam. Reservoir 4 km upstream of Taylor translocated into Kenney 2 are those that migrated to or near the Grey/Desolation Canyon Green River spawning site (km 232–256). Fish 1, 2 are those that migrated to or near the Grey/Desolation Canyon Green River spawning site (km 232–256). Fish No. days No. km Dates migrated No. days No. km Date monitored 1992 1993 1994 ______333777777777 73333377777777 55555 52333355555555 (mm) (g) Start End tracked traveled Start End tracked traveled Start End migrated traveled (km d 1. Length, weight, and telemetry data of 12 radio-tagged wild adult Colorado pikeminnow in the White, Green, and Yampa rivers, 1. Length, weight, and telemetry data of 12 radio-tagged wild adult Colorado pikeminnow in the White, Green, and Yampa ABLE a T 123 6477 6338 4099 — 484 — 743 — 9/30 654 1000 9/30 3750 11/30 10/1 2750 — 11/30 — 11/30 3 — 3 — 3 — 0.1 — — 0.0 — 0.1 1/6 — 1/6 — 10/29 1/6 — 9/22 — 4/9 10/29 20 4/12 10/29 4/14 8 13 755.9 9/22 9/22 12 631.0 5/15 722.4 9 18 678.4 8/31 5/19 5/19 985.1 8/31 10/29 5/15 787.5 108 6/15 10/29 163 6/15 104 720.3 9/22 167 9/8 722.4 548.1 6.7 99 646.4 4.4 85 5.3 4/20 951.4 3.9 4/20 7/13 7/1 710.7 9.6 7/13 7/1 7/13 3 8.4 7/13 7/1 3 2 4/20 339.7 7/13 2 395.7 7/13 525.6 2 381.1 3 419.7 348.9 456 632 451 430 — — — 10/1 10/1 11/30 10/2 10/15 10/15 3 2 2 0.1 0.1 0.1 1/6 1/6 9/22 2/3 9/22 10/29 17 12 13 679.0 541.4 447.4 5/15 5/19 5/19 8/16 9/22 8/31 93 126 104 635.0 541.2 437.1 6.8 4.3 4.2 4/20 7/13 4/20 7/13 7/13 7/13 3 1 3 313.8 304.2 315.9 n n 10 604 — — — — — 4/26 9/22 11 768.2 6/15 9/22 99 710.7 7.2 4/20 7/13 3 354.2 1112 624 652 1960 2100 — — — — — — — — 4/28 4/28 10/29 10/29 15 11 642.5 733.5 6/15 5/27 9/8 8/31 85 96 589.4 686.5 6.9 7.2 7/1 4/20 7/13 7/13 2 3 251.9 315.9 Std 112.9 1391.9 Std 107.8 99 Fish 1, 2, 3, 7, 8, 9, and 10 migrated to or near the Yampa Canyon Yampa River spawning site (km 0–32). Fish 4, 5, 6, 11, and 1 River spawning site (km 0–32). Fish Canyon Yampa 1, 2, 3, 7, 8, 9, and 10 migrated to or near the Yampa Fish Min 409 1000 9/30 11/30 3Min 0 430 1/6 1960 9/22 10/1 10/15 8 2 631 0.1 5/15 8/31 1/6 9/22 85 11 548.1 447.4 6.4 5/15 4/20 8/16 7/13 85 2 437.1 339.7 5.1 4/20 7/13 1 251.9 Fish Length Weight Date monitored Max 743 3750 10/1 11/30 3Max 0.1 652 4/26 2100 10/29 10/2 20 11/30 985.1 3 6/15 10/29 0.1 167 4/28 10/29 951.4 17 5.7 733.5 7/1 6/15 7/13 9/22 3 126 525.6 686.5 5.4 7/13 7/13 3 315.9 No. a 4, 7, 8, 9, 10, 11, and 12 are the 8 fish translocated in the White River 30 km upstream of Taylor Draw Dam. Fish 4 and 9 were Draw Dam. Fish 4, 7, 8, 9, 10, 11, and 12 are the 8 fish translocated in White River 30 km upstream of Taylor Mean 596.3 2500 9/30 11/30 3.0 0.1Mean 557.8 3/3 2030 10/7 10/1 13.0 10/30 761.2 2.3 5/29 9/24 0.1 117.9 2/25 10/14 715.7 13.6 6.1 608.8 5/20 5/25 7/13 9/3 2.6 100.8 395.0 577.8 5.7 5/21 7/13 2.4 300.3 Utah, 1992–1994. (Fish number refers to order in which fish was captured). Utah, 1992–1994. (Fish 2000] COLORADO PIKEMINNOW IN WHITE RIVER 21

Fig. 2. Movement patterns of 12 radio-tagged wild adult Colorado pikeminnow (Ptychocheilus lucius) that migrated from the White River to spawning sites in the Yampa River (7 fish, Yampa Canyon at km 0–32) and Green River (5 fish, Gray/Desolation Canyon at km 232–256), upper Colorado River basin, Colorado and Utah, 1992–1994. (Larval drift dates are adapted from Bestgen et al. 1998.) 22 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 3. Locations of 12 radio-tagged Colorado pikeminnow (Ptychocheilus lucius) translocated above Taylor Draw Dam and subsequently contacted in Kenney Reservoir and the White River, Colorado, above Taylor Draw Dam (km 168). the dam but had located themselves 5.6–26.6 DISCUSSION km below the dam by October 1993. Fish movement in September and October 1993 Colorado pikeminnow in the White River was 3- to 6-fold greater than the movement moved long distances annually. All 12 Colo- exhibited by these fish during the same period rado pikeminnow monitored from 1992 to in 1992. It is unknown why these fish moved 1994 migrated from the White River and were downstream of Taylor Draw Dam in 1993 located at or near the spawning sites, or appar- when they congregated below the dam during ently en route to the sites in the Green and the same period in 1992. The average dis- Yampa rivers. They then returned to areas charge at the dam during the months of August, near their original capture sites below Taylor September, and October was more than 1.5 Draw Dam. All demonstrated movements to times greater in 1993 than in 1992. In addition, spawning areas previously described by Tyus a new hydroelectric generator was installed and (1990): 7 migrated toward the Yampa Canyon in operation by summer 1993 and caused some spawning site and 5 toward the Gray/Desola- redirection and fluctuations of flows in the tion Canyon site. They also displayed fidelity river channel directly below the dam. to a single site and migrated the same direction Although these fish were not tracked again in successive years. Our observations indicate until April 1994, they showed movement pat- that many wild adult Colorado pikeminnow in terns similar to those in April 1993. The great- the White River undergo annual migrations to est amount of fish movement in the White spawning sites. It is unknown whether these River was displayed by the 8 fish placed above fish actually spawn each year. Taylor Draw Dam in April 1993 and the 2 fish Although we contacted all migrating fish placed in Kenney Reservoir in September 1993. within a few kilometers of the known spawn- The 8 fish moved 1.1–40.6 km between April ing sites, telemetry was limited, and we were and July 1993; the other 2 fish, which over- unable to locate each fish at its respective site. wintered in the river above the dam, moved Either they reached the sites between our con- 10.5–19.3 km between September 1993 and tacts or they might have migrated to other April 1994. concentration points near the spawning sites. 2000] COLORADO PIKEMINNOW IN WHITE RIVER 23

This study showed 5 of 7 Yampa River fish minnow represents a mixed stock recruited were within the spawning area in 1993 and from both upstream and downstream spawn- 1994. In 1994 one of the 2 fish found just ing populations. Tyus (1985, 1989, 1990) noted below the site in 1993 was found on the site that pikeminnow in the middle Green and and the other just above the site. One of 5 Yampa rivers tended to spawn at the Yampa Green River fish was at the site in 1993 and 3 River spawning site, and fish from the lower were there in 1994. Of the 4 fish located above Green River (i.e., Desolation and Gray canyons) the site in 1993, two were at the site in 1994 tended to migrate to the Gray Canyon spawn- and the remaining 2 fish above the site in both ing site. Although the White River confluence years. The only way to confirm that there are is located approximately equidistant from both more spawning sites in the upper Green River spawning sites (confluence–Yampa River site drainage is to tag more fish and follow their 159 km, confluence–Green River site 140 km), migration patterns more closely over succes- it is much nearer to known nursery areas up- sive years. stream of the White River (Irving and Burdick Presumably, 100% of the radio-tagged Colo- 1995, McAda et al. 1998). Thus, it is surprising rado pikeminnow survived over the 2-yr study. that about half the fish studied by us and oth- This rate is higher than the 85% annual sur- ers utilized the Gray Canyon site. This suggests vival rate reported by Osmundson et al. (1997) that occupation by subadult/adult fish moving for adult Colorado pikeminnow in the upper upstream, not the presence of nursery areas Colorado River. for juvenile fish, is the mechanism for coloniz- Our study confirms and expands the find- ing the habitat in the White River. Presumably, ings of other researchers. From 1980 through juvenile fish may move upstream in the main- 1990, radio telemetry detected 37 Colorado stem Green River for some time before explor- pikeminnow moving in and out of the White ing tributary streams. River (Tyus et al. 1981, Tyus 1990, Trammell et Spawning migration dates of this study also al. 1993). Twenty-three of these pikeminnow match well with Colorado pikeminnow larval remained in the White River, or at least were drift dates calculated by Bestgen et al. (1998). there on all monitoring dates. However, some He found that larvae drifted downstream of were not contacted each time, and several both spawning sites between late June and months sometimes elapsed between tracking mid-August 1993 and between mid-June and dates. It is thus possible that individuals mi- late July 1994 (Fig. 2). This study found that grated from the White River to spawning sites most tagged Colorado pikeminnow in the in the Green or Yampa rivers and returned White River began their migration to the Yampa undetected. Of the remaining 14 telemetered and Green river sites by mid-May or mid- pikeminnow, 9 moved to the Yampa River June and then migrated back to the White spawning area and 5 to the Gray/Desolation River by mid- to late August (Table 1). Canyon spawning area in the Green River. Eight fish relocated upstream of Kenney Only 2 of the 14 are known to have returned Reservoir remained there 2–3 months before to the White River. migrating downstream. Two fish relocated just All 12 of the Colorado pikeminnow we stud- above the dam in Kenney Reservoir in Sep- ied exhibited migratory behavior in 1993. This tember 1993 moved through the reservoir to is in contrast with previous studies in the Green historic riverine habitats above the reservoir River where about 50% were nonmigratory. where they overwintered before migrating This suggests that White River stocks are downstream to spawning areas the following composed entirely of reproductively active summer. individuals that utilize the White River exclu- Adult Colorado pikeminnow we studied re- sively for adult habitat. The long-distance sponded differently from hatchery-reared juve- migrations of these fish to spawning areas in nile and adult pikeminnow previously stocked the Green and Yampa rivers suggest that adult into Kenney Reservoir. Trammell et al. (1993) habitats may be limiting for such an energeti- stocked 96,597 juvenile Colorado pikeminnow cally costly mechanism to have evolved. In into the reservoir between April 1988 and addition, if natal imprinting is important in September 1990, but none remained in the homing to spawning destinations (Tyus 1990), impoundment following stocking. Results from the White River population of Colorado pike- 4 hatchery-reared adult fish implanted with 24 WESTERN NORTH AMERICAN NATURALIST [Volume 60 transmitters (Trammell et al. 1993) were incon- habitats, establish new home ranges, and con- clusive: 3 died within 36 d, and the survivor, tinue successful reproduction by using high- found in the impoundment on 12 June, moved quality habitats. However, hatchery-reared downstream of the reservoir and was located fishes may not. 12 km below the dam on 9 August 1990. To This study suggests that wild adult Colorado date, no hatchery-reared fish have displayed pikeminnow might use a fish passage facility if the type of spawning migration documented it were in place at Taylor Draw Dam. Research for the White River, nor have they utilized conducted by Burdick and Pfeifer (1999) shows unoccupied habitats upstream of Kenney that Colorado pikeminnow will use the fish Reservoir. However, behavior of wild fish was passage structure at Redlands Diversion Dam similar to our results. One of 3 wild adults on the Gunnison River near Grand Junction, implanted with transmitters died within 8 d, Colorado, to access riverine habitats upstream but the remaining 2 behaved similarly to the of this 12-ft dam. Since 1996, when the fish fish we studied: 1 moved upstream of the re- passage facility was opened, 47 subadult/adult servoir to occupy riverine habitats and the (TL 383–763 mm) Colorado pikeminnow have other moved downstream over the reservoir passed upstream through this structure. Six spillway. Contact was lost with the latter fish fish that used the structure in July and August from 12 June to 11 September; thus, it could 1997 and 1998 successfully passed downstream have migrated to a spawning area during this over the dam after that date and then used time. the passage structure again in either 1998 or Apparently, there is a net upstream move- 1999. One fish has been found upstream as far ment of subadult fishes into preferred habi- as 49 km. tats, but post-spawning Colorado pikeminnow This information can help guide present often exhibit home-range fidelity by returning recovery efforts in areas where historic habi- to the area (i.e., home range) they occupied tats have been blocked. Further, translocation before migration (Tyus 1986, 1990). Because of of wild fish offers another feasible alternative these behaviors, efforts to restore access (i.e., to stocking hatchery-reared fish whose behav- fish ladders, etc.) of adult fish to historic habi- ior may be problematic, such as not being tats may not be productive. Instead, younger imprinted to a successful spawning area nor fish would slowly colonize as they mature, thus being able to congregate with juvenile fish increasing the time necessary to occupy re- reared in high-quality nursery habitats. Finally, stored habitats. However, our study demon- recovery efforts can be more successful if life- strates that adult fish will use habitats if access history needs of Colorado pikeminnow are is provided them. better understood in areas where fish are most Migration and habitat use of White River abundant and least disturbed. fish indicate that powerful selection mechanisms have developed over perhaps thousands ACKNOWLEDGMENTS of years of evolution. This is evident in migration patterns and habitat use. When provided This study was initially proposed by the access, wild adult Colorado pikeminnow uti- Colorado Division of Wildlife. We thank T. lized historic, unoccupied habitats rather than Nesler and B. Elmblad for their assistance in returning to sites below the dam where they developing the study. A. Brady, Rio Blanco had been restricted following closure of Taylor Water Conservation District, and M. Caddy, Draw Dam. This assumes that these study fish Colorado Division of Wildlife, provided local and other wild fish present before the dam assistance in data collection and landowner was built have been attempting to ascend the permission. Assistance in field data collection White River since dam completion in 1985. was provided by H. Husband, B. Hilbert, D. On the other hand, hatchery-reared fish exhib- Beers, J. Baker, Q. Bradwich, B. Sheffer, R. ited a different behavior. They did not show Arment, and H. Hines. We are especially grate- the same tendency to occupy riverine habitats ful for thorough and thoughtful reviews by H. upstream of Kenney Reservoir nor undertake Tyus, K. Bestgen, M. Trammell, and K. Irving. such migrations. If restoration efforts connect Finally, we wish to thank Dinosaur National occupied habitats with historic reaches via fish Monument of the U.S. National Park Service, passages, wild adult fishes may access historic Ouray National Wildlife Refuge of the U.S. 2000] COLORADO PIKEMINNOW IN WHITE RIVER 25

Fish and Wildlife Service, and Utah Division Fishes of the Upper Colorado River Basin, U.S. Fish of Wildlife Resources for permits and permis- and Wildlife Service, Denver, CO. 21 pp + appen- dices. sion to collect fish in and fly over their respec- MINCKLEY, W.L. 1973. Fishes of Arizona. Arizona Game tive areas. This study was supported by the and Fish Department, Phoenix. Recovery Implementation Program for the OSMUNDSON, D.B., R.J. RYEL, AND T.E. MOURNING. 1997. Recovery of Endangered Fish in the Upper Growth and survival of Colorado squawfish in the Colorado River Basin. upper Colorado River. Transactions of the American Fisheries Society 126:687–698. RYDEN, D.W., AND L.A. AHLM. 1996. Observations on the LITERATURE CITED distribution and movements of Colorado squawfish, Ptychocheilus lucius, in the San Juan River, New BESTGEN, K.R., R.T. MUTH, AND M.A. TRAMMELL. 1998. Mexico, Colorado, and Utah. Southwestern Natural- Downstream transport of Colorado squawfish larvae ist 41:161–168. in the Green River drainage: temporal and spatial TRAMMELL, M.A., E.P. BERGERSEN, AND P. J . M ARTINEZ. variation in abundance and relationships with juve- 1993. Evaluation of Colorado squawfish stocking in a nile recruitment. Final report to Colorado River mainstem impoundment on the White River. South- Recovery Implementation Program, Project 32. Lar- western Naturalist 38:362–369. val Fish Laboratory, Department of Fishery and TYUS, H.M. 1985. Homing behavior noted for Colorado Wildlife Biology, Colorado State University, Fort squawfish. Copeia 1985:213–215. Collins. ______. 1986. Life strategies in the evolution of the Col- BURDICK, B.D., AND F.K. PFEIFER. 1999. Evaluation of the orado squawfish (Ptychocheilus lucius). Great Basin effectiveness of the fish passage structure at Red- Naturalist 46:656–661. lands Diversion Dam on the Lower Gunnison River. ______. 1990. Potamodromy and reproduction of Col- Colorado River Fishery Project, Grand Junction, orado squawfish Ptychocheilus lucius. Transactions Colorado. U.S. Fish and Wildlife Service. Recovery of the American Fisheries Society 119:1035–1047. Implementation Program for the Endangered Fishes ______. 1991. Ecology and management of Colorado of the Upper Colorado River Basin. squawfish. Pages 379–402 in W.L. Minckley and J.E. CARLSON, C.A., C.G. PREWITT, D.E. SNYDER, E.J. WICK, Deacon, editors, Battle against extinction: native fish E.L. AMES, AND W. D. F ONK. 1979. Fishes and management in the American West. University of macroinvertebrates of the White and Yampa rivers, Arizona Press, Tucson. Colorado. U.S. Bureau of Land Management. Bio- TYUS, H.M., AND G.B. HAINES. 1991. Distribution, abun- logical Science Series 1, Denver, CO. dance, habitat use, and movements of young Col- IRVING, D.B., AND B.D. BURDICK. 1995. Reconnaissance orado squawfish Ptychocheilus lucius. Transactions inventory and prioritization of existing and potential of the American Fisheries Society 120:79–89. bottomlands in the upper Colorado River basin, TYUS, H.M., AND C.A. KARP. 1989. Habitat use and stream- 1993–1994. Final report submitted to the Recovery flow needs of rare and endangered fishes, Yampa Implementation Program for the Endangered Fish River, Colorado. U.S. Fish and Wildlife Service, Bio- Species in the Upper Colorado Basin, U.S. Fish and logical Report 89(14). 27 pp. Wildlife Service, Denver, CO. TYUS, H.M., C.W. MCADA, AND B.D. BURDICK. 1981. Radio- IRVING, D.B., AND T. M ODDE. 1994. Assessment of Colo- telemetry of Colorado squawfish and razorback suck- rado squawfish in the White River, Colorado and ers, Green River system of Utah. Transactions of the Utah, 1992–1994. Final report. Recovery Implemen- Bonneville Chapter, American Fisheries Society tation Program, Upper Colorado River Basin. US. 1981:19–24. Fish and Wildlife Service, Denver, CO. WICK, E.J., J.A. HAWKINS, AND C.A. CARLSON. 1985. Colo- JORDAN, D.S., AND B.W. EVERMAN. 1986. The fishes of rado squawfish and humpback chub population and North and Middle America. Bulletin of U.S. Natural habitat monitoring 1981–1982. Draft. Colorado Museum 47 (4 parts), I-IX:1–3313. Division of Wildlife, Endangered Wildlife Investiga- MCADA, C.W., W.R. ELMBLAD, K.S. DAY, M.A. TRAMMELL, tions Job Progress Report SE3-6. Denver, CO. AND T.E. CHART. 1998. Interagency standardized monitoring program: summary of results, 1997. Recov- Received 31 March 1998 ery Implementation Program for the Endangered Accepted 30 November 1998 Western North American Naturalist 60(1), © 2000, pp. 26–33

JUNIPERUS OCCIDENTALIS (WESTERN JUNIPER) ESTABLISHMENT HISTORY ON TWO MINIMALLY DISTURBED RESEARCH NATURAL AREAS IN CENTRAL OREGON

Peter T. Soulé1 and Paul A. Knapp2

ABSTRACT.—While a trend toward western juniper ( Juniperus occidentalis spp. occidentalis) super-dominance in big sagebrush (Artemisia tridentata) communities of the Pacific Northwest since the late 1800s has been well documented, establishment dates of western juniper in less disturbed environments have not. In this paper we document the establishment history of western juniper on 2 minimally disturbed research natural areas that have substantial differences in their physical characteristics. On each site we randomly established twenty 0.05-ha plots to obtain per hectare counts of mature and juvenile western juniper and to obtain a sample of 100 trees closest to the plot center. These trees were then dated using standard dendrochronological techniques. The lower-elevation, more xeric site has an establishment history that suggests it is an emerging western juniper woodland, with the majority of trees sampled establishing since 1978. The higher-elevation site is an older, well-established woodland with a more even temporal distribution of trees. These results suggest that suitable establishment sites may switch from canopy dependence in emerging woodlands to open sites in mature woodlands and that neither domestic livestock grazing nor active fire suppression is a required mechanism for establishment.

Key words: western juniper, establishment history, expansion, central Oregon, dendrochronology.

The range of western juniper ( Juniperus in central Oregon despite a trend toward in- occidentalis spp. occidentalis Hook.) has ex- creasing aridity. panded considerably during the last century, Causes of western juniper expansion are and today these woodlands occupy >1 million complex, likely interactive, and site specific, ha of the inland Pacific Northwest (Caraher but generally are linked to some combination 1978, Miller and Wigand 1994). Studies exam- of domestic livestock grazing, altered fire re- ining establishment periods of western juniper gimes, and favorable climatic periods (Burk- indicate that expansion began in the late 1800s hardt and Tisdale 1976, Bedell et al. 1993, and, in many locations, has accelerated, includ- Miller and Wigand 1994). Additional possibili- ing sites in central Oregon (Eddleman 1987), ties include either a biological inertia effect as southeastern Oregon (Miller and Rose 1995), the seed rain of maturing western juniper and, at least for low sagebrush (Artemisia increases the number of progeny with time arbuscula Nutt.) sites, in northern California (Miller and Rose 1995), or the effects of ele- (Young and Evans 1981). Much of this historic vated atmospheric CO2 preferentially favoring expansion differs from prehistoric Holocene western juniper over herbaceous codominants expansions since establishment has been pri- (Miller and Wigand 1994, Knapp and Soulé marily confined to the 1998). Causes of expansion are difficult to determine, particularly when the role of land- more mesic sagebrush steppe communities use history complicates interpreting the effects rather than downslope into the Wyoming big of nonland-use mechanisms. Some sites do sagebrush Artemisia tridentata spp. wyomin- exist, however, with a history of minimal human gensis Nutt. communities (Miller and Wigand agency. Because of this, the primary purpose 1994:472). of this study is to document the establishment history of western juniper on 2 minimally dis- That said, there is evidence that expansion turbed research natural areas (RNAs) in cen- also may be occurring in the most marginal tral Oregon and to describe how differences in (i.e., xeric) areas (e.g., Knapp and Soulé 1996) physical characteristics of these sites relate to

1Department of Geography and Planning, Appalachian State University, Boone, NC 28608. 2Department of Anthropology and Geography, Georgia State University, Atlanta, GA 30303.

26 2000] WESTERN JUNIPER ESTABLISHMENT HISTORY 27 previously documented (Knapp and Soulé While HRRNA has been a 240-ha fenced 1996, 1998) expansion of western juniper exclosure only since 1974, historic impacts of within RNA boundaries. anthropogenic activities have likely been minimal because of a lack of permanent water to STUDY SITES support domestic livestock grazing (Hall 1972). The dominant plant community on HRRNA is Sites chosen for this study are both RNAs currently Juniperus occidentalis/Artemisia managed by the Bureau of Land Management tridentata/Festuca idahoensis (Idaho fescue; (BLM). As RNAs they are atypical of western Knapp and Soulé 1998). Carex filifolia (thread- juniper woodlands in central Oregon in that leaved sedge) is also present and has been their usage is limited, grazing is not allowed, classified as the dominant herbaceous species and they are not subject to active fire suppres- on the site in previous work (Gashwiler 1977, sion. Of the 2 sites, Island Research Natural Franklin and Dyrness 1988). Vegetation has Area (IRNA; Fig. 1) is less disturbed, largely developed on the Stookmoor-Westbutte com- because of its location at the confluence of the plex soil series, characterized by soils of vol- Crooked and Deschutes rivers. At 730 m ele- canic ash formed over basaltic and welded tuff vation, IRNA is an island mesa surrounded by colluvium (USDA-NRCS in press). Both Gash- 60- to 215-m vertical cliffs that limit access. wiler (1977) and Knapp and Soulé (1998) sug- The only historic record of domestic grazing gest that influences of fire on western juniper on IRNA was during the 1920s, when sheep stand dynamics on HRRNA are minimal. Sin- grazed on the plateau for 2 consecutive sum- gle or small groups of trees have burned on mers (Driscoll 1964, Knapp and Soulé 1996). HRRNA, but fire does not appear to carry Surface and subsurface soils are thick loams well because of insufficient fine fuels. (25–40 cm) with 1–2% organic matter in the Agency Sandy soil series (USDA-NRCS in METHODS press). They support a plant community domi- IRNA nated by Juniperus occidentalis/Artemisia tridentata/Agropyron spicatum (western juniper/ Beginning at a randomly chosen distance big sagebrush/bluebunch wheatgrass; Franklin between 100 m and 1000 m north-northwest and Dyrness 1988, Knapp and Soulé 1996). of the southernmost macroplot established by The climate is semiarid, with precipitation Driscoll (1964), we established 4 macroplot averaging 25 cm annually, and average tem- centers at 500-m intervals on a north-north- westerly vector that follows the natural align- peratures of 18.1°C in July and –0.4°C in Jan- ment of the plateau. We then established five uary at nearby Prineville (Fig. 1; Karl et al. 0.05-ha plots 30 m from the 4 macroplot cen- 1990). As documented by Knapp and Soulé ters at azimuths 0, 72, 144, 216, and 288. (1996), there have been no recent (since 1960) To determine the density of mature and fires of any significance to western juniper juvenile western juniper, we counted all indi- stand dynamics on IRNA. However, there is viduals within the 20 plots. All individuals <1 evidence (e.g., charcoal on snags, areas where m in height were counted as juveniles, and in- tree and shrub associations are not dominant; dividuals up to 1.25 m in height were counted Driscoll 1964, personal observations 1997) as juveniles if they displayed juvenile foliage that historical fires may have carried through (i.e., full needle or a mix of needles and awl- small sections of IRNA. like foliage). We also recorded the location of Horse Ridge Research Natural Area each juvenile using 4 categories: (1) within the (HRRNA) is approximately 31 km south- canopy of a mature western juniper, (2) within southeast of Bend, Oregon (Fig. 1), on rolling the canopy of a shrub (generally Artemisia tri- terrain of 1250–1430 m. Precipitation at both dentata, big sagebrush), (3) in grass, or (4) in Prineville and Bend is winter dominated, with interspace/rock. Bend recording an annual mean precipitation The center point of each 0.05-ha plot was of 31 cm. Mean temperatures at Bend range used for dendroecological sampling. Specifi- from 17.7°C in July to –0.6°C in January (Karl cally, we sampled 5 western juniper closest to et al. 1990), but the temperatures on HRRNA the plot center regardless of age, for a total are likely lower because of elevational cooling. sample of 100 trees. If the tree was large 28 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 1. Location of the study sites in central Oregon.

enough for us to core without damage (gener- JUVENILE SAMPLE FOR REGRESSION ESTIMA- ally basal diameter >5 cm and height >1 m), TION.—We obtained a separate random sam- we obtained 2 core samples using standard ple of n = 30 juveniles on land adjacent (<1 techniques (Phipps 1985). Core samples were km away) to IRNA with similar soils, slope, taken as close to ground level as possible, and elevation, aspect, climate, and vegetation asso- the height at which each sample was taken ciation. The use of adjacent land was needed (generally 20–40 cm) was recorded. If the tree because all work on RNAs must be nondestruc- was not coreable, its height was recorded and tive (i.e., no cutting of vegetation allowed). We age estimated through regression based on a measured the 30 juveniles, cut them at ground separate juvenile sample. Seedlings were iden- level, and obtained interior dates (dating done tified and aged as 0 yr old (i.e., 1997 represents by LTRR) using standard techniques (Stokes 1st growing season) if the cotyledon was still and Smiley 1968). We then developed linear attached. Collected tree cores were crossdated regression models to estimate age of uncore- by the Laboratory of Tree Ring Research (LTRR) able trees based on height, and to adjust for in Tucson, Arizona, using standard dendro- the height at which core samples were taken chronological techniques (Stokes and Smiley on mature trees (i.e., how many years did it 1968). For each tree in the age sample we also take the tree to reach the height at which core recorded height (measuring directly or with a samples were taken). clinometer), basal diameter, sexual development PRESENTATION OF ESTABLISHMENT HISTORY.— (male—no cones or berries, female—ample To examine establishment history, trees were cones or berries, mixed—cones or berries pre- placed into 4 categories and counts made for sent, but scarce), and full or strip bark. each decade ending in 1xx7 (e.g., 1818–1827, 2000] WESTERN JUNIPER ESTABLISHMENT HISTORY 29

1988–1997). While western juniper has been produced the following model: crossdated successfully in various locations throughout its range (Holmes et al. 1986) and age = 8.223 + 0.117(height); has a high crossdating index (Grissino-Mayer P = 0.0307, R2 = 0.16. 1993), it was not possible to definitively age each tree in our sample. Because of a combi- The model was positively heteroscedastic, with nation of heart rot and the asymmetrical nature variability in age prediction most pronounced of western juniper growth, we were unable to at heights >50 cm. As most trees were cored reach the pith (or near pith) on all trees dated at 30 cm height, age adjustment for borer through core samples. These trees were placed height was less influenced by this variability. in an “as old as” category, meaning we know All trees aged via regression established in the only that they are at least as old as the age pre- last 3 decades (Fig. 2), and only 15% fall into sented. Trees placed in the “aged” category the “as old as” category. Thus, the time line were samples in which pith was obtained or provides a relatively accurate assessment of the ring pattern was tight enough that the establishment history for western juniper on innermost ring was within a few rings (±4) of IRNA. pith. Trees placed in the “regression” category were juveniles aged through regression; seed- HRRNA lings were placed in the “seedling” category. Density of western juniper on HRRNA was 261 trees ha–1 (13% juvenile, 87% adult). Juve- HRRNA niles were found most frequently within grass For HRRNA, methods were identical to (49% of the per hectare count), followed by IRNA with 2 exceptions. First, on HRRNA we shrubs (29%), within the canopy of a mature randomly selected 20 sample plots from a 144- western juniper (11%), and in interspace or station (12 × 12) grid established by Gashwiler rock (11%). (1977). This grid is roughly in the center of the Because of an extremely tight ring pattern, fenced exclosure with plot centers located 3 mature trees sampled on HRRNA were 40.2 m apart and permanently marked with undatable. Thus, only the 97 trees closest to steel stakes. Second, the juvenile sample for plot centers were used to determine establish- age estimation was collected on land immedi- ment history. Of these, 15 were juveniles that ately outside the fenced boundaries of the we dated by regression (no seedlings were exclosure. found) and 82 were mature. The height of mature (coreable) western juniper ranged from RESULTS 110 cm to 945 cm (mean = 437 cm, s = 202 cm), with basal diameters of 5–90 cm (mean = IRNA 35 cm, s = 21 cm). The majority of trees were Density of western juniper on IRNA was of mixed development (66%), followed by 73 trees ha–1 (81% juvenile, 19% adult). Juve- male (24%), and female (10%). A small number niles were found most frequently under the were strip bark (9%), the remaining full bark canopy of mature western juniper (44% of the (91%). per hectare count), followed by shrubs (41%), The age/height relationship was linear and grasses (10%), and interspace or rock (5%). produced a model with the form: The separate sample of 100 trees closest to plot centers used to determine establishment age = 3.899 + 1.000(height); history had a slightly different ratio: 64% juve- P = 0.0001, R2 = 0.42. nile and 36% adult. The height of mature (coreable) western juniper ranged from 120 cm Residuals from this model were randomly dis- to 899 cm (mean = 560 cm, s = 203 cm), with tributed. With slower growth rates at basal diameters of 4–72 cm (mean = 40 cm, s HRRNA, trees aged via regression extend = 21 cm). Most mature trees were females back to the 1910s (Fig. 3). While a higher per- (78%), with 0% male and 22% mixed. All centage of trees in the HRRNA sample were mature trees were full bark. placed in the “as old as” category (30%), most The age/height relationship developed from (70%) were datable through core sampling or the 3rd independent sample was linear and regression techniques. 30 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 2. Establishment history, by decades ending in 1xx7, for western juniper on IRNA. Key to symbols: aoa = as old as, pith = dated by pith, reg = dated by regression, cot = dated by presence of cotyledon.

