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Four-wing Saltbush (Atriplex canescens) Seed and Seedling Consumption by Granivorous Rodents
Four-wing Saltbush (Atriplex canescens) Seed and Seedling Consumption by Granivorous Rodents By Charlie D. Clements and Daniel N. Harmon
On the Ground
• Four-wing saltbush is an important browse species
• •
• •
for wildlife and domestic livestock and has been reported to provide as much as 11.4% to 13.6% crude protein. Granivorous rodents are important in the ecology of plant communities as well as the management practices that occur in those communities. In any land management practice that involves seeding in restoration or rehabilitation efforts, land managers must be cognizant of the role that biotic and abiotic factors ultimately have on the success and failures of these efforts. Abiotic factors such as poor seed germination or lack of proper amount and periodicity of precipitation are more well understood than biotic factors such as seed and seedling predation by granivorous rodents. Granivorous rodents in this study consumed as much as 55% and 99% of the four-wing saltbush seed and seedlings, respectively. Understanding the possible effects of rodent behavior with four-wing saltbush seed and seedlings should help resource managers in their planning and implementation of future rehabilitation/restoration efforts.
Keywords: seed predation, seedling predation, saltbush, granivorous rodents. Rangelands 39(6):182—186 doi 10.1016/j.rala.2017.10.002 © 2017 The Society for Range Management.
F
our-wing saltbush (Atriplex canescens [Pursh] Nutt.), native to western North America, extends from Canada to Mexico and from the Great Plains to the Pacific Coast. 1 Shrubby species of Atriplex are in the family Chenopodiaceae, which contains other important shrubs such as winter fat (Krascheninnikovia lanata Pursh), and often
182
dominate landscapes in many arid and semi-arid regions, particularly in habitats that combine high soil salinity with aridity. 1 Four-wing saltbush is an important browse species for wildlife and livestock 2 and has been reported to provide as much as 11.4 % to 13.6% crude protein. 3 The use of four-wing saltbush in restoration and land rehabilitation plantings is well documented 2,4–8 and increasingly popular. Granivorous rodents are important in the ecology of plant communities and the management practices that occur in those communities. 9–13 Granivorous rodents exhibit two types of seed-caching behavior: They cache some seeds in larders deep within their burrows, referred to as “larder hoarding,” and they cache some seeds in shallow depressions they dig throughout their home range, referred to as “scatter hoarding.” 14 Larder hoard caches are buried at depths that may allow germination but are most often too deep to sprout, 15 whereas scatter hoard caches that are not recovered are buried at depths that often promote germination and therefore have been found to be an important mechanism for the recruitment of various range plants. 12,13,16–19 In any land management practice that involves seeding in restoration or rehabilitation efforts, land managers must be cognizant of the role that biotic and abiotic factors ultimately have on the success and failures of these efforts. 20 Four-wing saltbush has been reported to experience variable success in seeding efforts, 21,22 with abiotic factors such as poor seed germination or lack of proper amount and periodicity of precipitation being fairly well understood. Biotic factors such as seed and seedling predation by granivorous rodents are less understood. Longland and Bateman 18 reported that the rodents in their study seldom cached four-wing saltbush seed, and it has also been reported that rodents damage young four-wing saltbush plants. 23,24 This study was initiated to address 1) the harvest, consumption, and caching of four-wing saltbush seed, and 2) the possible consumption of four-wing saltbush seedlings by granivorous rodents. We hypothesized that granivorous rodents in this study would harvest, consume, and cache a portion of the four-wing saltbush seed with which they interacted. We also hypothesized that four-wing saltbush seedlings would be consumed by granivorous rodents in this study.