DISCUSSION Rose (1995:40, Fig. 1). Lack of fire, an abundance of nurse plants, and biological inertia The ratio of juveniles to adults at IRNA is manifested through an increased seed rain high, with >60% of all trees sampled establish- appear to be synergistically supporting the ing since 1978. Most juveniles have become rapid expansion of western juniper in south- established within the canopy of either shrubs eastern Oregon in recent decades (Miller and or western juniper, and there is a high per- Rose 1995), and these same factors are a com- centage of female trees. IRNA thus exhibits ponent of the recent history on IRNA. Recent characteristics of an emerging woodland where fires are rare (despite the lack of fire suppres- the importance of nurse-plant sites is para- sion) on IRNA, there is a high percentage of mount to successful establishment, particularly female trees (many with copious berry pro- in xeric, low-elevation locations. Burkhardt duction), and cover and density of trees and and Tisdale (1976) have shown that the mor- shrubs have increased significantly since 1960 tality rate for western juniper seedlings is low, (Knapp and Soulé 1996). even during drought conditions. Thus, barring Others (Burkhardt and Tisdale 1976:477, Fig. a widespread fire that could cause a high rate 1; Young and Evans 1981:503, Fig. 4; Eddle- of mortality, IRNA should exhibit large man 1987:256, Fig. 1) have documented sharp increases in density and cover in the next sev- increases in the rate of expansion of western eral decades as juveniles mature. juniper on disturbed sites during the 20th The accelerated establishment rate at IRNA century, although rates are not as extreme as in the last 2 decades (Fig. 2) is comparable to those found at IRNA during the last 2 decades. establishment data presented by Miller and Burkhardt and Tisdale (1976) suggest that the 2000] WESTERN JUNIPER ESTABLISHMENT HISTORY 31

Fig. 3. Establishment history, by decades ending in 1xx7, for western juniper on HRRNA. (Note: There were no seedlings in our n = 100 sample.) Key to symbols: aoa = as old as, pith = dated by pith, reg = dated by regression, cot = dated by presence of cotyledon.

rapid rate of juniper expansion on the Owyhee do not correspond to a peak of establishment Plateau in Idaho is related to a cessation of on HRRNA. periodic fires caused by fire suppression and a The presence of nurse-plant sites (i.e., estab- reduction in fine fuels associated with domes- lishment within the canopy of western juniper tic livestock grazing. In addition to fire and or big sagebrush) has been suggested as an grazing, Miller and Rose (1995:43) suggest element of western juniper expansion (e.g., that “optimal climatic conditions around the Eddleman 1987, Evans 1988). While the juve- turn of the century” may have contributed to nile location data for IRNA support this (i.e., the rapid expansion of western juniper on 85% of juveniles growing within the canopy of their study sites in southeastern Oregon dur- trees or shrubs), location data on HRRNA do ing the 20th century. While the majority of not. Of the more recent establishment dates, establishment on IRNA is recent, a minor these have been contributed by western juniper establishment spike appears to have occurred growing on the more open northeastern slope in the late 1800s, with 6% of sampled trees of HRRNA (nearly half of all juveniles were establishing in the 1880s (Fig. 2). found in open canopy sites), as opposed to the At HRRNA approximate periods of estab- more densely covered southeastern slope. lishment appear more evenly distributed (Fig. These results suggest that a cover/density thres- 3). Peaks of establishment occur in the late hold may exist that impedes future establish- 1600s and early 1700s, the 1830s, and the ment of western juniper. Similar conclusions 1910s through 1930s, but in no decade are >5 were drawn by Young and Evans (1981:502), trees (or roughly 5% of the sample) known to who speculated that low western juniper have established. Favorable climatic condi- establishment rates in big sagebrush commu- tions of the late 1800s (Miller and Rose 1995) nities of northern California could be the result 32 WESTERN NORTH AMERICAN NATURALIST [Volume 60 of high juniper cover (40–60%) and interspaces 1998), certainly must have been conducive for filled with roots that “effectively” excluded their establishment and expansion. study site stand from much future establishment. Our knowledge of growth characteristics of The value of examining establishment peri- western juniper in undisturbed environments ods for western juniper is manifested when is critical in making informed decisions about coupled with measurements of expansion rates land management throughout its range. Fur- of the corresponding sites. After examining ther research on undisturbed environments, multi-date, large-scale aerial photography dur- especially comparative analyses of establishing 1961–1994 at IRNA and 1951–1995 at ment histories of undisturbed sites with adja- HRRNA, Knapp and Soulé (1996, 1998) deter- cent disturbed sites exhibiting the same physi- mined that cover of western juniper increased cal characteristics, should help us understand by 5.2% and 19.9%, respectively. At HRRNA the driving forces behind juniper expansion recent expansion (measured as an increase in on semiarid lands. cover) has been linked primarily with matura- ACKNOWLEDGMENTS tion of adults and with the few juveniles that have established on open canopy sites. Much This work was funded by the U.S. Depart- of the cover change at HRRNA has occurred ment of the Interior, Bureau of Land Man- from significant increases in stems growing agement Challenge Cost Share Grant from the central trunk of mature trees (Knapp #1422HO50P97004 and by an Appalachian and Soulé 1998). While expansion may con- State University Research Council Grant. We tinue on HRRNA, especially on the more open thank Ron Halvorson for his assistance on this northeastern slope, establishment data suggest project. that the rate of expansion will be much slower than that observed on more open woodlands. LITERATURE CITED From the standpoint of establishment his- BEDELL, T.E., L.E. EDDLEMAN, T. DEBOODT, AND C. JACKS. tory, the most important variant for these 2 1993. Western juniper: its impact and management RNAs, especially IRNA, is the lack of domes- in Oregon rangelands. Oregon State University tic livestock grazing. While grazing is often Extension Service Publication EC1417. BURKHARDT, J.W., AND E.W. TISDALE 1976. Causes of viewed as an integral driving force behind juniper invasion in southwestern Idaho. Ecology 57: western juniper expansion, it is nearly absent 472–484. from the known land-use history of IRNA and CARAHER, D.L. 1978. The spread of western juniper in has not occurred at HRRNA since the comple- central Oregon. Pages 1–7 in R.E. Martin, J.E. Dealy, and D.L. Caraher, editors, Proceedings of the west- tion of the exclosure fence in 1974. Thus, graz- ern juniper ecology and management workshop. ing cannot be identified as a potential driving General Technical Report PNW-74, USDA Forest force behind expansion at IRNA, and its role Service, Portland, OR. at HRRNA has likely been minimal. DRISCOLL, R.S. 1964. A relict area in the central Oregon juniper zone. Ecology 45:345–353. We recognize that our results are based on EVANS, R.A. 1988. Management of pinyon-juniper wood- 2 sites and thus may not reflect western juniper lands. General Technical Report INT-249, United establishment characteristics on all minimally States Department of Agriculture, Ogden, UT. 34 pp. EDDLEMAN, L.E. 1987. Establishment and stand develop- impacted sites. They do, however, potentially ment of western juniper in central Oregon. Pages illustrate 3 aspects of western juniper expan- 255–259 in Proceedings—pinyon-juniper conference. sion. First, expansion (as manifested as an in- General Technical Report INT-215, United States crease in cover) is not necessarily associated Department of Agriculture, Ogden, UT. FRANKLIN, J.F., AND C.T. DYRNESS. 1988. Natural vegeta- with recent establishment periods but rather tion of Oregon and Washington. Oregon State Uni- may reflect the ongoing effects of canopy and versity Press, Corvallis. 452 pp. stem development. Second, suitable establish- GASHWILER, J.S. 1977. Bird populations in four vegeta- ment sites may switch from canopy depen- tional types in central Oregon. Special Scientific Report—Wildlife No. 205, United States Department dence in emerging woodlands to open sites in of Agriculture, Fish and Wildlife Service, Washing- maturing woodlands. Third, the role of domes- ton, DC. 20 pp. tic livestock grazing or active fire suppression GRISSINO-MAYER, H.D. 1993. An updated list of species is not required for establishment to occur, used in tree-ring research. Tree-ring Bulletin 53:19–41. although extensive fire-free periods, as these 2 HALL, F.C. 1972. Horse Ridge Research Natural Area. sites have experienced (Knapp and Soulé 1996, Pages HR1–HR7 in Federal research natural areas in 2000] WESTERN JUNIPER ESTABLISHMENT HISTORY 33

Oregon and Washington—a guidebook for scientists MILLER, R.F., AND P.E. WIGAND. 1994. Holocene changes and educators. Pacific Northwest Forest and Range in semiarid pinyon-juniper woodlands. BioScience Experiment Station, Portland, OR. 44:465–474. HOLMES, R.L., R.K. ADAMS, AND H.C. FRITTS. 1986. Tree- PHIPPS, R.L. 1985. Collecting, preparing, crossdating, and ring chronologies of western North America: Cali- measuring tree increment cores. U.S. Geologic Sur- fornia, eastern Oregon and northern Great Basin. vey Water-Resources Investigations Report 85-4148. Chronology Series VI. University of Arizona, Tucson. 48 pp. KARL, T.R., C.N. WILLIAMS, JR., F.T. QUINLAN, AND T.A. STOKES, M.A., AND T.L. SMILEY. 1968. Introduction to tree- BODEN. 1990. United States Historical Climatology ring dating. University of Chicago Press, Chicago. Network (HCN) serial temperature and precipitation USDA–NATURAL RESOURCES CONSERVATION SERVICE.In data. Carbon Dioxide Information Analysis Center, press. Upper Deschutes River, Oregon Soil Survey. Oak Ridge, TN. USDA-NRCS, Washington, DC. KNAPP, P.A., AND P. T. S OULÉ. 1996. Vegetation change and YOUNG, J.A., AND R.A. EVANS. 1981. Demography and fire the role of atmospheric CO2 enrichment on a relict history of a western juniper stand. Journal of Range site in central Oregon: 1960–1994. Annals of the Management 34:501–506. Association of American Geographers 86:387–411. ______. 1998. Recent expansion of western juniper on Received 11 June 1998 near-relict site in central Oregon. Global Change Accepted 6 May 1999 Biology 4:347–357. MILLER, R.F., AND J.A. ROSE. 1995. Historic expansion of Juniperus occidentalis (western juniper) in southeastern Oregon. Great Basin Naturalist 55:37–45. Western North American Naturalist 60(1), pp. 34–56

CHIRONOMIDAE (DIPTERA) SPECIES DISTRIBUTION RELATED TO ENVIRONMENTAL CHARACTERISTICS OF THE METAL-POLLUTED ARKANSAS RIVER, COLORADO

L.P. Ruse1, S.J. Herrmann2, and J.E. Sublette3

ABSTRACT.—Mining in the Upper Arkansas catchment has polluted the river with heavy metals for 140 yr. Pupal and adult chironomid species distribution and sedimentary metal concentrations are provided for 22 stations along 259 km of main river during 1984–85. Complete species identification was achieved only recently. This has produced an unprecedented record of chironomid species distribution for a comparable length of river in the USA. Chemically or physically perturbed sites had poor species richness compared with the next site downstream, suggesting that larvae may drift through unfavorable habitats to benign ones. Using canonical correspondence analysis, we found species composition to be most strongly related to variables expressing the longitudinal axis of the river (distance/altitude, temperature, latitude), while toxicity to zinc was a significant secondary correlate. These river-related environmental variables accounted for a greater proportion of pupal species variation than for adults. This was considered to result from a proportion of adults emerging from habitats beyond the main river. Multivariate analysis identified metal-tolerant and -intolerant species. Generic data revealed the same major trends but indicator taxa were lost. The study provides a disturbed-state reference for monitoring effects of remedial actions begun in 1991, and for comparisons with other Colorado rivers.

Key words: Chironomidae, heavy metals, multivariate analysis, pupal exuviae, adults, spatial distribution, sediments, species richness.

The Arkansas River in Colorado has been can be made easier and more efficient by sam- polluted by heavy metals since mining began pling pupal exuviae, compared with larvae (Fer- in 1859. Remedial action on the most affected rington et al. 1991). Although exuviae will sites started in 1991. There have been many remain afloat for 2–3 d after adult emergence, descriptive and experimental studies of pollu- they do not drift far before entrapment at river tion effects on benthic macroinvertebrates margins or midstream obstacles (McGill 1980, inhabiting the first 30 km of the river by Ruse 1995a). Exuvial collections should there- researchers of the Bureau of Reclamation and fore be representative of local adult emergence, Colorado State University (e.g., Roline and integrated over a few days before sampling. Boehmke 1981, Roline 1988, Kiffney and In 1983 a major surge of metal sludge in the Clements 1993, Clements 1994, Clements and Upper Arkansas River affected sites 220 km Kiffney 1994). Typically, invertebrates were downstream (Kimball et al. 1995). Emerging sampled using mesh sizes of 500 µm or greater adult chironomids, and later pupal exuviae, and Chironomidae (non-biting midges) were were collected from sites along this length of never identified beyond the subfamily level. the Arkansas River during 1984–85 to investi- Armitage and Blackburn (1985) demonstrated gate the effects of metal pollution on species that specific identification of Chironomidae spatial distribution. At that time many individ- distinguished varying degrees of metal pollu- uals could not be identified to species, particu- tion as efficiently as using all macroinverte- larly pupal exuviae. Associations between lar- brate data with chironomids identified only to vae, pupae, and adults from rivers in Colorado subfamily. Clements (1994) has accepted that and neighboring states have since enabled spe- research on metal tolerances of orthocladiine cific identification (Sublette et al. 1998). This species (a subfamily of Chironomidae) is nec- has led to a retrospective investigation of the essary for the Arkansas River. The collection relationship between species distribution and and specific identification of Chironomidae available environmental data using statistical

1Environment Agency (Thames Region), Fobney Mead, Rose Kiln Lane, Reading RG2 0SF, England. 2University of Southern Colorado, 2200 Bonforte Boulevard, Pueblo, CO 81001, USA. 33550 North Winslow Drive, Tucson, AZ 85750, USA.

34 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 35 packages that were not available during the Reservoir reveals that a substantial metal load survey period. This study also differed from is transported there from the Leadville area, other research on the Arkansas River by relat- particularly due to resuspension of river sedi- ing invertebrate distribution to sedimentary ments by snowmelt runoff (Kimball et al. 1995). concentrations of heavy metals rather than The U.S. Environmental Protection Agency water measurements. Kiffney and Clements (EPA) declared the California Gulch catch- (1993) found that suspended metal concentra- ment and the Arkansas River from above AR2 tions in the Arkansas River underestimated to below AR3 a Superfund site in 1983. New availability of metals to benthic macroinverte- water treatment plants on the Leadville Drain brates. Bioaccumulated metal concentrations and California Gulch were in operation by were better related to those measured in sedi- June 1992, and the last major mining opera- mentary minerals and periphyton. This survey tion in Leadville ceased in January 1999. provides the only reference for measuring the Biological Data effect of subsequent remedial actions on the chironomid assemblage of the Arkansas River We collected adult Chironomidae at each and relating their distribution to sedimentary site monthly from May 1984 until September metal concentrations during a period of severe 1985 using sweep net, beating sheet, water- pollution. skimming, hand-picking and ultraviolet light traps. Adults were dissected in absolute METHODS ethanol. Body parts, except for wings and 1 set of legs, were cleared in potassium hydroxide Study Sites and then all parts slide-mounted in Euparal. Twenty-two sites were chosen along 259 Adult Plecoptera and Trichoptera were also km of the East Fork (EF) and Arkansas River collected and are reported in the following (AR) between Climax and Pueblo, east of the paper (Ruse and Herrmann 2000). Continental Divide in central Colorado (Fig. We sampled chironomid pupal exuviae using 1). We adopted sites EF1 downstream to AR9 the “Thienemann net technique” (Thiene- from those surveyed by the Bureau of Recla- mann 1910): a 200-µm-mesh net attached to a mation and reported by Roline (1988). Other circular frame on a pole is used to collect float- biological surveys of the Upper Arkansas ing debris accumulating behind obstacles at catchment have adopted the same site codes, river margins. This method supplemented but since these may refer to different loca- adult collections during a 3-month visiting tions, care should be taken when cross-refer- scholarship by the senior author. Each site was encing with previous publications. sampled in July, August, and September 1985. Metal-rich water enters East Fork between The broad emergence period by many tem- EF1 and EF2 via Leadville Drain, but the perate, lotic species of Chironomidae should greatest source of metals to the catchment ensure that a large proportion of species pre- comes from California Gulch between AR2 sent over the whole year are represented by and AR3 (Kimball et al. 1995). This survey this frequency of sampling (Ruse and Wilson occurred between 2 major metal sludge surges 1984, Ruse 1995b). Samples were refloated, into California Gulch on 23 February 1983 and agitated, and randomly subsampled by sieve. 22 October 1985. Water diverted from the All chironomid pupal exuviae were removed western slopes of the Continental Divide sup- from a subsample and sufficient subsamples plements flows from Turquoise Lake and Twin were sorted to obtain about 200 exuviae, when Lakes, entering the Arkansas River above AR4 possible. Exuviae were mounted on glass micro- and AR9, respectively. Iowa Gulch, and dif- scope slides in Euparal or retained in vials of fuse sources of metals between AR4 and AR8, 70% ethanol. Initially identified to generic carried discharge from an active mine during level, the material remained in excellent con- the study period. Mining affects other tribu- dition until 12 yr later when it became possi- taries to the river downstream of AR8, but ble to determine species. Specific identifica- concentrations of metals are much lower than tion was achieved by comparing exuviae with those found upstream. The Arkansas River those obtained from adult rearings of larvae was impounded above AR19 by the Pueblo and pupae collected subsequently from the Dam in 1974. Sediment analysis of Pueblo Arkansas River and neighboring catchments in 36 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 1. Upper Arkansas River sampling points.

Colorado and New Mexico. The associated tum types, among 5 size classes, were assessed material is held by author JES. Unassociated visually. Latitude, longitude, altitude, slope, and pupal species are designated by the suffix n-P. distance downstream from EF1 were obtained from maps. Environmental Data We determined metals from 2 samples of At each site water temperature was recorded submerged fine sand taken at each site during once during each monthly visit to collect adult 18–19 October following the 2nd metal sludge insects. The 3 dominant superficial substra- surge into California Gulch. These data still 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 37 served to characterize the relative contamina- number of individuals identified from a site. tion of sites by metals emanating from Lead- Species recorded at 1 site only were omitted ville mines. A 25-mm-diameter PVC pipe was from CCA in case of spurious association with inserted to a depth of 15 cm. Sediments were a coincidental extreme environmental mea- dried at 70°C for 48 h and ground with a mor- surement; their distributions are recorded in tar and pestle until they passed through a the Appendix. An ordinal value representing 250-µm-mesh sieve. Metals were extracted relative variation in substratum between sites from triplicate subsamples of approximately was obtained by assuming a mean particle size 500 ± 0.1 mg using a sequence of hot diges- for each of 3 categories: boulder/bedrock (215 tions and evaporations with nitric and hydro- mm), rubble/gravel (9.5 mm), and sand (0.25 chloric acids (Caravajal et al. 1983). A reagent mm). The dominant substratum was assumed blank was prepared before and after each set to cover 50% of the site, and the next 2 re- of 6 sediment digestions for a site and taken corded substrata were assumed to cover 30% through the same protocol prior to metals and 20% of the site, respectively. Mean parti- determination. Determination of lead (Pb), iron cle size at each site was calculated from the (Fe), manganese (Mn), zinc (Zn), and copper sum of products of size times proportional (Cu) by flame atomic absorption spectrometry coverage. To account for the ameliorating effect followed the methods of Mahan et al. (1987). of increased hardness on metal toxicity to Cadmium (Cd) was measured by electrother- biota, we calculated EPA hardness-based water mal atomization atomic absorption spectrome- quality criterion for Zn (Clements and Kiffney try (Sandoval et al. 1992). The mean concen- 1995). Water hardness was not measured dur- tration of 6 samples from each site was used in ing this survey, but data were available for subsequent data analysis. sites EF1 to AR9 (Roline and Boehmke 1981, Clements and Kiffney 1995) and for inlet and Data Analysis outlet flows of Pueblo Reservoir (Herrmann Species abundances for samples from the and Mahan 1977). The presence of carbonate same site were combined for both pupal and rocks between AR10 and AR12 and river- adult data sets so they could be related to exposed deposits of calcium and magnesium environmental characteristics recorded on only near AR16 (Kimball et al. 1995) was also taken a single occasion. Spatial variation in these into account when estimating water hardness. data sets was directly compared with environ- For each site, we divided the observed sedi- mental variation using canonical correspon- mentary Zn-loading by the criterion value for dence analysis (CCA; Ter Braak and Prentice assumed water hardness. Resultant ratios 1988). CCA selected the linear combination of were classified into an ordinal scale of toxicity environmental variables achieving the maxi- to Zn: <2.0 = 1, 2.0–9.9 = 2, 10.0–19.9 = 3, mum separation of species by multiple regres- 20.0–39.9 = 4, >39.9 = 5. These broad bands sion along the 1st axis. Subsequent axes were reduced the effect of imprecise hardness esti- extracted from the residual variation to maxi- mates. Environmental data were not trans- mize dispersion of species, provided they formed for CCA; measurements of tempera- were uncorrelated to previous axes. Signifi- ture, slope, Zn toxicity, total Mn, and total Fe cance of the regression between biological and were normally distributed. Latitude and longi- environmental data was tested against the pos- tude values were decimalized and only the sibility of a random association by comparing maximum water temperature recorded at each the F-ratio with 99 unrestricted Monte Carlo site was used. Environmental data were stan- permutations of these data (Ter Braak 1990). A dardized to have a mean of zero and unit vari- probability of ≤0.05 was considered signifi- ance to remove arbitrary variation in units of cant. Forward stepwise regression was used to measurement. CCA species scores were objectively select variables, one at a time, weighted mean sample scores (CANOCO ver- according to the amount of biological variation sion 3.1 scaling + 2). The analysis was there- each explained. Selection stopped when there fore sensitive to relative variation between was no significant increase in explained varia- sites, and it was not necessary to have precise tion, tested against Monte Carlo permutations. data on particle size or water hardness to Before analysis, we converted chironomid relate these characteristics to trends in species species abundances to percentages of the total distribution. 38 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Direct statistical comparisons of pupal and Lake confluence, and then declined until AR10. adult species proportions were made using a Species numbers were high at AR11–AR12 χ2 test of independence (Sokal and Rohlf 1981). and depleted below Pueblo Reservoir at The null hypothesis was that proportions of AR19. Orthocladiinae was the dominant sub- each species collected were independent of family throughout the survey. There were no sampling method, aquatic netting, or aerial obvious downstream trends in total or subfam- netting. Pupal species unassociated with reared ily species richness except for the absence of adults were excluded, as were species with ex- Diamesinae below AR12. Classifying pupal pected counts <5 in both data sets. exuviae according to presumed feeding modes of their associated larvae (Table 2) revealed a RESULTS dominance by algal grazers at all sites (Fig. 3). Predators increased from AR13 until Pueblo Environmental Data Reservoir. Detritivores were present in low The obtuse-angled line of the main river proportions except at AR10. Filterers appeared prevented latitude or longitude having the from AR16 to AR18. simple linear relationship with distance that ORDINATION.—Stepwise regression selected altitude had (Table 1). The river gradient was distance downstream, maximum temperature, reduced at the last 3 sites, but the trend was latitude, and Zn toxicity as significantly corre- variable along most of the watercourse. Mean lated with variation in species composition particle size at the first 11 sites was often among sites. Altitude was also significant but smaller than at downstream sites. Site AR10 highly correlated with distance and was ex- was characterized by a steep gradient and tor- cluded to prevent multicollinearity (variation rential flow over a substratum dominated by inflation factor = 189; Ter Braak 1990). The 4 bedrock, boulder, and rubble. Maximum re- selected variables explained 43.4% of biologi- corded temperatures increased downstream to cal variation in CCA. The species-environ- AR7 but were suppressed below the Twin Lakes ment relationship was significantly different confluence until AR13. Hypolimnion flows from random for the first 2 CCA axes (P = from Pueblo Reservoir lowered temperature 0.01), accounting for 32.9% of all biological at AR19. Sedimentary total Cu was the only variation and 75.7% of explained variation. metal to reach a peak at AR3, below California Species turnover among samples was Gulch, while the next most Cu-contaminated strongly related to change along the longitudi- sites were AR5 and AR7. Zn toxicity, total Zn, nal axis of the river. Dominance of the 1st Mn, and Cd peaked at AR5, AR7, or AR8, all CCA axis compared with the 2nd resulted in reduced-gradient sites compared with AR3, an archlike configuration of sites in Figure 4. AR4, and AR6. Concentrations of sedimentary Gradient lengths for the first 2 unconstrained Fe below California Gulch remained high (biological data alone) axes were 6.24 and 2.82 throughout the river, except at AR12 and s units, respectively. Detrending or reduction AR19, peaking at AR11. of environmental variables did not remove the arching trend, and separation into 2 data sets Pupal Exuviae was impractical for the small number of sam- A total of 10,120 chironomid pupal exuviae ples. The 1st CCA axis was most significantly were identified to 127 species from 22 sites. related to downstream distance (canonical co- Species abundances are presented in Table 2, efficient t-value 5.42, interset correlation 0.97). with authors’ names, for species collected from The 2nd axis was principally related to varia- 2 or more sites. Species and sites in Table 2 tions in maximum temperature (t-value 6.05, are arranged according to the 1st axis of a cor- correlation –0.46) and Zn toxicity (t-value 2.77, respondence analysis (Ter Braak and Prentice correlation –0.29), resulting in lateral spread- 1988) so that downstream turnover in species ing of samples upstream of AR9, at AR13, and composition can be assessed. Species richness below Pueblo Reservoir. Sites EF2 and AR3, was lowest at EF2, below Leadville Drain, then downstream of the most significant metal increased downstream to the richest site at inputs of Leadville Drain and California Gulch, AR2, above the confluence with California respectively, were closely associated. Sites Gulch (Fig. 2). Species richness was poor at AR5–AR8 had the highest Zn toxicity ratios AR3, recovered at the 3 sites below Turquoise and similar species composition, although AR5 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 39 size (mm) dry weight –1 g µ C) ° ( (Deg.) (Deg.) temp. (m) (%) (km) tox. Cu Zn Pb Mn Fe Cd particle 1. Environmental data; mean total metal concentrations are ABLE T Site LatitudeEF1 LongitudeEF2 Max.AR1 39.28AR2 39.27 AltitudeAR3 39.25AR4 106.22 Slope 39.23AR5 106.33 39.22AR6 106.32 13.0 39.20AR7 106.35 Dist. 13.6 39.17AR8 106.35 14.5 39.13AR9 106.35 3042 14.2 Zinc 39.12AR10 106.33 2969 14.4 39.08AR11 106.32 2944 16.1 39.07 Total 1.1AR12 106.30 2905 38.97 17.4 1.1AR13 106.28 2899 38.78 18.1AR14 1.6 106.28 2865 38.53 Total 18.6 106.20AR15 1.4 2835 38.43 0.00 17.8 106.08AR16 1.4 2795 38.40 6.35 16.0 106.02 TotalAR17 1.0 15.5 2771 38.47 7.87 105.82AR18 0.5 11.11 1 16.5 2748 38.43 105.58AR19 1.7 11.18 2 Total 17.5 2743 38.31 105.40 2573AR20 0.8 14.48 2 19.4 38.26 105.25 2 2338 0.7 20.49 13.9 19.2 38.19 Total 105.00 3 2143 0.4 22.86 10.5 19.9 38.19 1.1 104.92 3 2033 25.91 21.5 0.9 6.0 104.70 5 Total 1879 29.08 132 21.5 4.8 157.0 0.6 104.67 4 1746 30.35 935 21.7 0.5 45.85 5 39.7 Mean 1618 19.6 548 0.6 71.75 4 80.0 1535 19.0 2374 320 21.0 104.77 0.6 2 46.6 1497 88.9 129.28 2 0.7 917 72.6 1444 156.59 2 2836 69.8 779.0 0.4 374 47.6 1431 2 41.0 177.80 1679 0.3 824 16.5 2 267.0 195.45 3038 14.0 0.2 865.0 2 824 825 217.80 8981 2392 21.7 0.3 602 451.0 2 228.98 8014 6.8 508 763.0 730 2 15.5 253.74 30400 420 780 6376 0.40 582.0 1 17.6 1149 258.56 5773 401 0.84 1 19.0 1017 12570 176.0 135 31000 161.4 2.97 1 263 18.0 1474 0.90 15760 2.9 112.7 0.57 1 269 30100 9.8 1.37 4.6 368 309 11.0 39.0 3.50 18570 590 59.6 2.70 4.6 332 4.6 4.8 473 36.3 4.6 4.23 12360 129 6.3 4.6 11350 59.1 1.65 123 198 4.6 256 32170 39.5 4.6 448 0.83 28 4.6 12.9 0.73 24.0 438 6910 20740 68 7.8 0.58 399 27370 115.0 4.6 30070 229 1.0 0.52 0.82 10.2 23720 21.9 290 0.50 18690 0.73 21.9 21.9 84 12410 0.35 143 21.9 0.38 21.9 18820 0.78 6810 21.9 3.2 0.08 0.25 3.2 45.3 4.6 40 WESTERN NORTH AMERICAN NATURALIST [Volume 60

TABLE 2. Proportions of pupal exuviae species at each site: 1 = 0.1–4.9%; 2 = 5.0–9.9%; 3 = 10.0–19.9%; 4 = 20.0–39.9%; 5 = 40.0+%. G = Grazer, D = Detritivore, P = Predator, F = Filterer. Trophic Code Species name group Site

EEAAAAAAAAAAAAAAAAAAAA 11111111112 1212345678901234567890 PROC_SUB Procladius subletti Roback P 1 – – 1 – – – 1 –––––––––––––– THIE_FUS Thienemannimyia fusciceps (Edwards) P 1 – – 1 – 1 –––––––––––––––– DIAM_HET Diamesa heteropus (Coquillet) G – – – 11211–––––––––––––– POTT_MON Potthastia montium (Edwards) D 1 – 1 ––––––––––––––––––– PAGA_PAR Pagastia partica (Roback) D 2111–11–1–1–11–––––––– HYDR_FUS Hydrobaenus fuscistylus (Goetghebuer) G 4 5 – 1211111––11–––––––– HYDR_PIL Hydrobaenus pilipes (Malloch) G – – – 1 – – – 1 –––––––––––––– DIPL_CUL Diplocladius cultriger Kieffer D – – – 1 1 1 – 1 –––––––––––––– EUKI_ILK Eukiefferiella ilkleyensis (Edwards) G – 1121111–1–111–1–––––– EUKI_2-P Eukiefferiella sp. 2-P G – 1112111–––1–1–––––––– EUKI_n9 Eukiefferiella n. sp. 9 G 1 1 – 3211–––––1––1–1–––– ORTH_DUB Orthocladius dubitatus Johannsen G – – – 1 – – 1 ––––––––––––––– ORTH_LUT Orthocladius luteipes Goetghebuer G – – 1111–1–1–––––––––––– ORTH_APP Orthocladius appersoni Soponis G – – – 1 – – 1 ––––––––––––––– ORTH_5-P Orthocladius sp. 5-P G – – – 1 ––––1––––––––––––– ORTH_NIG Orthocladius nigritus Malloch G – 3 – 1111–11––11–––––––– ORTH_OBU Orthocladius obumbratus Johannsen G – – – 1 1 1 – 1 1 ––––––––––––– PARA_n3 Paratrichocladius n. sp. 3 G – – 1 –––––––––1––––––––– PSEC_SPI Psectrocladius spinifer (Johannsen) G – – 1 1 – – – 1 –––––––––––––– RHEO_EMI Rheocricotopus eminelobus Sæther G – 311311111–11–––1––––– TVET_PAU Tvetenia paucunca (Sæther) G – – 444111111–11–––11––– CORY_LOB Corynoneura lobata Edwards G – – 1 1 – – – 1 –––––––––––––– CORY_5-P Corynoneura sp. 5-P G –––––1––––––1––––––––– KREN_CAM Krenosmittia camptophleps (Edwards) G – 11111––––––1––––––––– THIE_5-P Thienemanniella sp. 5-P G 1 – 1 1 – 1 –––––––––––––––– POLY_n1 Polypedilum n. sp. 1 D 1 – 11111–11–1–––––––––– TANY_8-P Tanytarsus sp. 8-P D 1 – 1 ––––––––––––––––––– TANY_n5 Tanytarsus n. sp. 5 D – – 1 1 ––––––––1––1–––––– BRUN_EUM Brundiniella eumorpha (Sublette) P ––––––1–1––––––––––––– CRIC_BIF Cricotopus bifurcatus Cranston & Oliver G –––––––11––––––––––––– CRIC_n18 Cricotopus n. sp. 18 G – – 1 1 – 112211–211–––1––– CRIC_19P Cricotopus sp. 19-P G ––––––11–––––––––––––– HETE_MAE Heterotrissocladius maeaeri Brundin D ––––––11––1–1––––––––– ORTH_FRI Orthocladius frigidus (Zetterstedt) G 4311154445411––1–––––– KREN_HAL Krenosmittia halvorseni (Cranston & Oliver) G ––––––112111–––––––––– SERG_ALB Sergentia albescens (Townes) P 1––1–––2–––––––––––––– CRIC_TRE Cricotopus tremulus (Linnaeus) G – – 1111111–12111111–1–– CRIC_SLO Cricotopus slossonae Malloch G – – 2 1 1 – 1111212121111––– ORTH_RVA Orthocladius rivicola Kieffer G 11422443323414344442–1 ORTH_MAL Orthocladius mallochi Kieffer G 1 – – 11133322112231111–1 ORTH_10P Orthocladius sp. 10-P G – – – 1 – – 1 ––––––––––1–––– THIE_1-P Thienemanniella sp. 1-P G – – 2121–1–––––1–––111–– POLY_ALB Polypedilum albicorne (Meigen) D – – – 1 – – – 1 –––––1–––––––– MICR_n6 Micropsectra n. sp. 6 D – – – 1 1 1 – – – 1 1 – – 1 – 1 – – –––1

was closer to sites downstream of outflows were associated with high sedimentary metal- from Turquoise Lake and Twin Lakes (AR4, loadings. Krenosmittia camptophleps, which AR9, and AR10). lives among coarse gravel, was found above Species toward the top left of Figure 4 were and below California Gulch but was absent at most abundant at, or restricted to, upstream sites with the highest sedimentary Zn-load- sites. Diplocladius cultriger was present below ings. Other species with an upstream distribu- California Gulch but absent from the most tion and which may be sensitive to high sedi- contaminated sites. Several Orthocladius species mentary Zn concentrations were Eukiefferiella 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 41

TABLE 2. Continued Trophic Code Species name group Site

EEAAAAAAAAAAAAAAAAAAAA 11111111112 1212345678901234567890 BORE_LUR Boreoheptagyia lurida (Garrett) G –––––––––––2––––1––––– MONO_1-P Monodiamesa sp. 1-P D ––––––11–––––1–––––––– EUKI_CLA Eukiefferiella claripennis (Lundbeck) G – – 1111223334332111111– STEN_2-P Stenochironomus sp. 2-P D –––––––1–––––––––––––1 PAGA_ORT Pagastia orthogonia Oliver D ––––––––––––11–––––––– BRIL_FLA Brillia flavifrons Johannsen G ––––––––––––1–1––––––– CRIC_BIC Cricotopus bicinctus (Meigen) G – – 1 – – – 1 – 1 –––––––––1111 CRIC_GLO Cricotopus globistylus Roback G ––––––––––––11–––––––– THIE_XEN Thienemanniella xena (Roback) G ––––––––––––1–1––––––– EUKI_1-P Eukiefferiella sp. 1-P G –––––––11–––1–11–11––– ORTH_RUB Orthocladius rubicundus (Meigen) G ––––1––1––1–311211–1–– ORTH_8-P Orthocladius sp. 8-P G ––––––––––––11–1–––––– DEMI_n1 Demicryptochironomus (irmaki) n. sp. 1 P ––––––––––––11–1–––––– ODON_FER Odontomesa ferringtoni Sæther D 1 ––––––1––––11111––1–1 CARD_PLA Cardiocladius platypus (Coquillett) P – – 1 1 – 11111121244443311 CRIC_HER Cricotopus herrmanni Sublette G – – – 1 – 1 – 1 1 – – – 1 2 1 – 1 1 1141 CRIC_INF Cricotopus infuscatus (Malloch) G –––––––––11––––––11111 EUKI_5-P Eukiefferiella sp. 5-P G – – – 1 –––––––––––11––1–1 NANO_SPI Nanocladius spiniplenus Sæther G – – 1 – – 1 1 –––––––––111––1 PARA_LUN Parametriocnemus lundbeckii (Johannsen) G ––––––11––1144123311–1 PHAE_PRO Phaenopsectra profusa (Townes) D 1 –––––––––––11–1––1111 POLY_LAE Polypedilum laetum (Meigen) D –––––––11–1––1111111–1 PENT_INC Pentaneura inconspicua (Malloch) P ––––––––––––––––––1––1 CRIC_ANN Cricotopus annulator Goetghebuer G –––––––––11–1111323313 CRIC_TFA Cricotopus trifascia Edwards G –––––––––––––1––––1133 CRIC_BLI Cricotopus blinni Sublette G ––––––––––––––1–111154 EUKI_4-P Eukiefferiella sp. 4-P G ––––––––––––––––1–1––– EUKI_COE Eukiefferiella coerulescens (Kieffer) G – – – 1 – 1 –––––––121111111 RHEOCRn1 Rheocricotopus n. sp. 1 (nr. chalybeatus) G ––––––––––––––––––11–– TVET_VIT Tvetenia vitraces (Sæther) G ––––––––––1––1–11111–1 HELE_1-P Heleniella sp. 1-P G ––––––––––––––1––1–––– LOPE_HYP Lopescladius hyporheicus Coffman & Roback D ––––––––––––––––1311–1 THIE_3-P Thienemanniella sp. 3-P G –––––––––––––––––243–– CHIR_DEC Chironomus decorus Johannsen D –––––––1–––––––11–11–1 CYPH_GIB Cyphomella gibbera Sæther D –––––––––––––1–––––1–1 DICR_FUM Dicrotendipes fumidus (Johannsen) D –––––––––––––1––––––11 MICR_PES Microtendipes sp. D –––––––––––––––––––1–1 POLY_PAR Polypedilum parascalaenum Beck D ––––––––––––––––––11–1 SAET_n1 Saetheria n. sp. 1 D –––––––––––––––––––1–1 PSEU_PSE Pseudochironomus pseudoviridis (Malloch) D ––––––––––––––––––––11 CLAD_2-P Cladotanytarsus sp. 2-P D –––––––––––––––––––111 RHEO_n4 Rheotanytarsus n. sp. 4 F –––––––––––––––––112––

n. sp. 9 and Tanytarsus n. sp. 5. Toward the spring (Tokeshi 1995) but was collected in bottom left of Figure 4 are species found at August at AR2 and AR6. Orthocladius frigidus sites with highest potential Zn toxicity such as was found at all sites upstream of AR12 and Krenosmittia halvorseni, in contrast to its con- was most abundant in East Fork and from AR4 gener. Brundiniella eumorpha may have to AR9. Orthocladius mallochi, O. rivicola, occurred at the most Zn-toxic sites due to the Cricotopus slossonae, C. tremulus, and Eukief- presence of numerous small springs. Hydro- feriella claripennis were the most widespread baenus pilipes is known to emerge in early and evenly distributed species throughout the 42 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 2. Pupal subfamily species richness at each site. main river, apparently unaffected by high Zn Species toward the far right of Figure 4 were toxicity. In the bottom right quarter, Cardio- more abundant downstream of AR11. The cladius platypus was also present at most sites orthoclads Cricotopus trifascia, C. blinni, Lopes- but particularly abundant below AR12 until cladius hyporheicus, and Thienemanniella sp. Pueblo Reservoir. Some species found at down- 3-P and several Chironominae were restricted stream sites were also present upstream of to these downstream sites. Species located in AR5 and largely absent at the most toxic sites. the top right cluster were most associated with These included Eukiefferiella coerulescens, E. the 2 sites downstream of Pueblo Reservoir. sp. 5-P, Nanocladius spiniplenus, and Phaeno- Adults psectra profusa. In the lower half of Figure 4, the diamesine Pagastia orthogonia, the ortho- Seventeen surveys provided 3896 adult clads Brillia flavifrons, Cricotopus globistylus, Chironomidae comprising 198 species. In addi- Thienemanniella xena, and Orthocladius sp. 8- tion, adult Diamesa leona Roback and D. caena P, and the chironominine Demicryptochirono- Roback were collected nonrandomly from mus (irmaki) n. sp. 1 were restricted to 2 or 3 shelf ice and boulders during winter (Herr- sites at intermediate elevations from AR11 to mann et al. 1987) and excluded from this AR13. These sites, in the driest part of the analysis. Species abundances are presented in catchment, receive high inputs of dissolved Table 3, with naming authors, for those species major ions from soft sedimentary and carbon- found at 2 or more sites, and rearranged by ate rocks. Parametriocnemus lundbeckii was correspondence analysis. There was no obvi- more widely distributed than these species ous downstream trend in species richness (Fig. but was most abundant at AR11 and AR12. 5). Fluctuations resembled those exhibited by 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 43

Fig. 3. Proportions of pupae classified by trophic group at each site.

pupal data except at sites AR5, AR7, and which was dominated by Chironominae, and AR20. Species richness fell downstream of at AR18 where they were the rarest trophic Iowa Gulch at AR5 and increased at the next 2 group. Grazers and detritivores were co-domi- sites. Both Leadville Drain and California nant at AR12. Filterers were an important Gulch preceded falls in species richness while component of the chironomid assemblage at the poorest site was AR10. Species richness AR18 but, as with pupal data, were absent declined after Pueblo Reservoir, contrasting below Pueblo Reservoir. the recovery exhibited by pupae from AR20. ORDINATION.—Latitude, Zn toxicity, and Adult data confirmed the dominance by Ortho- particle size were the only significant vari- cladiinae among pupal exuviae although ables selected, explaining 22.3% of biological species of Chironominae were relatively more variability. Total Fe was interchangeable with abundant. Adult Diamesinae were found at all Zn toxicity, but the latter was used to maintain sites except AR18 (if D. leona is included), comparability with pupal data. Only the 1st while Tanypodinae and Podonominae were CCA axis was significant (P = 0.01), explaining also more widely collected compared with 9.8% of all biological variation and 43.8% of pupal data. the species-environment relationship. Length- The relative abundance of Chironominae is wise variation, best explained by latitude, was reflected in the increased importance of detri- again the dominant influence along the pri- tivores in Figure 6 compared with pupal data. mary axis (t-value 19.2, correlation –0.94). Zn Grazers were dominant at all sites except AR5, toxicity (t-value 2.3, correlation –0.44) and 44 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 4. CCA ordination of pupal data. Arrows indicate importance and direction of maximum change in species composition among samples as the variable increases. Open circles used for sites, points for species. Species codes from Table 2. particle size (t-value 6.3, correlation 0.11) were tum particle sizes and site EF1 had the small- also significantly related to biological variation est. Site AR10 had the largest particle size, but along the first axis. its position reflects the greater importance of There was no arch effect in Figure 7 be- latitude and Zn toxicity. The association because the first 2 axes were of similar impor- tween Krenosmittia halvorseni and the most tance (4.41 and 3.56 s units). A north–to–south Zn-toxic sites revealed by pupal data was sup- distribution of sites occurred along the 1st ported by adult collections. Also in the top left axis, with lateral spreading of closely situated of Figure 7, two cold-water adapted species, upstream sites. Sites with the highest Zn toxi- Paracladius alpicola and Cladopelma viridula, city were positioned together in the top left of as well as Orthocladius subletti and Polypedi- Figure 7, while the least toxic sites were lum trigonus were all present at AR7 (high Zn placed diagonally opposite. Sites AR12–AR16 toxicity) and AR11. Adult Micropsectra nigrip- and AR19 had relatively large mean substra- ila were collected from East Fork downstream 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 45

Fig. 5. Adult subfamily species richness at each site. to AR16, dominating collections from AR5, bicinctus and Parametriocnemus lundbeckii whereas pupal exuviae were found only at were both widely distributed except at Zn- AR11. Gymnometriocnemus brumalis is proba- toxic sites; however, their pupal exuviae were bly terrestrial; it was absent from pupal collec- found at toxic sites. Adult and pupal C. infus- tions but adults were collected from AR4, catus had a downstream distribution but toler- AR5, and AR12, between 2000 and 3000 m. ated metals at AR8. Smittia n. sp. 3, Polypedilum Adults of Cricotopus coronatus were found at digitifer, and Micropsectra logani (pupae at sites with high Zn toxicity or at intermediate AR6) were collected from the first 4 sites altitude. Both adult and pupal collections of above California Gulch and then disappeared Orthocladius frigidus and O. nigritus indicated until AR17, or further downstream. that these were montane species tolerant of Independence of Zn concentrations downstream of California Sampling Method Gulch. Among downstream-distributed species In a test for association between pupal and located toward the lower right of Figure 7 adult data, χ2 = 5908.5, significantly (P < 0.001) χ2 were a few species that also occurred upstream exceeding the critical .05[65] of 106.0 for of AR4. Procladius subletti and Limnophyes n. associated data. Species most affected by the sp. 3 were collected at EF1 and AR2, respec- method of sampling were Micropsectra nigrip- tively, were absent at the most Zn-toxic sites, ila (pupae fewer than expected, adults greater), and were present in the vicinity of Pueblo Rheotanytarsus n. sp. 1 (pupae greater, adults Reservoir. Pupal exuviae of P. subletti, how- fewer), Orthocladius rivicola (adults fewer), O. ever, were collected at AR6. Adult Cricotopus obumbratus (adults greater), Diamesa heteropus 46 WESTERN NORTH AMERICAN NATURALIST [Volume 60

TABLE 3. Proportions of adult species collected at each site (see Table 2 for explanation). Trophic Code Species name group Site

AAAAAAAAAAAAAAAEEAAAAA 12111111 11 1 9078345656789121212340 LARS_PLA Larsia planensis (Johannsen) P ––––––––1–––––1––––––– PARO_KIE Parochlus kiefferi (Garrett) P –––––––––––––––11–1––– DIAM_DAV Diamesa davisi Edwards G –––––––––1––2–––––––34 DIAM_SPI Diamesa spinacies Sæther G ––––––––––––2––––––23– PAGA_ORT Pagastia orthogonia Oliver D ––––––––1–––––1––––––– PAGA_PAR Pagastia partica (Roback) D ––––––––––––111–––––1– ODON_FER Odontomesa ferringtoni Sæther D ––––––––––1–––1–––––1– HYDR_FUS Hydrobaenus fuscistylus (Goetghebuer) G –––––––––––––111––––1– ACRI_NIT Acricotopus nitidellus (Malloch) D –––––––––2––12–––––––– BRIL_FLA Brillia flavifrons Johannsen G –––––––––––––––2–31–1– CRIC_BIF Cricotopus bifurcatus Cranston & Oliv. G ––––––––11–––––––2–1–– CRIC_TIB Cricotopus tibialis (Meigen) G –––––––––––12––––––––– CRIC_GLO Cricotopus globistylus Roback G ––––––––––––1–1––––––– EUKI_n4 Eukiefferiella n. sp. 4 G –––––––––––––1–––1–––– ORTH_FRI Orthocladius frigidus (Zetterstedt) G ––––––1–121421–341––3– ORTH_SUB Orthocladius subletti Soponis G ––––––––––11–1–––––––– ORTH_WIE Orthocladius wiensi Sæther G ––––––––1–––––––––2––– PARA_ALP Paracladius alpicola (Zetterstedt) G ––––––––––1––1–––––––– PARA_n3 Paracladius n. sp. 3 G ––––––––––––––1––1–––– PSEC_SPI Psectrocladius spinifer (Johannsen) G ––––––––––1––––1––––1– RHEOCRn1 Rheocricotopus n. sp. 1 (nr. chalybeatus) G –––––––––1–111–1––1––– RHEO_EMI Rheocricotopus eminelobus Sæther G ––––––––1––––1–12111–– TOKU_ROW Tokunagaia rowensis (Sæther) D ––––––––––––––11–3–––– TVET_PAU Tvetenia paucunca (Sæther) G –––––––––––––––1211––– LIMN_ELT Limnophyes eltoni (Edwards) G –––––––––––––––12–2––– LIMN_NAT Limnophyes natalensis (Kieffer) G ––––––––––––––––––111– GYMN_BRU Gymnometriocnemus brumalis (Edwards) G ––––––––2–––––1–––––1– KREN_n1 Krenosmittia n. sp. 1 G ––––––––––––––––1––1–– KREN_HAL Krenosmittia halvorseni (Cranston & Oliver) G –––––––––111–––––––––– LIMN_n1 Limnophyes n. sp. 1 G –––––––––1––1–––4131–– LIMN_n2 Limnophyes n. sp. 2 G –––––––––––––––1––2–1– METR_BRU Metriocnemus brusti Sæther G –––––––––––1–––––1–1–– LIMN_n4 Limnophyes n. sp. 4 G ––––––––––––––––111––– PARAPSEU Paraphaenocladius pseudirritus nearticus Saether & Wang D –––––––––––1––––––13–– PARAPNAS Paraphaenocladius nasthecus Sæther D ––––––––––1––––––––11– SMIT_ATE Smittia aterrima (Meigen) G ––––––––––––1–1––––––– SMIT_n1 Smittia n. sp. 1 G –––––––––––––1–––––––2 THIE_ELA Thienemaniella spp. G ––––––––––––––1––11––– CHIR_RIP Chironomus riparius Meigen D –––––––––––11––––––12– CLAD_VIA Cladopelma viridula (Linnaeus) D ––––––––––1––1–––––––– DICR_NER Dicrotendipes nervosus (Staeger) D ––––––––––1–––––––––1– PARA_NIX Paracladopelma nixe (Townes) P ––––––––––––11–––––––– POLY_ALB Polypedilum albicorne (Meigen) D ––––––––1–11–––2111––– POLY_TRI Polypedilum trigonus Townes D ––––––––––1––1–––––––– TANY Tn2 Tanytarsus n. sp. 2 D ––––––––––1––––2––1––– CRIC_COR Cricotopus coronatus Hirvenoja G – – 1 – 1 – – – 1333221––––––– CRIC_SLO Cricotopus slossonae Malloch G – – 1 – – 1 – – 1 – – 1111–111–1– CRIC_SYL Cricotopus sylvestris (Fabricius) G ––––1–––––1–111––––––– EUKI_n9 Eukiefferiella n. sp. 9 G 1 ––––––––––111–––11––– ORTH_NIG Orthocladius nigritus Malloch G –––––1––1––1––––––––2– LIMN_ASQ Limnophyes asquamatus Andersen G –––––1–––––11––1––1–1– PSEU_FOR Pseudosmittia forcipata (Goetghebuer) G –––––1–––––1–2–––––11– 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 47

TABLE 3. Continued. Trophic Code Species name group Site

AAAAAAAAAAAAAAAEEAAAAA 12111111 11 1 9078345656789121212340 SERG_ALB Sergentia albescens (Townes) P –––––1––111–––1–––1––– MICR_POL Micropsectra polita (Malloch) D –––––––2––41––2––––––– PARA_SMI Paramerina smithae (Sublette) P – – – 1 –––––1––––––––1––– DIAM_HET Diamesa heteropus (Coquillet) G 4 1 – – 1 – – – 2 4 – – 2 –––––1–1– PSEU_PER Pseudodiamesa pertinax (Garrett) D ––––1––––––––11––––––– EUKI_CLA Eukiefferiella claripennis (Lundbeck) G 1 1 1 – 1 1 – 11112212–221–12 ORTH_MAL Orthocladius mallochi Kieffer G 4 1 – – 4 2 – – 12313111–21–1– CHAE_n1 Chaetocladius n. sp. 1 G ––––1–––1–––––––––––1– SMIT_n3 Smittia n. sp. 3 G – – 1 ––––––––––––11––––– MICR_NIG Micropsectra nigripila (Johannsen) D 1 – – – 1 – 1342–––2–2––111– MICR_LOG Micropsectra logani (Johannsen) D – 1 –––––––––––––1–1–––– CRIC_TRE Cricotopus tremulus (Linnaeus) G – – – 1 1 1 ––––––111–11–––2 CHIR_MAT Chironomus maturus Johannsen D – – – 1 1 ––––––––11––3–––– BORE_LUR Boreoheptygia lurida (Garrett) G ––––––14–––121–––11–14 POLY_n1 Polypedilum n. sp. 1 D – – 1 – 1 1 – 1 – – 1 1 – – – 1 – 1 1–1– ORTH_RVA Orthocladius rivicola Kieffer G 111131311111111111111– PSIL_n1 Psilometriocnemus n. sp. 1 G –––––1––––––––––––––1– PHAE_PRO Phaenopsectra profusa (Townes) D – 1 1 – – 1 – 1 – – 1 1 1 ––––1–––– PROC_CUL Procladius culiciformis (Linnaeus) P 1 – – 1 –––––––––1–––––––– PROC_FRE Procladius freemani Sublette P –––1–––––1–––––––––––– PROC_SUB Procladius subletti Roback P – – – 2 –––––––––1–1–––––– DIAM_ANC Diamesa ancysta (Roback) G ––––––41–111––––––1––– HYDR_PIL Hydrobaenus pilipes (Malloch) G 1 1 ––––––––2––––––––––– CARD_PLA Cardiocladius platypus (Coquillet) P – – 111311–2–1–1–1–––2–– CRIC_BIC Cricotopus bicinctus (Meigen) G 1 – 1 1 – – – 1 –––––1–11––––– CRIC_HER Cricotopus herrmanni Sublette G – – 413333–––1–221–––––– CRIC_INF Cricotopus infuscatus (Malloch) G 1131–––––––11––––––––– PARA_CNV Paracladius conversus (Walker) G 1 – 1121––––1––11––––––– PSEC_BMS Psectrocladius barbimanus (Edwards) D –––––1–––––––1–––––––– TVET_VIT Tvetenia vitraces (Sæther) G – – – 1 – 1 – 1 ––––1––––1–––– LIMN_n3 Limnophyes n. sp. 3 D – – 1 –––––––––––––––1––– PARA_LUN Parametriocnemus lundbeckii (Johannsen) G 1 – 1 1 – 1 1 –––––11–11––––– CHIR_DEC Chironomus decorus Johannsen D – – 1211–––11––111–––––– CHIR_ATR Chironomus atrella (Townes) D –––––1–––––––1–––––––– CYPH_COR Cyphomella cornea Sæther D – 1 – – 1 ––––––––1–––––––– DICR_FUM Dicrotendipes fumidus (Johannsen) D 1 2 – – 1 –––––––––4––––––– POLY_DIG Polypedilum digitifer Townes D 1 – – 1 –––––––––––1–––––– PSEU_RIC Pseudochironomus richardsoni (Malloch) D – – – 1 – – – 1 –––––1–––––––– PROC_BEL Procladius bellus (Loew) P 1 – – 1 – – – 1 –––––––––––––– ABLA_MAL Ablabesmyia mallochi (Walley) P 1 – – 1 –––––––––––––––––– CRIC_ANN Cricotopus annulator Goetghebuer G – – 323443––––11–––––––– CRIC_TFA Cricotopus trifascia Edwards G 2121–––––––––––––––––– CRIC_BLI Cricotopus blinni Sublette G 3431–––––1–––––2–––––– EUKI_COE Eukiefferiella coerulescens (Keiffer) G 1 2 –––––1–––––––––––––– ORTH_TRI Orthocladius trigonolabis Edwards G 1 1 1 – – – 1 1 ––––––––– –––– ORTH_OBU Orthocladius obumbratus Johannsen G 4 1 –––––1–––––––––––––– PARA.RUV Paratrichocladius rufiventris (Meigen) G ––––11–––––––––––––––– POLY_LAE Polypedilum laetum (Meigen) D – – 1111–1––––––1––––––– POLY_SUL Polypedilum sulaceps Townes D – – 1 1 1 ––––––1–––––––––– POLY_SCA Polypedilum scalaenum (Schrank) D – – 1311–1–––––––1––––1– STIC_MAR Stictochironomus marmoreus (Townes) D – – 1 1 –––––––––––––––––– CLAD_n1 Cladotanytarsus n. sp. 1 D – 1 – 1 –––––––––––––––––– RHEOTAn1 Rheotanytarsus n. sp. 1 F – – 1 4 – – – 2 ––––––––––––1– 48 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 6. Proportions of adults classified by trophic group at each site.

(adults greater), and Polypedilum scalaenum the 2 variables were independent (Pearson (adults greater). Species sampled equally well correlation –0.18, r.05[20] = 0.42) and all vari- as pupae and adults (combined χ2 < 1.6) were ance inflation factors were below 1.1. Sites Pagastia partica, Cricotopus herrmanni, Tvetenia were approximately ordered from warmest to vitraces, Cricotopus blinni, and Phaenopsectra coolest along the diagonal of the temperature profusa. vector in Figure 8. Almost at right angles was Effect of Classification Level a gradient of metal contamination; AR3 had almost twice the Cu concentration of the next Generic adult data were ordinated to inves- most contaminated samples from AR5 (Table tigate the influence of taxonomic level because 1). Except for AR3, sites were closer to the of the large number of species in this data set. origin of Figure 8 than they were in a species Stepwise regression selected maximum water temperature, total Cu, and mean particle size, CCA. No genera were solely associated with explaining 25.1% of generic adult chironomid AR3; the closest genera were Paraphaenocla- variability. The first 2 axes were significant dius (2 species used for adult CCA), Metrioc- (both P = 0.04), together explaining 18.3% of nemus (1 sp.), and Krenosmittia (2 sp.). These biological variation. The primary axis was sig- genera were found at several upstream sites nificantly explained by temperature (t-value but particularly the most metal-contaminated 6.93), while all 3 variables significantly ex- (AR3–AR8). In the lower half of Figure 8, plained the 2nd axis, particle size being the Parametriocnemus (1 sp.) exhibited metal intol- least important. Despite the overlap of tem- erance revealed by species CCA, as did Tvete- perature and particle size vectors in Figure 8, nia (2 sp.). Responses of other adult species, 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 49

Fig. 7. CCA ordination of specific adult data. Explanation as for Figure 4, species codes from Table 3.

previously highlighted as metal-intolerant, DISCUSSION have been lost among the conflicting trends of Comparisons of Pupal their congeners within species-rich genera and Adult Data such as Procladius (4 sp.), Cricotopus (13 sp.), and Polypedilum (7 sp.). Orthocladius (8 sp.), An unprecedented description of chirono- Chironomus (4 sp.), Eukiefferiella (4 sp.), and mid species distribution has been provided for Diamesa (4 sp.) were also central to the ordi- 259 km of a major U.S. river. Proportional nation because of counterbalancing species species abundances across the 22 Arkansas distributions. Limnophyes (7 sp.) was associated River sites were not equally represented by with low-temperature sites, as only 2 species samples of pupal exuviae and adults. Greater appeared downstream of AR9, and in small proportions of adult detritivores indicated that proportions. Micropsectra was associated with sources of associated larvae may have metal-impacted sites due to the distribution of included lentic, semi-terrestrial, and terres- M. nigripila and M. polita and despite occur- trial habitats beyond the Arkansas River. The rences of M. logani. absence of small-bodied Corynoneura and 50 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 8. CCA ordination of generic adult data. Explanation as for Figure 4.

Thienemanniella adults indicated that aerial Site AR18 was observed to have faster current nets were ineffective at catching these midges. than sites below the reservoir. Species sam- The large proportion of predators among pled equally well as adults and pupae may pupal data from sites AR13–AR18 was due to have had broad emergence patterns, being rheophilic Cardiocladius platypus, which may multivoltine or asynchronous. Cool-adapted have been underrepresented in adult collec- Diamesa heteropus, as well as Orthocladius tions. Assuming adult data included individu- obumbratus, were underrepresented as pupae als from external sources, this would explain because their main emergence period had why river-related environmental variables passed before pupal exuviae were collected. accounted for less biological variation than Adults of O. obumbratus were collected from that achieved with pupal data. Despite dis- AR16–AR20 while pupal exuviae were obtained crepancies in expected numbers of species, from cooler stations at AR2–AR7. Micropsec- there were similarities in species distribution tra nigripila, the most abundant adult species, between the 2 life stages. Examples cited were and Polypedilum scalaenum were also better Krenosmittia halvorseni, Orthocladius nigritus, represented in adult collections. Both species O. frigidus, and Cricotopus infuscatus. Both prefer lentic habitats and may have originated pupal and adult collections revealed the pres- from extraneous sources. Rheophilic Rheotany- ence of filterers upstream of Pueblo Reservoir tarsus n. sp. 1 and Orthocladius rivicola were and their absence downstream. Herrmann and the most abundant pupal species and were Mahan (1977) found that turbidity at the outlet underrepresented in adult collections, proba- was typically lower than in the reservoir, or at bly because they were “diluted” by species the inlet, during the first 2 yr of its existence. from other sources. 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 51

Species Richness sampled with 50-µm-mesh nets, has suggested Collections of pupal exuviae typically reveal that Chironomidae actively redistribute them- greater species richness than direct sampling selves and colonize preferred habitats through of stream habitats for larvae (Ferrington et al. drifting, particularly as 1st or 2nd instars. This 1991, Ruse 1995a). The present study obtained behavior would explain the contrast in species greater species richness from adult collections. richness between sites EF2 and AR1, AR3 and This could be explained partly by adults origi- AR4/6, and AR10 and AR11. nating from extrinsic habitats. Additionally, 17 Species Distribution and months of adult sampling would increase the the Effect of Metals number of species obtained compared with 3 months of pupal sampling. The pupal total of Environmental measurements most corre- 127 species compares favorably with species lated with a successive downstream turnover totals for other montane or subalpine streams in species composition (distance/altitude, lati- presented in a review by Lindegaard and tude, and temperature) were aligned with the Brodersen (1995), which gave an average mon- primary CCA axis of both data sets. Pupal data tane species total of 71 (range 26–144). The best reflected a smooth downstream gradient total of 200 adult species was not comparable in species turnover. In a neighboring river, with surveys of larvae or pupal exuviae because Ward (1986) classified 4 zones of species assem- of their uncertain origin. Both pupal and adult blage related to altitudes between 3414 m and data exhibited a decline in species richness at 1544 m, although chironomid taxa showed the 1st site below Leadville Drain and again much greater overlap than did Plecoptera and below California Gulch, the major sources of Trichoptera. A longitudinal zonation among metal pollution. Sites with the highest sedi- Chironomidae was suggested by Ward and mentary concentrations of Zn, Pb, Mn, and Cd Williams (1986) when Chironomini replaced (AR5, AR7, AR8) had about average species Orthocladiinae in a 36-km-long Canadian river. richness. Other research on the effects of In the Arkansas River pupal Chironominae in- metal-polluted mine drainage on chironomids creased from AR17 downstream, except below has demonstrated a reduction in species rich- the reservoir outlet, but there was no evidence ness (Winner et al. 1980, Armitage and Black- for altitudinal zonation rather than succession. burn 1985, Yasuno et al. 1985, Wilson 1988). The most abrupt changes were anthropogenic: Conversely, Cranston et al. (1997) demonstrated mining, regulation, and impoundment. In the an increase in chironomid species richness pupal CCA, localized effects of metal pollution below a mine adit, which they attributed to a within a 20-km reach were overwhelmed by greater pool of tolerant species in Australia effects of downstream succession along 259 compared with northern, temperate regions. km of the river. The importance of altitude Neither pupal nor adult data conformed to the and latitude to macroinvertebrate species downstream trend of increasing species rich- structure, mediated through their effect on ness found by Ward (1986) in a neighboring temperature, has been demonstrated locally catchment. Pupal and adult data sets revealed by Ward (1986) and globally by Jacobsen et al. a low number of species from site AR10, which (1997). Latitude was strongly related to dis- had the coarsest substratum and a strong cur- tance but, because it changed most between rent. Clements and Kiffney (1994) reported a sites EF1 and AR12, it also had a correlation reduced macroinvertebrate species richness at with chironomid species variability among a site approximately 10 km downstream of our metal-polluted sites. Longitude varied most site AR10. The next site downstream, AR11, between sites AR13 and AR20, where there had the highest number of adult species and was relatively less species variability; conse- the 3rd highest number of pupal species. Lar- quently, it was never selected by forward vae of species avoiding sites with metal inputs regression after latitude had been chosen. In a (EF2, AR3) or with high physical stress (AR10) study of 6 Colorado streams, including the may have drifted through to the next site, Arkansas River, Clements and Kiffney (1995) increasing its species richness. The effect is found that altitudinal variation confounded less dramatic below California Gulch because the effects of metal on benthic macroinverte- of high sedimentary metal concentrations fur- brates. Using CCA, we noted that metal pollu- ther downstream. Williams (1989), who pump- tion still had a significant explanatory value in 52 WESTERN NORTH AMERICAN NATURALIST [Volume 60 our study, even when generic-level adult data was a minor component of the Arkansas River were considered. Herrmann and Mahan (1977) chironomid assemblage, even at the most metal- found that metal-enriched water was reaching polluted sites. C. bicinctus did appear below Pueblo Reservoir, and subsequent research by Leadville Drain at EF2 (adults) and below Kimball et al. (1995) confirmed that metal California Gulch at AR5 and AR7 (pupae), inputs, and their transportation, extend through- while C. infuscatus did not appear until AR8 out 250 km of river. Sites AR3 and AR5–AR8 with a predominantly downstream distribution were extreme examples of metal pollution, (pupae and adults). C. slossonae was absent whereas concentrations of sedimentary Zn at from the 2 most metal-polluted sites on Elam’s remaining sites were still high downstream to run, but was present at all the most polluted Pueblo Reservoir. The work of Kiffney and Arkansas River sites. Eukiefferiella claripennis Clements (1993) revealed that macroinverte- was not found in Elam’s Run, but its presence brates bioaccumulated more Zn and Cd at site at Zn-polluted sites was recorded by the 2 AR5 than at AR3 while the reverse was usually English studies mentioned (Armitage and true for Cu. These results are in accord with Blackburn 1985, Wilson 1988) and was tolerant distributions of chironomid species reported of severely Cu-contaminated (>50 µg L–1) here. streams in southwest England (Gower et al. Metal-tolerant assemblages of chironomid 1994). E. claripennis, distributed extensively species below California Gulch are evident along the Arkansas River, was subdominant to from Tables 2 and 3. Individual species were Orthocladius species within pupal collections highlighted for their tolerance or intolerance, at the most metal-polluted sites. some of which have been connected previ- Species indicated as intolerant of severe ously with metal impacts by other researchers. heavy-metal pollution included some new In the English Pennines, Wilson (1988) found species: Eukiefferiella n. sp. 9, E. sp. 5-P, Limno- a high proportion of Krenosmittia camptopleps phyes n. sp. 3, and Tanytarsus n. sp. 5. E. co- below a Zn-polluted mine adit although the erulescens avoided the most toxic sites and was species was absent from a neighboring river of also reported by Wilson (1988) to be absent at the same catchment which was also Zn pol- Zn-polluted sites. Specific comparison of metal luted. Wilson suspected that metal pollution tolerance, especially across widely separated alone was not determining species distribution. In the Arkansas River this species was river systems, has its limitations. Postma et al. replaced by its congener K. halvorseni at sites (1995) have demonstrated that chironomid pop- with the highest sedimentary Zn-loadings. In ulations from metal-polluted rivers can exhibit the same catchment studied by Wilson, Ortho- less sensitivity to some metals compared with cladius frigidus was found by Armitage and conspecifics derived from unpolluted sites. Blackburn (1985) in moderately Zn-polluted They suggest this has a genetic basis. sites (0.77–1.68 mg L–1) but was absent at Future Study higher concentrations (2.08–7.6 mg L–1). O. frigidus reached its highest proportions at This study of the Arkansas River during sites AR4 and AR8; these sites have recorded 1984–85 provides a reference for assessing suspended Zn concentrations within the mod- changes that have occurred since remediation erate range (Roline and Boehmke 1981, Kim- work began in 1991. Now that Leadville mines ball et al. 1995) but could be exposed to higher have ceased operating, subsequent monitoring concentrations in spring (Clements 1994). The of chironomid species distribution would record study of Elam’s Run in Ohio by Winner et al. how the Arkansas River responds. Biomonitor- (1980) provided evidence of metal tolerance for ing using generic-level data would save time, several Arkansas River species that inhabited provided there was no significant loss of infor- sites AR3–AR8: Orthocladius dubitatus, O. mation. Generic data reduced the amount of obumbratus, Cricotopus bicinctus, C. infuscatus, unexplained species variation that probably Diplocladius cultriger, and Larsia planensis arose from the uncertain origin of the rarer (adult). Waterhouse and Farrell (1985) drew adult species. There was more homogeneity of attention to C. bicinctus being succeeded by generic assemblages between sites, although C. infuscatus along a gradient of declining sensitivity to Cu pollution, or perhaps sus- metal pollution in Elam’s Run. C. bicinctus pended metals, was greater than with specific 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 53 data. Generic data revealed the same 2 major communities? Canadian Journal of Fisheries and gradients, of longitudinal variation and metal Aquatic Sciences 54:1802–1807. CARAVAJAL, G.S., K.I. MAHAN, D. GOFORTH, AND D.E. contamination, identified by specific adult and LEYDEN. 1983. Evaluation of methods based on acid pupal data. Multivariate analysis of 10 benthic extraction and atomic absorption spectrometry for macroinvertebrate data sets by Bowman and multi-element determinations in river sediments. Bailey (1997) led them to suggest that if trade- Analytica Chimica Acta 147:133–150. CLEMENTS, W.H. 1994. Benthic invertebrate community offs were necessary to investigate community responses to heavy metals in the Upper Arkansas variation, it would be better to sacrifice taxo- River Basin, Colorado. Journal of the North Ameri- nomic resolution than quantitative data. An can Benthological Society 13:30–44. analysis of specific- and generic-level chirono- CLEMENTS, W.H., AND P. M . K IFFNEY. 1994. Integrated mid data along a metal-pollution gradient by laboratory and field approach for assessing impacts of heavy metals at the Arkansas River, Colorado. Waterhouse and Farrell (1985) revealed good Environmental Toxicology and Chemistry 13:397–404. agreement when using nonspecific diversity ______. 1995. The influence of elevation on benthic com- indices, but important information was lost if munity responses to heavy metals in Rocky Mountain indicators within species-rich genera were streams. Canadian Journal of Fisheries and Aquatic Sciences 52:1966–1977. relied upon. The importance of specific identi- CRANSTON, P. S . , P. D . C OOPER, R.A. HARDWICK, C.L. fication of chironomid indicators of metal pol- HUMPHREY, AND P.L. DOSTINE. 1997. Tropical acid lution was stressed by Gower et al. (1994) streams—the chironomid (Diptera) response in using CCA, although this was addressed to northern Australia. Freshwater Biology 37:473–483. researchers relying on subfamily chironomid FERRINGTON, L.C., M.A. BLACKWOOD, C.A. WRIGHT, N.H. CRISP, J.L. KAVANAUGH, AND F. T. S CHMIDT. 1991. A data. The metal-related distribution of several protocol for using surface-floating pupal exuviae of species belonging to the genera Cricotopus, Chironomidae for rapid bioassessment of changing Orthocladius, and Eukiefferiella would have water quality. Pages 181–190 in Sediment and stream been lost if identification of Arkansas River water quality in a changing environment: trends and explanation. IAHS Publication 203. pupae and adults had been generic only. Even GOWER, A.M., G. MYERS, M. KENT, AND M.E. FOULKES. among 2 species of Krenosmittia, pupal data 1994. Relationships between macroinvertebrate revealed a distinct difference in metal-related communities and environmental variables in metal- distribution. Generic data would be adequate contaminated streams in south-west England. Fresh- for a large-scale description of environmental water Biology 32:199–221. HERRMANN, S.J., AND K.I. MAHAN. 1977. Effects of im- influences but would have diminished value poundment on water and sediment in the Arkansas when monitoring recovery of individual sites. River at Pueblo Reservoir. Bureau of Reclamation Report REC-ERC-76-19. HERRMANN, S.J., J.E. SUBLETTE, AND M. SUBLETTE. 1987. CKNOWLEDGMENTS A Midwinter emergence of Diamesa leona Roback in the Upper Arkansas River, Colorado, with notes on LPR was in receipt of a Winston Churchill other diamesines (Diptera: Chironomidae). Entomo- Travelling Fellowship in 1985, and his subse- logica Scandinavica Supplement 29:309–322. quent work was supported by the U.K. Envi- JACOBSEN, D., R. SCHULTZ, AND A. ENCALADA. 1997. Struc- ture and diversity of stream invertebrate assem- ronment Agency. SJH and JES received fund- blages: the influence of temperature with altitude ing from the U.S. Environmental Protection and latitude. Freshwater Biology 38:247–261. Agency through the Colorado Department of KIFFNEY, P.M., AND W.H. CLEMENTS. 1993. Bioaccumula- Health (Contract C379551). We are indebted tion of heavy metals by benthic invertebrates at the to Mary Sublette for management of type spec- Arkansas River, Colorado. Environmental Toxicology and Chemistry 12:1507–1517. imens and data tabulation, and to Kent Mahan KIMBALL, B.A., E. CALLENDER, AND E.V. AXTMANN. 1995. for sediment chemistries. The views expressed Effects of colloids on metal transport in a river are the authors’ and do not necessarily repre- receiving acid mine drainage, Upper Arkansas River, sent those of their respective agencies. Colorado, USA. Applied Geochemistry 10:285–306. LINDEGAARD, C., AND K.P. BRODERSEN. 1995. Distribution of Chironomidae (Diptera) in the river continuum. LITERATURE CITED Pages 257–271 in P. Cranston, editor, Chironomids: from genes to ecosystems. CSIRO, Melbourne, Aus- ARMITAGE, P.D., AND J.H. BLACKBURN. 1985. Chironomi- tralia. dae in a Pennine stream system receiving mine MAHAN, K.I., T.A. FODERARO, T.L. GARZA, R.M. MARTINEZ, drainage and organic enrichment. Hydrobiologia G.A. MARONEY, M.R. TRIVISONNO, AND E.M. WILL- 121:165–172. GING. 1987. Microwave digestion techniques in the BOWMAN, M.F., AND R.C. BAILEY. 1997. Does taxonomic sequential extraction of calcium, iron, chromium, resolution affect the multivariate description of the maganese, lead and zinc in sediments. Analytical structure of freshwater benthic macroinvertebrate Chemistry 59:938–945. 54 WESTERN NORTH AMERICAN NATURALIST [Volume 60

MCGILL, J.D. 1980. The distribution of Chironomidae TER BRAAK, C.J.F. 1990. Update notes: CANOCO version throughout the River Chew drainage system, Avon, 3.1. Agricultural Mathematics Group, Wageningen, England. Doctoral thesis, University of Bristol, Eng- The Netherlands. land. TER BRAAK, C.J.F., AND I.C. PRENTICE. 1988. A theory of POSTMA, J.F., M. KYED, AND W. A DMIRAAL. 1995. Site spe- gradient analysis. Advances in Ecological Research cific differentiation in metal tolerance in the midge 18:271–317. Chironomus riparius (Diptera, Chironomidae). Hydro- TOKESHI, M. 1995. Life cycles and population dynamics. biologia 315:159–165. Pages 225–268 in P. Armitage, P.S. Cranston, and ROLINE, R.A. 1988. The effects of heavy metals pollution L.C.V. Pinder, editors, The Chironomidae: biology of the Upper Arkansas River on the distribution of and ecology of non-biting midges. Chapman and Hall, aquatic macroinvertebrates. Hydrobiologia 160:3–8. London. ROLINE, R.A., AND J.R. BOEHMKE. 1981. Heavy metals WARD, A.F., AND D.D. WILLIAMS. 1986. Longitudinal zona- pollution of the Upper Arkansas River, Colorado, tion and food of larval chironomids (Insecta: Diptera) and its effects on the distribution of the aquatic along the course of a river in temperate Canada. macrofauna. Bureau of Reclamation Report REC- Holarctic Ecology 9:48–57. ERC-81-15. WARD, J.V. 1986. Altitudinal zonation in a Rocky Mountain RUSE, L.P. 1995a. Chironomid community structure stream. Archiv für Hydrobiologie Supplement 74: deduced from larvae and pupal exuviae of a chalk 133–199. stream. Hydrobiologia 315:135–142. WATERHOUSE, J.C., AND M.P. FARRELL. 1985. Identifying ______. 1995b. Chironomid emergence from an English pollution related changes in chironomid communi- chalk stream during a three year study. Archiv für ties as a function of taxonomic rank. Canadian Jour- Hydrobiologie 133:223–244. nal of Fisheries and Aquatic Sciences 42:406–413. RUSE, L.P., AND S.J. HERRMANN. 2000. Plecoptera and Tri- WILLIAMS, C.J. 1989. Downstream drift of the larvae of choptera species distribution related to environmen- Chironomidae (Diptera) in the River Chew, S.W. tal characteristics of the metal-polluted Arkansas England. Hydrobiologia 183:59–72. River, Colorado. Western North American Naturalist WILSON, R.S. 1988. A survey of the zinc-polluted River 60:57–65. Nent (Cumbria) and the East and West Allen (North- RUSE, L.P., AND R.S. WILSON. 1984. The monitoring of umberland), England, using chironomid pupal exu- river water quality within the Great Ouse basin using viae. Spixiana Supplement 14:167–174. the chironomid exuvial analysis technique. Water WINNER, R.W., M.W. BOESEL, AND M.P. FARRELL. 1980. Pollution Control 83:116–135. Insect community structure as an index of heavy- SANDOVAL, L., J.C. HERRAEZ, G. STEADMAN, AND K.I. metal pollution in lotic ecosystems. Canadian Jour- MAHAN. 1992. Determination of lead and cadmium nal of Fisheries and Aquatic Sciences 37:647–655. in sediment slurries by ETA-AAS: a comparison of YASUNO, M., S. HATAKEYAMA, AND Y. S UGAYA. 1985. Char- methods for the preparation and analysis of sedi- acteristic distribution of chironomids in the rivers ment slurries. Mikrochimica Acta 108:19–27. polluted with heavy metals. Verhandlung der Inter- SOKAL, R.R., AND F. J . R OHLF. 1981. Biometry. Freeman, nationalen Vereinigung für Limnologie 22:2371–2377. New York. SUBLETTE, J.E., L.E. STEVENS, AND J.P. SHANNON. 1998. Received 28 September 1998 Chironomidae (Diptera) of the Colorado River, Grand Accepted 8 February 1999 Canyon, Arizona, USA, Ι: systematics and ecology. Great Basin Naturalist 58:97–146. THIENEMANN, A. 1910. Das Sammeln von Puppenhäuten der Chironomiden. Archiv für Hydrobiolgie 6: 213–214. 2000] CHIRONOMID DISTRIBUTION IN THE ARKANSAS RIVER 55