Rangelands
Data Collection The study area is located in Desert Queen Valley (39°43'N, 118°59'W; elevation 1,257 m), 80 km northeast of Reno, Nevada. The valley was an embayment of pluvial Lake Lahontan, but the lake sediments are buried in sands that eroded from the delta of the Truckee River and are trapped in the valley in the lee of the Hot Spring Mountain Range. 17,25 The sands at the site are dominated by an overstory of four-wing saltbush, shadscale (Atriplex confertifolia [Torrey & Fremont] S. Watson), spotted dalea (Dalea polydemii S. Watson), Bailey’s greasewood (SarcoCov.), and winter fat, while the understory is dominated by Indian ricegrass (Achnathereum hymenoides [Roemer & Schultes] Beckworth), and Russian thistle (Salsola tragus L.). An active rain gauge at the site reveals the site receives 12 to 16 cm of precipitation from 1 October through 30 September annually. The rodent census/population part of the study was conducted twice per month for the duration of the study, from September 2013 through April 2014, using the mark-and-release live-trapping method with Sherman livetraps. 13,26 Fifty live-trap stations were established in which a grid of 5 transects were spaced 15 m apart with 10 stations per transect that were also placed 15 m apart. At each station 2 live-traps were set out (100 traps), baited with millet (Panicum spp.) seed in the evening, and checked the following morning. All captured animals were identified by species and sex, marked with a numbered ear tag, and released at the point of capture. Trapping took place for three consecutive nights 13,19 twice per month over the duration of the study. Investigation of rodent interaction with four-wing saltbush seeds was conducted using portable live-trap enclosures where consumption and caching of four-wing saltbush by various rodents was recorded. These portable live-traps, 60 × 30 × 35 cm, were constructed with solid plywood bottoms, fronts, and backs and were covered with 0.7 cm mesh hardware cloth. A hole was cut out of the front plywood panel to accommodate the placement of a Sherman live-trap, with the back door of the live-trap removed, to allow rodents to enter but not exit the enclosure. 13,26 The back plywood was removable to allow for the placement and removal of a 54 × 26 × 5 cm deep soil flat. A total of 12 portable enclosures (2 control enclosures permitted no access) were randomly placed on a 12-transect by 10-station grid. Each transect and station was at 15 m spacing. Enclosures were set out each evening at 1600 h and baited with 4 g of millet seed (620 seeds) in the live-trap. One hundred four-wing saltbush seeds, collected from the site the previous year, were placed on the surface of the soil in the soil flats. Soil in the soil flat was collected at the site and sieved free of any seed. Enclosures were checked the following morning at 0600 h. Enclosures with a rodent capture were dealt with first. Rodents were recorded by species and sex and tagged with a numbered ear tag; in the case of a recapture, the ear tag number was recorded. Cheek pouches were checked for any seeds, which were removed and recorded. Rodents were released at the point of capture. The number of visible seed on the surface was noted. The soil flat then was sieved and the number of seeds was recorded as un-cached, cached, or consumed. The portable enclosures were then reset and December 2017
randomly placed within the grid. This process took place for 5 consecutive mornings over 4 separate weeks from late September 2013 through early November 2013, coinciding with the timing of four-wing saltbush seed fall in the area. These portable enclosures were also used to investigate any four-wing saltbush seedling consumption by the various rodents at the site. Four-wing saltbush seedlings were grown in soil flats in soil from the site in a greenhouse environment. Twenty-five seedlings were grown in each flat and placed into the portable enclosures. Using the same transects as described above, portable enclosures were placed out at 1600 h each evening, baited with 4 g of millet seed inside the live-trap, and checked the following morning at 0600 h. Enclosures with rodents were dealt with first. Rodent species, sex, and ear tag number were recorded as described above, and the rodent released at the point of capture. Consumption of four-wing saltbush seedlings was recorded, as was any damage to seedlings not consumed (e.g., digging up). New soil flats with fresh four-wing saltbush seedlings were placed inside the enclosures and reset at randomly selected stations within the grid. This process took place for 5 consecutive mornings for 4 separate weeks from late March 2014 through late May 2014, coinciding with the timing of four-wing saltbush seedling sprouting at the site. Seeds and seedlings consumed were analyzed using SAS JMP 27 with species fixed and week and week × species as random. Tukey’s adjustment for multiplicity was used to make comparisons among the species (least square means).
Results A total of 5,400 trap nights were conducted during this study, resulting in a total of 132 captures of 59 separate individuals of 4 separate species. The species richness and diversity of the rodent population at this site, as represented through the live-trap data, indicated that the site was dominated by the Merriam’s kangaroo rat (Dipodomys merriami) (n = 34), followed by the chisel-toothed kangaroo rat (Dipodomys microps) (n = 13), desert kangaroo rat (Dipodomys deserti) (n = 8), and white-tailed antelope ground squirrel (Ammospermophilus leucurus) (n = 4). The trapping grid was 1 ha in size and therefore represents a minimum rodent population of 59/ha. This is based on the minimum known number alive method, but could result in an over- or underestimate due to rodents being trap shy and not being captured or rodents outside the grid being captured. 25 Investigation of rodents (n = 103) with four-wing saltbush seed in the portable enclosures revealed that none of the 103 rodents harvested four-wing saltbush seed in their cheek pouches or cached any seed in the portable enclosure. Therefore, there was no evidence that rodents were attempting to cache four-wing saltbush seed, although all 103 rodents in this study did harvest and store a portion of the millet seed available in their cheek pouches or mouth cavity 100% of the time. The rodent population did, however, consume fourwing saltbush seed, as they excavated the embryos from the seed coat (Fig. 1). The Merriam’s and desert kangaroo rat and the white-tailed antelope ground squirrel significantly
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99.25 ± 6.62 (n = 12), Merriam’s kangaroo rat 92.94 ± 3.00 (n = 51), and the chisel-toothed kangaroo rat 74.59 ± 5.01 (n = 23), even though millet seed was available as an alternative food source and the 4 g of millet seed available was never totally consumed. The chisel-toothed kangaroo rat consumed significantly (P ≥ 0.05) less four-wing saltbush seedlings than the Merriam’s and Desert kangaroo rat (Fig. 3). As one may expect, the disturbance caused by individual rodents varies as some of the four-wing saltbush seedlings are trampled; therefore, we only counted those seedlings that had clearly been foraged upon and consumed.