APPENDIX. Species found at only 1 site, either as pupal exuviae or adults. Listed in alphabetical order within tribes. Species name Pupa/Adult Site Derotanypus alaskensis (Malloch) A AR3 Psectrotanypus dyari (Coquillet) A AR7 Radotanypus submarginella (Sublette) A AR11 Ablabesmyia basalis (Walley) A AR7 Ablabesmyia monilis (Linneaus) A AR11 Ablabesmyia sp. A AR2 Conchapelopia pallens (Coquillet) P AR18 Pentaneura inconspicua (Malloch) A AR18 Telopelopia okoboji (Walley) A AR18 Thienemannimyia barberi (Coquillet) A AR18 Thienemannimyia senata (Walley) A AR18 Zavrelimyia sp. 1-P P AR4 Procladius prolongatus Roback A AR11 Procladius ruris Roback A AR7 Tanypus neopunctipennis Sublette A AR18 Tanypus nubifer Coquillet A AR18 Tanypus stellatus Coquillet A AR18 Diamesa garretti Sublette & Sublette A AR12 Prodiamesa olivacea (Meigen) A AR2 Cardiocladius n. sp. 2 A AR14 Cricotopus intersectus (Staeger) A AR19 Cricotopus lestralis (Edwards) A AR6 Cricotopus sylvestris (Fabricius) P AR12 Cricotopus tricinctus (Meigen) A AR5 Cricotopus trifasciatus (Panzer) A AR5 Cricotopus vierriensis Goetghebuer P AR12 Cricotopus n. sp. 18 A AR8 Cricotopus sp. 14-P P AR4 Cricotopus sp. 15-P P AR2 Cricotopus sp. 18-P P AR12 Cricotopus sp. 20-P P AR11 Cricotopus sp. 21-P P AR20 Eukiefferiella brevineris (Malloch) A AR4 Eukiefferiella n. sp. 4 P AR11 Eukiefferiella n. sp. 8 A AR9 Eukiefferiella sp. 10-P P AR17 Heterotrissocladius sp. A AR7 Nanocladius anderseni Saether A AR17 Nanocladius distinctus (Malloch) A AR17 Nanocladius rectinervis (Kieffer) A AR15 Orthocladius anteilis (Roback) A AR15 Orthocladius appersoni Soponis A AR15 Orthocladius carlatus (Roback) A AR11 Orthocladius dorenus (Roback) A AR1 Orthocladius holsatus Goet A AR2 Orthocladius nanseni Kieffer P AR11 Orthocladius trigonolabis Edwards P AR5 Orthocladius sp. 13-P P AR19 Paracladius conversus (Walker) P EF1 Paratrichocladius skirwithensis (Edwards) A EF1 Psectrocladius vernalis (Malloch) A AR16 Rheocricotopus chapmani (Edwards) A AR11 Metriocnemus n. sp. 2 A AR6 Metriocnemus n. sp. 5 A AR11 Limnophyes hastulatus Saether A AR2 Corynoneura sp. 2-P P AR1 Lopescladius hyporheicus Coffman & Roback A AR16 Parakiefferiella subaterrima (Malloch) P/A EF1/AR20 Paraphaenocladius exagitans (Johannsen) A AR11 Paraphaenocladius tonsuratus Saether & Wang A AR5 Smittia polaris (Kieffer) A AR8 Smittia n. sp. 2 A EF1 Rheosmittia sp. 1-P P AR1 56 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Thienemanniella similis (Malloch) P AR1 Thienemanniella xena (Roback) A AR18 Thienemanniella n. sp. 2 P/A AR16/AR17 Thienemanniella sp. 6-P P AR11 Chironomus stigmaterus Say A AR20 Chironomus n. sp. 5 A AR20 Chironomus n. sp. 8 A AR12 Cladopelma sp. 4-P P AR6 Cryptochironomus fulvus (Johannsen) A AR18 Cryptochironomus sp. P AR17 Cryptotendipes casuaria (Townes) A AR11 Cryptotendipes sp. 2-P P EF1 Cyphomella gibbera Saether A AR18 Demicryptochironomus (irmaki) n. sp. 1 A AR18 Dicrotendipes crypticus Epler A AR18 Dicrotendipes lobiger (Kieffer) A AR2 Dicrotendipes modestus (Say) A AR18 Glyptotendipes sp. A AR19 Microtendipes caelum Townes A AR11 Nilothauma babiyi (Rempel) A AR14 Parachironomus abortivus (Malloch) A AR18 Parachironomus arcuatus (Goetghebuer) A AR18 Parachironomus directus (Dendy & Sublette) A AR19 Parachironomus tenuicaudatus (Malloch) A AR19 Paracladopelma undine (Townes) A AR11 Paracladopelma n. sp. 2 P AR17 Paracladopelma sp. 4-P P AR6 Paratendipes fuscitibia Sublette A AR7 Paratendipes subequalis (Malloch) A AR6 Paratendipes thermophilus Townes P AR17 Polypedilum artifer (Curran) A EF1 Polypedilum fuscipenne (Meigen) A AR12 Polypedilum illinoense (Malloch) P/A AR18/AR18 Polypedilum pedatum Townes A AR12 Polypedilum scalaenum (Schrank) P AR16 Polypedilum sp. 2-P P AR18 Polypedilum sp. 8-P P AR18 Polypedilum sp. 9-P P AR17 Stictochironomus varius (Townes) A AR19 Pseudochironomus rex Hauber A AR12 Robackia claviger (Townes) P/A AR17/AR18 Stictochironomus annulicrus (Townes) A AR2 Stictochironomus n. sp. 1 P/A AR18/AR18 Pseudochironomus pseudoviridis (Malloch) A AR18 Cladotanytarsus n. sp. 2 A AR6 Cladotanytarsus n. sp. 3 A AR2 Cladotanytarsus sp. 3-P P AR2 Micropsectra logani (Johannsen) P AR6 Micropsectra nigripila (Johannsen) P AR11 Micropsectra n. sp. 3 A AR4 Micropsectra n. sp. 5 A AR2 Micropsectra n. sp. 6 A EF1 Paratanytarsus dubius (Malloch) A AR12 Paratanytarsus similatus (Malloch) A AR11 Paratanytarsus tenuis (Meigen) A AR11 Paratanytarsus n. sp. 1 A AR7 Stempellinella sp. 1-P P AR12 Sublettea coffmani (Roback) A AR1 Tanytarsus bathophilus Kieffer A AR11 Tanytarsus fimbriatus Reiss & Fittkau A AR11 Tanytarsus pallidicornis (Walker) A AR12 Tanytarsus n. sp. 1 A AR20 Tanytarsus n. sp. 6 P AR12 Tanytarsus n. sp. 13 A AR7 Tanytarsus sp. 2-P P AR6 Western North American Naturalist 60(1), © 2000, pp. 57–65

PLECOPTERA AND TRICHOPTERA SPECIES DISTRIBUTION RELATED TO ENVIRONMENTAL CHARACTERISTICS OF THE METAL-POLLUTED ARKANSAS RIVER, COLORADO

L.P. Ruse1 and S.J. Herrmann2

ABSTRACT.—The Upper Arkansas catchment has been polluted with heavy metals from mining for almost 140 yr. Adult Plecoptera and Trichoptera species distributions were recorded from 22 stations along 259 km of main river during 1984–85 so that these could be related to metal deposition and other environmental characteristics. Chemically or physically perturbed sites had poor species richness compared with adjacent sites. There was no sequential downstream increase in species numbers. Filter-feeders proportionally increased downstream as predators declined; these proportions were reset at a high-energy site before the trend resumed. Using canonical correspondence analysis, we found that species composition was most strongly related to changes in distance/altitude and to temperature, particularly after regulatory flows entered the river. The proportion of biological variation explained by river measurements indicated that collected adults were largely derived from the main Arkansas River. Species tolerant of high sedimentary metal concentrations were identified while some other species appeared to be sensitive. The study provides a disturbed-state reference for monitoring effects of remedial actions begun in 1991, and for comparisons with other Colorado rivers.

Key words: Plecoptera, Trichoptera, multivariate analysis, adults, spatial distribution, sediments, species richness, heavy metals.

The Arkansas River in Colorado has been METHODS polluted by heavy metals since mining began Study sites in 1859. In 1983 serious metal pollution in the Upper Arkansas River affected sites up to 220 Twenty-two sites were chosen along 259 km km downstream (Kimball et al. 1995). Emerg- of the East Fork (sites EF1 and EF2) and ing adult Plecoptera and Trichoptera were col- Arkansas River (sites AR1–AR20) between Cli- lected along this length of the Arkansas River max and Pueblo, east of the Continental during 1984–85 so that species distribution Divide in central Colorado. A diagram and could be related to physical and chemical char- more complete description of sites can be found acteristics of the sampling sites. This study in the preceding paper (Ruse et al. 2000). The differed from other research on the Arkansas greatest source of metals to the catchment comes from Leadville Drain and California River by relating invertebrate distribution to Gulch. This survey occurred between 2 major sedimentary concentrations of heavy metals surges of metal sludge into California Gulch on rather than water measurements. Kiffney and 23 February 1983 and 22 October 1985. Water Clements (1993) found that metal concentra- from the western slopes of the Continental tions in the Arkansas River underestimated Divide is diverted to Turquoise Lake and Twin the availability of metals to benthic macro- Lakes, entering the Arkansas River above AR4 invertebrates. Bioaccumulated metal concen- and AR9, respectively. The Arkansas River was trations were better related to those measured impounded above AR19 by Pueblo Dam in in sedimentary minerals and periphyton. 1974. The U.S. Environmental Protection Remedial action on the worst affected sites Agency (EPA) declared the California Gulch began in 1991. Data provided here were col- catchment and the Arkansas River from above lected during one of the river’s most severe AR2 to below AR3 as a Superfund site in 1983. periods of metal pollution and could subse- New water treatment plants on Leadville quently serve as a baseline measure for the Drain and California Gulch were both in oper- effects of remediation. ation by June 1992.

1Environment Agency (Thames Region), Fobney Mead, Rose Kiln Lane, Reading RG2 0SF, England. 2University of Southern Colorado, 2200 Bonforte Boulevard, Pueblo, CO 81001, USA.

57 58 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Sampling and Analysis values were decimalized, and only the maxi- From May 1984 until September 1985 we mum water temperature recorded at each site collected adult Plecoptera and Trichoptera was used. Environmental data were standard- monthly using sweep net, beating sheet, water- ized to have a mean of zero and unit variance skimming, hand-picking, and ultraviolet light to remove arbitrary variation in units of mea- traps. Adult Chironomidae were also collected surement. CCA species scores were weighted and these data have been reported, together mean sample scores (CANOCO version 3.1 with pupal data, by Ruse et al. (2000). Numbers scaling + 2). This analysis was sensitive to rel- of collected adult Ephemeroptera were too ative variation between sites, and it was not few to warrant analysis. necessary to have precise particle size or water We characterized sites using environmental hardness data to relate these characteristics to data recorded on a single occasion, except for spatial variation in species distribution. water temperature, which was recorded during each monthly visit to collect adult insects. RESULTS The 3 most abundant superficial substratum types, among 5 size classes, were assessed Sampling provided 1809 adult Plecoptera, visually and used to calculate mean particle comprising 25 species, and 10,669 adult Tri- size for each site (Ruse et al. 2000). Latitude, choptera among 48 species. Species present at longitude, altitude, slope, and distance down- 2 or more sites are presented with their stream from EF1 were obtained from maps. author’s name in Table 1. Species have been Copper, zinc, lead, manganese, iron, and cad- arranged according to the primary axis of a mium concentrations were determined from 6 correspondence analysis (Ter Braak and Pren- subsamples of submerged fine sand using a tice 1988) since this made the sequential down- 25-mm-diameter PVC pipe inserted to a depth stream turnover in species composition read- of 15 cm. We sampled each site during 18–19 ily apparent. Apart from the reversal of AR10 October 1986, following the 2nd metal sludge and AR11, there was a successive downstream surge into California Gulch. Metals were replacement of species. extracted using a sequence of hot digestions Stonefly species richness declined down- and evaporations (Ruse et al. 2000). An ordinal stream of metal inputs from Leadville Drain scale of zinc toxicity was calculated to account and California Gulch (Fig. 1) and at sites AR6, for the ameliorating effect of increased water AR10, and sites downstream of AR11 where hardness on metal toxicity to biota (Ruse et al. water temperatures were high (environmental 2000). data provided in Ruse et al. 2000). No individ- We found it necessary to combine each uals were collected below Pueblo Reservoir. species abundance for samples from the same Chloroperlidae had an upstream distribution site to relate their spatial variation to a site’s while Perlidae were collected from sites fur- environmental characteristics. Spatial variation in biological data was directly compared ther downstream. Caddisfly species numbers with environmental variation using canonical were maintained throughout the study area, correspondence analysis (CCA; Ter Braak and with slight reductions below the 2 major inputs Prentice 1988). The same procedures of for- of metal pollution (Fig. 2). Lowest species ward selection and significance testing used numbers occurred at AR10 and AR13. There by Ruse et al. (2000) were adopted here. Before was also a decline in species and family rich- analysis, species abundances were converted ness below Pueblo Reservoir compared with to percentages of total number of individuals neighboring sites upstream. Most caddisfly collected from a site. Species recorded at a families were well represented at all sites single site only were omitted from CCA to avoid above the reservoir. Hydroptilidae had higher spurious association with a coinciding extreme species richness at downstream sites, Psy- environmental measurement; their distribu- chomyiidae were present only downstream of tions are recorded in the Appendix. Environ- AR10, and Leptoceridae were found only mental data were not transformed for CCA; downstream of AR16. measurements of temperature, slope, zinc tox- Stonefly and caddisfly species were classi- icity, total manganese, and total iron were nor- fied according to presumed feeding modes of mally distributed. Latitude and longitude their associated larvae (Table 1) and the data 2000] STONE- AND CADDISFLY DISTRIBUTION IN ARKANSAS RIVER 59

TABLE 1. Proportions of species at each site: 1 = 0.1–4.9%, 2 = 5.0–9.9%, 3 = 10.0–19.9%, 4 = 20.0–39.9%, 5 = 40.0+%. G = Grazer, D = Detritivore, P = Predator, F = Filterer. Trophic Code Species name group Site EEAAAAAAAAAAAAAAAAAAAA 11111111112 1212345678910234567890 CACO Capnia confusa Claassen D 1 – – 1 – 1 –––––––––––––––– PAVE Paraleuctra vershina Gaufin & Ricker D 1 1 – – 1111–––1–––––––––– AMBA Amphinemura banksi Baumann & Gaufin D 1213111–11–11––––––––– PODE Podmosta delicatula (Claassen) D 1211–1–––––––––––––––– PRBE Prostoia besametsa (Ricker) D – – – 1311111–––––––––––– SUPA Suwallia pallidula (Banks) P 2413532433112––––––––– SWCO Sweltsa coloradensis (Banks) P 3 – 21111–1111–––––––––– TRPI Triznaka pintada (Ricker) P 1111123–1111–––––––––– SKPA Skwala parallela (Frison) P – – – 1 – – – 1 – 1 –––––––––––– KOMO Kogotus modestus (Banks) P 1 – 1 – 1 ––––––––––––––––– PTBA Pteronarcella badia (Hagen) D 1 ––––11––11––––––––––– GLVR Glossosoma verdona Ross G 1231–1211––––––––––––– ARGR Arctopsyche grandis (Banks) P 1111111111–––––––––––– AGSA Agraylea saltesea Ross G – – 1 – – 1 –––––––––––––––– AMCA Amphicosmoecus canax (Ross) D 121111111111–––––––––– LIAB Limnephilus abbreviatus Banks D ––––11–1111––––––––––– OLMI Oligophlebodes minutus (Banks) G 1114252211–––––––––––– PHQU Philarctus quaeris (Milne) D –––––1–1–––––––––––––– RHAN Rhyacophila angelita Banks P 334111111––––––––––––– RHBR Rhyacophila brunnea Banks P 3111––11–––––––––––––– RHPE Rhyacophila pellisa Ross P 3 1 –––––––––1–––––––––– ISFU Isoperla fulva Claassen P – – – 1 – 111112111–––––––– TRSI Triznaka signata (Banks) P ––––––––1113–1–––––––– BRAM Brachycentrus americanus (Banks) F – 1222122312121–11––––– MIBA Micrasema bactro Ross D – – 1 1 –––––––1–1–––––––– AGBO Agapetus boulderensis Milne G ––––––––1––1–––––––––– OCLO Ochrotrichia logana (Ross) D 1 ––––––11111–––1–––––– UTLO Utacapnia logana (Nebeker & Gaufin) D –––––1––––––––1––––––– LEPL Lepidostoma pluviale (Milne) D –––––––––––111–1–––––– ONUN Onocosmoecus unicolor (Banks) D – 1 –––––1–––––1–––––––– BROC Brachycentrus occidentalis Banks F – 1111123345241–1–12––– GLPA Glossosa parvulum Banks G –––––24341253431111––– RHCO Rhyacophila coloradensis Banks P 3342––1313115335431––– HYOS Hydropsyche oslari Banks F –––––––––1–111111––1–– PSFL Psychomyia flavida Hagen D –––––––––––1–453411–11 HEPA Hesperoperla pacifica (Banks) P –––––––––––111––111––– ISMO Isoperla mormona Banks P ––––––––––––––111111–– ISQU Isoperla quinquepunctata (Banks) P –––––1111111–111131––– ISEL Isogenoides elongatus (Hagen) P ––––––––––––1––––1–––– CUTH Culoptila thoracica (Ross) G –––––1––––––––112111–– GLVN Glossosoma ventrale Banks G –––––––––––––––1–1–––– HYCO Hydropsyche cockerelli Banks F – – – 11111244111334432–1 LEPI Leucotrichia pictipes (Banks) G –––––––––––––1–1311–1– CLSA Claassenia sabulosa (Banks) P –––––––––––––1–––––1–– AGMU Agraylea multipunctata Curtis G –––––11––––––1–––––1–– MEFR Mesocapnia frisoni (Baumann & Gaufin) D –––––1–––––––––––––1–– CHPE Cheumatopsyche pettiti (Banks) F –––––––––––––––––11223 HYOC Hydropsyche occidentalis Banks F ––––––––1––––––2135545 HYAJ Hydroptila ajax Ross G –––––––––––––––––––233 HYAR Hydroptila argosa Ross G ––––––––––––––––––––11 HYPE Hydroptila pecos Ross G ––––––––––––––––––11–1 MAAY Mayatrichia ayama Mosely G –––––––––––––––––1–11– OCST Ochrotrichia stylata (Ross) D –––––––––––––––––11142 NELA Nectopsyche lahontanensis Haddock D –––––––––––––––––––11– OEIN Oecetis inconspicua (Walker) P ––––––––––––––––––111– LIDI Limnephilus diversus (Banks) D ––––––––––––––––––11–1 LITA Limnephilus taloga Ross D –––––––––––––––––––1–1 60 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 1. Distribution of Plecoptera families.

combined with that of adult species of Chi- Ordination ronomidae collected with them (Ruse et al. Stepwise regression progressively selected 2000). This provided a better perspective of distance downstream, latitude, and maximum stream function since these were the 3 domi- temperature as significantly correlated with nant groups of emerging insects. Including variation in species composition among sites. midges in the analyses did not greatly alter Altitude was also significant but highly nega- relative composition of the 4 trophic classes. tively correlated with distance and was ex- Proportions of predators at the first 3 sites cluded to prevent multicollinearity (variation were reduced by including midges, proportions inflation factor = 189; Ter Braak 1990). Total of grazers were increased at all sites, detriti- copper concentration was the 4th most explan- vores remained about the same, and filterers atory variable but did not have a significant were reduced at the last 4 sites. For the 3 relationship with species data after the previ- insect groups combined, proportions of preda- ous variables had been selected (P = 0.09). tors were highest at EF1, AR3, and AR10 and The 3 selected variables explained 37.5% of almost absent below Pueblo Reservoir (Fig. 3). biological variation in CCA. The species-environment relationship was significantly differ- Grazer proportions were lowest below Califor- ent from random for the first 2 CCA axes (P = nia Gulch at AR3, and at AR8 and AR9, recov- 0.01), accounting for 32.9% of all biological ering downstream to peak at AR4 and AR11. variation and 87.7% of explained variation. Detritivores (shredders and collector-gather- Species turnover among samples was ers) declined downstream from EF1 to AR10, strongly related to change along the longitudi- recovered by AR13, and then declined again. nal axis of the river. Dominance of the 1st In contrast, proportions of filterers increased CCA axis compared with the 2nd resulted in below the outflows of regulatory lakes down- an archlike configuration of sites in Figure 4. stream to AR9, declined by AR12, and mostly Gradient lengths for the first 2 unconstrained increased downstream. axes (biological data alone) were 5.72 and 2.78 2000] STONE- AND CADDISFLY DISTRIBUTION IN ARKANSAS RIVER 61

Fig. 2. Distribution of Trichoptera families.

s units, respectively. Detrending or reduction the caddisfly Rhyacophila pellisa and the of environmental variables did not remove the stonefly Podmosta delicatula, were associated arching trend, and separation into 2 data sets with sites on the East Fork and the most up- was impractical for the small number of sam- stream Arkansas River sites. Rhyacophila pellisa ples. The 1st CCA axis was most significantly reappeared below the most metal-polluted related to downstream distance (canonical sites at AR11. The nemourid Prostoia besametsa coefficient t-value 6.26, interset correlation and the chloroperlid Suwallia pallidula had 0.97). The 2nd axis was principally related to their highest abundances at AR3, the 1st site variations in maximum temperature (t-value below California Gulch. Other species that 3.51, correlation 0.32), and latitude (t-value thrived at sites with high sedimentary levels of 7.8, correlation –0.28). The dominant relation- heavy metals, AR3–AR8, were the chloroper- ship between species distribution and distance lid Triznaka pintada, the limnephilid Oligo- resulted in proximity of sites upstream of phlebodes minutus, Brachycentrus americanus, AR11 and the 2 sites below Pueblo Reservoir B. occidentalis, Glossosoma parvulum, and along axis 1. The clusters of sites, AR4–AR5 Hydropsyche cockerelli. The last 4 species were and AR9–AR10, were the 1st and 2nd sites, widely found at sites down to Pueblo Reser- respectively, downstream of outflows from voir while the first 2 species had a more up- Turquoise Lake and Twin Lakes. Sites AR6, stream distribution. Rhyacophila coloradensis AR7, and AR8, together with AR5, had the also appeared to be tolerant of high sedimen- highest sedimentary levels of heavy metals, tary metal concentrations and to have a wide with the exception of copper at AR3 (Ruse et distribution above the impoundment; how- al. 2000). ever, it was absent at the first 2 sites below Species in Figure 4 are placed close to California Gulch. R. angelita was the only rhy- modes of their distribution among sites. Species acophilid present at sites AR3 and AR4, but its at the extreme bottom left of Figure 4, such as distribution was limited in range of altitude. 62 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 3. Distribution of trophic classes of adult Chironomidae, Plecoptera, and Trichoptera.

Middle-elevation sites, AR11–AR14, draining uals derived from habitats beyond the main soft sedimentary and carbonate rocks were Arkansas River. Part of the evidence for this particularly suitable to the caddisflies Lepidos- conclusion was the relatively low proportion toma pluviale and Psychomyia flavida, although of adult species variation explained by river- the latter species was also present downstream related environmental variables within a CCA, to AR20. Species associated with lower-gradi- 22.3% compared to 43.4% for pupal species ent downstream sites appear in the bottom data. With CCA, 37.5% of adult stonefly and right corner of Figure 4. Isoperla quinque- caddisfly species variation was explained by punctata and I. mormona were the stoneflies river-related variables, suggesting that they most successful at colonizing these sites while were more likely to have been derived from Mesocapnia frisoni (male) was found at AR18. the main river than were adult chironomids Although no stoneflies were collected down- collected in the same samples. In terms of sig- stream of Pueblo Reservoir, the hydropsychids nificant CCA axes, 32.9% of stonefly and cad- Cheumatopsyche pettiti and Hydropsyche occi- disfly species distribution was explained, pre- dentalis and the hydroptilids Hydroptila ajax cisely the same as for pupal chironomids col- and Ochrotrichia stylata were dominant at lected directly from the river. AR19 and AR20. Species Richness and Function

DISCUSSION Assuming these adults were representative of the main river, total stonefly and caddisfly Ruse et al. (2000) concluded that collec- species richness in the Colorado section of the tions of adult Chironomidae included individ- Arkansas River did not conform to a trend of 2000] STONE- AND CADDISFLY DISTRIBUTION IN ARKANSAS RIVER 63

Fig. 4. CCA ordination of Plecoptera () and Trichoptera () species. Arrows indicate importance and direction of maximum change in species composition among samples as the variable increases. Bold circles used for sites. Species codes from Table 1. downstream increase. Allan (1975) and Ward of site AR10 appeared to cause a decline in (1986) demonstrated progressively increasing species numbers, just as it did for Chironomi- numbers of species down smaller Rocky Moun- dae (Ruse et al. 2000). Downstream trends tain streams in Colorado. Adult Chironomidae became more apparent at the family or trophic from the Arkansas River have also failed to level. The inclusion of adult chironomids with reveal a sequential downstream trend in species stoneflies and caddisflies in the trophic classi- numbers (Ruse et al. 2000). Stonefly species fication accounted for nearly all adult insects numbers were lowest at sites with a maximum collected during the survey. This should have recorded temperature above 19°C, all down- accounted for a large part of the macrobenthic stream of AR12, and were absent below Pueblo community since Ward (1986) found that adult Dam. The negative effect of heavy metal inputs insects accounted for nearly all macroinverte- from Leadville Drain and California Gulch on brate abundance and biomass of a neighboring stonefly or caddisfly species richness was less Colorado stream. Proportions of predators and than that of Pueblo Reservoir. Physical stress detritivores declined from site EF1 to AR9 as 64 WESTERN NORTH AMERICAN NATURALIST [Volume 60 grazers and/or filterers increased. Trends in perlodid Isoperla quinquepunctata, recorded trophic groups appeared to be reset at site by Ward (1986) as a plains species (<1700 m), AR10, possibly due to its hydraulic stress or to was present at high-altitude sites on the the reduction in sedimentary concentrations Arkansas River (up to 2865 m) with high sedi- of heavy metals compared with sites upstream mentary metal concentrations. I. quinquepunc- (Ruse et al. 2000). Perturbations imposed by tata did have a more downstream distribution California Gulch also upset this trend, and than most other stoneflies collected. Clements regulatory outflows from the 2 lakes were con- (1994) suggested that Rhyacophila was tolerant sidered responsible for the dominance of fil- of metals in the Upper Arkansas River. We terers downstream. Following the resetting of found 4 species of Rhyacophila that appeared proportions of trophic classes that occurred at to differ in their tolerances to metals. Only R. sites AR10–AR12, a similar downstream reduc- angelita was found at the next 2 sites down- tion in predators and detritivores resumed as stream of California Gulch. All 4 species de- proportions of filterers or grazers increased. clined in relative abundance below this discharge, or below Leadville Drain in the case Species Compositional Change of R. pellisa. Rhyacophila species distribution Trends in species turnover were most cor- was also related to altitude. The altitude range related with the sequential downstream order of R. coloradensis in the Arkansas River was of sites. Altitude, highly negatively correlated wider than suggested for this species by Allan with distance downstream, was positively cor- (1975) for another Colorado river, based on its related with latitude. The ultimate cause of site-to-microhabitat niche breadths. Among correlation between species spatial distribution species found in abundance below Pueblo and distance downstream could be related to Reservoir, the hydropsychid Cheumatopsyche changes in hydraulic stress (Statzner and Higler pettiti was reported to be a plains (<1700 m) 1986). This has already been suggested, in the species by Ward (1986). These differences in previous paragraph, as the cause of changes in findings between studies of neighboring Col- functional groups around site AR10. Water orado streams could be due to variation in temperature was also revealed, by CCA, as river size and habitat characteristics of the being a distinct contributor to biological varia- sites and to improvements in taxonomic keys. tion. Sequential downstream change in water It is also possible that the presence of high temperature was believed to be a controlling concentrations of heavy metals in the Arkansas factor in hydropsychid caddisfly distribution River was responsible for such differences. in a study by Hildrew and Edington (1979). In Major mining operations in the Leadville contrast to adult and pupal chironomid data, area ceased in January 1999. Adult stoneflies sedimentary metals concentrations had no sig- and caddisflies, together with midge pupal nificant explanatory value to caddis- and stone- skins, are sensitive to immediate impacts of flies, although copper was significant at the the most polluted tributaries and their downstream deposits of metals. A repeat survey of 10% probability level. At high-altitude sites, these organisms would be an effective monitor however, there were species tolerant of ambi- of the changes in the macrobenthos of the ent concentrations of heavy metals while a few Arkansas River following clean-up operations species appeared to be metal sensitive. These and the cessation of mining. responses occurred immediately below Lead- ville Drain and California Gulch, in contrast to ACKNOWLEDGMENTS the Chironomidae which were most affected at sites of greatest metal deposition, AR5–AR8 LPR was in receipt of a Winston Churchill (Ruse et al. 2000). The metal-tolerant chloro- Travelling Fellowship in 1985, and subsequent perlid Suwallia pallidula was described as a work was supported by the U.K. Environment euryzonal mountain species by Ward (1986). It Agency. SJH received funding from the U.S. was found from 3042 m down to 2338 m in the Environmental Protection Agency through the Arkansas River. Another tolerant stonefly, the Colorado Department of Health (Contract nemourid Prostoia besmetsa, was classified as C379551). The views expressed are the authors’ a lower-montane/foothills species (below 2500 and do not necessarily represent those of their m) but was not found below 2748 m (AR8). The respective agencies. 2000] STONE- AND CADDISFLY DISTRIBUTION IN ARKANSAS RIVER 65

LITERATURE CITED RUSE, L.P., S.J. HERRMANN, AND J.E. SUBLETTE. 2000. Chironomidae (Diptera) species distribution related ALLAN, J.D. 1975. The distributional ecology and diversity to environmental characteristics of the metal-pol- of benthic insects in Cement Creek, Colorado. Ecol- luted Arkansas River, Colorado. Western North ogy 56:1040–1053. American Naturalist 60: 34–56. CLEMENTS, W.H. 1994. Benthic invertebrate community STATZNER, B., AND B. HIGLER. 1986. Stream hydraulics as responses to heavy metals in the Upper Arkansas a major determinant of benthic invertebrate zona- River Basin, Colorado. Journal of the North Ameri- tion patterns. Freshwater Biology 16:127–139. can Benthological Society 13:30–44. TER BRAAK, C.J.F. 1990. Update notes: CANOCO version HILDREW, A.G., AND M. EDINGTON. 1979. Factors facilitat- 3.1. Agricultural Mathematics Group, Wageningen, ing the coexistence of hydropsychid caddis larvae The Netherlands. (Trichoptera) in the same river system. Journal of TER BRAAK, C.J.F., AND I.C. PRENTICE. 1988. A theory of Animal Ecology 48:557–576. gradient analysis. Advances in Ecological Research KIFFNEY, P.M., AND W.H. CLEMENTS. 1993. Bioaccumula- 18:271–317. tion of heavy metals by benthic invertebrates at the WARD, J.V. 1986. Altitudinal zonation in a Rocky Mountain Arkansas River, Colorado. Environmental Toxicology stream. Archiv für Hydrobiologie Supplement and Chemistry 12:1507–1517. 74:133–199. KIMBALL, B.A., E. CALLENDER, AND E.V. AXTMANN. 1995. Effects of colloids on metal transport in a river Received 28 September 1998 receiving acid mine drainage, Upper Arkansas River, Accepted 26 March 1999 Colorado, USA. Applied Geochemistry 10:285–306.

APPENDIX. Species found at only 1 site. Species name Stonefly/Caddisfly Site Capnia gracilaria Claassen S AR18 Malenka coloradensis (Banks) S AR4 Sweltsa lamba (Needham & Claassen) S AR4 Isogenoides zionensis Hanson S AR10 (4 males) Helicopsyche borealis (Hagen) C AR18 Hydropsyche bronta Ross C AR20 Hydroptila waubesiana Ross C AR16 Neotrichia halia Denning C AR16 Stactobiella brustia (Ross) C EF1 Triaenodes tarda Milne C AR18 Asynarchus nigriculus (Banks) C AR1 Hesperophylax occidentalis (Banks) C AR6 Limnephilus externus (Hagen) C AR6 Psychoglypha subborealis (Banks) C EF1 Polycentropus halidus Milne C AR17 Western North American Naturalist 60(1), © 2000, pp. 66–76

WOODY RIPARIAN VEGETATION RESPONSE TO DIFFERENT ALLUVIAL WATER TABLE REGIMES

Patrick B. Shafroth1,2, Juliet C. Stromberg1, and Duncan T. Patten1

ABSTRACT.—Woody riparian vegetation in western North American riparian ecosystems is commonly dependent on alluvial groundwater. Various natural and anthropogenic mechanisms can cause groundwater declines that stress riparian vegetation, but little quantitative information exists on the nature of plant response to different magnitudes, rates, and durations of groundwater decline. We observed groundwater dynamics and the response of Populus fremontii, Salix gooddingii, and Tamarix ramosissima saplings at 3 sites between 1995 and 1997 along the Bill Williams River, Arizona. At a site where the lowest observed groundwater level in 1996 (–1.97 m) was 1.11 m lower than that in 1995 (–0.86 m), 92–100% of Populus and Salix saplings died, whereas 0–13% of Tamarix stems died. A site with greater absolute water table depths in 1996 (–2.55 m), but less change from the 1995 condition (0.55 m), showed less Populus and Salix mortality and increased basal area. Excavations of sapling roots suggest that root distribution is related to groundwater history. Therefore, a decline in water table relative to the condition under which roots developed may strand plant roots where they cannot obtain sufficient moisture. Plant response is likely mediated by other factors such as soil texture and stratigraphy, availability of precipitation-derived soil moisture, physiological and morphological adaptations to water stress, and tree age. An understanding of the relationships between water table declines and plant response may enable land and water managers to avoid activities that are likely to stress desirable riparian vegetation.

Key words: groundwater, riparian habitat, Populus, Salix, Tamarix, Arizona, root distribution.

Although surface water flows and associated variability in stream flow and evapotranspiration fluvial processes exert strong influences on can result in intra- and interannual changes in woody riparian establishment in arid and semi- alluvial water tables. Fluvial processes such as arid regions (Stromberg et al. 1993, Scott et al. channel incision or bed aggradation may also 1996), the alluvial groundwater and associated cause groundwater regimes to change. Human capillary fringe and unsaturated zone are water activities such as groundwater pumping, sur- sources upon which many riparian plants rely face flow diversion, or in-stream sand and for most of the year (Busch et al. 1992, Kolb et gravel mining may lead to declines in riparian al. 1997, Snyder et al. 1998). The importance water tables (Groeneveld and Griepentrog of alluvial groundwater is pronounced in inter- 1985, Stromberg et al. 1992, Stromberg and mittent or ephemeral streams and in regions Patten 1996, Kondolf 1997). with little precipitation, such as the southwest- Water table declines can reduce riparian ern United States (Robinson 1958, Snyder et al. plant growth and potentially lead to mortality 1998). The need for high water tables (often (Scott et al. 1999). Declines in alluvial water <1.5 m from the ground surface) for success- tables also may change the distribution and ful seedling establishment of woody riparian abundance of different riparian plant associa- plants has been observed at numerous sites tions, which tend to thrive under different (Mahoney and Rood 1998) and experimentally groundwater conditions (Bryan 1928, Strom- demonstrated for Populus (Mahoney and Rood berg et al. 1996). Of particular research and 1991, 1992, Segelquist et al. 1993). In addition, management interest are conditions influenc- mature riparian trees and shrubs are often ing the relative abundance of dominant woody associated with water tables <3 m deep (Strom- floodplain species, including native Populus berg et al. 1996). and Salix spp. and exotic Tamarix spp. Populus Floodplain water tables can fluctuate con- and Salix require relatively shallow ground- siderably over time, resulting from a variety of water and are sensitive to drought associated natural and anthropogenic phenomena. Natural with groundwater declines (Busch et al. 1992,

1Department of Plant Biology, Arizona State University, Tempe, AZ 85287-1601. 2Present address: United States Geological Survey, Midcontinent Ecological Science Center, Fort Collins, CO 80525-3400.