Figure 1. De-winging and excavation of four-wing saltbush seed by granivorous rodents.
(P ≤ 0.0001) consumed four-wing saltbush seed (Fig. 2). The desert kangaroo rat consumed the most four-wing saltbush seed (55.11 ± 3.22; n = 29), followed by the Merriam’s kangaroo rat (54.70 ± 2.20; n = 62), white-tailed antelope ground squirrel (34.33 ± 8.14; n = 5), and chisel-toothed kangaroo rat (13.63 ± 6.60; n = 7). The desert and Merriam’s kangaroo rat consumed significantly (P ≤ 0.05) more four-wing saltbush seed than the other two species, and the white-tailed antelope ground squirrel consumed significantly (P ≤ 0.05) more than the chisel-toothed kangaroo rat (Fig. 2). The chisel-toothed kangaroo rat, which consumes saltbush leaves, may rely less on seed consumption, thereby explaining the lower consumption of four-wing saltbush seeds by this species. Seeds in the control cages were all present and were not moved by ants, wind, or any other occurrence. White-tailed antelope ground squirrels were not observed in our portable enclosures during the seedling interaction period of the study. The remaining three rodent species that entered the portable enclosures (n = 86) at the site significantly (P ≤ 0.001) consumed four-wing saltbush seedlings (Fig. 3). The consumption of four-wing saltbush seedlings by these rodents was very high: The desert kangaroo rat consumed an average of
Figure 2. Mean number of four-wing saltbush seeds consumed per 100 available seeds. Different letters represent significant differences between species.
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Discussion and Implications From field observations, we suspected that four-wing saltbush seed would not be a preferred seed species for granivorous rodents because there is visual evidence of four-wing saltbush seed falling to the ground beneath shrubs and accumulating over time, which is not the case with seeds from preferred shrub species such as antelope bitterbrush (Purshia tridentata Pursh). 28 Previous research has found four-wing saltbush seed to be the least preferred whereas antelope bitterbrush seed was the most preferred seed for some rodent species. 29 Heavily utilized seed, such as antelope bitterbrush, is rapidly harvested by granivorous rodents as it falls to the ground, and the seed dispersal of this important shrub through rodent scatter hoard caching activity results in beneficial dispersal and recruitment of antelope bitterbrush shrubs. 12,13,16,28 Four-wing saltbush seed has a wind dispersal mechanism because the seed has large winged appendages, whereas antelope bitterbrush seed does not have an active wind dispersal system and relies heavily on rodent seed dispersal. We did, however, hypothesize that rodent species tested in this study would harvest and cache a portion of the four-wing saltbush seed with which they interacted. Even though the large wing structures of four-wing saltbush seed and the very hard seed coat would be considered deterrents for
Figure 3. Mean percent of four-wing saltbush seedlings consumed. Different letters represent significant differences between species.
Rangelands
granivory, we observed a high degree of de-winged seeds and embryo excavation on four-wing saltbush seed. We also hypothesized that granivorous rodents would graze on four-wing saltbush seedlings because our field experience has resulted in the observation of numerous species being grazed at the early seedling stages, such as antelope bitterbrush, 13,28 Indian ricegrass (Achnatherum hymenoides Roemer & Schultes), and winter fat. Some research has reported increased consumption of green vegetation in the diet of Merriam’s kangaroo rat during the summer months, with Atriplex species contributing to that diet. 30 It is important that these plant species are vigorous and healthy to experience good flowering and yield substantial seeds to the environment. The more seeds that are available to germinate and emerge, the less the total effect of rodent predation on the recruitment of seedlings to sustain the plant population. 13,31 Although this research was conducted using portable enclosures, granivorous rodents in this study avoided caching four-wing saltbush seed while still excavating the embryo from the seed. The seedling predation may well be higher than in natural conditions, but the fact that such a high level of seedling predation occurred when an alternative millet seed food source was available suggests a preference for these seedlings at this young phenology stage. This research found that four-wing saltbush seed is not highly preferred because the rodents at this site are not harvesting and caching the seed for future consumption. The high consumption of four-wing saltbush seedlings at this site is alarming, however, and may be an explanation for the poor success at given sites after the seeding of four-wing saltbush. The clipping of seedlings by granivorous rodents is more detrimental to shrub seedlings than grass seedlings due to the removal of the hypocotyl or epicotyl. 32 In the past three decades, numerous years have seen large wildfires that have burned millions of acres. For example, in 1999, more than 728,000 ha burned in Nevada alone, which resulted in the largest rehabilitation/restoration undertaking in state history. This rehabilitation/restoration effort resulted in the purchase of nearly 2.2 million kg of grass, forb, and shrub seed to be placed on the burned rangelands. 33 Four-wing saltbush seed was second only to Wyoming big sagebrush (Artemisia tridentata ssp. wyomingesis Beetle & A. Young) in desired shrub species in the 40,000 ha to be drill seeded and the more than 150,000 ha to be aerial seeded. The importance of four-wing saltbush for wildlife and domestic livestock as well as its role in improving functional plant communities only enhances the need to successfully rehabilitate/restore degraded rangelands. The results from this study would suggest that resource managers cannot depend on granivorous rodents to harvest, disperse, and cache four-wing saltbush seed; therefore, drill seeding of four-wing saltbush seed may be necessary to get the seed into the ground where it has a higher chance of germination and emergence. The fact that four-wing saltbush seedlings were consumed at a high level may suggest to resource managers that transplanting older seedlings could result in less seedling predation. Understanding the possible effects of rodent behavior with four-wing saltbush seed and seedlings should help resource December 2017
managers in their planning and implementation of future rehabilitation/restoration efforts.