66 2000] PLANT RESPONSE TO WATER TABLE DECLINE 67

Tyree et al. 1994, Smith et al. 1998, Scott et al. flow. Average annual precipitation along the 1999). Tamarix is reported to be more tolerant river ranges from approximately 22 cm near of water stress than Populus or Salix (Busch Alamo Dam (National Climatic Data Center and Smith 1995, Cleverly et al. 1997, Devitt et stations; Alamo Dam 6ESE and Alamo Dam) al. 1997, Smith et al. 1998), and therefore it to 13 cm near the Colorado River (National should be able to survive where water tables Climatic Data Center station; Parker 6NE). are relatively deep. There are also likely criti- Mean annual flow in the Bill Williams River is cal water table depths beyond which given approximately 3.5 m3 s–1 (1941–1996; U.S. sized individuals of a given species cannot sur- Geological Survey Gaging Station #09426000). vive (Graf 1982). Flow regulation by Alamo Dam has dramati- Despite the importance of alluvial water cally reduced flood peaks and in recent years table conditions to riparian vegetation, little is has increased low flows (Shafroth et al. 1998). known about how established plants respond Riparian vegetation along the Bill Williams to different magnitudes, rates, and durations River is dominated by several woody species of groundwater decline. Quantifying plant common to low-elevation southwestern ripar- response to changing water table conditions ian ecosystems, including Populus fremontii S. may result in identification of stress or mortal- Watson (Fremont cottonwood), Salix good- ity thresholds and hence aid efforts to manage dingii Ball (Goodding willow), Tamarix ramo- land use and stream flow in ways that minimize sissima Ledebour (saltcedar), Baccharis salici- impacts to groundwater and promote survival folia (R. & P.) Pers. (seep willow), and Prosopis of desirable riparian species. Few studies in spp. (mesquite). western riparian ecosystems have reported a plant response to measured water table declines METHODS (Condra 1944, Judd et al. 1971, Stromberg et al. 1992, Devitt et al. 1997, Scott et al. 1999). In April 1995 we selected 8 sites along the The objective of our study was to add to this Bill Williams River as part of a larger study sparse database by quantifying the response of (Shafroth et al. 1998). The sites were subjec- 3 woody riparian species to different water tively selected to represent a range of geomor- table dynamics and to clarify factors that are phologic and vegetative conditions. For the likely to be important in determining plant present study we examined 3 of these sites response. We examined growth and survival of (BW1, BW5, BW7). At each site a cross-valley saplings of Populus fremontii, Salix goodingii, transect was established perpendicular to the and Tamarix ramosissima at 3 sites with differ- stream channel, and different patches of vege- ent groundwater regimes over a 3-yr period tation were identified along the transect based along the Bill Williams River in western Arizona. on a combination of overstory dominance and geomorphologic setting. For this study we ex- STUDY AREA amined patches that contained seedlings and saplings of Populus, Salix, and Tamarix that The Bill Williams River drains approxi- became established between 1993 and 1995 mately 13,700 km2, with headwaters in the (age determined by counts of annual rings; Central Highlands region of central Arizona at Shafroth et al. 1998). Seedling patches were approximately 1830 m, and downstream reaches those containing plants that became estab- in the Sonoran Basin and Range Province in lished in 1995, saplings in 1993–94. The num- west central Arizona. Beginning at the conflu- ber of seedling and sapling patches per tran- ence of the Big Sandy and Santa Maria rivers, sect was variable and included 2 patches along the Bill Williams River flows for approximately BW1 and 4 patches along BW5 and BW7. 70 km. The upstream-most 6.5 km now consists Within each patch we randomly located a 5 × of waters impounded behind Alamo Dam, which 20-m quadrat and in January 1996 measured was completed in 1968. Downstream of the the diameter of all saplings in the quadrat. dam the Bill Williams River flows 63 km to its During summer 1996, wilting, chlorosis, and confluence with the Colorado River (now Lake apparent shoot mortality of woody plants were Havasu) at an elevation of 137 m. Variation in observed at 1 of the sites (BW5). To quantify the depth of alluvium results in a mix of reaches the response, we resampled stem densities in with perennial and seasonally intermittent the 2 sapling quadrats at BW5 in October 68 WESTERN NORTH AMERICAN NATURALIST [Volume 60

1996. In December 1997 these sapling quadrats water table levels in 1996 (–2.55) and 1997 were again resampled and 2 quadrats contain- (–2.91) were 0.44 and 0.80 m deeper than the ing 1995 cohorts were also sampled. In Decem- lowest water table level in 1995. Soil texture at ber 1997 quadrats with plants of the same age BW1 ranged from strata containing principally as those at BW5 were also resampled at 2 coarse and medium sands to strata with large other sites (BW1, BW7) that had groundwater quantities of organic material and silt (Fig. 1b). dynamics different from those at BW5. At Electrical conductivity ranged from 0.7 to 1.6 each site a representative Populus fremontii dS m–1. At BW1 the 1997 rooting depth was sapling was excavated in December 1997, its approximately –1.40 m, where a flare of roots root distribution sketched, and the soil stratig- spread atop a soil layer rich in organic mater- raphy of the excavated pit described. ial and silt (Fig. 1b). Coarse roots also occurred Sandpoint wells were installed at each site at other locations throughout the soil column. in April 1995 and used to measure the depth Because of large fluctuations in the water table, to groundwater approximately monthly through most roots were inundated for part of the year October 1997. To obtain relative elevations of and were well above the water table at other the quadrats and monitoring wells, we sur- times. veyed the topography of each transect in Janu- At BW1 Populus and Salix sapling densities ary 1996. Soil samples were collected from 2 declined 88–89% between January 1996 and depths at each quadrat: 0–30 cm and 30–60 December 1997. However, basal area of these cm below ground surface. The proportion of species increased 110–160% over the same each sample in 5 particle size classes was period. Tamarix stem density at BW1 decreased determined by (1) visual estimation in the 50%, while its basal area increased 16%. In ± field for particles >2 cm median dimension, December 1997 the mean sx– density of Pop- (2) sieving for particles >2 mm and <2 cm, ulus/Salix and Tamarix was 70 ± 55 and 28 ± and (3) hydrometer method for sand, silt, and 23 stems 100 m–2, respectively (n = 2). The ± ± 2 clay (Day 1965). Electrical conductivity (dS mean sx– basal area was 3.46 2.64 cm 100 m–1) of the filtered solution from a 1:1 m–2 for Populus/Salix and 3.23 ± 3.07 cm2 100 soil:water slurry was determined with a Beck- m–2 for Tamarix (n = 2). man Instruments conductivity probe. At site BW5 the water table was relatively Groundwater level measurements were sum- high and stable throughout 1995 (ca –0.80 m), marized as follows: measured depths through but the lowest water tables in 1996 and 1997 time, maximum depth to the water table for were 1.11 and 2.28 m deeper than in 1995 each year, and difference between the deepest (Fig. 2a). Quadrats containing saplings at this water table level in 1995 and deepest levels in site were 1.55–1.97 m and 2.72–3.14 m above 1996 and 1997. Changes in stem density and the lowest water table in 1996 and 1997, basal area between January 1996 and Decem- respectively. Soils at BW5 primarily com- ber 1997 were calculated and expressed as per- prised sands and secondarily gravels (Fig. 2b); centages of the January 1996 measurements. electrical conductivity ranged from 0.3 to 1.5 To assess correlations between plant response dS m–1. At BW5 the excavated sapling was and groundwater level change, we conducted rooted to a depth of –0.65 m in 1997, and the simple linear regression analysis with change majority of root biomass was distributed be- in stem density and basal area for both Popu- tween –0.45 and –0.60 m (Fig. 2b), or 0.14–0.41 lus/Salix and Tamarix as dependent variables m above the high water tables observed be- and change in groundwater level as the inde- tween 1995 and 1997. pendent variable. Populus and Salix saplings at BW5 experienced a 92–100% reduction in stem density be- RESULTS tween January and October 1996. By December 1997 no Populus or Salix individuals were At site BW1 the water table had regular alive in the quadrats, and only scattered, older intra-annual fluctuations, with observed differ- trees survived in the transect vicinity. In the 2 ences between annual high and low water sapling quadrats at BW5, Tamarix stem den- tables ranging from 1.51 to 2.10 m (Fig. 1a). sity declined 0–13% by October 1996. By The maximum depth to water where saplings December 1997 stem density in 1 quadrat at BW1 survived was –2.91 m. The lowest increased by 105%, while in the other it 2000] PLANT RESPONSE TO WATER TABLE DECLINE 69

Fig. 1. Groundwater dynamics and Populus fremontii sapling root architecture at site BW1, Bill Williams River, Ari- zona: a, BW1 water table levels, measured approximately monthly from April 1995 through October 1997. Solid vertical bars depict annual water table level range, with lowest observed water table depth noted below the bar. Hashed vertical bars depict water table decline, defined as the difference between lowest observed water table depth in 1995 and lowest observed in 1996 and 1997. b, Root architecture of a Populus fremontii sapling at site BW1. Annual water table level range is shown for years 1995–1997. Also shown is the soil profile where the sapling was excavated.

decreased to 48% of the January 1996 level. equal to that of sand in most samples. Soil Basal area of Tamarix in 1997 increased 300% electrical conductivity ranged from 0.2 to 0.5 in 1 quadrat and decreased 33% in the other, dS m–1. At BW7 roots were much shallower, though the absolute changes were small. By reaching a depth of only –0.20 m (Fig. 3b), December 1997 only Tamarix survived at rela- always within 0.12 m of the annual high water tively low stem densities and basal area. Its table level. Where excavated, these roots were ± ± –2 mean sx– density was 55 39 stems 100 m , of large diameter and had spread laterally. ± ± 2 and mean sx– basal area was 0.57 0.48 cm At BW7 only Salix and Tamarix were pre- 100 m–2 (n = 4). sent in the sapling quadrats. Stem density of The water table at site BW7 was high and Salix decreased 57%, while Tamarix stem den- stable throughout the study period (ca –0.40 sity varied from a 48% decrease to a 400% m), except for a decline of 0.66 m in June and increase. Salix basal area increased 201%, while July 1997 (Fig. 3a). Even with this drop, the Tamarix basal area increased 43–78%. The ± water table was relatively high and was only December 1997 mean sx– density of Salix and 0.44 m lower than the lowest water table in Tamarix was 27 ± 18 and 176 ± 83 stems 100 1995 (–0.38 m) and no more than 0.82 m m–2, respectively (n = 4). For Salix the mean ± ± 2 –2 below the ground surface of a quadrat contain- sx– basal area was 10.58 4.94 cm 100 m ing saplings. Soil texture at BW7 was the and for Tamarix it was 2.87 ± 1.14 cm2 100 coarsest, with the proportion of gravel almost m–2. 70 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 2. Groundwater dynamics and Populus fremontii sapling root architecture at site BW5, Bill Williams River, Ari- zona. Details of a and b are as described in Figure 1.

Change in stem density between sampling composed largely of sand and gravel, and dates decreased in linear fashion with the complete mortality followed a decline of 2.28 change in water table depth (defined as the m in the subsequent year (from lowest level in maximum annual decline from the lowest 1995 to lowest level in 1997; site BW5). Where water table level observed in 1995) for Populus groundwater declines were smaller, decreases and Salix (Fig. 4a, r2 = 0.65, P = 0.05, df error in Populus and Salix density were smaller and = 4), but not for Tamarix (Fig. 4c, r2 = 0.04, P basal area increased. In contrast to Populus = 0.74, df error = 3). Stem density of Populus and Salix, some Tamarix individuals survived and Salix decreased in all sampled quadrats under all conditions and basal area increased (Fig. 4a), whereas Tamarix stem density in- in 80% of the measured quadrats. Decreases creased in some quadrats (Fig. 4c). Change in in stem density are typical as a stand of young basal area was also negatively correlated with trees ages and, except where complete mortal- change in water table depth for Populus and ity is observed, should be interpreted in con- Salix (Fig. 4b, r2 = 0.99, P < .01, df error = junction with basal area measurements. For 4), but not for Tamarix (Fig. 4d, r2 = 0.12, P = example, where plots were subjected to a 0.56, df error = 3). Basal area of Populus and groundwater change of 0.44–0.80 m, Populus Salix increased between January 1996 and and Salix density decreased 52–89% but basal December 1997, except at BW5 where all area increased 200–300% (Figs. 4a, 4c). plants died (Fig. 4b). Basal area of Tamarix in- These results are consistent with previous creased in 4 of 5 measured quadrats between studies that documented lethal effects of January 1996 and December 1997 (Fig. 4d). groundwater declines on Populus, but not on Tamarix. Scott et al. (1999) observed high mor- DISCUSSION tality of mature Populus deltoides ssp. monilif- era trees in eastern Colorado following a sus- Almost complete mortality of Populus and tained groundwater decline of 1.12 m, and Salix saplings was observed following a reduced branch growth where water tables groundwater decline of 1.11 m (from lowest declined by 0.47 m. Condra (1944) reported level in 1995 to lowest level in 1996) in soils mortality of shallow-rooted Populus, Fraxinus, 2000] PLANT RESPONSE TO WATER TABLE DECLINE 71

Fig. 3. Groundwater dynamics and Populus fremontii sapling root architecture at site BW7, Bill Williams River, Arizona. Details of a and b are as described in Figure 1.

and Acer negundo trees along the Platte River 1972). However, studies of Prosopis velutina in following water table declines of 0.61–0.91 m southwestern riparian ecosystems suggest that in coarse soils. Two-year-old Tamarix survived the absolute water table depth may effectively a water table decline (0.9 m) that stranded determine the expression of various physiolog- roots above moist soil for 30 d; roots resumed ical and morphological traits (Stromberg et al. growth immediately following rewetting (Devitt 1992). At 2 sites along the Bill Williams River, et al. 1997). Differential survival of Tamarix vs. Busch and Smith (1995) reported that leaf Populus/Salix at site BW5 corroborates reports number, leaf area, specific leaf area, and stem that greater tolerance of water stress can lead elongation of Populus fremontii were greater at to Tamarix dominance on relatively dry, ripar- the site with relatively high and stable water ian sites (Smith et al. 1998, Stromberg 1998). tables. Results of this study suggest the impor- We propose that the importance of change tance of change in groundwater depth relative from a previous groundwater depth is due to to a previous condition or pattern as opposed the influence of groundwater history on root to the absolute depth to the water table. For architecture. Root architecture has been shown example, saplings at site BW1 survived where to be a function of soil moisture conditions the depth to the alluvial water table was –2.91 and water table depth in Populus and Salix in m and their basal area increased, whereas Nebraska (Sprackling and Read 1979) and almost no saplings at site BW5 survived at Tamarix in Arizona (Gary 1963). At site BW1, water table depths of –1.55 to –1.97 m (1996), where relatively large fluctuations in ground- and none survived where water table depths water levels are the norm, Populus saplings were –2.72 to –3.14 m (1997). By contrast, the were rooted relatively deeply, with a some- change in water table was 1.11 m (1996) and what broad depth distribution of coarse roots. 2.38 m (1997) at BW5 vs. 0.48 m (1996) and At sites BW5 and BW7, roots were distributed 0.8 m (1997) at BW1. Water content of Tamarix largely in a flare above, but near, the annual cladophylls did not vary on plants growing at high water table, suggesting that water tables sites with different depths to the water table were stable in the early years of plant growth. in New Mexico (range of ca 1–3 m; Wilkinson When groundwater levels dropped in 1996 and 72 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Fig. 4. Change in stem density and basal area of stands of saplings as a function of change in annual low water table level. Lines are from linear regression analysis: a, stem density of Populus and Salix; density change = 32.8–14.9* (water table change; r2 = 0.65, P = 0.05, df error = 4); b, basal area of Populus and Salix; basal area change = 362.6–159.2* (water table change; r2 = 0.99, P < .01, df error = 4); c, stem density of Tamarix; density change = 194.0–33.9* (water table change; r2 = 0.04, P = 0.74, df error = 3); d, basal area of Tamarix; basal area change = 122.5 + 46.8 (water table change; r2 = 0.12, P = 0.56, df error = 3).

1997 at BW5, roots apparently were stranded these roots are located at a layer of fine sedi- well above the water table, resulting in shock ments and organic matter which likely retains to the plants. excess water even when the water table has Plant response to water table level change dropped to a lower level (Fig. 1). Water retained is mediated by soil water retention, which is above a clay lens at a site in the Carmel River largely a function of soil texture and stratigra- valley, California, apparently enabled trees to phy. Trees growing in finer-textured soils may maintain relatively vigorous growth, despite a survive greater water table changes than trees groundwater change in excess of 2.5 m ( J.G. growing in coarser soils (Condra 1944). Cooper Williams personal communication; Fig. 5). et al. (1999) have noted the importance of Relatively little water can be retained in fine-textured soils for the survival of Populus coarser soils found at BW5, which likely con- seedlings that have not yet tapped the alluvial tributed to mortality observed there. Textural water table. Stratification of the soil profile differences alone do not determine water may result in retention of significant quanti- availability, however, and better estimates can ties of water where a finer-textured layer lies be obtained with measures of soil water above a coarse layer (Brady 1990). This effect potential. may explain how saplings at site BW1 sur- Species differences in morphological and vived with their deepest roots more than 1.5 physiological above- and belowground adjust- m above the lowest water table, as many of ments to reduced soil moisture should result 2000] PLANT RESPONSE TO WATER TABLE DECLINE 73

Fig. 5. Conceptual model of woody riparian plant response to water table decline. Plant response (y-axis) scale is semi-quantitative and represents a gradient of growth and morphological responses. Position of plotted points on y-axis is estimated. Groundwater decline (x-axis) refers to a change in groundwater from a previous, presumably consistent, condition or dynamic. All plotted points are responses of either Populus or Salix spp. Lines are hypothetical response curves for data from this study and another. In this conceptual model hypothetical response curves would shift position along the x-axis and their slopes could be altered, depending on different combinations of groundwater decline rate and duration, species, soil texture, precipitation:evaporation ratio, and tree age.

in differential survival or growth following a erly et al. 1997), whereas Populus is vulnerable groundwater decline. At site BW5, some to cavitation at relatively high water potentials Tamarix individuals survived and increased in (Tyree et al. 1994). Additionally, whereas Popu- size, whereas all Populus and Salix died. Devitt lus and Salix may reduce leaf area in response et al. (1997) reported Tamarix survival follow- to dry conditions (Smith et al. 1991, Busch ing a depth and duration of water table decline and Smith 1995), Tamarix can maintain high similar to that observed at BW5. Tamarix has leaf areas under these conditions (Sala et al. been shown to have greater water-use effi- 1996, Cleverly et al. 1997). The ability of plants ciency than Populus or Salix and can maintain to grow new roots to respond to groundwater high rates of photosynthesis at relatively low declines is not well understood but would likely water potentials (Busch and Smith 1995, Clev- be effective only where water table changes 74 WESTERN NORTH AMERICAN NATURALIST [Volume 60 are gradual (Groeneveld and Griepentrog 1985, and more humid conditions result in lower Mahoney and Rood 1991, Segelquist et al. transpirational demand. 1993). Species differences in dependence on CONCLUSIONS groundwater may influence response to water table declines. Plants that rely on precipita- The impact of a particular water table tion-derived soil water for some of their water decline depends on several interacting factors supply (facultative phreatophytes) may experi- that influence both water uptake and water ence a reduction only in leaf area or crown demand. These factors include magnitude of volume in some situations that are lethal to groundwater decline relative to the pre-decline plants that must maintain root contact with distribution of roots, rate of decline, duration the groundwater or capillary fringe (obligate of decline, ability of soil to retain water follow- phreatophytes). Similarly, facultative phreato- ing the decline, ability of the plant to grow phytes should be able to survive a given water new roots to adjust to lowered water table, table decline for a longer duration than oblig- ability of the plant to adjust water demand ate phreatophytes. There appears to be mixed (e.g., via physiological and morphological adap- evidence in the literature for the phreato- tations), plant age and size, transpirational phytic status of Populus, Salix, and Tamarix. demand, and importance of other sources of There is some evidence that Tamarix is a fac- water (e.g., precipitation) to the overall plant ultative phreatophyte (Busch et al. 1992), al- water supply. We synthesize these variables into though it has been observed to use only a conceptual model of woody riparian plant response to water table decline in Figure 5. groundwater where this was readily available We have drawn hypothetical response curves (McQueen and Miller 1972). Populus fremontii for our data and another study (Scott et al. on the Bill Williams River has been shown to 1999) that span the plant response range from be dependent on groundwater (Busch et al. vigorous growth to complete mortality. The 1992), though it may be considered a faculta- basic shape of these curves may apply to other tive phreatophyte when including the full situations and species, but the position on the range of its growing sites (McQueen and Miller x-axis and the slope of the response curves 1972, Snyder et al. 1998). Salix gooddingii has may vary depending upon the particular com- been reported to be an obligate phreatophyte bination of rate and duration of groundwater (McQueen and Miller 1972, Busch et al. decline, species attributes, soil texture and 1992), although it is apparently more drought stratigraphy, climate and tree age (Fig. 5). tolerant than P. fremontii (Busch and Smith Future research incorporating more of the 1995). variables discussed above would provide a Climatic variables such as precipitation, better understanding of how particular magni- temperature, and humidity will also influence tudes, rates, and durations of alluvial ground- plant response to water table decline. The water decline will influence woody riparian degree to which plants use precipitation- vegetation in arid and semiarid regions. Such derived soil water depends in part on reliabil- research could have important management ity and quantity of precipitation and is there- implications. For example, on the Bill Williams fore probably more common in regions or at River, flows from Alamo Dam upstream of our elevations with higher precipitation. Detri- sites could be managed to promote survival of mental effects of water table declines may be desirable species. This could be accomplished mitigated where precipitation occurs and by intentionally varying flows in early years plants have roots near the surface. Climatic following an establishment event to promote factors are also important determinants of deeper root growth and hence less vulnerabil- transpirational demand (via temperature, humidity to lower water tables during inevitable dry ity). Consequently, in especially hot and dry periods. Another stream flow management settings such as low-elevation sites in western option would be to release a mid- to late-sum- Arizona, the lethal duration of water table de- mer pulse to resaturate the soil column and cline of a given magnitude is likely to be much raise water tables. Such summer pulses com- shorter than at sites where plants can utilize monly occurred prior to the construction of precipitation and where lower temperatures Alamo Dam in association with monsoonal 2000] PLANT RESPONSE TO WATER TABLE DECLINE 75 precipitation, but they have been virtually KOLB, T.E., S.C. HART, AND R. AMUNDSON. 1997. Boxelder eliminated since completion of the dam. Other water sources and physiology at perennial and ephemeral stream sites in Arizona. Tree Physiology human activities that impact alluvial water table 17:151–160. levels throughout western North America such KONDOLF, G.M. 1997. Hungry water: effects of dams and as groundwater pumping and sand and gravel gravel mining on river channels. Environmental mining could be managed to ensure that water Management 21:533–551. MAHONEY, J.M., AND S.B. ROOD. 1991. A device for study- tables do not fall at rates and magnitudes likely ing the influence of declining water table on poplar to kill existing stands of riparian vegetation. growth and survival. Tree Physiology 8:305–314. ______. 1992. Response of a hybrid poplar to water table ACKNOWLEDGMENTS decline in different substrates. Forest Ecology and Management 54:141–156. ______. 1998. Streamflow requirements for cottonwood This manuscript benefited from reviews by seedling recruitment—an integrative model. Wetlands G.T. Auble, D.E. Busch, J.M. Friedman, T.E. 18:634–645. Kolb, J.L. Horton, M.L. Scott, S.D. Smith, and MCQUEEN, I.S., AND R.F. MILLER. 1972. Soil-moisture an anonymous reviewer. and energy relationships associated with riparian vegetation near San Carlos, Arizona. Professional Paper 655-E. United States Geological Survey, Wash- LITERATURE CITED ington, DC. ROBINSON, T.W. 1958. Phreatophytes. United States Geo- BRADY, N.C. 1990. The nature and properties of soils. 10th logical Survey Water-supply Paper 1423. Washing- edition. MacMillan, New York. ton, DC. BRYAN, K. 1928. Change in plant associations by change in SALA, A., D.A. DEVITT, AND S.D. SMITH. 1996. Water use by ground water level. Ecology 9:474–478. Tamarix ramosissima and associated phreatophytes BUSCH, D.E., N.L. INGRAHAM, AND S.D. SMITH. 1992. in a Mojave Desert floodplain. Ecological Applica- Water uptake in woody riparian phreatophytes of the tions 6:888–898. southwestern United States: a stable isotope study. SCOTT, M.L., J.M. FRIEDMAN, AND G.T. AUBLE. 1996. Flu- Ecological Applications 2:450–459. vial process and the establishment of bottomland BUSCH, D.E., AND S.D. SMITH. 1995. Mechanisms associ- trees. Geomorphology 14:327–340. ated with decline of woody species in riparian eco- SCOTT, M.L., P.B. SHAFROTH, AND G.T. AUBLE. 1999. systems of the southwestern U.S. Ecological Mono- Responses of riparian cottonwoods to alluvial water graphs 65:347–370. table declines. Environmental Management 23: CLEVERLY, J.R., S.D. SMITH, A. SALA, AND D.A. DEVITT. 347–358. 1997. Invasive capacity of Tamarix ramosissima in a SEGELQUIST, C.A., M.L. SCOTT, AND G.T. AUBLE. 1993. Mojave Desert floodplain: the role of drought. Establishment of Populus deltoides under simulated Oecologia 111:12–18. alluvial groundwater declines. American Midland CONDRA, G.E. 1944. Drought, its effects and measures of Naturalist 130:274–285. control in Nebraska. Nebraska Conservation Bul- SHAFROTH, P.B., G.T. AUBLE, J.C. STROMBERG, AND D.T. letin 25. 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Plant water relations of Tamarix SNYDER, K.A., D.G. WILLIAMS, AND V.L. GEMPKO. 1998. ramosissima in response to the imposition and allevi- Water source determination in cottonwood/willow ation of soil moisture stress. Journal of Arid Environ- and mesquite forests on the San Pedro River in Ari- ments 36:527–540. zona. Pages 185–188 in E.F. Wood, editor, Proceed- GARY, H.L. 1963. Root distribution of five-stamen tama- ings of the American Meteorological Society Special risk, seepwillow, and arrowweed. Forest Science 9: Symposium on Hydrology. 78th Annual Meeting, 311–314. Phoenix, AZ. GRAF, W.L. 1982. Tamarix and river channel management. SPRACKLING, J.A., AND R.A. READ. 1979. Tree root systems Environmental Management 6:283–296. in eastern Nebraska. Nebraska Conservation Bul- GROENEVELD, D.P., AND T.E. GRIEPENTROG. 1985. Inter- letin 37. Lincoln, NE. 73 pp. dependence of groundwater, riparian vegetation, and STROMBERG, J. 1998. Dynamics of Fremont cottonwood streambank stability: a case study. USDA Forest Ser- (Populus fremontii) and saltcedar (Tamarix chinensis) vice, General Technical Report RM-120:44–48. populations along the San Pedro River, Arizona. JUDD, J.B., J.M. LAUGHLIN, H.R. GUENTHER, AND R. HAN- Journal of Arid Environments 40:133–155. DERGRADE. 1971. The lethal decline of mesquite on STROMBERG, J.C., AND D.T. PATTEN. 1996. Instream flow the Casa Grande National Monument. Great Basin and cottonwood growth in the eastern Sierra Nevada Naturalist 31:153–159. of California, USA. Regulated Rivers 12:1–12. 76 WESTERN NORTH AMERICAN NATURALIST [Volume 60

STROMBERG, J.C., B.D. RICHTER, D.T. PATTEN, AND L.G. TYREE, M.T., K.J. KOLB, S.B. ROOD, AND S. PATIÑO. 1994. WOLDEN. 1993. Response of a Sonoran riparian for- Vulnerability to drought-induced cavitation of ripar- est to a 10-year return flood. Great Basin Naturalist ian cottonwoods in Alberta: a possible factor in the 53:118–130. decline of the ecosystem? Tree Physiology 14: STROMBERG, J.C., R. TILLER, AND B. RICHTER. 1996. Effects 455–466. of groundwater decline on riparian vegetation of WILKINSON, R.E. 1972. Water stress in salt cedar. Botani- semiarid regions: the San Pedro, Arizona. Ecological cal Gazette 133:73–77. Applications 6:113–131. STROMBERG, J.C., J.A. TRESS, S.D. WILKINS, AND S.D. Received 5 October 1998 CLARK. 1992. Response of velvet mesquite to ground- Accepted 19 February 1999 water decline. Journal of Arid Environments 23: 45–58. Western North American Naturalist 60(1), © 2000, pp. 77–92

SUITABILITY OF SHRUB ESTABLISHMENT ON WYOMING MINED LANDS RECLAIMED FOR WILDLIFE HABITAT

Richard A. Olson1, James K. Gores1,2, D. Terrance Booth3, and Gerald E. Schuman3

ABSTRACT.—Restoring coal mined land to pre-mining shrub cover, density, height, community composition, and diversity to renew wildlife habitat quality is a priority for reclamation specialists. Long-term shrub reestablishment success on reclaimed mined land in Wyoming and suitability of these lands for wildlife habitat are unknown. Fourteen reclaimed study sites, 10 yr old or older, were selected on 8 mines in Wyoming to evaluate shrub reestablishment and wildlife habitat value for antelope (Antilocapra americana) and sage grouse (Centrocercus urophasianus). Five sites were categorized as fourwing saltbush (Atriplex canescens) sites and 9 as fourwing saltbush/big sagebrush (A. canescens/Artemisia tridentata spp. wyomingensis) sites. Published data describing antelope and sage grouse–preferred habitat requirements in sagebrush-grassland steppe ecosystems were used to evaluate shrub community value of sampled sites for wildlife habitat. Mean shrub canopy cover, density, and height for fourwing saltbush sites were 5.8%, 0.23 m–2, and 41.6 cm, respectively, compared to 5.6%, 0.61 m–2, and 31.1 cm for fourwing saltbush/big sagebrush sites. Two fourwing saltbush and 4 fourwing saltbush/big sagebrush sites provided sufficient cover for antelope, while 2 fourwing saltbush and 4 fourwing saltbush/big sagebrush sites were adequate for sage grouse. Only 1 fourwing saltbush/big sagebrush site provided high enough shrub densities for sage grouse. One fourwing saltbush and 7 fourwing saltbush/big sagebrush sites provided ample shrub heights for antelope, while 1 fourwing saltbush and 8 fourwing saltbush/big sagebrush sites were sufficient for sage grouse. One fourwing saltbush and 1 fourwing saltbush/big sagebrush site provided enough grass, forb, and shrub composition for antelope, while no site in either reclamation type was satisfactory for sage grouse. Shrub diversity was 3 times higher for fourwing saltbush/big sagebrush sites (0.984) than for fourwing saltbush sites (0.328). Individually, sites seeded with multiple shrub species had higher canopy cover, density, and diversity compared with single-species shrub seedings. Achieving pre- mining shrub cover, density, height, community composition, and diversity within existing bond-release time frames is unrealistic, considering that some native shrublands require 30-60 yr to reach maturity.

Key words: disturbed land, sagebrush, fourwing saltbush, community diversity.

Shrub reestablishment on reclaimed mined plant communities and importance for wildlife lands continues to be a controversial topic habitat. This important shrub provides year- among mining interests, regulatory agencies, long habitat for antelope (Antilocapra ameri- environmental groups, and state and federal cana [Ord.]) and sage grouse (Centrocercus wildlife management agencies. Because many urophasianus Bonaparte), 2 abundant and eco- wildlife species utilize reclaimed mined lands, nomically important game species in Wyoming. quality (height, cover, density, and diversity) of Although widely distributed across Wyoming shrub reestablishment on these lands is impor- and the Rocky Mountain West, big sagebrush tant for achieving good wildlife habitat condi- is sometimes difficult to reestablish due to low tions. Information on long-term success of seedling vigor, inability to compete with herba- shrub reestablishment is needed to assess ceous species, poor seed quality, and altered reclamation objectives for creating quality wild- edaphic conditions (Cockrell et al. 1995). The life habitat, formulating future seed mixes high cost and limited availability of big sage- for reclamation, and evaluating reclamation brush seed further confounds its use in recla- methodologies and regulations. mation. Shrub reestablishment practices in Wyoming Fourwing saltbush (Atriplex canescens [Pursh] on reclaimed mined land often emphasize Nutt.) is a highly palatable, nutritious shrub Wyoming big sagebrush (Artemisia tridentata used by wildlife and livestock for forage in all [Pursh] Nutt. ssp. wyomingensis [Beetle and seasons (Long 1981). Additionally, it provides Young]) due to its predominance in premining cover for game birds on arid rangeland (Shaw

1Department of Renewable Resources, University of Wyoming, Box 3354, University Station, Laramie, WY 82071. 2Current address: Wind River Publishing, Box 81, Laramie, WY 82070. 3High Plains Grasslands Research Station, USDA-ARS, 8408 Hildreth Road, Cheyenne, WY 82009.

77 78 WESTERN NORTH AMERICAN NATURALIST [Volume 60 et al. 1984). The use of fourwing saltbush in shrub species (Yoakum 1984b) and 10–30% reclamation was de-emphasized in recent years forb cover (Kindschy et al. 1982). Cook (1984) over concerns about low survival rates after reports similar antelope habitat requirements planting and competitive exclusion of other consisting of 13–30% shrub cover with 10–38% shrub species (Moghaddam and McKell 1975, herbaceous cover. Optimum shrub heights for Booth 1985). Fourwing saltbush seedlings are antelope are ≤38 cm (Sundstrom et al. 1973) sensitive to freezing and wet soil conditions and 38 cm (Yoakum 1984b), with a recom- that make them susceptible to a fungal disease mended range of 13–63 cm (Kindschy et al. (Plummer et al. 1966). However, fourwing salt- 1982). Cook (1984) reported the ideal range of bush is more tolerant to planting depth varia- big sagebrush heights is 22–46 cm and sug- tions than big sagebrush, which probably gested that big sagebrush heights <13 cm and explains its higher establishment success when >60 cm are less suitable for antelope. Preferred drill-seeded in earlier reclamation programs composition of grasses, forbs, and shrubs for (Hennessy et al. 1984). antelope in Wyoming (Sundstrom et al. 1973) A diverse mixture of shrub species provides is 40–60%, 25–35%, and 5–20%, respectively habitat diversity, and wildlife prefer it over (Table 1). Yoakum (1980) reported preferred monocultures (Postovit 1981, Roberson 1984, composition as 50–70% grasses, 20–40% forbs, Yoakum 1984a). Shrubs also provide critical and 5–10% shrubs for central Oregon. Find- forage and cover for a variety of wildlife (Pos- ings of these 5 studies are surprisingly similar tovit 1981, Cook 1984, Nydegger and Smith in their definition of optimum big sagebrush 1984, Roberson 1984, Ngugi et al. 1992). requirements for antelope. Antelope and sage grouse, species common to Table 2 summarizes preferred habitat char- big sagebrush communities (Braun et al. 1977, acteristics for sage grouse in sagebrush-grass- Yoakum 1984b), should benefit from big sage- land steppe ecosystems based on previous brush reestablishment success and subsequent studies. Sage grouse in northeastern Wyoming improvement of habitat quality on reclaimed prefer areas with an average big sagebrush mined land. density of 1.3 shrubs m–2 and an average shrub cover of 5.5% (Postovit 1981). For nesting, HABITAT REQUIREMENTS shrub patches with big sagebrush densities of 2.9 shrubs m–2 and 25% cover are recom- Habitat is defined as “the place where an mended. Hulet et al. (1984) reported that nest- organism lives, and includes both biotic and ing sage grouse in southern Idaho prefer areas abiotic components” (Scalet et al. 1996). Ter- having about 26% shrub cover, with big sage- restrial wildlife biologists most often evaluate brush comprising about 17% of the cover over habitat condition by assessing plant commu- a 9.3-m2 area. In this same study he found that nity characteristics. This paper focuses specifi- 62% of nests were under big sagebrush plants, cally on vegetative characteristics of shrub 14% under three-tip sagebrush (Artemisia tri- communities (e.g., shrub height, canopy cover, partata Rydb.), and 17% beneath antelope bit- density, and diversity), which are important terbrush (Purshia tridentata [Pursh] DC.). habitat parameters for antelope and sage grouse. Roberson (1984) in Utah, Braun et al. (1977) in Preferred habitat characteristics for ante- Colorado, and Dobkin (1995) in Oregon found lope and sage grouse were based on prior that wintering sage grouse prefer areas with research conducted in sagebrush-grassland 28%, ≥20%, and 25–40% shrub cover, respec- steppe ecosystems, since our study areas are tively, while desired nesting habitat consists of in bunchgrass steppe and the western edge 20–40%, 20–40%, and 15–25% shrub cover, (ecotone) of the northern mixed-grass prairie respectively (Table 2). (Hart 1994). These 2 major rangeland ecosys- Height of big sagebrush and other shrubs tems described by Hart (1994) are dominated preferred by sage grouse varies by season and by big sagebrush and are consistent with vege- specific use. Postovit (1981) reported that sage tation characteristics of our study sites. grouse prefer big sagebrush heights of about Desired habitat characteristics for antelope 22 cm in winter and 18 cm in summer and fall. in sagebrush-grassland steppe ecosystems are Where sage grouse nesting occurred, big sage- summarized in Table 1. Antelope prefer open brush heights averaged about 27 cm. Hulet et shrub habitat (5–20% cover) comprising 5–10 al. (1984) reported the average shrub height 2000] SHRUB ESTABLISHMENT ON RECLAIMED MINED LANDS 79

TABLE 1. Preferred habitat characteristics for antelope (Antilocapra americana) in shrub-grassland steppe ecosystems based on existing published literature. Shrub height (cm) Cover (%) Composition (%) No. ______shrub Sage- All Sage- Authority/Location species brush shrubs Forbs Shrubs Grass Forb Shrub brush Sundstrom et al. (1973), Wyoming 5a ≤38 40–60 25–35 5–15b 10–20 Cook (1984), Wyoming 22–46 10–38c 13–30 Yoakum (1980), central Oregon 50–70 20–40 5–10 Yoakum (1984b), Great Basin region 5–10 38 5–20 (mean) Kindschy et al. (1982)d, SE Oregon, Great Basin region 13–63 10–30 5–20

MINIMAL PREFERRED HABITAT REQUIREMENTS 5 22131054020510 aPreferred species include big sagebrush (Artemisia tridentata), sand sagebrush (A. filifolia), fringed sagebrush (A. frigida), silver sagebrush (A. cana), and Douglas rabbitbrush (Chrysothamnus viscidiflorus). bAll other shrub species, excluding big sagebrush (A. tridentata). cIncludes all herbaceous (grasses and forbs) cover. dOptimum combination of percent cover and shrub height are 10–20% forb cover, 10–20% shrub cover, and 13–25 cm shrub height.

TABLE 2. Preferred habitat characteristics for sage grouse (Centrocercus urophasianus) in shrub-grassland steppe ecosystems based on existing published literature. Sagebrush Shrub height (cm) Composition (%) density ______Shrub ______Authority/Location (no. m–2) Sagebrush All shrubs cover (%) Grass Forb Shrub Postovit (1981), NE Wyoming 1.3 (general) 26.6 (nesting) 5.5 (general) 2.9 (nesting) 18 (summer) 25.0 (nesting) 22 (winter) Hulet (1984), southern Idaho 46.7a 26.2b Roberson (1984), Great Basin, Utah 55.8 (winter) 17–79 20–40 (nesting) (nesting) 28 (winter) Martin (1970), SW Montana 42.0 28.4 29.6 Braun et al. (1977), NW Colorado 17–79 20–50 (general) (nesting) 20–40 (nesting) ≥20 (winter) Dobkin (1995), central Oregon 15–25 (nesting)c 25–40 (winter) 15–25 (brood)d

MINIMAL PREFERRED HABITAT REQUIREMENTS 1.3 (general) 17 (nesting) 17 (nesting) 5.5 (general) 42.0 28.4 29.6 2.9 (nesting) 18 (summer) 15 (nesting) 22 (winter) 25 (winter) 15 (brood) aMean shrub height surrounding nests. bBig sagebrush (Artemisia tridentata) should comprise 17.2% of total shrub cover. cShould also include 20% residual herbaceous cover. dShould also include 10–20% live herbaceous (grass and forb) cover. surrounding sage grouse nests was 47 cm, (42.0%, 28.4%, and 29.6%, respectively) for while Roberson (1984) reported a range of sage grouse. 17–79 cm being optimum for nesting habitat. The objectives of this study were to (1) Braun et al. (1977) also suggested sagebrush evaluate shrub reestablishment on reclaimed heights of 17–79 cm for nesting sage grouse. mined lands in Wyoming seeded prior to During winter sage grouse utilized big sage- 1985, (2) assess habitat suitability of these brush with an average height of 56 cm (Rober- seedings for antelope and sage grouse based son 1984). Martin (1970), in southwestern Mon- on prior research in sagebrush-grassland steppe tana, is the only researcher to report preferred ecosystems, and (3) develop recommendations composition of grasses, forbs, and shrubs for improving reclamation practices. 80 WESTERN NORTH AMERICAN NATURALIST [Volume 60

STUDY AREA DESCRIPTIONS lishment. Transects were oriented perpendicular to the longest dimension of each site using Fourteen pre-1985 reclaimed mine sites, a compass. Transect numbers were reduced on 10–17 yr old, were selected from 8 mines in 4 Belle Ayr (5) and WyoDak (10) sites because of geographic locations of Wyoming in 1994. the small size of available reclaimed area. Descriptions and locations of the 14 sample Thirty transects were used at 1 Pathfinder site sites are summarized in Table 3. (the first studied). Preliminary sampling (Path- Each site was classified as either a four- finder site) indicated that 20 transects were wing saltbush/grass (hereinafter called “four- adequate on larger sites to minimize data vari- wing”) or a fourwing saltbush/big sagebrush/ ance and ensure adequate representation of grass (hereinafter called “fourwing/sagebrush”) the revegetated areas. reclamation type depending upon the original Percent aerial cover of shrub species was seed mixture of fourwing saltbush only or a obtained using the line-intercept method (Can- fourwing saltbush/big sagebrush combination. field 1941). Along each transect we recorded Seed mixtures varied among sites, but four- species canopy cover in centimeters and wing saltbush and big sagebrush were the pri- divided that by the transect total (5000 cm). mary shrub species seeded (Table 4). Other Gaps in shrub canopy of ≤4 cm were consid- shrub species in the seed mixtures included ered part of the continuous canopy. rubber rabbitbrush (Chrysothamnus nauseosus Shrub density, expressed as number per [Pall.] Britt.), broom snakeweed (Gutierrezia m2, was determined by counting the number sarothrae [Pursh] Britt. & Rusby), fringed sage- of individual species within a belt transect of brush (Artemisia frigida Willd.), winterfat (Euro- 200 m2 (4 m × 50 m). A 2-m rule, held perpen- tia lanata [Pursh] Howell, syn. Kraschenin- dicular to the transect, was used as a guide nikova lanata [Pursh] Mueese & Smith, syn. when counting individual shrubs along each Ceratoides lanata [Pursh] Howell), grease- side of the transect (Pieper 1978). We included wood (Sarcobatus vermiculatus [Hook.] Torr.), both seedlings and mature plants in density woods rose (Rosa woodsii Lindl.), Gardner’s counts. Shrub height (cm) was also recorded saltbush (Atriplex gardnerii [Moq.] Dietr.), sil- for each species. ver sagebrush (Artemisia cana Pursh), and Shrub canopy cover and density by species shadscale (Atriplex confertifolia [Torr. & Frem.] was converted to relative cover and relative S.Wats.). Five fourwing and 9 fourwing/sagebrush sites were sampled. density. These values were summed for each Seed mixtures for the older fourwing sites species to provide an importance value used (Black Thunder, Belle Ayr, Pathfinder, and to identify community dominants (Curtis and Kemmerer #1) had generally higher grass McIntosh 1951). Relative cover was calculated seeding rates and lower shrub seeding rates by dividing absolute cover of each shrub than fourwing/sagebrush sites (Table 4). In species by total cover of all shrub species. addition, there were fewer shrub species in Likewise, relative shrub density was calcu- the mixture. lated by dividing absolute density of each Seed mixtures for fourwing/sagebrush sites species by total shrub density for all species. A usually contained more big sagebrush seeds larger importance value identifies community than fourwing saltbush seeds due to differ- dominants. ences in seed number per kg. Wyoming big We used importance values of shrub species sagebrush has 4–5.4 million seeds per kg to calculate a Shannon-Wiener diversity index (Meyer 2000) while dewinged fourwing salt- for each sample site (Krebs 1989). Higher bush has 120,000 seeds per kg (Foiles 1974). diversity indices indicate greater shrub com- Therefore, where big sagebrush and fourwing munity diversity. saltbush were both seeded at the same kg per We determined percent composition of ha pure-live-seed (pls) rate, 33–45 times more grasses, forbs, and shrubs at ground level using big sagebrush seeds were sown. point-frame sampling techniques (Pieper 1978). Along each transect, a 10-point sampling METHODS frame was placed every 5 m (100 hits per transect) and the number of pin hits on grass, forb, We placed twenty 50-m transects equidistant and shrub canopy recorded. Percent composi- across sample sites to evaluate shrub reestab- tion by vegetation class was calculated by 2000] SHRUB ESTABLISHMENT ON RECLAIMED MINED LANDS 81

TABLE 3. Descriptions and locations of sampled reclaimed mine sites to assess pre-1985 shrub establishment, 1994, Wyoming. Mean Mean Mean annual annual frost- Seeding Eleva- precipi- temper- free Area age in Reclamation tion tationa aturea periodb Soil parent Company/Location Site (ha) 1994 type (m) (mm) (°C) (days) materialc

NORTHEAST Black Thunder/ 1 26.3 13 Fourwing 1433 280 6.8 125 Tertiary Thunder Basin sandstone, Coal Co., Wright clay shale

Belle Ayr/Amax 1 2.0 13 Fourwing 1433 422 6.8 125 Tertiary Coal West, Gillette sandstone, clay shale

WyoDak/WyoDak 1 4.5 12 Fourwing/big 1341 422 6.8 125 Tertiary Resource Corp., 2 6.5 10 sagebrush 1341 422 6.8 125 sandstone, Gillette clay shale

CENTRAL Pathfinder/ 1 15.8 17 Fourwing 2195 244 4.1 100 Tertiary Pathfinder Mines 2 21.4 12 Fourwing/big 2195 244 4.1 100 sandstone, Corp., Shirley Basin sagebrush clay shale

Dave Johnston/ 1 23.9 10 Fourwing/big 1646 328 8.8 123 Cretaceous Glenrock Coal Co., sagebrush clay shale Glenrock

SOUTH CENTRAL Seminoe I/Arch 1 22.7 10 Fourwing 2012 261 5.5 106 Cretaceous Minerals, Hanna clay shale 2 7.7 10 Fourwing/big 2012 261 5.5 106 Cretaceous sagebrush clay shale

SOUTHWEST Kemmerer Coal/ 1 36.4 14 Fourwing 2225 274 3.5 71 Carboniferous Pittsburg & Midway 2 13.0 13 Fourwing/big 2225 274 3.5 71 linestone Coal Mining Co., sagebrush Kemmerer 3 37.6 13 Fourwing/big 2225 274 3.5 71 clay shale, sagebrush loamstones, Redbed sandstones

Bridger Coal/ 1 6.5 10 Fourwing/big 2073 225 5.9 112 Cretaceous Bridger Coal Co., sagebrush clay shale Rock Springs 2 33.2 10 Fourwing/big 2073 225 5.9 112 Cretaceous sagebrush clay shale

aOwenby and Ezell (1992) bMartner (1986) cYoung and Singleton (1977)

dividing hits of 1 vegetation type by total hits species are associated with these reclaimed for all vegetation types. sites, the absence of published habitat specifi- Wildlife habitat quality of these reclaimed cations limited their inclusion in this analysis. mined lands was assessed against habitat requirements for antelope and sage grouse. These RESULTS AND DISCUSSION species were selected because (1) both are Canopy Cover abundant and economically important game Shrub cover varied considerably between species, (2) they represent a mammal and bird species and sites. Mean cover for the 5 four- species having uniquely different habitat wing sites ranged from 1.9% to 15.7% for all requirements, yet closely associated with sur- shrub species, with a mean of 5.8% (Table 5). rounding sagebrush-grassland steppe ecosys- For the 9 fourwing/sagebrush sites, mean cover tems, and (3) habitat requirements of both ranged from 1.0% to 13.3%, with a mean of species are published. Although other wildlife 5.6% (Table 6). 82 WESTERN NORTH AMERICAN NATURALIST [Volume 60 = 0.1 = 0.6 = 0.6 = 0.6 = 1.7 = 1.1 = 3.4, = 3.4, Save Arfr Atco Atco Arca Arca Arfr Arfr = 1.1 = 3.4 = 0.6 = 0.6 Atco Atco Atga Atga = 0.1, = 2.2, = 0.6, = 0.6, = 2.2, = 3.4, = 5.6, = 5.6, Other shrubs Atga Save Save Atga Atga Atga Chvi Rowo a ) –2 — 1.1 — d Artr Chna Eula Seeding rates (kg ha c ifolia, Chna = Chrysothamnus nauseosus, Chvi viscidiflorus, Atca ) for study sites from 8 mines in 4 geographic locations of Wyoming. ) for study sites from 8 mines in 4 geographic locations of Wyoming. –2 — —— — — 3.9 — 1.1 3.9 2.2 1.1 2.2 24.4 6.729.1 2.2 5.6 — — 1.1 2.2 1.1 — 1.1 ______grasses forbs b e e e e 1984 19811984 19.5 2.8 — — 0.6 1.7 — 1984 1984 Area Year(s) Seeding All All IG SAGEBRUSH Arca = Artemisia cana, Arfr frigida, Artr tridentata, Atca Atriplex canescen, Atco confert /B 4. method, plant species selected, and seeding rates (kg ha Seeding year, ABLE Kemmerer #2Kemmerer #3Kemmerer Bridger Coal #1 3.0 37.7 6.5 1980 1981 1981 D D & B D 19.5 15.7 15.7 2.8 — — — 2.2 2.2 — 0.3 0.3 0.6 — — 1.7 — — — — — Seminoe I 7.7 1984 D 16.8 — 1.7 0.3 0.6 0.6 Kemmerer #1Kemmerer 36.5 1980 D 15.7 — 2.2 — — — — T Black Thunder Belle AyrPathfinderSeminoe I 26.3 #1WyoDak 1981 2.0 15.8Dave Johnston 22.7 D & B 1981 1977 1984 4.5 23.9 21.3 D D 1982 Unk. 1981Bridger Coal #2 — D & B 28.0 Unk. 16.8 D & B 1.1 15.1 33.2 Unk. 5.3 — 20.2 — 1980 2.2 0.6 3.4 1.7 1.1 — 1.1 — B — — 0.6 — — 0.6 0.1 0.6 13.4 0.6 3.4 — 1.1 0.6 — — — 2.2 0.6 0.6 — — — — — WyoDak #2WyoDak Pathfinder 4.5 21.5 1984 1982 D & B D 16.1 15.1 0.6 2.2 5.6 2.2 0.6 1.1 3.4 — OURWING OURWING Bulk seed, not pls D = drilled, B broadcasted Interseeded on same plot, different year(s) from original seeding Plant symbols: Pure live seed (pls) unless otherwise noted Eula = Eurotia lanata, Rowo Rosa woodsii, Save Sarcobatus vermiculatus F SitesF (ha) seeded method a b c d e 2000] SHRUB ESTABLISHMENT ON RECLAIMED MINED LANDS 83

TABLE 5. Summary of shrub plant community characteristics for fourwing saltbush/grass reclaimed mined sites. Mean Mean Mean height covera density Importance Diversity Site (cm) (%) (plants m–2) value index

BLACK THUNDER 0.033 Artemisia tridentata 11.0 ≤0.01 ≤ 0.01 Atriplex canescens 71.7 ± 19.8b 5.3 ± 0.4 0.10 ± 0.04 2.00 All shrubs 41.4c ± 20.1 5.3d 0.10d BELLE AYR 0.060 Atriplex canescens 74.3 ± 23.2 1.9 ± 0.3 0.14 ± 0.07 1.99 Eurotia lanata 34.0 ± 2.8 ≤0.01 0.01 All shrubs 54.1 ± 23.7 1.9 0.14 PATHFINDER 0.053 Artemisia tridentata 10.5 ± 2.4 ≤0.01 0.01 Atriplex canescens 41.1 ± 16.8 2.7 ± 0.4 0.12 ± 0.09 1.99 All shrubs 25.8 ± 17.0 2.7 0.12 SEMINOE I 1.428 Artemisia tridentata 11.6 ± 10.4 ≤0.1 0.01 0.12 Atriplex canescens 65.7 ± 24.9 2.5 ± 0.3 0.06 ± 0.04 1.43 Chrysothamnus spp. 28.1 ± 10.1 ≤0.01 0.02 Gutierrezia sarothrae 35.9 ± 10.8 ≤0.1 ≤0.01 0.03 Atriplex confertifolia 37.3 ± 12.7 0.2 ± 0.2 0.01 0.14 Sarcobatus vermiculatus 87.0 ± 30.5 0.6 ± 0.6 0.01 0.25 All shrubs 44.3 ± 30.4 3.4 0.09 KEMMERER #1 0.066 Artemisia tridentata 27.7 ± 9.7 ≤0.01 ≤0.01 Atriplex canescens 51.5 ± 24.6 15.7 ± 0.5 0.69 ± 0.17 1.99 Gutierrezia sarothrae 23.9 ± 7.7 0.01 0.01 Atriplex confertifolia 14.3 ± 13.3 ≤0.01 ≤ 0.01 Sarcobatus vermiculatus 94.0 ≤0.01 ≤0.01 All shrubs 42.3 ± 24.9 15.7 0.70

MEAN (ALL SITES) 41.6 5.8 0.23 0.328 aFrom line-intercept sampling techniques (Canfield 1941) bStandard deviation cMean of mean shrub species heights dSum of mean shrub species cover and density

Fourwing saltbush was clearly the major only fourwing sites at Black Thunder and component of canopy cover on fourwing sites Kemmerer #1 provided cover needs of ante- (Table 5). Although big sagebrush was not lope, 5.3% and 15.7%, respectively (Tables 1, included in the original seed mixture of these 5). Total shrub cover on fourwing/sagebrush sites (Table 4), it occurred at Black Thunder, sites at WyoDak #1 and #2 and Bridger Coal Pathfinder, Seminoe I, and Kemmerer #1 #1 and #2 was marginally adequate when (Table 5). Big sagebrush apparently immi- considering minimal preferred habitat require- grated and successfully colonized these sites, ments of 5% (Tables 1, 6). Based on Cook’s presumably from adjacent native plant com- (1984) guidelines for Wyoming, only the Kem- munities. merer #1 fourwing site and Bridger Coal #2 On 6 fourwing/sagebrush sites (WyoDak fourwing/sagebrush site had enough cover for #1, WyoDak #2, Dave Johnston, Seminoe I, antelope when considering total shrub cover Kemmerer #2, and Bridger Coal #1), big (Tables 1, 5, 6). sagebrush was the largest contributor to over- With regard to sage grouse habitat, Kem- all shrub canopy cover (Table 6). However, merer #1 and Black Thunder fourwing sites Pathfinder, Kemmerer #3, and Bridger Coal offered enough canopy cover (15.7% and 5.3%, #2 (fourwing/sagebrush) sites were dominated respectively) to meet requirements for general by fourwing saltbush. Fourwing saltbush was use (Tables 2, 5). But, since both sites were originally included in the seed mixture of dominated by fourwing saltbush and sage these sites. grouse are closely associated with big sage- When comparing percent shrub cover to brush, habitat characteristics of the Kemmerer preferred habitat requirements, we found that #1 and Black Thunder fourwing sites are 84 WESTERN NORTH AMERICAN NATURALIST [Volume 60

Table 6. Summary of shrub plant community characteristics for fourwing saltbush/big sagebrush/grass reclaimed mined sites. Mean Mean Mean height covera density Importance Density Site (cm) (%) (plants m–2) value index

WYODAK #1 0.857 Artemisia tridentata 64.1 ± 31.1b 7.4 ± 0.4 0.45 ± 0.3 1.65 Atriplex canescens 13.0 ≤0.01 ≤0.01 Artemisia frigida 14.1 ± 10.0 ≤0.1 0.08 ± 0.1 0.14 Eurotia lanata 28.7 ± 19.5 ≤0.01 ≤0.01 Artemisia cana 28.5 ± 14.8 0.4 ± 0.6 0.11 ± 0.2 0.21 All shrubs 29.7c ± 32.2 7.8d 0.64d WYODAK #2 0.940 Artemisia tridentata 32.9 ± 12.7 4.7 ± 0.4 0.37 ± 0.3 1.43 Artemisia frigida 17.0 ± 8.8 0.9 ± 0.2 0.24 ± 0.1 0.55 Chrysothamnus spp. 64.0 ≤0.01 ≤0.01 Gutierrezia sarothrae 16.2 ± 4.9 0.01 0.02 Rosa woodsii 84.0 ≤0.01 ≤0.01 All shrubs 39.1 ± 13.7 5.6 0.62 PATHFINDER 0.731 Artemisia tridentata 10.0 ± 4.0 ≤0.1 0.03 0.20 Atriplex canescens 50.7 ± 25.1 4.0 ± 0.5 0.11 ± 0.1 1.74 Artemisia frigida 7.3 ± 3.8 ≤0.01 0.01 Eurotia lanata 22.0 ± 11.6 0.01 0.04 Chrysothamnus spp. 6.4 ± 2.3 ≤0.01 0.01 Atriplex confertifolia 37.0 ± 4.5 0.1 ≤0.01 0.01 All shrubs 22.2 ± 27.7 4.1 0.15 DAVE JOHNSTON 1.398 Artemisia tridentata 19.9 ± 6.9 0.6 ± 0.1 0.16 ± 0.1 0.90 Atriplex canescens 20.2 ± 9.9 ≤0.1 ≤0.01 0.02 Artemisia frigida 9.5 ± 5.6 0.3 ± 0.1 0.31 ± 0.2 0.93 Eurotia lanata 23.4 ± 19.8 0.1 ± 0.1 0.04 0.16 Chrysothamnus spp. 20.5 ± 7.8 ≤0.01 ≤0.01 Gutierrezia sarothrae 23.0 ± 12.7 ≤0.01 ≤0.01 All shrubs 19.4 ± 10.5 1.0 0.51 SEMINOE I 1.116 Artemisia tridentata 46.1 ± 26.8 2.2 ± 0.3 0.17 ± 0.2 1.49 Atriplex canescens 82.3 ± 28.3 0.7 ± 0.4 0.01 0.27 Chrysothamnus spp. 32.9 ± 27.6 0.3 ± 0.2 0.03 0.24 Gutierrezia sarothrae 35.7 ± 4.5 ≤0.01 0.01 Sarcobatus vermiculatus 25.3 ± 31.1 ≤0.01 0.01 All shrubs 44.5 ± 28.8 3.2 0.21

probably undesirable for sage grouse (Table 5). study sites, with the exception of Kemmerer Only 1 fourwing site, Kemmerer #1, had suffi- #1 fourwing and Bridger Coal #2 fourwing/ cient cover for sage grouse nesting and brood sagebrush sites, provided only minimal cover rearing (Tables 2, 5). No site supported enough for antelope and sage grouse. Shrub reclama- winter cover for sage grouse. tion guidelines in Wyoming focus solely on Fourwing/sagebrush sites at WyoDak #1 shrub density to evaluate successful reclama- and #2 and Bridger Coal #1 and #2 also had tion. Research findings (Postovit 1981, Cook enough canopy cover for general use by sage 1984, Nydegger and Smith 1984, Roberson grouse (Tables 2, 6). However, only 1 fourwing/ sagebrush site, Bridger Coal #2, provided 1984) emphasize that shrub cover is equally as enough shrub cover for nesting and brood important as shrub density when evaluating rearing (Tables 2, 6). No site provided enough reclaimed mined land for wildlife habitat and winter cover for sage grouse. should be considered to provide a full assess- Shrub cover is an extremely important ment of the reclaimed site in meeting wildlife component of wildlife habitat quality. These habitat needs. 2000] SHRUB ESTABLISHMENT ON RECLAIMED MINED LANDS 85

Table 6. Continued. Mean Mean Mean height covera density Importance Density Site (cm) (%) (plants m–2) value index

KEMMERER #2 0.133 Artemisia tridentata 59.9 ± 25.3 2.2 ± 0.4 0.09 ± 0.1 1.97 Amelanchier alnifolia 14.0 ≤0.01 0.01 Chrysothamnus spp. 37.5 ± 10.6 ≤0.01 0.02 Gutierrezia sarothrae 24.0 ± 7.0 ≤0.1 ≤0.01 ≤0.01 All shrubs 33.9 ± 25.6 2.2 0.09 KEMMERER #3 0.777 Artemisia tridentata 41.9 ± 20.8 0.4 ± 0.6 0.02 0.19 Atriplex canescen 64.9 ± 28.4 4.3 ± 0.4 0.18 ± 0.2 1.72 Chrysothamnus spp. 31.4 ± 10.5 0.2 ± 0.2 0.01 0.07 Gutierrezia sarothrae 16.4 ± 3.5 ≤0.01 0.01 Artemisia tripartata 18.3 ± 4.3 ≤0.01 0.01 All shrubs 34.6 ± 29.1 4.9 0.21 BRIDGER COAL #1 1.505 Artemisia tridentata 34.6 ± 15.6 4.1 ± 0.4 1.71 ± 1.0 1.39 Atriplex canescens 38.5 ± 24.7 0.5 ± 0.4 0.02 0.07 Eurotia lanata 19.2 ± 10.0 ≤0.1 ≤0.01 ≤0.01 Chrysothamnus spp. 18.2 ± 15.4 0.1 0.02 0.03 Gutierrezia sarothrae 21.4 ± 12.7 ≤0.1 0.01 0.01 Atriplex confertifolia 36.3 ± 15.3 0.6 ± 0.3 0.02 0.08 Atriplex gardnerii 11.8 ± 5.7 2.0 ± 0.3 0.12 ± 0.1 0.30 Sarcobatus vermiculatus 43.7 ± 36.5 0.9 ± 0.3 0.02 0.12 All shrubs 28.0 ± 19.3 8.3 1.92 BRIDGER COAL #2 1.398 Artemisia tridentata 32.9 ± 14.5 1.4 ± 0.4 0.77 ± 0.6 0.80 Atriplex canescens 55.4 ± 41.5 10.7 ± 0.7 0.27 ± 0.1 1.05 Chrysothamnus spp. 21.3 ± 11.0 0.01 0.01 Gutierrezia sarothrae 16.2 ± 12.1 ≤0.1 ≤0.01 0.01 Atriplex confertifolia 29.8 ± 17.7 0.8 ± 0.6 0.04 0.09 Atriplex gardnerii 13.2 ± 11.5 0.4 ± 0.2 0.02 0.04 All shrubs 28.1 ± 33.7 13.3 1.11

MEAN (ALL SITES) 31.1 5.6 0.61 0.984 aFrom line-intercept sampling techniques (Canfield 1941) bStandard deviation cMean of mean shrub species heights dSum of mean shrub species cover and density

Density highest among all shrub species on fourwing/ sagebrush sites except Pathfinder, Dave John- Densities among dominant shrub species ston, and Kemmerer #3 (Table 6). Fourwing varied considerably between and among saltbush densities were greater on Pathfinder reclaimed mine sites, while densities of sub- and Kemmerer #3 sites, while fringed sage- dominant species were consistently low. Den- brush had the highest density on the Dave sities for all shrubs in the 5 fourwing sites Johnston site (Table 6). –2 –2 ranged from 0.09 m to 0.70 m , with a No site within the fourwing reclamation mean of 0.23 m–2 (Table 5). For the 9 four- type exhibited the minimal big sagebrush den- wing/sagebrush sites, densities for all species sity required by sage grouse. Only 1 site in the ranged from 0.09 m–2 to 1.92 m–2, with a fourwing/sagebrush reclamation type, Bridger mean of 0.61 m–2 (Table 6). Coal #1, had sufficient big sagebrush densi- Fourwing saltbush displayed the highest ties (1.92 m–2) for sage grouse (Table 6). How- density of any shrub species on fourwing sites ever, >90% of big sagebrush plants measured (Table 5), while big sagebrush density was at Bridger Coal #1 were seedlings <10 cm in 86 WESTERN NORTH AMERICAN NATURALIST [Volume 60 height and therefore did not represent high- higher percentages of forbs and shrubs (Table quality sage grouse habitat at that time. If this 2), these reclaimed mine sites are less desir- plant density persists over time, it should then able. produce desirable habitat. Despite high grass seeding rates on all study sites (Table 4), Booth et al. (1999) found Shrub Height no correlation between shrub density and Shrub heights varied greatly between grass seeding rates. Schuman et al. (1998) also species within and among study sites. Mean reported no differences in big sagebrush shrub heights for all species on 5 fourwing seedling density when grasses were seeded at sites ranged from 25.8 to 54.1 cm, with an 16 and 32 kg ha–1 pls. However, big sagebrush overall mean of 41.6 cm (Table 5). For 9 four- seedling density was significantly greater wing/sagebrush sites, mean shrub heights for when seeded without grass. all species were 19.4–44.5 cm, with an overall When evaluating mean percent vegetative mean of 31.1 cm (Table 6). Mean heights of big composition of fourwing sites against pre- sagebrush varied from 10.0 to 64.1 cm, while ferred standards of 40% grasses, 20% forbs, fourwing saltbush heights ranged from 13.0 to and 5% shrubs for antelope (Table 1), we 82.3 cm across sites. found that only Pathfinder satisfies antelope Big sagebrush heights at Kemmerer #1 habitat requirements (Table 7). Likewise, of averaged 27.7 cm (Table 5). All other fourwing fourwing/sagebrush sites, only WyoDak #1 sites had big sagebrush heights <22 cm rec- had sufficient vegetation composition pre- ommended for antelope (Table 1). Among four- ferred by antelope. The absence of forbs in all wing/sagebrush sites, 7 of 9 had mean big sage- sampled revegetated communities is the pri- brush heights greater than the preferred height, mary factor contributing to an unbalanced veg- but 5 of those sites were within Cook’s (1984) etation composition. No fourwing or fourwing/ optimum range of 22–46 cm (Tables 1, 6). sagebrush site met the minimal preferred Kemmerer #1 was the only fourwing site composition of 42.0% grasses, 28.4% forbs, providing sufficient big sagebrush height (27.7 and 29.6% shrubs for sage grouse (Table 2). cm) to offer nesting and summer or winter Importance Values habitat for sage grouse (Tables 2, 5). Eight of 9 fourwing/sagebrush sites provided sufficient Importance values provide a quantitative nesting (17 cm) and summer (18 cm) habitat approach to identify plant community domi- for sage grouse (Tables 2, 6). Seven of 9 four- nants (Curtis and McIntosh 1951). Dominant wing/sagebrush sites provided sufficient big species highly preferred by wildlife for food sagebrush heights for winter habitat. Only the and cover enhance wildlife habitat quality. Pathfinder site, with a mean big sagebrush Fourwing sites were dominated by four- height of 10 cm, did not meet the minimal wing saltbush with importance values ranging height for sage grouse. from 1.43 to 1.99 (Table 5), while other shrub species were subdominants. Among 9 four- Vegetative Composition wing/sagebrush sites, big sagebrush domi- Grasses dominated the vegetative composi- nated WyoDak #1 and #2, Seminoe I, Kem- tion on all fourwing and fourwing/sagebrush merer #2, and Bridger Coal #1 sites with sites except Bridger Coal #2 site (Table 7). importance values of 1.65, 1.43, 1.49, 1.97, and Considering that 67% of the total antelope 1.39, respectively (Table 6). Fourwing saltbush population in North America occupies grass- dominated Pathfinder, Kemmerer #3, and lands and highest antelope densities occur on Bridger Coal #2 sites and exhibited impor- grasslands (Yoakum 1978), these reclaimed mine tance values of 1.74, 1.72, and 1.05, respec- sites may be important for antelope from a tively. The Dave Johnston site reflected a shrub vegetation composition standpoint. Yoakum community dominated equally by fringed (1984a) reported that Bear Valley in central sagebrush and big sagebrush with importance Oregon supported the highest antelope doe: values of 0.93 and 0.90, respectively. fawn ratios of anywhere in the state after herbi- According to Sundstrom et al. (1973), pre- cides and mechanical practices changed preferred shrub species for antelope in Wyoming treatment grass composition from 10–40% to sagebrush-grassland steppe ecosystems are big 50–70%. However, for sage grouse requiring sagebrush, sand sagebrush (Artemisia filifolia), 2000] SHRUB ESTABLISHMENT ON RECLAIMED MINED LANDS 87

TABLE 7. Mean vegetative composition (%) of fourwing saltbush/grass and fourwing saltbush/big sagebrush/grass reclaimed mine sites.

______Mean composition (%) Site Grass Forb Shrub

FOURWING SALTBUSH/GRASS Black Thunder (20)a 82.9 ± 20.4b 0.4 ± 1.4 16.7 ± 20.4 Belle Ayr (5) 94.2 ± 7.1 5.0 ± 5.6 0.8 ± 1.8 Pathfinder (20) 67.9 ± 15.4 23.5 ± 16.2 8.6 ± 16.1 Seminoe I (20) 87.9 ± 16.8 0.0 12.1 ± 16.8 Kemmerer #1 (20) 56.9 ± 23.5 0.3 ± 1.2 42.8 ± 23.7 MEAN (ALL SITES) 77.9 5.8 16.2

FOURWING SALTBUSH/BIG SAGEBRUSH/GRASS WyoDak #1 (10) 48.5 ± 12.5 33.3 ± 15.7 18.2 ± 17.8 WyoDak #2 (10) 70.1 ± 19.3 15.9 ± 14.3 14.0 ± 17.0 Pathfinder (30) 87.0 ± 19.4 9.3 ± 16.2 3.7 ± 11.7 Dave Johnston (20) 92.8 ± 9.8 2.8 ± 4.6 4.4 ± 8.7 Seminoe I (20) 91.8 ± 11.8 3.6 ± 6.9 4.6 ± 9.9 Kemmerer #2 (20) 92.7 ± 11.9 1.2 ± 2.0 6.1 ± 10.8 Kemmerer #3 (20) 77.4 ± 25.4 5.7 ± 11.7 11.9 ± 18.4 Bridger Coal #1 (20) 45.3 ± 24.4 9.8 ± 13.6 44.9 ± 22.5 Bridger Coal #2 (20) 41.8 ± 24.6 8.0 ± 22.3 50.2 ± 25.6 MEAN (ALL SITES) 71.9 10.0 17.6 aNumber of transects sampled, 100 points per transect bStandard deviation

fringed sagebrush, silver sagebrush (Artemisia Seminoe I, Kemmerer #2, Bridger Coal #1, cana), and Douglas rabbitbrush (Chrysotham- and Dave Johnston sites are probably more nus viscidiflorus; Table 1). Four of 5 fourwing important for cover provided to sage grouse sites had only 1 of these preferred shrub and antelope since big sagebrush dominates species, big sagebrush (Table 5). In compari- the plant community composition. However, son, 4 fourwing/sagebrush sites had 3 pre- fourwing-dominated sites are valued for ferred species and 5 sites had 2 preferred highly palatable, nutritious forage provided to species (Table 6). Clearly, fourwing/sagebrush big game species. sites offered more preferred shrub species in Diversity Indices the community. From the standpoint of wildlife habitat qual- Shannon-Wiener diversity indices averaged ity, sites dominated by big sagebrush are espe- 3 times higher on fourwing/sagebrush sites cially important for sage grouse and antelope than on fourwing sites. Diversity indices on because this shrub species provides both year- fourwing sites ranged from 0.033 to 1.428, long food and cover for these wildlife species. with a mean of 0.328 (Table 5), and ranged In contrast, fourwing saltbush does not pro- from 0.133 to 1.505 on fourwing/sagebrush vide as much cover as big sagebrush, but it sites, with a mean of 0.984 (Table 6). This dif- does furnish highly palatable, nutritious forage ference is attributed to more shrub species in needed by big game. Cook (1972) reported the original seed mixtures of fourwing/sage- that average protein content for big sagebrush, brush sites compared to fourwing sites (Tables when evaluated over 4 seasons, was 11.2%. 4, 5, 6). Goodin (1979) reported mean protein content An individual site analysis showed that 4 of fourwing saltbush at 19.0% in a 2-yr green- fourwing sites had the lowest diversity indices house study, asserting that crude protein levels of all 14 study sites, while 8 fourwing/sage- were comparable to alfalfa (Medicago sativa). brush sites reflected the highest diversity Palatability of fourwing saltbush is good for indices (Fig. 1). Only the Kemmerer #2 four- several species of wildlife, with a digestibility wing/sagebrush site and Seminoe I fourwing of 63.5% (Northington and Goodin 1979). Based site displayed inconsistent patterns in diver- on these criteria, WyoDak #1 and #2, sity compared to other sites. Different initial 88 WESTERN NORTH AMERICAN NATURALIST [Volume 60 seed mixtures probably resulted in community prairie, his cover recommendations for the diversity differences between fourwing and sagebrush-grassland ecosystem were used to fourwing/sagebrush sites. evaluate our study sites for antelope. Numerous research studies have shown that Rather than reclamation practices, the greater reduction in big sagebrush and other range- time required by shrub species to reach maxi- land plants by burning, plowing, or 2,4-D mum canopy cover (Lommasson 1948) and applications results in decreases of wildlife possible browsing-induced mortality of big species richness, presumably due to decreases sagebrush from wild herbivores (McArthur et in plant species richness. Schroeder and al. 1988, Bilbrough and Richards 1993) may Sturges (1975), McAdoo and Klebenow (1978), account for low canopy cover on our sample and Castrale (1982) reported decreases in sites. Although shrub utilization by wild herbi- nongame bird species abundance as a result of vores was not a focus of this study, reclamation burning or plowing big sagebrush steppe. specialists may need to consider intensifying Sage grouse are negatively impacted by dras- wildlife damage control programs on newly tic reductions in big sagebrush cover and den- reclaimed areas, if browsing appears heavy, to sity by any method (Martin 1970, Wallestad enhance and successfully achieve shrub cover and Pyrah 1974, Swenson et al. 1987). Small requirements. mammal species abundance also decreases Shrub densities were also considered low when big sagebrush and other rangeland plants when evaluated against an extrapolation of the are reduced (Cook 1959, Johnson and Hansen reclamation regulation of 1 shrub m–2 on 20% 1969, Gashwiler 1970, Crowner and Barrett of the land (Federal Register 1996). These data 1979). However, Johnson et al. (1996) reported and information reported by Booth et al. (1999) that small mammal community diversity is also indicate that more shrub species in the positively correlated with plant community initial seed mixture improved shrub density. diversity. Considering these research findings, Some fourwing/sagebrush sites displayed en- the graphical representation of diversity indices couraging signs of increased shrub densities in Figure 1 indicates that higher shrub diver- by the presence of an age-stratified population. sity on fourwing/sagebrush sites may provide Shrub heights on fourwing/sagebrush sites more desirable wildlife habitat quality. were sufficient for both antelope and sage grouse, even providing enough winter cover CONCLUSIONS AND for sage grouse. In contrast, shrub heights on RECOMMENDATIONS fourwing sites were below minimal requirements for both antelope and sage grouse. This study evaluated long-term (>10 yr) The preferred compositions of grasses, forbs, shrub reestablishment success of pre-1985 and shrubs for antelope and sage grouse were reclamation practices and offers information to below minimal requirements on both reclama- enhance wildlife habitat and improve shrub tion types, due primarily to the absence of establishment and productivity in future recla- forbs. Original seed mixtures, which consisted mation. Sites selected for this investigation principally of grass and shrub species with are representative of pre-1985 era reclamation minimal forbs (Table 4), probably explain the methodologies and levels of success. These existing composition on reclaimed sites. How- sites demonstrate both reclamation inadequa- ever, Schuman et al. (1998) have shown that cies and successes which should be consid- big sagebrush establishment is significantly ered in future reclamation efforts. enhanced by limiting competition from herba- Individual shrub species canopy cover on ceous species. all sampled sites within the bunchgrass steppe Higher diversity indices on fourwing/sage- and those located on the western edge of the brush sites indicated that more species in the northern mixed-grass prairie (Hart 1994) was initial seed mixture enhanced plant commu- low, rarely exceeding 5%, when evaluated nity diversity, a highly desired characteristic against shrub cover recommendations for ante- for optimum wildlife habitat. Sites where more lope in sagebrush-grassland steppe ecosystems. shrub species were included in the initial seed Since our sites more closely resemble the mixture appeared to be progressing toward sagebrush-grassland ecosystem described by pre-mining vegetation conditions faster than Yoakum (1984a, 1984b) rather than shortgrass sites with fewer seeded shrub species. 2000] SHRUB ESTABLISHMENT ON RECLAIMED MINED LANDS 89

Fig. 1. Diversity indices for fourwing saltbush/grass (denoted by *) and fourwing saltbush/big sagebrush/grass reclaimed mined sites, 1994, Wyoming.