References 1. MCARTHUR, E.D., AND S.C. SANDERSON. 1984. Distribution, systematics, and evolution of Chenopodiacea: An overview. In: Tiedemann AR, Mc Arthur ED, Stutz HD, Stevens R, & Johnson KL, editors. Proceedings-Symposium on Cheatgrass Invasion, Shrub Die-off, and other Aspects of Shrub Biology and Management. Ogden, UT, USA: USDA Forest Service, Intermountain Forest and Range Experiment Station. Gen. Tech. Rpt. INT-172. p. 12-24. 2. PLUMMER, A.P., S.B. MONSEN, AND D.R. CHRISTENSEN. 1966. Four-wing saltbush: A shrub for future game ranges. Pub. No. 66-4. Salt Lake City, UT, USA: Utah State Department of Fish and Game. 12 pp. 3. DAVIS, A.M. 1979. Forage quality of prostrate kochia with three browse species. Agronomy Journal 71:822-824. 4. BLAUER, A.C., A.P. PLUMMER, E.D. MCARTHUR, R. STEVENS, AND B.C. GIUNTA. 1976. Characteristics and hybridization of important intermountain shrubs. II. Chenopod Family. USDA Forest Service, Resource Paper INT-77. 42 pp. 5. VAN EPPS, G.A., AND C.M. MCKELL. 1978. Major criteria and procedures for selecting and establishing range shrubs as rehabilitators of disturbed lands. In: & Hyder DN, editor. Proc. First Annual Rangeland Congress. Denver, CO, USA: Society for Range Management. p. 352-354. 6. MCARTHUR, E.D., A.P. PLUMMER, AND J.N. DAVIS. 1978. Rehabilitation of game ranges in the salt desert. In: & Johnson KL, editor. Wyoming Shrublands, Proc. Seventh Wyoming Shrub Ecology Workshop. Laramie, WY, USA: University Wyoming. p. 23-50. 7. PETERSON, J.L., D.N. UECKERT, R.L. POTTER, AND J.E. HUSTON. 1987. Ecotype variation in selected fourwing saltbush populations in western Texas. Journal of Range Management 40:361-366. 8. THOMPSON, T.W., B.A. ROUNDY, E.D. MCARTHUR, B.D. JESSOP, B. WALDRON, AND J.N. DAVIS. 2006. Fire rehabilitation using native and introduced species: A landscape trial. Rangeland Ecology & Management 59:237-248. 9. REICHMAN, O.J., AND D. OBERSTEIN. 1977. Selection of seed distribution types by Dipodomys merriami and Perognathus amplus. Ecology 58:636-643. 10. JOHNSON, T.K., AND C.D. JORGENSEN. 1981. Ability of desert rodents to find buried seeds. Journal of Range Management 34:312-314. 11. HESKE, E.J., J.H. BROWN, AND Q. GUO. 1996. Effects of kangaroo rat exclusion on vegetation structure and plant species diversity in the Chihuahuan Desert. Oecologia 95:520-524. 12. VANDER WALL, S.B. 1994. Dispersal and establishment of antelope bitterbrush by seed caching rodents. Ecology 17:19111926. 13. CLEMENTS, C.D., AND J.A. YOUNG. 1996. Influence of rodent predation on antelope bitterbrush seedlings. Journal of Range Management 49:31-34. 14. VANDER WALL, S.B. 1990. Food hoarding in animals. Chicago, IL, USA: University of Chicago Press. 445 pp. 15. LONGLAND, W.S. 1995. Desert rodents in disturbed shrub communities and their effect on plant recruitment. In: Roundy BA, Mc Arthur ED, Haley JS, & Mann DK, editors. Proc. Wildland Shrub and Arid Land Restoration Symposium. Ogden, UT, USA: USDA Forest Service, Intermountain Res. Sta., Gen. Tech. Rpt. INT-GTR-200. p. 209-215.