Inclusion of multiple species in the initial as shrub canopy cover, shrub height, commu- seeding mixture also enhanced overall cover, nity composition, and plant diversity, must be density, and diversity in reclaimed plant com- considered. munities, all important components of quality Comparisons of on-site shrub establish- wildlife habitat. However, with regard to ante- ment characteristics with published informa- lope and sage grouse, less than optimal shrub tion on habitat requirements of antelope and canopy cover, density, plant community com- sage grouse were not intended to provide spe- position, and diversity on these study sites cific benchmarks for evaluating reclamation suggest that a long time period or improved success, but rather to provide an initial, broad cultural methods will be required for reclaimed assessment of wildlife habitat quality where shrub communities to achieve desired wildlife none previously existed. There are no studies habitat characteristics similar to native sage- that relate quantitative wildlife population brush-grassland steppe ecosystems. Bond- characteristics (e.g., species richness, abun- release criteria requiring the reclaimed shrub dance, density, diversity) to reclaimed mined community to be similar to pre-mine condi- land plant community features (e.g., species tions within the 10-yr bonding period for this richness, canopy cover, density, standing crop region are unrealistic. Native shrub communi- biomass, diversity). ties may require 30–60 yr to develop through There are a number of interrelated biotic natural successional processes (Lommasson and abiotic environmental factors responsible 1948). for establishment and development of plant If one objective of mined land reclamation communities on reclaimed mined lands and, is to restore disturbed land to pre-mining con- subsequently, wildlife use of these areas. These ditions for wildlife habitat, then shrub density include site potential for vegetation develop- standards alone will not satisfy this objective. ment, original reclamation seeding mixtures, Other characteristics of wildlife habitat, such successional processes, disturbance factors 90 WESTERN NORTH AMERICAN NATURALIST [Volume 60

(e.g., grazing, fire), and post-seeding manage- LITERATURE CITED ment practices. For these reasons conclusions drawn from data in this study are limited to BILBROUGH, C.J., AND J.H. RICHARDS. 1993. Growth of sagebrush and bitterbrush following simulated win- precursory evaluations of shrub community ter browsing: mechanisms of tolerance. Ecology 74: characteristics for antelope and sage grouse 481–492. habitat quality. However, results from this BOOTH, D.T. 1985. The role of fourwing saltbush in mined study justify the need for future research land reclamation: a viewpoint. Journal of Range quantifying the relationship of wildlife popula- Management 38:562–565. BOOTH, D.T., J.K. GORES, G.E. SCHUMAN, AND R.A. OLSON. tion dynamics to reclaimed plant community 1999. Shrub densities on pre-1985 reclaimed mine characteristics. lands in Wyoming. Restoration Ecology 7:24–32. Future research should relate specific wild- BRAUN, C.E., T. BRITT, AND R.O. WALLESTAD. 1977. life population sample data (e.g., species rich- Guidelines for maintenance of sage grouse habitats. Wildlife Society Bulletin 5:99–106. ness, abundance, density, diversity) to various CANFIELD, R.H. 1941. Application of the line interception parameters of reclaimed mined land plant com- method in sampling range vegetation. Journal of munities (e.g., species richness, canopy cover, Forestry 39:388–394. density, standing crop biomass, diversity) to CASTRALE, J.S. 1982. Effects of two sagebrush control methods on nongame birds. Journal of Wildlife Man- better understand the function of these areas agement 46:945–952. as habitat for wildlife populations. Other indi- COCKRELL, J.R., G.E. SCHUMAN, AND D.T. BOOTH. 1995. rect wildlife use data, such as pellet counts, Evaluation of cultural methods for establishing forage utilization measurements, and fecal Wyoming big sagebrush on mined lands. Pages analysis for food habits information, should be 784–795 in G.E. Schuman and G.F. Vance, editors, Decades later: a time for reassessment. Proceedings included to further clarify the importance of of 12th Annual Meeting, American Society for Sur- reclaimed mined land for wildlife habitat value. face Mining and Reclamation, 5–8 June 1995, Additional research is also needed to prescribe Gillette, WY. Princeton, WV. initial seeding practices and post-seeding COOK, C.W. 1972. Comparative nutritive values of forbs, grasses, and shrubs. Pages 303–310 in C.M. McKell, management techniques that enhance wildlife J.P. Blaisdell, and J.R. Goodin, editors, Wildland habitat quality on these reclaimed areas. shrubs—their biology and utilization. USDA Forest Service, General Technical Report INT-1, Ogden, ACKNOWLEDGMENTS UT. 494 pp. COOK, J.G. 1984. Pronghorn winter ranges: habitat characteristics and a field test of a habitat suitability model. This work was supported in part by the Master’s thesis, University of Wyoming, Laramie. Abandoned Coal Mine Lands Research Pro- COOK, S.F., JR. 1959. The effects of fire on a population of gram at the University of Wyoming. Support small rodents. Ecology 40:102–108. was administered by the Wyoming Department CROWNER, A.W., AND G.W. BARRETT. 1979. Effects of fire on the small mammal component of an experimental of Environmental Quality from funds returned grassland community. Journal of Mammalogy 60: to Wyoming from the Office of Surface Mining 803–813. of the U.S. Department of Interior. CURTIS, J.T., AND R.P. MCINTOSH. 1951. An upland forest Authors thank the following mines and their continuum in the prairie-forest border region of reclamation specialists for cooperating in this Wisconsin. Ecology 32:476–496. DOBKIN, D.S. 1995. Management and conservation of sage study: Belle Ayr (Amax Coal West, Inc.), Black grouse, denominative species for the ecological Thunder (Thunder Basin Coal Co.), Bridger health of shrubsteppe ecosystems. USDI, Bureau of Coal (Bridger Coal Co.), Dave Johnston (Glen- Land Management, Portland, OR. 26 pp. rock Coal Co.), Kemmerer Coal (Pittsburg & FEDERAL REGISTER. 1996. Office of Surface Mining and Enforcement. 30 CFR, Part 95 D. Wyoming Regula- Midway Coal Mining Co.), Pathfinder (Path- tory Program—final rule; approval of amendment. finder Mines Corp.), Seminoe I (Arch Miner- Volume 61(152):40735. U.S. Government Printing als), and WyoDak (WyoDak Resources Devel- Office, Washington, DC. opment Corp.). We also thank Dr. Gary V. FOILES, M.W. 1974. Atriplex. Pages 240–243 in C.S. Schopmeyer, technical coordinators, Seeds of woody Richardson, statistician, USDA-ARS, Fort plants in the United States. Agricultural Handbook Collins, Colorado, for experimental design and 450. USDA, Forest Service, Washington, DC. statistical analysis assistance. Appreciation is GASHWILER, J.S. 1970. Plant and small mammal changes extended to Dr. Ed Redente, Dr. Carl Wam- on a clearcut in west-central Oregon. Ecology 51: boldt, Dr. Fred Lindzey, Paige Smith, and 1018–1026. GOODIN, J.R. 1979. The forage potential of Atriplex Chet Skilbred for their critical reviews of this canescens. Pages 418–424 in J.R. Goodin and D.K. manuscript. Northington, editors, Arid land plant resources. Pro- 2000] SHRUB ESTABLISHMENT ON RECLAIMED MINED LANDS 91

ceedings of International Arid Lands Conference on Conference on Plant Resources, July 1979, Interna- Plant Resources, July 1979, International Center for tional Center for Arid and Semi-Arid Land Studies, Arid and Semi-Arid Land Studies, Texas Tech Uni- Texas Tech University, Lubbock. 724 pp. versity, Lubbock. 724 pp. NYDEGGER, N.C., AND G.W. SMITH. 1984. Prey populations Hart, R.H. 1994. Rangeland. Pages 491–501 in Encyclo- in relation to Artemisia vegetation types in south- pedia of agricultural science. Volume 3. Academic western Idaho. Pages 152–156 in Proceedings of the Press, San Diego, CA. symposium on the biology of Artemisia and Chryso- HENNESSY, J.T., R.P. GIBBENS, AND M. CARDENAS. 1984. thamnus, 9–13 July 1984, Provo, UT. USDA Forest The effect of shade and planting depth on the emer- Service, Intermountain Research Station, Ogden, UT. gence of fourwing saltbush. Journal of Range Man- OWENBY, J.R., AND D.S. EZELL. 1992. Monthly station nor- agement 37:22–24. mals of temperature, precipitation, and heating and HULET, B.V., J.T. FLINDERS, J.S. GREEN, AND R.B. MURRAY. cooling degree days, 1961–1990 for Wyoming. 1984. Seasonal movements and habitat selection of National Climatic Data Center, Asheville, NC. sage grouse in southern Idaho. Pages 168–175 in PIEPER, R.D. 1978. Measurement techniques for herba- Proceedings of symposium on the biology of Artemisia ceous and shrubby vegetation. New Mexico State and Chrysothamnus, 9–13 July 1984, Provo, UT. University, Las Cruces. 148 pp. USDA Forest Service, Intermountain Research Sta- PLUMMER, P.A., S.B. MONSEN, AND D.R. CHRISTENSEN. tion, Ogden, UT. 1966. Fourwing saltbush: a shrub for future game JOHNSON, D.R., AND R.M. HANSEN. 1969. Effects of range ranges. Publication 66-4, Utah State Department of treatment with 2,4-D on rodent populations. Journal Fish and Game. of Wildlife Management 33:125–132. POSTOVIT, B.C. 1981. Suggestions for sage grouse habitat JOHNSON, K.H., R.A. OLSON, AND T.D. W HITSON. 1996. reclamation of surface mines in northeastern Composition and diversity of plant and small mam- Wyoming. Master’s thesis, University of Wyoming, mal communities in tebuthiuron-treated big sage- Laramie. brush (Artemisia tridentata). Weed Technology Jour- ROBERSON, J.A. 1984. Sage grouse–sagebrush relation- nal 10:404–416. ships: a review. Pages 157–165 in Proceedings of the KINDSCHY, R.R., C. SUNDSTROM, AND J.D. YOAKUM. 1982. symposium on the biology of Artemisia and Chryso- Wildlife habitats in managed rangelands, the Great thamnus, 9–13 July 1984, Provo, UT. USDA Forest Basin of southeastern Oregon: pronghorns. USDA Service, Intermountain Research Station, Ogden, UT. Forest Service, General Technical Report PNW-145, SCALET, C.G., L.D. FLAKE, AND D.W. WILLIS. 1996. Intro- Pacific Northwest Forest and Range Experiment duction to wildlife and fisheries: an integrated Station, Portland, OR. 18 pp. approach. W.H. Freeman Co., New York. 512 pp. KREBS, C.J. 1989. Ecological methodology. Harper and SCHROEDER, M.H., AND D.L. STURGES. 1975. The effect Row, New York. 645 pp. on Brewer’s sparrow of spraying big sagebrush. LOMMASSON, T. 1948. Succession in sagebrush. Journal of Journal of Range Management 28:294–297. Range Management 1:19–21. SCHUMAN, G.E., D.T. BOOTH, AND J.R. COCKRELL. 1998. LONG, S.G. 1981. Fourwing saltbush (Atriplex canescens). Cultural methods for establishing Wyoming big Page 85 in Characteristics of plants used in western sagebrush on mined lands. Journal of Range Man- reclamation. Environmental Research and Technol- agement 51:221–228. ogy, Inc., Fort Collins, CO. 146 pp. SHAW, N., A. SANDS, AND D. TURNIPSEED. 1984. Potential MARTIN, N.S. 1970. Sagebrush control related to habitat use of fourwing saltbush (Atriplex canescens [Pursh] and sage grouse occurrence. Journal of Wildlife Man- Nutt.) and other dryland shrub accessions for upland agement 34:313–320. game bird cover in southern Idaho. Pages 24–40 in MARTNER, B.E. 1986. Wyoming climate atlas. University of A.R. Tiedemann, K.L. Johnson, E.D. McArthur, S.B. Nebraska Press, Lincoln. 432 pp. Monsen, and H. Stutz, compilers, Proceedings of the MCADOO, J.K., AND D.A. KLEBENOW. 1978. Native faunal biology of Atriplex canescens and related chenopodes. relationship in sagebrush ecosystems. Pages 50–61 USDA Forest Service, General Technical Report in The sagebrush ecosystem: a symposium. Utah State INT-172, Ogden, UT. University, Logan. SUNDSTROM, C., W.G. HEPWORTH, AND K.L. DIEM. 1973. MCARTHUR, E.D., A.C. BLAUER, AND S.C. SANDERSON. Abundance, distribution, and food habits of the 1988. Mule deer–induced mortality of mountain big pronghorn. Wyoming Game and Fish Department, sagebrush. Journal of Range Management 41:114–117. Bulletin 12, Cheyenne. 61 pp. MEYER, S.E. 2000. Artemisia. In: F. Bonner, editor, Woody SWENSON, J.E., C.A. SIMMONS, AND C.D. EUSTACE. 1987. plant seed manual. 3rd edition. USDA, Forest Service, Decrease in sage grouse Centrocercus urophasianus Washington DC. (In press). after ploughing of sagebrush steppe. Biological Con- MOGHADDAM, M.R., AND C.M. MCKELL. 1975. Fourwing servation 41:125–132. saltbush for land rehabilitation in Iran and Utah. WALLESTAD, R.O., AND D.B. PYRAH. 1974. Movement and Utah Science 36:114–116. nesting of sage grouse hens in central Montana. NGUGI, K.R., J. POWELL, F.C. HINDS, AND R.A. OLSON. Journal of Wildlife Management 38:630–633. 1992. Range animal diet composition in southcentral YOAKUM, J.D. 1978. Pronghorn. Pages 103–121 in J.L. Wyoming. Journal of Range Management 45:542–545. Schmidt and D.L. Gilbert, editors, Big game of North NORTHINGTON, D.K. AND J.R. GOODIN. 1979. Atriplex America. Wildlife Management Institute, Washing- canescens as a potential forage crop introduction ton, DC. into the Middle East. Pages 425–429 in J.R. Goodin ______. 1980. Habitat management guides for the Ameri- and D.K. Northington, editors, Arid land plant can pronghorn antelope. USDI, Bureau of Land resources. Proceedings of International Arid Lands Management, Technical Note 347, Denver, CO. 77 pp. 92 WESTERN NORTH AMERICAN NATURALIST [Volume 60

______. 1984a. Pronghorn habitat requirements and recla- YOUNG, J.F., AND P.C. SINGLETON. 1977. Wyoming general mation. Symposium on Surface Coal Mining and soil map. Research Journal 117. University of Wyo- Reclamation in the Great Basin, 19–21 March 1984, ming, Agricultural Experiment Station, Laramie, WY. Billings, MT. ______. 1984b. Use of Artemisia and Chrysothamnus by Received 23 March 1998 pronghorns. Pages 176–180 in Proceedings of the Accepted 6 November 1998 symposium on the biology of Artemisia and Chryso- thamnus, 9–13 July 1984, Provo, UT. USDA Forest Service, Intermountain Research Station, Ogden, UT. Western North American Naturalist 60(1), © 2000, pp. 93–97

WOOD AND UNDERSTORY PRODUCTION UNDER A RANGE OF PONDEROSA PINE STOCKING LEVELS, BLACK HILLS, SOUTH DAKOTA

Daniel W. Uresk1, Carleton B. Edminster2, and Kieth E. Severson1

ABSTRACT.—Stemwood and understory production (kg ha–1) were estimated during 3 nonconsecutive years on 5 growing stock levels of ponderosa pine including clearcuts and unthinned stands. Stemwood production was consistently greater at mid- and higher pine stocking levels, and understory production was greater in stands with less pine; however, there were no differences in total (stemwood + understory) production. Based on loss of productivity, there is no argument that small clearcuts and unthinned stands should not be included in site plans. They contribute significantly to community structure, particularly to plant and animal species richness.

Key words: ponderosa pine, growing stock levels, stemwood production, understory production.

Forage and timber are 2 important products of ponderosa pine ranging from no trees to un- derived from ponderosa pine (Pinus ponderosa) thinned stands. Two size classes at the beginning forests. These commodities are, however, com- of the study in 1974 included pine saplings petitive. As tree parameters (basal area, den- (7.6–10.2 cm dbh) and poles (15.2–17.9 cm sity, or canopy cover) increase, forage in the dbh). Results of this study will enable man- understory decreases. As a result, studies on agers to contrast wood and forage production overstory-understory relationships have been and develop a better understanding of site rigorously pursued (Ffolliott and Clary 1982). productivity. Preliminary results were provided Ponderosa pine is the dominant tree in the by Severson and Boldt (1977). Black Hills of South Dakota and Wyoming. Well adapted to the environment of the Black STUDY AREA AND METHODS Hills, this pine produces regular seed crops in a moist regime that favors seedling establish- This study was conducted in the Black Hills ment. Harvested or burned stands are typically on the Black Hills Experimental Forest, about replaced by dense stands of pine seedlings 30 km west of Rapid City, South Dakota. The which eventually form crowded thickets (Boldt experimental forest encompasses approximately and Van Duesen 1974). Relationships between 1375 ha and ranges in elevation from 1620 to overstory and understory have been investi- 1800 m. Average annual precipitation is 600 gated in the Black Hills (Pase 1958, Bennett et mm, of which 70% falls from April to Septem- al. 1987, Uresk and Severson 1989). The pri- ber. Temperature averages 3°–9°C, and the mary objective in an earlier publication (Uresk growing season ranges from 80 to 140 d. Soils and Severson 1989) was to develop linear or are primarily gray wooded, shallow to moder- curvilinear models to describe relationships ately deep, and derived from metamorphic between overstory and understory. In a later rock. The environment of the Black Hills is publication we reported responses of individ- described by Boldt et al. (1983). Vegetation of ual understory species to changes in the pine the experimental forest is dominated by the overstory (Uresk and Severson 1998). Pinus ponderosa/Arctostaphylos uva-ursi habi- The purpose of this paper is to compare rel- tat type as described by Hoffman and Alexan- ative quantities of wood and forage produced der (1987) and Thilenius (1972). Mean fire under a range of tree stocking levels. Data were interval for the Black Hills between 1388 and collected from 5 different growing stock levels 1900 was 16 yr ± 14 (s) (Brown and Sieg 1996).

1USDA Forest Service, Rocky Mountain Research Station, Center for Great Plains Ecosystem Research, South Dakota School of Mines and Technology Campus, Rapid City, SD 57701. 2USDA Forest Service, Rocky Mountain Research Station, Southwest Forestry Science Complex, Flagstaff, AZ 86001.

93 94 WESTERN NORTH AMERICAN NATURALIST [Volume 60

We sampled 5 growing stock levels (GSL) 1978 to 1983. To facilitate comparisons with of ponderosa pine including small clearcuts understory production, we converted wood and unthinned stands (Uresk and Severson volume to oven-dried wood weight by applying 1989, 1998) These were numerically desig- locally developed models (Myers 1960, 1964). nated 0, 5, 14, 23, and unthinned (UT). Grow- Wood volume was first converted to dry weight ing stock indicates all living trees in a stand. with the following model: W = 25.0688(V) Growing stock level is the basal area (m2 ha–1) – 3.0096, where W is the oven-dried weight of of a stand adjusted to account for differences merchantable bole in pounds and V is the cor- in average size of trees left in the stand after responding volume in cubic feet, r2 = 0.98. thinning. Therefore, the numerical designation Once these values were obtained, we used the of GSL approximates but does not necessarily following equations to obtain oven-dried wood equal the basal area. Three replications of weight: V = 0.002297 D2H – 1.032297 for each of the 5 GSLs were established in each of D2H to 6700; V = 0.002407 D2H – 2.257724 2 size classes of pine, saplings and poles. Each for D2H larger than 6700 where D = diame- replication in the sapling stands was 0.10 ha, ter at breast height (dbh) outside bark (inches) and pole stands were each 0.20 ha, established and H = height in feet. Diameter breast high in a completely randomized design. Thirty for both sapling and pole plots in 1974 at the stands were sampled for both size classes. beginning of the study ranged from 7.6 to 19.9 Basal areas of unthinned pole stands ranged cm per site. Hence, comparisons are annual from 37 to 40 m2 ha–1 in 1981; unthinned sap- increments, on an oven-dried basis, of total ling stands ranged from 27 to 33 m2 ha–1. Plots aboveground understory (graminoids, forbs, were initially thinned in 1963 except 0 level, and shrubs) and stemwood of ponderosa pine which was cleared in 1966. We rethinned plots (bark, branches, and needles excluded). and removed seedlings at 5-yr intervals to Years and stand types were analyzed sepa- maintain original GSLs. rately using 1-way analysis of variance. Het- Production of understory vegetation was erogeneous variances precluded simultaneous measured during August 1974, 1976, and 1981 analysis. Significantly different means were separated using Tukey-HSD. Those data sets on six 15-m randomly placed transects per exhibiting heterogeneous variances were ana- plot (Uresk and Severson 1989, 1998). Twelve lyzed via post-hoc pairwise permutation tests 30 × 61-cm quadrats were randomly located with type I error maintained for each set of along each transect in 1974 and 1976. These tests using a Bonferroni adjustment (Miller data indicated that an increase in number of 1981, Meilke 1984). All statistical inferences quadrats would provide a better estimate of were made at a probability level of 0.05. minor plant species. Therefore, in 1981 we systematically located 25 circular plots mea- RESULTS suring 0.125 m2 each along 5 of the transects. Current annual growth of all herbage was har- Generally, understory production was high- vested at ground level for each species. All est where no trees were present and decreased leaves and terminal portions of twigs to the 1st with increasing GSL. It was least in unthinned node were clipped on shrubs, also by species, stands (Table 1; see also Uresk and Severson after which we oven-dried the material at 1989). More specifically, GSLs 0 and 5 pro- 60°C for 48 h and then weighed it. Weights duced significantly more understory than GSLs were averaged and expressed as mean per plot 23 and UT, but GSL 14 was often comparable for data analyses. to both groups. Understory production tended Total aboveground biomass production was to be greater in sapling stands than in pole estimated during August 1974, 1976, and 1981. stands, but differences were not significant Tree growth was estimated immediately post- (Uresk and Severson 1998). treatment 1963 and in 1968, 1973, 1978, and Annual stemwood production was generally 1983. Data for each specified year represent low in GSL 5 (Table 1) and in clearcuts. Pro- average annual growth over the interval period; duction in these 2 levels was often lower than that is, wood production data for 1974 is the GSLs 14, 23, and UT. No differences were evi- average annual production from 1968 to 1973; dent among the 3 higher GSLs. No differences for 1976, from 1973 to 1978; and 1981, from in wood production were noted in 1981 pole 2000] WOOD AND UNDERSTORY PRODUCTION, BLACK HILLS 95

TABLE 1. Annual stemwood and understory production (kg ha–1, oven-dried) sampled at 3 different years in sapling and pole-sized ponderosa pine stands each managed at 5 different growing stock levels.

______Growing stock level (GSL) Year Category 0 5 14 23 UT1

------Sapling-sized stands ------74 Understory 1112a2 1152ab 555bc 397c 98c 74 Stemwood 0a 475b 1193bc 1304c 1626c 74 Total 1112 1627 1748 1701 1748

76 Understory 2006a 2200a 1295ab 767b 340b 76 Stemwood 0a 552ab 1646c 2032c 1348bc 76 Total 2006ab 2752ab 2941a 2799ab 1689b

81 Understory 2449a 2279a 1476ab 952b 333b 81 Stemwood 0a 807ab 1964c 2023c 1348bc 81 Total 2449ab 3086ab 3440a 2974ab 1681b ------Pole-sized stands ------74 Understory 997a 625b 386bc 202c 73d 74 Stemwood 0a 998b 1647c 1834c 1543bc 74 Total 997a 1622ab 2034b 2036b 1616ab

76 Understory 1931a 1522ab 1179ab 756bc 112c 76 Stemwood 0a 836b 1733c 1991c 1022bc 76 Total 1931ab 2359a 2912a 2747a 1135b

81 Understory 2551a 1618b 1121b 640c 41d 81 Stemwood 0a 934b 1891cd 1949d 1022bc 81 Total 2551 2552 3012 2588 1063

1Unthinned stands 2Numbers within rows followed by different letters are significantly different (P = 0.05).

stands, again despite a range of no production DISCUSSION in GSL 0 to 1949 kg ha–1 in GSL 23. Pole stands tended to produce more wood than Increases of ponderosa pine, even at mini- sapling stands at GSL 5 and UT, but amounts mal levels, will reduce the amount of under- were nearly similar at other GSLs. story and therefore the available forage pro- Differences in combined production of duced. This is particularly important for live- wood and understory were generally similar stock and elk (Cervus elaphus) since grami- among GSLs (Table 1). Exceptions were in 1981 noids and forbs are among the 1st species to decrease and even disappear under increased sapling stands where total production was levels of pine (Uresk and Severson 1998). For- higher in GSL 14 (3440 kg ha–1) than in UT age for mule deer (Odocoileus hemionus) and (1681 kg ha–1) and in 1976 pole stands where –1 while-tailed deer (O. virginianus) is not as dra- GSLs 5, 14, and 23 (2359–2912 kg ha ) pro- matically affected. Although several forbs and –1 duced more than UT (1135 kg ha ). Although shrubs present in open stands decrease in not significant, there was a tendency for lower abundance, others, such as bearberry manzanita production values in GSLs 0 and UT compared (Arctostaphylos uva-ursi) and cream peavine with intermediate levels. Relative contribu- (Lathyrus ochroleucus), maintain levels or even tions of wood and understory to total produc- increase under a mid-range of pine stocking tion changed as GSL increased. More under- levels (Uresk and Severson 1998). Stemwood story than wood was produced at GSLs 0 and production is significantly curtailed at lower 5, but wood production was greater in the stocking levels, and a stand is not fully stocked remaining 3 higher GSLs (Table 1). until levels approach 14 m2 ha–1. Others have 96 WESTERN NORTH AMERICAN NATURALIST [Volume 60 reported that it is about 9 m2 ha–1 (Clary et al. LITERATURE CITED 1975). The lack of significance among fully stocked stands indicates that unthinned stands, BENNETT, D.L., G.D. LEMME, AND P. D . E VENSON. 1987. Understory herbage production of major soils within as defined herein, produce as much stemwood the Black Hills of South Dakota. Journal of Range as those stocked at lower levels (14–23 m2 Management 40:166–170. ha–1). BOLDT, C.E., R.R. ALEXANDER, AND M.J. LARSON. 1983. It is impractical to recommend a stocking Interior ponderosa pine in the Black Hills. Pages 80–83 in R.M. Burns, technical compiler, Silvicul- level of ponderosa pine that “optimizes” all ture systems for the major forest types of the United forest outputs in the Black Hills. If commodi- States. USDA Forest Service Handbook. USDA, ties such as livestock and timber production Washington, DC. were the only considerations, intermediate BOLDT, C.E., AND J.L. VAN DUESEN. 1974. Silviculture of stocking levels would likely offer an accept- ponderosa pine in the Black Hills: the status of our knowledge. USDA Forest Service, Research Paper able balance. However, recent emphasis on RM-124, Rocky Mountain Forest and Range Experi- ecosystem management, an approach that con- mental Station, Fort Collins, CO. 45 pp. siders ecosystem health, maintenance of nat- BROWN, P.M., AND C.H. SIEG. 1996. Fire history in interior ural systems, and economic and social needs, ponderosa pine communities of the Black Hills, mandates that all facets of the forest system be South Dakota, USA. Journal of Wildland Fire 6(3): 97–105. considered. Arguments have been presented CLARY, W.P., W.H. KRUSE, AND F.R. LARSON. 1975. Cattle that suggest a range of ponderosa pine stand grazing and wood production with different basal stocking levels are necessary to maintain a areas of ponderosa pine. Journal of Range Manage- viable forest ecosystem. ment 28:434–437. FFOLLIOTT, P.F., AND W. P. C LARY. 1982. Understory-over- Uresk and Severson (1998), for example, story vegetation relationships: an annotated bibliog- noted that while floristic diversity in pine raphy. USDA Forest Service, General Technical stands was greatest at lower GSLs, total floris- Report INT-136, Intermountain Forest and Range tic diversity was greater if all stocking levels, Experiment Station, Ogden, UT. 39 pp. including 0 and UT, were present. Similarly, HOFFMAN, G.R., AND R.R. ALEXANDER. 1987. Forest vegetation of the Black Hills National Forest of South many wildlife species including white-tailed Dakota and Wyoming: a habitat type classification. deer, turkey, and small birds use a range of for- USDA Forest Service, Research Paper RM-276, est structures within the pine community Rocky Mountain Forest and Range Experiment Sta- (Rumble and Anderson 1993, Mills et al. 1996, tion, Fort Collins, CO. 48 pp. Sieg and Severson 1996). This study supports MEILKE, P.W., JR. 1984. Meteorological applications of permutation techniques based on distance functions. the results of Clary et al. (1975), who found Pages 813–830 in P.R. Krishnaiah and P.K. Sen, edi- that lower pine stocking levels produced maxi- tors, Handbook of statistics. Volume 4. Elsevier Sci- mum forage for livestock while intermediate ence Publishing Company, Amsterdam. levels produced more wood fiber. MILLER, R.G., JR. 1981. Simultaneous statistical inference. There was a tendency for less total produc- 2nd edition. Springer-Verlag, New York. 299 pp. MILLS, T.R., M.A. RUMBLE, AND L.D. FLAKE. 1996. Evalu- tion on clearcuts and unthinned stands because ation of a habitat capability model for nongame birds of the absence of wood production on the for- in the Black Hills, South Dakota. USDA Forest Ser- mer and lack of understory and decrease in vice, Research Paper RM-RP-323, Rocky Mountain wood growth on the latter, but significant dif- Forest and Range Experiment Station, Fort Collins, CO. 30 pp. ferences were rare; hence, there is no strong MYERS, C.A. 1960. Estimating oven-dried weight of pulp- argument (based on loss of productivity) that wood in standing ponderosa pine stands. Journal of these levels should not be included in site plans. Forestry 58:889–891. Their value is magnified by contributions they ______. 1964. Volume tables and point-sampling factors make, in concert with other stands, to commu- for ponderosa pine in the Black Hills. USDA Forest Service, Research Paper RM-8, Rocky Mountain For- nity structure, particularly plant and animal est and Range Experiment Station, Fort Collins, CO. species richness. We therefore suggest that 16 pp. forest managers focus not on specific stocking PASE, C.P. 1958. Herbage production and composition levels to maximize forest productivity but under immature ponderosa pine stands in the Black rather on how a variety of stocking levels Hills. Journal of Range Management 11:238–243. RUMBLE, M.A., AND S.H. ANDERSON. 1993. Macrohabitat could be arranged in spatial and temporal associations of Merriam’s Turkey in the Black Hills, mosaics to optimize community structure. South Dakota. Northwest Science 67:238–244. 2000] WOOD AND UNDERSTORY PRODUCTION, BLACK HILLS 97

SEVERSON, K.E., AND C.E. BOLDT. 1977. Options for Black Rocky Mountain Forest and Range Experiment Sta- Hills forest owners: timber, forage, or both. Range- tion, Fort Collins, CO. 28 pp. man’s Journal 4(1):13–15. URESK, D.W., AND K.E. SEVERSON. 1989. Understory- SIEG, C.H., AND K.E. SEVERSON. 1996. Managing habitats overstory relationships in ponderosa pine forests, for white-tailed deer in the Black Hills and Bear Black Hills, South Dakota. Journal of Range Man- Lodge Mountains, South Dakota and Wyoming. agement 42:203–208. USDA Forest Service, General Technical Report ______. 1998. Managing species in the understory of pon- RM-GTR-27400, Rocky Mountain Forest and Range derosa pine in the Black Hills. Great Basin Natural- Experiment Station, Fort Collins, CO. 24 pp. ist 58:312–327. THILENIUS, J.F. 1972. Classification of deer habitat in the ponderosa pine forest of the Black Hills, South Dakota. Received 9 December 1998 USDA Forest Service, Research Paper RM-91, Accepted 7 April 1999 Western North American Naturalist 60(1), © 2000, pp. 98–100

REPRODUCTION IN THE TWIN-SPOTTED RATTLESNAKE, CR0TALUS PRICEI (SERPENTES: VIPERIDAE)

Stephen R. Goldberg1

Key words: reproduction, Crotalus pricei, twin-spotted rattlesnake.