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16. NORD, E.C. 1965. Autecology of bitterbrush in California. Ecological Monographs 35:307-334. 17. MCADOO, J.K., C.C. EVANS, B.A. ROUNDY, J.A. YOUNG, AND R.A. EVANS. 1983. Influence of heteromyid rodents on Oryzopsis hymenoides germination. Journal of Range Management 36:6164. 18. LONGLAND, W.S., AND S.L. BATEMAN. 1998. Implications of desert rodent seed preference for range remediation. Journal of Range Manangement 51:679-684. 19. LONGLAND, W.S., S.H. JENKINS, S.B. VANDER WALL, J.A. VEECH, AND S. PYARE. 2001. Seedling recruitment in Oryzopsis hymeniodes: Are desert granivores mutualists or predators? Ecology 82:3131-3148. 20. KELRICK, M.I., AND J.A. MACMAHON. 1985. Nutritional and physical attributes of seeds of some common sagebrush-steppe plants: Some implications for ecological theory and management. Journal of Range Management 38:65-69. 21. PETERSEN, J.L., D.N. UECKERT, AND M.W. WAGNER. 1990. Herbicides to aid establishment of fourwing saltbush. In: McArthur ED, Romney EM, Smith SD, & Tueller PT, editors. Proc. Symposium on cheatgrass invasion, shrub die-off, and other aspects of shrub biology and management. Ogden, UT, USA: USDA Forest Service, Intermountain Res. Sta. Gen. Tech. Rpt. INT-276. p. 305-309. 22. UECKERT, D.N., AND J.L. PETERSEN. 1991. Selecting Atriplex canescens for greater tolerance to competition. Journal of Range Management 44:220-222. 23. SPRINGFIELD, H.W., AND D.B. BELL. 1967. Depth to seed fourwing saltbush. Journal of Range Management 20:180-182. 24. SANDERSON, S.C., R.L. PENDLETON, E.D. MCARTHUR, AND K.T. HARPER. 1987. Saponin effect on small mammal forage preference in a planting of Atriplex canescens. In: Provenza DT, Flinders JT, & McArthur DE, editors. Proc. Symposium on plant-herbivore interactions. Ogden, UT, USA: USDA Forest Service, Intermountain Res. Sta. Gen. Tech. Rpt. INT-222. p. 74-77.
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25. MORRISON, R.B. 1964. Lake Lahontan: Geology of the southern Carson Desert, Nevada. U.S. Geological Survey Professional Paper 401. 156 pp. 26. CLEMENTS, C.D. 1994. Influence of rodent predation on antelope bitterbrush seeds and seedlings [thesis]. Reno, NV, USA: University of Nevada Reno. 50 pp. 27. SAS INSTITUTE, 2017. JMP Version 12.0.1. Cary, NC, USA: SAS Institute Inc. 28. YOUNG, J.A., AND C.D. CLEMENTS. 2002. Purshia: The Wild and Bitter Roses. Reno, NV, USA: University Nevada Reno Press. 266 pp. 29. EVERETT, R.L., R.O. MEEUWIG, AND R. STEVENS. 1978. Deer Mouse preference for seed of commonly planted species, indigenous weed seed, and sacrifice foods. Journal of Range Management 31:70-73. 30. O’CONNEL, M.A. 1975. Coexistence of two species of kangaroo rats (genus Dipodomys) in the Guadalpe Mountains National Park, TX [thesis]. Lubbock, TX, USA: Texas Tech University. 55 pp. 31. ADAMS, A.W. 1975. A brief history of juniper and shrub populations in southern Oregon. Wildlife Research Report 6. Corvallis, OR, USA: Oregon State Wildlife Commission. 33 pp. 32. BLEAK, A.T., N.C. FRISCHKNECHT, A.P. PLUMMER, AND R.E. ECKERT. 1965. Problems in artificial and natural revegetation of the arid shadscale vegetation zone of Utah and Nevada. Journal of Range Management 18:59-65. 33. CLEMENTS, C.D., J.A. YOUNG, D.N. HARMON, AND R.R. BLANK. 2013. Rehabilitation of cheatgrass-infested Rangelands: Concepts. Progressive Rancher 13:30-31.
Authors are Rangeland Scientist ([email protected], Clements); and Agricultural Research Science Technician, USDA, Agricultural Research Service, Great Basin Rangelands Research Unit Reno, NV, 89512, USA (Harmon).
Rangelands
On the Ground
• Four-wing saltbush is an important browse species
• •
• •
for wildlife and domestic livestock and has been reported to provide as much as 11.4% to 13.6% crude protein. Granivorous rodents are important in the ecology of plant communities as well as the management practices that occur in those communities. In any land management practice that involves seeding in restoration or rehabilitation efforts, land managers must be cognizant of the role that biotic and abiotic factors ultimately have on the success and failures of these efforts. Abiotic factors such as poor seed germination or lack of proper amount and periodicity of precipitation are more well understood than biotic factors such as seed and seedling predation by granivorous rodents. Granivorous rodents in this study consumed as much as 55% and 99% of the four-wing saltbush seed and seedlings, respectively. Understanding the possible effects of rodent behavior with four-wing saltbush seed and seedlings should help resource managers in their planning and implementation of future rehabilitation/restoration efforts.