The twin-spotted rattlesnake, Crotalus pricei, Not all tissues were available for histologi- occurs in mountainous terrain of southeastern cal examination due to damage or autolysis, Arizona (Pinaleño, Graham, Dos Cabezas, Santa but the following were examined: 9 ovaries, 19 Rita, Huachuca, and Chiricahua Mountains) testes, 18 kidneys, 14 vasa deferentia. and south in the Sierra Madre Occidental of There is no previous information on the C. México to southern Durango from around pricei testis cycle. Testicular histology was 1220 to 3200 m (Stebbins 1985). Because there similar to that reported by Goldberg and Parker is limited information on reproduction in this (1975) for 2 colubrid snakes, Masticophis tae- species (Ernst 1992), the purpose of this note niatus and Pituophis catenifer, and the viperid is to provide additional litter sizes and to pre- snake, Agkistrodon piscivorus, reported by sent data on the timing of yolk deposition, Johnson et al. (1982). In recrudescent testes ovulation, and testis cycle of C. pricei. there was renewal of spermatogenic cells Data are presented from 31 sexually mature characterized by spermatogonial divisions; C. pricei (12 females, mean snout-vent length primary and secondary spermatocytes and [SVL] = 400 mm ± 48 (s), range = 303–482 spermatids may have been present. In spermi- mm; 19 males, mean SVL = 433 mm ± 72 (s), ogenesis (which follows recrudescence), meta- range = 322–553 mm) and 1 litter of 7 morphosing spermatids and mature sperm neonates taken from the herpetology collec- were present. None of the C. pricei males had regressed testes. tions of Arizona State University (ASU), Nat- Males undergoing spermiogenesis were ural History Museum of Los Angeles County found June–October (Table 1). The smallest (LACM), and University of Arizona (UAZ), spermiogenic male measured 333 mm SVL, Tucson (Appendix). One of the above females although 1 male with recrudescent testes that gave birth to 4 young and was not a museum probably would have undergone spermiogene- specimen (D. Prival personal communication). sis measured 322 mm SVL. Males smaller than Counts were made of enlarged follicles (>6 this size (322 mm SVL) were excluded from mm length), oviductal eggs, or embryos. The the study to avoid the possibility of including left ovary was removed from females; the left immature specimens in analysis of the testis testis, vas deferens, and part of the kidney cycle. Testes in recrudescence were found were removed from males for histological June–August. Sperm were present in the vasa examination. Tissues were embedded in paraf- deferentia of 13/14 (93%) males including all fin and cut into sections at 5 µm. Slides were those from June–September, indicating C. pri- stained with Harris’ hematoxylin followed by cei has the potential for breeding throughout eosin counterstain. Testes slides were exam- this period. Because 6/7 (86%) July males had ined to determine stage of the male cycle; recrudescent testes and 7/8 (88%) late sum- ovary slides were examined for presence of mer–autumn males were undergoing spermio- yolk deposition. Vasa deferentia were exam- genesis, the C. pricei testicular cycle may fit ined for sperm. Slides of kidney sexual seg- the aestival spermatogenesis “D” and post- ments were examined for secretory activity. nuptial breeding pattern of Saint Girons (1982).

1Whittier College, Department of Biology, Whittier, California 90608.

98 2000] NOTES 99

TABLE 1. Monthly distribution of conditions in seasonal August and sacrificed 23 January (follicles testicular cycle of Crotalus pricei. Values shown are num- >10 mm length). Four females had already bers of males exhibiting each of the 2 conditions. ovulated (18 May, 7 June, 29 June, August, Month N Recrudescence Spermiogenesis LACM 2964, UAZ 30952, ASU 7031, UAZ June 4 2 2 47247, respectively) and likely would have July 7 6 1 given birth later that same year (Table 2). One August 3 1 2 female (LACM 104989) collected 7 July in September 4 0 4 Durango, México (SVL 375 mm), had a litter October 1 0 1 of 7 (mean SVL = 141 mm ± 4 s, range = 137–148 mm). It is not known whether the young were taken from the female or if she In this pattern spermatogenesis occurs from had given birth to them. One female gave June to October, with mating the following birth 17 August to 4 young a few days after spring using sperm stored overwinter in the capture (D. Prival personal communication). vasa deferentia, or during fall. Field observa- Young are born July–August (Lowe et al. tions of mating are needed to ascertain when 1986). C. pricei breeds. The above data on the female reproductive Kidney sexual segments were enlarged and cycle would lend support to the theory that C. contained secretory granules in 16/18 (89%) pricei has a biennial reproductive cycle with kidneys examined from June to October: 6/7 females generally reproducing every other (86%) males with recrudescent testes, 10/11 year as has been reported by Rahn (1942) for (91%) males with spermiogenic testes. Mating Crotalus viridis from southeastern Wyoming coincides with hypertrophy of the kidney sex- and Tinkle (1962) for Crotalus atrox from northwestern Texas. ual segment (Saint Girons 1982). Mean litter size for 7 C. pricei females The smallest reproductively active female (Table 2) was 5.1 ± 1.9 (s), range 3–8. This is (UAZ 30952) measured 330 mm SVL (oviductal within the 3–9 range reported by others for C. eggs). Three females (7 May, 11 June, 12 August; pricei (Kauffeld 1943a, 1943b, Stebbins 1954, UAZ 20642, UAZ 33963, LACM 134040, Wright and Wright 1957, Keasey 1969, Klauber respectively) were not undergoing yolk depo- 1972, Armstrong and Murphy 1979, Van sition (i.e., secondary vitellogenesis sensu Ald- Devender and Lowe 1979, Mahaney 1997). ridge 1979). Two of the above females (7 May While useful information on reproductive and 11 June) could have started yolk deposi- biology can be gathered from histological tion and ovulated the following year. The 3rd examination of museum specimens, field stud- (12 August) may have already given birth. Two ies on C. pricei are needed to reveal details of females, 1 from 6 July (UAZ 42075) and the the reproductive cycle. other from 27 September (LACM 75338) had started yolk deposition and may have ovulated I thank Charles H. Lowe (University of Ari- the next year. One female (UAZ 35463) had zona), Robert L. Bezy (Natural History Museum enlarged follicles and likely would have ovu- of Los Angeles County), and Michael E. Dou- lated the following year; it was collected 15 glas (Arizona State University) for permission

TABLE 2. Litter sizes for Crotalus pricei. Superscript letters indicate the following: c = captive born, e = embryos, f = enlarged follicles, o = oviductal eggs. SVL Litter Date (mm) size Locality Source

18 May 400 4o Cochise Co., AZ LACM 2964 7 June 330 4o Chihuahua, MX UAZ 30952 29 June 482 8e Graham Co., AZ ASU 7031 7 July 375 7c Durango, MX LACM 104989 August 430 3e Chihuahua, MX UAZ 47247 15 August 423 6f Chihuahua, MX UAZ 35463 17 August 441 4c Cochise Co., AZ D. Prival personal communication 100 WESTERN NORTH AMERICAN NATURALIST [Volume 60 to examine Crotalus pricei. David Prival (Uni- MAHANEY, P.A. 1997. Crotalus pricei (twin-spotted rattle- versity of Arizona) provided information on 1 snake). Reproduction. Herpetological Review 28:205. RAHN, H. 1942. The reproductive cycle of the prairie rat- litter size. Cheryl Wong assisted with histology. tler. Copeia 1942:233–240. SAINT GIRONS, H. 1982. Reproductive cycles of male snakes LITERATURE CITED and their relationships with climate and female reproductive cycles. Herpetologica 38:5–16. ALDRIDGE, R.D. 1979. Female reproductive cycles of the STEBBINS, R.C. 1954. Amphibians and reptiles of western snakes Arizona elegans and Crotalus viridis. Herpe- North America. McGraw-Hill Book Company, New tologica 35:256–261. York. 536 pp. ARMSTRONG, B.L., AND J.B. MURPHY. 1979. The natural ______. 1985. A field guide to western reptiles and history of Mexican rattlesnakes. University of Kansas, amphibians. Houghton-Mifflin, Boston. 336 pp. Museum of Natural History, Special Publication 5. TINKLE, D.W. 1962. Reproductive potential and cycles in 88 pp. female Crotalus atrox from northwestern Texas. ERNST, C.H. 1992. Venomous reptiles of North America. Copeia 1962:306–313. Smithsonian Institution Press, Washington, DC. 236 VAN DEVENDER, T.R., AND C.H. LOWE, JR. 1977. Amphib- pp. ians and reptiles of Yepómera, Chihuahua, Mexico. GOLDBERG, S.R., AND W. S. P ARKER. 1975. Seasonal testic- Journal of Herpetology 11:41–50. ular histology of the colubrid snakes, Masticophis WRIGHT, A.H., AND A.A. WRIGHT. 1957. Handbook of taeniatus and Pituophis melanoleucus. Herpetologica snakes. Volume 2. Comstock Publishing Associates, 31:317–322. Ithaca, NY. Pages 565–1105. JOHNSON, L.F., J.S. JACOB, AND P. T ORRANCE. 1982. Annual testicular and androgenic cycles of the cottonmouth Received 12 October 1998 (Agkistrodon piscivorus) in Alabama. Herpetologica Accepted 6 March 1999 38:16–25. KAUFFELD, C.F. 1943a. Field notes on some Arizona reptiles and amphibians. American Midland Naturalist 29:342–359. APPENDIX ______. 1943b. Growth and feeding of newborn Price’s and green rock rattlesnakes. American Midland Nat- Specimens examined from herpetology collections at uralist 29:607–614. the Natural History Museum of Los Angeles County KEASEY, M.S., III. 1969. Some records of reptiles at the (LACM) and the University of Arizona (UAZ). Arizona, Arizona-Sonora Desert Museum. International Zoo Cochise County: LACM 2964, 134040; UAZ 20642– Yearbook 9:16–17. 20643, 27657–27658, 27662, 42075, 42080–42081, 42084– KLAUBER, L.M. 1972. Rattlesnakes: their habits, life histo- 42086. Graham County: ASU 7031, 7047; UAZ 39586. ries, and influence on mankind. 2nd edition. Volume México, Chihuahua: LACM 75338; UAZ 30952, 33963, 1. University of California Press, Berkeley. 740 pp. 35080, 35234, 35463, 47247. Coahuila: UAZ 42556. LOWE, C.H., C.R. SCHWALBE, AND T.B. J OHNSON. 1986. The Durango: LACM 104986–104996, 136979. Nuevo Leon: venomous reptiles of Arizona. Arizona Game and Fish UAZ 46375. Department, Phoenix. 115 pp. Western North American Naturalist 60(1), © 2000, pp. 101–103

BOOK REVIEW

Contested Landscape. The Politics of Wilder- encyclopedic, one might question whether the ness in Utah and the West. Edited by editors checked all references for plagiarism. Doug Goodman and Daniel McCool. Uni- Having compared references used by students versity of Utah Press, Salt Lake City, UT. writing term papers, I know this is a tedious, yet 1999. $19.95, softcover; xvii + 266 pages. necessary process. Chapter 3 can be used as an example. Did the editors check for plagiarism all The origin of this book is most interesting. As 60 references listed? explained in the Preface (p. xiii), it grew out of a Some, but not all, chapters are well written. political science course, “The Politics of Wilder- Since it was apparent from the project’s incep- ness in Utah and the West,” taught by one of the tion that student contributions would make up editors. Students were required to author or co- most of the book, the editors should have given author a chapter of the book “based on original more direction to produce consistent organization research.” Contested Landscape, then, is really a of the chapters. Seven of the chapters, for instance, compilation of term papers. The 24 students, include both an introduction (or overview) and a singly or in teams of 2 or 3, wrote most of the conclusion, which one would expect of student book. It would be interesting to know how assign- term papers; 2 chapters have the introduction but ments were made. Did the student select his or no conclusion; 2 chapters have the conclusion but her coauthor(s) or were these assigned by the no introduction; and 3 chapters have neither professor? There must have been some degree of introduction nor conclusion. organization because the 4 sections (A Founda- Four maps are printed in Contested Landscape, tion of Facts; The Wilderness of Politics; Compe- 3 in chapter 7 and 1 in chapter 13. In the tition for Resources; and Lessons from the Past, reviewer’s opinion, these maps contribute little Proposals for the Future) each have meaningful to the book because they mostly lack definition. chapters. Assignments must have been made. Twenty tables are included in 10 chapters, but The Preface is authored by Daniel McCool; some of these simply take up space. the introduction to the 4 sections, each a 2-page An alphabetized list of 43 abbreviations is narrative, is authored by “The Editors”; and the found on pages ix and x. The editors stated that concluding chapter, The Community Context the “spell-checker could not recognize any of the Approach, is authored by Doug Goodman and acronyms listed at the beginning of the book” (p. Daniel McCool. The other 13 chapters are stu- 66 [emphasis added]). Most of these abbrevia- dent contributions. tions are NOT acronyms, but are initialisms. One would expect writing styles of the con- There are some abbreviations used in the text tributors to be diverse, and differences would be that are not included in this alphabetized list. expected in quality. In this reviewer’s 45 years of Usually the words to the abbreviation are given teaching college and university science courses parenthetically. However, the words to the acro- where students have been required to write term nym ANILCA (p. 104) could not be determined papers, it has become obvious that students write when it was first encountered. This reviewer had to impress the instructor who will ultimately grade to turn to the index to find the words explaining them at the end of the term. that acronym. Upon reading further, these words How much of the writing is original and in were discovered in the references section of that the author’s own words? In Contested Landscape chapter. it would appear from the list of references accom- The serious reader of this book would be panying each chapter that much of the material advised to memorize the abbreviations before is a compilation of previously published informa- ever attempting to read the chapters, or to tion. Students have been known to plagiarize. remove pages ix and x from the book to be used Inasmuch as the dialogue in many chapters is so as a handy reference while reading. Otherwise,

101 102 WESTERN NORTH AMERICAN NATURALIST [Volume 60 much of the text will not be understood. In one It would appear, then, that a wilderness area 9-line paragraph, 13 abbreviations are used (p. must be without roads. However, “neither the 52). This paragraph is quoted to illustrate how courts nor Congress have delineated a clear set meaningless the narrative becomes unless the of criteria that would define what constitutes a abbreviations are known. legal road. . . . Furthermore, since Congress has failed to define what a road is, states must use VERs in WSAs are protected by Section 701(h) their own definitions of what constitutes a road” of FLPMA and are subject only to the undue (pp. 181–182). This discussion is inconsistent. If degradation provisions of FLPMA. However, a wilderness area cannot have a tire track, how these restrictions may not unreasonably inter- can it have a road? What then is the purpose of fere with the benefit of existing rights, which usually consist of pre-FLPMA grazing rights the discussion on the definition of a road in and developed mining claims. A special VER terms of wilderness? exception does exist. The Director of the BLM First impressions of Contested Landscape may suspend pre-FLMPA VERs in a WSA when may be positive with the reader. The book is the President is expected to recommend a spe- clean with attractive type and printed on quality cial WSA for wilderness designation. Although paper; it is well organized and well referenced. Congress is expected to act quickly, the VERs Additionally, it would appear to be well written could be suspended for a maximum of two years and carefully edited. However, the concerns dis- (BLM 1995). cussed in this review show otherwise. Why is the word forgone repetitiously used 4 times in 9 In the Preface the editors state the purpose or lines of text (p. 210)? What is the meaning of the goal of the book is to compile the facts and word columnse in “These columnse 25,000 explain “the relevant laws, policies, court cases, acres” (p. 245)? Or is this merely a typographical and political activity . . . needed if the wilderness error not corrected? The editors “propose a spe- debate is ever going to move toward resolution.” cial commission to make formal proposals for One additional declaration states the book “is an wilderness designation” (p. 248). Note the repeti- effort to move the debate beyond the present tion in propose and proposals within the same stalemate.” This is an ambitious request that sentence. The people of these United States have likely will not be accomplished from reading been commissioned to death in recent years. Contested Landscape. It the last chapter the editors state, “The The controversy as to designation of wilder- wilderness debate is not about right or wrong; ness areas in Utah is apparent. It is printed it’s about needs and values” (p. 252), which state- almost daily in newspapers and magazines, is ment is also found on the back cover. If it’s deal- heard and seen frequently on radio and televi- ing in acreage that is either too small or too sion broadcasts, and is the subject of numerous large, it’s certainly dealing in right or wrong in books. This is another book to add to the list. the minds of taxpayers. Contested Landscape is about wilderness, an This reviewer, after reading and analyzing explanation of which is found on page 117. “For technical books written by professionals and cor- an area to be designated as wilderness, it must recting papers “authored” by college or univer- be roadless, have an acreage of five thousand sity students for well over half a century, has acres or more, be natural and without the finally discovered a book that is technically the imprint of man, and provide the opportunity for greatest challenge of all. Certainly a subtitle to solitude and/or primitive recreation.” (Note the Contested Landscape could well be written: Triv- repetition of acreage and acres within the space ium ad Infinitum or Nauseum ad Infinitum! of 5 words in the sentence. This is not good writ- Contested Landscape is not entertaining bed- ing.) It is very possible that no such area exists time reading. Don’t expect to see it on the best- anywhere. If a wilderness must be untouched by seller list in the near future. human hands, feet, or vehicle tires, it probably cannot be found. Directly or indirectly all land Andrew H. Barnum by this time has been contaminated by humans Professor Emeritus through overgrazing and introduction of noxious Department of Natural Sciences adventive weeds. The reference is made that Dixie State College “310 plant species . . . have been introduced into St. George, UT 84770 Utah” (p. 162). Can a plot of 5000 acres be found without noxious adventive weeds, footprints, or tire tracks? Western North American Naturalist

G UIDELINES

FOR

M ANUSCRIPTS

January 2000

Brigham Young University GUIDELINES FOR MANUSCRIPTS SUBMITTED TO THE WESTERN NORTH AMERICAN NATURALIST

JANUARY 2000 BRIGHAM YOUNG UNIVERSITY

We present the following information to provide authors with guidelines and examples to use in preparing manuscripts submitted to the WESTERN NORTH AMERICAN NATURALIST. Although this is not a comprehensive treatment, we believe the guidelines address some of the most common problems encountered by our authors. For more in-depth discussions, we recommend SCIENTIFIC STYLE AND FORMAT: THE CBE MANUAL FOR AUTHORS, EDITORS, AND PUBLISHERS, 6th ed. (ISBN 0-521-47154-0, Cambridge University Press, 110 Midland Avenue, Port Chester, NY 10573, USA; toll-free phone 1-800-872-7423.)

Manuscript Preparation Also, indicate the author to whom correspondence should be addressed if other than the 1st Using word processing software (our pref- author. erence is WordPerfect for Windows 6/7/8/9), type manuscripts so they print on standard • The title should be specific and concise bond (81/2 × 11 inches, 22 × 28 cm), leaving 1- (no longer than 15 words). It identifies inch (2.5-cm) margins on all sides. Submit 3 the article’s content or main topic rather hard copies to the Western North American than its conclusions. If appropriate, it Naturalist. (Authors should submit 5 copies of should include the name of the organ- manuscripts dealing with fish.) Diskettes are ism(s) involved. The use of order and not required until a manuscript has been family names for species that may be un- accepted for publication and all necessary familiar to many readers is appropriate. revisions made. To allow reviewers and editors sufficient space for notations, we require dou- • To avoid confusion, we recommend using ble-spacing throughout the manuscript—title full names of authors rather than initials. page, abstract, text, literature cited, appendixes, Omit academic degrees and profession- tables, and figure legends. We prefer that 12- al positions, but cite the department and point type be used in preparing the manuscript institution in which the research was done. If the present address differs from as this helps us more accurately estimate the the research institution, include the up- number of printed pages. Although we prefer dated address for correspondence and left justification, full justification is acceptable reprint requests. if the word-processing hyphenation feature is turned off. Number all pages consecutively. • Please provide a running head of fewer Manuscripts may be submitted as either than 40 letters and spaces. This is a scientific papers or notes, the major difference shorter, but nevertheless descriptive, being the lack of an abstract and headings version of the title; it will appear at the or subheadings in notes (see section under top of each right-hand page of the pub- Abstract). In addition, notes are generally lished article. shorter communications. Abstract. The abstract aids the reader in Title page. Included on the title page are comprehending the essence of the author’s the title; names, addresses, telephone numbers, research. It should state the objectives and and FAX numbers of authors; a running head; purpose of the study, methods and/or materials and footnotes to indicate change of address. used, results, and conclusions of the research.

104 2000] MANUSCRIPT GUIDELINES 105

If appropriate, scientific and common names • Study Site. It may be appropriate to of organisms should be included, with special include a description of the study area emphasis on new taxa or distribution records. in a separate section. This usually pre- Limit the abstract to approximately 250 words. cedes the methods section, but it may also be contained within that section. • Following the abstract are 6–12 key words, listed in order of decreasing • Methods. The methods section should importance, to be used for indexing. contain all information necessary for These words should reflect central topics other researchers to duplicate the study. of the article and may be from the title, Descriptions of the experimental or abstract, or text. Please list key words for sampling design should be clear to the both notes and articles. reader. Use a simple figure to present this information if it helps the reader Text. The significance of the text or, more understand the procedures. Another specifically, the author’s prose style, cannot be vital part of this section is a description underestimated. Ultimately, a scientific article of all statistical procedures used. must capture the reader’s attention by the importance of its content and its clarity of • Results. Results should be separate from expression. Chapter 6, Prose Style and Word the discussion. In this section state the Choice, in the CBE Style Manual offers help- results using text, figures, tables, or any ful suggestions for achieving succinctness and workable combination. This section is clarity, and avoiding verbiage and distressing not for interpretation of results. grammatical errors. Although frequently avoided, particularly • Discussion. The discussion is the forum in scientific articles, the active voice is the one in which study results are interpreted in which people usually speak and write. It is and compared with results from other perfectly acceptable and very useful in scien- studies. Interpretations should be con- tific writing. Not only is active voice (“We sistent with results, and they should determined”) less wordy and ambiguous than correspond with the stated purpose(s) passive voice (“It was determined”), but its of the research. use is also less likely to result in dangling par- We highly recommend the following article ticiples and other misplaced modifiers. When as one that is helpful to authors in writing and appropriate, use active voice. critiquing their own work: Verb tense is another area that deserves comment. Completed procedures and obser- KUYPER, B.J. 1991. Bringing up scientists vations are described in the past tense (“was,” in the art of critiquing research. Bio- “were”), but present tense is used when pre- Science 41:248–250. senting directions, conclusions, generaliza- tions, and references to stable or current con- Easily understood, effectively placed head- ditions. ings and subheadings help the reader quickly Because Western North American Natural- grasp the content and structure of the paper. ist articles cover diverse disciplines, we ask The Western North American Naturalist uses 3 our authors to avoid excessive use of unfamiliar levels of headings within textual material. acronyms, abbreviations, jargon, and overly technical vocabulary. Such terms hinder inter- • Primary headings are centered in all disciplinary understanding and prevent a free capital letters. These all-cap headings exchange of ideas. will, at typesetting, be converted to caps For maximum clarity, the body of the text and small caps. Authors can use the should be divided into the following sections. small caps feature on word processors if they wish. In general, primary headings • Introduction. The introduction need not should be restricted to STUDY AREA, be long, but it must adequately intro- MATERIALS AND METHODS, RESULTS, duce the research. At the end of the DISCUSSION, CONCLUSIONS, ACKNOWL- introduction, clearly state the purpose EDGMENTS, LITERATURE CITED, and of the research. APPENDIX, or variations of any of the 106 WESTERN NORTH AMERICAN NATURALIST [Volume 60

above. Do not use INTRODUCTION as a tively, American Midland Naturalist and West- heading; as the initial section, it logi- ern North American Naturalist. cally introduces the remainder of the As a general rule, too much bibliographical text. information is better than too little. Unneces- sary data can be deleted. • Secondary headings are centered in Following are examples of the most com- upper- and lowercase letters. mon types of bibliographic references. Please note that authors’ names are typed in upper- • Tertiary headings, set in caps and small and lowercase with no space between initials. caps using either method mentioned This format facilitates changing them at type- under primary headings, are indented setting to caps and small caps, our published from the left margin and followed by a style. However, if desired, the submitting period and a 1-em dash (the equivalent author can use the word processing small caps of 2 hyphens). Do not use secondary or feature. Please do not use standard all caps. tertiary headings unless major sections are long and/or the text is complex. In • Journals articles requiring only 2 levels of organization, tertiary headings should be Arcos, M.L., A. de Vicente, M.A. Morinigo, used directly below primary headings. P. Romero, and J.J. Borrego. 1988. Eval- uation of several selective media for Literature Cited. References to published recovery of Aeromonas hydrophila from literature and unpublished documents used in polluted waters. Applied and Environ- an article are cited in both the text and a sepa- mental Microbiology 54:2786–2792. rate bibliographic section. [Only the 1st author’s name is inverted; References in the text are cited by author use the 1st seven authors’ names and “et and date: Potter (1998) or (Potter 1998). Multi- al.” for papers with more than 7 authors.] ple citations should be listed in chronological order (Sigler and Sigler 1987, Wilson 1996, Eberharadt, L.E., R.G. Anthony, and W.H. Wilson and Belk 1996); commas are adequate Rickard. 1989. Survival of juvenile separators. In citations having more than 2 Canada Geese during the rearing per- authors, use “et al.” after the name of the 1st iod. Journal of Wildlife Management author (Parker et al. 1998). 53:372–377. [Issue numbers are not Use the heading LITERATURE CITED for the included unless each issue has indepen- list of references following the text. Include dent pagination; i.e., issue 1 is num- only references actually cited in the text. No bered 1–112, issue 2 is numbered 1–96, reference should be included unless pertinent etc. In such cases the issue, supple- publication facts have been verified against ment, or part number is also included the original document. Page numbers, for in parentheses after the volume num- example, seem to be particularly susceptible ber: 3(6):42–57, 56(supplement 4):8–13, to transposition errors. The responsibility for 2(3, part 4):2–15.] accuracy of reference material lies with the author, not the copy editor. Allen, K., and K. Hansen. 1999. [If the year The literature must be cited alphabetically of publication has not been determined, by author surname(s). Initials are usually suffi- use “In press” in place of the date.] cient for given names in this section. Chapter Geography of exotic plants adjacent to 30 in Scientific Style and Format contains gen- campgrounds, Yellowstone National Park, eral principles as well as examples of literature USA. Great Basin Naturalist: In press. citations. [Volume number and pagination are The Western North American Naturalist omitted for in-press citations.] does not abbreviate titles of periodicals and names of publishers (note that this is contrary • Books to CBE style). Include full titles as they appear on the title page but omit initial articles. The Bellrose, F.C. 1980. Ducks, geese and swans American Midland Naturalist and The Western of North America. 3rd edition. Stack- North American Naturalist become, respec- pole Books, Harrisburg, PA. 540 pp. 2000] MANUSCRIPT GUIDELINES 107

Snedecor, G.W., and W.G. Cochran. 1971. Literature citations of reports will not be Statistical methods. Iowa State Univer- used unless adequate information has been sity Press, Ames. [Repeating the state provided for the reader to readily locate the following the city seems redundant reference. inasmuch as the state is mentioned in the university name.] Appendixes. Long lists or material related only indirectly to the topic should be included • Parts of books in an appendix. Lists of specimens examined, for example, would be appropriate. Holden, P.B. 1991. Ghosts of the Green River: impacts of Green River on man- Tables. Tables are more costly than text to agement of native fishes. Pages 43–54 in typeset (even when submitted on diskette) and W.L. Minckley and J.E. Deacon, edi- therefore should be used only when they are tors, Battle against extinction: native deemed the most effective means of convey- fish management in the American West. ing information and summarizing data. If the University of Arizona Press, Tucson. data can be described in a few sentences within the text, do not present the information in a • Proceedings table. Tables should be self-explanatory. Title, headings, and footnotes must contain suffi- Mooers, G.B., and E.E. Willard. 1989. Crit- cient information for the reader to compre- ical environmental factors related to hend the data without referring to the text. success of spotted knapweed in western This will be achieved if the format is clear, Montana. Pages 126–135 in P.K. Fay and simple, and well organized. Also, tables of J.R. Lacey, editors, Proceedings of the similar information presented in similar or 1989 Knapweed Symposium, Montana parallel format will aid the reader. Chapter 31 State University, Bozeman. of the CBE Style Manual offers helpful suggestions on compiling, presenting, and condens- • Theses/Dissertations ing information in tabular formats. All tables should be numbered sequentially. Mullin, S.J. 1998. The foraging ecology of the Each table must be typed on a separate sheet(s), gray rat snake, Elaphe obsoleta spiloides given a complete, informative title, and referred Duméril, Bibron and Duméril. Doctoral to by number in the text. The title describes dissertation, University of Memphis, the topic or general trends shown in the table; Memphis, TN. it should also include species, localities, and dates of study when appropriate. Include the • Electronic Publications number of samples, i.e., n = 24, in the title or a column heading, whichever would be more See pages 665–669 in Scientific Style and helpful to the reader. Format for examples of various types of Make headings within tables brief and bibliographic entries. grammatically consistent with each other. Capitalize only the 1st word of column heads • Miscellaneous and items in row headings; do not use all uppercase letters. Footnotes to tables should Horton, J.S. 1977. The development and be kept to a minimum. One, 2, or 3 asterisks perpetuation of the permanent tamarisk (*) should be used for probability, P < 0.05, type in the phreatophyte zone of the 0.01, and 0.001, respectively. Lowercase let- Southwest. Pages 124–127 in R.R. John- ters are used to denote additional footnotes son and D.A. Jones, technical coordina- unless they might be confused with other data tors, Importance, preservation and within the table. In such cases numerals are management of riparian habitats: a sym- acceptable. posium. USDA Forest Service, General Finally, the smaller the table, the greater Technical Report RM-43, Fort Collins, the likelihood of its being printed near the CO. [Subtitles, including the 1st word, corresponding text. Two-column tables and are lowercase.] full-page tables printed vertically often are 108 WESTERN NORTH AMERICAN NATURALIST [Volume 60 several pages away from their reference in the black lines, it contains no grays. Graphs, text. diagrams, and charts fall into this category. Most line copy is now computer Figures. Well-designed and prepared illus- generated. Quality will vary, generally trative materials, whether photographs or depending on selection of fill patterns black-and-white artwork, not only augment and line width as well as required re- and clarify written material but also provide duction. If a chart or diagram is done by visual enhancement. On the other hand, hand, technical pens will give the most poorly prepared graphics may minimize the evenly weighted lines suitable for graphs author’s or journal’s credibility. and charts. Flexible pens and brushes In considering the addition of illustrations give smooth, tapered lines or softer, fuzzy to an article, be certain the text is long enough effects, respectively. to accommodate artwork. In general, 2 pages Although line copy does not contain of typescript are required for each figure or grays, the effect of gray areas can be table; we prefer 3 pages. When submitting an achieved on hand-drawn art by using article for review, please do not send original stippling, cross-hatching, or line con- photographs or black-and-white artwork; high- touring. Patterned screens with adhesive quality photocopies are adequate. backings are also used. Whether computer generated or hand • Computer-generated graphics, which drawn, black-and-white artwork should include photographs or line copy, are not be enlarged for publication as en- fairly easy to create and usually convert largement reveals and often magnifies well to the printed page. Adobe Photo- inconsistencies that may not be obvious shop files, 300–400 dpi and saved as on the original. Reductions should rarely TIF or EPS files, give excellent results. exceed 50%. It is important that all We can also accommodate charts and lines, symbols, and text be large enough graphs created using Microsoft Excel, on the original to withstand reduction Quattro Pro, Lotus, or common graph- and still maintain integrity and/or legi- ics programs. bility. If black-and-white artwork is scanned • Photographs, whether scanned at 300– and submitted on diskette, it must be 400 dpi and included on diskette or scanned in at 800 dpi for maximum submitted as originals, must have sharp clarity when printed. focus, a full range of tonal values, and • General considerations for illustrations: suitable contrast. Photographs that are slightly gray (low contrast) reproduce 1. For the sake of consistency, multiple better than those with high contrast pieces of artwork for 1 article or a (sharp blacks and whites). series of articles should be prepared, Photographs submitted as originals if possible, by the same artist. A uni- with the final manuscript upon accep- form reduction of multiple pieces tance by the Western North American will also aid consistency. Naturalist should be no larger than 22 × 28 cm. Ideally, the printed size will be 2. The general ratio of 2:3, in either a between 50% and 100% of original size. vertical or horizontal orientation, Smaller reductions tend to darken and will result in artwork compatible lose details. Photographs can also be with Western North American Natu- enlarged to about 150% of original size ralist page and/or column dimen- without adversely affecting quality. sions. Photomicrographs and electron micro- graphs should include a scale on the 3. Place necessary identifications, i.e., photograph or on an overlay. symbols, regression formulas, and scale bars, directly on the figure • Line copy is black-and-white artwork. rather than in the figure legend Prepared on a white background with whenever possible. 2000] MANUSCRIPT GUIDELINES 109

4. Use symbols for data points, partic- A Few Words About ularly on graphs. The most common Word Processing Formatting are , , , , , , ♦, ♦. The purpose of having authors submit man- 5. Identify all paper artwork on the uscripts on diskette is to simplify the work back. Using a soft blue or gray pen- done in our office and reduce the time and cil, mark author name and figure expense necessary to prepare manuscripts for number, and indicate “top.” publication. Following a few simple procedures from the outset will help immeasurably. General Style and Usage Conventions These procedures apply to manuscripts for- matted with WordPerfect but generally can be Provide the scientific name (genus and applied to other word processing software as species) of all organisms when first mentioned well. in the vernacular form in both abstract and • Begin each paragraph using the tab key text even if the name appears in the title. or paragraph styles feature (under For- Remember to use italics rather than underline. mat, Styles in WordPerfect) to indent. Do not use the space bar to simulate an Use a comma to separate elements (words, indent. phrases, or clauses) of a simple series of more than 2. A comma precedes the “and” or “or” • In LITERATURE CITED use hanging (e.g., blue grama, buffalograss, and needleleaf indents (under Format, Paragraph in sedge). WordPerfect). Do not use the space bar or indent key. Do not use boldface type in the manuscript. • Italicize P and r when expressing these values. The Western North American Naturalist follows Merriam Webster’s Tenth Collegiate Dic- • Use a lowercase italicized s for standard tionary for spelling and word-usage questions. deviation. Standard error of the mean is When 2 spellings are offered, we generally use sx–. the 1st. Also, consult a good unabridged dic- • Use WordPerfect characters from the tionary if necessary. Math/Scientific character set for the following symbols: In numbers consisting of 2 to 4 digits, run the numerals together: 1000 and 3959. Use 1. ° Degree symbol; not superscript comma separators for numbers of 5 or more o (“oh”) digits: 45,808. As a general rule, use numerals 2. ± Plus-minus; not underlined + rather than words for numbers. Two exceptions 3. ′ Minute symbol for latitude and are (1) at the beginning of a sentence and (2) longitude; not apostrophe where 2 numbers are adjacent within a sen- 4. ″ Seconds symbol for latitude and tence. In the latter case spell out the number longitude; not quotation mark easier to express in words and leave the other 5. ≤ Less than or equal to; not under- in numeric form (eight 50-g aliquots). lined < 6. ≥ More than or equal to; not Write dates with no punctuation: 16 August underlined > 1999. Standard abbreviations are acceptable for Most additional formatting questions can units of measure, directions and coordinates, be answered by checking recent issues of the statistical terms, and Latin terms (most of which Western North American Naturalist and fol- no longer require italics). Acronyms and other lowing examples within articles of similar sub- less common abbreviations should be defined ject matter or discipline. when first mentioned by writing out the term and enclosing the abbreviation in parentheses Since not all word processors are alike, please following the definition. mark on your diskette the type of computer 110 WESTERN NORTH AMERICAN NATURALIST [Volume 60

(PC or Mac) and word processor used. Pre- Throughout this book it is assumed that no ferred word processor is WordPerfect for Win- regulation contained therein is absolutely dows 6/7/8/9 for the PC. Microsoft Word for inviolable. . . . Each case . . . must largely be PC or Mac also works well. decided upon its own merits. Generally, it may be stated that, where no question of A Final Word good taste or good logic is involved, defer- ence should be shown to the expressed Although we agree that adhering to estab- wishes of the author. lished rules and maintaining a consistent style are hallmarks of good journalism, we also We thank you for choosing the Western agree with a statement in the preface to the North American Naturalist as a vehicle for University of Chicago’s first (1906) edition of a publishing results of your research. We hope Manual of Style: your experience with us will be a positive one. The 11th Annual Wildland Shrub Symposium will be held at Brigham Young University 13–15 June 2000. Sponsored by the Shrub Research Consortium and BYU Division of Continuing Education, the symposium theme will be Shrubland Ecosystem Genetics and Biodiversity.

Contributed oral and poster presentations are invited on shrubland ecosystem genetics and biodiversity as well as other aspects of shrubland biology and management. Submission deadline for abstracts (200 words or less) is 15 February 2000. Abstract should be sent to:

Dr. E.D. McArthur Shrub Sciences Laboratory Rocky Mountain Research Station 735 North 500 East Provo, UT 84606-1856 Phone: (801) 377-5717 E-mail: dmcarthur/[email protected]

Additional information, including abstract format, can be found on the following website: http://coned.byu.edu/cw/shrub

Among the special features included in the symposium is a field trip to southeastern Utah where the systematics, genetics, and diversity of native shrublands, especially chenopod shrublands, will be emphasized. The Natural Areas Association’s 27th Annual Conference will be held 16–20 October 2000 in St. Louis, Missouri. Managing the Mosaic: Connecting People and Natural Diversity in the 21st Century is the conference theme. The bicentennial celebration of the Lewis and Clark expedition is underway, and Dr. Daniel Botkin will discuss historical and future implications of the explorers’ journey. Plenary speakers include Dr. Peter Raven, director of the Missouri Botanical Garden, and Dr. William Burch, Yale University.

The conference, hosted by the Natural Areas Association and the Missouri Department of Conservation, will include symposia, contributed papers and poster sessions, social events, and business meetings. Field trips include excursions to various natural area in the Ozarks, cave visits, float trips on the Mississippi River, and walks on Missouri prairies.

To receive a registration packet or the call for papers, please contact: Natural Areas Conference 2000 Kate Leary, Conference Coordinator Missouri Department of Conservation PO Box 180 Jefferson City, MO 65102-0180 Phone: (573) 751-4115, ext. 183 E-mail: [email protected] Website: www.conservation.state.mo.us/nac Western North American Naturalist 60(1), © 2000, pp. 16–25