Keywords: seed predation, seedling predation, saltbush, granivorous rodents. Rangelands 39(6):182—186 doi 10.1016/j.rala.2017.10.002 © 2017 The Society for Range Management.
F
our-wing saltbush (Atriplex canescens [Pursh] Nutt.), native to western North America, extends from Canada to Mexico and from the Great Plains to the Pacific Coast. 1 Shrubby species of Atriplex are in the family Chenopodiaceae, which contains other important shrubs such as winter fat (Krascheninnikovia lanata Pursh), and often
182
dominate landscapes in many arid and semi-arid regions, particularly in habitats that combine high soil salinity with aridity. 1 Four-wing saltbush is an important browse species for wildlife and livestock 2 and has been reported to provide as much as 11.4 % to 13.6% crude protein. 3 The use of four-wing saltbush in restoration and land rehabilitation plantings is well documented 2,4–8 and increasingly popular. Granivorous rodents are important in the ecology of plant communities and the management practices that occur in those communities. 9–13 Granivorous rodents exhibit two types of seed-caching behavior: They cache some seeds in larders deep within their burrows, referred to as “larder hoarding,” and they cache some seeds in shallow depressions they dig throughout their home range, referred to as “scatter hoarding.” 14 Larder hoard caches are buried at depths that may allow germination but are most often too deep to sprout, 15 whereas scatter hoard caches that are not recovered are buried at depths that often promote germination and therefore have been found to be an important mechanism for the recruitment of various range plants. 12,13,16–19 In any land management practice that involves seeding in restoration or rehabilitation efforts, land managers must be cognizant of the role that biotic and abiotic factors ultimately have on the success and failures of these efforts. 20 Four-wing saltbush has been reported to experience variable success in seeding efforts, 21,22 with abiotic factors such as poor seed germination or lack of proper amount and periodicity of precipitation being fairly well understood. Biotic factors such as seed and seedling predation by granivorous rodents are less understood. Longland and Bateman 18 reported that the rodents in their study seldom cached four-wing saltbush seed, and it has also been reported that rodents damage young four-wing saltbush plants. 23,24 This study was initiated to address 1) the harvest, consumption, and caching of four-wing saltbush seed, and 2) the possible consumption of four-wing saltbush seedlings by granivorous rodents. We hypothesized that granivorous rodents in this study would harvest, consume, and cache a portion of the four-wing saltbush seed with which they interacted. We also hypothesized that four-wing saltbush seedlings would be consumed by granivorous rodents in this study.
Rangelands
Data Collection The study area is located in Desert Queen Valley (39°43'N, 118°59'W; elevation 1,257 m), 80 km northeast of Reno, Nevada. The valley was an embayment of pluvial Lake Lahontan, but the lake sediments are buried in sands that eroded from the delta of the Truckee River and are trapped in the valley in the lee of the Hot Spring Mountain Range. 17,25 The sands at the site are dominated by an overstory of four-wing saltbush, shadscale (Atriplex confertifolia [Torrey & Fremont] S. Watson), spotted dalea (Dalea polydemii S. Watson), Bailey’s greasewood (SarcoCov.), and winter fat, while the understory is dominated by Indian ricegrass (Achnathereum hymenoides [Roemer & Schultes] Beckworth), and Russian thistle (Salsola tragus L.). An active rain gauge at the site reveals the site receives 12 to 16 cm of precipitation from 1 October through 30 September annually. The rodent census/population part of the study was conducted twice per month for the duration of the study, from September 2013 through April 2014, using the mark-and-release live-trapping method with Sherman livetraps. 13,26 Fifty live-trap stations were established in which a grid of 5 transects were spaced 15 m apart with 10 stations per transect that were also placed 15 m apart. At each station 2 live-traps were set out (100 traps), baited with millet (Panicum spp.) seed in the evening, and checked the following morning. All captured animals were identified by species and sex, marked with a numbered ear tag, and released at the point of capture. Trapping took place for three consecutive nights 13,19 twice per month over the duration of the study. Investigation of rodent interaction with four-wing saltbush seeds was conducted using portable live-trap enclosures where consumption and caching of four-wing saltbush by various rodents was recorded. These portable live-traps, 60 × 30 × 35 cm, were constructed with solid plywood bottoms, fronts, and backs and were covered with 0.7 cm mesh hardware cloth. A hole was cut out of the front plywood panel to accommodate the placement of a Sherman live-trap, with the back door of the live-trap removed, to allow rodents to enter but not exit the enclosure. 13,26 The back plywood was removable to allow for the placement and removal of a 54 × 26 × 5 cm deep soil flat. A total of 12 portable enclosures (2 control enclosures permitted no access) were randomly placed on a 12-transect by 10-station grid. Each transect and station was at 15 m spacing. Enclosures were set out each evening at 1600 h and baited with 4 g of millet seed (620 seeds) in the live-trap. One hundred four-wing saltbush seeds, collected from the site the previous year, were placed on the surface of the soil in the soil flats. Soil in the soil flat was collected at the site and sieved free of any seed. Enclosures were checked the following morning at 0600 h. Enclosures with a rodent capture were dealt with first. Rodents were recorded by species and sex and tagged with a numbered ear tag; in the case of a recapture, the ear tag number was recorded. Cheek pouches were checked for any seeds, which were removed and recorded. Rodents were released at the point of capture. The number of visible seed on the surface was noted. The soil flat then was sieved and the number of seeds was recorded as un-cached, cached, or consumed. The portable enclosures were then reset and December 2017
randomly placed within the grid. This process took place for 5 consecutive mornings over 4 separate weeks from late September 2013 through early November 2013, coinciding with the timing of four-wing saltbush seed fall in the area. These portable enclosures were also used to investigate any four-wing saltbush seedling consumption by the various rodents at the site. Four-wing saltbush seedlings were grown in soil flats in soil from the site in a greenhouse environment. Twenty-five seedlings were grown in each flat and placed into the portable enclosures. Using the same transects as described above, portable enclosures were placed out at 1600 h each evening, baited with 4 g of millet seed inside the live-trap, and checked the following morning at 0600 h. Enclosures with rodents were dealt with first. Rodent species, sex, and ear tag number were recorded as described above, and the rodent released at the point of capture. Consumption of four-wing saltbush seedlings was recorded, as was any damage to seedlings not consumed (e.g., digging up). New soil flats with fresh four-wing saltbush seedlings were placed inside the enclosures and reset at randomly selected stations within the grid. This process took place for 5 consecutive mornings for 4 separate weeks from late March 2014 through late May 2014, coinciding with the timing of four-wing saltbush seedling sprouting at the site. Seeds and seedlings consumed were analyzed using SAS JMP 27 with species fixed and week and week × species as random. Tukey’s adjustment for multiplicity was used to make comparisons among the species (least square means).
Results A total of 5,400 trap nights were conducted during this study, resulting in a total of 132 captures of 59 separate individuals of 4 separate species. The species richness and diversity of the rodent population at this site, as represented through the live-trap data, indicated that the site was dominated by the Merriam’s kangaroo rat (Dipodomys merriami) (n = 34), followed by the chisel-toothed kangaroo rat (Dipodomys microps) (n = 13), desert kangaroo rat (Dipodomys deserti) (n = 8), and white-tailed antelope ground squirrel (Ammospermophilus leucurus) (n = 4). The trapping grid was 1 ha in size and therefore represents a minimum rodent population of 59/ha. This is based on the minimum known number alive method, but could result in an over- or underestimate due to rodents being trap shy and not being captured or rodents outside the grid being captured. 25 Investigation of rodents (n = 103) with four-wing saltbush seed in the portable enclosures revealed that none of the 103 rodents harvested four-wing saltbush seed in their cheek pouches or cached any seed in the portable enclosure. Therefore, there was no evidence that rodents were attempting to cache four-wing saltbush seed, although all 103 rodents in this study did harvest and store a portion of the millet seed available in their cheek pouches or mouth cavity 100% of the time. The rodent population did, however, consume fourwing saltbush seed, as they excavated the embryos from the seed coat (Fig. 1). The Merriam’s and desert kangaroo rat and the white-tailed antelope ground squirrel significantly
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99.25 ± 6.62 (n = 12), Merriam’s kangaroo rat 92.94 ± 3.00 (n = 51), and the chisel-toothed kangaroo rat 74.59 ± 5.01 (n = 23), even though millet seed was available as an alternative food source and the 4 g of millet seed available was never totally consumed. The chisel-toothed kangaroo rat consumed significantly (P ≥ 0.05) less four-wing saltbush seedlings than the Merriam’s and Desert kangaroo rat (Fig. 3). As one may expect, the disturbance caused by individual rodents varies as some of the four-wing saltbush seedlings are trampled; therefore, we only counted those seedlings that had clearly been foraged upon and consumed.
Figure 1. De-winging and excavation of four-wing saltbush seed by granivorous rodents.
(P ≤ 0.0001) consumed four-wing saltbush seed (Fig. 2). The desert kangaroo rat consumed the most four-wing saltbush seed (55.11 ± 3.22; n = 29), followed by the Merriam’s kangaroo rat (54.70 ± 2.20; n = 62), white-tailed antelope ground squirrel (34.33 ± 8.14; n = 5), and chisel-toothed kangaroo rat (13.63 ± 6.60; n = 7). The desert and Merriam’s kangaroo rat consumed significantly (P ≤ 0.05) more four-wing saltbush seed than the other two species, and the white-tailed antelope ground squirrel consumed significantly (P ≤ 0.05) more than the chisel-toothed kangaroo rat (Fig. 2). The chisel-toothed kangaroo rat, which consumes saltbush leaves, may rely less on seed consumption, thereby explaining the lower consumption of four-wing saltbush seeds by this species. Seeds in the control cages were all present and were not moved by ants, wind, or any other occurrence. White-tailed antelope ground squirrels were not observed in our portable enclosures during the seedling interaction period of the study. The remaining three rodent species that entered the portable enclosures (n = 86) at the site significantly (P ≤ 0.001) consumed four-wing saltbush seedlings (Fig. 3). The consumption of four-wing saltbush seedlings by these rodents was very high: The desert kangaroo rat consumed an average of
Figure 2. Mean number of four-wing saltbush seeds consumed per 100 available seeds. Different letters represent significant differences between species.
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Discussion and Implications From field observations, we suspected that four-wing saltbush seed would not be a preferred seed species for granivorous rodents because there is visual evidence of four-wing saltbush seed falling to the ground beneath shrubs and accumulating over time, which is not the case with seeds from preferred shrub species such as antelope bitterbrush (Purshia tridentata Pursh). 28 Previous research has found four-wing saltbush seed to be the least preferred whereas antelope bitterbrush seed was the most preferred seed for some rodent species. 29 Heavily utilized seed, such as antelope bitterbrush, is rapidly harvested by granivorous rodents as it falls to the ground, and the seed dispersal of this important shrub through rodent scatter hoard caching activity results in beneficial dispersal and recruitment of antelope bitterbrush shrubs. 12,13,16,28 Four-wing saltbush seed has a wind dispersal mechanism because the seed has large winged appendages, whereas antelope bitterbrush seed does not have an active wind dispersal system and relies heavily on rodent seed dispersal. We did, however, hypothesize that rodent species tested in this study would harvest and cache a portion of the four-wing saltbush seed with which they interacted. Even though the large wing structures of four-wing saltbush seed and the very hard seed coat would be considered deterrents for
Figure 3. Mean percent of four-wing saltbush seedlings consumed. Different letters represent significant differences between species.
Rangelands
granivory, we observed a high degree of de-winged seeds and embryo excavation on four-wing saltbush seed. We also hypothesized that granivorous rodents would graze on four-wing saltbush seedlings because our field experience has resulted in the observation of numerous species being grazed at the early seedling stages, such as antelope bitterbrush, 13,28 Indian ricegrass (Achnatherum hymenoides Roemer & Schultes), and winter fat. Some research has reported increased consumption of green vegetation in the diet of Merriam’s kangaroo rat during the summer months, with Atriplex species contributing to that diet. 30 It is important that these plant species are vigorous and healthy to experience good flowering and yield substantial seeds to the environment. The more seeds that are available to germinate and emerge, the less the total effect of rodent predation on the recruitment of seedlings to sustain the plant population. 13,31 Although this research was conducted using portable enclosures, granivorous rodents in this study avoided caching four-wing saltbush seed while still excavating the embryo from the seed. The seedling predation may well be higher than in natural conditions, but the fact that such a high level of seedling predation occurred when an alternative millet seed food source was available suggests a preference for these seedlings at this young phenology stage. This research found that four-wing saltbush seed is not highly preferred because the rodents at this site are not harvesting and caching the seed for future consumption. The high consumption of four-wing saltbush seedlings at this site is alarming, however, and may be an explanation for the poor success at given sites after the seeding of four-wing saltbush. The clipping of seedlings by granivorous rodents is more detrimental to shrub seedlings than grass seedlings due to the removal of the hypocotyl or epicotyl. 32 In the past three decades, numerous years have seen large wildfires that have burned millions of acres. For example, in 1999, more than 728,000 ha burned in Nevada alone, which resulted in the largest rehabilitation/restoration undertaking in state history. This rehabilitation/restoration effort resulted in the purchase of nearly 2.2 million kg of grass, forb, and shrub seed to be placed on the burned rangelands. 33 Four-wing saltbush seed was second only to Wyoming big sagebrush (Artemisia tridentata ssp. wyomingesis Beetle & A. Young) in desired shrub species in the 40,000 ha to be drill seeded and the more than 150,000 ha to be aerial seeded. The importance of four-wing saltbush for wildlife and domestic livestock as well as its role in improving functional plant communities only enhances the need to successfully rehabilitate/restore degraded rangelands. The results from this study would suggest that resource managers cannot depend on granivorous rodents to harvest, disperse, and cache four-wing saltbush seed; therefore, drill seeding of four-wing saltbush seed may be necessary to get the seed into the ground where it has a higher chance of germination and emergence. The fact that four-wing saltbush seedlings were consumed at a high level may suggest to resource managers that transplanting older seedlings could result in less seedling predation. Understanding the possible effects of rodent behavior with four-wing saltbush seed and seedlings should help resource December 2017
managers in their planning and implementation of future rehabilitation/restoration efforts.
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Authors are Rangeland Scientist ([email protected], Clements); and Agricultural Research Science Technician, USDA, Agricultural Research Service, Great Basin Rangelands Research Unit Reno, NV, 89512, USA (Harmon).
Rangelands